Volume 43 Issue 5
Sep.  2022
Turn off MathJax
Article Contents
Manuel Soler, Francisco Ruiz-Raya, Lucía Sánchez-Pérez, Juan Diego Ibáñez-Álamo, Juan José Soler. Functional explanation of extreme hatching asynchrony: Male Manipulation Hypothesis. Zoological Research, 2022, 43(5): 843-850. doi: 10.24272/j.issn.2095-8137.2021.455
Citation: Manuel Soler, Francisco Ruiz-Raya, Lucía Sánchez-Pérez, Juan Diego Ibáñez-Álamo, Juan José Soler. Functional explanation of extreme hatching asynchrony: Male Manipulation Hypothesis. Zoological Research, 2022, 43(5): 843-850. doi: 10.24272/j.issn.2095-8137.2021.455

Functional explanation of extreme hatching asynchrony: Male Manipulation Hypothesis

doi: 10.24272/j.issn.2095-8137.2021.455
#Authors contributed equally to this work
Funds:  This work was supported by the Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía (research project CVI-6653 to M.S.)
More Information
  • Corresponding author: E-mail: msoler@ugr.es
  • Received Date: 2022-03-16
  • Accepted Date: 2022-08-22
  • Published Online: 2022-08-25
  • Publish Date: 2022-09-18
  • Hatching asynchrony in birds is considered an adaptation to facilitate brood reduction because under conditions of food scarcity, the smallest nestling usually dies soon after hatching, thereby minimizing parental effort. However, in species with extreme hatching asynchrony, the last hatchlings paradoxically experience a very low probability of survival and death can take so long that it can hardly be considered an adaptation. Here, we propose and experimentally tested a new adaptive hypothesis explaining the brood reduction paradox, namely the “Male Manipulation Hypothesis”. Our hypothesis suggests that by inducing asynchronous hatching, females increase the feeding requirements of the brood, which will induce males to increase provisioning effort. In addition, females may extend the period of male manipulation by feeding the smallest nestling just enough to sustain life. Our study showed that male common blackbirds (Turdus merula) increased their effort (i.e., number of food items per hour) in experimental asynchronous broods compared to synchronous broods, while females reduced their contribution, as predicted by the hypothesis.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Amundsen T, Stokland JN. 1988. Adaptive significance of asynchronous hatching in the shag: a test of the brood reduction hypothesis. Journal of Animal Ecology, 57(2): 329−344. doi: 10.2307/4909
    Arcese P, Smith JNM. 1988. Effects of population density and supplemental food on reproduction in Song Sparrows. Journal of Animal Ecology, 57(1): 119−136. doi: 10.2307/4768
    Bengtsson H, Rydén O. 1981. Development of parent-young interaction in asynchronously hatched broods of altricial birds. Zeitschrift für Tierpsychologie, 56(3): 255−272.
    Budden AE, Beissinger SR. 2009. Resource allocation varies with parental sex and brood size in the asynchronously hatching green-rumped parrotlet (Forpus passerinus). Behavioral Ecology and Sociobiology, 63(5): 637–647.
    Caro SM, Griffin AS, Hinde CA, West SA. 2016. Unpredictable environments lead to the evolution of parental neglect in birds. Nature Communications, 7(1): 10985. doi: 10.1038/ncomms10985
    Clark AB, Wilson DS. 1981. Avian breeding adaptations: hatching asynchrony, brood reduction, and nest failure. The Quarterly Review of Biology, 56(3): 253−277. doi: 10.1086/412316
    Cramp S. 1988. The Birds of the Western Palearctic, Vol. V. Oxford: Oxford University Press.
    Del Hoyo J, Elliott A, Christie D. 2005. Handbook of the birds of the world, Vol. 10: Cuckoo-Shrikes to Thrushes. Barcelona: Lynx Edicions.
    Dell Inc. 2015. Dell Statistica (data analysis software system), version 13. software. dell. com.
    Ferretti V, Llambías PE, Martin TE. 2005. Life-history variation of a neotropical thrush challenges food limitation theory. Proceedings of the Royal Society B:Biological Sciences, 272(1564): 769−773. doi: 10.1098/rspb.2004.3039
    García-Navas V, Sanz JJ. 2010. Flexibility in the foraging behavior of blue tits in response to short-term manipulations of brood size. Ethology, 116(8): 744−754.
    Gottlander K. 1987. Parental feeding behaviour and sibling competition in the pied flycatcher Ficedula hypoleuca. Ornis Scandinavica, 18(4): 269–276.
    Grodzinski U, Johnstone RA. 2012. Parents and offspring in an evolutionary game: the effect of supply on demand when costs of care vary. Proceedings of the Royal Society B:Biological Sciences, 279(1726): 109−115. doi: 10.1098/rspb.2011.0776
    Halupka K, Wysocki D. 2004. The frequency and timing of courtship and copulation in blackbirds, Turdus merula, reflect sperm competition and sexual conflict. Behaviour, 141(4): 501–512.
    Harrison F, Barta Z, Cuthill I, Székely T. 2009. How is sexual conflict over parental care resolved? A meta-analysis. Journal of Evolutionary Biology, 22(9): 1800−1812. doi: 10.1111/j.1420-9101.2009.01792.x
    Hauber ME, Moskát C. 2008. Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behavioral Ecology, 19(1): 79−86. doi: 10.1093/beheco/arm108
    Hõrak P. 1995. Brood reduction facilitates female but not offspring survival in the great tit. Oecologia, 102(4): 515−519. doi: 10.1007/BF00341365
    Houston AI, Székely T, McNamara JM. 2005. Conflict between parents over care. Trends in Ecology & Evolution, 20(1): 33−38.
    Ibáñez-Álamo JD, Soler M. 2010. Does urbanization affect selective pressures and life-history strategies in the common blackbird (Turdus merula L. )?. Biological Journal of the Linnean Society, 101(4): 759−766. doi: 10.1111/j.1095-8312.2010.01543.x
    Jeon J. 2008. Evolution of parental favoritism among different-aged offspring. Behavioral Ecology, 19(2): 344−352. doi: 10.1093/beheco/arm136
    Julliard R, McCleery RH, Clobert J, Perrins CM. 1997. Phenotypic adjustment of clutch size due to nest predation in the great tit. Ecology, 78(2): 394−404. doi: 10.1890/0012-9658(1997)078[0394:PAOCSD]2.0.CO;2
    Koenig WD, Walters EL. 2012. An experimental study of chick provisioning in the cooperatively breeding acorn woodpecker. Ethology, 118(6): 566−574. doi: 10.1111/j.1439-0310.2012.02043.x
    Kontiainen P, Pietiäinen H, Karell P, Pihlaja T, Brommer JE. 2010. Hatching asynchrony is an individual property of female Ural owls which improves nestling survival. Behavioral Ecology, 21(4): 722−729. doi: 10.1093/beheco/arq045
    Lack D. 1947. The significance of clutch-size. Ibis, 89(2): 302−352.
    Lack DL. 1954. The Natural Regulation of Animal Numbers. Oxford: Clarendon Press.
    Lahaye SEP, Eens M, Iserbyt A, Groothuis TGG, De Vries B, Müller W, et al. 2015. Influence of mate preference and laying order on maternal allocation in a monogamous parrot species with extreme hatching asynchrony. Hormones and Behavior, 71: 49−59. doi: 10.1016/j.yhbeh.2015.03.009
    Lessells CM. 2012. Sexual conflict. In: Royle NJ, Smiseth PT, Kölliker M. The Evolution of Parental Care. New York: Oxford University Press, 150–170.
    Lotem A. 1998. Differences in begging behaviour between barn swallow, Hirundo rustica, nestlings. Animal Behaviour, 55(4): 809−818. doi: 10.1006/anbe.1997.0675
    MacGregor NA, Cockburn A. 2002. Sex differences in parental response to begging nestlings in superb fairy-wrens. Animal Behaviour, 63(5): 923−932. doi: 10.1006/anbe.2001.1991
    Macnair MR, Parker GA. 1979. Models of parent-offspring conflict. III. Intra-brood conflict. Animal Behaviour, 27: 1202−1209. doi: 10.1016/0003-3472(79)90067-8
    Magrath RD. 1989. Hatching asynchrony and reproductive success in the blackbird. Nature, 339(6225): 536−538. doi: 10.1038/339536a0
    Magrath RD. 1990. Hatching asynchrony in altricial birds. Biological Reviews, 65(4): 587−622. doi: 10.1111/j.1469-185X.1990.tb01239.x
    Mock DW, Dugas MB, Strickler SA. 2011. Honest begging: expanding from signal of need. Behavioral Ecology, 22(5): 909−917. doi: 10.1093/beheco/arr091
    Mock DW, Forbes LS. 1995. The evolution of parental optimism. Trends in Ecology & Evolution, 10(3): 130−134.
    Mock DW, Parker GA. 1997. The Evolution of Sibling Rivalry. Oxford: Oxford University Press.
    Mock DW, Ploger BJ. 1987. Parental manipulation of optimal hatch asynchrony in cattle egrets: an experimental study. Animal Behaviour, 35(1): 150−160. doi: 10.1016/S0003-3472(87)80220-8
    Mock DW, Schwagmeyer PL, Dugas MB. 2009. Parental provisioning and nestling mortality in house sparrows. Animal Behaviour, 78(3): 677−684. doi: 10.1016/j.anbehav.2009.05.032
    Olson VA, Liker A, Freckleton RP, Székely T. 2008. Parental conflict in birds: comparative analyses of offspring development, ecology and mating opportunities. Proceedings of the Royal Society B:Biological Sciences, 275(1632): 301−307. doi: 10.1098/rspb.2007.1395
    Ploger BJ, Medeiros MJ. 2004. Unequal food distribution among great egret Ardea alba nestlings: parental choice or sibling aggression?. Journal of Avian Biology, 35(5): 399−404. doi: 10.1111/j.0908-8857.2004.03253.x
    Price K, Harvey H, Ydenberg R. 1996. Begging tactics of nestling yellow-headed blackbirds, Xanthocephalus xanthocephalus, in relation to need. Animal Behaviour, 51(2): 421−435. doi: 10.1006/anbe.1996.0039
    R Core Team. 2021. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.https://www.scirp.org/reference/referencespapers.aspx?referenceid=3022946.
    Royle NJ, Smiseth PT, Kölliker M. 2012. The Evolution of Parental Care. Oxford: Oxford University Press.
    Ryser S, Guillod N, Bottini C, Arlettaz R, Jacot A. 2016. Sex-specific food provisioning patterns by parents in the asynchronously hatching European hoopoe. Animal Behaviour, 117: 15−20. doi: 10.1016/j.anbehav.2016.04.015
    Slagsvold T. 1982. Clutch size, nest size, and hatching asynchrony in birds: experiments with the fieldfare (Turdus pilaris). Ecology, 63(5): 1389−1399. doi: 10.2307/1938866
    Slagsvold T. 1984. Clutch size variation of birds in relation to nest predation: on the cost of reproduction. Journal of Animal Ecology, 53(3): 945−953. doi: 10.2307/4669
    Slagsvold T, Amundsen T, Dale S. 1995. Costs and benefits of hatching asynchrony in blue tits Parus caeruleus. Journal of Animal Ecology, 64(5): 563–578.
    Slagsvold T, Lifjeld JT. 1989a. Hatching asynchrony in birds: the hypothesis of sexual conflict over parental investment. American Naturalist, 134(2): 239−253. doi: 10.1086/284978
    Slagsvold T, Lifjeld JT. 1989b. Constraints on hatching asynchrony and egg size in pied flycatchers. Journal of Animal Ecology, 58(3): 837−849. doi: 10.2307/5127
    Smiseth PT, Amundsen T. 2002. Senior and junior nestlings in asynchronous bluethroat broods differ in their effectiveness of begging. Evolutionary Ecology Research, 4(8): 1177−1189.
    Soler M. 1989. Fracaso reproductor en grajilla (Corvus monedula): pérdidas de huevos y mortalidad de pollos. Ardeola, 36(1): 3−24.
    Soler M. 2001. Begging behaviour of nestlings and food delivery by parents: the importance of breeding strategy. Acta Ethologica, 4(1): 59−63. doi: 10.1007/s102110100047
    Soler M, Ruiz-Raya F, Sánchez-Pérez L, Ibáñez-Álamo JD. 2022. Parents preferentially feed larger offspring in asynchronously hatched broods irrespective of scramble competition. Animal Behaviour, in press.
    Soler M, Soler JJ. 1991. Growth and development of great spotted cuckoos and their magpie host. Condor, 93(1): 49−54. doi: 10.2307/1368605
    Soler M, Soler JJ. 1996. Effects of experimental food provisioning on reproduction in the jackdaw Corvus monedula, a semi-colonial species. Ibis, 138(3): 377−383.
    Stoleson SH, Beissinger SR. 1995. Hatching asynchrony and the onset of incubation in birds revisited: When is the critical period?. Current Ornithology, 12: 191−270.
    Therneau T. 2021. A Package for Survival Analysis in R. R package version 3.2–11.https://CRAN.R-project.org/package=survival.
    Trivers RL. 1972. Parental investment and sexual selection. In: Campbell B. Sexual Selection and the Descent of Man. Chicago: Aldine, 136–179.
    Wiebe KL, Wiehn J, Korpimäki E. 1998. The onset of incubation in birds: can females control hatching patterns?. Animal Behaviour, 55(4): 1043−1052. doi: 10.1006/anbe.1997.0660
    Wright J, Leonard ML. 2002. The Evolution of Begging: Competition, Cooperation and Communication. Dordrecht: Kluwer Academic Publishers.
    Wysocki D. 2005. Within-season divorce rate in an urban population of European Blackbird Turdus merula. Ardea, 92(2): 219–228.
    Wysocki D, Jankowiak Ł. 2018. The first case of successful polyterritorial polygyny in the European Blackbird Turdus merula. The Wilson Journal of Ornithology, 130(2): 515–517.
  • ZR-2021-455 Supplementary_Materials.pdf
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(2)  / Tables(1)

    Article Metrics

    Article views (1037) PDF downloads(135) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint