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Fecundity and population viability in female zoo elephants: problems and possible solutions

Published online by Cambridge University Press:  01 January 2023

R Clubb
Affiliation:
Wildlife Department, RSPCA, Wilberforce Way, Southwater, West Sussex RH13 9RS, UK
M Rowcliffe
Affiliation:
Institute of Zoology, Zoological Society of London, London NW1 4RY, UK
P Lee
Affiliation:
Department of Psychology, University of Stirling, Stirling FK9 4LA, UK Amboseli Trust for Elephants, PO Box 15135, 00509 Langata, Nairobi, Kenya
KU Mar
Affiliation:
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
C Moss
Affiliation:
Amboseli Trust for Elephants, PO Box 15135, 00509 Langata, Nairobi, Kenya
GJ Mason*
Affiliation:
Animal Sciences Dept, University of Guelph, Guelph N1G 2M7, Canada
*
* Contact for correspondence and requests for reprints: gmason@uoguelph.ca

Abstract

We previously reported that African (Loxodonta africana) and Asian (Elephas maximus) female elephants in European zoos have shorter adult lifespans than protected conspecifics in range countries. This effect was the cause of greatest concern in Asian elephants, and risk factors within this species included being zoo-born, transferred between zoos, and possibly removed early from the mother. Here, we investigate these risk factors further; assess fecundity and sustainability in European zoos; and propose testable hypotheses as to the causes of these animals’ problems. Although imported wild-born Asian elephants live longer than zoo-born conspecifics, being imported when juvenile or adult appears no more protective than being imported in infancy, suggesting that the benefits of being wild- rather than zoo-born are conferred early in life. Zoo-born Asian neonates are significantly heavier than those born to working animals in range countries, with a possible tendency to be fatter. In zoos, African elephants have tended to be removed from their mothers at older ages than young Asians, and were also transferred between zoos significantly less often: factors that could possibly underlie this species’ lower calf losses and improving adult survivorship in Europe. Both species have low fecundity in European zoos compared to in situ populations, and are not self-sustaining, declining at approximately 10% per annum if reliant on captive-bred females under historically prevailing conditions. Data from other species suggest that stress and/or obesity are parsimonious explanations for the suite of problems seen. We recommend specific screens for testing these hypotheses, and for potentially identifying vulnerable individuals within the extant zoo populations.

Type
Research Article
Copyright
© 2009 Universities Federation for Animal Welfare

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References

African Elephant Specialist Group 2003 Statement from the African Elephant Specialist Group of the IUCN Species Survival Commission on the removal of African Elephants for Captive Use. IUCN/SSC African Elephant Specialist Group: Mokuti Lodge, Namibia, AfricaGoogle Scholar
African Elephant Specialist Group 2004 Loxodonta africana. 2007 IUCN Red List of Threatened Species. www.iucnredlist.org. (Accessed 8 July 2008)Google Scholar
Albl, P 1971 Studies on assessment of physical condition in African elephants. Biological Conservation 3: 134140CrossRefGoogle Scholar
Ange, K, Crissey, SD, Doyle, C, Lance, K and Hintz, H 2001 A survey of African (Loxodonta africana) and Asian (Elephas maximus) Elephant diets and measured body dimensions compared to their estimated nutrient requirements. Proceedings of the Nutrition Advisory Group Conference 4: 514Google Scholar
Anthony, KRN, Connolly, SR and Hoegh-Guldberg, O 2007 Bleaching, energetics, and coral mortality risk: Effects of temperature, light, and sediment regime. Limnology and Oceanography 52: 716726CrossRefGoogle Scholar
Asian Elephant Specialist Group 1996 Elephas maximus. 2007 IUCN Red List of Threatened Species. www.iucnredlist.org. (Accessed 8 July 2008)Google Scholar
Bahr, NI, Pryce, CR, Dobeli, M and Martin, RD 1998 Evidence from urinary cortisol that maternal behaviour is related to stress in gorillas. Physiology and Behavior 64: 439–437CrossRefGoogle ScholarPubMed
Balmford, A, Leader-Williams, N and Green, MJB 1995 Parks or arks — where to conserve threatened mammals? Biodiversity and Conservation 4: 595607CrossRefGoogle Scholar
Balmford, A, Mace, G and Leader-Williams, N 1996 Designing the ark: Setting priorities for captive breeding. Conservation Biology 10: 719727CrossRefGoogle Scholar
Banks, WA, Phillips-Conroy, JE, Jolly, CE and Morley, JE 2001 Serum leptin levels in wild and captive populations of baboons (Papio spp): Implications for the ancestral role of leptin. Journal of Clinical Endocrinology & Metabolism 86: 43154320CrossRefGoogle Scholar
Baur, JA, Pearson, KJ, Price, NL, Jamieson, HA, Lerin, C, Kalra, A, Prabhu, W, Allard, JS, Lopez-Lluch, G, Lewis, K, Pistell, PJ, Poosala, S, Becker, KG, Boss, O, Gwinn, D, Wang, M, Ramaswamy, S, Fishbein, KW, Spencer, RG, Lakatta, EG, Le Couteur, D, Shaw, RJ, Navas, P, Puigserver, P, Ingram, DK, de Cabo, R and Sinclair, DA 2006 Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337342CrossRefGoogle ScholarPubMed
Bennett, PH 1999 Type 2 diabetes among the Pima Indians of Arizona: An epidemic attributable to environmental change? Nutrition Reviews 57: S51S54CrossRefGoogle ScholarPubMed
Blanc, JJ, Barnes, RFW, Craig, GC, Dublin, HT, Thouless, CR, Douglas-Hamilton, I and Hart, JA 2007 African Elephant Status Report 2007: An Update from the African Elephant Database. Occasional Paper of the IUCN Species Survival Commission No. 33. IUCN: Gland, SwitzerlandCrossRefGoogle Scholar
British Nutrition Foundation 1999 Obesity — the Report of the British Nutrition Foundation Task Force. Blackwell Science: Oxford, UKGoogle Scholar
Broom, DM and Johnson, KG 1993 Stress and Animal Welfare. Chapman & Hall: London, UKCrossRefGoogle Scholar
Brown, JL, Olson, D, Keele, M and Freeman, EW 2004 Survey of the reproductive cyclicity status of Asian and African elephants in North America. Zoo Biology 23: 309321CrossRefGoogle Scholar
Buff, PR, Dodds, AC, Morrison, CD, Whitley, NC, McFadin, EL, Daniel, JA, Djiane, J and Keisler, DH 2002 Leptin in horses: Tissue localization and relationship between peripheral concentrations of leptin and body composition. Journal of Animal Science 80: 29422948CrossRefGoogle Scholar
Capitanio, JP, Mendoza, SP, Lerche, NW and Mason, AW 1998 Social stress results in altered glucocorticoid regulation and shorter survival in simian acquired immune deficiency syndrome. Proceedings of the National Academy of Sciences, USA 95: 47144719CrossRefGoogle ScholarPubMed
Caswell, H 2000 Matrix Population Models: Construction, Analysis and Interpretation, 2nd Edition. Sinauer Associates: Sunderland, MA, USAGoogle Scholar
Caughley, G 1977 Analysis of Vertebrate Populations. Wiley: New York, USAGoogle Scholar
Cavigelli, SA and McClintock, MK 2003 Fear of novelty in infant rats predicts adult corticosterone dynamics and an early death. Proceedings of the National Academy of Science 100: 1613116136CrossRefGoogle Scholar
Cavigelli, SA, Yee, JR and McClintock, MK 2006 Infant temperament predicts life span in female rats that develop spontaneous tumors. Hormones and Behavior 50: 454462CrossRefGoogle ScholarPubMed
Chrousos, GP 2000 The role of stress and the hypothalamic-pituitary-adrenal axis in the pathogenesis of the metabolic syndrome: neuron-endocrine and target tissue-related causes. International Journal of Obesity 24: S50S55CrossRefGoogle Scholar
Clark, AM, Thornley, B, Tomlinson, L, Galletley, C and Norman, RJ 1998 Weight loss in obese infertile women results in improvement in reproductive outcome for all forms of fertility treatment. Human Reproduction 13: 15021505CrossRefGoogle ScholarPubMed
Clubb, R and Mason, G 2002 A Review of the Welfare of Elephants in European Zoos. RSPCA: Horsham, UKGoogle Scholar
Clubb, R and Mason, G 2003 Captivity effects on wide-ranging carnivores. Nature 410: 3536Google Scholar
Clubb, R and Mason, G 2007 Natural behavioural biology as a risk factor in carnivore welfare: how understanding species differences could help zoos redesign enclosures. Applied Animal Behaviour Science 102: 303328CrossRefGoogle Scholar
Clubb, R, Lee, P, Mar, KU, Moss, C, Rowcliffe, M and Mason, GJ 2008 Compromised survivorship in zoo elephants. Science 322: 1649CrossRefGoogle ScholarPubMed
Cronje, PB 2003 Foetal programming of immune competence. Australian Journal of Experimental Agriculture 43: 14271430CrossRefGoogle Scholar
Dale, RHI 2009 Birth statistics for African (Loxodonta africana) and Asian (Elephas maximus) elephants in human care: history and implications for elephant welfare. Zoo Biology, doi: 10.1002/zoo.20234CrossRefGoogle Scholar
Danese, A, Pariante, CM, Caspi, A, Taylor, A and Poulton, R 2007 Childhood maltreatment predicts adult inflammation in a life course study. Proceedings of the National Academy of Sciences 104: 13191324CrossRefGoogle Scholar
Del Giudice, GD, Fieberg, J, Riggs, MR, Carstensen Powell, M and Pan, W 2006 A long-term age-specific survival analysis of female white-tailed deer. Journal of Wildlife Management 70: 15561568CrossRefGoogle Scholar
Donaldson, R 2003 Experiences of Older Burglary Victims. Home Office Findings No 198. Home Office: London, UKGoogle Scholar
European Commission 2002 EC Zoo Directive 1999/22/EC. Zoo Licensing Act Amendment Regulations European Commission: Brussels, BelgiumGoogle Scholar
European Elephant Group (EEG) 2002 Elefanten in zoos und safariparks Europa. Schling Verlag: Munster, GermanyGoogle Scholar
Faust, L 2005 Technical Report on Demographic Analyses and Modeling of the North American African Elephant Population. African Elephant Modelling Technical Report, AZA. Association of Zoos and Aquariums: Silver Springs, Maryland, USAGoogle Scholar
Faust, LJ, Thompson, SD and Earnhardt, JM 2006 Is reversing the decline of Asian elephants in North American zoos possible? An individual-based modeling approach. Zoo Biology 25: 201218CrossRefGoogle Scholar
Fors, H, Matsuoka, H, Bosaeus, I, Rosberg, S, Wikland, KA and Bjarnson, R 1999 Serum leptin levels correlate with growth hormone secretion and body fat in children. Journal of Clinical Endocrinology & Metabolism 84: 35863590Google ScholarPubMed
Francis, D, Diorio, J, Liu, D and Meaney, J 1999 Nongenomic transmission across generations of maternal behavior and stress responses in the rat. Science 286: 11551158CrossRefGoogle ScholarPubMed
Freeman, EW, Weiss, E and Brown, JL 2004 Examination of the interrelationships of behavior, dominance status, and ovarian activity in captive Asian and African elephants. Zoo Biology 23: 431448CrossRefGoogle Scholar
Goswami, VR, Madhusudan, MD and Karanth, KU 2007 Application of photographic capture-recapture modelling to estimate demographic parameters for male Asian elephants. Animal Conservation 10: 391399CrossRefGoogle Scholar
Grambsch, PM and Therneau, TM 1994 Proportional hazards tests and diagnostics based on weighted residuals. Biometrika 81: 515526CrossRefGoogle Scholar
Ha, J, Robinette, RL and Sackett, GP 1999 Social housing and pregnancy outcome in captive pigtailed Macaques. American Journal of Primatology 47: 1531633.0.CO;2-D>CrossRefGoogle ScholarPubMed
Harris, M, Sherwin, S and Harris, S 2008 The welfare, housing and husbandry of elephants in UK zoos: final report. University of Bristol, DEFRA Science and Research Project WC05007, Bristol, UKGoogle Scholar
Hatt, JM and Clauss, M 2006 Feeding Asian and African elephants (Elephas maximus and Loxodonta africana) in captivity. International Zoology Yearbook 40: 8895CrossRefGoogle Scholar
Hayssen, V, van Tienhoven, A and van Tienhoven, A 1993 Asdell's Patterns of Mammalian Reproduction. Cornell University Press: Ithaca, USACrossRefGoogle Scholar
Hedges, S, Tyson, MJ, Sitompul, AF and Hammatt, H 2006 Why inter-country loans will not help Sumatra's elephants. Zoo Biology 25: 235246CrossRefGoogle Scholar
Hedges, S 2007 Conservation. In: Fowler, ME and Mikota, SK (eds) Biology, Medicine, and Surgery of Elephants pp 475490. Blackwell Publishing: UKGoogle Scholar
Hermes, R, Hildebrandt, TB and Göritz, F 2004 Reproductive problems directly attributable to long-term captivity: asymmetric reproductive aging. Animal Reproduction Science 82–83: 4960CrossRefGoogle ScholarPubMed
Hutchins, M and Keele, M 2006 Elephants importation from range countries: Ethical and practical considerations for accredited zoos. Zoo Biology 25: 219233CrossRefGoogle Scholar
International Species Inventory System (ISIS) 2002 Elephas maximus, Asian Elephant. Reference Ranges for Physiological Data Values (average values calculated for: females only). http://www.elephantcare.org/protodoc_files/Isis/isis2.htm (Accessed May 2009)Google Scholar
Janczak, AM, Pedersen, LJ, Rydhmer, L and Bakken, M 2003 Relation between early fear and anxiety-related behaviour and maternal ability in sows. Applied Animal Behavior Science 82: 121135CrossRefGoogle Scholar
Jimenez-Chillaron, JC and Patti, ME 2007 To catch up or not to catch up: is this the question? Lessons from animal models. Current Opinions in Endocrinology, Diabetes and Obesity 14: 2329CrossRefGoogle ScholarPubMed
Kaplan, JR and Manuck, SB 2004 Ovarian dysfunction, stress and disease: A primate continuum. ILAR Journal 45: 89115CrossRefGoogle ScholarPubMed
Kealy, RD, Lawler, BF, Ballam, JM, Mantz, SL, Biery, DN, Greeley, EH, Lust, G, Segre, M, Smith, GK and Stowe, HD 2002 Effects of diet restriction on life span and age-related changes in dogs. Journal of American Veterinary Medical Association 220: 13151320CrossRefGoogle ScholarPubMed
Keele, M, Lewis, K and Owens, T 2007 Asian Elephant (Elephus maximus) North American Regional Studbook Update 1 May 2005-16 July 2007. Association of Zoos and Aquariums: Silver Springs, Maryland, USAGoogle Scholar
Kiecolt-Glaser, JK, McGuire, L, Robles, TF and Glaser, R 2002 Emotions, morbidity, and mortality: new perspectives from psychoneuroimmunology. Annual Review of Psychology 53: 83107CrossRefGoogle ScholarPubMed
Kiecolt-Glaser, JK, Preacher, KJ, MacCallum, RC, Atkinson, C, Malarkey, WB and Glaser, R 2003 Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proceedings of the National Academy of Science 100: 90909095CrossRefGoogle ScholarPubMed
Kristensen, J, Vestergaard, M, Wisborg, K, Kesmodel, U, and J⊘rgen Secher, N 2005 Pre-pregnancy weight and the risk of still birth and neonatal death. BJOG: an International Journal of Obstetrics and Gynaecology 112: 403408CrossRefGoogle ScholarPubMed
Kronfeld, DS, Treiber, KH and Geor, RJ 2005 Comparison of nonspecific indications and quantitative methods for the assessment of insulin resistance in horses and ponies. Journal of American Veterinary Medical Association 226: 712719CrossRefGoogle ScholarPubMed
Kurt, F and Mar, DK 1996 Neonate mortality in captive Asian elephants (Elephas maximus). Zeitschrift für Säugetierkunde 61: 155164Google Scholar
Kurt, F and Kumarasinghe, JC 1998 Remarks on body growth and phenotypes in Asian elephant Elephas maximus. Acta Theriologica Supplement 5: 135153CrossRefGoogle Scholar
Lair, RC 1997 Gone Astray: The Care and Management of the Asian Elephant in Domesticity. FAO/RAP Publication 1997/16. FAO Regional Office for Asia and the Pacific: ThailandGoogle Scholar
Lewis, MH, Gluck, JP, Petitto, JM, Hensley, LL and Ozerd, H 2000 Early social deprivation in nonhuman primates: Long-term effects on survival and cell-mediated immunity. Biological Pshychiatry 47: 119126CrossRefGoogle ScholarPubMed
Mar, KU and Win, S 1997 Working elephants for the timber industry. Draught Animal News 26: 613Google Scholar
Mar, KU 2007 The demography and life history strategy of timber elephants in Myanmar. PhD Thesis, University College London, London, UK. http://www.zoo.cam.ac.uk.theses.htmGoogle Scholar
Mason, G and Veasey, J 2008 How should the psychological welfare of zoo elephants be investigated? In: Forthman, DL, Kane, LF and Waldau, PF (eds) An Elephant in the Room: the Science and Well Being of Elephants in Captivity pp 154174. Tufts University Cummings School of Veterinary Medicine's Center for Animals and Public Policy: North Grafton, MA, USAGoogle Scholar
Mason, G and Veasey, J 2009 How should the psychological well-being of zoo elephants be objectively investigated? Zoo Biology, in pressCrossRefGoogle Scholar
McCance, DR, Pettitt, DJ, Hanson, RL, Jacobsson, LTH, Knowler, WC and Bennett, PH 1994 Birth-weight and non-insulin-dependent diabetes - thrifty genotype, thrifty phenotype or surviving small baby genotype. British Medical Journal 308: 942945CrossRefGoogle ScholarPubMed
Moore, AS, Gonyou, HW, Stookey, JM and McLaren, DG 1994 Effect of group composition and pen size on behavior, productivity and immune response of growing pigs. Applied Animal Behaviour Science 40: 1330CrossRefGoogle Scholar
Moss, CJ 2001 The demography of an Africa elephant (Loxodonta africana) population in Amboseli, Kenya. Journal of Zoology 255: 145156CrossRefGoogle Scholar
Moss, CJ and Lee, PC Female reproductive strategies: individual life histories. In: Moss, CJ and Croze, H (eds) The Amboseli Elephant: a Long-term Perspective on a Long-lived Species. University of Chicago Press: Chicago, IL, USA, in pressGoogle Scholar
Olson, D and Wiese, RJ 2000 State of the North American African elephant population and projections for the future. Zoo Biology 19: 3113203.0.CO;2-O>CrossRefGoogle Scholar
Olson, D 2008 North American Regional Studbook for the African Elephant (Loxodonta africana). Association of Zoos and Aquariums: Silver Springs, Maryland, USAGoogle Scholar
Otten, W, Kanitz, M, Tuchscherer, M and Numberg, G 2001 Effects of prenatal restraint stress on hypothalamic-pituitary-adrenocortical and sympatho-adrenomedullary axis in neonatal pigs. Animal Science 73: 279287Google Scholar
Pryce, CR, Ruedi-Bettschen, D, Dettling, AC, Weston, A, Russig, H, Ferger, B and Feldon, J 2005 Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research. Neuroscience and Biobehavioral Reviews 29: 649674CrossRefGoogle ScholarPubMed
Raggi, P, Shaw, LJ, Berman, DS and Callister, TQ 2004 Prognostic value of coronary artery calcium screening in subjects with and without diabetes. Journal of the American College of Cardiology 43: 16631669CrossRefGoogle ScholarPubMed
Ramanthan, A and Mallapur, A 2008 A visual health assessment of captive Asian elephants (Elephas maximus) housed in India. Journal of Zoo & Wildlife Medicine 39: 148154CrossRefGoogle Scholar
Rasmussen, F and Johanssen, M 1998 The relation of weight, length and Ponderal index at birth to body mass index and overweight among 18-year-old males in Sweden. European Journal of Epidemiology 14: 373380CrossRefGoogle ScholarPubMed
Richman, LK, Montali, RJ, Garber, RL, Kennedy, MA, Lehnhardt, J, Hildebrandt, T, Schmitt, D, Hardy, D, Alcendor, DJ and Hayward, GS 1999 Novel endotheliotropic herpesviruses fatal for Asian and African elephants. Science 283: 11711176CrossRefGoogle ScholarPubMed
Rodríguez-Artalejo, F, Garcés, C, Gorgojo, L, López García, E, Martín-Moreno, JM, Benavente, M, del Barrio, JL, Rubio, R, Oretga, H, Fernandez, O and de Oya, M 2002 Dietary patterns among children aged 6-7 in four Spanish cities with widely differing cardiovascular mortality. European Journal of Clinical Nutrition 56: 141148Google ScholarPubMed
Royal College of Physicians 2004 Storing Up Problems: The Medical Case for a Slimmer Nation. Royal College of Physicians: London, UKGoogle Scholar
Samaras, TT, Eirick, H and Storms, LH 2003 Birthweight, rapid growth cancer and longevity: a review. Journal of the National Medical Association 95: 11701183Google ScholarPubMed
Saragusty, J, Hermes, R, Göritz, F, Schmitt, DL and Hildebrandt, TB 2008 Skewed birth sex ratio and premature mortality in elephants. Animal Reproduction Science. Oct 31 doi:10.1016/j.anireprosci.2008.10.019CrossRefGoogle Scholar
Siler, W 1979 Competing risk model for animal mortality. Ecology 60: 750757CrossRefGoogle Scholar
Singhal, A and Lucas, A 2004 Early origins of cardiovascular disease: is there a unifying hypothesis? The Lancet 363: 16421664CrossRefGoogle Scholar
Slotow, R, Garaï, ME, Reilly, B, Page, B and Carr, RD 2005 Population dynamics of elephants re-introduced to small fenced reserves in South Africa. South African Wildlife Research 35: 2332Google Scholar
Sukumar, R 1989 The Asian Elephant: Ecology and Management. Cambridge University Press: Cambridge, UKGoogle Scholar
Sukumar, R, Krishnamurthy, V, Wemmer, C and Rodden, M 1997 Demography of captive Asian elephants (Elephas maximus) in Southern India. Zoo Biology 16: 2632723.0.CO;2-8>CrossRefGoogle Scholar
Sukumar, R 2003 The Living Elephants: Evolutionary Ecology, Behaviour, and Conservation. Oxford University Press: Oxford, UKGoogle Scholar
Sukumar, R 2006 A brief review of the status, distribution and biology of wild Asian elephants. International Zoology Yearbook 40: 18CrossRefGoogle Scholar
Taylor, VJ and Poole, TB 1998 Captive breeding and infant mortality in Asian elephants: a comparison between twenty western zoos and three eastern elephant centers. Zoo Biology 17: 3113323.0.CO;2-C>CrossRefGoogle Scholar
Terio, KA, Marker, L and Munson, L 2004 Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. Journal of Wildlife Diseases 40: 259266CrossRefGoogle Scholar
Tiley, HA, Geor, RJ and McCutcheon, LJ 2007 Effects of dexamethasone on glucose dynamics and insulin sensitivity in healthy horses. American Journal of Veterinary Research 68: 753759CrossRefGoogle ScholarPubMed
van Aarde, RJ and Jackson, TP 2007 Megaparks for metapopulations: Addressing the causes of locally high elephant numbers in Southern Africa. Biological Conservation 134: 289297CrossRefGoogle Scholar
Vitetta, L, Anton, B, Cortizo, F and Sali, A 2005 Mind-Body Medicine: Stress and its impact on overall health and longevity. Annals of the New York Academy of Science 1057: 492505CrossRefGoogle ScholarPubMed
Waithaka, J, Osborne, L and Saiwana, L 1998 Captive breeding of elephants. Pachyderm 25: 100101Google Scholar
Whitehouse, AM and Kerley, GIH 2002 Retrospective assessment of long term conservation management of elephants in Addo Elephant National Park, South Africa. Oryx 36: 243248CrossRefGoogle Scholar
Wiese, RJ 2000 Asian elephants are not self sustaining in North America. Zoo Biology 19: 2993093.0.CO;2-Z>CrossRefGoogle Scholar
Wiese, RJ and Willis, K 2004 Calculation of longevity and life expectancy in captive elephants. International Zoo Yearbook 23: 365373Google Scholar
Wiese, RJ and Willis, K 2006 Population management of zoo elephants. Calculation of longevity and life expectancy in captive elephants. International Zoo Yearbook 40: 8087CrossRefGoogle Scholar
Wingfield, JC and Sapolsky, RM 2003 Reproduction and resistance to stress: when and how. Journal of Neuroendocrinology 15: 711724CrossRefGoogle ScholarPubMed
Wittemyer, G, Daballen, D, Rasmussen, H, Kahindi, P and Douglas-Hamilton, I 2005 Demographic status of elephants in the Sambusu and Buffalo Springs National Reserves, Kenya. African Journal of Ecology 43: 4447CrossRefGoogle Scholar
Zoo Licensing Act 1981 Statutory Instrument 2002, No 3080 Amendment (England and Wales). http://www.opsi.gov.uk/si/si2002/20023080.htmGoogle Scholar