Skip to main content
Advertisement
Browse Subject Areas
?

Click through the PLOS taxonomy to find articles in your field.

For more information about PLOS Subject Areas, click here.

  • Loading metrics

Welfare at Multiple Scales: Importance of Zoo Elephant Population Welfare in a World of Declining Wild Populations

  • Elissa Z. Cameron ,

    Contributed equally to this work with: Elissa Z. Cameron, Sadie J. Ryan

    elissa.cameron@canterbury.ac.nz

    Affiliations School of Biological Sciences, University of Canterbury, Christchurch, New Zealand, School of Biological Sciences, University of Tasmania, Hobart, Tasmania, Australia

  • Sadie J. Ryan

    Contributed equally to this work with: Elissa Z. Cameron, Sadie J. Ryan

    Affiliation Department of Geography, University of Florida, Gainesville, Florida, United States of America

In-situ elephant populations have been in decline for much of the last 200 years, driven by an inexorable combination of habitat loss and hunting for ivory, but with more recent and dramatic declines primarily driven by hunting [1]. Consequently, the distribution and sustainability of elephant populations are now better predicted by human factors than ecological ones [2], underscoring the importance of societal factors in the ongoing survival of elephants. Despite growing awareness of the conservation crisis, hunting pressure has not abated. Instead, there has been a recent surge in harvest rates [3,4], more than doubling of harvest since 2007 [5]. The rates are staggering, escalating from an estimated 40,000 African elephants killed in 2011 [4] and 41 tons of ivory seized, to possibly more than 10% of the remaining populations in 2013 (summarised in [6]). In April 2016, the Kenyan Wildlife Service burned the biggest stockpile of ivory since it began burning ivory in 1989, with 105 tonnes of ivory destroyed, representing 6000–7000 poached elephants [7,8]. Similar declines have been seen in forest [3,9] and Asian [10] elephants. The current harvest rate of elephants is unsustainable, creating a conservation crisis of global significance, with an immediate threat to their continued survival [11]. Novel genetic tracing techniques (e.g [6]) and strict anti-poaching law enforcement [5] are vital to conserve the remaining free-ranging elephant populations.

The significance of the current overharvesting crisis extends beyond obvious direct impacts on the number of elephants, to their demography, through a variety of influences. As large bodied mammals, with complex social interactions, social structures, and extended weaning periods, the impact of disruptions to demography are long-lasting. For example, matriarchs are a repository of social information [12], such that their loss can have a disproportionate impact on social cohesion, herd demography and fitness, and these effects can last for decades [13]. Furthermore, physiological stress can be increased in areas where elephants are exposed to anthropogenic stress [14,15], with potential impacts on reproductive senescence and lifetime reproductive success [16]. Finally, overharvesting can influence ecological dynamics beyond the harvested species, affecting larger food webs and ecological processes in the landscape [4,17]—including the loss of a large-scale ecological engineer and important seed-disperser [1821]. The disruption caused by poaching is likely to exacerbate issues of human-wildlife conflict involving elephants, affecting the lives and livelihoods of local human communities [2224]. This can also lead to the vicious cycle of ‘retaliatory’ killing, compounding population impacts. Therefore, the conservation crisis extends beyond the animals killed by poaching, to broad ecosystem and community impacts.

Populations experiencing dramatic declines in numbers become susceptible to a variety of demographic influences not seen in larger populations, and result in susceptibility to an extinction vortex. Many ‘wild’ populations of elephants are now clearly in the ‘small population’ biology paradigm, in terms of conservation [2527]. In addition, due to their extremely complex social system, large body size, and concomitant slow demographic turnover, plus potential for cultural isolation issues [28], understanding these influences is integral to managing for their survival. Consequently, all remnant populations of elephants become of vital importance to their continued existence, and can essentially be regarded as a metapopulation. Currently, only a minority of free-ranging elephants exist in large undisturbed protected areas [29]. Intensively managed populations in small reserves therefore become increasingly important for conservation, particularly since land tenure and type of land use impact conservation outcomes for elephants [30].

Intensively managed populations of elephants in small reserves closely resemble populations of elephants in zoo populations, some of which are kept in extensive enclosures, similar to small fenced reserves, and are important for future survival of the species. Valuable research conclusions can be based on non-wild populations, including both domestic and zoo animals [16,31], and in particular, factors that influence longevity, health and reproduction in zoo populations are likely to also play a role in wild populations, particularly those that are intensively managed. Furthermore, such information will be of particular value for future intensive conservation efforts, including translocations, reintroductions and possible rewilding (e.g. [32,33]). Thus, we call attention to the role of zoo elephant population research to in-situ conservation efforts, and stress the importance of understanding welfare, as a component of the scales of integral research into elephant conservation.

This collection of papers takes an epidemiological approach to exploring the connections between the daily lives of elephants in captivity and their welfare (introduced in [34]). By taking a multi-institutional approach, the collection is able to explore the overall trends in data without the usual small sample size issues that plague studies of animals in captivity [35]. As pointed out, the group of studies revealed that social and management factors were strongly implicated for multiple welfare indicators, while exhibit space was found to be less important [34]. The collection is timely, not only because of the broad public interest in captive animal care and management, as the authors themselves stress [34], but because amidst the global decline in elephants, these analyses have implications for conservation of a species in crisis, since welfare impacts demography, including longevity and reproductive success. Thus, effective research in captive facilities can fill key knowledge gaps, to which the series of papers contribute. By using a cross-institutional design, the authors are able to assess both institution-specific factors as well as factors that apply regardless of local management. In so doing, they assess factors associated with welfare, including housing and social environments [36], environmental enrichment [37], and social demography [38]. In addition, the authors assess impacts on physiological [39,40], physical [41,42] and behavioural outcomes [43,44], tying together patterns at multiple scales and dimensions.

This collection represents a timely collation of research using a collaborative, multi-institutional approach. This set of papers also represents the largest collected set of publications on the welfare of zoo elephants to date. Such a collaborative and innovative approach exemplifies the effort and research required to ensure the persistence of biodiversity globally, and elephants in particular.

Author Contributions

Wrote the paper: EZC SJR.

References

  1. 1. Milner-Gulland E, Beddington J. The exploitation of elephants for the ivory trade: an historical perspective. Proc R Soc Lond B Biol Sci. 1993;252: 29–37.
  2. 2. De Boer WF, van Langevelde F, Prins HH, de Ruiter PC, Blanc J, Vis MJ, et al. Understanding spatial differences in African elephant densities and occurrence, a continent-wide analysis. Biol Conserv. 2013;159: 468–476.
  3. 3. Maisels F, Strindberg S, Blake S, Wittemyer G, Hart J, Williamson EA, et al. Devastating decline of forest elephants in Central Africa. PloS One. 2013;8: e59469. pmid:23469289
  4. 4. Wittemyer G, Northrup JM, Blanc J, Douglas-Hamilton I, Omondi P, Burnham KP. Illegal killing for ivory drives global decline in African elephants. Proc Natl Acad Sci. 2014;111: 13117–13121. pmid:25136107
  5. 5. Bennett EL. Legal ivory trade in a corrupt world and its impact on African elephant populations. Conserv Biol. 2015;29: 54–60. pmid:25103555
  6. 6. Wasser S, Brown L, Mailand C, Mondol S, Clark W, Laurie C, et al. Genetic assignment of large seizures of elephant ivory reveals Africa’s major poaching hotspots. Science. 2015;349: 84–87.
  7. 7. Harvey Fiona. Kenya to burn biggest ever stockpile of ivory. The Guardian. UK; 29 Apr 2016. Available: http://www.theguardian.com/environment/2016/apr/29/kenya-to-burn-biggest-ever-stockpile-of-ivory. Accessed 20 May 2016.
  8. 8. Gettleman Jeffery. Kenya Burns Elephant Ivory Worth $105 Million to Defy Poachers. The New York Times. New York, NY, USA; 30 Apr 2016. Available: http://www.nytimes.com/2016/05/01/world/africa/kenya-burns-poached-elephant-ivory-uhuru-kenyatta.html?_r=0. Accessed 20 May 2016.
  9. 9. Breuer T, Maisels F, Fishlock V. The consequences of poaching and anthropogenic change for forest elephants. Conserv Biol. 2016;
  10. 10. Jathanna D, Karanth KU, Kumar NS, Goswami VR, Vasudev D, Karanth KK. Reliable monitoring of elephant populations in the forests of India: Analytical and practical considerations. Biol Conserv. 2015;187: 212–220.
  11. 11. UNEP C, IUCN T. Elephants in the Dust–The African Elephant Crisis. Rapid Response Assessment UNEP GRID-Arendal 2013. 2013;
  12. 12. McComb K, Moss C, Durant SM, Baker L, Sayialel S. Matriarchs as repositories of social knowledge in African elephants. Science. 2001;292: 491–494. pmid:11313492
  13. 13. Shannon G, Slotow R, Durant SM, Sayialel KN, Poole J, Moss C, et al. Effects of social disruption in elephants persist decades after culling. Front Zool. 2013;10: 1.
  14. 14. Gobush KS, Mutayoba BM, Wasser SK. Long-Term Impacts of Poaching on Relatedness, Stress Physiology, and Reproductive Output of Adult Female African Elephants. Conserv Biol. 2008;22: 1590–1599. pmid:18759771
  15. 15. Jachowski DS, Slotow R, Millspaugh JJ. Physiological stress and refuge behavior by African elephants. PLoS One. 2012;7: e31818. pmid:22384079
  16. 16. Mumby HS, Mar KU, Hayward AD, Htut W, Htut-Aung Y, Lummaa V. Elephants born in the high stress season have faster reproductive ageing. Sci Rep. 2015;5.
  17. 17. Ripple WJ, Newsome TM, Wolf C, Dirzo R, Everatt KT, Galetti M, et al. Collapse of the world’s largest herbivores. Sci Adv. 2015;1: e1400103. pmid:26601172
  18. 18. Rutina LP, Moe SR, Swenson JE. Elephant Loxodonta africana driven woodland conversion to shrubland improves dry-season browse availability for impalas Aepyceros melampus. Wildl Biol. 2005;11: 207–213.
  19. 19. Kerley GI, Landman M. The impacts of elephants on biodiversity in the Eastern Cape Subtropical Thickets. South Afr J Sci. 2006;102: 395–402.
  20. 20. Sukumar R. The Asian elephant: ecology and management. Cambridge University Press; 1992.
  21. 21. Santiapillai C, Suprahman H. The ecology of the elephant (Elephas maximus L.) in the Way Kambas Game Reserve, Sumatra. World Wildlife Fund; 1986.
  22. 22. Bunting E, Steele J, Keys E, Muyengwa S, Child B, Southworth J. Local Perception of Risk to Livelihoods in the Semi-Arid Landscape of Southern Africa. Land. 2013;2: 225–251.
  23. 23. Mackenzie CA, Ahabyona P. Elephants in the garden: Financial and social costs of crop raiding. Ecol Econ. 2012;75: 72–82.
  24. 24. Nyhus P, Tilson R. Agroforestry, elephants, and tigers: balancing conservation theory and practice in human-dominated landscapes of Southeast Asia. Agric Ecosyst Environ. 2004;104: 87–97.
  25. 25. Lande R. Genetics and demography in biological conservation. Science. 1988;241: 1455–1460. pmid:3420403
  26. 26. Shaffer ML. Minimum population sizes for species conservation. BioScience. 1981;31: 131–134.
  27. 27. Ballou JD, Gilpin ME, Foose TJ. Population management for survival and recovery: analytical methods and strategies in small population conservation. Columbia university press; 1995.
  28. 28. Ryan SJ. The Role of Culture in Conservation Planning for Small or Endangered Populations. Conserv Biol. 2006;20: 1321–1324. pmid:16922250
  29. 29. Van Aarde R, Jackson T, Ferreira S. Conservation science and elephant management in southern Africa. South Afr J Sci. 2006;102: 385.
  30. 30. Ihwagi FW, Wang T, Wittemyer G, Skidmore AK, Toxopeus AG, Ngene S, et al. Using Poaching Levels and Elephant Distribution to Assess the Conservation Efficacy of Private, Communal and Government Land in Northern Kenya. PloS One. 2015;10: e0139079. pmid:26407001
  31. 31. Ryan SJ, Thompson SD. Disease risk and inter-institutional transfer of specimens in cooperative breeding programs: Herpes and the elephant species survival plans. Zoo Biol. 2001;20: 89–101. pmid:11429780
  32. 32. Malhi Y, Doughty CE, Galetti M, Smith FA, Svenning J-C, Terborgh JW. Megafauna and ecosystem function from the Pleistocene to the Anthropocene. Proc Nat Acad Sci USA. 2016;113: 838–846. pmid:26811442
  33. 33. Thitaram C, Dejchaisri S, Somgird C, Angkawanish T, Brown J, Phumphuay R, Chomdech S, Kangwanpong D. Social group formation and genetic relatedness in reintroduced Asian elephants (Elephas maximus) in Thailand. Appl Anim Behav Sci. 2015;172: 52–57.
  34. 34. Meehan C, Mench JA, Carlstead K, Hogan JN. Determining connections between the daily lives of zoo elephants and their welfare: an epidemiological approach. PLOS ONE. in press;
  35. 35. Carlstead K, Mench JA, Meehan C, Brown JL. An epidemiological approach to welfare research in zoos: The elephant welfare project. J Appl Anim Welf Sci. 2013;16: 319–337. pmid:24079487
  36. 36. Meehan CL, Hogan JN, Bonaparte-Saller M, Mench JA. Housing and social environments of African (Loxodonta africana) and Asian (Elephas maximus) elephants in North American zoos. PLoS ONE 2016. doi: pone.0146703.
  37. 37. Greco BJ, Meehan CL, Miller LJ, Shepherdson DJ, Morfeld KA, Andrews J, Baker AM, Carlstead K, Mench JA. Elephant management in North American zoological facilities: environmental enrichment, feeding, exercise, and training. PLoS ONE 2016. doi:pone.0152490.
  38. 38. Prado-Oviedo N, Bonaparte-Saller MK, Malloy E, Meehan CL, Mench JA, Brown JL. Evaluation of demographics and social life events of Asian (Elephas maximus) and African elephants (Loxodonta africana) in North American zoos. PloS One 2016. doi: pone.0154750.
  39. 39. Brown JL, Paris S, Prado-Oviedo NA, Meehan CL, Hogan JN, Morfeld K, Carlstead K. Reproductive health assessment of female elephants in North American zoos and association of husbandry practices with reproductive dysfunction in African elephants (Loxodonta africana). PLoS ONE 2016. doi: pone.0145673.
  40. 40. Holdgate MR, Meehan CL, Hogan JN, Miller L, Rushen J, de Passillé AM, Soltis J, Andrews JA, Shepherdson D. Recumbence behavior in zoo elephants: determination of patterns and frequency of recumbent rest and associated environmental and social factors. PLoS ONE 2016. doi: pone.0153301.
  41. 41. Miller MA, Hogan JN, Meehan CL. Housing and demographic risk factors impacting foot and musculoskeletal health in African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) in North American zoos. PLoS ONE 2016. doi: pone.0155223.
  42. 42. Morfeld KA, Meehan CL, Hogan JN, Brown JL. Assessment of body condition in African (Loxodonta africana) and Asian (Elephas maximus) elephants in North American zoos and management practices associated with high body condition scores. PLoS ONE 2016. doi: pone.0155146.
  43. 43. Greco BJ, Meehan CL, Hogan JN, Leighty KL, Mellen J, Mason G, Mench JA. The days and nights of zoo elephants: using epidemiology to better understand stereotypic behavior of African elephants (Loxodonta africana) and Asian elephants (Elephas maximus) in North American zoos. PLoS ONE 2016. doi: pone.0144276.
  44. 44. Holdgate MR, Meehan CL, Hogan JN, Miller LJ, Soltis J., Andrews JA, Shepherdson D. Walking behavior of zoo elephants: associations between GPS-measured daily walking distances and environmental factors, social factors and welfare indicators. PLoS ONE 2016. doi: pone.0150331.