Journal of Comparative Physiology B

, Volume 183, Issue 1, pp 43–50 | Cite as

Temperature-dependent toxicity in mammals with implications for herbivores: a review

Review

Abstract

Diet selection in mammalian herbivores is thought to be primarily governed by intrinsic properties of food, such as nutrient and plant secondary compound (PSC) contents, and less so by environmental factors. However, several independent lines of evidence suggest that the toxicity of PSCs is mediated, in part, by ambient temperature and that the effect of small changes in ambient temperature is on par with several fold changes in PSC concentration. This review describes the disparate lines of evidence for temperature-dependent toxicity and the putative mechanisms causing this phenomenon. A model is described that integrates thermal physiology with temperature-dependent toxicity to predict maximal dietary intake of plant secondary compounds by mammalian herbivores. The role of temperature-dependent toxicity is considered with respect to the observed changes in herbivorous species attributed to climate change. Possible future investigations and the effects of temperature-dependent toxicity on other endotherms are presented. Temperature-dependent toxicity has the potential to apply to all endotherms that consume toxins. The effects of temperature-dependent toxicity will likely be exacerbated with increasing ambient temperatures caused by climate change.

Keywords

Mammalian herbivore Temperature-dependent toxicity Plant secondary compounds Xenobiotics 

Abbreviations

CYP2B

Cytochrome p450 2B

LCT

Lower critical temperature

PSC

Plant secondary compound

TDT

Temperature-dependent toxicity

TNZ

Thermal neutral zone

UCT

Upper critical temperature

Notes

Acknowledgments

Thanks to Patrice Kurnath for suggestions on the manuscript and Kathy Smith for assistance with the references. Three anonymous reviewers provided suggestions that improved the quality of the manuscript. Funding was provided by the National Science Foundation (IOS 0817527).

References

  1. Adams RP, Zanoni TA, Von Rudloff E, Hogge L (1981) The southwestern USA and northern Mexico one-seeded junipers: their volatile oils and evolution. Biochem Syst Ecol 9:93–96CrossRefGoogle Scholar
  2. Aldrich CG, Paterson JA, Tate JL, Kerley MS (1993) The effects of endophyte-infected tall fescue consumption on diet utilization and thermal regulation in cattle. J Anim Sci 71:164–170PubMedGoogle Scholar
  3. Atal CK, Dubey RK, Singh J (1985) Biochemical basis of enhanced drug bioavailability by piperine evidence that piperine is a potent inhibitor of drug metabolism. J Pharmacol Exp Ther 232:258–262PubMedGoogle Scholar
  4. Bale JS, Masters GJ, Hodkinson ID, Awmack C, Be-zemer TM, Brown VK, Butterfield J et al (2002) Herbivory in global climate change research: direct effects of rising temperature on insect herbivores. Global Change Biol 8:1–16CrossRefGoogle Scholar
  5. Ben-Zvi Z, Kaplanski J (1980) Effects of chronic heat exposure on drug metabolism in the rat. J Pharm Pharmacol 32:368–369PubMedGoogle Scholar
  6. Bryant JP, Kuropat PJ (1980) Selection of Winter Forage by Subarctic Browsing Vertebrates: The Role of Plant Chemistry. Annu Rev Ecol Syst 11:261–285CrossRefGoogle Scholar
  7. Crawford HS (1982) Seasonal food selection and digestibility by tame white-tailed deer in Central Maine. J Wildl Manag 46:974–982CrossRefGoogle Scholar
  8. Cross DL, Redmond LM, Strickland JR (1995) Equine fescue toxicosis: signs and solutions. J Anim Sci 73:899–908PubMedGoogle Scholar
  9. De Vries J, Strubbe JH, Wildering WC, Gorter JA, Prins AJA (1993) Patterns of body temperature during feeding in rats under varying temperatures. Physiol Behav 53:229–235PubMedCrossRefGoogle Scholar
  10. Dearing MD (1996) Disparate determinants of summer and winter diet selection of a generalist herbivore, Ochotona princeps. Oecologia 108:467–478CrossRefGoogle Scholar
  11. Dearing MD, Schall JJ (1992) Testing models of optimal diet assembly by the generalist herbivorous lizard, Cnemidophorus murinus. Ecology 73:845–858CrossRefGoogle Scholar
  12. Dearing MD, Mangione AM, Karasov WH (2000) Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123:397–405CrossRefGoogle Scholar
  13. Dearing MD, Foley WJ, McLean S (2005) The influence of plant secondary metabolites on the nutritional ecology of herbivorous terrestrial vertebrates. Annu Rev Ecol Evol Syst 36:169–189CrossRefGoogle Scholar
  14. Dearing MD, Skopec MM, Bastiani MJ (2006) Detoxification rates of wild herbivorous woodrats (Neotoma). Comp Biochem Physiol A Mol Integr Physiol 145:419–422PubMedCrossRefGoogle Scholar
  15. Dearing MD, Forbey JS, McLister JD, Santos L (2008) Ambient temperature influences diet selection and physiology of an herbivorous mammal, Neotoma albigula. Physiol Biochem Zool 81:891–897PubMedCrossRefGoogle Scholar
  16. Desjardins JP, Iversen PL (1995) Inhibition of the rat cytochrome P450 3A2 by an antisense phosphorothioate oligodeoxynucleotide in vivo. J Pharmacol Exp Ther 275:1608–1613PubMedGoogle Scholar
  17. Dial KP (1988) Three sympatric species of Neotoma: dietary specialization and coexisitence. Oecologia 76:531–537Google Scholar
  18. Dominguez-Bello MG, Michelangeli F, Ruiz MC, Garcia A, Rodriguez E (1994) Ecology of the folivorous hoatzin (Opisthocomus Hoazin) on the Venezuelan plains. Auk 11:643–651Google Scholar
  19. El-Merhibi A, Ngo SNT, Jones BR, Milic NL, Stupans I, McKinnon RA (2007) Molecular insights into xenobiotic disposition in Australian marsupials. Aust J Ecotoxicol 13:53–64Google Scholar
  20. Feldhamer GA, Drickamer LE, Vessey SH, Merritt JF, Krajewski C (2007) Mammalogy: adaptation, diversity, and ecology. Johns Hopkins Press, BaltimoreGoogle Scholar
  21. Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL (1995) Tissue-specific HSP70 response in animals undergoing heat stress. Am J Physiol 268:R28–R32PubMedGoogle Scholar
  22. Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals the role of plant secondary compounds. Am Nat 108:269–289CrossRefGoogle Scholar
  23. Gordon CJ (1993) Temperature regulation in laboratory rodents. Press Syndicate of the Unviersity of Cambridge, CambridgeCrossRefGoogle Scholar
  24. Gordon CJ, Fogelson L, Mohler F, Stead AG, Rezvani AH (1988a) Behavioral thermoregulation in the rat following the oral administration of ethanol. Alcohol Alcohol 23:383–390PubMedGoogle Scholar
  25. Gordon CJ, Mohler FS, Watkinson WP, Rezvani AH (1988b) Temperature regulation in laboratory mammals following acute toxic insult. Toxicology 53:161–178PubMedCrossRefGoogle Scholar
  26. Hales JR, Rowell LB, King RB (1979) Regional distribution of blood flow in awake heat-stressed baboons. Am J Physiol 237:H705–H712PubMedGoogle Scholar
  27. Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing MD (2007a) Xenobiotic metabolism of plant secondary compounds in oak (Quercus agrifolia) by specialist and generalist woodrat herbivores, genus Neotoma. J Chem Ecol 33:2111–2122PubMedCrossRefGoogle Scholar
  28. Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing MD (2007b) Xenobiotic metabolism of plant secondary compounds in juniper (Juniperus monosperma) by specialist and generalist woodrat herbivores, genus Neotoma. Comp Biochem Physiol C Toxicol Pharmacol 146:552–560PubMedCrossRefGoogle Scholar
  29. Heinrich B (1993) The Hot-blooded Insects: Strategies and Mechanisms of Thermoregulation. Harvard University Press, CambridgeGoogle Scholar
  30. IPCC (2007) Climate Change 2007: Synthesis Report. Contribution of Working Groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, GenevaGoogle Scholar
  31. Jakubas WJ, Guillion GW, Clausen TP (1989) Ruffed grouse feeding behavior and its relationship to secondary metabolites of quaking aspen flower buds. J Chem Ecol 15:1899–1917CrossRefGoogle Scholar
  32. Jori A, Bianchetti A, Prestini PE (1970) Relations between barbiturate brain levels and sleeping time in various experimental conditions. Biochem Pharmacol 19:2687–2694PubMedCrossRefGoogle Scholar
  33. Kaplanski J, Ben-Zvi Z (1980) Effect of chronic heat exposure on in vitro drug metabolism in the rat. Life Sci 26:639–642PubMedCrossRefGoogle Scholar
  34. Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy nutrients toxins. Princeton University Press, PrincetonGoogle Scholar
  35. Kawamichi T (1997) Seasonal changes in the diet of Japanese Giant Flying Squirrels in relation to reproduction. J Mamm 78:204–212CrossRefGoogle Scholar
  36. Keplinger ML, Lanier GE, Deich WB (1959) Effects of environmental temperature on the acute toxicity of a number of compounds in rats. Toxicol Appl Pharmacol 1:156–161CrossRefGoogle Scholar
  37. Kim EJ, Shin WH (2005) General pharmacology of CKD-732, a new anticancer agent: effects on central nervous, cardiovascular, and respiratory system. Biol Pharm Bull 28:217–223PubMedCrossRefGoogle Scholar
  38. Klaassen CD (2001) Cararett and Doull’s toxicology: the basic science of poisons. Mcgraw Hil, New YorkGoogle Scholar
  39. Lewis DF, Lake BG (1997) Molecular modelling of mammalian CYP2B isoforms and their interaction with substrates, inhibitors and redox partners. Xenobiotica 27:443–478PubMedCrossRefGoogle Scholar
  40. Macedo RH, Mares MA (1988) Neotoma albigula. Mamm Species 310:1–7CrossRefGoogle Scholar
  41. Magnanou E, Malenke JR, Dearing MD (2009) Expression of biotransformation genes in woodrat (Neotoma) herbivores on novel and ancestral diets: identification of candidate genes responsible for dietary shifts. Mol Ecol 18:2401–2414PubMedCrossRefGoogle Scholar
  42. Marsh K, Wallis I, Andrew R, Foley W (2006) The detoxification limitation hypothesis: where did it come from and where is it going? J Chem Ecol 32:1247–1266PubMedCrossRefGoogle Scholar
  43. 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 77:305–312PubMedCrossRefGoogle Scholar
  44. Moritz C, Patton JL, Conroy CJ, Parra JL, White GC, Beissinger SR (2008) Impact of a century of climate change on small-mammal communities in Yosemite National Park, USA. Science 322:261–264PubMedCrossRefGoogle Scholar
  45. Nixon CM, Worley DM, McClain MW (1968) Food habits of squirrels in Southeast Ohio. J Wildl Manag 32:294–305CrossRefGoogle Scholar
  46. Nunez-Hernandez G, Holechek JL, Wallace JD, Galyean ML, Tembo A, Valdez R, Carenas M (1989) Influence of native shrubs on nutritional status of goats: nitrogen retention. J Range Manag 42:228–232CrossRefGoogle Scholar
  47. Osborn TG, Schmidt SP, Marple DN, Rahe CH, Steenstra JR (1992) Effect of consuming fungus-infected and fungus-free tall fescue and ergotamine tartrate on selected physiological variables of cattle in environmentally controlled conditions. J Anim Sci 70:2501–2509PubMedGoogle Scholar
  48. Ozgul A, Childs DZ, Oli MK, Armitage KB, Blumstein DT, Olson LE, Tuljapurkar S, Coulson T (2010) Coupled dynamics of body mass and population growth in response to environmental change. Nature 466:482–485PubMedCrossRefGoogle Scholar
  49. Pachecka J, Kobylinska K, Miaskiewicz H, Bicz W (1983) Hepatic microsomal mixed-function oxidases in rats exposed to high ambient temperature. Acta Physiol Pol 34:563–568PubMedGoogle Scholar
  50. Price RJ, Scott MP, Walters DG, Stierum RH, Groten JP, Meredith C, Lake BG (2004) Effect of thiabendazole on some rat hepatic xenobiotic metabolising enzymes. Food Chem Toxicol 42:899–908PubMedCrossRefGoogle Scholar
  51. Raubenheimer D, Simpson SJ (2009) Nutritional PharmEcology: doses, nutrients, toxins, and medicines. Integr Comp Biol 49:329–337PubMedCrossRefGoogle Scholar
  52. Robbins CT (1983) Wildlife Feeding and Nutrition. Academic Press, New YorkGoogle Scholar
  53. Rosenthal GA, Berenbaum MR (1991) Herbivores: their interactions with secondary plant metabolites: the chemical participants, vol 1, II edn. Academic Press, Inc., San DiegoGoogle Scholar
  54. Rowe RJ, Terry RC, Rickart EA (2011) Environmental change and declining resource availability for small mammal communities in the Great Basin. Ecology 92:1366–1375PubMedCrossRefGoogle Scholar
  55. Sasaki N (1994) Effects of furazolidone on duration of righting reflex loss induced with hexobarbital and zoxazolamine in the rat. J Vet Med Sci 56:667–670PubMedCrossRefGoogle Scholar
  56. Schimdt-Nielsen K (1997) Animal physiology adaptation and environment. Cambridge University Press, CambridgeGoogle Scholar
  57. Settivari RS, Evans TJ, Eichen PA, Rottinghaus GE, Spiers DE (2008a) Short- and long-term responses to fescue toxicosis at different ambient temperatures. J Therm Biol 33:213–222CrossRefGoogle Scholar
  58. Settivari RS, Evans TJ, Rucker E, Rottinghaus GE, Spiers DE (2008b) Effect of ergot alkaloids associated with fescue toxicosis on hepatic cytochrome P450 and antioxidant proteins. Toxicol Appl Pharmacol 227:347–356PubMedCrossRefGoogle Scholar
  59. Settivari RS, Evans TJ, Yarru LP, Eichen PA, Sutovsky P, Rottinghaus GE, Antoniou E, Spiers DE (2009) Effects of short-term heat stress on endophytic ergot alkaloid-induced alterations in rat hepatic gene expression. J Anim Sci 87:3142–3155PubMedCrossRefGoogle Scholar
  60. Sheldon KS, Yang S, Tewksbury JJ (2011) Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. doi: 10.1111/j.1461-0248.2011.01689.x
  61. 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 Part D Genomics Proteomics 2:34–43PubMedCrossRefGoogle Scholar
  62. Sorensen JS, McLister JD, Dearing MD (2005) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139CrossRefGoogle Scholar
  63. Spiers DE, Eichen PA, Rottinghaus GE (2005) A model of fescue toxicosis: responses of rats to intake of endophyte-infected tall fescue. J Anim Sci 83:1423–1434PubMedGoogle Scholar
  64. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, PrincetonGoogle Scholar
  65. Toloza EM, Lam M, Diamond J (1991) Nutrient extraction by cold-exposed mice: a test of digestive safety margins. Am J Physiol (Gastrointest Liver Physiol) 24:G608–G620Google Scholar
  66. Waxman DJ, Azaroff L (1992) Phenobarbital induction of cytochrome P-450 gene expression. Biochem J 281(Pt 3):577–592PubMedGoogle Scholar
  67. Welty JC, Baptista LF (1988) Life of Birds. Saunders College Publishing, New YorkGoogle Scholar
  68. Westoby M (1980) Black-tailed jack rabbit diets in Curlew Valley, Northern Utah. J Wildl Manag 44:942–948CrossRefGoogle Scholar
  69. Zhang HJ, Xu L, Drake VJ, Xie L, Oberley LW, Kregel KC (2003) Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. FASEB J 17:2293–2295PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of UtahSalt Lake CityUSA

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