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Digging for answers: contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal


Due to the density-dependent nature of parasite transmission parasites are generally assumed to constrain the evolution of sociality. However, evidence for a correlation between group size and parasite burden is equivocal, particularly for mammals. Host contact rates may be modified by mobility of the host and parasite as well as social barriers. In the current study, we used the common mole-rat (Cryptomys hottentotus hottentotus), a social subterranean rodent, as a model system to investigate the effect of host density and frequency of contact rates on ectoparasite burdens. To address these factors we used a study species that naturally varies in population densities and intergroup contact rates across its geographic range. We found that ectoparasite prevalence, abundance and species richness decreased with increasing host density at a regional scale. At the same time, measures of parasite burden increased with intergroup contact rates. Ectoparasite burdens decreased with colony size at the group level possibly as a result of increased grooming rates. Equating group size with population density might be too simplistic an approach when assessing parasite distributions in social mammals. Our data suggest that frequency-dependent mechanisms may play a much greater role at a population level than density-dependent mechanisms in determining parasite distributions in social species. We suggest that future studies should explicitly consider behavioural mechanisms that may affect parasite distribution.

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  1. Altizer S, Nunn CL, Thrall PH 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. Altizer S, Dobson A, Hosseini P et al (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467–484. doi:10.1111/j.1461-0248.2005.00879.x

  3. Anderson RM, May RM (1978) Regulation and stability of host-parasite population interactions. I. Regulatory processes. J Anim Ecol 47:219–247

  4. Archer EK, Bennett NC, Ueckermann EA, Lutermann H (2014) Ectoparasite burdens of the common mole-rat (Cryptomys hottentotus hottentotus) from the Cape Provinces of South Africa. J Parasitol 100:79–84. doi:10.1645/13-270.1

  5. Arneberg P, Skorping A, Grenfell B, Read AF (1998) Host densities as determinants of abundance in parasite communities. Proc R Soc B 265:1283–1289

  6. Arnold W, Lichtenstein AV (1993) Ectoparasite loads decrease the fitness of alpine marmots (Marmota marmota) but are not a cost of sociality. Behav Ecol 4:36–39

  7. Bates D, Maechler M, Bolker B (2012) lme4: linear mixed-effects models using S4 classes.

  8. Bennett NC, Faulkes CG (2000) African mole-rats: ecology and eusociality. Cambridge University Press, Cambridge

  9. Bishop JM, Jarvis JUM, Spinks AC et al (2004) Molecular insight into patterns of colony composition and paternity in the common mole-rat Cryptomys hottentotus hottentotus. Mol Ecol 13:1217–1229. doi:10.1111/j.1365-294X.2004.02131.x

  10. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Lett 3:692–694. doi:10.1098/rsbl.2007.0393

  11. Bordes F, Morand S, Kelt DA, Van Vuren DH (2009) Home range and parasite diversity in mammals. Am Nat 173:467–474. doi:10.1086/597227

  12. Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, New York

  13. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. doi:10.1007/s00265-010-1029-6

  14. Chapman CA, Rothman JA, Hodder SAM (2009) Can parasite infections be a selective force influencing primate group size? A test with red colobus. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 423–440

  15. Chapman CA, Bowman DD, Ghai RIAR et al (2012) Protozoan parasites in group-living primates: testing the biological island hypothesis. Am J Primatol 517:510–517. doi:10.1002/ajp.20992

  16. Christe P, Arlettaz R, Vogel P (2000) Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis). Ecol Lett 3:207–212

  17. Cizauskas CA, Bellan SE, Turner WC et al (2014) Frequent and seasonally variable sublethal anthrax infections are accompanied by short-lived immunity in an endemic system. J Anim Ecol 83:1078–1090. doi:10.1111/1365-2656.12207

  18. Cizauskas CA, Turner WC, Pitts N, Getz WM (2015) Seasonal patterns of hormones, macroparasites, and microparasites in wild African ungulates: the interplay among stress, reproduction, and disease. PLoS One 10:e0120800. doi:10.1371/journal.pone.0120800

  19. Côté IM, Poulin R (1995) Parasitism and group size in a social animals: a meta-analysis. Behav Ecol 6:159–165

  20. Cutrera AP, Zenuto RR, Lacey EA (2014) Interpopulation differences in parasite load and variable selective pressures on MHC genes in Ctenomys talarum. J Mamm. doi:10.1644/13-MAMM-A-120

  21. Drewe JA (2010) Who infects whom? Social networks and tuberculosis transmission in wild meerkats. Proc R Soc B 277:633–642. doi:10.1098/rspb.2009.1775

  22. Ezenwa VO (2004a) Host social behavior and parasitic infection: a multifactorial approach. Behav Ecol 15:446–454. doi:10.1093/beheco/arh028

  23. Ezenwa VO (2004b) Interactions among host diet, nutritional status and gastrointestinal parasite infection in wild bovids. Int J Parasitol 34:535–542. doi:10.1016/j.ijpara.2003.11.012

  24. Ezenwa VO, Ekernas SL, Creel S (2012) Unravelling complex associations between testosterone and parasite infection in the wild. Funct Ecol. doi:10.1111/j.1365-2435.2011.01919.x

  25. Fournier DA, Skaug HJ, Ancheta J et al (2012) AD Model Builder: using automatic differentiation for statistical inference of highly parameterized complex nonlinear models. Optim Methods Softw 27:233–249

  26. Freeland WJ (1976) Pathogens and the evolution of primate sociality. Biotropica 8:12–24

  27. Freeland WJ (1979) Primate social groups as biological islands. Ecology 60:719–728

  28. Garamszegi LZ (2011) Information-theoretic approaches to statistical analysis in behavioural ecology: an introduction. Behav Ecol Sociobiol 65:1–11. doi:10.1007/s00265-010-1028-7

  29. Gillespie TR, Lonsdorf EV, Canfield EP et al (2010) Demographic and ecological effects on patterns of parasitism in eastern chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania. Am J Phys Anthropol 544:534–544. doi:10.1002/ajpa.21348

  30. Griffin RH, Nunn CL (2012) Community structure and the spread of infectious disease in primate social networks. Evol Ecol 26:779–800. doi:10.1007/s10682-011-9526-2

  31. Hickman GC (1979) A live trap and trapping technique for fossorial mammals. South Afr J Zool 14:9–12

  32. Hillegass MA, Waterman JM, Roth JD (2008) The influence of sex and sociality on parasite loads in an African ground squirrel. Behav Ecol 19:1006–1011. doi:10.1093/beheco/arn070

  33. Huffman MA, Pebsworth P, Bakuneeta C et al (2009) Chimpanzee-parasite ecology at Budongo Forest (Uganda) and the Mahale Mountains (Tanzania): influence of climatic differences on self-medicative behavior. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambrige University Press, Cambridge, pp 331–350

  34. Klompen H, Junge RE, Williams CV (2015) Ectoparasites of Propithecus diadema (Primates: Indriidae) with notes on unusual attachment site selection by Haemaphysalis lemuris (Parasitiformes: Ixodidae). J Med Entomol. doi:10.1093/jme/tjv032

  35. Leclaire S, Faulkner CT (2014) Gastrointestinal parasites in relation to host traits and group factors in wild meerkats Suricata suricatta. Parasitology 141:925–933. doi:10.1017/S0031182013002333

  36. Lindenfors P, Nunn CL, Jones KE et al (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographic range and population density. Glob Ecol Biogeogr 1:1–14

  37. Loehle C (1995) Social barriers to pathogen transmission in wild animal populations. Ecology 76:326–335

  38. Lopez J, Wey TW, Blumstein DT (2013) Patterns of parasite prevalence and individual infection in yellow-bellied marmots. J Zool 291:296–303. doi:10.1111/jzo.12076

  39. Luong LT, Grear DA, Hudson PJ (2014) Manipulation of host-resource dynamics impacts transmission of trophic parasites. Int J Parasitol 44:737–742. doi:10.1016/j.ijpara.2014.05.004

  40. Lutermann H, Bennett NC (2008) Strong immune function: a benefit promoting the evolution of sociality? J Zool 275:26–32. doi:10.1111/j.1469-7998.2007.00403.x

  41. Lutermann H, Bennett N, Speakman JR, Scantlebury M (2013) Energetic benefits of sociality offset the costs of parasitism in a cooperative mammal. PLoS One 8:e57969. doi:10.1371/journal.pone.0057969

  42. Lutermann H, Carpenter-Kling T, Ueckermann EA et al (2015) Ectoparasite burdens of the Damaraland mole-rat (Fukomys damarensis) from Southern Africa. J Parasitol. doi:10.1645/15-775

  43. Manlove KR, Cassirer EF, Cross PC et al (2014) Costs and benefits of group living with disease: a case study of pneumonia in bighorn lambs (Ovis canadensis). Proc R Soc B 281:20142331

  44. Marshall AG (1981) The ecology of ectoparasitic insects. Academic Press, London

  45. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018

  46. Morand S (2015) (macro-) Evolutionary ecology of parasite diversity: from determinants of parasite species richness to host diversification. Int J Parasitol Parasites Wildl 4:80–87. doi:10.1016/j.ijppaw.2015.01.001

  47. Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727

  48. Nunn CL, Dokey AT (2006) Ranging patterns and parasitism in primates. Comp Gen Pharmacol. doi:10.1098/rsbl.2006.0485

  49. Nunn CL, Altizer S, Jones KE, Sechrest W (2003a) Comparative test of parasite species richness in primates. Am Nat 162:597–614

  50. Nunn CL, Gittleman JL, Antonovics J (2003b) A comparative study of white blood cell counts and disease risk in carnivores. Proc R Soc B 270:347–356. doi:10.1098/rspb.2002.2249

  51. Nunn CL, Jordan F, McCabe CM et al (2015) Infectious disease and group size: more than just a numbers game. Philos Trans R Soc B Biol Sci 370:20140111. doi:10.1098/rstb.2014.0111

  52. Patterson JEH, Ruckstuhl KE (2013) Parasite infection and host group size: a meta-analytical review. Parasitology 140:803–813

  53. Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton

  54. Renwick AR, Lambin X (2013) Host-parasite interactions in a fragmented landscape. Int J Parasitol 43:27–35. doi:10.1016/j.ijpara.2012.10.012

  55. Rifkin JL, Nunn CL, Garamszegi LZ (2012) Do animals living in larger groups experience greater parasitism? A meta-analysis. Am Nat 180:70–82. doi:10.1086/666081

  56. Rimbach R, Bisanzio D, Galvis N et al (2015) Brown spider monkeys (Ateles hybridus): a model for differentiating the role of social networks and physical contact on parasite transmission dynamics. Philos Trans R Soc B 370:20140110. doi:10.1098/rstb.2014.0110

  57. Romanach SS (2005) Influences of sociality and habitat on African mole-rat burrowing patterns. Can J Zool 83:1051–1058

  58. Roper TJ, Bennett NC, Conradt L, Molteno AJ (2001) Environmental conditions in burrows of two species of African mole-rat, Georhychus capensis and Cryptomys damarensis. J Zology 254:101–107

  59. Spinks AC, Van der Horst G, Bennett NC (1997) Influence of breeding season and reproductive status on male reproductive characteristics in the common mole-rat, Cryptomys hottentotus hottentotus. J Reprod Fertil 109:79–86

  60. Spinks AC, O’Riain MJ, Polakow DA (1998) Intercolonial encounters and xenophobia in the common mole rat, Cryptomys hottentotus hottentotus (Bathyergidae): the effects of aridity, sex, and reproductive status. Behav Ecol 9:354–359

  61. Spinks AC, Bennett NC, Jarvis JUM (1999) Regulation of reproduction in female common mole-rats (Cryptomys hottentotus hottentotus): the effects of breeding season and reproductive status. J Zool 248:161–168

  62. Spinks AC, Bennett NC, Jarvis JUM (2000a) A comparison of the ecology of two populations of the common mole-rat, Cryptomys hottentotus hottentotus: the effect of aridity on food, foraging and body mass. Oecologia. doi:10.1007/s004420000460

  63. Spinks AC, Jarvis JUM, Bennett NC (2000b) Comparative patterns of philopatry and dispersal in two common mole-rat populations: implications for the evolution of mole-rat sociality. J Anim Ecol 69:224–234

  64. Sumbera R, Chitaukali WN, Elichová M et al (2004) Microclimatic stability in burrows of an Afrotropical solitary bathyergid rodent, the silvery mole-rat (Heliophobius argenteocinereus). J Zool 263:409–416. doi:10.1017/S095283690400545X

  65. Symonds M, Moussalli A (2011) A brief guide to model selection, multimodel inference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21. doi:10.1007/s00265-010-1037-6

  66. Thomas HG, Scantlebury M, Swanepoel D et al (2013) Seasonal changes in burrow geometry of the common mole rat (Rodentia: Bathyergidae). Naturwissenschaften 100:1023–1030. doi:10.1007/s00114-013-1105-7

  67. Van Vuren D (1996) Ectoparasites, fitness, and social behaviour of yellow-bellied marmots. Ethology 102:686–694

  68. Vicente J, Höxe U, Fernández-De-Mera IG, Gortazar C (2007) The importance of parasite life history and host density in predicting the impact of infections in red deer. Oecologia 152:655–664. doi:10.1007/s00442-007-0690-6

  69. Viljoen H, Bennett NC, Ueckermann EA, Lutermann H (2011) The role of host traits, season and group size on parasite burdens in a cooperative mammal. PLoS One 6:e27003. doi:10.1371/journal.pone.0027003

  70. Vleck D (1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Biol 52:391–396

  71. Walsh PD, Bermejo M, Rodríguez-Teijeiro JD (2009) Disease avoidance and the evolution of primate social connectivity: Ebola, bats, gorillas, and chimpanzee. In: Huffman MA, Chapman CA (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 183–197

  72. Wilson K, Bjørnstad ON, Dobson AP et al (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT et al (eds) The ecology of wildlife diseases. Oxford University Press, New York, pp 6–44

  73. Wilson K, Knell R, Boots M, Koch-Osborne J (2003) Group living and investment in immune defence: an interspecific analysis. J Anim Ecol 72:133–143

  74. Winternitz J (2012) Parasite infection and host dynamics in a naturally fluctuating rodent population. Can J Zool 1160:1149–1160. doi:10.1139/Z2012-083

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We thank the farm owners for access to their property and Northern and Western Cape Nature Conservation for issuing capture permits. This research was approved by the Animal Ethics Committee of the University of Pretoria (EC005-11). We are indebted to a number of volunteers during fieldwork, to Eddie Ueckermann and Eddie Green for their help with parasite identification, and the South African weather service for climatic data. The work was funded by the National Research Foundation–South African Research Chair for Mammalian Behavioural Ecology and Physiology to N. C. B. and a University of Pretoria Research Fellowship to H. L.

Author contribution statement

E. K. A. conducted the fieldwork, parasite identification and data analyses and wrote the first draft of the manuscript. H. L. contributed to the statistical analyses. H. L., N. C. B. and C. G. F. contributed to the study design and revisions of the manuscript.

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Correspondence to Heike Lutermann.

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Approval from the ethics committee of the University of Pretoria as well as the Nature Conservation authorities was obtained before this study was commenced.

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The authors declare that they have no competing interests.

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Communicated by Joanna E. Lambert.

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Archer, E.K., Bennett, N.C., Faulkes, C.G. et al. Digging for answers: contributions of density- and frequency-dependent factors on ectoparasite burden in a social mammal. Oecologia 180, 429–438 (2016).

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  • Cryptomys
  • Ectoparasite
  • Group size
  • Parasite transmission
  • Sociality