Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-18T13:59:57.860Z Has data issue: false hasContentIssue false

The potential of Social Network Analysis as a tool for the management of zoo animals

Published online by Cambridge University Press:  01 January 2023

PE Rose*
Affiliation:
Centre for Research in Animal Behaviour, Psychology, University of Exeter, Washington Singer, Perry Road, Exeter EX4 4QG, UK Wildfowl & Wetlands Trust, WWT Slimbridge Wetland Centre, Slimbridge, Gloucestershire GL2 7BT, UK
DP Croft
Affiliation:
Centre for Research in Animal Behaviour, Psychology, University of Exeter, Washington Singer, Perry Road, Exeter EX4 4QG, UK
*
* Contact for correspondence and requests for reprints: [email protected]
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Social Network Analysis (SNA) enables the fine scale of animal sociality and population structure to be quantified. SNA is widely applied to questions relating to behavioural ecology but has seen little use in the application to zoo animal management, despite its clear potential. Investment in social bonds between individuals positively affects health status, welfare state, long-term fitness and lifetime reproductive output. Such positive affective states can be maintained consistently within captive situations if more information is known about the social preferences of the individuals that are kept. Disruption to social bonds may lead to impoverished welfare and stress to individuals which have seen their social support compromised. The patterning of social relationships between individuals also influences how space is utilised and how animals interact with resources provided for them. With more detailed knowledge of the social structure of a group or population, social groupings (for example, for captive breeding) can be specifically designed to minimise social stress. Likewise, enhancing the chances of successful reproduction can be achieved if we understand the role that each individual within a network plays and how these roles may impact on the behaviour of others. This paper discusses key aspects of SNA applicable to zoo-based researchers wishing to investigate the social lives of zoo animals. We present a review of how SNA can be used to assess social behaviour and highlight directions for future research. Our aim is to stimulate new research to ultimately improve our understanding of reproductive success, decision-making, group leadership, animal health and enclosure use. We conclude that what can be learned about the dynamics of social zoo-housed species using SNA can directly impact on husbandry decisions and help underpin excellent standards of animal welfare.

Type
Research Article
Copyright
© 2015 Universities Federation for Animal Welfare

References

Anderson, M, Williams, S and O’Brien, E 2009 Individual dif-ferences in the preferred neck-resting position of Caribbean flamingos (Phoenicopterus ruber). Laterality 14: 6678. http://dx.doi.org/10.1080/13576500802233722CrossRefGoogle Scholar
Anderson, MJ, Williams, SA and Bono, AJ 2010 Preferred neck-resting position predicts aggression in Caribbean flamingos (Phoenicopterus ruber). Laterality 15: 629638. http://dx.doi.org/10.1080/13576500903081814CrossRefGoogle ScholarPubMed
Archie, EA, Tung, J, Clark, M, Altmann, J and Alberts, SC 2014 Social affiliation matters: both same-sex and opposite-sex relationships predict survival in wild female baboons. Proceedings of the Royal Society B: Biological Sciences 281: 20141261. http://dx.doi.org/10.1098/rspb.2014.1261CrossRefGoogle ScholarPubMed
Asa, CS, Traylor-Holzer, K and Lacy, RC 2011 Can conservation-breeding programmes be improved by incorporating mate choice? International Zoo Yearbook 45: 203212. http://dx.doi.org/10.1111/j.1748-1090.2010.00123.xCrossRefGoogle Scholar
Barnes, R, Greene, K, Holland, J and Lamm, M 2002 Management and husbandry of duikers at the Los Angeles Zoo. Zoo Biology 21: 107121. http://dx.doi.org/10.1002/zoo.10020CrossRefGoogle Scholar
Barroso, F, Alados, C and Boza, J 2000 Social hierarchy in the domestic goat: effect on food habits and production. Applied Animal Behaviour Science 69: 3553. http://dx.doi.org/10.1016/S0168-1591(00)00113-1CrossRefGoogle ScholarPubMed
Barton, R 1987 Allogrooming as mutualism in diurnal lemurs. Primates 28: 539542. http://dx.doi.org/10.1007/BF02380868CrossRefGoogle Scholar
Bashaw, M 2011 Consistency of captive giraffe behavior under two different management regimes. Zoo Biology 30: 371378. http://dx.doi.org/10.1002/zoo.20338CrossRefGoogle ScholarPubMed
Bashaw, MJ, Bloomsmith, MA, Maple, TL and Bercovitch, FB 2007 The structure of social relationships among captive female giraffe (Giraffa camelopardalis). Journal of Comparative Psychology 121:4653. http://dx.doi.org/10.1037/0735-7036.121.1.46CrossRefGoogle ScholarPubMed
Bejder, L, Fletcher, D and Brager, S 1998 A method for testing association patterns of socialanimals. Animal Behaviour 56: 719725. http://dx.doi.org/10.1006/anbe.1998.0802CrossRefGoogle Scholar
Bercovitch, FB and Berry, PS 2012 Herd composition, kinship and fission–fusion social dynamics among wild giraffe. African Journal of Ecology 51: 206216. http://dx.doi.org/10.1111/aje.12024CrossRefGoogle Scholar
Blonder, B and Dornhaus, A 2011 Time-ordered networks reveal limitations to information flow in ant colonies. PloS One 6: e20298. http://dx.doi.org/10.1371/journal.pone.0020298CrossRefGoogle ScholarPubMed
Blonder, B, Wey, TW, Dornhaus, A, James, R and Sih, A 2012 Temporal dynamics and network analysis. Methods in Ecology and Evolution 3: 958972. http://dx.doi.org/10.1111/j.2041-210X.2012.00236.xCrossRefGoogle Scholar
Boccia, ML, Scanlan, JM, Laudenslager, ML, Berger, CL, Hijazi, AS and Reite, ML 1997 Juvenile friends, behavior, and immune responses to separation in bonnet macaque infants. Physiology & Behaviour 61: 191198. http://dx.doi.org/10.1016/S0031-9384(96)00370-8CrossRefGoogle ScholarPubMed
Bøe, KE and Færevik, G 2003 Grouping and social preferences in calves, heifers and cows. Applied Animal Behaviour Science 80:175190. http://dx.doi.org/10.1016/S0168-1591(02)00217-4CrossRefGoogle Scholar
Borgatti, S 2006 Identifying sets of key players in a social net-work. Computational & Mathematical Organization Theory 12: 2134. http://dx.doi.org/10.1007/s10588-006-7084-xCrossRefGoogle Scholar
Borgatti, SP, Everett, MG and Johnson, JC 2013 Analysing Social Networks. Sage: London, UKGoogle Scholar
Boyd, LE 1991 The behaviour of Przewalski's horses and its importance to their management. Applied Animal Behaviour Science 29: 301318. http://dx.doi.org/10.1016/0168-1591(91)90256-WCrossRefGoogle Scholar
Bracke, MBM and Hopster, H 2006 Assessing the importance of natural behavior for animal welfare. Journal of Agricultural and Environmental Ethics 19: 7789. http://dx.doi.org/10.1007/s10806-005-4493-7CrossRefGoogle Scholar
Broom, DM 1991 Animal welfare: concepts and measurement. Journal of Animal Science 69: 41674175CrossRefGoogle ScholarPubMed
Buchanan-Smith, HM, Griciute, J, Daoudi, S, Leonardi, R and Whiten, A 2013 Interspecific interactions and welfare impli-cations in mixed species communities of capuchin (Sapajus apella) and squirrel monkeys (Saimiri sciureus) over 3 years. Applied Animal Behaviour Science 147: 324333. http://dx.doi.org/10.1016/j.applan-im.2013.04.004CrossRefGoogle Scholar
Cairns, SJ and Schwager, SJ 1987 A comparison of association indices. Animal Behaviour 35: 14541469. http://dx.doi.org/10.1016/S0003-3472(87)80018-0CrossRefGoogle Scholar
Caro, T 1995 Short-term costs and correlates of play in cheetahs. Animal Behaviour 49: 333345. http://dx.doi.org/10.1006/anbe.1995.9999CrossRefGoogle Scholar
Carter, AJ, Macdonald, SL, Thomson, VA and Goldizen, AW 2009 Structured association patterns and their energetic benefits in female eastern grey kangaroos, Macropus giganteus. Animal Behaviour 77: 839846. http://dx.doi.org/10.1016/j.anbe-hav.2008.12.007CrossRefGoogle Scholar
Carter, KD, Brand, R, Carter, JK, Shorrocks, B and Goldizen, AW 2013 Social networks, long-term associations and age-related sociability of wild giraffes. Animal Behaviour 86: 901910. http://dx.doi.org/10.1016/j.anbehav.2013.08.002CrossRefGoogle Scholar
Castles, DL, Whiten, A and Aureli, F 1999 Social anxiety, relationships and self-directed behaviour among wild female olive baboons. Animal Behaviour 58: 12071215. http://dx.doi.org/10.1006/anbe.1999.1250CrossRefGoogle ScholarPubMed
Castles, M, Heinsohn, R, Marshall, HH, Lee, AEG, Cowlishaw, G and Carter, AJ 2014 Social networks created with different techniques are not comparable. Animal Behaviour 96:5967. http://dx.doi.org/10.1016/j.anbehav.2014.07.023CrossRefGoogle Scholar
Clark, FE 2011 Space to choose: network analysis of social pref-erences in a captive chimpanzee community, and implications for management. American Journal of Primatology 73: 748757. http://dx.doi.org/10.1002/ajp.20903CrossRefGoogle Scholar
Clutton-Brock, T, Russell, A, Sharpe, L and Jordan, N 2005 ‘False feeding’ and aggression in meerkat societies. Animal Behaviour 69: 12731284. http://dx.doi.org/10.1016/j.anbe-hav.2004.10.006CrossRefGoogle Scholar
Cockburn, A 1998 Evolution of helping behavior in cooperative-ly breeding birds. Annual Review of Ecology and Systematics 29: 141177. http://dx.doi.org/10.1146/annurev.ecolsys.29.1.141CrossRefGoogle Scholar
Corner, LAL, Pfeiffer, DU and Morris, RS 2003 Social-net-work analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Preventive Veterinary Medicine 59: 147167. http://dx.doi.org/10.1016/S0167-5877(03)00075-8CrossRefGoogle ScholarPubMed
Cote, SD 2000 Dominance hierarchies in female mountain goats: stability, aggressiveness and determination of rank. Behaviour 137:15411566. http://dx.doi.org/10.1163/156853900502718CrossRefGoogle Scholar
Croft, DP, James, R and Krause, J 2008 Exploring animal social networks. Princeton University Press: Princeton, USA. http://dx.doi.org/10.1515/9781400837762CrossRefGoogle Scholar
Croft, DP, Krause, J and James, R 2004 Social networks in the guppy (Poecilia reticulata). Proceedings of the Royal Society of London. Series B: Biological Sciences 271: S516S519. http://dx.doi.org/10.1098/rsbl.2004.0206CrossRefGoogle ScholarPubMed
Croft, DP, Madden, JR, Franks, DW and James, R 2011 Hypothesis testing in animal social networks. Trends in Ecology & Evolution 26: 502507. http://dx.doi.org/10.1016/j.tree.2011.05.012CrossRefGoogle ScholarPubMed
Cross, PC, Lloyd-Smith, JO, Bowers, JA, Hay, CT, Hofmeyr, M and Getz, WM 2004 Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffa-lo in the Kruger National Park. Finnish Zoological and Botanical Publishing Board 41: 879892Google Scholar
Crowell-Davis, SL, Houpt, KA and Carini, CM 1986 Mutual grooming and nearest-neighbor relationships among foals of Equus caballus. Applied Animal Behaviour Science 15: 113123. http://dx.doi.org/10.1016/0168-1591(86)90057-2CrossRefGoogle Scholar
Dagg, AI 2011 Animal Friendships. Cambridge University Press: Cambridge, UK. http://dx.doi.org/10.1017/CBO9780511794155CrossRefGoogle Scholar
Darden, SK, James, R, Ramnarine, IW and Croft, DP 2009 Social implications of the battle of the sexes: sexual harassment disrupts female sociality and social recognition. Proceedings of the Royal Society B: Biological Sciences 276: 26512656. http://dx.doi.org/10.1098/rspb.2009.0087CrossRefGoogle ScholarPubMed
Daszak, P, Berger, L, Cunningham, AA, Hyatt, AD, Green, DE and Speare, R 1999 Emerging infectious diseases and amphibian population declines. Emerging Infectious Diseases 5: 735748. http://dx.doi.org/10.3201/eid0506.990601CrossRefGoogle ScholarPubMed
Dufour, V, Sueur, C, Whiten, A and Buchanan-Smith, HM 2011 The impact of moving to a novel environment on social net-works, activity and wellbeing in two new world primates. American Journal of Primatology 73: 802811. http://dx.doi.org/10.1002/ajp.20943CrossRefGoogle Scholar
Dunbar, RI 1991 Functional significance of social grooming in pri-mates. Folia Primatologica 57: 121131. http://dx.doi.org/10.1159/000156574CrossRefGoogle Scholar
Edwards, KL, Walker, SL, Bodenham, RF, Ritchie, H and Shultz, S 2013 Associations between social behaviour and adre-nal activity in female Barbary macaques: Consequences of study design. General & Comparative Endocrinology 186: 7279. http://dx.doi.org/10.1016/j.ygcen.2013.02.023CrossRefGoogle ScholarPubMed
Edwards, SD and Snowdon, CT 1980 Social behavior of captive, group-living orangutans. International Journal of Primatology 1:3962. http://dx.doi.org/10.1007/BF02692257CrossRefGoogle Scholar
Faerevik, G, Jensen, MB, and Bøe, KE 2006 Dairy calves social preferences and the significance of a companion animal during separation from the group. Applied Animal Behaviour Science 99:205221. http://dx.doi.org/10.1016/j.applanim.2005.10.012CrossRefGoogle Scholar
Flack, JC, Girvan, M, de Waal, FBM and Krakauer, DC 2006 Policing stabilizes construction of social niches in primates. Nature 439: 426429. http://dx.doi.org/10.1038/nature04326CrossRefGoogle ScholarPubMed
Flack, JC, Waal, FB and Krakauer, DC 2005 Social structure, robustness, and policing cost in a cognitively sophisticated species. The American Naturalist 165: E126E139. http://dx.doi.org/10.1086/429277CrossRefGoogle Scholar
Ford, S 2006 Does female mate choice in Canna wood mice (Apodemus sylvaticus) enhance reproductive success. In: Dow, S and Clark, F (eds) Proceedings of the 8th Annual BIAZA Symposium on Zoo Research pp 8392. 24-25 July 2006, Colchester Zoo, UKGoogle Scholar
Fox, M 1969 The anatomy of aggression and its ritualization in Canidae: a developmental and comparative study. Behaviour 35:242258. http://dx.doi.org/10.1163/156853969X00224CrossRefGoogle Scholar
Franks, DW, Ruxton, GD, and James, R 2010 Sampling animal association networks with the gambit of the group. Behavioral Ecology and Sociobiology 64: 493503. http://dx.doi.org/10.1007/s00265-009-0865-8CrossRefGoogle Scholar
Fraser, D, Weary, DM, Pajor, EA and Milligan, BN 1997 A scientific conception of animal welfare that reflects ethical con-cerns. Animal Welfare 6: 187205Google Scholar
Fruteau, C, Voelkl, B, Van Damme, E and Noë, R 2009 Supply and demand determine the market value of food providers in wild vervet monkeys. Proceedings of the National Academy of Sciences 106: 1200712012. http://dx.doi.org/10.1073/pnas.0812280106CrossRefGoogle ScholarPubMed
Fureix, C, Bourjade, M, Henry, S, Sankey, C and Hausberger, M 2012 Exploring aggression regulation in managed groups of horses Equus caballus. Applied Animal Behaviour Science 138: 216228. http://dx.doi.org/10.1016/j.applanim.2012.02.009CrossRefGoogle Scholar
Fürtbauer, I, Heistermann, M, Schülke, O and Ostner, J 2014 Low female stress hormone levels are predicted by same-or opposite-sex sociality depending on season in wild Assamese macaques. Psychoneuroendocrinology 48: 1928. http://dx.doi.org/10.1016/j.psyneuen.2014.05.022CrossRefGoogle ScholarPubMed
Gaillard, J-M, Festa-Bianchet, M, Yoccoz, N, Loison, A and Toigo, C 2000 Temporal variation in fitness components and population dynamics of large herbivores. Annual Review of Ecology and Systematics 31:367393. http://dx.doi.org/10.1146/annurev.ecolsys.31.1.367CrossRefGoogle Scholar
Gartner, MC and Weiss, A 2013 Scottish wildcat (Felis silvestris grampia) personality and subjective well-being: Implications for captive management. Applied Animal Behaviour Science 147: 261267. http://dx.doi.org/10.1016/j.applanim.2012.11.002CrossRefGoogle Scholar
Glatston, AR 1986 Studbooks: the basis of breeding pro-grammes. International Zoo Yearbook 24: 162167. http://dx.d oi.org/10.1111/j.1748-1090.1985.tb02533.xCrossRefGoogle Scholar
Gold, KC and Maple, TL 1994 Personality assessment in the gorilla and its utility as a management tool. Zoo Biology 13: 509522. http://dx.doi.org/10.1002/zoo.1430130513CrossRefGoogle Scholar
Guinet, C 1991 Intentional stranding apprenticeship and social play in killer whales (Orcinus orca). Canadian Journal of Zoology 69:27122716. http://dx.doi.org/10.1139/z91-383CrossRefGoogle Scholar
Hamede, RK, Bashford, J, McCallum, H and Jones, M 2009 Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) population: using social network analysis to reveal seasonal vari-ability in social behaviour and its implications for transmission of devil facial tumour disease. Ecology Letters 12: 11471157. http://dx.doi.org/10.1111/j.1461-0248.2009.01370.xCrossRefGoogle Scholar
Hansen, H, McDonald, DB, Groves, P, Maier, JAK and Ben-David, M 2009 Social networks and the formation and mainte-nance of river otter groups. Ethology 115: 384396. http://dx.doi.org/10.1111/j.1439-0310.2009.01624.xCrossRefGoogle Scholar
Harcourt, R 1991 The development of play in the South American fur seal. Ethology 88: 191202. http://dx.doi.org/10.1111/j.1439-0310.1991.tb00274.xCrossRefGoogle Scholar
Hediger, H 1950 Wild Animals in Captivity. Butterworths Scientific Publications: London, UKGoogle Scholar
Hill, SP and Broom, DM 2009 Measuring zoo animal welfare: theory and practice. Zoo Biology 28: 531544Google ScholarPubMed
Johnsgard, PA 1961 The taxonomy of the Anatidae; a behaviour-al analysis. Ibis 103: 7185Google Scholar
Kimura, R 1998 Mutual grooming and preferred associate relationships in a band of free-ranging horses. Applied Animal Behaviour Science 59: 265276. http://dx.doi.org/10.1016/S0168-1591(97)00129-9CrossRefGoogle Scholar
King, AJ, Johnson, DD and Van Vugt, M 2009 The origins and evolution of leadership. Current Biology 19: R911R916. http://dx.doi.org/10.1016/j.cub.2009.07.027CrossRefGoogle ScholarPubMed
Kraaijeveld, K and Mulder, RA 2002 The function of triumph ceremonies in the black swan. Behaviour 139: 4554. http://dx.doi.org/10.1163/15685390252902265CrossRefGoogle Scholar
Krause, J, Croft, DP and James, R 2007 Social network theory in the behavioural sciences: potential applications. Behavioral Ecology and Sociobiology 62: 1527. http://dx.doi.org/10.1007/s00265-007-0445-8CrossRefGoogle ScholarPubMed
Krause, J, Lusseau, D and James, R 2009 Animal social net-works: an introduction. Behavioral Ecology and Sociobiology 63: 967973. http://dx.doi.org/10.1007/s00265-009-0747-0CrossRefGoogle Scholar
Krause, J and Ruxton, GD 2002 Living in Groups. Oxford University Press: Oxford, UKGoogle Scholar
Kreger, MD, Estevez, I, Hatfield, JS and Gee, GF 2004 Effects of rearing treatment on the behavior of captive whooping cranes (Grus americana). Applied Animal Behaviour Science 89: 243261. http://dx.doi.org/10.1016/j.applanim.2004.07.005CrossRefGoogle Scholar
Kreger, MD, Hatfield, JS, Estevez, I, Gee, GF and Clugston, DA 2005 The effects of captive rearing on the behavior of newly-released whooping cranes (Grus americana). Applied Animal Behaviour Science 93: 165178. http://dx.doi.org/10.1016/j.applan-im.2004.12.004CrossRefGoogle Scholar
Lehmann, J and Boesch, C 2009 Sociality of the dispersing sex: the nature of social bonds in West African female chimpanzees, Pan troglodytes. Animal Behaviour 77: 377387. http://dx.d oi.org/10.1016/j.anbehav.2008.09.038CrossRefGoogle Scholar
Lehmann, J, Korstjens, AH and Dunbar, RIM 2007 Group size, grooming and social cohesion in primates. Animal Behaviour 74: 16171629. http://dx.doi.org/10.1016/j.anbehav.2006.10.025CrossRefGoogle Scholar
Leighty, KA, Soltis, J and Savage, A 2010 GPS assessment of the use of exhibit space and resources by African elephants (Loxodonta africana). Zoo Biology 29: 210220Google ScholarPubMed
Less, EH, Lukas, KE, Kuhar, CW and Stoinski, TS 2010 Behavioral response of captive western lowland gorillas (Gorilla gorilla gorilla) to the death of silverbacks in multi-male groups. Zoo Biology 29: 1629Google Scholar
Lewis, JS, Wartzok, D and Heithaus, MR 2011 Highly dynamic fission–fusion species canexhibit leadership when traveling. Behavioral Ecology and Sociobiology 65: 10611069. http://dx.do i.org/10.1007/s00265-010-1113-yCrossRefGoogle Scholar
Linklater, WL, Cameron, EZ, Minot, EO and Stafford, KJ 1999 Stallion harassment and the mating system of horses. Animal Behaviour 58: 295306. http://dx.doi.org/10.1006/anbe.1999.1155CrossRefGoogle ScholarPubMed
Makagon, MM, McCowan, B and Mench, JA 2012 How can social network analysis contribute to social behavior research in applied ethology? Applied Animal Behaviour Science 138: 152161. http://dx.doi.org/10.1016/j.applanim.2012.02.003CrossRefGoogle ScholarPubMed
Martin, PR and Bateson, PPG 2007 Measuring Behaviour: An Introductory Guide. Cambridge University Press: Cambridge, UK. http://dx.doi.org/10.1017/CBO9780511810893CrossRefGoogle Scholar
Massen, JJM and Koski, SE 2014 Chimps of a feather sit togeth-er: chimpanzee friendships are based on homophily in personali-ty. Evolution and Human Behavior 35: 18. http://dx.d oi.org/10.1016/j.evolhumbehav.2013.08.008CrossRefGoogle Scholar
Matsumura, S 1999 The evolution of ‘egalitarian’ and ‘despotic’ social systems among macaques. Primates 40: 2331. http://dx.doi.org/10.1007/BF02557699CrossRefGoogle ScholarPubMed
McCowan, B, Anderson, K, Heagarty, A and Cameron, A 2008 Utility of social network analysis for primate behavioral management and well-being. Applied Animal Behaviour Science 109:396405. http://dx.doi.org/10.1016/j.applanim.2007.02.009CrossRefGoogle Scholar
Melfi, V 2009 There are big gaps in our knowledge, and thus approach, to zoo animal welfare: a case for evidence-based zoo animal manage-ment. Zoo Biology 28: 574588Google Scholar
Mikota, SK 2006 Preventative health care and physical examination. In: Fowler, ME and Mikota, SK (eds) Biology, Medicine, and Surgery of Elephants pp 6775. Blackwell Publishing: Oxford, UK. http://dx.doi.org/10.1002/9780470344484.ch7CrossRefGoogle Scholar
Morrell, LJ, Croft, DP, Dyer, JR, Chapman, BB, Kelley, JL, Laland, KN and Krause, J 2008 Association patterns and foraging behaviour in natural and artificial guppy shoals. Animal Behaviour 76: 855864. http://dx.doi.org/10.1016/j.anbe-hav.2008.02.015CrossRefGoogle Scholar
Oh, KP and Badyaev, AV 2010 Structure of social networks in a passerine bird: consequences for sexual selection and the evo-lution of mating strategies. The American Naturalist 176: E80E89. http://dx.doi.org/10.1086/655216CrossRefGoogle Scholar
Perdue, BM, Gaalema, DE, Martin, AL, Dampier, SM and Maple, TL 2011 Factors affecting aggression in a captive flock of Chilean flamingos (Phoenicopterus chilensis). Zoo Biology 30: 5964Google Scholar
Perkins, SE, Cagnacci, F, Stradiotto, A, Arnoldi, D and Hudson, PJ 2009 Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. Journal of Animal Ecology 78: 10151022. http://dx.d oi.org/10.1111/j.1365-2656.2009.01557.xCrossRefGoogle ScholarPubMed
Pizzari, T and Gardner, A 2012 The sociobiology of sex: inclusive fitness consequences of inter-sexual interactions. Philosophical Transactions of the Royal Society B: Biological Sciences 367: 23142323. http://dx.doi.org/10.1098/rstb.2011.0281CrossRefGoogle ScholarPubMed
Plowman, AB 2003 A note on a modification of the spread of participation index allowing for unequal zones. Applied Animal Behaviour Science 83: 331336. http://dx.doi.org/10.1016/S0168-1591(03)00142-4CrossRefGoogle Scholar
Plowman, AB, Jordan, NR, Anderson, N, Condon, E and Fraser, O 2005 Welfare implications of captive primate population management: behavioural and psycho-social effects of female-based contraception, oestrus and male removal in hamadryas baboons (Papio hamadryas). Applied Animal Behaviour Science 90:155165. http://dx.doi.org/10.1016/j.applanim.2004.08.014CrossRefGoogle Scholar
Pluháček, J, Bartoš, L and Čulík, L 2006 High-ranking mares of captive plains zebra Equus burchelli have greater reproductive suc-cess than low-ranking mares. Applied Animal Behaviour Science 99:315329. http://dx.doi.org/10.1016/j.applanim.2005.11.003CrossRefGoogle Scholar
Power, DM 1967 Epigamic and reproductive behavior of orange-chinned parakeets in captivity. The Condor 69: 2841. http://dx.doi.org/10.2307/1366370CrossRefGoogle Scholar
Price, EE and Stoinski, TS 2007 Group size: determinants in the wild and implications for the captive housing of wild mammals in zoos. Applied Animal Behaviour Science 103: 255264. http://dx.doi.org/10.1016/j.applanim.2006.05.021CrossRefGoogle Scholar
Pullen, PK 2005 Preliminary comparisons of male/male interactions within bachelor and breeding groups of western lowland gorillas (Gorilla gorilla gorilla). Applied Animal Behaviour Science 90:143153. http://dx.doi.org/10.1016/j.applanim.2004.08.016CrossRefGoogle Scholar
Rault, J-L 2012 Friends with benefits: social support and its rele-vance for farm animal welfare. Applied Animal Behaviour Science 136: 114. http://dx.doi.org/10.1016/j.applanim.2011.10.002CrossRefGoogle Scholar
Rose, P 2010 Do you have friends in high places? Social attach-ment and partner preference in captive giraffe. In: Hill, S (ed) 12th BIAZA Research Symposium. 7-8 July 2010, Chester Zoo, UKGoogle Scholar
Ross, MR, Gillespie, KL, Hopper, LM, Bloomsmith, MA and Maple, TL 2013 Differential preference for ultraviolet light among captive birds from three ecological habitats. Applied Animal Behaviour Science 147: 278285. http://dx.doi.org/10.1016/j.applan-im.2013.05.006CrossRefGoogle Scholar
Rushmore, J, Caillaud, D, Hall, RJ, Stumpf, RM, Meyers, LA and Altizer, S 2014 Network-based vaccination improves prospects for disease control in wild chimpanzees. Journal of The Royal Society Interface 11: 20140349. http://dx.doi.org/10.1098/rsif.2014.0349CrossRefGoogle ScholarPubMed
Ryan, SJ and Thompson, SD 2001 Disease risk and inter-insti-tutional transfer of specimens in cooperative breeding programs: Herpes and the elephant species survival plans. Zoo Biology 20: 89101. http://dx.doi.org/10.1002/zoo.1009CrossRefGoogle ScholarPubMed
Ryder, OA and Wedemeyer, EA 1982 A cooperative breeding programme for the Mongolian wild horse Equus przewalskii in the United States. Biological Conservation 22: 259271. http://dx.doi.org/10.1016/0006-3207(82)90021-0CrossRefGoogle Scholar
Schel, A, Rawlings, B, Claidiere, N, Wilke, C, Wathan, J, Richardson, J, Pearson, S, Herrelko, ES, Whiten, A and Slocombe, K 2013 Network analysis of social changes in a captive chimpanzee community following the successful integration of two adult groups. American Journal of Primatology 75: 254266. http://dx.doi.org/10.1002/ajp.22101CrossRefGoogle Scholar
Shannon, PW 2000 Social and reproductive relationships of captive Caribbean flamingos. Waterbirds: The International Journal of Waterbird Biology 23: 173178. http://dx.doi.org/10.2307/1522162CrossRefGoogle Scholar
Sibbald, AM, Elston, DA, Smith, DJF and Erhard, HW 2005 A method for assessing the relative sociability of individuals within groups: an example with grazing sheep. Applied Animal Behaviour Science 91: 5773. http://dx.doi.org/10.1016/j.applanim.2004.09.002CrossRefGoogle Scholar
Sih, A and Watters, JV 2005 The mix matters: behavioural types and group dynamics in water striders. Behaviour 142: 14171431. http://dx.doi.org/10.1163/156853905774539454Google Scholar
Silk, JB 2007a The adaptive value of sociality in mammalian groups. Philosophical Transactions of the Royal Society B: Biological Sciences 362: 539559. http://dx.doi.org/10.1098/rstb.2006.1994CrossRefGoogle ScholarPubMed
Silk, JB 2007b Social components of fitness in primate groups. Science 317: 13471351. http://dx.doi.org/10.1126/science.1140734CrossRefGoogle ScholarPubMed
Silk, JB, Beehner, JC, Bergman, TJ, Crockford, C, Engh, AL, Moscovice, LR, Wittig, RM, Seyfarth, RM and Cheney, DL 2009 The benefits of social capital: close social bonds among female baboons enhance offspring survival. Proceedings of the Royal Society B: Biological Sciences 276: 30993104. http://dx.doi.org/10.1098/rspb.2009.0681CrossRefGoogle ScholarPubMed
Silk, JB, Beehner, JC, Bergman, TJ, Crockford, C, Engh, AL, Moscovice, LR, Wittig, RM, Seyfarth, RM and Cheney, DL 2010a Female chacma baboons form strong, equitable, and enduring social bonds. Behavioral Ecology and Sociobiology 64: 17331747. http://dx.doi.org/10.1007/s00265-010-0986-0CrossRefGoogle ScholarPubMed
Silk, JB, Beehner, JC, Bergman, TJ, Crockford, C, Engh, AL, Moscovice, LR, Wittig, RM, Seyfarth, RM and Cheney, DL 2010b Strong and consistent social bonds enhance the longevity of female baboons. Current Biology 20: 13591361. http://dx.d oi.org/10.1016/j.cub.2010.05.067CrossRefGoogle ScholarPubMed
Silk, JB, Brosnan, SF, Vonk, J, Henrich, J, Povinelli, DJ, Richardson, AS, Lambeth, SP, Mascaro, J and Schapiro, SJ 2005 Chimpanzees are indifferent to the welfare of unrelated group members. Nature 437: 13571359. http://dx.doi.org/10.1038/nature04243CrossRefGoogle Scholar
Spurr, E 1975 Orientation of Adélie penguins on their territories. The Condor 77: 335337. http://dx.doi.org/10.2307/1366231CrossRefGoogle Scholar
Stoinski, TS, Lukas, KE and Kuhar, CW 2013 Effects of age and group type on social behaviour of male western gorillas (Gorilla gorilla gorilla) in North American zoos. Applied Animal Behaviour Science 147: 316323. http://dx.doi.org/10.1016/j.applan-im.2013.07.003CrossRefGoogle Scholar
Stoinski, TS, Lukas, KE, Kuhar, CW and Maple, TL 2004 Factors influencing the formation and maintenance of all-male gorilla groups in captivity. Zoo Biology 23: 189203. http://dx.d oi.org/10.1002/zoo.20005CrossRefGoogle Scholar
Sueur, C, Jacobs, A, Amblard, F, Petit, O and King, AJ 2011 How can social network analysis improve the study of primate behavior? American Journal of Primatology 73: 703719. http://dx.doi.org/10.1002/ajp.20915CrossRefGoogle Scholar
Swedell, L 2002 Affiliation among females in wild hamadryas baboons (Papio hamadryas hamadryas). International Journal of Primatology 23:12051226. http://dx.doi.org/10.1023/A:1021170703006CrossRefGoogle Scholar
Tarou, LR, Bashaw, MJ and Maple, TL 2000 Social attachment in giraffe: Response to social separation. Zoo Biology 19: 4151. http://dx.doi.org/10.1002/(SICI)1098-2361(2000)19:1<41::AID-ZOO5>3.0.CO;2-J3.0.CO;2-J>CrossRefGoogle Scholar
Tetley, CL and O’Hara, SJ 2012 Ratings of animal personality as a tool for improving the breeding, management and welfare of zoo mammals. Animal Welfare 21: 463476. http://dx.doi.org/10.7120/09627286.21.4.463CrossRefGoogle Scholar
Tobach, E, Greenberg, G, Radell, P and McCarthy, T 1989 Social behavior in a group of orang-utans (Pongo pygmaeus abelii) in a zoo setting. Applied Animal Behaviour Science 23: 141154. http://dx.doi.org/10.1016/0168-1591(89)90014-2CrossRefGoogle Scholar
Turner, SP, Horgan, GW and Edwards, SA 2001 Effect of social group size on aggressive behaviour between unacquainted domestic pigs. Applied Animal Behaviour Science 74: 203215. http://dx.doi.org/10.1016/S0168-1591(01)00168-XCrossRefGoogle Scholar
Uher, J and Asendorpf, JB 2008 Personality assessment in the Great Apes: Comparing ecologically valid behavior measures, behavior ratings, and adjective ratings. Journal of Research in Personality 42: 821838. http://dx.doi.org/10.1016/j.jrp.2007.10.004CrossRefGoogle Scholar
Valuska, AJ, Leighty, KA, Ferrie, GM, Nichols, VD, Tybor, CL, Plassé, C and Bettinger, TL 2013 Attempted integration of multiple species of turaco into a mixed-species aviary. Zoo Biology 32: 216221. http://dx.doi.org/10.1002/zoo.21047CrossRefGoogle ScholarPubMed
Voelkl, B, Kasper, C and Schwab, C 2011 Network measures for dyadic interactions: stability and reliability. American Journal of Primatology 73: 731740. http://dx.doi.org/10.1002/ajp.20945CrossRefGoogle ScholarPubMed
Wachtmeister, C-A 2001 Display in monogamous pairs: a review of empirical data and evolutionary explanations. Animal Behaviour 61: 861868. http://dx.doi.org/10.1006/anbe.2001.1684CrossRefGoogle Scholar
Wakefield, M 2008 Grouping patterns and competition among female Pan troglodytes schweinfurthii at Ngogo, Kibale National Park, Uganda. International Journal of Primatology 29: 907929. http://dx.doi.org/10.1007/s10764-008-9280-7CrossRefGoogle Scholar
Wakefield, ML 2013 Social dynamics among females and their influence on social structure in an East African chimpanzee com-munity. Animal Behaviour 85: 13031313. http://dx.doi.org/10.1016/j.anbehav.2013.03.019CrossRefGoogle Scholar
Warburton, LS and Perrin, MR 2005 Nest-site characteristics and breeding biology of the black-cheeked lovebird Agapornis nigri-genis in Zambia. Ostrich Journal of African Ornithology 76: 162174. http://dx.doi.org/10.2989/00306520509485489CrossRefGoogle Scholar
Watters, JV and Powell, DM 2012 Measuring animal personali-ty for use in population management in zoos: suggested methods and rationale. Zoo Biology 31: 112. http://dx.doi.org/10.1002/zoo.20379CrossRefGoogle ScholarPubMed
Wedekind, C 2002 Sexual selection and life-history decisions: implications for supportive breeding and the management of captive populations. Conservation Biology 16: 12041211. http://dx.d oi.org/10.1046/j.1523-1739.2002.01217.xCrossRefGoogle Scholar
Wey, T, Blumstein, DT, Shen, W and Jordán, F 2008 Social network analysis of animal behaviour: a promising tool for the study of sociality. Animal Behaviour 75: 333344. http://dx.do i.org/10.1016/j.anbehav.2007.06.020CrossRefGoogle Scholar
Wey, TW, Burger, JR, Ebensperger, LA and Hayes, LD 2013 Reproductive correlates of social network variation in plurally breeding degus (Octodon degus). Animal Behaviour 85: 14071414. http://dx.doi.org/10.1016/j.anbehav.2013.03.035CrossRefGoogle ScholarPubMed
Whitehead, H 1999 Testing association patterns of social ani-mals. Animal Behaviour 57: 2629. http://dx.doi.org/10.1006/anbe.1999.1099CrossRefGoogle Scholar
Whitehead, H 2008 Analyzing animal societies: quantitative meth-ods for vertebrate social analysis. University of Chicago Press: Chicago, USA. http://dx.doi.org/10.7208/chicago/9780226895246.001.0001CrossRefGoogle Scholar
Whitehead, H 2009 SOCPROG programs: analysing animal social structures. Behavioral Ecology and Sociobiology 63: 765778. http://dx.doi.org/10.1007/s00265-008-0697-yCrossRefGoogle Scholar
Whitehead, H, Bejder, L and Andrea Ottensmeyer, C 2005 Testing association patterns: issues arising and extensions. Animal Behaviour 69: e1e6. http://dx.doi.org/10.1016/j.anbe-hav.2004.11.004CrossRefGoogle Scholar
Whitehead, H and Dufault, S 1999 Techniques for analyzing vertebrate social structure using identified individuals: review and recommendations. In: Slater, PJB, Rosenblat, JS, Snowden, CT and Roper, TJ (eds) Advances in the Study of Behavior pp 3374. Academic Press: Waltham, USAGoogle Scholar
Whitham, JC and Wielebnowski, N 2013 New directions for zoo animal welfare science. Applied Animal Behaviour Science 147:247260. http://dx.doi.org/10.1016/j.applanim.2013.02.004CrossRefGoogle Scholar
Wilkinson, R 2000 An overview of captive-management pro-grammes and regional collection planning for parrots. International Zoo Yearbook 37: 3658. http://dx.doi.org/10.1111/j.1748-1090.2000.tb00705.xCrossRefGoogle Scholar
Wilson, A, Krause, S, Dingemanse, N and Krause, J 2013 Network position: a key component in the characterization of social personality types. Behavioral Ecology and Sociobiology 67: 163173. http://dx.doi.org/10.1007/s00265-012-1428-yCrossRefGoogle Scholar
Wilson, ML, Bashaw, MJ, Fountain, K, Kieschnick, S and Maple, TL 2006 Nocturnal behavior in a group of female African elephants. Zoo Biology 25: 173186. http://dx.doi.org/10.1002/zoo.20084CrossRefGoogle Scholar
Wiszniewski, J, Allen, SJ and Möller, LM 2009 Social cohesion in a hierarchically structured embayment population of Indo-Pacific bottlenose dolphins. Animal Behaviour 77: 14491457. http://dx.doi.org/10.1016/j.anbehav.2009.02.025CrossRefGoogle Scholar
Wiszniewski, J, Lusseau, D and Möller, LM 2010 Female bisex-ual kinship ties maintain social cohesion in a dolphin network. Animal Behaviour 80: 895904. http://dx.doi.org/10.1016/j.anbe-hav.2010.08.013CrossRefGoogle Scholar
Wittemyer, G, Douglas-Hamilton, I and Getz, WM 2005 The socioecology of elephants: analysis of the processes creating multitiered social structures. Animal Behaviour 69: 13571371. http://dx.doi.org/10.1016/j.anbehav.2004.08.018CrossRefGoogle Scholar
Wittemyer, G, Getz, WM, Vollrath, F and Douglas-Hamilton, I 2007 Social dominance, seasonal movements, and spatial segregation in African elephants: a contribution to conser-vation behavior. Behavioral Ecology and Sociobiology 61: 19191931. http://dx.doi.org/10.1007/s00265-007-0432-0CrossRefGoogle Scholar
Wittig, RM, Crockford, C, Lehmann, J, Whitten, PL, Seyfarth, RM and Cheney, DL 2008 Focused grooming networks and stress alleviation in wild female baboons. Hormones and Behaviour 54: 170177. http://dx.doi.org/10.1016/j.yhbeh.2008.02.009CrossRefGoogle ScholarPubMed
Wolf, M and Weissing, FJ 2010 An explanatory framework for adaptive personality differences. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 39593968. http://dx.doi.org/10.1098/rstb.2010.0215CrossRefGoogle ScholarPubMed
Wyndham, E 1980 Diurnal cycle, behaviour and social organization of the budgerigar Melopsittacus undulatus. Emu 80: 2533. http://dx.doi.org/10.1071/MU9800025CrossRefGoogle Scholar
Yeates, JW and Main, DC 2008 Assessment of positive welfare: a review. The Veterinary Journal 175: 293300. http://dx.doi.org/10.1016/j.tvjl.2007.05.009CrossRefGoogle ScholarPubMed
Young, C, Majolo, B, Schülke, O and Ostner, J 2014 Male social bonds and rank predict supporter selection in cooperative aggression in wild Barbary macaques. Animal Behaviour 95: 2332. http://dx.doi.org/10.1016/j.anbehav.2014.06.007CrossRefGoogle Scholar