Skip to main content
Log in

Role of Tannin-Binding Salivary Proteins and Tannase-Producing Bacteria in the Acclimation of the Japanese Wood Mouse to Acorn Tannins

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

We studied the defense mechanisms against the negative effects of tannins in acorns by using the Japanese wood mouse (Apodemus speciosus) and acorns of a Japanese deciduous oak Quercus crispula, which contain 9.9% tannins on a dry weight basis. For the experiment, we allocated 26 wood mice into two groups: acclimated (N = 12) and nonacclimated (N = 14). Mice in the nonacclimated group were fed only acorns for 10 d after 4 wk of receiving a tannin-free diet. In contrast, mice in the acclimated group received ca. 3 g acorns daily in addition to the tannin-free diet for the first 4 wk, then they were fed only acorns for 10 d. Body weight, food intake, and digestibility were monitored. In addition, the amount of salivary proline-rich proteins (PRPs) and abundance of tannase-producing bacteria (TPB) in the feces of mice were measured. Of the 14 mice in the nonacclimated group, 8 died, whereas only 1 of the 12 in the acclimated group died. During the first 5 d of feeding acorns only, mice in the nonacclimated group lost, on average, 17.5% of their body mass, while those in the acclimated group lost only 2.5%. Food intake, dry matter digestibility, and nitrogen digestibility were higher in the acclimated group than in the nonacclimated group. The results indicate that wood mice can mitigate the negative effects of tannins by acclimation. Path analysis revealed that increased secretion of PRPs and abundance of Lactobacillus type of TPB might explain the acclimation to tannins.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Arbuckle, J. L. 2003. Amos 5.0 Update to the Amos User's Guide. SPSS, Inc., SmallWaters, Chicago.

    Google Scholar 

  • Arbuckle, J. L. and Wothke, W. 1999. Amos 4.0 User's Guide. SPSS, Inc., SmallWaters, Chicago.

    Google Scholar 

  • Austin, P. J., Suchar, L. A., Robbins, C. T., and 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  Google Scholar 

  • Bennick, A. 2002. Interaction of plant polyphenols with salivary proteins. Crit. Rev. Oral Biol. Med. 13:184–196.

    Article  PubMed  Google Scholar 

  • Bernays, E. A., Driver, G. C., and Bilgener, M. 1989. Herbivores and plant tannins. Adv. Ecol. Res. 19:263–302.

    Article  Google Scholar 

  • Blytt, H. J., Guscar, T. K., and Butler, L. G. 1988. Antinutritional effects and ecological significance of dietary condensed tannins may not be due to binding and inhibiting digestive enzymes. J. Chem. Ecol. 14:1455–1465.

    Article  CAS  Google Scholar 

  • Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal. Biochem. 72:248–254.

    Article  PubMed  CAS  Google Scholar 

  • Chung-MacCoubrey, A. L., Hagerman, A. E., and Kirkpatrick, R. L. 1997. Effect of tannins on digestion and detoxification activity in gray squirrels (Sciurus carolinensis). Physiol. Zool. 70:270–277.

    PubMed  CAS  Google Scholar 

  • Clauss, M., Gehrke, J., Hatt, J.-M., Dierenfeld, E. S., Flach, E. J., Hermes, R., Castell, J., Streich, W. J., and Fickel, J. 2005. Tannin-binding salivary proteins in three captive rhinoceros species. Comp. Biochem. Physiol. A 140:67–72.

    Article  CAS  Google Scholar 

  • Crespin, L., Verhagen, R., Stenseth, N. C., Yoccoz, N. G., PrÉvot-Julliard, A.-C., and Lebreton, J.-D. 2002. Survival in fluctuating bank vole populations: Seasonal and yearly variations. Oikos 98:467–479.

    Article  Google Scholar 

  • Dixon, M. D., Johnson, W. C., and Adkisson, C. S. 1997. Effects of caching on acorn tannin levels and blue jay dietary performance. Condor 99:756–764.

    Article  Google Scholar 

  • Eggum, B. E. and Christensen, K. D. 1975. Influence of tannin on protein utilization in feedstuffs with special reference to barley, pp. 135–143, in International Atomic Energy Agency (eds.). Breeding for Seed Protein Improvement Using Nuclear Techniques. International Atomic Energy Agency, Vienna.

    Google Scholar 

  • Elkinton, J. S., Healy, W. M., Buonaccorsi, J. P., Boettner, G. H., Hazzard, A. M., Smith, H. R., and Liebhold, A. M. 1996. Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77:2332–2342.

    Article  Google Scholar 

  • Fickel, J., Goritz, F., Joest, B. A., Hildebrandt, T., Hofmann, R. R., and Breves, G. 1998. Analysis of parotid and mixed saliva in Roe deer (Capreolus capreolus L.). J. Comp. Physiol. B 168:257–264.

    Article  PubMed  CAS  Google Scholar 

  • Fowler, M. E. and Richards, W. P. C. 1965. Acorn poisoning in a cow and a sheep. J. Am. Vet. Med. Assoc. 147:1215–1220.

    PubMed  CAS  Google Scholar 

  • Freeland, W. J. and 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. 1987. Radial diffusion method for determining tannin in plant extracts. J. Chem. Ecol. 13:437–449.

    Article  CAS  Google Scholar 

  • Hagerman, A. E. and 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 

  • Hoshizaki, K. and Miguchi, H. 2005. Influence of forest composition on tree seed predation and rodent responses: A comparison of monodominant and mixed temperate forests in Japan, pp. 253–267, in P.-M. Forget, J. E. Lambert, P. E. Hulme, and S. B. Vander Wall (eds.). Seed Fate: Predation, Dispersal, and Seedling Establishment. CABI Publishing, Wallingford.

    Google Scholar 

  • Jensen, T. S. 1982. Seed production and outbreaks of non-cyclic rodent populations in deciduous forests. Oecologia 54:184–192.

    Article  Google Scholar 

  • Johnson, W. C., Thomas, L., and Adkisson, C. S. 1993. Dietary circumvention of acorn tannins by blue jays. Oecologia 94:159–164.

    Article  Google Scholar 

  • Kirkpatrick, R. L. and Pekins, P. J. 2002. Nutritional value of acorns for wildlife, pp. 173–181, in W. J. McShea and W. M. Healy (eds.). Oak Forest Ecosystems. The Johns Hopkins University Press, Baltimore.

    Google Scholar 

  • Koenig, W. D. and Faeth, S. H. 1998. Effects of storage on tannin and protein content of cached acorns. Southernwestern Naturalist 43:170–175.

    Google Scholar 

  • McArthur, C., Sanson, G. D., and Beal, A. M. 1995. Salivary proline-rich proteins in mammals—Roles in oral homeostasis and counteracting dietary tannin. J. Chem. Ecol. 21:663–691.

    Article  CAS  Google Scholar 

  • McShea, W. J. 2000. The influence of acorn crops on annual variation in rodent and bird populations. Ecology 81:228–238.

    Article  Google Scholar 

  • Mehansho, H., Hagerman, A., Clements, S., Butler, L., Rogler, J., and Carlson, D. M. 1983. Modulation of proline-rich protein biosynthesis in rat parotid glands by sorghums with high tannin levels. Proc. Natl. Acad. Sci. USA. 80:3948–3952.

    Article  PubMed  CAS  Google Scholar 

  • Mehansho, H., Clements, S., Sheares, B. T., Smith, S., and Carlson, D. M. 1985. Induction of proline-rich glycoprotein-synthesis in mouse salivary-glands by isoproterenol and by tannins. J. Biol. Chem. 260:4418–4423.

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Miguchi, H. 1988. Two years of community dynamics of murid rodents after a beechnut mast year. J. Jpn. For. Soc. 70:472–480.

    Google Scholar 

  • Miguchi, H. 1994. Role of wood mice on the regeneration of cool temperate forest, pp. 115–121, in S. Kobayashi (ed.). Proceedings of NAFRO Seminar on Sustainable Forestry and Its Biological Environment. Japan Soc. Forest Planning Press, Tokyo.

    Google Scholar 

  • Mole, S., Butler, L. G., and Iason, G. 1990. Defense against dietary tannin in herbivores—A survey for proline-rich salivary proteins in mammals. Biochem. Syst. Ecol. 18:287–293.

    Article  CAS  Google Scholar 

  • Ohta, K., Abe, H., Kobayashi, T., Fujimaki, Y., Higuchi, S., Igarashi, B., Kuwahata, T., Maeda, M., Ueda, M., and Takayasu, T. 1976. A synecological study of murid rodents. Res. Bull. Coll. Exp. For. Univ. Hokkaido 34:119–159.

    Google Scholar 

  • Osawa, R. 1991. An investigation of Streptococcal flora in feces of koalas. J. Wildl. Manage. 55:623–627.

    Article  Google Scholar 

  • Osawa, R. and Sly, L. I. 1992. Occurrence of tannin–protein complex degrading Streptococcus sp. in feces of various animals. Syst. Appl. Microbiol. 15:144–147.

    Google Scholar 

  • Osawa, R., Bird, P. S., Harbrow, D. J., Ogimoto, K., and Seymour, G. J. 1993. Microbiological studies of the intestinal microflora of the koala, Phascolarctos cinereus. I. Colonisation of the caecal wall by tannin–protein-complex-degrading enterobacteria. Austral. J. Zool. 41:599–609.

    Article  Google Scholar 

  • Palo, R. T. and Robbins, C. T. 1991. Plant Defenses Against Mammalian Herbivory. CRC Press, Boca Raton, FL.

    Google Scholar 

  • Robbins, C. T. 1983. Wildlife Feeding and Nutrition. Academic Press, Orlando, FL.

    Google Scholar 

  • Robbins, C. T., Hanley, T. A., Hagerman, A. E., Hjeljord, O., Baker, D. L., Schwartz, C. C., and Mautz, W. W. 1987a. Role of tannins in defending plants against ruminants: Reduction in protein availability. Ecology 68:98–107.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Sasaki, E., Shimada, T., Osawa, R., Nishitani, Y., Spring, S., and Lang, E. 2005. Isolation of tannin-degrading bacteria isolated from feces of the Japanese large wood mouse, Apodemus speciosus, feeding on tannin-rich acorns. Syst. Appl. Microbiol. 28:358–365.

    Article  PubMed  Google Scholar 

  • Schnurr, J. L., Ostfeld, R. S., and Canham, C. D. 2002. Direct and indirect effects of masting on rodent populations and tree seed survival. Oikos 96:402–410.

    Article  Google Scholar 

  • Shimada, T. 2001. Nutrient compositions of acorns and horse chestnuts in relation to seed-hoarding. Ecol. Res. 16:803–808.

    Article  Google Scholar 

  • Shimada, T. 2006. Salivary proteins as a defense against dietary tannins. J. Chem. Eco. (in press).

  • Shimada, T. and Saitoh, T. 2003. Negative effects of acorns on the wood mouse Apodemus speciosus. Pop. Ecol. 45:7–17.

    Google Scholar 

  • Shimada, T., Saitoh, T., and Matsui, T. 2004. Does acclimation reduce the negative effects of acorn tannins in the wood mouse Apodemus speciosus? Acta Theriol. 49:203–214.

    Google Scholar 

  • Skopec, M. M., Hagerman, A. E., and Karasov, W. H. 2004. Do salivary proline-rich proteins counteract dietary hydrolyzable tannin in laboratory rats? J. Chem. Ecol. 30:1679–1692.

    Article  PubMed  CAS  Google Scholar 

  • Sone, K., Sekijima, T., and Okumura, H. 1986. Stomach contents of the wood mouse, Apodemus speciosus Temminck. Trans. Jpn. For. Soc. 97:467–468.

    Google Scholar 

  • Tatsukawa, K. and Murakami, O. 1976. On the food utilization of the Japanese wood mouse Apodemus speciosus (Mammalia: Muridae). Physiol. Ecol. Jpn. 17:133–144.

    Google Scholar 

  • Wada, N. 1993. Dwarf bamboos affect the regeneration of zoochorous trees by providing habitats to acorn-feeding rodents. Oecologia 94:403–407.

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Y. Segawa for assistance in laboratory work, Y. Takahata for instruction regarding the microbiological experiments, H. Itô for advice concerning path analysis, K. Hoshizaki for help in collecting acorns, I. Wallis for revising the manuscript, and two anonymous reviewers for instructive comments and discussion. All procedures in the field and laboratory followed the Guidelines for Animal Experimentation established by Japanese Association for Laboratory Animal Science. This study was supported in part by Grants-in-Aid (nos. 17570027 and 17370006) from the Ministry of Education, Science and Culture of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Takuya Shimada.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Shimada, T., Saitoh, T., Sasaki, E. et al. Role of Tannin-Binding Salivary Proteins and Tannase-Producing Bacteria in the Acclimation of the Japanese Wood Mouse to Acorn Tannins. J Chem Ecol 32, 1165–1180 (2006). https://doi.org/10.1007/s10886-006-9078-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-006-9078-z

Keywords

Navigation