Effects of life-history traits on parasite load in grey squirrels

Journal of Zoology

Volumn 282, Issue 4, 2010, Pages 246-255

  Scantlebury, M ^a   Maher McWilliams, M ^a   Marks, N J ^a   Dick, J T A ^a   Edgar, H ^b   Lutermann, H ^c  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b AGRI FOOD AND BIOSCIENCES INSTITUTE   (United Kingdom)

^c UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Parasite; Reproduction; Sexual selection; Size dimorphism; Testosterone

Indexed keywords

BODY CONDITION; BODY SIZE; HOST-PARASITE INTERACTION; IMMUNE SYSTEM; INSECT; LIFE HISTORY THEORY; LIFE HISTORY TRAIT; MORPHOLOGY; NEMATODE; REPRODUCTIVE COST; REPRODUCTIVE EFFORT; REPRODUCTIVE STRATEGY; RESOURCE ALLOCATION; RODENT; SEXUAL DIMORPHISM; SEXUAL SELECTION; TESTOSTERONE; TRADE-OFF;

CAROLINENSIS; MAMMALIA; NEMATODA; SCIURIDAE; SIPHONAPTERA (FLEAS);

EID: 78650131164     PISSN: 09528369     EISSN: 14697998     Source Type: Journal    
DOI: 10.1111/j.1469-7998.2010.00734.x     Document Type: Article

References (89)

1. Bachman, G.C. (2003). Food supplements modulate changes in leucocyte numbers in breeding male ground squirrel. J. Exp. Biol. 206, 2373-2380.
2. Barnard, C.J. & Behnke, J.M. (1990). Parasitsim and host behaviour. London: Taylor & Francis Ltd.
3. Bateman, A.J. (1948). Intra-sexual selection in Drosophila. Heredity 2, 349-368.
4. Becker, C.D. (1992). Proximate factors influencing the timing and occurrence of reproduction in red squirrels Tamiasciurus hudsonicus. PhD thesis, University of Alberta, Edmonton.
5. Becker, C.D., Boutin, S. & Larsen, K.W. (1998). Constraints on first reproduction in North American red squirrels. Oikos 81, 81-92.
6. Blanco, G., De La Puente, J., Corroto, M., Baz, A. & Colas, J. (2001). Condition-dependent immune defence in the Magpie: how important is ectoparasitism? Biol. J. Linn. Soc. 72, 279-286.
7. Boonstra, R., Lane, J.E., Boutin, S., Bradley, A., Desantis, L., Newman, A.E. & Soma, K.K. (2008). Plasma DHEA levels in wild, territorial red squirrels: seasonal variation and effect of ACTH. Gen. Comp. Endocrinol. 158, 61-67.
8. 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.
9. Clutton-Brock, T.H., Albon, S.D. & Guiness, F.E. (1988). Reproductive success in male and female red deer. In Reproductive success: 325-343. Clutton-Brock, T.H. (Ed.). Chicago: University of Chicago Press.
10. Corbin, E., Vicente, J., Martin-Hernando, M.P., Acevedo, P., Perez-Rodriguez, L. & Gortazar, C. (2008). Spleen mass as a measure of immune strength in mammals. Mammal Rev. 38, 108-115.
11. Crawley, M.J. (2007). The R book. Chichester: John Wiley & Sons Ltd.
12. Demas, G.E. & Sakaria, S. (2005). Leptin regulates energetic tradeoffs between body fat and humoural immunity. Proc. Roy. Soc. Lond. Ser. B 272, 1845-1850.
13. Deter, J., Chaval, Y., Galan, M., Berthier, K., Salvador, A.R., Garcia, J.C.C., Morand, S., Cosson, J.-F. & Charbonnel, N. (2007). Linking demography and host dispersal to Trichuris arvicolae distribution in a cyclic vole species. Int. J. Parasitol. 37, 813-824.
14. Devevey, G., Niculita-Herzel, H., Biollaz, F., Yvon, C., Chapuisat, M. & Christe, P. (2008). Developmental, metabolic and immunological costs of flea infestation in the common vole. Funct. Ecol. 22, 1091-1098.
15. Fernandez-Llario, P., Parra, A., Cerrato, R. & De Mendoza, J.H. (2004). Spleen size variations and reproduction in a Mediterranean population of wild boar (Sus scrofa). Eur. J. Wildl. Res. 50, 13-17.
16. Folstad, I. & Karter, A.J. (1992). Parasites, bright males, and the immunocompetence handicap. Am. Nat. 139, 603-622.
17. Gadgil, M. & Bossert, W.H. (1970). Life historical consequences of natural selection. Am. Nat. 104, 1-24.
18. Garside, P., Behnke, J.M. & Rose, R.A. (1989). The immune response of male DSN hamsters to a primary infection with Ancylostoma ceylanicum. J. Helminthol. 63, 251-260.
19. Gittleman, J.L. & Thompson, S.D. (1988). Energy allocation in mammalian reproduction. Am. Zool. 28, 863-875.
20. Guinet, C., Roux, J.P., Bonnet, M. & Mison, V. (1998). Effect of body size, body mass and body condition on reproduction of female South African fur seals (Arctocephalus pusillus) in Namibia. Can. J. Zool. 76, 1418-1424.
21. Gurnell, J. (1996). The effects of food availability and winter weather on the dynamics of a grey squirrel population in southern England. J. Appl. Ecol. 33, 325-338.
22. Hamilton, W. & Zuk, M. (1982). Hertitable true fitness and bright birds: a role for parasites? Science 218, 384-386.
23. Hanssen, S.A., Folstad, I. & Erikstad, K.E. (2003). Reduced immunocompetence and cost of reproduction in common eiders. Oecolgia 136, 457-464.
24. Harison, A., Scantlebury, M. & Montgomery, W.I. (2010). Body mass and sex-biased parasitism in wood mice. Apodemus sylvaticus. Oikos 119, 1099-1104.
25. Hawlena, H., Bashary, D., Abramsky, Z. & Krasnov, B.R. (2007). Benefits, costs and constraints of anti-parasitic grooming in adult and juvenile rodents. Ethology 113, 394-402.
26. Hawlena, H., Krasnov, B.R., Abramsky, Z., Khokhlova, I.S., Saltz, D., Kam, M., Tamir, A. & Degen, A.A. (2006). Flea infestation and energy requirements of rodent hosts: are there general rules? Funct. Ecol. 20, 1028-1036.
27. Hayssen, V. (2008). Patterns of body and tail length and body mass in Sciuridae. J. Mammal. 89, 852-873.
28. Hopkins, G.H.E. & Rothschild, M. (1971). An illustrated catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History) with keys and short descriptions for the identification of families, genera, species and subspecies of the order. Leptopsyllidae and Ancistropsyllidae, Vol. V. London: British Museum (Natural History).
29. Humphries, M.M. & Boutin, S. (1996). Reproductive demands and weight gains: a paradox in female red squirrels (Tamiasciurus hudsonicus). J. Anim. Ecol. 65, 332-338.
30. Humphries, M.M. & Boutin, S. (1999). Mass-dependent reproduction or reproduction-dependent mass? A comment on body mass and first-time reproduction in female sciurids. Can. J. Zool. 77, 171-173.
31. John, J.L. (1994). The avian spleen: a neglected organ. Quart. Rev. Biol. 69, 327-351.
32. Kakuma, Y., Takeuchi, Y., Mori, Y. & Hart, B.L. (2003). Hormonal control of grooming behavior in domestic goats. Physiol. Behav. 78, 61-66.
33. Kenward, R.E. (1985). Ranging behavior and population dynamics in grey squirrel. Symp. Br. Ecol. Soc. 25, 319-330.
34. Khokhlova, I.S., Krasnov, B.R., Kam, M., Burdelova, N.I. & Degen, A.A. (2002). Energy cost of ectoparasitism: the flea Xenopsylla ramensis on the desert gerbil Gerbillus dasyurus. J. Zool. (Lond.) 258, 349-354.
35. Klein, S.L. (2000). The effects of hormones on sex differences in infection: from genes to behavior. Neurosci. Biobehav. Rev. 24, 627-638.
36. Klein, S.L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunol. 26, 247-264.
37. Koprowski, J.L. (1993). Alternative reproductive tactics in male eastern grey squirrels - making the best of a bad job. Behav. Ecol. 4, 165-171.
38. Koprowski, J.L. (1994). Sciurus carolinensis. Mamm. Species 480, 1-9.
39. Koprowski, J.L. (1998). Conflict between the sexes: a review of social and mating systems of the tree squirrels. In Ecology and evolutionary biology of tree squirrels: 33-41. Steele, M.A., Merritt, J.F. & Zegers, D.A. (Eds). Martinsville: Virginia Museum of Natural History.
40. Koprowski, J.L. (2005). Annual cycles in body mass and reproduction of endangered Mt. Graham red squirrels. J. Mammal. 86, 309-313.
41. Koprowski, J.L. (2007). Alternative reproductive tactics and strategies of tree squirrels. In Rodent societies: an ecological and evolutionary perspective: 86-98. Wolff, J.O. & Sherman, P.W. (Ed.). Chicago: University of Chicago Press.
42. Krasnov, B.R., Morand, S., Hawlena, H., Khokhlova, I.S. & Shenbrot, G.I. (2005). Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia 146, 209-217.
43. Kristan, D.M. (2002). Effects of intestinal nematodes during lactation: consequences for host morphology, physiology and offspring mass. J. Exp. Biol. 205, 3955-3965.
44. Kristan, D.M. & Hammond, K.A. (2000). Combined effects of cold exposure and sub-lethal intestinal parasites on host morphology and physiology. J. Exp. Biol. 203, 3495-3504.
45. Kristan, D.M. & Hammond, K.A. (2003). Physiological and morphological responses to simultaneous cold exposure and parasite infection by wild-derived house mice. Funct. Ecol. 17, 464-471.
46. Li, F.-H., Zhong, W.-Q., Wang, Z. & Wang, D.-H. (2007). Rank in a food competition test and humoral immune functions in male Brandt's voles (Lasiopodomys brandtii). Physiol. Behav. 90, 490-495.
47. Lochmiller, R.L. & Deerenberg, C. (2000). Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88, 87-98.
48. McKean, K.A. & Nunney, L. (2001). Increased sexual activity reduces male immune function in Drosophila melanogaster. PNAS 98, 7904-7909.
49. Millar, J.S. (1987). Energy reserves in breeding small rodents. Symp. Zool. Soc. Lond. 57, 231-240.
50. Millesi, E., Huber, S., Dittami, J.P., Hoffmann, I.E. & Daan, S. (1998). Parameters of mating effort and success in male European ground squirrels, Spermophilus citellus. Ethology 104, 298-313.
51. Møller, A.P., Christe, P. & Mavarez, J. (1998). Condition, disease and immune defence. Oikos 83, 301-306.
52. Moore, S.L. & Wilson, K. (2002). Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297, 2015-2017.
53. Mooring, M.S., McKenzie, A.A. & Hart, B.L. (1996). Role of sex and breeding status in grooming and total tick load in impala. Behav. Ecol. Sociobiol. 39, 259-266.
54. Mooring, M.S., Patton, M.L., Reisig, D.D., Osborne, E.R., Kanallakan, A.L. & Aubery, S.M. (2006). Sexually dimorphic grooming in bison: the influence of body size, activity budget and androgens. Anim. Behav. 72, 737-745.
55. Mooring, M.S. & Samuel, W.M. (1998). The biological basis of grooming in moose: programmed versus stimulus-driven grooming. Anim. Behav. 56, 1561-1570.
56. 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.
57. Neuhaus, P. (2003). Parasite removal and its impact on litter size and body condition in Columbian ground squirrels (Spermophilus columbianus). Proc. Roy. Soc Lond. Ser. B 270, S213-S215.
58. Poulin, R. (1996a). Sexual inequalities in helminth infections: a cost of being a male? Am. Nat. 147, 287-295.
59. Poulin, R. (1996b). Helminth growth in vertebrate hosts: does host sex matter? Int. J. Parasitol. 26, 1311-1315.
60. Price, T., Schluter, D. & Heckman, N.E. (1993). Sexual selection when the female directly benefits. Biol J Linn Soc 48, 187-211.
61. Radespiel, U. (2000). Sociality in the Gray mouse lemur (Microcebus murinus) in Northwestern Madagascar. Am. J. Primatol. 51, 21-40.
62. Rolff, J. (2002). Bateman's principle and immunity. Proc. Roy. Soc. Lond. Ser. B 269, 867-872.
63. Rozsa, L., Reiczigel, J. & Majoros, G. (2000). Quantifying parasites in samples of hosts. J. Parasitol. 86, 228-232.
64. Saino, N., Møller, A.P. & Bolzern, A.M. (1995). Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): on experimental test of the immunocompetence hypothesis. Behav. Ecol. 6, 397-404.
65. Scantlebury, M., Waterman, J.M. & Bennett, N.C. (2008). Alternative reproductive tactics in male Cape ground squirrels Xerus inauris. Physiol. Behav. 94, 359-367.
66. Scantlebury, M., Waterman, J.M., Hillegass, M., Speakman, J.R. & Bennett, N.C. (2007). Energetic costs of parasitism in the Cape ground squirrel Xerus inauris. Proc. Roy. Soc. Lond. Ser. B 274, 2169-2177.
67. Schalk, G. & Forbes, M.R. (1997). Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78, 67-74.
68. Schradin, C., Scantlebury, M., Pillay, N. & König, B. (2009). Testosterone levels in dominant sociable males are lower than in solitary roamers: physiological differences between three male reproductive tactics in a sociably flexible mammal. Am. Nat. 173, 376-388.
69. Schwanz, L.E. (2006). Schistosome infection in deer mice (Peromyscus maniculatus): impacts on host physiology, behavior and energetics. J. Exp. Biol. 209, 5029-5037.
70. Schwanz, L.E. (2008). Chronic parasitic infection alters reproductive output in deer mice. Behav. Ecol. Sociobiol. 62, 1351-1358.
71. Sheldon, B.C. & Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol. Evol. 11, 317-321.
72. Sheridan, L.A.D., Poulin, R., Ward, D.F. & Zuk, M. (2000). Sex differences in parasitic infections amoung arthropod hosts: is there a male bias? Oikos 88, 327-334.
73. Soulsby, E.J.W. (1982). Helminths, arthropods and protozoa of domesticated animals, Seventh edn: 212-258. London/Philadelphia: Bailliere Tindall/Lea and Febiger.
74. Speakman, J.R. (2008). The physiological costs of reproduction in small mammals. Phil. Trans. Roy. Soc. Lond. Ser. B 363, 375-398.
75. Stearns, S.C. (1992). The evolution of life histories. Oxford: Oxford University Press.
76. Thompson, S.D. (1992). Gestation and lactation in small mammals: basal metabolic rate and the limits to energy use. In Mammalian energetics - interdisciplinary views of metabolism and reproduction: 213-259. Tomasi, T.E. & Horton, T.H. (Eds). Ithaca: Comstock Publishing Associates, Cornell University Press.
77. Trivers, R.L. (1972). Parental investment and sexual selection. In Sexual selection and the descent of man: 136-179. Campbell, B. (Ed.). Chicago: Aldine-Atherton.
78. Vicente, J., Pérez-Rodrígeuz, L. & Gortazar, C. (2007). Sex, age, spleen size, and kidney fat of red deer relative to infection intensities of the lungworm Elaphostrongylus cervi. Naturwissenschaften 94, 581-587.
79. Watkins, R.A., Moshier, S.E., Odell, W.D. & Pinter, A.J. (1991). Splenomegaly and reticulocytosis caused by Babesia microti infections in natural-populations of the montane vole, Microtus montanus. J. Protozool. 38, 573-576.
80. Wauters, L.A. & Dhondt, A.A. (1989). Body weight, longevity and reproductive success in red squirrels (Sciurus vulgaris). J. Anim. Ecol. 58, 637-651.
81. Wauters, L.A. & Dhondt, A.A. (1995). Lifetime reproductive success and its correlates in female Eurasian red squirrels. Oikos 72, 402-410.
82. Wauters, L.A., Vermeulen, M., Van Dongen, S., Bertolino, S., Molinari, A., Tosi, G. & Matthysen, E. (2007). Effects of spatio-temporal variation in food supply on red squirrel Sciurus vulgaris body size and body mass and its consequences for some fitness components. Ecography 30, 51-65.
83. Webley, L.S., Pope, G.S. & Johnson, E. (1985). Seasonal changes in the testis and accessory reproductive organs and seasonal and circadian changes in plasma testosterone concentrations in the male grey squirrel (Sciurus carolinensis). Gen. Comp. Endocrinol. 59, 15-23.
84. Westneat, D.F. & Birkhead, T.R. (1998). Alternative hypothesis linking immune system and mate choice for good genes. Proc. Roy. Soc. Lond. Ser. B 265, 1065-1073.
85. Wilson, K. & Grenfell, B.T. (1997). Generalized linear modelling for parasitologists. Parasitol. Today 13, 33-38.
86. Wilson, K., Grenfell, B.T. & Shaw, D.J. (1996). Analysis of aggregated parasite distributions: a comparison of methods. Funct. Ecol. 10, 592-601.
87. Wingfield, J.C., Hegner, R.E., Dufty, A.M. & Ball, G.F. (1990). The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems and breeding strategies. Am. Nat. 136, 829-846.
88. Woods, H.A. & Hellgren, E.C. (2003). Seasonal changes in the physiology of male Virginia opossums (Didelphis virginiana): signs of the Dasyurid Semelparity syndrome? Physiol. Biochem. Zool. 76, 406-417.
89. Zuk, M. & Stoehr, A.M. (2002). Immune defense and host life history. Am. Nat. 160, S9-S22.