Skip to main content
Log in

Maternal investment in last-laid eggs does not compensate for hatching asynchrony in a seabird

  • Behavioral ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Maternal and environmental effects can have profound effects on offspring performance by generating variation in offspring phenotypes, independent of genetic effects. Within avian broods, differential maternal investment of resources across the laying sequence is thought to be an adaptive strategy to modulate competitive hierarchies induced by hatching asynchrony. In this study, we evaluated the relative importance of maternally derived within-clutch variation and the asymmetric post-hatching environment for growth and survival of common tern (Sterna hirundo) siblings. We experimentally manipulated hatching order, resulting in chicks from last-laid eggs hatching first and vice versa. Although both initial age and size asymmetries were larger within experimental than control broods, the early survival of last-hatched chicks was similar between groups. Initial positive effects of egg size disappeared as siblings approached fledging. Ultimately at fledging, both within-brood growth and cumulative survival patterns were similar between experimental and control broods, suggesting that the effects of systematic variation of egg constituents (e.g., maternally derived yolk hormones) and egg size are too subtle and largely overwhelmed by the effects of hatching asynchrony. Therefore, we conclude that variation in offspring phenotypes is pre-dominantly determined by the social environment experienced post-hatching. Maternal effects may further fine-tune phenotypic variation in response to varying environmental conditions, but this needs to be tested through empirical studies in which multiple maternal effects are measured simultaneously under different environmental conditions.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • 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 

  • Arnold JM, Hatch JJ, Nisbet ICT (2006) Effects of egg size, parental quality and hatch-date on growth and survival of common tern Sterna hirundo chicks. Ibis 148:98–105

    Article  Google Scholar 

  • Becker PH (1996) Flußseeschwalben (Sterna hirundo) in Wilhelmshaven. Oldenburger Jahrb 1996:263–296

    Google Scholar 

  • Becker PH, Finck P (1985) The influence of weather and food situation on the breeding success of common terns (Sterna hirundo). J Ornithol 126:393–404

    Article  Google Scholar 

  • Becker PH, Ludwigs J-D (2004) Sterna hirundo common tern. BWP Update 6:91–137

    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

    Google Scholar 

  • Becker PH, Wendeln H, González-Solı́s J (2001) Population dynamics, recruitment, individual quality and reproductive strategies in common terns Sterna hirundo marked with transponders. Ardea 89:241–251

    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 44:179–188

    Article  Google Scholar 

  • Bernardo J (1996a) Maternal effects in animal ecology. Integr Comp Biol 36:83–105

    Google Scholar 

  • Bernardo J (1996b) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Integr Comp Biol 36:216–236

    Google Scholar 

  • Bitton P-B, Dawson RD, O’Brian EL (2006) Influence of intraclutch egg-mass variation and hatching asynchrony on relative offspring performance within broods of an altricial bird. Can J Zool 84:1721–1726

    Article  Google Scholar 

  • Blount JD, Surai PF, Nager RG et al (2002) Carotenoids and egg quality in the lesser black-backed gull Larus fuscus: a supplemental feeding study of maternal effects. Proc R Soc Lond B 269:29–36

    Article  CAS  Google Scholar 

  • Bogdanova MI, Nager RG (2008) Sex-specific costs of hatching last: an experimental study on herring gulls (Larus argentatus). Behav Ecol Sociobiol 62:1533–1541

    Article  Google Scholar 

  • Bollinger PB (1994) Relative effects of hatching order, egg-size variation, and parental quality on chick survival in common terns. Auk 111:263–273

    Article  Google Scholar 

  • Bollinger PB, Bollinger EK, Malecki RA (1990) Tests of three hypotheses of hatching asynchrony in the common tern. Auk 107:696–706

    Article  Google Scholar 

  • Christians JK (2002) Avian egg size: variation within species and inflexibility within individuals. Biol Rev 77:1–26

    Article  PubMed  Google Scholar 

  • Corp IBM (2011) IBM statistics for windows. IBM Corp, Armonk

    Google Scholar 

  • Dänhardt A, Becker PH (2011) Herring and sprat abundance indices predict chick growth and reproductive performance of common terns breeding in the Wadden Sea. Ecosystems 14:791–803

    Article  Google Scholar 

  • Dittmann T, Zinsmeister D, Becker PH (2005) Dispersal decisions: common terns, Sterna hirundo, choose between colonies during prospecting. Anim Behav 70:13–20

    Article  Google Scholar 

  • Droge DL, Gowaty PA, Weathers WW (1991) Sex-biased provisioning: a test for differences in field metabolic rates of nestling eastern bluebirds. Condor 93:793–798

    Article  Google Scholar 

  • Eising CM, Eikenaar C, Schwabl H, Groothuis TGG (2001) Maternal androgens in black-headed gull (Larus ridibundus) eggs: consequences for chick development. Proc R Soc Lond B 268:839–846

    Article  CAS  Google Scholar 

  • Eising CM, Müller W, Dijkstra C, Groothuis TGG (2003) Maternal androgens in egg yolks: relation with sex, incubation time and embryonic growth. Gen Comp Endocrinol 132:241–247

    Article  CAS  PubMed  Google Scholar 

  • Fletcher KL, Hamer KC (2004) Offspring sex ratio in the common tern Sterna hirundo, a species with negligible sexual size dimorphism. Ibis 146:454–460

    Article  Google Scholar 

  • Forbes S (2011) Social rank governs the effective environment of siblings. Biol Lett 7:346–348

    Article  PubMed  Google Scholar 

  • French JB, Nisbet ICT, Schwabl H (2001) Maternal steroids and contaminants in common tern eggs: a mechanism of endocrine disruption? Comp Biochem Physiol C 128:91–98

    Article  Google Scholar 

  • Gil D (2008) Hormones in avian eggs: physiology, ecology and behavior. In: Jane H, Brockmann TJR (eds) Advances in the study of behavior. Academic Press, New York, pp 337–398

    Google Scholar 

  • Gil D, Bulmer E, Celis P, López-Rull I (2008) Adaptive developmental plasticity in growing nestlings: sibling competition induces differential gape growth. Proc R Soc Lond B 275:549–554

    Article  Google Scholar 

  • Glassey B, Forbes S (2002) Begging and asymmetric nestling competition. In: Wright J, Leonard ML (eds) The evolution of begging. Springer, Netherlands, pp 269–281

    Chapter  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 

  • Governali FC, Gates HR, Lanctot RB, Holmes RT (2012) Egg volume can be accurately and efficiently estimated from linear dimensions for Arctic-breeding shorebirds. Wader Study Group Bull 119:46–51

    Google Scholar 

  • Groothuis TGG, Schwabl H (2002) Determinants of within- and among-clutch variation in levels of maternal hormones in black-headed gull eggs. Funct Ecol 16:281–289

    Article  Google Scholar 

  • Groothuis TGG, Schwabl H (2008) Hormone-mediated maternal effects in birds: mechanisms matter but what do we know of them? Phil Trans R Soc B 363:1647–1661

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TGG, Müller W W, von Engelhardt N et al (2005) Maternal hormones as a tool to adjust offspring phenotype in avian species. Neurosci Biobehav Rev 29:329–352

    Article  CAS  PubMed  Google Scholar 

  • Hargitai R, Prechl J, Török J (2006) Maternal immunoglobulin concentration in collared flycatcher (Ficedula albicollis) eggs in relation to parental quality and laying order. Funct Ecol 20:829–838

    Article  Google Scholar 

  • Hasselquist D, Nilsson J-Å (2009) Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity. Phil Trans R Soc B 364:51–60

    Article  PubMed  Google Scholar 

  • Kölliker M, Richner H, Werner I, Heeb P (1998) Begging signals and biparental care: nestling choice between parental feeding locations. Anim Behav 55:215–222

    Article  Google Scholar 

  • Kozlowski CP, Ricklefs RE (2010) Egg size and yolk steroids vary across the laying order in cockatiel clutches: a strategy for reinforcing brood hierarchies? Gen Comp Endocrinol 168:460–465

    Article  CAS  PubMed  Google Scholar 

  • Krist M (2011) Egg size and offspring quality: a meta-analysis in birds. Biol Rev 86:692–716

    Article  PubMed  Google Scholar 

  • Krist M, Remeš V (2004) Maternal effects and offspring performance: in search of the best method. Oikos 106:422–426

    Article  Google Scholar 

  • Krist M, Remeš V, Uvírová L et al (2004) Egg size and offspring performance in the collared flycatcher (Ficedula albicollis): a within-clutch approach. Oecologia 140:52–60

    Article  PubMed  Google Scholar 

  • Langham NPE (1972) Chick survival in terns (Sterna Spp.) with particular reference to the common tern. J Anim Ecol 41:385–395

    Article  Google Scholar 

  • Lipar JL (2001) Yolk steroids and the development of the hatching muscle in nestling European starlings. J Avian Biol 32:231–238

    Article  Google Scholar 

  • Lipar JL, Ketterson ED (2000) Maternally derived yolk testosterone enhances the development of the hatching muscle in the red-winged blackbird Agelaius phoeniceus. Proc R Soc Lond B 267:2005–2010

    Article  CAS  Google Scholar 

  • Maddox JD, Weatherhead P (2008) Egg size variation in birds with asynchronous hatching: is bigger really better? Am Nat 171:358–365

    Article  PubMed  Google Scholar 

  • Mainwaring MC, Dickens M, Hartley IR (2010) Environmental and not maternal effects determine variation in offspring phenotypes in a passerine bird. J Evol Biol 23:1302–1311

    Article  PubMed  Google Scholar 

  • Marshall J, Uller T (2007) When is a maternal effect adaptive? Oikos 116:1957–1963

    Article  Google Scholar 

  • Massias A, Becker PH (1990) Nutritive value of food and growth in common tern Sterna hirundo chicks. Ornis Scand 21:187–194

    Article  Google Scholar 

  • Merkling T, Agdere L, Albert E, Durieux R, Hatch SA, Danchin E, Blanchard P (2014) Is natural hatching asynchrony optimal? An experimental investigation of sibling competition patterns in a facultatively siblicidal seabird. Behav Ecol Sociobiol 68:309–319

    Article  Google Scholar 

  • Merkling T, Perrot C, Helfenstein F, Ferdy J-B, Gaillard L, Lefol E, Voisin E, Hatch SA, Danchin E, Blanchard P (2016) Maternal effects as drivers of sibling competition in a parent–offspring conflict context? An experimental test. Ecol Evol 6:3699–3710

    Article  PubMed  PubMed Central  Google Scholar 

  • Mlody B, Becker PH (1991) Körpermasse-Entwicklung und Mortalität von Küken der Flußseeschwalbe (Sterna hirundo) unter ungünstigen Umweltbedingungen. Vogelwarte 36:110–131

    Google Scholar 

  • Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, New York

    Google Scholar 

  • Mousseau TA, Fox CW (1998) The adaptive significance of maternal effects. Trends Ecol Evol 13:403–407

    Article  CAS  PubMed  Google Scholar 

  • Muck C, Nager RG (2006) The effect of laying and hatching order on the timing and asynchrony of hatching. Anim Behav 71:885–892

    Article  Google Scholar 

  • Müller M, Groothuis TGG (2013) Within-clutch variation in yolk testosterone as an adaptive maternal effect to modulate avian sibling competition: evidence from a comparative study. Am Nat 181:125–136

    Article  PubMed  Google Scholar 

  • Nisbet ICT (1978) Dependence of fledging success on egg-size, parental performance and egg-composition among common and roseate terns, Sterna hirundo and S. dougallii. Ibis 120:207–215

    Article  Google Scholar 

  • Nisbet ICT, Cohen ME (1975) Asynchronous hatching in common and roseate terns, Sterna hirundo and S. dougallii. Ibis 117:374–379

    Article  Google Scholar 

  • Parsons J (1970) Relationship between egg size and post-hatching chick mortality in the herring gull (Larus argentatus). Nature 228:1221–1222

    Article  CAS  PubMed  Google Scholar 

  • Parsons J (1972) Egg size, laying date and incubation period in the herring gull. Ibis 114:536–541

    Article  Google Scholar 

  • Reed WL, Vleck CM (2001) Functional significance of variation in egg-yolk androgens in the American coot. Oecologia 128:164–171

    Article  PubMed  Google Scholar 

  • Reed W-L, Clark M-E, Vleck C-M (2009) Maternal effects increase within-family variation in offspring survival. Am Nat 174:685–695

    Article  PubMed  Google Scholar 

  • Royle NJ, Surai PF, McCartney RJ, Speake BK (1999) Parental investment and egg yolk lipid composition in gulls. Funct Ecol 13:298–306

    Article  Google Scholar 

  • Ruuskanen S, Laaksonen T (2013) Sex-specific effects of yolk androgens on begging behavior and digestion in pied flycatchers. J Avian Biol 44:331–338

    Article  Google Scholar 

  • Schielzeth H (2010) Simple means to improve the interpretability of regression coefficients. Methods Ecol Evol 1:103–113

    Article  Google Scholar 

  • Schwabl H (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90:11446–11450

    Article  CAS  PubMed  Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the avian egg enhances postnatal growth. Comp Biochem Phys A 114:271–276

    Article  CAS  Google Scholar 

  • Schwabl H, Mock DW, Gieg JA (1997) A hormonal mechanism for parental favouritism. Nature 386:231

    Article  CAS  Google Scholar 

  • Slagsvold T, Sandvik J, Rofstad G et al (1984) On the adaptive value of intraclutch egg-size variation in birds. Auk 101:685–697

    Article  Google Scholar 

  • Smith T, Leonard M, Smith B (2005) Provisioning rules and chick competition in asynchronously hatching common terns (Sterna hirundov). Behav Ecol Sociobiol 58:456–465

    Article  Google Scholar 

  • Sockman KW, Sharp PJ, Schwabl H (2006) Orchestration of avian reproductive effort: an integration of the ultimate and proximate bases for flexibility in clutch size, incubation behaviour, and yolk androgen deposition. Biol Rev 81:629–666

    Article  PubMed  Google Scholar 

  • Stamps JA (1990) When should avian parents differentially provision sons and daughters? Am Nat 135:671–685

    Article  Google Scholar 

  • Stoleson SH, Beissinger SR (1995) Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period? In: Power DM (ed) Current ornithology, vol 12. Plenum Press, New York, pp 191–270

    Chapter  Google Scholar 

  • Sudmann SR (1998) Wie dicht können Flußseeschwalben Sterna hirundo brüten? Extremsituationen auf Brutflößen. Vogelwelt 119:181–192

    Google Scholar 

  • Tanner M, Kölliker M, Richner H (2007) Parental influence on sibling rivalry in great tit, Parus major, nests. Anim Behav 74:977–983

    Article  Google Scholar 

  • Tella JL, Forero MG, Bertellotti M et al (2001) Offspring body condition and immunocompetence are negatively affected by high breeding densities in a colonial seabird: a multiscale approach. Proc R Soc Lond B 268:1455–1461

    Article  CAS  Google Scholar 

  • Vedder O, Zhang H, Bouwhuis S (2017a) Early mortality saves energy: estimating the energetic cost of excess offspring in a seabird. Proc R Soc B 284:2016–2724

    Article  Google Scholar 

  • Vedder O, Kürten N, Bouwhuis S (2017b) Intraspecific variation in and environment-dependent resource allocation to embryonic development time in common terns. Physiol Biochem Zool 90:453–460

    Article  PubMed  Google Scholar 

  • Viñuela J (1997a) Adaptation vs. constraint: intraclutch egg-mass variation in birds. J Anim Ecol 66:781

    Article  Google Scholar 

  • Viñuela J (1997b) Laying order affects incubation duration in the black kite (Milvus migrans): counteracting hatching asynchrony? Auk 114:192–199

    Article  Google Scholar 

  • Viñuela J (1999) Sibling aggression, hatching asynchrony, and nestling mortality in the black kite (Milvus migrans). Behav Ecol Sociobiol 45:33–45

    Article  Google Scholar 

  • Wendeln H, Becker PH (1999) Effects of parental quality and effort on the reproduction of common terns. J Anim Ecol 68:205–214

    Article  Google Scholar 

  • Williams TD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 69:35–59

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Götz Wagenknecht for data processing and molecular sex determination, and Christina Bauch, Jana Sprenger, and Luis Schmidt for help with field work. We thank Gerold Gembler, Götz Wagenknecht, and Tom Ezard for constructing the breeding raft. We are grateful for constructive criticism on a previous draft of the manuscript by Oscar Vedder. We thank Oliver P. Love and three anonymous reviewers whose helpful comments greatly improved the paper. For technical support and the permission to work in otherwise restricted areas, we thank the Standortverwaltung and Marinearsenal of the Bundeswehr Wilhelmshaven. Funding for this project was provided by the German Research Foundation Deutsche Forschungsgemeinschaft (DFG, BE/916-8-2).

Author information

Authors and Affiliations

Authors

Contributions

AB and PHB conceived and designed experiments. AB performed experiments. AB and PHB collected data. AB analyzed the data. AB wrote the manuscript. PHB provided editorial advice.

Corresponding author

Correspondence to A. Braasch.

Additional information

Communicated by Oliver P. Love.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Braasch, A., Becker, P.H. Maternal investment in last-laid eggs does not compensate for hatching asynchrony in a seabird. Oecologia 190, 47–58 (2019). https://doi.org/10.1007/s00442-019-04399-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-019-04399-9

Keywords

Navigation