Differential Performance of a Specialist and Two G

Authors: Joanneke H Reudler Arjen Biere Jeff A Harvey Saskya van Nouhuys

Publish Date: 2011/06/21

Volume: 37, Issue: 7, Pages: 765-778

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Abstract

The ability to cope with plant defense chemicals differs between specialist and generalist species In this study we examined the effects of the concentration of the two main iridoid glycosides IGs in Plantago lanceolata aucubin and catalpol on the performance of a specialist and two generalist herbivores and their respective endoparasitoids Development of the specialist herbivore Melitaea cinxia was unaffected by the total leaf IG concentration in its host plant By contrast the generalist herbivores Spodoptera exigua and Chrysodeixis chalcites showed delayed larval and pupal development on plant genotypes with high leaf IG concentrations respectively This result is in line with the idea that specialist herbivores are better adapted to allelochemicals in host plants on which they are specialized Melitaea cinxia experienced less postdiapause larval and pupal mortality on its local Finnish P lanceolata than on Dutch genotypes This could not be explained by differences in IG profiles suggesting that M cinxia has adapted in response to attributes of its local host plants other than to IG chemistry Development of the specialist parasitoid Cotesia melitaearum was unaffected by IG variation in the diet of its host M cinxia a response that was concordant with that of its host By contrast the development time responses of the generalist parasitoids Hyposoter didymator and Cotesia marginiventris differed from those of their generalist hosts S exigua and C chalcites While their hosts developed slowly on highIG genotypes development time of H didymator was unaffected Cotesia marginiventris actually developed faster on hosts fed highIG genotypes although they then had short adult longevity The faster development of C marginiventris on hosts that ate highIG genotypes is in line with the “immunocompromized host” hypothesis emphasizing the potential negative effects of toxic allelochemicals on the host’s immune responsePlants have evolved a wide array of direct defenses against herbivores and diseases Direct defenses include morphological traits Cooper and OwenSmith 1986 and chemical toxins repellents or digestibility reducers Fraenkel 1959 Ehrlich and Raven 1964 These defenses not only affect the performance of herbivores but also can have positive or negative effects on natural enemies of herbivores Positive effects of chemical defense in the herbivore’s diet on natural enemies can arise in several ways For instance allelochemicals may slow down the growth rate of the herbivore extending the time window during which the herbivore is vulnerable to parasitism or predation by its natural enemies Clancy and Price 1987 Toxic allelochemicals also may weaken host immune responses making them more susceptible to parasitation or predation Nappi 1975 Smilanich et al 2009 On the other hand allelochemicals can have negative effects on the growth development or survival of predators and parasitoids Gunasena et al 1990 Paradise and Stamp 1993 Harvey et al 2007b For instance hosts may actively sequester these compounds in their haemolymph where they can again function as defense Bowers 1980 1981 Camara 1997b Nishida 2002The ability of herbivores to cope with plant allelochemicals varies among species that differ in their dietary range Polyphagous species generalists feed on many species in a range of plant families Bowers and Puttick 1988 Agrawal 2000 Even though many herbivores are polyphagous at the species level they are not necessarily so at the population or individual level since species can be comprised of populations or individuals that are specialized on a few or even a single food plant Singer 2008 Some studies support the idea that detoxification systems of generalists are capable of accepting a more structurally diverse array of compounds than those of specialists Li et al 2004 at the expense of a less efficient detoxification of individual compounds Johnson 1999 Oligophagous species specialists often are physiologically adapted to the nutritional and secondary chemistry of particular plant species Renwick et al 2001 Cornell and Hawkins 2003 They may use the allelochemicals to which they have adapted as hostfinding cues and feeding stimulants Rhoades 1979 Bowers 1981 A number of specialist herbivores sequester these substances as defense against their own natural enemies Bowers 1981 which requires physiological or morphological adaptations to prevent autotoxicity Duffey 1980The division between generalists and specialists also can be made for predators and parasitoids of herbivores Allelochemicals present in herbivores or in the diet of an herbivore can reduce the performance of generalist predators and parasitoids eg Duffey et al 1986 Gunasena et al 1990 Generalist parasitoids may attack a wide range of herbivorous host species that feed on plants with different defensive chemistry These parasitoids may suffer during development if their hosts are able to sequester or accumulate plant derived compounds to which they are not adapted Barbosa 1988 Barbosa et al 1991 Harvey et al 2005 In contrast specialized natural enemies such as many endoparasitoid wasps are restricted to attacking only one or a few related host species which generally feed on closely related plants Godfray 1994 Quicke 1997 These parasitoids may be adapted to the limited set of chemicals to which they are exposed Harvey et al 2005 allowing them to use hosts that sequester specific plant chemical defenses Barbosa et al 1986 Sznajder and Harvey 2003 Harvey et al 2007abThe types and concentrations of defensive substances found in plant tissues vary greatly among plant species as well as among individuals of the same species Denno and McClure 1983 Nieminen et al 2003 In this study we used genotypes of ribwort plantain Plantago lanceolata L Plantaginaceae that differ in constitutive concentrations of two iridoid glycosides IGs aucubin and catalpol to study the effects of allelochemical variation on specialist and generalist herbivoreparasitoid associations Iridoid glycosides are monoterpenoids Aucubin is the biosynthetic precursor of catalpol Damtoft et al 1983 The concentrations of IGs in P lanceolata show large natural variation among individuals and within individuals over time Bowers and Stamp 1992 Darrow and Bowers 1997 Barton 2007 Aucubin and to a greater extent catalpol are toxic or deterrent to generalists Puttick and Bowers 1988 Bowers 1991 At the same time these compounds serve as feeding and oviposition stimulants for some specialist herbivores Bowers 1984 Pereyra and Bowers 1988 Nieminen et al 2003 Reudler Talsma et al 2008 Larvae and adults of the specialist butterflies Melitaea cinxia Lepidoptera Nymphalidae and Junonia coenia Lepidoptera Nymphalidae sequester aucubin and catalpol Bowers and Collinge 1992 Suomi et al 2001 2003 Larvae of J coenia do this more efficiently than polyphagous insect herbivores Lampert and Bowers 2010 and they sequester catalpol more efficiently than aucubin Bowers and Collinge 1992 The latter is also observed for larvae of M cinxia and Parasemia plantaginis Lepidoptera Arctiidae Reudler Talsma unpublished Only few studies have assessed the effect of these compounds on preference or performance of parasitoids using dipteran Mallampalli et al 1996 or hymenopteran parasitoids Nieminen et al 2003 Harvey et al 2005 Lampert et al 2010 Our study extends that of Harvey et al 2005 by including two generalist herbivores each with two generalist parasitoids to investigate whether effects of IG are consistent across these generalist systems and compares them with a specialist system Moreover we include a series of plant genotypes that span a wide range of mean IG concentrations in order to gain quantitative insight into associations between plant IGs and insect development parametersWe address the following questions 1 Is the performance of herbivores and their parasitoids affected by the concentrations of the iridoid glycosides aucubin and catalpol in P lanceolata 2 Are there consistent differences in the effect of plant iridoid glycosides on the performance of specialist vs generalist herbivores and parasitoidsPlantago lanceolata is a perennial plant with a worldwide distribution Sagar and Harper 1964 In natural populations IG levels range from undetectable to ca 12 of the plant dry weight Bowers et al 1992 Fajer et al 1992 There generally is no correlation between IG concentrations aucubin or catalpol and tissue nutrient concentrations Marak et al 2000 Reudler Talsma 2007 Plants used for our experiments came from two sources Thirteen genotypes used in all experiments were derived from an artificial selection experiment in which lines were selected for high and low leaf IG concentrations for four generations originating from Dutch P lanceolata Marak et al 2000 These genotypes each originating from a different halfsib family were clonally propagated Wu and Antonovics 1975 in order to generate sufficient leaf material of each genotype For experiments involving the specialist butterfly M cinxia and its specialist endoparasitoid Cotesia melitaearum Hymenoptera Braconidae we augmented this set of genotypes with three additional genotypes from the selection experiment and ten genotypes collected from Åland Finland where the insects originated see below We tested the effects of quantitative variation in allelochemicals in the plants on the development of six different insect species two generalist herbivores two generalist endoparasitoids reared on each of these generalist herbivores and a specialist herbivore and its specialist endoparasitoidThe beet armyworm Spodoptera exigua Lepidoptera Noctuidae is polyphagous and a serious pest of many crops worldwide Females lay several clusters of 50–100 eggs that hatch within 2–3 d The larvae normally have five instars the first three are gregarious and the entire life cycle is about 4–5 weeks with several generations per year Wilson 1934 Tingle and Mitchell 1977 Cultures of S exigua were established from eggs originating from a laboratory culture maintained on artificial diet at the Department of Virology at Wageningen University the Netherlands

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