Behavioral Ecology and Sociobiology

, Volume 66, Issue 12, pp 1607–1617 | Cite as

Seasonal variation in ejaculate traits of male red-winged blackbirds (Agelaius phoeniceus)

  • Stefan LüpoldEmail author
  • Tim R. Birkhead
  • David F. Westneat
Original Paper


Many reproductive traits, including ejaculate characteristics, usually show remarkable seasonal variation, but the potential for such dynamics in sperm morphology has been overlooked. Several studies have revealed high within-male repeatability in sperm morphology, but samples have typically been collected within a few hours or days, and the consistency of sperm morphology over longer periods remains unexplored. Here, we tested whether ejaculate traits, including sperm morphology, sperm number, and sperm velocity, exhibit seasonal phenotypic plasticity in a long-lived seasonal breeder, the red-winged blackbird (Agelaius phoeniceus). We found absolute and/or relative flagellum length and sperm velocity to increase across the season, whereas sperm numbers within ejaculates declined. Sperm morphological traits were further positively associated with harem size or the total number of offspring that fledged in each male’s territory, suggesting that sperm morphology is likely to be linked to male reproductive quality. The underlying mechanisms of these patterns of seasonal variation remain unresolved, but we discuss our results in the context of dynamics of reproductive hormones, testicular structures and function, and reproductive behavior.


Sperm morphology Sperm velocity Sperm number Seasonal variation Sperm competition Phenotypic plasticity 



We thank J. M. Fraterrigo, J. Homan, G. M. Linz, L. Reinhardt, and A. Trutsch for their help in the field and R. Montgomerie and two anonymous referees for valuable comments. SL was supported by the Janggen-Poehn Foundation, the Swiss National Science Foundation, a Sheffield University Overseas Research Student Award, a Lauff Research Award, and an NSF LTER Graduate Research Award; TRB, by a grant from the Leverhulme Trust; and DFW, by the U.S. National Science Foundation and the University of Kentucky.

Ethical standards

All fieldwork complies with the current laws of the USA, where the study was performed, and samples of all populations were collected under license of the respective authorities.

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2012_1415_MOESM1_ESM.pdf (107 kb)
ESM 1 (PDF 106 kb)


  1. Beletsky L (1996) The red-winged blackbird. The biology of a strongly polygynous songbird. Academic, LondonGoogle Scholar
  2. Beletsky LD, Orians GH, Wingfield JC (1989) Relationships of steroid hormones and polygyny to territorial status, breeding experience, and reproductive success in male red-winged blackbirds. Auk 106:107–117CrossRefGoogle Scholar
  3. Birkhead TR, Fletcher F (1995) Male phenotype and ejaculate quality in the zebra finch Taeniopygia guttata. Proc R Soc Lond B 262:329–334CrossRefGoogle Scholar
  4. Birkhead TR, Martínez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc R Soc Lond B 266:1759–1764CrossRefGoogle Scholar
  5. Birkhead TR, Pellatt EJ, Brekke P, Yeates R, Castillo-Juarez H (2005) Genetic effects on sperm design in the zebra finch. Nature 434:383–387PubMedCrossRefGoogle Scholar
  6. Boschetto C, Gasparini C, Pilastro A (2011) Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 65:813–821CrossRefGoogle Scholar
  7. Calhim S, Birkhead TR (2007) Testes size in birds: quality versus quantity—assumptions, errors, and estimates. Behav Ecol 18:271–275CrossRefGoogle Scholar
  8. Calhim S, Immler S, Birkhead TR (2007) Postcopulatory sexual selection is associated with reduced variation in sperm morphology. PLoS One 2:e413PubMedCrossRefGoogle Scholar
  9. Calhim S, Double MC, Magraf N, Birkhead TR, Cockburn A (2011) Maintenance of sperm variation in a highly promiscuous wild bird. PLoS One 6:e28809PubMedCrossRefGoogle Scholar
  10. Cardullo RA, Baltz JM (1991) Metabolic regulation in mammalian sperm: mitochondrial volume determines sperm length and flagellar beat frequency. Cell Motil Cytoskelet 19:180–188CrossRefGoogle Scholar
  11. Clulow J, Jones RC (1982) Production, transport, maturation, storage and survival of spermatozoa in the male Japanese quail, Coturnix coturnix. J Reprod Fertil 64:259–266PubMedCrossRefGoogle Scholar
  12. Cohen J (1977) Reproduction. Butterworths, LondonGoogle Scholar
  13. Cornwallis CK, O’Connor EA (2009) Sperm: seminal fluid interactions and the adjustment of sperm quality in relation to female attractiveness. Proc R Soc Lond B 276:3467–3475CrossRefGoogle Scholar
  14. Cramer ERA, Laskemoen T, Kleven O, Lifjeld JT (2012) Sperm length variation in house wrens Troglodytes aedon. J Ornithol. In press, doi: 10.1007/s10336-012-0878-3
  15. Crean AJ, Marshall DJ (2008) Gamete plasticity in a broadcast spawning marine invertebrate. P Natl Acad Sci USA 105:13508–13513CrossRefGoogle Scholar
  16. de Reviers M (1988) Appareil génital mâle et production des spermatozoïdes. In: Sauveur B (ed) Reproduction des Volailles et Production d'Oeufs. INRA, Paris, pp 141–181Google Scholar
  17. Denk AG, Holzmann A, Peters A, Vermeirssen ELM, Kempenaers B (2005) Paternity in mallards: effects of sperm quality and female sperm selection for inbreeding avoidance. Behav Ecol 16:825–833CrossRefGoogle Scholar
  18. Dobler R, Hosken DJ (2010) Response to selection and realized heritability of sperm length in the yellow dung fly (Scathophaga stercoraria). Heredity 104:61–66PubMedCrossRefGoogle Scholar
  19. Dolbeer WA (1978) Movement and migration patterns of red-winged blackbirds: a continental overview. Bird Band 49:17–34CrossRefGoogle Scholar
  20. Dziminski MA, Roberts JD, Beveridge M, Simmons LW (2009) Sperm competitiveness in frogs: slow and steady wins the race. Proc R Soc Lond B 276:3955–3961CrossRefGoogle Scholar
  21. Farner DS, Serventy DL (1960) The timing of reproduction in birds in the arid regions of Australia. Anat Rec 137:354Google Scholar
  22. Fitzpatrick JL, Montgomerie R, Desjardins JK, Stiver KA, Kolm N, Balshine S (2009) Female promiscuity promotes the evolution of faster sperm in cichlid fishes. P Natl Acad Sci USA 106:1128–1132CrossRefGoogle Scholar
  23. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, Parker GA (2004) Spermatozoal traits and sperm competition in Atlantic salmon: relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14:44–47PubMedGoogle Scholar
  24. Gasparini C, Simmons LW, Beveridge M, Evans JE (2010) Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS One 5:e12146PubMedCrossRefGoogle Scholar
  25. Gomendio M, Roldan ERS (2008) Implications of diversity in sperm size and function for sperm competition and fertility. Int J Dev Biol 52:439–447PubMedCrossRefGoogle Scholar
  26. Green K (2003) Age-related variation in mean sperm length, in the rove beetle Aleochara bilineata. J Insect Physiol 49:993–998PubMedCrossRefGoogle Scholar
  27. Harris WE, Moore AJ, Moore PJ (2007) Variation in sperm size within and between ejaculates in a cockroach. Funct Ecol 21:598–602CrossRefGoogle Scholar
  28. Helfenstein F, Szép T, Nagy Z, Kempenaers B, Wagner RH (2008) Between-male variation in sperm size, velocity and longevity in sand martins Riparia riparia. J Avian Biol 39:647–652CrossRefGoogle Scholar
  29. Helfenstein F, Podevin M, Richner H (2010) Sperm morphology, swimming velocity, and longevity in the house sparrow Passer domesticus. Behav Ecol Sociobiol 64:557–565CrossRefGoogle Scholar
  30. Higdon JJL (1979) A hydrodynamic analysis of flagellar propulsion. J Fluid Mech 90:685–711CrossRefGoogle Scholar
  31. Humphries S, Evans JP, Simmons LW (2008) Sperm competition: linking form to function. BMC Evol Biol 8:319PubMedCrossRefGoogle Scholar
  32. Immler S, Birkhead TR (2005) A non-invasive method for obtaining spermatozoa from birds. Ibis 147:827–830CrossRefGoogle Scholar
  33. Immler S, Calhim S, Birkhead TR (2008) Increased postcopulatory sexual selection reduces the intramale variation in sperm design. Evolution 62:1538–1543PubMedCrossRefGoogle Scholar
  34. Immler S, Pryke SR, Birkhead TR, Griffith SC (2010) Pronounced within-individual plasticity in sperm morphometry across social environments. Evolution 64:1634–1643PubMedCrossRefGoogle Scholar
  35. Immler S, Pitnick S, Parker GA, Durrant K, Lüpold S, Calhim S, Birkhead TR (2011) Resolving variation in the reproductive tradeoff between sperm size and number. P Natl Acad Sci USA 108:5325–5330CrossRefGoogle Scholar
  36. Immler S, Griffith SC, Zann R, Birkhead TR (2012) Intra-specific variance in sperm morphometry: a comparison between wild and domesticated zebra finches Taeniopygia guttata. Ibis 154:480–487CrossRefGoogle Scholar
  37. Jamieson BGM (2007) Avian spermatozoa: structure and phylogeny. In: Jamieson BGM (ed) Reproductive biology and phylogeny of birds, vol 6A, Science. Enfield, New Hampshire, pp 349–511Google Scholar
  38. Johnsen TS (1998) Behavioural correlates of testosterone and seasonal changes of steroids in red-winged blackbirds. Anim Behav 55:957–965PubMedCrossRefGoogle Scholar
  39. Kirby JD, Froman DP (2000) Reproduction in male birds. In: Whittow GC (ed) Avian Physiology. Academic, LondonGoogle Scholar
  40. Kleven O, Fossøy F, Laskemoen T, Robertson RJ, Rudolfsen G, Lifjeld JT (2009) Comparative evidence for the evolution of sperm swimming speed by sperm competition and female sperm storage duration in passerine birds. Evolution 63:2466–2473PubMedCrossRefGoogle Scholar
  41. LaMunyon CW, Ward S (2002) Evolution of larger sperm in response to experimentally increased sperm competition in Caenorhabditis elegans. Proc R Soc Lond B 269:1125–1128CrossRefGoogle Scholar
  42. Laskemoen T, Kleven O, Fossøy F, Robertson RJ, Rudolfsen G, Lifjeld JT (2010) Sperm quantity and quality effects on fertilization success in a highly promiscuous passerine, the tree swallow Tachycineta bicolor. Behav Ecol Sociobiol 64:1473–1483CrossRefGoogle Scholar
  43. Lüpold S, Calhim S, Immler S, Birkhead TR (2009a) Sperm morphology and sperm velocity in passerine birds. Proc R Soc Lond B 276:1175–1181CrossRefGoogle Scholar
  44. Lüpold S, Linz GM, Birkhead TR (2009b) Sperm design and variation in the New World blackbirds (Icteridae). Behav Ecol Sociobiol 63:899–909CrossRefGoogle Scholar
  45. Lüpold S, Linz GM, Rivers JW, Westneat DF, Birkhead TR (2009c) Sperm competition selects beyond relative testes size in birds. Evolution 63:391–402PubMedCrossRefGoogle Scholar
  46. Lüpold S, Westneat DF, Birkhead TR (2011a) Geographical variation in sperm morphology in the red-winged blackbird (Agelaius phoeniceus). Evol Ecol 25:373–390CrossRefGoogle Scholar
  47. Lüpold S, Wistuba J, Damm OS, Rivers JW, Birkhead TR (2011b) Sperm competition leads to functional adaptations in avian testes to maximize sperm quantity and quality. Reproduction 141:595–605PubMedCrossRefGoogle Scholar
  48. Lüpold S, Manier MK, Berben KS, Smith K, Daley B, Buckley SH, Belote JM, Pitnick S (2012) How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 22:1667–1672Google Scholar
  49. Malo AF, Garde JJ, Soler AJ, Garcia AJ, Gomendio M, Roldan ERS (2005) Male fertility in natural populations of red deer is determined by sperm velocity and the proportion of normal spermatozoa. Biol Reprod 72:822–829PubMedCrossRefGoogle Scholar
  50. Martin PA, Reimers TJ, Lodge JR, Dziuk PJ (1974) Effect of ratios and numbers of spermatozoa mixed from two males on proportions of offspring. J Reprod Fertil 39:251–258PubMedCrossRefGoogle Scholar
  51. Matsuoka T, Imai H, Asakuma S, Kohno H, Fukui Y (2006) Changes of fructose concentrations in seminal plasma and glucose and testosterone concentrations in blood plasma in rams over the course of a year. J Reprod Dev 52:805–810PubMedCrossRefGoogle Scholar
  52. McDowell KJ, Little TV, Timoney PJ, Adams MH (1996) Characterisation of proteins in the seminal plasma of stallions, geldings and geldings supplemented with testosterone. Res Vet Sci 61:33–37PubMedCrossRefGoogle Scholar
  53. McLachlan RI, Wreford NG, Robertson DM, de Kretser DM (1995) Hormonal control of spermatogenesis. Trends Endocrinol Metab 6:95–101PubMedCrossRefGoogle Scholar
  54. McLachlan RI, Wreford NG, Odonnell L, de Kretser DM, Robertson DM (1996) The endocrine regulation of spermatogenesis: independent roles for testosterone and FSH. J Endocrinol 148:1–9PubMedCrossRefGoogle Scholar
  55. Miller GT, Pitnick S (2002) Sperm-female coevolution in Drosophila. Science 298:1230–1233PubMedCrossRefGoogle Scholar
  56. Morrow EH, Gage MJG (2001a) Artificial selection and heritability of sperm length in Gryllus bimaculatus. Heredity 87:356–362PubMedCrossRefGoogle Scholar
  57. Morrow EH, Gage MJG (2001b) Consistent significant variation between individual males in spermatozoal morphometry. J Zool 254:147–153CrossRefGoogle Scholar
  58. Mossman J, Slate J, Humphries S, Birkhead TR (2009) Sperm morphology and velocity are genetically co-determined in the zebra finch. Evolution 63:2730–2737PubMedCrossRefGoogle Scholar
  59. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956PubMedGoogle Scholar
  60. Nussey DH, Wilson AJ, Brommer JE (2007) The evolutionary ecology of individual phenotypic plasticity in wild populations. J Evol Biol 20:831–844PubMedCrossRefGoogle Scholar
  61. Oppliger A, Hosken DJ, Ribi G (1998) Snail sperm production characteristics vary with sperm competition risk. Proc R Soc Lond B 265:1527–1534CrossRefGoogle Scholar
  62. Partecke J, Van't Hof T, Gwinner E (2004) Differences in the timing of reproduction between urban and forest European blackbirds (Turdus merula): result of phenotypic flexibility or genetic differences? Proc R Soc Lond B 271:1995–2001CrossRefGoogle Scholar
  63. Pellatt EJ, Birkhead TR (1994) Ejaculate size in zebra finches Taeniopygia guttata and a method for obtaining ejaculates from passerine birds. Ibis 136:97–106CrossRefGoogle Scholar
  64. Pitnick S (1996) Investment in testes and the cost of making long sperm in Drosophila. Am Nat 148:57–80CrossRefGoogle Scholar
  65. Pitnick S, Hosken DJ, Birkhead TR (2009) Sperm morphological diversity. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: An evolutionary perspective. Elsevier, London, pp 69–149Google Scholar
  66. Pizzari T, Parker GA (2009) Sperm competition and sperm phenotype. In: Birkhead TR, Hosken DJ, Pitnick S (eds) Sperm biology: An evolutionary perspective. Elsevier, London, pp 207–245Google Scholar
  67. Ramm SA, Stockley P (2010) Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biol Lett 6:219–221PubMedCrossRefGoogle Scholar
  68. Robertson RJ (1973) Optimal niche space of the red-winged blackbird: spatial and temporal patterns of nesting activity and success. Ecology 54:1085–1093CrossRefGoogle Scholar
  69. Schlichting CD, Pigliucci M (1998) Phenotypic evolution: A reaction norm perspective. Sinauer, SunderlandGoogle Scholar
  70. Searcy WA, Yasukawa K (1995) Polygyny and sexual selection in red-winged blackbirds. Princeton University Press, PrincetonGoogle Scholar
  71. Selander RK, Hauser RJ (1965) Gonadal and behavioral cycles in the great-tailed grackle. Condor 67:157–182CrossRefGoogle Scholar
  72. Simmons LW, Kotiaho JS (2002) Evolution of ejaculates: patterns of phenotypic and genotypic variation and condition dependence in sperm competition traits. Evolution 56:1622–1631PubMedGoogle Scholar
  73. Simmons LW, Wernham J, García-González F, Kamien D (2003) Variation in paternity in the field cricket Teleogryllus oceanicus: no detectable influence of sperm numbers or sperm length. Behav Ecol 14:539–545CrossRefGoogle Scholar
  74. Sossinka R (1982) Domestication in birds. In: Farner DS, King AS, Parkes KC (eds) Avian Biology. Academic, London, pp 373–403Google Scholar
  75. Stearns SC (1989) The evolutionary significance of phenotypic plasticity. Bioscience 39:436–445CrossRefGoogle Scholar
  76. van de Pol M, Wright J (2009) A simple method for distinguishing within- versus between-subject effects using mixed models. Anim Behav 77:753–758CrossRefGoogle Scholar
  77. Ward PI (2000) Sperm length is heritable and sex-linked in the yellow dung fly (Scathophaga stercoraria). J Zool 251:349–353CrossRefGoogle Scholar
  78. Westneat DF (1992) Nesting synchrony by female red-winged blackbirds: effects on predation and breeding success. Ecology 73:2284–2294CrossRefGoogle Scholar
  79. Westneat DF (1993a) Polygyny and extrapair fertilizations in eastern red-winged blackbirds (Agelaius phoeniceus). Behav Ecol 4:49–60CrossRefGoogle Scholar
  80. Westneat DF (1993b) Temporal patterns of within-pair copulations, male mate guarding, and extra-pair events in eastern red-winged blackbirds (Agelaius phoeniceus). Behaviour 124:267–290CrossRefGoogle Scholar
  81. Westneat DF (1994) To guard mates or go forage: conflicting demands affect the paternity of male red-winged blackbirds. Am Nat 144:343–354CrossRefGoogle Scholar
  82. Westneat DF, Gray EM (1998) Breeding synchrony and extrapair fertilizations in two populations of red-winged blackbirds. Behav Ecol 9:456–464CrossRefGoogle Scholar
  83. Westneat DF, McGraw LA, Fraterrigo JM, Birkhead TR, Fletcher F (1998) Patterns of courtship behavior and ejaculate characteristics in male red-winged blackbirds. Behav Ecol Sociobiol 43:161–171CrossRefGoogle Scholar
  84. Wingfield JC, Moore MC (1987) Hormonal, social and environmental factors in the reproductive biology of free-living male birds. In: Drews D (ed) Psychobiology of reproductive behavior: An evolutionary perspective. Prentice-Hall, Princeton, pp 148–175Google Scholar
  85. Wolfson A (1954) Sperm storage at lower-than-body temperature outside the body cavity in some passerine birds. Science 120:68–71PubMedCrossRefGoogle Scholar
  86. Woltereck R (1909) Weitere experimentelle Untersuchungen über Artveränderung, speziell über das Wesen quantitativer Artunterschiede bei Daphniden. Verh Deutsch Zool Gesellsch 19:110–173Google Scholar
  87. Woolley DM (1971) Selection for the length of the spermatozoan midpiece in the mouse. Genet Res 16:261–275CrossRefGoogle Scholar
  88. Wright PL, Wright MH (1944) Reproductive cycle of the male red-winged blackbird. Condor 46:46–59CrossRefGoogle Scholar
  89. Zann RA (1996) The zebra finch: A synthesis of field and laboratory studies. Oxford University Press, New YorkGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Stefan Lüpold
    • 1
    • 2
    • 3
    Email author
  • Tim R. Birkhead
    • 2
  • David F. Westneat
    • 4
  1. 1.Department of Biology, Life Sciences Complex, 107 College PlaceSyracuse UniversitySyracuseUSA
  2. 2.Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  3. 3.Kellogg Biological StationMichigan State UniversityHickory CornersUSA
  4. 4.Department of Biology, 101 Morgan BuildingUniversity of KentuckyLexingtonUSA

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