Variable effects of host characteristics on species richness of flea infracommunities in rodents from three continents

Parasitology Research

Volumn 113, Issue 8, 2014, Pages 2777-2788

  Kiffner, Christian ^a,b   Stanko, Michal ^c   Morand, Serge ^d,e   Khokhlova, Irina S ^f   Shenbrot, Georgy I ^f   Laudisoit, Anne ^g,h   Leirs, Herwig ^g   Hawlena, Hadas ^f   Krasnov, Boris R ^f  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b The School for Field Studies   (Tanzania)

^c INSTITUTE OF CHEMISTRY   (Slovakia)

^d CIRAD   (France)

^e INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^f BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^g UNIVERSITY OF ANTWERP   (Belgium)

^h UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Body mass; Fleas; Infestation bias; Rodents; Sex

Indexed keywords

AFRICA; ARTICLE; BODY MASS; EUROPE; FLEA; HOST PARASITE INTERACTION; MALE; MIDDLE EAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; RODENT; SPECIES RICHNESS;

AFRICA, EASTERN; ANIMALS; BODY WEIGHT; ECTOPARASITIC INFESTATIONS; EUROPE; FEMALE; LINEAR MODELS; MALE; MIDDLE EAST; REPRODUCTION; RODENTIA; SEASONS; SIPHONAPTERA; SPECIES SPECIFICITY;

EID: 84905051577     PISSN: 09320113     EISSN: 14321955     Source Type: Journal    
DOI: 10.1007/s00436-014-3937-2     Document Type: Article

References (99)

1. 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
2. Alzaga V, Vicente J, Villanua D, Acevedo P, Casas F, Gortazar C (2008) Body condition and parasite intensity correlates with escape capacity in Iberian hares (Lepus granatensis). Behav Ecol Sociobiol 62:769-775 (Pubitemid 351199153)
3. Attuquayefio DK, Gorman ML, Wolton RJ (2009) Home rang sizes in the wood mouse Apodemus sylvaticus: habitat, sex and seasonal differences. J Zool 210:45-53
4. Bashenina NV(1962) Ecology of the common vole. Moscow Univ Press, Moscow, USSR (in Russian)
5. 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
6. Bates D, Maechler M (2009) lme4: Linear mixed-effects models using S4 classes. R package, version. http://lme4.r-forge.r-project.org/
7. Bordes F, Blumstein DT, Morand S (2007) Rodent sociality and parasite diversity. Biol Letters 3:692-694
8. Bordes F, Morand S (2009) Parasite diversity: an overlooked metric of parasite pressures? Oikos 118:801-806
9. 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
10. Borowski Z (2003) Habitat selection and home range size of field voles Microtus agrestis in Slowínski National Park, Poland. Acta Theriol 48:325-333
11. 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
12. Bronson FH (1989) Mammalian reproductive biology. University of Chicago Press, 325 pp
13. Bronson F, Desjardins C (1971) Steroid hormones and aggressive behaviour in mammals. p. 43-63 In B.E. Eleftheriou, JP Scott (eds) The physiology of aggression and defeat. Subject Strain Bibliography 1971. Paper 1041
14. Brunner JL, Ostfeld RS (2008) Multiple causes of variable tick burdens on small mammal hosts. Ecology 89:2259-2272
15. Buckling A, Rainey PB (2002) The role of parasites in sympatric and allopatric host diversification. Nature 6915:496-499 (Pubitemid 35477039)
16. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information - theoretic approach, 2nd edn. Springer, New York
17. 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
18. Caruso C, Accardi G, Virruso C, Candore G (2013) Sex, gender and immunosenescence: a key to understand the different lifespan between men and women? Immun Ageing 10:20
19. Casto JM, Jr Nolan V, Ketterson ED (2001) Steroid hormones and immune function: experimental studies in wild and captive dar-keyed juncos (Junco hyemalis). Am Nat 157:408-420 (Pubitemid 32235239)
20. Clay CA, Lehmer EM, Previtali A, St Jeor S, Dearing MD (2009) Contact heterogeneities in deer mice: implications for Sin Nombre virus transmission. Proc R Soc Lond B 276:1305-1312
21. Creel S, Creel N, Wildt DE, Monfort SL (1992) Behavioral and endocrine mechanisms of reproductive suppression in Serengeti dwarf mongooses. Anim Behav 43:231-245
22. 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 (Pubitemid 32531315)
23. Erlinge S, Hoogenboom I, Agrell J, Nelson J, Sandell M (1990) Density-related home-range size and overlap in adult field voles (Microtus agrestis) in southern Sweden. J Mammal 71:597-603
24. 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 (Pubitemid 38260811)
25. Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Amer Nat 139:603-622
26. 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/
27. Ginaldi L, Loreto MF, Corsi MP, Modesti M, de Martinis M (2001) Immunosenescence and infectious diseases. Microbes Infect 3:851-857 (Pubitemid 32913168)
28. Gleason ED, Fuxjager MJ, Oyegbile TO, Marler CA (2009) Testosterone release and social context: when it occurs and why. Front Neuroendocrinol 30:460-469
29. Gliwicz J (1988) Seasonal dispersal in non-cyclic populations of Clethrionomys glareolus and Apodemus flavicollis. Acta Theriol 33:263-272
30. Goüy de Bellocq J, Charbonnel N, Morand S (2008) Coevolutionary relationship between helminth diversity and MHC class II polymorphism in rodents. J Evol Biol 21:1144-1150 (Pubitemid 351832273)
31. Grueber CE, Nakagawa S, Laws RJ, Jamieson IG (2011) Multimodel inference in ecology and evolution: challenges and solutions. J Evol Biol 24:699-711
32. Harrison A, Scantlebury M, Montgomery W (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 119:1099-1104
33. Hilbe JM (2011) Negative binomial regression. Cambridge Univ Press, Cambridge
34. 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
35. Hirokawa K, Utsuyama M, Hayashi Y, Kitagawa M, Makinodan T, Fulop T (2013) Slower immune system aging in women versus men in the Japanese population. Immun Ageing 10:19
36. Ims RA (1987) Male spacing systems in microtine rodents. Am Nat 130:475-484
37. Jetz W, Carbone C, Fulford J, Brown JH (2004) The scaling of animal space use. Science 306:266-268 (Pubitemid 39336869)
38. Khokhlova IS, Spinu M, Krasnov BR, Degen AA (2004) Immune responses to fleas in two rodent species differing in natural prevalence of infestation and diversity of flea assemblages. Parasitol Res 94:304-311 (Pubitemid 39517844)
39. 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
40. Khokhlova IS, Serobyan V, Degen AA, Krasnov BR (2010) Host gender and offspring quality in a flea parasitic on a rodent. J Exp Biol 213:3299-3304
41. 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
42. 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 108:323-35
43. Kiffner C, Stanko M, Morand S, Khoklova IS, Shenbrot I, Laudisoit A, Leirs H, Hawlena H, Krasnov B (2013) Sex-biased parasitism is not universal: evidence from rodent-flea associations from three biomes. Oecologia 173:1009-1022. doi:10.1007/s00442-013-2664-1
44. Klimpel S, Förster M, Schmahl G (2007) Parasites of two abundant sympatric rodent species in relation to host phylogeny and ecology. Parasitol Res 100:867-875 (Pubitemid 46175255)
45. 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 (Pubitemid 46633440)
46. Koshev Y, Atanassov N, Kocheva M (2005) Relation between body mass and home range size of small mammals. In Proceedings of the Balkan Scientific Conference of Biology. Eds B. Gruev, M. Nikolov, A. Donev, p 437-444
47. Krasnov BR, Hastriter M, Medvedev SG, Shenbrot GI, Khokhlova IS, Vaschenok VS (1999) Additional records of fleas (Siphonaptera) on wild rodents in the southern part of Israel. Israel J Zool 45:333-340 (Pubitemid 30057032)
48. Krasnov BR, Kokhlova IS (2002) The effect of behavioural interactions on the exchange of flea (Siphonaptera) between two rodent species. J Vector Ecol 26:181-190
49. Krasnov BR, Matthee S (2010) Spatial variation in gender-biased parasitism: host-related, parasite-related and environment-related effects. Parasitology 137:1527-1536
50. 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 (Pubitemid 27095221)
51. Krasnov BR, Burdelova NV, Shenbrot GI, Khokhlova IS (2002) Annual cycles of four flea species (Siphonaptera) in the central Negev desert. Med Vet Entomol 16:266-276
52. Krasnov BR, Shenbrot GI, Khokhlova IS, Degen AA (2004) Flea species richness and parameters of host body, host geography and host "milieu". J Anim Ecol 73:1121-1128 (Pubitemid 39471160)
53. Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:209-217 (Pubitemid 41547136)
54. Krasnov BR, Shenbrot GI, Khokhlova IS, Hawlena H, DEGEN AA (2006a) Temporal variation in parasite infestations of a host individual: does a parasite-free host remain uninfested permanently? Parasitol Res 99:541-545 (Pubitemid 44337940)
55. Krasnov BR, Stanko M, Miklisova D, Morand S (2006b) Habitat variation in species composition of flea assemblages on small mammals in central Europe. Ecol Res 21:460-469 (Pubitemid 44127204)
56. 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 166:1099-1010
57. Krasnov BR, Bordes F, Khokhlova IS, Morand S (2012) Gender-biased parasitism in small mammals: patterns, mechanisms, consequences. Mammalia 76:1-13
58. 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
59. Leirs H (1992) Population ecology of Mastomys natalensis (SMITH, 1834) multimammate rats: possible implications for rodent control in Africa. 273 pp. UIA, Department of Biology, Antwerp.
60. Leirs H, Verheyen W, Michiels M, Verhagen R, Stuyck J (1989) The relation between rainfall and breeding season of Mastomys natalensis (Smith 1834) in Morogoro, Tanzania. Ann soc R zool Belg 119:59-64
61. Lindenfors P, Nunn CL, Jones KE, Cunnungham AA, Sechrest W, Gittleman JL (2007) Parasite species richness in carnivores: effects of host body mass, latitude, geographical range and population density. Global Ecol Biogeograph 16:496-509 (Pubitemid 46916999)
62. Lott DF (1991) Intraspecific variation in the social systems of wild vertebrates. Cambridge Univ Press, Cambridge
63. Luong LT, Perkins SE, Grear DA, Rizzoli A, Hudson PJ (2010) The relative importance of host characteristics and co-infection in generating variation in Heligmosomoides polygyrus fecundity. Parasitology 137:1003-1012
64. Makundi RH, Massawe AW, Mulungu LS (2007) Reproduction and population dynamics of Mastomys natalensis Smith, 1834 in an agricultural landscape in the Western Usambara. Integr Zool 2:233-238
65. 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
66. Matthysen E (2005) Density-dependent dispersal in birds and mammals. Ecography 28:403-416
67. Moller AP, Rosza L (2005) Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts. Oecologia 142:169-176 (Pubitemid 40171982)
68. Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015-2018
69. Morand S, Harvey PH (2000) Mammalian metabolism, longevity and parasite species richness. Proc Biol Sci 267:1999-2003
70. 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 (Pubitemid 39371881)
71. 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 Wildlife Res 57:639-645
72. Nunn CL, Altizer S, Sechrest W, Jones KE, Barton RA, Gittleman JL (2004) Parasites and the evolutionary diversification of primate clades. Am Nat 164:S90-103
73. Ostfeld RS (1985) Limiting resources and territoriality in microtine rodents. Am Nat 126:1-15
74. 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 (Pubitemid 37297458)
75. Poulin R (1996) Sexual inequalities in helminth infections: a cost of being male? Am Nat 147:289-295
76. Poulin R, George-Nascimento M (2007) The scaling of total parasite biomass with host body mass. Int J Parasitol 37:359-364 (Pubitemid 46215590)
77. Previtali MA, Lehmer EM, Pearce-Duvet JMC, Jones JD, Clay CA, Wood BA, Ely PW, Laverty SM, Dearing MD (2010) Roles of human disturbance, precipitation, and a pathogen on the survival and reproductive probabilities of deer mice. Ecology 91:582-592
78. R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.project.org
79. Råberg L, Sim D, Read AF (2007) Disentangling genetic variation for resistance and tolerance to infectious diseases in animals. Science 318:812-814 (Pubitemid 351411775)
80. Råberg L, Graham AL, Read AF (2009) Decomposing health: tolerance and resistance to parasites in animals. Phil Trans R Soc B 364:37-49
81. Razzoli M, Cushing BS, Carter CS, Valsecchi P (2003) Hormonal regulation of agonistic and affiliative behaviour in female Mongolian gerbils (Meriones unguiculatus). Horm Behav 43:549-553 (Pubitemid 36687842)
82. Rolff J (2002) Bateman's principle and immunity. Proc R Soc Lond B 269:867-872
83. Rueesch S, Lemoine M, Richner H (2012) Ectoparasite performance when host condition varies. Parasitol Res 111:1193-1203
84. Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67-74
85. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc Lond B 270:357-366
86. Schwarzenberger T, Klingel H (1994) Telemetrische Untersuchungen zur Raumnutzung und Aktivitätsrhytmik freilebender Gelbhalsmäuse, Apodemus flavicollis Melchior, 1834. Z Säugetierkunde 60:33-40
87. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defenses and trade offs in evolutionary ecology. Trends Ecol Evol 11:317-321
88. Šimková A, Lafond T, Ondrackova M, Jurajda P, Ottova E, Morand S (2008) Parasitism, life history traits and immune defence in cyprinid fish from Central Europe. BMC Evol Biol 8:29. doi:10.1186/1471-2148-8-29
89. 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 (Pubitemid 36064451)
90. Stenseth NC, Lidicker WZ (eds) (1992) Animal dispersal: small mammals as a model. Chapman & Hall, London, p 240
91. van Hooft P, Cosson JF, Vibe-Peteresen S, Leirs H (2008) Dispersal in Mastomys natalensis mice: use of fine-scale genetic analyses for pest management. Hereditas 145:262-273
92. 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
93. 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
94. 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
95. Waterman J (2007) Male mating strategies in rodents. In: Wolff JO, Sherman PW (eds) Rodent societies. An ecological & evolutionary perspective. The University of Chicago Press, Chicago, pp 27-41
96. Wolff JO (1993) Why are female small mammals territorial? Oikos 68:364-370
97. Zahn A, Rupp D (2004) Ectoparasite load in European vespertilionid bats. J Zool 262:383-391 (Pubitemid 38497924)
98. Zuk M (1996) Disease, endocrine-immune interactions, and sexual selection. Ecology 77:1037-1042
99. Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009-1024 (Pubitemid 26419313)