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Melanin and carotenoid ornaments are related to the individual condition in free-living grey partridges (Perdix perdix)

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Abstract

According to the viability indicator hypothesis, ornaments of many bird species honestly signal individual quality and health status. In this study, we investigated the health- and stress-indicating capacity of both feather- and skin-based ornamental traits in the grey partridge (Perdix perdix), a vulnerable avian species of the European agricultural landscape. In 50 free-living males, we assessed individual health status by examining the differential and absolute leukocyte counts, absolute erythrocyte count, complement activity, and pro-inflammatory immune responsiveness to phytohaemagglutinin (PHA). We found that males expressing extensive melanin-pigmented breast ornaments developed stronger skin inflammation after PHA stimulation than males with limited ornaments, suggesting that these are high-quality individuals that are able to mount a robust immune response. Furthermore, we found that the UV signal of the carotenoid-pigmented eye patch ornament is negatively related to the absolute immature erythrocyte count and the peripheral blood heterophil/lymphocyte (H/L) ratio, indicating that males with a slow pace of life and healthier males express skin ornaments with higher UV reflectance. Ornamental colouration in grey partridge males may, therefore, serve as a reliable signal of condition (in terms of resource balance) and health (in terms of stress resistance) to females.

Zusammenfassung

Melanin- und karotinoidbasierte Ornamentation hängt bei freilebenden Rebhühnern ( Perdix perdix ) von der individuellen Körperkondition ab.

Gemäß der Handicap-Hypothese dienen die Ornamente vieler Vogelarten als ehrliches Signal für individuelle Qualität und Gesundheitszustand. In dieser Studie untersuchten wir die gesundheits- und stressanzeigende Funktion von ornamentalen Merkmalen sowohl des Gefieders als auch der Hautpartien bei Rebhühnern (Perdix perdix), einer gefährdeten Vogelart europäischer Agrarlandschaften. Wir bewerteten den individuellen Gesundheitszustand von 50 freilebenden Männchen, indem wir die differenziellen und absoluten Leukozytenzahlen, die absoluten Erythrozytenzahlen, die Aktivität des Komplementsystems und die proinflammatorische Immunantwort auf Phytohämagglutinin (PHA) betrachteten. Wir stellten fest, dass Männchen, welche ausgedehnte melaninpigmentierte Brustornamente trugen, nach PHA-Stimulation eine stärkere entzündliche Hautreaktion zeigten, als Männchen mit begrenzten Ornamenten, was nahelegt, dass es sich hier um Individuen hoher Qualität handelt, die eine starke Immunantwort aktivieren können. Weiterhin fanden wir heraus, dass das UV-Signal des durch Karotinoidpigmente gefärbten Augenflecks in negativem Verhältnis zur absoluten Anzahl unreifer Erythrozyten und dem peripheren H/L-Verhältnis (Heterophile Granulozyten/Lymphozyten) steht, was andeutet, dass Männchen mit ruhigem Lebenswandel und besserer Gesundheit Hautornamente mit höherer UV-Reflexion ausbilden. Die Schmuckfärbung männlicher Rebhühner kann daher den Weibchen als zuverlässiges Signal für Körperkondition (im Hinblick auf die Ressourcenbilanz) und Gesundheit (bezüglich der Stressresistenz) dienen.

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Acknowledgments

We thank M. Šálek, D. Rymešová, and O. Tomášek for their help with the field work. We are very grateful to the members of the Hunting Club Borovina Vidonín, especially to J. Holý, P. Jobánek, and P. Jobánková for providing their facilities. This study was supported by the Czech Science Foundation (Project Nos. P206/08/1281 and P502/12/P179), Internal Grant Agency of CULS (IGA 20144268), and Institutional Research Support (Grant SVV-260 313/2016).

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Authors and Affiliations

  1. Department of Ecology, Faculty of Environmental Sciences, Czech University of Life Sciences, Kamýcká 1176, 165 21, Prague 6, Czech Republic

    Jana Svobodová

  2. Department of Zoology, Faculty of Science, Charles University in Prague, Viničná 7, 128 44, Prague, Czech Republic

    Barbora Gabrielová, Tomáš Albrecht & Michal Vinkler

  3. Department of Experimental Biology, Faculty of Science, Masaryk University, Kotlářská 2, 611 37, Brno, Czech Republic

    Pavel Hyršl

  4. Institute of Vertebrate Biology, v.v.i., The Czech Academy of Sciences, Květná 8, 603 65, Brno, Czech Republic

    Tomáš Albrecht

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  1. Jana Svobodová
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  2. Barbora Gabrielová
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Correspondence to Jana Svobodová.

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Communicated by K. C. Klasing.

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10336_2016_1349_MOESM1_ESM.docx

Supplementary Table S1: Correlations between parameters of ornaments in captive grey partridge males (n = 50), Spearman correlation coefficient (rs) above and probability level below (p) the diagonal (rs with p < 0.05 was significant) (DOCX 14 kb)

10336_2016_1349_MOESM2_ESM.docx

Supplementary Table S2: Correlations between haematological and immunological parameters in captive grey partridge males (n = 50), Spearman correlation coefficient (rs) above and probability level below (p) the diagonal (rs with p < 0.05 was significant) (DOCX 16 kb)

10336_2016_1349_MOESM3_ESM.docx

Supplementary Table S3: Summary statistics of the examined immunological traits, condition-related variables, and parameters of ornamentation in captive grey partridge males (n = 50). SD = standard deviation, SE = standard error, CV = coefficient of variation, TWBC = total white blood cell count (i.e. absolute leukocyte count), H/L = heterophil/lymphocyte ratio, TRBC = total red blood cell count (i.e., absolute erythrocyte count) (DOCX 16 kb)

10336_2016_1349_MOESM4_ESM.docx

Supplementary Table S4: Results of linear models where the red chroma, λ RUV, area of red patch, and area of the melanin ornament are response variables. Statistics for particular explanatory variables were found using a backward stepwise procedure. All statistics correspond to the step when they were removed from the model (n = 50, Δdf = 1) (DOCX 13 kb)

10336_2016_1349_MOESM5_ESM.docx

Supplementary Table S5: Results of linear models where λ RUV in 2009 and 2010, respectively, are response variables. Statistics for particular explanatory variables were found using a backward stepwise procedure. All statistics correspond to the step when they were removed from the model (n2009 = 30, n2010 = 20, Δdf = 1) (DOCX 12 kb)

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Svobodová, J., Gabrielová, B., Hyršl, P. et al. Melanin and carotenoid ornaments are related to the individual condition in free-living grey partridges (Perdix perdix). J Ornithol 157, 1007–1015 (2016). https://doi.org/10.1007/s10336-016-1349-z

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