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Low birth rates and reproductive skew limit the viability of Europe’s captive eastern black rhinoceros, Diceros bicornis michaeli

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Abstract

Ex situ populations play a critical role for the conservation of endangered species, especially where in situ populations face imminent threats. For such populations to act as vital reserves, they must be viable and sustainable. Eastern black rhinoceros (Diceros bicornis michaeli) epitomise the delicate nature of conservation, as a steady increase in the in situ population over the last two decades is threatened to reverse due to intense poaching pressures on rhinoceros across sub-Saharan Africa. This study utilized population viability analysis to evaluate the demographic and genetic viability of the European captive population of eastern black rhinoceros, and compared demographic parameters to in situ reference populations. Although self-sustaining, the ex situ population performs poorly relative to in situ counterparts, growing at a rate of only 1–2 % per annum compared to 6–8 % for managed wild populations. Captive females start reproducing later, have longer inter-calving intervals, and a lower proportion breed each year. Furthermore, over 40 % of reproductive-age animals have yet to reproduce, with additional implications for the maintenance of genetic diversity. Pedigree analysis highlights the unequal contribution of wild-caught founders to the current population; 69 % of which have no living descendants, and more than a third of the current population are related to five founders. This results in a current genome equivalent of just 13.39 equally reproducing founders. Although reproductive skew is not unusual in wild populations, it severely undermines efforts to maintain genetic and phenotypic diversity in captive breeding programmes. We suggest that understanding and alleviating the causes of reproductive skew must be an important consideration for small population management to maintain the genetic and demographic viability of ex situ populations.

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References

  • Akçakaya HR (2002) Estimating the variance of survival rates and fecundities. Anim Conserv 5:333–336

    Article  Google Scholar 

  • Armbruster P, Lande R (1993) A population viability analysis for African elephant (Loxodonta africana): how big should reserves be? Conserv Biol 7:602–610

    Article  Google Scholar 

  • Bakker VJ, Doak DF, Roemer GW, Garcelon DK, Coonan TJ, Morrison SA, Lynch C, Ralls K, Shaw R (2009) Incorporating ecological drivers and uncertainty into a demographic population viability analysis for the island fox. Ecol Monogr 79:77–108

    Article  Google Scholar 

  • Ballou JD, Lees C, Faust LJ, Long S, Lynch C, Bingaman Lackey L, Foose TJ (2010) Demographic and genetic management of captive populations. In: Kleiman DG, Thompson KV, Kirk Baer C (eds) Wild mammals in captivity: principles and techniques for zoo management. University of Chicago Press, Chicago and London, pp 219–252

    Google Scholar 

  • Beissinger SR, Westphal MI (1998) On the use of demographic models of population viability in endangered species management. J Wildl Manag 62:821–841

    Article  Google Scholar 

  • Biddle R, Pilgrim M (2011) Eastern Black Rhinoceros, Diceros bicornis michaeli, EEP annual studbook report 2011

  • Biddle R, Pilgrim M, (2013) Eastern Black Rhinoceros, Diceros bicornis michaeli, EEP annual studbook report 2013

  • Cain B, Wandera AB, Shawcross SG, Harris EW, Stevens-Wood B, Kemp SJ, Okita-Ouma B, Watts PC (2014) Sex-biased inbreeding effects on reproductive success and home range size of the critically endangered black rhinoceros. Conserv Biol 28:594–603

    Article  PubMed  Google Scholar 

  • Cant MA (1998) A model for the evolution of reproductive skew without reproductive suppression. Anim Behav 55:163–169

    Article  PubMed  Google Scholar 

  • Christensen BW, Troedsson MH, Young LJ, Oliva M, Penfold LM (2009) Effects of sociosexual environment on serum testosterone in captive male African rhinoceros. Theriogenology 71:1105–1111

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH (1988) Reproductive success: studies of individual variation in contrasting breeding systems. University of Chicago Press, Chicago

    Google Scholar 

  • Daleszczyk K, Bunevich AN (2009) Population viability analysis of European bison populations in Polish and Belarusian parts of Bialowieza Forest with and without gene exchange. Biol Conserv 142:3068–3075

    Article  Google Scholar 

  • Dennis PM, Rajala-Schultz PJ, Funk JA, Blumer ES, Miller RE, Wittum TE, Saville WJ (2007) Risk factors associated with a skewed natal sex ratio in captive black rhinoceroses (Diceros bicornis) in the United States. J Zoo Wildl Med 38:533–539

    Article  PubMed  Google Scholar 

  • du Toit R, Hearn M, Knight M, du Preez P, Rushworth I, Tindall B (2001) Report of working group 1: monitoring population performance. In: Emslie R (ed) SADC rhino management group (RMG) workshop on biological management to meet continental and national black rhino conservation goals. pp. 95–101, Giants Castle

  • Dunham AE, Erhart EM, Overdorff DJ, Wright PC (2008) Evaluating effects of deforestation, hunting, and El Nino events on a threatened lemur. Biol Conserv 141:287–297

    Article  Google Scholar 

  • Earnhardt JM, Thompson SD, Marhevsky EA (2001) Interactions of target population size, population parameters, and program management on viability of captive populations. Zoo Biol 20:169–183

    Article  Google Scholar 

  • Earnhardt JM, Thompson SD, Schad K (2004) Strategic planning for captive populations: projecting changes in genetic diversity. Anim Conserv 7:9–16

    Article  Google Scholar 

  • Edwards KL (2013) Investigating population performance and factors that influence reproductive success in the eastern black rhinoceros (Diceros bicornis michaeli). Thesis submitted in accordance with the requirements of the University of Liverpool for the degree of Doctor in Philosophy

  • Edwards KL, Shultz S, Pilgrim M, Walker SL (2015a) Irregular ovarian activity, body condition and behavioural differences are associated with reproductive success in female eastern black rhinoceros (Diceros bicornis michaeli). Gen Comp Endocrinol 214:186–194

    Article  CAS  PubMed  Google Scholar 

  • Edwards KL, Shultz S, Pilgrim M, Walker SL (2015b) Male reproductive success is correlated with testosterone in the eastern black rhinoceros (Diceros bicornis michaeli). Gen Comp Endocrinol 213:40–49

    Article  CAS  PubMed  Google Scholar 

  • Emslie R (2011) Diceros bicornis ssp. longipes., In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2

  • Emslie R (2012) Diceros bicornis, In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.2

  • Emslie RH (2013) African rhinoceroses—latest trends in rhino numbers and poaching. African Indaba, e-newsletter, pp. 11–12

  • Faust LJ, Thompson SD, Earnhardt JM (2006) Is reversing the decline of Asian elephants in North American zoos possible? An individual-based modeling approach. Zoo Biol 25:201–218

    Article  Google Scholar 

  • Foose TJ, Ballou JD (1988) Management of small populations. Int Zoo Yearb 27:26–41

    Article  Google Scholar 

  • Foose TJ, de Boer L, Seal US, Lande R (1995) Conservation management strategies based on viable populations. Population management for survival and recovery: analytical methods and strategies in small population conservation. Columbia University Press, New York, pp 273–294

    Google Scholar 

  • Foose, T.J., Wiese, R.J., 2006. Population management of rhinoceros in captivity. International Zoo Yearbook 40, 174-196

  • Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107

    Article  Google Scholar 

  • Frankham R, Ballou JD, Briscoe DA (2010) Introduction to conservation genetics, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Fyumagwa RD, Nyahongo JW (2010) Black rhino conservation in Tanzania: translocation efforts and further challenges. Pachyderm 47:59–65

    Google Scholar 

  • Garnier JN, Bruford MW, Goossens B (2001) Mating system and reproductive skew in the black rhinoceros. Mol Ecol 10:2031–2041

    Article  CAS  PubMed  Google Scholar 

  • Goddard J (1967) Home range, behaviour, and recruitment rates of two black rhinoceros populations. East Afr Wildl J 5:133–150

    Article  Google Scholar 

  • Gompper ME, Stacey PB, Berger J (1997) Conservation implications of the natural loss of lineages in wild mammals and birds. Conserv Biol 11:857–867

    Article  Google Scholar 

  • Hoffmann M, Hilton-Taylor C, Angulo A, Boehm M, Brooks TM, Butchart SHM, Carpenter KE, Chanson J, Collen B, Cox NA, Darwall WRT, Dulvy NK, Harrison LR, Katariya V, Pollock CM, Quader S, Richman NI, Rodrigues ASL, Tognelli MF, Vie J-C, Aguiar JM, Allen DJ, Allen GR, Amori G, Ananjeva NB, Andreone F, Andrew P, Aquino Ortiz AL, Baillie JEM, Baldi R, Bell BD, Biju SD, Bird JP, Black-Decima P, Blanc JJ, Bolanos F, Bolivar GW, Burfield IJ, Burton JA, Capper DR, Castro F, Catullo G, Cavanagh RD, Channing A, Chao NL, Chenery AM, Chiozza F, Clausnitzer V, Collar NJ, Collett LC, Collette BB, Fernandez CFC, Craig MT, Crosby MJ, Cumberlidge N, Cuttelod A, Derocher AE, Diesmos AC, Donaldson JS, Duckworth JW, Dutson G, Dutta SK, Emslie RH, Farjon A, Fowler S, Freyhof J, Garshelis DL, Gerlach J, Gower DJ, Grant TD, Hammerson GA, Harris RB, Heaney LR, Hedges SB, Hero JM, Hughes B, Hussain SA, Icochea MJ, Inger RF, Ishii N, Iskandar DT, Jenkins RKB, Kaneko Y, Kottelat M, Kovacs KM, Kuzmin SL, La Marca E, Lamoreux JF, Lau MWN, Lavilla EO, Leus K, Lewison RL, Lichtenstein G, Livingstone SR, Lukoschek V, Mallon DP, McGowan PJK, McIvor A, Moehlman PD, Molur S, Munoz Alonso A, Musick JA, Nowell K, Nussbaum RA, Olech W, Orlov NL, Papenfuss TJ, Parra-Olea G, Perrin WF, Polidoro BA, Pourkazemi M, Racey PA, Ragle JS, Ram M, Rathbun G, Reynolds RP, Rhodin AGJ, Richards SJ, Rodriguez LO, Ron SR, Rondinini C, Rylands AB, de Mitcheson YS, Sanciangco JC, Sanders KL, Santos-Barrera G, Schipper J, Self-Sullivan C, Shi Y, Shoemaker A, Short FT, Sillero-Zubiri C, Silvano DL, Smith KG, Smith AT, Snoeks J, Stattersfield AJ, Symes AJ, Taber AB, Talukdar BK, Temple HJ, Timmins R, Tobias JA, Tsytsulina K, Tweddle D, Ubeda C, Valenti SV, van Dijk PP, Veiga LM, Veloso A, Wege DC, Wilkinson M, Williamson EA, Xie F, Young BE, Akcakaya HR, Bennun L, Blackburn TM, Boitani L, Dublin HT, da Fonseca GAB, Gascon C, Lacher TE Jr, Mace GM, Mainka SA, McNeely JA, Mittermeier RA, Reid GM, Paul Rodriguez J, Rosenberg AA, Samways MJ, Smart J, Stein BA, Stuart SN (2010) The impact of conservation on the status of the world’s vertebrates. Science 330:1503–1509

    Article  CAS  PubMed  Google Scholar 

  • Hutchins M, Kreger MD (2006) Rhinoceros behaviour: implications for captive management and conservation. Int Zoo Yearb 40:150–173

    Article  Google Scholar 

  • ISIS (2004) SPARKS: single population animal record keeping system. International Species Information System, Apple Valley/Eagan, MN

  • IUCN (2002) Technical guidelines on the management of ex situ populations for conservation, In 14th Meeting of the Programme Committee of Council. Gland, Switzerland

  • Knight MH, Balfour D, Emslie RH (2013) Biodiversity management plan for the black rhinoceros (Diceros bicornis) in South Africa 2011–2020. Government Gazette (South Africa), pp. 1–80

  • KWS (2012) Conservation and management strategy for the Black Rhino (D. b. michaeli) in Kenya, (2012–2016), p. 57. Kenya Wildlife Service, Nairobi

  • Lacy RC (1989) Analysis of founder representation in pedigrees—founder equivalents and founder genome equivalents. Zoo Biol 8:111–123

    Article  Google Scholar 

  • Lacy RC, Ballou JD (2002) Population management 2000 user’s manual. Chicago Zoological Society, Brookfield

    Google Scholar 

  • Lande R, Barrowclough GF (1987) Effective population size, genetic variation, and their use in population management. In: Soule ME (ed) Viable populations for conservation. Cambridge University Press, Cambridge, pp 87–123

    Chapter  Google Scholar 

  • Lee AM, Saether B-E, Engen S (2011) Demographic stochasticity, Allee effects, and extinction: the influence of mating system and sex ratio. Am Nat 177:301–313

    Article  PubMed  Google Scholar 

  • Lees CM, Wilcken J (2009) Sustaining the ark: the challenges faced by zoos in maintaining viable populations. Int Zoo Yearb 43:6–18

    Article  Google Scholar 

  • Lees, C.M., Wilcken, J., 2011. Global programmes for sustainability, In WAZA magazine. pp. 2-5

  • Leimgruber P, Senior B, Uga, Aung M, Songer MA, Mueller T, Wemmer C, Ballou JD (2008) Modeling population viability of captive elephants in Myanmar (Burma): implications for wild populations. Anim Conserv 11:198–205

  • Lenz TL, Jacob A, Wedekind C (2007) Manipulating sex ratio to increase population growth: the example of the Lesser Kestrel. Anim Conserv 10:236–244

    Article  Google Scholar 

  • Leus K, Bingaman-Lackey L, van Lint W, de Man D, Riewald S, Veldkam A, Wijmans J (2011a) Sustainability of European Association of Zoos and Aquaria bird and mammal populations. WAZA Mag 12:11–14

    Google Scholar 

  • Leus K, Traylor-Holzer K, Lacy RC (2011b) Genetic and demographic population management in zoos and aquariums: recent developments, future challenges and opportunities for scientific research. Int Zoo Yearb 45:213–225

    Article  Google Scholar 

  • Link WA, Doherty PF (2002) Scaling in sensitivity analysis. Ecology 83:3299–3305

    Article  Google Scholar 

  • Long S, Dorsey C, Boyle P (2011) Status of Association of Zoos and Aquariums cooperatively managed populations. WAZA Mag 12:15–18

    Google Scholar 

  • McPhee ME, Carlstead K (2010) The importance of maintaining natural behaviours in captive mammals. In: Kleiman DG, Thompson KV, Baer CK (eds) Wild mammals in captivity: principles and techniques for zoo management. University of Chicago Press, Chicago, pp 303–313

    Google Scholar 

  • Milliken T, Shaw J (2012) The South Africa-Viet Nam rhino horn trade nexus: a deadly combination of institutional lapses, corrupt wildlife industry professionals and Asian crime syndicates. pp. 1–173, Johannesburg

  • Morris WF, Doak DF (2002) Quantitative conservation biology. Theory and practice of population viability analysis. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Nunney L (1996) The influence of variation in female fecundity on effective population size. Biol J Linn Soc 59:411–425

    Article  Google Scholar 

  • Nunney L, Elam DR (1994) Estimating the effective population size of conserved populations. Conserv Biol 8:175–184

    Article  Google Scholar 

  • Pilgrim M (2009) European regional black rhinoceros studbook 2009: Diceros bicornis

  • Pilgrim M, Biddle R (eds) (2014) EAZA Best practice guidelines black rhinoceros (Diceros bicornis)

  • Pollak JP, Lacy RC, Ballou JD (2002) Population management 2000. Chicago Zoological Society, Brookfield

    Google Scholar 

  • Roth TL (2006) A review of the reproductive physiology of rhinoceros species in captivity. Int Zoo Yearb 40:130–143

    Article  Google Scholar 

  • Rubenstein DI, Nunez CM (2009) Sociality and reproductive skew in horses and zebras. In: Hager R, Jones CB (eds) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge University Press, Cambridge, pp 196–226

    Chapter  Google Scholar 

  • Smith RL, Read B (1992) Management parameters affecting the reproductive potential of captive, female black rhinoceros, Diceros-bicornis. Zoo Biol 11:375–383

    Article  Google Scholar 

  • The MathWorks Inc (2008) MATLAB—the language of technical computing. The MathWorks Inc, Natick

    Google Scholar 

  • Williams SE, Hoffman EA (2009) Minimizing genetic adaptation in captive breeding programs: a review. Biol Conserv 142:2388–2400

    Article  Google Scholar 

  • Willis K, Wiese RJ (1993) Effect of new founders on retention of gene diversity in captive populations—a formalization of the nucleus population concept. Zoo Biol 12:535–548

    Article  Google Scholar 

  • Wittmer HU, Ahrens RNM, McLellan BN (2010) Viability of mountain caribou in British Columbia, Canada: effects of habitat change and population density. Biol Conserv 143:86–93

    Article  Google Scholar 

  • Wright S (1969) Evolution and the genetics of populations: the theory of gene frequencies. University of Chicago Press, Chicago

    Google Scholar 

  • Zeoli LF, Sayler RD, Wielgus R (2008) Population viability analysis for captive breeding and reintroduction of the endangered Columbia basin pygmy rabbit. Anim Conserv 11:504–512

    Article  Google Scholar 

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Acknowledgments

The authors would like to thank the Kenya Wildlife Service rhino programme for providing demographic information on in situ reference populations, and anonymous reviewers for constructive feedback on improving the manuscript. This work was funded by a NERC CASE studentship, and the North of England Zoological Society, with contribution from The Thriplow Charitable trust and the Association of British and Irish Wild Animal Keepers (ABWAK). S. Shultz is supported by a Royal Society University Research Fellowship.

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Correspondence to Katie L. Edwards.

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Communicated by Simon Ingram.

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Edwards, K.L., Walker, S.L., Dunham, A.E. et al. Low birth rates and reproductive skew limit the viability of Europe’s captive eastern black rhinoceros, Diceros bicornis michaeli . Biodivers Conserv 24, 2831–2852 (2015). https://doi.org/10.1007/s10531-015-0976-7

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