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Increased hormonal stress response of Apennine chamois induced by interspecific interactions and anthropogenic disturbance

  • Nicoletta Formenti
  • Roberto Viganó
  • Cristina Fraquelli
  • Tiziana Trogu
  • Marta Bonfanti
  • Paolo Lanfranchi
  • Rupert Palme
  • Nicola Ferrari
Original Article

Abstract

Responses of animals to environmental changes and their interactions with other species play an important role in conservation. Sharing a common habitat may lead to interspecific competition for resources, but field assessment of these biological events is not always easily accomplished. By using a non-invasive method, we evaluated the physiological stress responses of Apennine chamois (Rupicapra pyrenaica ornata) to the presence of cattle, sheep and goat, red deer (Cervus elaphus), people (hikers), and predators to identify which factors may affect this endangered species. During September 2012, November 2012, and July 2013, a total of 318 faecal samples were collected in representative sites and analysed for faecal cortisol metabolites (FCM). FCM concentration was analysed through linear mixed-effect models. A significant increase in FCM values in Apennine chamois sharing their habitat with domestic animals was recorded during all study periods. On the contrary, stress responses to red deer and people were limited in time and emerged only during summer months, when hikers are more frequent and red deer extend their altitudinal range reaching chamois’ habitat. The observed effects of domestic animals, red deer, and hikers should be considered in future Apennine chamois management plans, which should include the regulation of pastured domestic livestock, anthropogenic disturbances, and possible interferences with other wild species within parks.

Keywords

Competition Rupicapra pyrenaica ornata Cervus elaphus Domestic ruminants Human activities Glucocorticoids 

Notes

Acknowledgements

The authors are grateful to Sarah Perkins and Claudia Romeo for their contribution during editing and to anonymous reviewers and EJWR’ editors who greatly helped us to improve the manuscript through their constructive comments. We thank Loredana Bisegna for her suggestions in the text-editing process.

Funding

This research was supported by the ‘Project LIFE09 NAT/IT/000183 Coornata’ and partly by the Italian Ministry of University and Research (PRIN project no. 2010P7LFW4).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants performed by any of the authors.

References

  1. Anderwald P, Herfindal I, Haller RM, Risch AC, Schütz M, Schweiger AK, Filli F (2015) Influence of migratory ungulate management on competitive interactions with resident species in a protected area. Ecosphere 6(11):228CrossRefGoogle Scholar
  2. Antonucci A, Di Domenico G, Gentile D, Artese C (2010a) Documento operativo sulle corrette procedure per l’individuazione dei nuclei di camoscio oggetto di prelievo per le immissioni in natura. www.camoscioappenninico.it. Accessed 11 Jan 2017
  3. Antonucci A, Di Domenico G, Gentile D, Latini R, Asprea A, Pagliaroli D, Artese C (2010b) Protocollo per il controllo dei branchi e degli individui di camoscio appenninico (Rupicapra pyrenaica ornata) nell’ambito del Progetto Life Coornata. LIFE09 NAT/IT/000183 COORNATA. “Development of coordinated protection measures for Apennine chamois (Rupicapra pyrenaica ornata)”. www.camoscioappenninico.it. Accessed 11 Jan 2017
  4. Arlettaz R, Nusslé S, Baltic M, Vogel P, Palme R, Jenni-Eiermann S, Patthey P, Genoud M (2015) Disturbance of wildlife by outdoor winter recreation: allostatic stress response and altered activity-energy budgets. Ecol Appl 25:1197–1212CrossRefGoogle Scholar
  5. Asprea A (2009) Status, monitoraggio e conservazione del camoscio appenninico (Rupicapra pyrenaica ornata) nel Parco Nazionale d’Abruzzo, Lazio e Molise – Struttura di popolazione. Report of the National Park of Abruzzo, Lazio and MoliseGoogle Scholar
  6. Begon M, Harper JL, Townsend CR (2006) Ecology. From individuals to ecosystems. Blackwell Science, OxfordGoogle Scholar
  7. Berducou C (1984) Spatial and trophic interactions between wild and domestic ungulates, in the French mountain national parks. In: Joss PJ, Lynch PW, Williams OB (eds) Rangelands – a resource under siege. Cambridge University Press, Cambridge, pp 390–391Google Scholar
  8. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135CrossRefGoogle Scholar
  9. Bruno E, Lovari S (1989) Foraging behaviour of adult female Apennine chamois in relation to seasonal variation in food supply. Acta Theriol 34:513–523CrossRefGoogle Scholar
  10. Caughley G (1978) Analysis of vertebrate populations. John Wiley and Sons, London 234 pp Google Scholar
  11. Cederna A, Lovari S (1985) The impact of tourism on chamois feeding activities in an area of the Abruzzo National Park. In: Lovari S (ed) The biology and management of mountain ungulates. Croom Helm, London, pp 212–215Google Scholar
  12. Chirichella R, Ciuti S, Apollonio M (2013) Effects of livestock and non-native mouflon on use of high-elevation pastures by Alpine chamois. Mamm Biol 78:344–350CrossRefGoogle Scholar
  13. Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. Univ. Chicago Press, ChicagoGoogle Scholar
  14. Corlatti L, Palme R, Frey-Roos F, Hackländer K (2011) Climatic cues and glucocorticoids in a free ranging riparian population of red deer (Cervus elaphus). Folia Zool 60:176–180CrossRefGoogle Scholar
  15. Corlatti L, Bethaz S, von Hardenberg A, Bassano B, Palme R, Lovari S (2012) Hormones, parasites and male mating tactics in Alpine chamois: identifying the mechanisms of life history trade-offs. Anim Behav 84:1061–1070CrossRefGoogle Scholar
  16. Corlatti L, Palme R, Lovari S (2014) Physiological response to etho-ecological stressors in male Alpine chamois: timescale matters! Naturwissenschaften 101:577–586CrossRefGoogle Scholar
  17. Crestanello B, Pecchioli E, Vernesi C, Mona S, Martínková N, Janiga M, Hauffe HC, Bertorelle G (2009) The genetic impact of translocations and habitat fragmentation in chamois (Rupicapra) spp. J Hered 100:691–708CrossRefGoogle Scholar
  18. Dalmau A, Ferret A, Manteca X (2010) Vigilance behavior of pyrenean chamois Rupicapra pyrenaica pyrenaica: effect of sex and position in the herd. Curr Zool 56:232–237Google Scholar
  19. Di Domenico G, Antonucci A, Angelucci S, Gentile D, Innocenti M, Carafa M, Madonna L (2015) The Apennine chamois in the Majella National Park, from a reintroduced population to a source population: results of monitoring activity and first experiences of wild chamois capture for reintroductions. In: Antonucci A, Di Domenico G (eds) Chamois international congress proceedings. 17-19 June 2014, lama dei Peligni. Majella National Park, Chieti, pp 1–12Google Scholar
  20. Duprè E, Monaco A, Pedrotti L (2001) Piano d’azione nazionale per il camoscio appenninico (Rupicapra pyrenaica ornata). Quaderni di Conservazione della Natura, 10 Ministero dell’Ambiente- Istituto Superiore per la Protezione e Ricerca Ambientale-ISPRAGoogle Scholar
  21. Fankhauser R, Galeffi C, Suter W (2008) Dung avoidance as a possible mechanism in competition between wild and domestic ungulates: two experiments with chamois Rupicapra rupicapra. Eur J Wildl Res 54:88–94CrossRefGoogle Scholar
  22. Ferrari C, Rossi G, Cavani C (1988) Summer food habits and quality of female, kid and subadult Apennine chamois, Rupicapra pyrenaica ornata (Neumann, 1899). Z Saugetierk 53:170–177Google Scholar
  23. Ferretti F, Corazza M, Campana I, Pietrocini V, Brunetti C, Scornavacca D, Lovari S (2015) Competition between wild herbivores: reintroduced red deer and Apennine chamois. Behav Ecol 26:550–559CrossRefGoogle Scholar
  24. Fichtel C, Kraus C, Ganswindt A, Heistermann M (2007) Influence of reproductive season and rank on fecal glucocorticoid levels in freeranging male Verreaux’s sifakas (Propithecus verreauxi). Horm Behav 51:640–648CrossRefGoogle Scholar
  25. Formenti N, Viganó R, Bionda R, Ferrari N, Trogu T, Lanfranchi P, Palme R (2015) Increased hormonal stress reactions induced in an Alpine Black Grouse (Tetrao tetrix) population by winter sports. J Ornithol 156:317–321CrossRefGoogle Scholar
  26. Huber S, Palme R, Arnold W (2003) Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). Gen Comp Endocrinol 130:48–54CrossRefGoogle Scholar
  27. Jachowski DS, McCorquodale S, Washburn BE, Millspaugh JJ (2015) Human disturbance and the physiological response of elk in eastern Washington. Wildl Biol Pract 11:12–25CrossRefGoogle Scholar
  28. Kleinsasser C, Graml C, Klobetz-Rassam E, Barth K, Waiblinger S, Palme R (2010) Physiological validation of a non-invasive method for measuring adrenocortical activity in goats. Wien Tierarztl Monat - Vet Med Austria 97:259–262Google Scholar
  29. Konjević D, JanickiZ SA, Severin K, Krapinec K, Božić F, Palme R (2011) Non-invasive monitoring of adrenocortical activity in free ranging fallow deer (Dama dama L.). Eur J Wildl Res 57:77–81CrossRefGoogle Scholar
  30. La Morgia V, Bassano B (2009) Feeding habits, forage selection, and diet overlap in Alpine chamois (Rupicapra rupicapra L.) and domestic sheep. Ecol Res 24:1043–1050CrossRefGoogle Scholar
  31. Largo E, Gaillard J-M, Festa-Bianchet M, Toïgo C, Bassano B, Cortot H, Farny G, Lequette B, Gauthier D, Martinot J-P (2008) Can ground counts reliably monitor ibex Capra ibex populations. Wildl Biol 14:489–499CrossRefGoogle Scholar
  32. LIFE Coornata Team (2015) FINAL Report of Project LIFE09 NAT/IT/000183 Coornata. http://ec.europa.eu/environment/life/project/Projects/index.cfm?fuseaction=home.showFile&rep=file&fil=LIFE09_NAT_IT_000183_FTR_IT.pdf. Accessed 11 Jan 2017
  33. Loison A, Appolinaire J, Jullien J-M, Dubray D (2006) How reliable are total counts to detect trends in population size of chamois Rupicapra rupicapra and R. pyrenaica? Wildl Biol 12:77–88CrossRefGoogle Scholar
  34. Lovari S, Cosentino R (1986) Seasonal habitat selection and group size of the Abruzzo chamois (Rupicapra pyrenaica ornata). Boll Zool 53:73–78CrossRefGoogle Scholar
  35. Lovari S, Ferretti F, Corazza M, Minder I, Troiani N, Ferrari C, Saddi A (2014) Unexpected consequences of reintroductions: competition between increasing red deer and threatened Apennine chamois. Anim Conserv 17:359–370CrossRefGoogle Scholar
  36. McCallum H (2000) Population parameters: estimation for ecological models. Blackwell Science, OxfordGoogle Scholar
  37. McCullough DR (1994) What do herd composition counts tell us? Wildl Soc Bull 22:295–300Google Scholar
  38. McCullough DR, Weckerly FW, Garcia PI, Evett RR (1993) Sources of inaccuracy in black-tailed deer herd composition counts. J Wildl Manag 58:319–329CrossRefGoogle Scholar
  39. McEwen BS (1998) Stress, adaptation, and disease: allostasis and allostatic load. Ann N Y Acad Sci 840:33–44CrossRefGoogle Scholar
  40. Mooring MS, Patton ML, Lance VA, Hall BM, Schaad EW, Fetter GA, Fortin SS, McPeak KM (2006) Glucocorticoids of bison bulls in relation to social status. Horm Behav 49:369–375CrossRefGoogle Scholar
  41. Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23:67–74CrossRefGoogle Scholar
  42. Möstl E, Maggs JL, Schrötter G, Besenfelder U, Palme R (2002) Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26:127–139CrossRefGoogle Scholar
  43. Munerato MS, Marques JA, Caulkett NA, Tomás WM, Zanetti ES, Trovati RG, Pereira GT, Palme R (2015) Hormonal and behavioural stress responses to capture and radio-collar fitting in free-ranging pampas deer (Ozotoceros bezoarticus). Anim Welf 24:437–446CrossRefGoogle Scholar
  44. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142CrossRefGoogle Scholar
  45. Palme R (2012) Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals. Anim Welf 21:331–337CrossRefGoogle Scholar
  46. Palme R, Robia C, Messmann S, Hofer J, Möstl E (1999) Measurement of fecal cortisol metabolites in ruminants: a noninvasive parameter of adrenocortical function. Wien Tierarztl Monatsschr 86:237–241Google Scholar
  47. Palme R, Rettenbacher S, Touma C, El-Bahr SM, Möstl E (2005) Stress hormones in mammals and birds: comparative aspects regarding metabolism, excretion, and noninvasive measurement in fecal samples. Ann N Y Acad Sci 1040:162–171CrossRefGoogle Scholar
  48. Palme R, Touma C, Arias N, Dominchin MF, Lepschy M (2013) Steroid extraction: get the best out of faecal samples. Wien Tierarztl Monat - Vet Med Austria 100:238–246Google Scholar
  49. Patterson IJ (1988) Responses of Apennine chamois to human disturbance. Z Saugetierk 53:245–252Google Scholar
  50. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0Google Scholar
  51. Rebollo S, Robles L, Gómez-Sal A (1993) The influence of livestock management on land use competition between domestic and wild ungulates: sheep and chamois Rupicapra pyrenaica parva Cabrera in the Cantabrian range. Pirineos 141-142:47–62CrossRefGoogle Scholar
  52. Rehnus M, Hackländer K, Palme R (2009) A non-invasive method for measuring glucocorticoid metabolites (GCM) in Mountain hares (Lepus timidus). Eur J Wildl Res 55:615–620CrossRefGoogle Scholar
  53. Rehnus M, Wehrle M, Palme R (2014) Mountain hares (Lepus timidus) and tourism activities: stress events and reactions. J Appl Ecol 51:6–12CrossRefGoogle Scholar
  54. Richard-Hansen C, Gonzalez G, Gerard J-F (1992) Structure sociale de l’isard (Rupicapra pyrenaica) dans trois sites pyrénéens. Gibier Faune Sauvage 9:137–149Google Scholar
  55. Santos JPV, Acevedo P, Carvalho J, Queirós J, Villamuelas M, Fonseca C, Gortázar C, López-Olvera JR, Vicente J (2018) The importance of intrinsic traits, environment and human activities in modulating stress levels in a wild ungulate. Ecol Indic 89:706–715CrossRefGoogle Scholar
  56. Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying Glucocorticoids. Oecologia 166:869–887CrossRefGoogle Scholar
  57. Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173CrossRefGoogle Scholar
  58. Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046:54–74CrossRefGoogle Scholar
  59. Zbyryt A, Bubnicki JW, Kuijper DPJ, Dehnhard M, Churski M, Schmidt K (2018) Do wild ungulates experience higher stress with humans than with large carnivores? Behav Ecol 29:19–30CrossRefGoogle Scholar
  60. Zwijacz-Kozica T, Selva N, Barja I, Silván G, Martínez-Fernández L, Illera JC, Jodłowski M (2013) Concentration of fecal cortisol metabolites in chamois in relation to tourist pressure in Tatra National Park (South Poland). Acta Theriol 58:215–222CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Veterinary MedicineUniversità degli Studi di MilanoMilanItaly
  2. 2.Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna “Bruno Ubertini”BresciaItaly
  3. 3.Studio Associato AlpVetBusto ArsizioItaly
  4. 4.Department of Biomedical SciencesUniversity of Veterinary MedicineWienAustria
  5. 5.Centro di Ricerca Coordinata Epidemiologia e Sorveglianza Molecolare delle InfezioniUniversità degli Studi di MilanoMilanItaly

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