Dynamic vs. static social networks in models of parasite transmission: predicting Cryptosporidium spread in wild lemurs

Journal of Animal Ecology

Volumn 86, Issue 3, 2017, Pages 419-433

  Springer, Andrea ^a,e   Kappeler, Peter M ^a,b   Nunn, Charles L ^c,d  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

^c DUKE UNIVERSITY   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

Author keywords

Cryptosporidium; dynamic social networks; infectious disease modelling; Propithecus verreauxi; seasonality

Indexed keywords

DISEASE INCIDENCE; DISEASE SPREAD; DISEASE TRANSMISSION; DRY SEASON; ECOLOGICAL MODELING; ENVIRONMENTAL CONDITIONS; HOME RANGE; INFECTIOUS DISEASE; PARASITE TRANSMISSION; PATHOGEN; PRIMATE; SEASONALITY; SOCIAL NETWORK; WET SEASON;

CRYPTOSPORIDIUM; LEMURIDAE; PRIMATES; PROPITHECUS; PROPITHECUS VERREAUXI;

ANIMAL; ANIMAL BEHAVIOR; BIOLOGICAL MODEL; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; EPIDEMIC; MADAGASCAR; PARASITOLOGY; PHYSIOLOGY; PROSIMIAN; SEASON; SOCIAL BEHAVIOR; TRANSMISSION; VETERINARY;

ANIMALS; CRYPTOSPORIDIOSIS; CRYPTOSPORIDIUM; DISEASE OUTBREAKS; HOMING BEHAVIOR; MADAGASCAR; MODELS, BIOLOGICAL; SEASONS; SOCIAL BEHAVIOR; STREPSIRHINI;

EID: 85011266654     PISSN: 00218790     EISSN: 13652656     Source Type: Journal    
DOI: 10.1111/1365-2656.12617     Document Type: Article

References (49)

1. Anderson, R.C. (2000) Nematode Parasites of Vertebrates: Their Development and Transmission, 2nd edn. CABI Publications, Wallingford, UK.
2. Barton, K. (2016) MuMIn: Multi-Model Inference. R package v. 1.15.6. https://CRAN.R-project.org/package=MuMIn.
3. Benadi, G., Fichtel, C. & Kappeler, P. (2008) Intergroup relations and home range use in Verreaux's sifaka (Propithecus verreauxi). American Journal of Primatology, 70, 956–965.
4. Blower, S.M. & Dowlatabadi, H. (1994) Sensitivity and uncertainty analysis of complex models of disease transmission: an HIV model, as an example. International Statistical Review/Revue Internationale de Statistique, 62, 229–243.
5. Burnham, K. & Anderson, D. (2002) Model Selection and Multimodel Inference. Springer, New York, NY, USA.
6. Casemore, D.P. (1990) Epidemiological aspects of human cryptosporidiosis. Epidemiology & Infection, 104, 1–28.
7. Chappell, C.L., Okhuysen, P.C., Sterling, C.R. & DuPont, H.L. (1996) Cryptosporidium parvum: intensity of infection and oocyst excretion patterns in healthy volunteers. Journal of Infectious Diseases, 173, 232–236.
8. Charles-Smith, L.E., Cowen, P. & Schopler, R. (2010) Environmental and physiological factors contributing to outbreaks of Cryptosporidium in Coquerel's Sifaka (Propithecus coquereli) at the Duke Lemur Center: 1999–2007. Journal of Zoo and Wildlife Medicine, 41, 438–444.
9. Chen, S., White, B.J., Sanderson, M.W., Amrine, D.E., Ilany, A. & Lanzas, C. (2014) Highly dynamic animal contact network and implications on disease transmission. Scientific Reports, 4, 4472.
10. Craft, M.E., Volz, E., Packer, C. & Meyers, L.A. (2011) Disease transmission in territorial populations: the small-world network of Serengeti lions. Journal of the Royal Society Interface, 8, 776–786.
11. Cross, P., Lloyd-Smith, J., Bowers, J., Hay, C., Hofmeyr, M. & Getz, W. (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.
12. Csardi, G. & Nepusz, T. (2006) The igraph software package for complex network research. InterJournal, Complex Systems, 1695, 1–9.
13. Erkert, H.G. & Kappeler, P.M. (2004) Arrived in the light: diel and seasonal activity patterns in wild Verreaux's sifakas (Propithecus v. verreauxi; Primates: Indriidae). Behavioral Ecology and Sociobiology, 57, 174–186.
14. Fieberg, J., Kochanny, C.O. & Lanham (2005) Quantifying home-range overlap: the importance of the utilization distribution. Journal of Wildlife Management, 69, 1346–1359.
15. Freeland, W.J. (1979) Primate social groups as biological islands. Ecology, 60, 719–728.
16. Gómez, M.S., Torres, J., Gracenea, M., Fernandez-Morán, J. & Gonzalez-Moreno, O. (2000) Further report on Cryptosporidium in Barcelona zoo mammals. Parasitology Research, 86, 318–323.
17. Gramacy, R.B. (2007) tgp: an R package for Bayesian nonstationary, semiparametric nonlinear regression and design by treed Gaussian process models. Journal of Statistical Software, 19, 1–46.
18. Griffin, R. & Nunn, C. (2012) Community structure and the spread of infectious disease in primate social networks. Evolutionary Ecology, 26, 779–800.
19. Guenther, S., Ewers, C. & Wieler, L.H. (2011) Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Frontiers in Microbiology, 2, 246.
20. Hamede, R., Bashford, J., Jones, M. & McCallum, H. (2012) Simulating devil facial tumour disease outbreaks across empirically derived contact networks. Journal of Applied Ecology, 49, 447–456.
21. Hirsch, B.T., Reynolds, J.J.H., Gehrt, S.D. & Craft, M.E. (2016) Which mechanisms drive seasonal rabies outbreaks in raccoons? A test using dynamic social network models. Journal of Applied Ecology, 53, 804–813.
22. Johnson, P.T.J., de Roode, J.C. & Fenton, A. (2015) Why infectious disease research needs community ecology. Science, 349, 1259504.
23. Kappeler, P.M. & Fichtel, C. (2012) A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest. Long-Term Field Studies of Primates (eds P.M. Kappeler & D.P. Watts), pp. 101–121. Springer, Berlin, Heidelberg, Germany.
24. Koch, F., Signer, J., Kappeler, P.M. & Fichtel, C. (2016) Intergroup encounters in Verreaux's sifakas (Propithecus verreauxi): who fights and why? Behavioral Ecology and Sociobiology, 70, 797–808.
25. Loehle, C. (1995) Social barriers to pathogen transmission in wild animal populations. Ecology, 76, 326–335.
26. Newman, M.E.J. & Girvan, M. (2004) Finding and evaluating community structure in networks. Physical Review E, 69, 026113.
27. Nunn, C.L., Thrall, P.H. & Kappeler, P.M. (2014) Shared resources and disease dynamics in spatially structured populations. Ecological Modelling, 272, 198–207.
28. Olson, M.E., Goh, J., Phillips, M., Guselle, N. & McAllister, T.A. (1999) Giardia cyst and Cryptosporidium oocyst survival in water, soil, and cattle feces. Journal of Environmental Quality, 28, 1991–1996.
29. Pellis, L., Ball, F., Bansal, S., Eames, K., House, T., Isham, V. & Trapman, P. (2015) Eight challenges for network epidemic models. Epidemics, 10, 58–62.
30. Peng, X., Murphy, T. & Holden, N.M. (2008) Evaluation of the effect of temperature on the die-off rate for Cryptosporidium parvum oocysts in water, soils, and feces. Applied and Environmental Microbiology, 74, 7101–7107.
31. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
32. Rasambainarivo, F.T., Gillespie, T.R., Wright, P.C., Arsenault, J., Villeneuve, A. & Lair, S. (2013) Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. Journal of Wildlife Diseases, 49, 741–743.
33. Reynolds, J.J.H., Hirsch, B.T., Gehrt, S.D. & Craft, M.E. (2015) Raccoon contact networks predict seasonal susceptibility to rabies outbreaks and limitations of vaccination. Journal of Animal Ecology, 84, 1720-1731.
34. Risau-Gusman, S. (2011) Influence of network dynamics on the spread of sexually transmitted diseases. Journal of the Royal Society Interface, 9, 1363–1372.
35. Rosvall, M. & Bergstrom, C.T. (2008) Maps of random walks on complex networks reveal community structure. Proceedings of the National Academy of Sciences of the United States of America, 105, 1118–1123.
36. Salathé, M. & Jones, J.H. (2010) Dynamics and control of diseases in networks with community structure. PLoS Computational Biology, 6, e1000736.
37. Scholz, F. & Kappeler, P.M. (2003) Effects of seasonal water scarcity on the ranging behavior of Eulemur fulvus rufus. International Journal of Primatology, 25, 599–613.
38. Seaholm, S.K., Ackerman, E. & Wu, S.-C. (1988) Latin hypercube sampling and the sensitivity analysis of a Monte Carlo epidemic model. International Journal of Bio-Medical Computing, 23, 97–112.
39. Sijben, S. (2013) Movement Analysis: Analysis of Trajectory Data Using Linear or Brownian Motion Model. R package v. 0.6. http://www.win.tue.nl/~kbuchin/proj/R/movementAnalysis/.
40. da Silva, A.J., Cacciò, S., Williams, C., Won, K.Y., Nace, E.K., Whittier, C., Pieniazek, N.J. & Eberhard, M.L. (2003) Molecular and morphologic characterization of a Cryptosporidium genotype identified in lemurs. Veterinary Parasitology, 111, 297–307.
41. Springer, A. & Kappeler, P.M. (2016) Intestinal parasite communities of six sympatric lemur species at Kirindy Forest, Madagascar. Primate Biology, 3, 51–63.
42. Springer, A., Kappeler, P.M. & Nunn, C.L. (2016b) Replication Data for: Dynamic vs. static social networks in models of parasite transmission: predicting Cryptosporidium spread in wild lemurs. Harvard Dataverse, http://dx.doi.org/10.7910/DVN/OU5RKQ.
43. Springer, A., Mellmann, A., Fichtel, C. & Kappeler, P. (2016a) Social structure and Escherichia coli sharing in a group-living wild primate, Verreaux's sifaka. BMC Ecology, 16, 6.
44. Stehle, J., Voirin, N., Barrat, A. et al. (2011) Simulation of an SEIR infectious disease model on the dynamic contact network of conference attendees. BMC Medicine, 9, 87.
45. VanderWaal, K.L., Atwill, E.R., Isbell, L.A. & McCowan, B. (2013) Linking social and pathogen transmission networks using microbial genetics in giraffe (Giraffa camelopardalis). Journal of Animal Ecology, 83, 406–414.
46. Volz, E. & Meyers, L.A. (2009) Epidemic thresholds in dynamic contact networks. Journal of the Royal Society Interface, 6, 233–241.
47. White, L.A., Forester, J.D. & Craft, M.E. (2015) Using contact networks to explore mechanisms of parasite transmission in wildlife. Biological Reviews. doi: 10.1111/brv.12236.
48. Wobeser, G.A. (2013) Essentials of Disease in Wild Animals. Wiley-Blackwell, Oxford, UK.
49. Zohdy, S., Kemp, A.D., Durden, L.A., Wright, P.C. & Jernvall, J. (2012) Mapping the social network: tracking lice in a wild primate (Microcebus rufus) population to infer social contacts and vector potential. BMC Ecology, 12, 4.