Skip to main content

Advertisement

Log in

Laying date, incubation and egg breakage as determinants of bacterial load on bird eggshells: experimental evidence

  • Behavioral ecology - Original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Exploring factors guiding interactions of bacterial communities with animals has become of primary importance for ecologists and evolutionary biologists during the last years because of their likely central role in the evolution of animal life history traits. We explored the association between laying date and eggshell bacterial load (mesophilic bacteria, Enterobacteriaceae, Staphylococci, and Enterococci) in natural and artificial magpie (Pica pica) nests containing fresh commercial quail (Coturnix coturnix) eggs. We manipulated hygiene conditions by spilling egg contents on magpie and artificial nests and explored experimental effects during the breeding season. Egg breakage is a common outcome of brood parasitism by great spotted cuckoos (Clamator glandarius) on the nests of magpie, one of its main hosts. We found that the treatment increased eggshell bacterial load in artificial nests, but not in magpie nests with incubating females, which suggests that parental activity prevents the proliferation of bacteria on the eggshells in relation to egg breakage. Moreover, laying date was positively related to eggshell bacterial load in active magpie nests, but negatively in artificial nests. The results suggest that variation in parental characteristics of magpies rather than climatic variation during the breeding season explained the detected positive association. Because the eggshell bacterial load is a proxy of hatching success, the detected positive association between eggshell bacterial loads and laying date in natural, but not in artificial nests, suggests that the generalized negative association between laying date and avian breeding success can be, at least partially, explained by differential bacterial effects.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Baggott GK, Graeme-Cook K (2002) Microbiology of natural incubation. In: Deeming DC (ed) Avian incubation behaviour, environment and evolution. Oxford University Press, Oxford, pp 179–191

    Google Scholar 

  • Birkhead TR (1991) The magpies. In: The ecology and behaviour of black-billed and yellow-billed magpies. Poyser, London

  • Board RG, Tranter HS (1986) The microbiology of eggs. In: Stadelman WJ, Cotterill OJ (eds) Egg science and technology. AVI, Westport, pp 75–96

    Google Scholar 

  • Board RG, Clay C, Lock J, Dolman J (1994) The egg: a compartmentalized, aseptically packaged food. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman & Hall, London, pp 43–62

    Chapter  Google Scholar 

  • Bonisoli-Alquati A, Rubolini D, Romano M, Cucco M, Fasola M, Caprioli M, Saino N (2010) Egg antimicrobials, embryo sex and chick phenotype in the yellow-legged gull. Behav Ecol Sociobiol 64:845–855

    Article  Google Scholar 

  • Bruce J, Drysdale EM (1991) Egg hygiene: route of infection. In: Tullett SG (ed) Avian incubation. Butterworth Heinemann, Northampton, pp 257–276

    Google Scholar 

  • Bruce J, Drysdale EM (1994) Trans-shell transmission. In: Board RG, Fuller R (eds) Microbiology of avian eggs. Chapman & Hall, London, pp 63–91

    Chapter  Google Scholar 

  • Chastel O, Weimerskirch H, Jouventin P (1995) Influence of body condition on reproductive decision and reproductive success in the Blue Petrel. Auk 112:964–972

    Article  Google Scholar 

  • Christe P, Richner H, Oppliger A (1996) Of great tits and fleas: sleep baby sleep. Anim Behav 52:1087–1092

    Article  Google Scholar 

  • Christians JK, Evanson M, Aiken JJ (2001) Seasonal decline in clutch size in European starlings: a novel randomization test to distinguish between the timing and quality hypotheses. J Anim Ecol 70:1080–1087

    Article  Google Scholar 

  • Clark L, Mason JR (1985) Use of nest material as insecticidal and anti-pathogenic agents by the European starling. Oecologia 67:169–176

    Article  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2003) Trans-shell infection by pathogenic micro-organisms reduces the shelf life of non-incubated bird’s eggs: a constraint on the onset of incubation? Proc R Soc Lond B 270:2233–2240

    Article  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005a) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537

    Article  PubMed  Google Scholar 

  • Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2005b) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36

    Article  Google Scholar 

  • D’Alba L, Oborn A, Shawkey MD (2010) Experimental evidence that keeping eggs dry is a mechanism for the antimicrobial effects of avian incubation. Naturwissenschaften 97:1089–1095

    Article  PubMed  Google Scholar 

  • De Neve L, Soler JJ, Soler M, Pérez-Contreras T (2004) Differential maternal investment counteracts for late breeding in magpies Pica pica: an experimental study. J Avian Biol 35:237–245

    Article  Google Scholar 

  • De Neve L, Soler JJ, Ruiz-Rodríguez M, Martín-Gálvez D, Pérez-Contreras T, Soler M (2007) Habitat-specific effects of a food supplementation experiment on immunocompetence in Eurasian magpie Pica pica nestlings. Ibis 149:763–773

    Article  Google Scholar 

  • Godard RD, Morgan Wilson C, Frick JW, Siegel PB, Bowers BB (2007) The effects of exposure and microbes on hatchability of eggs in open-cup and cavity nests. J Avian Biol 38:709–716

    Article  Google Scholar 

  • Gordo O, Sanz JJ (2006) Climate change and bird phenology: a long-term study in the Iberian Peninsula. Glob Chang Biol 12:1993–2004

    Article  Google Scholar 

  • Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hochachka W (1990) Seasonal decline in reproductive performance of song sparrows. Ecology 71:1279–1288

    Article  Google Scholar 

  • Houston CS, Saunders JR, Crawford RD (1997) Aerobic bacterial flora of addled raptor eggs in Saskatchewan. J Wildl Dis 33:328–331

    Article  CAS  PubMed  Google Scholar 

  • Ibáñez-Álamo JD, Ruiz-Rodríguez M, Soler JJ (2014) The mucous covering of fecal sacs prevents birds from infection with enteric bacteria. J Avian Biol 45:354–358

    Article  Google Scholar 

  • Kozlowski S, Malysko E, Pinowski J, Kruszewicz A (1989) The effect of microorganisms on the mortality of house sparrow (Passer domesticus) and tree sparrow (Passer montanus) embryos. In: Pinowski J, Kavanagh BP, Gorski W (eds) Proceedings of the International Symposium Working Group on Granivorous Birds. Intecol, Slupsk, Poland, pp 121–128

  • Lee WY, Kim M, Jablonski PG, Choe JC, Si Lee (2014) Effect of incubation on bacterial communities of eggshells in a temperate bird, the Eurasian magpie (Pica pica). PLoS One 9:e103959

    Article  PubMed Central  PubMed  Google Scholar 

  • Maigetter RZ, Pfister RM (1975) A mixed bacterial population in a continuous culture with and without kaolinite. Can J Microbiol 21:173–180

    Article  CAS  PubMed  Google Scholar 

  • Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Soler M, Burke T (2007) Cuckoo parasitism and productivity in different magpie subpopulations predict frequencies of the 457bp allele: a mosaic of coevolution at a small geographic scale. Evolution 61:2340–2348

    Article  PubMed  Google Scholar 

  • Martín-Vivaldi M, Ruiz-Rodríguez M, Mendez M, Soler JJ (2006) Relative importance of factors affecting nestling immune response differs between junior and senior nestlings within broods of hoopoes Upupa epops. J Avian Biol 37:467–476

    Article  Google Scholar 

  • McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Lošo T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, Hentschel U, King N, Kjelleberg S, Knoll AH, Kremer N, Mazmanian SK, Metcalf JL, Nealson K, Pierce NE, Rawls JF, Reid A, Ruby EG, Rumpho M, Sanders JG, Tautz D, Wernegreen JJ (2013) Animals in a bacterial world, a new imperative for the life sciences. Proc Natl Acad Sci 110:3229–3236

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mennerat A, Mirleau P, Blondel J, Perret P, Lambrechts M, Heeb P (2009) Aromatic plants in nests of the blue tit Cyanistes caeruleus protect chicks from bacteria. Oecologia 161:849–855

    Article  PubMed  Google Scholar 

  • Merino S, Møller AP, de Lope F (2000) Seasonal changes in cell-mediated immunocompetence and mass gain in nestling barn swallows: a parasite-mediated effect? Oikos 90:327–332

    Article  Google Scholar 

  • Møller AP, Peralta-Sánchez JM, Nielsen JT, López-Hernández E, Soler JJ (2012) Goshawk prey have more bacteria than non-prey. J Anim Ecol 81:403–410

    Article  PubMed  Google Scholar 

  • Møller AP, Flensted-Jensen E, Mardal W, Soler JJ (2013) Host-parasite relationship between colonial terns and bacteria is modified by a mutualism with a plant with antibacterial defenses. Oecologia 173:169–178

    Article  PubMed  Google Scholar 

  • Moreno J (1998) The determination of seasonal declines in breeding success in seabirds. Etología 6:17–31

    Google Scholar 

  • Peralta-Sánchez JM, Møller AP, Martín-Platero AM, Soler JJ (2010) Number and colour composition of nest lining feathers predict eggshell bacterial community in barn swallow nests: an experimental study. Funct Ecol 24:426–433

    Article  Google Scholar 

  • Peralta-Sánchez JM, Møller AP, Soler JJ (2011) Colour composition of nest lining feathers affects hatching success of barn swallows, Hirundo rustica (Passeriformes: Hirundinidae). Biol J Linn Soc 102:67–74

    Article  Google Scholar 

  • Peralta-Sánchez JM, Martín-Vivaldi M, Martín-Platero AM, Martínez-Bueno M, Oñate M, Ruiz-Rodríguez M, Soler JJ (2012) Avian life history traits influence eggshell bacterial loads: a comparative analysis. Ibis 154:725–737

    Article  Google Scholar 

  • Peralta-Sánchez JM, Soler JJ, Martín-Platero AM, Knight R, Martínez-Bueno M, Møller AP (2014) Eggshell bacterial load is related to antimicrobial properties of feathers lining barn swallow nests. Microb Ecol 67:480–487

    Article  PubMed  Google Scholar 

  • Price T, Kirkpatrick M, Arnold SJ (1988) Directional selection and the evolution of breeding date in birds. Science 240:798–799

    Article  CAS  PubMed  Google Scholar 

  • Reif J, Vorisek P, St’astny K, Koschova M, Bejcek V (2008) The impact of climate change on long-term population trends of birds in a central European country. Anim Conserv 11:412–421

    Article  Google Scholar 

  • Said SA, Shibl AM, Abdullah ME (1980) Influence of various agents on adsorption capacity of kaolin for pseudomonas aeruginosa toxin. J Pharm Sci 69:1238–1239

    Article  CAS  PubMed  Google Scholar 

  • Saino N, Calza S, Møller AP (1998) Effects of a dipteran ectoparasite on immune response and growth trade-offs in barn swallow, Hirundo rustica, nestlings. Oikos 81:217–228

    Article  Google Scholar 

  • Saino N, Dall’ara P, Martinelli R, Møller AP (2002) Early maternal effects and antibacterial immune factors in the eggs, nestlings and adults of the barn swallow. J Evol Biol 15:735–743

    Article  CAS  Google Scholar 

  • Saino N, Ambrosini R, Rubolini D, von Hardenberg J, Provenzale A, Hueppop K, Hueppop O, Lehikoinen A, Lehikoinen E, Rainio K, Romano M, Sokolov L (2011) Climate warming, ecological mismatch at arrival and population decline in migratory birds. Proc R Soc Lond B 278:835–842

    Article  Google Scholar 

  • Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4:e4522

    Article  PubMed Central  PubMed  Google Scholar 

  • Siikamäki P (1998) Limitation of reproductive success by food availability and breeding time in pied flycatchers. Ecology 79:1789–1796

    Article  Google Scholar 

  • Soler JJ, Soler M (2000) Brood-parasite interactions between great spotted cuckoos and magpies: a model system for studying coevolutionary relationships. Oecologia 125:309–320

    Article  Google Scholar 

  • Soler JJ, Soler M, Møller AP, Martínez JG (1995) Does the great spotted cuckoo choose magpie hosts according to their parenting ability? Behav Ecol Sociobiol 36:201–206

    Article  Google Scholar 

  • Soler M, Soler JJ, Martínez JG (1997) Great spotted cuckoos improve their reproductive success by damaging magpie host eggs. Anim Behav 54:1227–1233

    Article  PubMed  Google Scholar 

  • Soler JJ, Møller AP, Soler M (1998) Nest building, sexual selection and parental investment. Evol Ecol 12:427–441

    Article  Google Scholar 

  • Soler JJ, Martínez JG, Soler M, Møller AP (1999) Genetic and geographic variation in rejection behavior of cuckoo eggs by European magpie populations: an experimental test of rejecter-gene flow. Evolution 53:947–956

    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 

  • Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, Peralta-Sánchez JM, Méndez M (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871

    Article  Google Scholar 

  • Soler JJ, Martín-Vivaldi M, Peralta-Sánchez JM, Ruiz-Rodríguez M (2010) Antibiotic-producing bacteria as a possible defence of birds against pathogenic microorganisms. Open Ornithol J 3:93–100

    Article  Google Scholar 

  • Soler JJ, Peralta-Sánchez JM, Martínez Bueno M, Martín-Vivaldi M, Martín-Gálvez D, Vela AI, Briones V, Pérez-Contreras T (2011) Brood parasitism is associated with increased bacterial contamination of host eggs: bacterial loads of host and parasitic eggs. Biol J Linn Soc 103:836–848

    Article  Google Scholar 

  • Soler JJ, Peralta-Sánchez JM, Martín-Platero AM, Martín-Vivaldi M, Martínez-Bueno M, Møller AP (2012) The evolution of size of the uropygial gland: mutualistic feather mites and uropygial secretion reduce bacterial loads of eggshells and hatching failures of European birds. J Evol Biol 25:1779–1791

    Article  CAS  PubMed  Google Scholar 

  • Soler JJ, Martin-Galvez D, De Neve L, Soler M (2013) Brood parasitism correlates with the strength of spatial autocorrelation of life history and defensive traits in magpies. Ecology 94:1338–1346

    Article  PubMed  Google Scholar 

  • Soler JJ, De Neve L, Martin-Galvez D, Molina-Morales M, Perez-Contreras T, Ruiz-Rodriguez M (2014) Do climatic conditions affect host and parasite phenotypes differentially? A case study of magpies and great spotted cuckoos. Oecologia 174:327–338

    Article  PubMed  Google Scholar 

  • Sorci G, Soler JJ, Møller AP (1997) Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica). Proc R Soc Lond B 264:1593–1598

    Article  Google Scholar 

  • Stadelman WJ (1994) Contaminats of liquid eggs products. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman & Hall, London, pp 139–151

    Chapter  Google Scholar 

  • Statsoft (2011) STATISTICA (data analysis software system), version 10. http://www.statsoft.com

  • Verhulst S, Nilsson JA (2008) The timing of birds’ breeding seasons: a review of experiments that manipulated timing of breeding. Philos Trans R Soc Lond B 363:399–410

    Article  Google Scholar 

  • Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc B Biol Sci 272:2561–2569

    Article  Google Scholar 

  • Wang JM, Firestone MK, Beissinger SR (2011) Microbial and environmental effects on avian egg viability: do tropical mechanisms act in a temperate environment? Ecology 92:1137–1145

    Article  PubMed  Google Scholar 

  • Wardrop SL, Ydenberg RC (2003) Date and parental quality effects in the seasonal decline in reproductive performance of the tree swallow Tachycineta bicolor: interpreting results in light of potential experimental bias. Ibis 145:439–447

    Article  Google Scholar 

  • Winkler DW, Allen PE (1996) The seasonal decline in tree swallow clutch size: physiological constraint or strategic adjustment? Ecology 77:922–932

    Article  Google Scholar 

  • Winkler DW, Ringelman KM, Dunn PO, Whittingham L, Hussell DJT, Clark RG, Dawson RD, Johnson LS, Rose A, Austin SH, Robinson WD, Lombardo MP, Thorpe PA, Shutler D, Robertson RJ, Stager M, Leonard M, Horn AG, Dickinson J, Ferretti V, Massoni V, Bulit F, Reboreda JC, Liljesthröm M, Quiroga M, Rakhimberdiev E, Ardia DR (2014) Latitudinal variation in clutch size—lay date regressions in Tachycineta swallows: effects of food supply or demography? Ecography 37:670–678

    Article  Google Scholar 

Download references

Acknowledgments

E. Campanario and E. López-Hernández performed all laboratory work. This work was financed by the Spanish Ministerio de Ciencia e Innovación, European funds (FEDER) (CGL2010-19233-C03-01, CGL2010-19233-C03-03, CGL2013-48193-C3-1-P, CGL2013-48193-C3-3-P). M. R. R. and G. T. respectively received a post-doctoral grant from the JAE-Doc and Juan de la Cierva programmes, and C. R.-C. had a pre-doctoral grant from the Spanish Government. We obtained permission to sample eggs and visit nests of magpies from the Consejería de Medio Ambiente (Junta de Andalucía).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Juan José Soler.

Additional information

Communicated by Indrikis Krams.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Soler, J.J., Ruiz-Rodríguez, M., Martín-Vivaldi, M. et al. Laying date, incubation and egg breakage as determinants of bacterial load on bird eggshells: experimental evidence. Oecologia 179, 63–74 (2015). https://doi.org/10.1007/s00442-015-3322-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-015-3322-6

Keywords

Profiles

  1. Magdalena Ruiz-Rodríguez