Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore

  • 673 Accesses

  • 17 Citations


Specialist herbivores are predicted to have evolved biotransformation pathways that can process large doses of secondary compounds from the plant species on which they specialize. It is hypothesized that this physiological specialization results in a trade-off such that specialists may be limited in ability to ingest novel plant secondary compounds (PSCs). In contrast, the generalist foraging strategy requires that herbivores alternate consumption of plant species and PSC types to reduce the possibility of over-ingestion of any particular PSC. The ability to behaviorally regulate is a key component of this strategy. These ideas underpin the prediction that in the face of novel PSCs, generalists should be better able to maintain body mass and avoid toxic consequences compared to specialists. We explored these predictions by comparing the feeding behavior of two herbivorous rodents: a juniper specialist, Neotoma stephensi, and a generalist, Neotoma albigula, fed diets with increasing concentrations of phenolic resin extracted from the creosote bush (Larrea tridentata), which produces a suite of PSCs novel to both species. The specialist lost more mass than the generalist during the 15-day trial. In addition, although the specialist and generalist both regulated phenolic resin intake by reducing meal size while on the highest resin concentration (4%), the generalist began to regulate intake on the 2% diet. The ability of the generalist to regulate intake at a lower PSC concentration may be the source of the generalist’s performance advantage over the specialist. These data provide evidence for the hypothesis that the specialist’s foraging strategy may result in behavioral as well as physiological trade-offs in the ability to consume novel PSCs.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2


  1. Adams RP, Zanoni TA, Von Rudloff E, Hogge L (1981) The south-western USA and northern Mexico one-seeded junipers: their volatile oils and evolution. Biochem Syst Ecol 9:93–96

  2. Adams RP, Von Rudloff E, Hogge L (1983) Chemosystematic studies of the Western North American junipers based on their volatile oils. Biochem Syst Ecol 11:189–193

  3. Alvares AP, Pratt WB (1990) Pathways of drug metabolism. In: Pratt WB, Taylor P (eds) Principles of drug action. The basis of pharmacology. Churchill Livingstone, New York

  4. Arteaga S, Andrade-Cetto A, Cardenas R (2005) Larrea tridentata (Creosote bush), an abundant plant of Mexican and US-American deserts and its metabolite nordihydroguaiaretic acid. J Ethnopharmacol 98:231–239

  5. Bernays EA, Cooper Driver G, Bilgener M (1989) Herbivores and plant tannins. Adv Ecol Res 19:262–302

  6. Boyle RR, McLean S (2004) Constraint of feeding by chronic ingestion of 1, 8-cineole in the brushtail possum (Trichosurus vulpecula). J Chem Ecol 30:757–775

  7. Boyle RR, McLean S, Brandon S, Wiggins N (2005) Rapid absorption of dietary 1, 8-cineole results in critical blood concentration of cineole and immediate cessation of eating in the common brushtail possum (Trichosurus vulpecula). J Chem Ecol 31:2775–2790

  8. Dearing MD (1996) Disparate determinants of summer and winter diet choice in a generalist herbivore (Ochotona princeps). Oecologia 108:467–478

  9. Dearing MD, Cork S (1999) The role of detoxification of plant secondary compounds on diet breadth in mammalian herbivores. J Chem Ecol 25:1205–1220

  10. Dearing MD, Mangione AM, Karasov WH, Morzunov S, Otteson E, St. Jeor S (1998) Prevalence of hantavirus in 4 species of Neotoma from Arizona and Utah. J Mammal 79:1254–1259

  11. Dearing MD, Mangione AM, Karasov WH (2000) Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123:397–405

  12. Dial KP (1988) Three sympatric species of Neotoma: dietary specialization and co-existence. Oecologia 76:531–537

  13. Dial KP, Czaplewski CJ (1990) Do packrat middens accurately represent the animals’ environmental diet? The Woodhouse Mesa study. In: Bentacourt JL, Ven Devender TR, Martin PS (eds) Fossil packrat middens: the last 40,000 years of biotic change in the arid west. University of Arizona Press, Arizona, pp 43–58

  14. Dziba LE, Provenza FD (2008) Dietary monoterpene concentrations influence feeding patterns of lambs. Appl Anim Behav Sci 109:49–57

  15. Foley JW, Iason GR, McArthur C (1999) Role of plant secondary metabolites in the nutritional ecology of mammalian herbivores: how far have we come in 25 years? In: Jung HG, Fahey GC (eds) Nutritional ecology of herbivores. American Society of Animal Science, Illinois, pp 130–209

  16. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289

  17. Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing DM (2007a) Xenobiotic metabolism of plant secondary compounds in juniper (Juniperus monosperma) by specialist and generalist woodrat herbivores, genus Neotoma. Comp Biochem Physiol C Toxicol Pharmacol 146:552–560

  18. Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing MD (2007b) Xenobiotic metabolism of plant secondary compounds in oak (Quercus agrifolia) by specialist and generalist woodrat herbivores, genus Neotoma. J Chem Ecol 33:2111–2122

  19. Kim SG, Kim EJ, KimYG LeeMG (2001) Expression of cytochrome p-450 s and glutathione s-transferase in the rat liver during water deprivation: effects of glucose supplementation. J Appl Toxicol 21:123–129

  20. Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998) Intraspecific variation in eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160–169

  21. Mabry TJ, Gill E (1979) Sesquiterpene lactones and other terpenoids. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic, New York, pp 501–537

  22. Mangione AM, Dearing MD, Karasov WH (2000) Interpopulation differences in tolerance to creosote bush resin in desert woodrats (Neotoma lepida). Ecology 81:2067–2076

  23. Mangione AM, Dearing MD, Karasov WH (2004) Creosote bush (Larrea tridentata) resin increases water demands and reduces energy availability in desert woodrats (Neotoma lepida). J Chem Ecol 30:1409–1429

  24. Marsh KJ, Wallis IR, Andrew RL, Foley WJ (2006) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32:1247–1266

  25. McLister JD, Sorensen JS, Dearing MD (2004) Effects of consumption of juniper (Juniperus monosperma) on cost of thermoregulation in the woodrats Neotoma albigula and Neotoma stephensi at different acclimation temperatures. Physiol Biochem Zool 77:305–312

  26. Ngo SN, McKinnon RA, Stupans I (2003) The effects of Eucalyptus terpenes on hepatic cytochrome P450 CYP4A, peroxisomal Acyl CoA oxidase (AOX) and peroxisome proliferator activated receptor alpha (PPARalpha) in the common brush tail possum (Trichosurus vulpecula). Comp Biochem Physiol C Toxicol Pharmacol 136:165–173

  27. Ngo SN, McKinnon RA, Stupans I (2006) Cloning and expression of koala (Phascolarctos cinereus) liver cytochrome P450 CYP4A15. Gene 376:123–132

  28. Randolph JC, Cameron GN (2001) Consequences of diet choice by a small generalist herbivore. Ecol Monogr 71:117–136

  29. Savolainen H, Pfaffli P (1978) Effects of long term turpentine inhalation on rat brain protein metabolism. Chem Biol Interact 21:271–276

  30. Shipley LA, Davilla TB, Thines NJ, Elias BA (2006) Nutritional requirements and diet choices of the pygmy rabbit (Brachylagus idahoensis): a sage brush specialist. J Chem Ecol 32:2455–2474

  31. Shitara Y, Horie T, Sugiyama Y (2006) Transporters as determinants of drug clearance and tissue distribution. Eur J Pharm Sci 27:425–466

  32. Skopec MM, Haley S, Dearing MD (2007) Differential hepatic gene expression of a dietary specialist (Neotoma stephensi) and generalist (Neotoma albigula) in response to juniper (Juniperus monosperma) ingestion. Comp Biochem Physiol D Genom Proteom 2:34–43

  33. Sorensen JS, McLister JD, Dearing MD (2005a) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139

  34. Sorensen JS, McLister JD, Dearing MD (2005b) Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology 86:140–154

  35. Spearling F, Marcus WL, Collins C (1967) Acute effects of turpentine vapor on rats and mice. Toxicol Appl Pharmacol 10:8–20

  36. Torregrossa A-M, Dearing MD (2009) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Func Ecol 23:48–56

  37. Torregrossa A-M, Azzara AV, Dearing MD (2011) Differential regulation of plant secondary compounds by herbivorous rodents (genus Neotoma). Funct Ecol (in press)

  38. Wiggins NL, McArthur C, McLean S, Boyle R (2003) Effects of two plant secondary metabolites, cineole and gallic acid, on nightly feeding patterns of the common brushtail possum. J Chem Ecol 29:1447–1464

  39. Wiggins NL, Marsh KJ, Wallis IR, Foley WJ, McArthur C (2006a) Sideroxylonal in Eucalyptus foliage influences foraging behaviour of an arboreal folivore. Oecologia 147:272–279

  40. Wiggins NL, McArthur C, Davies NW, McLean S (2006b) Behavioral responses of a generalist mammalian folivore to the physiological constraints of a chemically defended diet. J Chem Ecol 32:1133–1147

Download references


We would like to thank Dr. J. Lokvam and many undergraduate assistants for their help with the resin extraction procedures: R. Bares, A. Bares, A. Fitzgerald, M. Yeo, and A. Briles. Drs. P.D. Coley, F. Goller, W. Potts and anonymous reviewers provided helpful comments on the manuscript. We would also like to thank Dr. J. Malenke for assistance with creosote collection and Dr. N. Geary for the use of his equipment. Finally, we would like to thank Dr. G.P. Smith for his thoughtful comments on these ideas. This work was supported by NSF IOS-0817527 and IBN-0326402 to MDD and a grant from the American Museum of Natural History to A-M.T.

Author information

Correspondence to A-M. Torregrossa.

Additional information

Communicated by Jörg Ganzhorn.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Torregrossa, A., Azzara, A.V. & Dearing, M.D. Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore. Oecologia 168, 711–718 (2012). https://doi.org/10.1007/s00442-011-2121-y

Download citation


  • Neotoma
  • Meal size
  • Plant–animal interactions
  • Biotransformation
  • Dietary toxin