An exploratory investigation of glucocorticoids, personality and survival rates in wild and rehabilitated hedgehogs (Erinaceus europaeus) in Denmark

Sophie Lund Rasmussen1,2,3, Otto Kalliokoski4, Torben Dabelsteen2, Klas S P Abelson4
1Wildlife Conservation Research Unit, Department of Zoology, The Recanati-Kaplan Centre, University of Oxford, Abingdon, UK
2Department of Biology, Section for Ecology and Evolution, University of Copenhagen, Copenhagen Ø, Denmark
3Department of Chemistry and Bioscience, Aalborg University, Aaborg, Denmark
4Department of Experimental Medicine, University of Copenhagen, Copenhagen N, Denmark

Tóm tắt

Abstract Background The European population of hedgehogs (Erinaceus europaeus) is declining. It is therefore essential to optimise conservation initiatives such as the rehabilitation of sick, injured and orphaned hedgehogs. Wild animals placed in captivity may be prone to chronic stress, potentially causing negative health effects. Therefore, the effects of these rehabilitation efforts should consequently be evaluated. Furthermore, hand-raising orphaned hedgehogs is a laborious and costly task, and it is therefore relevant to document whether they have equal post release survival rates compared to their wild conspecifics. The objectives of this research were therefore to conduct an exploratory study of glucocorticoid levels in hedgehogs from different backgrounds and compare the post release survival of translocated, rehabilitated and wild, juvenile hedgehogs as well as the possible effect on survival of differences in shy or bold behaviour (personality) exhibited by individuals. Results We measured glucocorticoid levels in 43 wild-caught (n = 18) and rehabilitated (n = 25) hedgehogs and compared the post release survival and spatial behaviour of 18 translocated juvenile hedgehogs (eight hand-raised and ten wild) until hibernation. The possible effect on survival of differences in shy or bold behaviour (personality) exhibited by 17 juvenile individuals (seven hand-raised and ten wild) was also examined. Rehabilitated individuals and females had higher levels of faecal corticosterone metabolites compared to wild individuals and males, respectively. Rehabilitated individuals showed higher levels of saliva corticosterone than wild. The personality tests labelled 13 individuals as shy and 11 as bold. Post release survival was 57% for rehabilitated and 50% for wild individuals. Neither background nor personality affected post release survival. Home range measures were 3.54 and 4.85 ha. Mean dispersal length from the release sites was 217 ± 100 m. Conclusion The higher levels of corticosterone observed in rehabilitated compared to wild hedgehogs calls for consideration of the duration of admission to wildlife rehabilitation centres to reduce stress levels in the patients. Hand-raised juveniles appear to have the same prospects as wild, and personality does not seem to affect post release survival in hedgehogs, indicating that hand-raising of orphaned juvenile hedgehogs is a relevant contribution to the conservation of this species.

Từ khóa


Tài liệu tham khảo

Reeve N. Hedgehogs. London: Poyser; 1994.

Morris P. Hedgehogs. Stansted, Essex: Whittet Books Ltd.; 2014.

Müller F. Langzeit-Monitoring der Strassenverkehrsopfer beim Igel (Erinaceus europaeus L.) zur Indikation von Populationsdichteveränderungen entlang zweier Teststrecken im Landkreis Fulda. Beiträge zur Naturkunde in Osthessen. 2018;54:21–6.

SoBH. The state of Britain's Hedgehogs 2011. In: Edited by Wembridge D. British Trust for Ornithology (BTO) commissioned by People's Trust for Endangered Species (PTES) and the British Hedgehog Preservation Society (BHPS); 2011.

SoBH. The State of Britain’s Hedgehogs 2015. In.: British Hedgehog Preservation Society and People’s Trust for Endangered Species; 2015.

SoBH. The State of Britain’s Hedgehogs 2018. In: Edited by Wilson E, Wembridge D. British Hedgehog Preservation Society and People’s Trust for Endangered Species; 2018.

Hof AR, Bright PW. Quantifying the long-term decline of the West European hedgehog in England by subsampling citizen-science datasets. Eur J Wildl Res. 2016;62(4):407–13.

Krange M. Change in the occurrence of the West European Hedgehog (Erinaceus europaeus) in western Sweden during 1950–2010. MSc thesis. Sweden: Karlstad University; 2015.

van de Poel JL, Dekker J, van Langevelde F. Dutch hedgehogs Erinaceus europaeus are nowadays mainly found in urban areas, possibly due to the negative effects of badgers Meles meles. Wildl Biol. 2015;21(1):51–5.

Williams BM, Baker PJ, Thomas E, Wilson G, Judge J, Yarnell RW. Reduced occupancy of hedgehogs (Erinaceus europaeus) in rural England and Wales: the influence of habitat and an asymmetric intra-guild predator. Sci Rep. 2018;8(1):12156.

Brakes CR, Smith RH. Exposure of non-target small mammals to rodenticides: short-term effects, recovery and implications for secondary poisoning. J Appl Ecol. 2005;42(1):118–28.

Haigh A, O’Riordan RM, Butler F. Nesting behaviour and seasonal body mass changes in a rural Irish population of the Western hedgehog (Erinaceus europaeus). Acta Theriol. 2012;57(4):321–31.

Hof AR, Bright PW. The value of agri-environment schemes for macro-invertebrate feeders: hedgehogs on arable farms in Britain. Anim Conserv. 2010;13(5):467–73.

Huijser MP, Bergers PJM. The effect of roads and traffic on hedgehog (Erinaceus europaeus) populations. Biol Conserv. 2000;95(1):111–6.

Young RP, Davison J, Trewby ID, Wilson GJ, Delahay RJ, Doncaster CP. Abundance of hedgehogs (Erinaceus europaeus) in relation to the density and distribution of badgers (Meles meles). J Zool. 2006;269(3):349–56.

Hubert P, Julliard R, Biagianti S, Poulle M-L. Ecological factors driving the higher hedgehog (Erinaceus europeaus) density in an urban area compared to the adjacent rural area. Landsc Urban Plan. 2011;103(1):34–43.

Dowding CV, Harris S, Poulton S, Baker PJ. Nocturnal ranging behaviour of urban hedgehogs, Erinaceus europaeus, in relation to risk and reward. Anim Behav. 2010;80(1):13–21.

Dowding CV, Shore RF, Worgan A, Baker PJ, Harris S. Accumulation of anticoagulant rodenticides in a non-target insectivore, the European hedgehog (Erinaceus europaeus). Environ Pollut. 2010;158(1):161–6.

Wright PG, Coomber FG, Bellamy CC, Perkins SE, Mathews F. Predicting hedgehog mortality risks on British roads using habitat suitability modelling. PeerJ. 2020;7:e8154.

Rasmussen SL, Nielsen JL, Jones OR, Berg TB, Pertoldi C. Genetic structure of the European hedgehog (Erinaceus europaeus) in Denmark. PLoS ONE. 2020;15(1):e0227205.

Rasmussen SL, Yashiro E, Sverrisdóttir E, Nielsen KL, Lukassen MB, Nielsen JL, Asp T, Pertoldi C. Applying the GBS technique for the genomic characterization of a Danish population of European Hedgehogs (Erinaceus europaeus). Genet Biodivers (GABJ). 2019;3(2):78–86.

Rasmussen SL, Berg TB, Dabelsteen T, Jones OR. The ecology of suburban juvenile European hedgehogs (Erinaceus europaeus) in Denmark. Ecol Evol. 2019;9:13174–87.

Pettett CE, Moorhouse TP, Johnson PJ, Macdonald DW. Factors affecting hedgehog (Erinaceus europaeus) attraction to rural villages in arable landscapes. Eur J Wildl Res. 2017;63(3):12.

Walhovd H. Winter activity of Danish hedgehogs in 1973–74 with information on the size of the animals observed and location of the recordings. Flora og Fauna. 1976;82(2):35–42.

Jensen AB. Overwintering of European hedgehogs Erinaceus europaeus in a Danish rural area. Acta Theriol. 2004;49(2):145–55.

Walhovd H. Records of young hedgehogs (Erinaceus europaeus L.) in a private garden. Zeitschrift Fur Saugetierkunde. 1990;55(5):289–97.

Walhovd H. The overwintering pattern of Danish hedgehogs in outdoor confinement, during three successive winters. Natura Jutlandica. 1978;20:273–84.

Artsfredningsbekendtgørelsen BEK nr 1466 af 06/12/2018 [https://www.retsinformation.dk/eli/lta/2018/1466].

Guy AJ, Curnoe D, Banks PB. A survey of current mammal rehabilitation and release practices. Biodivers Conserv. 2013;22(4):825–37.

Molony SE, Dowding CV, Baker PJ, Cuthill IC, Harris S. The effect of translocation and temporary captivity on wildlife rehabilitation success: an experimental study using European hedgehogs (Erinaceus europaeus). Biol Conserv. 2006;130(4):530–7.

Molony SE, Baker PJ, Garland L, Cuthill IC, Harris S. Factors that can be used to predict release rates for wildlife casualties. Anim Welf. 2007;16(3):361–7.

Romero LM, Wingfield JC. Alterations in hypothalamic-pituitary-adrenal function associated with captivity in Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii). Comp Biochem Physiol B. 1999;122(1):13–20.

Harper JM, Austad SN. Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen Comp Endocrinol. 2001;123(3):337–44.

MacArthur RA, Geist V, Johnston RH. Cardiac responses of bighorn sheep to trapping and radio instrumentation. Can J Zool. 1986;64(5):1197–200.

Wingfield JC, et al. Environmental stress, field endocrinology, and conservation biology. In: Clemmons JR, Buchholz R, editors. Behavioral approaches to conservation in the wild. London: Cambridge University Press; 1997. p. 95–131.

Boissy A. Fear and fearfulness in animals. Q R Biol. 1995;70(2):165–91.

Adams LW, Hadidian J, Flyger V. Movement and mortality of translocated urban-suburban grey squirrels. Anim Welf. 2004;13(1):45–50.

Letty J, Marchandeau S, Clobert J, Aubineau J. Improving translocation success: an experimental study of anti-stress treatment and release method for wild rabbits. Anim Conserv. 2000;3:211–9.

Terio KA, Marker L, Munson L. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J Wildl Dis. 2004;40(2):259–66.

Dickens MJ, Delehanty DJ, Romero LM. Stress: an inevitable component of animal translocation. Biol Conserv. 2010;143(6):1329–41.

Carlstead K. Effects of captivity on the behavior of wild mammals. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity: principles and techniques. Chicago: University of Chicago Press; 1996. p. 317–333.

Newman SH, Anderson DW, Ziccardi MH, Trupkiewicz JG, Tseng FS, Christopher MM, Zinkl JG. An experimental soft-release of oil-spill rehabilitated American coots (Fulica americana): II. Effects on health and blood parameters. Environ Pollut. 2000;107(3):295–304.

Robertson CPJ, Harris S. The behaviour after release of captive-reared fox cubs. Anim Welf. 1995;4(4):295–306.

Collins R, Brazier H, Whelan J. Rehabilitating a herd of oiled mute swans Cygnus olor. Biol Environ. 1994;94B(1):83–9.

Breed D, Meyer LCR, Steyl JCA, Goddard A, Burroughs R, Kohn TA. Conserving wildlife in a changing world: understanding capture myopathy—a malignant outcome of stress during capture and translocation. Conserv Physiol. 2019. https://doi.org/10.1093/conphys/coz027.

Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R. Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia. 2011;166(4):869–87.

Koolhaas JM, Bartolomucci A, Buwalda B, de Boer SF, Flugge G, Korte SM, Meerlo P, Murison R, Olivier B, Palanza P, et al. Stress revisited: a critical evaluation of the stress concept. Neurosci Biobehav Rev. 2011;35(5):1291–301.

Nemeth M, Pschernig E, Wallner B, Millesi E. Non-invasive cortisol measurements as indicators of physiological stress responses in guinea pigs. PeerJ. 2016;4:e1590.

Menargues A, Urios V, Mauri M. Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Anim Welf. 2008;17:305–12.

Eriksson E, Royo F, Lyberg K, Carlsson HE, Hau J. Effect of metabolic cage housing on immunoglobulin A and corticosterone excretion in faeces and urine of young male rats. Exp Physiol. 2004;89(4):427–33.

Ganswindt A, Palme R, Heistermann M, Borragan S, Hodges J. Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen Comp Endocrinol. 2003;134(2):156–66.

Weaver S, Hynd P, Ralph C, Edwards JH, Burnard C, Narayan E, Tilbrook A. Chronic elevation of plasma cortisol causes differential expression of predominating glucocorticoid in plasma, saliva, fecal, and wool matrices in sheep. Domest Anim Endocrinol. 2021;74:106503.

Reale D, Martin J, Coltman DW, Poissant J, Festa-Bianchet M. Male personality, life-history strategies and reproductive success in a promiscuous mammal. J Evol Biol. 2009;22(8):1599–607.

Bremner-Harrison S, Prodohl PA, Elwood RW. Behavioural trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim Conserv. 2004;7:313–20.

Verbeek MEM, Drent PJ, Wiepkema PR. Consistent individual differences in early exploratory behavior of male great tits. Anim Behav. 1994;48(5):1113–21.

Frost AJ, Winrow-Giffen A, Ashley PJ, Sneddon LU. Plasticity in animal personality traits: does prior experience alter the degree of boldness? Proc R Soc B. 2007;274(1608):333–9.

Wilson DS, Coleman K, Clark AB, Biederman L. Shy bold continuum in pumpkinseed sunfish Lepomis gibbosus—an ecological study of a psychological trait. J Comp Psychol. 1993;107(3):250–60.

Smith BR, Blumstein DT. Fitness consequences of personality: a meta-analysis. Behav Ecol. 2008;19(2):448–55.

Boon AK, Reale D, Boutin S. Personality, habitat use, and their consequences for survival in North American red squirrels Tamiasciurus hudsonicus. Oikos. 2008;117(9):1321–8.

Stuart-Smith AK, Boutin S. Behavioural differences between surviving and depredated juvenile red squirrels. Ecoscience. 1995;2(1):34–40.

Reale D, Festa-Bianchet M. Predator-induced natural selection on temperament in bighorn ewes. Anim Behav. 2003;65:463–70.

Dingemanse NJ, Both C, Drent PJ, Tinbergen JM. Fitness consequences of avian personalities in a fluctuating environment. Proc R Soc B. 2004;271(1541):847–52.

Dingemanse NJ, Réale D. Natural selection and animal personality. Behaviour. 2005;142(9–10):1159–84.

Sæther HM. Overlevelse og tidlig spredning hos juvenile piggsvin (Erinaceus europaeus). MSc thesis. Norway: Norges Teknisk-Naturvitenskapelige Universitet; 1997.

Kristiansson H. Population variables and causes of mortality in a hedgehog (Erinaceus europaeus) population in southern Sweden. J Zool. 1990;220:391–404.

Rasmussen SL. Personality, survivability and spatial behaviour of juvenile hedgehogs (Erinaceus europaeus): a comparison between rehabilitated and wild individuals. MSc thesis. Denmark: University of Copenhagen; 2013.

Morris P. Released, rehabilitated hedgehogs: a follow-up study in Jersey. Anim Welf. 1997;6(4):317–27.

Morris P, Munn S, Craig-Wood S. The effects of releasing captive hedgehogs (Erinaceus europaeus) into the wild. Field Stud. 1992;8:89–99.

Morris P, Warwick H. A study of rehabilitated juvenile hedgehogs after release into the wild. Anim Welf. 1994;3(3):163–77.

Morris P, Meakin K, Sharafi S. The behaviour and survival of rehabilitated hedgehogs (Erinaceus europaeus). Anim Welf. 1993;2(1):53–66.

Reeve NJ. The survival and welfare of hedgehogs (Erinaceus europaeus) after release back into the wild. Anim Welf. 1998;7(2):189–202.

Sainsbury A, Cunningham A, Morris P, Kirkwood J, Macgregor S. Health and welfare of rehabilitated juvenile hedgehogs (Erinaceus europaeus) before and after release into the wild. Vet Rec. 1996;138(3):61–5.

Yarnell RW, Surgey J, Grogan A, Thompson R, Davies K, Kimbrough C, Scott DM. Should rehabilitated hedgehogs be released in winter? A comparison of survival, nest use and weight change in wild and rescued animals. Eur J Wildl Res. 2019;65(1):1–10.

Warwick H, Morris P, Walker D. Survival and weight changes of hedgehogs (Erinaceus europaeus) translocated from the Hebrides to Mainland Scotland. Lutra. 2006;49(2):89–102.

Seaman DE, Millspaugh JJ, Kernohan BJ, Brundige GC, Raedeke KJ, Gitzen RA. Effects of sample size on kernel home range estimates. J Wildl Manag. 1999;63(2):739–47.

Chelini MO, Otta E, Yamakita C, Palme R. Sex differences in the excretion of fecal glucocorticoid metabolites in the Syrian hamster. J Comp Physiol B. 2010;180(6):919–25.

Jensen MA, Moseby KE, Paton DC, Fanson KV. Non-invasive monitoring of adrenocortical physiology in a threatened Australian marsupial, the western quoll (Dasyurus geoffroii). Conserv Physiol. 2019;7(1):coz069.

Kalliokoski O, Timm JA, Ibsen IB, Hau J, Frederiksen A-MB, Bertelsen MF. Fecal glucocorticoid response to environmental stressors in green iguanas (Iguana iguana). Gen Comp Endocrinol. 2012;177(1):93–7.

Polich RL. Stress hormone levels in a freshwater turtle from sites differing in human activity. Conserv Physiol. 2016;4(1):cow016.

Rettenbacher S, Möstl E, Hackl R, Ghareeb K, Palme R. Measurement of corticosterone metabolites in chicken droppings. Br Poult Sci. 2004;45(5):704–11.

Fowler PA. Seasonal endocrine cycles in the European hedgehog, Erinaceus europaeus. J Reprod Fertil. 1988;84:259–72.

Hoo-Paris R. Hibernation et sécrétion corticotrope hypophysaire du hérisson (Erinaceus europaeus L.). Ann Endocrinol. 1971;32(6):743–52.

Hoo-Paris R. Études de quelques aspects de la fonction surrénalienne en relation avec le métabolisme glucidique et le métabolisme minéral chez le Hérisson (Erinaceus europaeus L.) exposé au froid. Ann Endocrinol. 1974;35:341–9.

Kirkebø A. Corticosteroids in plasma from hibernating and nonhibernating hedgehogs, Erinaceus europaeus L., vol. 2. Bergen: Norwegian Universities Press; 1964.

Saboureau M, Bobet JP, Boissin J. Cyclic activity of adrenal function and seasonal variations of cortisol peripheral metabolism in a hibernating mammal, the hedgehog (Erinaceus europaeus L.). J Physiol. 1980;76(6):617–29.

Saboureau M, Laurent G, Boissin J. Daily and seasonal rhythms of locomotor activity and adrenal function in male hedgehogs (Erinaceus europaeus L.). J Interdiscipl Cycle Res. 1979;10(4):249–66.

Werner R, Vens-Cappell F. Changes in plasma cortisol during acute cold exposure in euthermic European hedgehogs: thermoregulatory role of the hypothalamo-pituitary-adrenal axis. J Comp Physiol B. 1985;155:219–26.

Werner R, Wünnenberg W. Effect of the adrenocorticostatic agent, Metopirone, on thermoregulatory heat production in the European hedgehog. Pfügers Archiv. 1980;385:25–8.

Ottenweller JE, Tapp WN, Burke JM, Natelson BH. Plasma cortisol and corticosterone concentrations in the golden hamster, (Mesocricetus auratus). Life Sci. 1985;37(16):1551–8.

Koren L, Whiteside D, Fahlman Å, Ruckstuhl K, Kutz S, Checkley S, Dumond M, Wynne-Edwards K. Cortisol and corticosterone independence in cortisol-dominant wildlife. Gen Comp Endocrinol. 2012;177(1):113–9.

Solomon MB, Sakai RR, Woods SC, Foster MT. Differential effects of glucocorticoids on energy homeostasis in Syrian hamsters. Am J Physiol Endocrinol Metab. 2011;301(2):E307–16.

Reeder DM, Kosteczko NS, Kunz TH, Widmaier EP. Changes in baseline and stress-induced glucocorticoid levels during the active period in free-ranging male and female little brown myotis, Myotis lucifugus (Chiroptera: Vespertilionidae). Gen Comp Endocrinol. 2004;136(2):260–9.

Archard GA, Braithwaite VA. The importance of wild populations in studies of animal temperament. J Zool. 2010;281(3):149–60.

Reale D, Gallant BY, Leblanc M, Festa-Bianchet M. Consistency of temperament in bighorn ewes and correlates with behaviour and life history. Anim Behav. 2000;60:589–97.

Fucikova E, Drent PJ, Smits N, van Oers K. Handling stress as a measurement of personality in great tit nestlings (Parus major). Ethology. 2009;115(4):366–74.

Yarnell K, Hall C, Billett E. An assessment of the aversive nature of an animal management procedure (clipping) using behavioral and physiological measures. Physiol Behav. 2013;118:32–9.

Morris P. Hedgehog. Hedgehog [New Naturalist Vol 137] 2018:i-ix, 1–404.

Palme R. Non-invasive measurement of glucocorticoids: advances and problems. Physiol Behav. 2019;199:229–43.

Pettett CE, Johnson PJ, Moorhouse TP, Macdonald DW. National predictors of hedgehog Erinaceus europaeus distribution and decline in Britain. Mammal Rev. 2018;48(1):1–6.

Jones KA, Godin J-GJ. Are fast explorers slow reactors? Linking personality type and anti-predator behaviour. Proc R Soc B. 2010;277(1681):625–32.

Blaszczyk MB. Boldness towards novel objects predicts predator inspection in wild vervet monkeys. Anim Behav. 2017;123:91–100.

Riber AB. Habitat use and behaviour of European hedgehog Erinaceus europaeus in a Danish rural area. Acta Theriol. 2006;51(4):363–71.

Campbell PA. The feeding behaviour of the hedgehog Erinaceus europaeus in pasture land in New Zealand. N Zeal Ecol Soc Proc. 1973;20:35–40.

Wroot AJ. Feeding ecology of the European hedgehog Erinaceus europaeus. PhD thesis. Royal Holloway, University of London; 1984.

Swihart RK, Slade NA. Testing for independence of observations on animal movements. Ecology. 1985;66(4):1176–84.

R Core Team. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2019.

IBM Corp. IBM SPSS statistics for windows, version 25.0. Armonk, NY: IBM Corp.; 2017.