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DEMOGRAPHY OF A POPULATION COLLAPSE: THE NORTHERN IDAHO GROUND SQUIRREL (SPERMOPHILUS BRUNNEUS BRUNNEUS)

2002; Wiley; Volume: 83; Issue: 10 Linguagem: Inglês

10.1890/0012-9658(2002)083[2816

1939-9170

Paul W. Sherman, Michael C. Runge,

Wildlife Ecology and Conservation

EcologyVolume 83, Issue 10 p. 2816-2831 Regular Article DEMOGRAPHY OF A POPULATION COLLAPSE: THE NORTHERN IDAHO GROUND SQUIRREL (SPERMOPHILUS BRUNNEUS BRUNNEUS) Paul W. Sherman, Paul W. Sherman Department of Neurobiology and Behavior, W307 Mudd Hall, Cornell University, Ithaca, New York 14853 USA E-mail: [email protected]Search for more papers by this authorMichael C. Runge, Michael C. Runge USGS Patuxent Wildlife Research Center, 11510 American Holly Drive, Laurel, Maryland 20708 USASearch for more papers by this author Paul W. Sherman, Paul W. Sherman Department of Neurobiology and Behavior, W307 Mudd Hall, Cornell University, Ithaca, New York 14853 USA E-mail: [email protected]Search for more papers by this authorMichael C. Runge, Michael C. Runge USGS Patuxent Wildlife Research Center, 11510 American Holly Drive, Laurel, Maryland 20708 USASearch for more papers by this author First published: 01 October 2002 https://doi.org/10.1890/0012-9658(2002)083[2816:DOAPCT]2.0.CO;2Citations: 49 Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Abstract We studied the demography of a population of Northern Idaho ground squirrels (Spermophilus brunneus brunneus) in Adams County, Idaho. The population was completely censused yearly from 1987 to 1999, during which time it declined from 272 to 10 animals. The finite population growth rate, based on a Leslie matrix model of average life-history parameters, was only 0.72 (i.e., significantly <1.0). Growth rate was more sensitive to proportional changes in juvenile female survival than to any other single life-history parameter. Comparisons with self-sustaining populations of closely related ground squirrel species revealed that juvenile survival and breeding rates of yearling females were anomalously low. We believe that the ultimate cause of the population's collapse was inadequacy of food resources, particularly seeds, due to drying of the habitat and changes in plant species composition, likely the result of fire suppression and grazing. No “rescue” by immigration occurred, probably because S. b. brunneus seldom disperse long distances and fire suppression has allowed conifers to encroach on inhabited meadows, shrinking them and closing dispersal routes. The proximate cause of the population's collapse was mortality of older breeding females, which reduced the mean age of breeders. Younger females had lower average pregnancy rates and litter sizes. To place our results in context we developed a new, general classification of anthropogenic population declines, based on whether they are caused by changes in the means of the life-history parameters (blatant disturbances), their variances (inappropriate variations), or the correlations among them (evolutionary traps). Many S. b. brunneus populations have disappeared in recent years, apparently due to blatant disturbances, especially loss of habitat and changes in food-plant composition, resulting in inadequate prehibernation nutrition and starvation overwinter. In addition, our study population may have been caught in an evolutionary trap, because the vegetational cues that could potentially enable the animals to adjust reproduction to the anticipated food supply no longer correlate with availability of fat-laden seeds. Literature Cited Armitage, K. B. 2000. The evolution, ecology, and systematics of marmots. Oecologia Montana 9: 1– 18. Arnason, A. N., and K. H. Mills . 1981. Bias and loss of precision due to tag loss in Jolly-Seber estimates for mark–recapture experiments. Canadian Journal of Fisheries and Aquatic Sciences 38: 1077– 1095. Arno, S. F. 1980. Forest fire history in the northern Rockies. Journal of Forestry 78: 460– 465. Arno, S. F., and G. E. Gruell . 1983. Fire history at the forest–grassland ecotone in southwestern Montana. Journal of Range Management 36: 332– 336. Arno, S. F., and G. E. Gruell . 1986. Douglas-fir encroachment into mountain grasslands in southwestern Montana. Journal of Range Management 39: 272– 275. Bachman, G. C. 1994. Food restriction effects on the body composition of free-living ground squirrels (Spermophilus beldingi), variance, ontogeny, and the aerobic capacity model of endothermy. Physiological Zoology 67: 756– 770. Barrett, S. W. 1988. Fire suppression's effects on forest succession within a central Idaho wilderness. Western Journal of Applied Forestry 3: 76– 80. Boag, D. A., and J. O. Murie . 1981. Population ecology of Columbian ground squirrels in southwestern Alberta. Canadian Journal of Zoology 59: 2230– 2240. Brault, S., and H. Caswell . 1993. Pod-specific demography of killer whales (Orcinus orca). Ecology 74: 1444– 1454. Bronson, M. T. 1979. Altitudinal variation in the life history of the golden-mantled ground squirrel (Spermophilus lateralis). Ecology 60: 272– 279. Brown, J. H., and A. Kodric-Brown . 1977. Turnover rates in insular biogeography: effect of immigration on extinction. Ecology 58: 445– 449. Buck, C. L., and B. M. Barnes . 1999. Annual cycle of body composition and hibernation in free-living arctic ground squirrels. Journal of Mammalogy 80: 430– 442. Bunnell, F. L. 1995. Forest-dwelling vertebrate faunas and natural fire regimes in British Columbia: patterns and implications for conservation. Conservation Biology 9: 636– 644. Burnham, K. P., and D. R. Anderson . 1998. Model selection and inference: a practical information-theoretic approach. Springer-Verlag, New York, New York, USA. Bushberg, D. M., and W. G. Holmes . 1985. Sexual maturity in male Belding's ground squirrels: influence of body weight. Biology of Reproduction 33: 302– 308. Butler, D. R. 1986. Conifer invasion of subalpine meadows, central Lemhi mountains, Idaho. Northwest Science 60: 166– 173. Byrom, A. E., and C. J. Krebs . 1999. Natal dispersal of juvenile arctic ground squirrels in the boreal forest. Canadian Journal of Zoology 77: 1048– 1059. Cade, T. J., J. H. Enderson, C. G. Thelander, and C. M. White . 1988. The role of organochlorine pesticides in Peregrine population changes. Pages 463–468 in T. J. Cade, J. H. Enderson, C. G. Thelander, and C. M. White, editors. Peregrine Falcon populations: their management and recovery. The Peregrine Fund, Boise, Idaho, USA. Caswell, H. 1989. Matrix population models: construction, analysis, and interpretation. Sinauer Associates, Sunderland, Massachusetts, USA. Caswell, H. 2001. Matrix population models: construction, analysis, and interpretation. Second edition. Sinauer Associates, Sunderland, Massachusetts, USA. Caswell, H., M. Fujiwara, and S. Brault . 1999. Declining survival probability threatens the North Atlantic right whale. Proceedings of the National Academy of Sciences (USA) 96: 3308– 3313. Caughley, G. 1994. Directions in conservation biology. Journal of Animal Ecology 63: 215– 244. Charlesworth, B. 1980. Evolution in age structured populations. Cambridge University Press, New York, New York, USA. Clark, J. R. 1998. Endangered and threatened wildlife and plants; proposed threatened status for the northern Idaho ground squirrel. Federal Register 63 55 13825– 13832. Clark, J. R. 2000. Endangered and threatened wildlife and plants; determination of threatened status for the northern Idaho ground squirrel. Federal Register 65 66 17779– 17786. Cohen, D. 1966. Optimizing reproduction in a randomly varying environment. Journal of Theoretical Biology 12: 119– 129. Cohen, D. 1967. Optimizing reproduction in a randomly varying environment when a correlation may exist between the conditions at the time a choice has to be made and the subsequent outcome. Journal of Theoretical Biology 16: 1– 14. Cohen, D. 1968. A general model of optimal reproduction in a randomly varying environment. Journal of Ecology 56: 219– 228. Collins, S. L. 1987. Interaction of disturbances in tallgrass prairie: a field experiment. Ecology 68: 1243– 1250. Crane, M. F., and W. C. Fischer . 1986. Fire ecology of the forest habitat types of central Idaho. General Technical Report INT-218. USDA Forest Service, Intermountain Research Station, Ogden, Utah, USA. Diamond, J. M. 1989. Overview of recent extinctions. Pages 37–41 in D. Western and M. Pearl, editors. Conservation for the twenty-first century. Oxford University Press, New York, New York, USA. Dobson, F. S., and K. D. Kjelgaard . 1985. The influence of food resources on life history in Columbian ground squirrels. Canadian Journal of Zoology 63: 2105– 2109. Dobson, F. S., and J. O. Murie . 1987. Interpretation of intraspecific life history patterns: evidence from Columbian ground squirrels. American Naturalist 129: 382– 397. Dobson, F. S., and M. K. Oli . 2001. The demographic basis of population regulation in Columbian ground squirrels. American Naturalist 158: 236– 247. Dyni, E. J., and E. Yensen . 1996. Dietary similarity of sympatric Idaho and Columbian ground squirrels (Spermophilus brunneus and S. columbianus). Northwest Science 70: 99– 108. Fagerstone, K. A. 1988. The annual cycle of Wyoming ground squirrels in Colorado. Journal of Mammalogy 69: 678– 687. Fieller, E. C. 1940. The biological standardization of insulin. Journal of the Royal Statistical Society, Supplement 7: 1– 64. Fleischner, T. L. 1994. Ecological costs of livestock grazing in western North America. Conservation Biology 8: 629– 644. Florant, G. L. 1998. Lipid metabolism in hibernators: the importance of essential fatty acids. American Zoologist 38: 331– 340. Frank, C. L., E. S. Dierenfeld, and K. B. Storey . 1998. The relationship between lipid peroxidation, hibernation, and food selection in mammals. American Zoologist 38: 341– 349. Fujiwara, M., and H. Caswell . 2001. Demography of the endangered North Atlantic right whale. Nature 414: 537– 541. Gaillard, J.-M., M. Festa-Bianchet, N. G. Yoccoz, A. Loison, and C. Toïgo . 2000. Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics 31: 367– 393. Gates, J. E., and L. W. Gysel . 1978. Avian nest dispersion and fledging success in field–forest ecotones. Ecology 59: 871– 883. Gavin, T. A., P. W. Sherman, E. Yensen, and B. May . 1999. Population genetic structure of the Northern Idaho ground squirrel (Spermophilus brunneus brunneus). Journal of Mammalogy 80: 156– 168. Goodman, D. 1981. Life history analysis of large mammals. Pages 415–436 in C. W. Fowler and T. D. Smith, editors. Dynamics of large mammal populations. John Wiley and Sons, New York, New York, USA. Green, J. E. 1977. Population regulation and annual cycles of activity and dispersal in the Arctic ground squirrel. M.A. thesis. University of British Columbia, Vancouver, British Columbia, Canada. Hafner, D. J. 1984. Evolutionary relationships of the Nearctic Sciuridae. Pages 3–23 in J. O. Murie and G. R. Michener, editors. The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, Nebraska, USA. Harniss, R. O., and R. B. Murray . 1973. 30 years of vegetal change following burning of sagebrush–grass range. Journal of Range Management 26: 322– 325. Hedrick, P. W., R. C. Lacy, F. W. Allendorf, and M. E. Soulé . 1996. Directions in conservation biology: comments on Caughley. Conservation Biology 10: 1312– 1320. Hoffmann, R. S., C. G. Anderson, R. W. Thorington, Jr, and L. R. Heaney . 1993. Family Sciuridae. Pages 419–465 in D. E. Wilson and D. M. Reeder, editors. Mammal species of the world. Smithsonian Institution Press, Washington, D.C., USA. Holekamp, K. E. 1984. Dispersal in ground-dwelling Sciurids. Pages 297–320 in J. O. Murie and G. R. Michener, editors. The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, Nebraska, USA. Hoogland, J. L. 1995. The black-tailed prairie dog. University of Chicago Press, Chicago, Illinois, USA. Hubbs, A. H., and R. Boonstra . 1997. Population limitation in Arctic ground squirrels: effects of food and predation. Journal of Animal Ecology 66: 527– 541. Humphrey, L. D. 1984. Patterns and mechanisms of plant succession after fire on Artemisia–grass sites in southeastern Idaho. Vegetatio 57: 91– 101. Inouye, D. W., B. Barr, K. B. Armitage, and B. D. Inouye . 2000. Climate change is affecting altitudinal migrants and hibernating species. Proceedings of the National Academy of Sciences (USA) 97: 1630– 1633. Kendall, W. L., J. D. Nichols, and J. E. Hines . 1997. Estimating temporary emigration using capture–recapture data with Pollock's robust design. Ecology 78: 563– 578. Krebs, C. J. 1978. Ecology: the experimental analysis of distribution and abundance. Second edition. Harper and Row, New York, New York, USA. Lebreton, J.-D., K. P. Burnham, J. Clobert, and D. R. Anderson . 1992. Modeling survival and testing biological hypotheses using marked animals: a unified approach with case studies. Ecological Monographs 62: 67– 118. Leege, T. A., D. J. Herman, and B. Zamora . 1981. Effects of cattle grazing on mountain meadows in Idaho. Journal of Range Management 34: 324– 328. Leslie, P. H. 1945. The use of matrices in certain population mathematics. Biometrika 33: 183– 212. Lewontin, R. C., and D. Cohen . 1969. On population growth in a randomly varying environment. Proceedings of the National Academy of Sciences (USA) 62: 1056– 1060. Link, W. A. 1999. Modeling pattern in collections of parameters. Journal of Wildlife Management 63: 1017– 1027. Manly, B. F. J. 1997. Randomization, bootstrap, and Monte Carlo methods. Second edition. Chapman and Hall, London, UK. Mathworks. 1999. MATLAB: the language of technical computing, using MATLAB. Version 5. The Mathworks, Natick, Massachusetts, USA. May, R. M. 1994. Graeme Caughley and the emerging science of conservation biology. Trends in Ecology and Evolution 9: 368– 369. McCullagh, P., and J. A. Nelder . 1989. Generalized linear models. Chapman and Hall, London, UK. Michener, G. R. 1984. Age, sex, and species differences in the annual cycles of ground-dwelling sciurids: implications for sociality. Pages 81–107 in J. O. Murie and G. R. Michener, editors. The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, Nebraska, USA. Michener, G. R. 1985. Chronology of reproductive events for female Richardson's ground squirrels. Journal of Mammalogy 66: 280– 288. Michener, G. R. 1989a. Sexual differences in interyear survival and life-span of Richardson's ground squirrels. Canadian Journal of Zoology 67: 1827– 1831. Michener, G. R. 1989b. Reproductive effort during gestation and lactation by Richardson's ground squirrels. Oecologia 78: 77– 86. Michener, G. R., and L. Locklear . 1990. Differential costs of reproductive effort in male and female Richardson's ground squirrels. Ecology 71: 855– 868. Mueggler, W. F. 1962. Range resources and management problems in northern Idaho and northeastern Washington. General Technical Report INT-68. USDA Forest Service, Intermountain Research Station, Ogden, Utah, USA. Murie, J. O. 1985. A comparison of life history traits in two populations of Columbian ground squirrels in Alberta, Canada. Acta Zoologica Fennica 173: 43– 45. Neuhaus, P., and N. Pelletier . 2001. Mortality in relation to season, age, sex, and reproduction in Columbian ground squirrels (Spermophilus columbianus). Canadian Journal of Zoology 79: 465– 470. Nichols, J. D., W. Conley, B. Batt, and A. R. Tipton . 1976. Temporally dynamic reproductive strategies and the concept of r-selection and K-selection. American Naturalist 110: 995– 1005. Nichols, J. D., J. E. Hines, J.-D. Lebreton, and R. Pradel . 2000. Estimation of contributions to population growth: a reverse-time capture–recapture approach. Ecology 81: 3362– 3376. Nisbet, I. C. T., J. S. Hatfield, W. A. Link, and J. A. Spendelow . 1999. Predicting chick survival and productivity of Roseate Terns from data on early growth. Waterbirds 22: 90– 97. Nunes, S., P. A. Zugger, A. L. Engh, K. O. Reinhart, and K. E. Holekamp . 1997. Why do female Belding's ground squirrels disperse away from food resources? Behavioral Ecology and Sociobiology 40: 199– 207. Oli, M. K., and B. Zinner . 2001. Partial life-cycle analysis: a model for birth-pulse populations. Ecology 82: 1180– 1190. Olson, G. S., and B. Van Horne . 1998. Dispersal patterns of juvenile Townsend's ground squirrels in southwestern Idaho. Canadian Journal of Zoology 76: 2084– 2089. Patton, B. D., M. Hironaka, and S. C. Bunting . 1988. Effect of burning on seed production of bluebunch wheatgrass, Idaho fescue, and Columbia needlegrass. Journal of Range Management 41: 232– 234. Pfeifer, S. R. 1982. Variability in reproductive output and success of Spermophilus elegans ground squirrels. Journal of Mammalogy 63: 284– 289. Phillips, J. A. 1984. Environmental influences on reproduction in the golden-mantled ground squirrel. Pages 108–124 in J. O. Murie and G. R. Michener, editors. The biology of ground-dwelling squirrels. University of Nebraska Press, Lincoln, Nebraska, USA. Pollock, K. H. 1981. Capture–recapture models allowing for age-dependent survival and capture rates. Biometrics 37: 521– 529. Pradel, R. 1996. Utilization of capture–mark–recapture for the study of recruitment and population growth rate. Biometrics 52: 703– 709. Promislow, D. E. L., and P. H. Harvey . 1990. Living fast and dying young: a comparative analysis of life-history variation among mammals. Journal of Zoology (London) 220: 417– 437. Rieger, J. F. 1996. Body size, litter size, timing of reproduction, and juvenile survival in the Uinta ground squirrel, Spermophilus armatus. Oecologia 107: 463– 468. Risebrough, R. W., and D. B. Peakall . 1988. The relative importance of the several organochlorines in the decline of Peregrine Falcon populations. Pages 449–462 in T. J. Cade, J. H. Enderson, C. G. Thelander, and C. M. White, editors. Peregrine Falcon populations: their management and recovery. The Peregrine Fund, Boise, Idaho, USA. Rummell, R. S. 1951. Some effects of livestock grazing on ponderosa pine forest and range in central Washington. Ecology 32: 594– 607. Sæther, B.-E., T. H. Ringsby, and E. Roskaft . 1996. Life history variation, population processes and priorities in species conservation: toward a reunion of research paradigms. Oikos 77: 217– 226. SAS Institute. 1989. SAS/STAT user's guide. Version 6, Fourth edition, Volume 2. SAS Institute, Cary, North Carolina, USA. SAS Institute. 1993. SAS technical report P-243, SAS/STAT software: the GENMOD procedure. Release 6.09. SAS Institute, Cary, North Carolina, USA. Schlaepfer, M. A., M. C. Runge, and P. W. Sherman . 2002. Ecological and evolutionary traps. Trends in Ecology and Evolution 17:474–480. Schwartz, O. A., K. B. Armitage, and D. Van Vuren . 1998. A 32-year demography of yellow-bellied marmots (Marmota flaviventris). Journal of Zoology (London) 246: 337– 346. Sherman, P. W. 1977. Nepotism and the evolution of alarm calls. Science 197: 1246– 1253. Sherman, P. W. 1989. Mate guarding as paternity insurance in Idaho ground squirrels. Nature 338: 418– 420. Sherman, P. W., and M. L. Morton . 1984. Demography of Belding's ground squirrels. Ecology 65: 1617– 1628. Slade, N. A., and D. F. Balph . 1974. Population ecology of Uinta ground squirrels. Ecology 55: 989– 1003. Smith, G. W., and D. R. Johnson . 1985. Demography of a Townsend ground squirrel population in southwestern Idaho. Ecology 66: 171– 178. Stanton, N. L., L. M. Shults, and M. Parker . 1992. Variation in reproductive potential of the Wyoming ground squirrel in southeastern Wyoming. Prairie Naturalist 24: 261– 271. Steele, R., S. F. Arno, and K. Geier-Hayes . 1986. Wildfire patterns change in central Idaho's ponderosa pine–Douglas-fir forest. Western Journal of Applied Forestry 1: 16– 18. Stram, D. O., and J. W. Lee . 1994. Variance components testing in the longitudinal mixed effects model. Biometrics 50: 1171– 1177. Truska, A. S., and E. Yensen . 1990. Photographic evidence of vegetation changes in Adams County, Idaho. Journal of the Idaho Academy of Science 26: 18– 40. Tuljapurkar, S. D. 1982. Population dynamics in variable environments. III. Evolutionary dynamics of r-selection. Theoretical Population Biology 21: 141– 165. Tuljapurkar, S. D., and S. H. Orzack . 1980. Population dynamics in variable environments. I. Long-run growth rates and extinction. Theoretical Population Biology 18: 314– 342. USDA Forest Service. 1993. Region 4 range management resource value ratings guide. Section 27.4 (exhibit 02). Rangeland ecosystem analysis and management handbook (FSH 2209.21). USDA Forest Service, Ogden, Utah, USA. Van Horne, B., G. S. Olson, R. L. Schooley, J. G. Corn, and K. P. Burnham . 1997. Effects of drought and prolonged winter on Townsend's ground squirrel demography in shrubsteppe habitats. Ecological Monographs 67: 295– 315. White, G. C., and K. P. Burnham . 1999. Program MARK: survival estimation from populations of marked animals. Bird Study 46: (Supplement) S 120– S139. Wing, L. D. 1969. Ecology and herbivore use of five mountain meadows in the Idaho Primitive Area. Ph.D. dissertation. University of Idaho, Moscow, Idaho, USA. Wisdom, M. J., R. S. Holthausen, B. C. Wales, C. D. Hargis, V. A. Saab, D. C. Lee, W. J. Hann, T. D. Rich, M. M. Rowland, W. J. Murphy, and M. R. Eames . 2000. Source habitats for terrestrial vertebrates of focus in the Interior Columbia Basin: broad-scale trends and management implications. General Technical Report PNW-GTR-485. USDA Forest Service, Pacific Northwest Research Station, Portand, Oregon, USA. Yensen, E. 1991. Taxonomy and distribution of the Idaho ground squirrel, Spermophilus brunneus. Journal of Mammalogy 72: 583– 600. Yensen, E., M. P. Luscher, and S. Boyden . 1991. Structure of burrows used by the Idaho ground squirrel, Spermophilus brunneus. Northwest Science 65: 93– 100. Yensen, E., and P. W. Sherman . 1997. Spermophilus brunneus. Mammalian Species 560: 1– 5. Yensen, E., and P. W. Sherman . In press. Ground squirrels. In G. A. Feldhammer, B. C. Thompson, and J. A. Chapman, editors. Wild mammals of North America: biology, management, and economics. Second edition. Johns Hopkins University Press, Baltimore, Maryland, USA. Young, H. F. 1969. Hypotheses on Peregrine population dynamics. Pages 513–519 in J. J. Hickey, editor. Peregrine Falcon populations: their biology and decline. University of Wisconsin Press, Madison, Wisconsin, USA. Zammuto, R. M., and J. S. Millar . 1985. Environmental predictability, variability and Spermophilus columbianus life history over an elevational gradient. Ecology 66: 1784– 1794. Zegers, D. A. 1984. Spermophilus elegans. Mammalian Species 214: 1– 7. 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