Abstract
Immune traits may trade off against one another, or against other life history traits such as growth, development, and reproduction. Breeding introduces additional constraints on investment in immunity that may differ for each sex. During contests for access to females, males may be subjected to injuries that could result in infections. Thus, breeding males should show greater investment in first-line defenses against infection, as compared to other defenses, or as compared to investments by conspecific females. We tested these predictions of the immunoredistribution hypothesis by comparing white blood cell profiles of breeding male and female American toads. In this species, smaller males often occupy terrestrial positions as isolated satellites, while larger males are more likely to engage in attempted displacement of amplexed rivals, making the latter more likely to be injured and vulnerable to infections. Because heterophils are important first-line defenses against bacterial infections, we predicted that larger males would have higher proportions of heterophils in their leukocyte profiles than smaller males; this prediction was supported. However, contrary to expectation, females and larger males had similar proportions of heterophils, possibly because females were equally susceptible to injury during attempts to dislodge amplexed partners. Future work on white blood cell profiles of breeding amphibians is warranted, particularly for species where the sexes differ in likelihood of injury.
References
Adamo SA (2004) How should behavioural ecologists interpret measurements of immunity? Anim Behav 68:1443–1449
Adamo SA, Jensen M, Younger M (2001) Changes in lifetime immunocompetence in male and female Gryllus texensis (formerly G. integer): trade-offs between immunity and reproduction. Anim Behav 62:417–425
Alexander J, Stimson WH (1988) Sex hormones and the course of parasitic infection. Parasitol Today 4:189–193
Arak A (1983) Male–male competition and mate choice in anuran amphibians. In: Bateson P (ed) Mate choice. Cambridge University Press, Cambridge, pp 181–210
Bakkegard KA, Guyera C (2004) Sexual size dimorphism in the Red Hills salamander, Phaeognathus hubrichti (Caudata: Plethodontidae: Desmognathinae). J Herpetol 39:8–15
Bennett GF (1970) Simple techniques for making avian blood smears. Can J Zool 48:585–586
Black JG (1996) Microbiology: principles and applications. Simon & Schuster, Upper Saddle River, New Jersey
Braude S, Tang-Martinez Z, Taylor GT (1999) Stress, testosterone, and the immunoredistribution hypothesis. Behav Ecol 10:345–350
Brown CR, Bomberger Brown M (2002) Spleen volume varies with colony size and parasite load in a colonial bird. Proc R Soc Lond B 269:1367–1373
Canadian Council on Animal Care (1984) Guide to the care and use of experimental animals. Canadian Council on Animal Care, Ottawa, Ontario
Christein D, Taylor DH (1978) Population dynamics of the American toad Bufo americanus (Amphibia, Anura, Bufonidae). J Herpetol 12:17–24
Cooper EL, Wright RK, Klempau RE, Smith CT (1992) Hibernation alters the frog’s immune system. Cryobiology 29:613–616
Dhabhar FS (1998) Stress-induced enhancement of cell-mediated immunity. Ann NY Acad Sci 840:359–372
Dhabhar FS, McEwen B (1996) Stress-induced enhancement of antigen-specific cell-mediated immunity. J Immunol 156:2608–2615
Edwards DB, Mallory ML, Forbes MR (2006) Variation in baseline haematology of northern fulmars (Fulmarus glacialis) in the Canadian High Arctic. Comp Clin Pathol 14:206–209
Evans MR, Goldsmith AR, Norris SRA (2000) The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus). Behav Ecol Sociobiol 47:156–163
Fairchild L (1984) Male reproductive tactics in an explosive breeding toad population. Am Zool 24:407–418
Folstad I, Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am Nat 139:603–622
Folstad I, Nilssen AC, Halvorsen O, Andersen J (1989) Why do male reindeer (Rangifer tarandus tarandus) have higher abundance of second and third instar larvae of Hypoderma tarandi than females? Oikos 55:87–92
Forester DC, Thompson KJ (1998) Gauntlet behaviour as a male sexual tactic in the American toad (Amphibia: Bufonidae). Behaviour 135:99–119
Gobbetti A, Zerani M (1996) Possible mechanism for the first response to short captivity stress in the water frog, Rana esculenta. J Endocrinol 148:223–239
Grossman CJ (1985) Interactions between the gonadal steroids and the immune system. Science 227:257–261
Hopster H, van der Werf JTN, Blokhuis HJ (1998) Stress enhanced reduction in peripheral blood lymphocyte numbers in dairy cows during endotoxin-induced mastitis. Vet Immunol Immunopathol 66:83–97
Horton J, Ratcliffe N (1998) Evolution and immunity. In: Roitt I, Brostoff J, Male D (eds) Immunology, 4th edn. Mosby, Toronto, pp. 199–220
Howard RD (1988) Sexual selection on male body size and mating behaviour in American toads, Bufo americanus. Anim Behav 36:1796–1808
Howard RD, Palmer JG (1995) Female choice in Bufo americanus: effects of dominant frequency and call order. Copeia 1:212–217
Kruse KC, Mounce M (1982) The effects of multiple matings on fertilization capability in male American toads (Bufo americanus). J Herpetol 16:410–412
Licht LE (1976) Sexual selection in toads (Bufo americanus). Can J Zool 54:1277–1293
Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98
Maniero GD, Carey C (1997) Changes in selected aspects of immune function in the leopard frog, Rana pipiens, associated with exposure to cold. J Comp Physiol B 167:256–263
Maule AG, Tripp RA, Kaattari SL, Schreck CB (1988) Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha). J Endocrinol 120:135–142
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
McRuer DL (2001) An investigation of prevalence of Aeromonas hydrophila and of measures of immune function for frogs used in the Ontario baitshop industry: implications of past and present practices. M.S. thesis, Carleton University, Ottawa, Ontario
Møller AP, Sorci G, Erritzoe J (1998) Sexual dimorphism in immune defense. Am Nat 152:605–619
Moore SL, Wilson K (2002) Parasites as a viability cost of sexual selection in natural populations of mammals. Science 297:2015–2018
Nordling D, Andersson M, Zohari S, Gustafsson L (1998) Reproductive effort reduces specific immune response and parasite resistance. Proc R Soc Lond B 265:1291–1298
Oppliger A, Clobert J, Lecomte J, Lorenzon P, Boudjemadi K, John-Alder HB (1998) Environmental stress increases the prevalence and intensity of blood parasite infection in the common lizard Lacerta vivipara. Ecol Lett 1:129–138
Pap PL, Márkus R (2003) Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling barn swallows Hirundo rustica. J Avian Biol 34:434–438
Poulin R (1996) Sexual inequalities in helminth infections: a cost of being a male? Am Nat 147:287–295
Roulin A, Riols C, Dijkstra C, Ducrest AL (2001) Female plumage spottiness signals parasite resistance in the barn owl (Tyto alba). Behav Ecol 12:103–110
SAS Institute Inc (2000) JMP user’s guide: statistics. SAS Institute Inc., Cary, North Carolina
Schalk G, Forbes MR (1997) Male biases in parasitism of mammals: effects of study type, host age, and parasite taxon. Oikos 78:67–74
Shutler D, Alisauskas RT, McLaughlin JD (1999) Mass dynamics of the spleen and other organs in geese: measures of immune relationships to helminths? Can J Zool 77:351–359
Shutler D, Mullie A, Clark RG (2004) Tree swallow reproductive investment, stress, and parasites. Can J Zool 82:442–448
Sullivan BK (1992) Sexual selection and calling behavior in the American toad (Bufo americanus). Copeia 1:1–7
Zar JH (1996) Biostatistical analysis, 3rd edn. Prentice Hall, Upper Saddle River, NJ
Zuk M, Johnsen TS (1998) Seasonal changes in the relationship between ornamentation and immune response in red jungle fowl. Proc R Soc Lond B 265:1631–1635
Acknowledgements
The authors are indebted to the Natural Sciences and Engineering Research Council of Canada for financial support in the way of research grants to MRF and DS, and a PGS A scholarship to DLM. We are grateful for the support of the staff of the Queen’s Biological Station. Thanks also to Darryl Edwards for references on American toad biology.
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Forbes, M.R., McRuer, D.L. & Shutler, D. White blood cell profiles of breeding American toads (Bufo americanus) relative to sex and body size. Comp Clin Pathol 15, 155–159 (2006). https://doi.org/10.1007/s00580-006-0623-5
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DOI: https://doi.org/10.1007/s00580-006-0623-5