Volume 31 Issue 4
Jul.  2010
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HUI Xin, MA Zhi-Jun. Six Hypotheses of Protandry in Migratory Birds and Study Hotspots in the Future. Zoological Research, 2010, 31(4): 446-452. doi: 10.3724/SP.J.1141.2010.04446
Citation: HUI Xin, MA Zhi-Jun. Six Hypotheses of Protandry in Migratory Birds and Study Hotspots in the Future. Zoological Research, 2010, 31(4): 446-452. doi: 10.3724/SP.J.1141.2010.04446

Six Hypotheses of Protandry in Migratory Birds and Study Hotspots in the Future

doi: 10.3724/SP.J.1141.2010.04446
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  • Author Bio:

    HUI Xin

  • Corresponding author: MA Zhi-Jun
  • Received Date: 2010-03-08
  • Rev Recd Date: 2010-06-25
  • Publish Date: 2010-08-22
  • Protandry refers the earlier arrival at breeding sites or reproductive stages of males than females. Focusing on the general phenomenon of males arriving at breeding sites earlier than females in migratory birds, we introduced six hypotheses for explaining the protandrous arrival, including rank advantage, susceptibility, constraint, mate opportunity, waiting cost, and mate choice hypothesis. We also discussed the applicability of these hypotheses to explain the protandry in migratory birds. In addition, we put forward the issues which might be important in the future research, including 1) occurrences of protandry in species of sexually homomorphism, 2) effects of global warming on protandry, and 3) effects of intrasexual competition on protandry.
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  • [1]
    Arvidsson BL, Neergaard R. 1991. Mate choice in the willow warbler: A field experiment [J]. Behav Ecol Sociobiol, 29: 225-229.Bantock TM, Prys-Jones RP, Lee PL. 2008. New and improved molecular sexing methods for museum bird specimens [J]. Mol Ecol Resour, 8: 519-528.Brooke M de L. 1979. Differences in the quality of territories held by wheatears (Oenanthe oenanthe) [J]. J Anim Ecol, 48: 21-32.Catry P, Campos A, Almada V, Cresswell W. 2004. Winter segregation of migrant European robins Erithacus rubecula in relation to sex, age, and size [J]. J Avian Biol, 35: 204-209.Chandler CR, Mulvihill RS. 1990. Interpreting differential timing of capture of sex classes during spring migration [J]. J Field Ornithol, 61: 85-89.Cooke F, MacInnes CD, Prevett JP. 1975. Gene flow between breeding population of lesser snow geese [J]. Auk, 92: 493-510.Cooper NW, Murphy MT, Redmond LJ. 2009. Age- and sex-dependent spring arrival dates of Eastern Kingbirds [J]. J Field Ornithol, 80: 35-41.Coppack T, TØttrup AP, Spottiswoode C. 2006. Degree of protandry reflects level of extra-pair paternity in migratory songbirds [J]. J Ornithol, 147: 260-265.Cristol DA, Baker MB, Carbone C. 1999. Differential migration revisited: Latitudinal segregation by age and sex class [J]. Curr Ornithol, 15: 33-88.Currie D, Thompson DBA, Burke T. 2000. Patterns of territory settlement and consequences for breeding success in the Wheatear Oenanthe oenanthe [J]. Ibis, 142: 389-398.Dierschke V, Mendel B, Schmaljohann H. 2005. Differential spring migration in northern wheatears Oenanthe oenanthe: hurried males or weak females [J] Behav Ecol Sociobiol, 57: 470-480.Dunn PO, Cockburn A. 1999. Extrapair mate choice and honest signaling in cooperatively breeding superb fairy-wrens [J]. Evolution, 53: 938-946.Edwards DB, Forbes MR. 2007. Absence of protandry in the spring migration of a population of Song Sparrows Melospiza melodia [J]. Ibis, 149: 715-720.Ellegren H, Sheldon BC. 1997. New tools for sex identification and the study of sex allocation in birds [J]. Trends Ecol Evol, 12: 255-259.Fagerström T, Wiklund C. 1982. Why do males emerge before females? Protandry as a mating strategy in male and female butterflies [J]. Oecologia, 52: 164-166.Forstmeier W. 2002. Benefits of early arrival at breeding grounds vary between male [J]. J Anim Ecol, 71: 1-9.Francis CM, Cooke F. 1986. Differential timing of spring migration in wood warblers (Parulinae) [J]. Auk, 103: 548-556.Francis CM, Cooke F. 1990. Differential timing of spring migration in rose-breasted grosbeaks [J]. J Field Ornithol, 61: 404-412.Gauthreaux SA Jr. 1978. The ecological significance of behavioral dominance [M]// Bateson PPG, Klopfer PH. Perspectives in Ethology. New York: Plenum Press, 17-54.Grewal PS, Selvan S, Lewis EE, Gaugler R. 1993. Male insect-parasitic nematodes: A colonizing sex [J]. Experientia, 49: 605 -608.Griffiths R, Double MC, Orr K, Dawson RJG. 1998. A DNA test to sex most birds [J]. Mol Ecol, 7: 1071-1075.Gil D, Slater PJB. 2000. Multiple song characteristics in the willow warbler (Phylloscopus trochilus): Correlations with female choice and offspring viability [J]. Behav Ecol Sociobiol, 47: 319-326.Hasselquist D. 1998. Polygyny in great reed warblers: a long-term study of factors contributing to male fitness [J]. Ecology, 79: 2376-2390.Holmes RT. 1966. Breeding ecology and annual cycle adaptations of the red-necked phalaropes [J]. Ibis, 113: 335-348.Holzapfel CM, Bradshaw WE. 2002. Protandry: The relationship between emergence time male fitness in the pitcher-plant mosquito [J]. Ecology, 83: 607-611.Huyvaert KP, Anderson DJ, Parker PG. 2006. Mate opportunity hypothesis and extrapair paternity in waved albatrosses (Phoebastria irrorata) [J]. Auk, 123: 524-536.Iason GR. 1989. Growth and mortality in mountain hares: The effect of sex and date of birth [J]. Oecologia, 81: 540-546.Jehl JR. 1973. Breeding biology and systematic relationships of the stilt sandpiper [J]. Wilson Bull, 85: 115-147.Ketterson ED, Nolan V Jr. 1976. Geographic variation and its climatic correlates in the sex ration of eastern-wintering Dark-eyed Juncos (Junco hyemalis hyemalis) [J]. Ecology, 57: 679-693.Ketterson ED, Nolan VJr. 1983. The evolution of differential bird migration [J]. Curr Ornithol, 1: 357-402.Kissner KJ, Weatherhead PJ, Francis CM. 2003. Sexual size dimorphism and timing of spring migration in birds [J]. J Evol Biol, 16: 154-162.Kokko H. 1999. Competition for early arrival in migratory bird [J]. J Anim Ecol, 68: 940-950.Kokko H, Gunnarsson TG, Morrell LJ, Gill JA. 2006. Why do female migratory birds arrive later than males [J]. J Anim Ecol, 75: 1293-1303.Kokko H, Rintamäki PT, Alatalo RV, Höglund J, Karvonen E, Lundberg A. 1999. Female choice selects for lifetime lekking performance in black grouse males [J]. Proc R Soc London B, 226: 2109-2115.Komar O, O’Shea BJ, Peterson T, Navarro-Siguenza AG. 2005. Evidence of latitudinal sexual segregation among migratory birds wintering in Mexico [J]. Auk, 122: 938-948.Lampe HM, Epsmark YO. 1994. Song structure reflects male quality of pied flycatchers, Ficedula hypoleuca [J]. Anim Behav, 47: 869-876.Lehikoinen E, Sparks TH, Zalakevicius M. 2004. Arrival and departure dates [M] //Møller AP, Fiedler W, Berthold P . Effects of Climatic Change on Birds. London: Academic Press.Marra PP, Hobson KA, Holmes RT. 1998. Linking winter and summer events in a migratory bird by using stable-carbon isotopes [J]. Science, 282: 1884-1886.Michener GR. 1983. Spring emergence schedules and vernal behavior of Richardson’s ground squirrels: Why do males emerge from hibernation before females [J]. Behav Ecol Sociobiol, 14: 29-38.Michener GR. 1984. Age, sex, and species differences in the annual cycles of ground-dwelling sciurids: Implications for sociality [M]//Murie JO, Michener GR, Lincoln NE. The Biology of Ground-Dwelling Squirrels: Annual Cycles, Behav Ecol, and Sociality. Lincoln: University of Nebraska Press, 79-107.Møller AP. 1994. Sexual Selection and the Barn Swallow [M]. Oxford: Oxford University Press.Møller AP. 2004. Protandry, sexual selection and climate change [J]. Glob Chang Biol, 10: 2028-2035.Møller AP, Balbontin J, Cuervo JJ, Hermosell IG, del Lope F. 2009. Individual differences in protandry, sexual selection, and fitness [J]. Behav Ecol, 20: 433-440.Moore FR, Kerlinger P, Simons TR. 1990. Stopover on a gulf coast barrier island by spring trans-gulf migrants [J]. Wilson Bull, 102: 487-500.Morbey YE. 2000. Protandry in Pacific salmon [J]. Can J Fish Aquat Sci, 57: 1252-1257.Morbey YE, Ydenberg RC. 2001. Protandrous arrival timing to breeding areas: a review [J]. Ecol Lett, 4: 663-673.Muralimohan K, Srinivasa YB. 2008. Occurrence of protandry in an aseasonal multivoltine moth: Implications for body-size evolution [J]. Curr Sci, 94: 513-518.Myers JP. 1981. A test of three hypotheses for latitudinal segregation of the sexes in wintering birds [J]. Can J Zool, 19: 1527-1534.Ninni P, de Lope F, Saino N, Haussy C, Møller AP. 2004. Antioxidants and condition-dependence of arrival date in a migratory passerine [J]. Oikos, 105: 55-64.Olsson M, Madsen T. 1996. Costs of mating with infertile males selects for late emergence in female sand lizard (Lacerta agilis) [J]. Copeia, 1996: 462-464.Orians GH. 1980. Some Adaptations of Marsh-nesting Blackbirds [M]. Princeton: Princeton University Press.Oring LW, Lank DB. 1982. Sexual selection, arrival times, philopatry and site fidelity in the polyandrous spotted sandpiper [J]. Behav Ecol Sociobiol, 10: 185-191.Otahal CD. 1995. Sexual differences in Wilson’s warbler migration [J]. J Field Ornithol, 113: 173-184.Parmesan C. 2006. Ecological and evolutionary responses to recent climate change [J]. Annu Rev Ecol Syst, 37: 637-669.Potti J. 1998. Arrival time from spring migration in male pied flycatcher: individual consistency and familial resemblance [J]. Condor, 100: 702-708.Quinn TP, Unwin MJ. 1993. Variation in life history patterns among New Zealand chinook salmon (Oncorhynchus nerka) under varying operational sex ratios [J]. Can J Fish Aquat Sci, 50: 1414-1421.Rainio K, TØttrup AP, Lehikoinen E, Coppack T. 2007. Effects of climate change on the degree of protandry in migratory songbirds [J]. Clim Res, 35: 107-114.Reynolds JD, Colwell MA, Cooke F. 1986. Sexual selection and spring arrival times of red-necked and Wilson’s phalaropes [J]. Behav Ecol Sociobiol, 18: 303-310.Rubolini D, Spina F, Saion N. 2004. Protandry and sexual dimorphism in trans-Saharan migratory birds [J]. Behav Ecol, 15: 592-601.Rubolini D, Møller AP, Rainio K, Lehikoinen E. 2007. Intra-specific consistency and geographic variability in temporal trends of spring migration phenology among European bird species [J]. Clim Res, 35: 135-146.Semlitsch RD. 1985. Analysis of climatic factors influencing migrations of the salamander Ambystoma talpoideum [J]. Copia, 1985: 477-489.Semlitsch RD, Scott DE, Pechmann JHK, Gibbons JW. 1993. Phenotypic variation in the arrival time of breeding salamanders: individual repeatability and environmental influences [J]. J Anim Ecol, 62: 334-340.Slagsvold T, Lifjeld JT. 1988. Plumage color and sexual selection in the pied flycatcher Ficedula hypoleuca [J]. Anim Behav, 36: 395-407.Spottiswoode CN, TØttrup AP, Coppack T. 2006. Sexual selection predicts advancement of avian spring migration in response to climate change [J]. Proc R Soc Biol, 273: 3023-3029.Swanson DL, Liknes ET, Dean KL. 1999. Differences in migratory timing and energetic condition among sex/age classes in migrant ruby-crowned kinglets [J]. Wilson Bull, 111: 61-69.Székely T, Reynolds JD, Figuerola J. Sexual size dimorphism in shorebirds, gulls, and alcids: the influence of sexual and natural selection [J]. Evolution, 54: 1404-1413.Terril SB, Berthold P. 1989. Experimental evidence for endogenously programmed differential migration in the blackcap (Sylvia atricapilla) [J]. Cell Mol Life Sci, 45: 207-209.Tøttrup AP, Thorup K. 2008. Sex-differentiated migration patterns, protandry and phenology in North European songbird populations [J]. J Ornithol, 149: 161-167.Thornhill R, Alcock J. 1983. The Evolution of Insect Mating Systems [M]. Cambridge: Harvard University Press.Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F. 2002. Ecological responses to recent climate change [J]. Nature, 416: 389-395.Wang GY, Greenfield MD, Shelly TE. 1990. Inter-male competition for high-quality host-plants: the evolution of protandry in a territorial grasshopper [J]. Behav Ecol Sociobiol, 27: 191-198.Wang N, Zhang ZW. 2009. The novel primers for sex identification in the brown eared-pheasant and their application to other species [J]. Mol Ecol Resour, 9: 186-188.Weatherhead PJ, Hoysak DJ. 1989. Spatial and activity patterns of black rat snakes (Elaphe obsolete) from radiotelemetry and recapture data [J]. Can J Zool, 67: 463-468.Wedell N. 1992. Protandry and mate assessment in the wartbiter Dectitus verrucivorus (Ort: Tettigonidae) [J]. Behav Ecol Sociobiol, 31: 301-308.Wiklund C, Fagerström T. 1977. Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies [J]. Oecologia, 31: 153-158.Zhang FY, Yang RL. 1997. Bird Migration Research of China [M]. Beijing, China Forestry Publishing House. [张孚允, 杨若莉. 1997. 中国鸟类迁徙研究. 北京: 中国林业出版社.]

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