Can plants use entomopathogens as bodyguards?AbstractFor 20 years, ecologists have been gathering evidence in support of the hypothesis thatplants can use insect natural enemies such as predators and parasitoids as bodyguards toprotect themselves from herbivory, but entomopathogens have escaped thisconsideration. We extend the bodyguard hypothesis to ask whether plants can useentomopathogens as bodyguards. We first discuss the evolutionary context of suchtritrophic interactions and then categorize possible mechanisms as: (1) maintaining apopulation of bodyguards on the plant surface, (2) increasing contact rates betweeninsect host and pathogen and (3) increasing the susceptibility of the host. We explorethese mechanisms further, examining published studies for evidence for the hypothesis.We then discuss potential costs to the plant of promoting pathogens as bodyguardswhich may include a reduction in the efficiency of other ``bodyguard'' species, theincidental promotion of plant pathogens and the risk of entomopathogens developingphytopathogenicity. Aside from our intention to stimulate the testing of the bodyguardhypothesis with entompathogens and to provide a conceptual framework for this, wehope to bring evolutionary ecology and insect pathology closer together.KeywordsBiological control, bodyguards, epizootiology, insect pathology, mutualisms, plantdefence, tri±trophic interactions.Ecology Letters (2000) 3 : 228±235INTRODUCTIONThere is something of a gulf between insect pathology andevolutionary ecology. Insect pathologists have historicallybeen concerned with description of pathogens and theirapplication to the resolution of pest problems. Reviews ofthe field have mainly been mechanistic syntheses. Mean-while, many evolutionary ecologists developing theoryhave tended to skirt around insect pathogens.In the area of tri-trophic interactions between plant,insect herbivore and pathogen of the herbivore, therehave been many experimental studies of an applied bent,and one review (Duffey et al. 1995), the subject alsoreceiving brief treatments in other reviews (e.g. Cory et al.1997; Hajek 1997). Throughout this literature, there is amodest assumption that observed effects of the plant onthe pathogen are the result of evolved defences toherbivores or phytopathogens. In the meantime, ento-mologists working on predators and parasitoids havespent nearly 20 years following up a suggestion by Price etal (1980) that natural enemies of herbivores could beconsidered part of the battery of defences available to aplant. This is increasingly yielding evidence that plantsmay use natural enemies as bodyguards (a term ascribed tothe interaction more than a century ago; see Bentley 1977),by providing food or shelter for the enemies (e.g. Jolivet1996; Walter 1996) or by producing herbivore-inducedvolatiles to betray the presence of herbivores (see Sabeliset al. 1999a, b). Curiously, the possibility that pathogensmay be involved in similar mutualistic interactions withplants, whilst implicit throughout the literature, haslargely been overlooked by both sets of scientists.In this review, we ask whether plants can use entomo-pathogens as bodyguards. We argue that to understand theevolution of bodyguard interactions requires a connection tobe made from the plant trait which affects the pathogen,through direct and indirect effects on the dynamics of theherbivore on the plant, to fitness consequences for the plant.We use this approach to recast some empirical studies in thelight of the bodyguard hypothesis. In this, our aim is not toconvince the reader that our explanation is universallyapplicable. It is rather to provide an alternative hypothesis,which at times is inevitably speculative in nature, to thosenormally explored. We have avoided a taxonomic treatmentof the pathogens, or any related predictions according to lifehistory, as the absence of literature specifically testing thishypothesis would render any such generalities at bestpremature and at worst limiting.#2000 Blackwell Science Ltd/CNRSSam L. Elliot,1Maurice W.Sabelis,1Arne Janssen,1Leo P. S. van der Geest,1Ellen A. M. Beerling1,2and Joanne Fransen21Section Population Biology,University of Amsterdam,Postbus 94084, 1090 GBAmsterdam, The Netherlands.E-mail: [email protected] Station forFloriculture and GlasshouseVegetables, Linnaeuslaan 2a,1431 JV Aalsmeer, TheNetherlands.Ecology Letters, (2000) 3 : 228±235REVIEWAhedBhedChedDhedRef markerFig markerTable mar-kerRef endRef startPaper 137 DiscThe flip-side of bodyguard interactions is then examined:costs for the plant to promote the pathogens such aspotentially diminished efficiency of other ``bodyguard''species, the incidental promotion of plant pathogens andthe risk of entomopathogens developing phytopathogenicity.It is intended that our arguments will at once stimulatethe critical testing of the bodyguard hypothesis withpathogens whilst serving to bring food web ecology andevolutionary theory closer together with insect pathology.WHAT IS THE BASIS FOR THE EVOLUTION OFPLANT-ENTOMOPATHOGEN MUTUALISMS?For mutualisms to have evolved between a plant andpathogen of its insect herbivores requires that the plant beable to affect the pathogen so as to counter the loss of plantfitness arising from herbivory. If there is genetic variationin plant traits that can effect the herbivore±entomopatho-gen interaction and there are resulting fitness consequencesto the plant, then there is a basis for natural selection to act,i.e. plants may evolve to use entomopathogens as body-guards. Twin assumptions arising from this are thatherbivory in the absence of natural enemies reduces plantfitness and that pathogens are capable of limiting this lossof fitness. That the former is commonly (although by nomeans universally) the case is clear from the existence ofevolved plant defences to herbivory. The latter is perhapsless clear so we shall now briefly address this.An explanation for the anomaly that the world is greenwhen there are so many extant herbivores has been found inthe control of these herbivores by natural enemies on thethird trophic level (Hairston et al. 1960). This is commonlytaken to mean predators and parasitoids, but of course thereis no reason to exclude pathogens from this explanation.There is an abundance of evidence that natural epizootics ofpathogenic diseases can cause very high mortalities inpopulations of herbivorous insects (see Fuxa & Tanada1987). This has led to a body of work