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Jasmonate-induced plant defenses and prey availability impact the preference and performance of an omnivorous stink bug, Podisus maculiventris

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Abstract

Many omnivorous insects are important biological control agents, and their success is influenced by both plant resistance and prey availability. The potential impact of these two factors is complicated by the fact that they may not be independent: Resistant plants also often support fewer herbivorous prey. We studied how lifetime development, growth, fecundity and preference of the omnivorous stink bug, Podisus maculiventris, was affected by jasmonate-induced plant defenses and amount of prey available. P. maculiventris survival was 70 % lower on high-resistance (jasmonate-overexpressing) plants compared to low-resistance (jasmonate-insensitive) plants. However, surviving P. maculiventris grew and achieved equal fecundity on low- and high-resistance plants. When given a choice, P. maculiventris preferred low-resistance plants, but did not differentiate between caterpillar prey reared on high- or low-resistance plants. Low prey availability impacted distinct aspects of P. maculiventris performance: Development time was lengthened, and nymphal and adult mass were reduced, but survival was not impacted. We did not detect any interactive effects between plant resistance and prey availability for any measure of P. maculiventris. Thus, we found remarkably compartmentalized impacts of plant resistance and prey availability for this omnivorous insect.

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References

  • Agrawal AA, Klein CN (2000) What omnivores eat: direct effects of induced plant resistance on herbivores and indirect consequences for diet selection by omnivores. J Anim Ecol 69:525–535

    Article  Google Scholar 

  • Agrawal AA, Kobayashi C, Thaler JS (1999) Influence of prey availability and induced host-plant resistance on omnivory by western flower thrips. Ecology 80:518–523

    Article  Google Scholar 

  • Agren GI, Stenberg JA, Bjorkman C (2012) Omnivores as plant bodyguards—a model of the importance of plant quality. Basic Appl Ecol 13:441–448

    Article  Google Scholar 

  • Alvarez-Alfageme F, Martinez M, Pascual-Ruiz S, Castanera P, Diaz I, Ortego F (2007) Effects of potato plants expressing a barley cystatin on the predatory bug Podisus maculiventris via herbivorous prey feeding on the plant. Transgenic Res 16:1–13

    Article  CAS  PubMed  Google Scholar 

  • Armer CA, Wiedenmann RN, Bush DR (1998) Plant feeding site selection on soybean by the facultatively phytophagous predator Orius insidiosus. Entomol Exp Appl 86:109–118

    Article  Google Scholar 

  • Barbosa P, Gross P, Kemper J (1991) Influence of plant allelochemicals on the tobacco hornworm and its parasitoid, Cotesia congregata. Ecology 72:1567–1575

    Article  CAS  Google Scholar 

  • Bartlett R (2008) Negative interactions between chemical resistance and predators affect fitness in soybeans. Ecol Entomol 33:673–678

    Article  Google Scholar 

  • Bouchard E, Michaud D, Cloutier C (2003) Molecular interactions between an insect predator and its herbivore prey on transgenic potato expressing a cysteine proteinase inhibitor from rice. Mol Ecol 12:2429–2437

    Article  CAS  PubMed  Google Scholar 

  • Coll M, Guershon M (2002) Omnivory in terrestrial arthropods: mixing plant and prey diets. Annu Rev Entomol 47:267–297

    Article  CAS  PubMed  Google Scholar 

  • Coll M, Ridgway RL (1995) Functional and numerical responses of Orius insidiosus (Heteroptera, Anthocoridae) to its prey in different vegetable crops. Ann Entomol Soc Am 88:732–738

    Article  Google Scholar 

  • Cox D, Oakes D (1984) Analysis of survival data. Chapman and Hall, London

    Google Scholar 

  • Creelman RA, Mullet JE (1997) Biosynthesis and action of jasmonates in plants. Annu Rev Plant Physiol Plant Mol Biol 48:355–381

    Article  CAS  PubMed  Google Scholar 

  • Eubanks M, Denno RF (1999) The ecological consequences of variation in plants and prey for an omnivorous insect. Ecology 80:1253–1266

    Article  Google Scholar 

  • Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408

    Article  CAS  PubMed  Google Scholar 

  • Holtz AM, de Almeida GD, Fadini MAM, Zanuncio JS Jr, Zanuncio TV, Zanuncio JC (2009) Survival and reproduction of Podisus nigrispinus (Heteroptera: Pentatomidae): effects of prey scarcity and plant feeding. Chil J Agric Res 69:468–472

  • Howe GA, Ryan CA (1999) Suppressors of systemin signaling identify genes in the tomato wound response pathway. Genetics 153:1411–1421

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kaplan I, Thaler JS (2010) Plant resistance attenuates the consumptive and non-consumptive impacts of predators on prey. Oikos 119:1105–1113

    Article  Google Scholar 

  • Kaplan I, Thaler JS (2011) Do plant defenses enhance or diminish prey suppression by omnivorous Heteroptera? Biol Control 59:53–60

    Article  Google Scholar 

  • Kessler A, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Quaghebeur H, Felton GW (2011) Reiterative and interruptive signaling in induced plant resistance to chewing insects. Phytochemistry 72:1624–1634

    Article  CAS  PubMed  Google Scholar 

  • Lambert AM (2007) Effects of prey availability, facultative plant feeding, and plant defenses on a generalist insect predator. Arthropod Plant Interact 1:167–173

    Article  Google Scholar 

  • Legaspi JC, Oneil RJ (1993) Life-history of Podisus maculiventris given low numbers of Epilachna varivestis as prey. Environ Entomol 22:1192–1200

    Article  Google Scholar 

  • Legaspi JC, Oneil RJ (1994a) Developmental response of nymphs of Podisus maculiventris (Heteroptera, Pentatomidae) reared with low numbers of prey. Environ Entomol 23:374–380

    Article  Google Scholar 

  • Legaspi JC, Oneil RJ (1994b) Lipid and egg production of Podisus maculiventris (Heteroptera, Pentatomidae) under low rates of predation. Environ Entomol 23:1254–1259

    Article  Google Scholar 

  • Legaspi JC, Oneil RJ, Legaspi BC (1996) Trade-offs in body weights, egg loads, and fat reserves of field-collected Podisus maculiventris (Heteroptera: Pentatomidae). Environ Entomol 25:155–164

    Article  Google Scholar 

  • Li CY, Williams MM, Loh YT, Lee GI, Howe GA (2002) Resistance of cultivated tomato to cell content-feeding herbivores is regulated by the octadecanoid-signaling pathway. Plant Physiol 130:494–503

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Li L, Zhao YF, McCaig BC, Wingerd BA, Wang JH, Whalon ME, Pichersky E, Howe GA (2004) The tomato homolog of coronatine-insensitive 1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16:126–143

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McGurl B, Orozcocardenas M, Pearce G, Ryan CA (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase-inhibitor synthesis. Proc Natl Acad Sci USA 91:9799–9802

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Paschold A, Halitschke R, Baldwin IT (2007) Co(i)-ordinating defenses: naCOI1 mediates herbivore-induced resistance in Nicotiana attenuata and reveals the role of herbivore movement in avoiding defenses. Plant J 51:79–91

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez-Saona CR, Musser RO, Vogel H, Hum-Musser SM, Thaler JS (2010) Molecular, biochemical, and organismal analyses of tomato plants simultaneously attacked by herbivores from two feeding guilds. J Chem Ecol 36:1043–1057

    Article  CAS  PubMed  Google Scholar 

  • Scott IM, Thaler JS, Scott JG (2010) Response of a generalist herbivore Trichoplusia ni to jasmonate-mediated induced defense in tomato. J Chem Ecol 36:490–499

    Article  CAS  PubMed  Google Scholar 

  • Self LS, Hodgson E, Guthrie FE (1964) Metabolism of nicotine by tobacco-feeding insects. Nature 204:300–301

    Article  CAS  PubMed  Google Scholar 

  • Strohmeyer HH, Stamp NE, Jarzomski CM, Bowers MD (1998) Prey species and prey diet affect growth of invertebrate predators. Ecol Entomol 23:68–79

    Article  Google Scholar 

  • Thaler JS, Karban R, Ullman DE, Boege K, Bostock RM (2002) Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131:227–235

    Article  Google Scholar 

  • Tian DL, Tooker J, Peiffer M, Chung SH, Felton GW (2012) Role of trichomes in defense against herbivores: comparison of herbivore response to woolly and hairless trichome mutants in tomato (Solanum lycopersicum). Planta 236:1053–1066

    Article  CAS  PubMed  Google Scholar 

  • Venzon M, Janssen A, Sabelis MW (1999) Attraction of a generalist predator towards herbivore-infested plants. Entomol Exp Appl 93:305–314

    Article  Google Scholar 

  • Vieira CR, Blassioli Moraes MC, Borges M, Sujii ER, Laumann RA (2013) cis-Jasmone indirect action on egg parasitoids (Hymenoptera: Scelionidae) and its application in biological control of soybean stink bugs (Hemiptera: Pentatomidae). Biol Control 64:75–82

    Article  CAS  Google Scholar 

  • Walling LL (2000) The myriad plant responses to herbivores. J Plant Growth Regul 19:195–216

    CAS  PubMed  Google Scholar 

  • Weiser LA, Stamp NE (1998) Combined effects of allelochemicals, prey availability, and supplemental plant material on growth of a generalist insect predator. Entomol Exp Appl 87:181–189

    Article  CAS  Google Scholar 

  • Wink M, Theile V (2002) Alkaloid tolerance in Manduca sexta and phylogenetically related sphingids (Lepidoptera:Sphingidae). Chemoecology 12:29–46

    Article  CAS  Google Scholar 

  • Zhi JR, Margolies DC, Nechols JR, Boyer JE (2006) Host-plant-mediated interaction between populations of a true omnivore and its herbivorous prey. Entomol Exp Appl 121:59–66

    Article  Google Scholar 

Download references

Acknowledgments

We thank Jessica McArt and Natasha Tigreros for help with survival analysis and Ordom Huot for caring for experiments over breaks. This project was supported by the National Research Initiative of the USDA Grant 2006-35302-17431 (JST), the Hunter R. Rawlings III Cornell Presidential Research Scholars program (EO) and Federal Capacity Funds 139-7484 (JST).

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Authors and Affiliations

  1. Department of Entomology, Cornell University, 4138 Comstock Hall, Ithaca, NY, 14853, USA

    Jennifer S. Thaler & Elena L. Olsen

  2. Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, 14853, USA

    Jennifer S. Thaler

  3. Department of Biology, University of Fribourg, 1700, Fribourg, Switzerland

    Elena L. Olsen

  4. Department of Entomology, Purdue University, West Lafayette, IN, 47907, USA

    Ian Kaplan

Authors
  1. Jennifer S. Thaler
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  2. Elena L. Olsen
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  3. Ian Kaplan
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Correspondence to Jennifer S. Thaler.

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Handling Editor: Gary Felton.

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Thaler, J.S., Olsen, E.L. & Kaplan, I. Jasmonate-induced plant defenses and prey availability impact the preference and performance of an omnivorous stink bug, Podisus maculiventris . Arthropod-Plant Interactions 9, 141–148 (2015). https://doi.org/10.1007/s11829-015-9357-0

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  • DOI: https://doi.org/10.1007/s11829-015-9357-0

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