Behavioral Ecology and Sociobiology

, Volume 65, Issue 12, pp 2219–2227 | Cite as

Effect of gyrodactylid ectoparasites on host behaviour and social network structure in guppies Poecilia reticulata

  • Darren P. CroftEmail author
  • Mathew Edenbrow
  • Safi K. Darden
  • Indar W. Ramnarine
  • Cock van Oosterhout
  • Joanne Cable
Original Paper


Understanding how individuals modify their social interactions in response to infectious disease is of central importance for our comprehension of how disease dynamics operate in real-world populations. Whilst a significant amount of theoretical work has modelled disease transmission using network models, we have comparatively little understanding of how infectious disease impacts on the social behaviour of individuals and how these effects scale up to the level of the population. We experimentally manipulated the parasite load of female guppies (Poecilia reticulata) and introduced fish either infected with the ectoparasites Gyrodactylus spp. (experimental) or uninfected (control) into replicated semi-natural populations of eight size-matched female guppies. We quantified the behaviour and social associations of both the introduced fish and the population fish. We found that infected experimental fish spent less time associating with the population fish than the uninfected control fish. Using information on which fish initiated shoal fission (splitting) events, our results demonstrate that the population fish actively avoided infected experimental fish. We also found that the presence of an infected individual resulted in a continued decline in social network clustering up to at least 24 h after the introduction of the infected fish, whereas in the control treatment, the clustering coefficient showed an increase at this time point. These results demonstrate that the presence of a disease has implications for both the social associations of infected individuals and for the social network structure of the population, which we predict will have consequences for infectious disease transmission.


Social networks Social organisation Infection Disease transmission Parasite transmission Group living Shoaling 



We thank Jens Krause and Dick James for stimulating discussions and two anonymous reviewers for their constructive comments on the manuscript. JC was funded by an Advanced Natural Environment Research Council Research Fellowship (NER/J/S/2002/00706).


  1. Anderson RM, May RM (1979) Population biology of infectious diseases: part I. Nature 280(5721):361–367PubMedCrossRefGoogle Scholar
  2. Arnold W, Anja VL (1993) Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality. Behav Ecol 4(1):36–39. doi: 10.1093/beheco/4.1.36 CrossRefGoogle Scholar
  3. Barber I, Downey LC, Braithwaite VA (1998) Parasitism, oddity and the mechanism of shoal choice. J Fish Biol 53(6):1365–1368CrossRefGoogle Scholar
  4. Barber I, Hoare D, Krause J (2000) Effects of parasites on fish behaviour: a review and evolutionary perspective. Rev Fish Biol Fish 10(2):131–165CrossRefGoogle Scholar
  5. Bell DC, Atkinson JS, Carlson JW (1999) Centrality measures for disease transmission networks. Soc Networks 21(1):1–21. doi: 10.1016/s0378-8733(98)00010-0 CrossRefGoogle Scholar
  6. Borgatti SP, Everett MG, Freeman LC (2002) Ucinet for windows: software for social network analysis. Analytic Technologies, HarvardGoogle Scholar
  7. Brown CR, Brown MB (2004) Group size and ectoparasitism affect daily survival probability in a colonial bird. Behav Ecol Sociobiol 56(5):498–511. doi: 10.1007/s00265-004-0813-6 CrossRefGoogle Scholar
  8. Buckling A, Rainey PB (2002) The role of parasites in sympatric and allopatric host diversification. Nature 420(6915):496–499PubMedCrossRefGoogle Scholar
  9. Cable J (2011) Poeciliid parasites. In: Evans JP, Pilastro A, Schlupp I (eds) Ecology & evolution of poeciliid fishes. University of Chicago Press, ChicagoGoogle Scholar
  10. Cable J, Harris PD (2002) Gyrodactylid developmental biology: historical review, current status and future trends. Int J Parasitol 32(3):255–280PubMedCrossRefGoogle Scholar
  11. Cable J, Scott ECG, Tinsley RC, Harris PD (2002) Behavior favoring transmission in the viviparous monogenean Gyrodactylus turnbulli. J Parasitol 88(1):183–184. doi: 10.1645/0022-3395(2002)088[0183:bftitv];2 PubMedGoogle Scholar
  12. Choisy M, Guégan JF, Rohani P (2007) Mathematical modeling of infectious diseases dynamics. In: Tibayrenc M (ed) Encyclopedia of infectious diseases: modern methodologies. Wiley, Hoboken, pp 379–404CrossRefGoogle Scholar
  13. Christley RM, Pinchbeck GL, Bowers RG, Clancy D, French NP, Bennett R, Turner J (2005) Infection in social networks: using network analysis to identify high-risk individuals. Am J Epidemiol 162(10):1024–1031PubMedCrossRefGoogle Scholar
  14. Corner LAL, Pfeiffer DU, Morris RS (2003) Social-network analysis of Mycobacterium bovis transmission among captive brushtail possums (Trichosurus vulpecula). Prev Vet Med 59(3):147–167PubMedCrossRefGoogle Scholar
  15. Côté IM, Poulinb R (1995) Parasitism and group size in social animals: a meta-analysis. Behav Ecol 6(2):159–165. doi: 10.1093/beheco/6.2.159 CrossRefGoogle Scholar
  16. Craft ME, Volz E, Packer C, Meyers LA (2009) Distinguishing epidemic waves from disease spillover in a wildlife population. Proc R Soc Lond B Bio 276(1663):1777–1785. doi: 10.1098/rspb.2008.1636 CrossRefGoogle Scholar
  17. Croft DP, Albanese B, Arrowsmith BJ, Botham M, Webster M, Krause J (2003a) Sex biased movement in the guppy (Poecilia reticulata). Oecologia 137:62–68PubMedCrossRefGoogle Scholar
  18. Croft DP, Arrowsmith BJ, Bielby J, Skinner K, White E, Couzin ID, Magurran AE, Ramnarine I, Krause J (2003b) Mechanisms underlying shoal composition in the Trinidadian guppy (Poecilia reticulata). Oikos 100:429–438CrossRefGoogle Scholar
  19. Croft DP, Krause J, James R (2004) Social networks in the guppy (Poecilia reticulata). Proc R Soc Lond B Biol Sci 271:S516–S519CrossRefGoogle Scholar
  20. Croft DP, James R, Thomas POR, Hathaway C, Mawdsley D, Laland KN, Krause J (2006) Social structure and co-operative interactions in a wild population of guppies (Poecilia reticulata). Behav Ecol Sociobiol 59(5):644–650CrossRefGoogle Scholar
  21. Croft DP, James R, Krause J (2008) Exploring animal social networks. Princeton University Press, PrincetonGoogle Scholar
  22. Cross PC, Lloyd-Smith JO, Bowers JA, Hay CT, Hofmeyr M, Getz WM (2004) Integrating association data and disease dynamics in a social ungulate: bovine tuberculosis in African buffalo in the Kruger National Park. Ann Zool Fenn 41(6):879–892Google Scholar
  23. Darden SK, James R, Ramnarine IW, Croft DP (2009) Social implications of the battle of the sexes: sexual harassment disrupts female sociality and social recognition. Proc R Soc Lond B Biol Sci 276(1667):2651–2656. doi: 10.1098/rspb.2009.0087 CrossRefGoogle Scholar
  24. Dobson AP (1988) The population biology of parasite-induced changes in host behavior. Q Rev Biol 63:139–165PubMedCrossRefGoogle Scholar
  25. Drewe JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proc R Soc Lond B Biol Sci 277(1681):633–642. doi: 10.1098/rspb.2009.1775 CrossRefGoogle Scholar
  26. Eames KTD, Keeling MJ (2002) Modeling dynamic and network heterogeneities in the spread of sexually transmitted diseases. Proc Natl Acad Sci USA 99(20):13330–13335PubMedCrossRefGoogle Scholar
  27. Funk S, Salathé M, Jansen VAA (2010) Modelling the influence of human behaviour on the spread of infectious diseases: a review. J R Soc Interface. doi:10.1098/rsif.2010.0142
  28. Godfrey SS, Bull CM, James R, Murray K (2009) Network structure and parasite transmission in a group living lizard, the gidgee skink, Egernia stokesii. Behav Ecol Sociobiol 63(7):1045–1056. doi: 10.1007/s00265-009-0730-9 CrossRefGoogle Scholar
  29. Godfrey SS, Moore JA, Nelson NJ, Bull CM (2010) Social network structure and parasite infection patterns in a territorial reptile, the tuatara (Sphenodon punctatus). Int J Parasitol 40(13):1575–1585PubMedCrossRefGoogle Scholar
  30. Gudelj I, White KAJ (2004) Spatial heterogeneity, social structure and disease dynamics of animal populations. Theor Popul Biol 66(2):139–149. doi: 10.1016/j.tpb.2004.04.003 PubMedCrossRefGoogle Scholar
  31. Gupta S, Anderson RM, May RM (1989) Networks of sexual contacts—implications for the pattern of spread of HIV. Aids 3(12):807–817PubMedCrossRefGoogle Scholar
  32. Keeling M (2005) The implications of network structure for epidemic dynamics. Theor Popul Biol 67(1):1–8PubMedCrossRefGoogle Scholar
  33. Kolluru GR, Grether GF, Dunlop E, South SH (2009) Food availability and parasite infection influence mating tactics in guppies (Poecilia reticulata). Behav Ecol 20(1):131–137. doi: 10.1093/beheco/arn124 CrossRefGoogle Scholar
  34. Krause J, Godin JGJ (1996) Influence of parasitism on shoal choice in the banded killifish (Fundulus diaphanus, Teleostei, Cyprinodontidae). Ethology 102(1):40–49CrossRefGoogle Scholar
  35. Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, OxfordGoogle Scholar
  36. LeMenach A, Legrand J, Grais RF, Viboud C, Valleron A-J, Flahault A (2005) Modeling spatial and temporal transmission of foot-and-mouth disease in France: identification of high-risk areas. Vet Res 36(5–6):699–712CrossRefGoogle Scholar
  37. Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76(2):326–335CrossRefGoogle Scholar
  38. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford Series in Ecology and Evolution. Oxford University Press, OxfordGoogle Scholar
  39. May RM (1988) Conservation and disease. Conserv Biol 2(1):28–30. doi: 10.1111/j.1523-1739.1988.tb00332.x CrossRefGoogle Scholar
  40. May RM, Anderson RM (1979) Population biology of infectious diseases: part II. Nature 280(5722):455–461PubMedCrossRefGoogle Scholar
  41. Meyers LA, Pourbohloul B, Newman MEJ, Skowronski DM, Brunham RC (2005) Network theory and SARS: predicting outbreak diversity. J Theor Biol 232(1):71–81PubMedCrossRefGoogle Scholar
  42. Moore J (2002) Parasites and the behavior of animals. Oxford Series in Ecology and Evolution. Oxford University Press, OxfordGoogle Scholar
  43. Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82(4):591–605. doi: 10.1111/j.1469-185X.2007.00027.x PubMedCrossRefGoogle Scholar
  44. Newman MEJ (2001) Scientific collaboration networks. II. Shortest paths, weighted networks, and centrality. Phys Rev E 6401(1):7. doi: 016132 Google Scholar
  45. Newman MEJ (2003) Properties of highly clustered networks. Phys Rev E 68(2):art. no.-026121Google Scholar
  46. Pitcher TJ, Magurran AE, Allan JR (1983) Shifts of behaviour with shoal size in Cyprinids. In: Proceedings of the 3rd British Freshwater Fish Conference, 1983, pp 220–228Google Scholar
  47. 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. Vet Res 39(3):31PubMedCrossRefGoogle Scholar
  48. Potterat JJ, Rothenberg RB, Muth SQ (1999) Network structural dynamics and infectious disease propagation. Int J STD AIDS 10(3):182–185. doi: 10.1258/0956462991913853 PubMedCrossRefGoogle Scholar
  49. Pourbohloul B, Meyers LA, Skowronski DM, Krajden M, Patrick DM, Brunham RC (2005) Modeling control strategies of respiratory pathogens. Emerg Infect Dis 11(8):1249–1256PubMedGoogle Scholar
  50. Richards EL, van Oosterhout C, Cable J (2010) Sex-specific differences in shoaling affect parasite transmission in guppies. PLoS ONE 5(10):e13285PubMedCrossRefGoogle Scholar
  51. Rothenberg RB, Potterat JJ, Woodhouse DE, Muth SQ, Darrow WW, Klovdahl AS (1998) Social network dynamics and HIV transmission. Aids 12(12):1529–1536PubMedCrossRefGoogle Scholar
  52. Scott ME, Anderson RM (1984) The population-dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata. Parasitology 89:159–194PubMedCrossRefGoogle Scholar
  53. Steidl RJ, Hayes JP, Schauber E (1997) Statistical power analysis in wildlife research. J Wildlife Manage 61(2):270–279CrossRefGoogle Scholar
  54. Stoehr AM (1999) Are significance thresholds appropriate for the study of animal behaviour? Anim Behav 57(5):F22–F25PubMedCrossRefGoogle Scholar
  55. Thomas L (1997) Retrospective power analysis. Conserv Biol 11(1):276–280. doi: 10.1046/j.1523-1739.1997.96102.x CrossRefGoogle Scholar
  56. Tildesley MJ, House TA, Bruhn MC, Curry RJ, O’Neil M, Allpress JLE, Smith G, Keeling MJ (2010) Impact of spatial clustering on disease transmission and optimal control. Proc Natl Acad Sci USA 107(3):1041–1046. doi: 10.1073/pnas.0909047107 PubMedCrossRefGoogle Scholar
  57. Tobler M, Schlupp I (2008) Influence of black spot disease on shoaling behaviour in female western mosquitofish, Gambusia affinis (Poeciliidae, Teleostei). Environ Biol Fishes 81(1):29–34. doi: 10.1007/s10641-006-9153-x CrossRefGoogle Scholar
  58. van Oosterhout C, Joyce DA, Cummings SM, Blais J, Barson NJ, Ramnarine IW, Mohammed RS, Persad N, Cable J (2006) Balancing selection, random genetic drift, and genetic variation at the major histocompatibility complex in two wild populations of guppies (Poecilia reticulata). Evolution 60(12):2562–2574PubMedCrossRefGoogle Scholar
  59. van Oosterhout C, Mohammed RS, Hansen H, Archard GA, McMullan M, Weese DJ, Cable J (2007) Selection by parasites in spate conditions in wild Trinidadian guppies (Poecilia reticulata). Int J Parasitol 37(7):805–812. doi: 10.1016/j.ijpara.2006.12.016 PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Darren P. Croft
    • 1
    Email author
  • Mathew Edenbrow
    • 1
  • Safi K. Darden
    • 1
  • Indar W. Ramnarine
    • 2
  • Cock van Oosterhout
    • 3
  • Joanne Cable
    • 4
  1. 1.Centre for Research in Animal Behaviour, College of Life and Environmental Sciences, Washington Singer LabsUniversity of ExeterExeterUK
  2. 2.Department of Life SciencesThe University of the West IndiesSt. AugustineTrinidad & Tobago
  3. 3.School of Environmental SciencesUniversity of East AngliaNorwichUK
  4. 4.School of BiosciencesCardiff UniversityCardiffUK

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