Mechanisms of antimicrobial defense in avian eggs

Journal of Ornithology

Volumn 156, Issue , 2015, Pages 399-408

  D’Alba, Liliana ^a   Shawkey, Matthew D ^a  

^a UNIVERSITY OF AKRON   (United States)

Author keywords

Antimicrobial defense; Eggshell; Incubation; Infection

Indexed keywords

AVES;

EID: 85067614776     PISSN: 21937192     EISSN: 21937206     Source Type: Journal    
DOI: 10.1007/s10336-015-1226-1     Document Type: Review

References (123)

1. Afton AD, Paulus SL (1992) Incubation and brood care. In: Batt B, Afton A, Anderson M (eds) Ecology and management of breeding waterfowl. University of Minnesota Press, Minneapolis, pp 62–108
2. Amann RI, Ludwig W, Schleifer KH (1995) Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59:143–169
3. Baron F, Jan S, Nys Y, Bain M, Immerseel FV (2011) Egg and egg product microbiology. In: Nys Y, Bain M, Van Immerseel F (eds) Improving the safety and quality of eggs and egg products Vol 1: Egg chemistry, production and consumption. Woodhead Publishing, Cambridge, pp 330–350
4. Baxter M, Trotter MD (1969) The effect of fatty acids extracted from keratins on the growth of fungi, with particular reference to the free fatty acid content. Sabouraudia 7:199–206
5. Berger S, Disko R, Gwinner H (2003) Bacteria in starling nests. J Ornithol 144:317–322
6. Berrang ME, Cox NA, Frank JF, Buhr RJ (1999) Bacterial penetration of the eggshell and shell membranes of the chicken hatching egg: a review. J App Poultry Res 8:499–504
7. Board RG, Tranter HS (1995) The microbiology of eggs. In: Stadelman WJ, Cotterill OJ (eds) Egg Science and Technology. 4th edn. Binghamton, Food Products, pp 81–104
8. Board R et al. (1982) A novel pore system in the eggshells of the mallee fowl, Leipoa ocellata. J Exp Zool. 220
9. Bain Panheleux M, Fernandez M, Morales S, Gautron I, Arias J, Solomon JL, Hincke S, Nys MY (1999) Organic matrix composition and ultrastructure of eggshell: a comparative study. Br Poult Sci 40:240–252
10. Board RG (1966) Review article: the course of microbial infection of the hen’s egg. J of App Bacteriol 29(2):319–341
11. Board RG (1980) The avian eggshell—a resistance network. J of App Bacteriol 48:303–303 (I3)
12. Board RG (1982) Properties of avian egg shells and their adaptive value. Biol Rev 57:1–28
13. Board RG, Ayres JC (1965) Influence of iron on the course of bacterial infection of the hen’s egg. Appl Microbiol 13:358–364
14. Board RG, Fuller R (1974) Non-specific antimicrobial defences of the avian egg, embryo and neonate. BioI Rev 49:15–49
15. Board RG, Fuller R (1994) Microbiology of the avian egg. Chapman and Hall, London
16. Board RG, Hornsey DJ (1978) Plasma and Egg white proteins In: Brush AH (ed) Chemical zoology Academic Press, New York 10:53–67
17. Board RG, Loseby S, Miles VR (1979) A note on microbial growth on hen egg-shells. Br Poultry Sci 20:413–420
18. Board RG, Clay C, Lock J, Dolman J (1994) The egg: a compartmentalized, aseptically packaged food In microbiology of the avian egg. Springer, US, pp 43–61
19. Bonisoli-Alquati A et al (2010) Egg antimicrobials, embryo sex and chick phenotype in the yellow-legged gull. Behav Ecol Sociobiol 64:845–855
20. Brandl HB, van Dongen WF, Darolová A, Krištofík J, Majtan J, Hoi H (2014) Composition of bacterial assemblages in different components of reed warbler nests and a possible role of egg incubation in pathogen regulation. PLoS One 9(12):e114861
21. Brooks J, Taylor DJ (1955) Eggs and egg products department of science and industrial research food investigation special report. Her Majesty’s Stationery Office, London
22. Brouwer L, Komdeur J (2004) Green nesting material has a function in mate attraction in the European starling. Anim Behav 67:539–548
23. Bruce J, Drysdale EM (1991) Egg hygiene: routes of infection. In: Tullett SG (ed) Avian incubation. Butterworth Heinemann, Northampton, pp 257–276
24. Bruce J, Drysdale EM (1994) Trans-shell transmission. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Chapman and Hall, London, pp 63–91
25. Chattock AP (1925) On the physics of incubation Phil Trans Roy Soc London. Ser B 213:397–450
26. Clark L (1991) The nest protection hypothesis: the adaptive use of plant secondary compounds by European starlings. In: Loye JE, Zuk M (eds) Bird–parasite interactions: ecology, evolution and behavior. Oxford University Press, Oxford, pp 205–221
27. Clark L, Mason JR (1985) Use of nest material as insecticidal and anti- pathogenic agents by the European starling. Oecologia 67:169–176
28. 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 Biol Sci 270:2233–2240
29. 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
30. 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
31. Cooper J (1986) Biology of the bank cormorant, part 4: nest construction and characteristics. Ostrich 57(3):170–179
32. Cox NA, Berrang ME, Cason JA (2000) Salmonella penetration of egg shells and proliferation in broiler hatching eggs: a review. Poultry Sci 79:1571–1574
33. Cox NA, Stern NJ, Musgrove MT, Bailey JS, Craven SE, Cray PF, Buhr RJ, Hiett KL (2002) Prevalence and level of Campylobacter in commercial broiler breeders (parents) and broilers. J App Poultry Res. 11:187–190
34. Cramp S (1998) Cramp’s the complete birds of the Western Palearctic. Oxford University Press, Oxford
35. D’Alba L et al (2010a) Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness. Behav Ecol Sociobiol 64(6):1037–1045
36. D’Alba L, Oborn A, Shawkey M (2010b) Experimental evidence that keeping eggs dry is a mechanism for the antimicrobial effects of avian incubation. Naturwissenschaften 97:1–7
37. D’Alba L, Spencer KA, Nager RG, Monaghan P (2011) State dependent effects of elevated hormone: nest site quality, corticosterone levels and reproductive performance in the common eider. Gen Comp Endocrinol 172:218–224
38. D’Alba L et al (2014) Antimicrobial properties of a nanostructured eggshell from a compost-nesting bird. J Exp Biol 217(7):1116–1121
39. Davies JW, Anderson RC, Karstad L, Trainer DO (1971) Infectious and parasitic diseases of wild birds. Iowa State University Press, Ames
40. del Hoyo J, Elliott A, Sargatal AJ (1994) Handbook of the birds of the world vol 2: new world vultures to guineafowl. Lynx Edicions, Barcelona
41. Drent RH (1975) Incubation. In: Farner DS, King JR (eds) Avian biology, vol 5. Academic Press, NY, pp 333–420
42. Dubiec A, Góźdź I, Mazgajski TD (2013) Green plant material in avian nests Avian. Biol Res 6:133–146
43. Eckert J, Glock H, Schade R et al (1986) Synthesis of a precursor polypeptide of eggshell matrix in the liver of laying hen. J Anim Physiol Anim Nutr 56:258–265
44. Jacob J, Eigener, U and Hoppe, U 1997 The structure of preen gland waxes from pelecaniform birds containing 3,7-dimethyloctan-1-ol. An active ingredient against dermatophytes, Zeit Naturforsch C 52: 114/123
45. Elder W (1954) The oil gland of birds Wilson Bull 66(1):6–31
46. Franz CM, Van Belkum MJ, Holzapfel WH, Abriouel H, Gálvez A (2007) Diversity of enterococcal bacteriocins and their grouping in a new classification scheme. FEMS Microbiol Rev 31:293–310
47. Giraudeau M, Duval C, Czirják GÁ, BretagnolleV Eraud C, McGraw KJ, Heeb P (2011) Maternal investment of female mallards is influenced by male carotenoid-based coloration. Proc R Soc B 278:781–788
48. Giraudeau M, Czirják GÁ, Duval C, Bretagnolle V, Gutierrez C, Heeb P (2014) An experimental test in Mallards (Anas platyrhynchos) of the effect of incubation and maternal preen oil on eggshell microbial load. J Ornithol 155:671–677
49. Godard R et al (2007) The effects of exposure and microbes on hatchability of eggs in open-cup and cavity nests. J Avian Biol 38:709–716
50. Goodenough AE, Stallwood B (2010) Intraspecific variation and interspecific differences in the bacterial and fungal assemblages of Blue tit (Cyanistes caeruleus) and Great tit (Parus major) nests. Microb Ecol 59:221–232
51. Graves R, MacLaury D (1962) The effect of temperature, vapour pressure, and absolute humidity on bacteria contamination of shell eggs. Poultry Sci. 41:1219–1225
52. Grizard S, Dini-Andreote F, Tieleman BI, Salles JF (2014) Dynamics of bacterial and fungal communities associated with eggshells during incubation. Ecol Evol 4(7):1140–1157
53. Gwinner H (1997) The function of green plants in nests of European starlings (Sturnus vulgaris). Behaviour 134:337–351
54. Gwinner H, Berger S (2005) European starlings: nestling condition, parasites and green nest material during the breeding season. J Ornithol 146:365–371
55. Gwinner H, Oltrogge M, Trost L, Nienaber U (2000) Green plants in starling nests: effects on nestlings. Anim Behav 59:301–309
56. Hansell M (2000) Bird nests and construction behaviour. Cambridge University Press, Cambridge, p 2000
57. Hincke M, Gautron J, Nys Y, Rodriguez-Navarro AB, McKee MD, Bain M, van Immerseel F (2011) The eggshell: structure and protective function. In: Nys Y, Bain M, Van Immerseel F (eds) Improving the safety and quality of eggs and egg products Volume 1: Egg chemistry, production and consumption. Woodhead Publishing, Cambridge, pp 151–182
58. Horrocks NP et al (2014) Are antimicrobial defences in bird eggs related to climatic conditions associated with risk of trans-shell microbial infection? Front Zool 11:49
59. Hubalek Z (1978) Coincidence of fungal species with birds. Ecology 59:438–442
60. Gautron J, Hincke MT, Garcia-Ruiz JM, Dominguez J, Nys Y (1997) Ovotransferrin and lysozyme are constituent in eggshell matrix. In: Proceedings VII European symposium, Pozhaus, Poland, pp 66–75
61. Gautron J, Réhault-Godbert S, Nys Y, Mann K, Righetti PG, Bain M, Immerseel FV (2011) Use of high-throughput technology to identify new egg components. In: Nys Y, Bain M, Van Immerseel F (eds) Improving the safety and quality of eggs and egg products Volume 1: Egg chemistry, production and consumption. Woodhead Publishing, Cambridge, pp 133–150
62. Jacob J, Schoffeniels E, Balthazart J (1979) Sex differences in the chemical composition of uropygial gland waxes in domestic ducks. Biochem Syst Ecol 7:149–153
63. Jacob J, Zisweiler V (1982) The uropygial gland. In: Farner DS, King JR, Parkes KC (eds) Avian Biology, Vol 6. Academic, New York, pp 199–314
64. Javŭrková V, Albrecht T, Mrázek J, Kreisinger J (2014) Effect of intermittent incubation and clutch covering on the probability of bacterial trans-shell infection. Ibis 156:374–386
65. Jones D (1988) Hatching success of the Australian brush-turkey Alectura lathami in south-east Queensland. Emu 88(4):260–262
66. Kim JW, Slavik MF (1996) Changes in eggshell surface microstructure after washing with cetylpyridinium chloride or trisodium phosphate. J Food Protect 59:859–863
67. Krištofík J, Darolová A, Majtan J, Okuliarová M, Zeman M, Hoi H (2014) Do females invest more into eggs when males sing more attractively? Postmating sexual selection strategies in a monogamous reed passerine. Ecol Evol 4:1328–1339
68. Lafuma L, Lambrechts MM, Raymond M (2001) Aromatic plants in bird nests as a protection against blood-sucking flying insects? Behav Processes 56:113–120
69. Law-Brown J, Meyers PR (2003) Enterococcus phoeniculicola sp. nov., a novel member of the enterococci isolated from the uropygial gland of the red-billed Woodhoopoe, Phoeniculus purpureus Int J Syst Evol Microbiol 53:683–685
70. Lee WY, Kim M, Jablonski PG, Choe JC, Lee SL (2014) Effect of incubation on bacterial communities of eggshells in a temperate bird, the Eurasian magpie (Pica pica). PLoS One 9(8):e103959
71. Li-Chan EC, Kim HO (2008) Structure and chemical composition of eggs. In: Mine Y (ed) Egg bioscience and biotechnology. Wiley, New Jersey, pp 1–96
72. Lomholt JP (1976) Relationship of weight loss to ambient humidity of bird eggs during incubation. J Comp Physiol 105:189–196
73. Lorenz FW, Starr PB, Starr MP, Ogasawara FX (1952) The development of Pseudomonas spoilage in shell eggs penetration through the shell. J Food Sci 17:351–360
74. Madigan MT, Martinko JM, Dunlap PV, Clark DP (2005) Brock biology of microorganisms. Benjamin Cummings, New York
75. Mann K (2007) The chicken egg white proteome. Proteomics 7:3558–3568
76. Mann K, Maček B, Olsen JV. Proteomic analysis of the acid-soluble organic matrix of the chicken calcified eggshell layer. 2006;6:3801–10
77. Martin TE (1995) Avian life history evolution in relation to nest sites, nest predation, and food. Ecol Monogr 65:101–127
78. Martín-Platero AM, Valdivia E, Ruíz-Rodríguez M et al (2006) Characterization of antimicrobial substances produced by Enterococcus faecalis MRR 10-3, isolated from the uropygial gland of the hoopoe Upupa epops. Appl Environ Microbiol 72:4245–4249
79. Martín-Vivaldi M et al (2014) Special structures of hoopoe eggshells enhance the adhesion of symbiont-carrying uropygial secretion that increase hatching success. J Anim Ecol 83(6):1289–1301
80. McComb WC, Noble RE (1981) Microclimates of nest boxes and natural cavities in bottomland hardwoods. J Wildl Manage 45:284–289
81. McDougall P, Milne H (1978) The anti-predator function of defecation on their own eggs by female Eiders. Wildfowl. 29:29
82. Mennerat A, Perret P, Lambrechts MM (2009a) Local individual preferences for nest materials in a passerine bird. Plos One 4:e5104
83. Mennerat A, Perret P, Bourgault P, Blondel J, Gimenez O, Thomas WD, Heeb P, Lambrechts MM (2009b) Aromatic plants in nests of blue tits: positive effects on nestlings. Anim Behav 77:569–574
84. Menon CK, Menon J (2000) Avian epidermal lipids: functional considerations and relationship to feathering. Am Zool 40:540–552
85. Mikhailov KE (1997) Avian eggshells: an atlas of scanning electron micrographs. British Ornithologists’ Club, London
86. Mills TK, Lombardo MP, Thorpe PA (1999) Microbial colonization of the cloacae of nestling tree swallows. Auk 116:947–956
87. Mine Y, Oberle C, Kassaify Z (2003) Eggshell matrix proteins as defense mechanism of avian eggs. J Agri Food Chem 51:249–253
88. Morosinotto C, Ruuskanen S, Thomson RL, Siitari H, Korpimäki E, Laaksonen T (2013) Predation risk affects the levels of maternal immune factors in avian eggs. J Avian Biol 44:427–436
89. Nelson B (1978) The Sulidae: Gannets and Boobies. Oxford University Press, Oxford
90. Packard G, Packard M (1980) Evolution of the cleidoic egg among reptilian antecedents of birds. Integr Comp Biol 20:351
91. Padron M (1990) Salmonella typhimurium penetration through the eggshell of hatching eggs. Avian Dis 34:463–465
92. Peralta-Sanchez JM, Møller AP, Martin-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
93. Peralta-Sánchez JM et al (2012) Avian life history traits influence eggshell bacterial loads: a comparative analysis. Ibis 154:725–737
94. 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
95. Pinowski J, Barkowska M, Kruszewicz AH, Kruszewicz AG (1994) The causes of the mortality of eggs and nestlings of Passer sp. J Biosci 19:441–451
96. Pires AB, Belo FA, Rabaça EJ (2012) Aromatic plants in Eurasian Blue Tit nests: the ‘nest protection hypothesis’ revisited. Wilson J Ornithol 124:162–165
97. Rahn H, Ackerman R, Paganelli C (1977) Humidity in the avian nest and egg water loss during incubation. Physiol Zool 50:269–283
98. Rehault-Godbert S, Herve-Grepinet V, Gautron J, Cabau C, Nys Y, Hincke M (2011) Molecules involved in chemical defence of the chicken egg. In: Nys Y, Bain M, Van Immerseel F (eds) Improving the safety and quality of eggs and egg products volume 1: egg chemistry, production and consumption. Woodhead Publishing, Cambridge, pp 183–208
99. Ricklefs RE (1969) An analysis of nesting mortality in birds. Smith Contr Zool 9:1–48
100. Rose M, Hincke MT (2009) Protein constituents of the eggshell: eggshell-specific matrix proteins. Cell Molec Life Sci 66:2707–2719
101. Ruiz-de-Castañeda R, Vela AI, Lobato E, Briones V, Moreno J (2011) Bacterial loads on eggshells of the pied flycatcher: environmental and maternal factors. Condor 113:200–208
102. Martín-Vivaldi M, Peña A, Peralta-Sánchez JM, Sánchez L, Ananou S, Ruiz-Rodríguez M, Soler JJ (2010) Antimicrobial chemicals in hoopoe preen secretions are produced by symbiotic bacteria. Proc Biol Soc 277:123–130
103. Ruiz-Rodríguez M, Valdivia E, Soler JJ, Martín-Vivaldi M, Martin-Platero AM, Martínez-Bueno M (2009) Symbiotic bacteria living in the hoopoe’s uropygial gland prevent feather degradation. J Exp Biol 212:3621–3626
104. Ruiz-Rodríguez M, Tomás G, Martín-Gálvez D, Ruiz-Castellano C, Soler JJ. (2014) Bacteria and the evolution of honest signals. The case of ornamental throat feathers in spotless starlings. Funct Ecol. doi:10.1111/1365-2435.12376
105. Saino N, Dall’ara P, Martinelli R, Moller 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
106. Shawkey MD, Pillai SR, Hill GE (2003) Chemical warfare? Effects of uropygial oil on feather-degrading bacteria. J Avian Biol 34:345–349
107. Shawkey M, Kosciuch K, Liu M, Rohwer F, Loos E, Wang J, Beissinger S (2008) Do birds differentially distribute antimicrobial proteins within clutches of eggs? Behav Ecol 19:920–927
108. Shawkey MD, Firestone MK, Brodie EL, Beissinger SR (2009) Avian incubation inhibits growth and diversification of bacterial assemblages on eggs. PLoS One 4:e4522
109. Singleton DR, Harper RG (1998) Bacteria in old house wren nests. J Field Ornithol 69:71–74
110. Soler JJ et al (2008) Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Funct Ecol 22:864–871
111. 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 J3:93–100
112. Sparks NHC (1994) Shell accessory materials: structure and function. In: Board RG, Fuller R (eds) Microbiology of the avian egg. Springer, USA, pp 25–42
113. Sparks NHC, Board RG (1984) Cuticle, shell porosity and water uptake through hens’ eggshells. Br Poult Sci 25:267–276
114. Stein LR, Badyaev AV (2011) Evolution of eggshell structure during rapid range expansion in a passerine bird. Funct Ecol 25:1215–1222
115. Booth DT, Thompson MB (1991) A comparison of reptilian eggs with those of megapode birds. In: Deeming DC et al. (eds.) Egg incubation: its effects on embryonic development in birds and reptiles. Cambridge University Press, Cambridge, pp 325–344
116. Veiga PJ, Polo V, Viñuela J (2006) Nest green plants as a male status signal and courtship display in the spotless starling. Ethology 112:196–204
117. Vincze O, Vágási CI, Kovács I, Galván I, Pap PL (2013) Sources of variation in uropygial gland size in European birds. Biol J Linnean Soc 110:543–563
118. Walls JG, Hepp GR Eckhardt LG (2011) Effects of incubation delay on viability and microbial growth of Wood Duck (Aix sponsa) eggs. Auk 128:663–670
119. Walsberg GE (1980) The gaseous microclimate of the avian nest during incubation. Am Zool 20:363–372
120. Wang J, Firestone M, Beissinger S (2011) Microbial and environmental effects on avian egg viability: do tropical mechanisms act in a temperate environment? Ecology 92:1137–1145
121. Webb DR (1987) Thermal tolerance of avian embryos: a review. Condor 89:874–898
122. Wedral EM, Vadehra DU, Baker RC (1974) Chemical composition of the cuticle and inner and outer memebranes from eggs of Gallus gallus. Comp Biochem Physiol 47B:231–240
123. Wellman-Labadie O, Picman J, Hincke M (2008) Antimicrobial activity of the Anseriform outer eggshell and cuticle. Comp Biochem Phys B Biochem Mol Biol 149:640–649