Network transmission inference: Host behavior and parasite life cycle make social networks meaningful in disease ecology

Ecological Applications

Volumn 23, Issue 8, 2013, Pages 1906-1914

  Grear, Daniel A ^a,d   Luong, Lien T ^a,b   Hudson, Peter J ^a,c  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF ALBERTA   (Canada)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

Contact networks; Eastern chipmunk; Foraging behavior; Helminth gastrointestinal parasites; Macroparasite; Tamias striatus; Transmission dynamics; Trophic transmission

Indexed keywords

DISEASE PREVALENCE; DISEASE SPREAD; DISEASE TRANSMISSION; FORAGING BEHAVIOR; HOMOGENEITY; LIFE CYCLE; NEMATODE; PARASITIC DISEASE; RODENT; SOCIAL NETWORK;

ANIMAL; ANIMAL PARASITOSIS; ARTICLE; BIOLOGICAL MODEL; DISEASE TRANSMISSION; ECOSYSTEM; FECES; LIFE CYCLE STAGE; PARASITOLOGY; SCIURIDAE; STATISTICS;

ANIMALS; ECOSYSTEM; FECES; HELMINTHIASIS, ANIMAL; LIFE CYCLE STAGES; MODELS, BIOLOGICAL; SCIURIDAE; STOCHASTIC PROCESSES;

EID: 84891314045     PISSN: 10510761     EISSN: None     Source Type: Journal    
DOI: 10.1890/13-0907.1     Document Type: Article

References (52)

1. Altizer, S., et al. 2003. Social organization and parasite risk in mammals: integrating theory and empirical studies. Annual Review of Ecology, Evolution, and Systematics 34:517-547.
2. Anderson, R. C. 2000. Nematode parasites of vertebrates: their development and transmission. Second edition. CABI, New York, New York, USA.
3. Aparicio, J. P., and M. Pascual. 2007. Building epidemiological models from R0, an implicit treatment of transmission networks. Proceedings of the Royal Society B 274:505-512.
4. Bansal, S., B. T. Grenfell, and L. A. Myers. 2007. When individual behaviour matters: homogeneous and network models in epidemiology. Journal of the Royal Society Interface 4:879-891.
5. Bansal, S., J. Read, B. Pourbohloul, and L. A. Myers. 2010. The dynamic nature of contact networks in infectious disease epidemiology. Journal of Biological Dynamics 4:478-489.
6. Bowers, M. A. 1995. Use of space and habitats by the eastern chipmunk, Tamias striatus. Journal of Mammalology 76:12-21.
7. Brown, E. D., D. W. Macdonald, T. E. Tew, and I. A. Todd. 1994. Apodemus sylvaticus infected with Heligmosomoides polygyrus (Nematoda) in arable ecosystems: epidemiology and effects of infection on the movement of male mice. Journal of Zoology 234:623-640.
8. Bull, C. M., S. S. Godfrey, and D. M. Gordon. 2012. Social networks and the spread of Salmonella in a sleepy lizard population. Molecular Ecology 21:4386-4392.
9. Burnham, K. P., and D. R. Anderson. 2002. Model selection and multimodel inference: a practical information-theoretic approach. Second edition. Springer, New York, New York, USA.
10. Clay, C. A., E. M. Lehmer, A. Previtali, S. St. Joer, and M. D. Dearing. 2009. Contact heterogeneity in deer mice: implications for Sin Nombre virus transmission. Proceedings of the Royal Society B 276:1305-1312.
11. Craft, M. E., and D. Caillaud. 2011. Network models: an underutilized tool in wildlife epidemiology? Interdisciplinary Perspectives on Infectious Diseases 2011:676949.
12. Craft, M. E., E. Volz, C. Packer, and L. A. Myers. 2011. Disease transmission in territorial populations: the smallworld network of Serengeti lions. Journal of the Royal Society Interface 8:776-786.
13. Cross, P. C., J. O. Lloyd-Smith, J. A. Bowers, C. T. Hay, M. Hofmeyr, and W.M. Getz. 2004. Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffalo in the Kruger National Park. Annales Zoologici Fennici 41:879-892.
14. Dijkstra, E. W. 1959. A note on two problems in connexion with graphs. Numerische Mathematik 1:269-271.
15. Drewe, J. A. 2010. Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proceedings of the Royal Society B 277:633-642.
16. Ehman, K. D. 2001. Nematode parasites of the eastern chipmunk from Armstrong county, Pennsylvania. Journal of the Pennsylvania Academy of Science 75:62-65.
17. Elliot, L. 1978. Social behavior and foraging ecology of the eastern chipmunk (Tamias striatus) in the Adirondack Mountains. Smithsonian Contributions to Zoology 265:1-107.
18. Godfrey, S. S., C. M. Bull, R. James, and K. Murray. 2009. Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behavioral Ecology and Sociobiology 63:1045-1056.
19. Godfrey, S. S., J. A. Moore, N. J. Nelson, and M. Bull. 2010. Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Spenodon punctatus). International Journal for Parasitology 40:1575-1585.
20. Grear, D. A., S. E. Perkins, and P. J. Hudson. 2009. Does elevated testosterone result in increased exposure and transmission of parasites? Ecology Letters 12:528-537.
21. Hall, S. R., L. Sivars-Becker, C. Becker, M. A. Duffy, A. J. Tessier, and C. E. Caceres. 2007. Eating yourself sick: transmission of disease as a function of foraging ecology. Ecology Letters 10:207-218.
22. Hamede, R. K., J. Bashford, H. McCallum, and M. Jones. 2009. Contact networks in a wild Tasmanian devil (Sarcophilus harrisii) populations: using social network analysis to reveal seasonal variability on social behaviour and its implications for transmission of devil facial tumor. Ecology Letters 12:1147-1157.
23. Handcock, M. S., D. R. Hunter, C. T. Butts, S. M. Goodreau, and M. Morris. 2003. Statnet: software tools for the statistical modeling of network data. University of Washington, Seattle, Washington, USA. http://statnetproject. org
24. Keeling, M. J. 1999. The effects of local spatial structure of epidemiological invasions. Proceedings of the Royal Society B 266:859-867.
25. Kjaer, L. J., E. M. Schauber, and C. K. Nielsen. 2008. Spatial and temporal analysis of contact rates in female white-tailed deer. Journal of Wildlife Management 72:1819-1825.
26. Kramer, D. L., and W. Nowell. 1980. Central place foraging in the eastern chipmunk, Tamias striatus. Animal Behavior 28:772-778.
27. Kramer, D. L., and D. M. Weary. 1991. Exploration versus exploitation: a field study of time allocation to environmental tracking by foraging chipmunks. Animal Behavior 41:443-449.
28. Lacher, T. E., and M. A. Mares. 1996. Availability of resources and use of space in eastern chipmunks, Tamias striatus. Journal of Mammalogy 77:833-849.
29. Lloyd-Smith, J. O., S. J. Schreiber, P. E. Kopp, and W. M. Getz. 2005. Superspreading and the effect of individual variation on disease emergence. Nature 438:355-359.
30. Luong, L. T., E. G. Chapman, J. D. Harwood, and P. J. Hudson. 2013. Linking predator-prey interactions with exposure to a trophically transmitted parasite using PCRbased analyses. Molecular Ecology 22:239-248.
31. MacIntosh, A. J. J., A. Jacobs, C. Garcia, K. Shimizu, K. Mouri, M. A. Huffman, and A. D. Hernandez. 2012. Monkeys in the middle: parasite transmission through the social network of a wild primate. PLoS ONE 7(12):e51144.
32. Mares, M. A., T. E. Lacher, M. R. Willig, N. A. Bitar, R. Adams, A. Klinger, and D. Tazik. 1982. An experimental analysis of social spacing in Tamias striatus. Ecology 63:267-273.
33. May, R. M. 2006. Network structure and the biology of populations. Trends in Ecology and Evolution 21:394-399.
34. Moore, J. 2002. Parasites and the behavior of animals. Oxford University Press, Oxford, UK.
35. Myers, L. A., B. Pourbohloul, M. E. J. Newman, D. M. Skowronski, and R. C. Brunham. 2005. Network theory and SARS: predicting outbreak diversity. Journal of Theoretical Biology 232:71-81.
36. Newman, M. E. J. 2001. Scientific collaboration networks. II. Shortest paths, weighted networks, and centrality. Physical Review E 64:016132.
37. Patterson, L. D., and A. I. Schulte-Hostedde. 2011. Behavioral correaltes of parasitism and reproductive success in male eastern chipmunks, Tamias striatus. Animal Behavior 81:1129-1137.
38. Perkins, S. E., F. Cagnacci, A. Stradiotto, D. Arnoldi, and P. J. Hudson. 2009. A comparison of social networks derived from ecological data: implications for inferring infectious disease dynamics. Journal of Animal Ecology 78:1015-1022.
39. Poirier, S. R., M. E. Rau, and X. Wang. 1995. Diel locomotory activity of deer mice (Peromyscus maniculatus) infected with Trichinella nativa or Trichinella pseudospiralis. Canadian Journal of Zoology 73:1323-1334.
40. Poulin, R. 2010. Parasite manipulation of host behavior: an update and frequently asked questions. Advances in the Study of Behavior 41:151-186.
41. Proulx, S. R., D. E. L. Promislow, and P. C. Phillips. 2005. Network thinking in ecology and evolution. Trends in Ecology and Evolution 20:345-353.
42. R Development Core Team. 2009. R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. http://www.R-project.org
43. Rausch, R., and J. D. Tiner. 1948. Studies on the parasitic helminthes of the north central states. I. Helminths of Sciuridae. American Midland Naturalist 39:728-747.
44. Revilla, E., and F. Palomares. 2002. Spatial organization, group living and ecological correlates in low-density populations of Eurasian badgers, Meles meles. Journal of Animal Ecology 71:497-512.
45. Salathé, M., M. Kazandjieva, J. W. Lee, P. Levis, M. W. Feldman, and J. H. Jones. 2010. A high-resolution human contact network for infectious disease transmission. Proceedings of the National Academy of Sciences USA 107:22020-22025.
46. Schauber, E. M., D. J. Storm, and C. K. Nielsen. 2007. Effects of joint space use and group membership on contact rates among white-tailed deer. Journal of Wildlife Management 71:155-163.
47. Schwanz, L. E. 2006. Schistosome infection in deer mice (Peromyscus maniculatus): impacts on host physiology, behavior and energetics. Journal of Experimental Biology 209:5029-5030.
48. Shaw, D. J., B. J. Grenfell, and A. P. Dobson. 1998. Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597-610.
49. Sloss, M. W., and R. L. Kemp. 1978. Veterinary clinical parasitology. Iowa State University Press, Ames, Iowa, USA.
50. Snyder, D. P. 1982. Tamias striatus. Mammalian Species 168:1-8.
51. Weihong, J. I., P. C. L. White, and M. N. Clout. 2005. Contact rates between possums revealed by proximity data loggers. J. Appl. Ecol 42:595-604.
52. Yahner, R. H. 1978. Burrow system and home range use by eastern chipmunks, Tamias striatus: ecological and behavioral considerations. Journal of Mammalogy 59:324-329.