Abstract
The Goymann–Wingfield model predicts that glucocorticoid levels in social animals reflect the costs of acquiring and maintaining social status. The crested auklet is one of the few avian colonial species where a mutual ornament in males and females is used in both sexual and aggressive displays. Previous studies of the crested auklet support the notion that the crest ornament is a badge of status in this species. Here, we examined the relationship between the crest ornament size and the adrenocortical function in breeding crested auklets. Crest length was negatively correlated with corticosterone at baseline in males, but not in females. Baseline corticosterone in females (but not in males) was negatively correlated with body condition index. Although male and female crested auklets are monomorphic in their ornamental traits, our results suggest that the socially mediated physiological costs associated with status signaling may differ between the sexes.
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Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T Jr, Sapolsky RM (2003) Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Horm Behav 43:67–82
Andersson M (1994) Sexual selection. Princeton University Press, Princeton
Bailey EP (1990) Fox introductions on Aleutian Islands: history, impacts on avifauna, and eradication. US Fish and Wildlife Service, Homer
Balph MH, Balph DF, Romesburg HC (1979) Social status signaling in winter flocking bird: an examination of current hypothesis. Auk 96:78–93
Bédard J, Sealy SG (1984) Moults and feather generations in the Least, Crested and Parakeet auklets. J Zool (Lond) 202:461–488
Benowitz-Fredericks ZM, Shultz M, Kitaysky A (2008) Stress hormones suggest opposite trends of food availability between planktivorous and piscivorous seabirds in two years. Deep Sea Res II 55:1868–1876
Berglund A (1996) Armaments and ornaments: an evolutionary explanation of traits of dual utility. Biol J Linn Soc 58:385–399
Coates JM, Herbert J (2008) Endogenous steroids and financial risk taking on a London trading floor. Proc Natl Acad Sci USA 104:6167–6172
Croll DA, Gaston AJ, Noble DG (1991) Adaptive loss of mass in Thick-billed Murres. Condor 93:496–502
Darwin C (1871) The descent of man and selection in relation to sex. London, Murray
Douglas HD III, Kitaysky AS, Kitaiskaia EV (2008) Seasonal covariation in progesterone and odorant emissions among breeding crested auklets (Aethia cristatella). Horm Behav 54:325–329
Ebbert SE, Byrd GV (2002) Eradications of invasive species to restore natural biological diversity on Alaska Maritime National Wildlife Refuge. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. Proceedings of the international conference on eradication of island invasives. Occ. paper on the IUCN Species Survival Commission No. 27, pp 102–109
Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139:603–622
Fraser GS, Jones IL, Hunter FM (2002) Male–female differences in parental care in monogamous crested auklets. Condor 104:413–423
Fraser GS, Jones IL, Hunter FM, Cowen L (2004) Mate switching patterns in crested auklets (Aethia cristatella): the role of breeding success and ornamentation. Bird Behav 16:7–12
Gaston AJ, Jones IL (1998) The Auks. Oxford University Press, Oxford
Goymann W, Wingfield JC (2004) Allostatic load, social status and stress hormones: the costs of social status matter. Anim Behav 67:591–602
Hillgarth N, Wingfield JC (1997) Parasite-mediated sexual selection: endocrine aspects. In: Clayton DH, Moore J (eds) Host–parasite evolution: general principles and avian models. Oxford University Press, Oxford, pp 78–104
Hunter FM, Jones IL (1999) The frequency and function of aquatic courtship and copulation in least, crested, whiskered, and parakeet auklets. Condor 101:518–528
Johnstone RA, Norris K (1993) Badges of status and the costs of aggression. Behav Ecol Sociobiol 32:127–134
Jones IL (1993a) Crested auklet. In: Poole A, Stettenheim P, Gill F (eds) The birds of North America, vol 70. The Academy of Natural Sciences, Philadelphia, pp 1–15
Jones IL (1993b) Sexual differences in bill shape and external measurements of Crested Auklets. Wilson Bull 105:525–529
Jones IL (1994) Mass changes of least auklets Aethia pusilla during the breeding season: evidence for the programmed anorexia hypothesis. J Anim Ecol 63:71–78
Jones IL, Hunter FM (1993) Mutual sexual selection in a monogamous seabird. Nature 362:238–239
Jones IL, Hunter FM (1999) Experimental evidence for mutual inter- and intrasexual selection favouring a crested auklet ornament. Anim Behav 57:521–528
Jones IL, Hunter FM, Fraser G (2000) Patterns of variation in ornaments of Crested Auklets Aethia cristatella. J Avian Biol 31:119–127
Jones IL, Hunter FM, Robertson GJ, Fraser G (2004) Natural variation in the sexually selected feather ornaments of crested auklets (Aethia cristatella) does not predict future survival. Behav Ecol 15:332–337
Kitaysky AS, Wingfield JC, Piatt JF (1999a) Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Funct Ecol 13:577–584
Kitaysky AS, Piatt JF, Wingfield JC, Romano M (1999b) The adrenocortical stress-response of Black-legged Kittiwake chicks in relation to dietary restrictions. J Comp Physiol B 169:303–310
Kitaysky AS, Kitaiskaia EV, Wingfield JC, Piatt JF (2001) Dietary restriction causes chronic elevation of corticosterone and enhances stress response in red-legged kittiwake chicks. J Comp Physiol B 171:701–709
Kitaysky AS, Piatt JF, Wingfield JC (2002) Are seabirds breeding in the southeastern Bering Sea food-limited? Report to the North Pacific Research Program, University of Alaska Fairbanks, Fairbanks, p 41
Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140–149
Kitaysky AS, Romano MD, Piatt JF, Wingfield JC, Kikuchi M (2005a) The adrenocortical response of tufted puffin chicks to nutritional deficits. Horm Behav 47:606–619
Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2005b) A mechanistic link between chick diet and decline in seabirds? Proc R Soc Lond B 273:445–450
Kitaysky AS, Piatt JF, Wingfield JC (2007) Corticosterone links food stress to population processes in seabirds. Mar Ecol Prog Ser 352:245–258
Lanctot RG, Hatch S, Gill VA, Eens M (2003) Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? Horm Behav 43:489–502
Lima SL (1986) Predation risk and unpredictable feeding conditions: determinants of body mass in wintering birds. Ecology 67:377–385
Love OP, Breuner CW, Vézina F, Williams TD (2004) Mediation of a corticosterone-induced reproductive conflict. Horm Behav 46:59–65
Maynard Smith J, Harper DGC (1988) The evolution of aggression: can selection generate variability? Philos Trans R Soc Lond B Biol Sci 319:557–570
McEwen BS (1998) Protective and damaging effects of stress. New Eng J Med 338:171–179
McEwen BS, Wingfield JC (2003) The concept of allostasis in biology and biomedicine. Horm Behav 43:2–15
McNamara JM, Houston AI (1990) The value of fat reserves and the tradeoff between starvation and predation. Acta Biotheor 38:37–61
Metcalfe NB, Ure SE (1995) Diurnal variation in flight performance and hence potential predation risk in small birds. Proc R Soc Lond B 261:395–400
Møller AP (1987) Social control of deception among status signaling house sparrows Passer domesticus. Behav Ecol Sociobiol 20:307–311
Parker TH, Ligon DJ (2004) Dominant male red junglefowl (Gallus gallus) test the dominance status of other males. Behav Ecol Sociobiol 53:20–24
Pravosudov VV, Kitaysky AS, Wingfield JS, Clayton NS (2004) No latitudinal differences in adrenocortical stress response in wintering black-capped chickadees (Poecile atricapilla). Comp Biochem Physiol Part A: Mol Integr Physiol 137:95–103
Quarnström A (1997) Experimentally increased badge size increases male competition and reduces male parental care in the collared flycatcher. Proc R Soc Lond, Ser B 264:1225–1231
Rohwer S (1982) The evolution of reliable and unreliable badges of fighting ability. Am Zool 22:531–546
Romero LM, Wikelski M (2001) Corticosterone levels predict survival probabilities of Galápagos marine iguanas during El Niño events. Proc Natl Acad Sci USA 98:7366–7370
Romero LM, Reed JM (2005) Collecting baseline corticosterone samples in the field: is under three minutes good enough? Comp Biochem Physiol Part A: Mol Integr Physiol 140:73–79
Ryan MT (1983) Sexual selection and communication in a neotropical frog, Physalaemus pusulosus. Evolution 37(2):261–272
Shultz MT, Kitaysky AS (2008) Spatial and temporal dynamics of corticosterone and corticosterone binding globulin are driven by environmental heterogeneity. Gen Comp Endocrinol 155:117–128
Silverin B (1986) Corticosterone-binding proteins and behavior effects of high plasma levels of corticosterone during the breeding period in the pied flycatcher. Gen Comp Endocrinol 64:67–74
Springer AM, Kondratyev AY, Ogi H, Shibaev YV, van Vliet GB (1993) Status, ecology, and conservation of Synthliboramphus murrelets and auklets. In: Vermeer K, Briggs KT, Morgan H, Siegel-Causey D (eds) Status and conservation of seabirds in the North Pacific. Canadian Wildlife Service, Ottawa, pp 187–201
Townsend CA (1913) The crested auklet. Bird-Lore 15:133–136
Vehrencamp SL (2000) Handicap, index, and conventional signal elements of bird song. In: Espmark Y, Amundsen T, Rosenqvist G (eds) Animal signals: signalling and signal design in animal communication. Tapir Academic Press, Trondheim, pp 277–300
Williams CT, Kitaysky AS, Kettle AB, Buck CL (2008) Corticosterone levels of tufted puffins vary with breeding stage, body condition index, and reproductive performance. Gen Comp Endocrinol 158:29–35
Wingfield JC (1994) Modulation of the adrenocortical response to stress in birds. In: Davey KG, Peter RE, Tobe SS (eds) Perspectives in comparative endocrinology. Natl Res Council Canada, Ottawa, pp 520–528
Wingfield JC, Farner DS (1975) The determination of five steroids in avian plasma by radioimmunoassay and competitive protein binding. Steroids 26:311–327
Wingfield JC, Silverin B (1986) Effects of corticosterone on territorial behavior of free-living male Song sparrows Melospiza melodia. Horm Behav 20:405–417
Wingfield JC, Vleck CM, Moore MC (1992) Seasonal changes of the adrenocortical response to stress in birds of Sonoran Desert. J Exp Zool 264:419–428
Wingfield JC, Deviche P, Sharbaugh S, Astheimer LB, Holbertson R, Suydam R, Hunt K (1994a) Seasonal changes of the adrenocortical responses to stress in redpolls, Acanthis flammea, in Alaska. J Exp Zool 270:372–380
Wingfield JC, Suydam R, Hunt K (1994b) Adrenocortical responses to stress in snow buntings and Lapland longspurs at Barrow, Alaska. Comp Biochem Physiol 108:299–306
Wingfield JC, Hunt K, Breuner C, Dunlap K, Fowler GS, Freed L, Lepson J (1997) Environmental stress, field endocrinology, and conservation biology. In: Clemmons JR, Buchols R (eds) Behavioral approaches to conservation in the wild. Cambridge University Press, Cambridge, pp 95–131
Acknowledgments
Funding came from the Eppley Foundation for Research, Inc.; the Angus Gavin Memorial Bird Research Fund, University of Alaska Foundation; Center for Global Change and Arctic System Research and Alaska Sea Grant College Program; and the University of Washington. A. M. Springer, J. Galvin and J. C. Wingfield helped support this research. The Alaska Maritime National Wildlife Refuge and the Aleut Corporation granted permission to conduct research at Big Koniuji I. M. Benowitz-Fredericks, E. Murphy, C. Williams, S. Wang and several anonymous reviewers provided helpful comments on the manuscript. This research complied with applicable laws of Alaska and the USA.
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Communicated by H.V. Carey.
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Douglas, H.D., Kitaysky, A.S., Kitaiskaia, E.V. et al. Size of ornament is negatively correlated with baseline corticosterone in males of a socially monogamous colonial seabird. J Comp Physiol B 179, 297–304 (2009). https://doi.org/10.1007/s00360-008-0312-6
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DOI: https://doi.org/10.1007/s00360-008-0312-6