The effect of neighbouring contacts on the formation of behavioral types in Black‐headed Gull chicks
https://doi.org/10.18470/1992-1098-2021-3-19-32
Abstract
Aim. The early development of behavioral types and the influence of environmental, mostly social, factors have almost not been studied for natural animal populations. We investigated the effect of the density of non‐relative social environment on the development of the behavior of free‐living chicks of the Black‐headed Gull (Chroicocephalus ridibundus). Material and Methods. In order to exclude the influence of relationships with native parents on the development of chicks' behavior, 21 clutches were cross‐fostered so as to destroy any negative relationship between the aggressiveness of their parents and the density of their neighbors. The behavioral types of chicks were determined by a 3‐time testing in an “open field” arena at the ages of 2‐3, 8‐9 and 14‐15 days.
Results. Those parents, which effectively coped with close neighboring at the nest settling period, raised more active offspring. The behavior of chicks raised by foster parents, on the contrary, was more passive the fewer unrelated chicks there were nearby and was not associated with the aggressiveness of their parents.
Conclusion. Our work demonstrates the role of an unrelated social environment in the ontogeny of behavioral types in colonial birds. We suppose that the different ways in which influences of parents and neighbors optimize the trajectories of development of behavioral types at an individual level, increase the chances of chicks surviving in the diverse and variable environment of a breeding colony.
About the Authors
M. A. MininaRussian Federation
Maria A. Minina
Novosibirsk
A. V. Druzyaka
Russian Federation
Alexey V. Druzyaka, PhD in Biology, Research Fellow, Laboratory of Behavioral Ecology of Communities
11 Frunze St, Novosibirsk, 630091
Tel. +79232273238
References
1. Shilov I.A. Ekologo‐fiziologicheskiye osnovy populyatsionnykh otnosheniy u zhivotnykh [Ecological and physiological foundations of population relations in animals]. Moscow, Moscow University Publ., 1977, 262 p. (In Russian)
2. Ilyina T.A., Ivankina E.V., Kerimov A.B. Cherty individual'nosti i osobennost' kormovogo povedeniya tomnykh i svetlykh samtsov mukholovki‐pestrushki v period vykarmlivaniya ptentsov [Personality traits and peculiarities of foraging behaviour of dark and pale pied flycatcher males at the period of rearing of nestlings]. Materialy mezhdunarodnoy konferentsii «Ptitsyduplognozdniki kak model'nyye ob"yekty v reshenii problem populyatsionnoy ekologii i evolyutsii», Moskva, 22‐28 sentyabrya, 2014 [Proceedings of the international conference "Hollow‐nesting birds as model objects in solving problems of population ecology and evolution", Moscow, 22‐28 September, 2014]. Moscow, 2014, pp. 125‐128. (In Russian)
3. Koolhaas J.M., Korte S.M., de Boer S.F., van der Vegt B.J., van Reenen C.G., Hopster H. et al. Coping styles in animals: current status in behavior and stress physiology // Neuroscience & Biobehavioral Reviews. 1999. V. 23. N 7. P. 925‐935.
4. Dall S.R.X., Houston A.I., McNamara J.M., The behavioural ecology of personality: Consistent individual differences from an adaptive perspective // Ecology Letters. 2004. V. 7. P. 734‐739.
5. Sih A., Bell A., Johnson J.C. Behavioral syndromes: an ecological and evolutionary overview // Trends of Ecology and Evolution. 2004. N 19. P. 372‐378.
6. Sih A., Bell A., Johnson J.C., Ziemba R.E. Behavioural syndromes: an integrative overview // Q. Rev. Biol. 2004. N 79. P. 241‐277.
7. Ilyina T.A., Ivankina E.V. Seasonal variation of singling activity and relative effect of advertising behaviour of males with different plumage colour the Pied Flycatcher (Ficedula hypoleuca) // Acta Ornithologica. 2001. N 36. P. 85‐89.
8. Réale D., Dingemanse N.J. Animal personality // Encyclopedia of live sciences. 2012. URL: https://onlinelibrary.wiley.com/doi/abs/10.1002/9780470015902.a0023570 (дата обращения 07.09.2021)
9. Ilyina T.A., Ivankina Ye.V., Bushuyev A.V., Kerimov A.B. Issues of studying behavioral types in population biology of birds. Printsipy ekologii [Ecological principles]. 2016, vol. 5, no. 3, pp. 56‐56. (In Russian)
10. Bell A.M. Future directions in behavioral syndromes research // Proceedings of the Royal Society. London Series B. 2007. N 274. P. 755‐761.
11. Drent P.J., Marchetti C. Individuality, exploration and foraging in hand‐raised juvenile great tits // Proceedings of the 22 nd International Ornithological Congress, Johannesburg, 16‐22 August 1998, Durban, 1999. P. 896‐914.
12. Drent P.J., van Oers K., van Noordwijk A.J. Realised heritability of personalities in the great tit (Parus major) // Proceedings of the Royal Society of London B. 2003. V. 270. N 1510. P. 45‐51. DOI: 10.1098/rspb.2002.2168
13. Dingemanse N.J., Wolf M. Recent models for adaptive personality differences: a review // Philosophical Transactions of the Royal Society B: Biological Sciences. 2010. V. 365. P. 3947‐3958. DOI: 10.1098/rstb.2010.0221
14. Cockrem J.F. Individual variation in glucocorticoid stress responses in animals // General and Comparative Endocrinology. 2013. N 181. P. 45‐58. DOI: 10.1016/j.ygcen.2012.11.025
15. Dingemanse N.J., Both C., Drent P.J., van Oers K., van Noordwijk A.J. Repeatability and heritability of exploratory behaviour in great tits from the wild // Animal Behaviour. 2002. V. 64. N 6. P. 929‐938. DOI: 10.1006/anbe.2002.2006
16. Benus R.F., Henkelmann C. Litter composition influences the development of aggression and behavioural strategy in male Mus domesticus // Behaviour. 1998. V. 135. P. 1229‐1249.
17. Mendl M., Paul S.E. Litter composition affects parental care, offspring growth and the development of aggressive behaviour in wild house mice // Behaviour. 1990. V. 116. N 1‐2. P. 90‐108.
18. Stern J.M. Offspring‐induced nurturance: animal-human parallels // Developmental Psychobiology. 1997. V. 31. N 1. P. 19‐37.
19. Liu D., Tannenbaum B., Caldji C., Francis D., Freedman A., Sharma S. et al. Maternal care, hippocampal glucocorticoid receptor gene expression and hypothalamic– pituitary–adrenal responses to stress // Science. 1997. V. 277. N 5332. P. 1659‐1662.
20. Francis D.D., Diorio J., Liu D., Meaney M.J. Nongenomic transmission across generations in maternal behavior and stress responses in the rat. Science. 1999. V. 286. N 5442. P. 1155‐1158. DOI: 10.1126/science.286.5442.1155
21. Caldji C., Tannenbaum B., Sharma S., Francis D., Plotsky P.M., Meaney M.J. Maternal care during infancy regulates the development of neural systems mediating the expression of behavioral fearfulness in adulthood in the rat // Proceedings of the National Academy of Sciences. 1998. V. 95. N 9. P. 5335‐5340.
22. Zhang T.Y., Hellstrom I.C., Bagot R.C., Wen X., Diorio J., Meaney M.J. Maternal care and DNA methylation of the glutamic acid decarboxylase I promoter in rat hippocampus // Journal of Neuroscience. 2010. V. 30. P. 13130‐13137.
23. Carere C., Drent P.J., Koolhaas J.M., Groothuis T.G.G. Epigenetic effects on personality traits: early food provisioning and sibling competition // Behavior. 2005. V. 142. N 9‐10. P. 1329‐1355.
24. van Oers К., Kohn G.M., Hinde C.A., Naguib M. Parental food provisioning is related to nestling stress response in wild great tit nestlings: implications for the development of personality // Frontiers in Zoology. 2015. V. 12. Suppl. 1. S10. DOI: 10.1186/1742‐9994‐12‐S1‐S10
25. Wilson D.S., Coleman K., Clark A.B., Biederman L. Shybold continuum in pumpkinseed sunfish (Lepomis gibbosus): An ecological study of a psychological trait // Journal of Comparative Psychology. 1993. V. 107. N 3. P. 250‐260.
26. Groothuis T. The influence of social experience on the development and fixation of the form of displays in the Black‐headed Gull // Animal Behavior. 1992. V. 43. P. 1‐14.
27. Minina M.A., Druzyaka A.V. [Using the "Open Field" method to identify the mechanism of formation of strategies for feeding behavior of black‐headed gull chicks depending on early food supply]. Sovremennyye problemy nauki i obrazovaniya, 2015, no. 5. Available at: https://science‐education.ru/ru/article/view?id=22168 (accessed: 04.09.2021) (In Russian)
28. Hunt G.L., Meloon S.C. Activity patterns of gull chicks in relation to feeding by parents: their potential significance for density‐dependent mortality // Auk. 1975. V. 92. P. 523‐527.
29. Fetterolf P.M. Infanticide and non‐fatal attacks on chicks by ring‐billed gulls // Animal Behavior. 1983. V. 31. P. 1018‐1028. DOI: 10.1016/S0003‐3472(83)80007‐4
30. Kharitonov S.P. Kharitonov S.P. The relationship of black‐headed gulls (Larus ridibundus) in a local grouping within the colony. Zoologicheskiy zhurnal [Zoological journal]. 1981, vol. 60, no. 6, pp. 871‐877. (In Russian)
31. Mikhel'son Kh.A., Lein'sh G.T., Klimpin'sh V.A., Liyepa V.K. Study of population dynamics of some ducks in Latvia by continuous banding of incubating females and ducklings. Ornitologiya [Ornithology]. 1963, no. 6, pp. 280‐292. (In Russian)
32. Kim S.Y., Noguera J.C., Morales J., Velando A. The evolution of multicomponent begging display in gull chicks: sibling competition and genetic variability // Animal Behavior. 2011. V. 82. P. 113‐118.
33. Fucikova E., Drent P.J., Smits N., van Oers K. Handling stress as a measurement of personality in great tit nestlings (Parus major) // Ethology. 2009. V. 115. P. 366‐374. DOI: 10.1016/S0003‐3472(74)80027‐8
34. Minina M.A., Telegina Ya.R., Druzyaka A.V., Zotov A.Yu. Vliyaniye usloviy rannego razvitiya na formirovaniye individual'nykh povedencheskikh kharakteristik u ptentsov ozornoy chayki (Larus ridibundus) [Influence of conditions of early development on the formation of individual behavioral characteristics in the chicks of the black‐headed gull (Larus ridibundus)]. Materialy Vserossiyskoy konferentsii, posvyashchonnoy 120‐letiyu so dnya rozhdeniya professora G.P. Dement'yeva, Zvenigorod, 27 sentyabrya‐1 oktyabrya, 2018 [Materials of the All‐Russian conference dedicated to the 120th anniversary of the birth of Professor G.P. Dementiev, Zvenigorod, September 27‐October 1, 2018]. Zvenigorod, 2018, pp. 246‐253. (In Russian)
35. Favati A., Zidar J., Thorpe H., Jensen P., Løvlie H. The ontogeny of personality traits in the red junglefowl, Gallus gallus // Behavioral Ecology. 2015. V. 27. N 2. P. 484‐493. DOI: 10.1093/beheco/arv177
36. Ginsburg H.J., Brand W.G., Taylor R.D. Inhibition of distress vocalizations in the open field as a function of heightened fear or arousal in domestic fowl (Gallus gallus) // Animal Behavior. 1974. N 22. P. 745‐749. DOI: 10.1016/S0003‐3472(74)80027‐8
37. Okuliarová M., Škrobánek P., Zeman M. Effect of Increasing Yolk Testosterone Levels on Early Behaviour in Japanese Quail Hatchlings // Acta Veterinaria Brno. 2007. V. 76. P. 325‐331. DOI: 10.2754/avb200776030325
38. Viksne Ya.A. [Black‐headed gull – Larus ridibundus Linnaeus, 1766]. In: Ptitsy SSSR. Chaykovyye [Birds of the USSR. Gulls]. Moscow, Nauka Publ., 1988, 416 p. (In Russian)
39. Druzyaka A.V., Minina M.A., Chasovskikh Z.V. The early development of aggressive behavior and rapid growth of chicks in the Black‐headed Gull (Larus ridibundus) in conditions of diffused nesting. Biology Bulletin, 2015, vol. 42, no. 9, pp. 808‐820. DOI: 10.1134/S1062359015090034
40. Ros A.F.H. Effects of testosterone on growth, plumage pigmentation, and mortality in Black‐headed Gull chicks // Ibis. 1999. V. 141. P. 451‐459.
41. de Ruiter A.J.H., Koolhaas J.M., Keijser J.N., van Oortmerssen G.A. Differential testosterone secretory capacity of the testes of aggressive and nonaggressive mice during ontogeny // Aggressive Behavior. 1992. V. 18. N 2. P. 149‐157.
42. Spencer K., Verhulst S. Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata) // Hormones and Behavior. 2007. V. 51. N 2. P. 273‐280.
43. Loiseau C., Fellous S., Haussy C., Chastel O., Sorci G. Condition‐dependent effects of corticosterone on a carotenoid‐based begging signal in house sparrows // Hormones and Behavior. 2008. V. 53. N 1. P. 266‐273. DOI: 10.1016/j.yhbeh.2007.10.006
44. Kitaysky A.S., Wingfield J.C., Piatt J.F. Corticosterone facilitates begging and affects resource allocation in the black‐legged kittiwake // Behavioural Ecology. 2001. V. 12. N 5. P. 619‐625.
Review
For citations:
Minina M.A., Druzyaka A.V. The effect of neighbouring contacts on the formation of behavioral types in Black‐headed Gull chicks. South of Russia: ecology, development. 2021;16(3):19‐32. (In Russ.) https://doi.org/10.18470/1992-1098-2021-3-19-32