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Journal of Ornithology

, Volume 155, Issue 3, pp 671–677 | Cite as

An experimental test in Mallards (Anas platyrhynchos) of the effect of incubation and maternal preen oil on eggshell microbial load

  • M. GiraudeauEmail author
  • G. Á. Czirják
  • C. Duval
  • V. Bretagnolle
  • C. Gutierrez
  • P. Heeb
Original Article

Abstract

Microbial infection is one of the main factors reducing survival in the first stages of life in oviparous species, and recent studies have shown that the avian eggshell harbors an important variety of microorganisms that can rapidly multiply and penetrate the shell, leading to a decrease in hatchability. Here, we report the results of an experiment in which we examined how incubation and maternal preen oil affect the growth of avian eggshell microbes, using the Mallard (Anas platyrhynchos) as a model species. We compared the bacterial and fungal loads on the shell of non-incubated eggs and eggs incubated by females having free or blocked access to their preen gland. An increase of eggshell bacterial loads was observed in all conditions, but bacterial growth was higher on the shell of incubated eggs than on non-incubated eggs. We did not find any significant difference in eggshell bacterial growth for eggs incubated by females with free or blocked access to their preen gland. In addition, fungal growth during our experiment was not affected by incubation or the mother’s preen oil. Our findings are in contrast with those of previous studies which showed that incubation limited or had no effect on eggshell bacterial growth. Differences in environmental conditions and/or species ecology may explain the difference between the results of our experiment and those of previous studies. Our study provides the first data on the effect of maternal preen oil on eggshell microorganisms, showing that preen oil does not limit eggshell microbial growth.

Keywords

Preen oil Incubation Eggshell bacteria Anas platyrhynchos 

Zusammenfassung

Ein experimenteller Test an Stockenten ( Anas platyrhynchos ) zum Effekt von Bebrütung und mütterlichem Bürzeldrüsenfett auf die Mikrobenbelastung von Eierschalen

Mikrobielle Infektionen sind ein Hauptfaktor für reduzierte Überlebensraten der ersten Lebensstadien bei oviparen Arten. Aktuelle Studien belegen, dass bei Vögeln die Eierschale eine erhebliche Vielfalt an Mikroorganismen beherbergt, die sich schnell vermehren und in die Schale eindringen können. Dies führt zu einer verringerten Schlupfrate. Hier stellen wir die Ergebnisse eines Experimentes vor, bei dem wir untersucht haben, wie Bebrütung und mütterliches Bürzeldrüsenfett das Wachstum von Mikroben auf Eierschalen von Vögeln beeinflussen. Als Modellart diente die Stockente (Anas platyrhynchos). Wir verglichen den Bakterien- und Pilzbefall der Schalen bebrüteter und nicht-bebrüteter Eier mittels Weibchen, die einen freien oder blockierten Zugriff auf ihre Bürzeldrüse hatten. Bei allen Eierschalen wurde ein Anstieg der Bakterienbelastung beobachtet, wobei das Bakterienwachstum auf Schalen bebrüteter Eier höher war als auf den Schalen unbebrüteter Eier. Hinsichtlich der Weibchen mit freiem oder blockiertem Zugriff auf ihre Bürzeldrüse konnte kein signifikanter Unterschied im Bakterienwachstum auf den Eierschalen festgestellt werden. Darüber hinaus war das Pilzwachstum während des Experimentes nicht beeinflusst durch die Bebrütung oder das Bürzeldrüsensekret des Weibchens. Unsere Ergebnisse stehen im Gegensatz zu früheren Studien, die gezeigt haben, dass die Bebrütung entweder einen limitierten oder gar keinen Effekt auf das Bakterienwachstum auf Eierschalen hatte. Unterschiede in den Umweltbedingungen und/oder der Ökologie der Arten könnten den Unterschied zwischen diesem Experiment und vorherigen Studien erklären. Die vorliegende Studie liefert die ersten Daten zum Einfluss von mütterlichem Bürzeldrüsensekret auf Mikroorganismen von Eierschalen, die zudem zeigen, dass das Bürzeldrüsensekret das mikrobielle Wachstum auf Eierschalen nicht begrenzt.

Notes

Acknowledgments

We are grateful to Erika Hartmann, Nadine and Noël Guillon and Leopold Denoufoux for their help during field and laboratory work. We also thank Edward H. Burtt, Jr. and Steven R. Beissinger for their helpful comments. This project was partly supported by a French research grant from the ANR to Philipp Heeb (ANR-05, NT05-3_42075). MG was supported by a PhD scholarship of the French Government and GAC by an EGIDE grant.

References

  1. 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 638–646Google Scholar
  2. Bisson IA, Marra PP, Burtt EH Jr, Sikaroodi M, Gillevet PM (2007) A molecular comparison of plumage and soil bacteria across biogeographic, ecological, and taxonomic scales. Microb Ecol 54:65–81PubMedCrossRefGoogle Scholar
  3. Bisson IA, Marra PP, Burtt EH Jr, Sikaroodi M, Gillevet PM (2009) Variation in plumage microbiota depends on season and migration. Microb Ecol 58:212–220PubMedCrossRefGoogle Scholar
  4. Board RG, Fuller R (eds) (1994) Microbiology of the Avian egg. Chapman and Hall, LondonGoogle Scholar
  5. Board RG, Halls NA (1973) The cuticle: a barrier to liquid and particle penetration of the shell of the hen’s egg. Br Poult Sci 14:69–97CrossRefGoogle Scholar
  6. Burtt EH Jr, Ichida JM (1999) Occurrence of feather-degrading Bacilli in the plumage of birds. Auk 116:364–372CrossRefGoogle Scholar
  7. Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, PrincetonGoogle Scholar
  8. Cook MI, Beissinger SR, Toranzos GA, Rodriguez RA, Arendt WJ (2003) Trans-shell infection by pathogenic microorganisms reduces the shelf life of non-incubated bird’s eggs: a constraint on the onset of incubation? Proc R Soc Lond B 270:2233–2240CrossRefGoogle Scholar
  9. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005a) Microbial infection affects egg viability and incubation behavior in a tropical passerine. Behav Ecol 16:30–36CrossRefGoogle Scholar
  10. Cook MI, Beissinger SR, Toranzos GA, Arendt WJ (2005b) Incubation reduces microbial growth on eggshells and the opportunity for trans-shell infection. Ecol Lett 8:532–537PubMedCrossRefGoogle Scholar
  11. Czirják GÁ, Møller AP, Mousseau TA, Heeb P (2010) Microorganisms associated with feathers of barn swallows in radioactively contaminated areas around Chernobyl. Microb Ecol 60:373–380PubMedCrossRefGoogle Scholar
  12. 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 97:1089–1095PubMedCrossRefGoogle Scholar
  13. Giraudeau M, Duval C, Guillon N, Bretagnolle V, Gutierrez C, Heeb P (2010a) Effects of access to preen gland secretions on mallard plumage. Naturwissenschaften 97:577–581PubMedCrossRefGoogle Scholar
  14. Giraudeau M, Czirják GÁ, Duval C, Bretagnolle V, Eraud C, McGraw KJ, Heeb P (2010b) Mother self maintenance and maternal reproductive investment in mallards. PLoS One 5(10):e13555PubMedCentralPubMedCrossRefGoogle Scholar
  15. Giraudeau M, Czirják GÁ, Duval C, Guillon N, Gutierrez C, Bretagnolle V, Heeb P (2010c) No detected effect of moult on feather bacterial loads in mallards. J Avian Biol 41:678–680CrossRefGoogle Scholar
  16. Jacob J (1978) Uropygial gland secretions and feather waxes. In: Florkin M, Sheer BT, Brush AH (eds) Chemical zoology X, Aves. Academic Press, New York, pp 165–211Google Scholar
  17. Kowalczyk K, Daiss J, Halpern J, Roth TF (1985) Quantification of maternal-fetal IgG transport in the chicken. Immunology 54:755–762PubMedCentralPubMedGoogle Scholar
  18. Menon GK, Menon J (2000) Avian epidermal lipids: functional considerations and relationship to feathering. Am Zool 40:540–552CrossRefGoogle Scholar
  19. Møller AP, Czirják GÁ, Heeb P (2009) Feather micro-organisms and uropygial anti-microbial defenses in a colonial passerine bird. Funct Ecol 23:1097–1102CrossRefGoogle Scholar
  20. Reneerkens J, Versteegh MA, Schneider AM, Piersma T, Burtt EH Jr (2008) Seasonally changing preen wax composition: red knots’ (Calidris canutus) flexible defense against feather-degrading bacteria? Auk 125:285–290CrossRefGoogle Scholar
  21. Ruiz-De-Castaneda R, Velab AI, González-Braojosa S, Briones V, Moreno J (2011) Drying eggs to inhibit bacteria: incubation during laying in a cavity nesting passerine. Behav Process 88:142–148CrossRefGoogle Scholar
  22. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349CrossRefGoogle Scholar
  23. Shawkey MD, Liu M, Loos E, Rowher F, Wang JM, Beissinger SR (2008) Do birds differentially deposit anti-microbial proteins in clutches of eggs? Behav Ecol 19:920–927CrossRefGoogle Scholar
  24. Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4:4522CrossRefGoogle Scholar
  25. Smit E, Leeflang P, Gommans S, van den Broek J, van Mil S, Wernars K (2001) Diversity and seasonal fluctuations of the dominant members of the bacterial soil community in a wheat field as determined by cultivation and molecular methods. Appl Environ Microbiol 67:2284–2291PubMedCentralPubMedCrossRefGoogle Scholar
  26. 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(5):1137–1145PubMedCrossRefGoogle Scholar
  27. Wellman-Labadie O, Picman J, Hincke MT (2008) Antimicrobial activity of the Anseriform outer eggshell and cuticle. Comp Biochem Physiol Part B 149:640–649CrossRefGoogle Scholar
  28. Wellman-Labadie O, Lemaire S, Mann K, Picman J, Hincke MT (2010) Antimicrobial activity of lipophilic avian eggshell surface extracts. J Agric Food Chem 58:10156–10161PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2014

Authors and Affiliations

  • M. Giraudeau
    • 1
    • 5
    Email author
  • G. Á. Czirják
    • 1
    • 2
    • 7
  • C. Duval
    • 1
    • 6
  • V. Bretagnolle
    • 3
  • C. Gutierrez
    • 4
    • 8
  • P. Heeb
    • 1
  1. 1.Laboratoire Évolution et Diversité Biologique (EDB), UMR 5174 Centre National de la Recherche Scientifique (CNRS)Université Paul Sabatier (UPS)–Ecole Nationale de Formation Agronomique (ENFA)ToulouseFrance
  2. 2.Department of Infectious Diseases, Faculty of Veterinary MedicineUniversity of Agricultural Sciences and Veterinary MedicineCluj-NapocaRomania
  3. 3.Centre d’Etudes Biologiques de Chizé CNRS UPR 1934Beauvoir-sur-NiortFrance
  4. 4.Laboratoire de Microbiologie et Génétique Moléculaire (LMGM)UMR 5100 CNRS-UPSToulouseFrance
  5. 5.Institute of Evolutionary Biology and Environmental StudiesUniversity of ZurichZurichSwitzerland
  6. 6.Centre for Ornithology, School of BiosciencesBirmingham UniversityBirminghamUK
  7. 7.Leibniz Institute for Zoo and Wildlife ResearchBerlinGermany
  8. 8.Institut de Pharmacologie et Biologie Structurale (IPBS)UMR 5089, CNRS-UPSToulouseFrance

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