Disease transmission in territorial populations: The small-world network of Serengeti lions

Journal of the Royal Society Interface

Volumn 8, Issue 59, 2011, Pages 776-786

  Craft, Meggan E ^a   Volz, Erik ^b   Packer, Craig ^c   Meyers, Lauren Ancel ^d,e  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MINNESOTA   (United States)

^d UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^e SANTA FE INSTITUTE   (United States)

Author keywords

African lion; Contact rates; Epidemiological modelling; Network model; Territoriality; Wildlife disease

Indexed keywords

ANIMALS; DISTRIBUTED COMPUTER SYSTEMS; ECOSYSTEMS; POPULATION STATISTICS; VIRUSES;

AFRICAN LION; CONTACT RATES; EPIDEMIOLOGICAL MODELLING; NETWORK MODEL; TERRITORIALITY; WILDLIFE DISEASE;

COMPUTER VIRUSES;

ANIMAL DISEASE; ARTICLE; DISEASE TRANSMISSION; ECOSYSTEM; LION; MODEL; NONHUMAN; POPULATION; SOCIETY; TERRITORIALITY;

ANIMALIA; CANINE DISTEMPER VIRUS;

EID: 79955711378     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2010.0511     Document Type: Article

References (59)

1. Altizer, S. et al. 2003 Social organization and parasite risk in mammals: integrating theory and empirical studies. Annu. Rev. Ecol. Evol. Syst. 34, 517-547. (doi:10.1146/annurev.ecolsys.34.030102.151725)
2. Cross, P. C., Lloyd-Smith, J. O. & Getz, W. M. 2005 Disentangling association patterns in fission-fusion societies using African buffalo as an example. Anim. Behav. 69, 499-506. (doi:10.1016/j.anbehav.2004.08.006)
3. Greenwood, P. J. & Harvey, P. H. 1982 The natal and breeding dispersal of birds. Annu. Rev. Ecol. Syst. 13, 1-21. (doi:10.1146/annurev.es.13. 110182.000245)
4. Lidicker, W. Z. & Stenseth, N. C. 1992 To disperse or not to disperse: who does it and why? In Animal dispersal: small mammals as a model (eds N. C. Stenseth & J. W. Z. Lidicker), pp. 21-36. London, UK: Chapman & Hall.
5. Mech, L. D. 1987 Age, season, distance, direction, and social aspects of wolf dispersal from a Minnesota pack. In Mammalian dispersal patterns: the effects of social structure on population genetics (eds B. D. Chepko-Sade & Z. T. Halpin), pp. 55-74. Chicago, IL: University of Chicago Press.
6. Lloyd-Smith, J. O., Schreiber, S. J., Kopp, P. E. & Getz, W. M. 2005 Superspreading and the effect of individual variation on disease emergence. Nature 438, 355-359. (doi:10.1038/nature04153)
7. Meyers, L. A., Pourbohloul, B., Newman, M. E. J., Skowronski, D. M. & Brunham, R. C. 2005 Network theory and SARS: predicting outbreak diversity. J. Theoret. Biol. 232, 71-81. (doi:10.1016/j.jtbi.2004.07.026)
8. Loveridge, A. J. & Macdonald, D. W. 2001 Seasonality in spatial organization and dispersal of sympatric jackals (Canis mesomelas and C. adustus): implications for rabies management. J. Zool. 253, 101-111. (doi:10.1017/S0952836901000097)
9. Russell, C. A., Real, L. A. & Smith, D. L. 2006 Spatial control of rabies on heterogeneous landscapes. PLoS ONE 1, e27. (doi:10.1371/journal.pone. 0000027)
10. Keeling, M. 2005 The implications of network structure for epidemic dynamics. Theoret. Popul. Biol. 67, 1-8. (doi:10.1016/j.tpb.2004.08.002)
11. Meyers, L. A. 2007 Contact network epidemiology: bond percolation applied to infectious disease prediction and control. Bull. (New Series) Am. Math. Soc. 44, 63-86. (doi:10.1090/S0273-0979-06-01148-7)
12. Humphries, M. D. & Gurney, K. 2008 Network 'small-world-ness': a quantitative method for determining canonical network equivalence. PLoS ONE 3, e0002051. (doi:10.1371/journal.pone.0002051)
13. Watts, D. J. & Strogatz, S. H. 1998 Collective dynamics of 'small-world' networks. Nature 393, 440. (doi:10.1038/30918)
14. Latora, V. & Marchiori, M. 2003 Economic small-world behavior in weighted networks. Eur. Phys. J. B Condensed Matter and Complex Systems 32, 249-263. (doi:10.1140/epjb/e2003-00095-5)
15. Keeling, M. J. & Rohani, P. 2008 Modeling infectious diseases in humans and animals. Princeton, NJ: Princeton University Press.
16. Keeling, M. J. & Eames, K. T. D. 2005 Networks and epidemic models. J. R. Soc. Interface 2, 295-307. (doi:10.1098/rsif.2005.0051)
17. Kuperman, M. & Abramson, G. 2001 Small world effect in an epidemiological model. Phys. Rev. Lett. 86, 2909. (doi:10.1103/PhysRevLett.86. 2909)
18. Moore, C. & Newman, M. E. J. 2000 Exact solution of site and bond percolation on small-world networks. Phys. Rev. E 62, 7059. (doi:10.1103/ PhysRevE.62.7059)
19. Mossong, J. l. et al. 2008 Social contacts and mixing patterns relevant to the spread of infectious diseases. PLoS Med. 5, e74. (doi:10.1371/journal. pmed.0050074)
20. Read, J. M., Eames, K. T. D. & Edmunds, W. J. 2008 Dynamic social networks and the implications for the spread of infectious disease. J. R. Soc. Interface 5, 1001-1007. (doi:10.1098/rsif.2008.0013)
21. Krause, J., Croft, D. & James, R. 2007 Social network theory in the behavioural sciences: potential applications. Behav. Ecol. Sociobiol. 62, 15-27. (doi:10.1007/s00265-007-0445-8)
22. Wey, T., Blumstein, D. T., Shen, W. & Jordan, F. 2008 Social network analysis of animal behaviour: a promising tool for the study of sociality. Anim. Behav. 75, 333-344. (doi:10.1016/j.anbehav.2007.06.020)
23. Godfrey, S., Bull, C., James, R. & Murray, K. 2009 Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav. Ecol. Sociobiol. 63, 1045-1056. (doi:10.1007/s00265-009-0730-9)
24. Grear, D. A., Perkins, S. E. & Hudson, P. J. 2009 Does elevated testosterone result in increased exposure and transmission of parasites? Ecol. Lett. 12, 528-537. (doi:10.1111/j.1461-0248.2009.01306.x)
25. Porphyre, T., Stevenson, M., Jackson, R. & McKenzie, J. 2008 Influence of contact heterogeneity on TB reproduction ratio R0 in a free-living brushtail possum Trichosurus Vulpecula population. Veterinary Res. 39, 31. (doi:10.1051/vetres:2008007)
26. Packer, C., Hilborn, R., Mosser, A., Kissui, B., Borner, M., Hopcraft, G., Wilmshurst, J., Mduma, S. & Sinclair, A. R. E. 2005 Ecological change, group territoriality, and population dynamics in Serengeti lions. Science 307, 390-393. (doi:10.1126/science.1105122)
27. Packer, C., Gilbert, D. A., Pusey, A. E. & O'Brieni, S. J. 1991 A molecular genetic analysis of kinship and cooperation in African lions. Nature 351, 562-565. (doi:10.1038/351562a0)
28. Packer, C., Lewis, S. & Pusey, A. E. 1992 A comparative analysis of non-offspring nursing. Anim. Behav. 43, 265-281. (doi:10.1016/S0003-3472(05) 80222-2)
29. Grinnell, J., Packer, C. & Pusey, A. E. 1995 Cooperation in male lions: kinship, reciprocity or mutualism? Anim. Behav. 49, 95-105. (doi:10.1016/0003-3472(95)80157-X)
30. McComb, K., Pusey, A., Packer, C. & Grinnell, J. 1993 Female lions can identify potentially infanticidal males from their roars. Proc. R. Soc. Lond. B 252, 59-64. (doi:10.1098/rspb.1993.0046)
31. Schaller, G. B. 1972 The Serengeti lion; a study of predator-prey relations. Chicago, IL: University of Chicago Press.
32. Pusey, A. E. & Packer, C. 1987 The evolution of sex-based dispersal in lions. Behaviour 101, 275-310. (doi:10.1163/156853987X00026)
33. VanderWaal, K. L., Mosser, A. & Packer, C. 2009 Optimal group size, dispersal decisions and postdispersal relationships in female African lions. Anim. Behav. 77, 949-954. (doi:10.1016/j.anbehav.2008.12.028)
34. Bygott, J. D., Bertram, B. C. R. & Hanby, J. P. 1979 Male lions in large coalitions gain reproductive advantages. Nature 282, 839-841. (doi:10.1038/282839a0)
35. Mosser, A., Fryxell, J. M., Eberly, L. & Packer, C. 2009 Serengeti real estate: density versus fitness-based indicators of lion habitat quality. Ecol. Lett. 12, 1050-1060. (doi:10.1111/j.1461-0248.2009.01359.x)
36. Mosser, A. & Packer, C. 2009 Group territoriality and the benefits of sociality in the African lion, Panthera leo. Anim. Behav. 78, 359-370. (doi:10.1016/j.anbehav.2009.04.024)
37. Packer, C., Scheel, D. & Pusey, A. E. 1990 Why lions form groups: food is not enough. Am. Nat. 136, 1-19. (doi:10.1086/285079)
38. Scheel, D. & Packer, C. 1991 Group hunting behaviour of lions: a search for cooperation. Anim. Behav. 41, 697-709. (doi:10.1016/S0003-3472(05) 80907-8)
39. Packer, C., Pusey, A. E. & Eberly, L. E. 2001 Egalitarianism in female African lions. Science 293, 690-693. (doi:10.1126/science.1062320)
40. Glasserman, P. 2004 Monte Carlo methods in financial engineering. New York, NY: Springer.
41. Madan, D. B., Carr, P. P. & Chang, E. C. 1998 The variance gamma process and option pricing. Eur. Finance Rev. 2, 79-105. (doi:10.1023/A: 1009703431535)
42. Craft, M. E., Volz, E., Packer, C. & Meyers, L. A. 2009 Distinguishing epidemic waves from disease spillover in a wildlife population. Proc. R. Soc. B 276, 1777-1785. (doi:10.1098/rspb.2008.1636)
43. Craft, M. E. 2008 Predicting disease dynamics in African lion populations, pp. 1-126. PhD thesis, University of Minnesota, Saint Paul, MN.
44. Latora, V. & Marchiori, M. 2001 Efficient behavior of small-world networks. Phys. Rev. Lett. 87, 198701. (doi:10.1103/PhysRevLett.87.198701)
45. Gaskell, R. M., Dawson, S. & Radford, A. D. 2006 Feline respiratory disease. In Infectious diseases of the dog and cat, vol. 3 (ed. C. E. Greene), pp. 145-154. Philadelphia, PA: WB Saunders.
46. Packer, C., Altizer, S., Appel, M., Brown, E., Martenson, J., O'Brien, S. J., Roelke-Parker, M., Hofmann-Lehmann, R.& Lutz, H. 1999 Viruses of the Serengeti: patterns of infection and mortality in African lions. J. Anim. Ecol. 68, 1161-1178. (doi:10.1046/j.1365-2656.1999.00360.x)
47. Radford, A. D., Coyne, K. P., Dawson, S., Porter, C. J. & Gaskell, R. M. 2007 Feline calicivirus. Veterinary Res. 38, 319-335. (doi:10.1051/vetres: 2006056)
48. Greene, C. E. & Appel, M. J. 2006 Canine Distemper. In Infectious diseases of the dog and cat, vol. 3 (ed. C. E. Greene), pp. 25-27. Philadelphia, PA: WB Saunders.
49. Roelke-Parker, M. E. et al. 1996 A canine distemper virus epidemic in Serengeti lions (Panthera leo). Nature 379, 441-445. (doi:10.1038/379441a0)
50. Craft, M. E., Hawthorne, P. L., Packer, C. & Dobson, A. P. 2008 Dynamics of a multihost pathogen in a carnivore community. J. Anim. Ecol. 77, 1257-1264. (doi:10.1111/j.1365-2656.2008.01410.x)
51. Sundaresan, S., Fischhoff, I., Dushoff, J. & Rubenstein, D. 2007 Network metrics reveal differences in social organization between two fission-fusion species, Grevy's zebra and onager. Oecologia 151, 140-149. (doi:10.1007/s00442-006-0553-6)
52. Carter, S. P., Delahay, R. J., Smith, G. C., Macdonald, D. W., Riordan, P., Etherington, T. R., Pimley, E. R., Walker, N. J. & 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. Proc. R. Soc. B 274, 2769-2777. (doi:10.1098/rspb.2007.0998)
53. Donnelly, C. A. et al. 2006 Positive and negative effects of widespread badger culling on tuberculosis in cattle. Nature 439, 843-846. (doi:10.1038/nature04454)
54. Woodroffe, R. et al. 2009 Bovine tuberculosis in cattle and badgers in localized culling areas. J. Wildl. Dis. 45, 128-143.
55. Ezenwa, V. O. 2004 Host social behavior and parasitic infection: a multifactorial approach. Behav. Ecol. 15, 446-454. (doi:10.1093/beheco/arh028)
56. Bansal, S., Pourbohloul, B. & Meyers, L. A. 2006 A comparative analysis of influenza vaccination programs. PLoS Med. 3, e387. (doi:10.1371/journal.pmed.0030387)
57. Pourbohloul, B., Meyers, L. A., Skowronski, D. M., Krajden, M., Patrick, D. M. & Brunham, R. C. 2005 Modeling control strategies of respiratory pathogens. Emerg. Infect. Dis. 11, 1249-1256.
58. Mosser, A. 2008 Group territoriality of the African lion: behavioral adaptation in a heterogeneous landscape. PhD thesis, University of Minnesota, MN, USA.
59. Appel, M. 1987 Canine distemper virus. In Virus infections of carnivores (ed. M. J. G. Appel), pp. 132-159. New York, NY: Elsevier Science.