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Parental sex allocation and sex-specific survival drive offspring sex ratio bias in little owls

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Abstract

Although biased offspring sex ratios are common in species with sexual size dimorphism, the proximate causes are often unresolved. This is because two general mechanisms operating in different ways and in various periods of reproduction can lead to the bias: sex-biased survival or parental sex-allocation. We examined nestling sex ratio patterns between hatching and fledging, sexual size dimorphism, and factors affecting nestling survival using growth and survival data of 846 individual little owl Athene noctua nestlings with known sex from 307 broods from Germany, the Netherlands and Denmark. Nestling sex ratio was female-biased, mainly due to a significant female bias in the first-hatched chicks. Females showed a higher body weight than male nestlings at ringing and body weight of nestlings decreased with hatching sequence. Nestling survival was higher in females (Φ = 0.91) than in males (Φ = 0.85), and survival rates were positively related to body mass and negatively to brood size. Although the observed lower survival of males can cause an overall female-biased sex ratio, the sex dimorphism and survival patterns found here are unlikely to explain the conspicuous sex ratio pattern with a female bias in the first-hatched nestlings and the increase in female bias across the season. Thus, these results point towards interacting mechanisms of parental sex allocation strategies and sex-specific survival. As the female bias was allocated to the first rank that is most likely to survive, the female bias will increase under suboptimal breeding conditions. We therefore suggest that under suboptimal ecological conditions, higher investment into females is adaptive in little owls.

Significance statement

Biased sex ratios can have severe effects on the social behaviour and population dynamics of endangered species. However, the existence of subtle sex ratio bias is often unknown and its proximate mechanisms and ultimate consequences often remain unclear. Small sample sizes make the detection of subtle effects unlikely and often fail to disentangle diverging mechanisms such as sex-biased survival and parental sex allocation. We used a large dataset of 846 little owl nestlings from 307 broods from three countries to investigate offspring sex ratio patterns, sexual size dimorphism and nestling survival simultaneously. Our findings suggest interacting mechanisms of parental sex allocation strategies and sex-specific survival to drive biased offspring sex ratios in little owls. The context dependence of the sex ratio bias indicates that offspring sex ratio bias in little owls is both, a consequence of—and an adaptation to—suboptimal breeding conditions.

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Acknowledgments

We thank all field assistants and volunteers, in particular Gerhard Bauer, Wolfgang Graef, Josef Helmik, Thomas Henschel, Rudi Holleitner, Petra Kauder, Klaus Lopitz, Alexander Neu, Jens Polzien, Erwin Reichert, Volker Schlie, Dirk Unkelbach and Bruno Vollmar for their help in collecting data. Furthermore, we thank Fränzi Korner-Nievergelt for statistical support and three anonymous referees for their valuable comments.

Funding

This work was supported by the Swiss National Science Foundation (Grant 3100A 132951/1 to BN-D and MUG), the Hirschmann Foundation and the Karl Mayer Foundation.

Author information

Authors and Affiliations

  1. Swiss Ornithological Institute, Seerose 1, Sempach, CH-6204, Switzerland

    Matthias Tschumi, Jolanda Humbel, Julien Fattebert, Vanja T. Michel, Marco Perrig, Beat Naef-Daenzer & Martin U. Grüebler

  2. Institute of Evolutionary Biology and Environmental Studies, University of Zurich, Zurich, CH-8057, Switzerland

    Jolanda Humbel

  3. NABU Bad Kreuznach, Badenheimer Weg 6, Pleitersheim, 55576, Germany

    Joscha Erbes

  4. School of Life Sciences, University of KwaZulu-Natal, Durban, 4000, South Africa

    Julien Fattebert

  5. Brackenheim, Germany

    Jochen Fischer

  6. Bretten, Germany

    Gerhard Fritz

  7. NABU Rhein Selz, Berliner Strasse 72, Dienheim, 55276, Germany

    Barbara Geiger

  8. Steenuilen Overleg Nederland (STONE), De Kistemaker 12, Heiloo, 1852 GW, The Netherlands

    Ronald van Harxen & Pascal Stroeken

  9. Neustadt, Germany

    Bernd Hoos

  10. Institute of Biology I, Albert-Ludwigs-University Freiburg, Hauptstrasse 1, Freiburg, 79104, Germany

    Johanna Hurst

  11. Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark, University of Copenhagen, Universitetsparken 13, Copenhagen, 2100, Denmark

    Lars Bo Jacobsen

  12. Forschungsgemeinschaft zur Erhaltung einheimischer Eulen e.V, Brunnengasse 3/1, Oberriexingen, 71739, Germany

    Herbert Keil

  13. Wolfschlugen, Germany

    Werner Kneule

  14. Wolfschlungen, Germany

    Heinz Michels

  15. Erpolzheim, Germany

    Leander Möbius

  16. Köngen, Germany

    Philip Rößler

  17. Erkenbrechtsweiler, Germany

    Dieter Schneider

  18. Nierstein, Germany

    Siegfried Schuch

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  1. Matthias Tschumi
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  2. Jolanda Humbel
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Correspondence to Matthias Tschumi.

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Ethical approval

Handling and ringing of little owl nestlings in Germany was carried out under the permit of the regional council of Baden-Württemberg, Germany (licence No. 35e9185.81/0288), the regional council of Rheinland Pfalz (licence Az 42/553-253) and Stuttgart (licence Az 55-8853.17), the Struktur- und Genehmigungsdirektion (SGD) Süd and SGD Nord of Rheinland-Pfalz, as well as Vogelwarte Radolfzell (licences no. 1146, 1191; 1403 and 1903). Handling and ringing of the nestlings in Denmark was carried out under licence from Copenhagen Bird Ringing Centre (A-392 personal ringing licence to LBJ). The sampling of 5 growing breast feathers in Denmark was permitted by The Animal Experiments Inspectorate (#2011/561-17). Handling and ringing in the Netherlands was carried out under the licence from Vogeltrekstation, Dutch centre for avian migration and demography (R. van Harxen–848). The sampling of growing breast feathers in the Netherlands was permitted by Dierexperimentencommissie Koninklijke Academie van Wetenschappen/NIOO 13. 07 advies. All procedures followed the ASAB/ABS guidelines for the ethical treatment of animals in behavioural research and teaching and all applicable international, national, and/or institutional guidelines for the care and use of animals were followed. The handling of birds was performed with maximum care and disturbance to nests kept to a minimum. Ethical approval for involving animals in this study was received through the application procedure for ringing permits and the scientific commission of the Swiss Ornithological Institute.

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The authors declare that they have no conflicts of interest.

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Communicated by L. Z. Garamszegi

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Tschumi, M., Humbel, J., Erbes, J. et al. Parental sex allocation and sex-specific survival drive offspring sex ratio bias in little owls. Behav Ecol Sociobiol 73, 85 (2019). https://doi.org/10.1007/s00265-019-2694-8

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  • DOI: https://doi.org/10.1007/s00265-019-2694-8

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