Volume 43 Issue 2
Mar.  2022
Turn off MathJax
Article Contents
Juan José Soler, Manuel Martín-Vivaldi, Soňa Nuhlíčková, Cristina Ruiz-Castellano, Mónica Mazorra-Alonso, Ester Martínez-Renau, Manfred Eckenfellner, Ján Svetlík, Herbert Hoi. Avian sibling cannibalism: Hoopoe mothers regularly use their last hatched nestlings to feed older siblings. Zoological Research, 2022, 43(2): 265-274. doi: 10.24272/j.issn.2095-8137.2021.434
Citation: Juan José Soler, Manuel Martín-Vivaldi, Soňa Nuhlíčková, Cristina Ruiz-Castellano, Mónica Mazorra-Alonso, Ester Martínez-Renau, Manfred Eckenfellner, Ján Svetlík, Herbert Hoi. Avian sibling cannibalism: Hoopoe mothers regularly use their last hatched nestlings to feed older siblings. Zoological Research, 2022, 43(2): 265-274. doi: 10.24272/j.issn.2095-8137.2021.434

Avian sibling cannibalism: Hoopoe mothers regularly use their last hatched nestlings to feed older siblings

doi: 10.24272/j.issn.2095-8137.2021.434
#Authors contributed equally to this work
Funds:  This study was supported by the Spanish Ministerio de Ciencia, Innovación y Universidades and European (FEDER) Funds (CGL2017-83103-P)
More Information
  • Sibling cannibalism is relatively common in nature, but its evolution in birds and certain other vertebrates with extended parental care had been discarded. Here, however, we demonstrate its regular occurrence in two European populations of the Eurasian hoopoe (Upupa epops) and explore possible adaptive and non-adaptive explanations. Results showed that sibling cannibalism was more frequently detected in Spain (51.7%) than in Austria (5.9%). In these two populations, the hoopoes laid similar clutch sizes, resulting in similar fledging production, but hatching failures were more frequent in the northern population. Consequently, having more nestlings condemned to die in the southern population may explain the higher incidence of sibling cannibalism. In accordance with this interpretation, hatching span and failure, but not breeding date, explained the probability of sibling cannibalism in the Spanish hoopoes, while all three variables predicted brood reduction intensity. Furthermore, experimental food supply reduced the probability of sibling cannibalism, but not the intensity of brood reduction. Finally, females allocated fewer resources to the smallest nestlings when they were going to starve, but not necessarily when they were going to be used as food for their siblings. These results suggest that hoopoes produce extra eggs that, in the case of reduced hatching failure and food scarcity, produce nestlings that are used to feed older siblings. These findings provide the first evidence that sibling cannibalism occurs regularly in a bird species, thus expanding our evolutionary understanding of clutch size, hatching asynchrony, parent-offspring conflict, infanticide, and sibling cannibalism in the animal kingdom.
  • #Authors contributed equally to this work
  • loading
  • [1]
    Alexander RD. 1974. The evolution of social behavior. Annual Review of Ecology and Systematics, 5: 325−383. doi: 10.1146/annurev.es.05.110174.001545
    [2]
    Arlettaz R, Fournier J, Zbinden N. 2000. Evolution démographique (1979–1998) d’une population témoin de Huppe fasciée Upupa epops en Valais et stratégie de conservation ciblée. Nos Oiseaux, 47: 19−27.
    [3]
    Barbaro L, Couzi L, Bretagnolle V, Nezan J, Vetillard F. 2008. Multi-scale habitat selection and foraging ecology of the Eurasian hoopoe (Upupa epops) in pine plantations. Biodiversity and Conservation, 17(5): 1073−1087. doi: 10.1007/s10531-007-9241-z
    [4]
    Baur B, Baur A. 1986. Proximate factors influencing egg cannibalism in the land snail Arianta arbustorum (Pulmonata, Helicidae). Oecologia, 70(2): 283−287. doi: 10.1007/BF00379252
    [5]
    Bortolotti GR, Wiebe KL, Iko WM. 1991. Cannibalism of nestling American kestrels by their parents and siblings. Canadian Journal of Zoology, 69(6): 1447−1453. doi: 10.1139/z91-205
    [6]
    Caro SM, Griffin AS, Hinde CA, West SA. 2016. Unpredictable environments lead to the evolution of parental neglect in birds. Nature Communications, 7: 10985. doi: 10.1038/ncomms10985
    [7]
    Chan YH, Zafirah M, Cremades M, Divet M, Teo CHR, Ng SC. 2007. Infanticide-cannibalism in the oriental pied hornbill Anthracoceros albirostris. Forktail, 23: 170–173.
    [8]
    Crespi BJ. 1992. Cannibalism and trophic eggs in subsocial and eusocial insects. In: Elgar MA, Crespi BJ. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford, UK: Oxford University Press, 176–213.
    [9]
    Crump ML. 1992. Cannibalism in amphibians. In: Elgar MA, Crespi BJ. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford, UK: Oxford University Press, 256–276.
    [10]
    Dawkins R. 1976. The Selfish Gene. Oxford: Oxford University Press.
    [11]
    De Neve L, Soler JJ, Soler M, Pérez-Contreras T. 2004. Differential maternal investment counteracts for late breeding in magpies Pica pica: an experimental study. Journal of Avian Biology, 35(3): 237−245. doi: 10.1111/j.0908-8857.2004.03161.x
    [12]
    Dell-Inc. 2015. STATISTICA (data analysis software system), version 13. software. dell. com.
    [13]
    Díaz Lora S, Pérez-Contreras T, Azcárate-García M, Martínez Bueno M, Soler JJ, Martín-Vivaldi M. 2020. Hoopoe Upupa epops male feeding effort is related to female cosmetic egg colouration. Journal of Avian Biology, 51(8): e02433. doi: 10.1111/jav.02433
    [14]
    Eickwort KR. 1973. Cannibalism and kin selection in Labidomera clivicollis (Coleoptera: Chrysomelidae). The American Naturalist, 107(955): 452−453. doi: 10.1086/282847
    [15]
    Elgar MA, Crespi BJ. 1992. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford: Oxford University Press.
    [16]
    Engelbrecht D. 2013. Cannibalism in the southern Yellow-Billed Hornbill Tockus Leucomelas. Ornithological Observations, 4: 104–106.
    [17]
    Fitzgerald GJ, Whoriskey FG. 1992. Empirical studies of cannibalism in fish. In: Elgar MA, Crespi BJ. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford, UK: Oxford University Press, 238–255.
    [18]
    Forbes LS. 1990. Insurance offspring and the evolution of avian clutch size. Journal of Theoretical Biology, 147(3): 345−359. doi: 10.1016/S0022-5193(05)80492-8
    [19]
    Forbes LS. 1991. Insurance offspring and brood reduction in a variable environment: the costs and benefits of pessimism. Oikos, 62(3): 325−332. doi: 10.2307/3545497
    [20]
    Fournier J, Arlettaz R. 2001. Food provision to nestlings in the Hoopoe Upupa epops: implications for the conservation of a small endangered population in the Swiss Alps. Ibis, 143(1): 2−10. doi: 10.1111/j.1474-919X.2001.tb04163.x
    [21]
    Hardy ICW. 1992. The insurance hypothesis and the theory of clutch size in birds and in invertebrates. The Auk, 109(4): 936−937. doi: 10.2307/4088180
    [22]
    Hausfater G, Hrdy SB. 1984. Infanticide: Comparative and Evolutionary Perspectives. New York: Aldine Publishing Group.
    [23]
    Hildebrandt B, Schaub M. 2018. The effects of hatching asynchrony on growth and mortality patterns in Eurasian Hoopoe Upupa epops nestlings. Ibis, 160(1): 145−157. doi: 10.1111/ibi.12529
    [24]
    Hrdy SB, Hausfater G. 1984. Comparative and evolutionary perspectives on infanticide: introduction and overview. In: Hausfater G, Hrdy SB. Infanticide: Comparative and Evolutionary Perspectives. New York: Aldine Publishing Company.
    [25]
    Ingram C. 1962. Cannibalism by nestling short-eared owls. Auk, 79(4): 715.
    [26]
    Krištofík J, Mašán P, Šustek Z, Nuhličková S. 2013. Arthropods (Acarina, Coleoptera, Siphonaptera) in nests of hoopoe (Upupa epops) in Central Europe. Biologia, 68(1): 155−161. doi: 10.2478/s11756-012-0135-5
    [27]
    Lack D. 1954. The Natural Regulation of Animal Numbers. Oxford: Clarendon Press.
    [28]
    Lundblad CG, Conway CJ. 2021. Ashmole's hypothesis and the latitudinal gradient in clutch size. Biological Reviews, 96(4): 1349−1366. doi: 10.1111/brv.12705
    [29]
    Martín-Vivaldi M, Doña J, Romero-Masegosa J, Soto-Cárdenas M. 2014. Abubilla – Upupa epops. In: Salvador A, Morales MB. Enciclopedia Virtual de los Vertebrados Españoles. Madrid: Museo Nacional de Ciencias Naturales.
    [30]
    Martín-Vivaldi M, Palomino JJ, Soler M, Soler JJ. 1999. Determinants of reproductive success in the Hoopoe Upupa epops, a hole-nesting non-passerine bird with asynchronous hatching. Bird Study, 46(2): 205−216. doi: 10.1080/00063659909461132
    [31]
    Maynard Smith J, Price GR. 1973. The logic of animal conflict. Nature, 246(5427): 15−18. doi: 10.1038/246015a0
    [32]
    Mock DW. 1984. Infanticide, siblicide, and avian nestling mortality. In: Hausfater G, Hrdy SB. Infanticide: Comparative and Evolutionary Perspective. New York: Aldine Publishing Company, 3–30.
    [33]
    Mock DW. 2004. More Than Kin and Less than Kind: The Evolution of Family Conflict. Cambridge, Massachusetts: Harvard University Press.
    [34]
    Mock DW, Parker GA. 1998. Siblicide, family conflict and the evolutionary limits of selfishness. Animal Behaviour, 56(1): 1−10.
    [35]
    Morandini V, Ferrer M. 2015. Sibling aggression and brood reduction: a review. Ethology Ecology & Evolution, 27(1): 2−16.
    [36]
    Moreno J. 2012. Parental infanticide in birds through early eviction from the nest: rare or under-reported?. Journal of Avian Biology, 43(1): 43−49. doi: 10.1111/j.1600-048X.2011.05608.x
    [37]
    Ng SC, Lai HM, Cremades M, Lim MTS, Tali SB. 2011. Breeding observations on the oriental pied hornbill in nest cavities and in artificial nests in Singapore, with emphasis on infanticide-cannibalism. The Raffles Bulletin of Zoology, (S24): 15−22.
    [38]
    Nuhlíčková S, Krištín A, Degma P, Hoi H. 2016. Variability in nestling diet of European hoopoes: annual and sampling effect. Folia Zoologica, 65(3): 189−199. doi: 10.25225/fozo.v65.i3.a3.2016
    [39]
    Olson VA, Davies RG, Orme CDL, Thomas GH, Meiri S, Blackburn TM, et al. 2009. Global biogeography and ecology of body size in birds. Ecology Letters, 12(3): 249−259. doi: 10.1111/j.1461-0248.2009.01281.x
    [40]
    Plard F, Arlettaz R, Schaub M. 2018. Hoopoe males experience intra-seasonal while females experience inter-seasonal reproductive costs. Oecologia, 186(3): 665−675. doi: 10.1007/s00442-017-4028-8
    [41]
    Polis GA. 1981. The evolution and dynamics of intraspecific predation. Annual Review of Ecology and Systematics, 12: 225−251. doi: 10.1146/annurev.es.12.110181.001301
    [42]
    Polis GA. 1984. Intraspecific predation and "infant killing" among invertebrates. In: Hausfater G, Hrdy SB. Infanticide: Comparative and Evolutionary Perspective. New York: Aldine Publishing Company, 87–104.
    [43]
    Polis GA, Myers CA. 1985. A survey of intraspecific predation among reptiles and amphibians. Journal of Herpetology, 19(1): 99−107. doi: 10.2307/1564425
    [44]
    Rehsteiner U. 1996. Abundance and habitat requirements of the Hoopoe Upupa epops in Extremadura (Spain). Ornithol Beobachter, 93: 277−287.
    [45]
    Rieder I, Schulze CH. 2010. Breeding biology, feeding and habitat utilization of the hoopoe (Upupa epops). Carinthia II, 120(1): 167−182.
    [46]
    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
    [47]
    Sanz JJ, Moreno J. 1995. Experimentally induced clutch size enlargements affect reproductive success in the Pied Flycatcher. Oecologia, 103(3): 358−364. doi: 10.1007/BF00328625
    [48]
    Schaub M, Martinez N, Tagmann-Ioset A, Weisshaupt N, Maurer ML, Reichlin TS, et al. 2010. Patches of bare ground as a staple commodity for declining ground-foraging insectivorous farmland birds. PLoS One, 5(10): e13115. doi: 10.1371/journal.pone.0013115
    [49]
    Soler JJ, Martín-Vivaldi M, Ruiz-Rodríguez M, Valdivia E, Martín-Platero AM, Martínez-Bueno M, et al. 2008. Symbiotic association between hoopoes and antibiotic-producing bacteria that live in their uropygial gland. Functional Ecology, 22(5): 864−871. doi: 10.1111/j.1365-2435.2008.01448.x
    [50]
    Sorci G, Soler JJ, Møller AP. 1997. Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica). Proceedings of the Royal Society B:Biological Sciences, 264(1388): 1593−1598. doi: 10.1098/rspb.1997.0222
    [51]
    Stanback MT, Koenig WD. 1992. Cannibalism in birds. In: Elgar MA, Crespi BJ. Cannibalism: Ecology and Evolution among Diverse Taxa. Oxford: Oxford University Press, 277–298.
    [52]
    Stoleson SH, Beissinger SR. 1995. Hatching asynchrony and the onset of incubation in birds, revisited: when is the critical period?. In: Power DM. Current Ornithology. Boston: Springer, 191–270.
  • Supplementary Video S1.mp4
    Supplementary Video S5.mp4
    Supplementary Video S4.mp4
    Supplementary Video S3.mp4
    ZR-2021-434 Supplementary Materials.pdf
    Supplementary Video S2.mp4
  • 加载中

Catalog

    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(2)

    Article Metrics

    Article views (1170) PDF downloads(173) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return