Skip to main content
Log in

Seasonal changes in the concentrations of plant secondary metabolites and their effects on food selection by Microtus oeconomus

  • Original Investigation
  • Published:
Mammalian Biology Aims and scope Submit manuscript

Abstract

Using cafeteria trials conducted during June–September 2008 in Qinghai Province, China, we investigated the selection of 20 plant species by root voles (Microtus oeconomus). It was found that both favored and edible plant groups of root voles comprised 6 species, while the remaining 8 species were anorectic plants. Three plant secondary metabolites (PSMs): flavonoids, condensed tannins, and total phenols, exhibited seasonal changes in concentration; being lowest at June and gradually increasing from July to August/September. Total phenols was the only factor included in the best model of generalized linear models, indicating that total phenols was the most important factor deterring food selection by root voles. In contrast, tannins had a weak effect on food selection by root voles. This study indicated that PSMs play an important role in food selection by root voles; however, the effects of PSMs depend on the type of PSMs. Furthermore, this finding partly verifies the hypothesis that PSMs contribute to the defense strategy of plants, significantly influencing plant selection by root voles.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Austin, P.J., Suchar, L.A., Robbins, C.T., Hagerman, A.E., 1989. Tannin-binding proteins in saliva of deer and their absence in saliva of sheep and cattle. J. Chem. Ecol. 15, 1335–1347.

    Article  CAS  PubMed  Google Scholar 

  • Ball, J.P., Dahlgren, J., 2002. Browsing damage on pine (Pinus sylvestris and P. con-torta) by a migrating moose (Alcesalces) population in winter: relation to habitat composition and road barriers. Scand. J. Forest Res. 17, 427–435.

    Article  Google Scholar 

  • Batzli, G.O., 1985. Nutrition, in biology of new world Microtus. Am. Soc. Mammal. 8, 779–811 (special publication).

  • Batzli, G.O., Jung, H.G., 1980. Nutritional ecology of microtine rodents: resource utilization near Atkasook, Alaska. Arct. Alp. Res. 12, 483–499.

    Article  Google Scholar 

  • Bee, J.N., Tanentzap, A.J., Lee, W.G., Lavers, R.B., Mark, A.F., Mills, J.A., Coomes, D.A., 2011. Influence offoliartraits on forage selection by introduced red deer in New Zealand. Basic Appl. Ecol. 12, 56–63.

    Article  Google Scholar 

  • Benett, R.C., Wallsgrove, R.M., 1994. Tansley Review No 72. Secondary metabolites in plant defence mechanisms. New Phytol. 127, 617–633.

    Google Scholar 

  • Berg, T.B., 2003. Catechin content and consumption ratio of the collared lemming. Oecologia 135, 242–249.

    Article  PubMed  Google Scholar 

  • Black, J.L., 1990. Nutrition of the grazing ruminant. Proc. N. Z. Soc. Anim. Prod. 50, 7–27.

    Google Scholar 

  • Borchard, F., Berger, H.J., Bunzel-Drükec, M., Fartmannd, T., 2011. Diversity of plant-animal interactions: possibilities for a new plant defense indicator value? Ecol. Indic. 11, 1311–1318.

    Article  Google Scholar 

  • Bryant, J.P., Wieland, G.D., Reichardt, P.B., Lewis, V.E., McCarthy, M.C., 1983. Pinosylvin methyl-ether deters snowshoe hare feeding on green alder. Science 222, 1023–1025.

    Article  CAS  PubMed  Google Scholar 

  • Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edition. Springer, New York.

  • Caldwell, M.M., 1977. The effects of solar UV-B radiation (280-315 nm) on higher plants: implications of stratospheric ozone reduction. In: Caseellan, A. (Ed.), Research in Photobiology. Plenum Press, New York, p. 335.

    Google Scholar 

  • Clauss, M., Lason, K., Gehrke, J., Lechner-Doll, M., Fickel, J., Grune, T., Jürgen Streich, W., 2003. Captive roe deer (Capreolus capreolus) select for low amounts of tannic acid but not quebracho: fluctuation of preferences and potential benefits. Comp. Biochem. Phys. B 136, 369–382.

    Article  CAS  Google Scholar 

  • Cui, Q.H., Jiang, Z.G., Lian, X.M., Zhang, T.Z., Su, J.P., 2005. Factors influencing habitat selection of root voles (Microtus oeconomus). Acta Theriol. Sin. 25, 45–51.

    Google Scholar 

  • Dai, X., Zou, Z.Z., Zhang, T.T., Jiang, W., Wei, W.H., Yang, S.M., 2011. The effect of tannic acid on the gonad hormones in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). Acta Theriol. Sin. 31, 278–283.

    CAS  Google Scholar 

  • Dearing, M.D., Foley, W.J., 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 

  • Degabriel, J.L, Moore, B.D., Foley, W.J., Johnson, C.N., 2009. The effects of plant defensive chemistry on nutrient availability predict reproductive success in a mammal. Ecology 90, 711–719.

    Article  PubMed  Google Scholar 

  • Dixon, R.A., Paiva, N.L., 1995. Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085–1097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebel, J., Hahlbrock, K., 1982. In: Harbome, J.B., Mabry, T.J. (Eds.), The Flavonoids: Advances in Research. Chapman and Hall, London, pp. 641–679.

  • Ettle, T., Mentschel, K., Roth, F.X., 2004. Dietary self-selection for organic acids by the piglet. Arch. Anim. Nutr. 58, 379–388.

    Article  CAS  PubMed  Google Scholar 

  • Feeny, P., 1976. Plant apparency and chemical defense. In: Wallace, J.W., Nansel, R.L. (Eds.), Biological Interactions Between Plants and Insects. Recent Advances in Phytochemistry, vol. 10. Plenum Press, New York, USA, pp. 1–40.

    Google Scholar 

  • Feeny, P.P., 1970. Seasonal changes in oak leaf tannins and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51, 565–581.

    Article  Google Scholar 

  • Fickel, J., Pitra, C, Joest, B.A., Hofmann, R.R., 1999. A novel method to evaluate the relative tannin-binding capacities of salivary proteins. Comp. Biochem. Physiol. 122, 225–229.

    CAS  Google Scholar 

  • Freeland, W.J., Janzen, D.H., 1974. Strategies in herbivory by mammals: the role of plant secondary compounds. Am. Nat. 108, 269–289.

    Article  CAS  Google Scholar 

  • Hagerman, A.E., Robbins, C.T., Willson, T.C., 1992. annin chemistry in relation to digestion. J. Range Manage. 45, 57–62.

    Article  Google Scholar 

  • Hagerman, A.E., Robbins, C.T., 1993. Specificity of tannin-binding salivary proteins relative to diet selection by mammals. Can. J. Zool. 71, 628–633.

    Article  CAS  Google Scholar 

  • Hjältén, J., Palo, T., 1992. Selection of deciduous trees by free ranging voles and hares in relation to plant chemistry. Oikos, 477–484.

    Google Scholar 

  • Iason, G., 2005. The role of plant secondary metabolites in mammalian herbivory: ecological perspectives. Proc. Nutr. Soc. 64, 123–131.

    Article  CAS  PubMed  Google Scholar 

  • Iason, G.R., Hester, A.J., 1993. The response of heather (Calluna vulgaris) to shade and nutrients predictions ofthe carbon nutrient balance hypothesis. J. Ecol. 81, 75–80.

    Article  Google Scholar 

  • Iason, G.R., Villalba, J.J., 2006. Behavioral strategies of mammal herbivores against plant secondary metabolites: the avoidance-tolerance continuum. J. Chem. Ecol. 32, 1115–1132.

    Article  CAS  PubMed  Google Scholar 

  • Juntheikki, M.R., Riitta, J.T., Hagermans, A.E., 1996. Salivary tannin-binding proteins in root vole (Microtus oeconomus Pallas). Biochem. Syst. Ecol. 24, 25–35.

    Article  CAS  Google Scholar 

  • Koricheva, J., Barton, K.E., 2012. Temporal changes in plant secondary metabolite production: patterns causes and consequences. In: Iason, G.R., Dicke, M., Hartley, S.E. (Eds.), The Ecology of Plant Secondary Metabolites: From Genes to Global Processes. Cambridge University Press, Cambridge.

    Chapter  Google Scholar 

  • Laitinen, M.L., Julkunen-Tiitto, R., Yamaji, K., Heinonen, J., Rousi, M., 2004. Variation in birch bark secondary chemistry between and within clones: implications for herbivory by hares. Oikos 104, 316–326.

    Article  CAS  Google Scholar 

  • Lawler, I.R., Stapley, J., Foley, W.J., Eschler, B.M., 1999. Ecological example of conditioned flavor aversion in plant-herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. J. Chem. Ecol. 25, 401–415.

    Article  CAS  Google Scholar 

  • Li, J.N., Liu, J.K., Tao, S.L., 2003. Effects of tannic acid on the food intake and protein digestibility of root voles. Acta Theriol. Sin. 23, 52–57.

    CAS  Google Scholar 

  • Lindroth, G.R., 1991. Mammalian herbivore-plant interactions. In: Aehamson, W.C. (Ed.), Plant-Animal Interactions. McGraw-Hill, New York, pp. 163–206.

    Google Scholar 

  • Liu, J.K., Liang, J.R., Zhou, X.M., Li, J.H., 1982. Communities and quantity of rodents in alpine meadow ecosystem. In: Xia, W.P. (Ed.), Alpine Meadow Ecosystem, Fasc. 1. Gansu People’s Publishing House, Lanzhou, pp. 24–43.

    Google Scholar 

  • Liu, J.K., Wang, X., Liu, W., 1991. Studies on the nutritional ecology of small herbivorous mammals: 1. Patterns of food selection and resource utilization for root vole and Gansu pikas. In: Liu, J.K., Wang, Z.W. (Eds.), Alpine Meadow Ecosystem, Fasc.3. Science Press, Beijing, pp. 111–123.

    Google Scholar 

  • Makkar, H.P.S., Bluemmei, M., Borowy, N.K., 1993. Gravimetric determination oftan-nins and their correlation with chemical and protein precipitation methods. J. Sci. Food Agric. 61, 161–165.

    Article  CAS  Google Scholar 

  • Marsh, K., Wallis, I., Foley, W., 2007. Behavioural contributions to the regulated intake of plant secondary metabolites in koalas. Oecologia 154, 283–290.

    Article  PubMed  Google Scholar 

  • Marsh, K.J., Foley, W.J., Cowling, A., Wallis, I.R., 2003. Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Thichosurus vulpec-ula). J. Comp. Physiol. B 173, 69–78.

    CAS  PubMed  Google Scholar 

  • Mehansho, H., Butler, L.G., Carlson, D.M., 1987. Dietary tannins and salivary prolinerich proteins: interactions, induction and defense mechanisms. Annu. Rev. Nutr. 7, 423–440.

    Article  CAS  PubMed  Google Scholar 

  • Moore, B.D., Foley, W.J., Wallis, I.R., Cowling, A., Handasyde, K.A., 2005. A simple understanding of complex chemistry explains feeding preferences of koalas. Biol. Lett. 1, 64–67.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nie, H.Y., Liu, J.K., Su, J.P., 1995. Field experiment studies on the multifactorial hypothesis of population system regulation for small rodents: the effect pattern of food availability and predation on spacing behavior of root voles and the function of spacing behavior in population regulation. Acta Theriol. Sin. 15, 41–52.

    Google Scholar 

  • Niemelä, P., Danell, K., 1988. Comparison of moose browsing on Scotspine (Pinus sylvestris) and lodgepole pine (Pinus contorta).J. Appl. Ecol. 25, 761–775.

    Article  Google Scholar 

  • Porter, L.J., Hrstich, L.N., Chan, B.G., 1985. The conversion of procyanidins and prodelphinidins to cyanidin and delphinidin. Phytochemistry 25, 223–230.

    Article  Google Scholar 

  • Raymond, V., Barbehenn, C, Peter, C, 2011. Tannins in plant-herbivore interactions. Phytochemistry 72, 1551–1565.

    Article  CAS  Google Scholar 

  • Rhoades, D.F., Cates, R.G., 1976. Toward a general theory of plant antiherbivore chemistry. In: Wallace, J.W., Nansel, R.L. (Eds.), Biological Interactions Between Plants and Insects. Recent Advances in Phytochemistry, vol. 10. Plenum Press, New York, USA, pp. 169–213.

    Google Scholar 

  • Robbins, C.T., Hagerman, A.E., Austin, P.J., 1991. Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J. Mammal. 72, 480–486.

    Article  Google Scholar 

  • Robbins, C.T., Mole, S., Hagerman, A.E., Hanley, T.A., 1987. Role of tannins in defending plants against ruminants: reduction in dry matter digestion? Ecology 68, 1606–1615.

    Article  CAS  PubMed  Google Scholar 

  • Rozema, J., Chardonnents, A., Tosserams, M., Hafkenscheid, R., Bruijnzeel, S., 1997. Leaf thickness and UV-B absorbing pigments of plants in relation to an elevational gradient along the Blue Mountains, Jamaica. Plant Ecol. 128, 151–159.

    Article  Google Scholar 

  • Ruechmann, S., Leser, C, Bannert, M., Treutter, D., 2002. Relationship between growth, secondary metabolism, and resistance of apple. Plant Biol. 4, 137–143.

    Article  Google Scholar 

  • Schreiber, L.A., Swihar, R.K., 2009. Selective feeding of pine voles on roots of tree seedlings. Can. J. Zool. 87, 183–187.

    Article  Google Scholar 

  • Scott, L.L., Provenza, F.D., 1999. Variation in food selection among lambs: effects of basal diet and foods offered in a meal. J. Anim. Sci. 77, 2391–2397.

    Article  CAS  PubMed  Google Scholar 

  • Sorensen, J.S., McLister, J.D., Dearing, M.D., 2005. Novel plant secondary metabolites impact dietary specialists more than generalists (Neotoma spp.). Ecology 86, 140–154.

    Article  Google Scholar 

  • Stolter, C., Ball, J.P., Julkunen-Tiitto, R., 2013. Seasonal differences in the relative importance of specific phenolics and twig morphology result in contrasting patterns of foraging by ageneralist herbivore. Can. J. Zool. 91, 338–347.

    Article  CAS  Google Scholar 

  • Stolter, C., Ball, J.P., Niemelä, P., Julkunen-Tiitto, R., 2010. Herbivores and variation in the composition of specific phenolics of boreal coniferous trees: a search for patterns. Chemoecology 20, 229–242.

    Article  CAS  Google Scholar 

  • Stolter, C., Ball, J.P., Julkunen-Tiitto, R., Lieberei, R., Ganzhorn, J.U., 2005. Winter browsing of moose on two different willow species: food selection in relation to plant chemistry and plant response. Can. J. Zool. 83, 807–819.

    Article  CAS  Google Scholar 

  • Stolter, C., Niemelä, P., Ball, J.P., Julkunen-Tiitto, R., Vanhatalo, A., Danell, K., Varvikko, T., Ganzhorn, J.U., 2009. Comparison of plant secondary metabolites and digestibility of three different boreal coniferous trees. Basic Appl. Ecol. 10, 19–26.

    Article  Google Scholar 

  • Sunnerheim-Sjöberg, K., Hämäläinen, M., 1992. Multivariate study of moose browsing in relation to phenol pattern in pine needles. J. Chem. Ecol. 18, 659–672.

    Article  PubMed  Google Scholar 

  • Swain, T., 1979. Tannins and lignins. In: Rosenthal, G.A., Janzen, D.H. (Eds.), Herbivores: Their Interaction with Secondary Plant Metabolites. Academic Press, New York, pp. 657–682.

    Google Scholar 

  • Tast, J., 1974. The food and feeding habits of the root vole, Microtus oeconomus, in Finnish Lapland. Aquilo Ser. Zool. 15, 25–32.

    Google Scholar 

  • Torregrossa, A.M., Dearing, M.D., 2009. Nutritional toxicology of mammals: regulated intake of plant secondary compounds. Funct. Ecol. 23, 48–56.

    Article  Google Scholar 

  • Treutter, D., 2001. Biosynthesis of phenolic compounds and its regulation in apple. Plant Growth Regul. 34, 71–89.

    Article  CAS  Google Scholar 

  • Utsumia, S.A., Cibilsa, A.F., Estellb, R.E., Soto-Navarroa, S.A., Leeuwenc, D.V., 2009. Seasonal changes in one seed juniper intake by sheep and goats in relation to dietary protein and plant secondary metabolites. Small Rumin. Res. 81, 152–162.

    Article  Google Scholar 

  • Verheyden-Tixier, H., Duncan, P., 2000. Selection for small amounts of hydrolysable tannins by a concentrate-selecting mammalian herbivore. J. Chem. Ecol. 26, 351–358.

    Article  CAS  Google Scholar 

  • Villalba, J.J., Provenza, F.D., Bryant, J.P., 2002. Consequences of the interaction between nutrients and plant secondary metabolites on herbivore selectivity: benefits or detriments for plants? Oikos 97, 282–292.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Shengmei Yang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dai, X., Han, M., Liu, Q. et al. Seasonal changes in the concentrations of plant secondary metabolites and their effects on food selection by Microtus oeconomus. Mamm Biol 79, 215–220 (2014). https://doi.org/10.1016/j.mambio.2014.01.002

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1016/j.mambio.2014.01.002

Keywords

Navigation