Skip to main content
SpringerLink
Log in

Sex-specific traits in Common Tern Sterna hirundo chicks: associations with rearing environment, parental factors and survival

  • Original Article
  • Published:
Journal of Ornithology Aims and scope Submit manuscript

Abstract

Offspring phenotypic variation has important consequences for the future survival, reproductive success and individual fitness of nestlings, but the sex-specific reproductive value and fitness returns for parents of this variation have only rarely been explored. We analysed twelve phenotypic traits of nestling Common Terns (Sterna hirundo) in relation to their sex, age and hatching date, and explored whether sexual differences in these traits were associated with the rearing environment and survival. In addition, we studied sex-specific differences in offspring phenotype related to parental factors, since the existence of sexual dimorphism may reflect differential parental investment. Bill–head length and mediated immune response varied in relation to offspring sex, with males showing larger values than females. Immune response was also affected by environmental (year), rearing (competition over 14 days old) and parental (clutch size) factors. None of the morphological, serological and immunological variables were associated with chick mortality, but female nestlings that did not survive had suffered longer periods of within-brood competition. Although some parental traits influenced offspring phenotype, sexual differences among nestlings did not vary in relation to parental age, mass or arrival date, which may imply that there is no great difference in cost between raising sons and raising daughters, and thus no adjustment of parental effort in relation to nestling sex. However, the evidence that immune response was higher for sons in larger clutches that were raised with siblings indicates a difference in the developmental strategies for sons and daughters, which may be related to their reproductive value. These results therefore provide evidence of certain pathways for parental sex allocation that may differentially affect sons and daughters.

Zusammenfassung

Geschlechtsspezifische Merkmale von Flussseeschwalbenküken ( Sterna hirundo) : Zusammenhänge mit der Umwelt, elterlichen Faktoren und Überlebenschancen

Die phänotypische Variation von Nachkommen hat bedeutende Konsequenzen für ihr zukünftiges Überleben, den Reproduktionserfolg und die individuelle Fitness. Der durch diese Variation bedingte geschlechtsspezifische Reprodukionswert und der Fitnessgewinn für die Eltern wurden bislang wenig untersucht. Wir analysierten 12 phänotypische Merkmale von Küken der Flussseeschwalbe (Sterna hirundo) in Bezug zu ihrem Geschlecht, Alter und Schlüpfdatum, um zu ergründen, ob sexuelle Differenzen in diesen Merkmalen mit Umweltbedingungen und Überlebensraten während der Aufzucht in Verbindung standen. Außerdem untersuchten wir geschlechtsspezifische Differenzen im Phänotyp der Nachkommen bezüglich elterlicher Faktoren, da sexueller Dimorphismus unterschiedliches elterliches Investment widerspiegeln könnte. Kopf-Schnabellänge und Immunabwehr variierten geschlechtsspezifisch, wobei Söhne höhere Werte als Töchter aufwiesen. Die Immunabwehr wurde außerdem durch Umwelteinflüsse (Jahr), Aufzuchtbedingungen (Konkurrenz mit älteren Geschwistern) und elterliche Faktoren (Gelegegröße) beeinflusst. Keine der morphologischen, serologischen und immunologischen Variablen stand in Relation zur Sterblichkeit der Küken, doch stieg die Mortalität von Töchtern mit zunehmender unter Geschwisterkonkurrenz verbrachter Zeit an. Obwohl einige elterliche Merkmale den Phänotyp der Jungen beeinflussten, variierten die geschlechtsspezifischen Unterschiede nicht in Abhängigkeit von Alter, Körpergewicht oder Ankunftsdatum der Eltern. Dies widerlegt unterschiedliche Kosten der Aufzucht von Söhnen oder Töchtern und eine Anpassung des elterlichen Aufwands an das Geschlecht ihrer Jungen. Dass die Immunabwehr bei Söhnen aus größeren Gelegen bzw. unter Aufwachsen mit Geschwistern verstärkt war deutet aber Unterschiede in den Entwicklungsstrategien von Söhnen und Töchtern an, die in Bezug zu ihrem Reproduktionswert stehen dürften. Somit geben die Ergebnisse Hinweise auf bestimmte Bahnen elterlicher, geschlechtsspezifischer Allokation, die Söhne und Töchter in unterschiedlicher Weise beeinflussen dürfte.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Addison B, Kitaysky AS, Hipfner JM (2008) Sex allocation in a monomorphic seabird with a single-egg clutch: test of the environment, mate quality, and female condition hypotheses. Behav Ecol Sociobiol 63:135–141

    Article  Google Scholar 

  • Alonso-Alvarez C, Tella JL (2001) Effects of experimental food restriction and body-mass changes on the avian T-cell-mediated immune response. Can J Zool 79:101–105

    Article  Google Scholar 

  • Arnold JM, Hatch JJ, Nisbet ICT (2004) Seasonal declines in reproductive success of the common tern Sterna hirundo: timing or parental quality? J Avian Biol 35:33–45

    Article  Google Scholar 

  • Banbura J, Banbura M, Kalinsky A, Skwarska J, Slomczynski R, Wawrzyniac J, Zielinski P (2007) Habitat and year-to-year variation in haemoglobin concentration in nestling blue tits Cyanistes caeruleus. Comp Biochem Physiol A 148:572–577

    Article  CAS  Google Scholar 

  • Banbura J, Skwarska J, Kalinsky A, Wawrzyniac J, Slomczynski R, Banbura M, Zielinski P (2008) Effects of brood size manipulation on physiological condition of nestling Blue Tits Cyanistes caeruleus. Acta Ornithol 43:129–138

    Article  Google Scholar 

  • Becker PH, Wendeln H (1997) A new application for transponders in population ecology of the common tern. Condor 99:534–538

    Article  Google Scholar 

  • Becker PH, Wink M (2003) Influences of sex, sex composition of brood and hatching order on mass growth in common terns Sterna hirundo. Behav Ecol Sociobiol 54:136–146

    Article  Google Scholar 

  • Becker PH, Wendeln H, González-Solís J (2001) Population dynamics, recruitment, individual quality and reproductive strategies in common terns Sterna hirundo marked with transponders. Ardea 89:241–252

    Google Scholar 

  • Becker PH, Dittmann T, Ludwigs JD, Limmer B, Ludwig SC, Bauch C, Braasch A, Wendeln H (2008a) Timing of initial arrival at the breeding site predicts age at first reproduction in a long-lived migratory bird. Proc Natl Acad Sci USA 105:12349–12352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Becker PH, Ezard THG, Ludwigs JD, Sauer-Gürth H, Wink M (2008b) Population sex ratio shift from fledging to recruitment: consequences for demography in a philopatric seabird. Oikos 117:60–68

    Article  Google Scholar 

  • Benito MM, González-Solís J, Becker PH (2011) Carotenoid supplementation and sex-specific trade-offs between colouration and condition in common tern chicks. J Comp Physiol B 181:539–549

    CAS  PubMed  Google Scholar 

  • Benito MM, Schielzeth H, González-Solís J, Becker PH (2013) Sex ratio adjustments in common terns: influence of mate condition and maternal experience. J Avian Biol. doi:https://doi.org/10.1111/j.1600-048X.2012.00024.x

    Article  Google Scholar 

  • Birkhead TR, Fletcher F, Pellat EJ (1999) Nestling diet, secondary sexual traits and fitness in the zebra finch. Proc R Soc Lond B 266:385–390

    Article  Google Scholar 

  • Bonisoli-Alquati A, Boncoraglio G, Caprioli M, Saino N (2011) Birth order, individual sex and sex of competitors determine the outcome of conflict among siblings over parental care. Proc R Soc Lond B 278:1273–1279

    Google Scholar 

  • Braasch A, Palme R, Hoppen H-O, Becker PH (2011) Body condition, hormonal correlates and consequences for survival in common tern chicks. J Comp Physiol A 197:1009–1020

    Article  Google Scholar 

  • Burness G, McClelland GB, Wardrop SL, Hochachka PW (2000) Effect of brood size manipulation on offspring physiology: an experiment with passerine birds. J Exp Biol 203:3513–3520

    Article  CAS  PubMed  Google Scholar 

  • Charnov EL (1982) The theory of sex allocation. Princeton University Press, Princeton

    Google Scholar 

  • Clayton DH, Drown DM (2001) Critical evaluation of five methods for quantifying chewing lice (Insecta: Phthiraptera). J Parasitol 87:1291–1300

    Article  CAS  PubMed  Google Scholar 

  • Clayton DH, Walther BA (1997) Collection and quantification of arthropod parasites of birds. In: Clayton DH, Moore AJ (eds) Host–parasite evolution. General principles and avian models. Oxford University Press, Oxford, pp 428–429

  • Cordero PJ, Viñuela J, Aparicio JM, Veira JAR (2001) Seasonal variation in sex ratio and sexual dimorphism favouring daughters in first clutches of the spotless starling. J Evol Biol 14:829–834

    Article  Google Scholar 

  • Coulter MC (1986) Assortative mating and sexual dimorphism in the common tern. Wilson Bull 98:93–100

    Google Scholar 

  • de Ayala RM (2007) Mouth coloration of nestlings covaries with offspring quality and influences parental feeding behavior. Behav Ecol 18:526–534

    Article  Google Scholar 

  • Dubiec A, Cichon M, Deptuch K (2006) Sex-specific development of cell-mediated immunity under experimentally altered rearing conditions in blue tit nestlings. Proc R Soc Lond B 273:1759–1764

    Google Scholar 

  • Ellegren H, Gustafsson L, Sheldon BC (1996) Sex ratio adjustment in relation to paternal attractiveness in a wild bird population. Proc Natl Acad Sci USA 93:11723–11728

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ezard THG, Becker PH, Coulson T (2007) Correlations between age, phenotype, and individual contribution to population growth in common terns. Ecology 88:2496–2504

    Article  PubMed  Google Scholar 

  • Fargallo JA, Laaksonen T, Pöyri V, Korpimäki E (2002) Inter-sexual differences in the immune response of Eurasian kestrel nestlings under food shortage. Ecol Lett 5:95–101

  • Freeman S, Jackson WM (1990) Univariate metrics are not adequate to measure avian body size. Auk 107:69–74

    Google Scholar 

  • González-Solís J, Becker PH, Wendeln H, Wink M (2005) Hatching sex ratio and sex specific chick mortality in common terns Sterna hirundo. J Ornithol 146:235–243

    Article  Google Scholar 

  • Griggio M (2009) Nestlings’ carotenoid feather ornament affects parental allocation strategy and reduces maternal survival. J Evol Biol 22:2077–2085

    Article  CAS  PubMed  Google Scholar 

  • Hegyi G, Rosivall B, Szöllosi E, Eens M, Török J (2011) Context-dependent effects of nestling growth trajectories on recruitment probability in the collared flycatcher. Behav Ecol Sociobiol 65:1647–1658

    Article  Google Scholar 

  • Kim SY, Monaghan P (2006) Sex of the first hatched chick influences survival of the brood in the herring gull (Larus argentatus). J Zool 270:116–121

  • Klaassen M, Zwaan B, Heslenfeld P, Lucas P, Luijckx B (1992) Growth-rate associated changes in the energy-requirements of tern chicks. Ardea 80:19–28

    Google Scholar 

  • Laaksonen T, Fargallo JA, Korpimaki E, Lyytinen S, Valkama J, Poyri V (2004) Year- and sex-dependent effects of experimental brood sex ratio manipulation on fledging condition of Eurasian kestrels. J Anim Ecol 73:342–352

  • Lessells CM (1998) A theoretical framework for sex-biased parental care. Anim Behav 56:395–407

    Article  CAS  PubMed  Google Scholar 

  • Lessells CM (2002) Parentally biased favouritism: why should parents specialize in caring for different offspring? Phil Trans R Soc Lond B 357:381–403

    Article  CAS  Google Scholar 

  • Ligon JD, Hill GE (2010) Sex-biased parental investment is correlated with mate ornamentation in eastern bluebirds. Anim Behav 79:727–734

    Article  PubMed  PubMed Central  Google Scholar 

  • Limbourg T, Mateman AC, Andersson S, Lessells CM (2004) Female blue tits adjust parental effort to manipulated male UV attractiveness. Proc R Soc Lond B 271:1903–1908

    Article  Google Scholar 

  • Lobato E, Merino S, Morales J, Tomás G, Martínez-de la Puente J, Sánchez E, García-Fraile S, Moreno J (2008) Sex differences in circulating antibodies in nestling pied flycatchers Ficedula hypoleuca. Ibis 150:799–806

    Article  Google Scholar 

  • Lochmiller RL, Deerenberg C (2000) Trade-offs in evolutionary immunology: just what is the cost of immunity? Oikos 88:87–98

    Article  Google Scholar 

  • Mainwaring MC, Rowe LV, Kelly DJ, Grey J, Bearhop S, Hartley IR (2009) Hatching asynchrony and growth trade-offs within barn swallow broods. Condor 111:668–674

    Article  Google Scholar 

  • Mainwaring MC, Dickens M, Hartley IR (2011) Sexual dimorphism and growth trade-offs in blue tit Cyanistes caeruleus nestlings. Ibis 153:175–179

    Article  Google Scholar 

  • Mead PS, Morton ML, Fish BE (1987) Sexual dimorphism in egg size and implications regarding facultative manipulation of sex in Mountain White-crowned Sparrows. Condor 89:798–803

    Article  Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:254–260

    Article  PubMed  Google Scholar 

  • Moller AP, Sorci G, Erritzoe J (1998) Sexual dimorphism in immune defense. Am Nat 152:605–619

    Article  CAS  PubMed  Google Scholar 

  • Oddie K (2000) Size matters: competition between male and female great tit offspring. J Anim Ecol 69:903–912

    Article  PubMed  Google Scholar 

  • Råberg L, Stjernman M, Nilsson JÅ (2005) Sex and environmental sensitivity in blue tit nestlings. Oecol 145:496–503

    Article  Google Scholar 

  • Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225

    Article  PubMed  Google Scholar 

  • Ricklefs RE, White SC (1981) Growth and energetics of chicks of the sooty tern (Sterna fuscata) and common tern (S. hirundo). Auk 98:361–378

    Google Scholar 

  • Roberts ML, Buchanan KL, Evans MR (2004) Testing the immunocompetence handicap hypothesis: a review of the evidence. Anim Behav 68:227–239

    Article  Google Scholar 

  • Royle NJ, Hartley IR, Owens IPF, Parker GA (1999) Sibling competition and the evolution of growth rates in birds. Proc R Soc Lond B 266:923–932

    Article  Google Scholar 

  • Saino N, Ambrosini R, Martinelli R, Calza S, Moller AP, Pilastro A (2002) Offspring sexual dimorphism and sex-allocation in relation to parental age and paternal ornamentation in the barn swallow. Mol Ecol 11:1533–1544

    Article  CAS  PubMed  Google Scholar 

  • Simmons P, Lill A (2006) Development of parameters influencing blood oxygen carrying capacity in the welcome swallow and fairy martin. Comp Biochem Physiol A 143:459–468

    Article  CAS  Google Scholar 

  • Smits JE, Bortolotti GR, Tella JL (1999) Simplifying the phytohaemagglutinin skin-testing technique in studies of avian immunocompetence. Funct Ecol 13:567–572

    Article  Google Scholar 

  • Soler JJ, De Neve L, Pérez-Contreras T, Soler M, Sorci G (2003) Trade-off between immunocompetence and growth in magpies: an experimental study. Proc R Soc Lond B 270:241–248

    Article  Google Scholar 

  • Szostek KL, Becker PH (2012) Terns in trouble: demographic consequences of low breeding success and recruitment on a common tern population in the German Wadden Sea. J Ornithol 153:313–326

    Article  Google Scholar 

  • Teather KL (1989) The influence of sibling gender on the growth and survival of Great-tailed Grackle nestlings. Can J Zool 68:1925–1930

    Article  Google Scholar 

  • Teather KL (1992) An experimental study of competition for food between male and female nestlings of the red-winged blackbird. Behav Ecol Sociobiol 31:81–87

    Article  Google Scholar 

  • Tella JL, Negro JJ, Rodriguez-Estrella R, Blanco G, Forero MG, Blázquez MC, Hiraldo F (1998) A comparison of spectrophotometry and color charts for evaluating total plasma carotenoids in wild birds. Physiol Zool 71:708–711

    Article  CAS  PubMed  Google Scholar 

  • Wendeln H, Becker PH, Wagener M (1997) Beziehungen zwischen Körpermasse und Körpergröβe bei Paarpartnern der Fluβseeschwalbe (Sterna hirundo). Die Vogelwarte 39:141–148

    Google Scholar 

  • Zuk M, McKean KA (1996) Sex differences in parasite infections: patterns and processes. Int J Parasitol 26:1009–1023

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to all the indispensable people who formed the “Banter See team” over the years of the study, especially R. Mariano Jelicic, C. Bauch and J. Wieland. M.M.B. was supported by a postgraduate grant from the Generalitat de Catalunya (Spain). This project was done under licence from LAVES, Oldenburg, of the Stadt Wilhelmshaven and was financially supported by the Deutsche Forschungsgemeinschaft (BE 916/8-2).

Author information

Authors and Affiliations

  1. Dept. of Biologia Animal (Vertebrats), Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Av. Diagonal 643, 08028, Barcelona, Spain

    María M. Benito & Jacob González-Solís

  2. Institut für Vogelforschung “Vogelwarte Helgoland”, An der Vogelwarte 21, 26386, Wilhelmshaven, Germany

    Peter H. Becker

Authors
  1. María M. Benito
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacob González-Solís
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Peter H. Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to María M. Benito.

Additional information

Communicated by C. Barbraud.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Benito, M.M., González-Solís, J. & Becker, P.H. Sex-specific traits in Common Tern Sterna hirundo chicks: associations with rearing environment, parental factors and survival. J Ornithol 155, 937–949 (2014). https://doi.org/10.1007/s10336-014-1076-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10336-014-1076-2

Keywords

Search

Navigation