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

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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.

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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

References

  • 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 9:93–96

    Article  CAS  Google Scholar 

  • 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 71:164–170

    PubMed  CAS  Google Scholar 

  • 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 232:258–262

    PubMed  CAS  Google Scholar 

  • 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 8:1–16

    Article  Google Scholar 

  • Ben-Zvi Z, Kaplanski J (1980) Effects of chronic heat exposure on drug metabolism in the rat. J Pharm Pharmacol 32:368–369

    PubMed  CAS  Google Scholar 

  • Bryant JP, Kuropat PJ (1980) Selection of Winter Forage by Subarctic Browsing Vertebrates: The Role of Plant Chemistry. Annu Rev Ecol Syst 11:261–285

    Article  CAS  Google Scholar 

  • Crawford HS (1982) Seasonal food selection and digestibility by tame white-tailed deer in Central Maine. J Wildl Manag 46:974–982

    Article  Google Scholar 

  • Cross DL, Redmond LM, Strickland JR (1995) Equine fescue toxicosis: signs and solutions. J Anim Sci 73:899–908

    PubMed  CAS  Google Scholar 

  • 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 53:229–235

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Dearing MD, Schall JJ (1992) Testing models of optimal diet assembly by the generalist herbivorous lizard, Cnemidophorus murinus. Ecology 73:845–858

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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 36:169–189

    Article  Google Scholar 

  • Dearing MD, Skopec MM, Bastiani MJ (2006) Detoxification rates of wild herbivorous woodrats (Neotoma). Comp Biochem Physiol A Mol Integr Physiol 145:419–422

    Article  PubMed  CAS  Google Scholar 

  • 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 81:891–897

    Article  PubMed  CAS  Google Scholar 

  • Desjardins JP, Iversen PL (1995) Inhibition of the rat cytochrome P450 3A2 by an antisense phosphorothioate oligodeoxynucleotide in vivo. J Pharmacol Exp Ther 275:1608–1613

    PubMed  CAS  Google Scholar 

  • Dial KP (1988) Three sympatric species of Neotoma: dietary specialization and coexisitence. Oecologia 76:531–537

    Google Scholar 

  • Dominguez-Bello MG, Michelangeli F, Ruiz MC, Garcia A, Rodriguez E (1994) Ecology of the folivorous hoatzin (Opisthocomus Hoazin) on the Venezuelan plains. Auk 11:643–651

    Google Scholar 

  • 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 13:53–64

    CAS  Google Scholar 

  • Feldhamer GA, Drickamer LE, Vessey SH, Merritt JF, Krajewski C (2007) Mammalogy: adaptation, diversity, and ecology. Johns Hopkins Press, Baltimore

    Google Scholar 

  • Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL (1995) Tissue-specific HSP70 response in animals undergoing heat stress. Am J Physiol 268:R28–R32

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Gordon CJ (1993) Temperature regulation in laboratory rodents. Press Syndicate of the Unviersity of Cambridge, Cambridge

    Book  Google Scholar 

  • Gordon CJ, Fogelson L, Mohler F, Stead AG, Rezvani AH (1988a) Behavioral thermoregulation in the rat following the oral administration of ethanol. Alcohol Alcohol 23:383–390

    PubMed  CAS  Google Scholar 

  • Gordon CJ, Mohler FS, Watkinson WP, Rezvani AH (1988b) Temperature regulation in laboratory mammals following acute toxic insult. Toxicology 53:161–178

    Article  PubMed  CAS  Google Scholar 

  • Hales JR, Rowell LB, King RB (1979) Regional distribution of blood flow in awake heat-stressed baboons. Am J Physiol 237:H705–H712

    PubMed  CAS  Google Scholar 

  • 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 33:2111–2122

    Article  PubMed  CAS  Google Scholar 

  • 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 146:552–560

    Article  PubMed  Google Scholar 

  • Heinrich B (1993) The Hot-blooded Insects: Strategies and Mechanisms of Thermoregulation. Harvard University Press, Cambridge

    Google Scholar 

  • 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, Geneva

  • 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 15:1899–1917

    Article  CAS  Google Scholar 

  • Jori A, Bianchetti A, Prestini PE (1970) Relations between barbiturate brain levels and sleeping time in various experimental conditions. Biochem Pharmacol 19:2687–2694

    Article  PubMed  CAS  Google Scholar 

  • Kaplanski J, Ben-Zvi Z (1980) Effect of chronic heat exposure on in vitro drug metabolism in the rat. Life Sci 26:639–642

    Article  PubMed  CAS  Google Scholar 

  • Karasov WH, Martinez del Rio C (2007) Physiological ecology: how animals process energy nutrients toxins. Princeton University Press, Princeton

    Google Scholar 

  • Kawamichi T (1997) Seasonal changes in the diet of Japanese Giant Flying Squirrels in relation to reproduction. J Mamm 78:204–212

    Article  Google Scholar 

  • 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 1:156–161

    Article  CAS  Google Scholar 

  • 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 28:217–223

    Article  PubMed  CAS  Google Scholar 

  • Klaassen CD (2001) Cararett and Doull’s toxicology: the basic science of poisons. Mcgraw Hil, New York

    Google Scholar 

  • Lewis DF, Lake BG (1997) Molecular modelling of mammalian CYP2B isoforms and their interaction with substrates, inhibitors and redox partners. Xenobiotica 27:443–478

    Article  PubMed  CAS  Google Scholar 

  • Macedo RH, Mares MA (1988) Neotoma albigula. Mamm Species 310:1–7

    Article  Google Scholar 

  • 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 18:2401–2414

    Article  PubMed  CAS  Google Scholar 

  • 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 32:1247–1266

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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 322:261–264

    Article  PubMed  CAS  Google Scholar 

  • Nixon CM, Worley DM, McClain MW (1968) Food habits of squirrels in Southeast Ohio. J Wildl Manag 32:294–305

    Article  Google Scholar 

  • 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 42:228–232

    Article  Google Scholar 

  • 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 70:2501–2509

    PubMed  CAS  Google Scholar 

  • 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 466:482–485

    Article  PubMed  CAS  Google Scholar 

  • Pachecka J, Kobylinska K, Miaskiewicz H, Bicz W (1983) Hepatic microsomal mixed-function oxidases in rats exposed to high ambient temperature. Acta Physiol Pol 34:563–568

    PubMed  CAS  Google Scholar 

  • 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 42:899–908

    Article  PubMed  CAS  Google Scholar 

  • Raubenheimer D, Simpson SJ (2009) Nutritional PharmEcology: doses, nutrients, toxins, and medicines. Integr Comp Biol 49:329–337

    Article  PubMed  CAS  Google Scholar 

  • Robbins CT (1983) Wildlife Feeding and Nutrition. Academic Press, New York

    Google Scholar 

  • Rosenthal GA, Berenbaum MR (1991) Herbivores: their interactions with secondary plant metabolites: the chemical participants, vol 1, II edn. Academic Press, Inc., San Diego

    Google Scholar 

  • Rowe RJ, Terry RC, Rickart EA (2011) Environmental change and declining resource availability for small mammal communities in the Great Basin. Ecology 92:1366–1375

    Article  PubMed  Google Scholar 

  • Sasaki N (1994) Effects of furazolidone on duration of righting reflex loss induced with hexobarbital and zoxazolamine in the rat. J Vet Med Sci 56:667–670

    Article  PubMed  CAS  Google Scholar 

  • Schimdt-Nielsen K (1997) Animal physiology adaptation and environment. Cambridge University Press, Cambridge

    Google Scholar 

  • 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 33:213–222

    Article  CAS  Google Scholar 

  • 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 227:347–356

    Article  PubMed  CAS  Google Scholar 

  • 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 87:3142–3155

    Article  PubMed  CAS  Google Scholar 

  • 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

  • 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 2:34–43

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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 83:1423–1434

    PubMed  CAS  Google Scholar 

  • Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

    Google Scholar 

  • 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–G620

    Google Scholar 

  • Waxman DJ, Azaroff L (1992) Phenobarbital induction of cytochrome P-450 gene expression. Biochem J 281(Pt 3):577–592

    PubMed  CAS  Google Scholar 

  • Welty JC, Baptista LF (1988) Life of Birds. Saunders College Publishing, New York

    Google Scholar 

  • Westoby M (1980) Black-tailed jack rabbit diets in Curlew Valley, Northern Utah. J Wildl Manag 44:942–948

    Article  Google Scholar 

  • 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 17:2293–2295

    PubMed  CAS  Google Scholar 

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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).

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Correspondence to M. Denise Dearing.

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Communicated by I.D. Hume.

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Dearing, M.D. Temperature-dependent toxicity in mammals with implications for herbivores: a review. J Comp Physiol B 183, 43–50 (2013). https://doi.org/10.1007/s00360-012-0670-y

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