Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: The yellow-legged gull Larus michahellis

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Hammouda, Abdessalem ^a   Selmi, Slaheddine ^a   Pearce Duvet, Jessica ^b   Chokri, Mohamed Ali ^a   Arnal, Audrey ^b   Gauthier Clerc, Michel ^c   Boulinier, Thierry ^b  

^a UNIVERSITY OF GABES   (Tunisia)

^b CENTRE D ECOLOGIE FONCTIONNELLE ET EVOLUTIVE   (France)

^c STATION BIOLOGIQUE DE LA TOUR DU VALAT   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MATERNAL ANTIBODY; EGG PROTEIN; VIRUS ANTIBODY;

ANTIBODY PRODUCTION; ARTICLE; CONTROLLED STUDY; EGG LAYING; EGG YOLK; ENVIRONMENTAL EXPOSURE; FEMALE; GENETIC TRAIT; HEMATOCRIT; IMMUNOCOMPETENCE; INFLUENZA VIRUS A; LARUS MICHAHELLIS; MORPHOLOGY; NONHUMAN; PASSIVE IMMUNIZATION; SEABIRD; SEX DETERMINATION; VERTICAL TRANSMISSION; ANIMAL; AVIAN INFLUENZA; CHARADRIIFORMES; IMMUNOLOGY; PHYSIOLOGY;

AVES; LARUS MICHAHELLIS; ORTHOMYXOVIRIDAE;

ANIMALS; ANTIBODIES, VIRAL; CHARADRIIFORMES; EGG PROTEINS; EGG YOLK; FEMALE; INFLUENZA A VIRUS; INFLUENZA IN BIRDS;

EID: 84860712897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0034966     Document Type: Article

References (54)

1. Dobson A, Lafferty KD, Kuris AM, Hechinger RF, Jetz W, (2008) Homage to Linnaeus: How many parasites? How many hosts? Proc Natl Acad Sci USA 105: 11482-11489.
2. Grindstaff JL, Brodie ED 3rd, Ketterson ED, (2003) Immune function across generations: integrating mechanism and evolutionary process in maternal antibody transmission. P Roy Soc Lond B Bio 270: 2309-2319.
3. Boulinier T, Staszewski V, (2008) Maternal transfer of antibodies: raising immuno-ecology issues. Trends Ecol Evol 23: 282-290.
4. Hasselquist D, Nilsson JÅ, (2009) Maternal transfer of antibodies in vertebrates: Trans-generational effects on offspring immunity. Phil Trans R Soc B 364: 51-60.
5. Klasing KC, (1998) Nutritional modulation of resistance to infectious diseases. Poult Sci 77: 1119-1125.
6. Saino N, Martinelli R, Møller AP, (2001) Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica). J Evol Biol 14: 95-109.
7. Grindstaff JL, Demas GE, Ketterson ED, (2005) Diet quality affects egg size and number but does not reduce maternal antibody transmission in Japanese quail Coturnix japonica. J Anim Ecol 74: 1051-1058.
8. 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.
9. Buechler K, Fitze PS, Gottstein B, Jacot A, Richner H, (2002) Parasite-induced maternal response in a natural bird population. J Anim Ecol 71: 247-252.
10. Blount JD, Surai PF, Nager RG, Houston DC, Møller AP, 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 B 269: 29-36.
11. Müller W, Groothuis TGG, Dijkstra C, Siitarni H, Alatalo RV, (2004) Maternal antibody transmission and breeding densities in the Black-Headed Gull Larus ridibundus. Funct Ecol 18: 719-724.
12. Slagsvold T, Sandvik J, Rofstad G, Lorentsen O, Husby M, (1984) On the adaptive value of intraclutch egg-size variation in birds. Auk 101: 687-697.
13. Schwabl H, (1993) Yolk is a source of maternal testosterone for developing birds. Proc Natl Acad Sci USA 90: 11446-11450.
14. Lipar JL, Ketterson ED, Nolan V Jr, (1999) Intra-clutch variation in testosterone content of red-winged blackbird eggs. Auk 116: 231-235.
15. Schwabl H, Mock DW, Gieg JA, (1997) A hormonal mechanism for parental favouritism. Nature 386: 231.
16. Gil D, Graves J, Hazon N, Wells A, (1999) Male attractiveness and differential testosterone investment in zebra finch eggs. Science 286: 126-128.
17. Watson PJ, Thornhill R, (1994) Fluctuating asymmetry and sexual selection. Trends Ecol Evol 9: 21-25.
18. Møller AP, Swaddle JP, (1997) Developmental Stability & Evolution. Oxford Oxford University Press.
19. Parsons PA, (1990) Fluctuating asymmetry: an epigenic measure of stress. Biol Rev 65: 131-154.
20. Fair JM, Hanssen ES, Ricklefs RE, (1999) Growth, developmental stability and immune response in juvenile Japanese quail (Coturnix coturnix japonica). Proc R Soc Lond B 266: 1735-1742.
21. Brown CR, Brown MB, (2002) Ectoparasites cause increased bilateral asymmetry of naturally selected traits in a colonial bird. J Evol Biol 15: 1067-1075.
22. Møller AP, (2006) A review of developmental instability, parasitism and disease. Infect Genet Evol 6: 133-140.
23. Amat JA, Aguilera E, Visser GH, (2007) Energetic and developmental costs of mounting an immune response in greenfinches (Carduelis chloris). Ecol Res 22: 282-287.
24. Møller AP, (1999) Condition-dependent asymmetry is fluctuating asymmetry. J Evol Biol12: 450-459.
25. Polak M, (2003) Developmental Instability: Causes and Consequences. Oxford University Press, Oxford.
26. Mateos C, Alarcos S, Carranza J, Sánchez-Prieto CB, Valencia, J, (2008) Fluctuating asymmetry of red deer antlers negatively relates to individual condition and proximity to prime age. Anim Behav 75: 1629-1640.
27. Cramp S, (1998) The Birds of the Western Palearctic on CD Rom. Oxford Oxford University Press.
28. Rubolini D, Romano M, Martinelli R, Saino N, (2006) Effects of elevated yolk testosterone levels on survival, growth and immunity of male and female yellow-legged gull chicks. Behav Ecol Sociobiol 59: 344-352.
29. Saino N, Bertacche V, Bonisoli-Alquati A, Romano M, Rubolini D, (2008) Phenotypic Correlates of Yolk and Plasma Carotenoid Concentration in Yellow-Legged Gull Chicks. Physiol Biochem Zool 81: 211-225.
30. Bosch M, Oro D, Cantos FJ, Zabala M, (2000) Short-term effects of culling on the ecology and population dynamics of the Yellow-legged Gull. J Appl Ecol 37: 369-385.
31. Vidal E, Médail F, Tatoni T, (1998) Is the Yellow-legged Gull a superabundant species in the Mediterranean? Impact on fauna and flora, conservation measures and research priorities. Biodivers Conserv 7: 1013-1026.
32. Oro D, Martinez-Abrain A, (2007) Deconstructing myths on large gulls and their impact on threatened sympatric waterbirds. Anim Conserv 10: 117-126.
33. Cramp S, Simmons KEL, (1983) Handbook of the Birds of Europe, the Middle East and North Africa: The Birds of the Western Palearctic, Volume III. Oxford Oxford University Press.
34. Isenmann P, Gaultier T, Hili A, Azafzaf H, Dlensi H, et al. (2005) Oiseaux de Tunisie. Paris Société d'Études Ornithologiques de France.
35. Potti J, Moreno J, Merino S, Frias O, Rodriguez R, (1999) Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120: 1-8.
36. Hoi-Leitner M, Romero-Pujante M, Hoi H, Pavlova A, (2001) Food availability and immune capacity in serin (Serinus serinus) nestlings. Behav Ecol Sociobiol 49: 333-339.
37. Griffiths R, Double MC, Orr K, Dawson RJG, (1998) A DNA test to sex most birds. Mol Ecol 7: 1071-1075.
38. Fridolfsson AK, Ellegren H, (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30: 116-121.
39. Mohammed HO, Yamamoto R, Carpenter TE, Ortmayer HB, (1986) Comparison of egg yolk and serum for the detection of Mycoplasma gallisepticum and M. synoviae antibodies by enzyme-linked immunosorbent assays. Avian Dis 30: 398-408.
40. 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. P Roy Soc Lond B 268: 647-650.
41. Palmer AR, (1994) Fluctuating asymmetry analyses: A primer. Markow TA, ed Developmental stability its Origins and Evolutionary Implications. Dordrecht: Kluwer Academic Publishers pp. 335-364.
42. Harris MP, (1964) Aspects of the breeding biology of the gulls Larus argentatus, L. fuscus and L. marinus. Ibis 106: 432-456.
43. Bolton M, Monaghan P, Houston DC, (1993) Proximate determination of clutch size in lesser black-backed gulls: the roles of food supply and body condition. Can J Zool 71: 273-279.
44. SAS Statistical Institute (1998) SAS/STAT user's guide, version 8. Cary SAS Statistical Institute.
45. Balmford A, Jones IL, Thomas ALR, (1993) On avian asymmetry: evidence of natural selection for symmetrical tails and wings in birds. Proc R Soc Lond B. 252: 245-251.
46. Thomas ALR, (1993) The aerodynamic costs of asymmetry in the wings and tails of birds: asymmetric birds can't fly round tight corners. Proc R Soc Lond B 254: 181-189.
47. Read AF, Allen JA, (2000) The economics of immunity. Science 290: 1104-1105.
48. Pihlaja M, Siitari H, Alatalo RV, (2006) Maternal antibodies in a wild altricial bird: effects on offspring immunity, growth and survival. J Anim Ecol 75: 1154-1164.
49. Gasparini J, McCoy KD, Tveraa T, Boulinier T, (2002) Related concentrations of specific immunoglobulins against the Lyme disease agent Borrelia burgdorferi sensu lato in eggs, young and adults of the kittiwake (Rissa tridactyla). Ecol Lett 5: 519-524.
50. Klasing KC, Leshchinsky TV, (1999) Function, costs and benefits of the immune system during development and growth. Adams NJ & Slotow RH, eds Proceedings of the 22nd International Ornithology Congress Durban. Johannesburg Bird Life pp. 2817-2835.
51. Grindstaff JL, (2008) Maternal antibodies reduce costs of an immune response during development. J Exp Biol 211: 654-660.
52. Heeb P, Werner I, Kölliker M, Richner H, (1998) Benefits of induced host responses against an ectoparasite. Proc R Soc B 265: 51-56.
53. Sahin O, Luo ND, Huang SX, Zhang QJ, (2003) Effect of Campylobacter-specific maternal antibodies on Campylobacter jejuni colonization in young chickens. Appl Environ Microbiol 69: 5372-5379.
54. Sydeman WJ, Penniman JF, Penniman TM, Pyle P, Ainley DG, (1991) Breeding performance in the Western gull-Effects of parental age, timing of breeding and year in relation to food availability. J Anim Ecol 60: 135-149.