Skip to main content
Log in

Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus)

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Egg composition, which is under maternal control, can have a profound effect on offspring fitness. The presence of maternal testosterone and carotenoids in avian egg yolk, for example, is thought to enhance the development and competitive ability of the offspring and protect the hatching and growing chick against oxidative stress. Egg quality often differs between females and such variation can be due to differences in maternal social environment, e.g. breeding density. However, this is confounded by the possibility that the quality of individuals breeding in high- or low-density areas may vary. We tested if maternal social environment influences egg composition in a colonial seabird, the lesser black-backed gull (Larus fuscus). To control for confounding effects of female quality, we experimentally manipulated maternal social environment during egg formation. We increased the frequency of intra-specific interactions (i.e. aggressive encounters with conspecifics other than nest mates) in which the females were involved, by placing an elevated platform in their territory. Females that took part in more intra-specific interactions produced a heavier last egg, but the yolk testosterone concentration in eggs laid by control and experimental females did not differ. Differences in yolk testosterone concentration in relation to embryo sex were found neither in the control nor in the experimental group. In contrast, within the control group, eggs with a male embryo contained more carotenoids than eggs with a female embryo. Moreover, experimental females that had been involved in more intra-specific interactions produced female eggs with higher carotenoid levels compared to female eggs of control birds. An experimental increase in carotenoid levels was not observed in eggs containing a male embryo. Our results suggest that intra-specific interactions experienced by female birds during egg formation can influence conditions for embryonic development.

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

  • Anderson DJ, Reeve J, Bird DM (1997) Sexually dimorphic eggs, nestling growth and sibling competition in American kestrels Falco sparverius. Funct Ecol 11:331–335

    Article  Google Scholar 

  • Arcos M (1972) Steroids in egg yolk. Steroids 19:25–34

    Article  CAS  PubMed  Google Scholar 

  • Adkins-Regan E, Ottinger MA, Park J (1995) Maternal transfer of estradiol to egg yolks alters sexual differentiation of avian offspring. J Exp Zool 271:466–470

    CAS  Google Scholar 

  • Bjerkeng B, Johnsen K, Mayer I, Storebakken T, Nilssen KJ (1999) Influence of 11-ketotestosterone, 17β-estradiol, and 3,5,3’-triiodo-l-thyronine on distribution and metabolism of carotenoids in Arctic charr, Salvelinus alpinus L. Fish Physiol Biochem 21:353–364

    Article  CAS  Google Scholar 

  • Blanco G, Martínez-Padilla J, Serrano D, Dávila JA, Viñuela J (2003) Mass provisioning to different-sex eggs within the laying sequence: consequences for adjustment of reproductive effort in a sexually dimorphic bird. J Anim Ecol 72:831–838

    Article  Google Scholar 

  • Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, Trewby ML, Kennedy MW (2002a) 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  PubMed  Google Scholar 

  • Blount JD, Surai PF, Houston DC, Møller AP (2002b) Patterns of yolk enrichment vary with dietary carotenoids in gulls: the roles of pigment acquisition and utilization. Funct Ecol 16:445–453

    Article  Google Scholar 

  • Carey C (1996) Female reproductive energetics. In: Carey C (ed) Avian energetics and nutritional ecology. Chapman and Hall, New York, pp 324–374

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

    PubMed  Google Scholar 

  • Cordero PJ, Griffith SC, Aparicio JM, Parkin DT (2000) Sexual dimorphism in house sparrow eggs. Behav Ecol Sociobiol 48:353–357

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Cristol DA, Johnsen TS (1994) Spring arrival, aggression and testosterone in female red-winged blackbirds (Agelaius phoeniceus). Auk 111:210–214

    Google Scholar 

  • Donham RS (1979) Annual cycle of plasma luteinizing hormone and sex hormones in male and female mallards (Anas platyrhynchos). Biol Reprod 21:1273–1285

    CAS  PubMed  Google Scholar 

  • Eens M, Pinxten R (2000) Sex-role reversal in vertebrates: behavioural and endocrinological accounts. Behav Process 51:135–147

    Article  Google Scholar 

  • Eising CM (2004) Mother knows best? Costs and benefits of differential maternal hormone allocation in birds. PhD thesis, University of Groningen

  • Eising CM, Groothuis TGG (2003) Yolk androgens and begging behaviour in black-headed gull chicks: an experimental field study. Anim Behav 66:1027–1034

    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  PubMed  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 

  • Elekonich MM, Wingfeld JC (2000) Seasonality and hormonal control of territorial aggression in female song sparrows (Passeriformes: Embrizidae: Melospiza melodia). Ethology 106:493–510

    Article  Google Scholar 

  • Elf PK, Fivizzani AJ (2002) Changes in sex steroid levels in yolks of the leghorn chicken, Gallus domesticus, during embryonic development. J Exp Zool 293:594–600

    Article  CAS  PubMed  Google Scholar 

  • Feder HH, Storey A, Goodwin D, Reboulleau C, Silver R (1977) Testosterone and “5α-dihydrotestosterone” levels in peripheral plasma of male and female ring doves (Streptopelia risoria) during the reproductive cycle. Biol Reprod 16:666–677

    CAS  PubMed  Google Scholar 

  • Finkler MS, van Orman JB, Sotherland PR (1998) Experimental manipulation of egg quality in chickens: influence of albumen and yolk on the size and body composition of near-term embryos in a precocial bird. J Comp Physiol B 168:17–24

    Article  CAS  PubMed  Google Scholar 

  • Gasparini J, McCoy KD, Haussy C, Tveraa T, Boulinier T (2001) Induced maternal response to the Lyme disease spirochaete Borrelia burgdorferi sensu lato in a colonial seabird, the kittiwake Rissa tridactyla. Proc R Soc Lond B 268:647–650

    Article  CAS  PubMed  Google Scholar 

  • Goodwin TW (1984) The biochemistry of the carotenoids. II Animals. Chapmann and Hall, London

  • Griffiths R (1992) Sex-biased mortality in the lesser black-backed gull Larus fuscus during the nestling stage. Ibis 134:237–244

    Google Scholar 

  • Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075

    Article  CAS  PubMed  Google Scholar 

  • Groothuis TG, 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 

  • Hackl R, Bromundt J, Daisley J, Kotrschal K, Möstl E (2003) Distribution and origin of steroid hormones in the yolk of Japanese quail eggs (Coturnix coturnix japonica). J Comp Physiol B 173:327–331

    Article  CAS  PubMed  Google Scholar 

  • Hannon SJ, Wingfield JC (1990) Endocrine correlates of territoriality, breeding stage, and body molt in free-living willow ptarmigan of both sexes. Can J Zool 68:2130–2134

    CAS  Google Scholar 

  • Haq A-U, Bailey CA, Chinnah A (1996) Effect of β-carotene, canthaxanthin, lutein, and vitamin E on neonatal immunity of chicks when supplemented in broiler breeder diets. Poultry Sci 75:1092–1097

    CAS  Google Scholar 

  • Hario M, Rudbäck E (1999) Dying in the midst of plenty – the third chick fate in nominate lesser black-backed gulls Larus f. fuscus. Ornis Fenn 76:71–77

    Google Scholar 

  • Hayward LS, Wingfield JC (2004) Maternal corticosterone is transferred to avian yolk and may alter offspring growth and adult phenotype. Gen Comp Endocrinol 135:365–371

    Article  CAS  PubMed  Google Scholar 

  • Hõrak P, Surai PF, Møller AP (2002) Fat-soluble antioxidants in the eggs of great tits Parus major in relation to breeding habitat and laying sequence. Avian Sci 2:123–130

    Google Scholar 

  • Langmore NE, Cockrem JF, Candy EJ (2002) Competition for male reproductive investment elevates testosterone levels in female dunnocks, Prunella modularis. Proc R Soc Lond B 269:2473–2478

    Article  CAS  PubMed  Google Scholar 

  • Lindström J (1999) Early development and fitness in birds and mammals. Trends Ecol Evol 14:343–348

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (2002) SAS system for mixed models. SAS Institute, Carey, N.C.

  • Magrath MJL, Brouwer L, Komdeur J (2003) Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic brown songlark, Cinclorhamphus cruralis. Behav Ecol Sociobiol 54:240–248

    Article  Google Scholar 

  • Mazuc J, Bonneaud C, Chastel O, Sorci G (2003) Social environment affects female and egg testosterone levels in the house sparrow (Passer domesticus). Ecol Lett 6:1084–1090

    Article  Google Scholar 

  • Meathrel CE, Ryder JP (1987) Intraclutch variation in the size, mass and composition of ring-billed gull eggs. Condor 89:364–368

    Google Scholar 

  • Metcalfe NB, Monaghan P (2001) Compensation for a bad start: grow now, pay later? Trends Ecol Evol 16:248–254

    Article  PubMed  Google Scholar 

  • Metcalfe NB, Monaghan P (2003) Growth versus lifespan: perspectives from evolutionary ecology. Exp Gerontol 38:935–940

    Article  PubMed  Google Scholar 

  • Møller AP, Biard C, Blount JD, Houston DC, Ninni P, Saino N, Surai PF (2000) Carotenoid-dependent signals: indicators of foraging efficiency, immunocompetence or detoxification ability? Avian Poult Biol Rev 11:137–159

    Google Scholar 

  • Mousseau TA and Fox CW (1998) Maternal effects as adaptations. Oxford University Press, Oxford

  • Müller W, Eising CM, Dijkstra C, Groothuis TGG (2002) Sex differences in yolk hormones depend on maternal social status in leghorn chickens (Gallus gallus domesticus). Proc R Soc Lond B 269:2249–2255

    Article  PubMed  Google Scholar 

  • Nager RG Monaghan P, Griffiths R, Houston DC, Dawson R (1999) Experimental demonstration that offspring sex ratio varies with maternal condition. Proc Natl Acad Sci USA 96:570–573

    Article  CAS  PubMed  Google Scholar 

  • Nager RG, Monaghan P, Houston DC (2000) Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81:1339–1350

    Google Scholar 

  • Nelson RJ (1995) An introduction to behavioural endocrinology. Sinauer, Sunderland, Mass.

  • Nys Y (2000) Dietary carotenoids and egg yolk coloration – a review. Arch Geflugelk 64:45–54

    CAS  Google Scholar 

  • Olson VA, Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol Evol 13:510–514

    Article  Google Scholar 

  • Ottinger MA (1989) Sexual differentiation of neuroendocrine systems and behaviour. Poult Sci 68:979–989

    CAS  PubMed  Google Scholar 

  • Parsons J (1976) Factors determining the number and size of eggs laid by the herring gull. Condor 78:481–492

    Google Scholar 

  • Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Sex differences in avian yolk hormone levels. Nature 412:498

    Article  CAS  PubMed  Google Scholar 

  • Pilz KM, Smith HG (2004) Egg yolk androgen levels increase with breeding density in the European starling, Sturnus vulgaris. Funct Ecol 18:58–66

    Google Scholar 

  • Pilz KM, Smith HG, Sandell MI, Schwabl H (2003) Interfemale variation in egg yolk androgen allocation in the European starling: do high quality females invest more? Anim Behav 65:841–850

    Article  Google Scholar 

  • Råberg L, Grahn M, Hasselquist D, Svensson E (1998) On the adaptive significance of stress-induced immunosuppression. Proc R Soc Lond B 265:1637–1641

    Article  PubMed  Google Scholar 

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

    Article  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 

  • Royle NJ, Surai PF, Hartley IR (2001) Maternally derived androgens and antioxidants in bird eggs: complementary but opposing effects? Behav Ecol 12:381–385

    Article  Google Scholar 

  • Saino N, Romano M, Ferrari RP, Martinelli R, Møller AP (2003a) Maternal antibodies but not carotenoids in barn swallow eggs covary with embryo sex. J Evol Biol 16:516–522

    Article  CAS  PubMed  Google Scholar 

  • Saino N, Ferrari R, Romano M, Martinelli R, Møller AP (2003b) Experimental manipulation of egg carotenoids affects immunity of barn swallow nestlings. Proc R Soc Lond B 270:2485–2489

    Article  PubMed  Google Scholar 

  • Schwabl H (1992) Winter and breeding territorial behaviour and levels of reproductive hormones of migratory European robins. Ornis Scand 23:271–276

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Schwabl H (1996) Maternal testosterone in the avian egg enhances post-natal growth. Comp Biochem Physiol 114A:271–276

    Article  CAS  Google Scholar 

  • Schwabl H (1997a) The contents of maternal testosterone in house sparrow Passer domesticus eggs vary with breeding conditions. Naturwissenschaften 84:406–408

    Article  CAS  PubMed  Google Scholar 

  • Schwabl H (1997b) Maternal steroid hormones in the egg. In: Harvey S, Etches RJ (eds) Perspectives in avian endocrinology. Journal of Endocrinology, Bristol, pp 3–13

  • Sheffield JW, O’Shaughnessy PJ (1989) Effect of injection of gonadotropin-releasing hormone on testicular steroidgenesis in the hypogonadal (hpg) mouse. J Reprod Fert 86:609–617

    CAS  Google Scholar 

  • Sundbaum K, Näslund I (1998) Effects of woody debris on the growth and behaviour of brown trout in experimental stream channels. Can J Zool 76:56–61

    Article  Google Scholar 

  • Surai PF (2002) Natural antioxidants in avian nutrition and reproduction. Nottingham University Press, Nottingham, UK

  • Surai PF, Speake BK (1998) Distribution of carotenoids from the yolk to the tissues of the chick embryo. J Nutr Biochem 9:645–651

    Article  CAS  Google Scholar 

  • Tinbergen N (1953) The herring gull’s world. Collins, London

  • Verboven N, Monaghan P, Evans DM, Schwabl H, Evans N, Whitelaw C, Nager RG (2003) Maternal condition, yolk androgens and offspring performance: a supplemental feeding experiment in the lesser black-backed gull (Larus fuscus). Proc R Soc Lond B 270:2223–2232

    Article  PubMed  Google Scholar 

  • Whittingham LA, Schwabl H (2002) Maternal testosterone in tree swallow eggs varies with female aggression. Anim Behav 63:63–67

    Article  Google Scholar 

  • Williams JD (1994) Intraspecific variation in egg size and egg composition in birds: effects on offspring fitness. Biol Rev 68:35–69

    Google Scholar 

  • Wingfield JC, Hegner RE, Dufty, AM, Ball GF (1990) The ‘challenge hypothesis’: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am Nat 136:829–846

    Article  Google Scholar 

  • Wilson CM, McNabb FM (1997) Maternal thyroid hormones in Japanese quail eggs and their influence on embryonic development. Gen Comp Endocrinol 107:153–165

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Christine Whitelaw for help with the hormone assays, Kate Orr and Aileen Adam for sexing the embryos and Maria Bogdanova, Sin-Yeon Kim and the Cumbria Wildlife Trust for support on Walney. The experiment was approved by English Nature (license no. 20020764).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nanette Verboven.

Additional information

Communicated by J. Graves

Rights and permissions

Reprints and permissions

About this article

Cite this article

Verboven, N., Evans, N.P., D’Alba, L. et al. Intra-specific interactions influence egg composition in the lesser black-backed gull (Larus fuscus). Behav Ecol Sociobiol 57, 357–365 (2005). https://doi.org/10.1007/s00265-004-0862-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-004-0862-x

Keywords

Navigation