Different population responses of three sympatric rodent species to acorn masting—the role of tannin tolerance

Population Ecology - Tập 59 - Trang 29-43 - 2017
Rokuya Onodera1, Yuka Akimoto1, Takuya Shimada2, Takashi Saitoh3
1Graduate School of Environmental Science, Hokkaido University, Sapporo, Japan
2Tohoku Research Center, Forestry and Forest Products Research Institute, Morioka, Japan
3Field Science Center Hokkaido University Sapporo Japan

Tóm tắt

Rodent population dynamics are predicted to respond positively to the masting of acorns, but diverging results have been published. This study tested the hypothesis that population responses to acorn masting vary depending on differences in the tolerance to tannins of different rodent species. The effects of acorn abundance on the rodent population densities were analyzed using a dataset obtained in Hokkaido, Japan. Specifically, population fluctuations of three rodent species (Apodemus speciosus, A. argenteus, and Myodes rufocanus) and the abundance of Quercus crispula acorns have been monitored since 1992. Acorn production in previous years had a positive effect on the annual population growth rates of A. speciosus; however, this trend was not clear in the other two species. Tannin tolerance, assessed by body weight changes in an acorn feeding experiment, exhibited clear differences among the rodent species; namely, the body weight of A. speciosus increased, whereas that of the other two species decreased. The observed responses to acorn masting of populations of the three sympatric rodent species reflected tannin tolerance. It suggests that only populations of species with high tannin tolerance positively respond to acorn masting. Previous studies tend to overlook species-specific abilities of coping with tannins in acorns. Our results emphasize the necessity of evaluating the tannin tolerance of rodents and the tannin content of acorns to understand how rodent population dynamics and acorn production are related.

Tài liệu tham khảo

Bennick A (2002) Interaction of plant polyphenols with salivary proteins. Crit Rev Oral Biol Med (Baltimore) 13:184–196 Bjørnstad ON, Champely S, Stenseth NC, Saitoh T (1996) Cyclicity and stability of grey-sided voles, Clethrionomys rufocanus, of Hokkaido: Spectral and principal components analyses. Philos Trans R Soc Lond B 351:867–875 Bjørnstad ON, Stenseth NC, Saitoh T (1999) Synchrony and scaling in dynamics of voles and mice in northern Japan. Ecology 80:622–637 Bogdziewicz M, Szymkowiak J (2016) Oak acorn crop and Google search volume predict Lyme disease risk in temperate Europe. Basic Appl Ecol 17:300–307 Chung-MacCoubrey A, Hagerman A, Kirkpatrick R (1997) Effect of tannins on digestion and detoxification activity in gray squirrels (Sciurus carolinensis). Physiol Zool 70:270–277 Dearing MD, Foley WJ, 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 Elias SP, Witham JW, Hunter ML (2004) Peromyscus leucopus abundance and acorn mast: Population fluctuation patterns over 20 years. J Mammal 85:743–747 Elias SP, Witham JW, Hunter ML (2006) A cyclic red-backed vole (Clethrionomys gapperi) population and seedfall over 22 years in Maineha. J Mammal 87:440–445 Elkinton J, Healy W, Buonaccorsi J, Boettner G, Hazzard A, Smith H, Liebhold A (1996) Interactions among gypsy moths, white-footed mice, and acorns. Ecology 77:2332–2342 Hagerman AE, Robbins CT (1993) Specificity of tannin-binding salivary proteins relative to diet selection by mammals. Can J Zool 71:628–633 Hansen LP, Batzli GO (1979) Influence of supplemental food on local-populations of Peromyscus leucopus. J Mammal 60:335–342 Hanski I (1990) Density dependence, regulation and variability in animal populations. Philos Trans R Soc Lond B 330:141–150 Henttonen H, McGuire AD, Hansson L (1985) Comparisons of amplitudes and frequencies (spectral analyses) of density variations in long-term data sets of Clethrionomys species. Ann Zool Fenn 22:221–227 Hoshizaki K, Miguchi H (2005) Influence of forest composition on tree seed predation and rodent responses: a comparison of monodominant and mixed temperate forests in Japan. In: Forget P-M, Lambert JE, Hulme PE, Vander Wall SB (eds) Seed Fate. CAB International, Wallingford, pp 253–267 Hulme P, Benkman C (2002) Granivory. In: Herrera C, Pellmyr O (eds) Plant-animal interactions: an evolutionary approach. Blackwell Publishing, Malden, pp 132–154 Janzen D (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492 Jędrzejewska B, Jędrzejewski W (1998) Predation in vertebrate communities: the Białowieża primeval forest as a case study. Springer-Verlag, New York Jensen TS (1982) Seed production and outbreaks of non-cyclic rodent populations in deciduous forests. Oecologia 54:184–192 Jensen LM, Wallis IR, Marsh KJ, Moore BD, Wiggins NL, Foley WJ (2014) Four species of arboreal folivore show differential tolerance to a secondary metabolite. Oecologia 176:251–258 Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447 Kelly D, Koenig WD, Liebhold AM (2008) An intercontinental comparison of the dynamic behavior of mast seeding communities. Popul Ecol 50:329–342 King CM (1983) The relationships between beech (Nothofagus sp.) seedfall and populations of mice (Mus musculus), and the demographic and dietary responses of stoats (Mustela erminea), in three new zealand forests. J Anim Ecol 52:141–166 Kitamura S, Murata G (1979) Coloured illustrations of woody plants of Japan. Hoikusha Publishing Co. Ltd, Osaka (in Japanese) Kohl KD, Weiss RB, Cox J, Dale C, Dearing MD (2014) Gut microbes of mammalian herbivores facilitate intake of plant toxins. Ecol Lett 17:1238–1246 Kohl KD, Stengel A, Dearing MD (2015) Inoculation of tannin-degrading bacteria into novel hosts increases performance on tannin-rich diets. Environ Microbiol 18:1720–1729 Krebs CJ (1999) Ecological methodology. Benjamin/Cummings, Menlo Park Marsh K, Foley W, Cowling A, Wallis I (2003) Differential susceptibility to Eucalyptus secondary compounds explains feeding by the common ringtail (Pseudocheirus peregrinus) and common brushtail possum (Trichosurus vulpecula). J Comp Physiol B 173:69–78 McArthur C, Hagerman A, Robbins C (1991) Physiological strategies of mammalian herbivores against plant defenses. In: Palo RT, Robbins CT (eds) Plant defenses against mammalian herbivory. CRC Press, Boca Raton, pp 103–114 McArthur C, Sanson G, Beal A (1995) Salivary proline-rich proteins in mammals—roles in oral homeostasis and counteracting dietary tannin. J Chem Ecol 21:663–691 McCracken K, Hunter ML Jr (1999) Relationships between seed fall of three tree species and Peromyscus leucopus and Clethrionomys gapperi during 10 years in an oak-pine forest. J Mammal 80:1288–1296 McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Phys A 151:5–28 Merritt JF (1981) Clethrionomys gapperi. Mammal Species 146:1–9 Miyaki M, Kikuzawa K (1988) Dispersal of Quercus mongolica acorns in a broadleaved deciduous forest. 2. Scatterhoarding by mice. For Ecol Manag 25:9–16 Mole S, Butler L, Iason G (1990) Defense against dietary tannin in herbivores—a survey for proline rich salivary proteins in mammals. Biochem Syst Ecol 18:287–293 Montgomery W (1989) Peromyscus and Apodemus; patterns of similarity in ecological equivalents. In: Kirkland GL Jr, Layne J (eds) Advances in the study of Peromyscus (Rodentia). Texas Tech University Press, Lubbock, pp 293–366 National Research Council (1995) Nutrient requirements of laboratory animals. National Academy Press, Washington Nemoto K, Osawa R, Hirota K, Ono T, Miyake Y (1995) An investigation of Gram-negative tannin-protein complex degrading bacteria in fecal flora of various mammals. J Vet Med Sci 57:921–926 Ofcarcik RP, Burns EE (1971) Chemical and physical properties of selected acorns. J Food Sci 36:576–578 Ohdachi S, Ishibashi Y, Iwasa M, Saitoh T (2009) The wild mammals in Japan. Shokado, Kyoto Ohta K (1984) Study on wild murid rodents in Hokkaido. Hokkaido University Press, Sapporo (Japanese) Ohta K, Takatsu S, Abe H (1959) Fluctuations of numbers in small mammals at Mt. Moiwa, Sapporo. I. Seasonal fluctuations of small mammal populations. Mem Fac Agric Hokkaido Univ Hokkaido 3:49–69 Osawa R, Sly L (1992) Occurrence of tannin-protein complex degrading Streptococcus sp. in feces of various animals. Syst Appl Microbiol 15:144–147 Osawa R, Bird P, Harbrow D, Ogimoto K, Seymour G (1993) Microbiological studies of the intestinal microflora of the koala, Phascolarctos cinereus. I. Colonisation of the caecal wall by tannin-protein-complex-degrading enterobacteria. Aust J Zool 41:599–609 Ostfeld RS, Jones CG, Wolff JO (1996) Of mice and mast. Bioscience 46:323–330 Ostfeld RS, Canham CD, Oggenfuss K, Winchcombe RJ, Keesing F (2006) Climate, deer, rodents, and acorns as determinants of variation in lyme-disease risk. PLoS Biol 4:1058–1068 Robbins CT, Hanley TA, Hagerman AE, Hjeljord O, Baker DL, Schwartz CC, Mautz WW (1987a) Role of tannins in defending plants against ruminants—reduction in protein availability. Ecology 68:98–107 Robbins C, Mole S, Hagerman A, Hanley TA (1987b) Role of tannins in defending plants against ruminants: reduction in dry matter digestion? Ecology 68:1606–1615 Robbins C, Hagerman A, Austin P (1991) Variation in mammalian physiological responses to a condensed tannin and its ecological implications. J Mammal 72:480–486 Robbins CT, Spalinger DE, Hoven W (1995) Adaptation of ruminants to browse and grass diets: are anatomical-based browser-grazer interpretations valid? Oecologia 103:208–213 Saitoh T, Stenseth NC, Bjørnstad ON (1998) The population dynamics of the vole Clethrionomys rufocanus in Hokkaido, Japan. Res Popul Ecol 40:61–76 Saitoh T, Osawa J, Takanishi T, Hayakashi S, Ohmori M, Morita T, Uemura S, Vik J, Stenseth N, Maekawa K (2007) Effects of acorn masting on population dynamics of three forest-dwelling rodent species in Hokkaido, Japan. Popul Ecol 49:249–256 Sasaki E, Shimada T, Osawa R, Nishitani Y, Spring S, 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 Schmidt KA, Ostfeld RS (2008) Numerical and behavioral effects within a pulse-driven system: consequences for shared prey. Ecology 89:635–646 Schmidt KA, Rush SA, Ostfeld RS (2008) Wood thrush nest success and post-fledging survival across a temporal pulse of small mammal abundance in an oak forest. J Anim Ecol 77:830–837 Schnurr JL, Ostfeld RS, Canham CD (2002) Direct and indirect effects of masting on rodent populations and tree seed survival. Oikos 96:402–410 Selås V, Framstad E, Spidsø T (2002) Effects of seed masting of bilberry, oak and spruce on sympatric populations of bank vole (Clethrionomys glareolus) and wood mouse (Apodemus sylvaticus) in southern Norway. J Zool 258:459–468 Servello FA, Kirkpatrick RL (1989) Nutritional-value of acorns for ruffed grouse. J Wildl Manag 53:26–29 Shimada T (2001) Nutrient compositions of acorns and horse chestnuts in relation to seed-hoarding. Ecol Res 16:803–808 Shimada T (2006) Salivary proteins as a defense against dietary tannins. J Chem Ecol 32:1149–1163 Shimada T, Saitoh T (2003) Negative effects of acorns on the wood mouse Apodemus speciosus. Popul Ecol 45:7–17 Shimada T, Saitoh T (2006) Re-evaluation of the relationship between rodent populations and acorn masting: a review from the aspect of nutrients and defensive chemicals in acorns. Popul Ecol 48:341–352 Shimada T, Saitoh T, Matsui T (2004) Does acclimation reduce the negative effects of acorn tannins in the wood mouse Apodemus speciosus? Acta Theriol 49:203–214 Shimada T, Saitoh T, Sasaki E, Nishitani Y, Osawa R (2006) 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 Shimada T, Nishii E, Saitoh T (2011) Interspecific differences in tannin intakes of forest-dwelling rodents in the wild revealed by a new method using fecal proline content. J Chem Ecol 37:1277–1284 Spiegelhalter D, Thomas A, Best N, Lunn D (2003) WinBUGS user manual (version 1.4.). MRC Biostatistics Unit, Institute of Public Health, Cambridge Stenseth NC, Bjørnstad ON, Saitoh T (1996) A gradient from stable to cyclic populations of Clethrionomys rufocanus in Hokkaido, Japan. Proc R Soc Lond B 263:1117–1126 Tatsukawa K, Murakami O (1976) On the food utilization of the Japanese wood mouse Apodemus speciosus (Mammalia: Muridae). Physiological Ecology Japan 17:133–144 Tersago K, Verhagen R, Servais A, Heyman P, Ducoffre G, Leirs H (2009) Hantavirus disease (nephropathia epidemica) in Belgium: effects of tree seed production and climate. Epidemiol Infect 137:250–256 Wada N (1993) Dwarf bamboos affect the regeneration of zoochorous trees by providing habitats to acorn-feeding rodents. Oecologia 94:403–407 Watts C (1969) The regulation of wood mouse Apodemus silvaticus numbers in Wytham Woods, Berkshire. J Anim Ecol 38:285–304 Wolff J (1996) Population fluctuations of mast-eating rodents are correlated with production of acorns. J Mammal 77:850–856