Suggestions for unifying the terminologyin biological control
J. EILENBERG1, A. HAJEK2 and C. LOMER1
1Department of Ecology, Royal Veterinary and Agricultural University (KVL), Frederiksberg,Denmark;e-mail J. Eilenberg: [email protected]; e-mail C. Lomer: [email protected];2Department of Entomology, Cornell University, Ithaca, New York, USA;e-mail A. Hajek: [email protected]
Received 28 December 2000; accepted in revised form 3 August 2001
Abstract. This paper gives suggestions for unifying the terminology in biological controlacross different research disciplines, such as biological control of arthropods, weeds and plantpathogens. It is suggested that use of the term ‘biological control’ is restricted to the use ofliving organisms. Four strategies of biological control are outlined and defined: (1) Classicalbiological control, (2) Inoculation biological control, (3) Inundation biological control, and(4) Conservation biological control. It is proposed to use these four terms as defined, andavoid usage of the term ‘augmentation’. Terms for specific processes and modes of action (forexample, ‘parasitoid’ and ‘competitor’) can be defined by usage within the different biolog-ical control disciplines. Microbial control usually indicates biological control of invertebratesusing microbes and, as such, is a subdivision of biological control. Use of additional auxiliaryterms such as biopesticide is discussed.
Biological control is a rapidly growing area which brings together scientistsfrom many disciplinary backgrounds. Ecologists, entomologists, weed scient-ists, plant pathologists, insect pathologists and microbiologists all approachthe subject from different angles, and have in part developed specialisedvocabularies. The major uses of biological control agents are: (1) biolog-ical control of invertebrate pests using predators, parasitoids and pathogens,(2) biological control of weeds using herbivores and pathogens, and (3)biological control of plant pathogens using antagonistic micro-organisms and
388 J. EILENBERG, A. HAJEK AND C. LOMER
induced plant resistance. In addition, biological control is now also beginningto be explored in veterinary and human medicine research and practice. In thispaper, we will discuss the terminology for categorizing methods by whichbiological control agents are released, applied or manipulated.
Each discipline uses biological control toward a reduction in disease orpests through the activity of biological control agents. The different traditionsin the disciplines of biological control workers have, however, led to lack ofa common terminology. Each group has more or less their own terminologyor their own perception of the same terminology. Within plant pathology,there is a tendency to focus on the process (mode of action), so biologicalcontrol is often defined as the application of ‘antagonists’ and ‘competitors’,or ‘induced resistance’. Entomologists also often describe biological controlas the use of different organisms with specified modes of action, for example‘predators’ or ‘parasitoids’ or by the methodology for release: ‘mass release’or ‘inoculative augmentation’. Further, entomologists speak often of release,while plant pathologists use the term application. Insect pathologists tend topick up words from the pesticide industry and speak of ‘biopesticides’ (forexample, the use of Bacillus thuringiensis (Berliner)). The term ‘microbialcontrol’ is often used to describe biological control of invertebrate pests usingmicro-organisms. Within weed control research using arthropod biologicalcontrol agents, much terminology is in common with entomological research.For controlling weeds with microbes, while similar terminology for strategiesis used, definitions differ to some extent (Charudattan, 1988).
Certainly, we acknowledge that each discipline has good reasons forstressing specific processes or modes of action, but these are often not relevantacross disciplines. The use of different terms leads to confusion, and espe-cially as biological control is attracting public and regulatory attention, wefelt that an attempt to harmonise some of the terminology would be of benefitto scientists in all included disciplines as well as to agronomists, extensionagents, regulatory officials and other non-specialists. Although we approachthe subject from the perspective of applied entomology, we hope this paperwill provoke some discussion and lead eventually to some widely-accepteddefinitions that will be of use to practitioners in the field, no matter whichtype of pest needs to be controlled or which type of biological control agentis being used.
For ease of reference, we introduce the terms we are discussing in boldface, and our recommended definitions are inset in italics. Each definitionis then discussed. As far as possible, we have used authoritative sourcesfor the definitions, but in nearly all cases we have found it necessary tomodify the definitions we have found. We have attempted to identify caseswhere several different terms are used to describe the same concept, and
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Figure 1. The relationship between biological control and other strategies for pest manage-ment. The principal aim of the diagram is to place biological control in its larger IPM context.Placing the order of the boxes as shown helps draw parallels between cultural control (agro-nomic practices which target the pest itself) and conservation biological control (agronomicpractices targetting the pest’s natural enemies). Similarly, the close relationship between theuse of conventional pesticides and botanical pesticides (in biorational chemical agents) can beseen. We consider the use of transgenic plants to be included in the box ‘host plant resistance’.(Modified from Nordlund, 1996)
explain our recommendations aimed toward reducing the number of termsin use. Our goal throughout is to propose concise definitions of terms usedin biological control rather than to provide a complete history of the termin-ology. Several good and extensive reviews with many examples of biologicalcontrol terminology within entomology, plant pathology and weed sciencehave been published during recent years (for example, Barbosa and Braxton,1993; Nordlund, 1996; Crump et al., 1999).
As shown in Figure 1, we keep biological control in the framework ofintegrated pest management (IPM) as defined by Kogan (1998): ‘IPM is adecision support system for the selection and use of pest control tactics,singly or harmoniously co-ordinated into a management strategy, based oncost/benefit analyses that take into account the interest of and impact onproducers, society and the environment.’
Biological control is thus used along with other control strategies. IPMprovides a structure within which to choose control methods, possiblyincluding biological control, in order to select the control strategy which ismost favourable taking production, ecology and society into consideration.
‘The use of living organisms to suppress the population density or impact ofa specific pest organism, making it less abundant or less damaging than itwould otherwise be’
We use, as is generally accepted, the terms ‘biological control’ and ‘biocon-trol’ interchangeably. The definition we prefer is slightly modified from thatgiven by Crump et al. (1999). The often cited definition by DeBach (1974)includes the elements of biological control agents, referred to as naturalenemies, and population regulation. This is relevant for much biologicalcontrol with the focus on insects and mite pests using predators and para-sitoids (see Garcia et al., 1988). However, dynamics at the population levelhave not been as well studied for microbial biological control agents and, inmany cases, sustained regulation of the pest population is not expected afterrelease (or application) of microbes.
It is noteworthy that our definition stresses the point that ‘living organ-isms’ are used. We believe, that this definition should include insect viruses,while genes or gene fragments are excluded. Also, metabolites from insect orweed pathogens or competitors to plant pathogens, used without the organ-isms producing them, are excluded. We strongly recommend that the term‘biological control’ should always be restricted to the use of living organisms,including viruses.
Microbial control is a useful term to describe the use of micro-organismsas biological control agents. It should be considered a sub-set of biologicalcontrol. The strategy is often inundation, but authors should in any casealways clarify the intended use strategy in biological control, e.g., classical,inoculation, inundation or conservation (see below).
The relationships between biological control and other pest managementmethods are outlined in Figure 1. The subdivision of biological control thenincludes four strategies, each clearly separated from the other and withoutreference to the specific mode of action or processes involved. The fourstrategies are (Figure 1): ‘Classical biological control’, ‘Inoculation biolog-ical control’, ‘Inundation biological control’ and ‘Conservation biologicalcontrol’. While these four terms are not strictly speaking grammaticallyconsistent, it would be difficult to recommend grammatically precise termswithout introducing clumsiness – neither ‘conservative’ nor ‘conservational’would be likely to replace the current established usage of ‘conservation’biological control. As it is impossible to find consistency between the estab-lished terms ‘classical’ and ‘conservation’, it becomes largely a question ofpreference whether to use ‘inoculation’ and ‘inundation’ or ‘inoculative’ and
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‘inundative’. We prefer the two former terms in conjunction with ‘biologicalcontrol’, but the latter in conjunction with ‘releases’.
Classical biological control
‘The intentional introduction of an exotic, usually co-evolved, biologicalcontrol agent for permanent establishment and long-term pest control’
This definition is clear and concise and in agreement with other definitions,e.g., FAO (1996), Coombs and Hall (1998). This was the main strategyon which early growth of this field was based, after the great success ofreleases of the vedalia beetle (Rodolia (Vedalia) cardinalis Mulsant (Cole-optera: Coccinellidae)) against the cottony cushion scale, Icerya purchasiMask. (Homoptera: Margarodidae), in California in the late 1800s. Becauseof the early development and use of this strategy, it has been called ‘classical’(Greathead, 1994). The bulk of the literature on classical biological controlintroductions describes releases of insect parasitoids and predators to controlother insect pests and insect herbivores to control weeds. This strategy is alsoapplicable to the deliberate release of micro-organisms, and has been usedless frequently to control arthropods (e.g., Hajek et al., 2000) and weeds butis not used for control of plant pathogens. The principle focus in plant patho-logy is on agriculture and therefore, both plant pathogens and their associatedbiological control agents are largely considered to have extremely broad, ifnot world-wide, distributions, thus negating the primary classical biologicalcontrol requirement for exotic biological control agents.
This same strategy has been called ‘importation’ by Nordlund (1996), butagents used for other strategies, such as inundation and inoculation biologicalcontrol, can also be imported, so the term importation could lead to confu-sion. This practice is also referred to as ‘introduction of natural enemies’ byVan Driesche and Bellows (1996) or ‘initial augmentation’, but again suchterminology does not distinguish this strategy from others. The goal of clas-sical biological control, permanent establishment of a biological control agentfor self-sustained long term control, distinguishes clearly this strategy frominundation and inoculation biological control, thus requiring a distinct namefor this practice.
The definition of classical biological control does not depend on achievingcomplete control. Thus the term ‘semi-classical biological control’ usedto describe a programme using an exotic virus to control palm rhinocerosbeetle, Oryctes rhinoceros L. (Coleoptera: Scarabaeidae) in the South Pacific(Hunter-Fujita et al., 1998) is not necessary. This virus has been released onindividual islands but must be released again after a number of years because
392 J. EILENBERG, A. HAJEK AND C. LOMER
its effect diminishes with time. We feel that this additional term, based on theresult of the programme, is not needed. Instead, the strategy for the initialreleases should correctly be named classical biological control. However,because the virus only provides control temporarily from initial classicalbiological control releases, this would then be followed by inoculationbiological control (see below).
Classical biological control depends on finding an appropriate biolog-ical control agent that is not native to the area where the pest needs to becontrolled. Thus, classical biological control requires the introduction of an‘exotic’ organism. In practice, for some natural enemies different races orbiotypes within the same species can have vastly different attributes, complic-ating determination of whether an agent is exotic or not. Whether an organismis ‘exotic’ can also be complicated when the control operation is taking placeanywhere other than on an island. In the case of large countries with manydiffering ecozones, authorities often consider an organism from a differentecozone as exotic. In the case of small countries in the same ecozone, nationalauthorities generally consider any importation across a national border as anexotic introduction. More recently, use of molecular characterisation has beenmaking determination of the area of origin of both biological control agentsand pests possible, enabling scientists to determine whether a natural enemyis exotic or not.
Originally, classical biological control was predominantly focused oncontrol of introduced pests with the goal of re-establishing host/natural enemyassociations that keep pests in check in their areas of origin (Table 1).However, this strategy has also been applied against native pests, in somecases successfully (e.g., see Carruthers and Onsager, 1993). The term ‘neo-classical biological control’ has been used when an exotic natural enemy isintroduced against a native pest (Table 1). However, then how do we referto introductions of exotic natural enemies against exotic pests with whichthey did not coevolve? We feel a more simple and descriptive term specific-ally referring to introductions of any exotic natural enemies against pestswith which they did not coevolve is ‘new’ or ‘novel association’ (Hokkanenand Pimentel, 1989). This would be a subcategory within classical biolog-ical control, while introduction of natural enemies that co-evolved with anintroduced pest would be considered the standard type of classical biologicalcontrol, not needing a specialised name. We introduce this concept in thecontext of classical biological control because much of the discussion of theuse of new associations has centered around this area.
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Table 1. Types of classical biological control programs based on the history of the pest/naturalenemy association and the geographical origins of pest and natural enemy
Origin Origin of Recommended Other terms used
of pest biological control agent terminology
Exotic Exotic (same as pest) (Original) Classical
biological control
Native Exotic New association classical Neoclassical biological
biological control control
Exotic Exotic (different New association classical
from pest) biological control
Inoculation biological control
‘The intentional release of a living organism as a biological control agentwith the expectation that it will multiply and control the pest for an extendedperiod, but not permanently’
This definition is modified from the definition given by Crump et al. (1999).The separation of inoculation from inundation is clear. A release with theexpectation that the released organism will control the target after multi-plication, is inoculation. In glasshouses, the early release of parasitoidsand predators, often with alternative food sources, is inoculation biolog-ical control. Examples of this are the releases of Encarsia formosa Gahan(Hymenoptera: Aphelinidae) and other natural enemies, now commonly prac-tised in glasshouses (Eilenberg et al., 2000; van Lenteren, 2000). The numberof insects released is insufficient to control the pest insects, and successdepends on the ability of the released organisms to multiply and reduce thetarget population. At the end of the season, the glasshouse is emptied, andno permanent establishment of the biological control organisms is achieved.When the next generation of plants is grown in the glasshouse, the predatorsand parasitoids should be released again. This type of release or applicationto control pest insects is strongly dependent on population regulation anddensity dependent processes.
In naming the strategy being used, the number of biological controlagents released is not at issue. Rather, the necessity for reproduction bythe biological control agent is important. Usually with inoculative releasesof parasitoids and predators, low numbers are released, in part because ofunacceptable expenses of releasing large numbers. In contrast, for control of
plant pathogens, while larger numbers of microbial antagonists are released,it is the offspring from these releases that lend control, so these applicationswould be considered inoculative.
The term ‘augmentation’ poses difficulties. In glasshouses, this term hasbeen used for a long time to describe biological control when the balancebetween the inundative and inoculative effects of a released organism is notknown in detail and may not be highly relevant. However, precisely becausethe term ‘augmentation’ does not imply a clear understanding of the ecolo-gical process occurring, we recommend avoiding its use in descriptions ofbiological control strategies.
Insect pathogens can be used for inoculation. The fungus Beauveriabrongniartii (Sacc.) Petch (Deuteromycotina: Hyphomycetes) has beenreleased in Switzerland for control of the cockchafer Melolontha melolonthaL. (Coleoptera: Scarabaeidae) with the aim that the fungus would multiplyand more long term control would be obtained. In practice, the fungus prolif-erates, long term control is achieved, but additional inoculation is needed later(Keller et al., 1997).
An example from plant pathology is a rust fungus, Puccinia canicu-lata (Schw.) Lagerh. (Uredinales: Pucciniaceae), which occurs naturally andseasonally in parts of southern USA on yellow nutsedge. However, the rustdoesn’t build up to epidemic proportions until the plant is several weeks oldand has already affected crop yields. By releasing the rust spores a few weeksbefore the expected onset of the epidemic, it has been possible to trigger anearlier epidemic than normal (Phatak et al., 1987).
The distinction between inoculation biological control and classicalbiological control is principally as follows: For both strategies, low levelsof material are usually released, although this is not a prerequisite for eitherstrategy. However, if an exotic organism is released with the aim of long-term control without additional releases, it is classical biological control. Ifreleases only result in temporary control and additional releases are needed,this is inoculation biological control. In practice, if classical biological controlreleases only provide partial or temporary control, subsequent releases toachieve increases of biological control agents in the environment are inocu-lative because the organism is now present in the environment and not exoticany more.
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Inundation biological control
‘The use of living organisms to control pests when control is achievedexclusively by the released organisms themselves’
The definition is modified from Van Driesche and Bellows (1996). Asdiscussed above, it is important to distinguish clearly between inoculationbiological control and inundation biological control, as both the practicalapproach and ecological implications distinguish these two strategies. Inund-atively released biological control agents must normally contact and kill asufficiently high proportion of the pest population or by other means reducethe damage level to give economic control before dispersing or being inac-tivated. The success depends solely on the released population and not theirprogeny; thus attention is paid to storage, formulation and application. Bycontrast, if an inoculative release is intended, sufficient pest numbers (orother means for growth of the biological control agent) must be maintainedfollowing the initial release to support a second or third generation of thereleased agent, and attention must be focussed on ensuring that conditionsenable this multiplication to take place. An important feature of this definitionis that although we apply the biological control agent without the expectationthat it will reproduce, it must be a living organism capable of reproduction. Inpractice, inundation biological control is probably often followed by residualeffects (some inoculative effects), if there is limited multiplication of thereleased organism.
Understanding the difference between inoculative and inundative releasescan be important to regulatory agencies. To examine risks to non-targetorganisms, it is essential to know if an organism is expected to persist andproliferate in the environment (classical biological control and inoculationbiological control) or, if it is expected to decrease significantly over time (ausual assumption of inundation biological control).
Any mass-release with the expectation of immediate effects by the indi-viduals released should be termed inundation biological control, irrespectiveof the mode of action. An obvious example of inundation is the use of livingB. thuringiensis spores for insect control: The bacterium is released in highnumbers per unit area with the aim of quickly killing a sufficiently highnumber of target insects. B. thuringiensis spores will then decrease in numberover time and there is no expectation of long term pest control.
A further example of this is the use of Metarhizium anisopliae (Metschn.)Sorokin var. acridum Driver and Milner to control grasshoppers in the Sahel(Langewald et al., 1999). Although there is some evidence for recycling ofspores and thus the potential for inoculation biological control (Thomas etal., 1995), in practice there is not sufficient time during a hopper infestation to
wait for epizootics to develop. Sufficient inoculum, in the form of infectiousfungal conidia, is released to contact > 90% of the population. Secondaryinfections may develop; their role in control is unclear, but may contribute toinfection of invading and hatching insects (Lomer et al., 2001).
Agents used for inundative releases, especially micro-organisms, are alsocommonly called ‘biopesticides’. However, this term has been used byCopping (1998) and Hall and Menn (1999) to include botanical pesticidesand pheromones. Although there are strong arguments in favour of reservingthe term biopesticide for preparations containing living (micro-) organisms,our suggestion is that authors using the term ‘biopesticide’ should alwaysspecify what is meant. US-EPA regulations refer to ‘microbial pest controlagents’, which we feel is a more self-explanatory and complete term than‘biopesticide’ for these biological control agents. Crump et al. (1999) givea good discussion of other terms such as ‘mycoherbicide’ and ‘biopestistat’and we refer readers to this article about specialised terminology in microbialweed control. In general, however, the proliferation of novel terms unfamiliarto the reader should be avoided unless essential. Crump et al. (1999) also raisethe issue that the use of the suffix ‘-cide’ tends to highlight an associationwith pesticides. Whether this is a negative association in the mind of environ-mentalists, or an expectation of rapid kill in the mind of farmers, it is clearlyan association which should be avoided if inundation biological control is toachieve wide acceptance. In addition, use of ‘-cide’ refers to mortality andtherefore would be inappropriate for antagonists of plant pathogens that actthrough competition and not by direct mortality. Bateman and Luke (2000)have also given a recent review on the term ‘biopesticide’, and we refer tothis article.
Conservation biological control
‘Modification of the environment or existing practices to protect and enhancespecific natural enemies or other organisms to reduce the effect of pests’
This definition has been modified from Debach (1974) to include the fact thatbiological control agents and other living organisms can be both protected andenhanced. Importantly, conservation biological control is distinguished fromother strategies in that natural enemies are not released. This approach is acombination of protecting biological control agents and providing resourcesso that they can be more effective. Therefore, conservation practices includelimited and selective use of pesticides but also active processes such asproviding refuges adjacent to crops or within crops, facilitating transfer of
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natural enemies between crops or even directly provisioning food or shelterfor natural enemies (Van Driesche and Bellows, 1996).
As an example of conservation biological control, alternative habitats fornatural enemies are provided, in the form of ‘beetle-banks’ in Britain or‘sown seed strips’ in Switzerland in cereal crops. These practices are highlysuccessful and are among the few documented uptakes of a biological controloption in temperate open-field arable agriculture (Landis et al., 2000).
For controlling plant pathogens, use of ‘suppressive soils’ is conservationbiological control. Some suppressive soils are locally naturally occurringso those geographic areas should be used for specific crops. For example,in the Chateaurenard district of the Rhone Valley, soils suppress Fusariumoxysporum f.sp. melonis (Weimer) Snyder and Hansen that infects melonselsewhere. To enhance soils that are not naturally suppressive, adding organicmatter increases microbial activity leading to control of several differentroot pathogens, including the traditional addition of green organic matter atplanting to antagonize Streptomyces scabiei corrig. (ex Thaxter) Lambert andLoria, the pathogen causing potato scab (Campbell, 1989).
We suggest use of the term ‘conservation biological control’ whendescribing this strategy due to widespread and long term usage of this term(Debach, 1974; Barbosa, 1999). Van Driesche and Bellows (1996) calledthis practice ‘natural enemy conservation’. With a more divergent viewpoint,Nordlund (1996) proposed that ‘conservation’ includes ‘actions taken toprotect or maintain existing populations of biological control agents’. Under acategory of ‘augmentation’, he lists ‘environmental manipulation’ as ‘altera-tions of the environment designed to protect or increase existing populationsof biological control agents’. Our view of conservation would include boththe ‘conservation’ and ‘environmental manipulation’ of Nordlund (1996). Weprefer a more stream-lined approach, grouping the diversity of methods forutilising pre-existing biological control agents within the same category ofstrategy.
It can be hard to distinguish clearly between conservation biologicalcontrol, ‘cultural control’ and ‘good farming practice’. We consider thatconservation biological control is being practised when specified naturalenemies are protected and enhanced in order to obtain control of specifiedpests. Cultural control will tend to target the pest population directly and notthe biological control agent, and good farming practice may extend to newsituations, practices which have been shown to reduce pest incidence in other,similar situations.
Clearly, in attempting to provide dictionary-style definitions for complex real-life ecological interactions, areas of overlap in practical implementation ofbiological control will result. We also realise that our main entrance to discussthis subject is our experience in plant protection, and additional discussion isneeded for other areas such as medical and veterinary pest control or controlof marine pests. Nevertheless, we hope that these modified definitions willprove to be sufficiently clear and distinct to be useful. We hope that thiseffort will enhance the abilities for biological control practitioners in thesame as well as different disciplines to exchange information, more readilytransferring approaches and information from one field to another.We recommend that:
• Use of the terms ‘biological control’ or ‘biocontrol’ is restricted to the useof living organisms.
• The four definitions of different strategies are adopted within all biologicalcontrol work.
• The journal BioControl and similar journals introduce these four termsas key-words, indispensable for manuscripts on biological control fieldapplications.
• Plant pathologists and weed scientists should consider how customarymodes of action such as induced resistance and antagonism are used withinthe proposed definitions of strategies.
• Whenever using terms such as ‘biopesticides’, ‘mycoherbicides’, etc., andsimilar, authors should briefly define or give a short explanation of whatthey mean by these terms.
Acknowledgments
We have received constructive criticism and inputs from: Roy Bateman, R.Charudattan, Jim Deacon, Peter Esbjerg, Heikki Hokkanen, Joe Kloepper,Joop van Lenteren, Rachel MacFadyen, Nick Mills, Eric Nelson, PeterNeuenschwander, Chris Prior, Fritz Schulthess, and John Whipps, plus twoanonymous reviewers. We appreciated all inputs for our discussion and for thepreparation of the revised manuscript. The final definitions and discussions inour article are, however, the conclusion of the group of authors.
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