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Resident European ground squirrels exhibit higher stress levels than translocated individuals after conservation reinforcement

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Abstract

The European ground squirrel (Spermophilus citellus) is a rodent inhabiting the open grasslands of central and southeastern Europe. The species is endangered, and various conservation activities are being conducted to preserve and improve the populations’ status, especially during the recent years including translocations of individuals. The success of these measures has varied and is potentially strongly influenced by the chronic and acute stress associated with the translocation process itself. This stress load, however, has rarely been investigated in the framework of such conservation projects, neither in translocated nor in resident individuals. To fill this gap, we investigated glucocorticoid metabolite concentrations in translocated ground squirrels and compared these with concentrations in resident animals of a reinforced colony in southeastern Bulgaria. Between 2017 and 2019, we sampled a total of 252 individuals for faecal cortisol metabolite concentrations (FCM). The results showed that FCM decreased after the release in translocated individuals and that the time span after the translocation event was the key variable explaining the decrease. Surprisingly, the FCM levels were higher in the resident ground squirrels than in the translocated individuals throughout the active season and in the following spring. Furthermore, we found no effect of FCM concentrations on dispersal distances or body mass gain in translocated individuals.

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References

  • Apfelbeck B, Helm B, Illera JC, Mortega KG, Smiddy P, Evans NP (2017) Baseline and stress-induced levels of corticosterone in male and female Afrotropical and European temperate stonechats during breeding. BMC Evol Biol 17(1):114

    Article  Google Scholar 

  • Boonstra R, Hik D, Singleton GR, Tinnikov A (1998) The impact of predator-induced stress on the snowshoe hare cycle. Ecol Monogr 68:371–394

    Article  Google Scholar 

  • Boonstra R, Hubbs AH, Lacey EA, Mccoll CJ (2001) Seasonal changes in glucocorticoid and testosterone concentrations in free-living arctic ground squirrels from the boreal forest of the Yuko. Can J Zool 79:49–58

    Article  Google Scholar 

  • Bosson CO, Palme R, Boonstra R (2013) Assessing the impact of live-capture, confinement, and translocation on stress and fate in eastern grey squirrels. J Mammal 94:1401–1411. https://doi.org/10.1644/13-mamm-a-046.1

    Article  Google Scholar 

  • Boswell T, Woods SC, Kenagy GJ (1994) Seasonal changes in body mass, insulin, and glucocorticoids of free-living golden-mantled ground squirrels. Gen Comp Endocrinol 96:339–346

    Article  CAS  Google Scholar 

  • Brenner M, Turrini T, Hoffmann E, Millesi E (2017) Stress load in European ground squirrels living in habitats with high and low human impact. J Wildl Biodivers 1(2):94–109

    Google Scholar 

  • Cabezas S, Blas J, Marchant TA, Moreno S (2007) Physiological stress levels predict survival probabilities in wild rabbits. Horm Behav 51:313–320

    Article  CAS  Google Scholar 

  • Catalani A, Casolini P, Cigliana G, Scaccianoce S, Consoli C, Cinque C, Zuena AR, Angelucci L (2002) Maternal corticosterone influences behavior, stress response and corticosteroid receptors in the female rat. Pharmacol Biochem Behav 73(1):105–114

    Article  CAS  Google Scholar 

  • de Souza CJ, Meier AH (1987) Circadian and seasonal variations of plasma insulin and cortisol concentrations in the Syrian hamster, Mesocricetus auratus. Chronobiol Int 4:141–151

    Article  Google Scholar 

  • Dickens MJ, Delehanty DJ, Romero LM (2009) Stress and translocation: alterations in the stress physiology of translocated birds. Proc R Soc B 276(1664):2051–2056. https://doi.org/10.1098/rspb.2008.1778

    Article  PubMed  Google Scholar 

  • Dickens MJ, Delehanty DJ, Romero ML (2010) Stress: an inevitable component of animal translocation. Biol Conserv 143:1329–1341. https://doi.org/10.1016/j.biocon.2010.02.032

    Article  Google Scholar 

  • Gedeon CI, Boross G, Németh A, Altbäcker V (2012) Release site manipulation to favour European ground squirrel Spermophilus citellus translocations: translocation and habitat manipulation. Wildl Biol 18(1):97–104

    Article  Google Scholar 

  • Hegyeli Z (2020) Spermophilus citellus. The IUCN Red List of Threatened Species 2020: e.T20472A91282380. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T20472A91282380.en. Accessed 14 July 2020

  • Hernandez SE, Strona ALS, Leiner NO, Suzán G, Romano MC (2018) Seasonal changes of faecal cortisol metabolite levels in Gracilinanus agilis (Didelphimorphia: Didelphidae) and its association to life histories variables and parasite loads. Conserv Physiol 6(1):coy021

    Article  CAS  Google Scholar 

  • Hik DS, McColl CJ, Boonstra R (2001) Why are arctic ground squirrels more stressed in the boreal forest than in alpine meadows? Ecoscience 8:275–288

    Article  Google Scholar 

  • Humphries MM, Thomas DW, Kramer DL (2003) The role of energy availability in mammalian hibernation: a cost-benefit approach. Physiol Biochem Zool 76:165–179

    Article  Google Scholar 

  • Jenkins BR, Vitousek MN, Hubbard JK, Safran RJ (2014) An experimental analysis of the heritability of variation in glucocorticoid concentrations in a wild avian population. Proc R Soc B 281:20141302. https://doi.org/10.1098/rspb.2014.1302

    Article  PubMed  Google Scholar 

  • Keay JM, Singh J, Gaunt MC, Kaur T (2006) Faecal glucocorticoids and their metabolites as indicators of stress in various mammalian species: a literature review. J Zoo Wildl Med 37:234–244. https://doi.org/10.1638/05-050.1

    Article  PubMed  Google Scholar 

  • Kenagy GJ, Place NJ (2000) Seasonal changes in plasma glucocorticosteroids of free-living female yellow-pine chipmunks: effects of reproduction and capture and handling. Gen Comp Endocrinol 117:189–199. https://doi.org/10.1006/gcen.1999.7397

    Article  CAS  PubMed  Google Scholar 

  • Koshev Y (2013) Reports on distribution and determining conservation status of European ground squirrel (Spermophilus citellus) in Nature 2000 site BG0000219 “Derventski vazvishenia 2”. Project "Mapping and determining conservation status of mammals in NATURA 2000 network in Bulgaria 2011–2013". Funded by MOEW-Bulgaria and Operational Programme Environment 2007–2013. Online at: https://natura2000.moew.government.bg/Home/Natura2000ProtectedSites

  • Koshev Y, Kachamakova M, Arangelov S, Ragyov D (2019) Translocations of European ground squirrel (Spermophilus citellus) along altitudinal gradient in Bulgaria–an overview. Nat Conserv 35:63

    Article  Google Scholar 

  • Letty J, Marchandeau S, Aubineau J (2007) Problems encountered by individuals in animal translocations: lessons from field studies. Ecoscience 14:259–271. https://doi.org/10.2980/1195-6860(2007)14

    Article  Google Scholar 

  • Lindtner P, Šoltís M, Kubovčík V (2019) Translocation of keystone species may not mean translocation of keystone effect. Eur J Wildl Res 65(2):24

    Article  Google Scholar 

  • Matějů J, Říčanová Š, Ambros M, Kala B, Hapl E, Matějů K (2010) Reintroductions of the European ground squirrel (Spermophilus citellus) in Central Europe (Rodentia: Sciuridae). Lynx Series Nova 41:175–191

    Google Scholar 

  • Matějů J, Říčanová Š, Poláková S, Ambros M, Kala B, Matějů K, Kratochvíl L (2012) Method of releasing and number of animals are determinants for the success of European ground squirrel (Spermophilus citellus) reintroductions. Eur J Wildl Res 58:473–482. https://doi.org/10.1007/s10344-011-0597-8

    Article  Google Scholar 

  • Mateo JM (2007) Ecological and hormonal correlates of antipredator behavior in adult Belding’s ground squirrels (Spermophilus beldingi). Behav Ecol Sociobiol 62:37–49

    Article  Google Scholar 

  • Mateo JM (2008) Inverted-U shape relationship between cortisol and learning in ground squirrels. Neurobiol Learn Mem 89:582–590. https://doi.org/10.1016/j.nlm.2007.11.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mateo JM (2014) Development, maternal effects, and behavioral plasticity. Integr Comp Biol. https://doi.org/10.1093/icb/icu044

    Article  PubMed  Google Scholar 

  • Millesi E, Strijkstra AM, Hoffmann IE, Dittami JP, Daan S (1999) Sex and age differences in mass, morphology, and annual cycle in European ground squirrels, Spermophilus citellus. J Mammal 80:218–231

    Article  Google Scholar 

  • Millesi E, Hoffman IE, Huber S (2004) Reproductive strategies of male European sousliks (Spermophilus citellus) at high and low population density. Lutra 47:75–84

    Google Scholar 

  • Millspaugh JJ, Washburn BE (2004) Use of faecal glucocorticoid metabolite measures in conservation biology research: considerations for application and interpretation. Gen Comp Endocrinol 138:189–199. https://doi.org/10.1016/j.ygcen.2004.07.002

    Article  CAS  PubMed  Google Scholar 

  • Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23:67–74. https://doi.org/10.1016/S0739-7240(02)00146-7

    Article  PubMed  Google Scholar 

  • Munck A, Guyre PM, Holbrook NJ (1984) Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr Rev 5:25–44

    Article  CAS  Google Scholar 

  • Navarro-Castilla Á, Barja I, Olea PP, Piñeiro A, Mateo-Tomás P, Silván G, Illera JC (2014a) Are degraded habitats from agricultural crops associated with elevated faecal glucocorticoids in a wild population of common vole (Microtus arvalis)? Mamm Biol 79:36–43. https://doi.org/10.1016/j.mambio.2013.08.004

    Article  Google Scholar 

  • Navarro-Castilla Á, Mata C, Ruiz-Capillas P, Palme R, Malo JE, Barja I (2014b) Are motorways potential stressors of roadside wood mice (Apodemus sylvaticus) populations? PLoS ONE 9:e91942

    Article  Google Scholar 

  • Nunes S, Pelz KM, Muecke E, Holekamp KE, Zucker I (2006) Plasma glucocorticoid concentrations and body mass in ground squirrels: seasonal variation and circannual organization. Gen Comp Endocrinol 146:136–143

    Article  CAS  Google Scholar 

  • Patchev VK, Hassan AHS, Holsboer F, Almeida OFX (1996) The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacol 15:533–540

    Article  CAS  Google Scholar 

  • Ramos-Lara N, Koprowski JL, Kryštufek B, Hoffmann IE (2014) Spermophilus citellus (Rodentia: Sciuridae). Mamm Species 46(913):71–87. https://doi.org/10.1644/913.1

    Article  Google Scholar 

  • Říčanová Š, Koshev Y, Říčan O, Ćosić N, Ćirović D, Sedláček F, Bryja J (2013) Multilocus phylogeography of the European ground squirrel: cryptic interglacial refugia of continental climate in Europe. Mol Ecol 22:4256–4269. https://doi.org/10.1111/mec.12382

    Article  CAS  PubMed  Google Scholar 

  • Rogovin K, Randall JA, 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. Horm Behav 43:132–139

    Article  Google Scholar 

  • Romero LM (2002) Seasonal changes in plasma glucocorticoid concentrations in free-living vertebrates. Gen Comp Endocrinol 128:1–24. https://doi.org/10.1016/S0016-6480(02)00064-3

    Article  CAS  PubMed  Google Scholar 

  • Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Niño events. PNAS 98:7366–7370

    Article  CAS  Google Scholar 

  • Romero LM, Meister CJ, Cyr NE, Kenagy GJ, Wingweld JC (2008) Seasonal glucocorticoid responses to capture in wild free-living mammals. Am J Physiol Regul Integr Comp Physiol 294:R614–R622

    Article  CAS  Google Scholar 

  • Schöpper H, Palme R, Ruf T, Huber S (2012) Effects of prenatal stress on hypothalamic–pituitary–adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol 176(1):18–27

    Article  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2009) The sensitive hare: sublethal effects of predator stress on reproduction in snowshoe hares. J Anim Ecol 78:1249–1258

    Article  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2010) Assessing stress in animal populations: do faecal and plasma glucocorticoids tell the same story? Gen Comp Endocrinol 166:614–619. https://doi.org/10.1016/j.ygcen.2009.12.017

    Article  CAS  PubMed  Google Scholar 

  • Sheriff MJ, Krebs CJ, Boonstra R (2011) From process to pattern: how fluctuating predation risk impacts the stress axis of snowshoe hares during the 10-year cycle. Oecologia 166:593–605

    Article  Google Scholar 

  • Stefanov V (2015) European ground squirrel (Spermophilus citellus Linnaeus, 1776). In: Golemansky V, Peev DR (eds) Red data book of the Republic of Bulgaria. Part 2. Animals. BAS & MOEW, Sofia, p 232

    Google Scholar 

  • 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. Horm Behav 52:646–652

    Article  Google Scholar 

  • Turrini TA, Brenner M, Millesi E, Hoffmann I (2008) Home ranges of European ground squirrels (Spermophilus citellus) in two habitats exposed to different degrees of human impact. Lynx 39:323–332

    Google Scholar 

  • Wingfield JC, Sapolsky RM (2003) Reproduction and resistance to stress: when and how. J Neuroendocrinol 15:711–724

    Article  CAS  Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM (2009) Mixed effects models and extensions in ecology with R. Springer Science & Business Media, Berlin

    Book  Google Scholar 

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Acknowledgements

The study was supported by the Program for Support of Young Researchers and PhD Students at the Bulgarian Academy of Sciences (Grant no 17-110). The Western Strandzha translocation activities were funded by LAND for LIFE project (LIFE14 NAT/BG/001119, co-ordinated by the BSPB) (www.landforlife.org). Special thanks are due to Dimitra-Lida Rammou for her valuable assistance during the field work. We warmly thank Svetoslav Spasov and Dimitar Gradinarov (BSPB), without whom the translocation would not have been possible. We are grateful to Elisabeth Pschernig (University of Vienna) for sample analysis and to Yasen Mutafchiev for the review and the advice. We also thank Anton Sokolov, Svetla Todorova (Sofia University), Dimitar Ragyov (IBER-BAS) and Kristina Yonkova for their participation in the sampling process.

Funding

The study was supported by the Program for Support of Young Researchers and Ph.D. Students at the Bulgarian Academy of Sciences (Grant no. 17-110). The Western Strandzha translocation activities were funded by LAND for LIFE project (LIFE14 NAT/BG/001119, co-ordinated by the BSPB) (www.landforlife.org).

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Authors and Affiliations

  1. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, Tzar Osvoboditel Blvd 1, 1000, Sofia, Bulgaria

    Maria Kachamakova & Yordan Koshev

  2. Department of Behavioral and Cognitive Biology, University of Vienna, Althanstrasse 14, 1090, Vienna, Austria

    Eva Millesi

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  1. Maria Kachamakova
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  2. Yordan Koshev
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Correspondence to Maria Kachamakova.

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Kachamakova, M., Koshev, Y. & Millesi, E. Resident European ground squirrels exhibit higher stress levels than translocated individuals after conservation reinforcement. Mamm Biol 101, 127–136 (2021). https://doi.org/10.1007/s42991-020-00066-2

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