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

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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.

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References

  • 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):228

    Article  Google Scholar 

  • 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

  • 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

  • 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 25:1197–1212

    Article  Google Scholar 

  • 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 Molise

  • Begon M, Harper JL, Townsend CR (2006) Ecology. From individuals to ecosystems. Blackwell Science, Oxford

    Google Scholar 

  • 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 390–391

    Google Scholar 

  • 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 24:127–135

    Article  Google Scholar 

  • Bruno E, Lovari S (1989) Foraging behaviour of adult female Apennine chamois in relation to seasonal variation in food supply. Acta Theriol 34:513–523

    Article  Google Scholar 

  • Caughley G (1978) Analysis of vertebrate populations. John Wiley and Sons, London 234 pp

    Google Scholar 

  • 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 212–215

    Google Scholar 

  • 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 78:344–350

    Article  Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes. Univ. Chicago Press, Chicago

    Google Scholar 

  • 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 60:176–180

    Article  Google Scholar 

  • 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 84:1061–1070

    Article  Google Scholar 

  • Corlatti L, Palme R, Lovari S (2014) Physiological response to etho-ecological stressors in male Alpine chamois: timescale matters! Naturwissenschaften 101:577–586

    Article  CAS  Google Scholar 

  • 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 100:691–708

    Article  CAS  Google Scholar 

  • 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 56:232–237

    Google Scholar 

  • 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 1–12

    Google Scholar 

  • 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-ISPRA

  • 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 54:88–94

    Article  Google Scholar 

  • 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 53:170–177

    Google Scholar 

  • 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 26:550–559

    Article  Google Scholar 

  • 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 51:640–648

    Article  CAS  Google Scholar 

  • 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 156:317–321

    Article  Google Scholar 

  • 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 130:48–54

    Article  CAS  Google Scholar 

  • Jachowski DS, McCorquodale S, Washburn BE, Millspaugh JJ (2015) Human disturbance and the physiological response of elk in eastern Washington. Wildl Biol Pract 11:12–25

    Article  Google Scholar 

  • 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 97:259–262

    CAS  Google Scholar 

  • 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 57:77–81

    Article  Google Scholar 

  • La Morgia V, Bassano B (2009) Feeding habits, forage selection, and diet overlap in Alpine chamois (Rupicapra rupicapra L.) and domestic sheep. Ecol Res 24:1043–1050

    Article  Google Scholar 

  • 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 14:489–499

    Article  Google Scholar 

  • 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

  • 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 12:77–88

    Article  Google Scholar 

  • Lovari S, Cosentino R (1986) Seasonal habitat selection and group size of the Abruzzo chamois (Rupicapra pyrenaica ornata). Boll Zool 53:73–78

    Article  Google Scholar 

  • 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 17:359–370

    Article  Google Scholar 

  • McCallum H (2000) Population parameters: estimation for ecological models. Blackwell Science, Oxford

    Google Scholar 

  • McCullough DR (1994) What do herd composition counts tell us? Wildl Soc Bull 22:295–300

    Google Scholar 

  • McCullough DR, Weckerly FW, Garcia PI, Evett RR (1993) Sources of inaccuracy in black-tailed deer herd composition counts. J Wildl Manag 58:319–329

    Article  Google Scholar 

  • McEwen BS (1998) Stress, adaptation, and disease: allostasis and allostatic load. Ann N Y Acad Sci 840:33–44

    Article  CAS  Google Scholar 

  • 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 49:369–375

    Article  CAS  Google Scholar 

  • Möstl E, Palme R (2002) Hormones as indicators of stress. Domest Anim Endocrinol 23:67–74

    Article  Google Scholar 

  • Möstl E, Maggs JL, Schrötter G, Besenfelder U, Palme R (2002) Measurement of cortisol metabolites in faeces of ruminants. Vet Res Commun 26:127–139

    Article  Google Scholar 

  • 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 24:437–446

    Article  Google Scholar 

  • Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142

    Article  Google Scholar 

  • Palme R (2012) Monitoring stress hormone metabolites as a useful, non-invasive tool for welfare assessment in farm animals. Anim Welf 21:331–337

    Article  CAS  Google Scholar 

  • 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 86:237–241

    CAS  Google Scholar 

  • 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 1040:162–171

    Article  CAS  Google Scholar 

  • 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 100:238–246

    Google Scholar 

  • Patterson IJ (1988) Responses of Apennine chamois to human disturbance. Z Saugetierk 53:245–252

    Google Scholar 

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna ISBN 3-900051-07-0

    Google Scholar 

  • 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 141-142:47–62

    Article  Google Scholar 

  • 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 55:615–620

    Article  Google Scholar 

  • Rehnus M, Wehrle M, Palme R (2014) Mountain hares (Lepus timidus) and tourism activities: stress events and reactions. J Appl Ecol 51:6–12

    Article  Google Scholar 

  • Richard-Hansen C, Gonzalez G, Gerard J-F (1992) Structure sociale de l’isard (Rupicapra pyrenaica) dans trois sites pyrénéens. Gibier Faune Sauvage 9:137–149

    Google Scholar 

  • 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 89:706–715

    Article  Google Scholar 

  • Sheriff MJ, Dantzer B, Delehanty B, Palme R, Boonstra R (2011) Measuring stress in wildlife: techniques for quantifying Glucocorticoids. Oecologia 166:869–887

    Article  Google Scholar 

  • Stankowich T (2008) Ungulate flight responses to human disturbance: a review and meta-analysis. Biol Conserv 141:2159–2173

    Article  Google Scholar 

  • Touma C, Palme R (2005) Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann N Y Acad Sci 1046:54–74

    Article  CAS  Google Scholar 

  • 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 29:19–30

    Article  Google Scholar 

  • 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 58:215–222

    Article  Google Scholar 

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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).

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Author notes

  1. Nicoletta Formenti

    Present address: Istituto Zooprofilattico Sperimentale della Lombardia e dell’Emilia Romagna “Bruno Ubertini”, via Bianchi 7/9, 25124, Brescia, Italy

Authors and Affiliations

  1. Department of Veterinary Medicine, Università degli Studi di Milano, via Celoria 10, 20133, Milan, Italy

    Nicoletta Formenti, Tiziana Trogu, Marta Bonfanti, Paolo Lanfranchi & Nicola Ferrari

  2. Studio Associato AlpVet, Piazza Venzaghi 2, 21052, Busto Arsizio, VA, Italy

    Roberto Viganó & Cristina Fraquelli

  3. Department of Biomedical Sciences, University of Veterinary Medicine, Veterinärplatz 1, 1210, Wien, Austria

    Rupert Palme

  4. Centro di Ricerca Coordinata Epidemiologia e Sorveglianza Molecolare delle Infezioni, Università degli Studi di Milano, via Celoria 10, 20133, Milan, Italy

    Nicola Ferrari

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  1. Nicoletta Formenti
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Correspondence to Nicola Ferrari.

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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.

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Formenti, N., Viganó, R., Fraquelli, C. et al. Increased hormonal stress response of Apennine chamois induced by interspecific interactions and anthropogenic disturbance. Eur J Wildl Res 64, 68 (2018). https://doi.org/10.1007/s10344-018-1228-4

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  • DOI: https://doi.org/10.1007/s10344-018-1228-4

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