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Using the Specialization Framework to Determine Degree of Dietary Specialization in a Herbivorous Woodrat

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Abstract

To be considered a dietary specialist, mammalian herbivores must consume large quantities of a plant species considered “difficult” with respect to nutrient or toxin content, and possess specialized adaptations to deal with plant defensive compounds or low nutritional content. Populations of Neotoma lepida in the Great Basin consume Juniperus osteosperma, a plant heavily defended by terpenes, but a detailed dietary analysis of this population is lacking. Therefore, we investigated the extent of dietary specialization in this species in comparison with the better-studied specialist species, N. stephensi. Microhistological analysis of feces from N. lepida revealed that greater than 90 % of their diet in nature was comprised of juniper. In laboratory tolerance trials, N. lepida tolerated a diet of 80 % J. osteosperma, similar to that observed for N. stephensi. There was no difference in the abilities of N. lepida and N. stephensi to metabolize hexobarbital, a proxy compound for terpene metabolism. In preference tests of native and non-native juniper species, N. lepida did not exhibit a preference for its native or co-occurring juniper, J. osteosperma, over the non-native species, J. monosperma, whereas N. stephensi preferred its native or co-occurring juniper J. monosperma over non-native J. osteosperma. Behavioral and habitat differences between these woodrat species lead to the categorization of N. stephensi as an obligate juniper specialist with a small range that overlaps that of its preferred food, J. monosperma, and N. lepida as a facultative juniper specialist with a large range, and only a portion of its distribution containing populations that feed extensively on J. osteosperma.

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References

  • Adams RP (1994) Geographic variation in the volatile terpenoids of Juniperus monosperma and J. osteosperma. Biochem Syst Ecol 22:65–71

    Article  CAS  Google Scholar 

  • Adams RP, Skopec MM, Kohl KD, Dearing MD (2014) Comparison of volatile leaf terpenoids from Juniperus monosperma and J. osteosperma leaves: intact, ground and exposed to ambient temperature. Phytologia 96:207–217

    CAS  Google Scholar 

  • Anderson JR, Scott CB, Taylor CA, Owens CJ, Jackson JR, Steele DK, Brantley R (2013) Using experience and supplementation to increase juniper consumption by three different breeds of sheep. Rangel Ecol Manag 66:204–208

    Article  Google Scholar 

  • Bentacourt JL, Van Devender TR, Martin PS (1990) Packrat middens: the last 40,000 years of biotic change. University of Arizona Press, Tuscon

    Google Scholar 

  • Brown JH, Lieberman GA, Dengler WF (1972) Woodrats and cholla : dependence of a small mammal population on the density of cacti. Ecology 53:310–313

    Article  Google Scholar 

  • Cameron GN, Rainey DG (1972) Habitat utilization by Neotoma lepida in the Mohave desert. J Mammal 53:251–266

    Article  Google Scholar 

  • Dearing MD (2013) Temperature-dependent toxicity in mammals with implications for herbivores: a review. J Comp Physiol B Biochem Syst Environ Physiol 183:43–50

    Article  CAS  Google Scholar 

  • Dearing M, Cork S (1999) Role of detoxification of plant secondary compounds on diet breadth in a mammalian herbivore, Trichosurus vulpecula. J Chem Ecol 25:1205–1219

    Article  CAS  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, Mangione AM, Karasov WH (2001) Plant secondary compounds as diuretics: an overlooked consequence. Am Zool 41:890–901

    CAS  Google Scholar 

  • Dearing MD, Mangione AM, Karasov WH (2002) Ingestion of plant secondary compounds causes diuresis in desert herbivores. Oecologia 130:576–584

    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  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Estell RE, Utsumi SA, Cibils AF, Anderson DM (2014) Is differential use of Juniperus monosperma by small ruminants driven by terpenoid concentration? J Chem Ecol 40:285–293

    Article  CAS  PubMed  Google Scholar 

  • Falk AA, Hagberg MT, Lot AE, Wigaeus-Hjelm EM, Zhiping W (1990) Uptake, distribution and elimination of α-pinene in man after exposure by inhalation. Scand J Work Environ Health 16:372–378

    Article  CAS  PubMed  Google Scholar 

  • Flinders JT, Hansen RM (1972) Diets and habitats of jackrabbis in northeastern Colorado. Range Sci Dep Sci Ser 12:1–18

    Google Scholar 

  • Forister ML, Novotny V, Panorska A et al (2015)  The global distribution of diet breadth in insect herbivores. Proc Nat Acad Sci USA 112:442–447

  • Fox LR, Morrow, PA (1981) Specialization: speceis property or local phenomenon? Science 211:887–893.

  • 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 

  • Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3:408–414

    Article  CAS  PubMed  Google Scholar 

  • Hayes JP (1996) Arborimus longicaudis. Mamm Species 532:1–5

    Article  Google Scholar 

  • Karasov WH (1989) Nutritional bottleneck in a herbivore, the desert wood rat (Neotoma lepida). Physiol Zool 62:1351–1382

    Google Scholar 

  • Kohl KD, Miller AW, Marvin JE, Mackie F, Dearing MD (2014a) Herbivorous rodents (Neotoma spp.) harbour abundant and active foregut microbiota. Environ Microbiol 16:2869–2878

    Article  CAS  PubMed  Google Scholar 

  • Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD (2014b) Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17:1238–1246

    Article  PubMed  Google Scholar 

  • Kurnath P, Dearing MD (2013) Warmer ambient temperatures depress liver function in a mammalian herbivore. Biol Lett 9:20130562

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee ET, Wang J (2003) Statistical methods for survival data analysis. Wiley, Hoboken

    Book  Google Scholar 

  • MacMillen RE (1964) Population ecology, water relations, and social behavior of a southern California desert rodent fauna. Univ Calif Publ Zool 71:1–66

    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  CAS  PubMed  Google Scholar 

  • Malenke JR, Magnanou E, Thomas K, Dearing MD (2012) Cytochrome P450 2B diversity and dietary novelty in the herbivorous, desert woodrat (Neotoma lepida). PLoS One 7:e41510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Malenke JR, Skopec MM, Dearing MD (2014) Evidence for functional convergence in genes upregulated by herbivores ingesting plant secondary compounds. BMC Ecol 14:23

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • McEachern MB, Eagles-Smith CA, Efferson CM, Van Vuren DH (2006) Evidence for local specialization in a generalist mammalian herbivore, Neotoma fuscipes. Oikos 113:440–448

  • Murphy SM, Linhart YB (1999) Comparative morphology of the gastrointestinal tract in the feeding specialist Scirurus aberti and several generalist congeners. J Mammal 80:1325–1330

    Article  Google Scholar 

  • Patton JL, Huckaby DG, Alvarez-Castaneda ST (2014) The evolutionary history and a systematic revision of woodrats of the Neotoma lepida group. UC Publication in Zoology, Oakland

    Google Scholar 

  • Post DM, Post DM, Reichman OJ, Wooster DE (1993) Characteristics and significance of the caches of eastern woodrats (Neotoma floridana). J Mammal 74:688–692

    Article  Google Scholar 

  • Rausher, MD (1992). Natural selection and the evolution of plant-insect interactions. In: Roitberg K, Isman MB (eds) Insect chemical ecology: an evolutionary approach. Chapman and Hall, New York, p 20–88

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

    Article  CAS  PubMed  Google Scholar 

  • Schwartz CC, Nagy JG, Regelin WL (1980) Juniper oil yield, terpenoid concentration, and effects on deer. J Wildl Manag 44:107–113

    Article  CAS  Google Scholar 

  • Shipley LA, Forbey JS, Moore BD (2009) Revisiting the dietary niche: when is a mammalian herbivore a specialist. Integr Comp Biol 49:274–290

    Article  PubMed  Google Scholar 

  • 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 Genomics Proteomics 2:34–43

    Article  PubMed  Google Scholar 

  • Skopec MM, Malenke JR, Halpert JR, Dearing MD (2013) An in vivo assay for elucidating the importance of cytochromes P450 for the ability of a wild mammalian herbivore (Neotoma lepida) to consume toxic plants. Physiol Biochem Zool 86:593–601

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smith FA, Murray IW, Harding LE, Lease HM, Martin J (2014) Life in an extreme environment: a historical perspective on the influence of temperature on the ecology and evolution of woodrats. J Mammal 95:1128–1143

    Article  Google Scholar 

  • Sorensen JS, Dearing MD (2003) Elimination of plant toxins by herbivorous woodrats: revisiting an explanation for dietary specialization in mammalian herbivores. Oecologia 134:88–94

    Article  CAS  PubMed  Google Scholar 

  • Sorensen JS, McLister JD, Dearinga MD (2004) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Stones RC, Hayward CL (1968) Natural history of the desert woodrat, Neotoma lepida. Am Midl Nat 80:458–476

    Article  Google Scholar 

  • Torregrossa A-M, Dearing MD (2009) Caching as a behavioral mechanism to reduce toxin intake. J Mammal 90:803–810

    Article  Google Scholar 

  • Torregrossa AM, Azzara AV, Dearing MD (2011) Differential regulation of plant secondary compounds by herbivorous rodents. Funct Ecol 25:1232–1240

    Article  Google Scholar 

  • Vaughan TA, Czaplewski NJ (1985) Reproduction in Stephens’ woodrat: the wages of folivory. J Mammal 66:429–443

    Article  Google Scholar 

  • Verts BJ, Carraway LN (2002) Neotoma lepida. Mamm Species 699:1–12

    Article  Google Scholar 

  • Wilderman PR, Jang HH, Malenke JR, Salib M, Angermeier E, Lamime S, Dearing MD, Halpert JR (2014) Functional characterization of cytochromes P450 2B from the desert woodrat Neotoma lepida. Toxicol Appl Pharmacol 274:393–401

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zahler P, Khan M (2003) Evidence for dietary specialization on pine needles by the woolly flying squirrel (Eupetaurus cinereus). J Mammal 84:480–486

    Article  Google Scholar 

  • Zlatnik E (1999) Juniperus osteosperma. In: Fire Eff. Inf. Syst. http://www.fs.fed.us/database/feis. Accessed 10 Jun 2014

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Acknowledgments

We thank Andrew Corbin for his adept technical assistance. Support for this research came from NSF (IOS 1256383 and IOS 1461359).

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Authors and Affiliations

  1. Department of Zoology, Weber State University, 1415 Edvalson Dr., Ogden, UT, 84408, USA

    Michele M. Skopec & Katharina Schramm

  2. Department of Biology, University of Utah, Salt Lake City, 84112, UT, USA

    Kevin D. Kohl, Katharina Schramm & M. Denise Dearing

  3. School of Pharmacy, University of Connecticut, Storrs, CT, USA

    James R. Halpert

Authors
  1. Michele M. Skopec
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  2. Kevin D. Kohl
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  3. Katharina Schramm
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  4. James R. Halpert
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  5. M. Denise Dearing
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Correspondence to Michele M. Skopec.

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Skopec, M.M., Kohl, K.D., Schramm, K. et al. Using the Specialization Framework to Determine Degree of Dietary Specialization in a Herbivorous Woodrat. J Chem Ecol 41, 1059–1068 (2015). https://doi.org/10.1007/s10886-015-0654-y

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  • DOI: https://doi.org/10.1007/s10886-015-0654-y

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