Abstract
Terpenes, volatile plant secondary compounds produced by woody plants, have historically been thought to act as feeding deterrents for mammalian herbivores. However, three species of woodrats, Neotoma stephensi, N. lepida, and N. albigula, regularly consume juniper, which is high in terpenes, and N. stephensi and N. lepida are considered juniper specialists. By investigating the terpene profiles in Juniperus monosperma and J. osteosperma, which are browsed or avoided by woodrats in the field, and recording the caching and consumption of juniper foliage by woodrats in the lab, we have evidence that terpenes may serve as feeding and/or foraging cues. The obligate specialist N. stephensi chose to forage on trees higher in p-cymene and preferred to consume juniper rather than caching it in a laboratory setting. These observations provide evidence that terpenes serve as a feeding cue and that the obligate specialist’s physiological mechanism for metabolizing the terpenes present in juniper may negate the need for caching. The facultative specialist N. lepida chose to forage on trees lower in four terpenes and cached more juniper than the obligate specialist N. stephensi, providing evidence that terpenes serve as a feeding deterrent for N. lepida and that this woodrat species relies on behavioral mechanisms to minimize terpene intake. The generalist N. albigula foraged on trees with higher terpenes levels but consumed the least amount of juniper in the lab and preferred to cache juniper rather than consume it, evidence that terpenes act as foraging but not feeding cues in the generalist. Our findings suggest that volatile plant secondary compounds can act as feeding and/or foraging cues and not just feeding deterrents in mammalian herbivores.
Similar content being viewed by others
References
Adams RP (1991) Analysis of Juniper and other forest tree oils. In: Linskens HF, Jackson JF (eds) Modern methods of plant analysis, new series: oil and waxes. Springer-Verlag, Berlin, pp 131–157
Adams RP (1994) Geographic variation in the volatile terpenoids of Juniperus monosperma and J. osteosperma. Biochem Syst Ecol 22:65–71. https://doi.org/10.1016/0305-1978(94)90115-5
Adams RP (2007) Identification of essential oil components by gas chromatography/ mass spectrometry, 4th edn. Allured Publ., Carol Stream 804 pgs
Adams RP, Skopec MM, Muir JP (2014a) Comparison of leaf terpenoids and tannins in Juniperus monosperma from woodrat (Neotoma stephensi) browsed and non-browsed trees. Phytologia 96:63–70
Adams RP, Skopec MM, Kohl KD, Dearing MD (2014b) Comparison of volatile leaf terpenoids from Juniperus monosperma and J. osteosperma leaves: intact, ground and exposed to ambient temperature. Phytologia 96:207–217
Adams RP, Skopec MM, Muir JP (2016) Comparison of leaf terpenoids and tannins in Juniperus osteosperma from woodrat (Neotoma lepida) browsed and non-browsed trees. Phytologia 98:17–25
Bedoya-Pérez MA, Issa DD, Banks PB, McArthur C (2014) Quantifying the response of free-ranging mammalian herbivores to the interplay between plant defense and nutrient concentrations. Oecologia 175:1167–1177. https://doi.org/10.1007/s00442-014-2980-0
Brown JH, Lieberman GA, Dengler WF (1972) Woodrats and Cholla : dependence of a small mammal population on the density of cacti. Ecol 53:310–313. https://doi.org/10.2307/1934087
Bruce TJ, Wadhams LJ, Woodcock CM (2005) Insect host location: a volatile situation. Trends Plant Sci 10:269–274
Bryant JP, Reichardt PB, Clausen TP, Provenza FD, Kuropat PJ (1992a) Woody plant-mammal interactions. In: Rosenthal GA, Berenbaum MR (eds) Herbivores: their interactions with secondary plant metabolites, 2nd edn. Academic, San Diego, pp 343–370
Bryant JP, Reichardt PB, Clausen T (1992b) Chemically mediated interactions between woody plants and browsing mammals. J Range Manag 45:18–24
Cameron GN, Rainey DG (1972) Habitat utilization by Neotoma lepida in the Mohave Desert. J Mammal 53:251–266
Clark L (1991) The nest protection hypothesis: the adaptive use of plant secondary compounds by European starlings. In: Loye JE, Zuk M (eds) Bird–parasite interactions: ecology, evolution and behaviour. Oxford University Press, Oxford, pp 205–221
Dearing MD (1997) The manipulation of plant toxins by a food-hoarding herbivore, Ochotona princeps. Ecology 78:774–781
Dearing MD, Mangione AM, Karasov WH (2000) Diet breadth of mammalian herbivores: nutrient versus detoxification constraints. Oecologia 123:397–405
Dial KP (1988) Three sympatric species of neotoma : dietary specialization and coexistence coexistence. Oecologia 76:531–537
Finnerty PB, Stutz RS, Price CJ, Banks PB, McArthur C (2017) Leaf odour cues enable non-random foraging by mammalian herbivores. J Anim Ecol 86:1317–1328
Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289
Hagerman AE, Butler LG (1978) Protein precipitation method for the quantitative determination of tannins. J Agric Food Chem 26:809–812
Haley SL, Lamb JG, Franklin MR, Constance JE, Dearing MD (2007) 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
Haslam E (1989) Plant polyphenols: vegetable tannins revisited. Cambridge University Press, Cambridge
Iason G (2005) The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc Nutr Soc 64:123–131
Kohl K, Skopec MM, Dearing MD (2014) Captivity results in disparate loss of gut microbial diversity in closely related hosts. Conserv Physiol 2:cou009. https://doi.org/10.1093/conphys/cou009
Lev-Yadun S, Gould KS (2008) Role of anthocyanins in plant defence. In: Winefield C, Davies K, Gould K (eds) Anthocyanins. Springer, New York, pp 22–28
Luo Y, Yang Z, Steele MA, Zhang Z, Stratford JA, Zhang H (2014) Hoarding without reward: rodent responses to repeated episodes of complete cache loss. Behav Process 106:36–43
MacMillen RE (1964) Population ecology, water relations, and social behavior of a southern California desert rodent fauna. Univ Calif Publ Zool 71:1–66
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
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
Naumann HD, Hagerman AE, Lambert BD, Muir JP, Tedeschi LO, Kothmann MM (2013) Molecular weight and protein-precipitating ability of condensed tannins from warm-season perennial legumes. J Plant Interact 9:212–219
Palo RT, Robbins CT (1991) Plant defenses against mammalian herbivory. CRC Press, Boca Raton
Petit C, Hossaert-McKey M, Perret P, Blondel J, Lambrechts MM (2002) Blue tits use selected plants and olfaction to maintain an aromatic environment for nestlings. Ecol Lett 5:585–589
Savolainen H, Pfaffli P (1978) Effects of long-term turpentine inhalation on rat brain protein metabolism. Chem Biol Interact 21:271–276
Schmitt MH, Shuttleworth A, Ward D, Shrader AM (2018) African elephants use plant odours to make foraging decisions across multiple spatial scales. Anim Behav 141:17–27
Shipley LA, Forbey JS, Moore BD (2009) Revisiting the dietary niche: when is a mammalian herbivore a specialist. Integr Comp Biol 49:274–290
Sikes RS, Gannon WL (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92(1):235–253
Skopec MM, Dearing MD (2011) Differential expression and activity of catechol-O-methyl transferase (COMT) in a generalist (Neotoma albigula) and juniper specialist (Neotoma stephensi) woodrat. Comp Biochem Physiol C Toxicol Pharmacol 154:383–390
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
Skopec MM, Hale AJ, Torregrossa A, Dearing MD (2013a) Biotransformation enzyme expression in nasal epithelium of Woodrats. Comp Biochem Physiol C Toxicol Pharmacol 157:72–79
Skopec MM, Malenke JR, Halpert JR, Dearing MD (2013b) 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
Skopec MM, Kohl KD, Schramm K, Halpert JR, Dearing MD (2015) Using the specialization framework to determine degree of dietary specialization in an herbivorous woodrat. J Chem Ecol 41:1059–1068
Smith FA, Murray IW, Harding LE et al (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
Sorensen JS, McLister JD, Dearing MD (2004a) Plant secondary metabolites compromise the energy budgets of specialist and generalist mammalian herbivores. Ecology 86:125–139
Sorensen JS, Turnbull CA, Dearing MD (2004b) A specialist herbivore (Neotoma stephensi) absorbs fewer plant toxins than does a generalist (Neotoma albigula). Physiol Biochem Zool 77:139–148
Sorensen JS, Mclister JD, Dearing MD (2005) Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology 86:140–154
Sperling F (1969) In vivo and in vitro toxicology of turpentine. Clin Toxicol 2:21–35
Sperling F, Marcus WL, Collins C (1967) Acute effects of turpentine vapor on rats and mice. Toxicol Appl Pharmacol 10:8–20
Steele RGD, Torrie JH (1960) Principles and procedures of statistics. McGraw-Hill Book Co., New York
Stutz RS, Banks PB, Proschogo N, McArthur C (2016) Follow your nose: leaf odour as an important foraging cue for mammalian herbivores. Oecologia 182:643–651
Theis N, Lerdau M (2003) The evolution of function in plant secondary metabolites. Int J Plant Sci 164:S93–S102
Torregrossa A-M, Dearing MD (2009a) Caching as a behavioral mechanism to reduce toxin intake. J Mammal 90:803–810
Torregrossa AM, Dearing MD (2009b) Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct Ecol 23:48–56
Torregrossa A-M, Azzara AV, Dearing MD (2011) Differential regulation of plant secondary compounds by herbivorous rodents. Funct Ecol 25(6):1232–1240
Torregrossa A-M, Azzara AV, Dearing MD (2012) Testing the diet-breadth trade-off hypothesis: differential regulation of novel plant secondary compounds by a specialist and a generalist herbivore. Oecologia 168(3):711–718
Vaughan TA (1982) Stephens’ Woodrat, a Dietary Specialist. J Mammal 63(1):53–62
Vaughan TA, Czaplewski NJ (1985) Reproduction in Stephens’ woodrat: the wages of folivory. J Mammal 66:429–443
Visser JH (1986) Host odor perception in phytophagous insects. Annu Rev Entomol 31:121–144
Wimberger PH (1984) The use of green plant material in bird nests to avoid ectoparasites. Auk 101:615–618
Wolfe RM, Terrill TH, Muir JP (2008) Drying method and origin of standard affect condensed tannin (CT) concentrations in perennial herbaceous legumes using simplified butanol-HCl CT analysis. J Sci Food Agric 88:1060–1067
Acknowledgments
We thank Ashley Anderton for her adept technical assistance. Support for this research came from funds from Baylor University, Texas A&M AgriLife Research and Weber State University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Skopec, M.M., Adams, R.P. & Muir, J.P. Terpenes May Serve as Feeding Deterrents and Foraging Cues for Mammalian Herbivores. J Chem Ecol 45, 993–1003 (2019). https://doi.org/10.1007/s10886-019-01117-w
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-019-01117-w