Stress load in European ground squirrels living in habitats with high and low human impact
Stress load in European ground squirrels living in habitats with high and low human impact
DOI:
https://doi.org/10.22120/jwb.2017.28426Keywords:
Spermophilus citellus, behavioural ecology, anthropogenic influence, faecal samples, corticosteroids, progesteroneAbstract
Anthropogenic land use and its after-effects are potential sources of stress for European ground squirrel (Spermophilus citellus) populations, which increasingly have to cope with human impact throughout the species’ range. To determine whether habitat alteration impacts the stress load of free-ranging populations in Austria, we live-trapped and faecal-sampled individuals both in a nearly unaltered steppe habitat (TD) and in a strongly altered alfalfa meadow (FB). Overall and seasonal faecal cortisol metabolite (FCM) concentrations were analysed and compared between the two study sites. FCM levels of adult males and of juveniles of both sexes were higher at FB than at TD. Adult females showed no such differences, but exhibited increased faecal progesterone metabolites (FPM) levels at both sites during June. Our results indicate that human activities affected stress load in adult males and juveniles. The altered vegetation led to highly abundant food at FB and, together with the isolation of the habitat, caused a high population density. This apparently intensified social stress in certain periods of the active season. Elevated FCM levels in both adult males and juveniles at FB coincided with the period of highest population density, when all juveniles had emerged from the natal burrows, and hibernation had not started yet. At the same time, predation pressure and human recreational activities also peaked. The highest FCM levels were found in juveniles at FB shortly after natal emergence, suggesting that this age class is most vulnerable to social stress, predation and human disturbance. The lack of a measurable stress response in adult females may be due to increased progesterone concentrations attenuating the stress-induced elevation of glucocorticoids.
References
Barja I. Silván G. Rosellini S. Piñeiro A. González-Gil A. Camacho L., Illera J.C. 2007. Stress physiological responses to tourist pressure in a wild population of European pine marten. The Journal of Steroid Biochemistry and Molecular Biology 104(3-5):136–142.
Behie A.M., Pavelka M.S.M., Chapman C.A. 2010. Sources of variation in fecal cortisol levels in howler monkeys in Belize. American Journal of Primatology 72(7):600–606.
Boonstra R., Boag P.T. 1992. Spring declines in Microtus pennsylvanicus and the role of steroid hormones. Journal of Animal Ecology 61(2):339–352.
Boonstra R., Hik D.S., Singleton G.R., Tinnikov A. 1998. The impact of predator-induced stress on the snowshoe hare cycle. Ecological Monographs 79(5):371–394.
Boonstra R., Hubbs A.H., Lacey E.A., McColl C.J. 2001. Seasonal changes in glucocorticoid and testosterone concentrations in free-living Arctic ground squirrels from the boreal forest of the Yukon. Canadian Journal of Zoology 79(1):49–58.
Boswell T., Woods S.C., Kenagy G.J. 1994. Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. General and Comparative Endocrinology 96(3):339–346.
Brenner M., Turrini T., Hoffmann I.E. 2008. Does home-range overlap in the European ground squirrel increase with anthropogenic alteration? in: Book of Abstracts, II. European Ground Squirrel Meeting, Svaty Jan pod Skalou, Czech Republic, p. 15.
Castonguay T.W., Dallman M.F., Stern J.S. 1986. Some metabolic and behavioral effects of adrenalectomy on obese Zucker rats. American Journal of Physiology - Regulatory, Integrative and Comparative Physiology 251(5):923–933.
Coroiu C., Kryštufek B., Vohralík V., Zagorodnyuk I. 2008. Spermophilus citellus. The IUCN Red List of Threatened Species 2008: e.T20472A9204055. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T20472A9204055.en. Downloaded on 11 September 2017.
Creel S., Fox J.E., Hardy A., Sands J., Garrott B., Peterson R.O. 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conservation Biology 16(3):809–814.
Dirzo R., Young H. S., Galetti M., Ceballos G., Isaac N. J. B., Collen B. 2014. Defaunation in the Anthropocene. Science 345(6195):401–406.
Ehrlich P.R., Wilson E.O. 1991. Biodiversity studies: science and policy. Science 253(5021):758–762.
Feldhamer G.A., Drickamer L.C., Vessey S.H., Merritt J.F. 1999. Populations and life history, in: Feldhamer G.A., Drickamer L.C., Vessey S.H., Merritt J.F. (Eds.), Mammalogy: Adaptation, Diversity, and Ecology. WCB/McGraw-Hill, Boston, pp. 400–416.
Foley C.A.H., Papageorge S., Wasser S.K. 2001. Noninvasive stress and reproductive measures of social and ecological pressures in free-ranging African elephants. Conservation Biology 15(4):1134–1142.
Galletti F., Klopper A. 1964. The effect of progesterone on the quantity and distribution of body fat in the female rat. Acta Endocrinologica 46(3):379–386.
Gellersen B., Fernandes M.S., Brosens J.J. 2009. Non-genomic progesterone actions in female reproduction. Human Reproduction Update 15(1):119-138.
Goodman H.M. 2009. Basic Medical Endocrinology. London, Great Britain: Academic Press.
Goymann W., Möstl E., Van't Hof T., East M.L., Hofer H. 1999. Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. General and Comparative Endocrinology 114(3):340–348.
Hik D.S., McColl C.J., Boonstra R. 2001. Why are Arctic ground squirrels more stressed in the boreal forest than in alpine meadows? ÉcoSCIENCE 8(3):275–288.
Hofer H., East M.L. 1998. Biological conservation and stress, in: Møller A.P., Milinski. M., Slater P.J.B. (Eds.), Advances in the Study of Behavior Volume 27. Academic Press, San Diego, pp. 405–525.
Hoffmann I.E., Millesi E., Huber S., Everts L.G., Dittami J.P. 2003a. Population dynamics of European ground squirrels (Spermophilus citellus) in a suburban area. Journal of Mammalogy 84:615–626.
Hoffmann I.E., Millesi E., Pieta K., Dittami J.P. 2003b. Anthropogenic effects on the population ecology of European ground squirrels (Spermophilus citellus) at the periphery of their geographic range. Mammalian Biology - Zeitschrift fur Saugetierkunde 68(2):205–213.
Hoffmann I.E., Turrini T., Brenner M. 2008. Do European ground squirrels (Spermophilus citellus) in Austria adjust their life history to anthropogenic influence? Lynx 39(2):241–250.
Hubbs A.H., Millar J.S., Wiebe J.P. 2000. Effect of brief exposure to a potential predator on cortisol concentrations in female Columbian ground squirrels (Spermophilus columbianus). Canadian Journal of Zoology 78(4):578–587.
Huber S., Millesi E., Walzl M., Dittami J., Arnold W. 1999. Reproductive effort and costs of reproduction in female European ground squirrels. Oecologia 121(1):19–24.
Huber S., Hoffmann I.E., Millesi E., Dittami J., Arnold W. 2001. Explaining the seasonal decline in litter size in European ground squirrels. Ecography 24(2):205–211.
Johnson-Nistler C.M., Knight J.E., Cash S.D. 2005. Considerations related to Richardson's ground squirrel (Spermophilus richardsonii) control in Montana. Agronomy Journal 97(5):1460–1464.
Kenagy G.J., Place N.J. 2000. Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: Effects of reproduction and capture and handling. General and Comparative Endocrinology 117(2):189–199.
King B.M. 1988. Glucocorticoids and hypothalamic obesity. Neuroscience & Biobehavioral Reviews 12(1):29–37.
Kryštufek B. 1999. Spermophilus citellus (Linnaeus, 1766), in: Mitchell-Jones A.J., Amori G., Bogdanowicz W., Kryštufek B., Rreijnders P.J.H., Spitzenberger F., Stubbe M., Thissen J.B.M., Vohralik V., Zima J. (Eds.), The Atlas of European Mammals. London, Academic Press
Mateo J.M., Cavigelli S.A. 2005. A validation of extraction methods for noninvasive sampling of glucocorticoids in free-living ground squirrels. Physiological and Biochemical Zoology 78(6):1069–1084.
Mateo J.M. 2007. Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). Behavioral Ecology and Sociobiology 62(1):37–49.
McDonald I.R., Lee A.K., Than K.A., Martin R.W. 1988. Concentration of free glucocorticoids in plasma and mortality in the Australian bush rat (Rattus fuscipes Waterhouse). Journal of Mammalogy 69(4):740–748.
Millesi E., Huber S., Dittami J.P., Hoffmann I.E., Daan S. 1998. Parameters of mating effort and success in male European ground squirrels, Spermophilus citellus. Ethology 104(4):298–313.
Millesi E., Huber S., Everts L.G., Dittami J.P. 1999a. Reproductive decisions in female European ground squirrels: Factors affecting reproductive output and maternal investment. Ethology 105(2):163–175.
Millesi E., Strijkstra A.M., Hoffmann I.E., Dittami J.P., Daan S. 1999b. Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus. Journal of Mammalogy 80(1):218–231.
Millesi E., Hoffmann I.E., Huber S. 2004. Reproductive strategies of male European sousliks (Spermophilus citellus) at high and low population density. Lutra 47(2):75–84.
Millesi E., Divjak A., Strauss A. 2008a. Seasonal timing and pre-hibernation fattening in breeding and non-breeding European ground squirrels, in: Lovegrove B.G., McKechnie A.E. (Eds.), Hypometabolism in Animals: Torpor, Hibernation and Cryobiology. Interpak Books, Pietermaritzburg, pp. 291–296.
Millesi E., Strauss A., Burger T., Hoffmann I.E., Walzl, M. 2008b. Follicular development in European ground squirrels (Spermophilus citellus) in different phases of the annual cycle. Reproduction 136(2):205–210.
Möstl E., Palme R. 2002. Hormones as indicators of stress. Domestic animal endocrinology 23(1-2):67–74.
Nunes S., Pelz K.M., Muecke E., Holekamp K.E., Zucker I. 2006. Plasma glucocorticoid concentrations and body mass in ground squirrels: Seasonal variation and circannual organization. General and Comparative Endocrinology 146(2):136–143.
Palme R., Möstl E. 1994. Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar feces, in: Gorog S. (Ed.), Advances in Steriod Analyses ’93: Proceedings from the 5th Symposium on the Analysis of Steroids Szombathely, Hungary, May 3-5, 1993, Szombathely, pp.111–117.
Patchev V.K., Hassan A.H.S., Holsboer F., Almeida O.F.X. 1996. The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15(6):533–540.
Rogovin Ko., Randall J.A., Kolosova I., Moshkin M. 2003. Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities. Hormones and Behavior 43(1):132–139.
Rosenthal H.E., Slaunwhite W.R., Sandberg A.A. 1969a. Transcortin: A corticosteroid-binding protein of plasma. X. Cortisol and progesterone interplay and unbound levels of these steroids in pregnancy. Journal of Clinical Endocrinology and Metabolism 29(3):352–367.
Rosenthal H.E., Slaunwhite W.R., Sandberg A.A. 1969b. Transcortin: A corticosteroid-binding protein of plasma. XI. Effects of estrogens or pregnancy in guinea pigs. Endocrinology 85(4):825–830.
Ružic A. 1978. Der oder das Europäische Ziesel (Citellus citellus) in: Niethammer J., Krapp F. (Eds.), Handbuch der Säugetiere Europas Band 1/I, Akademische Verlagsgesellschaft, Wiesbaden, pp. 123–144.
Sapolsky R.M., Romero L.M., Munck A.U. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocrine Reviews 21(1):55–89.
Sheriff M.J., Krebs C.J., Boonstra R. 2010. Assessing stress in animal populations: Do fecal and plasma glucocorticoids tell the same story? General and Comparative Endocrinology 166(3):614–619.
Sheriff M.J., Krebs C.J., Boonstra R. 2011. From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia 166(3):1–13.
Smit C.J., van Wijngaarden A. 1981. Threatened Mammals in Europe. Wiesbaden, Germany: Akademische Verlagsgesellschaft.
Solano J.M., Jacobson L. 1999.Glucocorticoids reverse leptin effects on food intake and body fat in mice without increasing NPY mRNA. American Journal of Physiology - Endocrinology and Metabolism 277(4): E708–E716.
Soulé M.E. 1991. Conservation: Tactics for a constant crisis. Science 253(5021):744–750.
Spitzenberger F., Bauer K. 2001. Ziesel Spermophilus citellus (Linnaeus, 1766), in: Spitzenberger F. (Ed.), Die Säugetierfauna Österreichs, Grüne Reihe des Bundesministeriums für Land- und Forstwirtschaft, Umwelt und Wasserwirtschaft, Vienna, pp. 356–365.
Strauss A., Mascher E., Palme R., Millesi E. 2007. Sexually mature and immature yearling male European ground squirrels: A comparison of behavioral and physiological parameters. Hormones and Behavior 52(5):646–652.
Strauss A., Hoffmann I.E., Walzl M., Millesi E. 2009. Vaginal oestrus during the reproductive and non-reproductive period in European ground squirrels. Animal Reproduction Science 112(3-4):362–370.
Turrini T., Brenner M., Hoffmann I.E., Millesi E. 2008. Home ranges of European ground squirrels (Spermophilus citellus) in two habitats exposed to different degrees of human impact. Lynx 39(2):323–332.
Valli G., Sudha S., Ravi Sankar B., Govindarajulu P., Srinivasan N. 2000. Altered corticosterone status impairs steroidogenesis in the granulosa and thecal cells of Wistar rats. The Journal of Steroid Biochemistry and Molecular Biology 73(3-4):153–158.
Wade G.N., Gray J.M. 1979. Gonadal effects on food intake and adiposity: A metabolic hypothesis. Physiology and Behavior 22(3):583–593.
Wasser S.K., Thomas R., Nair P.P., Guidry C., Southers J., Lucas J., Wildt D.E., Monfort S.L. 1993. Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). Journal of Reproduction and Fertility 97(2):569–574.
Wikelski M., Cooke S.J. 2006. Conservation physiology. Trends in Ecology and Evolution 21:38–46.
Wilson E.O. 1985. The biological diversity crisis. BioScience 35:700–706.
Wingfield J.C., Sapolsky R.M. 2003. Reproduction and resistance to stress: When and how. Journal of Neuroendocrinology 15(8):711–724.
Yensen E., Sherman P.W. 2003. Ground squirrels, in: Feldhamer G.A., Thompson B.C., Chapman A.S. (Eds.), Wild Mammals of North America: Biology, Management, and Conservation. Johns Hopkins University Press, Baltimore, pp. 211–231.
JWB applies the 