SEXUAL DIFFERENTIATION OF AGGRESSIVE BEHAVIOR IN THE CHICKS OF THE BLACK-HEADED GULL (LARUS RIDIBUNDUS, LARIDAE, CHARADRIIFORMES) IN THE NATURAL ENVIRONMENT

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Abstract

Sexual differentiation of social behavior in gulls and its mechanisms remain unexplored beyond the breeding season. We described the development of aggressive territorial behavior in males and females of black-headed gulls at the age of 1–4 weeks, modeling the intrusion of a peer to the nesting territory. We also hypothesized that the sex differentiation of aggressive behavior may appear as a consequence of the development of small early differences between siblings in behavioral stress response. To test this assumption, we investigated the relationship between the priority among brood in aggressive contact with the intruder, and the within-broods level of activity of a chick to stress. To measure the behavioral stress response, we used the social isolation of chicks within a small water area with an island in the middle. Longer attempts to swim outside the fenced area were regarded as a more proactive stress response. At the age of up to 3 weeks, there were no sex differences in the aggressiveness, but the stress response of males was more proactive than that of their sisters, and a more proactive chick in the brood was usually the first to attack the intruder. At the fourth week of life, the aggressiveness of males increased significantly, and in broods of two sexes, brothers began to play a leading role in protecting the nesting territory in the absence of parents. They attacked the intruder more often and made aggressive calls more frequently. Thus, we were the first to reveal sexual differentiation of territorial behavior in gull chicks in the pre-fledging period. Our results suggest that under natural conditions, where the intruder does not persist in staying in the other nest, but recedes immediately when counteracted, more proactive males use to attack the intruder earlier than sisters do. As a result, they gain experience of aggressive interactions, and develop higher abilities of aggressive responses to social challenges.

About the authors

M. A. Minina

Institute of the Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences

Author for correspondence.
Email: maff14@yandex.ru
Russia, 630091, Novosibirsk

E. Yu. Agafonova

Novosibirsk State University

Email: maff14@yandex.ru
Russia, 630090, Novosibirsk

A. V. Druzyaka

Institute of the Systematics and Ecology of Animals, Siberian Branch, Russian Academy of Sciences; Novosibirsk State University

Email: maff14@yandex.ru
Russia, 630091, Novosibirsk; Russia, 630090, Novosibirsk

References

  1. Виксне Я.А., 1988. Озерная чайка – Larus ridibundus Linnaeus, 1766 // Птицы СССР. Чайковые. Под ред. В.Д. Ильичева, В.А. Зубакина. М.: Наука. С. 85–98.
  2. Гаузер М.Е., 1981. Значение места расположения гнезда для выживаемости птенцов в колониях пестроносой крачки на островах Красноводского залива // Экология и охрана птиц. Тез. докл. VII Всесоюз. орнитол. конф. Кишинев. С. 55–56.
  3. Зыкова Л.Ю., Панов Е.Н., 1983. Влияние численности и плотности гнездовых поселений на успех размножения у хохотуньи Larus argentatus cachinnans // Зоологический журнал. Т. 52. № 10. С. 1533–1540.
  4. Минина М.А., Телегина Я.Р., Друзяка А.В., 2018. Влияние условий раннего развития на формирование индивидуальных поведенческих характеристик у птенцов озерной чайки (Larus ridibundus) // Материалы Всерос. конф., посвященной 120-летию со дня рождения проф. Г.П. Дементьева, Звенигород, 27 сентября–1 октября. С. 246–253.
  5. Раттисте К., 1981. Методика изучения демографии сизой чайки в Эстонской ССР // Научные основы обследования колониальных гнездовий околоводных птиц. Под ред. В.Е. Флинта. М.: Наука. С. 97–107.
  6. Харитонов С.П., 1987. Опыт отлова и мечения некоторых видов околоводных птиц. Кольцевание и мечение животных, 1983–1984 годы. М.: Наука. С. 10–27.
  7. Харитонов С.П., Зубакин В.А., 1984. Процесс формирования пар у озерных чаек // Зоологический журнал. Т. 63. № 1. С. 95–104.
  8. Харитонов С.П., 2011. Пространственно-этологическая структура колоний околоводных птиц // Зоологический журнал. Т. 90. № 7. С. 846–860.
  9. Burger J., Beer C.G., 1975. Territoriality in the Laughing Gull (L. atricilla) // Behaviour. V. 55. № 3–4. P. 301–319.
  10. Butler R.G., Janes-Butler S., 1983. Sexual differences in the behavior of adult Great Black-backed Gulls (Larus marinus) during the pre-and post-hatch periods // The Auk. V. 100. № 1. P. 63–75.
  11. Carere C., Balthazart J., 2007. Sexual versus individual differentiation: the controversial role of avian maternal hormones // Trends in Endocrinology & Metabolism. V. 18. № 2. P. 73–80.
  12. Eising C.M., Müller W., Groothuis T.G.G., 2006. Avian mothers create different phenotypes by hormone deposition in their eggs // Biology letters. V. 2. № 1. P. 20–22.
  13. Fridolfsson A.K., Ellegren H., 1999. A simple and universal method for molecular sexing of non-ratite birds // Journal of avian biology. P. 116–121.
  14. Griffiths R., Double M.C., Orr K., Dawson R.J., 1998. A DNA test to sex most birds // Molecular ecology. V. 7. № 8. P. 1071–1075.
  15. Groothuis T.G.G., Ros A.F.H., 2005. The hormonal control of begging and early aggressive behavior: experiments in black-headed gull chicks // Hormones and Behavior. V. 48. № 2. P. 207–215.
  16. Groothuis T.G.G., Trillmich F., 2011. Unfolding personalities: the importance of studying ontogeny // Developmental Psychobiology. V. 53. № 6. P. 641–655.
  17. Groothuis T., 1989. On the ontogeny of display behaviour in the black-headed gull: I. The gradual emergence of the adult forms // Behaviour. V. 109. № 1–2. P. 76–123.
  18. Groothuis T., 1989a. On the ontogeny of display behaviour in the black-headed gull: II. Causal links between the development of aggression, fear and display behaviour: emancipation reconsidered // Behaviour. P. 161–204.
  19. Groothuis T., 1992. The influence of social experience on the development and fixation of the form of displays in the black-headed gull // Animal behaviour. V. 43. № 1. P. 1–14.
  20. Groothuis T., Meeuwissen G., 1992. The influence of testosterone on the development and fixation of the form of displays in two age classes of young black-headed gulls // Animal Behaviour. V. 43. № 2. P. 189–208.
  21. Groothuis T., Van Mulekom L., 1991. The influence of social experience on the ontogenetic change in the relation between aggression, fear and display behaviour in black-headed gulls // Animal behaviour. V. 42. № 6. P. 873–881.
  22. Groothuis T.G., Hsu B.Y., Kumar N., Tschirren B., 2019. Revisiting mechanisms and functions of prenatal hormone-mediated maternal effects using avian species as a model // Philosophical Transactions of the Royal Society B. V. 374. № 1770. P. 20180115.
  23. Loftus J.C., Perez A.A., Sih A., 2021. Task syndromes: linking personality and task allocation in social animal groups // Behavioral Ecology. V. 32. № 1. P. 1–17.
  24. Pierotti R., Annett C., 1994. Patterns of aggression in gulls: asymmetries and tactics in different social categories // The Condor. V. 96. № 3. P. 590–599.
  25. Podmokła E., Drobniak S.M., Rutkowska J., 2018. Chicken or egg? Outcomes of experimental manipulations of maternally transmitted hormones depend on administration method meta-analysis // Biological Reviews. V. 93. № 3. P. 1499–1517.
  26. Rokka K., Pihlaja M., Siitari H., Soulsbury C.D., 2014. Sex-specific differences in offspring personalities across the laying order in magpies Pica pica // Behavioural processes. V. 107. P. 79–87.
  27. Ros A.F.H., Dieleman S.J., Groothuis T.G.G., 2002. Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis // Hormones and Behavior. V. 41. № 3. P. 334–342.
  28. Sabbi K.H., Emery Thompson M., Machanda Z.P., Otali E., Wrangham R.W., Muller M.N., 2021. Sex differences in early experience and the development of aggression in wild chimpanzees // Proceedings of the National Academy of Sciences. V. 118. № 12. C. e2017144118.
  29. Schielzeth H., Nakagawa S., Stoffel M., 2019. rptR: repeatability estimation for Gaussian and nonGaussian data. Available from: https://rdrr.io/cran/rptR/man/rpt.html [Accessed 27.07.21]
  30. Southern L.K., 1981. Sex-related differences in territorial aggression by Ring-billed Gulls // The Auk. P. 179–181.
  31. Terkel A.S., Moore C.L., Beer C.G., 1976. The effects of testosterone and estrogen on the rate of long-calling vocalization in juvenile laughing gulls, Larus atricilla // Hormones and Behavior. V. 7. № 1. P. 49–57.
  32. Tinbergen N., 1956. On the functions of territory in gulls // Ibis. V. 98. № 3. P. 401–411.
  33. Tschirren B., 2015. Differential effects of maternal yolk androgens on male and female offspring: a role for sex-specific selection? // PLoS One. V. 10. № 7. P. e0133673.
  34. Van Rhijn J., 1985. Black-headed gull or black-headed girl? On the advantage of concealing sex by gulls and other colonial birds // Netherlands Journal of Zoology. V. 35. P. 87–102.
  35. Von Engelhardt N., Carere C., Dijkstra C., Groothuis T.G.G., 2006. Sex-specific effects of yolk testosterone on survival, begging and growth of zebra finches // Proceedings of the Royal Society B: Biological Sciences. V. 273. № 1582. P. 65–70.
  36. Wingfield J.C., Hegner R.E., Dufty Jr.A.M., Ball G.F., 1990. The “challenge hypothesis”: theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies // The American Naturalist. V. 136. № 6. P. 829–846.

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Copyright (c) 2023 М.А. Минина, Е.Ю. Агафонова, А.В. Друзяка

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