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Increased nitrogen availability influences predator–prey interactions by altering host-plant quality

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Abstract

Little is known about how plant nutritional and defensive qualities interact to influence predator–prey interactions. To address this need, we provided the neo-tropical milkweed, Asclepias curassavica, with two levels of nitrogen availability and examined how altered host-plant quality influenced the responses of a specialist aphid, Aphis nerii, and a coccinellid predator, Harmonia axyridis. Aphis nerii uses A. curassavica for multiple resources, including nutrition and sequestration of cardenolides for defense against natural enemies. Increased nitrogen availability improved A. curassavica quality by decreasing carbon-to-nitrogen (C:N) ratios and cardenolide concentrations, resulting in A. nerii that also had lower C:N ratios and cardenolide concentrations. Aphis nerii population growth was higher on plants with high nitrogen availability, compared with aphids on plants with low nitrogen availability. In no-choice feeding trials, Harmonia axyridis consumed more high C:N ratio aphids, suggesting a potential compensatory response to reduced aphid nutritional quality. Additionally, H. axyridis were able to consume more low-quality aphids at the expense of increasing exposure to increased cardenolide concentrations, suggesting that interactions between H. axyridis and A. nerii may be strongly influenced by prey nutritional quality. This work highlights the need to consider how variation in plant quality influences herbivore nutritional and defensive quality when examining mechanisms that influence predator–prey interactions.

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References

  • Agrawal AA (2004) Plant defense and density dependence in the population growth of herbivores. Am Nat 164:113–120

    Article  PubMed  Google Scholar 

  • Agrawal AA (2005) Natural selection on a common milkweed (Asclepias syrica) by a community of specialized insect herbivores. Evol Ecol Res 7:651–667

    Google Scholar 

  • Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844

    Google Scholar 

  • Baldwin IT (1989) Mechanism of damaged-induced alkaloid production in wild tobacco. J Chem Ecol 15:1661–1680

    Article  Google Scholar 

  • Botha CEJ, Malcolm SB, Evert RF (1977) An investigation of preferential feeding habit in four Asclepiadaceae by the aphid, Aphis nerii B. de F. Protoplasma 92:1–19

    Article  Google Scholar 

  • Brower LP, Ryerson WN, Coppinger LL, Glazier SC (1968) Ecological chemistry and the palatability spectrum. Science 27:1349–1350

    Article  Google Scholar 

  • Brower LP, McEvoy PB, Williamson KL, Flannery MA (1972) Variation in cardiac glycoside content of monarch butterflies from natural populations in Eastern North America. Science 177:426–429

    Article  PubMed  Google Scholar 

  • Cha DH, Hochwender CG, Bosecker EM, Tucker RE, Kaufman AD, Fritz RS, Smyth RR (2009) Do exotic generalist predators alter host plant preference of a native willow beetle? Agric For Entomol 11:175–184

    Article  Google Scholar 

  • Chen F, Ge F, Parajulee MN (2005) Impact of elevated CO2 on tri-trophic interaction of Gossypium hirsutum, Aphis gossypii, and Leis axyridis. Environ Entomol 34:37–46

    Article  Google Scholar 

  • Chen Y, Olson DM, Ruberson JR (2010) Effects of nitrogen fertilization on tritrophic interactions. Arthropod Plant Interact 4:81–94

    Article  Google Scholar 

  • Cheng L (1970) Timing of attack by Lypha dubia Fall. (Diptera: Tachinidae) on the winter moth, Operophthera brumata (Lepidoptera: Geometridae) as a factor affecting parasite success. J Anim Ecol 39:313–320

    Article  Google Scholar 

  • Coley PD, Bateman ML, Kursar TA (2006) The effects of plant quality on caterpillar growth and defense against natural enemies. Oikos 115:219–228

    Article  Google Scholar 

  • Denno RF, Fagan WF (2003) Might nitrogen limitation promote omnivory among carnivorous arthropods? Ecology 84:2522–2531

    Article  Google Scholar 

  • Fagan WF, Siemann E, Mitter C, Denno RF, Huberty AF, Woods HA, Elser JJ (2002) Nitrogen in insects: implications for trophic complexity and species diversity. Am Nat 160:784–802

    Article  PubMed  Google Scholar 

  • Gratton C, Denno RF (2003) Seasonal shift from bottom-up to top-down impact in phytophagous insect populations. Oecologia 134:487–495

    PubMed  Google Scholar 

  • Harvey JA, Van Dam NM, Gols R (2003) Interactions over four trophic levels: foodplant quality affects development of a hyperparasitoid as mediated through a herbivore and its primary parasitoid. J Anim Ecol 72:520–531

    Article  Google Scholar 

  • Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2 and O3. Oecologia 137:233–244

    Article  PubMed  Google Scholar 

  • Hugentobler UJ, Renwick AA (1995) Effects of plant nutrition on the balance on insect relevant cardenolides and glucosinolates in Erysimum cheiranthoides. Oecologia 102:95–101

    Google Scholar 

  • Hunter MD (2003) Effects of plant quality on the population ecology of parasitoids. Agric For Entomol 5:1–8

    Article  Google Scholar 

  • Hunter MD, Price PW (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732

    Google Scholar 

  • Kagata H, Ohgushi T (2007) Carbon-nitrogen stoichiometry in the tritrophic food chain willow, leaf beetle, and predatory ladybird beetle. Ecol Res 22:671–677

    Article  Google Scholar 

  • Kagata H, Nakamura M, Ohgushi T (2005) Bottom-up cascade in a tri-trophic system: different impacts of host-plant regeneration on performance of a willow leaf beetle and its natural enemy. Ecol Entomol 30:58–62

    Article  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. University of Chicago Press, Chicago

    Google Scholar 

  • Karowe DN, Schoonhoven LM (1992) Interactions among three trophic levels: the influence of host plant on performance of Pieris brassicae and its parasitoid, Cotesia glomerata. Entomol Exp Appl 61:241–251

    Article  Google Scholar 

  • Kytö M, Niemela P, Larrson S (1996) Insects on trees: population and individual responses to fertilization. Oikos 75:148–159

    Article  Google Scholar 

  • Lavoie B, Oberhauser KS (2004) Compensatory feeding in Danaus plexippus (Lepidoptera: Nymphalidae) in response to variation in host plant quality. Environ Entomol 33:1062–1069

    Article  Google Scholar 

  • Malcolm SB (1981) Defensive use of plant-derived cardenolides by Aphis nerii Boyer de Fonscolombe against predation. Dissertation, University of Oxford, Oxford

  • Malcolm SB (1986) Aposematism in a soft-bodied insect: a case for kin selection. Behav Ecol Sociobiol 18:387–393

    Article  Google Scholar 

  • Malcolm SB (1989) Disruption of web structure and predatory behavior of a spider by plant-derived chemical defenses of an aposematic aphid. J Chem Ecol 15:1699–1716

    Article  Google Scholar 

  • Malcolm SB (1990) Chemical defense in chewing and sucking herbivores: plant derived cardenolides in the monarch butterfly and the oleander aphid. Chemoecology 1:12–21

    Article  Google Scholar 

  • Malcolm SB (1991) Cardenolide-mediated interactions between plants and herbivores. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, 2nd edn, Volume I: The Chemical Participants. Academic Press, San Diego, pp 251–296

  • Malcolm SB (1992) Prey defense and predator foraging. In: Crawley MJ (ed) Natural enemies. The population biology of predators, parasites, and disease. Blackwell, Oxford, pp 458–475

    Google Scholar 

  • Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–161

    Article  Google Scholar 

  • Mayntz D, Toft S (2001) Nitrogen composition of the prey’s diet affects growth and survivorship of a generalist predator. Oecologia 127:213

    Article  Google Scholar 

  • Mooney KA, Halitschke R, Kessler A, Agrawal AA (2010) Evolutionary trade-offs in plants mediate the strength of trophic cascades. Science 327:1642–1644

    Article  PubMed  Google Scholar 

  • Müller MS, McWilliams SR, Podlesak D, Donaldson JR, Bothwell HM, Lindroth RL (2006) Tri-trophic effects of plant defenses: chickadees consume caterpillars based on host leaf chemistry. Oecologia 114:507–517

    Google Scholar 

  • Nelson CJ (1993) Sequestration and storage of cardenolides and cardenolide glycosides by Danaus plexippus and D. chrysippus petila when reared on Asclepias fruticosa: with a review of some factors that influence sequestration. In: Malcolm SB, Zalucki, MP (eds) Biology and conservation of the monarch butterfly. Natural History Museum of Los Angeles County, Los Angeles, California, USA, pp 83–90

  • Pasteels JM (1978) Apterous and brachypterous coccinellids at the end of the food chain, Cionura erecta (Asclepiadaceae) Aphis nerii. Entomol Exp Appl 24:579–584

    Article  Google Scholar 

  • Pasteels JM, Rowell-Rahier M, Braekman JC, Dupont A (1983) Salicin from host plant as precursor of salicylaldehyde in defensive secretions of Chrysomeline larvae. Physiol Entomol 8:307–314

    Article  Google Scholar 

  • Pasteels JM, Braekman J-C, Daloze D (1988) Chemical defense in the Chrysomelidae. In: Jolivet P, Petitpierre E, Hsiao TH (eds) Biology of the Chrysomelidae. Kluwer, Dordrecht, pp 233–252

  • Price PW, Bouton CE, Gross P, McPheron BA, Thompson JN, Weis AE (1980) Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annu Rev Ecol Syst 11:41–65

    Article  Google Scholar 

  • Rank NE (1994) Host-plant effects on larval survival of a salicin-using leaf beetle Chrysomela aeneicollis Schaeffer (Coleoptera: Chrysomelidae). Oecologia 97:342–353

    Google Scholar 

  • Rasmann S, Agrawal AA, Erwin AC, Cook SC (2009) Cardenolides, induced responses, and interactions between above and belowground herbivores in the milkweeds (Asclepias spp.). Ecology 90:2393–2404

    Article  PubMed  Google Scholar 

  • Rosenthal GA, Berenbaum MR (1991) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York

    Google Scholar 

  • Rothschild M, von Ewu J, Reichstein T (1970) Cardiac glycosides in the oleander aphid Aphis nerii. J Insect Physiol 16:1191–1195

    Article  Google Scholar 

  • Snyder WE, Joesph SB, Preziosi RF, Moore AJ (2000) Nutritional benefits of cannibalism for the lady beetle Harmonia axyridis (Coleoptera: Coccinellidae) when prey quality is poor. Environ Entomol 29:1173–1179

    Article  Google Scholar 

  • Teder T, Tammaru T (2002) Cascading effects of variation in plant vigour on the relative performance of insect herbivores and their parasitoids. Ecol Entomol 27:94–104

    Article  Google Scholar 

  • Throop HL (2005) Nitrogen deposition and herbivory affect biomass production and allocation in an annual plant. Oikos 111:91–100

    Article  Google Scholar 

  • Throop HL, Lerdau MT (2004) Effects of nitrogen deposition on insect herbivory: implications for community and ecosystem processes. Ecosystems 7:109–133

    Article  Google Scholar 

  • Zalucki MP, Brower LP (1992) Survival of first instar larvae Danaus plexippus (Lepidoptera: Danainae) in relation to cardiac glycoside and latex content of Asclepias humistrata (Asclepiadaceae). Chemoecology 3:81–93

    Article  Google Scholar 

  • Zalucki MP, Malcolm SB (1999) Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. J Chem Ecol 8:1827–1842

    Article  Google Scholar 

  • Zalucki MP, Malcolm SB, Paine TD, Hanlon CC, Brower LP, Clarke AR (2001) It’s the first bite that counts: survival of first-instar monarchs on milkweeds. Austral Ecol 26:1–9

    Article  Google Scholar 

  • Zhender C, Hunter M (2008) Effects of nitrogen deposition on the interaction between an aphid and its host plant. Ecol Entomol 33:24–30

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to S. B. Malcolm for supplying A. curassavica, A. nerii, and TNDP for cardenolide analysis. We would also like to thank L. M. Holeski, K. Keefover-Ring, K. F. Rubert, M. L. Hillstrom, C. H. Habeck, and C. Buhl for comments on the manuscript. This work was supported by U.S. Department of Energy (Office of Science, BER) grant DE-FG02-06ER64232.

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Correspondence to John J. Couture.

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Couture, J.J., Servi, J.S. & Lindroth, R.L. Increased nitrogen availability influences predator–prey interactions by altering host-plant quality. Chemoecology 20, 277–284 (2010). https://doi.org/10.1007/s00049-010-0058-y

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