Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses

Abstract

Animals have several strategies to contend with nutritionally poor diets, including compensatory consumption and enhanced food utilization efficiencies. Plants produce a diversity of defense compounds that affect the ability of herbivores to utilize these strategies in response to variation in food nutritional quality. Little is known, however, about effects of allelochemicals on herbivores utilizing integrated behavioral and morphological responses to reduced food quality. Our objectives were to (1) examine how variation in diet nutritional quality influences compensatory responses of a generalist insect herbivore, and (2) determine how plant defenses affect these processes. Gypsy moth (Lymantria dispar) larvae were administered one of nine combinations of diet having low, moderate, or high nutritional quality and 0, 2, or 4 % purified aspen (Populus tremuloides) salicinoids. We quantified larval growth, consumption, frass production, and biomass allocation to midgut tissue over a 4-day bioassay. In the absence of salicinoids, larvae compensated for reduced nutritional quality and maintained similar growth across all diets through increased consumption, altered midgut biomass allocation, and improved processing efficiencies. Dietary salicinoids reduced larval consumption, midgut biomass allocation, digestive efficiencies, and growth at all nutritional levels, but the effect size was more pronounced when larvae were fed nutritionally suboptimal diets. Our findings demonstrate that integrated behavioral and morphological compensatory responses to reduced food quality are affected by plant defenses, ultimately limiting compensatory responses and reducing larval performance.

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References

  1. Armstrong JB, Schindler DE (2011) Excess digestive capacity in predators reflects a life of feast and famine. Nature 476:84–87

    CAS  Article  PubMed  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  3. Barbehenn RV, Jaros A, Lee G, Mozola C, Weir Q, Salminen J (2009) Hydrolyzable tannins as “quantitative defenses”: limited impact against Lymantria dispar caterpillars on hybrid poplar. J Insect Phys 55:297–304

    CAS  Article  Google Scholar 

  4. Batzli GO, Broussard A, Oliver R (1994) The integrated processing response in herbivorous small mammals. In: Chivers DJ, Langer P (eds) The digestive system in mammals: food, form, and function. Cambridge University Press, Cambridge, pp 324–336

  5. Behmer S (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:167–187

    Article  Google Scholar 

  6. Behmer ST, Simpson SJ, Raubenheimer D (2002) Herbivore foraging in chemically heterogeneous environments: nutrients and secondary metabolites. Ecology 83:2489–2501

    Article  Google Scholar 

  7. Bingaman BR, Hart ER (1993) Clonal and leaf age variation in Populus phenolic glycosides: implications for host selection by Chrysomela scripta (Coleoptera: Chrysomelidae). Environ Entomol 22:397–403

    CAS  Article  Google Scholar 

  8. Boeckler GA, Gershenzon J, Unsicker SB (2011) Phenolic glycosides of the Salicaceae and their role as anti-herbivore defenses. Phytochemistry 72:1497–1509

    CAS  Article  PubMed  Google Scholar 

  9. Clissold FJ, Tedder BJ, Conigrave AD, Simpson SJ (2010) The gastrointestinal tract as a nutrient-balancing organ. Proc R Soc London B Biol Sci 277:1751–1759

  10. Couture JJ, Meehan TD, Lindroth RL (2012) Atmospheric changes alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168:863–876

    Article  PubMed  Google Scholar 

  11. Denno RF, McClure MS (1983) Variability: a key to understanding plant–herbivore interactions. In: Denno RF (ed) Variable plants and herbivores in natural and managed systems. Academic Press, Inc, Cambridge, pp 1–12

  12. Donaldson JR, Lindroth RL (2007) Genetics, environment, and their interaction determine efficacy of chemical defense in trembling aspen. Ecology 88:729–739

    Article  PubMed  Google Scholar 

  13. Donaldson JR, Stevens MT, Barnhill HR, Lindroth RL (2006) Age-related shifts in leaf chemistry of clonal aspen (Populus tremuloides). J Chem Ecol 32:1415–1429

    CAS  Article  PubMed  Google Scholar 

  14. Hemming JDC, Lindroth RL (2000) Effects of phenolic glycosides and protein on gypsy moth (Lepidoptera: Lymantriidae) and forest tent caterpillar (Lepidoptera: Lasiocampidae) performance and detoxication activities. Environ Entomol 29:1108–1115

    CAS  Article  Google Scholar 

  15. 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 

  16. Johnson MTJ (2011) Evolutionary ecology of plant defences against herbivores. Funct Ecol 25:305–311

    Article  Google Scholar 

  17. Karasov WH, del Rio CM, Caviedes-Vidal E (2011) Ecological physiology of diet and digestive systems. Annu Rev Physiol 73:69–93

    CAS  Article  PubMed  Google Scholar 

  18. Knepp RG, Hamilton JG, Zangerl AR, Berenbaum MR, DeLucia EH (2007) Foliage of oaks grown under elevated CO2 reduces performance of Antheraea polyphemus (Lepidoptera: Saturniidae). Environ Entomol 36:609–617

    Article  PubMed  Google Scholar 

  19. Kruse JJ, Raffa KF (1999) Effect of food plant switching by a herbivore on its parasitoid: Cotesia melanoscela development in Lymantria dispar exposed to reciprocal dietary crosses. Ecol Entomol 24:37–45

    Article  Google Scholar 

  20. Le Gall M, Behmer ST (2014) Effects of protein and carbohydrate on an insect herbivore: the vista from a fitness landscape. Integr Comp Biol 54:942–954

    Article  PubMed  Google Scholar 

  21. Lindroth RL, Hemming JDC (1990) Responses of the gypsy moth (Lepidoptera: Lymantriidae) to tremulacin, an aspen phenolic glycoside. Environ Entomol 19:842–847

    CAS  Article  Google Scholar 

  22. Lindroth RL, Hwang S-Y (1996) Diversity, redundancy, and multiplicity in chemical defense systems of aspen. In: Romeo J, Saunders J, Barbosa P (eds) Recent advances in phytochemistry: phytochemical diversity and redundancy in ecological interactions. Plenum Press, New York, pp 26–51

    Google Scholar 

  23. Lindroth RL, Peterson SS (1988) Effects of plant phenols on performance of southern armyworm larvae. Oecologia 75:185–189

    Article  Google Scholar 

  24. Lindroth RL, St. Clair SB (2013) Adaptations of quaking aspen (Populus tremuloides Michx.) for defense against herbivores. For Ecol Manage 299:14–21

    Article  Google Scholar 

  25. Lindroth RL, Scriber JM, Hsai MTS (1986) Differential responses of tiger swallowtail subspecies to secondary metabolites from tulip tree and quaking aspen. Oecologia 70:13–19

    Article  Google Scholar 

  26. Lindroth RL, Scriber JM, Hsai MTS (1988) Chemical ecology of the tiger swallowtail: mediation of host use by phenolic glycosides. Ecology 69:814–822

    CAS  Article  Google Scholar 

  27. Linton SM, Greenaway P (2007) A review of feeding and nutrition of herbivorous land crabs: adaptations to low quality plant diets. J Comp Physiol B 177:269–286

    Article  PubMed  Google Scholar 

  28. Machado RAR, Arce CCM, Ferrieri AP, Baldwin IT, Erb M (2015) Jasmonate-dependent depletion of soluble sugars compromises plant resistance to Manduca sexta. New Phytol 207:91–105

    CAS  Article  PubMed  Google Scholar 

  29. Mason CJ, Couture JJ, Raffa KF (2014) Plant-associated bacteria degrade defense chemicals and reduce their adverse effects on an insect defoliator. Oecologia 175:901–910

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  31. Mcwilliams SR, Karasov WH (2001) Phenotypic flexibility in digestive system structure and function in migratory birds and its ecological significance. J Comp Physiol A 128:579–593

    CAS  Google Scholar 

  32. Meyer GA, Montgomery ME (1987) Relationships between leaf age and the food quality of cottonwood foliage for the gypsy moth, Lymantria dispar. Oecologia 72:527–532

    Article  Google Scholar 

  33. Mole S, Waterman PG (1987) Tannins as antifeedants to mammalian herbivores—still an open question? In: Waller GR (ed) Allelochemicals: role in agriculture and forestry. ACS symposium series 330. American Chemical Society, Washington, pp 572–587

    Google Scholar 

  34. Orlando P, Browen J, Whelan C (2009) Co-adaptations of feeding behaviors and gut modulation as a mechanism of co-existence. Evol Ecol Res 11:541–560

    Google Scholar 

  35. Perkins MC, Woods HA, Harrison JF, Elser JJ (2004) Dietary phosphorus affects the growth of larval Manduca sexta. Arch Insect Biochem Physiol 55:153–168

    CAS  Article  PubMed  Google Scholar 

  36. Raubenheimer D, Bassil K (2007) Separate effects of macronutrient concentration and balance on plastic gut responses in locusts. J Comp Physiol B 177:849–855

    CAS  Article  PubMed  Google Scholar 

  37. Raubenheimer D, Simpson S (1993) A multi-level analysis of feeding behaviour: the geometry of nutritional decisions. Philos Trans R Soc Lond B Biol Sci 342:381–402

    Article  Google Scholar 

  38. Riolo MA, Rohani P, Hunter MD (2015) Local variation in plant quality influences large-scale population dynamics. Oikos 124:1160–1170

    Article  Google Scholar 

  39. Shikano I, Oak MC, Halpter-Scanderbeg O, Cory JS (2015) Tradeoffs between transgenerational transfer of nutritional stress tolerance and immune priming. Funct Ecol 29:1156–1164

    Article  Google Scholar 

  40. Simpson S, Raubenheimer D (2001) The geometric analysis of nutrient–allelochemical interactions: a case study using locusts. Ecology 82:422–439

    Google Scholar 

  41. Simpson SJ, Sibly RM, Lee KP, Behmer ST, Raubenheimer D (2004) Optimal foraging when regulating intake of multiple nutrients. Anim Behav 68:1299–1311

    Article  Google Scholar 

  42. Slansky F, Scriber JM (1985) Food consumption and utilization. Compr Insect Physiol Biochem Pharmacol 4:87–163

    Google Scholar 

  43. Slansky F, Wheeler G (1991) Food consumption and utilization responses to dietary dilution with cellulose and water by velvetbean caterpillars, Anticarsia gemmatalis. Physiol Entomol 16:99–116

    Article  Google Scholar 

  44. Steppuhn A, Baldwin IT (2007) Resistance management in a native plant: nicotine prevents herbivores from compensating for protease inhibitors. Ecol Lett 10:499–511

    Article  PubMed  Google Scholar 

  45. Stockhoff BA (1992) Diet-switching by gypsy moth: effects of diet nitrogen history switching on growth, consumption, and food utilization. Entomol Exp Appl 64:225–238

    Article  Google Scholar 

  46. Stockhoff BA (1993) Diet heterogeneity: implications for growth of a generalist herbivore, the gypsy moth. Ecology 74:1939–1949

    Article  Google Scholar 

  47. Stoyenoff AJL, Witter JA, Montgomery ME, Chilcote CA (1994) Effects of host switching on gypsy moth (Lymantria dispar (L.)) under field conditions. Oecologia 97:143–157

    Article  Google Scholar 

  48. Sullam KE, Dalton CM, Russell JA, Kilham SS, El-Sabaawi R, German DP, Flecker AS (2015) Changes in digestive traits and body nutritional composition accommodate a trophic niche shift in Trinidadian guppies. Oecologia 177:245–257

    Article  PubMed  Google Scholar 

  49. Thaler JS, Contreras H, Davidowitz G (2014) Effects of predation risk and plant resistance on Manduca sexta caterpillar feeding behaviour and physiology. Ecol Entomol 39:210–216

    Article  Google Scholar 

  50. Winterer J, Bergelson J (2001) Diamondback moth compensatory consumption of proteinase inhibitor-transformed plants. Mol Ecol 10:1069–1074

    CAS  Article  PubMed  Google Scholar 

  51. Woods H (1999) Patterns and mechanisms of growth of fifth-instar Manduca sexta caterpillars following exposure to low- or high-protein food during early instars. Physiol Biochem Zool 4:445–454

    Article  Google Scholar 

  52. Yang Y, Joern A (1994) Gut size changes in relation to variable food quality an body size in grasshoppers. Funct Ecol 8:36–45

    Article  Google Scholar 

  53. Young Owl M, Batzli GO (1998) The integrated processing response of voles to fibre content of natural diets. Funct Ecol 12:4–13

    Article  Google Scholar 

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Acknowledgments

We are grateful to Kennedy Rubert-Nason for chemical analysis of salicinoid extracts. Early iterations of this manuscript were improved by critical assessments by Ikkei Shikano, Marion Le Gall, and several anonymous reviewers. This work was supported by National Science Foundation grant DEB-0841609 to RLL, US Environmental Protection Agency Science to Achieve Results Fellowship Program to CWH, and USDA NIFA AFRI Fellowship Grant 2012-67012-19900 to JJC.

Author contributions

RLL secured funding for the experiment; JJC and CWH conceptualized and designed the experiment, with input from RLL; JJC and CWH collected foliar material and performed salicinoid extractions; JJC constructed the dietary treatments, performed the bioassays, and collected and analyzed the data; JJC and CJM wrote the manuscript, with input from RLL and CWH.

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Correspondence to J. J. Couture.

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J. J. Couture and C. J. Mason have contributed equally to the writing of this manuscript.

Handling Editor: Gimme Walter.

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Couture, J.J., Mason, C.J., Habeck, C.W. et al. Behavioral and morphological responses of an insect herbivore to low nutrient quality are inhibited by plant chemical defenses. Arthropod-Plant Interactions 10, 341–349 (2016). https://doi.org/10.1007/s11829-016-9439-7

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Keywords

  • Compensatory feeding
  • Gypsy moth
  • Integrated response
  • Nutritional ecology
  • Populus
  • Salicinoid