Wildlife Research Wildlife Research Society
Ecology, management and conservation in natural and modified habitats
RESEARCH ARTICLE

Use of proximity loggers and network analysis to quantify social interactions in free-ranging wild rabbit populations

Maija K. Marsh A , Steven R. McLeod B , Michael R. Hutchings C and Piran C. L. White A D

A Environment Department, University of York, York YO10 5DD, UK.

B Vertebrate Pest Research Unit, New South Wales Department of Primary Industries, Forest Road, Orange, NSW 2800, Australia.

C Disease Systems, SAC, West Mains Road, Edinburgh EH9 3JG, UK.

D Corresponding author. Email: piran.white@york.ac.uk

Wildlife Research 38(1) 1-12 http://dx.doi.org/10.1071/WR10150
Submitted: 27 August 2010  Accepted: 5 November 2010   Published: 15 March 2011

Abstract

Context: Social structure of group-living animals has important implications for processes such as gene flow, information transfer, resource utilisation, and disease spread. However, due to the difficulties associated with measuring relationships among wild animals and deriving meaningful estimates of social structure from these interactions, quantifying sociality of evasive species can be challenging.

Aims: Our aim was to quantify the pattern of social interactions among free-ranging European wild rabbits (Oryctolagus cuniculus) in a temperate region of Australia.

Methods: We used proximity logging devices to collect data on the dyadic interactions among two populations of rabbits. We then applied recently developed social structure and network analytical techniques to infer estimates of sociality and contact networks from recorded interactions.

Key results: We found large heterogeneities in the strength of association indices and network centrality measures within but not between populations. Network analytical techniques revealed clustering of rabbits into distinct social groups.

Conclusions: Most associations within social groups were strong and highly stable over time whereas interactions between groups were rare and transient, indicating low levels of inter-group mixing. Despite the apparent differences in habitat quality between sites, the network characteristics were extremely similar between the two populations.

Implications: Our results highlight the importance of heterogeneities in individual behaviour in determining the dynamics of directly transmitted diseases at the population level.

Additional keywords: contact network, European wild rabbit, Oryctolagus cuniculus, RHDV, social network, social structure.


References

Böhm, M., Palphramand, K. L., Newton-Cross, G., Hutchings, M. R., and White, P. C. L. (2008). Dynamic interactions among badgers: implications for sociality and disease transmission. Journal of Animal Ecology 77, 735–745.
Dynamic interactions among badgers: implications for sociality and disease transmission.CrossRef | 18355241PubMed | open url image1

Böhm, M., Hutchings, M. R., and White, P. C. L. (2009). Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle. PLoS One 4, e5016.
Contact networks in a wildlife-livestock host community: identifying high-risk individuals in the transmission of bovine TB among badgers and cattle.CrossRef | 19401755PubMed | open url image1

Borgatti, S. P. (2002) ‘Netdraw: Graph Visualization Software.’ (Analytic Technologies: Lexington, KY.)

Cairns, S. J., and Schwager, S. J. (1987). A comparison of association indices. Animal Behaviour 35, 1454–1469.
A comparison of association indices.CrossRef | open url image1

Carter, S. P., Delahay, R. J., Smith, G. C., Macdonald, D. W., Riordan, P., Etherington, T. R., Pimley, E. R., Walker, N. J., and Cheeseman, C. L. (2007). Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology. Proceedings. Biological Sciences 274, 2769–2777.
Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology.CrossRef | open url image1

Christley, R. M., Pinchbeck, G. L., Bowers, R. G., Clancy, D., French, N. P., Bennett, R., and Turner, J. (2005). Infection in social networks: using network analysis to identify high-risk individuals. American Journal of Epidemiology 162, 1024–1031.
Infection in social networks: using network analysis to identify high-risk individuals.CrossRef | 1:STN:280:DC%2BD2MrpsFCnsg%3D%3D&md5=d29ed5c86bbbd50d17c2dca0e9e6ace9CAS | 16177140PubMed | open url image1

Connor, R. C., Mann, J., Tyack, P. L., and Whitehead, H. (1998). Social evolution in toothed whales. Trends in Ecology & Evolution 13, 228–232.
Social evolution in toothed whales.CrossRef | 1:STN:280:DC%2BC3M7itF2jsg%3D%3D&md5=c21122cb6e1b0b8cedff26b72f522af3CAS | open url image1

Cooke, B. D., and Fenner, F. (2002). Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildlife Research 29, 689–706.
Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand.CrossRef | open url image1

Cowan, D. P. (1987a). Aspects of the social organisation of the European wild rabbit (Oryctolagus cuniculus). Ethology 75, 197–210.
Aspects of the social organisation of the European wild rabbit (Oryctolagus cuniculus).CrossRef | open url image1

Cowan, D. P. (1987b). Group living in the European rabbit (Oryctolagus cuniculus): mutual benefit or resource localization? Journal of Animal Ecology 56, 779–795.
Group living in the European rabbit (Oryctolagus cuniculus): mutual benefit or resource localization?CrossRef | open url image1

Cowan, D. P., and Garson, P. J. (1985). Variations in the social structure of rabbit populations: causes and demographic consequences. In ‘Behavioural Ecology: Ecological Consequences of Adaptive Behaviours’. (Eds R. M. Sibly and R. H. Smith.) pp. 537–554. (Blackwell Scientific Publications: Oxford.)

Daniels, M. J., Lees, J. D., Hutchings, M. R., and Greig, A. (2003). The ranging behaviour and habitat use of rabbits on farmland and their potential role in the epidemiology of paratuberculosis. Veterinary Journal (London, England) 165, 248–257.
The ranging behaviour and habitat use of rabbits on farmland and their potential role in the epidemiology of paratuberculosis.CrossRef | open url image1

Edwards, G. P., Pople, A. R., Saalfeld, K., and Caley, P. (2004). Introduced mammals in Australian rangelands: future threats and the role of monitoring programmes in management strategies. Austral Ecology 29, 40–50.
Introduced mammals in Australian rangelands: future threats and the role of monitoring programmes in management strategies.CrossRef | open url image1

Godfrey, S. S., Bull, C. M., James, R., and Murray, K. (2009). Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behavioral Ecology and Sociobiology 63, 1045–1056.
Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii.CrossRef | open url image1

James, R., Croft, D. P., and Krause, J. (2009). Potential banana skins in animal network social analysis. Behavioral Ecology and Sociobiology 63, 989–997.
Potential banana skins in animal network social analysis.CrossRef | open url image1

Ji, W., White, P. C. L., and Clout, M. N. (2005). Contact rates between possums revealed by proximity data loggers. Journal of Applied Ecology 42, 595–604.
Contact rates between possums revealed by proximity data loggers.CrossRef | open url image1

Krause, J., Lusseau, D., and James, R. (2009). Animal social networks: an introduction. Behavioral Ecology and Sociobiology 63, 967–973.
Animal social networks: an introduction.CrossRef | open url image1

Lehman, M. (1991). Social behaviour in young domestic rabbits under semi-natural conditions. Applied Animal Behaviour Science 32, 269–292.
Social behaviour in young domestic rabbits under semi-natural conditions.CrossRef | open url image1

Lusseau, D. (2007). Evidence for social role in a dolphin social network. Evolutionary Ecology 21, 357–366.
Evidence for social role in a dolphin social network.CrossRef | open url image1

Lusseau, D., Wilson, B., Hammond, P. S., Grellier, K., Durban, J. W., Parsons, K. M., Barton, T. R., and Thompson, P. M. (2006). Quantifying the influence of sociality on population structure in bottlenose dolphins. Journal of Animal Ecology 75, 14–24.
Quantifying the influence of sociality on population structure in bottlenose dolphins.CrossRef | 16903039PubMed | open url image1

Lusseau, D., Whitehead, H., and Gero, S. (2008). Incorporating uncertainty into the study of animal social networks. Animal Behaviour 75, 1809–1815.
Incorporating uncertainty into the study of animal social networks.CrossRef | open url image1

McLeod, R. (2004). ‘Counting the Cost: Impact of Invasive Animals in Australia 2004.’ (Cooperative Research Centre for Pest Animal Control: Canberra.)

Meyers, L. A., Newman, M. E. J., Martin, M., and Schrag, S. (2003). Applying network theory to epidemics: control measures for Mycoplasma pneumoniae outbreaks. Emerging Infectious Diseases 9, 204–210.
| 12603991PubMed | open url image1

Mitani, J. C. (2009). Male chimpanzees form enduring and equitable social bonds. Animal Behaviour 77, 633–640.
Male chimpanzees form enduring and equitable social bonds.CrossRef | open url image1

Myers, K., and Poole, W. E. (1959). A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. I. The effects of density on home range and the formation of breeding grounds. CSIRO Wildlife Research 4, 14–26. open url image1

Myers, K., and Poole, W. E. (1961). A study of the biology of the wild rabbit, Oryctolagus cuniculus (L.), in confined populations. II. The effects of season and population increase on behaviour. CSIRO Wildlife Research 6, 1–41. open url image1

Mykytowycz, R. (1958). Social behaviour of an experimental colony of wild rabbits, Oryctolagus cuniculus (L.) I. Establishment of the colony. CSIRO Wildlife Research 3, 7–25. open url image1

Newman, M. E. J. (2001). Scientific collaboration networks. II. Shortest paths, weighted networks, and centrality. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics 64, 016132.
Scientific collaboration networks. II. Shortest paths, weighted networks, and centrality.CrossRef | 1:STN:280:DC%2BD38%2FisVyrtg%3D%3D&md5=fffea154eab404e422478d795b1fa56fCAS | open url image1

Newman, M. E. J. (2004). Analysis of weighted networks. Physical Review E: Statistical, Nonlinear, and Soft Matter Physics 70, 056131.
Analysis of weighted networks.CrossRef | 1:STN:280:DC%2BD2cnis1KgtA%3D%3D&md5=e721e9cb041e6f38daa72e88154e72b9CAS | open url image1

Newman, M. E. J. (2006). Modularity and community structure in networks. Proceedings of the National Academy of Sciences of the United States of America 103, 8577–8582.
Modularity and community structure in networks.CrossRef | 1:CAS:528:DC%2BD28XlvVCitLw%3D&md5=b151f1b9a85a2c6780e78375bbf82acaCAS | 16723398PubMed | open url image1

Perkins, S. E., Cagnacci, F., Stradiotto, A., Arnoldi, D., and Hudson, P. J. (2009). Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. Journal of Animal Ecology 78, 1015–1022.
Comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics.CrossRef | 19486206PubMed | open url image1

Porphyre, T., Stevenson, M., Jackson, R., and McKenzie, J. (2008). Influence of contact heterogeneity on TB reproduction ratio R-0 in a free-living brushtail possum Trichosurus vulpecula population. Veterinary Research 39, 31.
Influence of contact heterogeneity on TB reproduction ratio R-0 in a free-living brushtail possum Trichosurus vulpecula population.CrossRef | 18275805PubMed | open url image1

Prange, S., Jordan, T., Hunter, C., and Gehrt, S. D. (2006). New radiocollars for the detection of proximity among individuals. Wildlife Society Bulletin 34, 1333–1344.
New radiocollars for the detection of proximity among individuals.CrossRef | open url image1

Sih, A., Hanser, S. F., and McHugh, K. A. (2009). Social network theory: new insights and issues for behavioural ecologists. Behavioral Ecology and Sociobiology 63, 975–988.
Social network theory: new insights and issues for behavioural ecologists.CrossRef | open url image1

Surridge, A. K., Bell, D. J., and Hewitt, G. M. (1999a). From population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus). Biological Journal of the Linnean Society. Linnean Society of London 68, 57–71.
From population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus).CrossRef | open url image1

Surridge, A. K., Ibrahim, K. M., Bell, D. J., Webb, N. J., Rico, C., and Hewitt, G. M. (1999b). Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus). Molecular Ecology 8, 299–307.
Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus).CrossRef | 1:STN:280:DyaK1M7msV2gug%3D%3D&md5=49aa6429e0967500fd50913cbb83ac3dCAS | 10065544PubMed | open url image1

Swain, D. L., and Bishop-Hurley, G. J. (2007). Using contact logging devices to explore animal affiliations: quantifying cow-calf interactions. Applied Animal Behaviour Science 102, 1–11.
Using contact logging devices to explore animal affiliations: quantifying cow-calf interactions.CrossRef | open url image1

Volz, E., and Meyers, L. A. (2007). Susceptible-infected-recovered epidemics in dynamic contact networks. Proceedings. Biological Sciences 274, 2925–2934.
Susceptible-infected-recovered epidemics in dynamic contact networks.CrossRef | open url image1

von Holst, D., Hutzelmeyer, H., Kaetzke, P., Khaschei, M., Rödel, H. G., and Schrutka, H. (2002). Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus). Behavioral Ecology and Sociobiology 51, 245–254.
Social rank, fecundity and lifetime reproductive success in wild European rabbits (Oryctolagus cuniculus).CrossRef | open url image1

Vonhof, M. J., Whitehead, H., and Fenton, M. B. (2004). Analysis of Spix’s disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats. Animal Behaviour 68, 507–521.
Analysis of Spix’s disc-winged bat association patterns and roosting home ranges reveal a novel social structure among bats.CrossRef | open url image1

Wey, T., Blumstein, D. T., Shen, W., and Jordan, F. (2008). Social network analysis of animal behaviour: a promising tool for the study of sociality. Animal Behaviour 75, 333–344.
Social network analysis of animal behaviour: a promising tool for the study of sociality.CrossRef | open url image1

White, P. C. L., and Harris, S. (1994). Encounters between red foxes (Vulpes vulpes): implications for territory maintenance, social cohesion and dispersal. Journal of Animal Ecology 63, 315–327.
Encounters between red foxes (Vulpes vulpes): implications for territory maintenance, social cohesion and dispersal.CrossRef | open url image1

White, P. C. L., Newton-Cross, G. A., Gray, M., Ashford, R., White, C., and Saunders, G. (2003). Spatial interactions and habitat use of rabbits on pasture and implications for the spread of rabbit haemorrhagic disease in New South Wales. Wildlife Research 30, 49–58.
Spatial interactions and habitat use of rabbits on pasture and implications for the spread of rabbit haemorrhagic disease in New South Wales.CrossRef | open url image1

White, P. C. L., Böhm, M., Marion, G., and Hutchings, M. R. (2008). Control of bovine tuberculosis in British livestock: there is no ‘silver bullet’. Trends in Microbiology 16, 420–427.
Control of bovine tuberculosis in British livestock: there is no ‘silver bullet’.CrossRef | 1:CAS:528:DC%2BD1cXhtVOiu7fF&md5=b552af684594bed4e45130da09d217d6CAS | 18706814PubMed | open url image1

Whitehead, H. (1995). Investigating structure and temporal scale in social organizations using identified individuals. Behavioral Ecology 6, 199–208.
Investigating structure and temporal scale in social organizations using identified individuals.CrossRef | open url image1

Whitehead, H. (2006). ‘Socprog: Programs for the Analysis of Animal Social Structure.’ Halifax: Hal Whitehead. Available at http://myweb.dal.ca/hwhitehe/social.htm [accessed 1 September 2009].

Whitehead, H. (2007). Selection of models of lagged identification rates and lagged association rates using AIC and QAIC. Communications in Statistics Simulation and Computation 36, 1233–1246.
Selection of models of lagged identification rates and lagged association rates using AIC and QAIC.CrossRef | open url image1

Whitehead, H. (2008a). ‘Analyzing Animal Societies: Quantitative Methods for Vertebrate Social Analysis.’ (University Chicago Press: Chicago.)

Whitehead, H. (2008b). Precision and power in the analysis of social structure using associations. Animal Behaviour 75, 1093–1099.
Precision and power in the analysis of social structure using associations.CrossRef | open url image1

Whitehead, H. (2009). SOCPROG programs: analysing animal social structures. Behavioral Ecology and Sociobiology 63, 765–778.
SOCPROG programs: analysing animal social structures.CrossRef | open url image1

Whitehead, H., Bejder, L., and Ottensmeyer, C. A. (2005). Testing association patterns: issues arising and extensions. Animal Behaviour 69, e1–e6.
Testing association patterns: issues arising and extensions.CrossRef | open url image1

Woodroffe, R., Donnelly, C. A., Cox, D. R., Bourne, F. J., Cheeseman, C. L., Delahay, R. J., Gettinby, G., McInerney, J. P., and Morrison, W. I. (2006). Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis. Journal of Applied Ecology 43, 1–10.
Effects of culling on badger Meles meles spatial organization: implications for the control of bovine tuberculosis.CrossRef | open url image1



Export Citation