Abstract
Pregnancy and parturition are often difficult to detect in wild-living animals, especially in species that give birth to altricial young in burrows or caves. Current methods to detect pregnancy and birth in hibernating animals often entail disturbances that can affect the animals' reproductive success. We developed a new method to confirm pregnancy and parturition in hibernating brown bears (Ursus arctos) using activity data recorded in dual-axis motion sensors mounted on GPS–GSM neck collars on 30 brown bears during 52 hibernation seasons in Sweden. We adjusted recorded activity to the individual basal activity level for each bear. Pregnant females showed characteristic activity patterns during the period of pregnancy, with significantly higher daily activity levels and frequency of active periods during pregnancy than nonpregnant bears. Pregnant females were active on average 2.20 times more often during the pregnancy period than during the postpartum period, compared with 0.97 times for nonpregnant females. A pregnancy index was defined as the average of the proportion of mean daily activity levels and the proportion of activity events during the pregnancy period compared with the postpartum period. It averaged 2.61 ± 1.73 (SD) for pregnant females and 0.94 ± 0.24 for nonpregnant females. Using this method, we evaluated a group of adult females that had an unverified reproductive status but were classified as not pregnant because no cubs had been observed after den emergence. The results suggested that 35 % of those females had, in fact, been pregnant.
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References
Alt GL (1983) Timing of parturition of black bears (Ursus americanus) in northeastern Pennsylvania. J Mammal 64(2):305–307
Arnemo JM, Ahlqvist P, Andersen R, Berntsen F, Ericsson G, Odden J, Brunberg S, Segerström P, Swenson JE (2006) Risk of capture-related mortality in large free-ranging mammals: experiences from Scandinavia. Wildl Biol 12(1):109–113. doi:10.2981/0909-6396(2006)12[109:rocmil]2.0.co;2
Bauman JE, Clifford DL, Asa CS (2008) Pregnancy diagnosis in wild canids using a commercially available relaxin assay. Zoo Biology 27(5):406–413. doi:10.1002/zoo.20196
Craighead FC Jr, Craighead JJ (1972) Data on grizzly bear denning activities and behavior obtained by using wildlife telemetry. Proceedings of the International Conference on Bear Research and Management 2:84–106
Dahle B, Swenson JE (2003) Seasonal range size in relation to reproductive strategies in brown bears Ursus arctos. J Anim Ecol 72(4):660–667
Elfström M, Swenson JE (2009) Effects of sex and age on den site use by Scandinavian brown bears. Ursus 20(2):85–93. doi:10.2192/09gr005.1
Elfström M, Swenson JE, Ball JP (2008) Selection of denning habitats by Scandinavian brown bears Ursus arctos. Wildl Biol 14(2):176–187. doi:10.2981/0909-6396(2008)14[176:sodhbs]2.0.co;2
Evans AL, Sahlén V, Støen O-G, Fahlman Å, Brunberg S, Madslien K, Fröbert O, Swenson JE, Arnemo JM (2012) Capture, anesthesia, and disturbance of free-ranging brown bears (Ursus arctos) during hibernation. PLoS One 7(7):e40520. doi:10.1371/journal.pone.0040520
Foresman KR, Gagnon PM (1986) Plasma protein profile as an index of pregnancy in the black bear. Proceedings of the International Conference on Bear Research and Management 6:223–226
Friebe A, Swenson JE, Sandegren F (2001) Denning chronology of female brown bears in central Sweden. Ursus 12:37–45
Frković A, Huber D, Kusak J (2001) Brown bear litter sizes in Croatia. Ursus 12:103–105. doi:10.2307/3873235
Garrison EP (2004) Reproductive ecology, cub survival and denning ecology of the Florida black bear. Master of Science. University of Florida
Gervasi V, Brunberg S, Swenson JE, Bowman J (2006) An individual-based method to measure animal activity levels: a test on brown bears. Wildl Soc Bull 34(5):1314–1319. doi:10.2193/0091-7648(2006)34[1314:aimtma]2.0.co;2
Hellgren EC (1998) Physiology of hibernation in bears. Ursus 10:467–477
Hensel RJ, Troyer WA, Erickson AW (1969) Reproduction in the female brown bear. J Wildl Manag 33(2):357–365
Hissa R (1997) Physiology of the European brown bear (Ursus arctos arctos). Ann Zool Fennici 34(4):267–287
Hissa R, Siekkinen J, Hohtola E, Saarela S, Hakala A, Pudas J (1994) Seasonal patterns in the physiology of the European brown bear (Ursus arctos arctos) in Finland. Comparative Biochemistry and Physiology Part A: Physiology 109(3):781–791. doi:10.1016/0300-9629(94)90222-4
Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost benefit approach. Physiol Biochem Zool 76(2):165–179
Judd SL, Knight RR, Blanchard BM (1986) Denning of grizzly bears in the Yellowstone National Park area. Proceedings of the International Conference on Bear Research and Management 6:111–117
Kähn W (1992) Ultrasonography as a diagnostic tool in female animal reproduction. Anim Reprod Sci 28(1–4):1–10. doi:10.1016/0378-4320(92)90085-R
Kiddy CA (1977) Variation in physical activity as an indication of estrus in dairy cows. Journal of Dairy Science 60(2):235–243
Kleiman DG, Thompson KV, Baer CK (2010) Wild mammals in captivity: principles and techniques for zoo, management. University of Chicago Press, Chicago
Kordek WS, Lindzey JS (1980) Preliminary analysis of female reproductive tracts from Pennsylvania black bears. Proceedings of the International Conference on Bear Research and Management 4:159–161
Labyak SE, Lee TM (1995) Estrus- and steroid-induced changes in circadian rhythms in a diurnal rodent, Octodon degus. Physiol Behav 58(3):573–585. doi:10.1016/0031-9384(95)00096-2
Laske TG, Garshelis DL, Iaizzo PA (2011) Monitoring the wild black bear's reaction to human and environmental stressors. BMC Physiol 11:13
Lightfoot JT (2008) Sex hormones' regulation of rodent physical activity: a review. Int J Biol Sci 4(3):126–132
Linnell JDC, Jon ES, Andersen R, Barnes B (2000) How vulnerable are denning bears to disturbance? Wildl Soc Bull 28(2):400–413
Manchi S, Swenson JE (2005) Denning behaviour of Scandinavian brown bears Ursus arctos. Wildl Biol 11(2):123–132. doi:10.2981/0909-6396(2005)11[123:dbosbb]2.0.co;2
Miller SD (1990) Denning ecology of brown bears in Southcentral Alaska and comparisons with a sympatric black bear population. Proceedings of the International Conference on Bear Research and Management 8:279–287
Moen R, Pastor J, Cohen Y (1996) Interpreting behavior from activity counters in GPS collars on moose. Alces 32:1101–1108
Perrigo G (1987) Breeding and feeding strategies in deer mice and house mice when females are challenged to work for their food. Anim Behav 35(5):1298–1316. doi:10.1016/S0003-3472(87)80002-7
Robbins CT, Lopez-Alfaro C, Rode KD, Tøien Ø, Nelson OL (2012) Hibernation and seasonal fasting in bears: the energetic costs and consequences for polar bears. J Mammal 93(6):1493–1503. doi:10.1644/11-mamm-a-406.1
Roth HU, Huber D (1986) Diel activity of brown bears in Plitvice Lakes National Park, Yugoslavia. Proceedings of the International Conference on Bears and Management 6:177–181
Sato M, Tsubota T, Yamamoto K, Komatsu T, Hashimoto Y, Katayama A, Hazumi T, Kita I, Kudo T (2000) Serum progesterone and estradiol-17beta concentrations in captive and free-ranging adult female Japanese black bears (Ursus thibetanus japonicus). J Vet Med Sci 62(4):415–420
Sato M, Tsubota T, Komatsu T, Watanabe G, Taya K, Murase T, Kita I, Kudo T (2001) Changes in sex steroids, gonadotropins, prolactin, and inhibin in pregnant and nonpregnant Japanese black bears (Ursus thibetanus japonicus). Biol Reprod 65(4):1006–1013. doi:10.1095/biolreprod65.4.1006
Schoen JW, Beier LR, Lentfer JW, Johnson LJ (1987) Denning ecology of brown bears on Admiralty and Chichagof Islands. Proceedings of the International Conference on Bear Research and Management 7:293–304
Schwarzenberger F, Möstl E, Palme R, Bamberg E (1996) Faecal steroid analysis for non-invasive monitoring of reproductive status in farm, wild and zoo animals. Anim Reprod Sci 42(1–4):515–526. doi:10.1016/0378-4320(96)01561-8
Servheen C, Klaver R (1983) Grizzly bear dens and denning activity in the Mission and Rattlesnake Mountains, Montana. Proceedings of the International Conference on Bear Research and Management 5:201–207
Seton ET (1929) Lives of game animals. Doubleday, New York 2(1):117–194
Spady TJ, Lindburg DG, Durrant BS (2007) Evolution of reproductive seasonality in bears. Mammal Review 37(1):21–53. doi:10.1111/j.1365-2907.2007.00096.x
Stearns SC (1992) The evolution of life histories. Oxford University Press, London
Steyaert SMJG, EndrestøL A, Hackländer K, Swenson JE, Zedrosser A (2012) The mating system of the brown bear Ursus arctos. Mammal Review 42(1):12–34. doi:10.1111/j.1365-2907.2011.00184.x
Steyaert SMJG, Swenson JE, Kindberg J, Brunberg S, Zedrosser A (2013) Making the best of a bad situation: sexual segregation of a non-social mammal in a risky landscape. Journal of Animal Ecology Accepted
Swenson JE, Haroldson MA (2008) Observations of mixed-aged litters in brown bears. Ursus 19(1):73–79
Swenson JE, Sandegren F, Brunberg S, Wabakken P (1997) Winter den abandonment by brown bears Ursus arctos: causes and consequences. Wildl Biol 3:35–38
Swenson JE, Adamic M, Huber D, Stokke S (2007) Brown bear body mass and growth in northern and southern Europe. Oecologia 153(1):37–47. doi:10.1007/s00442-007-0715-1
Takahashi JS, Menaker M (1980) Interaction of estradiol and progesterone: effects on circadian locomotor rhythm of female golden hamsters. Am J Physiol Regul Integr Comp Physiol 239(5):R497–R504
Tøien Ø, Blake J, Edgar DM, Grahn DA, Heller HC, Barnes BM (2011) Hibernation in black bears: independence of metabolic suppression from body temperature. Science 331(6019):906–909. doi:10.1126/science.1199435
Tomasi TE, Hellgren EC, Tucker TJ (1998) Thyroid hormone concentrations in black bears (Ursus americanus): hibernation and pregnancy effects. Gen Comp Endocrinol 109(2):192–199. doi:10.1006/gcen.1997.7018
Tsubota T, Takahashi Y, Kanagawa H (1987) Changes in serum progesterone levels and growth of fetuses in Hokkaido brown bears. Proceedings of the International Conference on Bear Research and Management 7:355–358
Van Daele LJ, Barnes VG Jr, Smith RB (1990) Denning characteristics of brown bears on Kodiak Island, Alaska. Proceedings of the International Conference on Bear Research and Management 8:257–267
Williams C, Sheriff M, Schmutz J, Kohl F, Tøien Ø, Buck CL, Barnes B (2011) Data logging of body temperatures provides precise information on phenology of reproductive events in a free-living arctic hibernator. Journal of Comparative Physiology B 181(8):1101–1109. doi:10.1007/s00360-011-0593-z
Wimsatt WA (1963) Delayed implantation in the Ursidae, with particular reference to the black bear. In: Enders AC (ed) Delayed implantation. University of Chicago Press, Chicago, pp 49–76
Wollnik F, Turek FW (1988) Estrous correlated modulations of circadian and ultradian wheel-running activity rhythms in LEW/Ztm rats. Physiol Behav 43(3):389–396. doi:10.1016/0031-9384(88)90204-1
Zedrosser A, Rauer G, Kruckenhauser L (2004) Early primiparity in brown bears. Acta Theriol 49(3):427–432. doi:10.1007/bf03192540
Zedrosser A, Støen O-G, Sæbø S, Swenson JE (2007) Should I stay or should I go? Natal dispersal in the brown bear. Anim Behav 74(3):369–376. doi:10.1016/j.anbehav.2006.09.015
Zedrosser A, Dahle B, Stoen OG, Swenson JE (2009) The effects of primiparity on reproductive performance in the brown bear. Oecologia 160(4):847–854. doi:10.1007/s00442-009-1343-8
Acknowledgments
We thank the Swedish Environmental Protection Agency, the Norwegian Directorate for Nature Management, the Swedish Association for Hunting and Wildlife Management, the Research Council of Norway, and the Austrian Science Foundation (project P20182) for funding the Scandinavian Brown Bear Research Project. We also thank the Vereinigung von Freunden und Förderern der Goethe-Universität Frankfurt in Germany for their financial support. This is scientific paper no. 151 from the Scandinavian Brown Bear Research Project.
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Friebe, A., Zedrosser, A. & Swenson, J.E. Detection of pregnancy in a hibernator based on activity data. Eur J Wildl Res 59, 731–741 (2013). https://doi.org/10.1007/s10344-013-0728-5
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DOI: https://doi.org/10.1007/s10344-013-0728-5