Botana, Sainz (Eds.

)
Climate Change and Mycotoxins
Also of interest
Climate Change and Marine and Freshwater Toxins
Botana, Louzao and Vilariño (Eds.), 2015
ISBN 978-3-11-033303-9, e-ISBN 978-3-11-033359-6

Chemistry of the Climate System

Detlev Möller, 2014
ISBN 978-3-11-033080-9, e-ISBN 978-3-11-033194-3

Miniaturization in Sample Preparation

Pena Pereira (Ed.); 2014
ISBN 978-3-11-041017-4, e-ISBN 978-3-11-041018-1

Introduction to Modern Instrumentation:

For Hydraulics and Environmental Sciences
Guaraglia and Pousa; 2014
ISBN 978-3-11-040171-4, e-ISBN 978-3-11-040172-1

Freshwater Fungi and Fungal-like Organisms

Jones, Hyde and Pang (Eds.), 2014
ISBN 978-3-11-033345-9, e-ISBN 978-3-11-033348-0

Reviews on Environmental Health

Carpenter, David O. and Sly, Peter (Editors-in-Chief)
ISSN 0048-7554, e-ISSN 2191-0308
Climate Change
and Mycotoxins

|
Edited by
Luis M. Botana and María J. Sainz
Editors
Prof. Luis M. Botana
Universidad de Santiago de Compostela
Facultad de Veterinaria
Departamento de Farmacología
27002 Lugo, Spain
[Link]@[Link]

Prof. María J. Sainz

Universidad de Santiago de Compostela
Facultad de Veterinaria
Departamento de Producción Vegetal
27002 Lugo, Spain
[Link]@[Link]

ISBN 978-3-11-033305-3
e-ISBN (PDF) 978-3-11- 033361-9
e-ISBN (EPUB) 978-3-11- 039015-5
Set-ISBN 978-3-11- 033362-6

Library of Congress Cataloging-in-Publication Data

A CIP catalog record for this book has been applied for at the Library of Congress.

Bibliographic information published by the Deutsche Nationalbibliothek

The Deutsche Nationalbibliothek lists this publication in the Deutsche Nationalbibliografie;
detailed bibliographic data are available on the Internet at [Link]

© 2015 Walter de Gruyter GmbH, Berlin/Boston

Cover image: Dangdumrong/iStock/thinkstock
Typesetting: PTP-Berlin, Protago-TEX-Production GmbH, Berlin
Printing and binding: CPI books GmbH, Leck
♾ Printed on acid-free paper
Printed in Germany

[Link]
Preface
Climate change is expected to strongly affect agricultural productivity, food safety, and
food security worldwide in the coming decades, due to higher temperatures, changes
in water supply and availability, year-to-year climate variability, and extreme weather
events. The impact on food and feed crops is expected to manifest not only in changes
to plant physiology, yield, and quality, but also in incidence and severity of pests and
diseases. Of particular concern are the potential changes in geographical distribu-
tion, natural inoculum, activity, and biological fitness of some of those fungal species
which cause disease in staple food crops, particularly cereals, or grow saprophytically
on stored plant products and produce mycotoxins.
Mycotoxins are secondary metabolites produced by filamentous fungi either pre-
or postharvest and which can contaminate agricultural food and feed products and
have detrimental effects on human and animal health. Although awareness of the fact
that mycotoxins are ubiquitous in food and feed products is not very high, they are
deeply ingrained in human culture, as their presence has been associated with deaths
and serious feed and food poisoning throughout history. Those from Claviceps have
even been an inspiration to artists, for example in paintings (e.g. by Peter Brueghel)
and sculptures.
Nowadays, more than 100 countries have regulations specifying maximum tolera-
ble levels for the most toxic and/or abundant mycotoxins, mainly in human food. Cri-
teria for limits have not been harmonized worldwide, however. Much of the research
on mycotoxins, including recent research on the effects of climate change on myco-
toxins, has focused on the Aspergillus, Fusarium, and Penicillium species, as they are
the major mycotoxin-producing fungi in field crops and stored products in the world.
When we decided to edit a book on climate change and mycotoxins, we were aware
that, although it is relatively easy to identify climate change from the study of clima-
tological records and the development of predictive models, it is not so easy to clearly
define a link between climate change and expected mycotoxin risks in the different
geographical zones of the world. In this book, the authors wrote outstanding chapters
on the subject by reviewing the effects of changes in temperature, water availability,
and CO2 on the biodiversity, plasticity, occurrence, and mycotoxin profile of the most
prevalent mycotoxigenic fungi on cereals in different regions, as there is no historical
record to compare the amounts of toxins now and a century or more ago. The book pro-
vides information on the trends in mycotoxin occurrence in agricultural commodities
over the last ten years. Toxins have been discovered by modern science, and therefore
their presence, structure, or levels in food have only been known recently. The science
of mycotoxins has significantly advanced in recent years as a result of the implemen-
tation of sensitive analytical detection technology, such as mass spectrometry, and
the availability of the first certified standards; but improved standardized multitoxin
detection analysis and further certified reference materials will have to be developed
VI | Preface

to support current and future mycotoxin regulation for the protection of human and
animal health. They will also be essential to track any shift in the mycotoxin levels
within the food chain worldwide in a climate change scenario.
This book intends to highlight the importance of the study of climate change im-
pacts on mycotoxigenic fungi and their mycotoxins in food and feed crops in order
to guarantee safe and sufficient food and feed in the future. The book is thus suit-
able for mycologists, mycotoxicologists, pathologists, epidemiologists, toxicologists,
physicians, veterinarians, nutritionists, the food and feed industries, legislators, an-
alytical chemists, microbiologists, biologists, or students of these fields.
As always, a book of this kind is unthinkable without the valuable work of the
authors of the individual chapters. We wish to thank them, not only for their time,
effort, and generosity in contributing their experience and expertise to this book, but
also for their commitment to a difficult project, as is indeed the effect of climate change
on food security.

The editors
Contents
Preface | V

List of contributing authors | XI

Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

1 Climate change and plant diseases caused by mycotoxigenic fungi:
implications for food security | 1
1.1 Introduction | 1
1.1.1 Mycotoxigenic fungi and food security | 2
1.1.2 Climate change and food security | 3
1.1.3 Climate change effects on plant diseases and food security | 4
1.2 Effects of climate change on plant diseases caused by
mycotoxigenic fungi | 5
1.2.1 Epidemiology and resistance | 5
1.2.2 Pathogen population genetics and evolution | 10
1.3 Prediction of climate change effects on epidemics | 12
1.3.1 Bioclimatic niche models | 13
1.3.2 Climate change scenario models | 16
1.4 Management of plant diseases caused by mycotoxigenic fungi
under climate change | 19
1.5 Outlook and conclusions | 20

X. Li and X. B. Yang
2 Impact of climate change on genetically engineered plants and
mycotoxigenic fungi in the north central region of the US | 29
2.1 Introduction | 29
2.2 GMO cropping systems in US agriculture | 33
2.2.1 The establishment of GMO cropping systems in the US | 33
2.2.2 Glyphosate-resistant crops and Bt transgenic techniques | 34
2.2.3 General impact of GM crops on US agriculture | 34
2.2.4 Impact of GM crops on mycotoxigenic fungi | 35
2.3 Global climate change and current situation in the US | 36
2.4 Impacts of climate change on the occurrence
of mycotoxigenic fungi | 38
2.4.1 The impact of climate change in the off-seasons: winter and
early spring | 38
2.4.2 Impact of climate change on planting date and fungi
at seedling stages | 39
VIII | Contents

2.4.3 Impact of climate change on crops and diseases in late spring

and summer | 41
2.4.4 Increased use of fungicides | 44
2.5 Summary and future risks | 44

José-Miguel Barea
3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic
fungi related to food crop health in a scenario of climate change | 53
3.1 Introduction | 53
3.2 Arbuscular mycorrhizal (AM) symbiosis | 55
3.2.1 AM establishment, function, and management | 55
3.2.2 AM and stress alleviation in plants | 57
3.2.3 Effects of agricultural practices on AM symbiosis | 58
3.3 Interactions among plants, AM symbiosis, and mycotoxigenic fungi
related to plant health | 59
3.3.1 The effect of AM on plant protection against pathogens and pests | 59
3.3.2 Mycorrhiza-induced resistance and priming of plant defenses | 60
3.3.3 Interactions between AM symbiosis and mycotoxigenic fungi | 62
3.3.4 Impact of climate change on AM fungi and repercussions for the
protection of food crops against fungal diseases | 63
3.3.5 Research perspectives and opportunities for exploiting the interactions
between mycotoxigenic and AM fungi with regard to plant health as
affected by climate change | 64

Angel Medina, Alicia Rodriguez, and Naresh Magan

4 Changes in environmental factors driven by climate change: effects on the
ecophysiology of mycotoxigenic fungi | 71
4.1 Background | 71
4.1.1 Environmental change, fungal adaptation, and mycotoxins | 71
4.1.2 Climate change and mycotoxigenic fungi | 72
4.2 Ecophysiological modifications on mycotoxigenic fungi under climate
change conditions | 75
4.2.1 Two-way a w × temperature interactions | 75
4.2.2 Three-way a w × temperature × CO2 interactions | 79
4.3 Climate change impact on mycotoxin gene cluster expression and its
relationship to growth and toxin production. | 82
4.4 Conclusions | 85

Antonio Moretti and Antonio F. Logrieco

5 Climate change effects on the biodiversity of mycotoxigenic fungi and their
mycotoxins in preharvest conditions in Europe | 91
5.1 Introduction | 91
 Contents | IX

5.2 Climate change and the risk of aflatoxin and Aspergillus contamination
in Europe | 93
5.3 Fusarium head blight (FHB) of cereals: impact of climate change on the
risk of trichothecenes and Fusarium contamination in Europe | 96
5.3.1 Organization of TRI loci and trichothecene structural variation | 97
5.3.2 FHB of minor cereals | 98
5.3.3 Impact of climate change on the Fusarium species profile associated
with FHB | 101

Leif Sundheim and Trond Rafoss

6 Fumonisin in maize in relation to climate change | 109
6.1 Introduction | 109
6.2 Fumonisin-producing fungi | 110
6.2.1 Biology of fungi producing fumonisin | 111
6.3 Fumonisin accumulation in developing maize kernels | 113
6.3.1 Fumonisins are not required for pathogenicity | 113
6.3.2 Insect damage increases risk of fumonisin contamination | 114
6.3.3 Small grain cereals contaminated with fumonisins | 115
6.3.4 Other crops and commodities contaminated with fumonisins | 115
6.4 Geographical distribution of fumonisins in maize | 116
6.4.1 Africa | 117
6.4.2 Europe | 118
6.4.3 South America | 119
6.4.4 North America | 119
6.4.5 Asia | 120
6.5 Climate change predicted by IPCC | 121
6.5.1 Climate effects on fungi producing fumonisin in maize | 121
6.5.2 Effects of temperature | 122
6.5.3 Effects of drought | 122
6.5.4 Effects of elevated CO2 level | 124
6.6 Conclusions on the effect of climate change on fumonisin | 124

Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder
7 Climate change impacts on mycotoxin production | 133
7.1 Introduction | 133
7.2 Impact of temperature, water availability, and CO2 on mycotoxin
production | 134
7.3 Prediction strategies | 135
7.4 Other factors to consider | 136
7.5 Insights into potential mycotoxin production: focus on Europe | 137
7.6 Trends in mycotoxin occurrence | 138
7.7 Conclusion | 149
X | Contents

María J. Sainz, Amparo Alfonso, and Luis M. Botana

8 Considerations about international mycotoxin legislation, food security,
and climate change | 153
8.1 Introduction | 153
8.1.1 Main mycotoxins | 154
8.2 Impacts of climate change on agriculture | 155
8.3 Detection methods | 157
8.3.1 Sampling procedures | 157
8.3.2 Extraction procedures | 157
8.3.3 Mycotoxin analysis | 159
8.3.4 Requirements for mycotoxin analysis methods | 161
8.4 International mycotoxin regulations | 162
8.5 Mycotoxin legislation and climate change | 173

Index | 181
List of contributing authors

Amparo Alfonso X. Li
Department of Pharmacology College of Plant Protection
Faculty of Veterinary Hunan Agricultural University
University of Santiago de Compostela Changsha, China
Campus s/n, 27002 Lugo, Spain and
Chapter 8 Department of Plant Pathology and Microbiology
Iowa State University
José-Miguel Barea Ames, IA 50011, USA
Departamento de Microbiología del Suelo linuslee@[Link]
y Sistemas Simbióticos Chapter 2
Estación Experimental del Zaidín (CSIC)
Profesor Albareda 1 Yin-Jung Liu
18008 Granada, Spain Erber AG
[Link]@[Link] Industriestraße 21
Chapter 3 3130 Herzogenburg, Austria
Karin Nahrer
Eva M. Binder Biomin Holding GmbH
Erber AG Industriestraße 21
Industriestraße 21 3130 Herzogenburg, Austria
3130 Herzogenburg, Austria Chapter 7
[Link]@[Link]
Chapter 7 Antonio F. Logrieco
Institute of Sciences of Food Production
Luis M. Botana (Ed.) Via Amendola 122/O
Department of Pharmacology 70126 Bari, Italy
Faculty of Veterinary [Link]@[Link]
University of Santiago de Compostela Chapter 5
Campus s/n, 27002 Lugo, Spain
[Link]@[Link] Naresh Magan
Chapter 8 Applied Mycology Group
Cranfield Soil and AgriFood Institute
Christian Joseph R. Cumagun Cranfield University, Cranfield
Crop Protection Cluster Bedford MK43 0AL, U.K.
College of Agriculture Chapter 4
University of the Philippines Los Baños
College, Laguna, Philippines 4031 Angel Medina
Chapter 1 Applied Mycology Group
Cranfield Soil and AgriFood Institute
Cranfield University, Cranfield
Bedford MK43 0AL, U.K.
[Link]@[Link]
Chapter 4
XII | List of contributing authors

Antonio Moretti María J. Sainz (Ed.)

Institute of Sciences of Food Production Department of Plant Production
Via Amendola 122/O University of Santiago de Compostela
70126 Bari, Italy Campus s/n, 27002 Lugo, Spain
Chapter 5 mjsainz@[Link]
Chapter 8
Ireneo B. Pangga
Crop Protection Cluster Arnold R. Salvacion
College of Agriculture Department of Community and Environmental
University of the Philippines Los Baños Resource Planning
College, Laguna, Philippines 4031 College of Human Ecology
ibpangga@[Link] University of the Philippines Los Baños
Chapter 1 College, Laguna, Philippines 4031
Chapter 1
M. P. Kovalsky Paris
Biomin Holding GmbH Leif Sundheim
Industriestraße 21 Norwegian Institute of Agricultural and
3130 Herzogenburg, Austria Environmental Research
Chapter 7 Plant Health and Plant Protection Division
1430 Ås, Norway
Trond Rafoss [Link]@[Link]
Norwegian Institute of Agricultural and Chapter 6
Environmental Research
Plant Health and Plant Protection Division X. B. Yang
1430 Ås, Norway Department of Plant Pathology and Microbiology
Chapter 6 Iowa State University
Ames, IA 50011, USA
Alicia Rodriguez xbyang@[Link]
Applied Mycology Group Chapter 2
Cranfield Soil and AgriFood Institute
Cranfield University, Cranfield
Bedford MK43 0AL, U.K.
Chapter 4
Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph
R. Cumagun
1 Climate change and plant diseases caused by
mycotoxigenic fungi: implications for food security

1.1 Introduction

The contribution of Working Group I to the International Panel on Climate Change

(IPCC) 5th Assessment Report (AR5) reaffirmed that the warming of the climate sys-
tem is unequivocal and the observed changes are unprecedented over decades to mil-
lennia. Compared to the 4th Assessment Report (AR4), improved climate models and
longer and more detailed observations showed that human influence on the climate
system is clearly indicated by increasing greenhouse gas concentrations in the atmo-
sphere and observed global warming. The atmospheric concentration of carbon diox-
ide (CO2 ) of 391 ppm in 2011 has increased by 40 % since pre-industrial times due to
emissions from fossil fuel combustion and changes in land use. The total change in
energy fluxes caused by natural and anthropogenic drivers for 2011 relative to 1750
(radiative forcing) is positive, leading to energy uptake by the climate system with the
largest contribution by CO2 [1].
Representative Concentration Pathways (RCP), a new set of climate change sce-
narios, were identified by their approximate total radiative forcing (watts (W) per m2 )
in the year 2100 relative to 1750: mitigation scenario with very low radiative forcing
level (RCP2.6), two stabilization scenarios (RCP 4.5 and 6), and very high greenhouse
emission scenario (RCP8.5). Climate model simulations make high confidence pro-
jections that the global temperature changes will likely exceed 1.5 °C at the end of
the 21st century, relative to 1850–1990 for all RCP scenarios except RCP2.6 with 1 °C
mean change. The global mean surface temperature change from 2016–2035 relative to
1986–2005 will likely be in the range of 0.3–0.7 °C (medium confidence). As the mean
global temperature increases, it is virtually certain (99–100 % probability) that more
frequent hot and fewer cold extremes in temperature will occur and that heat waves
will very likely (90–100 % probability) occur with higher frequency and duration [1].
Changes in the global water cycle in response to global warming in the 21st cen-
tury will not be uniform. The contrast between wet/dry regions and seasons will in-
crease except for some regions. Extreme precipitation over most of the mid-latitude
land masses and wet tropical regions will very likely become more intense and fre-
quent at the end of the 21st century. In many mid-latitude and subtropical dry regions,
mean precipitation will likely (66–100 % probability) decrease. Due to the increase in
atmospheric moisture, the variability in El-Niño-Southern Oscillation (ENSO)-related
precipitation in regional scales and monsoon precipitation will likely intensify [1].
2 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

The contribution of Working Group II (WG II) to IPCC AR5 assessed a substantially
larger knowledge base of relevant scientific, technical and socioeconomic literature
compared to past reports. This facilitated a comprehensive assessment of impacts,
adaptation, and vulnerability of climate change risks in human and natural systems.
WG II AR5 found that a high likelihood that all aspects of food security will potentially
be affected by climate change, from food production to food access, utilization, and
price stability [2].
Climate change poses a considerable challenge to food security as the global de-
mand for food will increase to feed 9.2 billion people in 2050 [3, 4]. Without adaptation
a negative impact of climate change on food production is projected for ≥ 2 °C temper-
ature increase above late 20th century levels for wheat, rice, and maize in tropical and
temperate areas, but impacts will vary across crops, regions, and adaptation scenar-
ios [2]. Expanded geographic ranges and altered dynamics of insect pests and diseases
due to climate change can exacerbate the reductions in crop yields [5–7]. Plant dis-
ease is a major constraint in food production, as direct yield losses due to pathogens
cause 16 % overall loss in agricultural productivity [8], but the indirect harmful effects
on food quality and safety are very serious in many crops and environments world-
wide [9].
This chapter aims to discuss the effects of climate change on mycotoxigenic fungi
on the three major food crops vital to food security such as wheat, rice, and maize.
Maize, wheat, and rice provide 30 % of the food calories for 4.5 billion people in 100
developing countries [10]. Mycotoxin contamination has become one of the most im-
portant and challenging problems facing plant pathologists today [11, 12]. For exam-
ple, in Fusarium head blight of wheat, environmental conditions such as rainfall and
temperature are the dominant factor associated with disease infection [13, 14]. Knowl-
edge of population genetics and epidemiology are the keys to Fusarium head blight
management [15, 16]. The effects of climate change variables on epidemics in major
food crops caused by pre- and post-harvest mycotoxigenic fungi will be analyzed in
terms of plant disease epidemiology and population genetics.

1.1.1 Mycotoxigenic fungi and food security

Significant crop losses in major food crops due to mycotoxigenic fungi remain a major
hindrance in achieving food security. Fusarium head blight of wheat and barley is
considered a re-emerging disease due to historical and recent epidemics worldwide
[17, 18]. In the USA, a direct economic loss of US $ 2.491 billion was observed due
to Fusarium head blight from 1993–2001 [19]. In 2003, another Fusarium head blight
epidemic in southeastern USA caused a pre-milling economic loss of over US $ 13.6
million [20].
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 3

The production of mycotoxins by fungi in major food crops is another important

factor which has a severe impact on food security. It has been estimated that 25 %
of the world food crops are affected by mycotoxins [21]. The three most important
genera of mycotoxigenic fungi are Aspergillus, Fusarium, and Penicillium, producing
the following classes of mycotoxins: aflatoxin (Aspergillus), ochratoxin (Aspergillus
and Penicillium), trichothecenes and fumonisins (Fusarium) [22]. The potential annual
cost of food and feed contamination in the US with aflatoxins, fumonisins, and de-
oxynivalenol (DON) was estimated at US $ 946 million [23]. Annual average losses of
US $ 163 million to aflatoxins and US $ 40 million to fumonisins were estimated for
US maize [24]. In 2010, 10 % of the Kenyan maize harvest was contaminated with afla-
toxins resulting in an economic loss of approximately US $ 100 million [25]. In 2012,
Aspergillus and Fusarium ear rot caused yield losses of 94.7 and 80.8 million bushels
in top corn producing US states and Ontario, Canada with 18 % loss from mycotoxin
contamination [26].
Mycotoxin contamination of the food chain is a food safety risk globally, leading to
human health threats because it can cause mycotoxicosis, resulting in acute or chronic
disease episodes [22]. The mycotoxin hazard can be exacerbated by food insecurity
because mycotoxin-contaminated food can be consumed rather than discarded and
malnutrition enhances the susceptibility to lower mycotoxin levels [27]. A fitting ex-
ample of the adverse effect of mycotoxin contamination on human health is the 2004
aflatoxin contamination in Kenya where 125 people died [28]. In Thailand, Indonesia,
and the Philippines the total annual social cost of aflatoxins in maize was AUS $ 319
million in 1991 [29].

1.1.2 Climate change and food security

Food production is an important aspect of food security, and it needs to be increased

by 60 % by 2050 under current food consumption trends, assuming no significant re-
duction in food waste [30]. Climate change is projected to negatively affect food pro-
duction as local temperature increases by 2 °C or more above late 20th century levels,
but some individual locations will have positive impact (medium confidence). Process-
based models and regional statistical analysis showed negative impacts of tempera-
ture above 30–34 °C on crop yields depending on the crop and region [5]. Based on
statistical crop models and climate projections for 2030 from 20 general circulation
models, the production of wheat in South Asia, rice in Southeast Asia, and maize in
Southern Africa will suffer negative impact in the absence of adaptation [31].
Climate change could slow down the progress towards food security. Climate
change can have a range of direct and indirect effects on all four dimensions of food
security: food availability, access, utilization, and stability [2, 32]. The direct impacts
of climate change on food availability will occur throughout the food chain but will be
greatest for agriculture considering its climate sensitivity and key role in food supply.
4 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

Indirect impacts of climate change on nutrition, health, livelihoods, and poverty will
be more complex and highly differentiated. The impacts of climate change on food
systems are expected to be widespread, complex, geographically and temporally vari-
able, and greatly influenced by socio-economic conditions [33]. The overall impact of
climate change on food security is considered more complex and potentially greater
than the projected impact on agricultural productivity [5]. Food security is diminished
when food systems are stressed. Climate change effects on the food system will vary
between regions [34] and food inequalities will increase from local to global levels
due to spatial variation in climate change effects [32].
The impacts of climate change on food security will be worst in countries already
suffering high levels of hunger [32]. Sub-Saharan Africa had the highest proportion of
food insecure people with an estimated regional average of 20 % of the population is
undernourished in 2010–2012, while the largest number is in South Asia with 300 mil-
lion undernourished [30]. The risks of food insecurity and breakdown of food systems
are linked to global warming, drought, flooding, and variable and extreme precipi-
tation particularly for poorer populations in urban and rural settings of Africa, Asia,
and Central and South America. Based on IPCC WG II AR5, reduced crop productivity
associated with heat and drought stress will have strong adverse effects on food secu-
rity while increased pest and disease damage and flood impacts on food system are
projected in Africa. Increased risk of drought-related water and food shortage causing
malnutrition is projected for Asia whereas decreased food production and food quality
are projected for Central America [2].
Climate change can destabilize the food system resulting in high and volatile food
prices [4, 35]. Increased temperature and altered precipitation without CO2 effects will
contribute to increased global food prices by 2050 from 3–84 % (medium confidence).
Any negative impact of climate change on global crop yields is expected to lead to
increases in international food prices and the proportion of population which is food-
insecure [5].

1.1.3 Climate change effects on plant diseases and food security

Food security is defined as the access to sufficient, safe, and nutritious food for dietary
needs and food preferences [36]. One major factor contributing to low productivity is
crop loss due to plant health problems, which is poorly recognized as an important
driver of food security [37]. Nevertheless, plant diseases have enormous impacts on
food security as exemplified by the Irish potato famine in 1845 due to the potato late
blight epidemic caused by Phytophthora infestans, which resulted in the death of 1
million people and the emigration of 1.5 million to mainland US [38]. A further ex-
ample is the great Bengal famine of 1943 due to the rice brown spot epidemic caused
by Helminthosporium oryzae in India, resulting in the starvation of 2 million people
[39]. During these two plant disease epidemics, the weather conditions were very con-
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 5

ducive for severe infection. One current example of a transboundary plant disease
which can have a severe impact on global food production is the black stem rust of
wheat caused by Puccinia graminis tritici race Ug99, a virulent strain which has al-
ready spread from Africa to the Middle East and is threatening wheat production in
South Asia [40].
Around 10–16 % of the global harvest is estimated to result in financial losses of
US $ 220 billion annually due to plant diseases [8, 41]. The worldwide actual losses
to plant pathogens in major food crops from 2001–2003 were 10.2, 10.8, and 8.5 %
for wheat, rice, and maize, respectively [8]. However, the limited quantitative data on
crop losses hinders estimation of crop losses with significant effects on food security
[37, 42]. According to Zeigler and Savary [43], plant diseases are key yield reducers.
Any factor which reduces actual yield will impede increase in rice productivity and
high elasticity in rice production-consumption; factors needed to prevent spikes in
cereal prices which can lead to food crises.

1.2 Effects of climate change on plant diseases caused by

mycotoxigenic fungi

The ability to predict the effects of climate change on plant pathogens and subse-
quently on yield is limited due to lack of data because studies have focused on individ-
ual diseases rather than a complete set [2, 9]. Studies showed that climate change can
have positive, negative or neutral effects on individual pathosystems due to the spe-
cific nature of the host-pathogen interaction [44]. Indeed, the interaction of direct ef-
fects of climate change factors and indirect effects of global change factors contribute
to pathosystem complexity under climate change, thereby hindering attempts to gen-
eralize pathogen responses [9, 45–47]. A recent analysis indicated that accelerated
evolution and the changing geographic distribution of plant diseases are the main ef-
fects of climate change on plant pathogens [48]. Climate is a potent selective force in
natural populations [49, 50] and can alter selection in host-parasite interactions [51].

1.2.1 Epidemiology and resistance

Climate change can alter stages and rates of pathogen development and modify host
resistance and host-pathogen interactions [6, 44]. The assessment of climate change
effects on fungal colonization and growth, and on mycotoxin production needs to be
based on individual pathogens due to the different optimum conditions of tempera-
ture and water activity for growth and mycotoxin production [52]. The two most im-
portant factors affecting mycotoxigenic fungi are water availability or moisture and
temperature [53, 54].
Tab. 1.1: A summary of recent findings on the influence of elevated CO2 on disease intensity and mycotoxin and fitness of mycotoxigenic fungi.

Disease Pathogen Crop Disease/Mycotoxin at elevated CO2 Fitness/Aggressiveness Reference

Crown rot Fusarium pseudo- Wheat Increased fungal biomass and stem No difference in saprophytic fitness be- Melloy et al. [63]
graminearum browning; tween CO2 levels
Stem browning increased by 68 % without
irrigation in partially resistant cv. 249 and
not influenced by irrigation in susceptible
cv. Tamaroi
Crown rot Fusarium pseudo- Wheat Disease incidence increased with crop- Aggressiveness increased by up to 110 % Khudhair et al. [61]
graminearum; ping cycles in susceptible cv. Tamaroi but after 5 cropping cycles at both CO2 levels.
Fusarium culmorum not in resistant cv. 249. F. pseudograminearum increased fre-
Resistance was induced in susceptible quency on susceptible cv. Tamaroi and
cv. Tamaroi. decreased frequency on resistant cv. 249.
Reduced deoxynivalenol in grains
Ear rot Fusarium Maize Enhanced susceptibility; Vaughan et al. [62]
verticillioides Reduced fumonisin levels
6 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 7

[Link] Elevated CO2

There is limited knowledge about the effects of elevated CO2 on mycotoxigenic fungi
especially in the field. Previous in vitro studies have shown that mycotoxigenic fungi
can tolerate concentrations of CO2 which are much higher than the concentration pro-
jected under climate change scenarios [55]. Furthermore, fungal species growth and
mycotoxin production interact with other factors such as moisture, temperature, and
nutrients [56]. Based on the study of Samapundo et al. [57], 10 % CO2 completely inhib-
ited fumonisin B1 production by Fusarium verticillioides, but 40 % CO2 is needed to in-
hibit fumonisin B1 production of F. proliferatum at 0.984 water activity (a w ). A modified
atmosphere containing 20 % CO2 generally inhibited mold growth, while 20–60 % CO2
significantly reduced mycotoxin production by Fusarium, Aspergillus, and Penicillium
spp. [58]. Regardless of moisture and temperature, latent periods preceding fungal
growth were significantly increased by > 5 % CO2 , while sporulation was unaffected
by increased CO2 [56]. In free air carbon enrichment (FACE) studies which provide
a more realistic climate change assessment of plant and disease interactions under
natural field conditions [59], elevated CO2 altered plant growth and development and
increased disease levels of necrotrophic pathogens [60]. However, the effect of ele-
vated CO2 on mycotoxin production and disease levels varied. Elevated CO2 reduced
DON levels in wheat grains but increased Fusarium crown rot incidence [61], while in
maize it reduced fumonisin levels but enhanced susceptibility to F. verticillioides [62].
Disease resistance can interact with elevated CO2 and other environmental condi-
tions, as shown in Fusarium diseases of wheat (Tab. 1.1). In a FACE experiment, Melloy
et al. [63] found that at elevated CO2 , crown rot interacted with moisture conditions
and disease resistance with greater effect on the partially resistant cultivar. In the 2007
dry season, stem browning and pathogen biomass increased at elevated CO2 in both
susceptible cv. Tamaroi and partially resistant cv. 249 because F. pseudograminearum
grows best under dry conditions of −1 mpa [64]. However in the 2008 wet season,
pathogen biomass decreased at elevated CO2 on both cvs. Tamaroi and 249 but the
differences were not significant. In another FACE experiment over five wheat cropping
cycles, Fusarium crown rot incidence increased with cropping cycles in susceptible cv.
Tamaroi but not in partially resistant cv. 249 [61].
Induced resistance was observed in Fusarium crown rot in a FACE experiment
of continuous wheat cropping, in which elevated CO2 induced partial resistance in
susceptible cv. Tamaroi but not in partially resistant cv. 249 (Tab. 1.1). However, the
induced resistance was observed only in the first three of five cropping cycles, indicat-
ing that it is transient and inadequate to reduce crown rot or impede the selection and
enrichment of highly aggressive strains in the pathogen population [61]. Induced tran-
sient resistance was also observed in another necrotrophic pathogen, Colletotrichum
gloeosporioides, causing anthracnose disease of Stylosanthes, where resistance was
induced in plants at elevated CO2 but failed to operate when plants raised in a con-
trolled environment at elevated CO2 were exposed to pathogen inoculum under am-
8 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

bient CO2 in the field [65]. The relationship between resistance and aggressiveness
needs to be investigated, as aggressiveness interacted with resistance to F. pseudo-
graminearum [61].

[Link] Elevated temperature

Temperature governs the growth and development rates of the different stages of the
pathogen life cycle [66]. Elevated temperature can modify host physiology and resis-
tance [44]. The effects of temperature on mycotoxigenic fungal growth and mycotoxin
production in vitro and in vivo have been determined in numerous studies and sum-
marized in many reviews [56, 67–69].
Projected higher temperatures in the next decades will possibly affect the preva-
lence of different mycotoxigenic fungal species and their growth, epidemiology, and
mycotoxin production. F. graminearum favors the warm climate of southern Europe
[52], and has become the dominant species responsible for Fusarium head blight in
wheat in Europe, replacing F. culmorum based on surveys [16, 70–72]. This shift is pos-
sibly due to the higher optimum temperature range of F. graminearum. In Belgium,
F. graminearum was predominant in 2004–2005 due to warm weather, while F. culmo-
rum was dominant in 2001–2002 due to a low average July temperature of 17.4 °C [73].
For F. verticillioides, the risk of infection is high in areas with high temperatures (sub-
tropical) than in temperate areas [74]. The systemic transmission of F. verticillioides
from plant to kernels was increased at above average temperatures [75]. Fumonisin
risk is typically higher at lower altitudes and latitudes due to warm conditions than
high altitude and latitude regions [76].
Temperature influences the fungal growth and aflatoxin production of Aspergillus
flavus in maize [56, 77]. The infection of A. flavus on maize ears is favored by high
temperatures of 35–38 °C [78]. Paterson and Lima [77] stated that as temperature is
projected to increase in temperate regions due to climate change, the risk of aflatoxin
contamination increases based on the optimum temperature range of 30–33 °C. The
percentage of highly toxigenic S strain of A. flavus communities increased as soil tem-
perature increased from 16–32 °C, while the overall propagule density increased from
20–28 °C, suggesting that global warming would likely allow the S strain to dominate
contaminated areas and increase aflatoxin contamination [79]. On the other hand,
heat waves or extreme temperature can also be detrimental to aflatoxin production.
A study showed that aflatoxin production was optimum at 28–30 °C but production
stopped at 37 °C because aflatoxin biosynthesis was turned off [80].
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 9

[Link] Extreme rainfall

Above average rainfall has been attributed to the occurrence of Fusarium head blight
epidemics. In North and South Dakota, USA in 1993, 250–600 % above normal pre-
cipitation was observed during a severe Fusarium head blight epidemic [81]. In the
2003 Fusarium head blight epidemic in southeastern USA, post-flowering rainfall was
the most important weather variable that drove the epidemic [20]. Monthly average
rainfall during anthesis and post anthesis was 10–150 % higher than long term aver-
ages when an outbreak of Fusarium head blight and DON contamination occurred in
Australia in 2010 [82]. Similar severe epidemics of Fusarium head blight occurred in
Norway from 2008–2012 when precipitation was above normal during anthesis and
grain maturation [83].
Erratic rainfall patterns and high rain intensity can play a significant role in high
levels of moisture in harvested grains leading to deterioration of grain quality, fungal
growth, and mycotoxin contamination [55, 84, 85]. Unseasonable rains during harvest
probably caused the aflatoxin contamination of maize stored under damp conditions
which led to the 2004 Kenyan aflatoxicosis [28]. However, effects of climate change on
stored grain are complex because moisture and temperature can interact with biotic
factors such as insect pests to influence fungal species composition and dominance
and mycotoxin production [55, 56, 77, 86].

[Link] Drought
The occurrence of drought episodes influences the growth and development of my-
cotoxigenic fungi and mycotoxin production in major food crops. In maize, environ-
mental conditions leading to drought or water stress resulted in increased risk of fu-
monisin contamination by F. verticillioides but not F. proliferatum [87]. Severe wheat
kernel rot due to F. pseudograminearum ensues when drought occurs post anthesis, as
shown by “whiteheads”, shriveled grains, or no grains [88]. The occurrence of severe
crown rot epidemics in drought-stressed environments may be due to an evolution-
ary response which recognizes polyamines in response to water stress. Polyamines
are plant metabolites produced in response to abiotic stress such as water stress [89].
Spray inoculation of F. graminearum at mid-anthesis led to an increase in polyamines,
fungal biomass, and DON in spike tissue [90].
Drought stress in addition to high temperature favors the growth, conidiation, and
dispersal of A. flavus in maize with increased silk cut which compromises kernel in-
tegrity [91]. In Europe, hot and dry weather contributed to the 2003 outbreak of the
previously uncommon A. flavus [55, 92]. Water stress also influences the composition
of the communities of mycotoxin producers present. A. flavus, a more xerotolerant
species than F. verticillioides, was able to colonize maize at the ripening stage by out-
competing the non-xerophilic Fusarium species [56]. A. flavus aflatoxin producers are
associated with hot and dry agroecological zones [93].
10 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

[Link] Interactions of temperature and moisture

Quantitative knowledge of the interactions of climate change variables on mycotox-
igenic fungi has been integrated into contour maps, for example the interaction of
temperature and water availability on mycotoxigenic fungal growth and mycotoxin
production [56, 69]. These data are important in generating baseline information for
the understanding of basic relationships under climate change. For example, predic-
tion of a 3 °C increase in temperature at water stressed conditions of 0.9 and 0.95 a w
showed no change in maximum growth rates of F. verticillioides and F. graminearum
and a reduction in the maximum growth rate of A. flavus [56].
Temperature, moisture, and relative humidity are the most important climatic
factors affecting Fusarium head blight development and DON accumulation [54, 94].
Fusarium head blight is favored by warm and wet weather at anthesis, resulting in
partial or complete head blighting, reduced yield and quality, and mycotoxin produc-
tion [84]. Window pane analysis using rank-based nonparametric correlation showed
that the highest correlation was observed between Fusarium head blight intensity and
15–30 day windows (periods) during the final 60 day period (near anthesis) of com-
bined moisture and temperature [95].
High temperature and drought stress are key factors for A. flavus growth and afla-
toxin production [91, 96, 97]. Aflatoxin contamination occurs in two phases: during
crop development due to physiologic stress or insect activity in the preharvest phase,
and after maturation, either prior to harvest or postharvest during transport and stor-
age in the second phase. Hot, dry conditions during crop development favor the first
phase of contamination, while rain and warm temperatures with high humidity favor
the second [98]. The developing maize crop is frequently resistant to A. flavus infec-
tion, but heat or drought stress and insect damage can compromise kernel integrity
by increased “silk cut” [99]. Low rainfall and maximum temperature were found to be
related to aflatoxin contamination in maize in various locations in Georgia, USA [100].
Relationships have been observed between teleconnections or variations in cli-
mate patterns in different regions of the globe and Fusarium head blight disease of
wheat. The risk of Fusarium head blight was higher during El Niño or “neutral” years
than La Niña years, when rainfall is higher in spring months in El Niño years [101].
In Ohio, USA, the Fusarium head blight epidemic risk occurs about a year following
La Niña, while risk is low about a year after an El Niño episode. The epidemic can be
location specific, however [95].

1.2.2 Pathogen population genetics and evolution

The impacts of climate change on the risk of mycotoxigenic fungal infection and myco-
toxin production are complicated by concomitant effects of fungal species composi-
tion [76, 102] and evolutionary adaptation [48]. Shifts in the population composition of
mycotoxigenic fungi have been observed, which may indicate adaptive evolution from
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 11

nonrandom gene flow [48]. Fusarium head blight communities can produce different
epidemics due to shifts in population composition which could be due to a chang-
ing climate [45, 103, 104]. Populations of F. graminearum, F. pseudograminearum, and
F. culmorum are highly diverse in different countries and continents, and even indi-
vidual fields with high gene flow, and therefore highly flexible in adapting to the en-
vironment as shown by rapid evolutionary changes on a large geographical scale [16].
The ability to evolve new phenotypes and genotypes via sexual recombination in As-
pergillus might be accelerated by environmental stressors under climate change, such
as intense heat and drought [105]. Most mycotoxins are mutagenic, and the rate of
mycotoxin formation and mutation could increase under climate change [55].
Different environmental conditions may have driven epidemics of different Fusar-
ium species. Canonical correlation analysis showed associations of F. graminearum
with warm and humid conditions, F. culmorum with cooler, wet and humid conditions,
and F. poae with drier and warmer conditions in wheat [106]. The increase in occur-
rence of F. graminearum in Europe may be due to its adaptation to cooler regions or
climate change may have led to regions becoming warmer [102]. In the Netherlands in
the 1980s–1990s, F. culmorum was the most predominant species but F. graminearum
was more predominant in Western Europe from 2000 [16, 71, 103]. F. asiaticum occurs
in warm regions > 15 °C while F. graminearum occurs in cooler regions in China [107].
Different environmental conditions affect composition of the Fusarium species in
maize. In Europe, red ear rot (fusariosis), primarily caused by F. graminearum, results
in contamination of ears with DON, zearalenone (ZEA), and nivalenol (NIV) [108]. It is
severe in locations and years with frequent rainfall and low temperatures in summer
and early fall [109]. Pink ear rot, caused by F. verticillioides and F. proliferatum, oc-
curs frequently in warm, dry conditions, while pink ear rot, caused by F. subglutinans,
occurs in cold, humid conditions [110]. Drought stress and temperatures above 25 °C
favor F. verticillioides over F. graminearum in maize [94].
Shifts in the Fusarium chemotype or strain producing a type of trichothecene type
B toxin were observed in recent epidemics which can be attributed to changes in en-
vironmental conditions. DON chemotype strains of F. graminearum are classified into
two groups: (1) DON-chemotype 1A, producing DON and 3-acetylated deoxynivalenol
(3ADON), mostly European strains from warmer regions, and (2) DON chemotype 1B
producing DON and 15-acetylated deoxynivalenol (15ADON), mostly American strains
from slightly cooler regions [111].
The rapid spread of a highly toxigenic F. graminearum population was observed in
North America, in which 3ADON population chemotype frequency increased > 14 fold
from 1998–2004. However, the basis for the shift remains unclear, although changes in
agricultural practices or environmental conditions may have driven the shift in Fusar-
ium head blight pathogen composition [112]. On exposure to extreme high and low
temperatures, F. graminearum 3ADON showed faster mycelial growth and produced
more DON and ZEA than 15ADON [113]. A similar shift was observed in China, in which
the 3ADON producer of F. asiaticum increased significantly in the middle valley of the
12 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

Yangtze River between 1999 and 2005. This highly toxigenic and aggressive chemo-
type population is spreading east to west in China, which may be due to natural selec-
tion [114]. In controlled conditions, recovery of 15ADON was predominant at 18–22 °C
and 3ADON at 28 °C, and mixed at 24 °C. However, no correlation with chemotype and
temperature or precipitation was found [115].
The shifts from 15ADON to 3ADON chemotypes may be due to a general fitness
advantage, as shown by the higher growth rate and spore production observed by
Ward et al. [112]. However, no detectable advantage of 3ADON isolates over 15ADON
isolates in saprophytic or pathogenic fitness was observed on a susceptible wheat
cultivar [116]. Different components of host-parasite fitness such as infectivity and fe-
cundity are differentially altered by the environment [51]. The shifts are unlikely to
result in higher aggressiveness but indicated by higher DON levels in moderately re-
sistant or susceptible genotypes [117]. Yet one study showed that the 3ADON chemo-
type was more aggressive than the 15ADON and NIV chemotypes [118], the latter being
mostly associated with maize [119]. In an earlier study using a crossing population
of F. graminearum, DON producing progeny were twice as aggressive as NIV produc-
ers [120]. Different inoculation methods and/or environmental conditions may have
caused the differences in the recent work [118], hence more research is needed.
Aggressiveness as a quantitative trait is highly affected by temperature, rainfall,
and relative humidity; and variation in aggressiveness among and within populations
partly determines adaptation and fitness of the pathogen [121, 122]. For example, in a
cross between two European DON-producing isolates of F. graminearum, the progeny ×
environmental interaction was one of the most important sources of variance, ac-
counting for 29 % of total variance for aggressiveness and 19 % for DON production,
suggesting the importance of multi-environmental trials [121].
The strains or morphotypes of A. flavus are adapted to distinct ecological niches.
A. flavus S strain produce more aflatoxin than the L strain isolates [79], and was the
primary cause of the aflatoxin contamination in the 2004 Kenyan epidemic [123]. In the
Sonoran desert, Arizona, USA, A. flavus S strains dominated during the warmest pe-
riod and L strain during winter and spring [124]. The incidence of A. flavus S strain was
also higher in warm than in cold seasons in South Texas, USA [79]. A. flavus S BG strain
(unknown aflatoxin B and G producing strain) was more prevalent in areas with the
highest average temperature [93] and had the highest frequency in crops from semi-
arid and sub-humid parts of West Africa [125]. The variation of S BG incidence across
agroecological zones may be caused partly by crop rotation [126].

1.3 Prediction of climate change effects on epidemics

Forecasting systems are needed for strategic long term decisions [127] such as address-
ing the effects of climate change on plant diseases [45]. Predictive models will provide
the foresight for strategic climate change adaptation and policy guidance [52]. In or-
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 13

der to use plant disease models in forecasting climate change effects, a quantitative
understanding of plant disease epidemiology and rigorous model verification and val-
idation are warranted [128]. Scientifically valid forecasts of climate change effects on
plant diseases are needed to formulate robust food security policies [129].
Quantitative approaches dealing with scenarios and interactions are needed for
impact assessment of climate change effects on plant health [44, 45]. Realistic climate
change scenarios are needed in predictive modeling of risks of mycotoxigenic fungal
growth and mycotoxin production [77]. However, typical scenario analysis may be lim-
ited by simplistic assumptions and there is a need to use more complete scenarios
incorporating thresholds, interactions, and feedback loops [45]. In vitro studies on
interacting factors of elevated CO2 , temperature, and/or moisture on mycotoxigenic
fungal growth and mycotoxin production have been investigated [56]; this can provide
baseline information for simulation modeling [55].

1.3.1 Bioclimatic niche models

Ecological niche or bioclimatic envelope models are correlative models which pre-
dict species distributions with climate variables or through an understanding of
species’ physiological responses to climate change [130]. The bioclimatic envelope
approach can provide a useful first approximation of the potential impact of climate
change [131]. This modeling technique can be used to investigate the effect of cli-
mate change on plant diseases based on climatic data [9], but caution is needed in
the assumption of the climate limits of species distribution and representation of
uncertainties [132].
The effect of climate change on mycotoxin risk was projected in major maize grow-
ing provinces in the Philippines [133] as a case study (Fig. 1.1), and related to food
production and security. Bioclimatic envelope modeling was used to predict the pre-
harvest risks of Aspergillus and Fusarium maize ear rots during dry (first) and wet
(second) cropping seasons based on the projected temperature increase for the year
2050 under the RCP8.5 climate change scenario (Fig. 1.2). The model was developed
based on temperature ranges of A. flavus and F. verticillioides from Sumner and Lee
[134] and Stewart et al. [135], respectively, using R programming [136]. Aflatoxin con-
tamination in agricultural crops is a serious problem in the Philippines because of
high temperatures and high relative humidity [137, 138], while F. verticillioides is the
predominant fumonisin-producing Fusarium species in the country [139, 140].
Comparison of current and predicted distributions of Aspergillus ear rot showed
an increased risk in 2050 in the Philippines (Fig. 1.3). As expected, higher risk was es-
timated during dry season compared to wet season cropping. Under climate change,
medium risk was projected for the province of North Cotabato and Maguindanao,
while high risk was projected for the province of Isabela during dry season cropping
 14 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

Provinces
Bukidnon
20N Isabela
Lanao del Sur
Maguindanao
North Cotabato
South Cotabato

15N

Proportion (%) of production to country’s total

1
2
3
4
10N
5
6
7
8
9
10
5N 11
12
117.5E 120E 122.5E 125E

Fig. 1.1: Map of the Philippines showing major maize producing provinces and their contribution (%)
to the country’s total maize production.

6°C 6°C
Change in temperature

Change in temperature

4°C 4°C

2°C 2°C

0°C 0°C
April May June July Sep Oct Nov Dec
(a) Month (b) Month

Fig. 1.2: Projected change in average monthly temperature for the 1st (a) and 2nd (b) cropping sea-
sons of maize in the Philippines based on IPCC AR5 climate scenario RCP8.5.
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 15

(Tab. 1.2). These results can be explained by the high temperature requirement for
Aspergillus ear rot development observed in the dry season [78].
Comparison of current and predicted distributions of Fusarium ear rot showed
increased risks in 2050 (Fig. 1.4). The current Fusarium risks are medium to high and
low to medium in the dry and wet seasons, respectively. There will be medium to high
risk of Fusarium ear rot infection in both dry and wet seasons. In the major maize
growing areas in the dry season, there will be high risk in Isabela, North Cotabato and
Maguindanao, and medium risk in South Cotabato. However, in the wet season there
will be high risk in North Cotabato and Maguindanao, and medium risk in Isabela
and South Cotabato (Tab. 1.2). These results showed increased Fusarium ear rot risks
in both dry and wet seasons because high temperatures are favorable for Fusarium ear
rot development [135].
These results have significant implications regarding the risk of mycotoxigenic
fungi on maize which could affect food security under climate change. Fumonisin pro-
duction of F. verticillioides isolates was significantly higher in Isabela province as com-
pared to Laguna province [140]. Maguindanao province, with a projected high risk for
Fusarium ear rot and medium risk for Aspergillus ear rot, has the highest proportion of
families (84.5 %) spending more than 50 % of their total expenditure on food. Isabela
province, with high risk for Aspergillus ear rot and Fusarium ear rot, has 64.5 % of
families spending more than 50 % of their total expenditure on food [141].

Tab. 1.2: Projected Aspergillus and Fusarium ear rot preharvest risks for major maize producing
areas in the Philippines based on projected temperature increase for the year 2050 under IPCC
climate change scenario RCP8.5.

Top maize producing Isabela South Bukidnon North Maguin- Lanao

provinces Cotabato Cotabato danao del Sur

Proportion of country’s
total production (%) 12 11 10 7 6 5
Average annual
production (metric tons)a 641 936 583 631 547 155 396 812 335 241 297 977
Aspergillus 1st Cropping High Very low Very low Medium Medium Very low
ear rot
2nd Cropping Low Very low Very low Low Low Very low
Fusarium 1st Cropping High Medium Low High High Very low
ear rot
2nd Cropping Medium Medium Low High High Very low

a Data source: Philippine Statistical Authority-Bureau of Agricultural Statistics [133]

16 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

First Second

20°N Aspergillus risk

Very low

15°N Low

Current
Medium

10°N High

Very high
5°N

20°N

15°N

Projected
10°N

5°N

120°N 125°N 120°N 125°N

Fig. 1.3: Current and projected preharvest risk of Aspergillus ear rot development during the first
and second cropping seasons in the Philippines in 2050 based on projected temperature in-
crease for the year 2050 under the IPCC AR5 climate scenario RCP8.5. Risk categories are: very low
(1–20 %), low (21–40 %), medium (41–60 %), high (61–80 %), and very high (81–100 %).

1.3.2 Climate change scenario models

The modeling approach to simulating plant disease development under future climate
change needs to address model uncertainty and complexity. Uncertainty in model in-
puts can compromise the reliability of simulation results due to the propagation of
errors [44]. To reduce uncertainty, multiple models [45] or a comparison of different
models can be implemented [142]. Climate change effects on plant health can have
direct effects of climate variables and indirect effects via global changes such as crop-
ping practices [9, 47], leading to system complexity [46]. An analytical framework was
developed to evaluate and improve the plant disease model to address complexity.
For Fusarium head blight, complexity arises from having multiple host species, the
importance of spatial components, risk from crop residues, and potential to reduce
ecosystem services such as the production of food and efficiency of conversion of nat-
ural resources into food [45].
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 17

First Second

20°N Fusarium risk

Very low

15°N Low

Current
Medium

10°N High

Very high
5°N

20°N

15°N
Projected

10°N

5°N

120°N 125°N 120°N 125°N

Fig. 1.4: Current and projected preharvest risk of Fusarium ear rot development during the first and
second cropping seasons in the Philippines in 2050 based on projected temperature increase for
the year 2050 under the IPCC AR5 climate scenario RCP8.5. Risk categories are: very low (1–20 %),
low (21–40 %), medium (41–60 %), high (61–80 %) and very high (81–100 %).

Predictions of risks of disease intensity and mycotoxin contamination under climate

change from different studies are shown in Table 1.3. Qualitative assessments based
on expert knowledge of epidemiology indicated no increase [143–145], but this method
serves as an initial step in climate change impact assessment. The simulation results
using coupled climate disease and crop models showed increased [146–148] or de-
creased risks [149]. Simulated risk variability [150, 151] and inconsistency among stud-
ies indicate the influences of model uncertainties and spatial and climatic variation
between regions [47, 50, 152]. Application of current Fusarium head blight disease and
mycotoxin models in new regions or countries (models developed elsewhere) yielded
poor results, indicating site and year specificity as in descriptive models [82, 146, 148,
153] prompting the need for thorough field validation of models before use. The com-
parison of simulation results is difficult across different approaches in climate change
research considering spatial and temporal variations in many interacting factors such
as crop development, cultivar, isolate or species, and climate [152].
Tab. 1.3: A summary of mycotoxigenic fungal disease and mycotoxin predictive models used to predict climate change impacts.

Country Disease Crop Model Prediction Reference

Brazil Fusarium head blight Wheat Linked process based model Increase in Passo Fundo and Fernandes et al. [150]
(Fusarium graminearum) Estanzuela; no change in Perga-
mino
Canada Fusarium head blight Wheat Qualitative assessment No change Boland et al. [143]
(Fusarium spp.)
Canada Fusarium ear rot Maize Qualitative assessment Increase Boland et al. [143]
UK Fusarium head blight Wheat Qualitative assessment (Ecotype) Slight increase Madgwick et al. [144]
Sweden Fusarium head blight Wheat Qualitative assessment Increase in mycotoxin levels Roos et al. [145]
due to more humid climate
UK Fusarium head blight Wheat Combined crop and disease Increase in Southern England West et al. [168]
model by 2050s
Europe Aspergillus flavus Maize A .flavus – AFB1 model Risk increase in maize Battilani et al. [151]
Aflatoxin Wheat Low risk in wheat
Rice Absent in rice
Europe Fusarium head blight Wheat DON prediction model Increase in DON levels by a factor Van der Fels-Klerx et al. [147]
DON of 3
Netherlands Fusarium head blight Winter wheat DON prediction model Decrease (HG model) and no Van der Fels-Klerx et al. [149]
DON Maize effect (KNM1 climate model)
in maize
18 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

Slight decrease in DON in wheat

(both climate models)
China Fusarium head blight Wheat Logistic weather based regres- Increase in southern locations in Zhang et al. [148]
sion model Anhui province in 2020–2050
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 19

1.4 Management of plant diseases caused by mycotoxigenic

fungi under climate change

When ensuring food security under climate change, the primary basis of developing
effective plant disease management strategies in major food crops is realistic predic-
tion of climate change impacts on plant diseases. The combined effects of climate and
global changes may have unexpected consequences [9]. Modeling efforts should be
able to reduce model uncertainty and address complexity [45]. Mechanistic incorpo-
ration of pathogens in crop models could produce more realistic predictions of crop
production on a regional scale which could aid the formulation of appropriate food
security policies [34, 129].
Investment in adaptation and mitigation strategies is necessary to prevent the
negative impacts of climate change on plant diseases via crop losses hampering
progress in achieving food security. Resilience to climate change requires an inte-
grated approach which addresses all dimensions of the food system [32], with par-
ticular attention to reducing climate change vulnerability [154]. A practical approach
is to prepare for all likely eventualities, but risks based on probabilities generated
by stochastic models can better guide a judicious and effective development of man-
agement options [155]. Thus, diverse disease management strategies can be used
involving participatory and interdisciplinary approaches [47]. There is a need to eval-
uate the efficacy of current disease management strategies and develop new disease
management tools and methods [84].
Reducing the level of infection of mycotoxigenic fungi and associated mycotoxin
production in grains is the foremost requirement in securing crop yields to guarantee
food security. Necrotrophic pathogens such as Aspergillus and Fusarium species have
wide host ranges and do not follow gene-for-gene specificity, thus lacking major genes
for resistance [27, 156]. Fusarium head blight resistance is a complex quantitative trait
which depends on environmental conditions. Partial resistance needs to be combined
with agronomic practices to develop robust integrated disease management strategies
[84, 156]. Breeding for passive Fusarium head blight resistance based on morpholog-
ical traits such as canopy and spike architecture involving plant height and anther
extrusion, and physiological traits such as flowering date [156] need to consider the
modifying effects of elevated CO2 and temperature on disease resistance, canopy ar-
chitecture, and microclimate [157, 158]. When the environment is highly favorable for
Fusarium head blight infection, implementation of a single management strategy fails
and the use of disease resistance and fungicides is necessary to achieve the 75 % re-
duction in Fusarium head blight index required to manage the disease [159].
20 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

1.5 Outlook and conclusions

An improved understanding of the effects of climate change on biological and food

systems is a critical step towards addressing the impacts of climate change on food se-
curity [160], which includes the effects on pests, pathogens, and weeds. The changing
geographic distribution of mycotoxigenic fungal species composition and chemotypes
in cereals and related accelerated evolution under climate change are paramount re-
search topics which need to be addressed [48]. Research is also needed to study prob-
able mycotoxigenic fungal shifts in rice due to the recent emergence of Fusarium fu-
jikuroi causing bakanae disease, previously a minor disease, in the Philippines [161,
162], and infection of rice by Fusarium proliferatum in Costa Rica [163]. In the first
study, the most important sources of variation of aggressiveness of F. fujikuroi are
isolate and isolate-environment interaction accounting for about 34 % and 42 %, re-
spectively, of the total variance for PSBRc82 and IR42 varieties [162]. Basic research is
needed to study the effects of the main climate change variables: elevated CO2 , tem-
perature, and moisture and their interactions on mycotoxigenic fungal diseases and
mycotoxins since comprehensive knowledge is still lacking [55, 56, 76].
Realistic predictions of climate change impact on mycotoxin and disease risk
through the development of reliable predictive models are imperative to minimize pro-
duction losses and achieve food security. Approaches to model improvement should
address model uncertainty and complexity [46, 47, 50]. Monitoring and ‘early warning’
of mycotoxins and application of geographic information systems and geostatistics
are important research needs in surveillance [9, 56, 164, 165].
The formulation of adaptive disease management strategies is the key to ensuring
food security under climate change. A shift to adaptation and mitigation strategies
is needed in addition to impact assessment. Current disease management strategies
should be evaluated for climate change adaptation but novel technologies will be very
helpful [84, 166, 167].

References

[1] IPCC. Summary for policymakers. In: Stocker TF, Qin D, Plattner GK, et al., eds. Climate
Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assess-
ment Report of the Intergovernmental Panel on Climate Change Cambridge, United Kingdom
and New York, NY, USA: Cambridge University Press; 2013.
[2] IPCC. Summary for policymakers. In: Field CB, Barros VR, Dokken DJ, et al., eds. Climate
Change 2014: Impacts, Adaptation, and Vulnerability. Part A: Global and Sectoral Aspects.
Contribution of Working Group II to the Fifth Assessment Report of the Intergovernmental
Panel on Climate Change Cambridge, United Kingdom and New York, NY, USA: Cambridge
University Press; 2014. p. 1–32.
[3] Godfray HCJ, Beddington JR, Crute IR, et al. Food security: the challenge of feeding 9 billion
people. Science 2010;327:812–818.
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 21

[4] Lal R. Food security in a changing climate. Ecohydrology and Hydrobiology 2013;13:8–21.
[5] Porter M, Xie L, Challinor AJ, et al. Food Security and Food Production Systems. In: Field CB,
Barros VR, Dokken DJ, et al., eds. Climate Change 2014: Impacts, Adaptation, and Vulner-
ability. Part A: Global and Sectoral Aspects. Contribution of Working Group II to the Fifth
Assessment Report of the Intergovernmental Panel on Climate Change Cambridge, United
Kingdom and New York, NY, USA: Cambridge University Press; 2014. p. 1–82.
[6] Rosenzweig C, Iglesias A, Yang XB, Epstein PR, Chivian E. Climate change and extreme
weather events: Implications for food production, plant diseases, and pests. Global Change
and Human Health 2001;2:90–104.
[7] Rosenzweig C. Climate change and agriculture. In: Meyers RA, ed. Extreme Environmental
Events: Complexity in Forecasting and Early Warning. Springer Reference 2011. p. 31–41.
[8] Oerke EC. Crop losses to pests. J Agr Sci 2006; 144: 31–43.
[9] Savary S, Nelson A, Sparks AH, et al. International agriculture research tackling the ef-
fects of global and climate changes on plant diseases in the developing world. Plant Dis
2011;95:1204–1216.
[10] Hellin J, Shiferaw B, Cairns JE, et al. Climate change and food security in the developing
world: Potential of maize and wheat research to expand options for adaptation and mitiga-
tion. Journal of Development and Agricultural Economics 2012;4:311–321.
[11] Esker PD, Savary S, McRoberts N. Crop loss analysis and global food supply: focusing now
on required harvests. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition
and Natural Resources 2012;7:1–14.
[12] Savary S, Ficke A, Aubertot JN, Hollier C. Crop losses due to diseases and their implications
for global food production losses and food security. Food Sec 2012;4:519–537.
[13] Bottalico A, Perrone G. Toxigenic Fusarium species and mycotoxins associated with head
blight in small-grain cereals in Europe. Eur J Plant Pathol 2002; 108: 611–624.
[14] Osborne LE, Stein JM. Epidemiology of Fusarium head blight on small-grain cereals. Int J Food
Microbiol 2007;119:103–108.
[15] Chakraborty S, Liu CJ, Mitter V, et al. Pathogen population structure and epidemiology
are keys to wheat crown rot and Fusarium head blight management. Australas Plant Path
2006;35:643–455.
[16] Miedaner T, Cumagun CJR, Chakraborty S. Population genetics of three important head blight
pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. J Phytopathol
2008;156:129–139.
[17] McMullen M, Jones R, Gallenberg D. Scab of wheat and barley: A re-emerging disease of dev-
astating impact. Plant Dis 1997;81:1340–1348.
[18] McMullen M, Bergstrom G, De Wolf ED, et al. A unified effort to fight an enemy of wheat and
barley: Fusarium head blight. Plant Dis 2012;96:1712–1728.
[19] Nganye WE, S. K, Wilson WW, Leistritz FL, Bangsind DA. Economic Impacts of Fusarium Head
Blight in Wheat and Barley: 1993–2001. Fargo, Narth Dakota: Agricultural Experiment Station
North Dakota State University, 2004.
[20] Cowger C, Sutton AL. The southwestern U.S. Fusarium head blight epidemic of 2003. Plant
Health Prog 2005.
[21] Charmley LL, Trenholm HL, Prelusky DA, Rosenberg A. Economic losses and decontamination.
Nat Toxins 1995; 3: 99–203.
[22] Bryden Wl. Mycotoxins in the food chain: human health implications. Asia Pac J Clin Nutr
2007;16:95–101.
[23] CAST. Mycotoxins: Risks in plant, animal, and human systems systems. Ames, Iowa, Council
for Agricultural Science and Technology, 2003.
22 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

[24] Wu F. Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts.
Transgenic Res 2006;15:277–289.
[25] Institute M. Economic impact of aflatoxin: Aflatoxin’s negative impact on trade. 2014.
[26] Wise K. Diseases of Corn: Corn Disease Loss Estimates From the United States and Ontario,
Canada - 2012: Purdue University, 2013.
[27] Marasas WF, Gelderbrom WCA, Shephard GS, Vismer HF. Mycotoxins: A global problem. In:
Leslie JF, Bandyopadhyay R, Visconti A, eds. Mycotoxins: Detection Methods, Management,
Public Health and Agricultural Trade. Wallingford, UK: CAB International; 2008. p. 29–39.
[28] Lewis L, Onsongo M, Njapau H, Schurz-Rogers H, Luber G, Kieszak S. Aflatoxin contamina-
tion of commercial maize products during an outbreak of acute aflatoxicosis in Eastern and
Central Kenya. Environ Health Persp 2005;113:1763–1777.
[29] Lubulwa ASG, Davis JS. Estimating the social costs of the impacts of fungi and aflatoxins in
maize and peanuts. In: Highley E, Wright EJ, Banks HJ, Champ BR, eds. Stored product protec-
tion: Proceedings of the 6th International Working Conference on Stored-product Protection,
Wallingford, UK: CAB International: 1994.
[30] FAO, WFP, IFAD. The State of Food Insecurity in the World 2012. Economic Growth is Neces-
sary but Not Sufficient to Accelerate Reduction of Hunger and Malnutrition. Rome, Italy: FAO;
2012.
[31] Lobell DB, Burke MB, Tebaldi C, Mastrandea MD, Falcon WP, Naylor RL. Prioritizing climate
change adaptation needs for food security in 2030. Science 2008;319:607–610.
[32] Wheeler T, von Braun J. Climate change impacts on global food sesurity. Science
2013;341:508–513.
[33] Vermeulen SJ, Campbell BM, Ingram JSI. Climate change and food systems. Ann Rev Environ
Resour 2012;37:195–222.
[34] Gregory PJ, Johnson RH, Newton AC, Ingram JSI. Integrating pests and pathogens into the
climate change/food security debate. J Exp Bot 2009;60:2827–2838.
[35] Nelson GC, Rosegrant MW, Palazzo A, et al. Food Security, Farming, and Climate Change to
2050: Scenarios, Results, Policy Options. Washington, DC: International Food Policy Re-
search Institute; 2010.
[36] FAO. Rome Declaration and World Food Summit Plan of Action. Rome, Italy: FAO; 1996.
[37] Flood J. The importance of plant health to food security. Food Sec 2010; 2: 215–231.
[38] Carefoot GL, Sprott ER. Famine on the Wind Chicago: Rand McNally; 1967.
[39] Padmanabhan SY. The great Bengal famine. Ann Rev Phytopathol 1973;11:11–26.
[40] Singh RP, Hodson DP, Huerta-Espino J, et al. The emergence of Ug99 races of the stem rust
fungus is a threat to world wheat production. Ann Rev Phytopathol 2011;49:465–481.
[41] Strange RN, Scott PR. Plant disease: A threat to global food security. Ann Rev Phytopathol
2005;43:83–116.
[42] Pinstrup-Andersen P. Food security: definition and measurement. Food Sec 2000;1:5–7.
[43] Zeigler RS, Savary S. Plant diseases and the world’s dependence on rice. In: Strange RN,
Gullino ML, eds. The Role of Plant Pathology in Food Safety and Food Security. Dordrecht:
Springer; 2010. p. 3–9.
[44] Coakley SM, Scherm H, Chakraborty S. Climate change and plant disease management. Ann
Rev Phytopathol 1999;37:399–426.
[45] Garrett KA, Forbes GA, Savary S, et al. Complexity in climate-change impacts: an analytical
framework for effects mediated by plant disease Plant Pathol 2011;60:15–30.
[46] Juroszek P, Tiedemann AV. Plant pathogens, insect pests, andweeds in a changing global
climate: a review of approaches, challenges, research gaps, key studies and concepts. J Agr
Sci 2012.
[47] Pautasso M, Doring TF, Garbelotto M, Pellis L, Jeger MJ. Impacts of climate change on plant
diseases – opinions and trends. Eur J Plant Pathol 2012; 133: 295–313.
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 23

[48] Chakraborty S. Migrate or evolve: options for plant pathogens underclimate change. Glob
Change Biol 2013;19:1985–2000.
[49] Jump AS, Penuelas J. Running to stand still: Adaptation and the resopnse of plants to rapid
climate change. Ecol Lett 2005;8:1010–1020.
[50] Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE. Climate change effects on plant dis-
ease: Genomes to ecosystems. Ann Rev Phytopathol 2006; 44: 489–509.
[51] Wolinksa J, King KC. Environment can alter selection in host-parasite interactions. Trends
Parasitol 2009;25:236–244.
[52] Miraglia M, Marvin HJP, Kleter GA, et al. Climate change and food safety: An emerging issue
with special focus on Europe. Food Chem Toxicol 2009;47:1009–1021.
[53] Magan N. Fungi in extreme environments. In: Kubicek CP, Drizhinina IS, eds. Environmental
and Microbial Relationships. The MYCOTA IV. 2nd ed. Berlin, Germany: Springer Verlag; 2007.
p. 85–103.
[54] Wegulo SN. Factors influencing deoxynivalenol accumulation in small grain cereals. Toxins
2012;4:1157–1180.
[55] Paterson RRM, Lima N. Further mycotoxin effects from climate change. Food Res Int
2011;44:2555–2566.
[56] Magan N MA, Aldred D. Possible climate-change effects on mycotoxin contamination of food
crops pre- and postharvest. Plant Pathol 2011;60:150–163.
[57] Samapundo S, De Meulenaer B, Atukwase A, Debevere J, Devlieghere F. The influence of mod-
ified atmospheres and their interaction with water activity on the radial growth and fumon-
isin B1 production of Fusarium verticillioides and F. proliferatum on corn. Part I: The effect of
initial headspace carbon dioxide concentration. Int J Food Microbiol 2007;114:160–167.
[58] Hocking AD. Responses of fungi to modified atmospheres. Fumigation and Controlled At-
mosphere Storage of Grain. Proceedings of an International Conference 1989; Singapore.
p. 70–82.
[59] Chakraborty S, Luck J, Hollaway G, et al. Impacts of global change on diseases of agricultural
crops and forest trees. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition
and Natural Resources 2008;3:1–15.
[60] Eastburn DM, McElrone AJ, Bilgin DD. Influence of atmospheric and climatic change on plant-
pathogen interactions. Plant Pathol 2011;60:54–69.
[61] Khudhair M, Melloy P, Lorenz DJ, et al. Fusarium crown rot under continuous cropping of sus-
ceptible and partially resistant wheat in microcosms at elevated CO2 . Plant Pathol 2013;1–11.
[62] Vaughan MM, Huffaker A, Schmelz EA, et al. Effects of elevated [CO2 ] on maize defence
against mycotoxigenic Fusarium verticillioides. Plant Cell Environ 2014.
[63] Melloy P, Hollaway G, Luck J, Norton R, Aitken E, Chakraborty S. Production and fitness of
Fusarium pseudograminearum inoculum at elevated carbon dioxide in FACE. Glob Change
Biol 2010;16:3363–3373.
[64] Singh DP, Backhouse D, Kristiansen P. Interactions of temperature and water potential indis-
placement of Fusarium pseudograminearum from cereal residues by fungal antagonists. Biol
Control 2009;48:188–195.
[65] Pangga IB, Chakraborty S, Yates D. Canopy size and induced resistance in Stylosanthes
scabra determine anthracnose severity at high CO2 . Phytopathology 2004;94:221–227.
[66] Agrios GN. Plant Pathology 5th ed. UK: Elsevier; 2005.
[67] Doohan FM, Brennan J, Cooke BM. Influence of climatic factors on Fusarium species
pathogenic to cereals. Eur J Plant Pathol 2003;109:755–768.
[68] Champeil A, Doré T, Fourbet JF. Fusarium head blight: epidemiological origin of the effects of
cultural practices on head blight attacks and the production of mycotoxins by Fusarium in
wheat grains. Plant Sci 2004;166:1389–1415.
24 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

[69] Sanchis V, Magan N. Environmental conditions affecting mycotoxins. In: Magan N, Olsen M,
eds. Mycotoxins in Food: Detection and Control. Boca Raton: CRC Press; 2004. p. 174–179.
[70] Waalwijk C, Kastelein P, Vries PM, et al. Major changes in Fusarium spp. in wheat in the
Netherlands. Eur J Plant Pathol 2003;109:743–754.
[71] Jennings P, Coates ME, Turner JA, Chandler EA, Nicholson P. Determination of deoxynivalenol
and nivalenol chemotypes of Fusarium culmorum isolates from England and Wales by PCR
assay. Plant Pathol 2004;53:182–190.
[72] Yli-Mattila T, Rämö S, Hietaniemi V, Hussien T, Lopez ALC, Cumagun CJR. Molecular quantifi-
cation and genetic diversity of toxigenic Fusarium species in Northern Europe as compared to
those in southern Europe. Microorganisms 2013;1:162–174.
[73] Isebaert S, De Saeger S, Devreese R, Verhoeven R, Maene P, Heremans B. Mycotoxin-
producing Fusarium species occurring in winter wheat in Belgium (Flanders) during 2002–
2005. J Phytopathol 2009;157:108–16.
[74] de la Campa R, Hooker DC, Miller JD, Schaafsma AW, Hammond BC. Modelling effects of envi-
ronment, insect damage, and Bt genotypes on fumonisin accumulation in maize in Argentina
and the Philippines. Mycopathologia 2005;154:539–552.
[75] Murillo-Williams A, Munkvold G. Systemic infection by Fusarium verticillioides in maize plants
grown under three temperature regimes. Plant Dis 2008;92:1695–1700.
[76] Wu F, Bhatnagar D, Bui-Klime T, et al. Climate change impacts on mycotoxin risks in US
maize. World Myco J 2011;4:79–93.
[77] Paterson RRM, Lima N. How will climate change affect myctotoxins in food? Food Res Int
2010;43:1902–1914.
[78] Jones R, Duncan H, Payne G, Leonard K. Factors influencing infection by Aspergillus flavus in
silk-inoculated corn. Plant Dis 1980;64:859–863.
[79] Jaime-Garcia R, Cotty PJ. Crop rotation and soil temperature influence the community struc-
ture of Aspergillus flavus in soil. Soil Biol Biochem 2010;42:1842–1847.
[80] OBrian GR, Georgianna DR, Wilkinson JR, et al. The effect of elevated temperature on gene
transcription and aflatoxin biosynthesis. Mycologia 2007;99:232–239.
[81] Wiersma JV, Peters EL, Hanson MA, Bouvette RJ, Busch RH. Fusarium head blight in hard red
spring wheat: cultivar responses to natural epidemics. Agron J 1996;88:223–230.
[82] Obanor F, Neate S, Simpfendorfer S, Sabburg R, Wilson P, Chakraborty S. Fusarium gramin-
earum and Fusarium pseudograminearum caused the 2010 headblight epidemics in Aus-
tralia. Plant Pathol 2013;62:79–91.
[83] Sundheim L, Brodal L, Hofgaard IS, Rafoss T. Temporal variation of mycotoxin producing fungi
in Norwegian cereals. Microorganisms 2013;1:188–198.
[84] Chakraborty S, Newton AC. Climate change, plant diseases and food security: an overview.
Plant Pathol 2011;60:2–14.
[85] Marroquin-Cardona AG, Johnson NM, Philips TD, Hayes AW. Mycotoxins in a changing envi-
ronment - A review. Food Chem Toxicol 2014;69:220–230.
[86] Magan M, Hope R, Cairns V, Aldred D. Post-harvest fungal ecology: Impact of fungal growth
and mycotoxin accumulation in stored grain. Eur J Plant Pathol 2003;109:723–730.
[87] Marin P, Magan N, Vazquez C, Gonzalez-Jaen MT. Differential effect of environmental condi-
tions on the growth and regulation of the fumonisin biosynthetic gene FUM1 in the maize
pathogens and fumonisin producers Fusarium verticillioides and Fusarium proliferatum.
FEMS Microbial Ecol 2010;73:303–311.
[88] Luck J, Spackman M, Freeman A, et al. Climate change and diseases of food crops. Plant
Pathol 2011;60:113–121.
[89] Tunali B, Obanor F, Erginbas G, Westecott RA, Nicol J, Chakraborty S. Fitness of three Fusar-
ium pathogens of wheat. FEMS Microbial Ecol 2012;81:596–609.
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 25

[90] Gardiner D, Kazan K, Praud S, Torney F, Rusu A, Manners J. Early activation of wheat
polyamine biosynthesis during Fusarium head blight implicates putrescine as an inducer
of trichothecene mycotoxin production. BMC Plant Biol 2010;10:289.
[91] Cotty J, Jaime-Garcia R. Influence of climate on aflatoxin producting fungi and aflatoxin con-
tamination. Int J Food Microbiol 2007;119:109–115.
[92] Giorni P, Magan N, Pietri A, Bertuzzi T, Battilani P. Studies on Aspergillus section Flavi iso-
lated from maize in northern Italy. Int J Food Microbiol 2007;113:330–338.
[93] Cardwell KF, Cotty PJ. Distribution of Aspergillus Section Flavi among field soils from the four
agroecological zones of the Republic of Benin, South Africa. Plant Dis 2002;86:434–439.
[94] Miller JD. Mycotoxins in small grains and maize: Old problems, new challenges. Food Addi-
tives and Contaminants 2008;25:219–230.
[95] Kriss AB, Paul PA, Madden LV. Relationship between yearly fluctuations in Fusarium head
blight intensity and environmental variables: A window-pane analysis. Phytopathology
2010;100:784–797.
[96] Jones RK, Duncan HE, Hamilton PB. Planting date, harvest date, and irrigation effects on
infection and aflatoxin production by Aspergillus flavus in field corn. Phytopathology
1981;71:810–816.
[97] Payne GA. Aspergillus flavus of maize silk and kernels. Aflatoxin in Maize. Proceedings of the
CIMMYT Workshop 1986, Mexico. p. 119–126.
[98] Cotty PJ. Cottonseed losses and mycotoxins. In: Kirkpatrick TL, Rothrock CS, eds. Com-
pendium of Cotton Diseases. Minnesota: The American Phytopathological Society; 2001.
p. 9–13.
[99] Odvody GN, Spencer N, Remmers J. A description of silk cut, a stress-related loss of kernel
integrity in preharvest maize. Plant Dis 1997;81:439–444.
[100] Salvacion AR, Ortiz BV, Scully BT, Wilson DM, Hoogenboom G, Lee RD. Effect of rainfall and
maximum temperature on corn aflatoxin contamination in the Southeast US. Climate Informa-
tion for Managing Risks 2011, May 24–27, 2011, Orlando, Florida.
[101] Del Ponte EM, Fernandes JMC, Pavan W, Baethgen WE. A model-based assessment of the
impacts of climate variability on Fusarium head blight seasonal risk in southern Brazil. J Phy-
topathol 2009;157:675–681.
[102] Xu X, Nicholson P. Community ecology of fungal pathogens causing wheat head blight. Ann
Rev Phytopathol 2009;47:83–103.
[103] Waalwijk C, van der Lee T, Yang L, de Vries I, Gortz A, Kerma G. Are changes in the compo-
sition of the Fusarium head blight complex caused by climate change? Pests and Climate
Change 2008;240–241.
[104] Yli-Mattila T. Ecology and evolution oftoxigenic Fusarium species in cereals in northern Eu-
rope and Asia. J Plant Pathol 2010;92:7–18.
[105] Moore GG. Sex and recombination in aflatoxigenic Aspergilli: global implications. Front Mi-
crob 2014;5:1–5.
[106] Xu XM, Nicholson P, Thomsett MA, et al. Relationship between the fungal complex causing
Fusarium head blight of wheat and environmental conditions. Phytopathology 2008;98:
69–78.
[107] Qu B, Li HP, Zhang JB, et al. Geographic distribution and genetic diversity of Fusarium
graminearum and F. asiaticum on wheat spikes throughout China. Plant Pathol 2008;57:
15–24.
[108] Marasas WFO, Nelson PE, Toussoun TA. Toxigenic Fusarium Species: Identity and Mycotoxi-
cology. University Park, PA: The Pennsylvania State University Press; 1984.
[109] Bottalico A. Fusarium diseases of cereals: species complex and related mycotoxins profiles in
Europe. J Plant Pathol 1998;80:85–103.
26 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

[110] Logrieco A, Mule G, Moretti A, Bottalico A. Toxigenic Fusarium species and mycotoxins asso-
ciated with maize ear rot in Europe. Eur J Plant Pathol 2002;108:597–609.
[111] Miller JD, Greenholgh R, Wang YZ, Lu M. Trichothecene chemotype of three Fusarium species.
Mycologia 1991;83:121–130.
[112] Ward TJ, Clear RM, Rooney AP. An adaptive evolutionary shift in Fusarium head blight
pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in
North Ameica. Fungal Genet Biol 2008;45:473–484.
[113] Vujanovic V, Goh YK, Daida P. Heat- and cold-shock responses in Fusarium graminearum
3 acetyl- and 15 acetyl-deoxynivalenol chemotypes. The Journal of Microbiology 2012;50:
97–102.
[114] Zhang H, Zhang Z, van der Lee T, et al. Population genetic analysis of Fusarium asiaticum
populations from barley suggest a recent shift favoring 3ADON producers in southern China.
Phytopathology 2010;100:328–336.
[115] Gilbert J, Brûlé-Babel A, Guerrieri AT, et al. Ratio of 3-ADON and 15-ADON isolates of Fusar-
ium graminearum recovered from wheat kernels in Manitoba from 2008 to 2012. Can J Plant
Pathol 2014;36:54–63.
[116] Spolti P, Del Ponte EM, Cummings AYD, Bergstrom GC. Fitness attributes of Fusarium gramin-
earum isoaltes from wheat in New York possessing a 3-ADON or a 15-ADON tricothecene
genotpye. Phytopathology 2014;104:513–519.
[117] von der Ohe C, Gauthier V, Tamburic-Ilincic L, et al. A comparison of aggressiveness and de-
oxynivalenol production between Canadian Fusarium graminearum isolates with 3-acetyl
and 15-acetyldeoxynivalenol chemotypes in field-grown spring wheat. Eur J Plant Pathol
2010;127:407–417.
[118] Malihipour A, Gilbert J, Piercey-Normore M, Cloutier S. Molecular phylogenetic analysis,
trichothecene chemotype patterns, and variation in aggressiveness of Fusarium isolates
causing headblight in wheat. Plant Dis 2012;96:1016–1025.
[119] Szecsi A, Bartok T. Trichothecene chemotypes of Fusarium graminearum from corn in Hun-
gary. Mycotoxin Research 1995;11:85–92.
[120] Cumagun CJR, Bowden RL, Jurgenson JJ, Leslie JF, Miedaner T. Genetic mapping of pathogenic-
ity and aggressiveness of Gibberella zeae (Fusarium graminearum) toward wheat. Phy-
topathology 2004;94:520–526
[121] Cumagun CJR, Miedaner T. Segregation for aggressiveness and deoxynivalenol production
of a population of Gibberella zeae (Fusarium graminearum). Eur J Plant Pathol 2004;110:
789–799.
[122] Cumagun CJR, Vargas MLD, Alviar AN. Evaluation of greenhouse and field aggressive-
ness of Fusarium verticillioides from corn in Laguna province, Philippines. Afr J Agric Res
2011;6:6586–6591.
[123] Probst C, Njapau H, Cotty PJ. Outbreak of an acute aflatoxicosis in Kenya in 2004: Identifica-
tion of the causal agent. Appl Environ Microb 2007;73:2762–2764.
[124] Cotty PJ, Probst C, Jaime-Garcia R. Etiology and management of aflatoxin contamination. In:
Leslie JF, Bandyopadhyay R, Visconti R, eds. Mycotoxins, Detection Methods, Management,
Public Health and Agricultural Trade. Oxfordshire, UK: CAB International; 2008. p. 287–299.
[125] Probst C, Bandyopadhyay R, Cotty PJ. Diversity of aflatoxin-producing fungi and their impact
on food safety in sub-Saharan Africa. Int J Food Microbiol 2014;174:113–122.
[126] Donner M, Atehnkeng J, Sikora RA, Bandyopadhyay R, Cotty PJ. Distribution of Aspergillus
section Flavi in soils of maize fields in three agroecological zones of Nigeria. Soil Biol
Biochem 2009;41:37–44.
[127] Teng PS, Savary S. Implementing the systems approach in pest management. Agr Syst
1992;40:237–264.
 1 Climate change and plant diseases caused by mycotoxigenic fungi | 27

[128] Shaw M. Preparing for changes in plant disease due to climate change. Plant Prot Sci
2009;45:S3-S10.
[129] Ingram JSI, Gregory PJ, Izac A-M. The role of agronomic research in climate change and food
security policy. Agr Ecosys Environ 2008;126:4–12.
[130] Guisan A, Zimmermann NE. Predictive habitat distribution models in ecology. Ecol Model
2000;135:147–186.
[131] Pearson RG, Dawson TP. Predicting the impacts of climate change on the distribution of
species: are bioclimate envelope models useful? Global Ecol Biogeogr 2003;12:361–371.
[132] Sutherst RW, Constable F, Finlay KJ, Harrington R, Luck J, Zalucki MP. Adapting to crop pest
and pathogen risks under climate change. Wiley Interdisciplinary Reviews: Climate Change
2011;2:220–237.
[133] Philippine Statistical Authority-Bureau of Agricultural Statistics (PSA-BAS). 2014 CountrySTAT
Philippines. [Link] (accessed: 9 June 2014).
[134] Sumner PE, Lee D. Reducing aflatoxin in corn during harvest and storage. The University of
Georgia Cooperative Extension Bulletin 2012.
[135] Stewart DW, Reid LM, Nicol RW, Schaafsma AW. A mathematical simulation of growth of
Fusarium in maize ears after inoculation. Phytopathology 2002;92:534–541.
[136] R: A language and environment for statistical computing R Foundation for Statistical Comput-
ing 2014. at [Link] (accessed 9 June 2014).
[137] Quitco RT. Aflatoxin studies in the Philippines. In: Champ BR, Highley E, Hocking AD, eds.
Fungi and Mycotoxins in Stored Products. Bangkok, Thailand; 1991. p. 180–186.
[138] FAO. Aflatoxin contamination in foods and feeds in the Philippines. FAO/WHO Regional Con-
ference on Food Safety for Asia and Pacific, 2004, Seremban, Malaysia, FAO.
[139] Cumagun CJR. Population genetic analysis of plant pathogenic fungi with emphasis on Fusar-
ium species. Philipp Agric Sci 2007;90:244–256.
[140] Cumagun CJR, Ramos JS, Dimaano AO, Munaut F, Van Hove F. Genetic characteristics of Fusar-
ium verticillioides from corn in the Philippines. J Gen Plant Pathol 2009;75:405–412.
[141] Programme WF. Philippine Food and Nutrition Security Atlas. World Food Programme – Philip-
pines; 2012.
[142] Schaafsma AW, Hooker DC. Climatic models to predict occurrence of Fusarium toxins in wheat
and maize. Int J Food Microbiol 2007;119:116–125.
[143] Boland GJ, Meizer MS, Hopkin A, Higgins V, Nassurth A. Climate change and plant diseases in
Ontario. Can J Plant Pathol 2004;26:335–350.
[144] Madgwick JW, West JW, White RP, et al. Impacts of climate change on wheat anthesis and
fusarium ear blight in the UK. Eur J Plant Pathol 2011;130:117–131.
[145] Roos J, Hopkins R, Kvarnheden A, Dixelius C. The impact of global warming on plant diseases
and insect vectors in Sweden. Eur J Plant Pathol 2011;129:9–19.
[146] West JS, Townsend JA, Stevens M, Fitt BDL. Comparative biology of different plant pathogens
to estimate effects of climate change on crop diseases in Europe. Eur J Plant Pathol
2012;133:315–331.
[147] van der Fels-Klerx HJ, Olesen JE, Madsen MS, Goedhart PW. Climate change increases
deoxynivalenol contamination of wheat in north-western Europe. Food Addit Contam A
2012;29:1593–1604.
[148] Zhang X, Halder J, White RP, et al. Climate change increases risk of Fusarium ear blight on
wheat in central China. Ann Appl Biol 2014;164:384–395.
[149] Van der Fels-Klerx HJ, van Asselt ED, Madsen MS, Olesen JE. Impact of climate change effects
on contamination of cereal grains with deoxynivalenol. PLOS ONE 2013;1–6.
[150] Fernandes JM, Cunha GR, Del Ponte E, et al. Modeling Fusarium head blight in wheat under
climate change using linked process-based models. Proceedings of the 2nd International
28 | Ireneo B. Pangga, Arnold R. Salvacion, and Christian Joseph R. Cumagun

Symposium on Fusarium Head Blight, incorporating the 8th European Fusarium Seminar
2004: 11–15 December 2004: Orlando. p. 441–443.
[151] Battilani P, Rossi V, Giorni P, et al. Modeling, predicting, and mapping the emergence of afla-
toxins in cereals in the EU due to climate change. Scientific report submitted to EFSA 2012.
[152] Juroszek P, Tiedemann AV. Climate change and potential future risks through wheat diseases:
a review. Eur J Plant Pathol 2013;136:21–33.
[153] Shaw MW, Osborne TM. Geographic distribution of plant pathogens in response to climate
change. Plant Pathol 2011;60:31–43.
[154] McIntyre B, Kim Y, Fruci J, Rosenthal E. The best-laid plans: climate change and food security.
Climate and Development 2011;3:281–284.
[155] Garrett KA, Dobson ADM, Kroschel J, et al. The effects of climate variability and the color of
weather time series on agricultural diseases and pests, and on decisions for their manage-
ment. Agr Forest Meteorol 2013;170:216–227.
[156] Terzi V, Tumino G, Stanca AM, Morcia C. Reducing the incidence of cereal head infection and
myctoxins in small grain cereal species. Journal of Cereal Science 2013;59:284–293.
[157] Pangga IB, Hanan J, Chakraborty S. Pathogen dynamics in a crop canopy and their evolution
under changing climate. Plant Pathol 2011;60:70–81.
[158] Pangga IB, Hanan J, Chakraborty S. Climate change impacts on plant canopy architecture:
implications for pest and pathogen management. Eur J Plant Pathol 2013;135:595–610.
[159] Willyerd KT, Li C, Madden LV, et al. Efficacy and stability of integrating fungicide and cul-
tivar resistance to manage Fusarium head blight and deoxynivalenol in wheat. Plant Dis
2012;96:957–967.
[160] Thornton PK, Ericksen PJ, Herrero M, Challinor AJ. Climate variability and vulnerability to cli-
mate change: a review. Glob Change Biol 2014.
[161] Cruz A, Marin P, Gonzalez-Jaen MT, Aguilar KG, Cumagun CJR. Phylogenetic analysis, fu-
monisin production and pathogenicity of Fusarium fujikuroi strains isolated from rice in the
Philippines. J Sci Food Agric 2013;93:3032–3039.
[162] Cumagun CJR. The rise of bakanae disease of rice in the Philippines. Forum for Agriculture
Risk Management in Development 2012.
[163] Campos-Sánchez V, Esker PD, Murillo-Williams A. A shift in the mycotoxin profile in Costa Rica
under climate change – A case study on mycotoxigenic Fusarium proliferatum in rice (Oryza
sativa). International Conference on Climate Change Impacts and Adaptation for Food and
Environmental Security. 21–22 November 2012, Conference Summary Report, Los Banos,
Laguna, SEARCA. p. 23.
[164] Muller MEH, Brenning A, Verch G, Koszinski S, Sommer M. Multifactorial spatial analysis
of mycotoxin contamination of winter wheat at the field and landscape scale. Agr Ecosyst
Environ 2010;139:245–254.
[165] Marvin HJP, Kleter GA, Van der Fels-Klerx HJ, et al. Proactive systems for early warning of po-
tential impacts of natural disasters on food safety: Climate change-induced extreme events a
case in point. Food Control 2013;34:444–456.
[166] Gaudet DA, Tronsmo AM, Laroche A. Climate change and plant diseases. In: Storey KB,
Tanino KK, eds. Temperature Adaptation in a Changing Climate: Nature at Risk. Wallingford:
CAB International, 2012. p. 144–159.
[167] Dixon MA. Climate change – impacts on crop growth and food production, and plant
pathogens. Can J Plant Pathol 2012;34:262–379.
[168] West JS, Holdgate S, Townsend JA, Edwards SG, Jennings P, Fitt BDL. Impacts of chang-
ing climate and agronomic factors on Fusarium ear blight of wheat in the UK. Fungal Ecol
2012;5:53–61.
X. Li and X. B. Yang
2 Impact of climate change on genetically
engineered plants and mycotoxigenic fungi in the
north central region of the US

2.1 Introduction

Global climate change is a major challenge facing modern human society [1]. The im-
pact of climate change to aspects of human life and the global environment are pro-
found and full of uncertainty. Climate change has great impact on ecosystems as well,
especially agro-ecosystems [1–3]. In agriculture, plant diseases present a great threat
to global food security [4]. Most economic losses are due to direct yield losses in the
field and the cost of disease management. It has been estimated that diseases and
other pests cause 42 % loss in the 8 most important food and cash crops worldwide [5].
A plant disease system belongs to an agro-ecosystem, which consists of the host,
the pathogen(s), and the environment [6, 7]. The environment, largely associated with
regional climate, interacts with both the host and the pathogen(s). Plant pathogens
are usually very sensitive to weather conditions as well as climatic changes [6, 7].
Chakraborty et al. [8] suggested that climate change may have an impact on plant dis-
eases in three main aspects: geographic distribution, intensity of disease occurrence,
and effects of disease management. Since the 1980s, a number of researchers have
addressed the impact of climate change on agriculture and plant diseases, and many
of these studies were set in the US [1, 3, 8–16].
The US is one of the largest agricultural producers in the world in terms of planting
area, yield, and economic value. Historically, a number of infectious crop diseases
have attacked US agriculture, especially the row crops in the Great Plains and North
Central region (Fig. 2.1). Many outbreaks were due to native or exotic fungal pathogens,
e.g., southern corn leaf blight by Cochliobolus heterostrophus, corn gray leaf spot by
Cercospora zeae-maydis, wheat rusts by Puccinia spp., wheat head blight by Fusarium
graminearum, and soybean rust (exotic) by Phakopsora pachyrhizi [6, 17–24]. It has
been estimated that plant diseases caused about $ 33 billion economic loss each year
on average to US agriculture [5, 25].
A group of plant fungal diseases are caused by mycotoxigenic fungi, which are
capable of producing secondary toxic substances in their metabolisms. Mycotoxigenic
fungi are widely spread throughout the world and cause diseases in major food and
row crops such as corn, cotton, soybeans, and wheat in many countries. These dis-
eases not only cause yield losses, but also adversely impact on human health and
society [6, 26, 27]. The damage from mycotoxigenic fungi may occur at different times
or places, such as during crop production, postharvest/storage, food processing, or
30 | X. Li and X. B. Yang

North Dakota
Minnesota
Michigan
Wisconsin
South Dakota Vermont
Michigan
Wyoming New York
Iowa
Nebraska
Pennsylvania
Illinois Indiana Ohio
Colorado West virginia Maryland
Kansas Missouri
Kentucky Virginia
Oklahoma Arkansas Tennessee North Carolina
New Mexico
South Carolina
Mississippi Alabama
Georgia
Texas Louisiana
Legend
Florida Corn
Cotton
600 300 0 Kilometers Soybean

Fig. 2.1: Distribution of three field crops: corn, cotton, and soybeans in the US. The majority of these
crops are genetically engineered varieties. Corn and soybeans are largely overlapping in the states
of Illinois, Indiana, Iowa, and Ohio.

commodity trading. Yet the most important aspect is when the toxins produced by
these fungi enter food and animal feed which may then cause various diseases, such
as cancer, or acute mycotoxicoses in human and animals, sometimes fatal. For ex-
ample, several aflatoxins are produced by Aspergillus spp. in different crops. Since
their discovery in the early 1960s, aflatoxins have been considered among the most
carcinogenic chemicals to human [27]. The discovery was largely due to the death
of 100 000 turkeys after they fed on peanut meal contaminated by aflatoxins in Lon-
don in 1962 [28]. An outbreak of mycotoxicosis caused by aflatoxins in Kenya in 2004
claimed 125 lives of 317 diagnosed cases [29]. Similar cases are common in developing
countries where mycotoxigenic fungi are not properly managed and harvested grains
are often stored under natural conditions [30–32]. Deoxynivalenol (DON) or vomitoxin
produced by F. graminearum is another mycotoxin commonly detected in wheat, corn,
and barley grains worldwide. When high dose DON from contaminated grains is in-
gested by animals it may cause acute nausea, vomiting, and diarrhea.
Similar to the situation in many countries, there are a variety of diseases caused
by mycotoxigenic fungi in the US (Tab. 2.1). For instance, major toxins (aflatoxins
from Aspergillus spp., fumonisin from Fusarium spp., and zearalenone from Gib-
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 31

Tab. 2.1: Important mycotoxigenic fungi and mycotoxins commonly found in major field crops in the
United States.

Mycotoxigenic fungi Mycotoxins produced Affected genetically Favorable

engineered crops environments

Aspergillus flavus Aflatoxins (B1, B2, Corn, cotton, rapeseed, Hot and dry in
Aspergillus parasiticus G1, G2, and M1) soybeans growing season,
humid at or after
harvest
Fusarium verticillioides Fumonisin Corn Warm and humid
(syn. F. moniliforme)
Fusarium proliferatum
Fusarium graminearum Deoxynivalenol (DON) Corn Warm, humid,
(teleomorph Gibberella Zearalenone and rainy
zeae)

berella zeae) are commonly detected in the corn-growing regions. In wheat, DON
from F. graminearum, which causes wheat scab or head blight, is of the most concern.
Cotton, peanuts, and soybeans can be infected by Aspergillus spp., causing aflatoxin
contaminations of lesser importance compared with the mycotoxin problems in corn
and wheat. Several other less important mycotoxigenic fungi in fruits, nuts, and feed
crops also occur in this country [26, 27, 33].
A number of major crops suffer significant losses from mycotoxins in the US, es-
pecially from aflatoxin [34–36]. Estimates of these losses in terms of economic value
vary greatly. One estimated economic loss as a result of major mycotoxins, i.e. aflatox-
ins, fumonisin, and deoxynivalenol, in the US was about $ 932 million per year, plus
an average of $ 466 million annually for regulatory enforcement, testing, and other
quality control measures [35]. More specifically, aflatoxins caused an average $ 225
million economic loss in feed corn and $ 25.8 million loss in peanuts per year in the
US from 1993 to 1996 [35, 37]. The estimated loss due to DON contamination in the US
was $ 655 million per year, mostly in the wheat industry [38].
The presence of mycotoxins, particularly aflatoxins and DON, in food and feed is
regulated by the Food and Drug Administration (FDA) to insure quality and safety in
the US. A series of regulatory limits or action levels for aflatoxin of different products
has been established by the FDA since the 1960s [39]. For instance, the aflatoxin action
level is 20 ppb for all products for human consumption, except milk, and for all corn
used for immature animals and dairy cattle. The action level for aflatoxin M1 in milk is
only 0.5 ppb. The FDA currently sets up advisory levels for DON, e.g., 1 ppm in finished
wheat products for human consumption. In grain production and trading, hundreds
of grain samples were tested each year by elevators and exporters for mycotoxins. The
threshold level, or so-called Limit of Detection (LOD) used by the US Grain Council
32 | X. Li and X. B. Yang

is different for various mycotoxins. For example, in the 2013 season, the limits were
2.5 ppb for aflatoxins and 0.3 ppm for DON [40].
The occurrence of mycotoxigenic fungi is impacted by a changing climate too. Be-
cause of their importance in agriculture production, food safety, and public health,
climate change effects on these diseases is a concern for researchers, the public, and
governments worldwide [10, 32, 33, 38, 41–49]. However, in the US, the situation differs
to some extent compared to other major agricultural regions.
The most notable characteristic in US agriculture regarding mycotoxigenic fungi
is the high adoption rate of genetically modified (GM) crops. GM crops are genetically
modified organisms (GMO) by definition. A GMO is obtained normally by genetic engi-
neering (GE) or genetic modification techniques, which directly manipulate the DNA
sequence in an organism’s genome so that the modified genome will have modified or
new genes to express new traits. In a GMO, specific genes may be inserted, modified,
or deleted, so that the traits associated with these particular genes will express differ-
ently from the original organism. Using beneficial genes from other organisms, a GM
crop can have good traits which cannot be normally obtained by classical breeding
techniques, e.g., hybridization. The beneficial genes can be genes which resist herbi-
cides, insects, or abiotic stresses, which produce useful byproducts, or improve the
quality of nutrition and harvesting.
As a major advocator of the development of GMO techniques, the US has the
longest history of using GM crops on a large scale. The US has the largest GM cropping
system in the world, with 70.1 million hectares of GM crops planted in 2013 [50]. The
GM crops widely used in this country include alfalfa, corn, cotton, papaya, rape-
seeds, soybeans, squash, and sugar beet. Several others, such as GM wheat and rice,
are ready for commercial release [50]. Currently, Roundup Ready (RR, glyphosate-
resistant) and insect-resistant Bt (bacterium Bacillus thuringiensis) transgenic crops
are the major ones, including RR alfalfa, corn, soybeans etc., and Bt cotton, corn,
and potato. Therefore, the occurrence of diseases caused by mycotoxigenic fungi in
GM crops in the US is largely different from that in other countries where GM crops
were recently planted on a large scale, because GM crops have a great impact on these
disease systems [51–58]. The effects of a changing climate on these fungal diseases
are more complicated in the US than in other agricultural regions.
On the other hand, global climate change does not occur evenly in different re-
gions. Greater changes, mainly warming and changes in precipitation patterns, oc-
curred in the middle to high latitude regions of the northern hemisphere [1]. The major
US agricultural zones occur in these regions. Therefore, the impacts of climate change
on mycotoxigenic diseases in GM cropping systems in the US may be of greater mag-
nitude and particularly important compared to other major GM crop planting coun-
tries, such as Brazil, because climate change has generally had less impact on tropical
countries [1]. In this chapter we will focus on the important mycotoxigenic fungi of the
major GM crops planted in the mid-latitude regions, i.e. the northern central US, and
discuss the impact of climate change on the interactions and possible future trends.
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 33

2.2 GMO cropping systems in US agriculture

2.2.1 The establishment of GMO cropping systems in the US

The first GM plant was developed in 1982 by the Monsanto Company, which expressed
an antibiotic-resistant gene in tobacco plants [59]. The first field tests of GM plants,
with only a marker gene, were in the US and France in 1986 to develop a herbicide-
resistant tobacco. The US then conducted 1952 field trials of GMO between 1986 and
1995 [60]. A large number of herbicide-resistant (or herbicide-tolerant), e.g. resistant
to 2,4-D, glyphosate, and bromoxynil, GM crops were developed in response to the
great need for weed management in agriculture. The first GM crop approved in the Eu-
ropean Union was a herbicide-resistant tobacco in 1994 [60]. In the US, the glyphosate-
resistant technique was developed by Monsanto Company and released first in the soy-
bean market in 1996. Another major type of transgenic plant, insect-resistant plants,
began in 1987, when an insecticidal protein gene cry from B. thuringiensis (Bt) was
transferred to tobacco plants by Plant Genetic Systems, previously a Belgian com-
pany [56]. This technique was soon employed in cotton, corn, potato, and other crops
once developed.

100

80
Percent of planted area

60

40

HT soybean
Bt cotton
20
Bt corn
HT cotton
HT corn
0
1996 2000 2004 2008 2012

Fig. 2.2: Adoption of genetically engineered crops in the United States 1996–2013. HT: herbicide
tolerant traits. Bt: Bacillus thuringiensis toxin traits.

From 1996 the use of glyphosate-resistant and Bt techniques soared in soybeans, corn,
and cotton in the US (Fig. 2.2). By 2013, about 80–90 % of corn, cotton, and soybeans
in the US were GM crops. The distribution of these GM crops covers a vast geographic
area (Fig. 2.1), including the Corn Belt and the Great Plains. Glyphosate-resistant and
Bt crops are the most successfully used GM crops worldwide. About 90 % of them
34 | X. Li and X. B. Yang

(in terms of planting area; millions of hectares) are concentrated in 5 countries: the
US (70.1), Brazil (40.3), Argentina (24.4), India (11), and Canada (10.8), mainly in the
canola, corn, cotton, and soybean cropping systems [50].

2.2.2 Glyphosate-resistant crops and Bt transgenic techniques

Glyphosate (N-(phosphonomethyl) glycine), the active ingredient in Roundup® prod-

ucts, was introduced to the market by Monsanto in 1971 as a non-selective and systemic
herbicide [61]. It targets an enzyme (5-enolpyruvylshikimic acid-3-phosphate (EPSP)
synthase) commonly found in plants, fungi, and bacteria. Glyphosate inhibits this
enzyme and causes reduced protein synthesis, growth, and premature cell death in
sensitive organisms [62]. Glyphosate has low toxicity to human and animals with a
Toxicity Class of III (on a scale of I to IV, IV is the least toxic) according to the US Envi-
ronmental Protection Agency’s (EPA) assessment. This makes it safer than many other
commonly used herbicides, such as paraquat and imazapyr. Thus, it has been widely
used in agriculture, horticulture, and home gardening. Roundup Ready® (RR) refers
to a GM crop with a glyphosate resistant trait, which enables the GM crop to resist
glyphosate in culturing practices [63]. It allows producers to use glyphosate against a
wide spectrum of weeds without killing the crops. Glyphosate resistance genes have
been licensed to several major US seed companies, such as Pioneer and Syngenta, by
Monsanto to be used in alfalfa, corn, soybeans, and wheat (RR wheat is not currently
on the market).
Bt crops are based on the transformation of toxin-encoding genes from B. thu-
ringiensis to crops to create insect-resistant traits [64]. B. thuringiensis itself can be
used as a biocontrol agent in the field. There are a number of cry genes (Cry1A.105,
CryIAb, CryIF, Cry2Ab, Cry3Bb1, Cry34Ab1, Cry35Ab1, and mCry3A) which can pro-
duce delta endotoxins to kill lepidopteran and coleopteran larvae, especially Euro-
pean corn borer (Ostrinia nubilalis) and western corn rootworm (Diabrotica virgifera
virgifera) larvae [64]. They can be used either individually or stacked in a GM crop.
Another class of Bt genes used against insects is vegetative insecticidal protein (VIP)
genes, which have a different mode of action from cry genes [65, 66].

2.2.3 General impact of GM crops on US agriculture

GM crops have had a profound impact on US agriculture [50, 51, 54, 58, 63, 64, 67–
73]. Breeders have developed crops with stacked transgenic traits, e.g. corn varieties
with Bt and RR traits. This has allowed growers to reduce applications of insecticide
and other herbicides. According to estimations by Benbrook [67], using Bt transgenic
crops reduced insecticide applications in the field by about 56 000 tons during 1996–
2011. Inevitably, the use of glyphosate increased drastically [74]. It was estimated that
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 35

glyphosate use in soybean fields increased from 3935 tons in 1996 to 40 273 tons in
2006 (Chemical Use Program, National Agricultural Statistics Service (NASS), United
States Department of Agriculture (USDA)). Along with roundup ready technique, post-
emergence weed management became simpler, more flexible, and often cheaper [69,
75]. However, after two decades of intensive use of glyphosate in GM cropping systems,
more and more weed populations, such as waterhemp (Amaranthus rudis), horse-
weed (Conyza canadensis), and ragweed (Ambrosia artemisiifolia and A. trifida) have
evolved high resistance to this herbicide, and are sometimes called super weeds [67,
70, 76]. In response to the glyphosate-tolerant weeds, several other herbicide-resistant
GM crops have been developed. These new herbicide-resistant crops include Enlist® ,
incorporating both glyphosate resistance and 2,4-D resistance, and LibertyLink® , re-
sistant to Liberty® herbicide (Glufosinate ammonium), but their market share is still
much smaller than RR crops. Similar to glyphosate-resistant crops, Bt crops also put
steady selection pressure on the target insects, resulting in the emergence of insect
populations resistant to the cry and VIP traits [77]. Collateral damage to other non-
targeted insects and GMO pollen pollution of some organic farming systems may occur
as well.
The use of herbicide-tolerant, mainly glyphosate-resistant, crops helped the
adoption of conservation tillage and no-till in the US greatly [68]. According to a
report by the USDA, no-till in corn, cotton, soybeans, and rice increased at a median
rate of about 1.5 % per year from 2000–2007 [72]. The soybean-corn rotation systems
in the corn belt had the highest increase, with about 50 % no-till in soybean and 29.5 %
in corn crops in 2009. Also, a large percentage of fields is under conservation tillage,
in which large amounts (usually > 30 %) of crop residue are left on the soil surface.
No-till reduces soil erosion and compaction with less operational costs in labor and
machinery, improves water and fertilizer use efficiency, and creates less disturbed
habitats for biocontrol agents and beneficial insect predators [54, 73, 78]. On the
other hand, increased crop residues seem to have contributed to recent epidemics
of several diseases, e.g., Fusarium head blight in wheat (F. graminearum) and gray
leaf spot in corn (C. zeae-maydis) [17, 18, 79]. Also, surface plant residues reduce soil
surface temperatures and temperature fluctuation, and provide a better habitat for
microorganisms, some of which are pathogenic [51, 54].

2.2.4 Impact of GM crops on mycotoxigenic fungi

Using GM crops to reduce the damage of mycotoxigenic fungi is also one of the pur-
poses of developing genetic modification techniques [80]. In Bt GM cropping systems,
particularly Bt corn, crop injuries resulting from insects, e.g. European corn borer,
were significantly reduced, leading to reduced Fusarium spp. infections and myco-
toxin concentration in kernels [55, 81]. The estimated direct economic benefits based
on the use of Bt crops against mycotoxigenic fungi was about $ 22 million annually
36 | X. Li and X. B. Yang

according to an analysis by Wu [58] in 2004, without considering potential benefits

in aspects of human and animal health [57]. On the other hand, no-till or reduced
tillage increases plant residue on the soil surface significantly, providing more food
sources for the survival of several major mycotoxigenic fungi. The recent increases
in Fusarium head blight of wheat and ear/stalk rot of corn were attributed to this
by various researchers [17, 79, 82, 83]. Recently, serious debate on the intense use of
glyphosate in RR cropping systems and its impact on plant diseases has been initi-
ated by researchers who suggested that glyphosate has caused increases in certain
diseases [52, 53, 84, 85]. Most of their evidence is from Fusarium spp., including some
mycotoxigenic ones [86–88]. The mechanisms are not fully understood yet. It is likely
that glyphosate changes the balance of soil microenvironment, nutrition situation,
and competition among fungi in soil, especially around the rhizosphere [53, 71].

2.3 Global climate change and current situation in the US

Climate change on global or regional scales has been discussed in numerous research
articles, books, and reports [1, 2, 9, 10, 89–91]. In the latest assessment report (AR5)
by the Intergovernmental Panel on Climate Change (IPCC), the major trends of global
climate change have been further clarified. According to various investigations and
observational data, average global surface temperature has increased by 0.85 °C (0.65
to 1.06 °C) since 1880, along with diminished glaciers and rising sea levels. On a
climatic scale, the last 30 years have been the warmest period since 1850 based on
human instrumental records, and are also likely to have been the warmest in the
northern hemisphere in the last 1400 years [1]. Cold days are fewer and warm days
are more frequent globally, resulting in an earlier spring [92]. Changes in patterns of
extreme weather and climate events have been observed in recent decades in many
regions [1].
Climate change differs in various aspects on a regional scale. More heat waves
seem to have occurred in Australia, Asia, and Europe. In the mid-latitude areas of the
northern hemisphere, precipitation has increased since 1951 with high statistical con-
fidence. In North America and Europe, heavy rainfall likely increased in more land
regions, though drought prevailed in some areas [1, 89, 90]. Observations of extreme
weather events, such as tropical cyclones, increased in several regions [91].
The 2012 growing season was the warmest in the US since 1895 according to the
US National Climatic Data Center (NCDC). In most regions of the US, annual mean
temperatures have increased in general, though significant geographical differences
exist. For example, Alaska, which is at high latitude, had the largest increase, followed
by the northern Midwest, i.e., north central region, and the southwest. Seasonally, au-
tumn temperatures increased the least and winter temperatures increased the most.
Warmer springs were seen in most regions as well, e.g. the warmest on record in 2012.
The warming in spring has resulted in longer growing season, at a changing rate of
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 37

1–4 days longer per decade [10]. In Iowa, a north central state, the annual number of
frost-free days increased by 8–9 days from 1893–2008 [9]. Changes in summer tem-
peratures were more complex: in the southeast they were actually cooling, although
the trend is diminishing, while the north central region had slightly warmer sum-
mers [10, 90]. Annually, there is generally more rainfall now in the northwestern, cen-
tral, and southern US than 100 years ago. The most notable rainfall increase occurred
in central US. According to observations in the north central region, where mainly
corn and soybeans are grown, rainfall, mainly in spring and summer, increased by
about 15 % in the last 100 years [9, 89]. The southern US had more rainfall in au-
tumn [10, 90].
The increase in precipitation has two aspects: frequency and intensity. Generally,
there are more rainy days, and more heavy rains. Such an increase cooled the region,
sometimes called the “warming hole”, in the US north central compared to the tem-
perature increases on the whole continent [93, 94]. An increase in summer rainfall
can lead to a wet and warm growing season, such as those of 2010 and 2011, or a wet
and cool growing season, such as the 2009 season, which was close to the coolest
summer recorded in North Central (Data from NCDC). In contrast, parts of the east-
ern US, the Rocky Mountains, and much of the southwest received less rainfall, and
southwestern US experienced more frequent drought. Most recently, severe droughts
occurred in 2012 and 2013 in the southern Great Plains, where wheat is the major
crop, as well as part of the north central region, resulting in yield losses of corn (Data
from DCDC).
In the US, heavy rainfall, drought, heat waves, tornados, and hurricanes are
weather extremes observed in growing seasons. Increases in the frequency of weather
extremes are considered important indicators for changes in regional climates. With
increased occurrences of weather extremes, annual variations of weather patterns
may become greater than before [10, 89, 90]. According to NCDC data, extreme
weather events have increased in frequency in recent years, causing significantly
different weather patterns each year, particularly in the north central region, for
example the record cool summer in 2009, the very wet summer in 2010 with record
floods in several states, a hot and humid 2011 summer leading to outbreaks of fungal
diseases in corn and soybeans, and a sudden severe drought in 2012. The 2013 season
was of no difference with a near record wettest May and cool/dry summer in the
north central region (DCDC). An extreme event in one year is insufficient to suggest
climate change in a region. When extreme weather patterns occur several years in
a row, we can confidently say that this region is experiencing significant changes in
climate.
38 | X. Li and X. B. Yang

2.4 Impacts of climate change on the occurrence

of mycotoxigenic fungi

2.4.1 The impact of climate change in the off-seasons: winter and early spring

Most fungi are very sensitive to changes in environment, including mycotoxigenic

ones. Among the major mycotoxigenic fungi in the US, Penicillium spp are of less con-
cern because they are more important during storage than in the growing season, and
the US has advanced storage facilities to minimize their impact. During the growing
season, Fusarium spp. and Aspergillus spp. (Tab. 2.1), the major fungal agents causing
disease and toxin contamination, would certainly be impacted more by a changing
climate.
Generally speaking, these diseases have relatively simple disease cycles. These
fungi normally overwinter either as mycelium or as resistant structures, e.g., chlamy-
dospores (F. graminearum), thickened hyphae (F. verticillioides), or as sclerotia (As-
pergillus spp.) in soil or on crop residues, mainly corn [95–97]. As mentioned above,
warming in winter and spring were most significant in temperate climate zones, es-
pecially in middle to high latitude regions, such as the north central region in the US
[1, 9, 90]. Winter temperatures in these locations can frequently reach −10 to −20 °C or
even lower. Fusarium spp. in crop residue have long-term survivability and high toler-
ance of cold weather. A study conducted in Kansas by Manzo and Claflin [98] assessing
the survival rate of F. moniliforme hyphae and conidia in sorghum residue showed that
the fungus had no loss of viability after 6 months at −16 °C. Cotten and Munkvold [99]
reported that when buried in soil in Iowa, nearly half of the corn residue inoculated
with F. moniliforme, F. proliferatum, and F. subglutinans still had the fungi one year
later, similar to survival rates on the surface. Inch and Gilbert [100] found that G. zeae
could survive in wheat kernels for at least 2 years on soil surface in Canada. These
reports suggest that winter warming in cold regions would have minimal impact on
the survival of Fusarium spp. in crop residue.
Aspergillus species prefer a warmer environment, thus winter temperatures would
certainly appear more important for their survival in the north. It is well-documented
that sclerotia of Aspergillus species are abundant in the southern US, especially
A. flavus [101]. Even in southern Texas, a warm region, the density of A. flavus propag-
ule followed a negative correlation in soil daily temperature range of 18–30 °C across
different seasons [102]. In the north, e.g. Iowa, low levels of A. flavus presence could
still be detected in years of unfavorable conditions with a high annual variation in
population density [103]. But Shearer et al [104] suggested that these fungi do not
produce sclerotia in the north as readily as in the southern US due to lower autumn
temperatures in September and October which are unfavorable for sclerotia devel-
opment. A comparative study by Wicklow [97] showed that the decay of conidia of
Aspergillus species was slower in Illinois than that in Georgia, and A. parasiticus
survived better than A. flavus. It seems that low winter temperatures in the north may
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 39

favor survival of conidia of Aspergillus species, but cool autumn weather still hinders
the production of sclerotia, the longer-surviving fruiting body. Warming in winter
and early spring in the north may impair the survival of local Aspergillus species in
the long-run since their population seems to decline faster in a warmer environment,
while unfavorable environment conditions for propagule production in summer and
autumn do not change much according to observed climate changes. In addition,
various bacteria and fungi may colonize sclerotia of Aspergillus species, reducing
their viability [97, 105]. Warming in winter and spring may enhance these parasitic
activities, deteriorating the soil environment for Aspergillus sclerotia.
Insects which are vectors of these pathogens are certainly affected by climate
change in winter as well [106]. A warmer winter and spring allow more generations
a year and a gradual expansion of the distribution range of the European corn borer
and corn rootworms further north in the US and Canada has been predicted [107, 108].
In the newly colonized areas in the north, low population of these insects would per-
haps not have much impact on diseases caused by Aspergillus spp., since low summer
temperatures are more important as a limiting factor to infections and to mycotoxin
contamination than insect damage. In the Corn Belt, the European corn borer pop-
ulation normally produces two generations in a season or part of the 3rd generation
in an extended growing season. Their overwintering populations generally suffer less
cold stress in warm winters if only the air temperature increases [109, 110]. However,
warming in winter also leads to more rain in winter in some areas, such as Iowa [9, 10].
If the warming causes reduced snow cover or more frequent freeze-thaw cycles during
the period of insect diapause, higher mortality may occur for some insects, e.g. larvae
of the European corn borer and corn earworm (Heliothis zea), which overwinter better
in a snow-covered or less moist environment [106, 111, 112]. Nonetheless, compared to
the effects of Bt corn which is widely used in this region, impacts of climate change in
winter may be secondary in affecting insects and related fungal diseases.

2.4.2 Impact of climate change on planting date and fungi at seedling stages

Planting dates are important to the seasonal occurrence of many crop diseases in the
US. Earlier planting has been adopted by many growers, largely due to the earlier oc-
currence of spring. For example, corn can be planted in mid-April in Iowa, the core
planting area in the US Corn Belt (Fig. 2.3). As Fusarium ear rot grows better in a moder-
ate temperature range, warm weather early in a spring would be highly favorable to the
pathogen’s activities in surface crop residue, leading to more propagule production.
However, the temperature below the soil surface does not increase rapidly in fields
with no-till or conservation tillage because of the crop residue coverage [73]. Thus,
seedlings in early planting fields may suffer from longer exposure to low soil temper-
atures, a relatively stressful condition. Observations in recent years from Ohio State
suggested that seedling diseases caused by F. graminearum and other Fusarium spp.
40 | X. Li and X. B. Yang

in wheat-corn-soybean rotation appeared increased even after seeds were treated with
fungicides [113]. For the early seedling stage, conidia on residues in the soil may be
the major sources of inoculum since they can overwinter as well [100]. The increase of
Fusarium seedlings may be related to the increased activities of Fusaria under warmer
conditions in conjunction with increased inoculum from infested crop residue.

May 20
Date of 30% planted

Date of 50% planted

May 10

Apr 30

Apr 20

Apr 10

2014
1994
1995
1996
1997
1998
1999
2000
2001
2002
2003
2004

2006
2007
2008
2009
2010
2011
2012
2013
2005

Fig. 2.3: Planting dates of corn in Iowa in the last 20 years according to the weekly crop progress re-
ports issued by the United States Department of Agriculture. There have been more early plantings
since the 2000s, though planting was delayed in two recent years due to excessively wet springs.
A similar trend can be found in soybean planting, which normally occurs after corn planting.

Early planting allows crops to accumulate biomass for a longer period. Increased
biomass in no-till or conservation tillage is favorable to the initial inoculum produc-
tion in crop residue, which certainly favors the survival of mycotoxigenic fungi on crop
residues, especially Fusarium spp. since they do not produce sclerotia. On the other
hand, in the US Corn Belt, 2nd generation European corn borers usually cause more
damage, especially in late planted corn [114]. Early planted corn or early maturing
corn may escape this period of great damage, having less damaged kernels for the
infection of mycotoxigenic fungi. However, this effect may also be secondary and
could be masked by the suppressive effect of Bt toxins on insect populations.
Fast warming in early spring causes rapid melting of snow and sometimes heavy
convective precipitation during the early planting season [10]. A wetter spring causes
fewer workable days in the field, leading to planting difficulties [9]. For example,
in the 2013 spring, Iowa experienced an extended planting season delay, and many
fields were planted in June, after the wettest May on record (NCDC). According to
the Crop Progress Reports released by NASS of USDA, by May 19, only 71 % of corn
fields were planted, much less compared to the average level of 92 % in the previous
5 years. Soybeans are normally planted after corn. By June 2, only about 44 % of
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 41

the soybean fields in Iowa had been planted, in contrast to the average level of the
previous 5 years, which was 91 % by that date. Late planted corn suffers the greatest
damage from 2nd generation European corn borers. This in turn is favorable for the
occurrence of F. verticillioides, F. proliferatum, or F. subglutinans, the dominant species
for Fusarium ear rot via insect wounds [115–118], leading to fumonisin contamination
if warm and dry weather persists during the late reproductive stages. In another
case, later maturing fields may escape the infection peak of F. graminearum causing
Gibberella ear rot during the silking stage, which is normally in July. However, cool
and wet conditions in late summer and early autumn are favorable for F. graminearum
infection and DON contamination in kernels if severe insect damage has occurred.
Even with normal or early planting, heavy spring rainfall can cause field to flood.
A few days of flooding can also slow crop growth, reduce crop stands, or delay harvest.
In extreme cases, impact may be passed on to the next season because crops in a late
planted field may not be harvested due to early frost or other weather events during the
harvest season. Consequently, massive amounts of infected kernels and crop residue
are left on the surface for the next season as primary inoculum sources. Collectively,
frequent rainfall in spring involves more uncertainty regarding disease occurrence.

2.4.3 Impact of climate change on crops and diseases in late spring and summer

Late spring and summer are the key transition stages for crop development from the
vegetative to the reproductive stages. Weather events will have great impact on in-
oculum dispersal, infection, and development of mycotoxigenic diseases. In the north
central US, changes in temperatures in late spring and summer were minor, but pre-
cipitation pattern changes were significant, resulting in heavy storms, floods, drought,
and crop physical injuries [9, 89]. As mentioned above, events of heavy rainfalls in-
creased in the north central US. In Iowa (Fig. 2.4), the Storm Events Database main-
tained by NCDC indicate that events of damaging heavy rain and storm wind (strong
winds arising from convection with speeds > 50 knots, i.e. 92.6 kph) have increased
in recent decades in terms of overall occurrence, affected areas, occurrence time, and
strength. These events lead to great uncertainty in disease occurrence.
Several major mycotoxigenic fungi, particularly A. flavus and F. graminearum, in-
fect kernels during the silking stages of corn, a critical time for disease development.
The primary sources of inoculum for Fusarium spp. and Aspergillus spp. infections
are from fungal structures on residue and other crop tissues [82, 83, 95, 118, 119]. For
instance, infectious propagules of F. graminearum are ascospores discharged from
perithecia, survival structures in residue [95], and macroconidia in sporodochia in
crop residue may also serve as a minor source [83]. Rainfall has a strong influence on
the initial infection of F. graminearum because ascospore discharge normally occurs
when perithecia are dried during the day and moistened suddenly at night, either by
high relative humidity or light rain [120] with 16 °C as optimal [121]. A rainfall event
42 | X. Li and X. B. Yang

Number of observed thunderstorm wind

800 Number of counties affected
Days of events reported
Number of damaging heavy rain observed
600 since 1996

400

200

0
1974

1978

1982

1986

1990

1994

1998

2002

2006

2010
Fig. 2.4: Numbers of strong storm winds and damaging heavy rains observed May–August in Iowa
in the north central US region in recent decades.

can easily have suitable environmental conditions for ascospore discharge by provid-
ing moisture and low temperature. Thus, the observed increase of rainy days and hu-
midity in the north central region during the corn silking stage brings more frequent
changes in air moisture and cool weather [9], thus favoring discharge and infection of
F. graminearum ascospores, setting the initial disease level high [83].
Corn kernel infections by F. verticillioides, F. subglutinans, and F. proliferatum are
mainly via airborne microconidia and macroconidia on crop residues [83]. The sclero-
tia of Aspergillus [Link] to produce hyphae or conidia, which can be dispersed
in the soil or carried by winds and insects to infect corn [119]. A. parasiticus infects
mainly peanut, while A. flavus appears more on corn and cotton, where aerial infec-
tions mainly occur, and is thus more important in the north central region [119, 123,
124]. The more frequent occurrence of heavy rainfall and high speed storm winds favor
dispersal and wet deposition of these airborne inocula among fields and within crop
canopies [125]. Thus, a higher prevalence of Gibberella and Fusarium ear rot in this
region could occur.
Extreme precipitation causes various crop stressors, such as flood, hail damage,
and lodging. Stressed crops are less resistant to fungal infections, particularly to those
entering through wounds. Fusarium and Aspergillus species can infect plants through
wounds, thus weather extremes such as heavy rainfall, hail storms, strong winds will
increase infections. However, disease occurrence data associated with these events
are scarce. Another aspect of the impact of heavy precipitation could be on insect
development. Normally, a dry year is more favorable for insects. Heavy rainfall may
cause high mortality during insect egg hatching. For F. verticillioides, frequent heavy
rainfalls could reduce European corn borer infestations, which is important in spore
dispersal [126]. Cool weather during a period of rainy days may hinder development
of insect larvae, leading to lower population density in the late season.
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 43

Warming is not as significant as that in winter and spring in the north central
region during late spring and summer. This region is a temperate zone, thus days with
high temperatures above 30 °C are relatively rare in states such as Iowa, Illinois, and
Indiana. Yet, increased night temperatures have been observed in this region [9, 90].
It has been clear that warming in the night impairs corn yield greatly [127–129]. For
example, the hot summer nights of 2011 cut the national corn yield to 147.2 bushels
per acre (NASS/USDA). Furthermore, elevated temperatures often cause heat stress in
corn in the early reproductive stages, but less so in soybeans, if drought occurs in the
meantime. A recent case was in 2012: average corn yield dropped to 123.4 bushels per
acre due to hot and dry weather (NASS/ USDA).
In general, Fusarium spp. prefer a moderate temperature range, though F. gramin-
earum prefers cooler temperatures (optimal about 24–28 °C), while F. verticillioides and
the others prefer the warmer side (optimal about 30 °C) [130–132]. They therefore pre-
vail in the central to northern US. A hot season will be unfavorable to Gibberella ear
rot. For instance, the testing results for DON reported by the US Grain Council showed
that 91.6 % of samples had less than 0.5 ppm of the mycotoxin in 2013, slightly lower
than in 2012 at 96 %, while the 2012 summer was much warmer (about 2–4 °C region-
ally) than 2013 in the north central region [40]. Overall, current changes in summer
temperatures may not impact Fusarium and Gibberella ear rot in this region as much
as other factors such as no-till and heavy precipitations.
In contrast, A. flavus favors hot and dry conditions. The fungus can grow well
in a temperature range of 25–42 °C, but favors a high optimum temperature of 37 °C
[119]. High night temperatures, above 30 °C, certainly favor kernel infection of A. flavus
[119, 133]. Insects are also favored by hot and dry weather, resulting in rapid develop-
ment of new generations and causing more kernel wounds. These aspects of negative
impacts from hot and dry weather would thus create a synergetic effect for Aspergillus
ear rot, leading to rapid disease progress and mycotoxin contamination in a hot and
dry year. Historically, when much warmer than normal and relatively dry summers
occurred in Iowa, high rates of aflatoxin contamination occurred in grain, such as
in 1983 (37 % positive) and 1988 (30 % positive) [134]. According to harvest quality re-
ports from the US Grain Council, in 2012, the percentage of samples with no detectable
aflatoxin was 78 %, much lower than that in 2013 (about 98 %) [40], indicating the im-
pact of hot dry weather in 2012 on the occurrence of A. flavus. In 2012, in response
to the severe drought and potential aflatoxin contamination, the state government of
Iowa requested mandatory testing of milk for aflatoxins in late summer [135]. Although
these data were not systematically collected, given that July of 2012 was much hotter
and drier than July of 1983, the lower rates of aflatoxin-positive samples in 2012 (22 %)
than in the previous drought (1983) may reflect the significant effect of Bt GM crops on
controlling mycotoxin contamination. Nonetheless, regional drought and hot weather
similar to that in 2012 may alert to potential problems of mycotoxin contamination
resulting from extreme weather events from climate change in the future, not men-
tioning that insects are also evolving with higher resistance to Bt toxins [77].
44 | X. Li and X. B. Yang

2.4.4 Increased use of fungicides

Fungicide use in row crops such as corn and soybeans has increased significantly in
the US Corn Belt since the year 2000, including seed treatment and foliar spray [136–
138]. There are several reasons for this increase: increasing crop prices making fungi-
cides more affordable, more disease pressure resulting from early planting and no-till
practices, new fungicides such as strobilurin available for these crops, favorable en-
vironments due to climate change, and even the invasion of continental US with soy-
bean rust [139]. Many researchers still suggest that fungicide spray should be applied
only when disease pressure is high [138–141]. In corn, it was reported that fungicide
application can reduce Fusarium stalk rot significantly, leading to higher yield by re-
ducing lodging from stalk rot. Meanwhile, seed treatment has been widely used in
corn and soybean fields to protect seeds from seedling disease in the early season,
helping adoption of early planting. These changes are partially under the influence
of climate change in this region and would inevitably affect mycotoxigenic fungi. Nat-
urally, fungicides can protect crops from mycotoxigenic fungal infection, leading to
reduced occurrence of mycotoxin contamination.

2.5 Summary and future risks

The impact of climate change in north central US on local mycotoxigenic fungi is

great, and directly or indirectly affects the regional occurrence of diseases caused by
mycotoxin-producing fungi. Directly, climate change affects fungal survival, growth,
dispersal, infection, and disease development. Indirectly, climate change affects
planting dates, culturing practices, and disease management, etc. The impacts of
climate change are different for different crop diseases. Current changes in climate
favor the occurrence of Gibberella ear rot in corn because of increased rainfall, warmer
spring weather, and more crop residue. More occurrence of this disease is likely to be
seen in the Corn Belt as in wheat production regions such as Indiana and Ohio. The
occurrence of Fusarium ear rot in this region may increase slightly in the near future
as well because frequent thunderstorms aid their dispersal and initial infections, as
well as slight summer warming. Bt crops and fungicides will still play important roles
in reducing the threat. Aspergillus spp. is severe in the north central US when severe
hot dry summer weather similar to that in 2012 occurs, especially for more than one
year in a row.
However, these factors combined with the use of GM crops, will have synergis-
tic effects on mycotoxigenic fungi, leading to greater uncertainty and difficulties in
predicting future trends [142]. It is even more difficult to make a long-term prediction
for disease risk due to the lack of monitoring data and comprehensive understanding
of the often highly non-linear synergistic impacts [143]. Nonetheless, it is clear that
the regional climate in north central US has experienced more weather extremes and
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 45

greater annual fluctuations in recent decades. Under these circumstances, it is likely to

have seasons which meet the occurrence conditions of the major mycotoxigenic fungi
in the near future. This implies that the local diversity and prevalence of the diseases
caused by mycotoxigenic fungi may increase, though the overall severity, except Gib-
berella ear rot, may not necessarily be much higher than before, especially when the
insects are well controlled by Bt crops and fungicides are used. In the long run, if the
regional temperatures increase as predicted by IPCC and extended droughts occur,
particularly in summer and autumn, Aspergillus spp. could become more a significant
threat.

References

[1] IPCC. Climate change 2013: the physical science basis. Contribution of Working Group I to
the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge,
United Kingdom and New York, NY, USA: Cambridge University Press; 2013.
[2] IPCC. Climate change 2007: the physical science basis. Contribution of Working Group I to the
Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge,
United Kingdom and New York, NY, USA: Cambridge University Press; 2007.
[3] Rosenzweig C, Iglesias A, Yang XB, Epstein PR, Chivian E. Climate change and extreme
weather events; implications for food production, plant diseases, and pests. Global change
& human health 2001;2:90–104.
[4] Strange RN, Scott PR. Plant disease: A threat to global food Security, Ann Rev Phytopathol
2005;43:83–116.
[5] Oerke EC, Dehne HW, Schonbeck F, Weber A. Crop production and crop protection: Estimated
losses in major food and cash crops. Amsterdam, the Netherlands: Elsevier; 1994.
[6] Agrios G. Plant Pathology. Burlington, MA, USA: Academic Press; 2005.
[7] Kranz J. Epidemics of plant diseases. New York, NY, USA: Springer Verlag; 1990.
[8] Chakraborty S, Tiedemann AV, Teng PS. Climate change: potential impact on plant diseases.
Environmental Pollution 2000;108:317–326.
[9] Iowa Climate Change Impacts Committee. Climate change impacts on Iowa 2010: Report to
the Governor and the Iowa General Assembly. Iowa Climate Change Impacts Committee, Des
Moines, IA, USA; 2010.
[10] Walthall C, Hatfield J, Backlund P, et al. Climate change and agriculture in the United States:
Effects and adaptation. USDA Technical Bulletin 1935. Washington DC, USA; 2012.
[11] Anderson PK, Cunningham AA, Patel NG, Morales FJ, Epstein PR, Daszak P. Emerging infec-
tious diseases of plants: Pathogen pollution, climate change and agro-technology drivers.
Trends Ecol Evol 2004;19:535–544.
[12] Coakley SM, Scherm H. Plant disease in a changing global environment. Aspects Appl Biol
1996;45:227–238.
[13] Coakley SM, Scherm H, Chakraborty S. Climate change and plant disease management. Ann
Rev Phytopathol 1999;37:399–426.
[14] Garrett KA, Dendy SP, Frank EE, Rouse MN, Travers SE. Climate change effects on plant dis-
ease: Genomes to ecosystems. Ann Rev Phytopathol 2006;44:489–509.
[15] Garrett KA, Dobson ADM, Kroschel J, et al. The effects of climate variability and the color of
weather time series on agricultural diseases and pests, and on decisions for their manage-
ment. Agricultural and Forest Meteorology 2013;170:216–227.
46 | X. Li and X. B. Yang

[16] Chakraborty S, Newton AC. Climate change, plant diseases and food security: An overview.
Plant Pathology 2011;60:2–14.
[17] McMullen M, Roger J, Gallenberg D. Scab of wheat and barley: a re-emerging disease of dev-
astating impact. Plant disease 1997;81:1340–1348.
[18] Ward JM, Stromberg EL, Nowell DC, Nutter FW Jr. Gray leaf spot: A disease of global impor-
tance in maize production. Plant Disease 1999;83:884–895.
[19] Ullstrup AJ. The impacts of the southern corn leaf blight epidemics of 1970–1971. Ann Rev
Phytopathol 1972;10:37–50.
[20] Li X, Esker PD, Pan Z, Dias AP, Xue L, Yang XB. The uniqueness of the soybean rust pathosys-
tem: An improved understanding of the risk in different regions of the world. Plant Disease
2010;94:796–806.
[21] Roelfs AP, Bushnell WR. The Cereal Rusts. Vol. II, New York, NY, USA: Academic Press; 1985.
[22] McMullen M, Bergstrom G, De Wolf E, et al. A unified effort to fight an enemy of wheat and
barley: Fusarium head blight. Plant Disease 2012;96:1712–1728.
[23] Tatum LA. The southern corn leaf blight epidemic. Science 1971;171:1113–1116.
[24] Brown JKM, Hovmøller MS. Aerial dispersal of pathogens on the global and continental scales
and its impact on plant disease. Science 2002;297:537–541.
[25] Pimentel D, Lach L, Zuniga R, Morrison D. Environmental and economic costs of nonindige-
nous species in the United States. Bioscience 2000;50:53–65.
[26] Richard JL. Some major mycotoxins and their mycotoxicoses–an overview. International jour-
nal of food microbiology 2007;119:3–10.
[27] Bennett JW, Klich MA. Mycotoxins. Clinical Microbiology Reviews 2003;106:497–516.
[28] Van der Zijden AS, Koelensmid WAA, Boldingh J. Aspergillus flavus and Turkey X disease: Iso-
lation in crystalline form of a toxin responsible for Turkey X disease. Nature 1962;195:1060–
1062.
[29] Azziz-Baumgartner E, Lindblade K, Gieseker K, et al. Case-control study of an acute aflatoxi-
cosis outbreak in Kenya, 2004. Environmental Health Perspectives 2004;113:1779–1783.
[30] Williams JH, Phillips TD, Jolly PE, Stiles JK, Jolly CM, Aggarwal D. Human aflatoxicosis in de-
veloping countries: a review of toxicology, exposure, potential health consequences, and
interventions. The American Journal of Clinical Nutrition 2004;80:1106–1122.
[31] Ngindu A, Johnson BK, Kenya PR, Ngira JA, Ocheng DM. Outbreak of acute hepatitis caused by
aflatoxin poisoning in Kenya. Lancet 1982;319:1346–1348.
[32] Shephard GS. Impact of mycotoxins on human health in developing countries. Food Additives
and Contaminants 2008;25:146–151.
[33] Wood GE. Mycotoxins in foods and feeds in the United States. Journal of Animal Science
1992;70:3941–3949.
[34] Robens J, Cardwell K. The costs of mycotoxin management to the USA: Management of afla-
toxins in the United States. Journal of Toxicology 2003;22:139–152.
[35] CAST. Mycotoxins: Risks in plant, animal, and human systems. Ames, IA, USA: Council of
Agricultural Science and Technology; 2003.
[36] Zubera MS, Lillehoj EB. Status of the aflatoxin problem in Corn. J Environ Qual 1979;8:1–5.
[37] Lamb MC, Sternitzke DA. Cost of aflatoxin to the farmer, buying point, and sheller segments
of the Southeast United States peanut industry. Peanut Science 2001;28:59–63.
[38] Schmale DG, Munkvold GP. Mycotoxins in crops: A threat to human and domestic animal
health. In: The Plant Health Instructor. St. Paul, MN, USA: American Phytopathological So-
ciety; 2009 (accessed June 20, 2014, at [Link]
mycotoxins/Pages/[Link].)
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 47

[39] NGFA. FDA mycotoxin regulatory guidance: A guide for grain elevators, feed manufacturers,
grain processors and exporters. Washington DC, USA: National Grain and Feed Association;
2011.
[40] U.S. Grains Council. Corn export cargo quality report 2013/14. Washington DC, USA: U.S.
Grains Council; 2014.
[41] Scholthof KBG. One foot in the furrow: Linkages between agriculture, plant pathology, and
public health. Annu Rev Public Health 2003;24:153–74.
[42] Tirado MC, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank JM. Climate change and food
safety: A review. Food Research International 2010;43:1745–1765.
[43] Miraglia M, Marvin HJP, Kleter GA, et al. Climate change and food safety: an emerging issue
with special focus on Europe. Food and Chemical Toxicology 2009;47:1009–1021.
[44] Lake IR, Hooper L, Abdelhamid A, et al. Climate change and food security: Health impacts in
developed countries. Environmental Health Perspectives 2012;120:1520–1526.
[45] Wu F, Bhatnagar D, Bui-Klimke T, et al. Climate change impacts on mycotoxin risks in US
maize. World Mycotoxin Journal 2011;4:79–93.
[46] Schaafsma AW, Hooker DC. Climatic models to predict occurrence of Fusarium toxins in wheat
and maize. International Journal of Food Microbiology 2007;119:116–125.
[47] Paterson RRM, Lima N. Further mycotoxin effects from climate change. Food Research Interna-
tional 2011;44:2555–2566.
[48] Paterson RRM, Lima N. How will climate change affect mycotoxins in food? Food Research
International 2010;43:1902–1914.
[49] Cotty PJ, Jaime-Garcia R. Influences of climate on aflatoxin producing fungi and aflatoxin
contamination. International Journal of Food Microbiology 2007;119:109–115.
[50] James C. Global status of commercialized biotech/GM crops: 2013. Ithaca, New York, NY, USA:
International Service For the Acquisition of Agri-biotech Applications; 2013.
[51] Dunfield KE, Germida JJ. Impact of genetically modified crops on soil- and plant-associated
microbial communities. J Eviron Qual 2004;33:806–815.
[52] Johal GS, Huber DM. Glyphosate effects on disease and disease resistance in plants. Eur
J Agron 2009;31:144–152.
[53] Kremer RJ, Means NE. Glyphosate and glyphosate-resistant crop interactions with rhizo-
sphere microorganisms. Eur J Agron 2009;31:153–161.
[54] Lundgren JG, Gassmann AJ, Bernal JJ, Duan JJ, Ruberson J. Ecological compatibility of GM
crops and biological control. Crop Protection 2009;28:1017–1030.
[55] Munkvold GP, Hellmich RL, Rice LG. Comparison of fumonisin concentrations in kernels of
transgenic Bt maize hybrids and nontransgenic hybrids. Plant Disease 1999;83:130–138.
[56] Vaeck M, Reynaerts A, Höfte H, et al. Transgenic plants protected from insect attack. Nature
1987;328:33–37.
[57] Wu F, Miller JD, Casman EA. The economic impact of Bt corn resulting from mycotoxin reduc-
tion. Journal of Toxicology–Toxin Reviews 2004;23:397–424.
[58] Wu F. Mycotoxin reduction in Bt corn: potential economic, health, and regulatory impacts.
Transgenic Research 2006;15:277–289.
[59] Fraley RT, Rogers SG, Horsch RB, et al. Expression of bacterial genes in plant cells. Proc Natl
Acad Sci USA 1983;80:4803–4807.
[60] James C, Krattiger AF. Global review of the field testing and commercialization of transgenic
plants: 1986 to 1995. Ithaca, New York, NY, USA: The International Service for the Acquisition
of Agri-biotech Applications; 1996.
[61] Franz JE, Mao MK, Sikorski JA. Glyphosate: A unique global herbicide. ACS Monograph
No. 189. Washington DC, USA: American Chemical Society; 1997.
48 | X. Li and X. B. Yang

[62] Amrhein N, Deus B, Gehrke P, Steinrücken HC. The site of the inhibition of the shikimate
pathway by glyphosate II. Interference of glyphosate with chorismate formation in vivo and
in vitro. Plant Physiology 1980;66:830–834.
[63] Dill GM. Glyphosate-resistant crops: History, status. Pest Manag Sci 2005;61:219–224.
[64] Castagnola AS, Jurat-Fuentes JL. Chapter 15: Bt crops: past and future. In: Sansinenea E,
(ed.) Bacillus Thuringiensis Biotechnology. New York, NY, USA: Springer Netherlands; 2012.
p. 283–304.
[65] Yu CG, Mullins MA, Warren GW, Koziel MG, Estruch JJ. The Bacillus thuringiensis vegetative
insecticidal protein Vip3A lyses midgut epithelium cells of susceptible insects. Appl Environ
Microbiol 1997;63:532–536.
[66] Lee MK, Walters FS, Hart H, Palekar N, Chen JS. The mode of action of the Bacillus thuringien-
sis vegetative insecticidal protein Vip3A differs from that of Cry1Ab δ-Endotoxin. Appl Environ
Microbiol 2003;69:4648–4657.
[67] Benbrook CM. Impacts of genetically engineered crops on pesticide use in the U.S. – the first
sixteen years. Environmental Sciences Europe 2012;24:1–13.
[68] Cerdeira AL, Duke SO. The current status and environmental impacts of glyphosate-sesistant
crops: A review. J Environ Qual 2006;35:1633–1658.
[69] Gianessi LP. Economic and herbicide use impacts of glyphosate-resistant crops. Pest Manag
Sci 2005;61:241–245.
[70] Powles SB. Evolved glyphosate-resistant weeds around the world: Lessons to be learnt. Pest
Manag Sci 2008;64:360–365.
[71] Zablotowicz, RM, Reddy KN. Impact of glyphosate on the Bradyrhizobium japonicum sym-
biosis with glyphosate-resistant transgenic soybean: A minireview. J Environ Qual 2004;33:
825–831.
[72] Horowitz J, Ebel R, Ueda K. “No-Till” Farming Is a Growing Practice/EIB-70. Washington DC,
USA: Economic Research Service, United States Department of Agriculture; 2010.
[73] Triplett GB, Dick WA. No-tillage crop production: A revolution in agriculture!. Agronomy Jour-
nal 100 Supplement 3 2008;S-153.
[74] Shaner DL. The impact of glyphosate-tolerant crops on the use of other herbicides and on
resistance management. Pest Manag Sci 2000;56:320–326.
[75] Wilcut SD, Askew JW. Cost and weed management with herbicide programs in glyphosate-
resistant cotton (Gossypium hirsutum). Weed Technology 1999;13:308–313.
[76] Johnson WG, Davis V, Kruger G, Weller S. Influence of glyphosate-resistant cropping systems
on weed species shifts and glyphosate-resistant weed populations. Eur J Agron 2009;31:
162–172.
[77] Sanchis V, Bourguet D. Bacillus thuringiensis: Applications in agriculture and insect resis-
tance management: A review. Agronomy for Sustainable Development 2008;28:11–20.
[78] Holland JM. The environmental consequences of adopting conservation tillage in Europe:
Reviewing the evidence. Agriculture, Ecosystems & Environment 2004;103:1–25.
[79] Dill-Macky R, Jones RK. The effect of previous crop residues and tillage on Fusarium head
blight of wheat. Plant Disease 2000;84:71–76.
[80] Munkvold GP. Cultural and genetic approaches to manage mycotoxins in maize. Ann Rev Phy-
topathol 2003;41:99–116.
[81] Munkvold GP, Hellmich RL, Showers WB. Reduced Fusarium ear rot and symptomless in-
fection in kernels of maize genetically engineered for European corn borer resistance. Phy-
topathology 1997;87:1071–1077.
[82] Parry D, Jenkinson P, McLeod L. Fusarium ear blight (scab) in small grain cereals – a review.
Plant Pathology 1995;44:207–238.
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 49

[83] Munkvold GP. Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Eur
J Plant Path 2003;109:705–713.
[84] Fernandez MR, Zentner RP, Basnyat P, Gehl D, Selles F, Huber D. Glyphosate associations
with cereal diseases caused by Fusarium spp. in the Canadian Prairies. Eur J Agron 2009;31:
133–143.
[85] Fernandez MR, Zentner RP, DePauw RM, Gehl D, Stevenson FC. Impacts of crop production
factors on common root rot of barley in Eastern Saskatchewon. Crop Sci 2007;47:1585–1595.
[86] Lévesque CA, Rahe JE, Eaves DM. Effects of glyphosate on Fusarium spp.: Its influence on root
colonization of weeds, propagule density in the soil, and crop emergence. Can J Microbiol
1987;33:354–360.
[87] Sanogo S, Yang XB, Scherm H. Effects of herbicides on Fusarium solani f. sp. glycines and
development of sudden death syndrome in glyphosate-tolerant soybean. Phytopathology
2000;90:57–66.
[88] Fernandez MR, Selles F, Gehl D, DePauw RM, Zentner RP. Crop production factors associ-
ated with Fusarium head blight in spring wheat in eastern Saskatchewan. Crop Sci 2005;45:
1908–1916.
[89] Karl TR, Melillo JM, Peterson TC. Global climate change impacts in the United States. U.S.
Global Climate Change Research Program. Cambirdge, United Kingdom: Cambridge Univer-
sity Press; 2009.
[90] Mearns L. The North American regional climate change assessment program (NARCCAP):
Overview of phase II results, 21st Conference on climate variability and change, Jan. 11–14,
2009, Phoenix, NV.
[91] Webster PJ, Holland GJ, Curry JA, Chang HR. Changes in tropical cyclone number, duration,
and intensity in a warming environment. Nature 2005;309:1844–1846.
[92] Stine AR, Huybers P, Fung IY. Changes in the phase of the annual cycle of surface tempera-
ture. Nature 2009;457:435–440.
[93] Kunkel KE, Liang XZ, Zhu J, Lin Y. Can CGCMs simulate the 20th century “warming hole” in the
central United States. J Climate 2006;19:4137–4153.
[94] Pan Z, Arritt RW, Takle ES, Gutowski WJ Jr, Anderson CJ, Segal M. Altered hydrologic feed-
back in a warming climate introduces a “warming hole”. Geophysical Research Letters
2004;31:L17109.
[95] Sutton JC. Epidemiology of wheat head blight and maize ear rot caused by Fusarium gramin-
earum. Can J Plant Path 1982;4:195–209.
[96] Nyvall RF, Kommedahl T. Individual thickened hyphae as survival structures of Fusarium
moniliforme in corn. Phytopathology 1968;58:1704–1707.
[97] Wicklow DT, Wilson DM, Nelsen TC. Survival of Aspergillus flavus sclerotia and conidia buried
in soil in Illinois or Georgia. Phytopathology 1993;83:1141–1147.
[98] Manzo SK, Claflin LE. Survival of Fusarium moniliforme hyphae and conidia in grain sorghum
stalks. Plant Disease 1984;68:866–867.
[99] Cotton TK, Munkvold GP. Survival of Fusarium moniliforme, F. proliferatum, and F. subgluti-
nans in maize stalk residue. Phytopathology 1998;88:550–555.
[100] Inch SA, Gilbert J. Survival of Gibberella zeae in Fusarium-damaged wheat kernels. Plant
Disease 2003;87:282–287.
[101] Born BW. Biodiversity of Aspergillus section Flavi in the United States: A review. Food Addi-
tives and Contaminants 2007;24:1088–1101.
[102] Jaime-Garcia R, Cotty PJ. Crop rotation and soil temperature influence the community struc-
ture of Aspergillus flavus in soil. Soil Biology & Biochemistry 2010;42:1842–1847.
50 | X. Li and X. B. Yang

[103] McGee DC, Olanya OM, Hoyos GM, Tiffany LH. Populations of Aspergillus flavus in the Iowa
cornfield ecosystem in years not favorable for aflatoxin contamination of corn grain. Plant
Disease 1996;80:742–746.
[104] Shearer JF, Sweets LE, Baker NK, Tiffany LH. A study of Aspergillus flavus/parasiticus in Iowa
crop fields 1988–1990. Plant Disease 1992;76:19–22.
[105] Will ME, Wilson DM, Wicklow DT. Evaluation of Paecilomyces lilacinus, chitin, and cellulose
amendments in the biological control of Aspergillus flavus fungi. Biology and Fertility of Soils
1994;17:281–284.
[106] Bale JS, Hayward SAL. Insect overwintering in a changing climate. Journal of Experimental
Biology 2010;213:980–994.
[107] Diffenbaugh NS, Krupke CH, White MA, Alexander CE. Global warming presents new chal-
lenges for maize pest management. Environment Research Letters 2008;3:1–9.
[108] Kocmánková E, Trnka M, Eitzinger J, et al. Estimating the impact of climate change on
the occurrence of selected pests at a high spatial resolution: A novel approach. J Agri Sci
2011;149:185–195.
[109] Bradshaw W, Holzapfel C. Evolutionary response to rapid climate change. Science
2006;312:1477–1478.
[110] Chiang HC, Hodson AC. Population fluctuations of the European corn borer, Ostrinia nubi-
lalis, at Waseca, Minnesota, 1948–70. Environmental Entomology 1972;1:7–16.
[111] Barber GW, Dicke FF. Effect of temperature and moisture on overwintering pupae of the corn
Earworm in the northeastern states. J Agri Res 1939;59(10):711–723.
[112] Hanec W, Beck SD. Cold hardiness in the European corn borer, Pyrausta nubilalis (Hübn.).
Journal of Insect Physiology 1960;5:169–180.
[113] Broders KD, Lipps PE, Paul PA, Dorrance AE. Evaluation of Fusarium graminearum associated
with corn and soybean seed and seedling disease in Ohio. Plant Disease 2007;91:1155–1160.
[114] Spangler SM, Calvin DD, Russo J, Schlegel J. Predicting risk of European corn borer infesta-
tion in sweet corn based on harvest date. HortTechnology 2009;19:173–180.
[115] Koehler B. Corn ear rots in Illinois Bulletin 639, Urbana-Champaign, IL, USA: Agricultural
Experiment Station, University of Illinois; 1959.
[116] Kommedahl T, Windels CE. Root-, stalk-, and ear-infecting Fusarium species on corn in the
USA. In: Nelson PE, Toussoun TA, Cook RJ (eds). Fusarium: Diseases, Biology, and Taxonomy.
University Park, PA, USA: Pennsylvania State University Press; 1981. p. 94–104.
[117] Foley D. Systemic infection of corn by Fusarium moniliforme. Phytopathology 1962;52:
870–872.
[118] Smith DR, White DG. Diseases of corn. In: Corn and Corn Improvement, 3rd ed Agronomy
Series No. 18. Am Soc Agronomy: Madison, WI, USA; 1988. p. 687–766.
[119] Diener UL, Cole RJ, Sanders TH, Payne GA, Lee LS, Klich MA. Epidemiology of aflatoxin forma-
tion by Aspergillus flavus. Ann Rev Phytopathol 1987;25:249–70.
[120] Paulitz T. Diurnal release of ascospores by Gibberella zeae in inoculated wheat plots. Plant
Disease 1996;80:674–678.
[121] Tschanz AT, Horst RK, Nelson P E. The effect of environment on sexual reproduction of Gib-
berella zeae. Mycologia 1976;68:327–340.
[122] Aylor DE. Aerobiology of fungi in relation to capture and release by plants. In: Lindow SE,
Hecht-Poinar EI, Elliott VJ (eds.) Phyllosphere Microbiology. American Phytopathological
Society: St. Paul, MN, USA; 2002. p. 341–361.
[123] Diener VL, Davis ND. Invasion of peanut pods in the soil by Aspergillus flavus. Plant Dis Rep
1965;49:931–935.
[124] Gourama H, Bullerman LB. Aspergillus flavus and Aspergillus parasiticus: Aflatoxigenic fungi
of concern in foods and feeds: A review. Journal of Food Protection 1995;58:1395–1404.
 2 Impact of climate change on genetically engineered plants and mycotoxigenic fungi | 51

[125] Gregory PH. The microbiology of the atmosphere. John Wiley & Sons: New York, USA; 1973.
[126] Sobek EA, Munkvold GP. European corn borer larvae as vectors of Fusarium moniliforme,
causing kernel rot and symptomless infection of maize kernels. Journal of Economic Entomol-
ogy 1999;92:503–509.
[127] Peters D, Pendleton J, Hageman R, Brown CM. Effect of night air temperature on grain yield of
corn, wheat, and soybeans. Agron J 1971;63:809.
[128] Chang JH. Corn yield in relation to photoperiod, night temperature, and solar radiation. Agri-
cultural Meteorology 1981;24:253–262.
[129] Lobell DB, Asner GP. Climate and management contributions to recent trends in U.S. agricul-
tural yields. Science 2003;299:1032.
[130] Reid LM, Nicol RW, Ouellet T, et al. Interaction of Fusarium graminearum and F. moniliforme in
maize ears: Disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology
1999;89:1028–1037.
[131] Booth C. The genus Fusarium. Kew, Surrey, England: Commonwealth Mycological Institute:
1971.
[132] Marín S, Magan N, Bellí N, Ramos AJ, Canela R, Sanchis V. Two-dimensional profiles of fumon-
isin B1 production by Fusarium moniliforme and Fusarium proliferatum in relation to envi-
ronmental factors and potential for modelling toxin formation in maize grain. International
Journal of Food Microbiology 1999;51:159–167.
[133] Jones RK, Duncan HE, Payne GA, Leonard KJ. Factors influencing infection by Aspergillus
flavus in silk-inoculated corn. Plant Disease 1980;64:859–863.
[134] Robens JF. A perspective on aflatoxins in field crops and animal food products in the United
States: A symposium. ARS-83. United States Department of Agriculture, Agricultural Research
Service (USDA-ARS): Peoria, Illinois, United States; 1990.
[135] Ingwersen J. Iowa begins mandatory testing of milk for aflatoxin, 2012 (accessed April 4,
2014, at [Link]
idUSBRE87U0ZV20120831.)
[136] Hershman DE, Vincelli P, Kaiser CA. Foliar fungicide use in corn and soybeans, PPFS-MISC-05.
Kentucky Cooperative Extension Service, University of Kentucky: Lexington, KY, USA; 2011.
[137] Dorrance AE, Cruz C, Mills D, et al. Effect of foliar fungicide and insecticide applications on
soybeans in Ohio. Online. Plant Health Progress doi:10.1094/PHP-2010-0122-01-RS, 2010.
[138] Henry RS, Johnson WG, Wise KA. The impact of a fungicide and an insecticide on soybean
growth, yield, and profitability. Crop Protection 2011;30:1629–1634.
[139] Wise K, Mueller D. Are fungicides no longer just for fungi? An analysis of foliar fungicide
use in corn. American Phytopathological Society, St. Paul, MN, USA: APSnet Features.
doi:10.1094/APSnetFeature-2011-0531; 2011.
[140] Paul PA, Madden LV, Bradley CA, et al. Meta-analysis of yield response of hybrid field corn to
foliar fungicides in the U.S. Corn Belt. Phytopathology 2011;101:1122–1132.
[141] Swoboda C, Pedersen P. Effect of fungicide on soybean growth and yield. Agron J 2009;
101:352–356.
[142] Garrett KA, Forbes GA, Savary S, et al. Complexity in climate-change impacts: an analytical
framework for effects mediated by plant disease. Plant Pathology 2011;60:15–30.
[143] Jeger MJ, Pautasso M. Plant disease and global change-the importance of long-term data
sets. New Phytologist 2008,177:8–11. doi:10.1111/j.1469-8137.2007.02312.x
José-Miguel Barea
3 Interactions among plants, arbuscular mycorrhizal
and mycotoxigenic fungi related to food crop
health in a scenario of climate change

3.1 Introduction

Climate change is a widely accepted probability, therefore its impacts on agro-ecosys-

tem stability and productivity must be considered [1–3]. Predictive climate models
support the likelihood that temperature increases and drought will have negative
influences on agricultural productivity in the present century [2]. Diverse studies have
therefore been performed to assess the impact of climate change on the different
agents and scenarios which interact in relation to agricultural developments [3]. One
field which has attracted remarkable research interest is the potential repercussion
of climate change on the incidence of plant diseases [4–6], with special emphasis
on those affecting production and quality of the main staple food crops as they can
negatively affect food security, especially in resource-poor regions [7, 8].
The 2009 Declaration of the World Summit on Food Security [9] considered that
“food security exists when all people, at all times, have physical, social and economic
access to sufficient, safe and nutritious food which meets their dietary needs and food
preferences for an active and healthy life”, identifying four pillars of food security:
availability, access, utilization, and stability. Agricultural output, especially cereal
crop production, will have to increase by 70 % to feed a world population expected
to surpass 9 billion in 2050 [9]. Cereals constitute approximately 56 % and 44 % of
the human and animal, energy consumption worldwide, respectively, and to meet de-
mands by 2050 the cereal crop production is projected to increase from the 2.5 billion
tons expected for 2014 to three billion tons [10, 11].
Diseases on cereals caused by species of the fungal genera Fusarium and As-
pergillus are of particular concern because these fungi can not only cause important
yield losses but also produce mycotoxins which enter the food chain and are detrimen-
tal to human and animal health [12]. Prior to harvest, the effects of climate change on
mycotoxins may occur via the fungi, hosts, or host-fungal interactions [13]. A number
of predictive models have been developed worldwide to estimate the risk of myco-
toxin contamination in cereals which take variables related to mycotoxigenic fungi
and plants into consideration[14], but none have taken the fact that most globally
important food crops establish beneficial relationships with mutualistic fungi, which
can help reduce crop losses from both biotic and abiotic above-belowground stresses
and address issues of food security into account [15].
54 | José-Miguel Barea

The multitrophic interactions which take place in soil, where the components of
soil microbiome are significant protagonists, have a great influence on food crop pro-
duction and health. These interactions are responsible for C sequestering, nutrient
cycling, pathogen suppression, biotic and abiotic stress alleviation, etc. A review of
the related literature suggests that climate change clearly affects these interactions,
and the design of appropriate predictive modeling approaches has therefore been rec-
ommended. However, elaboration of these models is hampered by high levels of un-
certainty when trying to put all the interacting agents together [3].
Among the members of plant-associated microbiomes, the arbuscular mycor-
rhizal (AM) fungi are recognized as one of the most beneficial groups of soil biota
[16]. These fungi are known to establish mutualistic AM symbiosis with most globally
important food crops, being fundamental for plant growth and health [17]. All cereals
hosting mycotoxigenic fungi are known to form AM symbiosis, but information on
interactions between AM and mycotoxigenic fungi is scarce.
The AM association can be considered an adaptive strategy which increases the
plant’s ability to capture nutrients and induces increased tolerance of environmen-
tal stress factors, either biotic (e.g. pathogen attack), or abiotic (e.g. drought, salinity,
heavy metals, organic pollutants, etc.) [18]. In particular, AM symbiosis protects plants
against deleterious organisms including microbial pathogens, herbivorous insects,
and parasitic plants. It has recently been clearly established that AM colonization can
prime plant immunity by boosting the plant’s ability to respond to a pathogen attack,
as part of the “mycorrhiza-induced systemic resistance” [19]. The diversity and activ-
ity of AM fungi, and the formation and functioning of AM symbiosis are all affected by
climatic change [20–22].
Considering the above ideas, the aims of this chapter are: (1) to offer an overview
of a key activity within the interactions between AM fungi and plants, namely the
impact of AM symbiosis on plant stress alleviation, particularly in inducing resis-
tance/tolerance of plants to/of pathogens and pests. Emphasis is put on the ability
of AM symbiosis to control shoot pathogens by eliciting a systemic, plant-mediated
resistance response, and the way in which AM colonization can prime plant immu-
nity by boosting the plant’s ability to respond to a pathogen attack, as part of the
“mycorrhiza-induced systemic resistance” abilities of AM fungi. (2) To analyze the
scarce publications on the interactions between mycotoxigenic and AM fungi in re-
lation to crop health, and to propose appropriate research approaches to improve our
understanding of these interactions; and (3) to discuss the perspectives, challenges,
and opportunities for exploiting AM services to control the activities of mycotoxigenic
fungi, with regards to promotion of food security in the current scenario of climatic
change.
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 55

3.2 Arbuscular mycorrhizal (AM) symbiosis

Most plants growing on earth live associated with endophytic soil fungi forming the
so-called mycorrhizas, but arbuscular mycorrhizal (AM) associations, the most com-
mon mycorrhizal type, form nearly 80 % of the major plant families, including eco-
nomically important crop species [16].
AM fungi are universally distributed soil-borne microbial fungi which originated
and diverged nearly 500 million years ago, as determined by molecular analyses and
fossil records. They form AM symbioses, the result of a common evolution history with
plants dating back more than 400 million years which seems to have facilitated the
adaptation of plants to the terrestrial environment. Actually, there is evidence to sug-
gest that AM fungi played a crucial role in land colonization by early plants and in
their evolution [23].
AM fungi are a subset of endophyte microorganisms which colonize plant tis-
sues symbiotically. Other endophytes include both bacteria and fungi, either mutu-
alistic or pathogens [14, 24–27]. AM fungi are asexual, unculturable and obligatorily
biotrophic microbes as they are unable to complete their life cycle without coloniz-
ing a host plant, a characteristic which hampered research of their biology and their
biotechnological applications [28]. The AM fungi belong to the phylum Glomeromy-
cota [23, 29, 30]. Diverse studies based on molecular approaches have indicated that
individual AM fungal ecotypes possess little host specificity, but a certain degree of
host preference (functional compatibility) was shown to occur [17].
Obviously, the more relevant biological characteristic of AM fungi is their capac-
ity to form AM associations involving almost all phyla of land plants in all soil and
biomes [16].

3.2.1 AM establishment, function, and management

AM fungi colonize plant roots from three types of propagules: spores, fragments of
mycorrhizal roots, and extraradical hyphae, all of which are a mycelial network ex-
panding in the soil. When a hypha from an AM mycelium approaches a host root,
a molecular dialogue between both symbionts occurs. This activates specific signal-
ing pathways which affect both fungal development and plant gene expression from
appressorium formation to the intracellular accommodation of the fungal symbiont
to ends with the formation of the characteristic tree-like structures, termed “arbus-
cules”, within the root cortical cells [28]. The arbuscules which give their name to the
mycorrhizal type are involved in the nutrient exchange between fungus and plant. The
major nutrient flux is the transfer of carbon from plant to fungus (and thereby to the
soil), and the movement of mineral nutrients from fungus to plant.
Once AM fungi consolidate the internal colonization of plant roots, they form an
extensive mycelial network outside the root by establishing an extraradical mycelium
56 | José-Miguel Barea

where AM spores develop, thereby ending the fungal life cycle. The extraradical
mycelium is actually a tri-dimensional structure specialized in the acquisition of
plant nutrients from soil, particularly those present in low concentrations in the soil
solution or which diffuse slowly to the uptake zone at the root (the rhizosphere), as
is the case with phosphate and ammonia [28]. In addition to the uptake of nutri-
ents, AM symbiosis improves plant fitness by increasing resistance to/tolerance of
environmental stresses, whether biotic (e.g. pathogens and pests) or abiotic (e.g. nu-
trient deficiencies, drought, salinity, heavy metals toxicity, or the presence of organic
pollutants), and also enhances soil structure through the formation of hydro-stable
aggregates necessary for good soil structure [28].
AM function concerning plant nutrient acquisition is based on the fact that the ex-
ternal mycelium of AM fungi extends from the roots to absorb and transport nutrients,
at a distance of up to 25 cm, while hyphal length densities in field soils range from 3
to 14 m/g [16]. Analysis of the biochemical and molecular mechanisms involved in the
coordinated nutrient transport processes in AM and in the bidirectional nutrient ex-
change between symbionts at the symbiotic interfaces is matter of recent and current
interest, as recently reviewed [28]. In summary, transport proteins putatively involved
in Pi uptake from soil solution by AM fungi and those implicated in the uptake of
the Pi exported across the membrane of the arbuscule have been identified in several
plant species. Gene expression studies of the plant Pi transporters have revealed that
development of symbiosis induces the novo expression of the so-called mycorrhiza-
specific Pi transporters, which are exclusively expressed in mycorrhizal roots, and up-
regulation of Pi transporters which have a basal expression in non-mycorrhizal roots,
the mycorrhiza up-regulated transporters.
Some advances have also been made in recent years in understanding the mech-
anisms of N transport. The N taken up by extraradical hyphae (either as ammonium
or nitrate), is assimilated in the fungal cytoplasm into arginine, transferred via the
tubular vacuoles to the intraradical hyphae to be released as urea, and either trans-
ported to the plant directly or after cleavage as ammonium. Genes encoding ammo-
nium transporters have so far been identified [31]. Both profiling technologies and
gene-to-phenotype reverse genetic tools are revealing the plant and fungal protein in-
volved in sustaining AM symbiosis, mostly on the basis of host-induced gene silencing
approaches [32].
AM fungi management has attracted greater interest as a result of the increased
demand for low-input agriculture because the manipulation and use of beneficial soil
microorganisms is recognized as a recommended strategy for more sustainable food
crop production based on the reduction of agrochemical maintenance while minimiz-
ing environmental degradation [17, 33]. Because of the importance of AM symbiosis in
sustainable agriculture, the development of techniques for AM inoculant production
and inoculation has become a central research topic and the available information
was recently reviewed [18]. The difficulty in culturing obligate symbionts such as AM
fungi in the absence of their host plant is a major obstacle for massive production
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 57

of inoculum. Despite this problem, a number of companies worldwide are producing

AM inoculum products which are being applied in forestry, agriculture, and horticul-
ture. Specific procedures are required to multiply AM fungi and produce high quality
inocula, and AM fungi are applied using different carriers, resulting in a wide range
of formulations, including encapsulation. Recent developments in AM inoculum pro-
duction systems include in vitro monoxenic root organ cultures.

3.2.2 AM and stress alleviation in plants

As indicated earlier, it is commonly accepted that AM associations helped plants to

thrive in hostile environments during their evolution, and continue to help plants de-
velop in stressed environments [18]. This is a critical AM role in the current scenario
of climate change, where adverse conditions tend to exacerbate diverse stress situa-
tions which negatively affect the functionality/productivity of agricultural systems. In
order to cope with adversity plants must develop adaptive strategies to increase their
resilience and overcome negative impacts of natural or anthropogenic environmental
stress conditions. AM symbiosis is considered an adaptive strategy since it increases
plant tolerance of environmental constraints [17]. As a general phenomenon, plant
perception of environmental stress cues triggers the activation of signaling molecules,
(for which phytohormones are protagonists), which, once the signal is processed, ends
with signal output enabling plants to respond to environmental constraints. Under-
standing how phytohormones act and interact in the signaling network, where jas-
monic acid (JA) plays a key role, is fundamental to learning how AM plant systems
thrive and survive in stressed environments. This understanding is essential to deci-
pher the complex regulation of plant growth and immunity, and to design biotechno-
logical strategies to optimize plant adaptation mechanisms and improve the ability of
AM fungi and other soil microbes to alleviate stress in crops [34].
Apart from this hormone-controlled signaling cascade, other ecological, physio-
logical, and molecular mechanisms are involved in the AM role in stress alleviation.
These mechanisms have been the subject of diverse experimental studies and reviews
over the last decade [18]. This information is briefly summarized in this chapter. The
mechanisms involved in AM activity to increase resistance to/tolerance of pathogens
and pests will be analyzed in depth in Section 3.3. We concentrate here on the mecha-
nisms related to the alleviation of abiotic stressors (nutrient deficits, salinity, drought,
and contamination).
The key AM fungi mechanisms for alleviation of the negative effects of nutrient
deficits are based primarily on those described earlier: both the characteristics of the
external mycelium, and the fact that gene expression related to the transport proteins
is up-regulated under P and N deficit [28].
To alleviate the negative effects of osmotic stressors (drought, salinity . . . ), plants
must develop a number of adaptation mechanisms, mainly including fine regulation
58 | José-Miguel Barea

of their water uptake capacity and transpiration rate, and activation of the antioxidant
machinery to overcome the overproduction of reactive oxygen species (ROS) caused
by stress. These two general mechanisms (maintaining water and ROS balance) may
be ameliorated by the establishment of AM symbiosis which acts via diverse specific
mechanisms. These can be summarized as follows: (1) cell osmoregulation; (2) ionic
homeostasis; (3) regulation of root water uptake and redistribution along plant tissues
by aquaporins; (4) defense against antioxidants; and (5) maintenance of photosyn-
thetic capacity. Such microbial activities result in better regulation of plant water sta-
tus and contribute to increasing plant resistance to osmotic stress conditions. Finally,
the improved water uptake capacity of microbized plants allows them to have higher
transpiration rates and hence higher photosynthetic rates under conditions of water
deficit. Particular attention is being paid to the role played by AM fungi in improving
plant water status based on the improvement of root hydraulic conductance, which
ultimately depends on aquaporin function. The available information on the subject
was recently discussed [35–39].

3.2.3 Effects of agricultural practices on AM symbiosis

Agricultural practices such as tillage, fertilizer and pesticide application, monocul-

tures, crop rotations with non-host plants, and fallow periods are known to have a
significant negative effect on the natural biodiversity, abundance, and mycelial de-
velopment of AM fungi in soils and on the establishment of AM symbiosis [17]. In
uncultivated soils, host plants are colonized by extraradical hyphae, which consti-
tute the main source of AM fungal inoculum [40]. In agricultural systems, soil tillage
breaks up the network of extraradical AM hyphae formed by indigenous AM fungal
populations, hindering colonization of the roots of cultivated plants and thereby re-
ducing or preventing the benefits associated with symbiosis [41, 42]. The richness and
abundance of AM fungal species and their spores have also been found to decrease
in conventionally tilled soils relative to untilled soils [43, 44]. Similar effects on AM
root colonization and spore abundance have been observed in agricultural systems of
continuous monoculture, after non-host corps, or after long fallow periods [45–47].
Phosphorus (P) fertilization leading to a P supply in the soil which exceeds the
crop’s requirements frequently preclude mycorrhizal development, whilst low-input
crop production systems may enhance mycorrhizal activity [48]. Under high P avail-
ability in soil, the P concentration in plant tissue increases to a level which causes a
reduction both in the extent of root AM colonization and in the length of extraradical
hyphae [49].
The reported effects of pesticides on AM symbiosis have been very varied. Recent
studies [50, 51] have shown that glyphosate, a herbicide used globally, significantly
decreases root mycorrhization and AM fungal spore viability and biomass in soil. How-
ever, no negative effects of nicosulfuron (used for the post-emergence control of weeds
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 59

in maize) on mycorrhizal colonization and AM fungal richness in the field at dose rates
× 1, × 2 and × 5 the recommended dose were found [52]. Increasing doses of fenpropi-
morph and fenhexamid, fungicides belonging to the family of sterol biosynthesis in-
hibitors (SBI), widely used in agriculture, have negative effects on hyphal develop-
ment, physiology, and metabolism of AM fungi [53, 54]. In contrast, several insecti-
cides (aldicarb, fenamiphos and dimethoate) did not affect AM symbiosis [55].

3.3 Interactions among plants, AM symbiosis, and mycotoxigenic

fungi related to plant health

Before properly discussing the scarce information on the interactions between AM and
mycotoxigenic fungi related crop plant health, we present a brief analysis of the role
of AM fungi on plant protection against pathogens and pests and the mechanisms
underlying such effects. Special attention will be given to the modulation of the plant
immune system by AM fungi for induced systemic resistance and to priming for en-
hanced defense by AM fungi. These mechanisms may be involved in possible interac-
tions between AM and mycotoxigenic fungi.

3.3.1 The effect of AM on plant protection against pathogens and pests

Diverse studies have shown the protective effect of AM colonization against infections
by microbial pathogens, pests, and parasitic plants [19, 56, 57]. Remarkably, AM for-
mation protects plants not only against soil-borne plant pathogens, but also against
some which attack shoots. For the most part because of this systemic protection, the
term mycorrhiza-induced resistance (MIR) was therefore coined [58].
In fact, AM symbiosis is known to reduce the damage caused by diverse soil-borne
pathogens including fungi (Fusarium, Rhizoctonia, Verticillium, Phytophthora, and
Pythium), bacteria, and parasitic nematodes [57]. Several mechanisms can operate
simultaneously including competition with soil-borne pathogens for space and nutri-
ents, altering root morphology or the quality and quantity of root exudates. The use
of experimental split-root systems allowed us to confirm that protection by AM fungi
is manifested in non-colonized areas of the root system. These experiments based on
physical separation of AM fungi and the aggressor demonstrated the involvement of
plant-mediated responses in enhancing plant resistance, as discussed later [57].
Furthermore, the ability of AM symbiosis to control shoot pathogens by eliciting
a systemic, plant-mediated, resistance response was also shown [57, 58]. Transcrip-
tional regulation of defense-related genes and accumulation of insect antifeedant
compounds have been reported in the shoots of AM plants. The effect of AM symbiosis
on controlling pathogens with a hemibiotrophic lifestyle varies from no effect to a re-
60 | José-Miguel Barea

duction of the disease, but there is evidence of a more generalized positive effect of AM
symbiosis in promoting plant resistance against necrotrophic shoot pathogens [57].
Multitrophic AM-plant-herbivore interactions have been the subject of diverse
studies [57]. According to this review, AM symbiosis can influence the performance of
insect herbivores, but the end result will depend on a compromise between a positive
effect derived from enhanced plant growth and a negative effect derived from induced
resistance in the plant, and depends on the type of insect attacking. Generalist insects
are usually affected negatively by the presence of AM fungi, while specialist insects
usually perform better on AM plants, probably because of the improved nutritional
quality of the host. The degree of protection also depends on feeding type of the attack-
ing insect. Phloem-sucking insects are little affected by the host immune response,
while leaf chewers and miners are usually negatively affected by AM fungi.
Some plants (Striga, Orobanche, and Phelipanche) can parasitize a number of
important crop plants and are considered amongst the most damaging agricultural
pests [59]. López-Ráez et al. [59] revised several experimental studies and concluded
that germination and emergence of Striga seeds are reduced in AM plants. They dis-
cussed the potential role of strigolactones, a new class of plant hormones, emerging
as a new biological control strategy against weeds. Strigolactones are exuded into
soil, where they are known to act both as host detection signals for AM formation
and as germination stimulants for root parasitic plant seeds. As strigolactone pro-
duction is significantly reduced on establishment of AM symbiosis, a lowering of the
germination rate of weed seeds is shown. This reduction therefore seems to be the
mechanism underlying the decrease in incidence and damage of root parasitic weeds
on crop plants when properly mycorrhizal and suggests the potential of AM symbiosis
in controlling root parasitic weeds.

3.3.2 Mycorrhiza-induced resistance and priming of plant defenses

Both AM and pathogenic fungi have to cope with the plant immune system and diverse
elicitors (microbe-associated molecular partners [MAMPs]) and effectors, the micro-
bial molecules responsible for triggering resistance mechanisms, have been charac-
terized. In AM fungi, lipochitooligosaccharides have been described as fundamental
elicitors which activate responses in the host plants [30]. During the early stages of in-
teraction in AM formation, the plant reacts to the presence of AM fungi by activating
defense-related responses which are subsequently suppressed. Therefore, AM fungi
have to modulate plant defense responses to achieve functional root colonization.
Consequently, a mild but effective activation of the plant immune response occurs
both locally and systemically [57].
Once the AM fungus is established in root tissue, the plant has to regulate the level
of AM fungal proliferation within the roots, prevent colonization of vascular tissue,
and avoid carbon drainage due to excessive colonization. Maintaining the equilibrium
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 61

in this mutual symbiosis is associated with the modulation of the host plant’s immune
system by AM fungi, resulting in plant defense mechanisms not only regulating and
controlling the symbiosis, but also directly impacting on root pathogens [19]. Such
modulation may precondition plant tissue, allowing more efficient activation of de-
fense mechanisms in response to attack by potential enemies, a phenomenon known
as priming [58].
The mechanisms underlying the modulation of plant defense responses by AM
fungi, which behave as a biotrophic microorganism, involve a quick but transient
increase of endogenous salicylic acid (SA) in the roots combined with an accumu-
lation of defensive compounds such as reactive oxygen species, specific isoforms of
hydrolytic enzymes, and the activation of the phenylpropanoid pathway [40]. Recent
studies demonstrate that AM fungi suppress plant defense reactions by secreting ef-
fector proteins which interfere with the host’s immune system [60]. In the case of
AM symbiosis, the levels of SA and other defense-related phytohormones such as jas-
monic acid (JA), abscisic acid (ABA), and ethylene (ET) appear altered in AM roots,
where ABA is also fundamental for AM function [61]. The regulation of defense signal-
ing molecules involved in the modulation of plant immunity by AM fungi may play a
major role in MIR which is also expressed in aboveground plant tissues, producing a
systemic response effective against plant pathogens and herbivores. Interestingly, AM
plants are more resistant to necrotrophs and chewing insects, which are sensitive to
JA-dependent defense responses, while AM plants are more susceptible to biotrophs,
which are sensitive to SA-regulated defenses. In fact, the activation of JA-dependent
and repression of SA-dependent defenses have been demonstrated during develop-
ment of AM symbiosis [58, 59, 61, 62].
A key point to consider is that the constitutive expression of defenses is too costly
for the plant in the absence of challenging attackers. However, some microorganisms
have developed the ability to enhance resistance not only via direct activation of de-
fenses but also by inducing sensitization of the tissues on appropriate stimulation to
express basal defense mechanisms more efficiently after a subsequent pathogen at-
tack. This preconditioning of plant tissues is known as the priming of the plant defense
[58, 59, 63]. Priming maintains the plant in an “alert” state in which defenses are not
actively expressed but get the plant prepared to respond to any attack in a faster and/or
stronger manner in comparison to plants which have not had the priming stimulus.
This results in increased plant resistance. Priming therefore confers important plant
fitness benefits in terms of plant health [57]. Additionally, preconditioning of plant
tissues for a quick and more effective activation of defenses on attack has important
ecological fitness benefits compared to direct activation of defenses. This boost (prim-
ing) of basal defenses is successfully developed by AM fungi and can be considered
the main mechanism operating in MIR, as deduced by the stronger defense reactions
triggered in the AM plant upon attack [58].
Studies on primed defense responses in AM plants have been reviewed [58]. Pre-
liminary studies referred to primed roots and include experiments involving attack
62 | José-Miguel Barea

by Fusarium (AM transformed carrot roots), Phytophthora parasitica (tomato), Rhi-

zoctonia (potato), and F. oxysporum (date palm trees). It was shown that the primed
response is not restricted to the root system but also operates in the shoots of AM
plants. In fact, in tomato plants AM symbiosis induced systemic resistance against
the necrotrophic foliar pathogen Botrytis cinerea. It was found that the amount of
pathogen in the leaves of AM plants was significantly lower, while the expression of
some JA-regulated, defense-related genes was higher in AM plants [64]. Gene expres-
sion and enzymatic activities were monitored in a time-course experiment after shoot
(tomato) treatment with JA, ET, and SA. Transcript profiling of the leaves of AM and
non-AM plants on treatment with JA indicated a stronger induction of JA-regulated
genes in AM plants, including typical defense-related JA responsive genes supporting
a prominent role of priming for JA-dependent responses in AM-induced resistance [19].

3.3.3 Interactions between AM symbiosis and mycotoxigenic fungi

It would be expected that the prophylactic ability of AM symbiosis could be applied

to the biological control of mycotoxigenic fungi. However, to our knowledge the pub-
lished information on this topic is scarce. Using confrontation cultures Ismail et al. [65]
reported that the growth of Fusarium sambucinum, the causal agent of tuber sprout
rotting in potato [66], was significantly reduced in the presence of the AM fungus
Glomus irregulare, and that the relative expression of the TRI5 gene in F. sambucinum
was up-regulated and that of TR101 gene greatly down-regulated after confrontation
with isolates of G. irregulare. The predominant mycotoxin of F. sambucinum is 4,15-
diacetoxyscirpenol (DAS), a trichothecene toxic to humans and animals [65, 67].
TR15 encodes the first enzyme involved in the trichothecene biosynthesis pathway
and TR101 encodes a trichothecene 3-O-acetyltransferase which acetylates the C-3 of
various Fusarium trichothecenes, converting them to less toxic products [68, 69].
The role of G. irregulare on the biocontrol of F. sambucinum on potato has been
studied [70]. The authors demonstrated that inoculation of the AM fungus signifi-
cantly reduced disease severity of F. sambucinum on mycorrhizal potato plants with
respect to those infected and non-mycorrhizal, also decreasing the negative effects of
the pathogen on biomass and potato tuber production. The study also showed that
G. irregulare could regulate expression of certain defense-related potato genes and
thus promote resistance against F. sambucinum.
Although further research is needed, the scarce information available suggests
that AM symbiosis may play an important role in the protection of cultivated plants
against pathogenic Fusarium species and their mycotoxins, through the regulation of
defense-related genes and/or the modulation of mycotoxin gene expression.
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 63

3.3.4 Impact of climate change on AM fungi and repercussions for the protection
of food crops against fungal diseases

Intensive agriculture production is fundamental to satisfy food requirements for the

growing world population. However, its realization is associated with the mass con-
sumption of non-renewable natural resources, with environmental contamination,
and with the emission of greenhouse gases causing climate change. Society and
science are becoming aware that sustainable agricultural approaches are therefore
needed, but the impacts of climate change must be considered because of their in-
fluence on soil fertility, crop nutrition, and on the production of healthy food [1, 2].
Actually, evidence is accumulating to show that the CO2 emissions derived from man-
mediated activities are submitting the earth to warming regardless of the mitigation
strategies now applied [20], therefore the mitigation approaches must be improved.
Factors involved in climate change, such as elevated CO2 levels, are known to influ-
ence the incidence and effect of plant diseases, particularly the appearance of new
diseases, and also to influence the performance of mycotoxigenic fungi, as discussed
in other chapters. We will therefore deal specifically with AM fungi.
How climate change affects the activity of plant-associated microorganisms re-
lated to nutrient cycling or to disease occurrence has been the subject of a number of
analyses [20, 71, 72]. The general conclusion of these studies is that the information is
fragmentary and that much more research is needed to understand and predict plant
responses to global changes under natural conditions. Actually, our ability to predict
the impact of global environmental change on plant-microbiome interactions and to
know how the biotic responses to such changes are regulated is hampered because of
our limited understanding of these interactions.
The first analyses on the impact of climate change on AM formation and function,
reviewed ten years ago, mainly addressed natural ecosystems, and either studied the
potential of AM symbiosis to mitigate the impact of global change on plant communi-
ties [73] or described the response of AM symbiosis to elevated atmospheric CO2 [74]. It
appears that the effects on AM fungi were largely controlled by host-plant responses,
however, these fungi can respond directly to elevated soil temperature, a fact which
may have large implications for the rates of C cycling. Evidence shows that AM fungal
hyphae may have a very short life, resulting in rapid return of C to the atmosphere;
evaluation of the impact of soil temperature on hyphal turnover is therefore funda-
mental [74].
More recent review articles support that predicted global surface temperature rise
affects AM fungi. The general conclusion of one of these studies [24] is that soil tem-
perature increase has a positive impact on AM fungal root colonization and hyphal
length. Another review article [75] emphasizes that rising global atmospheric CO2 lev-
els also affect AM fungal diversity, abundance, and function. As an increase in CO2 en-
hances photosynthetic rates, more C is directed to the soil pool and AM fungi, which
will benefit AM services, including nutrient cycling and plant health promotion. In
64 | José-Miguel Barea

contrast, anthropogenic N deposition reduces AM fungal diversity and abundance;

however literature describing the effects of elevated CO2 and N deposition interaction
on AM fungi is scarce.
In an exhaustive analysis of the rhizosphere responses to elevated CO2 [22], it was
found that an increased allocation of CO2 from photosynthesis is directed to myc-
orrhizas, which then translocate C into microbial communities. This is traduced in
changes in structure, size, and activities of the plant associated microbiome in the
mycorrhizosphere. These changes result in an increased rate of respiration and the
subsequent return of CO2 to the atmosphere.
Environmental changes, such as elevated CO2 , are recognized as a key factor in-
fluencing the incidence of plant diseases or the appearance of new diseases [2, 7]. All
in all, predictions have considerable uncertainty and future disease trends may be
different for each geographic region [76].

3.3.5 Research perspectives and opportunities for exploiting the interactions

between mycotoxigenic and AM fungi with regard to plant health as affected
by climate change

Implementation of control practices for mycotoxigenic fungi is necessary to produce

healthy foods. Because sustainable agricultural practices must be followed, the log-
ical techniques are those based on applying biological control approaches. Here we
propose the use of AM fungi for such purposes. In fact, AM fungi are considered
a biotechnological tool for linking biotic and abiotic agricultural facts involved in
healthy crop production in a climate change scenario [77].
Concerning the interactions between mycotoxigenic and AM fungi in relation to
plant health, it is necessary to propose research approaches, firstly, to improve our
understanding of these interactions, and secondly to establish appropriate conditions
allowing the expression of the AM abilities to control the pathogen. To the author’s
knowledge, the first available studies in this field of research are those discussing the
possibility of using AM fungi for the biocontrol of the mycotoxigenic fungus Fusarium
sambucinum [65, 70]. However, in order to further develop the use of AM fungi for
the biological control of mycotoxigenic fungi, other considerations related to the pro-
phylactic possibilities of AM fungi must be taken into account. In this context, a key
mechanism for efficient protection against pathogens is defense priming, the precon-
ditioning of immunity induced by microbial colonization after seed germination [78].
AM fungi are particularly recognized for their ability to prime plant defense [19], and
have coevolved with plants by establishing AM symbiosis, also evolving developmen-
tal signals involved in immunity maturation [28].
In the future, the exploitation of AM symbiosis to protect plants against deleteri-
ous organisms, particularly fungal pathogens, is highly recommended by exploiting
the recently established fact that AM colonization can prime plant immunity by boost-
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 65

ing plant defenses to respond to pathogen attack, as part of the “mycorrhiza-induced

systemic resistance” ability of AM fungi [19]. This ability must be explored using AM
fungi isolated from the rhizosphere of the target food crop plants to be screened in
greenhouse assays challenging mycotoxigenic fungi. Such studies under controlled
conditions may help improve our understanding of the interactions between AM and
mycotoxigenic fungi and to define the conditions where mycotoxin production can be
reduced. The selected AM fungi must then be tested in small-scale studies under field
conditions. All in all, we need to improve our knowledge of the interactions among
plants, mycotoxigenic and AM fungi, to establish biocontrol measurements in a cli-
mate change scenario. Meta-analyses aimed at analyzing the responses of plants and
their fungal associates to global change factors are recommended in order to allow
us to establish general trends in the responses of plant–fungal symbioses to future
environments.
A model study on this subject [79] was based on a meta-analysis of 434 studies an-
alyzing the responses of plants and their associated fungal symbionts, including class
I leaf endophytes and AM fungi, to four global change factors (enriched CO2 , drought,
N deposition, and warming). The class I leaf endophytes are known to protect plants
against insect pests and vertebrate herbivores, drought, and nutrient deficits, but also
to produce secondary metabolites toxic for animals. In general, fungal symbionts in-
crease plant biomass and ameliorate the negative effects of global change, but the
meta-analysis revealed gaps in current research analyzing the responses of plant–
fungal symbioses to global change. The authors [79] confirm that it is critical to con-
sider plant-fungal symbiosis to predict plant responses to global change. Most studies
in the meta-analysis were conducted within the greenhouse and therefore may not
reflect responses under field conditions. Multiple fungal symbionts were analyzed by
means of paired studies aimed at analyzing effects on plant performance, but hardly
commented on how mycosymbionts interact amongst themselves, and did not focus
on biological control of AM fungi over mycotoxigenic fungi.
In conclusion, several issues can be pointed out. Probably the most critical point
is that information on interactions between symbiotic fungi, such as mutualistic AM
and mycotoxigenic fungi (pathogenic Fusarium and others in cereals), is scarce. Only
a small number of publications refer to changes in the colonization rates of the sym-
bionts involved, which is important in controlling pathogen development. Consider-
ing the prophylactic ability of AM fungi, more research on their interactions with my-
cotoxigenic fungi are highly recommended. This may be more urgently needed in the
current/future scenario of climate change, where AM services appear fundamental for
the production of healthy crops, and where the impact of mycotoxigenic fungi appears
to pose a threat to food security. In fact, AM symbiosis can be considered an adaptive
strategy which provides the plant with an increased ability to alleviate stress, be it
biotic (pathogen attack) or abiotic (nutrient deficit, drought, salinity, etc.).
For the aims of this chapter we have concentrated on biotic stress alleviation. As
stated earlier, it is fundamental to remember that AM symbiosis protects plants against
66 | José-Miguel Barea

deleterious organisms, including microbial pathogens, herbivorous insects, and par-

asitic plants. Furthermore, the ability of AM symbiosis to control shoot pathogens by
eliciting a systemic, plant-mediated resistance response has also been shown. Results
from the last few years have clearly shown that AM colonization can prime plant im-
munity by boosting the plant’s ability to respond to pathogen attack, as part of the
“mycorrhiza-induced systemic resistance”. The mechanisms involved in modulation
of the host plant’s immune system by AM fungi and the priming of plant defense have
been established. These findings support the scientific basis for proposing appropriate
research approaches to understand how mycotoxigenic and AM fungi interact. This is
relevant in order to define perspectives, challenges, and opportunities for exploiting
AM services to control the activities of mycotoxigenic fungi, with regards to promoting
food security in the current scenario of climate change.

References

[1] St Clair SB, Lynch JP. The opening of Pandora’s Box: climate change impacts on soil fertility
and crop nutrition in developing countries. Plant Soil 2010;335:101–115.
[2] Dwivedi S, Sahrawat K, Upadhyaya H, Ortiz R. Food, nutrition and agrobiodiversity under
global climate change. Adv Agron 2013;120:1–128.
[3] Chakraborty S, Pangga IB, Roper MM. Climate change and multitrophic interactions in soil: the
primacy of plants and functional domains. Glob Change Biol 2012;18:2111–2125.
[4] Coakley SM, Scherm H, Chakraborty S. Climate change and plant disease management. Annu
Rev Phytopathol 1999;37:399–426.
[5] Roos J, Hopkins R, Kvarnheden A, Dixelius C. The impact of global warming on plant diseases
and insect vectors in Sweden. Eur J Plant Pathol 2011;129:9–19.
[6] Pautasso M, Doering TF, Garbelotto M, Pellis L, Jeger MJ. Impacts of climate change on plant
diseases-opinions and trends. Eur J Plant Pathol 2012;133:295–313.
[7] West JS, Townsend JA, Stevens M, Fitt BDL. Comparative biology of different plant pathogens
to estimate effects of climate change on crop diseases in Europe. Eur J Plant Pathol
2012;133:315–331.
[8] Newton AC, Johnson SN, Gregory PJ. Implications of climate change for diseases, crop yields
and food security. Euphytica 2011;179:3–18.
[9] FAO 2009. World Summit on Food Security 2009. Declaration of the World Summit on Food
Security. WSFS 2009/2. Rome: Food and Agriculture Organization of the United Nations (FAO).
Available at [Link]
WSFS09_Declaration.pdf.
[10] FAO. 2014. Crop Prospects and Food Situation № 2. Rome: Trade and Markets Division, Food
and Agriculture Organization of the United Nations (FAO). Available at [Link]
[Link].
[11] Alexandratos N, Bruinsma J. World agriculture towards 2030/2050: the 2012 revision. Rome:
Food & Agriculture Organization of the United Nations Statistics. 2012.
[12] Chakraborty BN, Chakraborty U, Rai K, Allay S, Dey PL. Molecular detection of fungal
pathogens of Citrus reticulata grown in Darjeeling hills and their management. II International
Symposium on Citrus Biotechnology 2011;892:189–206.
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 67

[13] Paterson RRM, Lima N. How will climate change affect mycotoxins in food? Food Res Int
2010;43:1902–1914.
[14] Magan N, Medina A, Aldred D. Possible climate-change effects on mycotoxin contamination of
food crops pre- and postharvest. Plant Pathol 2011;6:150–163.
[15] Orrell P, Bennett AE. How can we exploit above–belowground interactions to assist in address-
ing the challenges of food security? Front Plant Sci 2013;4.
[16] Smith SE, Read DJ. Mycorrhizal Symbiosis. 3rd ed. New York: Elsevier Academic Press; 2008.
[17] Jeffries P, Barea JM. Arbuscular Mycorrhiza – a key component of sustainable plant-soil ecosys-
tems. In: Hock B (ed). The Mycota, a comprehensive treatise on fungi as experimental systems
for basic and applied research. Berlin, Heidelberg: Springer; 2012. p. 51–75.
[18] Barea JM, Pozo MJ, López-Ráez JA, Aroca R, Ruíz-Lozano JM, Ferrol N, Azcón R, Azcón-Aguilar
C. Arbuscular Mycorrhizas and their significance in promoting soil-plant systems sustainabil-
ity against environmental stresses In: Rodelas B, González-López J. (eds). Beneficial Plant-
Microbial Interactions: Ecology and Applications. Boca Raton, USA: CRC Press; 2013. p. 353–
387.
[19] Pozo MJ, Jung SC, Martínez-Medina A, López-Ráez JA, Azcón-Aguilar C, Barea JM. Root allies:
Arbuscular mycorrhizal fungi help plants to cope with biotic stresses. In: Aroca R (ed.) Symbi-
otic Endophytes. Berlin Heidelberg: Springer-Verlag; 2013. p. 289–307.
[20] Compant S, van der Heijden M, Sessitsch A. Soil warming effects on beneficial plant-microbe
interactions. In: de Bruijn FJ (ed). Molecular Microbial Ecology of the Rhizosphere. Hoboken,
New Jersey, USA: John Wiley & Sons; 2013. p. 1045–1054.
[21] Rodríguez AA, Córdoba AR, Ortega L, Taleisnik E. Decreased reactive oxygen species concen-
tration in the elongation zone contributes to the reduction in maize leaf growth under salinity.
J Exp Bot 2004;55:1383–1390.
[22] Drigo B, Kowalchuk GA. Rhizosphere responses to elevated CO2 . In: de Bruijn FJ (ed.) Molecu-
lar Microbial Ecology of the Rhizosphere. Hoboken, New Jersey, USA: John Wiley & Sons; 2013.
p. 1063–1074.
[23] Schüßler A, Walker C. Evolution of the ‘plant-symbiotic’ fungal phylum, Glomeromycota. In:
Pöggeler S, Wöstemeyer J (eds). Evolution of Fungi and Fungal-Like Organisms. Berlin, Heidel-
berg: Springer-Verlag; 2011. p. 163–185.
[24] Zuccaro A, Lahrmann U, Langen G. Broad compatibility in fungal root symbioses. Curr Opin
Plant Biol 2014;20:135–145.
[25] Porras-Alfaro A, Bayman P. Hidden fungi, emergent properties: Endophytes and microbiomes.
Ann Rev Phytopathol 2011;49:291–315.
[26] Mercado-Blanco, J. 2015. Life of microbes inside the plant. In: Lugtenberg B (ed). Principles of
Plant-Microbe Interactions. Switzerland, Heidelberg: Springer International Publishing; 2015.
p. 25–32.
[27] Malfanova N, Lugtenberg BJJ, Berg G. Bacterial endophytes: who and where, and what are they
doing there? In: de Bruijn FJ (ed). Molecular Microbial Ecology of the Rhizosphere. Hoboken,
New Jersey, USA: Wiley Blackwell; 2013. p. 393–403.
[28] Barea JM, Azcón-Aguilar C. Evolution, biology and ecological effects of arbuscular mycorrhiza.
In: Camisao AF, Pedroso CC (eds). Symbiosis: Evolution, Biology and Ecological Effects. New
York: Nova Science; 2013. p. 1–34.
[29] Schüßler A, Gehrig H, Schwarzott D, Walker C. Analysis of partial Glomales SSU rRNA gene
sequences: implications for primer design and phylogeny. Mycol Res 2001;105:5–15.
[30] Corradi N, Bonfante P. The arbuscular mycorrhizal symbiosis: Origin and evolution of a benefi-
cial plant infection. PLoS Pathog 2012;8(4);e1002600. Doi: 10.1371/[Link].1002600.
68 | José-Miguel Barea

[31] Ferrol N, Pérez-Tienda J. Coordinated nutrient exchange in arbuscular mycorrhiza. In: Azcón-
Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds). Mycorrhizas Functional Pro-
cesses and Ecological Impact. Berlin, Heidelberg: Springer-Verlag; 2009. p. 73–87.
[32] Recorbet G, Abdallah C, Renaut J, Wipf D, Dumas-Gaudot E. Protein actors sustaining arbuscu-
lar mycorrhizal symbiosis: underground artists break the silence. New Phytol 2013;199:26–40.
[33] Fester T, Sawers R. Progress and challenges in agricultural applications of arbuscular mycor-
rhizal fungi. Crit Rev Plant Sci 2011;30:459–470.
[34] Pozo M, López-Ráez J, Azcón-Aguilar C, García-Garrido JM. Phytohormones as integrators of
environmental signals in the regulation of mycorrhizal symbioses. New Phytol 2015;205:1431–
1436.
[35] Ruíz-Lozano JM, Porcel R, Azcón C, Aroca R. Regulation by arbuscular mycorrhizae of the in-
tegrated physiological response to salinity in plants: new challenges in physiological and
molecular studies. J Exp Bot 2012;63:4033–4044.
[36] Ruíz-Lozano JM, Porcel R, Barzana G, Azcón R, Aroca R. Contribution of arbuscular mycorrhizal
symbiosis to plant drought tolerance: state of the art. In: Aroca R (ed). Plant Responses to
Drought Stress From Morphological to Molecular Features. Heidelberg, Germany: Springer;
2012. p. 335–362.
[37] Aroca R, Porcel R, Ruíz-Lozano JM. Regulation of root water uptake under abiotic stress condi-
tions. J Exp Bot 2012;63:43–57.
[38] Porcel R, Aroca R, Ruíz-Lozano JM. Salinity stress alleviation using arbuscular mycorrhizal
fungi. A review. Agron Sustain Develop 2012;32:181–200.
[39] Calvo-Polanco M, Sánchez-Romera B, Aroca R. Arbuscular mycorrhizal fungi and the tolerance
of plants to drought and salinity. In: Aroca R (ed). Symbiotic Endophytes. Berlin, Heidelberg:
Springer-Verlag; 2013. p. 271–288.
[40] Bárzana G, Aroca R, Bienert GP, Chaumont F, Manuel Ruíz-Lozano J. New Insights into the
regulation of aquaporins by the arbuscular mycorrhizal symbiosis in maize plants under
drought stress and possible implications for plant performance. Mol Plant-Microbe Interact
2014;27:349–363.
[41] McGonigle TP, Miller MH. Development of fungi below ground in association with plants grow-
ing in disturbed and undisturbed soils. Soil Biol Biochem 1996;28:263–269.
[42] Kabir Z. Tillage or no-tillage: Impact on mycorrhizae. Can J Plant Sci 2005;85:23–29.
[43] Boddington CL, Dodd JC. The effect of agricultural practices on the development of in-
digenous arbuscular mycorrhizal fungi. I. Field studies in an Indonesian ultisol. Plant Soil
2000;218:137–144.
[44] Curaqueo, G, Barea, JM, Acevedo, E, Rubio, R, Cornejo, P, Borie, F. Effects of different tillage
system on arbuscular mycorrhizal fungal propagules and physical properties in a Mediter-
ranean agroecosystem in central Chile. Soil Till Res 2011;113:11–18.
[45] Smith TF. The effect of season and crop-rotation on the abundance of spores of vesicular-
arbuscular (VA) mycorrhizal endophytes. Plant Soil 1980;57:475–479.
[46] Sieverding E, Leihner DE. Influence of crop-rotation and intercropping of cassava with legumes
on va mycorrhizal symbiosis of cassava. Plant Soil 1984;80:143–146.
[47] Thompson JP. Decline of vesicular-arbuscular mycorrhizae in long fallow disorder of field crops
and its expression in phosphorus deficiency of sunflower. Aust J Agric Res 1987;38:847–867.
[48] Grant C, Bittman S, Montreal M, Plenchette C, Morel C. Soil and fertilizer phosphorus: Effects
on plant P supply and mycorrhizal development. Can J Plant Sci 2005;85:3–14.
[49] Liu A, Hamel C, Hamilton RI, Ma BL, Smith DL. Acquisition of Cu, Zn, Mn and Fe by mycor-
rhizal maize (Zea mays L.) grown in soil at different P and micronutrient levels. Mycorrhiza
2000;9:331–336.
 3 Interactions among plants, arbuscular mycorrhizal and mycotoxigenic fungi | 69

[50] Druille M, Cabello MN, Omacini M, Golluscio RA. Glyphosate reduces spore viability and root
colonization of arbuscular mycorrhizal fungi. Appl Soil Ecol 2013;64:99–103.
[51] Zaller JG, Heigl F, Ruess L, Grabmaier A. Glyphosate herbicide affects belowground interactions
between earthworms and symbiotic mycorrhizal fungi in a model ecosystem. Scientific Reports
2014;4.
[52] Karpouzas DG, Papadopoulou E, Ipsilantis I, Friedel I, Petric I, Udikovic-Kolic N, Djuric S, Kan-
deler E, Menkissoglu-Spiroudi U, Martin-Laurent F. Effects of nicosulfuron on the abundance
and diversity of arbuscular mycorrhizal fungi used as indicators of pesticide soil microbial
toxicity. Ecol Indicators 2014;39:44–53.
[53] Zocco D, Fontaine J, Lozanova E, Renard L, Bivort C, Durand R, Grandmougin-Ferjani A, Declerck
S. Effects of two sterol biosynthesis inhibitor fungicides (fenpropimorph and fenhexamid) on
the development of an arbuscular mycorrhizal fungus. Mycol Res 2008;112:592–601.
[54] Zocco D, Van Aarle IM, Oger E, Lanfranco L, Declerck S. Fenpropimorph and fenhexamid impact
phosphorus translocation by arbuscular mycorrhizal fungi. Mycorrhiza 2011;21:363–374.
[55] Schweiger PF, Jakobsen I. Dose-response relationships between four pesticides and phospho-
rus uptake by hyphae of arbuscular mycorrhizas. Soil Biol Biochem 1998;30:1415–1422.
[56] Lugtenberg BJJ, Malfanova N, Kamilova F, Berg G. Microbial control of plant root diseases. In:
de Bruijn FJ (ed). Molecular Microbial Ecology of the Rhizosphere. Hoboken, New Jersey, USA:
Wiley Blackwell; 2013. p. 575–586.
[57] Jung SC, Martínez-Medina A, López-Ráez JA, Pozo MJ. Mycorrhiza-induced resistance and prim-
ing of plant defenses. J Chem Ecol 2012;38:651–664.
[58] Pozo MJ, Azcón-Aguilar C. Unraveling mycorrhiza-induced resistance. Curr Opin Plant Biol
2007;10:393–398.
[59] López-Ráez JA, Bouwmeester H, Pozo MJ. Communication in the rhizosphere, a target for pest
management In: Lichtfouse E (ed). Sustainable Agriculture Reviews vol. 8 Agroecology and
Strategies for Climate Change. Netherlands: Springer; 2012. p. 109–133.
[60] Kloppholz S, Kuhn H, Requena N. A secreted fungal effector of Glomus intraradices promotes
symbiotic biotrophy. Curr Biol 2011;21:1204–1209.
[61] López-Ráez JA, Pozo MJ, García-Garrido JM. Strigolactones: a cry for help in the rhizosphere.
Botany-Botanique 2011;89:513–522.
[62] López-Ráez JA, Charnikhova T, Fernández I, Bouwmeester H, Pozo MJ. Arbuscular mycorrhizal
symbiosis decreases strigolactone production in tomato. J Plant Physiol 2011;168:294–297.
[63] Pozo MJ, Verhage A, García-Andrade J, García JM, Azcón-Aguilar C. Priming plant defence
against pathogens by arbuscular mycorrhizal fungi. In: Azcón-Aguilar C, Barea JM, Gianinazzi
S, Gianinazzi-Pearson V (eds). Mycorrhizas Functional Processes and Ecological Impact. Berlin,
Heidelberg: Springer-Verlag; 2009. p. 123–135.
[64] Pozo MJ, Jung SC, López-Ráez JA, Azcón-Aguilar C. Impact of arbuscular mycorrhizal symbiosis
on plant response to biotec stress: The role of plant defence mechanisms. In: Koltai H, Kapul-
nik Y (eds). Arbuscular Mycorrhizas: Physiology and Function. Netherlands: Springer; 2010.
p. 193–207.
[65] Ismail Y, McCormick S, Hijri M. A fungal symbiont of plant-roots modulates mycotoxin
gene expression in the pathogen Fusarium sambucinum. PloS One 2011;6(3):E17990.
doi:10.1371/[Link].0017990.
[66] Wharton PS, Tumbalam P, Kirk WW. First report of potato tuber sprout rot caused by Fusarium
sambucinum in Michigan. Plant Dis 2006;90:1460.
[67] Desjardins AE, Hohn TM. Mycotoxins in plant pathogenesis. Mol Plant-Microbe Interact
1997;10:147–152.
70 | José-Miguel Barea

[68] McCormick SP, Alexander NJ, Trapp SE, Hohn TM. Disruption of TRI101, the gene encoding tri-
chothecene 3-O-acetyltransferase, from Fusarium sporotrichioides. Appl Environ Microbiol
1999;65:5252–5256.
[69] Garvey GS, McCormick SP, Rayment I. Structural and functional characterization of the TRI101
trichothecene 3-O-acetyltransferase from Fusarium sporotrichioides and Fusarium gramin-
earum - Kinetic insights to combating fusarium head blight. J Biol Chem 2008;283:1660–1669.
[70] Ismail Y, Hijri M. Arbuscular mycorrhisation with Glomus irregulare induces expression of
potato PR homologues genes in response to infection by Fusarium sambucinum. Funct Plant
Biol 2012;39:236–245.
[71] Lynch JP, St Clair SB. Mineral stress: the missing link in understanding how global climate
change will affect plants in real world soils. Field Crops Res 2004;90:101–115.
[72] Pritchard SG. Soil organisms and global climate change. Plant Pathol 2011;60:82–99.
[73] Rodríguez RJ, Redman RS, Henson JM. The role of fungal symbioses in the adaptation of plants
to high stress environments. Mitig Adapt Strat Gl 2004;9:261–272.
[74] Fitter AH, Heinemeyer A, Husband R, Olsen E, Ridgway KP, Staddon PL. Global environmental
change and the biology of arbuscular mycorrhizas: gaps and challenges. Can J Bot-Rev Can Bot
2004;82:1133–1139.
[75] Willis A, Rodrigues BF, Harris PJC. The ecology of arbuscular mycorrhizal fungi. Crit Rev Plant
Sci 2013;32:1–20.
[76] Juroszek P, von Tiedemann A. Climate change and potential future risks through wheat dis-
eases: a review. Eur J Plant Pathol 2013;136:21–33.
[77] Polle A, Luo ZB. Biotic and abiotic interactions in plants: Novel ideas for agriculture and
forestry in a changing environment. Environ Exp Bot 2014;108:1–3.
[78] Selosse MA, Bessis A, Pozo MJ. Microbial priming of plant and animal immunity: symbionts as
developmental signals. Trends Microbiol 2014;22:607–613.
[79] Kivlin SN, Emery SM, Rudgers JA. Fungal symbionts alter plant responses to global change. Am
J Bot 2013;100:1445–1457.
Angel Medina, Alicia Rodriguez, and Naresh Magan
4 Changes in environmental factors driven by
climate change: effects on the ecophysiology of
mycotoxigenic fungi

4.1 Background

4.1.1 Environmental change, fungal adaptation, and mycotoxins

The famous philosopher Jean-Jacques Rousseau wrote, back in 1778, a sentence which
is still current when applied to the knowledge in contemporary ecology: “Everything
is in constant flux on this earth” [1].
Living organisms live in an ever-changing world and are exposed to constant en-
vironmental fluctuations in their surroundings (biotic, e.g. other species; and abiotic,
e.g. temperature, water availability, gas composition, substrate). This requires them
to adapt relatively quickly for effective exploitation of resources and to compete effec-
tively in a particular ecosystem.
Filamentous fungi are a group of eukaryotes with tremendous physiological plas-
ticity which has contributed to their capacity for adaptation and facilitated their active
colonization in a range of extreme environments [2, 3]. They can be competitive in such
environments because of their ability to produce a battery of extracellular hydrolytic
enzymes, secondary metabolites, and volatiles (Fig. 4.1).
A number of Aspergillus and Penicillium species are xerotolerant or xerophilic
and able to colonize intermediate moisture food products (reduced water activity; a w )
which represent environmentally stressed conditions for many other fungi and bac-
teria (Tab. 4.1). This physiological plasticity gives these species an important ecolog-
ical advantage which allows them to successfully colonize a range of different food
matrices.
As a result, many staple crops (cereals, nuts, fruits) can be colonized and infected
by Aspergillus/Penicillium and Fusarium species which can then contaminate the edi-
ble parts with toxic secondary metabolites, the so-called mycotoxins. Although Fusar-
ium species are not xerophiles, they can often colonize crops preharvest and produce
mycotoxins when they are under relative water and temperature stress (0.90–0.93 a w ;
10–15, > 30 °C) for these species.
Mycotoxins have significant toxicological impact on both human and animal
health. This has resulted in strict legislative limits for mycotoxins in many parts of
the world in a wide range of foodstuffs with the strictest limits in the EU [4]. However,
in many African countries where legislation is often applied to export crops only,
consumption of mycotoxin contaminated staple foods poses a significant risk, espe-
72 | Angel Medina, Alicia Rodriguez, and Naresh Magan

Gas
balance
e.g. CO2
Secondary
metabolites
Temp e.g. mycotoxins,
volatiles
sugar-alcohols

aw
Fungi

Biological
interactions

Substrate
pH

Fig. 4.1: Illustration showing the effect of different biotic and abiotic factors on the ecophysiology
of fungi.

cially in rural populations and subgroups such as children and immunocompromised

people.
The most important mycotoxins are aflatoxins (produced by Aspergillus sec-
tion Flavi species), ochratoxin A (OTA) (Aspergillus section Circumdati species, As-
pergillus section Nigri species, Penicillium nordicum, P. verrucosum), fumonisins
(Fusarium verticillioides, F. sporotrichioides), type A trichothecenes, T-2 and HT-2 toxin
(F. langsethiae, F. sporotrichioides), type B trichothecenes (F. graminearum and related
species), and patulin (P. expansum). The European Food Safety Authority (EFSA) is
now examining the relative hazard posed by mycotoxins produced by Alternaria
species across the EU to obtain information of the levels in different food products
and make decisions as to whether limits should also be considered.

4.1.2 Climate change and mycotoxigenic fungi

Agricultural production of staple foodstuffs requires optimized agronomic practices

to provide the yields and amount of raw food commodities required to feed an ever-
increasing global population. Thus, climate change scenarios could have a profound
impact on the production and delivery of sufficient food. Climate change is expected
to have a great effect on our landscape worldwide and the way we interact with it.
Climate change models have projected a marked decrease in summer precipitation
 4 Changes in environmental factors driven by climate change | 73

Tab. 4.1: Food products, their moisture content and equivalent water activity, and the predominant
microbial genera which can colonize and cause spoilage.

Type of product Water content Water activity Common spoilage

(% w/w) (a w ) microorganisms

Fresh meat and fish 0.99 Bacteria, yeasts

Carbonated drinks 0.999–0.977 Bacteria, yeasts
Cream, 25 % fat 0.973 Bacteria
Bread 0.95 Yeasts and molds
Muffins ≈ 0.95 Yeasts and molds
Salami, dry 0.875 Molds
Sausage, snack, fully dry 29–10.6 0.87–0.66 Molds
Aged cheddar 0.85 Yeasts and molds
Jams and jellies 0.80 Yeasts and molds
Plum pudding 0.80 Yeasts and molds
Fruits, dried 0.80–0.72 Xerophilic molds
0.78 Aspergillus flavus
0.77 Aspergillus niger
Wheat ≤ 14.5 ≤ 0.70 GRAS
> 14.5 > 0.70 Xerophilic molds
Maize ≤ 14 ≤ 0.70 GRAS
> 14 > 0.70 Xerophilic molds
Rice ≤ 12–15 ≤ 0.70 GRAS
> 12–15 > 0.70 Xerophilic molds
0.70 Eurotium amstelodami
0.656 Xeromyces bisphorus
Biscuits 0.30 GRAS
Honey 0.552 GRAS
Milk powder 0.20 GRAS
Instant coffee 0.20 GRAS

GRAS: Generally recognized as safe

and increases in CO2 (double or triple existing concentrations) and temperature for
some areas, which would result in concomitant drought stress episodes.
The EU green paper on climate change in Europe has suggested that effects will
be regional and either be detrimental or advantageous depending on geographical
area [5]. Even if some changes in climate may be positive for some northern European
regions, many will be negative, affecting regions already suffering from environmental
or other changes. According to the intergovernmental panel on climate change [6],
the worst consequences may not be felt until 2050, but significant adverse effects are
expected even in the short term from more frequent extreme conditions.
Generally, the atmospheric concentration of CO2 is expected to at least dou-
ble (from 350–400 to 800–1000 ppb). Because of this increase and that of other
greenhouse gases, the global temperature is expected to increase by between +2 and
+5 °C depending on levels of industrial activity. Hence, changes in southern Europe
74 | Angel Medina, Alicia Rodriguez, and Naresh Magan

may equate to an increase of 4–5 °C with important reductions in rainfall and longer
drought periods, resulting in increasing desertification, and a decrease in crop yields
and arable areas. In areas of western and Atlantic Europe, changes of 2.5–3.5 °C with
dryer and hotter summers are envisaged. In Central Europe, an increase of 3–4 °C,
higher rainfall and floods are forecast, although longer growing periods may benefit
crop yields. Northern Europe would expect a mean temperature increase of 3–4.5 °C,
with a significant increase in precipitation of 30–40 %. This may lead to increases in
crop yields and perhaps new crop cultivation patterns [5, 7]. A recent EFSA report [8]
suggests that because of early ripening in cereals, especially wheat and maize, expo-
sure to plant diseases and possibly increased contamination with aflatoxins can be
expected in the next 25 years in most of southern and central Europe. Similar effects
have been described in other areas of the world, especially parts of Asia and Central
and South America, which are important producers of staple crops [6].
Such environmental changes are slowly but steadily shaping the relationship be-
tween plant growth and the associated fungal diseases and pest populations. Recent
predictions suggest that on a global scale, pests and diseases are moving to the poles
at the rate of 3–5 km/year and the diversity of pest populations will also significantly
change and have profound economic impact on staple food production systems [9, 10].
While these studies did not focus on mycotoxigenic fungal pathogens, this suggests a
significant potential impact on mycotoxin contamination of staple foods/crops. In-
creases in pest reproduction rates would increase damage to ripening crops (during
anthesis in wheat, and silking in maize) and facilitate more infection by mycotoxigenic
fungi and contamination with mycotoxins.
The key environmental factors identified in these future changes therefore in-
clude: fluctuating humidity, including changes in rainfall patterns and extended pe-
riods of drought stress, increases and extreme temperature fluxes (global warming
+3–5 °C), and an increase in CO2 (two or three times present levels) [8, 11, 12].
This strong evidence showing a marked change in the environment in which sta-
ple crops will be grown in the next 10–25 years has increased the concern regarding
the impact that predicted climate change scenarios may have on agriculture, myco-
toxigenic fungal infection, and contamination with mycotoxins [11, 13–17].
Unfortunately, the current predictions and hypotheses about the real effect of cli-
mate change on mycotoxigenic fungi are based on historical or current climatic condi-
tion datasets which mostly consider interactions between water availability and tem-
perature. Presently there are only very few studies examining the effect of 3-way inter-
actions between the environmental factors identified (temperature, water availability,
and CO2 ) and what changes in terms of the ecophysiology of mycotoxigenic fungi and
mycotoxin accumulation might have [16–18].
This chapter will consider the effects of the forecasted climate change factors of
(1) a w × temperature interactions and (2) three-way a w × temperature × CO2 interac-
tions, on the ecophysiology of the main mycotoxigenic species. Potential future re-
search areas which will need to be addressed will also be discussed.
 4 Changes in environmental factors driven by climate change | 75

4.2 Ecophysiological modifications on mycotoxigenic fungi under

climate change conditions

4.2.1 Two-way a w × temperature interactions

As discussed above, two of the key environmental factors identified in these future
changes are fluctuating humidity and temperature. With regard to humidity, these
fluctuations will vary from extreme rainfall to long periods of drought that will reduce
the available water for living organisms. In soil, survival of water stress is predom-
inantly determined by the total water potential and matric and solute components,
whilst in food matrices the solute component and hence water activity (a w ) are more
important [2]. On the other hand, as part of the forecasted environmental change, in-
creases and extreme temperature fluxes have been predicted.
It is now accepted that these factors and their interactions are able to modulate
germination, growth, sporulation, expression of genes involved in mycotoxins, and
phenotypic mycotoxin production [19, 20] by mycotoxigenic fungi. Extreme drought
episodes, desertification and fluctuations in wet/dry cycles will have an impact on
their life cycles [21].
Magan et al. [11] reviewed the available ecological data on optimum and marginal
interacting conditions of a w × temperature for growth and mycotoxin production by
several mycotoxigenic species. Effects on the growth of Alternaria alternata, Fusarium
proliferatum, F. verticillioides, F. culmorum, F. graminearum, Aspergillus westerdijkiae,
A. carbonarius, A. flavus, Penicillium verrucosum, P. expansum and production of al-
ternariol, alternariol monomethyl ether, altenuene, fumonisins, trichothecenes, OTA,
aflatoxin B1 and patulin were considered when temperature was increased by either +3
or +5 °C at different water availabilities. These datasets have been combined with the
available information from other publications [19, 22–26] and are shown in Tab. 4.2.
Only a w × temperature interactions are considered. It is shown, however, that
fungi would normally grow slower and in most cases produce similar or smaller
amounts of mycotoxins under temperature and water stress. For some species how-
ever, such as Aspergillus flavus, which is able to grow and produce aflatoxin B1 under
high temperatures and to colonize maize efficiently under drought conditions, the
forecasted conditions could become a problem particularly in the Mediterranean and
other temperate regions [27].
Some examples of how extremely dry and warm conditions have affected the
prevalence of mycotoxigenic fungi and mycotoxin contamination of staple food have
been described. In 2003 and 2004 in northern Italy, and subsequently in the 2012
summer season, drought and extreme elevated temperatures (> 35 °C) resulted in a
switch from Fusarium verticillioides and contamination with fumonisins to significant
contamination of maize grain with A. flavus and aflatoxins, with later entry of aflatoxin
M1 into milk via the animal feed chain [27]. A. flavus has a wide range of temperature
tolerance (19–35 °C) with about 28 °C being ideal for growth and 28–30 °C for aflatoxin
Tab. 4.2: Changes in growth and toxin production by Alternaria spp., Fusarium spp., Aspergillus spp., and Penicillium spp. as a result of increase in tempera-
ture of 3 or 5 °C under different water stress conditions.

Growth Toxins
aw μmax range / Temp μ+3 μ+5 aw τmax range / Temp τ+3 τ+5
Alternaria alternata 0.95 2–1 / 25 2–1 1–0.5 Altenuene 0.95 100–40 / 25 40–20 20–5
0.90 0.1–0.5 / 25 0.5–0.1 NG 0.90 20–5 / 25 5–NP NP
Alternariol 0.95 500–100 / 25 40–20 20–5
0.90 20–5 / 25 NP NP
Alternariol 0.95 400–100 / 25 100–10 NP
monomethyl ether 0.90 100–10 / 25 NP NP
Alternaria tenuissima 0.98 13.5–14 / 30 8–9.5 7.5–9 Altertoxin II 0.98 50–150 / 30 100–250 125–250
0.95 5–6 / 30 4.5–5.5 4.5–5.5 0.95 600–2100 / 30 500–1000 400–1300
Fusarium proliferatum 0.95 4–3 / 28 3–2 2–1 Fumonisin 0.95 > 1000 / 20 1000–100 100–50
0.90 0.5–0.1 / 28 NG NG 0.93a 50–10 / 15 50–10 50–10
Fusarium verticil- 0.95 4–3 / 25 4–3 4–3 Fumonisin 0.95 10 000–1000 / 20 10 000–1000 1000–100
76 | Angel Medina, Alicia Rodriguez, and Naresh Magan

lioides
0.90 0.5–0.1 / 25 0.5–0.1 NG 0.93a 10 / 15 50–10 50–10
Fusarium culmorum 0.95 3–1 / 20 3–1 3–1 DON 0.95 1–0.25 / 20 0.25–0.1 0.1–0.01
0.90 1–0.1 / 20 1–0.1 1–0.1 0.93a 0.25–0.01 / 20 NP NP
Fusarium gramin- 0.95 >4 / 20 4–2 2–1 DON 0.95 1–0.1 / 20 1–0.1 0.1–0.01
earum
0.90 1–0.1 / 20 1–0.1 1–0.1 0.93a NP / NP NP
Fusarium langsethiae 0.98 4.6–5.1 / 25 4.6–4.1 3.6–3.1 T-2 + HT-2 0.98 10–11 / 25 13–14 14–15
0.95 2.6–2.1 / 25 1.1–1.6 1.6–1.1 0.95 0–1 / 25 0–1 0–1
Tab. 4.2 (continued)

Growth Toxins
aw μmax range / Temp μ+3 μ+5 aw τmax range / Temp τ+3 τ+5
Aspergillus westerdijkiae 0.95 5–4.5 / 30 4.45–3.95 4.25–3.75 Ochratoxin A 0.95 1065.7–1014.9 / 30 719.4–685.1 488.5–465.3
0.90 1.85–1.35 / 30 1.85–1.35 1.80–1.30 0.90 54.1–51.6 / 30 51.6–49.2 49.9–47.6
Aspergillus carbonarius 0.95 >6 / 30 >6 6–5 Ochratoxin A 0.95 2000–1500 / 20 1000–500 500–NP
0.90 4–3 / 30 4–3 4–3 0.90 1000–500 / 20 500–NP 500–NP
Aspergillus flavus 0.95 6.9 / 35 5.6 5.0 Aflatoxin B1 0.95 3082–2278 / 37 102–138 6.1–NP
0.90 2.9 / 37 1.4 0.7 0.90 448.5–331.5 / 37 1–NP NP
Penicillium verrucosum 0.97 2.2–2.4 / 25 1.8–1.9 0.9–1 Ochratoxin A 0.97 60–50/20 / 75 70– > 80
0.95 3–4 / 25 4–3 3–2 0.95 > 50 / 20 > 50 50–25
0.90 2.5–1 / 25 2–1 2–0.5 0.90 50–30 / 20 50–30 50–30 (5–3a )
Penicillium nordicum 0.97 1.4–1.5 / 20 1.5 2–1 Ochratoxin A 0.97 7–6 / 20 6–5 4–3
0.94 1.8–2.0 / 20 1.8–1.7 1.4–1.7 0.94 7–6 / 20 7–6 7–6
0.90 1.2–1.3 / 20 1.2–1.3 1.2–1.4 0.90 8–7 / 20 9–8 9–8
Penicillium expansum 0.98 9.1 / 20 Patulin 0.98 3.5–0.55 / 20 NS NS
0.95 6.9–5.5a / 25 6.9–5.5 6.9–5.5 0.95 NS / NS NS
0.90 2.9–1.6a / 25 2.9–1.6 2.9–1.6 0.90 NS / NS NS

μmax : Maximum growth rate (mm day−1 ); μ+3 : Growth rate increasing 3 °C; μ+5 Growth rate increasing 5 °C;
τmax : Maximum toxin production (μg ml−1 ); τ+3 : Predicted toxin increase 3 °C; τ+5 : Predicted toxin increase 5 °C;
NG: no growth; NP: no toxin production; NS: not studied.

For Aspergillus and Penicillium species:

τmax : Maximum toxin production (ng g−1 ); τ+3, predicted toxin production with 3 °C increase; τ+5, predicted toxin production with 5 °C increase.

a Minimum water availability for toxin production.

4 Changes in environmental factors driven by climate change | 77
78 | Angel Medina, Alicia Rodriguez, and Naresh Magan

production [19]. It has been shown that sporulation from sclerotia on maize stalks is
maximized at 20–25 °C in a range of wet to dry conditions (0.995–0.90 a w ). Reduced
sporulation occurred under drier conditions of ≤ 0.90 a w [28]. Some strains of A. flavus
can even grow at 0.73 a w (in host tissue) and produce aflatoxins at 0.85 a w , while in
contrast, F. verticillioides growth is very marginal at 0.90 a w and fumonisins are pro-
duced only at > 0.93 a w [19]. A. flavus, a more xerotolerant mycotoxigenic species than
F. verticillioides, was able to actively colonize ripening maize by outcompeting the
more common non-xerophilic Fusarium species. Isolated strains were able to colonize
ripening maize rapidly and produce both aflatoxins and cyclopiazonic acid [27]. Thus,
because of the very dry and warm conditions in those years, A. flavus became a signif-
icant problem resulting in significant economic losses in the valuable and important
cheese industry of the region. More recently, a Serbian maize survey in 2009–2011
identified no aflatoxin contamination. However, prolonged hot and dry weather in
2012 resulted in 69 % of samples being contaminated with aflatoxins [29]. Similarly, in
Hungary, it has also been shown that an increase in aflatoxins may be due to climate
change conditions [30]. However, there are only a few more concrete examples of such
incidences where climate change factors have been implicated.
Magan et al. [11] suggested that drought conditions favored by climate change
may result in xerophilic fungi such as Wallemia sebi, Xeromyces bisporus, and Chryso-
sporium species becoming more important as colonizers of food commodities. These
species are able to grow under very dry conditions (0.65–0.75 a w ) where there is much
less competition from the majority of mesophilic fungi [2, 31]. This potential change
in the food ecosystem may pose a risk, since W. sebi can produce metabolites such as
walleminol and walleminone which can be toxic to animals and humans [32]. Recent
research by Leong et al. [33] suggests that there are competitive interactions between
these xerophilic fungi in extreme dry conditions and that secondary metabolites may
play a role.
Another group of species which could benefit from these warmer and drier condi-
tions could be species from the Aspergillus section Nigri. Their optimal growth condi-
tions have been shown to be between 0.95–0.99 a w and 30–37 °C and optimal OTA pro-
duction between 0.95–0.99 a w and 15–20 °C [33, 35–38]. Among these species A. car-
bonarius has been identified as being able to produce high OTA amounts in a wide
range of fruits and dried fruits. However, other species from the A. niger aggregate
have also been reported to be OTA producers. Among these, for example, A. tubingen-
sis, was described as an OTA producer by Medina et al. [39], although it has a different
growth and toxin production pattern. In strains isolated from Morocco, the optimal
temperature and a w conditions for OTA production was in the range of 25–30 °C and
0.95–0.99 a w for A. carbonarius and 30–37 °C and 0.90–0.95 a w for A. niger and A. tub-
ingensis [40]. Interestingly, Chiotta et al. [41] studied the effect of interactions between
A. tubingensis and A. carbonarius strains and found that OTA production by the latter
species was mainly dependent on temperature. At 35 °C, A. tubingensis reduced OTA
production by A. carbonarius, an effect not observed at 20 °C. Recently, García-Cela
 4 Changes in environmental factors driven by climate change | 79

et al. [42] concluded that climate change prediction points to drier and hotter climatic
scenarios where A. tubingensis and A. niger could be even more prevalent than A. car-
bonarius, since they are better adapted to extreme high temperatures and drier con-
ditions. Gil-Serna et al. [43] also studied growth and OTA production by A. steynii and
A. westerdijkiae in a green-coffee based medium under different environmental con-
ditions. They demonstrated that the optimal conditions of both species to grow and
produce OTA were at 28–32 °C and a w levels > 0.95 a w . A. steynii was able to grow and
produce OTA over a wider set of conditions than A. westerdijkiae. Thus, climate change
might result in a shift of the main source of OTA in several products since drier and
warmer conditions will benefit the colonization and OTA production by species from
the Aspergillus section Nigri species.
There might also be changes in mycotoxin prevalence among the same species.
As an example, Alternaria alternata is able to produce a range of secondary metabo-
lites. Among others, it produces mycotoxins such as alternariol (AOH) and alternariol
monomethyl ether (AME). While maximum AOH production is reached at 21 °C and
0.95 a w , AME production was maximized at the same a w levels but at much warmer
conditions of 35 °C. Thus, increases in temperature may equate to shifts from AOH
to AME under the forecasted conditions [44]. Schmidt-Heydt et al. [45] also demon-
strated that temperature affects mycotoxin production pattern of A. parasiticus; with
an increasing temperature (> 30 °C), there is a shift from aflatoxin G1 to aflatoxin B1 .
However, these studies exclude interaction with CO2 which is necessary to examine
the impact of predicted climate change scenarios in more detail.

4.2.2 Three-way a w × temperature × CO2 interactions

The addition of CO2 as a potential factor influencing mycotoxigenic fungi seems to be

more than plausible. Doubling its current concentration around 2050 and tripling it
around 2100, CO2 will have a significant effect on all living species around the globe
and plants and fungal species will be no exception. Considering the effect on plants,
photosynthesis, leaf area, plant height, total biomass and crop yield, sugar and starch
content, water-use efficiency, growth, and yield are generally increased in the pres-
ence of higher levels of CO2 [46].
In contrast, fungi, including mycotoxigenic fungi, are able to withstand quite high
concentrations of CO2 [47]. Thus, tolerance of climate change factors where perhaps a
tripling of the existing CO2 is predicted to occur may not be problematic for the growth
of mycotoxigenic fungi.
The available evidence also shows that the predicted climate change conditions
are expected to alter the potential risk of plant diseases [48, 49] and elicit changes in
host and pathogen interactions, such as an increase or decrease in disease symptoms,
infection or pest fecundity [46] which will affect crop yield and quality [50, 51]. Carbon
dioxide may also influence plant resistance [52].
80 | Angel Medina, Alicia Rodriguez, and Naresh Magan

Although there are currently serious concerns regarding food security and food
safety accompanying crop productivity and mycotoxin contamination in the context
of global climate change, our understanding of how elevated temperature × water
stress × elevated CO2 interactions are able to modulate crop plants, mycotoxigenic
fungi, and the plant/fungus interaction is still very limited.
In the last two decades, research on the impact of CO2 focused predominantly on
its use as part of a modified atmosphere storage system to control growth and dam-
age to commodities during storage. With regard to mycotoxigenic fungi, it has been
shown that they are very tolerant of between 25–75 % CO2 , regardless of a w or temper-
ature [47]. The approach has been to reduce the O2 concentration to < 2 % and increase
CO2 to > 50–60 %. However, many fungi are microaerophilic and will still be able to
grow slowly under such conditions in storage systems and packaging [53, 54]. Wil-
son and Jay [55] tested a high CO2 treatment (61.7 % CO2 balanced with O2 and N2 )
on moist maize and found that A. flavus growth was visible after 4 weeks at 27 °C.
Contamination with aflatoxins at elevated CO2 was lower than that in air. Although no
mycotoxin analyses were carried out, Magan and Lacey [56] examined the interactions
between reduced O2 concentration (21–0.14 %) or elevated CO2 (5–15 %) balanced with
nitrogen and interactions with temperature (14, 23 °C) and water stress (0.98–0.85 a w )
for a range of 6 phyllosphere cereal fungi and 10 spoilage Aspergillus and Penicillium
species on wheat-based media. For example, the latent periods prior to growth (lag
times) for Alternaria alternata and Fusarium culmorum were significantly increased
by > 5 % CO2 , regardless of a w or temperature. Growth of A. alternata at 23 °C was in-
hibited by > 5 % CO2 at 0.98 and 0.95 a w . On the other hand, at 0.90 a w growth was
stimulated by 5 % and 10 % CO2 . This also occurred at 14 °C and 0.95 a w . In contrast,
growth of F. culmorum was inhibited significantly by > 5 % CO2 at 0.98 and 0.95 a w at
both temperatures, whilst appearing to be unaffected at 0.90 a w [56, 57].
The effects of elevated CO2 on A. ochraceus (= A. westerdijkiae) and P. verrucosum
growth and OTA production have also been determined [58, 59]. Studies by Pateraki
et al. [53] suggested that up to 50 % CO2 had only a slight impact of OTA production
by A. carbonarius over a range of a w conditions, with this being a more important fac-
tor than CO2 . Samapundo et al. [60] found that fumonisin B1 production by Fusarium
section Liseola species (F. verticillioides, F. proliferatum) was inhibited by 30 % CO2 at
0.984 a w .
In both in vitro and in situ studies, Giorni et al. [54] demonstrated that CO2 ×
a w interactions significantly decreased the ability of A. flavus to grow and colonize
maize grain. The use of modified atmospheres at 25 % and 50 % CO2 resulted in about
30–35 % inhibition of growth (CFU g−1 grain). Exposure to 75 % CO2 resulted in > 50 %
inhibition of growth and aflatoxin B1 production, regardless of the a w level. Other
studies of modified atmospheres with different CO2 levels balanced with O2 and N2
showed that A. flavus grew on wheat and rye bread with up to 75 % CO2 [61]. Exposure
to 70 % CO2 at 0.80 a w prevented spoilage of bakery products; however, when a w
was 0.85 or 0.90 spoilage was delayed [62]. These previous studies demonstrate that
 4 Changes in environmental factors driven by climate change | 81

very high CO2 concentrations are needed to control growth and associated mycotoxin
production by the main mycotoxigenic fungi.
Medina et al. [16] recently examined the effect of current environmental condi-
tions and compared them with forecasted conditions. Temperatures were changed
from 34 to 37 °C, drought stress was imposed, and CO2 was increased from 350 to 650
and 1000 ppm. The effects on growth of A. flavus and aflatoxin B1 production were
examined. This was the first time a combination of expected climate change factors
were used to establish the potential effects of these scenarios on the ecophysiology
of mycotoxigenic fungi. The results showed that for growth of A. flavus there was rel-
atively little effect of these interacting conditions (Fig. 4.2 (a)). In contrast, the three-
way interacting conditions had a more profound effect on aflatoxin B1 production. This
clearly demonstrates a stimulation of aflatoxin B1 production under slightly elevated
CO2 conditions, especially under drought stress at 37 °C and 650 and 1000 ppm CO2
exposure (Fig. 4.2 (b)). It seems that the interactions between all three factors are crit-
Growth rate (mm diameter/day)

14
12
10
8
6
4
2
0
350 650 1000 350 650 1000 350 650 1000
0.97 0.95 0.92
(a)

2500

2000
ng AFB1 / g of agar

1500

1000

500

0
350 650 1000 350 650 1000 350 650 1000
0.97 0.95 0.92
(b)

Fig. 4.2: Effect of water activity (0.97, 0.95, 0.92) × elevated CO2 levels (350, 650, 1000 ppm) on
(a) relative growth rates; and (b) aflatoxin B1 production, of an A. flavus strain on a conducive YES
medium at 37 °C. Bars indicate standard errors. Adapted from Medina et al. [16].
82 | Angel Medina, Alicia Rodriguez, and Naresh Magan

ical in the impact that slightly elevated CO2 has. This is clear from the results obtained
at 0.92 and 0.95 a w × 37 °C and 650 or 1000 ppm CO2 , where a statistically significant
increase in aflatoxin B1 was observed.
Vaughan et al. [18] recently investigated the impact of elevated CO2 on the inter-
action between maize and F. verticillioides. They found that elevated CO2 of approx.
800 μmol CO2 mol−1 air (≈ double current CO2 ) increased maize susceptibility to F. ver-
ticillioides colonization. Interestingly, fumonisin production was not affected by these
interactions. They also found that fumonisin production was not proportional to the
increase in the biomass of F. verticillioides, and the amount of fumonisin produced per
unit pathogen was reduced in elevated CO2 . Their study also showed that physiologi-
cal impacts on maize agronomy were evident when grown under the climate change
treatments used, including 28 °C day/25 °C night temperature cycles, 500 μmol m−2 s−1
photosynthetic photo flux density 12 h photoperiod and 400 μmol CO2 mol−1 air (≈ cur-
rent CO2 ) and the other at 800 μmol CO2 mol−1 air (≈ double current CO2 ). These phys-
iological effects on the maize plant could further impact on infection and contamina-
tion with mycotoxins, especially during silking.

4.3 Climate change impact on mycotoxin gene cluster expression

and its relationship to growth and toxin production.
Integration of the correlation of ecophysiological conditions with expression of spe-
cific mycotoxin biosynthesis genes and phenotypic production of toxins could help
improve knowledge and understanding of how climate change conditions influence
the growth and regulation of mycotoxins. The clusters of genes involved in the produc-
tion of key toxic secondary metabolites including aflatoxins, OTA, trichothecenes such
as deoxynivalenol, and fumonisins have been largely identified [63, 64]. The genes in-
volved in mycotoxin production are often clustered together and key marker genes in
the pathways have been identified. Most studies have focused on research into how
key abiotic factors, such as a w and temperature, affect expression of the genes in-
volved in mycotoxin biosynthesis. Practically none have examined the effects of CO2 .
The aflatoxin cluster of genes consists of 25 genes, including the key regulatory
genes (aflR and aflS) and a series of up and downstream structural genes. It has been
shown that both a w and temperature modifications affect the expression of these
clusters of genes, relative growth rate, and aflatoxin production in both A. flavus and
A. parasiticus [45, 65]. It has been suggested that that there is a relationship between
aflatoxin biosynthetic genes (aflS/aflR ratio and aflD genes) and aflatoxin B1 produc-
tion when exposed to elevated temperature and drought stress conditions [66]. How-
ever, the effect of CO2 was not included in these studies. More recent detailed studies
using a mycotoxin microarray [67] have been useful in elucidating the relationship be-
tween both key regulatory genes and the structural genes and interacting conditions
of a w × temperature [66]. As the a w increased, the expression of aflD was reduced; the
 4 Changes in environmental factors driven by climate change | 83

regulatory genes aflR and aflS were less sensitive to a w having a similar sensitivity. As
the temperature was increased, the expression of aflD and aflR was reduced and that
of aflS increased. A slight change in temperature caused a large change in expression
of aflD and aflR. Recently, Medina et al. [16] studied the effect of temperature × a w ×
CO2 on the relative expression of the mycotoxin biosynthetic genes, specifically, on
structural aflD and the regulatory aflR genes involved in aflatoxin B1 production.
There was a stimulation of aflD gene expression when temperature increased from
34 to 37 °C and at 650 and 1000 ppm CO2 at both 0.97 and 0.95 a w . For the regulatory
gene aflR expression, there was an increase at either 650 or 1000 ppm CO2 exposure,
especially at 0.95 and 0.92 a w and at 37 °C. In addition, it was demonstrated that these
three-way interactions of climate change factors stimulated the relative expression of
genes involved in the biosynthesis of aflatoxin production, resulting in an increase in
phenotypic aflatoxin B1 being produced.
The fumonisin cluster of genes for F. verticillioides has 17 genes, among them the
FUM1 and FUM21 genes are considered important, while F. sporotrichioides and F. oxy-
sporum have 18 [63]. Medina et al. [68] integrated toxin gene expression, growth and
fumonisin B1 and B2 by a strain of F. verticillioides under different a w × temperature
combinations. This study showed that activation of the expression of nine biosyn-
thetic cluster genes (FUM1, FUM7, FUM10, FUM11, FUM12, FUM13, FUM14, FUM16,
and FUM19) was related to growth and phenotypic FB1 and FB2 production. Thus, for
example, FUM11 and FUM13 gene expression was stimulated when the temperature
was increased from 20 to 25 °C and at 0.93 a w (Fig. 4.3). For FUM1 gene expression,

Fum3
Fum12
Fum14
Fum10
Fum1
Fum7
Fum8
Fum11
Fum13
Fum16
Fum18
Fum17
Fum6
Fum15
Fum19
0.95 20°C

0.98 30°C

0.95 25°C

0.93 25°C

0.995 25°C

0.995 20°C

0.995 30°C

0.95 35°C

0.98 20°C

0.93 30°C

0.98 35°C

0.95 30°C

0.995 35°C

0.98 25°C

0.93 20°C

Fig. 4.3: Heat map: relative expression of 15 genes from the fumonisins gene cluster in relation
to a w × temperature conditions. Data obtained using a mycotoxin microarray [67]. Adapted from
Medina et al. [68].
84 | Angel Medina, Alicia Rodriguez, and Naresh Magan

there was an increase at 0.95 a w and at 20 °C. Lazzaro et al. [69] also studied the effect
of temperature and a w on two fumonisin biosynthetic genes (FUM1 and FUM21) and
fumonisin production by F. verticilloides. It was shown that temperature only signifi-
cantly affected FUM21 expression, with the optimum at 25 °C, while a w did not have a
significant effect.
Although some of the genes involved in the trichothecene pathway such as Tri7
and Tri13 [70], and Tri12 [71] have been used as targets for developing PCR assays for
characterization of chemotypes of different Fusarium species, the Tri5 gene has been
used to study its expression in relation to deoxynivalenol production by mycotoxigenic
Fusarium species under different temperatures and a w conditions. Marin et al. [72] in-
vestigated the effect of a w and temperature on Tri5 gene expression by F. graminearum.
They found that the expression of the Tri5 gene was constant in all conditions tested,
although some induction was observed between 20 and 30 °C. Schmidt-Heydt et al. [73]
used a microarray to check the expression of six genes (Tri4, Tri5, Tri6, Tri10, Tri12,
and Tri13) involved in trichothecene biosynthesis to model the relationship between
environmental factors, transcriptional genes, and deoxynivalenol mycotoxin produc-
tion by strains of F. graminearum and F. culmorum. This study showed that there were
different patterns of gene expression depending on abiotic conditions and species.
The expression data for the strain of F. culmorum were relatively much higher than for
the F. graminearum strain. It was observed that at warmer conditions (25 °C) and high
a w levels, but also at low a w , the biosynthetic genes were more expressed. Therefore,
these species could be considered well-adapted in predicted climate change scenarios
resulting in a potential high risk source of trichothecenes contamination.
Regarding the OTA biosynthesis pathway, OTA producing Penicillia have been
found to have at least 4 genes involved in OTA production with the otapks and otanps
genes key biosynthetic pathway genes [74]. Although both key genes have been used
for expression studies, these focused mainly on evaluating the effect of preservatives
or ionic solutes such as NaCl on relative gene expression changes [25, 75, 76]. Some
studies showed that the highest otapks gene expression in P. nordicum was at 15 and
25 °C [77], and when the a w was 0.98 in P. verrucosum. The PKS and P450 related genes
have recently been found to be important markers for A. carbonarius and A. westerdi-
jkiae in the biosynthetic pathway [78–80]. Furthermore, it has been shown that VeA
and LaeA transcriptional factors regulate OTA biosynthesis in A. carbonarius [81]. Un-
fortunately no investigations have been performed to analyze changes in expression
of the former genes under different environmental conditions.
The genetic basis of the biosynthetic pathway of patulin in P. expansum has been
recently characterised [82]. It consists of 15 genes with the patK and patN genes being
necessary for patulin production [83]. So far no studies have been carried out to eval-
uate the influence of environmental factors and/or climate change scenarios on the
expression of genes involved in patulin production.
Although a number of relevant investigations have examined the effect of environ-
mental factors (a w , temperature) on biosynthetic genes, it is of paramount importance
 4 Changes in environmental factors driven by climate change | 85

to continue research on the influence of biotic and abiotic factors on different genes
which have not been studied previously and which may provide better insights into the
impact of slightly elevated CO2 on the physiology of the plant and the interface with
infection/colonization by different mycotoxigenic fungi. Quantification of key biosyn-
thetic toxin genes under different climate change scenarios in the host/pathogen in-
terface could be a valuable tool for gaining knowledge of the ecophysiological basis for
mycotoxin biosynthesis in relation to climate change factors and also facilitate better
control strategies to avoid mycotoxin contamination of staple food commodities.

4.4 Conclusions

Because of their ability to adapt to change, fungal species, especially mycotoxigenic

ones, may become a primary concern in the coming 20–25 years. They exert an as
yet incompletely understood mechanism of metabolism with a high degree of plastic-
ity which allows them to shape the metabolic responses to interacting environmen-
tal factors. Thus, precise forecasting with regard to mycotoxigenic fungal populations
and mycotoxin contamination and prevalence in the coming years remains an area
for research. This chapter points out that interactions between CO2 , temperature, and
a w may have differential effects which are related to both plant physiology and fun-
gal pathogenic species involved. While for some fungal species growth or mycotoxin
production remains similar under the forecasted conditions, for others environmental
changes may have significant effects, e.g. increasing toxin production or leading to a
switch in the major mycotoxin produced or the ratio of different mycotoxins. Perhaps
the addition of the new findings with regard to toxin production under elevated CO2
and temperature conditions discussed in this chapter would reshape the outcome of a
recent report published by EFSA with regard to relative risk of contamination with afla-
toxin B1 in maize, rice, and wheat [8]. Nonetheless, much more data is required to en-
able a better understanding of fungal and plant ecophysiology and the pathogen/host
interface and to improve the potential for making more accurate and relevant global
predictions.
Furthermore, toxin production/mycotoxin biosynthetic gene expression are not
related to growth per se, so more research is needed to establish the potential effect
of these factors and to understand how gene expression is related to phenotypic toxin
production. Considering all the information, several questions remain unanswered
and research efforts are needed to improve the current understanding. Are the new
climate change factors going to change toxin production patterns? Will other myco-
toxins now considered secondary become more abundant and thus more important
in the future? Are the current control/mitigation strategies going to be effective in the
future? Will the agricultural practices used currently in order to minimize toxin con-
tamination be suitable when marked environmental changes become standard? Are
mycotoxigenic fungal populations going to shift their location in the coming years?
86 | Angel Medina, Alicia Rodriguez, and Naresh Magan

More research is urgently required to address these key questions and allow effective
prediction of the relative level of risk of different mycotoxins in economically impor-
tant staple food crops.

Dedication

The authors wish to dedicate this chapter to the memory of Dr. Sejakhosi Alexis Mo-
hale (University of Lesotho), who completed his PhD at Cranfield in 2013 on “Biolog-
ical control of aflatoxins using atoxigenic strains of A. flavus”, and who sadly passed
away in August 2014.

References

[1] Rousseau JJ. Meditations (Reveries) of the solitary walker. London, UK: Penguin Books; 1995.
[2] Magan N. Fungi in extreme environments. In: Kubicek CP, Druzhinina IS, eds. Environmental
and Microbial Relationships, 2nd ed. Berlin, Germany: Springer Verlag; 2007. p. 85–103.
[3] Williams JP, Hallsworth JE. Limits of life in hostile environments: no barriers to biosphere func-
tion? Environ Microbiol 2009;11:3292–3308.
[4] European Commission. Commission regulation (EC) 1881/2006 of 19 December 2006 setting
maximum levels for certain contaminants in foodstuffs. OJEU 2006;L364:5–24.
[5] European Commission. Adapting to climate change in Europe–options for EU action. Green pa-
per from the Commission to the Council, the European Parliament, the European Economic and
Social Committee of the Regions. COM (2007) 354, Brussels, Belgium: European Commission;
2007. (Accessed May 5, 2014, at [Link]
52007DC0354)
[6] IPCC. Climate change 2007: Synthesis report. Intergovernmental panel on climate change.
Geneva, Switzerland; 2007. (Accessed May 5, 2014, at [Link]
data/publications_ipcc_fourth_assessment_report_synthesis_report.htm)
[7] Solomon S, Alley RB, Bertsen T et al. Technical summary. In: Solomon S, Qin D, Manning M et
al, eds. Climate Change 2007: The physical science basis – Contribution of Working Group1 to
the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge,
UK: Cambridge University Press; 2007. p. 19–91.
[8] Battilani P, Rossi V, Giorni P et al. Modelling, predicting and mapping the emergence of aflatox-
ins in cereals in the EU due to climate change. European Food Safety Authority (EFSA), Support-
ing publication, 2012. (Accessed May 5, 2014, at [Link]
pub/[Link])
[9] Bebber DP, Ramotowski MAT, Gurr SJ. Crop pests and pathogens move poleward in a warming
world. Nature Clim Change 2013;3:985–988.
[10] Bebber DP, Holmes T, Gurr SJ. The global spread of crop pests and pathogens. Global Ecol
Biogeogr 2014;23:1398–1407.
[11] Magan N, Medina A, Aldred D. 2011. Possible climate-change effects on mycotoxin contamina-
tion of food crops pre- and postharvest. Plant Pathol 2011;60:150–163.
[12] Beddington J, Asaduzzaman M, Clark M et al. Achieving food security in the face of climate
change: Final report from the Commission on Sustainable Agriculture and Climate Change.
 4 Changes in environmental factors driven by climate change | 87

CGIAR Research Program on Climate Change, Agriculture and Food Security (CCAFS). Copen-
hagen, Denmark; 2012. (Accessed May 5, 2014, at [Link]
.VOTbnCSDOUk)
[13] Paterson R, Lima N. How will climate change affect mycotoxins in food? Food Res Int
2010;43:1902–1914.
[14] Paterson R, Lima N. Further mycotoxin effects from climate change. Food Res Int 2011;44:
2555–2566.
[15] Wu F, Bhatnagar D, Bui-Klimke T et al. Climate change impacts on mycotoxin risks in US maize.
World Mycotoxin J 2011;4:79–93.
[16] Medina A, Rodriguez A, Magan N. Effect of climate change on Aspergillus flavus and aflatoxin
B1 production. Front Microbiol 2014;5:348. doi: 10.3389/fmicb.2014.00348.
[17] Medina A, Rodríguez A, Sultan Y, Magan N. Climate change factors and Aspergillus flavus:
effects on gene expression, growth and aflatoxin production. World Mycotoxin J 2015;8:171–
179.
[18] Vaughan MM, Huffaker A, Schmelz EA et al. Effects of elevated [CO2 ] on maize defence against
mycotoxigenic Fusarium verticillioides. Plant Cell Environ 2014;37:2691–2706.
[19] Sanchis V, Magan N. Environmental conditions affecting mycotoxins. In: Magan N, Olsen M,
eds Mycotoxins in food: detection and control. Abington, Cambridge, UK: Woodhead Publish-
ing Ltd and CRC Press LLC; 2004. p. 174–189.
[20] Magan N, Geisen R, Schmidt-Heydt M, Medina A, Parra R, Abdel-Hadi A. A systems approach to
integrating molecular, ecophysiological data and phenotypic data for a better understanding
of mycotoxin contamination. J Plant Pathol 2012;94:39.
[21] Garcia D, Barros G, Chulze S, Ramos AJ, Sanchis V, Marín S. Impact of cycling temperatures
on Fusarium verticillioides and Fusarium graminearum growth and mycotoxins production in
soybean. J Sci Food Agric 2012;92:2952–2959.
[22] Medina A, Magan N. Comparisons of water activity and temperature impacts on growth of
Fusarium langsethiae strains from northern Europe on oat-based media. Int J Food Microbiol
2010;142:365–369.
[23] Medina A, Magan N. Temperature and water activity effects on production of T-2 and HT-2
by Fusarium langsethiae strains from north European countries. Food Microbiol 2011;28:
392–398.
[24] Patriarca A, Medina A, Fernández Pinto V, Magan N. Temperature and water stress impacts on
growth and production of altertoxin-II by strains of Alternaria tenuissima from Argentinean
wheat. World Mycotoxin J 2014;7:329–334.
[25] Rodríguez A, Medina A, Córdoba JJ, Magan N. The influence of salt (NaCl) on ochratoxin A
biosynthetic genes, growth and ochratoxin A production by three strains of Penicillium
nordicum on a dry-cured ham-based medium. Int J Food Microbiol 2014;178:113–119.
[26] Rodríguez A, Capela D, Medina A, Córdoba JJ, Magan N. Relationship between ecophysiological
factors, growth and ochratoxin A contamination of dry-cured sausage based matrices. Int J
Food Microbiol 2015;194:71–77.
[27] Giorni P, Magan N, Pietri A, Bertuzzi T, Battilani P. Studies on Aspergillus section Flavi isolated
from maize in northern Italy. Int J Food Microbiol 2007;113:330–338.
[28] Giorni P, Camardo Leggieri M, Magan N, Battilani P. Comparison of temperature and moisture
requirements for sporulation of Aspergillus flavus sclerotia on natural and artificial substrates.
Fungal Biol 2012;116:637–642.
[29] Kos J, Mastilović J, Janić Hajnal E, Šarić B. Natural occurrence of aflatoxins in maize harvested
in Serbia during 2009–2012. Food Control 2013;34:31–34.
[30] Dobolyi C, Sebők F, Varga J et al. Occurrence of aflatoxin producing Aspergillus flavus isolates
in maize kernel in Hungary. Acta Aliment Hung 2013;42:451–459.
88 | Angel Medina, Alicia Rodriguez, and Naresh Magan

[31] Magan N, Aldred D. Environmental fluxes and fungal interactions: maintaining a competitive
edge. In: van West P, Avery S, Stratford M, eds Stress in Yeasts and Filamentous Fungi. Amster-
dam, the Netherlands: Elsevier Ltd; 2008. p. 19–35.
[32] Piecková E, Kunová Z. Indoor fungi and their ciliostatic metabolites. Ann Agric Environ Med
2002;9:59–63.
[33] Leong S, Pettersson OV, Rice T, Hocking AD, Schnurer J. The extreme xerophilic mould Xe-
romyces bisporus – growth and competition at various water activities. Int J Food Microbiol
2011;145:57–63.
[34] Bellí N, Ramos AJ, Sanchís V, Marín S. Incubation time and water activity effects on ochratoxin
A production by Aspergillus section Nigri strains isolated from grapes. Lett Appl Microbiol
2004;38:72–77.
[35] Esteban A, Abarca ML, Bragulat MR, Cabañes FJ. Effects of temperature and incubation time on
production of ochratoxin A by black aspergilli. Res Microbiol 2004;155:861–866.
[36] Mitchell D, Parra R, Aldred D, Magan N. Water and temperature relations of growth and ochra-
toxin A production by Aspergillus carbonarius strains from grapes in Europe and Israel. J Appl
Microbiol 2004;97:439–445.
[37] Astoreca AL, Magnoli CE, Dalcero A. Ecophysiology of Aspergillus section Nigri species poten-
tial ochratoxin A producers. Toxins 2010;2:2593–2605.
[38] Astoreca AL, Barberis CL, Magnoli CE, Dalcero A. Growth and ochratoxin A production by As-
pergillus niger group strains in coffee beans in relation to environmental factors. World Myco-
toxin J 2010;3:59–65.
[39] Medina A, Mateo R, López-Ocaña L, Valle-Algarra FM, Jiménez M. Study of Spanish grape myco-
biota and ochratoxin A production by Isolates of Aspergillus tubingensis and other members of
Aspergillus section Nigri. Appl Environ Microbiol 2005;71:4696–4702.
[40] Selouane A, Bouya D, Lebrihi A, Decock C, Bouseta A. Impact of some environmental factors
on growth and production of ochratoxin A of/by Aspergillus tubingensis, A. niger, and A. car-
bonarius isolated from moroccan grapes. J Microbiol 2009;47:411–419.
[41] Chiotta ML, Sosa DM, Ponsone ML, Chulze SN. Effect of water activity and temperature on
growth of Aspergillus carbonarius and Aspergillus tubingensis and their interactions on ochra-
toxin A production. World Mycotoxin J 2015;8:99–105.
[42] García-Cela E, Crespo-Sempere A, Ramos AJ, Sanchis V, Marin S. Ecophysiological characteri-
zation of Aspergillus carbonarius, Aspergillus tubingensis and Aspergillus niger isolated from
grapes in Spanish vineyards. Int J Food Microbiol 2014;173:89–98.
[43] Gil-Serna J, Vázquez C, García Sandino F, Márquez Valle A, González-Jaén MT, Patiño B. Eval-
uation of growth and ochratoxin A production by Aspergillus steynii and Aspergillus wester-
dijkiae in green-coffee based medium under different environmental conditions. Food Res Int
2014;61:127–131.
[44] Vaquera S, Patriarca A, Fernández Pinto V. Water activity and temperature effects on growth of
Alternaria arborescens on tomato medium. Int J Food Microbiol 2014;185:136–139.
[45] Schmidt-Heydt M, Rüfer CE, Abdel-Hadi A, Magan N, Geisen R. The production of aflatoxin B1
or G1 by Aspergillus parasiticus at various combinations of temperature and water activity is
related to the ratio of aflS to aflR expression. Mycotoxin Res 2010;26:241–246.
[46] Eastburn DM, DeGennaro MM, DeLucia EH, Dermody O, McElrone AJ. Elevated atmospheric
carbon dioxide and ozone alter soybean diseases at SoyFACE. Glob Change Biol 2010;16:
320–330.
[47] Magan N, Aldred D. Post-harvest control strategies: minimizing mycotoxins in the food chain.
Int J Food Microbiol 2007;119:131–139.
[48] Chakraborty S, Newton AC. Climate change, plant diseases, and food security: an overview.
Plant Pathol 2011;60:2–14.
 4 Changes in environmental factors driven by climate change | 89

[49] Juroszek P, von Tiedemann A. Potential strategies and future requirements for plant disease
management under a changing climate. Plant Pathol 2011;60:100–112.
[50] Ziska LH, Morris CF, Goins EW. Quantitative and qualitative evaluation of selected wheat va-
rieties released since 1903 to increasing atmospheric carbon dioxide: can yield sensitivity to
carbon dioxide be a factor in wheat performance? Glob Change Biol 2004;10:1810–1819.
[51] Dixon GR. Climate change impact on crop growth and food production, and plant pathogens.
Can J Plant Pathol 2012;34:362–379.
[52] Plazek A, Hura K, Rapacz H, Zur I. The influence of ozone fumigation on metabolic efficiency
and plant resistance to fungal pathogens. J Appl Bot 2001;75:8–13.
[53] Pateraki M, Dekanea A, Mitchell D, Lydakis D, Magan N. Influence of sulphur dioxide, con-
trolled atmospheres and water availability on in vitro germination, growth and ochra-
toxin A production by strains of Aspergillus carbonarius from grapes. Postharvest Biol Tec
2007;44:141–149.
[54] Giorni P, Battilani P, Pietri A, Magan N. Effect of a w and CO2 level on Aspergillus flavus
growth and aflatoxin production in high moisture maize post-harvest. Int J Food Microbiol
2008;122:109–113.
[55] Wilson DM, Jay E. Influence of modified atmosphere storage on aflatoxin production in high
moisture corn. Appl Microbiol 1975;29:224–228.
[56] Magan N, Lacey J. Effect of gas composition and water activity on growth of field and storage
fungi and their interactions. T Brit Mycol Soc 1984;82:305–314.
[57] Magan N. Studies on the mycoflora of wheat grain: Ecology of the fungi and effects of fungi-
cides. Reading, UK: Reading University; PhD thesis 1982.
[58] Paster N, Lisker N, Chet I. Ochratoxin A production by Aspergillus flavus Wilhelm grown under
controlled atmospheres. Appl Environ Microbiol 1983;45;1136–1139.
[59] Cairns-Fuller V, Aldred D, Magan N. Water, temperature and gas composition interactions affect
growth and ochratoxin A production by isolates of Penicillium verrucosum on wheat grain.
J Appl Microbiol 2005;99:1215–1221.
[60] Samapundo S, De Meulenaer B, Atukwase A, Debevere J, Devlieghere F. The influence of modi-
fied atmospheres and their interaction with water activity on the radial growth and fumonisin
B1 production of Fusarium verticillioides and F. proliferatum on corn. Part 1: The effect of initial
headspace carbon dioxide concentration. Int J Food Microbiol 2007;114:160–167.
[61] Suhr KI, Nielsen PV. Inhibition of fungal growth on wheat and rye bread by modified at-
mosphere packaging and active packaging using volatile mustard essential oil. J Food Sci
2005;70:37–44.
[62] Guynot ME, Marín S, Sanchis V, Ramos AJ. Modified atmosphere packaging for prevention of
mold spoilage of bakery products with different pH and water activity levels. J Food Protect
2003;66:1864–1872.
[63] Brown DW, Proctor RH. Fusarium: genomics, molecular and cellular biology. Portland, OR, USA:
Caister Academic Press; 2013.
[64] Yu J, Chang PK, Ehrlich KC et al. Clustered pathway genes in aflatoxin biosynthesis. Appl Envi-
ron Microbiol 2004;70:1253–1262.
[65] Schmidt-Heydt M, Abdel-Hadi A, Magan N, Geisen R. Complex regulation of the aflatoxin
biosynthesis gene cluster of Aspergillus flavus in relation to various combinations of water
activity and temperature. Int J Food Microbiol 2009;135:231–237.
[66] Abdel-Hadi A, Schmidt-Heydt M, Parra R, Geisen R, Magan N. A systems approach to model the
relationship between aflatoxin gene cluster expression, environmental factors, growth and
toxin production by Aspergillus flavus. J R Soc Interface 2012;9:757–767.
[67] Schmidt-Heydt M, Geisen R. A microarray for monitoring the production of mycotoxins in food.
Int J Food Microbiol 2007;117:131–140.
90 | Angel Medina, Alicia Rodriguez, and Naresh Magan

[68] Medina A, Schmidt-Heydt M, Cárdenas-Chávez DL, Parra R, Geisen R. Magan N. Integrating

toxin gene expression, growth and fumonisin B1 and B2 production by a strain of Fusarium
verticillioides under different environmental factors. J R Soc Interface 2013;10:20130320.
doi: 10.1098/rsib.2013.0320.
[69] Lazzaro I, Susca A, Mulè G et al. 2012. Effects of temperature and water activity on FUM2 and
FUM21 gene expression and fumonisin B production in Fusarium verticillioides. Eur J Plant
Pathol 2012;134:685–695.
[70] Chandler EA, Simpson DR, Thomsett MA, Nicholson P. Development of PCR assays to Tri7
and Tri13 trichothecene biosynthetic genes, and characterisation of chemotypes of Fusar-
ium graminearum, Fusarium culmorum and Fusarium cerealis. Physiol Mol Plant Pathol
2003;62:355–367.
[71] Nielsen LK, Jensen JD, Rodríguez A, Jørgensen LN, Justesen AF. Tri12 based quantitative real-
time PCR assays reveal the distribution of trichothecene genotypes of F. graminearum and
F. culmorum isolates in Danish small grain cereals. Int J Food Microbiol 2012;157:384–392.
[72] Marin P, Jurado M, Magan N, Vázquez C, González-Jaén MT. Effect of solute stress and temper-
ature on growth rate and TRI5 gene expression using real time RT–PCR in Fusarium gramin-
earum from Spanish wheat. Int J Food Microbiol 2010;140:169–174.
[73] Schmidt-Heydt M, Parra R, Geisen R, Magan N. Modelling the relationship between environ-
mental factors, transcriptional genes and deoxynivalenol mycotoxin production by strains of
two Fusarium species. J R Soc Interface 2011;8:117–126.
[74] Geisen R, Schmidt-Heydt M, Karolewiez A. A gene cluster of the ochratoxin A biosynthetic
genes in Penicillium. Mycotoxin Res 2006;22:34–41.
[75] Schmidt-Heydt M, Baxter E Geisen R, Magan N. Physiological relationship between food
preservatives, environmental factors, ochratoxin and otapksPV gene expression by Penicillium
verrucosum. Int J Food Microbiol 2007;119:277–283.
[76] Schmidt-Heydt M., Graf E, Stoll D, Geisen R. The biosynthesis of ochratoxin A by Penicillium as
one mechanism for adaptation to NaCl rich foods. Food Microbiol 2012;29:233–241.
[77] Geisen R. Molecular monitoring of environmental conditions influencing the induction of
ochratoxin A biosynthesis genes in Penicillium nordicum. Mol Nutr Food Res 2004;48:532–
540.
[78] O’Callaghan J, Dobson ADW. Molecular characterization of ochratoxin A biosynthesis and pro-
ducing fungi. Adv Appl Microbiol 2005;58:227–243.
[79] Bacha N, Atoui A, Mathieu F, Liboz T, Lebrihi A. Aspergillus westerdijkiae polyketide synthase
gene “aoks1” is involved in the biosynthesis of ochratoxin A. Fungal Genet Biol 2009;46:77–
84.
[80] Gallo A, Knox BP, Bruno KS, Solfrizzo M, Baker SE, Perrone G. Identification and characteriza-
tion of the polyketide synthase involved in ochratoxin A biosynthesis in Aspergillus carbonar-
ius. Int J Food Microbiol 2014;179:10–17.
[81] Crespo-Sempere A, Marín S, Sanchis V, Ramos AJ. VeA and LaeA transcriptional factors regu-
late ochratoxin A biosynthesis in Aspergillus carbonarius. Int J Food Microbiol 2013;166:479–
486.
[82] Tannous J, El Khoury R, Snini S. et al. Sequencing, physical organization and kinetic expres-
sion of the patulin biosynthetic gene cluster from Penicillium expansum. Int J Food Microbiol
2014;189:51–60.
[83] Puel O, Tadrist S, Delaforge M, Oswald IP, Lebrihi A. The inability of Byssochlamys fulva to
produce patulin is related to absence of 6-methylsalicylic acid synthase and isoepoxydon
dehydrogenase genes. Int J Food Microbiol 2007;115:131–139.
Antonio Moretti and Antonio F. Logrieco
5 Climate change effects on the biodiversity of
mycotoxigenic fungi and their mycotoxins in
preharvest conditions in Europe

5.1 Introduction

Changes in climate have already been apparent in temperatures and a warming of cli-
mate faster than the average global warming measured in the last century. Reliable re-
ports from specialized institutions of the United Nations Intergovernmental Panel on
Climate Change (IPCC) and the World Meteorological Organization (WMO) have con-
firmed that climate changes are occurring nowadays which may be connected with the
ever-increasing human activities of a tremendously growing world population since
the commencement of the industrial revolution. Meteorological extremities such as
droughts, or even torrential rains, floods, and increasing frequency and duration of
heat waves are connected to climate change. It is expected that such phenomena will
increase during the coming decades.
Climate change has a direct and significant effect on agricultural production, di-
minishing thereby food security as well as creating public health risks, including de-
creasing safety of our foods [1]. Recently, particular emphasis has been placed on the
climate shift regarding Europe. Challenges of climate change for European agriculture
include the effects on crop yields and production risks such as heat waves, droughts,
and pests. The global warming tendency [2] and increasing contamination and stress
effects in relation to meteorological extremities, food and feed safety, as well as that
of water sources may increase infections and poisoning occurrences in this region [3].
Drought stresses reduce phytoimmunity of crop plants, and extreme precipitation and
heat waves increase the opportunity for plant pathogenic microorganisms to grow [4].
In particular, the EU green paper on climate change in Europe also suggests that effects
will be regional and either detrimental or advantageous depending on the geograph-
ical area [5]. Thus, in southern Europe, changes may lead to a temperature increase
of 4–5 °C with longer drought periods, resulting in increasing desertification and de-
creasing crop yields. In central Europe, the predictions are for an increase of 3–4 °C,
and higher rainfall and floods, while in northern Europe a mean temperature increase
of 3–4.5 °C and a significant increase in precipitation of 30–40 % are expected. This
may lead to increases in crop yields and perhaps new crop cultivation patterns for
central and northern Europe on the one hand, but could also dramatically affect the
species profile and biochemical characterization of microbial communities occurring
on crops with the introduction of new diseases [5].
92 | Antonio Moretti and Antonio F. Logrieco

Mycotoxins are low molecular weight toxic compounds produced by fungi which
pose a serious risk to human and animal health worldwide. Cereals are often the
most severely affected crops, and because they are a staple food for a large portion of
humanity, mycotoxins are the most prevalent food-related health risk in field crops.
Worldwide scientific and economic focus on mycotoxins also results from the signifi-
cant economic losses associated with their negative impact on human health, animal
productivity, and international trade.
The mycotoxins of greatest concern to food and feed safety are produced primar-
ily by three genera of filamentous fungi: Aspergillus, Fusarium, and Penicillium [6]. In
addition, although fungi can collectively produce hundreds of mycotoxins, only the
following are of serious concern worldwide: aflatoxins, fumonisins, ochratoxins, pat-
ulin, trichothecenes, and zearalenone [6]. Some of these mycotoxins exhibit a very
high degree of structural diversity, reflecting genetic diversity of the species they are
produced by. Some of the mycotoxigenic species of the greatest concern occur world-
wide. However, other important species have more limited distribution. In some cases
mycotoxin contamination can result from the presence of multiple fungal species in a
single crop.
An important component of efforts to control mycotoxin contamination problems
is the study of the morphological, molecular genetic, metabolic, and plant patholog-
ical diversity of mycotoxigenic fungi. The plasticity of agriculturally relevant traits
contributes to the collective ability of fungi to colonize a wide variety of crop species
and to adapt to a range of environmental conditions. Knowledge of environmental
factors which affect the ability of fungi to grow, survive, and interact with plants
is important in order to better understand the variation in the population struc-
tures of mycotoxigenic fungi, their interactions with crop plants, and their ability
to produce mycotoxins. Because climate can profoundly affect growth, distribution,
and mycotoxin production in fungi, climate change has the potential to increase the
risks that mycotoxigenic fungi pose to food and feed safety. The appearance of new
mycotoxin-commodity combinations is of further concern and provides evidence for
the emergence of new fungal genotypes with higher levels of aggressiveness and al-
tered mycotoxin production. Trans-global trade of plant products can also contribute
to the spread of toxigenic fungi and has led to increasing interest in the molecular
diversity of toxigenic fungi on a global scale [7].
Fungal biodiversity is one of the most important contributors to the occurrence
and severity of mycotoxin contamination of crop plants. Phenotypic and metabolic
plasticity has enabled mycotoxigenic fungi to colonize a broad range of agriculturally
important crops, especially cereals, and to adapt to a range of environmental con-
ditions. New mycotoxin-commodity combinations provide evidence for the ability of
fungi to adapt to changing conditions and the emergence of genotypes which confer
enhanced aggressiveness toward plants and/or altered mycotoxin production profiles.
Beside the shifts in the profiles of mycotoxigenic genera and species which colo-
nize important cereals, perhaps the most important contributor to qualitative differ-
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 93

ences in mycotoxin production among fungi is the variation in mycotoxin biosynthetic

genes. Molecular genetic and biochemical analyses of toxigenic fungi have elucidated
specific differences in biosynthetic genes responsible for intra- and interspecific differ-
ences in mycotoxin production. For Aspergillus and Fusarium, the mycotoxigenic gen-
era of greatest concern, variations in biosynthetic genes responsible for production of
individual families of mycotoxins appear to be the result of evolutionary adaptation.
Examples of such variation have been reported for: (a) aflatoxin biosynthetic genes in
Aspergillus flavus; (b) trichothecene biosynthetic genes within and among Fusarium
species; and (c) fumonisin biosynthetic genes in Aspergillus and Fusarium species.
Understanding variation in these biosynthetic genes and the basis for the variation
in mycotoxin production is important for accurate assessment of the risks that fungi
pose to food safety and for the prevention of mycotoxin contamination of crops in
the field and in storage. On the other hand, it is also important to evaluate the main
shifts of the toxigenic fungi colonizing cereals due to the impact of climate change in
order to provide more accurate estimations of the mycotoxigenic risks related to these
crops. The overview provided in this chapter will mainly refer to cereals since they are
a staple food and extremely sensitive to mycotoxin contamination [8]. In particular
aflatoxin and fumonisin contamination of maize and deoxynivalenol (DON) of minor
cereals due to Fusarium head blight (FHB) will be considered in order to estimate fu-
ture changes caused by both climatic factors and cultivation practices.

5.2 Climate change and the risk of aflatoxin and Aspergillus

contamination in Europe
Aflatoxins are potent carcinogens which include four major structural analogues:
AFB1 , AFB2 , AFG1 , and AFG2 . The International Agency for Research on Cancer (IARC)
has classified AFB1 as a group 1 carcinogen, i.e. carcinogenic to humans [9]. In addi-
tion to hepatocellular carcinoma, aflatoxins are associated with occasional outbreaks
of acute aflatoxicosis which lead to death shortly after exposure [10]. Aflatoxins are
produced in diverse agricultural products by several species of Aspergillus, but the
two species of greatest concern are A. flavus and A. parasiticus [11].
Aflatoxin outbreaks are most severe in tropical and subtropical areas around the
world, with temperate regions, such as the United States Midwest, also subject to afla-
toxin contamination. Until 2004, the European perspective regarding aflatoxin con-
tamination was confined to imported foods such as peanut cake, palm kernel, copra,
and corn gluten meal (depending on origin; European Food Safety Authority (EFSA)
[12]). Several surveys which have been conducted to detect AFs in feed samples in Eu-
rope found a small percentage of materials contaminated with AFB1 concentrations
above the regulatory limit. In fact, a survey of 110 maize samples in northern Italy in
2003, initially planned to monitor the occurrence of fumonisins, found 75 % positive
AFB samples with a mean concentration of 4.4 and a maximum of 154.5 μg/kg [13].
94 | Antonio Moretti and Antonio F. Logrieco

In 2006, aflatoxin contaminated rice meal used in dairy cattle feed production was
identified as the cause of elevated AFM1 levels in Swedish milk.
However, a big survey conducted by the EFSA [14] established the emerging issue
of potential aflatoxin contamination of corn, almonds, and pistachios grown in areas
of southern Europe due to the subtropical climate which had occurred in recent years.
Changes in climate have already become apparent in temperatures and warm-
ing of the climate faster than the average global warming measured in the last cen-
tury. Challenges of climate change for European agriculture include the effects on
crop yields and production risks such as heat waves, droughts and pests. Due to the
so-called “mediterraneanization” of southern Europe, aflatoxigenic species, formerly
known in tropical and subtropical regions, may invade this region, which was of tem-
perate climate in previous centuries. A shift in traditional occurrence areas for afla-
toxins is therefore to be expected due to the increasing average temperatures. In this
respect, the Mediterranean zones have been identified as a climate change hotspot
where extreme changes in temperature, CO2 levels, and rainfall patterns are predicted.
Regarding aflatoxins, their contamination events are more prevalent during times of
high heat and drought, which may stress the host plant and thereby facilitate A. flavus
infection [15, 16].
In 2003/2004 and 2012/2013, hot and dry seasons led to severe A. flavus infec-
tion of maize in northern Italy. As a result of the very dry conditions in those years,
A. flavus became a significant problem as a dominant pathogen in maize. The EFSA
therefore issued a call at the end of 2009 for a project to investigate the possibility of
the emergence of aflatoxin B1 in cereals in the EU due to climate change by modelling,
predicting, and mapping. The results of this project [17] led to the main conclusion,
based on the predictive model developed for A. flavus growth and AFB1 production
linked to crop phenology data, that the risk of aflatoxin contamination will increase
in maize in the future due to the climate change trend. In the +2 °C climate change sce-
nario there is a clear increase in aflatoxin risk in areas such as central and southern
Spain, the south of Italy, Greece, northern and southeastern Portugal, Bulgaria, Al-
bania, Cyprus, and European Turkey as compared to the actual current temperature.
In addition to the high aflatoxin risk in these southern European countries, low and
medium aflatoxin risk at harvest in the four main maize producing countries (Roma-
nia, France, Hungary, and northeast Italy) were predicted. It will be therefore be more
important across Europe each year to: (1) improve harmonization of surveillance and
monitoring of aflatoxins; (2) improve databases on the geographical distribution and
prevention methods for aflatoxins; (3) develop models for the prediction of aflatoxin
contamination in the new biogeographical agricultural scenarios.
The ability to produce aflatoxins is highly conserved in some species but vari-
able in others. For example, 94–97 % of the A. parasiticus strains which have been
examined produce aflatoxins, whereas production in A. flavus is highly variable and
depends on genotype, substrate, and geographic origin [18, 19].
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 95

The aflatoxin biosynthetic gene (afl) cluster includes 25 genes [20]. The gene con-
tent and organization of the cluster is highly conserved among Aspergillus species in
section Flavi, which includes A. flavus and A. parasiticus. Sequence variability and
deletions in various genes/regions of the afl cluster have also been used to assess vari-
ability in A. flavus [21]. Moreover, differences in afl genes have been used to distinguish
between aflatoxin-producing and nonproducing strains of A. flavus and A. parasiticus.
Understanding such genetic differences is important because aflatoxin-nonproducing
strains of A. flavus are used to control aflatoxin contamination in some crops [22]. Re-
cently, Gallo et al. [23] examined a collection of aflatoxin-producing and nonproduc-
ing isolates of A. flavus for the presence of seven afl genes, two regulatory genes aflR
and aflS, and the structural genes aflD, aflM, aflO, aflP, and aflQ. The result was the
grouping of strains into four different amplification patterns. All aflatoxin-producing
isolates yielded the complete set of amplification products, whereas nonproducing
isolates did not yield products for three, four, or all seven genes, indicating a high
level of genetic variability among A. flavus isolates. Together, analyses of variation in
the afl cluster in A. flavus have illustrated the genetic complexity of this species, which
includes variability in the afl cluster. This genetic variability has provided markers
which can be used to monitor variation in A. flavus and to evaluate the risk they pose
when present on food commodities.
The genetic diversity of A. flavus populations collected from maize kernels in
northern Italy from 2003 to 2010 was also assessed by Mauro et al. [24], who evalu-
ated the presence or absence of several aflatoxin genes. Six deletion patterns of genes
in aflatoxin clusters were detected. Regarding the atoxigenic isolates, some had no
deletion in the cluster, others had the entire cluster deleted, and only a single strain
had a deletion pattern with only two genes amplified of the thirteen tested.
Therefore, the genetic variability of aflatoxin cluster in non-aflatoxigenic isolates
appears diverse and complex but its understanding is important for the selection of
safe and effective nonproducing strains which could potentially be used for biocontrol
to limit aflatoxin contamination.
Magan et al. [25] have shown that in addition to temperature, changes in CO2 con-
centration and water activity can influence the growth and mycotoxin production of
some mycotoxigenic species, including A. flavus, especially under water stress. More-
over, Medina et al. [26] also studied the effects of the interaction of aw , temperature,
and elevated CO2 on ten structural and regulatory aflatoxin biosynthetic gene expres-
sion. The data generated showed that these interactions have a significant impact
on gene expression stronger than on the growth of A. flavus and can stimulate the
AFB1 production. Therefore, due to the effect that the above mentioned environmen-
tal factors have on the expression of A. flavus aflatoxin genes, accurate knowledge of
the genetic variability of the A. flavus populations occurring in the field is of extreme
importance for both phylogenetic relationships among fungal strains and mycotoxin
gene biosynthetic pathways. This would strengthen the possibility of predicting afla-
96 | Antonio Moretti and Antonio F. Logrieco

toxin production according to changes in environmental factors and would allow bet-
ter management of aflatoxin risk in the field.
In conclusion, the occurrence of AFB1 at high levels in Europe in the years 2003–
2004 and 2012–2013 underlines the fact that climate change will entail a change in the
mycotoxin distribution patterns observed today. Global trade of plant products can
also contribute to the spread of aflatoxigenic fungi and to the increase of diversity of
local fungal populations. The study of the biodiversity of aflatoxigenic fungi occur-
ring in maize in Europe is essential for the development of strategies for the control of
aflatoxin contamination. In this regard, the molecular characterization of native atox-
igenic strains, acting through competitive exclusion of aflatoxin producers, with supe-
rior adaptation to a geographical region, should provide benefit of long-term displace-
ment of toxigenic strains in maize environment. Finally, the development of predictive
models for aflatoxin occurrence based on regional weather data would be a valuable
tool for estimating the risk of contamination after a given growing season, together
with the use of biopesticides in the framework of integrated pest management.

5.3 Fusarium head blight (FHB) of cereals: impact of climate

change on the risk of trichothecenes and Fusarium
contamination in Europe

The fungal genus Fusarium consists of over 90 described species and likely many
additional as yet undescribed but phylogenetically distinct species [27–30]. Many of
these species are plant pathogens and produce a range of mycotoxins, the most agri-
culturally important being trichothecenes and fumonisins [31]. Trichothecenes are a
family of terpene-derived mycotoxins produced by multiple species of Fusarium and
are among the most economically significant mycotoxins worldwide because of their
potency and widespread occurrence in cereals [32]. These mycotoxins are strong in-
hibitors of eukaryotic protein biosynthesis, causing a wide range of toxic effects in
humans and animals, including vomiting, hemorrhagic, and immunosuppressive ef-
fects. They can be toxic to plants and contribute to the pathogenesis of Fusarium on
some crops [31]. All trichothecenes have a tricyclic skeleton structure with an epoxide
group, but they can be divided into two structurally distinct groups based on the ab-
sence (type A trichothecenes) and presence (type B trichothecenes) of a keto group at
carbon atom 8 (C-8) of the skeleton. The type A trichothecenes of greatest concern are
T-2 toxin and HT-2 toxin, while the type B trichothecenes of greatest concern are DON,
nivalenol (NIV), and their acetyl-derivatives [31].
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 97

5.3.1 Organization of TRI loci and trichothecene structural variation

Multiple studies have revealed that structural variation of trichothecene mycotoxins

produced by different species of Fusarium, and in some cases different strains of the
same species, result from DNA sequence polymorphism causing variation in the func-
tionality of trichothecene gene cluster (TRI genes). The different organization of the
TRI genes among the genomes of the Fusarium species shows how widely genetic di-
versity can also be expressed in the biosynthetic gene pathways along this important
phytopathogenic and toxigenic fungal genus.
Fusarium graminearum sensu stricto (Fusarium graminearum s.s.) and F. sporotri-
chioides are the two species in which the trichothecene biosynthetic gene cluster was
first characterized. In both species, the cluster consists of 12 genes which are respon-
sible for synthesis of the core trichothecene skeleton and several modifications to it.
Both species also have two smaller TRI loci. The first of these consists of one gene,
TRI101, and the second locus consists of two genes, TRI1, and TRI16 [33]. Analysis of
TRI loci in 16 species of Fusarium revealed that TRI1 and TRI101 are located in the core
TRI cluster in four species of Fusarium [33] which are members of the F. incarnatum-
equiseti species complex [28]. Relocation of TRI1 and TRI101 into the core TRI cluster
of the F. incarnatum-equiseti species complex provided evidence for growth of a fun-
gal secondary metabolite gene cluster by gene relocation rather than by gene dupli-
cation and subsequent divergence of pre-existing cluster genes [33]. TRI1 was shown
to be a polymorphic gene. This polymorphism contributes to the differences in func-
tion of TRI1 which are responsible for the difference in production of type B or type
A trichothecenes by F. graminearum and F. sporotrichioides, respectively [34]. More-
over, polymorphism in TRI13 is responsible for variations in the presence and absence
of a C-4 hydroxyl, an important structural difference which occurs within type B tri-
chothecenes. Strains which differ according to their ability to produce different types
of trichothecenes are defined as chemotypes.
Similar patterns of deletions within TRI13 occur in isolates of the so-called
F. graminearum clade (F. graminearum species complex (FGSC), F. crookwellense,
and F. culmorum [31]). Strains of these fungi with a functional TRI13 produce the C-4
hydroxylated trichothecene NIV, whereas strains with a nonfunctional TRI13 (i.e. with
the deletions) produce DON [31]. Another trichothecene chemotype difference exhib-
ited by members of the F. graminearum clade is production of 3-acetyldeoxynivalenol
(3-ADON) versus 15-acetyldeoxynivalenol (15-ADON). The genetic basis for this differ-
ence resides in the TRI cluster gene TRI8. Alexander et al. [35] identified consistent
DNA sequence differences in the coding region of TRI8 in 3-ADON and 15-ADON
strains. They also showed that TRI8 in NIV-producing Fusarium strains functions
like that in 15-ADON strains, and that TRI3 was functional in all three chemotypes.
Together, this data indicated that differential activity of TRI8 determines the 3-ADON
and 15-ADON chemotypes in Fusarium.
98 | Antonio Moretti and Antonio F. Logrieco

5.3.2 FHB of minor cereals

FHB, caused by a complex of Fusarium species, is one of the most important fungal
diseases associated with wheat and several other minor cereals, the main species of
which is F. graminearum s.s. The effects of FHB are related to yield and quality reduc-
tion of the infected kernels, due to the accumulation of mycotoxins, especially DON,
in the raw grain and in the processed wheat products [36]. Fusarium graminearum is
more appropriately defined as FGSC, since in the last decade it has been described as a
group of related species, differing in geographical distribution, mycotoxin production,
and pathogenicity [30]. According to the latest reports, FGSC consists of 15 different
species based on multilocus phylogenetic analyses [30]. The species F. graminearum
s.s. is the most common and widespread species of the FGSC, prevalent in North Amer-
ica [37] and Europe [38], but reported worldwide, whereas other species are geograph-
ically more restricted. As an example, F. asiaticum is a widely distributed species in
Asia and South America [39], F. gerlachii and F. louisianense are typical of US [7, 30],
F. aethiopicum is endemic to Africa [40], F. acaciae-mearnsii to Australia and South
Africa [39, 41], F. nepalense is a new species recently discovered in Nepal [30], F. vorosii
and F. ussurianum are endemic to Asia [7, 42], F. boothi and F. mesoamericanum are typ-
ical of Central America [39, 40], and F. cortaderiae, F. brasilicum, F. austroamericanum
and F. meridionale are typical of South America [39]. However, strains of F. meridionale
and F. boothii were also discovered in South Africa [41], in South Korea [43], and in
Nepal [44], suggesting that world trade could contribute to the spread of some FGSC
species to countries in which they are not endemic [42].
Besides F. graminearum s.s., many other Fusarium species have been associated
worldwide with FHB, such as F. avenaceum, F. culmorum and F. poae primarily, and
F. acuminatum, F. cerealis (syn. F. crookwellense), F. equiseti, F. langsethiae, F. sporotri-
chioides, and F. tricinctum to a lesser extent. The toxigenic potential of FHB pathogens
can greatly vary between species, since each can produce a specific range of myco-
toxins [31]. Although agricultural practices play a key role in the prevalence of FHB
pathogens, the predominance of FHB species is determined, to a greater extent, by
climatic factors, particularly temperature and moisture [45], and can therefore dra-
matically change in different geographical areas. In particular Europe, which is char-
acterized by a wide range of climatic conditions from the southern (Mediterranean
countries) to central and northern regions, shows dramatic differences in the species
composition associated with FHB [8]. Indeed, these pathogens can occur on wheat
heads in different combinations leading to multiple mycotoxin contaminations in the
harvested grain. It is therefore of key importance to determine the exact nature of the
FHB complex for more reliable disease prediction and management, and in order to
manage the food risks associated with consumption of contaminated kernels.
F. graminearum is the most common cereal head blight pathogen in moist, warm
continental climates of Europe, while F. culmorum and F. avenaceum are more preva-
lent in maritime and cooler European regions. Inoculum production of the Fusarium
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 99

species is dependent on rainfall, and warm and moist conditions during anthesis are
key factors for disease development [46]. The species differ in their climatic distribu-
tion and in the optimum climatic conditions they require [47]. Significant yield losses
and mycotoxin accumulation have been reported under the hot, wet climatic condi-
tions favorable for F. graminearum, while the species is sensitive to lower temperatures
[48]. Disease progress can cease at cool temperatures (lower than 15 °C) and a signifi-
cantly longer wet period is required at temperatures of 20 °C as opposed to 25 °C, while
perithecial production and development is optimal at temperatures between 15 °C and
24 °C and limited in higher or lower temperatures and dry conditions [49]. Cool and
moist conditions at the end of summer season favor F. avenaceum infection because it
can infect at lower temperatures when there is enough humidity. On the other hand,
F. poae favor a warm dry environment, and precipitation has a negative effect on in-
fection, while correlations between temperatures over 15 °C at maturity and F. poae
infection were positive. F. tricinctum favors precipitation after, but not during flower-
ing. F. culmorum prefers cooler temperatures than F. graminearum, while higher hu-
midity is also more favorable to F. graminearum than F. culmorum. Langseth and Elen
[50] observed that spring drought seems to make cereals more susceptible to Fusarium
infection and high DON concentrations. F. langsethiae infects flowers and developing
kernels early in the season, when high humidity occurs [51], but it can also be preva-
lent on oats in dry conditions [52]. Finally, exposure to cold and wet weather due to
late harvest can also lead to high DON contamination [50].
The cool and rather humid climate in northern Europe influences the Fusarium
flora. The dominant species reported in Finland is F. avenaceum, together with the
related species F. arthrosporioides, which is also the most common Fusarium species
in all Scandinavian countries [53]. This species does not produce trichothecene myco-
toxins, but minor toxic metabolites such as moniliformin, beauvericin, and enniatins
[31]. Fusarium tricinctum is also relatively common on minor cereals depending on
the year, and produces enniatins and moniliformin [54]. The incidence of F. poae,
infection of which is favored by dry weather readily at ear emergence, has been re-
cently observed to have increased in Norway [55]. Moreover, F. poae is not considered
a seedling pathogen, does not affect plant development, does not cause head blight
symptoms [56], and produces beauvericin, and both types A and B trichothecene [31].
While F. graminearum is the main DON producer in central and southern Europe, in
Nordic areas F. culmorum has been reported as dominant [8], being common on ce-
real roots, stem base, and heads in all Scandinavian countries, including Finland [8].
Fusarium culmorum tolerates cold conditions, survives very well in crop cereal debris
and soil, its infection is induced by high temperatures and rainfall during anthesis,
and can proceed until harvest. However, a decline in the presence of F. culmorum and
an increase in F. graminearum have been reported in the last decade in some areas of
central and northern Europe by several authors [57, 58].
Fusarium langsethiae, a species formally described in the last decade, is very com-
mon in all northern European countries, often being the first colonizer of kernels after
100 | Antonio Moretti and Antonio F. Logrieco

ear emergence [51]. Fusarium langsethiae produces T-2 and HT-2, the most harmful type
A trichothecene toxins [31] also in cool and humid conditions. According to Pettersson
et al. [59], T-2/HT-2 contaminations have increased on minor cereals during the past
20 years in northern Europe due to increased infections of F. langsethiae.
In the cooler, maritime climate of Britain and the Netherlands, the most common
species involved in FHB in cereal grain are F. culmorum, F. graminearum s.s., F. ave-
naceum, and F. poae. At the beginning of 2000, F. graminearum was the most abundant
Fusarium species on wheat in the Netherlands; a significant change in the situation
had occurred compared with the early 1990s when F. culmorum was the dominating
species in wheat [57]. The same was observed in the UK, where F. graminearum has
increased on wheat, while the previously common F. culmorum has become less im-
portant [60]. However, also in the cooler temperate climates of Europe areas such as
Germany, where F. culmorum used to be the prevalent species, F. graminearum has be-
come the dominant species in the last decade, because the higher temperatures favor
its dominance in the FHB complex [61]. In more eastern locations, such as Poland,
F. poae has been the predominant species for a long period, followed by F. tricinctum,
F. avenaceum, F. culmorum, and F. graminearum [8]. However, a significant increase in
the frequency of F. graminearum was observed during the last decade in all regions of
Poland, including the northern areas, as reported by Stępień and Chełkowski [62].
T-2 and HT-2 toxin contamination have become more prevalent on oats and barley
in the UK, which has been connected to F. langsethiae detection in grains [60]. In addi-
tion, in northern France, this species has become prevalent on barley in recent years
[63]. The species grows and produces toxins in a wide temperature range [25]. Fusar-
ium langsethiae is an emerging mycotoxin producer also in Poland, where Lukanowski
and Sadowski [64] reported the occurrence of infection on winter wheat.
The species profile of strains causing FHB in southern Europe varies annually
depending on environmental conditions. In general, FHB incidence is low and in the
most southern regions of Italy and Spain the disease is absent. However, in the more
northern regions of Italy, Spain, and Portugal, southern France, and the whole Balkan
Peninsula, F. graminearum and F. poae are reported to be the largely dominant species
on cereals at maturity, with DON being the most frequently occurring mycotoxin
on grains and F. avenaceum and F. culmorum rarely associated with FHB diseased
plants [8]. However, more recently, in the southern regions of the Balkan Peninsula,
F. verticillioides, and, to a lesser extent, F. sporotrichioides have been more frequently
identified on cereals, showing fumonisins [65] and T-2 and HT-2 [66], respectively,
as possible further mycotoxin risk associated with Fusarium colonization of cereal
kernels. Interestingly, increased occurrence of F. langsethiae has been reported in
Italy, with an increase of the T-2 and HT-2 contamination of kernels [67].
Trichothecene production by Fusarium species is broadly species specific [8]. The
most important mycotoxins produced by FGSC members are type B trichotecenes,
which are mainly produced by F. graminearum s.s., the most frequent and virulent
species within the FHB complex, usually occurring in warm and humid environmental
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 101

conditions [38, 45]. Three chemotypes can be distinguished within FGSC populations:
the NIV chemotype for strains producing NIV and 4NIV; the 3ADON for strains pro-
ducing DON and 3ADON; and the 15ADON chemotype for strains producing DON
and 15ADON. Some strains produce both DON and NIV and have been defined as
“unknown chemotype” [68]. The DON chemotypes are pathogenically more aggres-
sive towards wheat, compared to the NIV chemotype, probably reflecting a selective
advantage [69]. Various investigations worldwide showed that DON chemotypes (in
particular the 15ADON chemotype) predominate in North America, South America and
Europe, while the NIV chemotype is more common in Europe than in North or South
America. More recent surveys indicate that in northwestern Europe F. graminearum
sensu lato is segregating for all three chemotypes [70, 71]. An increasing frequency
of 3ADON was observed in North America besides the prevalent 15ADON [68, 72]. In
addition, the NIV chemotypes are being replaced by DON-producing strains in Russia
[42]. In contrast the presence of all DON and NIV chemotypes was reported in China,
Japan, Korea and Nepal [73–75].

5.3.3 Impact of climate change on the Fusarium species profile associated with FHB

Several reports have tried to comprehend the possible shifting of Fusarium species
involved in FHB in different geographic areas according to future environmental sce-
narios. According to Parikka et al. [53], the North European climate is predicted to
become milder and more humid towards 2050. The subsequent climate change effects
will therefore lead to a slight shift in composition of Fusarium flora in cereal grains [53].
Fusarium poae may become more prevalent in dry years, while the predicted increase
of spring drought would benefit F. culmorum, which would otherwise be decreasing
with higher temperatures [53]. Moreover, F. langsethiae will possibly utilize dry spring
and summer periods and may infect the expanding winter wheat crops to some extent,
in addition to oats and barley where it is now mainly detected [53]. Finally, the above-
mentioned authors suggested that tillage practices need to be changed towards con-
servation and reduced tillage, which predispose cereals to head blight infections [53].
Madgwick et al. [76] studied how the impact of climate change on wheat anthesis
date could influence the impact of FHB in UK mainland arable areas. The authors used
a wheat growth model for projections of incidence of anthesis date, and a weather-
based model was developed for use in projections of incidence of FHB in the UK. Daily
weather data, generated for 14 sites in arable areas of the UK for a baseline scenario
and for high and low CO2 emissions in the 2020s and 2050s, were used to project wheat
anthesis dates and FHB incidence for each site and climate change scenario. The in-
cidence of FHB was related to rainfall during anthesis and temperature during the
preceding 6 weeks. The conclusion of this study was that, with the expected climate
change in 2050, wheat anthesis dates will be earlier and FHB epidemics will be more
102 | Antonio Moretti and Antonio F. Logrieco

severe, especially in southern England, mainly because of an increase of F. graminer-

aum and the associated DON.
A relevant study outside Europe was carried out by Zhang et al. [77] and investi-
gated the impacts on FHB on wheat in China due to climate change. The estimation
of incidence of wheat FHB in central China was evaluated by developing a logistic
weather-based regression model, using up to 10 years (2001–2010) of disease, anthe-
sis date, and weather data available for 10 locations in Anhui and Hubei provinces.
How climate change may affect wheat anthesis date and FHB in central China was
estimated for the period 2020–2050 using the wheat growth model Sirius and simu-
lated weather data obtained employing the regional climate modelling system PRECIS
[77]. The study suggested that climate change will increase the risk of serious FHB
epidemics on winter wheat in central China by the middle of this century, as also pre-
dicted for the UK by Madgwick et al. [76]. The implications for food security in China
are extremely serious, because FHB is already a cause of substantial losses in wheat
yield and quality, exacerbated by the high level of Fusarium mycotoxin accumulation
in the kernels [77]. Because wheat is an essential staple crop over large areas of China,
these predicted impacts of climate change would provide a guide to the Chinese gov-
ernment and industry in preparation for adaptation to climate change [77].
Other weather-based models for predicting the risk of FHB have been developed
for Argentina, the USA, Italy, Brazil, and the UK [76, 78–81]. All these models develop
country specific projections of impacts of climate change. However, they also need to
incorporate impacts of climate change on crops by combining a crop growth model as
performed by Madgwick et al. [76]. This latter model evaluated the impact of climate
change on important crop stages such as date of anthesis, which is a key factor for
FHB development, because Fusarium species infect during anthesis [82]. The model
used by Zhang et al. [77] showed that incidence of FHB is related to the number of days
of rainfall in a 30-day period after anthesis, and that high temperatures 2 to 3 weeks
before anthesis increase the incidence of disease. The relationship with rainfall after
anthesis is related to the effect of rain on infection and subsequent growth of Fusarium
within the wheat ear [82], while high temperatures before anthesis may relate to the
influence of increased temperature on Fusarium growth and sporulation [47].
Besides the environmental conditions, further important factors affect FHB epi-
demic development, such as agronomic practices. This limits the efficacy of weather-
based disease models [77]. In particular, the proximity of previous maize crops can
dramatically affect FHB development, because maize debris is a potent source of in-
ocula of F. graminearum [83]. An expected increase of maize in rotations can be consid-
ered a significant risk factor for F. graminearum infections, especially in no-till prac-
tices, since in warm and humid conditions the ascospore production in crop residues
could cause frequent epidemics. Therefore, an indirect impact of climate change on
the severity of FEB epidemics will be the increase of maize cultivation in many geo-
graphic areas where the future climate scenario will allow farmers to grow this crop,
well adapted to the higher temperatures [73].
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 103

In general, the information obtained from all investigations on the impacts of cli-
mate change on FHB will allow the definition of strategies for both governments and
industry for reduction of the risk related to the more favorable conditions for FHB
and mycotoxin contamination of grains. New wheat cultivars with higher tolerance
and more effective fungicide treatments to control Fusarium species which cause FHB
should be considered [84]. Since both strategies could require many years to become
effective, it is important to begin adapting to the impacts of climate change on crop
disease soon. Such strategies for adaptation to impacts of climate change on FHB
will contribute to sustainable wheat production and improved food safety and secu-
rity [73].
In conclusion, the impacts of climate change on FHB could result in a dramatic
increase of disease severity worldwide with higher risks due to the mycotoxin con-
tamination of the end products. Moreover, the deep profile modifications of toxigenic
Fusarium species occurring on kernels at maturity in different geographical areas of
the world will cause the development of new mycotoxin risks in specific regions, due
to the changed ability of given Fusarium species to colonize new environments. Exam-
ples are the increase of DON in the most northern regions of Europe, the higher risk
of contamination by T-2 and TH-2 toxins in many regions of Europe, and the increase
of fumonisin risk in the Balkan Peninsula. Finally, the influence of climate change
on the expression of mycotoxin biosynthetic genes in the different Fusarium species
needs to be more thoroughly investigated. This knowledge will be of key importance
in understanding the genetic mechanisms used by the toxigenic Fusarium species to
increase genetic variability and will allow better definition of strategic solutions for
disease management.

References

[1] WHO. Protecting health in Europe from climate change. Menne B, Apfel F, Kovats S, Racioppi F
eds. Copenhagen, Denmark: World Health Organization Regional Office for Europe; 2008.
[2] Nature Editorial on Berkeley Earth Surface Temperature (BEST) studies. Scientific climate.
Nature 2011;478:428.
[3] Farkas J, Beczner J. A klímaváltozás hatásai az élelmiszerbiztonságra (Potential effects of cli-
mate change on the safety of foods). Élelmiszervizsgálati Közlemények 2010;56:219–230.
[4] Tirado MC, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank J. Climate change and food safety:
A review. Food Res Int 2010;43:1745–1765.
[5] European Commission. Adapting to climate change in Europe–options for EU action. Green pa-
per from the Commission to the Council, the European Parliament, the European Economic and
Social Committee of the Regions. COM (2007) 354. Brussels, Belgium: European Commission:
2007. (Accessed December 5, 2014, at [Link]
CELEX:52007DC0354).
[6] Marasas WFO, Gelderblom WCA, Shephard GS, Vismer HF. Mycotoxins: A global problem. In:
Leslie JF, Bandyopadhyay R, Visconti A (eds). Mycotoxins: Detection methods, management,
public health and agricultural trade. Wallingford, Oxfordshire, UK: CABI; 2008. p. 29–40.
104 | Antonio Moretti and Antonio F. Logrieco

[7] Starkey DE, Ward TJ, Aoki T et al. Global molecular surveillance reveals novel Fusarium head
blight species and trichothecene toxin diversity. Fungal Genet Biol 2007;44:1191–1204.
[8] Logrieco A.F, Moretti A. Between emerging and historical problems: An overview of the main
toxigenic fungi and mycotoxin concerns in Europe. In: Leslie JF, Bandyopadhyay R, Visconti
A (eds). Mycotoxins: Detection methods, management, public health and agricultural trade.
Wallingford, Oxfordshire, UK: CABI; 2008. p. 139–153.
[9] IARC. Some naturally occurring substances: Food items and constituents, heterocyclic aromatic
amines and mycotoxins. IARC Monographs on the evaluation of carcinogenic risks to humans,
vol. 56. UK: International Agency for Research on Cancer; 1993.
[10] Azziz-Baumgartner E, Lindblade K, Gieseker K et al. Case-control study of an acute aflatoxico-
sis outbreak, Kenya, 2004. Environ Health Perspect 2005;113:1779–1783.
[11] Frisvad JC, Skouboe P, Samson RA. Taxonomic comparison of three different groups of afla-
toxin producers and a new efficient producer of aflatoxin B1 , sterigmatocystin and 3-O-
methylsterigmatocystin, Aspergillus rambellii sp. nov. Syst Appl Microbiol 2005;28:442?453.
[12] European Food Safety Authority. Opinion of the Scientific Panel on Contaminants in the Food
Chain on a request from the Commission related to aflatoxin B1 as undesirable substance in
animal feed. EFSA J 2004;39:1–27.
[13] Piva G, Battilani P, Pietri A. Emerging issues in southern Europe: Aflatoxins in Italy. In: Barug
D, Bhatnagar D, van Egmond HP, van der Kamp J W, van Osenbruggen WA, Visconti A (eds). The
mycotoxin fact book: Food and feed topics. Wageningen, the Netherlands: Academic Publish-
ers; 2006. p. 139–153.
[14] European Food Safety Authority. Opinion of the Scientific Panel on Contaminants in the Food
Chain on a request from the Commission related to the potential increase of consumer health
risk by a possible increase of the existing maximum levels for aflatoxins in almonds, hazelnuts
and pistachios and derived products. EFSA J. 2007;446:1–127.
[15] Schmidt-Heydt M, Abdel-Hadi A, Magan N, Geisen R. Complex regulation of the aflatoxin
biosynthesis gene cluster of Aspergilus flavus in relation to various combinations of water
activity and temperature. Int J Food Microbiol 2009;135:231–237.
[16] Mohale S, Medina A, Magan N. Effect of environmental factors on in vitro and in situ interac-
tions between atoxigenic and toxigenic A. flavus strains and control of aflatoxin contamination
of maize. Biocontrol Sci Techn 2013;23:776–793.
[17] Battilani P, Rossi V, Giorni P et al. Modelling, predicting and mapping the emergence of afla-
toxins in cereals in the EU due to climate change. European Food Safety Authority (EFSA) sup-
porting publication; 2012. (Accessed December 5, 2014, at [Link]
supporting/pub/[Link])
[18] Vaamonde G, Patriarca A, Pinto VF, Comerio R, Degrossi C. Variability of aflatoxin and cyclopi-
azonic acid production by Aspergillus section Flavi from different substrates in Argentina. Int J
Food Microbiol 2003;88:79–84.
[19] Pildain MB, Vaamonde G, Cabral D. Analysis of population structure of Aspergillus flavus from
peanut based on vegetative compatibility, geographic origin, mycotoxin and sclerotia produc-
tion. Int J Food Microbiol 2004;93:31?40.
[20] Yu J, Chang PK, Ehrlich KC et al. Clustered pathway genes in aflatoxin biosynthesis. Appl Envi-
ron Microbiol 2004;70:1253?1262.
[21] Chang PK, Ehrlich KC, Hua SST. Cladal relatedness among Aspergillus oryzae isolates and
Aspergillus flavus S and L morphotype isolates. Int J Food Microbiol 2006;108:172?177.
[22] Dorner JW, Horn BW. Separate and combined applications of nontoxigenic Aspergillus flavus
and A. parasiticus for biocontrol of aflatoxin in peanuts. Mycopathologia 2007;163:215?223.
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 105

[23] Gallo A, Stea G, Battilani P, Logrieco AF, Perrone G. Molecular characterization of an As-
pergillus flavus population isolated from maize during the first outbreak of aflatoxin contami-
nation in Italy. Phytopathol Mediterr 2012;51:198−206.
[24] Mauro A, Battilani P, Callicott KA, Giorni P, Pietri A. Cotty PJ. Structure of an Aspergillus flavus
population from maize kernels in northern Italy. Int J Food Microbiol 2013;162:1–7.
[25] Magan N, Medina A, Aldred D. Possible climate change effects on mycotoxin contamination of
food crops pre- and postharvest. Plant Pathol 2011;60:150–163.
[26] Medina A, Rodriguez A, Magan N. Effect of climate change on Aspergillus flavus and aflatoxin
B1 production. Front Microbiol 2014;5:348. doi: 10.3389/fmicb.2014.00348.
[27] Leslie JF, Summerell BA. The Fusarium laboratory manual. Ames, Iowa, USA: Blackwell Publish-
ing; 2006.
[28] O’Donnell K, Sutton DA, Rinaldi MG, Gueidan C, Crous PW, Geiser DM. Novel multilocus se-
quence typing scheme reveals high genetic diversity of human pathogenic members of the
Fusarium incarnatum-F. equiseti and F. chlamydosporum species complexes within the United
States. J Clin Microbiol 2009;47:3851−3861.
[29] O’Donnell K, Rooney AP, Proctor RH et al. Phylogenetic analyses of RPB1 and RPB2 support
a middle Cretaceous origin for a clade comprising all agriculturally and medically important
fusaria. Fungal Genet Biol 2013;52:20−31.
[30] Sarver BA, Ward TJ, Gale LR et al. Novel Fusarium head blight pathogens from Nepal
and Louisiana revealed by multilocus genealogical concordance. Fungal Genet Biol
2011;48:1077−1152.
[31] Desjardins AE. Fusarium mycotoxins: Chemistry, genetics and biology. St. Paul, Minnesota,
USA: APS Press; 2006.
[32] CAST. Mycotoxins: Risks in plant, animal and human systems, Task Force Report № 139. Ames,
Iowa, U.S.A: Council for Agricultural Science and Technology (CAST); January 2003.
[33] Proctor RH, McCormick SP, Alexander NJ, Desjardins AE. Evidence that a secondary metabolic
biosynthetic gene cluster has grown by gene relocation during evolution of the filamentous
fungus Fusarium. Mol Microbiol 2009;74:1128−1142.
[34] McCormick SP, Alexander NJ, Proctor RH. Heterologous expression of two trichothecene P450
genes in Fusarium verticillioides. Can J Microbiol 2006;52:220−226.
[35] Alexander NJ, McCormick P, Waalwijk C, van der Lee T, Proctor RH. The genetic basis
for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal Genet Biol
2011;48:485−495.
[36] van der Fels-Klerx HJ, Stratakou I. T-2 toxin and HT-2 toxin in grain and grain-based commodi-
ties in Europe: occurrence, factors affecting occurrence, co-occurrence and toxicological ef-
fects. World Mycotoxin J 2010;3:349−367.
[37] Ward TJ, Clear RM, Rooney AP et al. An adaptive evolutionary shift in Fusarium head blight
pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in
North America. Fungal Genet Biol 2008;45:473−484.
[38] Yli-Mattila T. Ecology and evolution of toxigenic Fusarium species in cereals in northern Europe
and Asia. J Plant Pathol 2010;92:7–18.
[39] O’Donnell K, Ward TJ, Geiser DM, Kistler HC, Aoki T. Genealogical concordance between the
mating type locus and seven other nuclear genes supports formal recognition of nine phy-
logenetically distinct species within the Fusarium graminearum clade. Fungal Genet Biol
2004;41:600–623.
[40] O’Donnell K, Ward TJ, Aberra D et al. Multilocus genotyping and molecular phylogenetics re-
solve a novel head blight pathogen within the Fusarium graminearum species complex from
Ethiopia. Fungal Genet Biol 2008;45:1514–1522.
106 | Antonio Moretti and Antonio F. Logrieco

[41] Boutigny AL, Ward TJ, Van Coller GJ et al. Analysis of the Fusarium graminearum species com-
plex from wheat, barley, and maize in South Africa provides evidence of species-specific differ-
ences in host preference. Fungal Genet Biol 2011;48:914–920.
[42] Yli-Mattila T, Gagkaeva T, Ward TJ, Aoki T, Kistler HC, O’Donnell K. A novel Asian clade within
the Fusarium graminearum species complex includes a newly discovered cereal head blight
pathogen from the Russian Far East. Mycologia 2009;101:841–852.
[43] Lee YW, Jeon JJ, Kim H et al. Lineage composition and trichothecene production of Gibberella
zeae population in Korea. In: Yoshizawa T (ed). New horizons of mycotoxicology for assuring
food safety. Kagawa, Japan: Japanese Association of Mcyotoxicology; 2004. p. 117–122.
[44] Desjardins AE, Proctor RH. Genetic diversity and trichothecene chemotypes of the Fusarium
graminearum clade isolated from maize in Nepal and identification of a putative new lineage.
Fungal Biol 2011;115:38–48.
[45] Xu XM, Nicholson P, Thomsett et al. Relationship between the fungal complex causing Fusar-
ium head blight of wheat and environmental conditions. Phytopathology 2008;98:69–78.
[46] Xu X. Effects of environmental conditions on the development of Fusarium ear blight. Eur J
Plant Pathol 2003;109:683–689.
[47] Doohan FM, Brennan J, Cooke BM. Influence of climatic factors on Fusarium species
pathogenic to cereals. Eur J Plant Pathol 2003;109:755–768.
[48] Parry DW, Jenkinson P, McLeod L. Fusarium ear blight (scab) in small grain cereals – a review.
Plant Pathol. 1995;44:207–238.
[49] Dufault NS, De Wolf ED, Lipps PE, Madden LV. Role of temperature and moisture in the produc-
tion and maturation of Gibberella zeae perithecia. Plant Dis 2006;90:637–644.
[50] Langseth W, Elen O. Differences between barley, oats and wheat in the occurrence of deoxyni-
valenol and other trichothecenes in Norwegian grain. J Phytopathol 1996;144:113–118.
[51] Parikka P, Hietaniemi V., Rämö S. The effect of tillage on Fusarium infection and mycotoxins
on barley and oats. In: The BCPC International Congress Crop Science & Technology 2005:
Congress Proceedings, vol. 1, SECC, 31 Oct-2 Nov 2005. Glasgow, UK. British Crop Protection
Council; 2005. p. 423–428.
[52] Parikka P, Hietaniemi V, Rämö S, Jalli H. Fusarium infection and mycotoxin contents of oats
under different tillage treatments. J Plant Pathol 2008;90(S3):75.
[53] Parikka P, Hakala K, Tiilikkala K. Expected shifts in Fusarium species’ composition on cereal
grain in Northern Europe due to climatic change. Food Addit Contam A 2012;29:1543–1555.
[54] Kokkonen M, Ojala L, Parikka P, Jestoi M. Mycotoxin production of selected Fusarium species
at different culture conditions. Int J Food Microbiol 2010;143:17–25.
[55] Elen O, Klemsdal SS, Clasen P-E, Razzaghian MJ. Fusarium spp. and mycotoxins in Norwegian
wheat grain (2001–2004). In: Abstracts, XV Congress of European Mycologists, Sept 16–21
2007, St. Petersburg, Russia; 2007. p. 275–276.
[56] Imathiu SM, Hare MC, Ray RV, Back M, Edwards SG. Evaluation of pathogenicity and ag-
gressiveness of F. langsethiae on oat and wheat seedlings relative to known seedling blight
pathogens. Eur J Plant Pathol 2010;126:203–216.
[57] Waalwijk C, van der Lee T, de Vries I, Hesselink T, Arts J, Kema GHJ. Synteny in toxigenic Fusar-
ium species: The fumonisin gene cluster and the mating type region as examples. Eur J Plant
Pathol 2004;110:533–544.
[58] Nielsen LK, Jensen JD, Nielsen GC et al. Fusarium head blight of cereals in Denmark: Species
complex and related mycotoxins. Phytopathology 2011;101:960–969.
[59] Pettersson H, Borjesson T, Persson L, Leirenius C, Berg G, Gustafsson G. T-2 and HT-2 toxins in
oats grown in Northern Europe. Cereal Res Commun 2008;36B:591–592.
[60] Edwards SG. Fusarium mycotoxin content of UK organic and conventional oats. Food Addit
Contam A 2009;26:1063–1069.
 5 Climate change effects on the biodiversity of mycotoxigenic fungi | 107

[61] Miedaner T, Cumagun CJR, Chakraborty S. Population genetics of three important head blight
pathogens Fusarium graminearum, F. pseudograminearum and F. culmorum. J Phytopathol
2008;156:129–139.
[62] Stępień L, Chełkowski J. Fusarium head blight of wheat: pathogenic species and their myco-
toxins. World Mycotox J. 2010;3:107–119.
[63] Strub C, Pocaznoi D, Lebrihi A, Fournier R, Mathieu F. Influence of barley malting operating
parameters on T-2 and HT-2 toxinogenesis of Fusarium langsethiae, a worrying contaminant of
malting barley in Europe. Food Addit Contam A 2010;27:1247–1252.
[64] Lukanowski A, Sadowski C. Fusarium langsethiae on kernels of winter wheat in Poland – Oc-
currence and mycotoxigenic abilities. Cereal Res Commun 2008;36B:453–457.
[65] Stanković S, Lević J, Ivanović D, Krnjaja V, Stanković G, Tančić S. Fumonisin B1 and its co-
occurrence with other fusariotoxins in naturally-contaminated wheat grain. Food Control
2012;23:384–348.
[66] Ivić D, Domijan AM, Peraica M, Miličević T, Cvjetković B. Fusarium spp. contamination of
wheat, maize, soybean, and pea grain in Croatia. Arh Hig Rada Toksikol 2009;60:435–442.
[67] Infantino A, Pucci N, Conca G, Santori A. First report of Fusarium langsethiae on durum wheat
kernels in Italy. Plant Dis 2007;91:1362.
[68] Ward TJ, Bielawski JP, Kistler HC, Sullivan E, O’Donnell K. Ancestral polymorphism and adaptive
evolution in the trichothecene mycotoxin gene cluster of phytopathogenic Fusarium. Proc Natl
Acad Sci USA 2002;99:9278–9283.
[69] Desjardins AE, Jarosz AM, Plattner RD, Alexander NJ, Brown DW, Jurgenson JE. Patterns of tri-
chothecene production, genetic variability, and virulence to wheat of Fusarium graminearum
from smallholder farms in Nepal. J Agric Food Chem 2004;52:6341–6346.
[70] Jennings P, Coates ME, Walsh K, Turner JA, Nicholson P. Determination of deoxynivalenol- and
nivalenol-producing chemotypes of Fusarium graminearum isolated from wheat crops in Eng-
land and Wales. Plant Pathol 2004;53:643–652.
[71] Qu B, Li HP, Zhang JB et al. Comparison of genetic diversity and pathogenicity of fusarium head
blight pathogens from China and Europe by SSCP and seedling assays on wheat. Plant Pathol
2008;57:642–651.
[72] Schmale DG, Wood-Jones AK, Cowger C, Bergstrom GC, Arellano C. Trichothecene genotypes of
Gibberella zeae from winter wheat fields in the eastern USA. Plant Pathol 2011;60:909–617.
[73] Zhang H, van der Lee T, Waalwijk C et al. Population analysis of the Fusarium graminearum
species complex from wheat in China shows a shift to more aggressive isolates. PLoS ONE
2012;7(2):e31722. Doi:10.137/[Link].0031722.
[74] Karugia GW, Suga H, Gale LR, Nakajima T, Tomimura K, Hyakumachi M. Population structure
of the Fusarium graminearum species complex from a single Japanese wheat field sampled in
two consecutive years. Plant Dis 2009;93:170–174.
[75] Lee SH, Lee J, Nam YJ, Lee S, Ryu JG, Lee T. Population structure of Fusarium graminearum from
maize and rice in 2009 in Korea. Plant Pathol 2010;26:321–327.
[76] Madgwick JW, West JS, White RP et al. Impacts of climate change on wheat anthesis and fusar-
ium ear blight in the UK. Eur J Plant Pathol 2011;129:117–131.
[77] Zhang X, Halder J, White RP et al. Climate change increases risk of fusarium ear blight on
wheat in central China. Ann Appl Biol 2014;164:384–395.
[78] Moschini RC, Pioli R, Carmona M, Sacchi O. Empirical predictions of wheat head blight in the
northern Argentinian Pampas region. Crop Sci 2001;41:1541–1545.
[79] De Wolf ED, Madden LV, Lipps PE. Risk assessment models for wheat fusarium head blight
epidemics based on within-season weather data. Phytopathology 2003;93:428–435.
[80] Rossi V, Giosuè S, Pattori E, Spanna F, Del Vecchio A. A model estimating the risk of Fusarium
head blight on wheat. Bull OEPP 2003;33:421–425.
108 | Antonio Moretti and Antonio F. Logrieco

[81] Del Ponte EMD, Fernandes JMC, Pavan W. A risk infection simulation model for fusarium head
blight of wheat. Fitopatol Bras 2005;30:634–642.
[82] Xu XM, Monger W, Ritieni A, Nicholson P. Effect of temperature and duration of wetness during
initial infection periods on disease development, fungal biomass and mycotoxin concentra-
tions on wheat inoculated with single, or combinations of, Fusarium species. Plant Pathol
2007;56:943–956.
[83] West JS, Holdgate S, Townsend JA, Edwards SG, Jennings P, Fitt BDL. Impacts of changing cli-
mate and agronomic factors on fusarium ear blight of wheat in the UK. Fungal Ecol 2012;5:
53–61.
[84] Xu XM, Nicholson P. Community ecology of fungal pathogens causing wheat head blight. Ann
Rev Phytopathol 2009;47:83–103.
Leif Sundheim and Trond Rafoss
6 Fumonisin in maize in relation to climate change

6.1 Introduction

In 1904 the American plant pathologist Sheldon described Fusarium moniliforme

J. Sheld. from moldy maize, which was suspected of causing animal diseases in the
state of Nebraska, USA [1]. Fusarium moniliforme is today considered a synonym of
F. verticillioides (Sacc.) Nirenberg [2].

Fig. 6.1: Maize infected with Fusarium verticillioides. Photo: Hadush Tsehaye.

Maize infected with F. verticillioides was implicated in several human and animal
diseases in the twentieth century. Esophageal cancer of humans was associated with
consumption of maize infected with F. verticillioides in a region of South Africa [3].
Outbreaks of a serious horse disease, equine leukoencephalomalacia (ELEM), in
South Africa during the 1970s led to an intensified search for the causal agent, and
feeding trials with infected maize confirmed the suspicion that maize contaminated
with F. verticillioides resulted in ELEM in horses [4]. In 1988 South African scientists
from the “Programme on Mycotoxins and Experimental Carcinogenesis” (PROMEC)
isolated a toxin from F. verticillioides cultures which represented a new class of fungal
toxins. Gelderblom et al. named the toxin fumonisin [5], and Bezuidenhout et al.
published its chemical structure [6]. Marasas et al. demonstrated that fumonisin
B1 (FB1 ) caused ELEM in horses in South Africa [7], and Rheeder et al. reported on
higher levels of the fumonisins FB1 and FB2 in maize samples from areas with high
rates of human esophageal cancer than in areas with low rates of that cancer in the
110 | Leif Sundheim and Trond Rafoss

country [8]. Swine in the USA fed maize infected with F. verticillioides died of porcine
pulmonary edema and hydrothorax, and fumonisin B1 (FB1 ) was shown to be the
causal agent [9]. The high incidence of human neural tube defects in Texas, USA, was
associated with fumonisin-contaminated maize [10].
The fumonisins are grouped in A, B, C, and P series, and FB1 is the most common
and most toxic fumonisin. The members of the FB series have been most intensively
studied because of their toxicity and potential carcinogenicity. The highest levels of
FB1 toxin occur in moldy maize and maize-based food and animal feed [11]. Several
research groups have studied the phytotoxicity of FB1 . Naik et al. found no effect of
F. verticillioides on maize seed germination, emergence, and maize yield [12]. Doehlert
et al. reported that, while 100 ppm FB1 had no effect on germination of maize seed, the
toxin inhibited radicle elongation [13]. Lamprecht et al. found that fumonisins caused
dose-dependent reductions in shoot and root length and dry mass of maize and tomato
seedlings, and the authors concluded that FB1 was more phytotoxic to seedlings than
FB2 and FB3 [14].
The fumonisin FB1 was classified as a group 2B carcinogen (probably carcinogenic
in humans) in 1993 by the International Agency for Research on Cancer [15]. The asso-
ciation between consumption of fumonisin-contaminated maize and a high incidence
of human esophageal cancer in South Africa was one of the reasons for the classifica-
tion [8]. In Linxian County, a high-risk area for esophageal cancer in China, 80 maize
samples from local households contained high levels of fumonisins [16]. In Iran, ele-
vated fumonisin levels in maize have been reported in an area with high esophageal
cancer frequency [17].

6.2 Fumonisin-producing fungi

The teleomorph of F. verticillioides was described as Gibberella fujikuroi (Sawada)

Wollenw. in 1931 [18]. In currently accepted nomenclature, F. verticillioides is the
anamorph mating population A of G. fujikuroi [19]. In maize, F. verticillioides and
F. proliferatum (Matsush.) Nirenberg are the major fumonisin producers because both
species are widely distributed and yield high levels of the toxin [20]. Under optimal
conditions in vitro a selected strain of F. verticillioides produced 3 to 4 g of FB1 per kg of
culture material [21]. Following the elucidation of the structure of FB1 , the fumonisins
FB2 and FB3 were discovered, and these three are the major fumonisins in maize nat-
urally infected by F. verticillioides and F. proliferatum [20]. Only the FB series occurs
at significant levels in naturally contaminated maize in the field, while fumonisins
of the A, C, and P series are minor metabolites produced on synthetic media in the
laboratory [22].
A total of 15 Fusarium spp. are known to produce fumonisins [20, 23]. In addition
to F. verticillioides and F. proliferatum there are 13 known fumonisin producers within
the genus Fusarium [20]. Less than 50 % of the isolates from each of these 13 species
 6 Fumonisin in maize in relation to climate change | 111

have been shown to produce fumonisins [23]. Only trace amounts of fumonisins have
been reported from strains of F. andiyazi and F. pseudonygamai [20].
Fumonisin-producing species within the genus Fusarium:
– F. andiyazi Marasas, Rheeder, Lampr., K. A. Zeller, and J. F. Leslie
– F. anthophilum (A. Braun) Wollenw.
– F. dlaminii Marasas, P. E. Nelson, and Toussoun
– F. fujikuroi Nirenberg
– F. globosum Rheeder, Marasas, and P. E. Nelson
– F. napiforme Marasas, P. E. Nelson, and Rabie
– F. nygamai L. W. Burgess, and Trimboli
– F. oxysporum Schltdl.
– F. polyphialidicum Marasas, P. E. Nelson, Toussoun, and P. S. van Wyk
– F. proliferatum (Matsush.) Nirenberg
– F. pseudonygamai O’Donnell, and Nirenberg
– F. sacchari (E. J. Butler and Hafiz Khan) W. Gams
– F. subglutinans (Wollenw. and Reinking) P. E. Nelson, Toussoun, and Marasas
– F. thapsinum Klittich, J. F. Leslie, P. E. Nelson, and Marasas
– F. verticillioides (Sacc.) Nirenberg

In Denmark, Frisvad et al. discovered that the industrially important, saprophytic fun-
gus Aspergillus niger Thiegh. produced low levels of FB2 on synthetic media [24]. From
a collection of 180 industrial and non-industrial A. niger strains, as much as 81 % of the
strains produced FB2 , FB4 or FB6 [25]. One A. niger strain used for industrial citric acid
production yielded 3.3 ppm fumonisin in broth culture, while among 17 other black
Aspergillus species none produced fumonisin [25]. In Portugal, 270 A. niger strains
were isolated from 73 maize samples, and 39 % of the strains produced FB2 in vitro.
The mean in vitro FB2 production of A. niger strains obtained in three geographical
regions in Portugal were from 0.37 to 0.52 μg g−1 [26].

6.2.1 Biology of fungi producing fumonisin

Maize is the crop most often contaminated with fumonisin, but a limited number of
other crop plants and commodities may also contain the toxins [27, 28]; see Fig. 6.1.
The major fumonisin producers F. verticillioides and F. proliferatum are important
maize pathogens causing seedling blight, root rot, stalk rot, and ear rot [28–30].
Munkvold et al. compared methods for inoculation of maize plants with F. verticil-
lioides strains labeled as nitrate-nonutilizing (nit) mutants [31]. Seed inoculation
resulted in systemic infection of plants and kernels, but local inoculation of the silks
resulted in more kernel infection than systemic growth of the fungus from infected
kernels [31].
112 | Leif Sundheim and Trond Rafoss

Survival of F. verticillioides in the field has not been studied to the same extent as
for other Fusarium spp. In most countries maize is grown in fields where the crop was
cultivated the previous year or in short rotations with other crops. Studies by Cotton
and Munkvold demonstrated that F. verticillioides survives in maize stalks in the field
for at least 630 days, and survival after one year in maize stalks buried 30 cm deep was
equivalent to survival on the soil surface [32]. Fusarium verticillioides and F. prolifer-
atum rarely develop perithecia, but they produce large amounts of microconidia and
macroconidia, which are the most important inoculum for the fungi [28, 30].
Systemic infection by F. verticillioides in maize was first studied by Foley [33]. He
isolated the fungus from symptom-free stalks, leaf sheaths and axillary buds. Isolation
frequency was highest from leaf sheaths, and successful isolations of F. verticillioides
from nodes were more frequent than isolation from internodes of maize [33]. The endo-
phytic growth of F. verticillioides was further investigated by Munkvold et al. [34]. They
inoculated seeds and followed transmission of the fungus to stalks and developing
kernels. In three field experiments seed infection had no significant effect on the per-
centage of crown, stalk, and kernel infected by F. verticillioides [34]. Silk inoculation
with the fungus was the only method which significantly increased kernel infection,
and on individual ears up to 100 % of the kernels became infected. The mean result
from silk inoculation was 83.7 % infected kernels [34]. In a controlled environment
F. verticillioides developed more rapidly at high temperature than at moderate tem-
perature during the vegetative stage, but temperature did not affect the incidence of
kernel or ear infection [35]. Three F. verticillioides strains, which were transformed with
the gusA reporter gene, maintained their ability to infect maize, and the transformed
strains facilitated study of the endophyte-maize relationship [36]. Mycelia with GUS
(β-glucuronidase) activity were recovered from roots on maize seedlings developing
from kernels infected with isolates carrying the gusA gene [36].
Both the fumonisin-producing F. verticillioides and the DON-producing F. gramin-
earum are common maize pathogens, and the two fungi frequently compete in
maize plants. Reid et al. inoculated maize ears with mixtures of F. verticillioides and
F. graminearum, and DNA analysis revealed that F. verticillioides had the greater
growth rate of the two pathogens [37]. The FB1 level was not different when the two
fungi were applied together to when F. verticillioides was applied alone [37]. Based on
single, mixed, and sequential inoculations with the two fungi Picot et al. concluded
that previous contamination by F. graminearum can facilitate subsequent infection by
F. verticillioides [38]. In southern Europe F. verticillioides and F. proliferatum frequently
occur in maize [39].
Both environmental factors and maize genotype determine infection by fumon-
isin-producing Fusarium spp. and accumulation of the mycotoxin in maize. Field tri-
als with 15 maize genotypes at 17 locations in the USA revealed a highly significant
hybrid × location interaction [40]. The mean fumonisin content in the maize hybrids
varied from 0.5 to 48.5 μg g−1 , and there was an increase in fumonisin content as the
latitude of the location decreased [40]. Desjardins and Plattner inoculated maize with
 6 Fumonisin in maize in relation to climate change | 113

F. verticillioides strains with different fumonisin production potential to study interac-

tion in field experiments [41]. There was no consistent difference in fumonisin content
of maize following inoculation with low fumonisin-producing strains and inoculation
with strains with high fumonisin production [41]. Doko et al. determined fumonisin
levels in 26 maize genotypes grown in three European and two African countries, and
found a positive correlation between high FAO maturity class of the genotype and fu-
monisin contamination [42]. To develop methods for F. verticillioides inoculation of
maize in a breeding program, Clements et al. compared injection of inoculum through
the ear husk leaves, spray inoculum twice on the silk with ear subsequently covered
by a bag, and insertion of toothpicks infected with F. verticillioides [43]. Only injection
through the husk leaves significantly increased severity of Fusarium ear rot and the
concentration of fumonisin in grain compared to the control [43].

6.3 Fumonisin accumulation in developing maize kernels

In field trials with three maize hybrids at two locations in North Carolina, USA, Bush
et al. sampled maize kernels weekly to follow F. verticillioides infection and FB1 accu-
mulation [44]. FB1 contamination appeared as kernels neared physiological maturity
four weeks after pollination and increased up to the harvest date. Peak FB1 content
varied from 5 to 10 μg g−1 in the hybrids [44]. The authors suggested that early maize
harvest at > 25 % grain moisture may reduce the level of fumonisin contamination in
years with heavy infection [44].
In Japan Uegaki et al. studied the increase in fumonisin concentration during
growth of the maize plant [45]. Maize planted in the field in mid-May was sampled ev-
ery two weeks from mid-June. The fumonisin concentration in maize kernels increased
abruptly after the dough-ripe stage and kept increasing until the full-ripe stage [45].
The mean concentration of FB1 in the ears exceeded 80 % of final fumonisin content in
mid-September, and continued to increase to the full ripe stage in late October, when
the mean concentration was 2.3 μg g−1 [45].
In field trials at two locations in France maize was inoculated with F. verticillioides
four days after silking [46]. Samples for F. verticillioides DNA and fumonisin (FB1 , FB2 ,
and FB3 ) analysis were collected at intervals. Fungal DNA was detected seven days
after inoculation, while fumonisin was first detected 15 days after inoculation and con-
tinued to increase up to 42 days after inoculation. The authors concluded that the dent
stage is the most significant period for fumonisin biosynthesis in maize kernels [46].

6.3.1 Fumonisins are not required for pathogenicity

The F. verticillioides genome has been partly sequenced. The fumonisin biosynthesis
cluster of the genome consists of several FUM genes which are required for fumon-
114 | Leif Sundheim and Trond Rafoss

isin biosynthesis [47]. There are 17 FUM genes known, and evidence for epigenetic
regulation of FUM genes in F. verticillioides was presented by Visentin et al. [48]. Fu-
monisin accumulation correlates with the amount of transcript from the key genes,
FUM1, FUM21, and FUM8 [48].
Proctor et al. developed fumonisin nonproducing mutants which were virulent on
maize [49]. Transformation of the FUM5 gene into a fumonisin nonproducing mutant
restored fumonisin production, and disruption of the FUM5 gene reduced fumonisin
production by 99 % [50]. Fusarium verticillioides strains which produced only one of
the fumonisins (FB1 , FB2 , or FB3 ) and a fumonisin nonproducing strain did not lose
their ability to cause ear rot of maize [51]. Desjardins and Plattner concluded that these
results indicate that loss of fumonisin production does not affect the ability of F. ver-
ticillioides to cause maize ear rot [51].

6.3.2 Insect damage increases risk of fumonisin contamination

Several insect species are serious pests on maize ears. In USA, the European corn borer
(ECB; Ostrinia nubilalis) larvae develop in the stalks and ears of maize. The first gener-
ation infests plants during the vegetative stage, while adults of the second generation
lay egg masses on leaf surfaces, and the larvae feed on leaves, stalks, and ears [52].
Maize hybrids were genetically modified to express Bacillus thuringiensis genes
coding for the CryIAb protein, which give a high level of resistance to feeding by ECB
larvae. In field trials conducted over three years Munkvold et al. found that trans-
gene maize hybrids expressing the CryIAb protein in kernels had less Fusarium ear rot
compared to near-isogenic hybrids lacking the cryIAb gene [53]. In an area of France
where maize was regularly infested with ECB and a maize borer (Sesamia nonagri-
oides), Folcher et al. found 90 % reduction in concentration of fumonisin in maize ge-
netically modified for resistance to ECB compared to nonmodified isogenic lines [54].
The CryIAb protein is not effective against the Western bean cutworm (WBC; Stria-
costa albicosta), corn earthworm (CEW; Helicoverpa zea) and some other Lepidopteran
maize pests [55]. In field trails in Iowa, USA, Bowers et al. planted maize hybrids genet-
ically modified to express both the ViP3Aa protein and the CryIAb protein for protec-
tion against several Lepidopteran pests. Natural infestation by WBC, ECB, and CEW
was the treatment in the experiments [55]. The insect damage was reduced and the
mean fumonisin content was 0.56 μg g−1 in maize hybrids expressing the two proteins
CryIAb and ViP3Aa, while the mean fumonisin contamination of nontransgenic maize
hybrids was 5.47 μg g−1 [55].
Insect infestation may be stimulated by F. verticillioides infection. In inocula-
tion experiments at the International Institute of Tropical Agriculture (IITA), Nige-
ria, Cardwell et al. found that F. verticillioides-inoculated maize had higher levels of
Coleopteran beetles and Lepidopteran borers than non-inoculated maize [56].
 6 Fumonisin in maize in relation to climate change | 115

6.3.3 Small grain cereals contaminated with fumonisins

Fusarium spp. cause ear rot, stalk rot, and yield losses in sorghum (Sorghum bicolor)
and pearl millet (Pennisetum glaucum), but fumonisin contamination of these African
staple food crops has been less studied than in maize. Leslie et al. determined fumon-
isin production in five strains of each of five Fusarium spp. isolated from sorghum
and pearl millet grown in Africa and Australia [57]. The two species, F. nygamai and
F. verticillioides, produced high levels of FB1 and FB2 , while strains of F. andiyazi, F.
pesudonygamai, and F. thapsinum yielded only low levels or no fumonisins [57].
In a two-year survey of durum wheat in Italy, Palacios et al. found F. proliferatum
to be the most common Fusarium species, with infection frequencies ranging from
8 % to 66 % [58]. During the 2007 season the fumonisin contamination (FB1 + FB2 )
levels varied from 0.01 to 1.25 μg g−1 , while only very low levels were detected in sam-
ples from 2008 [58]. Desjardins et al. reported that in wheat grown in Nepal, kernel
black point disease and fumonisins were associated with F. proliferatum strains [59].
In inoculation experiments F. proliferatum reduced yield, and one strain obtained from
wheat grown in Nepal produced 49 μg g−1 of fumonisins (FB1 , FB2 , and FB3 ) on wheat
[59]. When Busman et al. analyzed wheat samples with wheat kernel black point dis-
ease from across the USA, most samples did not contain fumonisins above the level
of detection (LOD), while low levels of fumonisins were detected in 9 of 43 samples
[60]. Five samples contained > 0.05 μg g−1 (FB1 , FB2 , and FB3 ), including one sample
with 2.2 μg g−1 and one sample with 1.2 μg g−1 (FB1 , FB2 , and FB3 ) [60]. Fusarium pro-
liferatum was the dominant Fusarium species,but the low levels of fumonisin in the
samples provided evidence that fumonisins are not likely to contribute to the ability
of Fusarium spp. to cause kernel black point disease of wheat in USA [60].
Thailand is the leading rice export country in the world. In a survey, Tansakul
et al. analyzed unpolished samples of Thai red cargo rice from the retail market, and
only 2 of 58 samples were found to be contaminated with fumonisins above LOD, both
with only trace levels (< 5.0 ng g−1 ) of FB1 , and no FB2 [61]. Two years’ analysis of rice
samples sold in Canada which originated from several countries including the USA,
Canada, Pakistan, India, and Thailand revealed fumonisins in 15 of 99 samples the
first year, and in 1 of 100 samples the second year [62]. The average concentration of
FB1 was 4.5 ng g−1 in the positive samples. In addition, FB2 and FB3 were detected in
concentrations of > 1 ng g−1 [62].

6.3.4 Other crops and commodities contaminated with fumonisins

Noonmin et al. detected FB2 in coffee bean samples of Coffea arabica and C. canephora
grown in Thailand [63]. No Fusarium species known to produce fumonisin were iden-
tified in the coffee, but strains of Aspergillus niger isolated from the coffee beans pro-
duced low levels of FB2 and FB4 in a culture medium [63]. Very low levels of FB2 (1.0–
116 | Leif Sundheim and Trond Rafoss

9.7 ng g−1 ) were detected in seven of twelve coffee bean samples analyzed [63]. All of
the 50 randomly selected strains of F. proliferatum isolated from asparagus crowns in
China produced FB1 and FB2 in maize grain cultures and on asparagus spear extracts,
and FB3 was isolated from most of the culture extracts as well [64]. Marín et al. did in-
oculation experiments on edible pine nuts (Pinus pinea) with eleven strains of F. prolif-
eratum isolated from pine nuts, and identified six strains which produced fumonisins
in shelled pine nuts and two strains which produced fumonisins in whole pine nuts
[65]. The FB1 levels in inoculated pine nuts varied from 0.10 to 0.69 μg g−1 [65].
Stratakou et al. conducted a survey to determine the level of mycotoxins in Euro-
pean grapes and wines, reporting on frequent occurrence of low levels of fumonisins
in European wine [66]. Logrieco et al. analyzed 51 market samples of Italian red, white,
and rosé wines, and reported that 9 of the 45 red wine samples contained FB2 at levels
ranging from 0.4 to 2.4 ng ml−1 , while FB4 was not detected in any of the samples [67].
Mogensen et al. analyzed 77 wine samples from 13 countries, and 23 % of the sam-
ples contained FB2 in the range of 1 to 25 ng ml−1 [68]. Powdery mildew caused by
the fungus Erysiphe necator is one of the most common grape diseases. Damage to
the berry surface by powdery mildew infection was identified as an infection site for
strains of A. niger producing FB2 in grapes [69]. Black Aspergillus strains were isolated
from grapes in Argentina, and fumonisin production was assessed on a Czapek yeast
medium. The only strains able to produce fumonisins were five A. niger strains, while
strains of A. carbonarius, A. japonicas, and A. tubingensis did not produce fumonisins
on the medium [70].
The fumonisins are water soluble and withstand the beer production process,
which includes malting, mashing, boiling, and fermentation. In a survey of 29 do-
mestic and imported beer brands marketed in the United States, 86 % contained FB1
and 41 % contained FB2 [71]. The total fumonisins (FB1 and FB1 ) varied from 0.3 to
12.7 ng ml−1 , with a mean concentration of 4.0 ng ml−1 in positive samples [71]. Sam-
ples of home brewed beer in South-Africa all contained fumonisins (FB1 , FB2 and FB3 ),
and the mean concentration was 0.37 μg ml−1 (range 0.04–1.33 μg ml−1 ; [72]). Transfer
of FB1 from naturally contaminated malted barley and maize grit to beer was studied
by Pietri et al. in Italy (73]. Beer production based on maize grit contaminated with 1.1
to 3.2 μg g−1 FB1 was followed, and the measured concentrations of FB1 in the brewed
beer varied from 37 to 89 ng ml−1 , while FB2 was not found in the beer samples [73].

6.4 Geographical distribution of fumonisins in maize

Maize is widely grown in tropical, subtropical, and temperate climates, and cultivation
of the crop is expanding. The yield potential has increased, and the current maize
harvest weight is larger than any other cereal crop. In maize growing countries the
crop is commonly contaminated with fumonisin [22].
 6 Fumonisin in maize in relation to climate change | 117

6.4.1 Africa

Fandohan et al. reviewed the fumonisin situation for maize in Africa [74]. While maize
is an important crop in Africa, only limited information on fumonisin contamination
is available, except for South Africa, and there is a need for increased monitoring of
maize in the continent [74].
The mycotoxin situation of food crops in Sub-Saharan Africa was summarized by
Bankole et al., who concluded that fumonisins are the most important Fusarium myco-
toxins in Sub-Saharan Africa [75]. Maize fumonisin contamination is widespread in
West Africa, and contamination levels are frequently high. Maize samples from Nige-
ria had an FB1 incidence of 78.6 % and a concentration range of 0.07 to 1.78 μg g−1 ,
with a mean concentration of 0.50 μg g−1 , while FB2 was detected in 66 % of the sam-
ples with a mean concentration of 0.11 μg g−1 [76]. All 32 maize samples collected on
maize farms in Burkina Faso contained fumonisin in the range of 0.11 to 3.12 μg g−1 ,
and the mean fumonisin content was 1.17 μg g−1 [77]. Analysis of 72 maize samples
from a large Burkina Faso market revealed a 100 % fumonisin incidence and a mean
contamination of 2.90 μg g−1 with a range of 0.13 to 16.04 μg g−1 [77]. Fusarium verticil-
lioides, with an incidence of 68 %, and F. proliferatum, with an incidence of 31 %, were
the most common Fusarium spp. isolated from maize in Benin, and the FB1 and FB2
levels varied from LOD to 6.7 μg g−1 [78]. Maize was analyzed at harvest and during
storage in different regions of Benin. The fumonisin levels were lowest in the Sudan
Savannah region [78]. Rice, maize, and groundnuts were analyzed in Côte d’Ivoire for
mycotoxins, but only low levels of fumonisin were detected [79].
Ethiopian scientists analyzed barley, wheat, sorghum, and teff (Eragrostis tef ) for
mycotoxins, but only detected fumonisins in sorghum samples, and the maximum
concentration was 2.12 μg g−1 [80]. Maize is the major cereal crop in Uganda and an
important export commodity. Fusarium and fumonisins in maize grain stored in tradi-
tional structures were analyzed by Atukwase et al., who found that all maize samples
analyzed contained fumonisins in the range of 0.27 to 10.0 μg g−1 [81]. The Fusarium in-
cidence level increased after harvest from 61.9 % to 77.5 % during the first two months
of storage and then decreased to 31.9 % after sixth months of storage in Uganda [82].
Fumonisin levels decreased at one site in Uganda from an average of 5.7 μg g−1 at har-
vest to 2.8 μg g−1 after six months of storage [82].
In Kenya F. verticillioides is the dominant cause of maize ear rot [83]. 70 isolates of
F. verticillioides were obtained from maize samples collected in the important maize
growing regions of the country, and in vitro 74 % of the isolates produced fumonisin
B1 in the range of 0.07 to > 5.0 μg g−1 , with a mean of 1.51 μg g−1 [83]. Analysis of 20
inbred maize lines from Zambia gave a median concentration of 0.10 μg g−1 (FB1 and
FB2 ) with a variation from 0.02 to 1.71 μg g−1 (FB1 and FB2 ) [42]. In field experiments
in Zambia with maize hybrids artificially inoculated with F. verticillioides, the mean
concentration content of (FB1 and FB2 ) was 0.67 μg g−1 in the harvested maize, with a
variation from LOD to 13.05 μg g−1 (FB1 and FB2 ) [84]. A survey in Zambia suggested
118 | Leif Sundheim and Trond Rafoss

that subsistence farmers and consumers might be exposed to dangerous levels of fu-
monisins, as in six districts the concentration was ten times higher than the level rec-
ommended by FAO/WHO [85]. Maize samples in Egypt were analyzed for fumonisin
over a period of two years. The mean FB1 content for the 2012 samples was 0.5 μg g−1
and 0.98 μg g−1 for the 2013 samples. The range of FB1 content in the samples was 0.17
to 1.9 μg g−1 [86].

6.4.2 Europe

The maximum level of fumonisins in the EU is regulated by the Commission Regula-

tion (EC) No 1126/2007 at 2.0 μg g−1 (FB1 and FB2 ) for unprocessed maize, 1.0 μg g−1
(FB1 and FB2 ) for maize flour, maize meal, maize grits, maize germ, and refined maize
oil, 0.4 μg g−1 (FB1 and FB2 ) in maize-based food intended for direct human consump-
tion, and 0.2 μg g−1 (FB1 and FB2 ) in processed maize-based foods and baby foods for
infants and young children [87]. Visconti and Doko assayed fumonisin production in
28 strains of F. verticillioides and one strain of F. proliferatum from Italy, Spain, and
France, and found that all strains produced FB1 [88]. Logrieco et al. reported that the
fumonisin-producing species F. verticillioides and F. proliferatum are commonly iso-
lated from maize ear rot in southern Europe [39]. Up to 80 % of ears damaged by the
corn borer (Pyralis nubilalis) are infected [39]. Ariño et al. did not find any difference
in fumonisin content between tillage systems, type of irrigation, and harvest date in
Spain, while higher levels of nitrogen fertilizers tended to increase fumonisin content
in maize and cultivation of insect resistant varieties reduced fumonisin levels [89].
Binder et al. found fumonisin in 19 of 26 maize samples analyzed from Europe, with a
median fumonisin concentration of 0.43 μg g−1 [29]. Ivic et al. isolated F. verticillioides
from barley grain in Bosnia and Herzegovina, but the average FB1 content in barley
grain was very low, with an average of 2.40 ng g−1 , with a range of 1.01 to 5.35 ng g−1
in the samples analyzed [90].
The incidence of F. verticillioides and F. proliferatum is commonly low in the maize
growing countries of central and northern Europe [91]. Van Asselt et al. presented data
from mycotoxin monitoring in silage maize from the Netherlands, Belgium, Germany,
and France during the period 2003–2007 [91]. High fumonisin concentrations were
found in 2003 and 2007, indicating of suitable conditions for infection by F. verticil-
lioides and F. proliferatum in Western Europe in two of five recent years. The mean fu-
monisin contents of positive samples were 1.55 μg g−1 in 2003 and 0.84 μg g−1 in 2007,
demonstrating that west European maize crops may contain fumonisin above the EU
maximum level of 2.0 μg g−1 [87, 91]. No fumonisin was detected in 12 samples in 2005
and only very low levels in 2004 and 2006 [91]. In France maize products in horse feed
led to two cases of ELEM in the region of Toulouse, and Bailly et al. analyzed the feed
and found that it contained 125 μg g−1 FB1 [21].
 6 Fumonisin in maize in relation to climate change | 119

Maize is currently cultivated for silage in Denmark and in the Baltic states. Even
in the best climatic zones of Norway, Sweden, and Finland growers have successfully
grown maize during recent years. The species F. verticillioides and F. proliferatum were
not detected in a recent Danish survey [92]. Higher temperatures will stimulate more
maize cultivation, and warmer climate may increase the risk for fumonisin contami-
nation in maize by F. verticillioides in the Nordic and Baltic countries [93].

6.4.3 South America

An outbreak of ELEM in the Buenos Aires province, Argentina, in 2007 was caused
by contaminated maize. The dead horses had the symptoms of ELEM, and analyses
revealed a content of 12.49 μg g−1 FB1 and 5.25 μg g−1 FB2 in the horse feed [94]. Fu-
monisins were determined in maize samples from the Entre Rios Province, Argentina,
for two consecutive years, and in 2003 a total of 14 samples were analyzed. The me-
dian fumonisin content of the 12 positive samples was 5.80 μg g−1 , while seventeen
samples were analyzed in 2004 and the median content of the 12 positive samples was
2.40 μg g−1 [95]. The maximum level detected was 34.70 μg g−1 [95]. Ono et al. detected
fumonisins in 98 % of 150 samples from maize 62 hybrids in Brazil, and 62 % of the
samples had < 5.0 μg g−1 [96]. Fumonisin contamination was higher in maize samples
originating in the northern and central western regions than in those from the central
southern region of Brazil [96]. Stumpf et al. analyzed 29 maize kernel samples form
the Rio Grande do Sul state of Brazil. FB1 was detected in 58.6 % and FB2 was detected
in 37.9 % of the samples. The mean FB1 level was 0.66 μg g−1 , and the mean FB2 level
was 0.42 μg g−1 [97].

6.4.4 North America

Shelby et al. concluded that fumonisin risk is highest in the southern USA states [40].
A significant negative correlation between latitude and fumonisin contamination was
found in trials with the same genotype at 17 locations in the country. The mean total
fumonisin contamination of the hybrids ranged from 5.8 to 48.5 μg g−1 . Maize from the
southern and central states up to Iowa, Illinois, and Kansas was more contaminated
than maize from the upper mid-western states [40]. Hooker and Schaafsma analyzed
fumonisin content of maize from Ontario, Canada, over eight years. The FB1 concen-
tration at maturity was highly variable between fields and from year to year. Between
17 % and 56 % of the maize samples contained > 1.0 μg g−1 FB1 over the years. Based
on the analytical data the authors concluded that maize hybrid was more important
for fumonisin contamination than climatic variation between years in Canada [98].
Fusarium species of the Gibberella fujikuroi complex from pearl millet and maize
grown in Georgia, USA, were studied by Jurjevic et al. [99]. Of the crosses between pearl
120 | Leif Sundheim and Trond Rafoss

millet isolates of Fusarium spp. and F. verticillioides, 50.4 % were successful, and when
crossed with F. proliferatum 10.1 % of the crosses succeeded [99]. The percentages of
maize isolates compatible with F. verticillioides ranged from 70.2 % to 89.5 %. When
maize samples collected in the survey over three years were analyzed, between 63 %
and 91 % of the samples contained fumonisins, and the fumonisin levels ranged from
0.6 to 33.3 μg g−1 , while FB1 and FB2 were not detected in any of the 81 pearl millet
samples [99]. Wu et al. maintained that the risk for fumonisin contamination is greater
in warm and relatively dry areas of lower latitudes and altitudes than in cooler and
more humid climates in high latitudes and altitudes [100].

6.4.5 Asia

Binder et al. analyzed maize samples from 10 countries in Asia and two countries of
Oceania, and fumonisins were detected in 69 % of 309 maize samples [29]. The average
fumonisin concentration in maize was 1.34 μg g−1 , and the median fumonisin concen-
tration was 0.53 μg g−1 [29]. The highest fumonisin concentration was determined in a
maize sample from China with 14.71 μg g−1 fumonisin [29]. Only 4 of 98 wheat samples
were contaminated with fumonisin, with a median concentration of 0.24 μg g−1 , and of
122 soybean meal samples only 9 contained fumonisin with a median concentration
of 0.26 μg g−1 [29]. Wei et al. analyzed FB1 and FB2 in maize samples originating in
four provinces of China [101]. In 307 maize samples the incidence of fumonisins (FB1
and FB2 ) varied from 31.5 % in the Gansu province to 81.1 % in the Shandong province.
The average (FB1 and FB2 ) concentration was 0.70 μg g−1 and the range was from ≤0.01
to 13.11 μg g−1 . Seventeen of the 307 samples had higher fumonisin content than the
current EU-regulated maximum level for human consumption [101].
Very high fumonisin levels in maize were reported from areas with a high risk
of esophageal cancer in the Golestan Province, Iran [16]. The mean FB1 concentra-
tion in 66 maize samples was 223.64 μg g1 , and the mean FB1 concentration in 66 rice
samples was 21.59 μg g1 .There was a significant, positive correlation between risk of
esophageal cancer and fumonisin content and rice grown in this region, but the au-
thors did not find a significant correlation between fumonisin content of maize and
risk of esophageal cancer [17]. Azizi and Rouhi analyzed biscuits and cookies obtained
from supermarkets in Babol City, Iran for fumonisins [102]. All of the 30 biscuit and
cookie samples contained fumonisins above the LOD. 28 contained < 2 μg g−1 total fu-
monisin, and 2 samples contained > 2 μg g−1 fumonisin with 2.3 μg g−1 total fumonisin
the highest level recorded [102]. In a Japanese study of maize the mean concentration
of FB1 was 2.31 μg g−1 at the full ripe stage. [45]. In Vietnam 8 of 25 samples of maize
for human consumption were contaminated with FB1 , and the level ranged from 0.4
to 3.3 μg g−1 [103].
 6 Fumonisin in maize in relation to climate change | 121

6.5 Climate change predicted by IPCC

The Intergovernmental Panel on Climate Change (IPCC) concluded in its 2013 re-
port that the troposphere has warmed since the mid-20th century [104]. There is
medium confidence in the rate of global warming in the Northern Hemisphere and
low confidence elsewhere. IPPC has medium confidence that the projected increase
in global mean surface temperature during the next twenty years will be in the range
of 0.3–0.7 °C [104]. According to IPPC there will be an increase in global mean surface
temperature for the period 2081–2100 relative to 1986–2005 [104]. IPCC has very high
confidence that the Arctic region will warm more rapidly than the global mean, and
the mean warming over land will be larger than over ocean. It is virtually certain
that there will be more frequent hot and fewer cold temperature extremes over most
land areas on daily and seasonal timescales as the global mean temperature increases
[104]. IPPC concluded that there is high confidence that global warming has increased
crop production in some high latitude regions in China and Europe [104]. For maize
and other major crops temperature increases of 2 °C or more above late 20th century
levels without adaptation will negatively impact maize production in tropical and
temperate regions [104].
According to the IPPC precipitation has increased since 1901 in the Northern
Hemisphere, and high latitudes are likely to experience an increase in precipita-
tion by the end of this century [104]. Confidence in precipitation changes averaged
over global land areas since 1901 is medium prior to 1951 and high afterwards. Area-
averaged long-term positive or negative precipitation trends have low confidence for
other latitudes [104]. The frequency or intensity of heavy precipitation has increased in
North America and Europe. Confidence in changes in precipitation is at most medium
in other continents [104].
IPPC concluded that the level of CO2 in the atmosphere has increased in the last
three centuries. From an estimated concentration of 280 ppm CO2 in the atmosphere
around 1750, the concentration had increased to 391 ppm CO2 by 2011 [104]. According
to the IPPC, man-made emissions are projected to further increase CO2 in the atmo-
sphere [104].

6.5.1 Climate effects on fungi producing fumonisin in maize

While maize production has doubled over the last 40 years, the percentage of loss due
to plant pests in the crop has not changed much, amounting to almost one third of
attainable yield during the period 2001–2003 [105]. Coakley et al. concluded that the
effects of climate change may differ depending on the global location [106]. The rates
of pathogen development may change and the physiology of host-plant interaction
may be altered. The effects of climate change on plant disease management may be
122 | Leif Sundheim and Trond Rafoss

less important than changes in land-use patterns, transgenic technologies, and avail-
ability of chemical pesticides [106].
De la Campa et al. used fumonisin analysis data of maize grown in Argentina and
the Philippines to develop a model for the effects of climate, insect damage, and hy-
brid maize on fumonisin contamination at harvest [107]. The fumonisin content varied
from 0.3 to 12.0μg g−1 in the data from Argentina and from 0.3 to 1.8 μg g−1 in the data
from the Philippines. Weather or location explained 47 %, insect damage severity in
mature ears explained 17 %, and hybrid explained 14 % of the variability in fumonisin
contamination [107]. Schaafsma and Hooker analyzed maize grown in the province
of Ontario, Canada, and concluded that weather accounted for 19 % of the variation
in fumonisin contamination [108]. The levels of fumonisin in Canadian maize were
rather low, as only 17 % to 56 % of the maize samples contained > 1.0 μg g−1 fumon-
isin. Schaafsma and Hooker emphasized that the Fusarium-crop interaction is more
complex in maize than in wheat because of the variations in the maize flowering pe-
riod, the important role of insect damage for the Fusarium infection in maize, and the
rapid turnover in maize genotypes [108].

6.5.2 Effects of temperature

Marin et al. determined the optimum in vitro temperature for growth of F. verticillioides
and F. proliferatum, and when growth at 25 °C and 30 °C was compared, F. verticillioides
grew faster at 30 °C than at 25 °C, while 25 °C was the optimum temperature for growth
of F. proliferatum [109]. Growth of the two fungi was determined over a range of tem-
peratures from 5 °C to 40 °C on sterile layers of maize, and the optimum temperature
for growth was 30 °C for both F. verticillioides and F. proliferatum [110]. Based on evalu-
ation in 36 environments in Spain, Cao et al. found that high temperature during flow-
ering increased fumonisin content of maize kernels, while ear damage by corn borer
and hard rainfall favored fumonisin accumulation in the kernel drying period [111].

6.5.3 Effects of drought

The IPCC concluded that precipitation will increase at higher latitudes, but in the
major maize producing areas of the world precipitation will not compensate for the
temperature-driven increase in evaporation, which will result in more droughts for
most maize producing countries [104].
Water activity (a w ) is a measure of available water in the substrate. Free water has
a water activity of 1.0 a w , which also characterizes 100 % relative humidity. Marin et al.
concluded that in vitro water availability of 0.994–0.98 a w is optimal for fumonisin
production by F. verticillioides [109]. At temperatures that were not optimal for fungal
growth fumonisin production is higher at lower a w values. Maize starch production
 6 Fumonisin in maize in relation to climate change | 123

in the kernels decreases water availability in the late phase of maturation [112]. Ju-
rado et al. reported that a w of 0.937 reduced growth of F. verticillioides, but increased
expression of the FUM1 gene [112]. Thus, water stress may be an important factor for
fumonisin accumulation in the final phase of maize kernel development [112]. Marín
et al. concluded that water stress resulted in an induction of the FUM1 gene in F. verti-
cillioides, but F. proliferatum showed a stable expression of the FUM1 gene regardless
of water potential [113].
Based on two years of field trials in four different states of the USA, Parsons and
Munkvold concluded that dry weather after pollination and thrips infestation of the
ears increased the risk for fumonisin contamination [114]. Wu et al. concluded that in
North-America fumonisin risk is higher in Texas and the south-eastern states than in
central USA, but the fumonisins are the most common mycotoxins in all the corn belt
states of the USA [100]. In Central and South America and Southeast Asia the risk for
fumonisin contamination of maize is higher in lower elevation maize production areas
than in maize produced at higher elevations [100]. There has been an increase in maize
cultivation in southern and central Europe, and a northward expansion of maize cul-
tivation in Europe has been predicted with the projected climate changes [115].
Shelby et al. did field experiments in the 11 major maize producing states of the
USA, and mean fumonisin content for 15 hybrids varied from 0.5 to 48.5 μg g−1 at the
different locations [40]. June precipitation was negatively correlated with fumonisin
content, and June rainfall was the most important factor for the fumonisin levels of
maize hybrids in the USA [40]. Drought just prior to pollination creates physiological
stress for the maize plant, which is likely to create good conditions for infection and
fumonisin production by Fusarium spp. [40].
The effect of water deficit on accumulation of FB1 and FB2 in maize was studied
in the state of São Paulo, Brazil [116]. 35 cultivars were planted at three locations and
sampled for fumonisin analysis during two seasons. All samples were contaminated
with fumonisins with a content of FB1 from 0.10 to 43.80 μg g−1 , and the FB2 content
varied from 0.04 to 11.65 μg g−1 . Fumonisin concentration was negatively correlated
with precipitation in the period from silking to kernel milky stage [116]. Precipitation
in the month before harvest increased the fumonisin content of the maize crop. In the
period from maturity to harvest there were positive correlations between fumonisin
concentration and precipitation and between water surplus in the soil and fumonisin
concentration [116]. 92 % of samples analyzed in the northern region of Brazil had
a fumonisin content > 1.0 μg g−1 , while only 18.5 % of the samples from the central
southern region were contaminated with a fumonisin content > 1.0 μg g−1 [117]. Precip-
itation in the month preceding harvest in the southern region was 92.8 mm, whereas
the northern region had 202 mm precipitation in the month before harvest [117].
Schjøth et al. did field experiments with maize in Zambia in the high rainfall zone
(HRZ), which has an annual precipitation of 1000–1500 mm, and in the medium rain-
fall zone (MRZ) with an annual precipitation of 800–1000 mm [84]. Three commercial
maize hybrids were inoculated by a mixture of six isolates of F. verticillioides obtained
124 | Leif Sundheim and Trond Rafoss

from Zambian maize at both sites. Combined FB1–2 concentration varied from LOD
to 13.05 μg g−1 , with an overall mean concentration of 0.7 μg g−1 . Maize from the HRZ
had a low incidence of FB1–2 positive samples (mean 41 %) which all, apart from one,
contained FB1–2 < 0.5 μg g−1 . There was a higher incidence of FB1–2 positive samples
(mean 97 %) in the MRZ, and higher concentrations (40 % of the samples > 1.0 μg g−1 )
were recorded [84].
Studies by Herrera et al. in Spain showed that water activity of the grain at above
0.93 a w (20.0 % grain moisture) was the critical condition for fumonisin production in
mature grain [118]. The frequency of fumonisin detection in field samples was 48.3 %,
and the positive samples contained from LOD to 5.82 μg g−1 fumonisin. High tempera-
ture during flowering combined with wet weather in the last month preceding harvest
were the most important factors for fumonisin contamination of maize [118].

6.5.4 Effects of elevated CO2 level

Fungi can tolerate increased CO2 and the predicted levels of 800–1000 ppm CO2 may
not limit growth of fungi producing mycotoxins in crops [119]. Plant anatomy may be
altered with increased CO2 concentration in the ambient air [120]. Greater leaf thick-
ness and more leaves per plant are noted when plants are grown in elevated CO2
environments. Increased leaf growth results more often from increased cell expan-
sion than from increased cell division. Crop plants exhibit greater leaf thickness than
leaves from wild plant species when grown at increased CO2 concentration [120].

6.6 Conclusions on the effect of climate change on fumonisin

Maize is commonly contaminated with fumonisin. Predicting climate change effects

on fumonisin in maize is challenging, since the mycotoxin is an end product of the in-
teraction between two living partners: the maize plant and the fungus parasitizing the
host plant and synthesizing fumonisin in the maize kernels. The Fusarium spp. which
produce fumonisin in maize are known in all continents where the crop is cultivated.
In the temperate climates of Asia, Europe, and North America the risk for fumonisin
contamination is highest at lower altitudes and latitudes. In tropical and subtropi-
cal countries the latitude is less important. The risk for fumonisin contamination is
lower at high altitudes than in the lowlands of the tropical and subtropical countries
of Africa, Asia, and South America.
The IPCC has published the opinion that the temperature increase will be highest
over land and in northern latitudes. For the major maize producing countries of the
Northern Hemisphere there is high confidence that the temperature increase will be in
the range of 0.3–0.7 °C over the next twenty years [104]. In the major maize producing
areas of the world, precipitation will not compensate for the temperature-driven in-
 6 Fumonisin in maize in relation to climate change | 125

crease in evaporation. Higher temperatures combined with greater fluctuations in pre-

cipitation will increase plant stress and predispose maize to infection with fumonisin-
producing fungi.
The IPCC predicts that precipitation will increase at high latitudes, while in tropi-
cal and subtropical areas precipitation will decrease [104]. The prevalence of drought
will increase with higher temperatures. The risk for summer drought will be great-
est in mid-continental areas. Water deficit in the period from silking to kernel milky
stage will make maize more susceptible to development of fumonisin in the maize
kernels [104].
The predicted elevation of CO2 concentrations in the atmosphere during the
21st century is unlikely to affect the risk for fumonisin contamination of maize.
The IPPC is of the opinion that climate change has negatively affected maize yields
for many regions, and they state that there is medium confidence for this opinion [104].
Further climate change without adaptation is projected to further reduce maize pro-
duction. The IPPC emphasizes that there is medium confidence in this statement [104].
The effects of climate change on plant diseases have not received much attention
in the debate on the consequences of increased temperature and reduced precipita-
tion on global crop production. Fungi producing fumonisin in maize have specific tem-
perature and water availability requirements for infection and fumonisin production.
Whether the reported increase in fumonisin contamination in dry and hot summers
is the result of increased fungal growth in the maize kernels or of the up-regulation of
FUM gene expression has not been elucidated.
However, both the currently observed changes in average climate, as well as the
projected changes are relatively small compared to the variability in weather condi-
tions which both the maize plant and the fumonisin producing fungi have to cope
with during growing seasons, single crop seasons, and even sometimes within the
diurnal cycle of a day. Although the key weather factors of air and soil temperature,
rainfall, and air and soil moisture will change in range and possibly shift their pat-
terns, the response of the plant and the pathogen to the relatively huge variability
in current weather conditions provides ample opportunities to infer a robust causal
relationship regarding the responses of fumonisin-producing fungi in maize under
various weather conditions. We are somewhat surprised to observe that the scientific
literature, including review articles, provides little emphasis on information from his-
torical observations, compared to information derived from model simulations which
typically take future climate scenarios as input.
The latter type of studies provides highly uncertain results, with the uncertainty
resulting from both the climate scenarios and the scientific basis for fumonisin-
producing fungi’s responses to weather under various conditions. In general, the
scientific literature reporting on studies on the potential impacts of climate change
focus on scenarios for the average future weather conditions, which do not normally
pretend to describe the full variability of future weather conditions. The latter com-
ponent has, in studies of Fusarium head blight of wheat, been simulated with the
126 | Leif Sundheim and Trond Rafoss

additional aid of a weather generator [121]. However, the current and recent past vari-
ability in weather conditions actually completely covers the average future weather
conditions of the next century, but not the full range of the expected future variability.
These facts call for further studies that can reduce the uncertainty on how weather
conditions affect the interaction of the maize plant and fumonisin-producing fungi.

References

[1] Sheldon JL. A corn mold. Annu Rep Agric Exp Stn Nebr 1904;17:23–32.
[2] Seifert KA, Aoki T, Baayen RP et al. The name Fusarium moniliforme should no longer be
used. Mycol Res 2003;107:643–4.
[3] Marasas WFO, Wehner FC, van Rensburg SJ, van Schalkwyk DJ. Mycoflora of corn produced
in human esophageal cancer areas in Transkei, Southern Africa. Phytopathology 1981;71:
792–796.
[4] Wilson TM, Nelson PF, Ryan TB. Linking leukoencephalomalacia to commercial horse rations.
Vet Med 1985;80:63–69.
[5] Gelderblom WCA, Jaskiewicz J, Marasas WFO et al. Fumonisins: Novel mycotoxins with
cancer-promoting activity produced by Fusarium moniliforme. Appl Environ Microbiol
1988;54:1806–1811.
[6] Bezuidenhout SG, Gelderblom WCA, Gorst-Allman CP et al. Structure elucidation of the
fumonisins, mycotoxins from Fusarium moniliforme. J Chem Soc Chem Commun 1988;11:
743–745.
[7] Marasas WFO, Kellerman TS, Gelderblom WCA, Coetzer JA, Thiel PG, van der Lugt JJ. Leukoen-
cephalomalacia in a horse induced by fumonisin B1 isolated from Fusarium moniliforme.
Onderstepoort J Vet Res 1988;55:197–203.
[8] Rheeder JP, Marasas WFO, Thiel PG, Sydenham EW, Shepard GS, van Schalkwyk DJ. Fusarium
moniliforme and fumonisins in corn in relation to human esophageal cancer in Transkei.
Phytopathology 1992;82:353–357.
[9] Harrison LR, Colvin BM, Greene JT, Newman LE, Cole JR. Pulmonary edema and hydrothorax
in swine produced by fumonisin B1 , a toxic metabolite of Fusarium moniliforme. J Vet Diagn
Investig 1990;2:217–221.
[10] Hendricks K. Fumonisins and neural tube defects in south Texas. Epidemiology 1999;10:
198–200.
[11] Marasas WFO. Fumonisins: Their implications for human and animal health. Nat Toxins
1995;3:193–198.
[12] Naik DM, Nawa IN, Raemakers RH. Absence of an effect from internally seed-borne Fusar-
ium moniliforme on emergence, plant growth and yield of maize. Seed Sci Technol 1982;10:
347–356.
[13] Doehlert DC, Knutson CA, Vesonder RF. Phytotoxic effects of fumonisin B1 on maize seedling
growth. Mycopathologia 1994;127:117–121.
[14] Lamprecht SC, Marasas WFO, Alberts JF et al. Phytotoxicity of fumonisins and TA-toxin to corn
and tomato. Phytopathology 1994;84:383–391.
[15] International Agency for Research on Cancer (IARC). Toxins derived from Fusarium monil-
iforme: fumonisins B1 and B2 and fusarin C. In IARC Monographs on the evaluation of
the carcinogenic risks to humans: Some naturally occurring substances: Food items and
constituents, heterocyclic aromatic amines and mycotoxins. Lyon, France: IARC; 1993;56:
445–466.
 6 Fumonisin in maize in relation to climate change | 127

[16] Wang J, Zhou Y, Liu W, Zhu X, Du L, Wang Q. Fumonisin level in corn-based food and feed
from Linxian County, a high-risk area for esophageal cancer in China. Food Chemistry
2008;106:241–246.
[17] Alizadeh AM, Roshandel G, Roudbarmohammadi S, et al. Fumonisin B1 contamination of
cereals and risk of esophageal cancer in high risk area in Northeastern Iran. Asian Pacific J
Cancer Prev 2012;13:2625–2628.
[18] Wollenweber HW, Reinking OA. Die Fusarien, ihre Beschreibung, Schadwirkung und Bekämp-
fung. Berlin, Germany: Paul Parey; 1935.
[19] Leslie JF, Summerell BA. The Fusarium laboratory manual. Ames, Iowa, USA: Blackwell Pub-
lishing; 2006.
[20] Rheeder JP, Marasas WFO, Vismer HF. Production of fumonisin analogs by Fusarium species.
Appl Environ Microbiol 2002;68:2101–2105.
[21] Bailly JD, Querin A, Tardieu D, Guerre P. Production and purification of fumonisins from a
highly toxigenic Fusarium verticillioides strain. Revue Méd Vét 2005;156:547–554.
[22] Desjardins A. Fusarium mycotoxins. Chemistry, genetics, and biology. St. Paul, Minnesota,
USA: American Phytopathological Society; 2006.
[23] Nelson PE, Plattner RD, Shackelford DD, Desjardins AE. Fumonisin B1 production by Fusar-
ium species other than F. moniliforme in Section Liseola and by some related species. Appl
Environ Microbiol 1992;58:984–989.
[24] Frisvad JC, Smedsgaard J, Samson RA, Larsen TO, Thrane U. Fumonisin B2 production by As-
pergillus niger. J Agric Food Chem 2007;55:9727–9732.
[25] Frisvad JC, Larsen TO, Thrane U et al. Fumonisin and ochratoxin production in industrial As-
pergillus niger strains. PLoS ONE 2011;6(8):e23496. doi:10.1371/[Link].0023496
[26] Soares C, Calado T, Venâncio A. Mycotoxin production by Aspergillus niger aggregate strains
isolated from harvested maize in three Portuguese regions. Rev Iberoam Micol 2013;30:9–13.
[27] Nelson PE, Desjardins AE, Plattner RD. Fumonisins, mycotoxins produced by Fusarium
species: Biology, chemistry, and significance. Ann Rev Phytopathol 1993;31:233–252.
[28] Munkvold GP, Desjardins AE. Fumonisins in maize. Can we reduce their occurrence? Plant Dis
1997;81:556–565.
[29] Binder EM, Tan LM, Chin LJ, Handl J, Richard J. Worldwide occurrence of mycotoxins in com-
modities, feeds and feed ingredients. Anim Feed Sci Technol 2007;137:265–282.
[30] Munkvold GP. Epidemiology of Fusarium diseases and their mycotoxins in maize ears. Eur J
Plant Pathol 2003;109:705–713.
[31] Munkvold GP, Carlton WM. Influence of inoculation method on systemic Fusarium monili-
forme infection of maize plants grown from infected seeds. Plant Dis 1997;81:211–216.
[32] Cotten TK, Munkvold GP. Survival of Fusarium moniliforme, F. proliferatum, and F. subgluti-
nans in maize stalk residue. Phytopathology 1998;88:550–555.
[33] Foley DC. Systemic infection of corn by Fusarium moniliforme. Phytopathology 1962;52:
870–872.
[34] Munkvold, McGee DC, Carlton WM. Importance of different pathways for maize kernel infec-
tion by Fusarium moniliforme. Phytopathology 1997;87:209–217.
[35] Murillo-Williams A, Munkvold GP. Systemic infection by Fusarium verticillioides in maize
plants grown under three temperature regimes. Plant Dis 2008;92:1695–1700.
[36] Yates IE, Hiett KL, Kapczynski DR et al. GUS transformation of the maize fungal endophyte
Fusarium moniliforme. Mycol Res 1999;103:129–136.
[37] Reid LM, Nicol RW, Ouellet T et al. Interaction of Fusarium graminearum and F. moniliforme in
maize ears: Disease progress, fungal biomass, and mycotoxin accumulation. Phytopathology
1999;89:1028–1037.
128 | Leif Sundheim and Trond Rafoss

[38] Picot A, Hourcade-Marcolla D, Barreau C et al. Interactions between Fusarium verticillioides

and Fusarium graminearum in maize ears and consequences for fungal development and
mycotoxin accumulation. Plant Pathol 2012;61:140–151.
[39] Logrieco A, Mulè G, Moretti A, Bottalico A. Toxigenic Fusarium species and mycotoxins asso-
ciated with maize ear rot in Europe. Eur J Plant Pathol 2002;108:597–609.
[40] Shelby RA, White DG, Bauske EM. Differential fumonisin production in maize hybrids. Plant
Dis 1994;78:582–584.
[41] Desjardins AE, Plattner RD, Lu M, Claflin LE. Distribution of fumonisins in maize ears in-
fected with strains of Fusarium moniliforme that differ in fumonisin production. Plant Dis
1998;82:953–958.
[42] Doko MB, Rapior S, Visconti A, Schjøth JE. Incidence and levels of fumonisin contamination in
maize genotypes grown in Europe and Africa. J Agric Food Chem. 1995;43:429–434.
[43] Clements MJ, Kleinschmidt CE, Maragos CM, Pataky JK, White DG. Evaluation of inoculation
techniques for Fusarium ear rot and fumonisin contamination of corn. Plant Dis 2003;87:
147–153.
[44] Bush BJ, Carson ML, Cubeta MA, Hagler WM, Payne GA. Infection and fumonisin production
by Fusarium verticillioides in developing maize kernels. Phytopathology 2004;94:88–93.
[45] Uegaki R, Kobayashi H, Tohno M, Tsukiboshi T. Identification of mycotoxin-producing Fusar-
ium spp. isolated from corn and the changes in concentration of fumonisin during the cultiva-
tion period. Grassland Sci 2012;58:121–126.
[46] Picot A, Barreau C, Pinson-Gadais L et al. The dent stage of maize kernels is the most con-
ducive for fumonisin biosynthesis. Appl Environ Microbiol 2011;77:8382–8390.
[47] Seo J-A, Proctor RH, Plattner RD. Characterization of four clustered and coregulated genes
associated with fumonisin biosynthesis in Fusarium verticillioides. Fungal Genet Biol
2001;34:155–165.
[48] Visentin I, Montis V, Döll K et al. Transcription of genes in the biosynthetic pathway for
fumonisin mycotoxins is epigenetically and differentially regulated in the fungal maize
pathogen Fusarium verticillioides. Eucaryotic Cell 2012;11:252–259.
[49] Proctor RH, Desjardins AE, Plattner RD, Hohn TM. A polyketide synthase gene required for
biosynthesis of fumonisin mycotoxins in Gibberella fujikuroi mating population A. Fungal
Genet Biol 1999;27:100–112.
[50] Proctor RH, Desjardins AE, McCormick SP, Plattner RD, Alexander NJ, Brown DW. Genetic anal-
ysis of the role of trichothecene and fumonisin mycotoxins in the virulence of Fusarium. Eur J
Plant Pathol 2002;108:691–698.
[51] Desjardins AE, Plattner RD. Fumonisin B1 –Nonproducing strains of Fusarium verticillioides
cause maize (Zea mays) ear infection and ear rot. J Agric Food Chem 2000;48:5773–5780.
[52] Witkowski JF, Wedberg JL, Steffey KL et al. Bt corn and European corn borer. Long-term suc-
cess through resistance management. University of Minnesota Extension: Crop News 2013;
1–15.
[53] Munkvold GP, Hellmich RL, Showers WB. Reduced Fusarium ear rot and symptomless in-
fection in kernels of maize genetically engineered for European corn borer resistance. Phy-
topathology 1997;87:1071–1077.
[54] Folcher L, Delos M, Marengue E et al. Lower mycotoxin levels in Bt maize grain. Agron Sustain
Dev 2010;30:711–719.
[55] Bowers E, Hellmich R, Munkvold G. Vip3Aa and Cry1Ab proteins in maize reduce Fusarium
ear rot and fumonisins by deterring kernel injury from multiple Lepidopteran pests. World
Mycotox J 2013;6:127–135.
 6 Fumonisin in maize in relation to climate change | 129

[56] Cardwell KF, Kling JG, Maziya-Dixon B, Bosque-Pérez NA. Interactions between Fusarium
verticillioides, Aspergillus flavus, and insect infestation in four maize genotypes in lowland
Africa. Phytopathology 2000;90:276–284.
[57] Leslie JF, Zeller KA, Lamprecht SC, Rheeder JP, Marasas WFO. Toxicity, pathogenicity, and
genetic differentiation of five species of Fusarium from sorghum and millet. Phytopathology
2005;95:275–283.
[58] Palacios SA, Ramirez ML, Zalazar MC et al. Occurrence of Fusarium spp. in durum wheat
grains. J Agric Food Chem 2011;59:12 264–12 269.
[59] Desjardins AE, Busman M, Proctor RH, Stessman R. Wheat kernel black point and fumonisin
contamination by Fusarium proliferatum. Food Addit Contam 2007;24:1131–1137.
[60] Busman M, Desjardins AE, Proctor RH. Analysis of fumonisin contamination and the presence
of Fusarium in wheat with kernel black point disease in the United States. Food Addit Contam
2012;29:1092–1100.
[61] Tansakul N, Limsuwan S, Trongvanichnam K. Fumonisin monitoring in Thai red cargo rice by
reversed-phase high-performance liquid chromatography with electrospray ionization trap
mass spectrometry. Int Food Res J 2012;19:1561–1566.
[62] Bansal J, Pantazopoulus P, Tam J et al. Surveys of rice sold in Canada for aflatoxins, ochra-
toxin A and fumonisins. Food Addit Contam Part A 2011;28:767–774.
[63] Noonim P, Mahakarnchanakul W, Nielsen KF, Frisvad JC, Samson RA. Fumonisin B2 production
by Aspergillus niger in Thai coffee beans. Food Addit Contam Part A 2009;26:94–100.
[64] Liu C, Xu W, Liu F, Jiang S. Fumonisin production by Fusarium proliferatum strains isolated
from asparagus crown. Mycopathologia 2007;164:127–134.
[65] Marín S, Ramos AJ, Vázquez C, Sanchis V. Contamination of pine nuts by fumonisin pro-
duced by strains of Fusarium proliferatum isolated from Pinus pinea. Lett Appl Microbiol
2007;44:68–72.
[66] Stratakou I, van der Fels-Klerx HJ. Mycotoxins in grapes and wine in Europe: Occurrence,
factors affecting the occurrence and related toxicological effects. World Mycotox J 2010;3:
283–300.
[67] Logrieco A, Ferracane R, Visconti A, Ritieni A. Natural occurrence of fumonisin B2 in red wine
from Italy. Food Addit Contam Part A 2010;27:1136–1141.
[68] Mogensen JM, Larsen TO, Nielsen KF. Widespread occurrence of the mycotoxin fumonisin B2
in wine. J Agric Food Chem 2010;58:4853–4857.
[69] Cozzi G, Paciolla C, Haidukowski M, Leonardis S de, Mule G, Logrieco A. Increase of fumon-
isin B2 and ochratoxin A production by black Aspergillus species and oxidative stress in
grape berries damaged by powdery mildew. J Food Prot 2013;76:2031–2036.
[70] Chiotta ML, Susca A, Stea G et al. Phylogenetic characterization and ochratoxin A – Fu-
monisin profile of black Aspergillus isolated from grapes in Argentina. Int J Food Microbiol
2011;149:171–176.
[71] Hlywka JJ, Bullerman LB. Occurrence of fumonisin B1 and B2 in beer. Food Addit Contam
1999;16:319–324.
[72] Shephard GS, Van der Westhuizen L, Gatyeni PA, Smodyala NIM, Burger H-M, Marasas WFO.
Fumonisin mycotoxins in traditional Xylosa maize beer in South Africa. J Agric Food Chem
2005;53:9634–9637.
[73] Pietri A, Bertuzzi T, Agosti B, Donadini G. Transfer of aflatoxin B1 and fumonisin B1 from nat-
urally contaminated raw materials to beer during an industrial brewing process. Food Addit
Contam Part A 2010;27:1431–1439.
[74] Fandohan P, Hell K, Marasas WFO, Wingfield MJ. Infection of maize by Fusarium species and
contamination with fumonisin in Africa. African J Biotech 2003;2:570–579.
130 | Leif Sundheim and Trond Rafoss

[75] Bankole S, Schollenberger M, Drochner W. Mycotoxins in food systems in Sub Saharan Africa:
A review. Mycotoxin Res 2006;22:163–169.
[76] Bankole SA, Mabekoje OO. Occurrence of aflatoxins and fumonisins in preharvest maize from
south-western Nigeria. Food Addit Contam 2004;21:251–255.
[77] Nikièma PN, Worrillow L, Traoré AS, Wild CP, Turner PC. Fumonisin contamination of maize
from Burkina Faso, West Africa. Food Addit Contam 2004;21:865–870.
[78] Fandohan P, Gnonlonfin G, Hell K, Marasas WFO, Wingfield MJ. Natural occurrence of Fusar-
ium and subsequent fumonisin contamination in preharvest and stored maize in Benin, West
Africa. Int J Food Microbiol. 2005;99:173–183.
[79] Sangare-Tigori B, Moukha S, Kouadio HJ, Betbeder A-M, Dano DS, Creppy EE. Co-occurrence
of aflatoxin B1 , fumonisin B1 , ochratoxin A and zearalenone in cereals and peanuts from Côte
d’Ivoire. Food Addit Contam 2006;23:1000–1007.
[80] Ayalew A, Fehrmann H, Lepschy J, Beck R, Abate D. Natural occurrence of mycotoxins in staple
cereals from Ethiopia. Mycopathologia 2006;162:57–63.
[81] Atukwase A, Kaaya AN, Muyanja C. Factors associated with fumonisin contamination of maize
in Uganda. J Sci Food Agric 2009;89:2393–2398.
[82] Atukwase A, Kaaya AN, Muyanja C. Dynamics of Fusarium and fumonisins in maize during
storage – A case of traditional storage structures commonly used in Uganda. Food Control
2012;26:200–205.
[83] Alkonya AE, Monda EO, Ajanga S. Variation in in vitro fumonisin B1 production by differ-
ent Fusarium verticillioides isolates in Kenya. American-Eurasian J Agric & Environ Sci
2008;4:368–371.
[84] Schjøth JE, Visconti A, Sundheim L. Fumonisins in maize in relation to climate, planting time
and hybrids in two agroecological zones in Zambia. Mycopathologia 2009;167:209–219.
[85] Mukanga M, Derera J, Tongoona P, Laing MD. A survey of pre-harvest ear rot diseases
of maize and associated mycotoxins in south and central Zambia. Int J Food Microbiol
2010;141:213–221.
[86] Nooh A, Amra H, Youssef MM, El-Banna AA. Mycotoxin and toxigenic fungi occurrence in
Egyptian maize. Int J Adv Res 2014;2:521–532.
[87] European Commission 2007. Commission Regulation (EC) No 1126/2007 of 28.9.2007
amending regulation (EC) No 1181/2006 setting maximum levels for certain contaminants
in foodstuffs as regards Fusarium toxins in maize and maize products. Off J Eur Union L
2007;254:14–17.
[88] Visconti A, Doko MB. Survey of fumonisin production by Fusarium isolated from cereals in
Europe. J AOAC Int 1994;77:546–550.
[89] Ariño A, Herrera A, Juan T et al. Influence of agricultural practices on the contamination of
maize by fumonisin mycotoxins. J Food Prot 2009;72:898–902.
[90] Ivic D, Kovacevik B, Vasilj V, Idzakovic N. Occurrence of potentially toxigenic Fusarium verti-
cillioides and low fumonisin B1 content on barley grain in Bosnia and Herzegovina. J Appl Bot
Food Quality 2011;84:121–124.
[91] Van Asselt ED, Azambuja W, Moretti A et al. A Dutch field survey on fungal infection and myco-
toxin concentration in maize. Food Addit Contam Part A. 2012;29:1556–1565.
[92] Nielsen LK, Jensen JD, Nielsen GC et al. Fusarium head blight of cereals in Denmark: Species
complex and related mycotoxins. Phytopathology 2011;101:960–969.
[93] Parikka P, Hakala K, Tiilikkala K. Expected shifts in Fusarium species’ composition on ce-
real grain in Northern Europe due to climatic change. Food Addit Contam Part A 2012;29:
1543–1555.
[94] Giannitti F, Diab SS, Pacin AM et al. Equine leukoencephalomalacia (ELEM) due to fumonisins
B1 and B2 in Argentina. Pesq Vet Bras 2011;31:407–412.
 6 Fumonisin in maize in relation to climate change | 131

[95] Broggi LE, Pacin AM, Gasparovic A et al. Natural occurrence of aflatoxins, deoxynivalenol,
fumonisins and zearalenone in maize from Entre Rios Province, Argentina. Mycotoxin Res
2007;23:59–64.
[96] Ono EYS, Ono MA, Funo FY et al. Evaluation of fumonisin-aflatoxin co-occurrence in Brazilian
corn hybrids by ELISA. Food Addit Contam Part A 2001;18:719–729.
[97] Stumpf R, dos Santos J, Gomes LB et al. Fusarium species and fumonisins associated with
maize kernels produced in Rio Grande do Sul State for the 2008/09 and 2009/10 growing
seasons. Braz J Microbiol 2013;44:89–95.
[98] Hooker DC, Schaafsma AW. Agronomic and environmental impacts on concentration of de-
oxynivalenol and fumonisin B1 in corn across Ontario. Can J Plant Pathol 2005;27:347–356.
[99] Jurjevic Z, Wilson DM, Wilson JP et al. Fusarium species of the Gibberella fujikuroi complex
and fumonisin contamination of pearl millet and corn in Georgia, USA. Mycopathologia
2005;159:401–406.
[100] Wu F, Bhatnager D, Bui-Klimke T et al. Climate change impacts on mycotoxin risks in US
maize. World Mycotox J 2011;4:79–93.
[101] Wei T, Zhu W, Pang M, Liu Y, Dong JG. Natural occurrence of fumonisins B1 and B2 in corn in
four provinces of China. Food Addit Contam Part B 2013;6:270–274.
[102] Azizi IG, Rouhi S. The comparison of total fumonisin and total aflatoxin levels in biscuit and
cookie samples in Babol City, Northern Iran. Iranian J Publ Health 2013;42:422–427.
[103] Trung TS, Tabuc C, Bailly S, Querin A, Guerre P, Bailly JD. Fungal mycoflora and contamination
of maize from Vietnam with aflatoxin B1 and fumonisin B1 . World Mycotox J 2008;1:87–94.
[104] Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midg-
ley PM (eds). IPCC 2013: Summary for Policymakers. In: Climate Change 2013: The Physical
Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Inter-
governmental Panel on Climate Change. Cambridge, United Kingdom and New York, NY, USA:
Cambridge University Press; 2013.
[105] Oerke E-C. Crop losses to pests. J Agric Sci 2006;144:31–43.
[106] Coakley SM, Scherm H, Chakraborty S. Climate change and plant disease management. Ann
Rev Phytopathol 1999;37:399–426.
[107] de la Campa R, Hooker DC, Miller JD, Schaafsma AW, Hammond BG. Modelling effects of envi-
ronment, insect damage, and Bt genotypes on fumonisin accumulation in maize in Argentina
and the Philippines. Mycopathologia 2005;159:539–552.
[108] Schaafsma AW, Hooker DC. Climatic models to predict occurrence of Fusarium toxins in wheat
and maize. Int J Food Microbiol 2007;119:116–125.
[109] Marin S, Sanchis V, Magan N. Water activity, temperature and pH effects on growth of
Fusarium moniliforme and Fusarium proliferatum isolates from maize. Can J Microbiol
1995;41:1063–1070.
[110] Marin S, Sanchis V, Vinas I, Canela R, Magan N. Effect of water activity and temperature on
growth and fumonisin B1 and B2 production by Fusarium proliferatum and F. moniliforme on
maize grain. Letters Appl Microbiol 1995;21:298–301.
[111] Cao A, Santiago R, Ramos AJ et al. Critical environmental and genotypic factors for Fusarium
verticillioides infection, fungal growth and fumonisin contamination in maize grown in north-
western Spain. Int J Food Microbiol 2014;177:63–71.
[112] Jurado M, Marín P, Magan N, González-Jeán MT. Relationship between solute and matric po-
tential stress, temperature, growth and FUM1 gene expression in two Fusarium verticillioides
strains from Spain. Appl Environ Microbiol 2008;74:2032–2036.
[113] Marín P, Magan N, Vázquez C, González-Jeán MT. Differential effect of environmental condi-
tions on the growth and regulation of the fumonisin biosynthesis gene FUM1 in the maize
132 | Leif Sundheim and Trond Rafoss

pathogens and fumonisin-producers Fusarium verticillioides and Fusarium proliferatum.

FEMS Microbiol Ecol 2010;73:303–311.
[114] Parsons MW, Munkvold GP. Effects of planting date and environmental factors on fusarium
ear symptoms and fumonisin B1 accumulation in maize grown in six North American loca-
tions. Plant Pathol 2012;61:1130–1142.
[115] Elsgaard L, Børgesen CD, Olesen JE et al. Shifts in comparative advantages for maize, oat and
wheat cropping under climate change in Europe. Food Addit Contam Part A 2012;29:1514–
1526.
[116] Camargos SM, Soares LMV, Sawazaki E, Bolonhezi D, Castro JL, Bortolleto N. Accumulation
of fumonisin B1 and B2 in freshly harvested Brazilian commercial maize at three locations
during two nonconsecutive seasons. Mycopathologia 2001;155:219–228.
[117] Ono EYS, Sugiura Y, Homechin M et al. Effect of climatic conditions on natural mycoflora
and fumonisins in freshly harvested corn of the State of Paraná, Brazil. Mycopathologia
1999;147:139–148.
[118] Herrera M, Conchello P, Juan T, Estopañan G, Herrera A, Ariño A. Fumonisin concentrations
in maize as affected by physio-chemical, environmental and agronomic conditions. Maydica
2010;55:121–126.
[119] Magan N, Medina A, Aldred D. Possible climate-change effects on mycotoxin contamination
of food crops pre- and postharvest. Plant Pathol 2011;60:150–163.
[120] Pritchard SG, Rogers HH, Prior SA, Peterson CM. Elevated CO2 and plant structure: A review.
Global Change Biol 1999;5:807–837.
[121] Semenow MA, Pilkington-Bennett S, Calanca P. Validation of ELPIS 1980–2010 baseline sce-
narios using the observed European climate assessment data set. Clim Res 2013;57:1–9.
Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and
Eva Maria Binder
7 Climate change impacts on mycotoxin production

7.1 Introduction

Prices of staple grains have increased significantly in the last five years and climate
change is bound to add pressure to the supply and quality of food, and the sustain-
ability of production practices worldwide. The impact of climate change on food pro-
duction has been identified as an emerging hazard for food and feed security world-
wide [1, 2], and the consequent risks are being received with increasing scientific at-
tention [3]. One key aspect in food and feed safety is the changing pattern of mycotoxin
contamination in cereals such as wheat, maize, and rice due to climate change, which
the EFSA’s Emerging Risks Unit has recognized as a potential emerging hazard [1].
The 2014 Intergovernmental Panel on Climate Change (IPCC) report illustrates
different global warming projections depending on low- or high-emission scenarios.
The prediction for the year 2100 is that global temperatures may increase by up to
4.8 °C [4]. The world is undergoing extreme weather events, such as hurricanes, which
are causing the spread of plant pathogens to new areas [5]. This is expected to increase
with the projected increase in the frequency of extreme weather events due to climate
change [6].
The distribution of species around the world will also show an overall shift pole-
wards. Bebber et al. found that plant pathogens and pests are moving at a rate of about
2.7 km/year towards the poles [7], which is very close to the rate of climate change [8].
For some areas, projections of decreasing summer precipitation and increases in tem-
perature would ultimately lead to drought stress episodes. Changes are also expected
to occur among crops grown in the next 10 to 20 years due to the predicted rise in
atmospheric CO2 concentrations at a rate of 1.5 μmol/year [3].
The impact of climate change on fungal colonization has not yet been fully elu-
cidated. However, it is known that temperature, humidity, and precipitation have an
effect on toxigenic fungi and on pathogen-plant host interaction [9]. It has also been
suggested that slightly elevated CO2 concentrations and interactions with temperature
and water availability may stimulate the growth of some mycotoxigenic fungi, par-
ticularly those under water stress [3]. Displacements of fungal species by other more
virulent or aggressive fungi have already been observed [10]. Other secondary factors
may have an additional impact on the mycotoxigenic fungal profile, including insect
attacks and effectiveness of fungicides and pesticides, as well as the alteration of ge-
ographical distribution or the life cycle of insects which promote fungal infections in
crops [3].
134 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

7.2 Impact of temperature, water availability, and CO2

on mycotoxin production
The life cycle of all microorganisms, including mycotoxigenic molds, depends on two
main factors: water availability and temperature [11]. These factors interact to influ-
ence a series of parameters including germination, growth, sporulation, and myco-
toxin production [12]. In general, there is a temperature range within which fungi per-
form best. Therefore, increasing average temperatures may alter the range at which
fungi are able to compete.
As concentrations of methane, carbon dioxide, nitrous oxide, and chlorofluoro-
carbons in the atmosphere increase, so will incidences of environmental warming,
higher precipitation, or drought [13]. These extreme weather conditions will have
wide-ranging impacts, depending on world region and mycotoxin systems [14]. Sev-
eral authors have reviewed some aspects of the impact that climate change may have
on plant breeding, plant diseases, and mycotoxins in Europe, Australia, and Africa
[2, 15–18]. There are some predicted effects of temperature increase and water avail-
ability on both fungal growth rates and on the production of some of the most relevant
mycotoxins: Alternaria toxins, fumonisins, trichothecenes, ochratoxin A, aflatoxin B1 ,
and patulin. However, these predictions do not take the possible additional effect of
CO2 into account [3]. Typically, high concentrations of mycotoxins in grains depend
on the number of rainy days and days with relative humidity above 75 %, but there
can be a decrease in mycotoxin concentrations at temperatures below 12 or above
32 °C [19].
Aspergillus flavus and A. parasiticus, the main aflatoxin producers, are xerophilic
fungi which thrive under higher temperatures and lower rainfall [1]. For instance, dur-
ing the hot and dry episodes in northern Italy in 2003, A. flavus was able to actively
colonize the ripening maize, a key crop, by outcompeting the more common Fusarium
species [20]. This led to an uncommon increase in Afla B1 contamination in Europe.
Fumonisin occurrence is linked to drought stress. Dry season maize in Southern
and Eastern Africa may contain high levels of this toxin, even if the maize appears to
be of very good quality. Fumonsins are less significant in northern temperate zones
with cooler climates. High temperatures favor the growth of the fumonisin producer
Fusarium verticillioides, which means that a warming trend would lead to greater dom-
ination of the fungus compared to other maize-borne Fusarium species [9].
The displacement of the formerly predominant species, F. culmorum and Micro-
dochium nivale, by the more virulent plant pathogen F. graminearum as a result of
warm European summers has been reported [9]. Since M. nivale is nontoxigenic and
F. culmorum generally produces a lower number of mycotoxins than F. graminearum,
the concentration of mycotoxins may consequently increase [6]. In Canada, a more
toxigenic 3-acetylated deoxynivalenol (3ADON) chemotype of F. graminearum re-
placed the 15-acetylated deoxynivalenol (15ADON) chemotype, indicating genetic
differentiation [21]. Novel strains which form unexpected toxins are also being discov-
 7 Climate change impacts on mycotoxin production | 135

ered and may have resulted from changing environments. Such shifts in mycotoxigenic
fungi may also lead to changes in the mycotoxin chemical profile [9]. Minnesota,
for instance, has witnessed the emergence of a novel Fusarium isolate called the
“Northland population” which does not produce the trichothecenes deoxynivalenol
or nivalenol [10].
Climate change is expected to increase the biomass of crops and alternative host
plants will further increase inoculum production. Chakraborty et al. have shown that
an increase in atmospheric CO2 concentration will directly increase the amounts of
Fusarium head blight (FHB) and Crown Rot (CR) inoculum. The authors showed that
the saprotrophic fitness of F. graminearum remained at elevated CO2 levels and did not
suffer any decrease in its ecological fitness [6].
A deterioration of grain quality may occur as a direct effect of increasing temper-
ature and CO2 , resulting in a reduction in the protein and micronutrient content in
grain. Such an effect could facilitate mold growth and mycotoxin production, which
could affect quality during storage and transport [6]. It has been shown that extreme
drought episodes, desertification, and variations in wet/dry cycles will impact myco-
toxigenic fungi. In developing countries, drought stress may play an important role
in terms of food security. Maize, peanuts, and pistachios are particularly prone to in-
fection during heat/drought stress due to cracking or splitting, which may result in
a significant increase in A. flavus and, consequently, aflatoxin contamination. An in-
crease in preharvest aflatoxin contamination will affect nutritional quality and have
an impact on consumption or the ability to export [9].
Water availability is predicted to be altered by climate change, and some areas
will experience drought while others experience greater precipitation. The effects of
humidity on mycotoxin production in crops are less straightforward than those for
temperature [14]. In a postharvest scenario, grain silos which harbor pests which can
multiply more rapidly under warmer temperatures could contain higher amounts of
metabolic water. This increase in condensation could initiate spoilage, potentially in-
creasing contamination with mycotoxins such as ochratoxin A, aflatoxins, and per-
haps trichothecenes in damp grain. This means that the distribution and types of
mycotoxins postharvest may change significantly, giving way to new emerging myco-
toxins [9].

7.3 Prediction strategies

Geostatistics is a tool which enables the investigation of specific regional hotspots

which may represent high risk of mycotoxin contamination based on meteorological
data. This method could be used to predict the optimal time points for fungicide ap-
plications and pest control in order to minimize contamination [3].
Aflatoxin prediction strategies have already been applied worldwide. For in-
stance, Battilani et al. studied the regions in Europe which may be hot spots for
136 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

A. carbonarius contamination of wine grapes and at a higher risk for contamination

with ochratoxin A [22]. The authors showed that the highest contamination with
this fungus was just prior to harvest. In Australia, recent studies have demonstrated
that it is possible to use an agricultural production systems simulator to calculate
an aflatoxin risk index (ARI) in both maize and peanuts [17]. The use of advanced
high resolution radiometer (AVHRR) satellite data has also been used in Mali, West
Africa, to examine the relationship between peanut yield, total precipitation, and the
maximum reproductive phase of peanut plants and aflatoxin contamination [16].
The main prediction tool for Fusarium head blight (FHB) and the risk of DON
contamination in small grain cereals and maize is DONCAST, a model based on the
weather conditions just prior to and during wheat head emergence. The method in-
cludes the input of local or regional weather data, the number of rainy days prior
to and after anthesis. Other factors which are taken into account include weather
data during ripening, and maximum, minimum and mean temperatures of the region.
Other approaches to DON prediction are based on the life cycle of F. graminearum in a
method called the TOX-risk, which is a risk index calculated daily for F. graminearum
and F. culmorum over the growing season [23, 24].
A similar approach to that used for DONCAST was developed to predict fumon-
isin contamination, taking climatic information relevant to the growing period into
account. Changes in temperature and the amount of rain post-silking were used to
predict the risk of fumonisins in maize and genetically modified maize [19, 25].
The potential use of the geographical emerging mycotoxin identification system
(GEMIS) model has been tested across Europe to examine the effects of changes in
temperature (+2 °C) and rainfall (+3 mm) on heading date and cereal productivity ar-
eas [26].

7.4 Other factors to consider

Temperature, water availability, and CO2 are believed to be the most important com-
ponents affecting changes in mycotoxin patterns. However, other less considered
climate-influenced factors such as insect and other pest attacks, the effectiveness of
fungicides, and the possible effects on mycotoxin biosynthetic pathways should also
be recognized as potential and indirect triggers of fungi colonization and mycotoxin
production [9].
Insect attacks are known to lower the resistance of plants to stress, and the re-
sulting wounds on kernels may favor infection by the fungus. There is substantial ev-
idence to indicate that there will be an overall increase in the number of outbreaks of
various insects [9]. The IPCC report predicts that more insect pests will occur at higher
temperatures [4], leading to a higher distribution of mycotoxigenic fungi [27, 28]. Also,
more insects may increase insect-feeding birds which may result in more bird dam-
age to crops, making the ecological implications of climate change even more com-
plex [14].
 7 Climate change impacts on mycotoxin production | 137

Fungicide effectiveness may be significantly modified by climate variation, lead-

ing to less effective control of mycotoxigenic pathogens and toxin contamination [3].
Medina et al. showed that both water availability and temperature modulate the effect
of carbendazim [29] and natamycin [30] against ochratoxin A-producing A. carbonar-
ius.
Mycotoxin biosynthetic pathways have been elucidated for many of the key myco-
toxigenic fungi, such as the aflatoxin B1 -producing A. flavus, the DON-producing
F. graminearum, and the fumonisin B1 -producing F. verticillioides. Genes involved in
the production of mycotoxins are often clustered together. Microarray analysis has
been used to investigate the effect of stress factors on such genes. Schmidt-Heydt
et al. suggested that changes in both temperature and water availability may increase
mycotoxin production [31, 32].

7.5 Insights into potential mycotoxin production: focus on Europe

Patterson et al. have suggested that just as in the scenario where climate change will
lead to an increase in total mycotoxins because more crops are produced within a re-
gion, conversely there would be a decrease in total mycotoxins because fewer crops
are produced within a region [14]. According to the IPCC report, more crops or higher
yields will occur in regions which are currently cool, and fewer crops or yields will
occur in the currently warm regions [4]. However, warm regions are expected to see
more encroachment of arid and semi-arid land, heightening drought stress in crops
and leading perhaps to an increase in mycotoxins. In currently cool regions, storage
conditions may worsen as temperatures increase [14].
According to the IPCC, it is predicted that annual precipitation in the Mediter-
ranean regions of Europe and Africa will decrease [4]. An increase in aflatoxins
and ochratoxin A from Aspergillus spp., as well as fumonisins is expected in sub-
Mediterranean countries as a result of temperature increases. For instance in northern
Portugal, the ochratoxin A producer A. carbonarius was the main mycotoxigenic fun-
gus found on grapes [33, 34]. A. flavus and Penicillium expansum were present in lower
amounts. It is predicted that in 100 years, A. flavus may outcompete A. carbonarius,
increasing the threat of aflatoxins compared to ochratoxin A. Temperatures may also
be too high for P. expansum, resulting in a possible reduction of patulin [14]. Aflatoxins
have been reported in northern Italy [20], while A. flavus has been isolated in Hungary
in regions where the fungus was not present before [35].
High temperatures and drought are expected to reduce water availability and con-
sequently crop productivity in the south of Europe. Daily precipitation is expected to
increase in northern Europe [4]. In southern and south-eastern Europe, including Por-
tugal, Spain, southern France, Italy, Slovenia, Greece, Malta, Cyprus, Bulgaria, and
southern Romania, an increase of 4–5 °C is predicted and water availability is expected
to be reduced, especially in the summer [14].
138 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

Western and Atlantic European countries, such as Benelux, western and north-
ern France, northern Germany, United Kingdom, Irish Republic, the Netherlands, and
Denmark are predicted to experience an increase of 2.5–3.5 °C with drier and hotter
summers [14].

7.6 Trends in mycotoxin occurrence

As part of its mycotoxin risk management program, Biomin has been conducting a
yearly mycotoxin survey since 2004 which provides insight into the risks caused by
the main mycotoxins found in agricultural commodities such as corn, wheat, barley,
silage, as well as finished feed and others. Till now, more than 26 000 samples from
different countries around the world have been evaluated for the presence of aflatoxins
(Afla), zearalenone (ZEN), deoxynivalenol (DON), fumonisins (FUM) and ochratoxin A
(OTA). The Biomin Mycotoxin Survey summarizes the importance of the co-occurrence
of various mycotoxins in different samples.
Table 7.1 provides a global overview of the mycotoxins present in all commodities
analyzed each year. The percentage of samples above the EC guideline for aflatoxin
B1 or the EC recommended levels for all other toxins are indicated in the last column
of the table to allow comparison of the results. These percentages are illustrated to
provide an overview of the trends for the particular mycotoxin across the different
years. The results worldwide depict the changes in the most problematic mycotoxins
for each year. For instance, zearalenone levels were particularly high in 2006; the high-
est ochratoxin contaminations were observed in 2007; the contamination of aflatoxins
was at its highest so far in 2008; fumonisin levels were at a maximum in 2009; and
2010 is considered a DON-contamination peak year.
As DON is one of most commonly occurring mycotoxins worldwide, it was the most
extensively analyzed within the mycotoxin survey. In 2005, a total of 1432 samples
were analyzed for DON content and the number of samples increased each year to
almost 4000 samples in 2013. The EC recommended value for complementary and
complete feedstuffs for pigs (900 ppb) was used for means of comparison [36]. The
percentage of samples over the years with concentrations of DON above 900 ppb show
fluctuations between a minimum of 9.4 % in the first half of 2014 and a maximum of
18.2 % in 2010.
The global occurrence of zearalenone was also intensively studied within the
mycotoxin survey. The EC recommendation for ZEN in complementary and complete
feedstuffs for piglets and gilts (young sows) is set at 100 ppb [36], due to the high
sensitivity of these animals to this estrogen-like substance. There was a high variation
in the percentage of samples above 100 ppb, a level which lies above the EC recom-
mendation. This ranged from 9.5 % in 2013 to 22.4 % of all samples in 2006, which is
a considerably large number of samples that could potentially affect sow fertility.
 7 Climate change impacts on mycotoxin production | 139

From 2005 to 2013, a total of 700 to 2800 samples were analyzed in the respective
years for total aflatoxin content. Results show that 13.2 % (in 2012) to almost 24 % (in
2008) of the samples analyzed lie above the European maximum value of 5 ppb for
aflatoxin B1 for complete feedstuffs for dairy animals [37]. It is well known that afla-

Tab. 7.1: Results of the BIOMIN Mycotoxin Survey for all commodities analyzed worldwide.

1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples

≥ 900 ppb DON

(EC recomm.
Mycotoxin Year ppb pigs)

2005 1432 10.3 % 21.2 % 1.2 % 6.8 % 2.9 % 0.2 % 0.1 % 11.2 %
2006 1880 11.5 % 22.4 % 2.0 % 8.4 % 4.5 % 0.7 % 0.3 % 15.9 %
2007 1289 15.1 % 18.3 % 1.6 % 6.2 % 3.2 % 0.8 % 1.2 % 13.0 %
2008 1729 15.2 % 27.2 % 2.0 % 8.8 % 5.1 % 0.8 % 0.2 % 16.9 %
2009 2413 12.5 % 23.4 % 1.5 % 6.7 % 3.3 % 0.4 % 0.3 % 12.2 %
DON
2010 2948 12.8 % 23.8 % 1.7 % 8.4 % 5.7 % 1.6 % 0.8 % 18.2 %
2011 3509 15.0 % 23.1 % 1.6 % 8.1 % 5.3 % 0.9 % 0.7 % 16.6 %
2012 3712 19.7 % 17.9 % 1.8 % 6.6 % 6.2 % 1.5 % 1.2 % 17.2 %
2013 3931 18.5 % 21.3 % 1.1 % 5.9 % 4.2 % 0.5 % 0.5 % 12.2 %
2014 1655 19.2 % 22.0 % 1.5 % 4.6 % 2.7 % 0.5 %
500–1999 0.1 % 9.4 %
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples

≥ 100 ppb ZEN

(EC recomm.
Mycotoxin Year ppb pigs)

2005 1110 4.8 % 8.6 % 6.5 % 2.9 % 4.3 % 2.8 % 1.1 % 17.6 %
2006 1663 4.8 % 7.9 % 8.2 % 2.3 % 4.8 % 5.4 % 1.7 % 22.4 %
2007 1121 12.6 % 9.8 % 5.3 % 1.2 % 2.2 % 1.2 % 0.8 % 10.7 %
2008 1424 9.7 % 14.5 % 9.1 % 1.5 % 3.1 % 3.3 % 0.6 % 17.6 %
2009 2303 8.4 % 9.6 % 6.2 % 1.4 % 3.5 % 2.2 % 0.5 % 13.8 %
ZEN
2010 2634 10.5 % 9.3 % 8.0 % 1.9 % 4.8 % 4.4 % 0.6 % 19.7 %
2011 3061 11.6 % 8.9 % 7.0 % 1.8 % 4.0 % 3.4 % 0.4 % 16.6 %
2012 3320 10.8 % 5.5 % 4.3 % 1.3 % 3.4 % 4.9 % 1.2 % 15.1 %
2013 3470 11.8 % 6.5 % 4.9 % 0.9 % 1.8 % 1.6 % 0.3 % 9.5 %
2014 1613 11.4 % 10.9 % 4.3 % 1.0 % 2.9 % 2.5 % 0.2 % 11.0 %
10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200

≥ 5 ppb AfB1
(EC max for
Mycotoxin Year ppb dairy cattle)

2005 698 0.9 % 5.3 % 4.7 % 4.4 % 0.7 % 15.2 %

2006 1132 2.2 % 5.2 % 4.4 % 8.2 % 0.8 % 18.6 %
2007 807 2.9 % 6.2 % 5.7 % 8.2 % 1.2 % 21.3 %
Total 2008 1132 7.1 % 4.7 % 4.9 % 12.1 % 2.1 % 23.8 %
aflatoxin 2009 1661 9.7 % 4.8 % 4.9 % 10.5 % 2.8 % 22.9 %
B1 , B2 , 2010 1950 10.7 % 4.2 % 3.2 % 9.0 % 0.9 % 17.3 %
G 1 , G2 2011 2770 10.6 % 2.6 % 3.0 % 8.2 % 1.9 % 15.7 %
2012 2636 10.7 % 4.7 % 3.2 % 4.7 % 0.6 % 13.2 %
2013 2839 12.8 % 5.6 % 3.7 % 5.5 % 0.8 % 15.6 %
2014 1267 9.6 % 4.1 % 2.9 % 8.2 % 1.9 % 17.1 %
140 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

Tab. 7.1 (continued)

5000–19 999
≥ 5000 ppb

1000–1499

1500–2999

3000–4999
200–999

≥ 20 000
total fumo-
nisins

# samples
(EC recomm.
pigs/horses)
Mycotoxin Year ppb

2005 698 30.2 % 3.3 % 4.3 % 1.0 % 1.1 % 0.3 % 1.4 %

2006 1000 26.1 % 5.0 % 5.3 % 2.7 % 3.0 % 0.5 % 3.5 %
2007 646 34.1 % 6.2 % 8.4 % 2.9 % 1.1 % 0.2 % 1.2 %
2008 1074 32.4 % 5.7 % 5.8 % 2.8 % 2.7 % 0.0 % 2.7 %
Total fu-
2009 1579 22.1 % 7.3 % 9.4 % 5.3 % 6.6 % 0.4 % 7.1 %
monisin
B1 , B2 2010 2108 23.2 % 7.2 % 9.6 % 4.6 % 4.3 % 0.2 % 4.5 %
2011 2548 21.6 % 5.8 % 9.5 % 3.7 % 2.9 % 0.3 % 3.2 %
2012 2570 26.1 % 6.8 % 8.9 % 3.2 % 2.3 % 0.1 % 2.5 %
2013 2699 24.1 % 5.7 % 9.1 % 3.6 % 2.8 % 0.1 % 2.9 %
2014 1298 27.7 % 5.9 % 8.5 % 4.2 % 3.4 % 0.3 % 3.7 %

100–149

150–399
10–49

50–79

80–99
5–9.9
# samples

≥ 400
≥ 50 ppb OTA
(EC recomm.
Mycotoxin Year ppb pigs)

2005 145 2.8 % 2.1 % 0.0 % 0.0 % 0.7 % 1.4 % 0.7 % 2.8 %
2006 269 4.5 % 5.6 % 1.1 % 0.4 % 0.0 % 0.4 % 0.0 % 1.9 %
2007 207 2.9 % 2.4 % 0.0 % 1.4 % 1.0 % 1.9 % 2.9 % 7.2 %
2008 930 4.1 % 3.5 % 0.5 % 0.1 % 0.2 % 0.1 % 0.0 % 1.0 %
2009 1034 4.0 % 4.1 % 0.3 % 0.0 % 0.0 % 0.4 % 0.1 % 0.8 %
OTA
2010 1558 4.4 % 2.4 % 0.4 % 0.1 % 0.1 % 0.1 % 0.0 % 0.7 %
2011 1966 3.2 % 4.4 % 0.2 % 0.1 % 0.1 % 0.2 % 0.1 % 0.6 %
2012 2230 3.6 % 2.8 % 0.4 % 0.0 % 0.0 % 0.0 % 0.0 % 0.5 %
2013 2459 2.0 % 2.8 % 0.2 % 0.0 % 0.1 % 0.3 % 0.0 % 0.7 %
2014 1113 1.8 % 1.9 % 0.4 % 0.0 % 0.0 % 0.0 % 0.0 % 0.4 %

toxins often co-occur with fumonisins. The animals most sensitive to fumonisins are
pigs and horses, therefore the EC recommended level for fumonisins in complemen-
tary and complete feedstuffs for these animals has been set at 5000 ppb. A fumonisin
contamination peak was observed in 2009, as 7.1 % of samples contained fumonisins
at concentrations above the EC recommended level.
Compared to all other toxins, the worldwide contamination by ochratoxins was
relatively low. Nonetheless, 2007 was a peak year for OTA contamination in which
7.2 % of all samples had a concentration above the EC recommendation of 50 ppb OTA
in complementary and complete feedstuffs for pigs.
Tab. 7.2 illustrates the results of the mycotoxin survey for all European samples.
Although most samples originate from central Europe and fewer from southern Eu-
rope, some differences can be observed. A more detailed overview of the results for
samples originating from central and southern Europe can be found in Tab. 7.3 and
Tab. 7.4, respectively.
 7 Climate change impacts on mycotoxin production | 141

Tab. 7.2: Results of the BIOMIN Mycotoxin Survey for all European samples.

1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples
≥ 900 ppb DON
(EC recomm.
Mycotoxin Year ppb pigs)

2005 703 4.1 % 22.0 % 1.1 % 7.7 % 3.0 % 0.3 % 0.0 % 12.1 %
2006 616 4.7 % 24.8 % 2.9 % 12.7 % 6.2 % 1.5 % 0.0 % 23.2 %
2007 484 11.2 % 29.8 % 2.9 % 11.2 % 6.2 % 1.9 % 3.3 % 25.4 %
2008 655 9.9 % 35.9 % 2.7 % 11.5 % 5.5 % 1.1 % 0.2 % 20.9 %
2009 1137 11.0 % 25.9 % 1.3 % 6.1 % 2.6 % 0.1 % 0.0 % 10.1 %
DON
2010 1103 9.2 % 29.3 % 2.3 % 9.0 % 5.6 % 2.0 % 1.4 % 20.2 %
2011 1481 10.3 % 30.4 % 2.1 % 9.7 % 7.1 % 0.7 % 0.5 % 20.1 %
2012 1580 22.2 % 21.9 % 2.1 % 6.5 % 4.7 % 0.5 % 0.4 % 14.2 %
2013 1854 17.7 % 24.1 % 1.5 % 7.8 % 5.6 % 0.3 % 0.4 % 15.5 %
2014 736 21.7 % 27.6 % 2.4 % 7.2 % 3.3 % 0.8 % 0.1 % 13.9 %

500–1999
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples

≥ 100 ppb ZEN

(EC recomm.
Mycotoxin Year ppb pigs)

2004 566 2.5 % 1.8 % 1.6 % 0.5 % 1.2 % 0.5 % 0.2 % 4.1 %
2005 378 2.4 % 8.7 % 4.2 % 1.9 % 2.9 % 0.8 % 0.0 % 9.8 %
2006 412 2.4 % 5.8 % 8.0 % 2.9 % 3.6 % 2.7 % 2.4 % 19.7 %
2007 300 14.0 % 11.0 % 6.0 % 1.3 % 3.0 % 1.7 % 0.7 % 12.7 %
2008 413 7.3 % 9.2 % 6.1 % 0.7 % 1.2 % 0.7 % 0.0 % 8.7 %
ZEN
2009 967 5.7 % 5.6 % 4.3 % 1.3 % 2.3 % 1.2 % 0.0 % 9.2 %
2010 759 5.5 % 6.9 % 6.7 % 1.4 % 0.9 % 0.5 % 0.0 % 9.6 %
2011 1089 10.4 % 8.5 % 7.8 % 1.3 % 2.6 % 2.0 % 0.0 % 13.7 %
2012 1199 11.4 % 3.8 % 2.4 % 0.3 % 1.3 % 0.5 % 0.0 % 4.5 %
2013 1413 7.2 % 4.3 % 2.3 % 0.5 % 0.6 % 0.4 % 0.1 % 4.0 %
2014 607 13.8 % 7.6 % 3.1 % 1.0 % 0.8 % 0.7 % 0.0 % 5.6 %
10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200

≥ 5 ppb AfB1
(EC max for
Mycotoxin Year ppb dairy cattle)

2007 57 14.0 % 0.0 % 0.0 % 3.5 % 0.0 % 3.5 %

2008 57 12.3 % 1.8 % 0.0 % 7.0 % 1.8 % 10.5 %
Total 2009 334 23.4 % 6.0 % 3.6 % 0.3 % 0.3 % 10.2 %
aflatoxin 2010 74 18.9 % 2.7 % 1.4 % 1.4 % 0.0 % 5.4 %
B1 , B2 , 2011 199 27.6 % 4.0 % 1.5 % 0.5 % 0.0 % 6.0 %
G 1 , G2 2012 369 25.5 % 7.6 % 1.9 % 2.2 % 0.0 % 11.7 %
2013 711 20.7 % 7.7 % 3.2 % 3.2 % 0.0 % 14.2 %
2014 279 23.7 % 5.0 % 0.4 % 1.1 % 0.4 % 6.8 %
142 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

Tab. 7.2 (continued)

5000–19 999
1000–1499

1500–2999

3000–4999
200–999

≥ 20 000
≥ 5000 ppb

# samples
total fumo-
nisins
(EC recomm.
Mycotoxin Year ppb pigs/horses)

2009 253 10.3 % 6.3 % 17.0 % 17.0 % 27.3 % 1.6 % 28.9 %

2010 70 11.4 % 2.9 % 11.4 % 7.1 % 8.6 % 0.0 % 8.6 %
Total fu-
2011 229 21.8 % 3.1 % 4.4 % 5.7 % 1.3 % 0.0 % 1.3 %
monisin
B1 , B2 2012 358 39.1 % 0.8 % 3.6 % 1.1 % 1.1 % 0.0 % 1.1 %
2013 584 25.0 % 2.9 % 6.8 % 3.1 % 1.5 % 0.2 % 1.7 %
2014 314 23.6 % 3.8 % 4.5 % 2.9 % 3.2 % 0.0 % 3.2 %

100–149

150–399
10–49

50–79

80–99
5–9.9
# samples

≥ 400
≥ 50 ppb OTA
(EC recomm.
Mycotoxin Year ppb pigs)

2004 25 4.0 % 4.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %

2005 27 3.7 % 11.1 % 0.0 % 0.0 % 0.0 % 7.4 % 3.7 % 11.1 %
2006 49 0.0 % 2.0 % 2.0 % 0.0 % 0.0 % 2.0 % 0.0 % 4.1 %
2007 12 8.3 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2008 38 0.0 % 5.3 % 2.6 % 0.0 % 0.0 % 0.0 % 0.0 % 2.6 %
OTA 2009 139 6.5 % 2.9 % 0.0 % 0.0 % 0.0 % 2.9 % 0.0 % 2.9 %
2010 90 3.3 % 3.3 % 0.0 % 0.0 % 0.0 % 1.1 % 0.0 % 1.1 %
2011 261 8.0 % 6.1 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2012 400 9.0 % 5.0 % 1.5 % 0.0 % 0.0 % 0.0 % 0.0 % 1.5 %
2013 614 3.3 % 6.0 % 0.3 % 0.0 % 0.5 % 0.8 % 0.2 % 1.8 %
2014 259 2.7 % 0.4 % 0.4 % 0.0 % 0.0 % 0.0 % 0.0 % 0.4 %

Tab. 7.3: Results of the BIOMIN Mycotoxin Survey for samples sourced in central Europe.
1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples

≥ 900 ppb DON

(EC recomm.
Mycotoxin Year ppb pigs)

2004 502 24.5 % 15.5 % 0.6 % 3.2 % 1.2 % 0.4 % 0.2 % 5.6 %
2005 496 4.8 % 22.8 % 1.0 % 6.7 % 2.0 % 0.0 % 0.0 % 9.7 %
2006 595 4.5 % 24.7 % 3.0 % 13.1 % 6.2 % 1.5 % 0.0 % 23.9 %
2007 478 11.3 % 29.7 % 2.9 % 11.3 % 6.1 % 1.9 % 3.3 % 25.5 %
2008 620 10.0 % 35.3 % 2.7 % 11.6 % 5.8 % 1.1 % 0.2 % 21.5 %
DON 2009 964 10.3 % 23.8 % 1.1 % 6.2 % 2.4 % 0.1 % 0.0 % 9.9 %
2010 972 9.1 % 29.2 % 2.4 % 9.6 % 5.9 % 2.3 % 1.4 % 21.5 %
2011 1040 10.0 % 31.3 % 1.9 % 10.8 % 7.9 % 0.8 % 0.6 % 21.9 %
2012 1158 22.5 % 23.7 % 2.2 % 6.9 % 4.6 % 0.5 % 0.4 % 14.6 %
2013 1331 17.3 % 26.0 % 1.5 % 8.3 % 6.5 % 0.3 % 0.1 % 16.8 %
2014 568 23.8 % 30.1 % 3.0 % 6.2 % 2.8 % 0.7 % 0.2 % 12.9 %
 7 Climate change impacts on mycotoxin production | 143

Tab. 7.3 (continued)

500–1999
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples
≥ 100 ppb ZEN
(EC recomm.
Mycotoxin Year ppb pigs)

2004 480 0.8 % 0.8 % 0.8 % 0.0 % 0.6 % 0.2 % 0.2 % 1.9 %
2005 220 4.1 % 9.1 % 5.0 % 1.4 % 1.4 % 0.5 % 0.0 % 8.2 %
2006 393 2.5 % 6.1 % 8.1 % 3.1 % 3.8 % 2.8 % 2.5 % 20.4 %
2007 295 14.2 % 11.2 % 5.8 % 1.0 % 3.1 % 1.7 % 0.7 % 12.2 %
2008 382 7.3 % 9.4 % 6.3 % 0.8 % 1.3 % 0.8 % 0.0 % 9.2 %
ZEN 2009 814 6.0 % 6.1 % 4.8 % 1.6 % 2.7 % 1.5 % 0.0 % 10.6 %
2010 643 6.1 % 7.3 % 7.6 % 1.6 % 1.1 % 0.6 % 0.0 % 10.9 %
2011 669 10.9 % 10.9 % 10.0 % 1.3 % 2.7 % 1.3 % 0.0 % 15.4 %
2012 829 12.9 % 4.8 % 2.5 % 0.2 % 1.4 % 0.4 % 0.0 % 4.6 %
2013 930 6.8 % 4.0 % 2.4 % 0.5 % 0.4 % 0.2 % 0.2 % 3.8 %
2014 442 12.2 % 5.2 % 2.7 % 0.7 % 1.1 % 0.2 % 0.0 % 4.8 %
10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200 ≥ 5 ppb AfB1

(EC max for
Mycotoxin Year ppb dairy cattle)

2007 52 13.5 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %

2008 34 5.9 % 0.0 % 0.0 % 8.8 % 2.9 % 11.8 %
Total 2009 286 25.5 % 6.3 % 4.2 % 0.3 % 0.3 % 11.2 %
aflatoxin 2010 29 13.8 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
B1 , B2 , 2011 26 15.4 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
G 1 , G2 2012 119 10.1 % 1.7 % 2.5 % 2.5 % 0.0 % 6.7 %
2013 357 15.7 % 3.6 % 3.9 % 3.6 % 0.0 % 11.2 %
2014 169 21.3 % 0.0 % 0.0 % 0.6 % 0.0 % 0.6 %
5000–19 999
1000–1499

1500–2999

3000–4999
200–999

≥ 20 000

≥ 5000 ppb
# samples

total fumo-
nisins
(EC recomm.
Mycotoxin Year ppb pigs/horses)

2007 42 45.2 % 11.9 % 19.0 % 11.9 % 4.8 % 0.0 % 4.8 %

2008 15 13.3 % 0.0 % 13.3 % 0.0 % 26.7 % 0.0 % 26.7 %
2009 233 11.2 % 5.6 % 16.3 % 17.2 % 28.8 % 1.7 % 30.5 %
Total fu-
2010 41 9.8 % 0.0 % 0.0 % 0.0 % 9.8 % 0.0 % 9.8 %
monisin
B1 , B2 2011 88 19.3 % 4.5 % 4.5 % 0.0 % 0.0 % 0.0 % 0.0 %
2012 111 4.5 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2013 290 10.3 % 2.4 % 2.1 % 0.7 % 0.0 % 0.0 % 0.0 %
2014 200 19.0 % 2.0 % 1.0 % 0.0 % 1.0 % 0.0 % 1.0 %
144 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

Tab. 7.3 (continued)

100–149

150–399
10–49

50–79

80–99
5–9.9
# samples

≥ 400
≥ 50 ppb OTA
(EC recomm.
Mycotoxin Year ppb pigs)

2004 14 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %

2005 14 7.1 % 7.1 % 0.0 % 0.0 % 0.0 % 14.3 % 0.0 % 14.3 %
2006 27 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2007 9 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2008 24 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
OTA 2009 119 6.7 % 2.5 % 0.0 % 0.0 % 0.0 % 3.4 % 0.0 % 3.4 %
2010 46 0.0 % 6.5 % 0.0 % 0.0 % 0.0 % 2.2 % 0.0 % 2.2 %
2011 76 3.9 % 2.6 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2012 135 3.7 % 3.0 % 2.2 % 0.0 % 0.0 % 0.0 % 0.0 % 2.2 %
2013 313 1.9 % 8.0 % 0.0 % 0.0 % 0.0 % 0.3 % 0.0 % 0.3 %
2014 162 1.2 % 0.0 % 0.6 % 0.0 % 0.0 % 0.0 % 0.0 % 0.6 %

Tab. 7.4: Results of the BIOMIN Mycotoxin Survey for samples sourced in southern Europe.
1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples

≥ 900 ppb DON

(EC recomm.
Mycotoxin Year ppb pigs)

2008 33 9.1 % 45.5 % 3.0 % 9.1 % 0.0 % 0.0 % 0.0 % 12.1 %

2009 281 9.6 % 12.5 % 2.1 % 1.4 % 1.1 % 0.0 % 0.0 % 4.6 %
2010 63 14.3 % 20.6 % 0.0 % 4.8 % 1.6 % 0.0 % 0.0 % 6.3 %
DON 2011 147 8.2 % 17.7 % 1.4 % 4.1 % 4.8 % 0.0 % 0.0 % 10.2 %
2012 215 19.5 % 7.0 % 0.5 % 1.9 % 0.5 % 0.0 % 0.5 % 3.3 %
2013 342 21.3 % 12.6 % 0.0 % 3.8 % 0.6 % 0.0 % 0.3 % 4.7 %
2014 84 7.1 % 20.2 % 1.2 % 9.5 % 3.6 % 0.0 % 0.0 % 14.3 %
500–1999
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples

≥ 100 ppb ZEN

(EC recomm.
Mycotoxin Year ppb pigs)

2009 268 7.1 % 9.0 % 11.6 % 4.5 % 7.1 % 2.2 % 0.0 % 25.4 %
2010 47 4.3 % 8.5 % 4.3 % 2.1 % 0.0 % 0.0 % 0.0 % 6.4 %
2011 133 5.3 % 3.0 % 2.3 % 0.0 % 2.3 % 1.5 % 0.0 % 6.0 %
ZEN
2012 193 4.1 % 0.5 % 3.1 % 0.0 % 0.5 % 1.0 % 0.0 % 4.7 %
2013 306 6.2 % 3.3 % 2.3 % 0.3 % 0.7 % 0.3 % 0.0 % 3.6 %
2014 80 17.5 % 6.3 % 3.8 % 2.5 % 0.0 % 3.8 % 0.0 % 10.0 %
 7 Climate change impacts on mycotoxin production | 145

Tab. 7.4 (continued)

10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200
≥ 5 ppb AfB1
(EC max for
Mycotoxin Year ppb dairy cattle)

2008 21 23.8 % 4.8 % 0.0 % 4.8 % 0.0 % 9.5 %

2009 253 28.9 % 7.9 % 4.7 % 0.4 % 0.4 % 13.4 %
Total 2010 34 29.4 % 5.9 % 2.9 % 2.9 % 0.0 % 11.8 %
aflatoxin
2011 126 24.6 % 3.2 % 2.4 % 0.8 % 0.0 % 6.3 %
B1 , B2 ,
G 1 , G2 2012 173 29.5 % 3.5 % 1.7 % 2.9 % 0.0 % 8.1 %
2013 286 29.7 % 11.9 % 3.1 % 2.8 % 0.0 % 17.8 %
2014 55 40.0 % 1.8 % 1.8 % 3.6 % 1.8 % 9.1 %

5000–19 999
1000–1499

1500–2999

3000–4999
200–999

≥ 20 000
≥ 5000 ppb
# samples

total fumo-
nisins
(EC recomm.
Mycotoxin Year ppb pigs/horses)

2009 225 10.2 % 7.1 % 18.2 % 19.1 % 30.2 % 1.8 % 32.0 %

2010 24 8.3 % 8.3 % 33.3 % 20.8 % 8.3 % 0.0 % 8.3 %
Total fu-
2011 105 25.7 % 2.9 % 4.8 % 10.5 % 1.9 % 0.0 % 1.9 %
monisin
B1 , B2 2012 166 60.2 % 0.6 % 7.2 % 2.4 % 2.4 % 0.0 % 2.4 %
2013 231 39.8 % 3.9 % 11.7 % 6.1 % 3.9 % 0.4 % 4.3 %
2014 65 33.8 % 7.7 % 18.5 % 12.3 % 10.8 % 0.0 % 10.8 %

It is noteworthy that more than 10 % of samples tested each year originating from
different European countries, especially from central Europe, showed levels of DON
exceeding the EC recommended level of 900 ppb. In 2006, 2008, 2010, and 2011 more
than 20 % of the samples tested exceeded this level, and 2007 can be considered the
DON-contamination peak year, as one-fourth of the samples was above 900 ppb. Com-
pared to worldwide results, the contamination of ZEN in all European samples, mainly
originating from central Europe, was relatively lower. However, between 4.1 % and
19.7 % of all samples was above the EC recommended level of 100 ppb. Comparable
with the global results, the ZEN-contamination peak year in Europe was also 2006.
Until a few years ago, aflatoxins were not considered an actual threat in Europe.
However, the results from the mycotoxin survey illustrate that 3.5 % to 14.2 % of Eu-
ropean samples contain concentrations above the European guideline of 5 ppb afla-
toxin B1 for feed intended for dairy. As expected, Europe experienced the highest afla-
toxin contamination in 2013. In the first quarter of 2013, several European countries,
including Romania, Serbia, and Croatia, reported that milk for human consumption
had been contaminated with aflatoxins. Thereafter, feed originating from Serbia im-
ported to the Netherlands and Germany appeared to be contaminated with aflatoxins.
Fumonisins are also not recognized as a threat in Europe. Nonetheless, in 2009 almost
29 % of the European samples tested contained concentrations above the 5000 ppb EC
recommended level. The contamination of ochratoxins in Europe showed a peak in
146 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

2005 with 11.1 % of samples containing concentrations above the EC recommendation

of 50 ppb for feed intended for pigs.
The results for samples sourced in central Europe presented in Tab. 7.3 are very
similar to those for all European samples. The results show that 2008, 2009, and 2013
were peak years in terms of aflatoxin contamination, as the concentration of more
than 11 % of the samples tested in these periods were above the 5 ppb EU guidance
level for feed for dairy cows. These results should raise the awareness of the problem
of aflatoxins in a region where these toxins were not previously considered a problem.
As expected, the aflatoxin contamination was higher in southern Europe than in
central European countries. The highest concentrations were observed in 2013, as the
concentration of almost 18 % of all samples tested was above the 5 ppb EU maximum
level (Tab. 7.4). The fumonisin levels in southern European countries were also higher
than in central Europe. In 2009, the concentrations of zearalenone were at a peak in
southern Europe, with 25 % of samples above the 100 ppb EC recommendation for feed
intended for pigs. The results for the first half of 2014 show high concentrations of
ZEN and DON in this region. The co-occurrence of zearalenone and DON is a known
phenomenon, as both mycotoxins are produced by the same fungus.
In the past decade, a total of 2738 corn samples (Tab. 7.5) and 1714 wheat samples
(Tab. 7.6) originating from Europe have been analyzed for their mycotoxin content. Eu-
ropean wheat showed the highest DON contamination in 2005, 2008, 2012, and 2013.
During these years more than 20 % of the samples contained DON at concentrations
above the EC recommended value of 900 ppb. The DON-contamination peak was ob-
served in the first half of 2014, when the concentrations of almost 36 % of the samples
tested were above 900 ppb. The highest aflatoxin concentrations in wheat were ob-
served in 2009 with almost 15 % of the samples above the EU maximum of 5 ppb for
feed intended for dairy cows.

Tab. 7.5: Results of the BIOMIN Mycotoxin Survey for corn and corn silage samples sourced in Europe.
1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples

≥ 900 ppb DON

(EC recomm.
Mycotoxin Year ppb pigs)

2004 148 25.0 % 22.3 % 1.4 % 4.1 % 0.0 % 0.7 % 0.0 % 6.1 %
2005 192 7.3 % 27.6 % 1.0 % 10.9 % 6.8 % 0.0 % 0.0 % 18.8 %
2006 214 1.4 % 36.0 % 6.5 % 21.5 % 11.7 % 2.3 % 0.0 % 42.1 %
2007 159 6.3 % 44.7 % 5.0 % 18.2 % 9.4 % 0.6 % 1.9 % 35.2 %
2008 234 9.4 % 37.6 % 2.1 % 16.2 % 9.4 % 2.1 % 0.4 % 30.3 %
DON 2009 280 13.2 % 36.1 % 1.1 % 6.8 % 4.3 % 0.4 % 0.0 % 12.5 %
2010 254 7.9 % 31.5 % 2.0 % 14.2 % 11.0 % 8.7 % 2.8 % 38.6 %
2011 400 7.5 % 31.3 % 2.0 % 15.0 % 14.0 % 1.8 % 0.8 % 33.5 %
2012 329 24.0 % 25.8 % 3.6 % 5.8 % 2.1 % 0.0 % 0.3 % 11.9 %
2013 405 12.1 % 26.2 % 0.7 % 10.4 % 6.4 % 0.7 % 0.0 % 18.3 %
2014 193 10.4 % 27.5 % 4.7 % 7.3 % 2.6 % 0.5 % 0.0 % 15.0 %
 7 Climate change impacts on mycotoxin production | 147

Tab. 7.5 (continued)

500–1999
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples
≥ 100 ppb ZEN
(EC recomm.
Mycotoxin Year ppb pigs)

2004 139 1.4 % 1.4 % 1.4 % 0.0 % 1.4 % 0.0 % 0.0 % 2.9 %
2005 70 2.9 % 12.9 % 10.0 % 2.9 % 7.1 % 2.9 % 0.0 % 22.9 %
2006 119 4.2 % 16.0 % 19.3 % 6.7 % 9.2 % 2.5 % 1.7 % 39.5 %
2007 85 11.8 % 18.8 % 12.9 % 2.4 % 5.9 % 2.4 % 0.0 % 23.5 %
2008 125 11.2 % 8.0 % 11.2 % 2.4 % 2.4 % 1.6 % 0.0 % 17.6 %
ZEN 2009 200 2.5 % 7.0 % 3.5 % 0.5 % 0.5 % 0.0 % 0.0 % 4.5 %
2010 188 9.0 % 13.3 % 19.1 % 3.7 % 2.1 % 1.1 % 0.0 % 26.1 %
2011 241 12.9 % 7.5 % 12.0 % 1.2 % 3.7 % 3.7 % 0.0 % 20.7 %
2012 248 8.1 % 4.4 % 1.6 % 0.4 % 1.6 % 0.8 % 0.0 % 4.4 %
2013 338 12.1 % 8.3 % 5.9 % 1.5 % 2.4 % 1.2 % 0.6 % 11.5 %
2014 164 11.6 % 14.0 % 4.3 % 1.8 % 1.8 % 0.6 % 0.0 % 8.5 %
10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200 ≥ 5 ppb AfB1

(EC max for
Mycotoxin Year ppb dairy cattle)

Total 2011 51 29.4 % 2.0 % 3.9 % 2.0 % 0.0 % 7.9 %

aflatoxin 2012 74 17.6 % 4.1 % 2.7 % 1.4 % 0.0 % 8.1 %
B1 , B2 , 2013 213 11.3 % 5.2 % 4.7 % 3.3 % 0.0 % 13.1 %
G 1 , G2 2014 83 28.9 % 0.0 % 0.0 % 3.6 % 0.0 % 3.6 %
5000–19 999
1000–1499

1500–2999

3000–4999
200–999

≥ 20 000

≥ 5000 ppb
# samples

total fumo-
nisins
(EC recomm.
Mycotoxin Year ppb pigs/horses)

2011 72 31.9 % 8.3 % 8.3 % 8.3 % 11.1 % 0.0 % 11.1 %

Total fu-
2012 63 36.5 % 0.0 % 12.7 % 4.8 % 3.2 % 0.0 % 3.2 %
monisin
B1 , B2 2013 169 21.3 % 4.1 % 13.6 % 7.7 % 3.6 % 0.6 % 4.1 %
2014 82 24.4 % 7.3 % 6.1 % 7.3 % 1.2 % 0.0 % 1.2 %
100–149

150–399
10–49

50–79

80–99
5–9.9
# samples

≥ 400

≥ 50 ppb OTA
(EC recomm.
Mycotoxin Year ppb pigs)

2011 41 2.4 % 9.8 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %

2012 85 1.2 % 3.5 % 1.2 % 0.0 % 0.0 % 0.0 % 0.0 % 1.2 %
OTA
2013 168 3.0 % 3.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2014 79 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
148 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

Tab. 7.6: Results of the BIOMIN Mycotoxin Survey for wheat samples sourced in Europe.

1000–1999

2000–4999

5000–7999
100–299

300–899

900–999

≥ 8000
# samples
≥ 900 ppb DON
(EC recomm.
Mycotoxin Year ppb pigs)

2004 98 34.7 % 28.6 % 1.0 % 4.1 % 7.1 % 1.0 % 1.0 % 14.3 %

2005 87 5.7 % 21.8 % 3.4 % 16.1 % 2.3 % 0.0 % 0.0 % 21.8 %
2006 95 10.5 % 16.8 % 0.0 % 9.5 % 2.1 % 0.0 % 0.0 % 11.6 %
2007 66 1.5 % 19.7 % 3.0 % 6.1 % 1.5 % 4.5 % 1.5 % 16.7 %
2008 159 3.8 % 41.5 % 5.0 % 10.7 % 6.9 % 1.3 % 0.0 % 23.9 %
DON 2009 374 5.6 % 18.4 % 1.1 % 4.5 % 2.1 % 0.0 % 0.0 % 7.8 %
2010 194 6.7 % 28.4 % 3.1 % 7.2 % 4.6 % 0.0 % 2.1 % 17.0 %
2011 202 5.4 % 31.7 % 2.0 % 5.9 % 3.0 % 0.5 % 0.5 % 11.9 %
2012 253 13.8 % 32.4 % 3.2 % 11.1 % 10.3 % 2.0 % 0.8 % 27.3 %
2013 332 13.0 % 28.0 % 1.5 % 12.3 % 8.7 % 0.3 % 0.3 % 23.2 %
2014 56 14.3 % 19.6 % 3.6 % 17.9 % 10.7 % 3.6 % 0.0 % 35.7 %

500–1999
100–199

200–249

250–499

≥ 2000
20–49

50–99
# samples

≥ 100 ppb ZEN

(EC recomm.
Mycotoxin Year ppb pigs)

2004 96 6.3 % 5.2 % 2.1 % 2.1 % 1.0 % 1.0 % 1.0 % 7.3 %

2005 54 3.7 % 13.0 % 0.0 % 5.6 % 7.4 % 1.9 % 0.0 % 14.8 %
2006 63 3.2 % 0.0 % 4.8 % 0.0 % 0.0 % 0.0 % 0.0 % 4.8 %
2007 37 2.7 % 0.0 % 0.0 % 0.0 % 2.7 % 0.0 % 0.0 % 2.7 %
2008 103 5.8 % 17.5 % 4.9 % 0.0 % 1.9 % 1.0 % 0.0 % 7.8 %
ZEN 2009 346 5.5 % 6.9 % 8.4 % 3.5 % 5.5 % 1.7 % 0.0 % 19.1 %
2010 97 3.1 % 3.1 % 4.1 % 0.0 % 1.0 % 0.0 % 0.0 % 5.2 %
2011 144 2.1 % 6.3 % 6.9 % 1.4 % 1.4 % 0.7 % 0.0 % 10.4 %
2012 162 12.3 % 3.1 % 6.2 % 0.6 % 2.5 % 1.2 % 0.0 % 10.5 %
2013 213 1.9 % 1.4 % 0.5 % 0.0 % 0.0 % 0.0 % 0.0 % 0.5 %
2014 45 4.4 % 2.2 % 6.7 % 0.0 % 0.0 % 0.0 % 0.0 % 6.7 %
10–19.9

20–199
1–4.9

5–9.9
# samples

≥ 200

≥ 5 ppb AfB1
(EC max for
Mycotoxin Year ppb dairy cattle)

2009 222 32.0 % 8.6 % 5.4 % 0.5 % 0.5 % 14.9 %

Total 2010 14 14.3 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
aflatoxin 2011 22 36.4 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
B1 , B2 , 2012 15 13.3 % 6.7 % 0.0 % 0.0 % 0.0 % 6.7 %
G 1 , G2 2013 95 12.6 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2014 24 16.7 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
 7 Climate change impacts on mycotoxin production | 149

Tab. 7.6 (continued)

100–149

150–399
10–49

50–79

80–99
5–9.9
# samples

≥ 400
> 50 ppb (EC
recomm. Pigs)
Mycotoxin Year ppb

2010 19 5.3 % 0.0 % 0.0 % 0.0 % 0.0 % 5.3 % 0.0 % 5.3 %

2011 23 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
OTA 2012 30 6.7 % 3.3 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2013 94 1.1 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %
2014 24 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 % 0.0 %

In European corn and corn silage, the results for DON and ZEN showed similar trends
due to their common co-occurrence. In 2006, 2007, 2008, 2010, and 2011, over 30 %
of these samples contained concentrations of DON above the EC recommendation of
900 ppb. Accordingly, ZEN contamination was also high in the years mentioned. The
highest concentrations of both DON and ZEN were detected in 2006.

7.7 Conclusion

Food safety is undoubtedly linked to a complex web of different factors and would be
incomplete without taking the effects caused by climate change into consideration.
Weather extremes are clearly affecting fungal profiles, and consequently mycotoxin
patterns, on a worldwide scale and global trade makes mycotoxin prediction even
more difficult than it currently is. An integrated systems approach would be necessary
to warrant the accuracy of predictions. Constant monitoring and continual research
on the prevention and mitigation of mycotoxin contamination are therefore necessary.
The first steps towards preventing the negative effects of these harmful substances are
the implementation of good agricultural practices and proper storage conditions.

References

[1] EFSA 2012. Modelling, Predicting and Mapping the Emergence of Aflatoxins in Cereals in the EU
Due to Climate Change. EFSA Scientific Report; 2012.
[2] Miraglia M, Marvin HJP, Kleter GA. Climate change and food safety: An emerging issue with
special focus on Europe. Food and Chemical Toxicology 2009;47:1009–1021.
[3] Magan N, Medina A, Aldred D. Possible climate-change effects on mycotoxin contamination of
food crops pre- and postharvest. Plant Pathology 2011;60:150–163.
[4] IPCC 2014. Climate Change 2014: Impacts, Adaptation, and Vulnerability. IPCC Report 2014.
[5] Rosenzweig C, Yang XB, Anderson P, Epstein P, Vicarelli M. Agriculture: climate change, crop
pests and diseases. In: Epstein P,Mills E, eds Climate Change Futures: Health, Ecological and
Economic Dimensions 2005:70–77.
150 | Maria Paula Kovalsky Paris, Yin-Jung Liu, Karin Nahrer, and Eva Maria Binder

[6] Chakraborty S, Newton AC. Climate change, plant diseases and food security: an overview.
Plant Pathology 2011;60:2–14.
[7] Bebber D, Ramotowski MAT, Gurr SJ. Crop pests and pathogens move polewards in a warming
world. Nature climate change 2013.
[8] Burrows M, Schoeman DS, Buckley LB. The pace of shifting climate in marine and terrestrial
ecosystems. Science 2011;334:652–655.
[9] FA2008. Climate change: Implications for food safety. FAO Report 2008.
[10] Miller D, Richardson SN. Mycotoxins in Canada: A perspective for 2013. Regulatory Governance
Initiative Report 2013.
[11] Magan N. Fungi in extreme environments. In: Kubicek CP, Druzhinina IS, eds Environmen-
tal and Microbial Relationships TheMYCOTA IV 2nd ed. Berlin, Germany: Springer Verlag
2007:85–103.
[12] Sanchis V, Magan N. Environmental profiles for growth and mycotoxin production. In:
Magan N, Olsen M (eds.). Mycotoxins in Food: Detection and Control Cambridge, UK: Wood-
head Publishing Ltd 2004:174–189.
[13] Sant’Ana AS. Special issue on climate change and food science. Food Research International
2010;43:1727–1728.
[14] Paterson R, Lima N. Further mycotoxin effects from climate change. Food Research Interna-
tional 2011;44:2555–2566.
[15] Garrett K, Dendy SP, Frank EE, Rouie MN, Travers SE. Climate change effects on plant disease:
genomes to ecosystems. Annual Review of Phytopathology 2006;44:489–509.
[16] Boken V, Hoogenboom G, Williams JH, Diarra B, Dione S, Easson GL. Monitoring peanut con-
tamination in Mali (Africa) using the AVHRR satellite data and a crop simulation model. Inter-
national Journal of Remote Sensing 2008;29:117–129.
[17] Chauhan Y, Wright GC, Rachaputi NC. Modelling climatic risks of aflatoxin contamination in
maize. Australian Journal of Experimental Agriculture 2008;48:358–366.
[18] Paterson R, Lima N. How will climate change affect mycotoxins in food? Food Research Interna-
tional 2010;43:1902–1914.
[19] Schaafsma A, Hooker DC. Climatic models to predict occurrence of Fusarium toxins in wheat
and maize. International Journal of Food Microbiology 2007;119:116–125.
[20] Giorni P, Battilani P, Magan N. Effect of solute and matric potential on in vitro growth and
sporulation of strains from a new population of Aspergillus flavus isolated in Italy. Fungal
Ecology 2008;1:102–106.
[21] Ward T, Clear RM, Rooney AP. An adaptive evolutionary shift in fusarium head blight pathogen
populations is driving the rapid spread of more toxigenic Fusarium graminearum in North
America. Fungal Genetics and Biology 2008;45:473–484.
[22] Battilani P, Barbano C, Marin S, Sanchis V, Kozakiewicz Z, Magan N. Mapping of Aspergillus
section Nigri in Southern Europe and Israel based on geostatistical analysis. International
Journal of Food Microbiology 2006;111:72–82.
[23] Rossi V, Giosue S, Delogu G. A model estimating risk for Fusarium mycotoxins in wheat ker-
nels. Aspects of Applied Biology 2003a;68:229–234.
[24] Rossi V, Giosue S, Pattori E, Spanna F, Del Vechio A. A model estimating the risk of fusarium
head blight in wheat. EPPO Bulletin 33 2003b:421–425.
[25] de la Campa R, Hooker DC, Miller JD, Schaafsma AW, Hammond BG. Modelling the effects of
environment, insect damage, and Bt genotypes on fumonisin accumulation inmaize in Ar-
gentina and the Phillipines. Mycopathologia 2005;159:539–552.
[26] van der Fels-Klerx H, Kandhai MC, Brynestad S. Development of a European system for identifi-
cation of emerging mycotoxins in the wheat supply chain. World Mycotoxin Journal 2009;2:119.
 7 Climate change impacts on mycotoxin production | 151

[27] Beniston M, Diaz HF. The 2003 heat wave as an example of summers in a greenhouse climate?
Observations and climate model simulations for Basel, Switzerland. Global and Planetary
Change 2004;44:73–81.
[28] Tirado M, Clarke R, Jaykus LA, McQuatters-Gollop A, Frank JM. Climate change and food safety:
A review. Food Research International 2010;43:1745–1765.
[29] Medina A, Mateo R, Valle-Algarra FM, Mateo E, Jimenez M. Effect of carbendazim and physic-
ochemical factors on the growth and ochratoxin A production of Aspergillus carbonarius iso-
lated from grapes. International Journal of Food Microbiology 2007a;119:230–235.
[30] Medina A, Jimenez M, Mateo R, Magan N. Natamycin efficacy for control of growth and ochra-
toxin production by Aspergillus carbonarius isolates under different environmental regimes.
Journal of Applied Microbiology 2007b;103:2234–2239.
[31] Schmidt-Heydt M, Magan N, Geisen R. Stress induction of mycotoxin biosynthesis genes in
relation to abiotic factors. FEMS Microbiology Letters 2008;284:142–149.
[32] Schmidt-Heydt M, Abdel-Hadi A, Magan N, Geisen R. Complex regulation of the aflatoxin
biosynthesis gene cluster of A. flavus in relation to various combinations of water activity and
temperature. International Journal of Food Microbiology 2009;135:231–237.
[33] Serra R, Lourenço A, Alípio P, Venâncio A. Influence of the region of origin on the mycobiota
of grapes with emphasis on Aspergillus and Penicillium species. Mycological Research
2006;110:971–978.
[34] Serra R, Mendonca C, Venancio A. Ochratoxin A occurrence and formation in Portuguese
wine grapes at various stages of maturation. International Journal of Food Microbiology
2006;111:35–39.
[35] Varga J, Koncz Z, Kocsube S. Mycobiota of grapes collected in Hungarian and Czech vineyards
in 2004. Acta Alimentaria 2007;36:329–341.
[36] European Commission 2006. COMMISSION RECOMMENDATION of 17 August 2006 on the pres-
ence of deoxynivalenol, zearalenone, ochratoxin A, T-2 and HT-2 and fumonisins in products
intended for animal feeding. 2006.
[37] European Parliament 2002. DIRECTIVE 2002/32/EC OF THE EUROPEAN PARLIAMENT AND OF THE
COUNCIL of 7 May 2002 on undesirable substances in animal feed. 2002.
María J. Sainz, Amparo Alfonso, and Luis M. Botana
8 Considerations about international mycotoxin
legislation, food security, and climate change

8.1 Introduction

Mycotoxins are low molecular-weight products (250 to 720 Da) with different chemi-
cal structure and activity. These compounds are secondary metabolites produced by
species of several fungal genera, primarily Fusarium, Aspergillus, Penicillium, Clavi-
ceps, and Alternaria, which can colonize plants cultivated for human and/or animal
consumption. The infection can occur either in the field or after harvesting, during
storage, transport, and processing. Warm temperatures and high humidity are key
factors for growth of mycotoxigenic fungi. This is why food and feed contaminated
with mycotoxins are most frequently found in the warmer agricultural regions of the
world, and also why climate change is expected to strongly affect their activity and
impact on plant production and quality [77].
More than 300 mycotoxins have been identified, but about 20 can be present nat-
urally in food and feeds at significant levels and frequently enough to become a food
safety concern [76]. Seven classes of mycotoxins frequently occur: aflatoxins, ochra-
toxin A, patulin, trichothecenes, zearalenone, fumonisins, and ergot alkaloids. These
compounds are not affected by temperature or long-term storage and are chemically
stable under manufacturing conditions. Different toxic effects, acute or chronic, have
been associated with these fungal metabolites, such as carcinogenicity, nephrotoxi-
city, hepatotoxicity, reproductive problems, gastrointestinal effects, immunosuppres-
sion, skin problems, and central nervous system disorders. Mycotoxins therefore rep-
resent a major concern for human health and cause significant economic losses in
many production areas. Most countries have developed continuous monitoring pro-
grams and adopted regulations to limit exposure to these compounds in order to avoid
intoxication because mycotoxins contaminate food and feed, both raw and processed
materials. In order to prevent and reduce risks for consumers and to minimize the
economic impact caused by the presence of these substances, public administrations
pass regulations regarding permissible levels of mycotoxins in foodstuffs and official
controls. To this end, a broad range of analytical techniques are available for detection
and quantification of mycotoxins, however highly sensitive methods are still neces-
sary in order to avoid food poisoning and to guarantee the detection of known and
new contaminants. Besides, mycotoxins are not homogeneously distributed in prod-
uct lots; in addition to the detection method, the sampling plan therefore plays a cru-
cial part in identifying these products. Thus, the criteria that both sampling and de-
tection methods should comply have already been fixed by several regulations in the
European Union [74, 75]. In the case of detection methods, the performance criteria
154 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

are independent of the method used and are addressed to ensure that control labora-
tories use analysis techniques with minimum performance characteristics to achieve
comparable levels of operation, since no official detection methods have been estab-
lished. This is a fundamental difference compared to marine toxins, basically because
mycotoxins pose a chronic risk, while phycotoxins are mostly an acute food risk [73]; a
specific validated method has been implemented for marine toxins in the Commission
Regulation (EU) No 15/2011 of January 10, 2011 [72].

8.1.1 Main mycotoxins

Aflatoxins are produced by several species of Aspergillus genus, manly A. flavus and
A. parasiticus. This group of compounds includes aflatoxin B1 , B2 , G1 , and G2 . Aflatox-
ins are difuranocoumarin derivatives which can be metabolized in the liver through
the cytochrome-P450 family to epoxide or hydroxylated derivatives. These toxins are
found primarily in warm and humid climates and contaminate crops and raw materi-
als of cereals, oilseeds, spices, fruits, cottonseed, and nuts [71]. Aflatoxin B1 is the most
toxic and carcinogenic to humans and animals, with an LD50 (mean lethal dose; lethal
dose, 50 %) of between 0.3 and 18 mg/kg depending on the route of administration and
the animal species [70]. When ruminants are fed with aflatoxin B1 -contaminated feed-
stuffs, AFB1 is metabolized in the liver to secondary metabolites. The major metabolite
is the hydroxylated metabolite aflatoxin M1 (AFM1 ) which is excreted into milk and can
be found in milk and other dairy products [69]. AFM1 is considered a possible human
carcinogen by the IARC.
Ochratoxin A is a phenylalanine-dihydroisocoumarin derivative produced by
Aspergillus and Penicillium genera. This compound is found as a contaminant in
crops and raw materials of cereals, spices, cocoa, coffee, dry grapes, wine, and pork
and chicken meat [71]. This toxin is structurally similar to the amino acid pheny-
lalanine and can therefore participate in cellular pathways where the amino acid is
involved [68]. The LD50 of ochratoxin A ranges from 50 mg/kg for dogs to 0.5 mg/kg
for mice [70].
Trichothecenes are tetracyclic sesquiterpenoids produced by several Fusarium
species. There are more than 170 identified compounds divided into four types, A–D.
The main representatives are HT-2 and T-2 toxins, from type A group, and deoxyni-
valenol from type B group. These toxins can be found in cereals and toxic effects such
as gastroenteritis, intestinal hemorrhage, immunosuppression, and dermatotoxicity
have been associated with exposure to them.
Fumonisins are a group of compounds produced by several Fusarium species
found in maize from warm regions. These toxins, structurally similar to the sph-
ingolipid precursor sphinganine, interfere with sphingosine synthesis leading to
cytotoxic compounds which are carcinogenic and neurotoxic. At least 12 fumonisin
 8 International mycotoxin legislation, food security, and climate change | 155

analogs are known. Fumonisin B1 , B2 , and B3 are the most important compounds
within this group.
Zearalenone is a lactone produced by several Fusarium species, found as a con-
taminant in cereals and maize oil with estrogenic activity.
Patulin is an unsaturated heterocyclic lactone mainly produced by Penicillium
expansum, but also by species of Aspergillus, Byssochlamys, Eupenicillium, and Pae-
cilomyces. This compound has high affinity with sulfhydryl groups and consequently
is involved in several enzymatic processes. Patulin induces acute symptoms such as
lung and brain edema, liver, spleen and kidney damage, and is toxic for the immune
system. In addition, patulin is related to protein synthesis inhibition. The LD50 oscil-
lates between 15 and 25 mg/kg [70]. This toxin has been detected in apples and apple
products, although high contamination levels have rarely been reported.
Species of the genus Claviceps, notably C. purpurea, infect seed heads, usually of
rye, replacing the developing grain with the sclerotium of ergot which contains alka-
loids.
Ergot alkaloids are tetracyclic compounds, derived from 6-methylergoline, which
are produced by Claviceps species. These mycotoxins can be partial agonist or antag-
onist of adrenergic, dopaminergic, and serotoninergic receptors. Ischemias of the ex-
tremities, miscarriage, and central disorders have been described after consumption
of grain infected by the fungi.
Alternaria species, particularly A. alternata, infect a wide range of crops, such as
cereals, both pre- and postharvest, and produce alternariol, alternariol monomethyl
ether, altertoxins I–III, altenuene, and tenuazonic acid. Their toxic effects are com-
plex, but esophageal cancer has been proposed after epidemiologic studies in China
[67].
In addition to trichothecenes, zearalenone, and fumonisins, other emerging
Fusarium toxins such as fusaproliferin, enniatins, beauvericin, moniliformin, and
modified forms of DON, ZON, NIV, FUM, and T-2 and HT-2 toxins have been reported.
These compounds have different structures and are not yet regulated, although several
toxic effects have been described after cellular exposition of these toxins.

8.2 Impacts of climate change on agriculture

The observed increases in average global air and ocean temperatures, widespread
melting of snow and ice, and the rising of average global sea level since the beginning
of the 20th century are evidence of the process of global warming [66]. Global land-
ocean temperature in the decade 2000–2010 was about 0.8 °C warmer than at the be-
ginning of the 20th century, and two thirds of the warming occurred since 1975 [65].
Further to this, global climate models have shown a greater than 90 % probability
that the hottest seasons on record will represent the future norm in many temperate
locations, and that growing season temperatures in the tropics and subtropics will ex-
156 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

ceed the most extreme seasonal temperatures recorded in the 20th century [64]. All
cropland areas are thus expected to experience some degree of warming, with the
largest change being predicted in high latitudes, and small increases in temperature,
although probably with a significant impact on agriculture, in low latitudes [63].
Currently ca 1600 Mha of the world are cultivated, of which 1300 Mha (80 %) are
rainfed and produce about 60 % of the global crop output, with the most productive
systems concentrated in the temperate zones of Europe, followed by northern America
and areas in the subtropics and humid tropics [62]. Irrigated agriculture account for
the remaining 20 % of arable land, providing 40 % of total crop production (nearly
60 % of cereal production) [61]. Although irrigated agriculture is expected to increase
to provide 47 % of global crop production by 2030, rainfed agriculture will remain an
important contributor to global food production [61, 62]. Any precipitation change,
especially changes in seasonal precipitation, will thus greatly influence the magni-
tude and direction of climate impacts on water availability, crop production, and food
security [63]. Although projections of precipitation change in climate models depend
on the relative rates of warming in all regions, a general increase in precipitation is
expected in high latitudes, especially in winter, and an overall decrease in many parts
of the tropics and subtropics [66].
Agricultural productivity and food security worldwide are thus expected to be
strongly affected by climate change in the coming decades, with higher risk and vul-
nerability of crop production related to higher temperatures [64], water supply, and
water availability [60]. Although, as reported in a recent review [63], greater risks for
food security might be posed by changes in year-to-year climate variability and ex-
treme weather events, such as extreme temperatures, drought, heavy rainfall, and
flooding. Climate change is expected to increase the incidence and severity of crop
pests and diseases [59], and might also have a significant effect on mycotoxins [58].
Mycotoxigenic fungi can infect cereals in the field and during storage. In the field,
the most frequent fungal species belong to the genus Fusarium. Aspergillus species can
infect plants in the field, especially if crops suffer drought stress or insect attack, but
usually develop, as Penicillium species, postharvest under poor storage conditions.
A large number of Fusarium species are important pathogens for nearly all economi-
cally important plant species.
Of particular relevance are cereals, the world’s most important source of food and
feed, which occupy more than half of the world’s harvested area [57], and are common
hosts for Fusarium and Aspergillus. For 2014, the world cereal production was forecast
at 2525 million tons, the forecast world cereal utilization was put at 2416 million tons,
of which 1094 million tons were destined for food and 851 million tons for feed use,
and the world cereal trade was forecast at 356 million tons, all figures higher than
those reached in 2013 [56].
Improved sampling and analytical methods for mycotoxins should be developed
to determine any climate change effects on the mycotoxin contamination of food and
feeds [58].
 8 International mycotoxin legislation, food security, and climate change | 157

8.3 Detection methods

The presence of mycotoxins in food and feedstuffs can be checked by fast and simple
methods, employed as rapid screening tools, and with sophisticated analytical meth-
ods useful for identification and quantification of the amount of each toxin. A detec-
tion method should be sensitive, robust, reproducible, and applicable to a wide range
of compounds. The screening methods used to detect the presence or absence of toxins
are rapid, economic and simple, no skilled personnel is necessary and limited or no
sample treatment is required. In contrast, analytical methods are expensive and time-
consuming and often require sample pre-treatment. These methods are usually based
on liquid chromatography coupled with different detectors, therefore trained person-
nel is required. In addition to the detection method, the collection of representative
samples and the sample extraction protocol are critical issues in obtaining accurate
results.

8.3.1 Sampling procedures

As already mentioned, mycotoxins are heterogeneously distributed in food lots with

large particle size such as dried figs, groundnuts, or fruits. The distribution of myco-
toxins in processed products is generally less heterogeneous than in unprocessed
food. The sampling procedure should therefore be different in each case. Taking this
into account, the European Commission has established methods of sampling for of-
ficial controls of the levels of mycotoxins in foodstuffs [74, 75]. These official controls
shall be in accordance with provisions of regulations about animal feed and food
laws, animal health and animal welfare regulations, the maximum limits for certain
mycotoxins, and the sampling criteria for the control of levels of these compounds
[53–55, 75]. Depending on the sample, the size of the lot, on volume and weight,
the number of incremental samples and the volume or weight of aggregate samples
should be different. All of these parameters have recently been clearly established and
the variability in results due to the sampling procedure can almost be eliminated [74].

8.3.2 Extraction procedures

The presence of mycotoxins is often analyzed in many different matrices, from food
and feedstuffs to processed products. In some cases, therefore, other substances such
as salts, proteins, oils, lipids, or sugars can interfere with the analysis. In addition, the
amount of toxins is sometimes small and can be masked by interfering compounds.
For these reasons, extraction and several cleanup steps are sometimes necessary be-
fore mycotoxin analysis.
158 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

The initial extraction of toxins from solid matrices usually consists of a solid-
liquid extraction, employing organic solvents such as methanol or acetonitrile mixed
with water in different proportions and an acidic compound like acetic acid or formic
acid [52, 102, 103]. Polar molecules such as fumonisins and hydrophobic compounds
such as aflatoxins can thus be extracted. Depending on matrix interferences, different
operations can be performed after this. In the case of non-processed products, such
as wheat or maize, a centrifugation/filtration step might be enough and the extract
can be directly analyzed [52, 103]. In other cases, the solid-liquid extraction is fol-
lowed by a cleanup step using different strategies such as immunoaffinity columns
(IACs; [98–101]). These columns are toxin-selective and useful when only analyzing
one group of toxins. However, the availability of antibodies is limited and therefore
these columns are not appropriate for performing multi-toxin analysis. In addition,
IACs can only be used once, in consequence are expensive, and some mycotoxins can
be underestimated after this cleanup [97].
Other solid phase extraction (SPE) or in-tube solid-phase microextractions (SPME)
are also cleanup procedures used to avoid matrix effect [92–96]. SPE cartridges are less
expensive and less selective than IACs and are often used for mycotoxin analysis. Many
different column packings have been described for SPE cleanup, such as silica-gel, C18 ,
florisil or ion-exchange materials, as well as polymers and synthetic peptides [70, 71].
Further, other solid extraction procedures, such as selective or dispersive matrix solid-
phase have also been developed to clean and prepare samples from different matrices
[89–91]. However, mycotoxins have different chemical properties and universal car-
tridges are not available when multitoxin analysis is necessary.
Based on all these extractions and from technology developed for pesticide anal-
ysis of food and feedstuffs, the QuEChERS methodology (from Quick, Easy, Cheap,
Effective, Rugged and Safe) has been used to extract and clean samples for myco-
toxin analysis in different matrices [84–88, 102]. This methodology involves first an
extraction step based on partitioning with salt-out extraction, and then a dispersive
matrix solid-phase step. In this way, excess water, organic acids, fatty acids, lipids,
sugar, or pigments are eliminated. However, reduced mycotoxin recovery has been
reported [102].
Liquid-liquid partitions and dispersive liquid-liquid extractions have also been
used, either to extract and clean liquid samples, or to clean extracts from solid samples
[81–83]. Different solvents such as methanol, acetonitrile, acetone, ethyl acetate, chlo-
roform, diethyl ether or mixtures are selected for liquid-liquid extractions. In general,
polar solvents and pH play a key role during the extraction process. Two immiscible
liquid phases are used to clean samples. For this purpose, solvents such as hexane or
cyclohexane are used to eliminate nonpolar contaminants like lipids or cholesterol.
Supercritical fluids have also been used to extract aflatoxins and zearalenone deriva-
tives from different matrices [25, 78–80].
Using one or more of the above-mentioned procedures can therefore eliminate
the matrix effect and the final extract can be directly analyzed or concentrated before
 8 International mycotoxin legislation, food security, and climate change | 159

analysis when toxins are present in very low concentrations. These methods can be
used under analyst criteria but should guarantee high toxin recovery in order to avoid
toxin underestimation.

8.3.3 Mycotoxin analysis

Several detection methods can be used after extraction and cleanup to check for the
presence of mycotoxins in samples. The analytical method should be simple, rapid,
robust, accurate, highly sensitive, and able to detect a wide range of compounds si-
multaneously. In addition, high throughput of analyzed samples is also important
when a method is selected. Chromatographic methods are often used to analyze the
presence of mycotoxins, although ELISAs (enzyme linked immune–sorbent assays) or
biosensors have also been applied.

[Link] Thin layer chromatography (TLC)

Thirteen methods were adopted as official AOAC methods for aflatoxins in different
matrices by AOAC International from 1970 to 1980, most based on TLC [24]. TLC is
considered useful as a screening method for both semiquantitative and quantitative
purposes. This planar chromatography has been an official AOAC method for identifi-
cation and quantification of mycotoxins at 1 ng/g level since 1990 [23]. In the station-
ary phase, silica, alumina or cellulose, is immobilized over a glass or plastic plate and
different solvents are used as mobile phase. Both 1- and 2-dimensional analyses are fre-
quently used in order to improve resolution. After chromatographic development, the
plate is visualized with ultraviolet (UV) or fluorescence detectors. This is a powerful,
rapid, and low-cost separation method for detecting the presence of toxins but not the
exact amount. High-performance TLC and overpressured layer chromatography tech-
niques are modifications of TLC used for quantitative determination of mycotoxins
[20–22].

[Link] Immunoassay techniques

There are several ELISA kits for detection of mycotoxins. These assays are based on
a competitive direct or indirect assay using a primary antibody specific for a toxin, a
conjugate of an enzyme and the toxin, or secondary antibodies [18, 19]. This technique,
the same as IACs, is useful for detection of a toxin or a family of toxins; the simulta-
neous detection of multiple toxins was thus developed with a magnetoresistive-based
immunoassay with a low detection limit [17]. Although ELISA shows high specificity,
cross-reactivity with secondary antibodies may occur, resulting in non-specific sig-
nals, results should thus sometimes be confirmed by other analytical methods [70].
160 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

[Link] Bioassays
Bioassays are an alternative to chemical analysis where the toxicity or activity of myco-
toxins over cellular lines is checked. Qualitative and quantitative detection can be
performed in this way [13–16]. These are highly sensitive and low-cost assays. The
receptor-assays recently developed to detect fungal toxins are based on the activity
over cells [12].

[Link] Biosensor technique

The immobilization of molecules such as antibodies, receptors or aptamers over
sensor surfaces allows the development of highly sensitive detection methods for
mycotoxins. The surfaces have different natures depending on the equipment and the
molecule to be immobilized. Several biosensor assays have been developed in this
way [8–11]

[Link] High performance liquid chromatography (HPLC)

HPLC and the newly developed ultrahigh pressure liquid chromatography (UPLC)
are the main chromatography techniques used to separate and identify mycotoxins
[23]. The toxins can easily be separated with this technique, using different columns
and elution mixtures and gradients, and then identified by UV and/or fluorescence.
A number of toxins already have natural fluorescence and others can be chemically
derivatized. HPLC has thus been a standard method for detection of multiple myco-
toxins in several matrices with a wide range of detection limits. This methodology
has recently been improved coupled with mass detection (MS). The selectivity of
MS detection increases the analysis capacity, including samples without cleanup
process, and also enlarges the sensitivity, 50 times greater than fluorescence detec-
tion [70]. A number of protocols, impossible to summarize in this chapter, have so far
been published for multitoxin analysis using MS detection and various techniques
and equipment (atmospheric pressure chemical ionization (APCI), electrospray ion-
ization (ESI), MS-MS detection, ion trap, time of flight (TOF), etc.; [6, 7, 23]). MS
detection is accurate and specific and problems derived from compound interference
within HPLC separation are avoided. Complex and expensive laboratory equipment
is required, however, as is skilled personnel. In addition, high quality mycotoxin
standards are needed. Although standards are available for the majority of regulated
toxins, certified reference materials (CRM) are necessary to definitively identify and
quantify mycotoxins, and this grade of purity is not always available. In addition, new
toxic compounds will not be detected, since it is necessary to know in advance which
molecules will be checked in MS detection. MS techniques are essential, however,
and regularly used in food safety and environmental monitoring.
 8 International mycotoxin legislation, food security, and climate change | 161

[Link] Gas chromatography

Gas chromatography can be applied to identify and quantify the presence of myco-
toxins using MS, ionization, or spectroscopy detection. In this case the toxins should
be volatile or converted into volatile derivatives. This technique is expensive and not
regularly used although many references are available [23].

[Link] Other analytical methods

Capillary electrophoresis, rapid colorimetric and fluorescent test, fluorescence polar-
ization or competitive lateral flow assays have also been developed to detect myco-
toxins [70, 71].

8.3.4 Requirements for mycotoxin analysis methods

As previously mentioned, there are no official methods for mycotoxin analysis. How-
ever, the methods in Europe must comply with European Community regulations on
screening and confirmatory methods for detection of these compounds [74]. In this
sense, methods of analysis should be characterized by the criteria of accuracy, appli-
cability (matrix and concentration range), limit of detection, limit of determination,
precision, repeatability, reproducibility, recovery, selectivity, linearity, and measure-
ment of uncertainty. The precision values should be obtained with internationally
recognized protocols (ISO or IUPAC international harmonized protocols), and the re-
peatability and reproducibility should be expressed in an internationally recognized
form [55]. In addition to these general requirements, mycotoxin analysis methods must
comply with different requirements for confirmatory or semi-quantitative screening
methods. The procedures for validation of screening methods by means of an inter-
laboratory validation, the verification of the performance of a method validated by
means of an inter-laboratory exercise and the single-laboratory validation of a screen-
ing method are fixed [74]. In terms of performance criteria, full validation is recom-
mended for confirmatory methods in relevant matrices. The method should be vali-
dated in-house including CRMs according to performance criteria for each toxin. Semi-
quantitative screening methods are used to select samples with levels of toxins which
exceed the concentration of interest. The result in this case will be negative or suspect
and should later be verified with a confirmatory method. These methods need inter-
laboratory or single validation for each individual mycotoxin and commodity. When
new mycotoxins are added to the scope of an existing screening method, a full vali-
dation is required to demonstrate the suitability of the method. Continuous method
verification must be programmed after the initial validation [74]. In summary, perfor-
mance criteria for mycotoxin screening methods are used to guarantee comparable
results to be applied for public health risk assessment and new legislation.
162 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

The Joint Research Centre (JRC) of the European Commission has hosted four Eu-
ropean Union Reference Laboratories (EURLs) in the area of food safety control since
2006. The JRC’s IRMM (Institute for Reference Materials and Measurements) is the Eu-
ropean Union Reference Laboratory (EURL) for mycotoxins. The EURL for mycotoxins
coordinates a network of national reference laboratories (NRLs) to facilitate the imple-
mentation of European legislation on mycotoxins in food and feed and to obtain high
quality results by development and validation of methods, organization of compar-
ative testing, and training of laboratory staff. The activities of the EURL with regard
to mycotoxins currently concern aflatoxin B1 , total aflatoxins, ochratoxin A, patulin,
deoxynivalenol, zearalenone, fumonisins B1 and B2 , T-2 toxin, HT-2 toxin, and ergot
alkaloids. In order to meet demands for certified reference materials, the JRC joined
the German Federal Institute for Materials Research and Testing (BAM) and the British
company LGC Ltd. to establish a high quality brand of CRMs in Europe, the European
Reference Material (ERM® ), which was launched in 2004. The 2015 JRC catalog pro-
vides 16 certified reference materials for mycotoxins (Tab. 8.1), of which 11 are aflatox-
ins.

8.4 International mycotoxin regulations

Epidemics of mycotoxicosis (acute or chronic diseases of humans and animals caused

by exposure to mycotoxins) have severely affected human populations over whole
regions or several countries throughout history, often in connection with times of
famine [5]. In Europe, for example, several large-scale outbreaks of ergotism, a my-
cotoxicosis caused by toxins produced by the ascomycete Claviceps purpurea on
rye, killed thousands of people during the Middle Ages, and small epidemics of the
disease occurred after the Renaissance. Another mycotoxicosis epidemic took place
in some regions of the USSR between 1942 and 1948, when thousands of people
died from a hemorraghic disease associated with consumption of bread and other
cereal products made from grains left in fields over winter and infected by Fusarium
sporotrichoides and F. poae, which produce the toxin T-2, one of the most acutely
toxic trichothecenes [4].This mycotoxicosis is now called alimentary toxic aleukia
(ATA). Some severe mycotoxicoses have also affected animals in the 20th century.
More than 5000 horses died of equine leukoencephalomalacia (ELEM) in 1934 and
1935 in the United States Midwest after consuming maize infected with F. verticillioides
(syn. F. moniliforme). More than 50 years later, in 1989, F. verticillioides was found to
produce a toxic metabolite, named fumonisin B1 , which was shown to elicit typical
ELEM symptoms in horses and to cause liver cancer in rats and lung edema in pigs [3].
Feeding moldy grain and foods has thus been known to be harmful to humans
since at least the Middle Ages. However, the fungal compounds associated with the
diseases were not identified until the second half of the 20th century. It was not until
the early 1960s that the study of mycotoxins began, triggered by the outbreak of
 8 International mycotoxin legislation, food security, and climate change | 163

Tab. 8.1: Certified reference materials for mycotoxins available from the 2015 JRC catalog.

Reference Mycotoxin Material/matrix Certified value

material code μg/kg
ERM-BD282 Aflatoxin M1 Whole milk powder < 0.02
(zero level)
ERM-BD283 Aflatoxin M1 Whole milk powder 0.68 ± 0.1
(low level)
ERM-BD284 Aflatoxin M1 Whole milk powder 0.68 ± 0.1
(high level)
BCR-262R Aflatoxin B1 Defatted peanut meal <3
(blank)
BCR-263R Aflatoxin B1 Defatted peanut meal 1.7 ± 2.4
Aflatoxin B2 (medium level) 3.0 ± 2.4
Aflatoxin G1 3.0 ± 0.5
BCR-264 Aflatoxin B1 Defatted peanut meal 206 ± 13
(high level)
BCR-401R Aflatoxin B1 Peanut butter < 0.2
Aflatoxin B2 (very low level) < 0.2
Aflatoxin G1 < 0.2
Aflatoxin G2 < 0.2
BCR-385R Aflatoxin B1 Peanut butter 1.77 ± 0.30
Aflatoxin B2 (low level) 0.48 ± 0.08
Aflatoxin G1 0.9 ± 0.4
Aflatoxin G2 0.30 ± 012
Total aflatoxins 3.5 ± 0.5
BCR-375 Aflatoxin B1 Compound feed <1
(very low level blank)
ERM-BE375 Aflatoxin B1 Compound feed 2.6 ± 0.4
Aflatoxin B2 (very low level) 0.2 ± 0.04
Aflatoxin G1 0.4 ± 0.1
Aflatoxin G2 <2
ERM-BE376 Aflatoxin B1 Compound feed 12.9 ± 1.8
Aflatoxin B2 (high level) 0.68 ± 0.1
Aflatoxin G1 5.2 ± 0.8
BCR-471 Ochratoxin A Wheat (blank) < 0.06
ERM-BC716 Zearalenone (ZON) Maize <5
ERM-BC717 Deoxynivalenol (DON) Maize 673 ± 187
Nivalenol (NIV) 53 ± 10
Zearalenone (ZON) 83 ± 9
BCR-377 Deoxynivalenol (DON) Maize flour < 0.05 mg/kg
(very low level blank)
BCR-396 Deoxynivalenol (DON) Wheat flour < 0.05 mg/kg
(very low level blank)
164 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

Turkey-X disease in the United Kingdom in 1960, an epidemic which resulted in the
deaths of thousands of turkey poults, ducklings, and chicks fed diets containing
peanut meal from Brazil. The toxicity of the meal was discovered to be due to the
presence of Aspergillus flavus, and the toxic agent was named aflatoxin (from A. flavus
toxin). Between 1961 and 1963, several researchers showed that aflatoxins could in-
duce acute liver disease in ducklings and liver cancer in rats, while others were able
to discover the existence of four major naturally occurring aflatoxins (B1 , B2 , G1 , G2 ),
to isolate purified aflatoxins from A. flavus cultures, and to accomplish structural
characterization and synthesis of aflatoxin B1 [2]. The discovery of aflatoxins led to
extensive international research in the following years, to develop analytical methods
for their detection and quantification in food. The methodology was used in epidemi-
ological studies carried out from 1968–1985, uncovering the association of aflatoxin
ingestion and incidence of hepatocellular carcinoma (HCC) in human populations,
and resulting in the classification of aflatoxins as human carcinogens (Group 1) by the
International Agency for Research on Cancer (IARC) [2]. Many fungi were screened
for toxic secondary compounds in that period, and over 240 fungal metabolites were
reported to be toxigenic by 1984.
In 1969, the Food and Drug Administration (FDA) of the United States set an action
level for aflatoxins at 20 ppb for all foods, including animal feed, based on the analyt-
ical methodology developed and with the aim of restricting aflatoxin exposure to the
lowest possible level. This was the first regulation of mycotoxins in the world. After
carrying out animal feed studies in the 1970s and 1980s, the FDA revised this action
level in 1982, 1989, and 1990 to 300 ppb for aflatoxins in cottonseed meal and 100 ppb
for aflatoxins in maize and peanut products intended for use as feed ingredient for
beef cattle, swine, and poultry, keeping the level of 20 ppb for human food and all
feed intended for immature animals, dairy animals or unknown destinations.
In the decades following the first mycotoxin regulation by FDA, many countries
adopted regulations specifying maximum tolerable levels for the most toxic and/or
abundant mycotoxins in many food and feed commodities and products, in order
to limit exposure to mycotoxins and protect human and animal health. There were
33 countries with known specific mycotoxin regulations for food and/or feed in 1981,
56 in 1987, 77 in 1995, and 100 in 2003 [1].
The first regulation on aflatoxins in the EU was for aflatoxin B1 in animal feed in
1976, and EU-harmonized regulations for several aflatoxins in human food were estab-
lished in 1998 [1]. European regulations for aflatoxins were amended and new EU regu-
lations were established for several other mycotoxins in different foodstuffs, including
foods for babies and children, in the following years [51, 53, 54]. The progressive in-
troduction of regulatory limits for mycotoxins by the European Commission has been
the main driving force for the development of official mycotoxin analysis methods in
food and feed [24].
Aflatoxins in food are the most commonly regulated mycotoxins worldwide. Afla-
toxin B1 is the most common food mycotoxin. The most pronounced aflatoxin contam-
 8 International mycotoxin legislation, food security, and climate change | 165

ination has usually been found in food crops grown or stored in the warmer agricul-
tural regions of the world. However, global trading of agricultural commodities makes
aflatoxin contamination a worldwide problem for human and animal health. All coun-
tries have regulatory limits for at least aflatoxin B1 or the sum of aflatoxins B1 , B2 , G1 ,
and G2 in food and/or feed [50].
Depending on the country, specific regulations have been set up for other myco-
toxins mainly in human foods: aflatoxin M1 ; the trichothecenes deoxynivalenol, dia-
cetoxyscirpenol, T-2 toxin, and HT-2 toxin; the fumonisins B1 , B2 , and B3 ; ochratoxin A;
zearalenone; patulin; the ergot alkaloids; agaric acid; phomopsins; and sterigmato-
cystin [50]. There are less recommended mycotoxin levels for animal feed and they are
typically higher than for human food [1, 58].
New mycotoxin regulations are continuously being established as scientific and
technological progress provides new evidence of risks to human and/or animal health.
They concern not only maximum mycotoxin levels in food and feed but also sampling
procedures and criteria for analysis methods. A guidance value for the sum of T-2 and
HT-2 toxin in cat food was established in 2013 in the EU, given the toxicity of both
mycotoxins for cats [49]. The European Commission has recently set maximum lev-
els for citrinin in food supplements based on rice fermented with red yeast Monascus
purpureus, due to the nephrotoxicity of this mycotoxin [47, 48]. In addition, meth-
ods for sampling of large lots, spices, and food supplements have been regulated,
performance criteria for T-2 and HT-2 updated, and criteria for citrinin performance
and mycotoxin screening methods have been established [74]. Current regulations are
based on scientific opinions of authoritative bodies, such as the Joint FAO/WHO Expert
Committee on Food Additives (JECFA), Codex Alimentarius, and the European Food
Safety Authority (EFSA), which regularly assess the risk of mycotoxins and advise on
controls to reduce consumer exposure.
The criteria used as a basis for deciding limits have not been harmonized world-
wide and vary in different countries. The most common criteria are: scientific criteria
related to data from surveys, toxicological data, analytical methods and distribution
of mycotoxins in contaminated commodities [46]. Harmonization of mycotoxin regu-
lations in food and feed have taken place within groups of countries: the European
Union (EU-28), MERCOSUR (Mercado Común del Sur, i.e. Common Market of South
America), Australia/New Zealand, ASEAN (Association of South East Asian Nations),
GCC (Gulf Cooperation Council), and COMESA (Common Market of Eastern and South-
ern Africa) [58]. However, different mycotoxin limits exist among these groups [50].
Although most food consumed worldwide is grown locally, global food and feed
trade increased greatly between 2000 and 2010, affecting cereals, fruit and vegetables,
oilseeds, coffee, tea, cocoa, and spices [57]. Mycotoxin contamination of exported food
and feeds above legislated maximum levels resulted in trade disruptions with poten-
tially important economic implications [77].
The EU has applied a strict control system to keep out food and feedstuffs with
mycotoxin levels above those permitted. A rapid alert system for food and feed
166 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

(RASFF) has been in place since 1992 which enables rapid exchange of information
between food and feed control authorities in member states and the European Com-
mission, thus easing the coordination of responses to food safety threats, including
mycotoxins. Imported food and feed consignments are tested for mycotoxins and other
possible hazards, depending on the material, at the external borders of the EU (and
the European Economic Area – EEA), and are rejected if they pose a risk to human and
animal health. RASFF notification of border rejections are sent to all EEA border posts
to ensure that the rejected products do not re-enter the EU through another border
post.
Alert and information notifications on mycotoxins were included in the ‘Chem-
ical’ risk group in RASFF reports until 2002 and thereafter as a separate identified
risk. Most RASFF notifications of mycotoxin contamination have concerned aflatox-
ins, and the European Commission has been establishing new regulations for the pro-
tection of public health. The RASFF received a very high number of aflatoxin noti-
fications concerning pistachios from Iran and also for peanuts and hazelnuts from
2003 to 2007. The Council Directive 2005/85/EC was established on January 26, 2005
by the European Commission (EC) and imposed special conditions on pistachios and
certain products derived from pistachios originating in and or consigned from Iran.
As a result fewer notifications occurred in 2006, although import quantities remained
about the same [45]. Further Commission decisions came into force in 2006 and 2007
related to the control of aflatoxins in foodstuffs imported from Egypt, China, Turkey,
Brazil, and Iran (Commission Decision 2006/504/EC of July 12, 2006), in almonds and
derived products from the United States (Commission Decision 2007/5063/EC of Au-
gust 1, 2007), and in peanuts and derived products from Brazil (Commission Decision
2007/759/EC of November 19, 2007). All of these regulations have resulted in a decreas-
ing number of aflatoxin notifications from 2003 to 2007 [44].
In 2008, however, there was a 28 % increase in aflatoxin notifications and 23 %
for mycotoxins in general. The increase was noted in the product categories ‘Nuts, nut
products and seeds’ and ‘Cereal products’, although no single cause for this could be
identified [43].
In the period 2008–2014, there were 9338 EU border rejection notifications from
third countries for food, of which 3174 (34 %) were due to mycotoxins [37–43]; see
Fig. 8.1.
Most rejections were of nuts and nut products imported from China, Turkey, and
Iran, and to a lesser extent from the United States and Argentina, but also remarkable
was a record of 480 rejections of figs (classified in the category ‘Fruits and vegetables’)
from Turkey, and 202 in the category ‘Herbs and spices’ from India; see Fig. 8.2.
As in the previous years, most mycotoxin rejections were due to elevated levels of
aflatoxins (Fig. 8.3) according to the EU aflatoxin regulations (European Commission
2006, 2010). The number of border rejections of food due to aflatoxin contamination
greatly decreased from 2008 to 2014, which might be related to changes in EU aflatoxin
regulations. According to RASFF data, the frequency of control of the import of cer-
 8 International mycotoxin legislation, food security, and climate change | 167

tain foodstuffs from certain third countries due to contamination risk by aflatoxin was
increased with the adoption of Commission Regulation (EC) No 1152/2009 of Novem-
ber 27, 2009. In February 2010 Commission Regulation (EU) No 165/2010 amended the
in force Regulation (EC) no 1881/2006 increasing maximum levels for aflatoxins in al-
monds, hazelnuts, pistachios, and other tree nuts, taking into account developments
in Codex Alimentarius and new scientific information.
The first RASFF notifications of aflatoxins in different feed materials (only two)
were reported in 2005 [36]. There were 618 EU border rejection notifications from third
countries for feed in the period 2008–2014, and 235 (38 %) were of feed materials and
pet food (Fig. 8.4) contaminated with aflatoxins [37–43].
The number of border rejections peaked in 2011 and 2012, and there were fewer EU
aflatoxin rejections of feed products in 2013 and 2014 (Fig. 8.5). Most of the contam-
inated feedstuffs (72 %) were groundnuts and groundnut kernels from India for bird
feed. The Indian authorities presented an action plan to address the issue in 2011 on
request of the European Commission.

1600 Total number EU rejections for all food categories

Total number EU mycotoxin rejections
for all food categories
1400

1200

1000

800

600

400

200

0
Turkey

Brazil

Egypt
United States

South Africa
China

Iran

Argentina

Nigeria

Indonesia

Ghana

Australia
India

Pakistan

Uzbekistan

Fig. 8.1: Number of EU border rejections (total and mycotoxin) from third countries for food, 2008–
2014. Data extracted from information published by the EU-Rapid Alert System for Foods and Feeds
(RASFF).
168 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

600 Fruits and vegetables

Nuts, nut products and seeds
Herbs and spices
500 Cereals and bakery products

400

300

200
200

100
100

0
0
Turkey

Brazil

Egypt
United States

South Africa
China

Iran

Argentina

Nigeria

Indonesia

Ghana

Australia
India

Pakistan

Uzbekistan
Fig. 8.2: Number of EU mycotoxin border rejections from third countries according to food product
category and country of origin, 2008–2014. Data extracted from information published by the EU-
Rapid Alert System for Foods and Feeds (RASFF).

Aflatoxin testing is not mandatory for domestically produced or imported foods and
feed ingredients in the United States, although the FDA regularly takes samples of food
and feed imports [35]. This explains the significant differences between the EU and the
US in the pattern of rejections, reflecting both trade patterns and distinct food safety
and other requirements, as well as the associated systems of enforcement [34]. The
most frequent reason for rejection of food imports is non-compliance with labelling
in the US (Fig. 8.6), being associated with 58 % of all rejections. However, the EU does
not generally enforce labelling requirements through border inspection.
The food supply chain is increasingly interconnected and the world market faces
different national and international food safety regulations and standards which
might create an uncertain global regulatory environment. The commercial interests
of individual countries and the need for sufficient availability of food have hampered
global harmonization of mycotoxin regulations.
The European Union is revising mycotoxin legislation continuously. In 2013, at
the request of the European Commission, the EFSA CONTAM Panel delivered a state-
ment regarding the public health risks related to a possible increase in the maximum
 8 International mycotoxin legislation, food security, and climate change | 169

900 Aflatoxins
Deoxynivalenol (DON)
800 Fumonisins
Ochratoxin A
700 Zearalenone
Total mycotoxins
600

500

400

300

200

100

0
2008 2009 2010 2011 2012 2013 2014

700 Fruits and vegetables

Nuts, nut products and seeds
Herbs and spices
600 Cereals and bakery products

500

400

300

200

100

0
2008 2009 2010 2011 2012 2013 2014

Fig. 8.3: Number of EU mycotoxin border rejections from third countries for food based on legislated
mycotoxins and according to food product category, 2008–2014. Data extracted from information
published by the EU-Rapid Alert System for Foods and Feeds (RASFF).
170 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

300 Total number EU rejections for

all hazard categories in feed
Total number EU rejections for
mycotoxins in feed

200

100

0
India Brazil Argentina Sudan Gambia Nicaragua Egypt Nigeria

160 Feed materials

Pet food
140

120

100

80

60

40

20

0
India Brazil Argentina Sudan Gambia Nicaragua Egypt Nigeria

Fig. 8.4: Number of EU border rejections (total and mycotoxin) from third countries for feed, and
according to feed category, 2008–2014. Data extracted from information published by the EU-Rapid
Alert System for Foods and Feeds (RASFF).
 8 International mycotoxin legislation, food security, and climate change | 171

120 India
Brazil
Argentina
100

80

60

40

20

0
2008 2009 2010 2011 2012 2013 2014

Fig. 8.5: Number of EU mycotoxin border rejections from third countries for feed according to coun-
try of origin, 2008–2014. Data extracted from information published by the EU-Rapid Alert System
for Foods and Feeds (RASFF).

level of DON for certain semi-processed cereal products from 750 μg/kg to 1000 μg/kg
[30]. The study concluded that an increase in DON maximum level could be expected
to be associated with an increase in DON and its 3- and 15-acetyl-derivatives, there-
fore increasing exposure of the group health based guidance values. The European
Commission also recently requested an urgent scientific statement on the increased
public health risk related to a possible temporary derogation from the maximum level
(tML) of deoxynivalenol (DON), fumonisins (FUM), and zearalenone (ZON) in maize
and maize products. The request referred to the remarkable increase in DON, FUM,
and ZON contamination in maize and maize products from the 2013 harvest in France
which led this country to request a temporary derogation of the maximum levels for
those mycotoxins. The EFSA concluded that, together with the uptake of other food
commodities, the detected increase in mycotoxin contamination was already close to
what is considered a safe level for some consumers, and an extended study on maize
mycotoxins from the 2013 harvest in other European production regions was neces-
sary [28].
Regulations should be optimized to protect human and animal health, and at the
same time not obstruct the free trade market [33].
172 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

2500 EU Total rejections

EU Mycotoxin rejections

2000

1500

1000

500

Thailand
Turkey

United
States

Brazil

Egypt

Philippines
Iran

China

India

Argentina

Ghana

Nigeria

Vietnam

Indonesia
14000 Pakistan USA Total rejections
USA Labelling rejections
USA Mycotoxin rejections
12000

10000

8000

6000

4000

2000

0
Turkey

Phillipines
India

Canada

Vietnam

China

Guatemala

Indonesia
Mexico

Pakistan

Fig. 8.6: Number of EU rejections of food and feed products and of USA rejections of food products,
from third countries, 2002–2008. Data extracted from information published by the United Nations
Industrial Development Organization (UNIDO) [34].
 8 International mycotoxin legislation, food security, and climate change | 173

8.5 Mycotoxin legislation and climate change

Climate change is expected to increase the incidence and severity of pests and dis-
eases in crops [59], and might have a significant effect on mycotoxins and their regu-
lation [58].
In 2012, there were five notifications of aflatoxin M1 in milk at levels above the
maximum level of 0.05 ppb imposed by EU legislation. All were related to an increased
prevalence of aflatoxins in maize for animal feed from southeast Europe [39]. The
growing season of maize in that area had been characterized by a very severe drought,
making the crop vulnerable to infection by Aspergillus flavus and A. parasiticus and
resulting in increased prevalence of aflatoxins [39].
In the EU, risk of aflatoxin contamination in maize is expected to be higher in some
southern European countries, and low to medium in the four main maize producing
countries (Romania, France, Hungary, and northeast Italy) in a +2 °C climate change
scenario, whilst in a +5 °C scenario, aflatoxin levels are predicted to be lower but risks
are expected to be broader and increase towards northern EU countries [32]. These
predictions of aflatoxin risks will force a change in the notion that aflatoxins are mostly
a problem of imported food and feed in Europe. In a climate change scenario, a strict
control system will have to be applied not only to imported food and feedstuffs but
also to national agricultural commodities susceptible to contamination by aflatoxins.
Although research on the effects of climate change on mycotoxins has been fo-
cused on aflatoxins due to their high toxicity for humans and animals, much attention
will have to be paid in the future to the other regulated mycotoxins and to those not
yet regulated.
In the last five years the European Food Safety Authority (EFSA) has delivered sci-
entific opinions on the risks for animal and public health related to the presence of
nivalenol, T-2 and HT-2 toxin, citrinin, beauvericin and enniatins, and modified forms
of the Fusarium toxins zearalenone, nivalenol, T-2 and HT-2 toxins and fumonisins
in food and feed [27–31]. Modified mycotoxins are metabolites of the parent myco-
toxin formed in the plant or fungus, e.g. by conjugation with polar compounds, com-
monly glucose but also with sulfate and glutathione. Although some conclusions were
drawn, the CONTAM panel identified a number of uncertainties and data gaps. The
need for evaluation of the analytical methods in inter-laboratory validation studies,
development of performance criteria, development of reference materials in food and
feed, performance of in vivo toxicity studies and human risk assessment, acquisition of
more data on farm animal toxicity and the investigation of the carry-over of one of the
studied mycotoxins from feed to animal products intended for human consumption
was highlighted with regard to some of the mycotoxins studied.
In a further scientific opinion from December 2014 on the risks for human and
animal health related to the presence of modified forms of the Fusarium toxins zear-
alenone, nivalenol, T-2 and HT-2 toxins and fumonisins [26], the CONTAM Panel asked
for more information on the chemical structures and toxicological data of modified
174 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

mycotoxins, as well as for further work to identify modified mycotoxins not yet charac-
terized, development of properly validated and sensitive routine analytical methods,
and further investigation of the fate of modified forms upon food and feed processing.
Mycotoxin regulations may have an impact not only on international trade of
food and feed products but also on food security in developing countries in a climate
change scenario, as demand for agricultural products is estimated to increase by
about 50 % by 2030 as the world population increases [61].
The interaction between mycotoxigenic fungi and food crops in the field will not
only continue but could be extended to newer agricultural areas, so the challenge to
limit global exposure to mycotoxins for the protection of human and animal health
will rely on scientific and political collaboration both nationally and internationally.
As suggested by Van Egmond [58], regulations may force food and feed business oper-
ators to apply good agricultural, manufacturing, storage, and hygiene practices with
regard to mycotoxins, which might eventually result in reduced occurrences of unde-
sired human exposure. Regular monitoring of fungi and their mycotoxins in the field
and in the food and feed-processing companies will be indispensable, but most efforts
will need to be focused on the prevention of mycotoxin contamination in the field (bio-
control of mycotoxigenic fungi, control of insects, procurement of resistant cultivars,
sustainable irrigation, and the development of predictive models for early stages in
crop growth on smaller scales), and on ensuring safe storage conditions for food and
feedstuffs.

References

[1] Van Egmond H. Regulations relating to mycotoxins in food. Anal Bioanal Chem
2007;389:147–157.
[2] Kensler TW, Roebuck BD, Wogan GN, Groopman JD. Aflatoxin: a 50-year odyssey of mechanis-
tic and translational toxicology. Toxicological sciences 2011;120 Suppl 1:S28–48.
[3] Dutton MF. Fumonisins, mycotoxins of increasing importance: their nature and their effects.
Pharmacology & therapeutics 1996;70:137–161.
[4] Li Y, Wang Z, Beier RC et al. T-2 toxin, a trichothecene mycotoxin: review of toxic-
ity, metabolism, and analytical methods. Journal of agricultural and food chemistry
2011;59:3441–3453.
[5] Peraica M, Rasic D. The impact of mycotoxicoses on human history. Arhiv za higijenu rada i
toksikologiju 2012;63:513–518.
[6] O’Mahony J, Clarke L, Whelan M, O’Kennedy R, Lehotay SJ, Danaher M. The use of ultra-high
pressure liquid chromatography with tandem mass spectrometric detection in the analysis
of agrochemical residues and mycotoxins in food - challenges and applications. Journal of
chromatography A 2013;1292:83–95.
[7] Li P, Zhang Z, Hu X, Zhang Q. Advanced hyphenated chromatographic-mass spectrome-
try in mycotoxin determination: current status and prospects. Mass spectrometry reviews
2013;32:420–452.
 8 International mycotoxin legislation, food security, and climate change | 175

[8] Xu X, Liu X, Li Y, Ying Y. A simple and rapid optical biosensor for detection of aflatoxin
B1 based on competitive dispersion of gold nanorods. Biosensors & bioelectronics
2013;47:361–367.
[9] Park JH, Byun JY, Mun H et al. A regenerable, label-free, localized surface plasmon reso-
nance (LSPR) aptasensor for the detection of ochratoxin A. Biosensors & bioelectronics
2014;59:321–327.
[10] Zhu Z, Feng M, Zuo L et al. An aptamer based surface plasmon resonance biosensor for the
detection of ochratoxin A in wine and peanut oil. Biosensors & bioelectronics 2014;65C:
320–326.
[11] Vidal JC, Bonel L, Ezquerra A et al. Electrochemical affinity biosensors for detection of myco-
toxins: A review. Biosensors & bioelectronics 2013;49:146–158.
[12] Molina-Molina JM, Real M, Jimenez-Diaz I et al. Assessment of estrogenic and anti-androgenic
activities of the mycotoxin zearalenone and its metabolites using in vitro receptor-specific
bioassays. Food and chemical toxicology 2014;74:233–9.
[13] Clarke R, Connolly L, Frizzell C, Elliott CT. Cytotoxic assessment of the regulated, co-existing
mycotoxins aflatoxin B1 , fumonisin B1 and ochratoxin, in single, binary and tertiary mixtures.
Toxicon 2014;90:70–81.
[14] Wang SK, Liu S, Yang LG, Shi RF, Sun GJ. Effect of fumonisin B(1) on the cell cycle of normal
human liver cells. Molecular medicine reports 2013;7:1970–1976.
[15] Moscone D, Arduini F, Amine A. A rapid enzymatic method for aflatoxin B detection. Methods
in molecular biology 2011;739:217–235.
[16] Abolmaali S, Mitterbauer R, Spadiut O et al. Engineered bakers yeast as a sensitive bioassay
indicator organism for the trichothecene toxin deoxynivalenol. Journal of microbiological
methods 2008;72:306–312.
[17] Mak AC, Osterfeld SJ, Yu H et al. Sensitive giant magnetoresistive-based immunoassay for
multiplex mycotoxin detection. Biosensors & bioelectronics 2010;25:1635–1639.
[18] Abramson D, Usleber E, Martlbauer E. Rapid determination of citrinin in corn by fluores-
cence liquid chromatography and enzyme immunoassay. Journal of AOAC International
1999;82:1353–1356.
[19] Abramson D, Usleber E, Martlbauer E. An indirect enzyme immunoassay for the mycotoxin
citrinin. Applied and environmental microbiology 1995;61:2007–2009.
[20] Moricz AM, Ott PG, Billes F, Otta KH, Tyihak E. The influence of L-ascorbic acid on the
antibacterial-toxic activity of aflatoxins on adsorbent layer. Journal of applied microbiology
2007;103:2525–2532.
[21] Otta KH, Papp E, Bagocsi B. Determination of aflatoxins in food by overpressured-layer chro-
matography. Journal of chromatography A 2000;882:11–16.
[22] Kumagai S, Nakajima M, Tabata S et al. Aflatoxin and ochratoxin A contamination of retail
foods and intake of these mycotoxins in Japan. Food additives & contaminants Part A, Chem-
istry, analysis, control, exposure & risk assessment 2008;25:1101–1106.
[23] Rahmani A, Jinap S, Soleimany F. Qualitative and quantitative analysis of mycotoxins. Com-
prehensive reviews in food science and food safety 2009;8:202–251.
[24] Senyuva H. Official methods and performance criteria for determining mycotoxins in food and
feed. In: Saeger D (ed). Determining mycotoxins and mycotoxigenic fungi in food and feed.
Sawston, Cambridge, UK: Woodhead Publishing Limited; 2011:171–193.
[25] Zougagh M, Rios A. Supercritical fluid extraction of macrocyclic lactone mycotoxins in maize
flour samples for rapid amperometric screening and alternative liquid chromatographic
method for confirmation. Journal of chromatography A 2008;1177:50–57.
[26] EFSA. Scientific Opinion on the risks for human and animal health related to the presence of
modified forms of certain mycotoxins in food and feed. EFSA J 2014a;12:3916.
176 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

[27] EFSA. Scientific Opinion on the risks to human and animal health related to the presence of
beauvericin and enniatins in food and feed. EFSA J 2014b;12:3802.
[28] EFSA. Evaluation of the increase of risk for public health related to a possible temporary dero-
gation from the maximum level of deoxynivalenol, zearalenone and fumonisins for maize and
maize products. EFSA J 2014c;12:3699.
[29] EFSA. Scientific Opinion on the risks for animal and public health related to the presence of
T-2 and HT-2 toxin in food and feed. EFSA J 2011;9:2481.
[30] EFSA. Scientific Opinion on risks for animal and public health related to the presence of ni-
valenol in food and feed. EFSA J 2013;11:3262.
[31] EFSA. Scientific Opinion on the risks for public and animal health related to the presence of
citrinin in food and feed. EFSA J 2012;10:2605.
[32] Battilani P, Rossi V, Giorni P et al. Modelling, predicting and mapping the emergence of afla-
toxins in cereals in the EU due to climate change. European Food Safety Authority (EFSA) Sup-
porting publication 2012.
[33] Tasheva-Petkova Y, Christova-Bagdassarian V, Tachev A, Atanassova M. Harmonize ap-
proaches to analysis and risk assessment of mycotoxins in foodstuffs. Int J Adv Res
2014;2:1097–1116.
[34] Henson S, Olale E. What do border rejections tell us about trade standards compliance of
developing countries? Analysis of EU and US Data 2002–2008. In. Slovakia: Secretariat of the
United Nations Industrial Development organization(UNIDO) working paper. 2011.
[35] Dohlman E. Mycotoxin hazards and regulations: Impacts on food and animal feed crop trade.
In: Buzby J (ed). International Trade and Food Safety: Economic theory and case studies.
Washington DC: USDA Agricultural Economic Report; 2003:97–108.
[36] RASFF-EU. RASFF Annual report 2005. Luxemburg; 2005.
[37] RASFF-EU. RASFF Annual report 2014. Luxemburg; 2014.
[38] RASFF-EU. RASFF Annual report 2013. Luxemburg; 2013.
[39] RASFF-EU. RASFF Annual report 2012. Luxemburg; 2012.
[40] RASFF-EU. RASFF Annual report 2011. Luxemburg; 2011.
[41] RASFF-EU. RASFF Annual report 2010. Luxemburg; 2010.
[42] RASFF-EU. RASFF Annual report 2009. Luxemburg; 2009.
[43] RASFF-EU. RASFF Annual report 2008. Luxemburg; 2008.
[44] RASFF-EU. RASFF Annual report 2007. Luxemburg; 2007.
[45] RASFF-EU. RASFF Annual report 2006. Luxemburg; 2006.
[46] van Egmond HP, Dekker WH. Worldwide regulations for mycotoxins in 1994. Natural toxins
1995;3:332–336; discussion 341.
[47] (212/2014) CRE. COMMISSION REGULATION (EU) No 212/2014 of 6 March 2014 amending
Regulation (EC) No 1881/2006 as regards maximum levels of the contaminant citrinin in food
supplements based on rice fermented with red yeast Monascus purpureus. In: Communities
CoTE (ed). Official Journal of the European Union; 2014:L 67/3–4.
[48] Flajs D, Peraica M. Toxicological properties of citrinin. Arhiv za higijenu rada i toksikologiju
2009;60:457–464.
[49] 2013/367/EU CR. COMMISSION RECOMMENDATION of 4 November 2013 amending Recom-
mendation 2006/576/EC as regards T-2 and HT-2 toxin in compound feed for cats. In: Com-
munities CoTE (ed). Official Journal of the European Union; 2013:L 294/44.
[50] FAO (ed). Worldwide regulations for mycotoxins in food and feed in 2003. Rome, FAO; 2004.
[51] (105/2010) CRE. Commission Regulation (EU) No 105/2010 of 5 February 2010 amending Reg-
ulation (EC) No 1881/2006 setting maximum levels for cetain contaminants in foodstuffs
as regards ochratoxin A. In: Communities CoTE (ed). Official Journal of the European Union;
2010:L 35/7-/8.
 8 International mycotoxin legislation, food security, and climate change | 177

[52] Sulyok M, Berthiller F, Krska R, Schuhmacher R. Development and validation of a liquid chro-
matography/tandem mass spectrometric method for the determination of 39 mycotoxins in
wheat and maize. Rapid communications in mass spectrometry: RCM 2006;20:2649–59.
[53] (1126/2007) CRE. Commission Regulation (EC) No 1126/2007 of 28 September 2007 amend-
ing Regulation (EC) No 1881/2006 setting maximum levels for certain contaminants in food-
stuffs as regards Fusarium toxins in maize and maize products. In: Communities CoTE (ed).
Official Journal of the European Union; 2007:L 255/14-/17.
[54] (1881/2006) CRE. Commission Regulation (EC) No 1881/2006 of 19 December 2006 setting
maximum levels for certain contaminants in foodstuffs. In: Communities CoTE (ed). Official
Journal of the European Union; 2006:L 364/5-/24.
[55] (882/2004) CRE. Regulation (EC) No 882/2004 of the European Parliament and of the Council
of 29 April 2004 on official controls performed to ensure the verification of compliance with
feed and food law, animal health and animal welfare rules In: Communities CoTE (ed). Official
Journal of the European Union; 2004:L 165/1-/41.
[56] FAO. Cereal supply and demand brief. Rome, FAO; 2014.
[57] FAO. Statistical year book 2013. World book and agriculture. Rome, FAO; 2013.
[58] Van Egmond H. Mycotoxins: Risks, regulations and European cooperation. J Nat sci, Matica
Srpska Novi Sad 2013;125:7–20.
[59] Roos J, Hopkins R, Kvarnheden A, Dixelius C. The impact of global warming on plant diseases
and insect vectors in Sweden. Eur J Plant Pathol 2011;129:9–19.
[60] FAO. Climate change, water and food security. Rome, FAO; 2008.
[61] Bruinsma J (ed). World agriculture: towards 2015/2030. An FAO perspective. Rome, FAO and
London, UK: Earthscan Publications Ltd; 2003.
[62] FAO. The state of the world’s land and water resources for food and agriculture. Managing
systems at risk. Rome, FAO and London, UK: Earthscan Ltd; 2011.
[63] Gornall J, Betts R, Burke E et al. Implications of climate change for agricultural productivity
in the early twenty-first century. Philosophical transactions of the Royal Society of London
Series B, Biological sciences 2010;365:2973–2989.
[64] Battisti DS, Naylor RL. Historical warnings of future food insecurity with unprecedented sea-
sonal heat. Science 2009;323:240–244.
[65] Hansen J, Sato M, Ruedy R, Lo K. Global surface temperature change. Reviews of Geophysics
2010;48,RG4004, doi:10.1029/2010RG000345.
[66] IPCC. Climate change 2007: the physical science basis. Contribution of Working Group I to the
Fourth Assessment Report of the Intergovenmental Panel on Climate Change. Cambridge, UK:
Cambridge University Press; 2007.
[67] Osytry V. Alternaria mycotoxins: an overview of chemical characterization, producers, toxic-
ity, analysis and occurrence in foodstuffs. World Mycotoxin Journal 2008;1:175–188.
[68] Marin S, Ramos AJ, Cano-Sancho G, Sanchis V. Mycotoxins: occurrence, toxicology, and expo-
sure assessment. Food and chemical toxicology 2013;60:218–237.
[69] Prandini A, Tansini G, Sigolo S, Filippi L, Laporta M, Piva G. On the occurrence of aflatoxin M1
in milk and dairy products. Food and chemical toxicology 2009;47:984–991.
[70] Yang J, Li J, Jiang Y et al. Natural occurrence, analysis, and prevention of mycotoxins in fruits
and their processed products. Critical reviews in food science and nutrition 2014;54:64–83.
[71] Anfossi L, Baggiani C, Giovannoli C, Giraudi G. Mycotoxins in food and feed: Extraction, anal-
ysis and emerging technologies for rapid and on-field detection. Recent patents on food,
nutrition & agriculture 2010;2:140–153.
[72] (15/2011) CRE. Commission Regulation (EU) No 15/2011 of 10 January 2011 amending Regu-
lation (EC) No 2074/2005 as regards recognised testing methods for detecting marine bio-
toxins in live bivalve molluscs. Official Journal of the European Communities 2011;L6:3–4.
178 | María J. Sainz, Amparo Alfonso, and Luis M. Botana

[73] Botana LM. A perspective on the toxicology of marine toxins. Chemical research in toxicology
2012;25:1800–1804.
[74] (519/2014) CRE. Commission Regulation (EU) No 519/2014 of 16 May 2014 amending Regula-
tion (EC) No 401/2006 as regards methods of sampling of large lots, spices and food supple-
ments, performance criteria for T-2, HT-2 toxin and citrinin and screening methods of analy-
sis. In: Communities CoTE (ed). Official Journal of the European Union; 2014:L 147/29-/43.
[75] (401/2006) CRE. Commission Regulation (EC) No 401/2006 of 23 February 2006 laying down
the methods of sampling and analysis for the official control of the levels of mycotoxins in
foodstuffs. In: Communities CoTE (ed). Official Journal of the European Union; 2006:L 70/12–
70/34.
[76] Smith JE, Lewis CW, Anderson JG, Solomon GL. Mycotoxins in Human Nutrition and Health.
Directorate-General XII Science, Research and Development. EUR 16048 EN 1994.
[77] Tirado M, Clarke R, Jaykus L, McQuatters-Gollop A, Frank J. Climate change and food safety:
A review. Food Research International 2010;43:1745–1765.
[78] Ehlers D, Czech E, Quirin KW, Weber R. Distribution of aflatoxins between extract and extrac-
tion residue of paprika using supercritical carbon dioxide. Phytochem Anal 2006;17:114–120.
[79] Starr JM, Selim MI. Supercritical fluid extraction of aflatoxin B(1) from soil. Journal of chro-
matography A 2008;1209:37–43.
[80] Liau BC, Jong TT, Lee MR, Chang CM. Supercritical fluid extraction and quantification of afla-
toxins in Zizyphi Fructus by liquid chromatography/atmospheric pressure chemical ion-
ization tandem mass spectrometry. Rapid communications in mass spectrometry 2007;21:
667–673.
[81] Arroyo-Manzanares N, Huertas-Perez JF, Gamiz-Gracia L, Garcia-Campana AM. A new ap-
proach in sample treatment combined with UHPLC-MS/MS for the determination of multiclass
mycotoxins in edible nuts and seeds. Talanta 2013a;115:61–67.
[82] Shephard GS, Marasas WF, Leggott NL, Yazdanpanah H, Rahimian H, Safavi N. Natural
occurrence of fumonisins in corn from Iran. Journal of agricultural and food chemistry
2000;48:1860–1864.
[83] Sorensen LK, Elbaek TH. Determination of mycotoxins in bovine milk by liquid chromatogra-
phy tandem mass spectrometry. J Chromatogr B 2005;820:183–196.
[84] Liu Y, Han S, Lu M, Wang P, Han J, Wang J. Modified QuEChERS method combined with ultra-
high performance liquid chromatography tandem mass spectrometry for the simultaneous
determination of 26 mycotoxins in sesame butter. J Chromatogr B 2014;970:68–76.
[85] Zhang JM, Wu YL, YB. L. Simultaneous determination of carbamate insecticides and myco-
toxins in cereals by reversed phase liquid chromatography tandem mass spectrometry us-
ing a quick, easy, cheap, effective, rugged and safe extraction procedure. J Chromatogr B
2013;915–916:13–20.
[86] Arroyo-Manzanares N, Garcia-Campana AM, Gamiz-Gracia L. Comparison of different sam-
ple treatments for the analysis of ochratoxin A in wine by capillary HPLC with laser-induced
fluorescence detection. Anal Bioanal Chem 2011;401:2987–2994.
[87] Rasmussen RR, Storm IM, Rasmussen PH, Smedsgaard J, Nielsen KF. Multi-mycotoxin analy-
sis of maize silage by LC-MS/MS. Anal Bioanal Chem 2010;397:765–776.
[88] Zachariasova M, Lacina O, Malachova A et al. Novel approaches in analysis of Fusarium myco-
toxins in cereals employing ultra performance liquid chromatography coupled with high reso-
lution mass spectrometry. Analytica chimica acta 2010;662:51–61.
[89] Cavaliere C, Foglia P, Guarino C, Nazzari M, Samperi R, Lagana A. Determination of aflatoxins
in olive oil by liquid chromatography-tandem mass spectrometry. Analytica chimica acta
2007;596:141–148.
 8 International mycotoxin legislation, food security, and climate change | 179

[90] Blesa J, Soriano JM, Molto JC, Marin R, Manes J. Determination of aflatoxins in peanuts by
matrix solid-phase dispersion and liquid chromatography. Journal of chromatography A
2003;1011:49–54.
[91] Bacaloni A, Cavaliere C, Cucci F, Foglia P, Samperi R, Lagana A. Determination of aflatoxins in
hazelnuts by various sample preparation methods and liquid chromatography-tandem mass
spectrometry. Journal of chromatography A 2008;1179:182–189.
[92] Nonaka Y, Saito K, Hanioka N, Narimatsu S, Kataoka H. Determination of aflatoxins in food
samples by automated on-line in-tube solid-phase microextraction coupled with liquid
chromatography-mass spectrometry. Journal of chromatography A 2009;1216:4416–4422.
[93] Vosough M, Bayat M, Salemi A. Matrix-free analysis of aflatoxins in pistachio nuts using par-
allel factor modeling of liquid chromatography diode-array detection data. Analytica chimica
acta 2010;663:11–18.
[94] Saito K, Ikeuchi R, Kataoka H. Determination of ochratoxins in nuts and grain samples by in-
tube solid-phase microextraction coupled with liquid chromatography-mass spectrometry.
Journal of chromatography A 2012;1220:1–6.
[95] Fu Z, Huang X, Min S. Rapid determination of aflatoxins in corn and peanuts. Journal of chro-
matography A 2008;1209:271–274.
[96] Wang J, Liu XM. Contamination of aflatoxins in different kinds of foods in China. Biomedical
and environmental sciences 2007;20:483–487.
[97] Castegnaro M, Tozlovanu M, Wild C, Molinie A, Sylla A, Pfohl-Leszkowicz A. Advantages and
drawbacks of immunoaffinity columns in analysis of mycotoxins in food. Molecular nutrition
& food research 2006;50:480–487.
[98] Trucksess MW, Weaver CM, Oles CJ et al. Determination of aflatoxins B1 , B2 , G1 , and G2
and ochratoxin A in ginseng and ginger by multitoxin immunoaffinity column cleanup and
liquid chromatographic quantitation: collaborative study. Journal of AOAC International
2008;91:511–523.
[99] Stroka J, Van Otterdijk R, Anklam E. Immunoaffinity column clean-up prior to thin-layer chro-
matography for the determination of aflatoxins in various food matrices. Journal of chro-
matography A 2000;904:251–256.
[100] Cheraghali AM, Yazdanpanah H, Doraki N et al. Incidence of aflatoxins in Iran pistachio nuts.
Food and chemical toxicology 2007;45:812–816.
[101] Fazekas B, Tar A, Kovacs M. Aflatoxin and ochratoxin A content of spices in Hungary. Food
additives and contaminants 2005;22:856–863.
[102] Arroyo-Manzanares N, Garcia-Campana AM, Gamiz-Gracia L. Multiclass mycotoxin analysis
in Silybum marianum by ultra high performance liquid chromatography-tandem mass spec-
trometry using a procedure based on QuEChERS and dispersive liquid-liquid microextraction.
Journal of chromatography A 2013b;1282:11–19.
[103] Vishwanath V, Sulyok M, Labuda R, Bicker W, Krska R. Simultaneous determination of 186
fungal and bacterial metabolites in indoor matrices by liquid chromatography/tandem mass
spectrometry. Anal Bioanal Chem 2009;395:1355–1372.
Index

Aflatoxin 30, 93, 154, 164, 166, 167, 173 Bacillus thuringiensis (Bt) 32, 33
– aflatoxin contamination 3, 8–10, 13, 31, 43, 78, – genes 34
93–96, 135, 136, 145, 146, 165, 166, 173 – toxins 40, 43
– aflatoxin B1 75, 134, 154, 165 Bakery product 80, 168, 169
– aflatoxin B2 165 Beer 116
– aflatoxin biosynthetic gene 95 Bioassay 160
– aflatoxin G1 165 Biocontrol 34, 35, 62, 64, 65, 95, 174
– aflatoxin G2 165 Biosynthesis gene 82
– aflatoxin M1 154, 165 – aflD 82, 83, 95
Agaric acid 165 – aflR 82, 83, 95
Agricultural commodity 138, 165, 173 – aflS 82, 83, 95
Agricultural practice 11, 58, 64, 85, 98, 149 Border rejection notification 166
Agricultural productivity 2, 4, 53, 156 – figs 166
Altenuene 76, 155 – herbs and spices 166
Alternaria 72, 76, 134, 153, 155 – nuts and nut products 166
– alternata 75, 76, 79, 80, 155
Cereal 5, 20, 53, 54, 65, 71, 74, 80, 92–94, 96,
Alternariol 75, 76, 79, 155
98–101, 115–117, 133, 136, 154–156, 162,
Alternariol monomethyl ether 79, 155
165, 166, 168, 169, 171
Altertoxin 76, 155
China 11, 12, 18, 101, 102, 110, 116, 120, 121,
Arbuscular mycorrhizal (AM) symbiosis 55
155, 166–168, 172
– adaptive strategy 57
Class I leaf endophyte 65
– AM inoculum production 57
Climate change scenario 1, 7, 13, 15, 16, 64, 65,
– endophyte microorganisms 55
72, 74, 79, 84, 85, 94, 101, 173, 174
– gene expression 55–57, 62
Climate variability 156
– hormone-controlled signaling cascade 57
Co-occurrence 138, 146, 149
– mycorrhiza-induced systemic resistance 54
CO2 1, 4, 6–8, 13, 19, 20, 63–65, 73, 74, 79–83,
– plant immunity 54 85, 94, 95, 101, 121, 124, 125, 133–136
– preconditioning of immunity 64 Codex Alimentarius 165, 167
– priming of plant defense 60, 66 Coffea arabica 115
– prophylactic ability 65 Coffea canephora 115
– specific signalling pathways 55 Contamination 133–138, 140, 145, 146, 149
– triggering resistance mechanism 60 Control of the import 166
Asparagus 116 Corn 3, 29–44, 94, 123, 138, 146, 149
Aspergillus 3, 7, 15, 19, 71, 92, 156 Corn rootworm 34, 39
– carbonarius 75, 77–80, 84, 116, 136, 137 Crop loss 2, 4, 5, 19, 53
– ear rot 3, 13, 15, 16, 43 Crop plant 32, 59, 60, 65, 80, 91, 92, 111, 124
– flavus 8–10, 12, 13, 18, 31, 38, 41–43, 73, 75,
77, 78, 80–82, 86, 93–95, 134, 135, 137, Defense-related phytohormone 61
154, 164, 173 Deoxynivalenol 30, 93, 97, 134–138, 145, 146,
– niger 73, 78, 79, 111, 115, 116 149, 154
– ochraceus 80 Detection method 157
– parasiticus 31, 38, 42, 79, 82, 93–95, 134, – food lot 157
154, 173 – liquid cromatography 157
– westerdijkiae 75, 77, 79, 80, 84 – liquid-liquid extraction 158
a w 7, 10, 71, 73–80, 82–85, 95, 122–124 – matrix 157
182 | Index

– microextraction 158 Food and Drug Administration (FDA) 164

– organic solvent 158 – action level 164
– processed product 157 Food security 1–5, 13, 15, 19, 20, 29, 53, 54, 65,
– sample extraction 157 66, 80, 91, 102, 135, 153, 156, 174
– screening 157, 159, 161, 165 Food supply chain 168
– solid-liquid extraction 158 Forecasting 12, 13, 85
– unprocessed food 157 – bioclimatic niche models 13
Developing country 2, 30, 135, 174 FUM gene 113, 114, 125
Dispersal 9, 41, 42, 44 – FUM1 83, 84, 114, 123
DON see Deoxynivalenol – FUM21 83, 84, 114
Drought 4, 9–11, 36, 37, 41, 43, 45, 53, 54, 56, Fumonisin 83, 109, 134, 136–138, 140, 146,
57, 65, 73–75, 78, 81, 82, 91, 94, 99, 101, 154, 165
122, 123, 125, 133–135, 137, 156, 173 – fumonisin B1 110, 155
– aflatoxin contamination 10, 43, 135 – fumonisin B2 110, 155
– drought stress 156 – fumonisin B3 110, 155
Durum wheat 115 Fungal disease 18, 20, 29, 32, 37, 39, 63, 74, 98
Fungicide 19, 40, 44, 45, 59, 103, 133, 135–137
Fusarium 2, 3, 7, 11, 19, 71, 92, 96, 103, 156
Economic impact 74, 153
– asiaticum 11, 98
Economic implications 165
– avenaceum 98–100
Ecophysiology 71, 72, 74, 81, 85
– crookwellense 97, 98
EFSA see European Food Safety Authority
– crown rot 6, 7, 9, 135
Elevated CO2 6, 7, 13, 19, 20, 63, 64, 80–82, 85,
– culmorum 6, 8, 11, 75, 76, 80, 84, 97–101,
95, 124, 133, 135
134, 136
Elevated temperature 8
– ear rot 3, 6, 11, 13, 15, 17, 18, 39, 42–44, 111,
Emerging Fusarium toxin 155
113–115, 117, 118
Endophytic growth 112
– fujikuroi 20, 111
Environmental change 63, 64, 71, 74, 75
– graminearum 8–12, 29–31, 35, 38, 39, 41–43,
Environmental degradation 56
72, 75, 76, 84, 97–100, 102, 112, 134–137
Ergot alkaloid 153, 155, 162, 165
– graminearum sensu stricto 97, 98, 100
Esophageal cancer 109, 110, 120, 155
– head blight 2, 8–11, 16–19, 29, 31, 35, 36, 93,
European corn borer 34, 35, 39–42, 114,
96, 98, 100–103, 135, 136
118, 122
– incarnatum-equiseti species complex 97
European Food Safety Authority (EFSA) 72, 74,
– langsethiae 101
85, 93, 94, 133, 165, 168, 171, 173
– moniliforme 109
Exposure 11, 39, 74, 80, 81, 83, 93, 99, 153, 154, – poae 11, 98–101, 162
162, 164, 165, 171, 174
– proliferatum 7, 9, 11, 20, 31, 38, 41, 42, 75, 76,
Extreme condition 73 80, 110–112, 115–120, 122, 123
Extreme precipitation 1, 4, 9, 42, 43, 91 – pseudograminearum 6–9, 11
Extreme weather event 156 – sporotrichioides 72, 83, 97, 98, 100
– subglutinans 11, 38, 41, 42, 111
FB1 see Fumonisin B1 – verticillioides 6–11, 13, 15, 31, 38, 41–43, 72,
FB2 see Fumonisin B2 75, 76, 78, 80, 82, 83, 100, 109–115,
FB3 see Fumonisin B3 118–120, 122, 123, 134, 137, 162
Feed 2, 3, 30, 31, 53, 72, 75, 91–94, 110, 118, Fusarium chemotype 11, 84, 97
119, 133, 138, 145, 146, 153, 156, 157, – 15-acetyldeoxynivalenol 11, 12, 97, 101, 134
162–174 – 15-ADON see 15-acetyldeoxynvalenol
Feedstuff 138–140, 154, 157, 158, 165, 167, – 3-acetyldeoxynivalenol 11, 12, 97, 101, 134
173, 174 – 3-ADON see 3-acetyldeoxynivalenol
FHB see Fusarium head blight – NIV 12, 101
 Index | 183

Gas chromatography 161 Joint FAO/WHO Expert Committee on Food

Genetically modified organism 32 Additives (JECFA) 165
– Bt transgenic techniques 34 Joint Research Centre (JRC) of the European
– glyphosate-resistant 33–35 Commission 162
Gibberella fujikuroi 110, 119 – European Reference Material (ERM® ) 162
Global food production 5, 156 – European Union Reference Laboratories
Global warming 1, 4, 8, 74, 91, 94, 121, 133, 155 (EURLs) 162
– land-ocean temperature 155 – IRMM (Institute for Reference Materials
– new diseases 63, 64, 91 and Measurements) 162
– phytoimmunity 91 – National reference laboratories (NRLs) 162
– temperature increase 1–3, 8, 13, 15–17, 37, 39,
53, 63, 74, 83, 91, 121, 124, 134, 137 Labelling 168, 172
Glyphosate 33–36 Land-Ocean 71, 153, 161, 162, 168, 173
GM crops 32–35, 44 Legislation 161
– Bt corn 32, 35, 39 Low-input agriculture 56
– Bt cotton 32
– Bt crops 32–35, 43–45
Maximum level 118–120, 146, 165, 167, 171, 173
– corn 33, 35, 39
Maximum tolerable level 164
– cotton 33
Mediterraneanization 94
– herbicide-tolerant 33, 35
Microbial pathogen 54, 59, 66
– Roundup Ready® 32, 34, 35
Milk 31, 43, 73, 75, 94, 145, 154, 163, 173
– soybeans 32–34
Mitigation strategy 19, 20, 63, 85
Grape 116, 136, 137, 154
Models 1, 3, 12, 13, 16–20, 53, 54, 72, 94, 96,
102, 155, 156, 174
Harmonization 94, 165, 168 – bioclimatic niche models 13
Healthy food 63, 64 Modified atmosphere 7, 80
Heavy rain 36, 37, 41, 42, 156 Modified mycotoxin 173
Helicoverpa zea 114 Monitoring program 153
Hepatocellular carcinoma (HCC) 93, 164 Multitoxin analysis 158, 160
High performance liquid chromatography Mutualistic fungi 53
(HPLC) 160 Mycotoxicosis 162
– certified reference materials (CRM) 160 – alimentary toxix aleukia (ATA) 162
– mass detection 160 – ergotism 162
– time of flight (TOF) 160 – equine leukoencephalomalacia
– ultrahigh pressure liquid cromatography (ELEM) 109, 162
(UPLC) 160 – Turkey-X disease 164
HT-2 toxin 100, 154 Mycotoxin analysis 159, 161
Human and animal health 36, 53, 71, 92, – AOAC 159
164–166, 171, 173, 174 – biosensor 159
Human carcinogen 154, 164 – biosensor technique 160
Hungary 78, 94, 137, 193 – CRM 161
– detector 159
Immunoassay technique 159 – ELISAs (enzume linked immune-sorbent
Insect attack 60, 133, 136, 156 assays) 159
Insect herbivore 60 – high throughput 159
Intergovernmental Panel on Climate Change – screening method 161
(IPCC) 1, 2, 4, 14–17, 36, 45, 73, 91, 121, Mycotoxin gene expression 75, 82–85, 95, 103,
122, 124, 125, 133, 136, 137 123, 125
Irrigated agriculture 156 Mycotoxin regulation 162, 164, 165, 168, 174
184 | Index

Mycotoxin rejection 166 Precipitation 1, 12, 32, 36, 37, 40, 41, 72, 74, 99,
– almond 167 121–125, 133–137, 156
– bird feed 167 Prediction 10, 12, 17–20, 44, 64, 74, 79, 85, 86,
– hazelnut 167 91, 94, 98, 133–136, 149, 173
– groundnut 167 Prevalence 8, 42, 45, 75, 79, 85, 98, 125, 173
– groundnut kernel 167 Public health 32, 91, 161, 166, 168, 171, 173
– pistachio 167
– feed material 167 QuEChERS methodology 158
– pet food 167
Mycotoxin survey 138–141, 144–146, 148 Rainfall 2, 9–12, 36, 37, 41, 42, 44, 74, 75, 91,
94, 99, 101, 102, 122, 123, 125, 134, 136, 156
Nivalenol (NIV) 97 Rainfed agriculture 156
No-till 35, 36, 39, 40, 43, 44, 102 Rapid alert system for food and feed
Non-aflatoxigenic 95 (RASFF) 166
Northern Europe 73, 74, 91, 99, 100, 118, 137 – exchange of information 166
– food safety threats 166
Ochratoxin A (OTA) 78, 134–138, 140, 145, – European Commission 166
154, 165 Regulatory limit 31, 93, 164, 165
Ostrinia nubilalis 34, 114 Relative risk 85
OTA biosynthesis pathway 84 Resistance 5–8, 19, 34, 35, 43, 54, 56–62, 65,
– otanps 84 66, 79, 114, 136
– otapks 84 Rice 2–5, 18, 20, 32, 35, 73, 85, 94, 115, 117,
120, 133, 165
Parasitic plant 54, 59, 60, 66 Risk assessment 161, 173
Pathogen suppression 54
Pathogenic species 85 Scandinavian country 99
Pattern of rejections 168 Secondary metabolite 65, 71, 72, 78, 79, 97,
Patulin 72, 75, 77, 84, 92, 134, 137, 153, 155, 153, 154
162, 165 Serbia 78, 145
Penicillium 3, 7, 38, 71, 76, 80, 92, 153, 154, 156 Sesamia nonagrioides 114
– expansum 75, 76, 137, 155 Sorghum bicolor 115
– nordicum 72, 76 Southern Europe 94, 100
– verrucosum 72, 75, 76 Sterigmatocystin 165
Pennisetum glaucum 115 Stimulation 61, 81, 83
Pesticide 58, 122, 133, 158 Storage 10, 29, 38, 80, 93, 117, 135, 137, 149,
Phomopsin 165 153, 156, 174
Physiological maturity 113 Storm wind 41, 42
Physiological plasticity 71 Stress factor 54, 137
Physiological stress 123 Striacosta albicosta 114
Physiological traits 19 Super weeds 35
Pinus pinea 116 Survivability 38
Plant disease management 19, 121 Sustainable agricultural approach 63
Plant diseases 1, 4, 5, 12, 13, 19, 29, 36, 53, 63, Systemic infection 111, 112
64, 74, 79, 125, 134
Plant immunity 54, 61, 64, 66 T-2 toxin 100, 154
Plant physiology 85, 121 Temperature 1–5, 7–17, 19, 20, 35–39, 41–43,
Planting season 40 45, 53, 63, 71, 73–76, 78–85, 91, 94, 95,
– early planting 39–41, 44 98–102, 112, 119, 121, 122, 124, 125,
Porcine pulmonary edema 110 133–137, 153, 155, 156
Postharvest 10, 29, 135, 155, 156 Toxic effect 96, 153–155
 Index | 185

Trade market 171 Water availability 5, 10, 71, 74, 77, 122, 123, 125,
TRI gene 97 133–137, 156
Tri5 62, 84 Water supply 156
Trichothecene 62, 93, 96, 134, 135, 154, 165 Weather extremes 37, 42, 44, 149, 156
Trichothecene gene cluster 97 Wet deposition 42
Wine 116, 136, 154
Triggering resistance mechanism 60
Winter 12, 36, 38–40, 43, 156, 162

Xerotolerant 9, 71, 78
UK 18, 100–102
Uncertainty 16, 19, 20, 29, 41, 44, 54, 64, 125, Zearalenone 138, 145, 146, 149, 155, 165
126, 161 ZEN see Zearalenone