Abstract
The distribution of parasites is often characterised by substantial aggregation with a small proportion of hosts harbouring the majority of parasites. This pattern can be generated by abiotic and biotic factors that affect hosts and determine host exposure and susceptibility to parasites. Climate factors can change a host’s investment in life-history traits (e.g. growth, reproduction) generating temporal patterns of parasite aggregation. Similarly, host age may affect such investment. Furthermore, sex-biased parasitism is common among vertebrates and has been linked to sexual dimorphism in morphology, behaviour and physiology. Studies exploring sex-biased parasitism have been almost exclusively conducted on polygynous species where dimorphic traits are often correlated. We investigated the effects of season and life-history traits on tick loads of the monogamous eastern rock sengi (Elephantulus myurus). We found larger tick burdens during the non-breeding season possibly as a result of energetic constraints and/or climate effects on the tick. Reproductive investment resulted in increased larval abundance for females but not males and may be linked to sex-specific life-history strategies. The costs of reproduction could also explain the observed age effect with yearling individuals harbouring lower larval burdens than adults. Although adult males had the greatest larval tick loads, host sex appears to play a minor role in generating the observed parasite heterogeneities. Our study suggests that reproductive investment plays a major role for parasite patterns in the study species.
References
Altizer S, Dobson A, Hosseini P, Hudson P, Pascual M, Rohani P (2006) Seasonality and the dynamics of infectious diseases. Ecol Lett 9:467. doi:10.1111/j.1461-0248.(2005)00879.x
Benoit JB, Denlinger DL (2010) Meeting the challenges of on-host and off-host water balance in blood-feeding arthropods. J Insect Physiol 56:1366–1376. doi:10.1016/j.jinsphys.2010.02.014
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. doi:10.1111/j.1365-2656.2010.01659.x
Burnham KP, Anderson DR (2002) Model selection and multimodel inference, 2nd edn. Springer, New York
Cattadori IM, Boag B, Bjornstad ON, Cornell SJ, Hudson PJ (2005) Peak shift and epidemiology in a seasonal host–nematode system. Proc R Soc B 272:1163–1169. doi:10.1098/rspb.2004.3050
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
Cornell SJ, Bjornstad ON, Cattadori IM, Boag B, Hudson PJ (2008) Seasonality, cohort-dependence and the development of immunity in a natural host–nematode system. Proc R Soc B 275:511–518. doi:10.1098/rspb.2007.1415
Fitzgibbon CD (1997) The adaptive significance of monogamy in the golden-rumped elephant-shrew. J Zool 242:167–177
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622
Fourie LJ, Horak IG, van den Heever JJ (1992) The relative importance of rock elephant shrews Elephantulus myurus and Namaqua rock mice Aethomys namaquensis for economically important ticks. S Afr J Zool 27:108–114
Fourie LJ, Du Toit JS, Kok DJ, Horak IG (1995) Arthropod parasites of elephant-shrews, with particular reference to ticks. Mammal Rev 25:31–37
Fourie LJ, Du Toit JS, Kok DJ, Horak IG (2005) Elephant shrews as hosts of immature ixodid ticks. Onderstepoort J Vet Res 72:293–301
Harrison A, Scantlebury M, Montgomery WI (2010) Body mass and sex-biased parasitism in wood mice Apodemus sylvaticus. Oikos 199:1099–1104. doi:10.1111/j.1600-0706.2009.18072.x
Hawlena H, Abramsky Z, Krasnov BR (2006) Ectoparasites and age-dependent survival in a desert rodent. Oecologia 148:30–39. doi:10.1007/s00442-005-0345-4
Hughes VL, Randolph SE (2001) Testosterone depresses innate and acquired resistance to ticks in natural rodent hosts: a force for aggregated distributions of parasites. J Parasitol 87:49–54
Klein SL (2004) Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol 26:247–264
Krasnov BR, Morand S, Hawlena H, Khokhlova IS, Shenbrot GI (2005) Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146:219–217. doi:10.1007/s00442-005-0189-y
Lourenco SI, Palmeirin JM (2008) Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? Parasitol Res 104:127–134. doi:10.1007/s00436-008-1170-6
Lutermann H, Medger K, Horak IG (2012) Abiotic and biotic determinants of tick burdens in the eastern rock sengi (Elephantulus myurus). Med Vet Entomol. doi:10.1111/j.1365-2915.2011.01002.x
Martin LB, Weil ZM, Nelson RJ (2008) Seasonal changes in vertebrate immune activity: mediation by physiological trade-offs. Phil Trans R Soc Lond B 363:329–339. doi:10.1098/rstb.2007.2142
Medger K (2010). The reproductive biology of two small southern African mammals, the spiny mouse, Acomys spinosissimus (Rodentia: Muridae) and the Eastern rock elephant-shrew, Elephantulus myurus (Macroscelidea: Macroscelididae). PhD thesis. University of Pretoria
Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018
Morand S, Goüy de Belloco J, Stanko M, Miklisovà D (2004) Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129:505–510. doi:10.1017/S0031182004005840
Mougeot F, Irvine JR, Seivwright L, Redpath SM, Piertney SB (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav Ecol 15:930–937. doi:10.1093/beheco/arh087
Mougeot F, Redpath SM, Piertney SB (2005) Elevated spring testosterone increases parasite intensity in male red grouse. Behav Ecol 17:117–125. doi:10.1093/beheco/arj005
Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285–296
Needham GR, Teel PD (1991) Off-host physiological ecology of ixodid ticks. Ann Rev Entomol 36:659–681
Nelson RJ (2004) Seasonal immune function and sickness responses. Trends Immunol 25:187–192
Nelson RJ, Demas GE, Klein SL, Kriegsfeld LJ (2002) Seasonal patterns of stress, immune function, and disease. Cambridge University Press, Cambridge
Olsson M, Wapstra E, Madsen T, Silverin B (2000) Testosterone ticks and travels: a test of the immunocompetence-handicap hypothesis in free-ranging male sand lizards. Proc R Soc B 267:239–2343. doi:10.1098/rspb.2000.1289
Pelletier F, Page KA, Ostiguy T, Festa-Bianchet M (2005) Fecal counts of lungworm larvae and reproductive effort in bighorn sheep, Ovis canadensis. Oikos 110:473–480
Porteus IS, Pankhurst SJ (1998) Social structure of the mara (Dolichotis patagonium) as a determinant of gastro-intestinal parasitism. Parasitology 116:269–275
Poulin R (2007) Evolutionary ecology of parasites. Princeton University Press, Princeton
Randolph SE (2004) Tick ecology: processes and patterns behind the epidemiological risk posed by ixodid ticks as vectors. Parasitology 129:S37–S65. doi:10.1017/S0031182004004925
Randolph SE, Green RM, Hoodless AN, Peacey MF (2002) An empirical quantitative framework for the seasonal population dynamics of the tick Ixodes ricinus. Int J Parasitol 32:979–989
Rathbun GB (1979) The social structure and ecology of elephant shrews. Adv Ethol 20:1–79
Rathbun GB, Rathbun CD (2006) Social structure of the bushveld sengi (Elephantulus intufi) in Namibia and the evolution of monogamy in the Macroscelidea. J Zool 269:391–399. doi:10.1111/j.1469-7998.2006.00087.x
Ribble DO, Perrin MR (2005) Social organization of the Eastern elephant shrew (Elephantulus myurus): the evidence for mate guarding. Belg J Zool 135:167–173
Rolff J (2002) Bateman’s principle and immunity. Proc R Soc Lond B 269:867–872. doi:10.1098/rspb.2002.1959
Rózsa L, Reiczigel J, Majoros G (2000) Quantifying parasites in samples of hosts. J Parasitol 86:228–232
Scantlebury M, Maher McWilliams M, Marks NJ, Dick JTA, Edgar H, Lutermann H (2010) Effects of life history traits on parasitism in Grey squirrels (Sciurus carolinensis). J Zool 282:246–255. doi:10.1111/j.1469-7998.2010.00734.x
Schubert M, Pillay N, Ribble DO, Schradin C (2009a) The round-eared sengi and the evolution of social monogamy: factors that constrain males to live with a single female. Ethology 115:972–985. doi:10.1111/j.1439-0310.2009.01684.x
Schubert M, Schradin C, Rödel HG, Pillay N, Ribble DO (2009b) Male mate guarding in a socially monogamous mammal, the round-eared sengi: on costs and trade-offs. Behav Ecol Sociobiol 64:257–264. doi:10.1007/s00265-009-0842-2
Skinner JD, Chimimba CT (2005) The mammals of the southern African subregion, 3rd edn. Cambridge University Press, Cambridge
Soliman S, Marzouk AS, Main AJ, Montasser AA (2001) Effect of sex, size, and age of commensal rat hosts on the infestation parameters of their ectoparasites in a rural area of Egypt. J Parasitol 87:1308–1316
Symonds MRE, Moussalli A (2011) A brief guide to model selection, multimodel interference and model averaging in behavioural ecology using Akaike’s information criterion. Behav Ecol Sociobiol 65:13–21
Wilson K, Bjornstad ON, Dobson AP, Merler S, Poglaen G, Randolph SE, Read AF, Skorping A (2001) 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
Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1024
Acknowledgements
We thank the management, particularly D. Dewsnap, and staff of the Goro Game Reserve for permission to collect animals in the reserve and their continuous support. A. Harwood, A. Köhler, W. Matten, K. Ntuli, A. Prins, L. Riato and M. Sebonego are thanked for help during the field work. The manuscript was greatly improved by the comments of three anonymous reviewers. KM acknowledges a doctoral grant from the National Research Foundation (NRF), HL a Research Fellowship from the University of Pretoria and IGH funding from the University of Pretoria and the NRF.
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Lutermann, H., Medger, K. & Horak, I.G. Effects of life-history traits on parasitism in a monogamous mammal, the eastern rock sengi (Elephantulus myurus). Naturwissenschaften 99, 103–110 (2012). https://doi.org/10.1007/s00114-011-0874-0
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DOI: https://doi.org/10.1007/s00114-011-0874-0