Reproduction, relative abundance, and variability in North American arvicoline rodent populations
Keywords:
Breeding seasons, litter sizes, population variability, reproductive potential, variability in abundance.Abstract
The ecological and life history characteristics of North American arvicoline rodents vary greatly. A general model suggests that changes in reproduction, as a response to changes in climatic harshness and habitat type, likely affect variation in relative abundance of arvicoline populations. Previous work indicated that variability in abundance does not always increase with mean litter size or with latitude, but litter size does tend to increase as the length of the breeding season decreases. I therefore propose the reproductive potential (RP) hypothesis which states that under favorable conditions, populations with higher reproductive potential can grow more rapidly and can reach higher densities during the breeding season, which leads to greater variability in abundance because very high populations eventually decline to low densities. I define reproductive potential as the maximum number of offspring a typical female could produce during a year and calculate it as the product of mean litter size (m) and length of the breeding season in weeks (b) divided by 3 (RP = mb/3). I then review the problems associated with estimation of the necessary parameters and indicate my criteria for accepting data. To test the RP hypothesis I correlate RP to a measure of variability in abundance for populations with at least 10 years of data, and I compare populations of the same or different arvicoline species at the same and different sites. Most results did not support the RP hypothesis. However, three species had different litter sizes in habitats with different vegetation, and all three reached higher maximum densities where reproductive potential was greater.References
Batzli, G. O. 1985. Nutrition. Pp. 779-811, in Biology of New World Microtus (Tamarin, R. H., ed.). Special Publications No 8, American Society of Mammalogists. Lawrence, U.S.A.
BATZLI, G. O. 1992. Dynamics of small mammal populations: a review. Pp. 831-850, in Wildlife 2001: Populations (McCullough, D. R., and R. H. Barrett, eds.). Elsevier Applied Science. New York, U.S.A.
BATZLI, G. O., AND H.-J. G. JUNG. 1980. Nutritional ecology of microtine rodents: resource utilization near Atakasook, Alaska. Arctic and Alpine Research 12:483-499.
BATZLI, G. O., ET AL. 1980. The herbivore-based trophic system. Pp. 335-410, in An arctic ecosystem: the coastal tundra at Barrow, Alaska (Brown, J., P. Miller, and F. Bunnell, eds.). Dowden, Hutchinson, and Ross. Stroudsburg, U.S.A.
BEER, J. R., C. F. MACLEOD, AND L. D. FRENZEL. 1957. Prenatal survival and loss in some cricetid rodents. Journal of Mammalogy 38:392-401.
BOONSTRA, R., AND C. J. KREBS. 2006. Population limitation of the northern red-backed vole in the boreal forests of northern Canada. Journal of Animal Ecology 75:1269-1284.
BOONSTRA, R., AND C. J. KREBS. 2012. Population dynamics of red-backed voles (Myodes) in North America. Oecologia 168:601-620.
BRADY, M. J., AND N. A. SLADE. 2004. Long-term dynamics of a grassland rodent community. Journal of Mammalogy 85:552-561.
BROOKS, R. T., H. R. SMITH, AND W. M. HEALEY. 1998. Small-mammal abundance at three elevations on a mountain in central Vermont, USA: a sixteen-year record. Forest Ecology and Management 110:181-193.
CHARNOV, E. L., AND S. K. M. ERNEST. 2006. The offspring-size/clutch trade-off in mammals. American Naturalist 167:578-582.
Cole, F. R. and G. O. Batzli. 1978. The influence of supplemental feeding on a population of the prairie vole Micrtotus ochrogaster. Journal of Mammalogy 58:809-819.
COLE, F. R., AND G. O. BATZLI. 1979. Nutrition and population dynamics of the prairie vole, Microtus ochrogaster, in central Illinois. Journal Animimal Ecology 48:455-470.
COLLETT, R. 1911-1912. Norges Pattedyr. Kristiania, Norway.
DEJACO, C. E., AND G. O. BATZLI. 2013. Palatability of plants to small mammals in nonnative grasslands of east-central Illinois. Journal of Mammalogy 94:427-435.
DESY, E. A., AND G. O. BATZLI. 1989. Effects of food availability and predation on prairie vole demography: a field experiment. Ecology 70:411-421.
ELIAS, S. P., J. W. WITHAM, AND M. L. HUNTER, JR. 2006. A cyclic red-backed vole population and seedfall over 22 years in Maine. Journal of Mammalogy 87:440-445.
ELTON, C. 1924. Periodic fluctuations in the number of animals: their causes and effects. British Journal of Experimental Biology 2:119-163.
ERRINGTON, P. 1946. Predation and vertebrate populations. Quarterly Review of Biology 21:144-177.
ERRINGTON, P. 1951. Concerning fluctuations in populations of the prolific and widely distributed muskrat. American Naturalist 85:273-292.
FITCH, H. S. 1957. Aspects of reproduction and development in the prairie vole (Microtus ochrogaster). University of Kansas Miscellaneous Publications of the Museum of Natural History 10:129-161.
FITCH, H. S., V. R. FITCH, AND W. D. KETTLE. 1984. Reproduction, population changes and interactions of small mammals on natural area in northeastern Kansas. Occasional Papers of the Museum of Natural History of Kansas 109:1-37.
FORBES, K. M., ET AL. 2014. Diet quality limits summer growth of field vole populations. Plos Ones 9:e91113.
FRYXELL, J. M., JET AL. 1998. Long-term dynamics of small mammal populations. Ecology 79:213-225.
FULLER, W. A. 1969. Changes in the numbers of three species of small rodent near Great Slave Lake, N.W.T., Canada, 1964-1967, and their significance for general population theory. Annales Zoologici Fennici 6:113-144.
FULLER, W. A. 1985. Demography of Clethriomomys gapperi and parapatric C. rutilus and sympatric Peromyscus leucopus in northern Canada. Annales Zoologici Fennici 22:229-241.
GASHWILER, J. S. 1970. Plant and mammal changes on a clearcut in west-central Oregon. Ecology 51: 1018-1026.
GASHWILER, J. S. 1977. Reproduction of the California red-backed vole in western Oregon. Northwest Science 51:56-59.
GETZ, L. L. ET AL. 2001. Twenty-five years of population fluctuations of Microtus ochrogaster and M. pennsylvanicus in three habitats in east-central Illinois. Journal of Mammalogy 82:22-34.
GIFFORD, C. L., AND R. WHITEBREAD. 1951. Mammal survey of south central Pennsylvania. Pennsylvania Game Commission. Harrisburg, U.S.A.
GILBERT, B. S., AND C. J. KREBS. 1991. Population dynamics of Clethrionomys and Peromyscus in southwestern Yukon 1973-1989. Holarctic Ecology 14:250-259.
GRANT, P. R. 1976. An 11-year study of small mammal populations at Mont St. Hilaire, Quebec. Canadian Journal of Zoology 54:2156-2173.
GRIMM, W. C., AND R. WHITEBREAD. 1952. Mammal survey of western Pennsylvania. Pennsylvania Game Commission. Harrisburg, U.S.A.
HANSSON, L., AND H. HENTTONEN. 1985a. Gradients in density variations of small rodents: the importance of latitude and snow cover. Oecologia 67:397-402.
HANNSON, L., AND H. HENTTONEN. 1985b. Regional differences in cyclicity and reproduction in Clethrionomys species: Are they related? Annales Zoologici Fennici 22:277-288.
HASLER, J. F. 1975. A review of reproduction and sexual maturation in the microtine rodents. The Biologist 57:52-86.
HEATH, J. P. 2006. Quantifying temporal variability in population abundance. Oikos 115:573- 581.
INNES, D. G. 1978. A reexamination of litter size in some North American microtines. Canadian Journal of Zoology 56:1488-1496.
INNES, D. G., AND J. S. MILLAR. 1994. Life histories of Clethrionomys and Microtus (Microtinae). Mammal Review 24:179-207.
IVERSON, S. L., AND B. N. TURNER. 1976. Small mammal radioecology: natural reproductive patterns of seven species. Atomic Energy of Canada Limited Report, AECL-5393.
KELLER, B. L. 1985. Reproductive patterns. Pp. 725-778, in Biology of New World Microtus. Special Publication No. 8, American Society of Mammalogists, Lawrence, Kansas.
KELLER, B. L., AND C. J. KREBS. 1970. Microtus population biology. III. Reproductive changes in fluctuating populations of M. ochrogaster and M. pennsylvanicus in southern Indiana 1965-1967. Ecological Monographs 40:263-294.
KREBS, C. J. 2013. Population fluctuations in rodents. The University of Chicago Press. Illinois, U.S.A.
KREBS, C. J., AND I. WINGATE. 1985. Population fluctuations in the small mammals of the Kluane region, Yukon Territory. Canadian Field Naturalist 99:51-61.
KREFTING, L. W., AND C. E. AHLGREN. 1974. Small mammals and vegetation changes after fire in a mixed conifer-hardwood forest. Ecology 55:1391-1398.
KROHNE, D. T. 1980. Intraspecific litter size variation in Microtus californicus. II. Variation between populations. Evolution 34:1174-1182.
KROHNE, D. T. 1982. The demography of low-litter-size populations of Microtus californicus. Canadian Journal of Zoology 60:368-374.
LACK, D. 1954. The natural regulation of animal numbers. Oxford University Press. London, U. K.
LIDICKER, W. Z., JR. 1973. Regulation of numbers in an island population of the California vole, a problem of community dynamics. Ecological Monographs 43:271-302.
LORD, R. D., JR. 1960. Litter size and latitude in North American mammals. American Midland Naturalist 64:488-499.
MARTELL, A. M., AND W. A. FULLER. 1979. Comparative demography of Clethrionomys rutilus in taiga and tundra in the low arctic. Canadian Journal of Zoology 57:2106-2120.
MERRITT, J. F., M. LIMA, AND F. BOZINOVIC. 2001. Seasonal regulation in fluctuating small mammal populations: feedback structure and climate. Oikos 94:505-514.
MILLAR, J. S. 1977. Adaptive features of mammalian reproduction. Evolution 31:370-386.
MILLAR, J. S. 1981. Pre-partum reproductive characteristic of eutherian mammals. Evolution 35:1149-1163.
MIHOK, S. 1984. Life history profiles of boreal meadow voles (Microtus pennsylvanicus). Pp. 91-102, in Winter ecology of mammals (Merritt, J. F., ed.). Carnegie Museum of Natural History Special Publication No. 10. Pittsburgh, U.S.A.
MIHOK, S., B. SCHWARTZ, AND S. L. IVERSON. 1985a. Ecology of red-backed voles (Clethrionomys gapperi) on gradient of gamma radiation. Annales Zoologici Fennici 22:257-271.
MIHOK, S., B. N. TURNER, AND S. L. IVERSON. 1985b. The characterization of vole population dynamics. Ecological Monographs 55:399-420.
NEGUS, N. C., P. J. BERGER, AND L. G. FORSLUND. 1977. Reproductive strategies of Microtus montanus. Journal of Mammalogy 58:347-353.
OLI, M. K. 2004. The fast-slow continuum and mammalian life-history patterns: an empirical evaluation. Basic and Applied Ecology 5:449-463.
PATRIC, E. F. 1962. Reproductive characteristics of the red-backed vole during years of different densities. Journal of Mammalogy 43:200-205.
PEARSON, O. P. 1964. Carnivore-mouse predation: an example of its intensity and bioenergetics. Journal of Mammalogy 45:177-188.
PEARSON, O. P. 1966. The prey of carnivores during one cycle of mouse abundance. Journal of Animal Ecology 35:217-233.
PEARSON, O. P. 1971. Additional measurement of the impact of carnivores on California voles (Microtus californicus). Journal of Mammalogy 52:41-49.
PERRIN, M. R. 1979. The roles of reproduction, survival, and territoriality in the seasonal dynamics of Clethrionomys gapperi populations. Acta Theriologica 24:475-500.
PINTER, A. J. 1986. Population dynamics and litter size of the montane vole, Microtus montanus. Canadian Journal of Zoology 64:1487-1490.
PITELKA, F. A. 1973. Cyclic pattern in lemming populations near Barrow, Alaska. Pp. 199-215, in Alaskan arctic tundra (Britton, M. E., ed.). Arctic Institute of North America Technical Paper No. 25. Washington, U.S.A.
PITELKA, F. A., AND G. O. BATZLI. 1993. Distribution, abundance and habitat use by lemmings on the north slope of Alaska. Pp. 213-236, in The biology of lemmings (Stenseth, N. C., and R. A. Ims, eds.). Linnaean Society Symposium Series No. 15, Academic Press. London, U.K.
PITELKA, F. A., AND G. O. BATZLI. 2018. Demography and condition of brown lemmings (Lemmus trimucronatus) during cyclic density fluctuations near Barrow, Alaska. Annales Zoologici Fennici 55:187-236.
SMITH, A. 1988. Patterns of pika (Genus Ochotona) life history variation. Pp. 233-256, in Evolution of life histories of mammals: theory and pattern (Boyce, M. S., ed.). Yale University Press. New Haven, U.S.A.
SMITH, C. C., AND S. D. FRETWELL. 1974. The optimal balance between size and number of offspring. American Naturalist 108:499-506.
SPENCER, A. W., AND H. W. STEINHOFF. 1968. An explanation of geographic variation in litter size. Journal of Mammalogy 49:281-286.
STENSETH, N. C., O. N. BJORNSTAD, AND T. SAITOH. 1996. A gradient from stable to cyclic populations of Clethrionomys rufocanus in Hokkaido, Japan. Proceedings of the Royal Society of London B 263:1117-1126.
STENSETH, N. C., AND E. FRAMSTAD. 1980. Reproductive effort and optimal reproductive rates in small rodents. Oikos 34:23-34.
STENSETH, N. C., T. O. GUSTAFSSON, L. HANSSON, AND K. I. UGLAND. 1985. On the evolution of reproductve rates in microtine rodents. Ecology 66:1795-1808.
STENSETH, N. C., AND R. A. IMS. 1993. The history of lemming research: from the Nordic sagas to the biology of lemmings. Pp. 3-34, in The biology of lemmings (Stenseth, N. C., and R. A. Ims, eds.) Linnaean Society Symposium Series No. 15, Academic Press. London, U. K.
SULLIVAN, T. P., D. S. SULLIVAN, R. BOONSTRA, C. J. KREBS, AND A. VYSE. 2017. Mechanisms of population limitation in the southern red-backed vole in conifer forests of western North America: insights from a long-term study. Journal of Mammalogy 98:1367-1378.
SULLIVAN, T. P., D. S. SULLIVAN, R. BOONSTRA, AND C. J. KREBS. 2021. Population change and limitation in the montane vole (Microtus montanus) in perennial old-field grasslands: insights from a long-term study. Journal of Mammalogy 102:doi.org/10.1093/jmamm/gyaa/55
TAMARIN, R. H. 1977a. Reproduction in the island beach vole, Microtus breweri, and the mainland meadow vole, Microtus pennsylvanicus, in southeastern Massachusetts. Journal of Mammalogy 58:36-548.
TAMARIN, R. H. 1977b. Demography of the beach vole (Microtus breweri) and the meadow vole (Microtus pennsylvanicus) in southeastern Massachusetts. Ecology 58:1310-1321.
TAMARIN, R. H., G. H. ADLER, M. SHERIDAN, AND K. ZWICKER. 1987. Similarity of spring population densities of the island beach vole (Microtus breweri), 1972-1986. Canadian Journal of Zoology 65:2039-2041.
TURCHIN, P. 2003. Complex population dynamics: a theoretical/empirical synthesis. Monographs in Population Biology No. 35, Princeton University Press. Princeton, U.S.A.
WILLIAMS, G. 1967. Natural selection, the costs of reproduction, and a refinement of Lack’s principle. American Naturalist 100:687-690.
WILSON, D. E., T. E. LACHER, JR., AND R. A. MITTERMEIER (EDS.). 2017. Family Cricetidae, Subfamily Arvicolinae. Pp. 288-353, in Handbook of the mammals of the world, Volume 7, Rodents II. Lynx Edicions. Barcelona, Spain.
WOLF, J., AND W. Z. LIDICKER, JR. 1980. Population ecology of the taiga vole, Microtus xanthognathus, in interior Alaska. Canadian Journal of Zoology 58:1800-1812.
WRIGLEY, R. E. 1969. Ecological notes on the mammals of southern Quebec. Canadian Field Naturalist 83:201-211.
Published
Issue
Section
License
THERYA is based on its open access policy allowing free download of the complete contents of the magazine in digital format. It also authorizes the author to place the article in the format published by the magazine on your personal website, or in an open access repository, distribute copies of the article published in electronic or printed format that the author deems appropriate, and reuse part or whole article in own articles or future books, giving the corresponding credits.
