Monoterpenes as inhibitors of digestive enzymes and counter-adaptations in a specialist avian herbivore
- 282 Downloads
Many plants produce plant secondary metabolites (PSM) that inhibit digestive enzymes of herbivores, thus limiting nutrient availability. In response, some specialist herbivores have evolved digestive enzymes that are resistant to inhibition. Monoterpenes, a class of PSMs, have not been investigated with respect to the interference of specific digestive enzymes, nor have such interactions been studied in avian herbivores. We investigated this interaction in the Greater Sage-Grouse (Phasianidae: Centrocercus urophasianus), which specializes on monoterpene-rich sagebrush species (Artemisia spp.). We first measured the monoterpene concentrations in gut contents of free-ranging sage-grouse. Next, we compared the ability of seven individual monoterpenes present in sagebrush to inhibit a protein-digesting enzyme, aminopeptidase-N. We also measured the inhibitory effects of PSM extracts from two sagebrush species. Inhibition of aminopeptidase-N in sage-grouse was compared to inhibition in chickens (Gallus gallus). We predicted that sage-grouse enzymes would retain higher activity when incubated with isolated monoterpenes or sagebrush extracts than chicken enzymes. We detected unchanged monoterpenes in the gut contents of free-ranging sage-grouse. We found that three isolated oxygenated monoterpenes (borneol, camphor, and 1,8-cineole) inhibited digestive enzymes of both bird species. Camphor and 1,8-cineole inhibited enzymes from chickens more than from sage-grouse. Extracts from both species of sagebrush had similar inhibition of chicken enzymes, but did not inhibit sage-grouse enzymes. These results suggest that specific monoterpenes may limit the protein digestibility of plant material by avian herbivores. Further, this work presents additional evidence that adaptations of digestive enzymes to plant defensive compounds may be a trait of specialist herbivores.
KeywordsAminopeptidase-N Digestive enzymes Greater sage-grouse Monoterpenes Sagebrush
We would like to thank Dr. William Karasov, Dr. Mark Cook, and Taylor Jarmes for assistance with obtaining tissues from chickens. We also thank S. Vasilchenko, N. Wiggins, falconers T. Maechtle, D. Skinner, and H. Quade as well as Gus, the German short-haired pointer, Jack and Kenna the English setters, Grace and Bob the gyrfalcons, and Gabriel the gyrfalcon/peregrine falcon hybrid for assistance with collecting tissues in the field. This research was funded by the Idaho Department of Fish and Game, Idaho Governor’s Office for Species Conservation to J. S. F, a University of Utah Undergraduate Research Opportunities Grant to E. P, the National Science Foundation (DEB-1146194 and IOS-1258217 to J. S. F, DEB-1210094 to M. D. D and K. D. K, and DBI-1400456 to K. D. K), and Idaho INBRE Program-NIH Grant #P20 GM103408 to J.S.F., This is a contribution from Idaho Federal Aid in Wildlife Restoration Project W-160-R.
- Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naive trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79:3468–3475CrossRefPubMedCentralPubMedGoogle Scholar
- Birdlife International (2012) Centrocercus urophasianus. Accessed 15 Nov 2014Google Scholar
- Chauhan A, Gupta S, Mahmood A (2007) Effect of tannic acid on brush border disaccharidases in mammalian intestine. Ind J Exp Biol 45:353–358Google Scholar
- Cheng C, Liu XW, Du FF, Li MJ, Xu F, Wang FQ, Liu Y, Li C, Sun Y (2013) Sensitive assay for measurement of volatile borneol, isoborneol, and the metabolite camphor in rat pharmacokinetic study of Borneolum (Bingpian) and Borneolum syntheticum (synthetic Bingpian). Acta Pharm Sinic 34:1337–1348CrossRefGoogle Scholar
- Connelly JW, Braun CE (1997) Long-term changes in Sage Grouse Centrocercus urophasianus populations in western North America. Wildl Biol 3:229–234Google Scholar
- Howard PH (1997) Handbook of environmental fate and exposure data for organic chemicals. CRC Press, Boca RatonGoogle Scholar
- Karasov WH, Martinez del Rio C (2007) Physiological Ecology: How Animals Process Energy, Nutrients, and Toxins. Princeton University Press, PrincetonGoogle Scholar
- McArthur C, Hagerman AE, Robbins CT (1991) Physiological strategies of mammalian herbivores against plant defenses. In: Palo RT, Robbins CT (eds) Plant defenses against mammalian herbivory. CRC Press, Boca Raton, USA, pp 103–114Google Scholar
- Rhoades DF (1977) The antiherbivore chemistry of Larrea. In: Mabry TJ, Hunziker JH, DiFeo DR (eds) Creosote bush: biology and chemistry of Larrea in New World deserts. Hutchinson and Ross, Stroudsberg, pp 135–175Google Scholar