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Journal of Ornithology

, Volume 157, Issue 1, pp 303–310 | Cite as

Maternal influence on eggshell maculation: implications for cryptic camouflaged eggs

  • Camille Duval
  • Phillip Cassey
  • P. George Lovell
  • Ivan Mikšík
  • S. James Reynolds
  • Karen A. Spencer
Original Article

Abstract

Egg camouflage may explain the adaptive significance of avian eggshell pigmentation in ground-nesting species. Eggshell maculation (spots) is predominantly due to protoporphyrin, but both biliverdin (antioxidant) and protoporphyrin (pro-oxidant) may be present in spotted eggshells. Because of their role in oxidative stress, the deposition of eggshell pigments might be condition-dependent. However, because of the fitness benefits of eggshell coloration, cryptic eggshell appearance should be strongly conserved in ground-nesting species regardless of female condition and eggshell pigment concentrations. We investigated whether Japanese quails (Coturnix coturnix japonica) maintained eggshell maculation under food restriction. We quantified eggshell maculation (i.e., percentage of spot coverage) using digital photography, and both protoporphyrin and biliverdin concentrations of eggs laid by females either on a food-restricted or an ad libitum diet. Females on a high quality diet, which are known to decrease the deposition of eggshell protoporphyrin, decreased eggshell maculation compared with food-restricted females that maintained it. For the first time, we propose an experimental study which suggests that eggshell maculation depends on female body condition and that manipulating eggshell maculation may be the strategy used by females to potentially optimize egg camouflage.

Keywords

Body condition Camouflage Coturnix coturnix japonica Eggshell maculation Protoporphyrin 

Zusammenfassung

Maternaler Einfluss auf die Befleckung der Eierschale: Folgen für kryptische getarnte Eier

Die Tarnung von Eiern könnte die adaptive Bedeutung der Pigmentierung der Eierschale bodenbrütender Vögel erklären. Die Befleckung der Eierschale ist hauptsächlich auf Protoporphyrin zurückzuführen, aber sowohl Biliverdin (ein Antioxidant) als auch Protoporphyrin (ein Prooxidant) können in gefleckten Eierschalen enthalten sein. Aufgrund der Rolle von Eierschalenpigmenten bei oxidativem Stress könnte ihre Einlagerung in die Eierschale konditionsabhängig sein. Aufgrund der Fitnessvorteile einer Färbung der Eierschale sollte ein kryptisches Aussehen der Eier bei Bodenbrütern jedoch hochkonserviert sein, unabhängig von der Kondition der Weibchen und der Konzentration der Eierschalenpigmente. Wir haben untersucht, ob Japanwachteln (Coturnix coturnix japonica) die Befleckung ihrer Eierschale bei Futterknappheit beibehielten. Wir haben die Eierschalenbefleckung (d.h. den Anteil der Abdeckung mit Flecken) mit Hilfe digitaler Fotografie quantifiziert sowie die Protoporphyrin- und Biliverdin-Konzentrationen der Eier von Weibchen ermittelt, die entweder eingeschränkt oder ad libitum Futter erhielten. Weibchen mit hochwertiger Kost, die bekannterweise die Einlagerung von Protoporphyrin in die Eierschale reduzieren, reduzierten die Befleckung der Eierschale im Vergleich zu Weibchen mit eingeschränkter Kost, welche sie beibehielten. Zum ersten Mal liefern wir eine experimentelle Studie ab, die darauf hindeutet, dass die Befleckung der Eierschale von der Kondition des Weibchens abhängt und dass Weibchen die Befleckung der Eierschale beeinflussen könnten, als Strategie, um die Tarnung der Eier potenziell zu optimieren.

Notes

Acknowledgments

We thank Carole Chestnut and Malcolm McColl from Cochno Farm (Glasgow) for their help with animal husbandry. Funding was provided by the Human Frontier Science Program (RGY0069 to PC), a Birmingham University Teaching Assistantship (to CD) and a Biotechnology and Biological Sciences Research Council (BBSRC) David Phillips Fellowship (BBE024459, to KAS). PC is an Australian Research Council (ARC) Future Fellow (FT0991420).

Compliance with ethical standards

All of the procedures were agreed by the local ethics committee at the University of Glasgow and the experiment was conducted under the Animals (Scientific Procedures) Act 1986 (under PIL 30/8939 held by CD and PPL 60/4068 held by KAS).

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

10336_2015_1278_MOESM1_ESM.xls (38 kb)
Supplementary material 1 (XLS 38 kb)

References

  1. Amat JA, Fraga RM, Arroyo GM (2001) Intraclutch egg-size variation and offspring survival in the Kentish Plover Charadrius alexandrinus. Ibis 143:17–23CrossRefGoogle Scholar
  2. Arnold TW (1991) Intraclutch variation in egg size of American Coots. Condor:19–27Google Scholar
  3. Bernardo J (1996) The particular maternal effect of propagule size, especially egg size: patterns, models, quality of evidence and interpretations. Am Zool 36:216–236CrossRefGoogle Scholar
  4. Birkhead T, Nettleship D (1982) The adaptive significance of egg size and laying date in Thick-billed Murres Uria lomvia. Ecology:300–306Google Scholar
  5. Board R (1980) The avian eggshell—a resistance network. J Appl Bacteriol 48:303–313CrossRefGoogle Scholar
  6. Board R, Halls N (1973) Water uptake by eggs of mallards and guinea fowl. Br Poult Sci 14(3):311–314. doi: 10.1080/00071667308416033 CrossRefGoogle Scholar
  7. Brulez K, Cassey P, Meeson A, Mikšík I, Webber SL, Gosler AG, Reynolds SJ (2014) Eggshell spot scoring methods cannot be used as a reliable proxy to determine pigment quantity. J Avian Biol 45:94–102CrossRefGoogle Scholar
  8. Butcher GD, Miles RD (2011) Factors causing poor pigmentation of brown-shelled eggs. http://edis.ifas.ufl.edu/VM047
  9. Cassey P, Maurer G, Lovell PG, Hanley D (2011) Conspicuous eggs and colourful hypotheses: testing the role of multiple influences on avian eggshell appearance. Avian Biol Res 4:185–195CrossRefGoogle Scholar
  10. Cassey P, Hauber ME, Maurer G, Ewen JG (2012a) Sources of variation in reflectance spectrophotometric data: a quantitative analysis using avian eggshell colours. Methods Ecol Evol 3:450–456CrossRefGoogle Scholar
  11. Cassey P et al (2012b) Why are birds eggs colourful? Eggshell pigments co-vary with life-history and nesting ecology among British breeding non-passerine birds. Biol J Linn Soc 106:657–672CrossRefGoogle Scholar
  12. Castilla AM, Herrel A, Díaz G, Francesch A (2007) Developmental stage affects eggshell-breaking strength in two ground-nesting birds: the partridge (Alectoris rufa) and the quail (Coturnix japonica). J Exp Zool Part A Ecol Genetics Physiol 307:471–477CrossRefGoogle Scholar
  13. Collias NE, Collias EC (2014) Nest building and bird behavior. Princeton University Press, USAGoogle Scholar
  14. Costantini D (2010) Complex trade-offs in the pigeon (Columba livia): egg antioxidant capacity and female serum oxidative status in relation to diet quality. J Comp Physiol B Biochem Syst Environ physiol 180:731–739. doi: 10.1007/s00360-010-0456-z CrossRefGoogle Scholar
  15. Cuthill IC, Stevens M, Sheppard J, Maddocks T, Párraga CA, Troscianko TS (2005) Disruptive coloration and background pattern matching. Nature 434:72–74PubMedCrossRefGoogle Scholar
  16. De Coster G, De Neve L, Lens L (2012) Intraclutch variation in avian eggshell pigmentation: the anaemia hypothesis. Oecologia 170:297–304PubMedCrossRefGoogle Scholar
  17. De Coster G, De Neve L, Lens L (2013) Intra-clutch variation in avian eggshell pigmentation covaries with female quality. J Ornithol 154:1057–1065CrossRefGoogle Scholar
  18. Duval C, Cassey P, Desaivre S, Reynolds S, Spencer K (2012) On the use of commercial quails as study organisms: lessons about food intake from individual variation in body mass. Avian Biol Res 5:137–141CrossRefGoogle Scholar
  19. Duval C, Cassey P, Mikšík I, Reynolds SJ, Spencer KA (2013) Condition-dependent strategies of eggshell pigmentation: an experimental study of Japanese quail (Coturnix coturnix japonica). J Exp Biol 216:700–708PubMedCrossRefGoogle Scholar
  20. Giordano M, Costantini D, Pick JL, Tschirren B (2015) Female oxidative status, egg antioxidant protection and eggshell pigmentation: a supplemental feeding experiment in great tits. Behav Ecol Sociobiol 69:777–785CrossRefGoogle Scholar
  21. Gosler AG, Barnett PR, Reynolds SJ (2000) Inheritance and variation in eggshell patterning in the great tit Parus major. Proc Biol Sci R Soc 267:2469–2473. doi: 10.1098/rspb.2000.1307 CrossRefGoogle Scholar
  22. Gosler AG, Higham JP, Reynolds SJ (2005) Why are birds eggs speckled? Ecol Lett 8:1105–1113. doi: 10.1111/j.1461-0248.2005.00816.x CrossRefGoogle Scholar
  23. Götmark F (1992) Blue eggs do not reduce nest predation in the song thrush. Turdus philomelos Behav Ecol Sociobiol 30:245–252CrossRefGoogle Scholar
  24. Handrich Y (1989) Incubation water loss in king penguin egg. I. Change in egg and brood pouch parameters. Physiol Zool:96–118Google Scholar
  25. Hill WL (1993) Importance of prenatal nutrition to the development of a precocial chick. Dev Psychobiol 26:237–249PubMedCrossRefGoogle Scholar
  26. Holm S (1979) A simple sequentially rejective multiple test procedure. Scandinavian J Statistics:65–70Google Scholar
  27. Holveck M-J, Grégoire A, Staszewski V, Guerreiro R, Perret P, Boulinier T, Doutrelant C (2012) Eggshell spottiness reflects maternally transferred antibodies in blue tits. PloS one 7:e50389PubMedPubMedCentralCrossRefGoogle Scholar
  28. Kilner R (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406PubMedCrossRefGoogle Scholar
  29. Lessells C, Boag PT (1987) Unrepeatable repeatabilities: a common mistake. Auk:116–121Google Scholar
  30. López-de-Hierro MDG, Moreno-Rueda G (2010) Egg-spot pattern rather than egg colour affects conspecific egg rejection in the house sparrow (Passer domesticus). Behav Ecol Sociobiol 64:317–324CrossRefGoogle Scholar
  31. Lovell PG, Tolhurst DJ, Párraga CA, Troscianko J, Troscianko T, Baddeley R, Leonards U (2005) Stability of the color-opponent signals under changes of illuminant in natural scenes. J Opt Soc Am A 22(10):2060–2071CrossRefGoogle Scholar
  32. Lovell PG, Ruxton GD, Langridge KV, Spencer KA (2013) Egg-laying substrate selection for optimal camouflage by quail. Curr Biol 23:260–264PubMedCrossRefGoogle Scholar
  33. Loyau A, Saint Jalme M, Mauget R, Sorci G (2007) Male sexual attractiveness affects the investment of maternal resources into the eggs in peafowl (Pavo cristatus). Behav Ecol Sociobiol 61:1043–1052CrossRefGoogle Scholar
  34. Mägi M, Mänd R, Konovalov A, Tilgar V, Reynolds S (2012) Testing the structural–function hypothesis of eggshell maculation in the Great Tit: an experimental approach. J Ornithol 153:645–652CrossRefGoogle Scholar
  35. Martínez-de la Puente J et al (2007) Are eggshell spottiness and colour indicators of health and condition in blue tits Cyanistes caeruleus? J Avian Biol 38:377–384CrossRefGoogle Scholar
  36. Martínez-Padilla J, Dixon H, Vergara P, Pérez-Rodríguez L, Fargallo JA (2010) Does egg colouration reflect male condition in birds? Naturwissenschaften 97:469–477PubMedCrossRefGoogle Scholar
  37. Maurer G, Portugal SJ, Cassey P (2011) Review: an embryo’s eye view of avian eggshell pigmentation. J Avian Biol 42:494–504CrossRefGoogle Scholar
  38. Mazuc J, Chastel O, Sorci G (2003) No evidence for differential maternal allocation to offspring in the house sparrow (Passer domesticus). Behav Ecol 14:340–346CrossRefGoogle Scholar
  39. McDonagh AF (2001) Turning green to gold. Nat Struct Mol Biol 8:198–200CrossRefGoogle Scholar
  40. McGraw KJ, Ardia DR (2003) Carotenoids, immunocompetence, and the information content of sexual colors: an experimental test. Am Nat 162:704–712PubMedCrossRefGoogle Scholar
  41. Mikšík I, Holáň V, Deyl Z (1996) Avian eggshell pigments and their variability. Comp Biochem Physiol B Biochem Mol Biol 113:607–612CrossRefGoogle Scholar
  42. Montevecchi WA (1976) Field experiments on the adaptive significance of avian eggshell pigmentation. Behaviour 58:26–39CrossRefGoogle Scholar
  43. Nguyen LP, Nol E, Abraham KF (2007) Using digital photographs to evaluate the effectiveness of plover egg crypsis. J Wildl Manag 71:2084–2089CrossRefGoogle Scholar
  44. Petrie M, Schwabl H, Brande-Lavridsen N, Burke T (2001) Maternal investment: sex differences in avian yolk hormone levels. Nature 412:498. doi: 10.1038/35087652 PubMedCrossRefGoogle Scholar
  45. Pike TW (2011) Egg recognition in Japanese quail. Avian Biol Res 4:231–236CrossRefGoogle Scholar
  46. Reynolds SJ, Perrins CM (2010) Dietary calcium availability and reproduction in birds. In: Current Ornithology, vol 17. Springer, Heidelberg, pp 31–74Google Scholar
  47. Reynolds SJ, Mänd R, Tilgar V (2004) Calcium supplementation of breeding birds: directions for future research. Ibis 146:601–614CrossRefGoogle Scholar
  48. Saino N, Ferrari RP, Martinelli R, Romano M, Rubolini D, Møller AP (2002) Early maternal effects mediated by immunity depend on sexual ornamentation of the male partner. Proc R Soc Lond Ser B Biol Sci 269:1005–1009CrossRefGoogle Scholar
  49. Sanz JJ, Garcia-Navas V (2009) Eggshell pigmentation pattern in relation to breeding performance of blue tits Cyanistes caeruleus. J Anim Ecol 78:31–41. doi: 10.1111/j.1365-2656.2008.01465.x PubMedCrossRefGoogle Scholar
  50. Shan Y, Pepe J, Lu TH, Elbirt KK, Lambrecht RW, Bonkovsky HL (2000) Induction of the heme oxygenase-1 gene by metalloporphyrins. Arch Biochem Biophys 380:219–227PubMedCrossRefGoogle Scholar
  51. Sheldon BC (2000) Differential allocation: tests, mechanisms and implications. Trends Ecol Evol 15:397–402PubMedCrossRefGoogle Scholar
  52. Solis J, De Lope F (1995) Nest and egg crypsis in the ground-nesting stone curlew Burhinus oedicnemus. J Avian Biol:135–138Google Scholar
  53. Solomon SE (1997) Egg and eggshell quality. Iowa State University Press, USAGoogle Scholar
  54. Stoddard MC, Stevens M (2010) Pattern mimicry of host eggs by the common cuckoo, as seen through a bird’s eye. Proc R Soc B Biol Sci 277(1686):1387–1393. doi: 10.1098/rspb.2009.2018 CrossRefGoogle Scholar
  55. Stoddard MC, Fayet AL, Kilner RM, Hinde CA (2012) Egg speckling patterns do not advertise offspring quality or influence male provisioning in great tits. PloS One 7:e40211PubMedPubMedCentralCrossRefGoogle Scholar
  56. Tamura T, Fujii S (1967) Comparative observations on the distribution of fluorescent pigments (porphyrins) in the egg coverings of chicken and quail. J Fac Fish Anim Husb Hiroshima Univ 7:35–41Google Scholar
  57. Tinbergen N, Broekhuysen G, Feekes F, Houghton J, Kruuk H, Szulc E (1962) Egg shell removal by the black-headed gull, Larus ridibundus L.; a behaviour component of camouflage. Behaviour 19:74–116CrossRefGoogle Scholar
  58. Underwood T, Sealy S (2002) Adaptive significance of egg coloration. Oxf Ornithol Ser 13:280–298Google Scholar
  59. 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 Ser B Biol Sci 270:2223–2232CrossRefGoogle Scholar
  60. Wallace AR (1889) Darwinism: an exposition of the theory of natural selection with some of its applications. Cosimo Inc., USAGoogle Scholar
  61. Weidinger K (2001) How well do predation rates on artificial nests estimate predation on natural passerine nests? Ibis 143:632–641CrossRefGoogle Scholar
  62. Westmoreland D (2008) Evidence of selection for egg crypsis in conspicuous nests. J Field Ornithol 79:263–268CrossRefGoogle Scholar
  63. Williams TD (2012) Physiological adaptations for breeding in birds. Princeton University Press, USAGoogle Scholar
  64. Yahner RH, Mahan CG (1996) Depredation of artificial ground nests in a managed, forested landscape. Conserv Biol:285–288Google Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2015

Authors and Affiliations

  • Camille Duval
    • 1
    • 6
  • Phillip Cassey
    • 2
  • P. George Lovell
    • 3
  • Ivan Mikšík
    • 4
  • S. James Reynolds
    • 5
  • Karen A. Spencer
    • 1
  1. 1.School of Psychology and NeuroscienceUniversity of St AndrewsSt AndrewsUK
  2. 2.School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia
  3. 3.Division of Psychology, Social and Health SciencesThe University of AbertayDundeeUK
  4. 4.Institute of PhysiologyAcademy of Sciences of the Czech RepublicPragueCzech Republic
  5. 5.Centre for Ornithology, School of Biosciences, College of Life and Environmental SciencesUniversity of BirminghamBirminghamUK
  6. 6.Tournon Sur RhôneFrance

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