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Sex-biased parasitism is not universal: evidence from rodent–flea associations from three biomes

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Abstract

The distribution of parasites among individual hosts is characterised by high variability that is believed to be a result of variations in host traits. To find general patterns of host traits affecting parasite abundance, we studied flea infestation of nine rodent species from three different biomes (temperate zone of central Europe, desert of Middle East and tropics of East Africa). We tested for independent and interactive effects of host sex and body mass on the number of fleas harboured by an individual host while accounting for spatial clustering of host and parasite sampling and temporal variation. We found no consistent patterns of the effect of host sex and body mass on flea abundance either among species within a biome or among biomes. We found evidence for sex-biased flea infestation in just five host species (Apodemus agrarius, Myodes glareolus, Microtus arvalis, Gerbillus andersoni, Mastomys natalensis). In six rodent species, we found an effect of body mass on flea abundance (all species mentioned above and Meriones crassus). This effect was positive in five species and negative in one species (Microtus arvalis). In M. glareolus, G. andersoni, M. natalensis, and M. arvalis, the relationship between body mass and flea abundance was mediated by host sex. This was manifested in steeper change in flea abundance with increasing body mass in male than female individuals (M. glareolus, G. andersoni, M. natalensis), whereas the opposite pattern was found in M. arvalis. Our findings suggest that sex and body mass are common determinants of parasite infestation in mammalian hosts, but neither of them follows universal rules. This implies that the effect of host individual characteristics on mechanisms responsible for flea acquisition may be manifested differently in different host species.

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References

  • Anderson RM, Gordon DM (1982) Processes influencing the distribution of parasite numbers within host populations with special emphasis on parasite-induced host mortality. Parasitology 85:373–398

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Arneberg P (2002) Host population density and body mass as determinants of species richness in parasite communities: comparative analyses of directly transmitted nematodes of mammals. Ecography 25:88–94

    Article  Google Scholar 

  • Bartón K (2013) Model selection and model averaging based on information criteria (AICc and alike). Available at: http://cran.r-project.org/web/packages/MuMIn/index.html

  • Bashenina NV (1962) Ecology of the common vole. Moscow University Press, Moscow (in Russian)

    Google Scholar 

  • Bashenina NV (ed) (1981) Bank vole. Nauka, Moscow (in Russian)

    Google Scholar 

  • Bates D, Maechler M (2009) lme4: Linear mixed-effects models using S4 classes. R package, version. http://lme4.r-forge.r-project.org/

  • Bordes F, Ponlet N, Goüy de Bellocq J, Ribas A, Krasnov BR, Morand S (2012) Is there sex biased resistance and tolerance in Mediterranean wood mouse (Apodemus sylvaticus) populations facing multiple helminth infections? Oecologia 170:123–135

    Article  PubMed  Google Scholar 

  • Boyer N, Réale D, Marmet J, Pisanu B, Chapuis J-L (2010) Personality, space use and tick load in an introduced population of Siberian chipmunks Tamias sibiricus. J Anim Ecol 79:538–547

    Article  PubMed  Google Scholar 

  • Brunner JL, Ostfeld RS (2008) Multiple causes of variable tick burdens on small mammal hosts. Ecology 89:2259–2272

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach, 2nd edn. Springer, New York

    Google Scholar 

  • Calabrese JM, Brunner JL, Ostfeld RS (2011) Partitioning the aggregation of parasites on hosts into intrinsic and extrinsic components via an extended Poisson-Gamma Mixture Model. PloS ONE 6:e29215

    Article  PubMed  CAS  Google Scholar 

  • Clough D, Heistermann M, Kappeler PM (2010) Host-intrinsic determinants and potential consequences of parasite infection in free-ranging red-fronted lemurs (Eulemur fulvus rufus). Am J Phys Anthropol 142:441–452

    Article  PubMed  Google Scholar 

  • Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. University of Chicago Press, Chicago

    Google Scholar 

  • Demas GE, Nelson RJ (1998) Photoperiod, ambient temperature, and food availability interact to affect reproductive and immune function in adult male deer mice (Peromyscus maniculatus). J Biol Rhythm 13:253–262

    Article  CAS  Google Scholar 

  • Elston DA, Moss R, Boulinier T, Arrowsmith C, Lambin X (2001) Analysis of aggregation, a worked example: numbers of ticks on red grouse chicks. Parasitology 122:563–569

    Article  PubMed  CAS  Google Scholar 

  • Ferrari N, Cattadori IM, Nespereira J, Rizzoli A, Hudson PJ (2004) The role of host sex in parasite dynamics: field experiments on the yellow-necked mouse Apodemus flavicollis. Ecol Lett 7:88–94

    Article  Google Scholar 

  • Folstad I, Krater AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622

    Article  Google Scholar 

  • Gelman A, Su Y-S, Yajima M, Hill J, Pittau MG, Kermann J, Zheng T (2013) arm: data analysis using regression and multilevel/hierarchical models. http://cran.r-project.org/web/packages/arm/

  • Gliwicz J (1988) Seasonal dispersal in non-cyclic populations of Clethrionomys glareolus and Apodemus flavicollis. Acta Theriol 33:263–272

    Google Scholar 

  • Gliwicz J (1992) Patterns of dispersal in non-cyclic populations of small mammals. In: Stenseth NC, Lidicker WZ (eds) Animal dispersal. Small mammals as a model. Chapman and Hall, London, pp 147–159

    Chapter  Google Scholar 

  • Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699–711

    Article  PubMed  CAS  Google Scholar 

  • Gummer DL, Forbes MR, Bender DJ, Barclay RMR (1997) Botfly (Diptera: Oestridae) parasitism of Ord’s kangaroo rats (Dipodomys ordii) at Suffield National Wildlife Area, Alberta, Canada. J Parasitol 83:601–604

    Article  PubMed  CAS  Google Scholar 

  • Harrison A, Scantlebury M, Montgomery W (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119:1099–1104

    Article  Google Scholar 

  • Hart BL, Hart LA, Mooring MS, Olubayo R (1992) Biological basis of grooming behaviour in antelope: the body size, vigilance and habitat principles. Anim Behav 44:615–631

    Article  Google Scholar 

  • Hawlena H, Abramsky Z, Krasnov BR (2005) Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146:200–208

    Article  PubMed  CAS  Google Scholar 

  • Hawlena H, Abramsky Z, Krasnov B, Khokhlova I (2006) Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148:30–39

    Article  PubMed  Google Scholar 

  • Hawlena H, Bashary D, Abramsky Z, Khokhlova IS, Krasnov BR (2008) Programmed versus stimulus-driven anti-parasitic grooming in a rodent: efficiency, time allocation and age-dependence. Behav Ecol 19:929–935

    Article  Google Scholar 

  • Hilbe JM (2011) Negative binomial regression. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jetz W, Carbone C, Fulford J, Brown JH (2004) The scaling of animal space use. Science 306:266–268

    Article  PubMed  CAS  Google Scholar 

  • Khokhlova IS, Serobyan V, Krasnov BR, Degen AA (2009) Is the feeding and reproductive performance of the flea, Xenopsylla ramesis, affected by the gender of its rodent host, Meriones crassus? J Exp Biol 212:1429–1435

    Article  PubMed  Google Scholar 

  • Kiffner C, Lödige C, Alings M, Vor T, Rühe F (2011a) Body-mass or sex-biased tick parasitism in roe deer (Capreolus capreolus)? A GAMLSS approach. Med Vet Entomol 25:39–45

    Article  PubMed  CAS  Google Scholar 

  • Kiffner C, Vor T, Hagedorn P, Niedrig M, Rühe F (2011b) Factors affecting patterns of tick parasitism on forest rodents in tick-borne encephalitis risk areas, Germany. Parasitol Res 108:323–335

    Article  PubMed  Google Scholar 

  • Korallo NP, Vinarsky MV, Krasnov BR, Shenbrot GI, Mouillot D, Poulin R (2007) Are there general rules governing parasite diversity? Small mammalian hosts and gamasid mite assemblages. Divers Distrib 13:353–360

    Article  Google Scholar 

  • Krasnov BR (2008) Functional and evolutionary ecology of fleas. A model for ecological parasitology. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Krasnov BR, Matthee S (2010) Spatial variation in gender-biased parasitism: host-related, parasite-related and environment-related effects. Parasitology 137:1527–1536

    Article  PubMed  Google Scholar 

  • Krasnov BR, Shenbrot GI, Medvedev SG, Vatschenok VS, Khokhlova IS (1997) Host-habitat relations as an important determinant of spatial distribution of flea assemblages (Siphonaptera) on rodents in the Negev Desert. Parasitology 114:159–173

    Article  PubMed  Google Scholar 

  • Krasnov BR, Khokhlova IS, Fielden LJ, Burdelova NV (2001) The effect of air temperature and humidity on the survival of pre-imaginal stages of two flea species (Siphonaptera: Pulicidae). J Med Entomol 38:629–637

    Article  PubMed  CAS  Google Scholar 

  • Krasnov BR, Khokhlova I, Shenbrot G (2002a) The effect of host density on ectoparasite distribution: an example with a desert rodent parasitized by fleas. Ecology 83:164–175

    Article  Google Scholar 

  • Krasnov BR, Burdelova NV, Shenbrot GI, Khokhlova IS (2002b) Annual cycles of four flea species (Siphonaptera) in the central Negev desert. Med Vet Entomol 16:266–276

    Article  PubMed  CAS  Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004a) Flea species richness and parameters of host body, host geography and host “milieu”. J Anim Ecol 73:1121–1128

    Article  Google Scholar 

  • Krasnov BR, Shenbrot GI, Khokhlova IS (2004b) Sampling fleas: the reliability of host infestation data. Med Vet Entomol 18:232–240

    Article  PubMed  CAS  Google Scholar 

  • Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005a) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209–217

    Article  PubMed  Google Scholar 

  • Krasnov BR, Khokhlova IS, Arakelyan M, Degen AA (2005b) Is a starving host tastier? Reproduction in fleas parasitizing food limited rodents. Funct Ecol 19:625–631

    Article  Google Scholar 

  • Krasnov BR, Stanko M, Morand S (2006) Age-dependent flea (Siphonaptera) parasitism in rodents: a host’s life history matters. J Parasitol 92:242–248

    Article  PubMed  Google Scholar 

  • Krasnov BR, Stanko M, Matthee S, Laudisot A, Leirs H, Khokhlova IS, Korallo-Vinarskaya NP, Vinarski MV, Morand S (2011) Male hosts drive infracommunity structure of ectoparasites. Oecologia 166:1099–1100

    Article  PubMed  Google Scholar 

  • Laudisoit A, Leirs H, Makundi RH, Krasnov BR (2009) Seasonal and habitat dependence of species composition of flea assemblages parasitic on small mammals in Tanzania. Integr Zool 4:196–212

    Article  PubMed  Google Scholar 

  • Lloyd-Smith JO, Schreiber SJ, Kopp PE, Getz WM (2005) Superspreading and the effect of individual variation on disease emergence. Nature 438:355–359

    Article  PubMed  CAS  Google Scholar 

  • Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge University Press, Cambridge

    Google Scholar 

  • Matthee S, McGeoch MA, Krasnov BR (2010) Gender-biased ectoparasite infections: species-specific variation and the extent of male-biased parasitism. Parasitology 137:651–660

    Article  PubMed  Google Scholar 

  • McCurdy DG, Shutler D, Mullie A, Forbes MR (1998) Sex-biased parasitism of avian hosts: relations to blood parasite taxon and mating system. Oikos 82:303–312

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Morales-Montor J, Chavarria A, De Leon MA, Del Castillo LI, Escobedo EG, Sanchez EN, Vargas JA, Hernandez-Flores M, Romo-Gonzalez T, Larralde C (2004) Host gender in parasitic infections of mammals: an evaluation of the females host supremacy paradigm. J Parasitol 90:531–546

    Article  PubMed  CAS  Google Scholar 

  • Morand S, Pointier J-P, Borel G, Theron A (1993) Pairing probability of schistosomes related to their distribution among the host population. Ecology 74:2444–2449

    Article  Google Scholar 

  • Morand S, De Bellocq JG, Stanko M, Miklisova D (2004) Is sex-biased ectoparasitism related to size dimorphism in small mammals of Central Europe? Parasitology 129:505–510

    Article  PubMed  CAS  Google Scholar 

  • Navarro-Gonzalez N, Verheyden H, Hoste H, Cargnelutti B, Lourtet B, Merlet J, Daufresne T, Lavín S, Hewison AJM, Morand S, Serrano E (2011) Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape. Eur J Wildl Res 57:639–645

    Article  Google Scholar 

  • Perkins SE, Cattadori IM, Tagliapietra V, Rizzoli AP, Hudson PJ (2003) Empirical evidence for key hosts in persistence of a tick-borne disease. Int J Parasitol 33:909–917

    Article  PubMed  Google Scholar 

  • Peters RH (1983) The ecological implications of body size. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Peus F (1972) Zur Kenntnis der Flöhe Deutschlands (Insecta, Siphonaptera). IV. Faunistik und Ökologie der Säugetierflöhe. Zool Jahrb Abt Syst Oekol Geogr Tiere 99:400–418

    Google Scholar 

  • Poulin R (1996) Sexual inequalities in helminth infections: a cost of being male? Am Nat 147:289–295

    Article  Google Scholar 

  • Poulin R (2007) Evolutionary ecology of parasites. From individuals to communities, 2nd edn. Princeton University Press, Princeton

  • Poulin R, George-Nascimento M (2007) The scaling of total parasite biomass with host body mass. Int J Parasitol 37:359–364

    Article  PubMed  Google Scholar 

  • R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.project.org

  • Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812–814

    Article  PubMed  Google Scholar 

  • Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Philos Trans R Soc Lond B 364:37–49

    Article  Google Scholar 

  • Rossin A, Malizia AI (2002) Relationship between helminth parasites and demographic attributes of a population of the subterranean rodent Ctenomys talarum (Rodentia: Octodontidae). J Parasitol 88:1268–1270

    PubMed  CAS  Google Scholar 

  • Scantlebury M, McWilliams MM, Marks NJ, Dick JTA, Edgar H, Lutermann H (2010) Effects of life-history traits on parasite load in grey squirrels. J Zool 282:246–255

    Article  Google Scholar 

  • Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74

    Article  Google Scholar 

  • Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597–610

    Article  PubMed  Google Scholar 

  • Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade offs in evolutionary ecology. Trends Ecol Evol 11:317–321

    Article  PubMed  CAS  Google Scholar 

  • Skorping A, Jensen KH (2004) Disease dynamics: all caused by males? Trends Ecol Evol 19:219–220

    Article  PubMed  Google Scholar 

  • Speakman JR (2007) The energy cost of reproduction in small rodents. Acta Theriol Sin 27:1–13

    Google Scholar 

  • Stanko M, Miklisova D, Gouy de Bellocq J, Morand S (2002) Mammal density and patterns of ectoparasite species richness and abundance. Oecologia 131:289–295

    Article  Google Scholar 

  • Stanko M, Krasnov BR, Morand S (2006) Relationship between host abundance and parasite distribution: inferring regulating mechanisms from census data. J Anim Ecol 75:575–583

    Article  PubMed  Google Scholar 

  • Stasinopoulos M, Rigby B (2012) gamlss.dist: distributions to be used for GAMLSS modelling. http://cran.r-project.org/web/packages/gamlss.dist/index.html

  • Teichroeb JA, Kutz SJ, Parkar U, Thompson RCA, Sicotte P (2009) Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: possible anthropozoonotic transmission. Am J Phys Anthropol 140:498–507

    Article  PubMed  Google Scholar 

  • Vázquez L, Panadero R, Dacal V, Pato FJ, López C, Díaz P, Arias MS, Fernández G, Díez-Baños P, Morrondo P (2011) Tick infestation (Acari: Ixodidae) in roe deer (Capreolus capreolus) from northwestern Spain: population dynamics and risk stratification. Exp Appl Acarol 53:399–409

    Article  PubMed  Google Scholar 

  • Viljoen H, Bennet NC, Ueckermann EA, Luterman H (2011) The role of host traits, season and group size on parasite burdens in a cooperative mammal. PloS ONE 6:e27003

    Article  PubMed  CAS  Google Scholar 

  • Vor T, Kiffner C, Hagedorn P, Niedrig M, Rühe F (2010) Tick burden on European roe deer (Capreolus capreolus). Exp Appl Acarol 51:405–417

    Article  PubMed  Google Scholar 

  • Wilson K, Bjørnstad ON, Dobson AP, Merler S, Poglayen G, Randolph SE, Read AF, Skorping A (2002) Heterogeneities in macroparasite infections: patterns and processes. In: Hudson PJ, Rizzoli A, Grenfell BT, Heesterbeek H, Dobson AP (eds) The ecology of wildlife diseases. Oxford University Press, Oxford, pp 6–44

    Google Scholar 

  • Wirsing AJ, Azevedo FCC, Lariviere S, Murray DL (2007) Patterns of gastrointestinal parasitism among five sympatric prairie carnivores: are males reservoirs? J Parasitol 93:504–510

    Article  PubMed  Google Scholar 

  • Woolhouse MEJ, Dye C, Etard F-F, Smith T, Charlwood JD, Garnett GP, Hagan P, Hii JL, Ndhlovu PD, Quinnell RJ, Watts CH, Chandiwana SK, Anderson RM (1997) Heterogeneities in the transmission of infectious agents: implications for the design of control programs. Proc Natl Acad Sci USA 94:338–342

    Article  PubMed  CAS  Google Scholar 

  • Zahn A, Rupp D (2004) Ectoparasite load in European vespertilionid bats. J Zool 262:383–391

    Article  Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024

    PubMed  CAS  Google Scholar 

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Acknowledgments

Allan Degen read an earlier version of the manuscript and made helpful comments. Two anonymous referees provided excellent comments that considerably improved the manuscript. C.K. received a postdoctoral scholarship from the German Academic Exchange Service (DAAD). Studies in Israel were partly supported by Israel Science Foundation (grant 26/12 to I.S.K. and B.R.K.). Studies in Slovakia were conducted under the licenses of the Ministry of Environment of the Slovak Republic No. 297/108/06-3.1 and No. 6743/2008-2.1. Studies in Tanzania were supported by the Belgian Fund for the Research in Industry and Agro-alimentary, the Fund for Scientific Research—Flanders for scientific research, the University of Antwerp, and the Sokoine University of Agriculture (Tanzania). This is publication no. 798 of the Mitrani Department of Desert Ecology.

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Kiffner, C., Stanko, M., Morand, S. et al. Sex-biased parasitism is not universal: evidence from rodent–flea associations from three biomes. Oecologia 173, 1009–1022 (2013). https://doi.org/10.1007/s00442-013-2664-1

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