DOI: 10.1111/epp.

13072

ORIGINAL ARTICLE

The utilization of biological control against regulated pests in the

EPPO region: challenges and opportunities

R. Tanner1 | S. Bluemel2 | A. Kapranas3 | M. Kenis4 | D. Matosevic5 | N. Horn1

1
European and Mediterranean Plant Abstract
Protection Organization, Paris, France
2
Biological control is a pest control method that can offer an environmentally
International Organisation for Biological
and Integrated Control, Zurich,
safer alternative to chemical pesticides. The proven safety record of both
Switzerland augmentative and classical biological control technologies allows its utilization
3
School of Agriculture, Aristotle against indigenous and non-­indigenous but well-­established pests, whether under
University of Thessaloniki, Thessaloniki, protected conditions (e.g., glasshouses) or in open field cropping systems. This
Greece
4
manuscript has been developed by the Joint European and Mediterranean Plant
CABI, Delémont, Switzerland
5
Protection Organization (EPPO) and the International Organization for Biological
Croatian Forest Research Institute,
Jastrebarsko, Croatia
and Integrated Control (IOBC) Panel on Biological Control Agents and presents
an assessment on the current use of classical and augmentative biological control
Correspondence for the control of regulated plant pests. The paper discusses challenges for the
R. Tanner, European and Mediterranean
Plant Protection Organization, Paris,
uptake of biological control for regulated pests and provides recommendations to
France. increase the safe use of biological control agents in the EPPO region.
Email: [email protected]

K EY WOR DS
augmentative biological control, awareness raising, classical biological control, invertebrate pests,
regional guidance, regulation

L’utilisation de la lutte biologique contre les organismes nuisibles réglementés dans

la région de l’OEPP : défis et opportunités
La lutte biologique est une méthode de lutte contre les organismes nuisibles qui
peut offrir une meilleure alternative pour l’environnement que les pesticides
chimiques. La sécurité des technologies de lutte biologique augmentatives et
classiques a été démontrée, et cela permet leur utilisation contre les organismes
nuisibles bien établis (indigènes et non indigènes), dans des conditions protégées
(par exemple, en serres) ou dans des systèmes de culture en plein air. Ce
manuscrit a été élaboré par le Panel sur les agents de lutte biologique conjoint
entre l’Organisation Européenne et méditerranéenne pour la Protection des
Plantes (OEPP) et l’Organisation Internationale pour la Lutte Biologique (OILB)
et présente une évaluation de l’utilisation actuelle de la lutte biologique classique
et augmentative contre les organismes nuisibles aux plantes qui sont réglementés.
Cet article aborde les défis du recours à la lutte biologique contre les organismes
nuisibles réglementés et fournit des recommandations pour accroître l’utilisation
en sécurité des agents de lutte biologique dans la région de l’OEPP.

Применение биологических мер борьбы с регулируемыми вредными

организмами в регионе ЕОКЗР: вызовы и возможности
Биологическая защита растений является комплексом методов борьбы с вредными
организмами, которые способны предложить более безопасную альтернативу
по сравнению с использованием химических пестицидов. Доказанные примеры

© 2025 European and Mediterranean Plant Protection Organization.

EPPO Bulletin. 2025;00:1–12.  wileyonlinelibrary.com/journal/epp | 1

 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
2 |    UTILIZATION OF BIOLOGICAL CONTROL

безопасного применения технологий массового выпуска агентов биометода и

классической биологической борьбы позволяют применять их против местных и
чужеродных успешно акклиматизированных вредных организмов, и делать это
как в защищенных условия (например, в теплицах), так и в системах открытого
земледелия. Данная статья подготовлена Совместной рабочей группой по
агентам биологической борьбы Европейской и Средиземноморской организацией
по карантину и защите растений (ЕОКЗР) и Международной организации
по биологической борьбе с вредными животными и растениями (МОББ). В
ней представлена оценка современного применения классических методов
биологической борьбы и технологий массового выпуска агентов биометода
для борьбы с регулируемыми вредными для растений организмами. В статье
рассматриваются проблемы внедрения биологической защиты растений от
регулируемых вредных организмов и даются рекомендации по повышению
безопасного использования агентов биологической борьбы в регионе ЕОКЗР.

1 | I N T RODUC T ION the non-­native target pest or with a closely related spe-
cies, and is introduced for permanent establishment and
The introduction and spread of plant pests such as long-­term control of the pest. This method is mostly
fungi, bacteria, viruses and invertebrates into new re- applied against invasive plant pests and invasive alien
gions threatens plant health and food security (Mwangi plants that may have become too widespread for the
et al., 2023; Riegler, 2018). We need to produce enough effective use of alternative control methods, such as
food to sustain the increasing global population, both phytosanitary measures, cultural or chemical control.
now and into the future, therefore measures to miti- Augmentative biological control can be defined as pe-
gate and control pest species before they have an eco- riodic and systematic release of mass-­produced BCAs
nomic impact on crops are paramount. Historically, the (either indigenous or non-­ i ndigenous), and these are
control of pests has relied heavily on the application often produced commercially. Augmentative biological
of chemical synthetic pesticides (van Lenteren, 2000). control can be further subdivided into seasonal inocula-
More recently, as concerns have grown over their neg- tion, in which BCAs can reproduce and persist through-
ative effects, consumer demand has swayed away from out the growing season, and inundation, in which BCAs
their use. This is echoed and engrained into regional cannot reproduce and must be frequently reapplied
policy, which is driven by societal and environmental throughout the growing season. These BCAs can be
safety [e.g., the European Green Deal and the Farm to applied within protected conditions as well as outdoors
Fork strategy (European Commission, 2024; European in cropping systems. Conservation biological control is
Union, 2020), EU biodiversity strategy for 2030 the practice of manipulating the environment or habi-
(European Commission, 2020)]. tat to promote beneficial organisms. Conservation bi-
The demand for a reduction in chemical pesticides ological control is practiced extensively throughout
begets novel, pragmatic and environmentally friendly the European and Mediterranean Plant Protection
approaches to pest control. Biological control is one Organization (EPPO) region, for instance with the es-
such approach. It is defined as the exploitation of living tablishment of field margins planted with plants or
agents (including viruses) to combat pests (including cover crops to attract and support natural enemies or in
pathogens, invertebrates and weeds) for diverse pur- protected crops by, for example, providing supplemen-
poses to provide human benefits (Stenberg et al., 2021). tary diets or shelters for BCAs (Castella et al., 2022; Van
Thus, biological control agents (BCAs) include viruses, Emedn, 1974).
microorganisms (microbial pesticides) and inverte- In some areas, the fact that biological control can
brates, such as entomopathogenic nematodes, preda- offer an environmentally safer alternative to chemi-
tory, parasitic and herbivorous arthropods and mites cal pesticides has led to certain BCAs wholly replacing
(macrobials). These organisms can be used to control chemical pesticides and in other cases to a significant
plant pests (including invertebrates and microorgan- reduction in chemical application (Calvo et al., 2012;
isms) and invasive alien plants, although the latter is van Lenteren, 2000). Usually, the aim of biological con-
not covered comprehensively in this paper. trol is to suppress the target pest population to an eco-
There are three types of applied biological control nomically acceptable damage level or below. However,
practices (Mason, 2021 and chapters within). Classical some BCAs can also be used for the control of pests,
biological control (or importation biological control) for example Encarsia formosa Gahan (Hymenoptera:
can be defined as the utilization of a non-­native nat- Aphelinidae) is sometimes recommended to eradicate
ural enemy that shares a co-­evolutionary history with Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae)
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
TANNER et al.     | 3

from greenhouses in situations where pesticides cannot control can also be applied to regulated pests under a
be used, such as in butterfly houses (M. Everatt, per- systems approach (ISPM 14: IPPC, 2019), where coun-
sonal communication). tries put into place two or more measures to control a
Biological control methods are most commonly pest to allow trade of a commodity to another country.
used against well-­established pests, whether under pro- The measures include pre-­and post-­harvest measures.
tected conditions or in open field conditions, either Biological control can be used to maintain a Pest Free
within a crop or the natural environment. For regulated Area (PFA) (ISPM 4: IPPC, 2017) and Areas of Low Pest
pests [defined as a quarantine pest or a regulated non-­ Prevalence (AoLPP) (ISPM 22: IPPC, 2016). In the for-
quarantine pest (RNQP) (ISPM 5; IPPC, 2023)], classi- mer, biological control could be used in the buffer zone
cal biological control has historically been applied when of a PFA, while for the latter, biological control can
the pest is too widespread for traditional control tech- be used in an AoLPP to suppress a pest population to
niques to be effective. However, more novel approaches below a threshold.
are being explored where, for example, pre-­emptive bi- Certain situations may warrant the use of biologi-
ological control of regulated Al pests (EPPO A1 pests cal control for the control of regulated pests instead of
absent from the region) is receiving increased attention chemical pesticides, for example in butterfly houses,
(Avila et al., 2023; Kenis et al., 2024; Kumar et al., 2020). post-­entry plant quarantine stations, public areas, or-
Additionally, biological control of pests with a restricted ganic farming and certain habitats within the natural
distribution (e.g., EPPO A2 pests) can be implemented environment (e.g., on or near water bodies).
as part of integrated pest management (IPM) to halt or
slow spread and reduce impact (e.g., Gotta et al., 2023;
Pérez-­Rodríguez et al., 2019). 2.1 | Classical biological control
The European and Mediterranean Plant Protection
Organization has worked on BCAs since 1997. In Classical biological control of insects has been repeatedly
2008, EPPO and the International Organization for shown to be a successful management practice since
Biological and Integrated Control (IOBC) formed the the successful release of the ladybird Rodolia cardinalis
Joint EPPO/IOBC Panel on Biological Control Agents (Mulsant) (Coleoptera: Coccinellidae) against Icerya
with the remit to work on the assessment and regula- purchasi Maskell (Hemiptera: Margarodidae) in citrus
tion of the import and release of BCAs agents in plant orchards in California, USA in 1888–89. In Europe,
protection. The Joint Panel has developed Standards there have been approximately 650 releases of classical
in the PM 6 series: Safe use of biological control (see BCAs, with around 130 of these releases significantly
Section 3.2). These Standards cover a range of biolog- impacting the target pest (Castella et al., 2022).
ical control practices, from the first import of a BCA Examples of successes in classical biological con-
for research purposes to conducting an environmen- trol in Europe include, among others, the control of the
tal risk assessment with the potential for release. The chestnut gall wasp [Dryocosmus kuriphilus Yasumatsu
Joint EPPO/IOBC Panel on Biological Control Agents (Hymenoptera: Cynipidae) using Torymus sinensis Kamijo
focuses its work mainly on invertebrate BCAs imple- (Hymenoptera: Torymidae)] (see Appendix 1), control
mented against invertebrate pests, and as such, this of the woolly whitefly [Aleurothrixus floccosus Maskell
manuscript mainly provides and discusses examples (Hemiptera: Aleyrodidae)] using Amitus spiniferus
within this context. (Brethes) (Hymenoptera: Platygastridae) and Cales no-
This manuscript discusses challenges for the uptake acki (Howard) (Hymenptera: Aphelinidae), control of
of biological control for regulated pests and provides San Jose scale [Comstockaspis perniciosa (Comstock)
recommendations to increase the safe use of BCAs in (Hemiptera: Diaspididae)] using Encarsia pernici-
the EPPO region. Examples of regulated pests given osi (Tower) (Hymenoptera: Aphelinidae), control of
in the paper may be recommended for regulation the citrus leafminer [Phyllocnistis citrella Stainton
by EPPO (A1 or A2 pests), regional regulated pests (Lepidoptera: Gracillariidae)] using Citrostichus phyl-
(e.g., EU) or pests regulated by specific EPPO coun- locnistoides Narayanan (Hymenoptera: Eulophidae),
tries. For further details on pest categorization see control of the eucalyptus psyllid (Ctenarytaina eucalypti
EPPO (2024a). Maskell (Hemiptera: Psyllidae) using Psyllaephagus pi-
losus (Hymenoptera: Encyrtidae, classical BCA PM 6/3)
and control of the cottony cushion scale (Icerya purchasi)
2 | USE OF B CA S AGA I N ST using R. cardinalis (Gerber & Schaffner, 2016).
R E GU L AT E D PE ST S Classical biological control against invasive
weeds in Europe has shown an increase in recent
Biological control can be applied against RNQPs, years with the release of Aphalara itadori Shinji
with the aim to reduce the level of pest presence below (Hemiptera: Aphalaridae) against Reynoutria ja-
a threshold to allow movement of plants for planting ponica (Polygonaceae), Aculus crassulae Knihinicki
(ISPM 16: IPPC, 2021; ISPM 21: IPPC, 2004). Biological & Petanović (Acarida: Eriophyidae) against
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
4 |    UTILIZATION OF BIOLOGICAL CONTROL

Crassula helmsii (Crassulaceae), Listronotus elonga- The steps of a classical biological control programme
tus (Hustache) (Coleoptera: Curculionidae) against include, among others, assessments of similar pro-
Hydrocotyle ranunculoides (Araliaceae), Puccinia ko- grammes implemented elsewhere against the same pest,
marovii var. glanduliferae Tanner, Ellison, Evans & surveys for natural enemies in the area of origin of the
Kiss (Pucciniales: Puccinia) against Impatiens glandu- pest and studies of their biology and ecology, importa-
lifera (Balsaminaceae) and Trichilogaster acaciaelongi- tion of natural enemies into quarantine laboratories, as-
foliae Froggatt (Hymenoptera: Pteromalidae) against sessments of their potential non-­target effects in the area
Acacia longifolia (Fabaceae). Globally, classical biolog- of introduction, application for release, field releases
ical control against invasive plants has achieved a good and post-­release studies (FAO, 2019). The whole process
rate of success, with over a quarter of biocontrol pro- up until the field release can take between 3 and 10 years
grammes resulting in complete control (where no other depending on whether efficient and safe natural enemies
control methods are needed to suppress the target spe- are already known at the beginning of the process, but
cies) and 50–70% achieving partial control (resulting also on various other factors (e.g., ease of rearing the
in a substantial reduction of other control methods) pest and natural enemies in the laboratory, number of
(Hinz et al., 2020). generations per year).
Historically, classical biological control has been To allow a BCA to be released at the same time or
criticized for its potential negative impact on native just after an outbreak of a regulated pest, the concept
biodiversity, which has occurred very occasionally of pre-­emptive classical biological control has been de-
(De Clercq et al., 2011; Palevsky et al., 2012; Rondoni veloped (Avila et al., 2023; Hoddle, 2023). This process
et al., 2020; van Lenteren et al., 2006). However, now- implies that risk and impact assessments are carried out
adays the selection of non-­indigenous natural enemies for natural enemies in advance of the arrival of a pest.
to be released as a classical biological control is more It may also mean that the BCA is approved for release
rigorous, and studies on the specificity of BCAs have prior to the pest arriving. Pre-­emptive biological control
become common practice, which strongly reduces the has already been applied for the egg parasitoid Trissolcus
risks of non-­target impacts (Hajek et al., 2016; Kenis japonicus (Ashmead) (Hymenoptera: Scelionidae), which
et al., 2017). Host specificity testing is a requirement has been approved for release in New Zealand to control
of many countries' regulatory systems. Most classical the brown marmorated stink bug (Halyomorpha halys)
biological control programmes now also comply with should it arrive in the country (Charles et al., 2019). Avila
Nagoya Protocol and access and benefit sharing agree- et al. (2023) provides guidelines and a decision frame-
ments (Leskien, 2023; Silvestri & Mason, 2023). work that can be used to assess the feasibility of conduct-
Classical biological control does not aim to eradicate ing pre-­emptive risk assessment for candidate BCAs.
a pest, but rather bring its population density below an In the EPPO region, a pre-­emptive biological control
appropriate ecological or economic threshold. It is ap- approach could be considered for all arthropod pests of
plied at the transitional phase between a quarantine pest the EPPO A1 List, but also priority pests on the EPPO
status and deregulation. Often, host plant destruction A2 List. Countries where the pest is not present could
and chemical control are preferred when attempting to start a classical biological control programme pre-­
eradicate a new outbreak of a regulated pest (Branco emptively in collaboration with countries where the pest
et al., 2023). When classical biological control is applied is present. A previous Euphresco project (Preparedness
early in the invasion process, it can potentially be very in biological control of priority biosecurity) has pro-
efficient to slow the spread of the invasive species under duced fact sheets for 30 regulated pests in the EU or
containment strategies. However, classical biological Oceania, describing current or past classical biological
control is often implemented late in the invasion process control efforts and suitable natural enemies for classical
against well-­ established invasive species, when other biological control against these pests. These fact sheets,
control methods are not successful or not sustainable available at the project website (https://​biolo​gical​contr​ol.​
and represent high risks for human health and the envi- eu/​), can be used to identify the most promising BCAs.
ronment. To be efficient against regulated pests, classi-
cal biological control programmes should be conducted
as soon as a pest arrives into a new region. However, 2.2 | Augmentative biological control
implementing a classical biological control programme
requires significant funding and infrastructure (quar- Augmentative biological control has been applied success-
antine facilities), specialized scientific personnel and fully in various agricultural systems from citrus orchards
time to develop both in terms of administration (e.g., in the Mediterranean (Jacas & Urbaneja, 2010) to the con-
issuing permits) and scientific investigation (foreign ex- trol of vegetable pests in large-­scale production facilities in
ploration, clearance from safety tests, application and Northern Europe for over 100 years (van Lenteren, 2012).
evaluation). Classical biological control is generally un- It is estimated that over 350 species of natural enemies
dertaken by public or not-­for-­profit agencies and applied have been utilized for augmentative biological control
non-­commercially, as a public good. against plant pests worldwide (Van Lenteren et al., 2018).
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
TANNER et al.     | 5

In recent decades, advances have been made in the mass Invertebrate BCAs are not covered by EU regula-
production, storage and methods for delivery and appli- tion. They are not relevant for consideration under
cation of BCAs that have led to products becoming more Regulation 1107/2009, which regulates pesticides and
widely available (van Lenteren, 2012). Nowadays, Europe the placement of such products on the market because
is the largest commercial market for invertebrate BCAs this is only relevant for micro-­organisms and viruses.
(Van Lenteren et al., 2018). Although BCAs can fall under other regulations [e.g.,
Augmentative biological control is applied against Regulation (EU) 1143/2014 on the prevention and
regulated and non-­regulated pests, and as well as in- management of the introduction and spread of inva-
vertebrates, microbial BCAs are used. For example, the sive alien species and Regulation (EU) 2016/2031 on
bacterium Bacillus thuringiensis is commonly used to protective measures against pests of plants], these are
eradicate new outbreaks of gypsy moth [Lymantria dis- not specific for their utilization as a BCA, but if the
par L (Lepidoptera: Erebidae)] and Asian gypsy moth (L. organism is to be assessed as a plant pest (Castella
dispar asiatica Vnukovskij) in North America and has et al. 2022).
also been used for the eradication of the painted apple The same is true for classical BCAs where their re-
moth [Teia anartoides Walker (Lepidoptera: Erebidae)] in lease can be restricted by environmental regulations,
the United States (Liebhold & Kean, 2019). Parasitoids and plant health regulations provide no provisions ex-
and predators are almost never used in eradication pro- cept to ensure, through pest risk analysis, that the or-
grammes because they are not sufficiently efficient to kill ganism is not a pest to plants (IPPC, 2005).
all their hosts or prey. However, they may be utilized in Regarding national legislation, detailed information
very specific cases where chemical insecticides cannot be for all EPPO countries is lacking. For the EU Member
applied (e.g., against regulated pests in butterfly houses States, Castella et al. (2022) detailed that 15 Member
or when several pests need to be controlled at the same States have introduced specific provisions in their na-
time, e.g., in post-­entry plant quarantine stations). tional legislation regarding invertebrate BCAs, three
As for classical biological control, pre-­ emptive bi- countries were developing regulatory provisions (at the
ological control can be carried out for microbial and national or regional level) and nine countries did not
macrobial augmentative BCAs against a regulated pest have any specific process to accommodate the use of in-
that is not yet in a country or a continent. For example, vertebrate BCAs. These differences can hinder the up-
Kenis et al. (2024) tested three European Trichogramma take of BCAs and restrict their effectiveness of regional
Westwood species to assess which one would be the biological control programmes (Barratt et al., 2021;
most efficient against the fall armyworm [Spodoptera Mason et al., 2017).
frugiperda (Smith) (Lepidoptera: Noctuidae)] in Europe. EPPO provides a framework for the safe use of BCAs
When efficient augmentative BCAs are known from in the EPPO region. The EPPO Standard PM 6/3 (5) bi-
the area of origin of the pest or from already invaded ological control agents safely used in the EPPO region
areas, those may be assessed for performance and safety (EPPO, 2021) provides a list of BCAs which are used in
in other (EPPO) countries. If safe indigenous or non-­ the EPPO region with no adverse effects or with accept-
indigenous BCAs are found, the registration procedure able adverse effects. In essence, this list (Appendix 1
could then be started before the arrival of the regulated Commercially or officially used BCAs and Appendix 2
pests (Babendreier et al., 2022). Classical BCAs successfully established in the EPPO
region) constitutes a ‘positive’ list of BCAs for the
EPPO region. Member countries may consider adopt-
3 | C H A L L E NGE S ing a simplified notification procedure for these BCAs
(EPPO, 2021).
There remain a number of challenges to achieve a higher
utilization of biological control against regulated pests
in the EPPO region. The Joint EPPO/IOBC Panel on 3.2 | Guidance
BCAs identified a number of these during the Joint
EPPO/COST SMARTER Workshop on the evaluation A lack of guidance and information on all aspects of
and regulation of the use of BCAs in the EPPO region, biological control can hinder its uptake and hamper
which was held in Budapest in 2015 (EPPO, 2015; harmonization. This can lead to different methods
Ward, 2016). Still, some of these challenges remain and being adopted between countries and can lead to a
key ones are detailed in the following sections. reduction in efficiency and quality of delivery. For the
EPPO region, the EPPO PM 6 Standards on safe use
of biological control provide a comprehensive set of
3.1 | Regulation guidance documents (see below) that can be used from
the first import of a BCA to evaluating an application
Augmentative invertebrate BCAs straddle a num- for release. Further guidance can be developed on
ber of different regulatory categories (Ward, 2016). specific technical aspects.
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
6 |    UTILIZATION OF BIOLOGICAL CONTROL

3.2.1 | EPPO PM 6 Standards 4.1 | Information dissemination

EPPO PM 6 series: Safe use of biological control Information dissemination acts to share knowledge on
biological control from risk assessments, educational
• PM 6/1 (2) First import of non-­indigenous biological material, information fact sheets and species-­specific in-
control agents for research under confined conditions formation along with successful case studies. Technology
(EPPO, 2023b). transfer can facilitate the uptake of biological control in
• PM 6/2 (4) Import and release of non-­indigenous bio- countries and regions where the method has a low rate of
logical control agents (EPPO, 2025). adoption and at the same time strengthen regional cooper-
• PM 6/3 (5) Biological control agents safely used in the ation. Information needs for different stakeholders implies
EPPO region (EPPO, 2022). the necessity to produce information in different formats.
• PM 6/4 (1) Decision-­support scheme for import and For example, risk assessors and risk managers may re-
release of biological control agents of plant pests quire different information formats compared to farmers,
(EPPO, 2018). managers and the general public. Information should in-
• PM 6/5 (1) Host specificity testing of non-­indigenous clude current case studies in addition to detailing historic
(classical) biological control agents used against inva- examples. Information also needs to be readily available,
sive alien plants (EPPO, 2023c). preferably on a dedicated platform. This was highlighted
in the 2022 EU Study on invertebrate BCAs (Castella
et al., 2022) and it is a concept that EPPO is exploring.
3.3 | Information Information deriving from risk assessment of non-­
indigenous BCAs should be available in a suitable
A paucity of information can lead to a lack of format to be disseminated to stakeholders along with
understanding by stakeholders and hinder the uptake a clear presentation of the risk/benefits of releasing
of biological control (Collatz et al., 2021). Castella a BCA. For instance, Defra in the United Kingdom
et al. (2022) highlighted that farmers often do not have asked stakeholders for their views on the potential re-
sufficient knowledge on invertebrate BCAs and their lease of Torymus sinensis (Kamijo) (Hymenoptera:
potential benefits, which can lead to a lack of uptake. Torymidae) into England to suppress populations of
Basic information on the methods used to determine Dryocosmus kuriphilus (oriental chestnut gall wasp)
the safety and efficiency of a BCA is often lacking in by presenting them with the full risk analysis report
popular information disseminated to stakeholders (Defra, 2020). The documented efficacy of this par-
(Catton, 2021). This can lead to scepticism in the way asitoid, at least in some countries has led to multiple
biological control practitioners select BCAs and a requests for releases (e.g., by chestnut growers, tim-
general perception of distrust. ber producers and natural forest managers), despite
the ability of the parasitoid to move naturally over
distances and across country boundaries (Matošević
3.4 | Awareness raising of biological control et al., 2017; Nieves-­A ldrey et al., 2019). This highlights
safety between all national bodies the need to explain scientific evidence in the context of
the expectations of stakeholders. It also highlights that
Biological control has a well-­established safety record some stakeholders are the ones who push for the imple-
(Barratt et al., 2018). However, there remains some ap- mentation of biological control.
prehension to adopt biological control techniques due Information will facilitate better decision making
to perceived uncertainty as to the safety of the method. when it comes to assessing BCA applications.
It is beyond the scope of this current paper to critically
discuss this specific aspect in detail, but it is evident that
a clear message on the benefits and successes in modern 4.2 | Awareness raising
day biological control programmes should be dissemi-
nated to all interested national bodies. Public interest and engagement for biological con-
trol of invasive pests can be more pronounced in sit-
uations where pests create significant social and
4 | R E COM M E N DAT ION S economic impacts for residents in urban and peri-­
urban neighbourhoods, such as the case of the emerald
The Joint EPPO/IOBC Panel on Biological Control ash borer Agrilus planipennis Fairmaire (Coleoptera:
Agents has produced a number of recommendations Buprestidae), which causes significant tree mortality
that can promote and strengthen the utilization of and involves a wide variety of stakeholders from the
biological control in the EPPO region. These are listed private and public sector. In Europe the native parasi-
below, in no particular order. toid Spathius polonicus Niezabitowski (Hymenoptera:
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
TANNER et al.     | 7

Braconidae) may be a suitable BCA for A. planipennis devastate the Mediterranean citrus growing region. The
and its potential for mass rearing and augmentative re- BCA Tamarixia radiata (Waterston) (Hymenoptera:
lease programmes is currently being examined (Evans Eulophidae) has been successfully used against D. citri
et al., 2020). However, experience shows that stake- in other regions of the world and a regional approach
holders might have a mixed perception of the advan- can act to facilitate its successful use in the EPPO region.
tage of using biological control for A. planipennis. On Countries at risk from D. citri can collectively conduct
the one hand, parasitoids may not act quickly enough research and implementation activities while in parallel
to reduce tree mortality in the short term, but on the they can prepare the groundwork for a risk assessment.
other hand biological control can be viewed as an en-
gagement tool with ‘officials being seen to take action’
(Marzano et al., 2020). In the latter situation it should 4.4 | Regional guidance
be communicated that the parasitoids will not save in-
fested trees but will reduce the population and slow the It is important to develop regional guidance for a biologi-
spread. Εven more, acceptance of biological control cal control framework. Priorities for EPPO Standards are
can be easier when alternative approaches such as pre-­ developed in the Joint EPPO/IOBC Panel on Biological
emptive felling of trees is also a measure. This can have Control Agents and agreed and approved at the coun-
low support among the general public due to the change try level by the EPPO Working Party on Phytosanitary
of neighbourhood aesthetics and also over uncertain- Regulation and the EPPO Council, respectively (see
ties of the cost of felling and replacement of trees. Section 3.2. for the current PM 6 Standards). New
The public should be informed about the threat reg- Standards are developed in consultation with the Joint
ulated species can cause to plant health and the natu- EPPO/IOBC Panel on Biological Control Agents. Two
ral environment, and agricultural commodities and the new Standards are to be developed in 2025: (1) a Standard
conditions under which biological control can be the on host specificity testing of invertebrate BCAs for inver-
appropriate strategy. The public should also be made tebrate pests and (2) a Standard on establishment poten-
aware that government agencies follow all regulatory tial of augmentative BCAs.
rules to safeguard public interest and therefore enhance To promote harmonization, countries may utilize
public trust (Warner & Kinslow, 2013). EPPO PM 6 Standards in national regulations.
The participation of stakeholders in online forums
and expert working groups can support the regulatory
underpinnings of using BCAs. This is the case for using 4.5 | Pre-­emptive biological control
exotic generalist arthropods in greenhouses which are
currently widely commercially available, yet in some Countries and networks should consider initiating pre-­
cases permits for their use have been declined (Paula emptive biological control against priority regulated
et al., 2021). pests currently absent from the EPPO region. Pre-­
emptive biological control requires careful communica-
tion with all stakeholders, including the public. In the
4.3 | Regional cooperation case of the pre-­emptive biological control programme
against H. halys in New Zealand, representatives
Regional cooperation in biological control should be from many cooperatives of various commodities (ap-
encouraged and fostered across the EPPO region and ples, pears, stone fruits, tomatoes, grapes etc.) formed
beyond. This is particularly important for research and the brown marmorated stinkbug (BMSB) Council
collaboration in classical biological control techniques, (GIA, 2024), which applied for pre-­emptive biological
but it can also facilitate the technology transfer of control to the New Zealand Environmental Protection
augmentative biological control. Authority. However, at the same time, notifications were
Classical biological control programmes are long-­ sent to the Ministry of Environment Primary Industries,
term investments that demand careful planning and a the Department of Conservation and other crown enti-
precautionary approach. The involvement and coopera- ties and local authorities such as Māori organizations,
tion of stakeholders is necessary for the implementation NGOs and stakeholders who had expressed an interest
and monitoring of progress whereas public engagement in being notified about applications for new organisms
and approval are essential. (e.g. Environmental Protection Authority, 2018). The
Regional cooperation is essential for a harmonized BMSB Council also runs ongoing public, importer and
and joined-­ up approach to the management of regu- tourist awareness campaigns for the BMSB. In addition,
lated pests. Take, for example, the recent occurrence of an oversight committee involving industry, government
Diaphorina citri Kuwayama (Hemiptera: Liviidae): EPPO and research representatives was established to rapidly
A1 pest) in the EPPO region (Israel 2022 and Cyprus approve to release a BCA for BMSB. Now T. japonicus is
2023) (EPPO, 2022, 2023a). As a vector of Candidatus approved for conditional release in the event that a pop-
Liberibacter spp., these pests have the potential to ulation of H. halys is detected (Caron et al., 2021).
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
8 |    UTILIZATION OF BIOLOGICAL CONTROL

4.6 | Contingency plans AC K NOW L E D GE M E N T S

The EPPO/IOBC Panel on Biological Control Agents
When relevant, biological control techniques should be provided important comments on previous drafts of this
included in contingency planning to ensure biological manuscript.
control is integrated, where possible, into emergency
measures and to understand any regulatory difficulties R EF ER ENCE S
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TANNER et al.     | 11

Silvestri LC, Mason PG (2023) Improved access to biological con-

trol genetic resources: navigating through the Convention on APPENDIX 1 - CASE STUDIES
Biological Diversity and the Nagoya Protocol. BioControl 68,
299–310. https://​doi.​org/​10.​1007/​s1052​6 -­​023-­​10183​-­​9
Stenberg JA, Sundh I, Becher PG, Björkman C, Dubey M, Egan PA, TORYMUS SINENSIS (HYMENOPTERA;
Friberg H, Gil JF, Jensen DF, Jonsson M, Karlsson M, Khalil
TORYMIDAE)
S, Ninkovic V, Rehermann G, Vetukuri RR, Viketoft M (2021)
When is it biological control? A framework of definitions, mech- One of the recent successful cases of classical biological
anisms, and classifications. J Pest Sci 94, 665–676. control of alien invasive species in the EPPO region is
Tanner R, Orlinkski A, Meyer J, Ward M, Lukić S, Glavendekić M, the introduction of the parasitoid Torymus sinensis for
McCann D (2019) EPPO contingency exercise workshop for a biological control of Dryocosmus kuriphilus Yasumatsu
forest pest, Zlatibor, Serbia, 2018-­11-­27/29. EPPO Bulletin, 49,
(Hymenoptera; Cynipidae), which is an EPPO A2 pest
298-300.
Torres JB, Bueno ADF (2018) Conservation biological control using and an EU Protected Zone Quarantine pest (Annex
selective insecticides – a valuable tool for IPM. Biological III). It is a pest on chestnuts (Castanea) that are native
Control, 126: 53–64 to China (Avtzis et al., 2019; Gibbs et al., 2011) and
Torrini G, Paoli F, Mazza G, Simoncini S, Benvenuti C, Strangi have been accidentally introduced with infested plant
A, Tarasco E, Barzanti GP, Bosio G, Cutino I, et al. (2020)
material to other parts of Asia, North America and
Evaluation of indigenous entomopathogenic nematodes as po-
tential biocontrol agents against Popillia japonica (Coleoptera: Europe (CABI, 2016; EFSA, 2010). It is considered as
Scarabaeidae) in Northern Italy. Insects 11, 804 one of the most serious pests of chestnuts as it seriously
Ugolini F, Massetti L, Pedrazzoli F, Tognetti R, Vecchione A, Zulini impacts yield (Battisti et al., 2014) and tree vigour
L, Maresi G (2014) Ecophysiological responses and vulnerabil- (Sartor et al., 2015; Ugolini et al., 2014).
ity to other pathologies in European chestnut coppices, heavily
Torymus sinensis has successfully been used as a
infested by the Asian chestnut gall wasp. Forest Ecology and
Management 314:38–49 classical BCA against D. kuriphilus in Japan (Aebi
Urbaneja-­Bernat P, Pérez-­Rodríguez J, Krüger K, Catalán J, Rizza et al., 2006; Gyoutoku & Uemura, 1985), the United
R, Hernández-­Suárez E, Urbaneja A, Tena A (2019) Host range States (Cooper & Rieske, 2007, 2011), and across Europe
testing of Tamarixia dryi (Hymenoptera: Eulophidae) sourced where Castanea is grown (Avtzis et al., 2019; Borowiec
from South Africa for classical biological control of Trioza er-
et al., 2014; Matošević et al., 2017; Nieves-­A ldrey
ytreae (Hemiptera: Psyllidae) in Europe. Biological Control 135,
110-116 et al., 2019; Quacchia et al., 2008). Like D. kuriphilus,
Van Emedn HF (1974) Conservation biological control: from the- Torymus sinensis is native to China. The parasitoid is
ory to practice. In 1st International Symposium on Biological highly specific, with a biology perfectly synchronized
Control of Arthropods. with its host. After release, it spreads very quickly by ac-
van Lenteren JC (2012) The state of commercial augmentative biolog-
tive flight or aided by the wind, which enables the para-
ical control: plenty of natural enemies, but a frustrating lack of
uptake. BioControl 57, 1-120. sitoid to cover huge distances in short periods of time
Van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja (Colombari & Battisti, 2016a; Matošević et al., 2017).
A (2018) Biological control using invertebrates and microorgan- When host populations are high, it builds its population
isms: plenty of new opportunities. BioControl 63, 39-59. very quickly and reaches high parasitism rates, which
van Lenteren JC (2000) A greenhouse without pesticides: fact or fan-
enables it to lower the host population quickly and ef-
tasy? Crop Protection, 19, 375-384.
van Lenteren JC, Bale J, Bigler F, Hokkanen HMT, Loomans AJM ficiently (Avtzis et al., 2019; Matošević et al., 2017). Post-­
(2006) Assessing risks of releasing exotic biological control release studies on the effects of T. sinensis showed that it
agents of arthropod pests. Annual Reviews of Entomology, 51: has no unacceptable impacts on non-­target species and
609–634. doi: 10.​1146/​annurev. that it can be safely used as a BCA (Ferracini et al., 2017;
Ward M (2016) The regulatory landscape for biological control
Gil-­Tapetado et al., 2023). Torymus sinensis has stable
agents. EPPO Bulletin, 46 249-253.
Warner K, Kinslow F (2013) Manipulating risk communication: and genetically diverse populations, which is not always
value predispositions shape public understandings of invasive the case with introduced classical BCAs (Matošević
species science in Hawaii. Public Understanding of Science et al., 2017). All these traits have enabled it to lower host
22:203–218. populations quickly to pre-­epidemic levels (Colombari
& Battisti, 2016b; Matošević et al., 2017).

How to cite this article: Tanner, R., Bluemel, S., TAMARIXIA DRYI (HYMENOPTERA:
Kapranas, A., Kenis, M., Matosevic, D. & Horn, EULOPHIDAE)
N. (2025) The utilization of biological control Tamarixia dryi [Waterston: Classical BCA (PM 6/3)]
against regulated pests in the EPPO region: is a classical BCA of Trioza erytreae Del Guercio
challenges and opportunities. EPPO Bulletin, 00, (Hemiptera: Triozidae), a vector of Citrus greening
1–12. Available from: https://doi.org/10.1111/ (‘Candidatus Liberibacter africanus’, ‘Ca. Liberibacter
epp.13072 americanus’ and ‘Ca. Liberibacter asiaticus’: EPPO A1
Pests). Trioza erytreae [EPPO A2 pest and a regulated
 13652338, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/epp.13072 by Rob Tanner - Cochrane France , Wiley Online Library on [04/02/2025]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
12 |    UTILIZATION OF BIOLOGICAL CONTROL

EU A2 Quarantine pest (Annex II B)] transmits the and Steinernema carpocapsae were frequently found to
bacterium under natural conditions in Africa, parts of infect P. japonica larvae in surveys (Glazer et al., 2022).
the Arabic peninsula and some Indian Ocean islands Commercially produced strains of H. bacteriophora
(Gottwald, 2010; McClean & Oberholzer, 1965). Trioza caused 46% grub mortality in field trials in northern Italy
erytreae is an EPPO A2 pest and a regulated EU A2 (Paoli et al., 2017). In Italy there are restrictions for releas-
Quarantine pest (Annex II B). ing non-­indigenous nematodes and therefore the search
Tamarixia dryi was utilized on the island of Réunion for local and better adapted strains is advised (Gotta
in the 1970s. As part of the TROPICSAFE EU funded et al., 2023; Torrini et al., 2020). It is important to mention
project, research was undertaken on the potential to that the indigenous nematodes responded in a density-­
use T. dryi in Europe (Urbaneja-­ Bernat et al., 2019). dependent manner to the presence of P. japonica but the
Host range testing showed that T. dryi only attacks extent of possible cascading effects on native scarab bee-
T. erytreae. The parasitoid was released in spring 2018 tle populations remains to be thoroughly assessed (Glazer
in Tenerife. It was originally released in the north of et al., 2022).
the island and 6 months later it had spread throughout
the island. It was also found in other Canary Islands.
In Tenerife, Gran Canaria and La Palma, the propor- TRICHOGRAMMA SPP. (HYMENOPTERA:
tion of orchards with T. erytreae had significantly re- TRICHOGRAMMATIDAE)
duced, highlighting an impact of the BCA. In mainland Spodoptera frugiperda (Lepidoptera; Noctuidae), the
Spain, the parasitoid was released in Galicia in 2019 fall armyworm, is a pest of maize and other crops na-
and 2020, and within 6 months it had spread more than tive to the Americas. Since 2016, it has been found in
20 km from the point of release. Eighteen months later Africa, Asia and Oceania (Kenis et al., 2023). It has
and with more than 45 releases, it had spread widely. In recently been detected in the EU (Cyprus, Greece
Pontevedra, A Coruña and Lugo, significant decreases and Romania), where it is a regulated quarantine pest
in the proportion of orchards infested with T. erytreae (EPPO, 2024b). Trichogramma spp. (Hymenoptera:
were recorded (Pérez-­Rodríguez et al., 2019). Trichogrammatidae) are egg parasitoids that are used
as BCA against S. frugiperda in other continents (Li,
de Freitas, et al., 2023a). However, Trichogramma spe-
HETERORHABDITIS BACTERIOPHORA cies vary in their ability to parasitize S. frugiperda egg
(RHABDITIDA: HETERORHABDITIDAE) masses, which are composed of one to three layers
Popillia japonica Newman (Coleoptera: Scarabaeidae) of eggs and are usually covered with a variable num-
was detected in northern Italy in 2014 and now affects ber of scales and hairs (Li, Ma, et al., 2023b; Navik
a considerable area of northern Italy and southern et al., 2024), therefore Kenis et al. (2024) preventively
Switzerland. It is a highly polyphagous species. Adults tested three common European Trichogramma spp.
can be found feeding on a wide range of trees, shrubs, on S. frugiperda eggs in quarantine in Switzerland:
wild plants and crops whereas larvae feed on roots in the Trichogramma brassicae Bezdenko, T. dendrolimi
soil (EPPO, 2024a). Popillia japonica is an EPPO A2 pest Matsumura and T. cacoeciae Marchal. They found
and a regulated EU A2 Quarantine pest (Annex II B). significant differences in the ability of Trichogramma
Heterorhabditis bacteriophora is a nematode species species to oviposit through the hairs and scales and
that is widely available, including for augmentative bio- to reach the lower egg layers. T. dendrolimi was shown
logical control of P. japonica larvae (grubs) in the soil. In to be the most efficient parasitoid of the three species
earlier studies it was determined that indigenous northern tested They concluded that more Trichogramma spp.
Italian strains were efficient for controlling P. japonica and other local natural enemies should be tested pre-­
(Marianelli et al., 2018). In fact, native H. bacteriophora emptively before S. frugiperda has invaded Europe.