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Sustainability in Plant and Crop Protection

Sergei A. Subbotin
John J. Chitambar Editors

Plant Parasitic
Nematodes in
Sustainable
Agriculture of North
America
Vol.1 - Canada, Mexico and Western USA
Sustainability in Plant and Crop Protection

Series editor
Aurelio Ciancio, Sezione di Bari, Consiglio Nazionale delle Ricerche Istituto per la
Protezione delle Piante, Bari, Italy
More information about this series at http://www.springer.com/series/13031
Sergei A. Subbotin • John J. Chitambar
Editors

Plant Parasitic Nematodes

in Sustainable Agriculture
of North America
Vol.1 - Canada, Mexico and Western USA
Editors
Sergei A. Subbotin John J. Chitambar
California Department of Food and California Department of Food and
Agriculture Agriculture
Plant Pest Diagnostic Center Plant Pest Diagnostic Center
Sacramento, CA, USA Sacramento, CA, USA

ISSN 2567-9805     ISSN 2567-9821 (electronic)

Sustainability in Plant and Crop Protection
ISBN 978-3-319-99584-7    ISBN 978-3-319-99585-4 (eBook)
https://doi.org/10.1007/978-3-319-99585-4

Library of Congress Control Number: 2018965500

© Springer Nature Switzerland AG 2018

Chapter 8 is a U.S. government work and not under copyright protection in the U.S.; foreign copyright
protection may apply 2018
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or part of
the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation,
broadcasting, reproduction on microfilms or in any other physical way, and transmission or information
storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology
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The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication
does not imply, even in the absence of a specific statement, that such names are exempt from the relevant
protective laws and regulations and therefore free for general use.
The publisher, the authors and the editors are safe to assume that the advice and information in this book
are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the
editors give a warranty, express or implied, with respect to the material contained herein or for any errors
or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims
in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Foreword

Nematodes are invertebrate roundworms that inhabit marine, freshwater, and ter-
restrial environments. They comprise the phylum Nematoda which includes para-
sites of plants and of animals, including humans, as well as species that feed on
bacteria, fungi, algae, and other nematodes. Estimates are that four out of every five
multicellular animals on the planet are nematodes. The majority of nematodes are
microscopic, but some of the animal parasites are quite large and readily visible to
the naked eye. Most soil nematodes are 1 mm or less although some species may be
several times that length. They are aquatic organisms, living and moving in the
water films that surround the soil particles. They are adapted to moving through the
soil pore spaces without having to move the particles or to create burrows.
Nathan Cobb is often described as the “father” of the discipline of Nematology
in North America. To illustrate the abundance of soil nematodes, he famously wrote,
in 1914, that if the nematodes resident in a single acre of soil near San Antonio,
Texas, USA, were to proceed in head-to-tail procession to Washington, D.C., some
2,000 miles away, the first nematode would reach Washington before the rear of the
procession left San Antonio! So, select a field of interest and, on a map, draw around
it a circle of radius 2,000 miles. Where might the procession of nematodes from an
acre of your field extend? And, how many nematodes of average length 1 mm will
be in the procession when it reaches its destination? While a first reaction might be
one of horror at the magnitude of the nematode-pest problem in the field, if the
source is a healthy soil, the majority of species present in the procession are benefi-
cial and contribute to essential ecosystem services. In fact, most nematodes in our
environment are not parasites of plants or animals. Nematodes that feed on other
organisms are important participants in the cycling of minerals and nutrients in the
ecosystem that is fundamental to other biological activities. Consequently, the inci-
dence and abundance of nematode species with different feeding habits and life-­
history attributes provide useful indicators of environmental quality and soil health.
North America, the geographic purview of this book, is the third largest conti-
nent on the planet, stretching from arctic regions in the north to tropical zones in the
south. The continent encompasses an enormous diversity of geographic features,
soil conditions, and climatic variation and, consequently, supports a concomitantly

v
vi Foreword

enormous diversity of agricultural production systems and crop commodities.

Specific cadres of pest and disease organisms, well adapted to the local conditions,
exploit most of crop commodities in North America and, indeed, in the world. Many
species of plant parasitic nematodes are among those pests and, because of their
usually belowground habitat and microscopic sizes, are often the last to be diag-
nosed as the root cause of poor crop performance. Except for the few species that
cause plants to exhibit characteristic symptoms, the development and availability of
the microscope had enormous impact on our study and knowledge of plant parasitic
and other soil nematodes. The diagnostic tools provided by modern molecular
methods further enhance our ability to identify nematode species and to diagnose
causes of crop damage.
One could argue that the magnitudes of nematode and other pest problems in
North America largely are due to the design of cropping systems that are monocul-
tures or at least center on the continuous production of a specific crop type. That
lack of diversity in cropping systems is, of course, dictated by climatic, social, and
economic factors; it is determined by which crops will grow in an area, whether
there is a market demand, and what investments have been made in expensive farm
machinery designed for use in specific crops. The limited diversity of crop species
or varieties in an area favors pest and disease organisms that are well adapted to
local conditions, and it tends to deplete rather than build the nutrient status of the
soil. Consequently, agricultural systems become driven and protected through the
use of mineral fertilizers and synthetic pesticides, which further disrupt the natural
balance of organisms in the ecosystem.
Agricultural sustainability is based on the fusion of agricultural, environmental,
and social sciences with evolving advances in technology. Sustainability is a goal that
we pursue for the health of our planet and the preservation of living organisms that it
supports. Sustainability is, and must be, a moving target, ever changing with environ-
mental shifts and advances in our experiences and understanding. As we pursue the
goal, we need to evaluate our past and intended trajectories, where we have come
from, where we are now, and where we are trying to go. In this book, you will find
documentation of these three components of the journey with regard to the impact and
management of plant parasitic nematodes in agricultural systems of North America.
You will find details of our understanding of nematodes as pests of plants and the
evolution of management tools from those physically and chemically disruptive of the
environment to strategies that are less disruptive and more information intensive.
Cumulative experience and evolving technology, both digital and mechanical,
provide tools for assessment, analysis, and dissemination of information and advice
and for changes in agricultural practices. With the fusion of the component sciences
of sustainability comes a renewed realization that everything is connected. At one
scale, the physical, chemical, and biological components of our planet are interde-
pendent. At a finer scale, assemblages of organisms are interconnected with each
other and with their environment. Through their life processes, as they acquire
resources, grow, produce, die, and decompose, their component molecules return to
states that are available to other life forms. Those functions that we consider
­beneficial to the pursuit of sustainability can be termed ecosystem services. The
Foreword vii

recycling of nutrients through mineralization and the regulation of pest species

through predation and parasitism that we term biological control are important eco-
system services. Management practices that disrupt the delicate balances underly-
ing such ecosystem services are non-sustainable.
We are developing a greater understanding of the interconnectedness of soil
organisms in agricultural production systems. As a proxy for understanding inter-
connectedness, there exists on the planet, in soils, water, and plant material, a vast
and diverse array of soil nematodes with wide ranges of ecological adaptations,
activity, feeding habits, and ecosystem functions. Some of the species are parasites
of domestic and wild animals, human, and plants, including agricultural crops.
Many others are beneficial in their contributions to ecosystem services, participat-
ing in decomposition and mineralization cycles, as predators of pest species or as
resources that sustain other predator organisms.
Sustainable management seeks to conserve and enhance the activities of benefi-
cial organisms in the agricultural production system by minimizing physical and
chemical disruption of their environment and by providing continued availability of
resources. A diversity of plant species in space and time offers a greater array of
resources to soil organisms. Cover-crop mixtures present different spatial patterns
of root systems and provide resources in different microhabitats for organisms of
the soil food web. Therefore, plant diversity supports greater diversity of soil organ-
isms with differing behavior, activity, sizes, and temporal dominances, which must
enhance the service capacity of the whole assemblage by accessing different loca-
tions, depths, and aggregations of the soil matrix. The assemblage of beneficial
organisms provides top-down regulation of pest species in agricultural systems. In
the same systems, bottom-up regulation of pest species can be provided by diversi-
fying resource availability in time and space through non-host and resistant variet-
ies, crop rotation, and cover cropping with non-host or even antagonistic plants that
are sources of toxic compounds. Of course, the design of such multifactorial, holis-
tic management systems requires information, including rapid and accurate diagno-
sis of organism habits and functions and the availability of plants with desired
attributes. Chemical, physical, and resource disruptions of agricultural systems have
major impact on soil organisms. It is important to conserve and enhance healthy
systems; it is easier to destroy the systems than it is to rebuild them.
In the descriptions of plant parasitic nematodes in cropping systems documented
in these chapters, you will find examples of the evolution of knowledge and tools to
facilitate pursuit of the goals of sustainability. You will find documentation of where
we came from, where we are now, and where we hope to go. You will read of sys-
tems in all phases and stages of sustainable transition. In addition, you will gain
understanding of the forces and advances that have allowed and driven these
changes.

Department of Entomology and Nematology Howard Ferris

University of California,
Davis, CA, USA
June 4, 2018
Preface

The main idea behind this book is to document the nematological problems and
their solutions implemented in various regions of North America. There are several
wonderful and useful books and reviews written on nematode disease problems and
their control measures for various crops of certain countries, but we could not find
a single book that presented the reader a broad and detailed view of nematological
problems throughout North America. To have such a book to remove from the shelf,
so that on opening the table of contents, the reader could immediately obtain all the
important information on nematode diseases provided by highly qualified nema-
tologists, would be an invaluable resource. The importance of plant parasitic nema-
todes in each region is determined by the selection of crops grown and the structure
of agriculture, so we asked our authors to include this information in their respective
chapters. The history of nematological research is also included in most chapters.
To understand the present and to anticipate nematological problems in future agri-
cultural practices, one must know, remember, and learn from the past. We also asked
the authors to address related management strategies of their regions with a perspec-
tive of “Sustainability of Agriculture,” which we try to follow and regard as our
future goal. Obviously, not all nematological problems of each region could be fully
represented nor could complete lists of plant parasitic nematode species be given
due to limitation of the edition volume; however, the most important ones are well
described. The reader can also find extensive lists of references and links on the
Internet if he or she wants to delve deeper into any problem in detail. Due to exten-
sive information received, Plant Parasitic Nematodes in Sustainable Agriculture of
North America is incorporated in two volumes. Volume 1 includes Canada, Mexico,
and the Western USA, while Volume 2 covers the Northeastern, Midwestern, and
Southern USA.

ix
x Preface

In conclusion, we would like to thank all our 55 authors for their enormous
contribution to this project, Howard Ferris for the Foreword to the first volume,
Aurelio Ciancio for the Preface to the second volume of our book, many of our
colleagues for their constant support and valuable advices and comments, and
Springer Publisher and their editorial staff for publishing this book.

Sacramento, CA, USA Sergei A. Subbotin

June 4, 2018  John J. Chitambar
Contents

1 Current State of Plant Parasitic Nematodes in Canada����������������������   1

Guy Bélair, Tom Forge, Benjamin Mimee, Mario Tenuta,
and Qing Yu
2 Plant Parasitic Nematodes and Management Strategies
of Major Crops in Mexico ���������������������������������������������������������������������� 31
Ignacio Cid del Prado-Vera, Francisco Franco-Navarro,
and Damaris Godinez-Vidal
3 Plant Parasitic Nematodes of Montana and Wyoming������������������������ 69
Shabeg S. Briar, Govinda Shrestha, and Gadi V. P. Reddy
4 Plant Parasitic Nematodes and Their Economic
Relevance in Utah and Nevada �������������������������������������������������������������� 87
Renato N. Inserra, Saad L. Hafez, Nicola Vovlas,
Byron J. Adams, and Claudia Nischwitz
5 Plant Parasitic Nematodes of New Mexico and Arizona���������������������� 113
Stephen H. Thomas and Claudia Nischwitz
6 Plant Parasitic Nematodes in California Agriculture �������������������������� 131
John J. Chitambar, Becky B. Westerdahl, and Sergei A. Subbotin
7 Plant Parasitic Nematodes in Hawaiian Agriculture���������������������������� 193
Brent Sipes and Roxana Myers
8 Plant Parasitic Nematodes of the Pacific Northwest:
Idaho, Oregon and Washington�������������������������������������������������������������� 211
Inga A. Zasada, Louise-Marie Dandurand, Cynthia Gleason,
Christina H. Hagerty, and Russell E. Ingham
9 Plant Parasitic Nematodes in Alaska������������������������������������������������������ 241
Ernest C. Bernard

Index������������������������������������������������������������������������������������������������������������������ 247

xi
Contributors

Byron J. Adams College of Life Sciences, Brigham Young University, Provo,

UT, USA
Guy Bélair Saint-Jean-sur-Richelieu Research and Development Centre,
Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu, QC, Canada
Ernest C. Bernard Department of Entomology and Plant Pathology, University of
Tennessee, Knoxville, TN, USA
Shabeg S. Briar Department of Research Centers, Western Triangle Agricultural
Research Center, Montana State University, Conrad, MT, USA
John J. Chitambar Plant Pest Diagnostic Center, California Department of Food
and Agriculture, Sacramento, CA, USA
Louise-Marie Dandurand University of Idaho, Moscow, ID, USA
Tom Forge Agassiz Research and Development Centre, Agriculture and Agri-­
Food Canada, Summerland, BC, Canada
Francisco Franco-Navarro Programa de Fitopatología, Colegio de Postgraduados-­
Campus Montecillo, Texcoco, Estado de México, México
Cynthia Gleason Washington State University, Pullman, WA, USA
Damaris Godinez-Vidal Departamento de Biología Molecular de Plantas, Instituto
de Biotecnología-UNAM, Cuernavaca, Morelos, México
Saad L. Hafez Southwest Idaho Research and Extension Center, University of
Idaho, Parma, ID, USA
Christina H. Hagerty Columbia Basin Agriculture Research Center, Oregon State
University, Adams, OR, USA
Russell E. Ingham Oregon State University, Corvallis, OR, USA

xiii
xiv Contributors

Renato N. Inserra Florida Department of Agriculture and Consumer Services,

DPI, Nematology Section, Gainesville, FL, USA
Benjamin Mimee Saint-Jean-sur-Richelieu Research and Development Centre,
Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu, QC, Canada
Roxana Myers USDA-ARS, Daniel K. Inouye U.S. Pacific Basin Agricultural
Research Center, Hilo, HI, USA
Claudia Nischwitz Biology/Natural Resources (BNR) 243, Utah State University,
Logan, UT, USA
Ignacio Cid del Prado-Vera Programa de Fitopatología, Colegio de
Postgraduados-­Campus Montecillo, Texcoco, Estado de México, México
Gadi V. P. Reddy Department of Research Centers, Western Triangle Agricultural
Research Center, Montana State University, Conrad, MT, USA
Govinda Shrestha Department of Research Centers, Western Triangle Agricultural
Research Center, Montana State University, Conrad, MT, USA
Brent Sipes Department of Plant and Environmental Protection Sciences,
University of Hawaii at Manoa, Honolulu, HI, USA
Sergei A. Subbotin Plant Pest Diagnostic Center, California Department of Food
and Agriculture, Sacramento, CA, USA
Mario Tenuta Department of Soil Science, University of Manitoba, Winnipeg,
MB, Canada
Stephen H. Thomas Entomology, Plant Pathology and Weed Science, New
Mexico State University, Las Cruces, NM, USA
Nicola Vovlas CNR, Istituto per la Protezione Sostenibile delle Piante, Bari, Italy
Becky B. Westerdahl Department of Entomology and Nematology, University of
California, Davis, CA, USA
Qing Yu Ottawa Research and Development Centre, Agriculture and Agri-Food
Canada, Ottawa, ON, Canada
Inga A. Zasada United States Department of Agriculture, Agricultural Research
Service, Corvallis, OR, USA
About the Editors

Sergei A. Subbotin obtained an M.Sc. degree in Plant Protection in 1981 from

the Moscow Agricultural Academy in Russia. In the same year, he joined the Plant
Pathology Laboratory in the V. R. Williams All-Russian Fodder Research Institute,
Moscow region, and later All-Russian Scientific Research Institute of Fundamental
and Applied Parasitology of Animals and Plants named after K. I. Skryabin (former
VIGIS), Moscow, where he was awarded the Ph.D. degree in Helminthology
(Nematology) in 1987. Dr. S. A. Subbotin has worked as a researcher in the Center
of Parasitology of the A. N. Severtsov Institute of Ecology and Evolution (Moscow,
Russia), IACR-Rothamsted (UK), Institute for Agricultural and Fisheries Research
(ILVO, Merelbeke, Belgium), Julius Kühn-Institut (Münster, Germany), and
Department of Nematology, University of California (Riverside, USA). Presently,
he serves as Senior Nematologist in the Plant Pest Diagnostic Center, California
Department of Food and Agriculture, Sacramento, California, USA, and has affilia-
tion positions as Scientist in the Center of Parasitology, Russia; Visiting Professor
in Ghent University, Belgium; and Associate Scientist in the University of California,
USA. Dr. S. A. Subbotin is one of the Founders and Chief Editors of the Russian
Journal of Nematology. He has published more than 180 scientific articles in peer-­
reviewed journals on different aspects of molecular systematics and diagnostics of
nematodes. Dr. S. A. Subbotin is the author of 21 chapters and 2 books, one of them
in co-authorship with J. Baldwin and M. Mundo-Ocampo titled Systematics of Cyst
Nematodes (Nematoda: Heteroderinae), 2010 (two volumes), and another one in
co-authorship with Dr. J. J. Chitambar titled Systematics of the Sheath Nematodes
of the Superfamily Hemicycliophoroidea, 2014, published by Brill in Nematology
Monographs and Perspectives series. His research studies have been focused
on molecular systematics, diagnostics, and phylogeography of nematodes.
Dr. S. A. Subbotin has a wide range of collaborative projects with nematologists
across the world.

xv
xvi About the Editors

John J. Chitambar obtained an M.Sc. degree in Plant Pathology in 1977 from the
University of Allahabad, Agricultural Institute, in India. In 1983, he obtained a
Ph.D. degree in Plant Pathology from the University of California at Davis, USA,
with specialization in nematology under the guidance of Dr. D. J. Raski. Following
this, he was an Associate Scientist at the Nematology Department of the University
of California at Riverside, USA, for a short term and then traveled to India to teach
courses in plant pathology and nematology at the Allahabad Agricultural Institute
for a year. He then worked as Postdoctoral Researcher at the Department of
Nematology, University of California, Davis, after which he was employed as
Associate and Senior Nematologist at the Plant Pest Diagnostic Center, California
Department of Food and Agriculture. Presently, Dr. J. J. Chitambar serves as
Primary Nematologist/Plant Pathologist at the State of California Department of
Food and Agriculture and has worked for the State for over 31 years. He is also an
Associate Scientist at the University of California, Davis. Dr. J. J. Chitambar is a
specialist in the field of nematode diagnostics and morphology. His credits include
at least 50 articles in nematological journals and co-authored chapters in profes-
sional books plus a book on sheath nematode systematics with Dr. S. A. Subbotin.
As lead nematologist for the State Department, he has also produced several nema-
tological reports, training manuals, advisory articles, and state legal documents. In
addition, he has produced numerous pest risk assessments of plant parasitic nema-
todes and other pathogens for regulatory action in California. In collaboration with
federal, state, and county government agencies, Dr. J. J. Chitambar has served on
several committees presenting scientific basis in dealing with many regulatory nem-
atology issues. He has trained state and county regulatory officials in nematode
sampling, processing, identification, and laboratory methods for handling nema-
todes for diagnostics.
Chapter 1
Current State of Plant Parasitic
Nematodes in Canada

Guy Bélair, Tom Forge, Benjamin Mimee, Mario Tenuta, and Qing Yu

1.1 Introduction

In Canada, there is a consensus among experienced nematologists that although

crop losses related to plant parasitic nematodes (PPN) have not been exactly esti-
mated, they could be in the range of 5–15% (Potter and McKeown 2003). Similar to
many countries, the damages caused by PPNs are most often overlooked, mainly
because the typical above ground symptoms of yellowing and stunting are often
confused with other diseases, environmental factors such as drought and nutrient
deficiencies. A relatively small portion of Canada’s land is suitable for agriculture,
or about 7% (65 million ha). Across the country, the character of agriculture differs
from one province to the next, with climates and soil types influencing the com-
modities produced. Over 80% of arable land in Canada is located in the Western
Prairie provinces. Saskatchewan accounts for almost 38% of farmland, with Alberta

G. Bélair (*) · B. Mimee

Saint-Jean-sur-Richelieu Research and Development Centre,
Agriculture and Agri-Food Canada, Saint-Jean-sur-Richelieu, QC, Canada
e-mail: [email protected]; [email protected]
T. Forge
Agassiz Research and Development Centre, Agriculture and Agri-Food Canada,
Summerland, BC, Canada
e-mail: [email protected]
M. Tenuta
Department of Soil Science, University of Manitoba, Winnipeg, MB, Canada
e-mail: [email protected]
Q. Yu
Ottawa Research and Development Centre, Agriculture and Agri-Food Canada,
Ottawa, ON, Canada
e-mail: [email protected]

© Springer Nature Switzerland AG 2018 1

S. A. Subbotin, J. J. Chitambar (eds.), Plant Parasitic Nematodes in Sustainable
Agriculture of North America, Sustainability in Plant and Crop Protection,
https://doi.org/10.1007/978-3-319-99585-4_1
2 G. Bélair et al.

and Manitoba accounting for 31% and 11%, respectively. Ontario accounts for 8%
of the land, Quebec 5%, British Columbia 4%, while Nova Scotia, New Brunswick
and Prince Edward Island each contain only 1%, and Newfoundland and Labrador
account for less than 1% of Canada’s total arable land.
The area per farm continues to increase with great variation from one region to
another reflecting regional differences in commodities grown according to differ-
ences in soil, climate, topography and markets. Larger farms are located in the
Canadian Prairies, where the crops produced are mainly grains, cereals with wheat
by far the largest crop and pulses, oilseeds, mainly canola, and tame or native pas-
ture for backgrounding of cattle. The average farm size in Saskatchewan is approxi-
mately 675 ha, more than twice the national average. In Alberta, the average farm
size is about 472 ha, a little over one and a half times the national average. In the
other Prairie province, Manitoba, it is 459 ha (Statistics Canada 2014). Compared to
farms of the Prairies, the average size of farms is much smaller elsewhere; British
Columbia (132 ha), Quebec (113 ha), Ontario (99 ha) and the Atlantic Provinces
(ranging from 161 ha in Prince Edward Island to 62 ha in Newfoundland and
Labrador) (Statistics Canada 2014). In terms of area, corn and soybean are the major
crops in Ontario and Quebec, but specialized crops such as greenhouse, floriculture
and nursery trees are also produced. Fruit and vegetable production is concentrated
in Ontario, Quebec, British Columbia and the Atlantic Provinces. Canada is 1 of the
20 largest potato-producing countries in the world. In fact, potatoes are the largest
vegetable crop in the country (162,515 ha). They are grown in all provinces and are
economically important in several provinces. Prince Edward Island is the largest
producer (about 39,512 ha), followed by Manitoba (32,630 ha), New Brunswick
(24,228 ha) and Alberta (22,160 ha) (Statistics Canada 2014). Alberta is poised to
increase its potato production with the establishment of more processing facilities.
Thus, the Prairies are set to become the major growing region in Canada.
Canadian agroecosystems have historically been less affected by PPNs when
compared to other countries, mainly because Canada has a relatively cool climate.
Winters are sufficiently severe in most agricultural areas of Canada to prevent sur-
vival of many of the most pathogenic PPN species found in more southern regions
of North America. The cool climate also restricts cropping to one annual crop per
year in most agricultural areas, which limits population buildup of those PPN spe-
cies that do persist in Canada. Diverse crop rotations are often used allowing for
breaks in susceptible hosts. Thus, the climate directly and indirectly dictates the
PPN species and their severity.
The most common and damaging groups are root lesion nematodes (Pratylenchus
spp.), and cyst nematodes (Heterodera spp., and Globodera spp.). With the accel-
eration of climate change, quarantined and invasive alien nematode species pose
greater challenges, for example the stem and bulb nematode (Ditylenchus dipsaci)
has become a serious pest in recent years, illustrating the need for development of
nematology programs and extension in Canada. It is likely that the most devastating
PPNs in the future will be different from the ones being dealt with at the present.
For the management of PPN, Canada, like other developed countries, has transi-
tioned from the wide use of broad spectrum fumigant nematicides in the 1990s and
1 Current State of Plant Parasitic Nematodes in Canada 3

early 2000s, to the adoption of integrated pest management (IPM) practices such as
rotation with non-host crops and resistant varieties, and the use of green manure
cover crops and other types of organic amendments.
Canada faces great challenges, as does the rest of the world, in understanding and
controlling PPN in order to increase productivity for an ever-increasing human pop-
ulation while minimizing impacts of agriculture on the environment. This chapter
attempts to read the past in order to understand the present, with some hints for the
future, related to PPN in Canada.

1.2 Root Lesion Nematodes, Pratylenchus spp.

Root lesion nematodes are migratory endoparasites, and the most common PPN in
Canadian agroecosystems. Twelve species have been recorded: Pratylenchus alleni,
P. crenatus, P. fallax, P. flakkensis, P. hexincisus, P. macrostylus, P. neglectus, P.
penetrans, P. pratensis, P. sensillatus, P. thornei, and P. zeae. The most common and
destructive species is P. penetrans and the highest diversity of species is observed in
the province of Ontario, followed by the province of Quebec (Townshend et al.
1978; Yu 2008; Bélair et al. 2013). In Manitoba, P. neglectus was found to be the
predominant species, and P. penetrans was reported decades ago near the USA bor-
der but not currently (Mahran et al. 2010a). P. neglectus is present in every Prairie
Province in about a quarter of commercial crop fields (Tenuta et al. unpublished).
Elsewhere, co-infestations by multiple species are common, e.g., P. neglectus, P.
crenatus, and P. penetrans were found in the same potato fields in Ontario (Olthof
et al. 1982), while P. crenatus and P. penetrans were found to be sympatric in Prince
Edward Island (Kimpinski 1979). Interestingly P. neglectus has never been detected
in Prince Edward Island, while this species is found in large populations in Ontario
(Olthof 1990). Surveys for PPN in golf courses, in different climate regions within
Ontario and Quebec, also revealed that Pratylenchus was the most frequently
detected genus (Yu et al. 1998; Simard et al. 2008). These nematodes are ubiquitous
in all provinces and affect many crops (Potter and McKeown 2003). As an illustra-
tion of the ubiquitous nature of this genus, a survey of nematodes associated with
highbush blueberry in British Columbia and other areas of the Pacific Northwest
reported that 73% of fields were affected by PPN and that Pratylenchus was the
most common genus (Zasada et al. 2010).

1.2.1 Pratylenchus penetrans

Overall, Pratylenchus penetrans is the most serious pest in Canada, attacking most
of the high-value horticultural crops (Table 1.1). In addition, P. penetrans interacts
with pathogenic fungi to cause serious replant disease complexes of tree-fruit crops
such as the peach replant disease and the apple replant disease (Patrick 1955;
4 G. Bélair et al.

Table 1.1 The agriculturally important plant parasitic nematodes and their associated hosts in
Canada
Nematode Provincea Crop Reference
Anguina agrostis NS, NW, ON, Turfgrass Baker (1955, 1957, 1959)
SK
Ditylenchus ON, PE Garlic, potato Baker (1946) and Yu et al.
destructor (2012)
D. dipsaci AL, BC, MN, Alfalfa, garlic, onion Mountain (1957), Vrain and
ON, PE, QC, Lalik (1983), Vrain (1987),
SK CABI/EPPO (2009), Réseau
d’avertissements phytosanitaires
(2013), and Hajihassani and
Tenuta (2017)
Globodera NF Potato Stone (1977)
pallida
G. rostochiensis BC, NF, QC Potato Olsen and Mulvey (1962),
Orchard (1965), and Sun et al.
(2007)
Heterodera ON Corn, oat Putnam and Chapman (1935)
avenae and Fushtey (1965)
H. carotae ON Carrot Yu et al. (2017)
H. fici ON Fig Sun et al. (2017)
(greenhouse)
H. glycines ON, QC Soybean Anderson et al. (1988) and
Mimee et al. (2014a)
H. schachtii AL, ON Sugar beet Baker (1942) and Lilly et al.
(1961)
Longidorus ON Peach Eveleigh and Allen (1982)
diadecturus
L. ON Apple, cherry, peach, Van Driel et al. (1990) and
breviannulatus raspberry, turfgrass Simard et al. (2009)
L. elongatus BC, ON Strawberry, turfgrass McElroy (1977), Allen and
Ebsary (1988), and Pedram et al.
(2010)
Meloidogyne BC, MN, NB, Cabbage, carrot, Olthof and Potter (1972), Potter
hapla ON, PE, QC cauliflower, lettuce, and Townshend (1973), Sayre
onion, potato, and Toyama (1964), Vrain et al.
strawberry, tomato (1981), Bélair (1992), and
CABI/EPPO (2002)
M. incognita ON, QC Tomato, cucumber Bird (1969), Johnson and
(greenhouse) Boekhoven (1969), and Bélair
(unpublished)
M. microtyla ON Grass Mulvey et al. (1975)
M. naasi QC Turfgrass Bélair et al. (2006)
Paratrichodorus BC Blueberry, potato Kawchuk et al. (1997), Xu and
renifer Nie (2006), and Forge et al.
(2009, 2012)
Pratylenchus QC Soybean Bélair et al. (2013)
alleni
(continued)
1 Current State of Plant Parasitic Nematodes in Canada 5

Table 1.1 (continued)

Nematode Provincea Crop Reference
P. crenatus BC, ON, PE Blue berry, potato Kimpinski (1979), Olthof et al.
(1982), and Zasada et al. (2017)
P. fallax ON Turfgrass Yu et al. (1997)
P. neglectus AL, BC, MN, Potato Olthof et al. (1982), Mahran
ON, QC et al. (2010a), and Forge et al.
(2015a)
P. penetrans AL, BC, SK, Apple, barley, bluberry, Baker (1955), Potter and
MN, NB, NS, carrot, corn, grapes, oat, Townshend (1973), Oltholf et al.
ON, PE, QC onion, pea, peach, pear, (1982), Kimpinski (1987),
plum, potato, raspberry, Dauphinais et al. (2005), Yu
soybean, strawberry, (2008), Forge et al. (2012), and
tabacco, wheat Bélair et al. (2018)
P. thornei ON Wheat Yu (1997)
Trichodorus ON Turfgrass Pedram et al. (2010)
primitivus
Xiphinema ON, QC Apple, blueberry, peach Vrain and Rousselle (1980),
americanum Allen et al. (1984), and Ebsary
et al. (1984)
X. rivesi ON Apple Ebsary et al. (1984)
Names of the provinces and territories of Canada are represented by two letter. AL Alberta, BC
a

British Columbia, MB Manitoba, NB New Brunswick, NL Newfoundland and Labrador, NS Nova

Scotia, NW North West Territory, ON Ontario, QC Quebec, PE Prince Edward Island, SK
Saskatchewan

Wensley 1956; Mountain and Boyce 1958a, b; Ward and Durkee 1956; Mountain
and Patrick 1959; Potter and Olthof 1974, 1977; Braun et al. 2010; Forge et al.
2016a). It also interacts with particular fungal pathogens to cause brown root rot of
tobacco (Olthof 1967, 1971; Elliot and Marks 1972), and early dying disease on
potato (Kimpinski et al. 2001; Bélair et al. 2005; Dauphinais et al. 2005). In Prince
Edward Island, P. penetrans has been recognized as a widespread constraint on
potato production since the 1970s (Kimpinski et al. 1992). In Quebec, severe symp-
toms of early dying have been observed in potato fields (Bélair unpublished). A
similar interaction with Verticillium dahliae was also observed in strawberry fields
(Bélair et al. 2018). In soybean, P. penetrans was found in 42% of the tested fields
(78 out of 185) in the province of Quebec and 8% of the fields showed a population
density exceeding the theoretical economic threshold (Dauphinais et al. 2018).

1.2.2 Pratylenchus neglectus

In Manitoba, P. neglectus was recently found in a third of 31 commercial potato

fields examined (Mahran et al. 2010a). However, the dominant potato cultivar
‘Russet Burbank’ was not a good host for the Manitoba populations of P. neglectus,
or if the nematode had significant effects on yields (Mahran et al. 2010a). The
6 G. Bélair et al.

studies in Manitoba suggested that rotation crops other than potato such as canola
and wheat, were likely primary hosts to the nematode, as shown in the U.S.A.
(Smiley et al. 2004; Johnson 2007). More recently, a survey of pulse fields across
the Prairies found widespread distribution of P. neglectus (Tenuta et al. unpub-
lished). In Alberta, high level of P. neglectus populations was associated with potato
yield losses in a study where short crop rotations, with wheat preceding potato,
resulted in the greatest expression of potato early dying disease symptoms and the
lowest yields of several alternative rotations (Forge et al. 2015a). It is unclear if the
apparent differences between the Manitoba and Alberta studies are due to differ-
ences in the inherent pathogenicity of P. neglectus populations or the environments
(e.g. soil texture, irrigation) and crop rotations. Previous research also suggests that
there may be differences in the ability of P. neglectus populations to parasitize and
damage potato (Olthof 1990; Hafez et al. 1999).
Worldwide, P. neglectus is recognized as a significant pest of small grain and
oilseed crops (Taylor et al. 1999; Smiley et al. 2004; Johnson 2007). Considering
the importance of these crops to agriculture in Western Canada, research on the
impacts of P. neglectus on small grain and oilseed crops in Western Canada is
urgently needed. The species was also recently found north of Quebec City, which
lies outside of what was previously known as the northern limit of its distribution
(Bélair unpublished).

1.2.3 Other Pratylenchus Species

Even though P. penetrans is still the most common species in Canada, Canadian
nematologists should remain vigilant for any outbreaks of other species. Pratylenchus
thornei, a serious pest on wheat in some countries, was found in wheat in Ontario
(Yu 1997). The recent isolation of P. alleni in a Quebec soybean field has also raised
some concerns about the possible establishment of species that are more aggressive.
The yield losses from P. alleni in diseased areas ranged from 38% to 54% (Bélair
et al. 2013). In USA, the pathogenicity of P. alleni in soybean has been established
(Acosta and Malek 1981), but the species is also known to affect other crops such as
corn and wheat (Wartman and Bernard 1985). Recently, P. crenatus was found to be
the main species parasitizing highbush blueberry in British Columbia, as well as, in
other areas of the Pacific Northwest (Zasada et al. 2017).

1.2.4 Management of Pratylenchus penetrans

Given the ubiquitous presence of Pratylenchus penetrans in Canadian fruit and veg-
etable production systems, a major focus of research has been the identification of
cultural practices that may minimize impacts of P. penetrans on high-value fruit and
vegetable crops. Crop rotation is a challenging approach for P. penetrans
1 Current State of Plant Parasitic Nematodes in Canada 7

management due to its wide host range, which also includes many weed species
(Bélair et al. 2007). In their comprehensive analysis of weed hosts, Bélair et al.
(2007) found that the family Brassicaceae was shown to be the best hosts while
representatives of the Cyperaceae were the worst. Annual bluegrass crops were
shown to be tolerant to P. penetrans under controlled conditions (Bélair and Simard
2008). Despite its wide host range, Canadian research has shown that rotation with
suppressive cover crops can be a successful approach to managing P. penetrans in
annual cropping systems. Ball-Coelho et al. (2003) and Bélair et al. (2005) demon-
strated that rotating to a specific variety of forage pearl millet, CFPM 101, prior to
planting the potato cash crop resulted in lower P. penetrans populations at the time
of potato planting. As a consequence, they observed increased yields relative to
other types of cover crops including other varieties of forage pearl millet. The culti-
var CFPM 101 has been shown to be a poor host to P. penetrans that does not allow
population buildup. It is not clear if it may also stimulate active suppression via
toxic metabolites, or perhaps, by stimulating the development of a suppressive soil
food web. Mahran et al. (2008a, b), in a laboratory and field study found that volatile
fatty acids in pig slurry and acidified pig slurry could kill the nematode. In British
Columbia, however, frequent modest applications of dairy manure slurry to tall fes-
cue resulted in greater P. penetrans population densities than a corresponding fertil-
izer treatment or an untreated control, presumably, as a result of enhanced nutritional
value of root tissue (Forge et al. 2005). This research indicates that the utility of
manure slurries for P. penetrans control will depend on the interplay of application
rates with growth responses of the crops. Brassica “bio-fumigant” green manures
have also been evaluated extensively for control of P. penetrans in Canadian vege-
table rotations. In related Canadian research, glucosinolate-containing Brassica
seed meals suppressed P. penetrans under greenhouse conditions (Yu et al. 2007a)
but not in corn fields (Yu et al. 2007b).
As part of an integrated replant management program for perennial fruit crops,
Forge et al. (2015a, b, 2016b) have shown that heavy applications (>50 Mg/ha) of
poultry manure or compost can suppress populations of P. penetrans through at least
two full growing seasons after replanting raspberry (Forge et al. 2016b) or sweet
cherry (Forge et al. 2015b; Watson et al. 2017). The authors speculated that the
poultry manure could have bio-fumigant effects owing to the relatively high amounts
of ammonia released into the soil environment at such high application rates, but the
duration of suppression suggests that stimulation of suppressive soil food webs or
rhizosphere communities could also be involved. The researchers demonstrated that
the reductions in numbers of P. penetrans in compost-treated soil was associated
with increased colonization of the cherry rhizosphere by bacteria with nematode
suppressive activity but speculate that other biological antagonists could also be
involved in the suppression (Watson et al. 2017).
Options for cultural management in perennial fruit crops are constrained by the
lack of annual tillage to facilitate incorporation of organic amendments, antagonis-
tic cover crops or control agents. The use of paper mulch in an apple orchard reduced
P. penetrans populations and could explain the increased root growth of the apple
trees (Forge et al. 2008). Other types of organic mulches, including, alfalfa hay
8 G. Bélair et al.

(Forge et al. 2003, 2013) seem to give similar results. Concomitant increases in food
web structure suggest that organic mulches may increase the presence of nematode
antagonists, creating a suppressive food web, thereby decreasing the damage caused
by P. penetrans (Forge and Kempler 2009).

1.3 Root Knot Nematodes, Meloidogyne spp.

Root knot nematodes are sedentary PPN and among the most damaging of soil-­
borne pests of horticultural and field crops. Most damages are attributed to these
four species: Meloidogyne incognita, M. arenaria, M. javanica, and M. hapla, with
M. chitwoodi being a major pest of potato (Nicol et al. 2011). However, because of
our temperate climate, the problems associated with root knot nematodes are far
less important in Canada; M. incognita, M. arenaria and M. javanica are unable to
persist where the soil freezes, and M. chitwoodi has not been introduced to Canada.
Consequently, the main species of concern for Canadian agriculture is currently the
northern root knot nematode (M. hapla), which has been reported in British
Columbia, Manitoba, Ontario, Quebec and Prince Edward Island parasitizing a
range of horticultural crops (Zimmer and Walkof 1968; Potter and Townshend 1973;
Willis et al. 1976; Vrain and Dupré 1982; Bélair 2005) and alfalfa (Townshend et al.
1973).
Several other root knot nematode species are potential concerns on limited crops
in Canada, or pose a risk of establishment. In a survey nematodes in golf course turf
in Quebec, M. naasi was isolated from severely damaged annual bluegrass plants
(Bélair et al. 2006). Although it is a common species in Europe and in several states
in the USA where it causes significant damage, M. naasi has rarely been observed
in Canada. Meloidogyne microtyla, a new species at the time was found on grass in
Southwestern Ontario in 1975 (Mulvey et al. 1975).
Southern root knot nematode (M. incognita) has, so far, only been found on sev-
eral vegetable crops in greenhouses in Southwestern Ontario (Mountain and Sayre
1961) and Southern Quebec (Bélair unpublished). This species could take advan-
tage of climate change to move to open fields, or spread from nearby USA states of
New York and Pennsylvania (Walters and Barker 1994) to the neighbouring
provinces.
The Columbia root knot nematode (M. chitwoodi), which is on the quarantine list
of the Canadian Food Inspection Agency (CFIA), was first described in the Columbia
River basin of Oregon and Washington in 1980 (Santo et al. 1980). This nematode is
substantially more damaging to potato than M. hapla (Van Der Beek et al. 1998). It
also has a very wide host range that covers many crop species, including tomato and
cereals (Ferris et al. 1994). Thus, this species is more difficult to control by means of
crop rotation than M. hapla, which has a narrower host range and does not reproduce
on cereals. Considering the proximity of M. chitwoodi-infested areas in the US to
Canadian potato production areas, Canadian nematologists must continue to be vigi-
1 Current State of Plant Parasitic Nematodes in Canada 9

lant. Other species of concern include M. fallax, M. minor, M. enterolobii, M. exigua,

and M. paranaensis, because they have only recently been described (Elling 2013).

1.3.1 Management of Meloidogyne hapla

Meloidogyne hapla has been reported in the provinces of New Brunswick, Ontario,
Prince Edward Island, British Columbia and Quebec (CABI/EPPO 2002). Although
the nematode is widespread, the populations are generally low. Many vegetable
crops such as cabbage, cauliflower, onion and tomato have been shown to be affected
by the nematode (Olthof and Potter 1972; Sayre and Toyama 1964), but it is on car-
rots cultivated in muck soils that the pest has received most attention. Crop rotation
with a non-host crops such as cereals or grasses are used to maintain M. hapla den-
sities below damaging levels, which are extremely low for carrots (Bélair 1992;
Bélair and Parent 1996). Even at the detectable level of 1 infective juvenile per
100 ml soil, severe forking and stunting of the tap root are induced in carrots, which
are rendered unmarketable (Bélair 1992).
Several nematicides were effective in reducing the M. hapla populations and
increasing yields of marketable carrot (Vrain et al. 1981). In strawberry production,
the presence of multiple root pathogens including M. hapla, justifies preplant fumi-
gation with chloropicrin and metham sodium to increase vigor and yields over the
2-year production period. In potato production, M. hapla is not considered to be a
primary problem. However, soil fumigation using chloropicrin, metham sodium, or
metham potassium is occasionally performed by some growers to manage other
soil-borne pathogens, especially Verticillium dahliae and root lesion nematodes
which together cause the potato early dying disease complex (Celetti and
Al-Mughrabi pers. comm.). The planting of certified seed also contributes to limit-
ing the dispersal and losses caused by PPN in potato production. Occasionally,
potato tubers containing M. hapla females can be observed causing some necrosis
underneath the potato peel during storage, but no direct actions are taken by the
growers to manage this disorder in Eastern Canada (Bélair unpublished).
With the withdrawal of dichloropropene from the registered list of nematicides,
combined with additional restrictions on the use of chloropicrin and metham sodium
in Canada, growers have been forced to consider more sustainable cultural practices
to control M. hapla. A small number of studies were done in Canada in recent years
to find alternative and sustainable methods of controlling M. hapla. Seed exudates
of Tagetes spp. (Riga et al. 2005) and oriental mustard bran (Yu et al. 2007a) dem-
onstrated nematicidal activity on root knot nematodes. The effect of nicotine was
also studied and proved to be toxic to several species of nematodes including M.
hapla (Yu and Potter 2008). Soil amendment with Streptomyces lydicus signifi-
cantly decreased M. hapla juveniles in soil (Bélair et al. 2011).
Market garden production of vegetables is increasing rapidly in areas around
most major Canadian cities. As M. hapla can parasitize many of the popular crops
in market garden production, the impact of this nematode on market garden
10 G. Bélair et al.

p­ roduction is likely to increase. At this point in time, however, there is limited

awareness of the prevalence of root knot nematodes in small-scale vegetable pro-
duction in Canada.

1.4 Cyst Nematodes, Heterodera spp. and Globodera spp.

Heterodera spp., and Globodera spp. commonly known as cyst nematodes, are sed-
entary endoparasites that are well adapted for cold-temperate climate regions such as
Canada. They infect the roots of many plants including many important crops grown
in Canada such as cereals, corn, soybean and potato. They are very difficult to control
because of the ability of eggs in dried cysts to survive in soil for extended periods.

1.4.1 Heterodera spp.

Heterodera species of significance in Canada include soybean cyst nematode (H.

glycines), sugar beet cyst nematode (H. schachtii), cereal cyst nematodes (H. avenae
and H. filipjevi) and carrot cyst nematode (H. carotae).
The soybean cyst nematode is particularly important as soybean production has
been expanding in Canada. The pest was first reported in Southwest Ontario in 1987
(Anderson et al. 1988). Since then it has spread north and northeastwards along the
St. Lawrence River and, in 2013, was found in Quebec (Mimee et al. 2014a). It is
currently present at low population densities in all areas producing soybean in
Quebec (Mimee et al. 2016). It is considered likely that soybean cyst nematode was
present and causing soybean yield losses in Southwest Ontario by the 1970s, but
had gone undiagnosed (Tenuta pers. comm.). The nematode has expanded north-
ward in North Dakota and Minnesota to the Manitoba border though surveys of
soybean conducted in Manitoba between 2013 and 2015 did not find the nematode
(Tenuta et al. unpublished). Surveys continue in Manitoba as the area of production
has increased from insignificant in the early 2000 and expected to cap at 1.2 million
hectares within 30 years. Soybean cyst nematode was a regulated pest in Canada
until the fall of 2013 when it was de-regulated (CFIA 2013).
The sugar beet cyst nematode, H. schachtii, was a serious pest in Southern
Ontario in the early 1950s when the crop was widely cultivated (Baker 1942). It was
first found in Alberta in 1961 (Lilly et al. 1961) and has become recognized as a
significant pest for the sugar beet industry in Southern Alberta. Currently, the nema-
tode is successfully managed using a 4-year rotation. The Manitoba Sugar Company
conducted extensive surveys for H. schachtii when sugar beet was grown in the
province. The nematode was first reported in 1976 and over several years, found on
light soils near the city of Winkler (Zednai 1979). The pest has recently been
reported in North Dakota where sugar beet is still grown in the Red River Valley,
which is contiguous with Southern Manitoba (Nelson et al. 2012).
1 Current State of Plant Parasitic Nematodes in Canada 11

The cereal cyst nematode, H. avenae, was first reported damaging oat in Ontario
in the 1930s (Putnam and Chapman 1935), with further investigation occurring
through the 1940s (Baker and Chapman 1946). Later, the nematode was found
infesting corn in the same regions (Fushtey 1965; Fushtey and Johnson 1966).
Heterodera avenae is widespread on wheat in the Northwestern US states of
Washington, Idaho and Montana that border British Columbia, Alberta and
Saskatchewan (Smiley and Nicol 2009). A closely related species, H. filipjevi, is
also present in Washington (Smiley and Yan 2015) and recently reported in Montana
(Dyer et al. 2015). Neither species appears to have become established in the major
Canadian cereal-producing regions of Saskatchewan and Alberta despite the prox-
imity to infestations in nearby Washington, Idaho and Montana. Considering this
precarious situation and the long-recognized importance of the nematode in Ontario,
surprisingly little research has been directed at this nematode in Canada.
The carrot cyst nematode, H. carotae, was recently reported in the Holland
Marsh region in the province of Ontario (Madani et al. 2017; Yu et al. 2017). These
are the first reports of the pest in Canada. A preliminary survey indicated that the
pest is wide spread in the region (Vander Kooi et al. 2017). A diagnostic conven-
tional PCR method was developed based on populations of H. carotae from Ontario
and Italy using primer sets based on the coxI gene sequence in real-time PCR and
melt curve analysis (Madani et al. 2017).

1.4.1.1 Management of Heterodera spp.

Plant resistance remains the most effective and economically viable strategy to con-
trol soybean cyst nematode, but the presence of new virulent populations, or HG
types, can reduce the efficacy of this strategy (Niblack et al. 2002). A recent pheno-
typic characterization of soybean cyst nematode populations in Ontario reported 24
different HG types (Faghihi et al. 2010). This diversity of HG types is a major con-
cern, given that the number of resistance genes available in commercial cultivars is
very limited. Fortunately, 73% of the populations did not reproduce well on PI
88788, which is the resistance source used in the vast majority of resistant cultivars.
However, the study also demonstrated that 15% of the populations developed well
on PI 548402 (cv. Peking), even though that source of resistance is not generally
present in commercial cultivars in Ontario. Thus, the development of new cultivars
based on novel resistance sources is necessary. Fortunately, future breeding will be
facilitated by new technologies such as marker-assisted selection (MAS) and geno-
typing by sequencing (GBS). These techniques have already been used to identify
early maturity genes (Tardivel et al. 2014), another meaningful trait for Canadian
productivity, as soybean is grown farther north each year.
Unfortunately, a modelling of the soybean cyst nematode life cycle under current
and future (2041–2070) conditions in Quebec predicts that it could survive in all
soybean-growing areas (Mimee et al. 2014b). Because the optimal temperature for
soybean cyst nematode is warm (27 °C) and the production of cysts is directly influ-
enced by temperature (Da Rocha et al. 2008), it will be interesting to see if this pest
12 G. Bélair et al.

will really become problematic in colder regions. If so, these environmental condi-
tions will likely exert a strong selection pressure on the pest, and the resulting HG
types may be difficult to predict. New methods for studying the population genetics
of cyst nematodes (Mimee et al. 2015a) and current studies to rapidly quantify their
abundance in soil using real-time PCR (Tenuta et al. unpublished) will be very use-
ful for monitoring. Another popular management tool in managing the pest is
through rotating soybean with non-host crops. We must also remain vigilant on the
potential spread of the pest to the new soybean producing provinces of Manitoba
and the Atlantic Maritime Provinces.
The cereal cyst nematode has not warranted the development of management
strategies in Canada because oats were historically grown mostly for animal feed
and the economic impact of the nematode was low. This situation could change as
oats are increasingly being grown for human consumption and therefore, considered
to be of greater economic value. Wheat is the most important crop to Canada.
Although the cereal cyst nematodes have not yet been found infesting wheat in
Canada, in recognition of the fact that they are serious pests on the crop in many
countries of the world, Canadian researchers must remain vigilant for the possibility
that they could one day become serious pests of the most valuable crop for the
nation.

1.4.2 Globodera spp.

The genus Globodera comprises several species, including golden cyst nematode (G.
rostochiensis) and pale cyst nematode (G. pallida), that are major pests of potato in
the world. They are both of high economic importance, and quarantined under strict
regulations in Canada by the Canadian Food Inspection Agency (CFIA) as well as in
many other countries. In Canada, G. rostochiensis has been present on the Saanich
Peninsula of Vancouver Island, British Columbia, since 1965 (Orchard 1965), and
both G. rostochiensis and G. pallida have been present on the Island of Newfoundland
since 1962 (Olsen and Mulvey 1962; Stone 1977). In 2006, G. rostochiensis was
reported from potato in the Saint-Amable region, Quebec (Sun et al. 2007), con-
firmed by morphological and a phylogenetic analysis (Yu et al. 2010c) and later
determined to be pathotype Ro1 (Mahran et al. 2010b). Genetic analyses strongly
suggest that both species were probably introduced to Canada from Europe, and that
multiple introductions of G. rostochiensis occurred (Madani et al. 2010; Boucher
et al. 2013). In the bioclimatic condition of Quebec, the species was found to do a
single life cycle each year, however, a second hatching cohort was observed each year
and could soon result in a full second generation in light of climate change (Mimee
et al. 2015b). A few G. rostochiensis cysts were recovered from a sample from each
of two farms out of 2721 samples taken in Alberta in 2007 by CFIA (unpublished).
As a result, CFIA and USDA-APHIS instituted a bi-lateral monitoring program and
guidelines for declaration of a field containing PCN (CFIA USDA-­APHIS 2014).
1 Current State of Plant Parasitic Nematodes in Canada 13

1.4.2.1 Management of Globodera spp. in Canada

The potato cyst nematodes have a narrow host range, and their distribution in
Canada remains limited to a few well-defined sites. The management of the pests
includes containment and population reduction by using resistant varieties.
Immediately after the finding of the pests either in Newfoundland, BC, and Quebec,
delimitation surveys were carried out establishing the boundaries of the infestations,
followed by strict phytosanitary measures. A minimum measure was a ban on plant-
ing susceptible cultivars of potato. Good outcomes have resulted. On the Saanich
Peninsula a recent survey did not reveal any positive samples for G. rostochiensis
with the exception of one field with a history of quarantine infractions (Rott et al.
2010). In Saint-Amable, CFIA has authorized a 1-year production of resistant culti-
vars followed by a 2-year rotation with a non-host crop (Mahran et al. 2010b). This
strategy appears to have been effective, given that population densities quickly
dropped below detection levels (Bélair et al. 2016) and very few viable eggs remain
10 years after the establishment of the quarantine area (Mimee et al. 2017). However,
the implementation of quarantine measures was shown to modify the biodiversity
and abundance of weeds in the regulated fields, resulting in a significant increase of
nightshade weed species (Solanum spp.) that could support and serve as pest ref-
uges for G. rostochiensis (Mimee et al. 2014c). Globodera rostochiensis was already
known to reproduce on Canadian nightshades, and interestingly, the nematode pop-
ulations in the different provinces showed dissimilar host preferences for these
weeds (Rott et al. 2011).
Detection and precise species-level identification are critical issues in potato
cyst nematode management. For this purpose, a multiplex quantitative polymerase
chain reaction (qPCR) assay was developed for the simultaneous differentiation of
G. rostochiensis, G. pallida, and G. tabacum (Madani et al. 2008; Mimee et al.
2017). The same team also developed a method based on the heat shock gene hsp90
(Madani et al. 2011). It was recently shown that potato cyst nematode pathotypes
could be differentiated with specific single-nucleotide polymorphisms (Mimee
et al. 2015a). Thus, the next step will be to replace the long and expensive pathot-
yping assays in greenhouses with rapid and simple allele-specific oligonucleotide
PCR assays.
Even though the current Canadian populations have been characterized and strict
containment and monitoring is in place, awareness and vigilance is required moving
forward. Recently, a new species of potato cyst nematode, G. ellingtonae, was
described in Oregon (Handoo et al. 2012), and G. pallida was found in numerous
fields in Idaho (Skantar et al. 2007). These findings serve as reminders that under-
standing of the phylogenetic and geographic origins of potato cyst nematodes is not
complete and additional research is needed. Especially, new strategies effective against
all the pathotypes should be explored. For that, the recent publication of the genome
sequence of G. rostochiensis (Eves-van den Akker et al. 2016) and the transcriptome
variation during hatching and survival (Duceppe et al. 2017) will be very useful.
14 G. Bélair et al.

1.5 Ditylenchus spp.

1.5.1 Stem and Bulb Nematode, Ditylenchus dipsaci

Stem and bulb nematode is one of the most destructive nematode pests especially in
temperate regions. If not controlled, it can cause complete failure of host crops such
as onions, garlic, cereals, legumes, strawberries and ornamental plants, especially
flower bulbs. It is also an international quarantined nematode pest. In Canada,
Ditylenchus dipsaci was first reported on onion in one area of Ontario in 1957
(Mountain 1957) and then was found in nearby counties of Ontario in subsequent
years (Sayre and Mountain 1962; Johnson and Kayler 1972; Fushtey and Kelly
1975). It was reported in Saskatchewan on creeping thistle in 1979 (Watson and
Shorthouse 1979), then in British Columbia on alfalfa in 1983 (Vrain and Lalik
1983), Alberta in 1987 (Vrain 1987), and then in Quebec and Prince Edward Island
(CABI/EPPO 2009). The reported finding in Saskatchewan was likely a find of a
closely related D. weischeri. Although widely distributed, D. dipsaci was not con-
sidered to be a serious pest in Canada until the recent outbreak on garlic in Ontario.
The identity of the nematode in the outbreak was confirmed (Yu et al. 2010b), and a
subsequent survey showed that it was widespread in most garlic growing fields in
Ontario (Qiao et al. 2013). It has since spread to the neighbouring provinces of
Quebec (Réseau d’avertissements phytosanitaires 2013) and Manitoba (Hajihassani
and Tenuta 2017) and is an ongoing economic concern in Ontario (Celetti 2011).
One of the main challenges is the precise identification of D. dipsaci, which has
several races, each of which exhibits a different host preference, and thus managing
this nematode is complicated. A recent study showed that two distinct introductions
of this parasite into Ontario likely occurred and found genetic differences within a
race (Qiao et al. 2013). Sequence analyses of D. dipsaci and D. destructor (potato
rot nematode), initiated by Agriculture and Agri-Food Canada and the CFIA (Yu
et al. 2014), should make it easier to develop specific molecular diagnostic tests in
the future.
Recently, Ditylenchus populations that parasitize creeping thistle in Russia
(Chizhov et al. 2010) as well as Manitoba and Saskatchewan (Watson and Shorthouse
1979; Tenuta et al. 2014) were recognized to be D. weischeri. This species has a
very different host preference than D. dipsaci with specialization to creeping thistle
and no host compatibility with onion and strawberry (Chizhov et al. 2010), common
bean, chickpea, lentil, canola, wheat and garlic (Hajihassani et al. 2016). Yellow pea
seems to be a very weak host for D. weischeri, with Hajihassani et al. (2016) report-
ing that the nematode could survive but not reproduce on two of five varieties of
yellow pea examined. A follow-up study failed to show development and reproduc-
tion of the nematode on yellow pea at 17 and 22 °C but at a very high average tem-
perature of 27 °C (Hajihassani et al. 2017). Further, the nematode did not reproduce
or cause yield damage to yellow pea in a field study (Hajihassani et al. 2017).
Madani et al. (2015) reported species-specific PCR primers to differentiate D. dip-
saci and D. weischeri to aid screening of export and import commodities for the
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