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Entomology Publications Entomology 2010 Tritrophic Effects of Host Plants on an Herbivore- Pathogen Interaction Aaron J. Gassmann Iowa State University, [email protected] S. Patricia Stock University of Arizona Bruce E. Tabashnik University of Arizona Michael S. Singer Wesleyan University Follow this and additional works at: http://lib.dr.iastate.edu/ent_pubs Part of the Agronomy and Crop Sciences Commons, Entomology Commons, and the Systems Biology Commons The ompc lete bibliographic information for this item can be found at http://lib.dr.iastate.edu/ ent_pubs/181. For information on how to cite this item, please visit http://lib.dr.iastate.edu/ howtocite.html. This Article is brought to you for free and open access by the Entomology at Iowa State University Digital Repository. It has been accepted for inclusion in Entomology Publications by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Tritrophic Effects of Host Plants on an Herbivore-Pathogen Interaction Abstract Tritrophic interactions may include directly harmful effects of host plants on herbivores, and directly or indirectly harmful effects of host plants on the natural enemies of herbivores. Tritrophic interactions involving parasitoids and predators have received considerable attention but less is known about how host plants affect entomopathogens. We compared growth and resistance to entomopathogenic nematodes for “woolly bear” caterpillars, Grammia incorrupta(=geneura) (Hy. Edwards) (Lepidoptera: Arctiidae) fed lettuce, Lactuca sativa L. (Asteraceae), versus threadleaf groundsel, Senecio longilobus Benth. (Asteraceae). Both plants are members of the Asteraceae, but only S. longilobus contains pyrrolizidine alkaloids. Caterpillars gained more mass when fed L. sativa compared with S. longilobus; yet, in one of four cases studied, resistance to nematodes was higher when caterpillars ate S. longilobus.Caterpillar resistance to nematodes did not differ between host plants in the other cases. In addition, nematode reproduction was higher in cadavers of G. incorrupta that had been fed L.sativa instead of S. longilobus, suggesting that S. longilobus had indirectly detrimental effects on entomopathogenic nematodes. Our results illustrate how trade-offs may arise in tritrophic interactions involving entomopathogens, as the cost of decreased growth imposed by S.longilobus was accompanied by the benefit of greater resistance to entomopathogenic nematodes. Keywords alkaloids, entomopathogenic nematodes, pathogen reproduction, polyphagy, tradeoff Disciplines Agronomy and Crop Sciences | Entomology | Systems Biology Comments This article is from Annals of the Entomological Society of America 103 (2010): 371, doi:10.1603/AN09130. Posted with permission. Rights This article is the copyright property of the Entomological Society of America and may not be used for any commercial or other private purpose without specific permission of the Entomological Society of America. This article is available at Iowa State University Digital Repository: http://lib.dr.iastate.edu/ent_pubs/181 Tritrophic Effects of Host Plants on an Herbivore-Pathogen Interaction Author(s): Aaron J. Gassmann, S. Patricia Stock, Bruce E. Tabashnik, and Michael S. Singer Source: Annals of the Entomological Society of America, 103(3):371-378. 2010. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1603/AN09130 URL: http://www.bioone.org/doi/full/10.1603/AN09130 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/ terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. ECOLOGY AND POPULATION BIOLOGY Tritrophic Effects of Host Plants on an Herbivore–Pathogen Interaction AARON J. GASSMANN,1,2 S. PATRICIA STOCK,1 BRUCE E. TABASHNIK,1 3 AND MICHAEL S. SINGER Ann. Entomol. Soc. Am. 103(3): 371Ð378 (2010); DOI: 10.1603/AN09130 ABSTRACT Tritrophic interactions may include directly harmful effects of host plants on herbi- vores, and directly or indirectly harmful effects of host plants on the natural enemies of herbivores. Tritrophic interactions involving parasitoids and predators have received considerable attention but less is known about how host plants affect entomopathogens. We compared growth and resistance to entomopathogenic nematodes for “woolly bear” caterpillars, Grammia incorrupta (ϭgeneura) (Hy. Edwards) (Lepidoptera: Arctiidae) fed lettuce, Lactuca sativa L. (Asteraceae), versus threadleaf groundsel, Senecio longilobus Benth. (Asteraceae). Both plants are members of the Asteraceae, but only S. longilobus contains pyrrolizidine alkaloids. Caterpillars gained more mass when fed L. sativa compared with S. longilobus; yet, in one of four cases studied, resistance to nematodes was higher when caterpillars ate S. longilobus. Caterpillar resistance to nematodes did not differ between host plants in the other cases. In addition, nematode reproduction was higher in cadavers of G. incorrupta that had been fed L. sativa instead of S. longilobus, suggesting that S. longilobus had indirectly detrimental effects on entomopathogenic nematodes. Our results illustrate how trade-offs may arise in tritrophic interactions involving entomopathogens, as the cost of decreased growth imposed by S. longilobus was accompanied by the beneÞt of greater resistance to entomopathogenic nematodes. KEY WORDS alkaloids, entomopathogenic nematodes, pathogen reproduction, polyphagy, trade- off Tritrophic interactions may include direct effects of teraction that has received considerable study in- host plants on herbivores and direct or indirect effects cludes the polyphagous “woolly bear” caterpillar of host plants on the natural enemies of herbivores. Grammia incorrupta (ϭgeneura) (Hy. Edwards) Host plants may reduce the Þtness of herbivores (Lepidoptera: Arctiidae), several of its host plants, and through the presence toxic allelochemicals or physical parasitoids (Hymenoptera and Diptera) (Singer defenses (Rosenthal and Berenbaum 1991). However, 2007). In this system, inclusion of plants with pyrroli- these harmful effects may be offset by beneÞts if the zidine alkaloids (PAs) in the herbivoreÕs diet imposed plant defenses are detrimental to the natural enemies the cost of reduced growth efÞciency but also con- of herbivores and increase survival of herbivores when ferred the beneÞt of higher survival when caterpillars challenged with natural enemies (Price et al. 1980, were challenged with hymenopteran and dipteran Jeffries and Lawton 1984). Greater resistance to nat- parasitoids (Singer et al. 2004b). However, it is un- ural enemies may result from direct effects of plant known whether these tritrophic effects might extend defenses on natural enemies, such as a plantÕs to entomopathogenic organisms, which are an impor- trichomes reducing access of natural enemies to her- tant group of natural enemies (Roy et al. 2009). More- bivores (e.g., Gassmann and Hare 2005) and through over, compared with parasitoids and predators, far less indirect effects if consumption of plant allelochemi- is known about plant-mediated interactions between cals by herbivores increases their resistance to para- herbivorous insects and pathogens, and the extent to sitoids (e.g., Barbosa et al., 1991) or deters predators which greater resistance to entomopathogens may from feeding (e.g., Dyer, 1995). offset detrimental effects of host plant defenses on Several examples exist of such trade-offs arising in herbivores (Cory and Hoover 2006). tritrophic interactions with parasitoids and predators In the current study, we consider interactions (Kennedy 2003, Ode 2006). A natural tritrophic in- among entomopathogenic nematodes, host plants with and without PAs, and G. incorrupta. Because 1 Department of Entomology, University of Arizona, Tucson, AZ entomopathogenic nematodes differ in their biology 85721. from other natural enemies of insects, effects observed 2 Corresponding author: Department of Entomology, Iowa State with entomopathogens could differ considerably from University, Ames, IA 50011 (e-mail: [email protected]). 3 Department of Biology, Wesleyan University, Middletown, CT those observed between herbivores and predators or 06549. parasitoids. Unlike other natural enemies, nematodes 0013-8746/10/0371Ð0378$04.00/0 ᭧ 2010 Entomological Society of America 372 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 103, no. 3 kill their hosts through the action of symbiotic bac- juveniles subsequently dispersing (Kaya and Gaugler teria, which the nematodes harbor (Burnell and Stock 1993). Both nematode species occur in the top 20 cm 2000, Dowds and Peters 2002, Park and Stanley 2006). of soil (Stock and Gress 2006), although their
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