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The influence of diet on nestling body condition of an apex predator: a multi-biomarker approach

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Abstract

Animal body condition refers to the health and physiological state of individuals, and multiple parameters have been proposed to quantify this key concept. Food intake is one of the main determinants of individual body condition and much debate has been generated on how diet relates to body condition. We investigated this relationship in free-living Bonelli’s eagle (Aquila fasciata) nestlings sampled at two geographically distant populations in Spain. Nestlings’ main prey consumption was estimated by isotopic analyses. A multi-biomarker approach, including morphometric and blood biochemical measures (i.e. hematocrit, plasma biochemistry and oxidative stress biomarkers), enabled us to integrate all the body condition measures taken. A greater consumption of a preferred prey [i.e. the European rabbit (Oryctolagus cuniculus)] improved nestling body condition, as indicated by lower levels of cholesterol in plasma, greater activity of enzymes mediating in protein catabolism, higher levels of tocopherol and glutathione, and less glutathione peroxidase activity, which also suggested lower degree of oxidative stress. On the other hand, increased diet diversity was positively correlated with higher levels of oxidized glutathione, which suggests that these nestlings had poorer body condition than those with a higher frequency of preferred prey consumption. Several factors other than diet [i.e. altitude of nesting areas, nestling sex and age, sampling time (before or after midday) and recent food ingestion] had an effect on certain body condition measures. Our study reveals a measurable effect of diet on a predator’s body condition and demonstrates the importance of considering the potential influence of multiple intrinsic and extrinsic factors when assessing animal body condition.

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Abbreviations

SIA:

Stable isotope analyses

AO:

Antioxidant

OS:

Oxidative stress

ROS:

Reactive oxygen species

RBC:

Red blood cell

H’:

Shannon–Weaver index

SMI:

Scaled mass index

GLMMs:

Generalized linear mixed models

AICc :

Akaike’s information criterion adjusted for sample size

AICcw :

Akaike weights

R 2m :

Marginal coefficient of determination

R 2c :

Conditional coefficient of determination

OC:

Rabbit consumption

AR:

Consumption of partridges

CP:

Consumption of wood pigeons

CL:

Consumption of domestic pigeons

PAS:

Consumption of passerines

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Acknowledgments

We thank the “Grup de Suport de Muntanya” from the “Cos d’Agents Rurals” (Departament d’Agricultura, Generalitat de Catalunya), V. García (Ministerio de Agricultura, Alimentación y Medio Ambiente, Gobierno de España), J. Bautista, J.M. Gil-Sánchez, A. González-Aranda, J. Soria, S. Vegas, Andalusian wardens, technicians from EGMASA and GREFA, for their help during fieldwork. We also thank C. Castell from the “Diputació de Barcelona” for his valuable help. We are indebted to P. Teixidor, P. Rubio, R.M. Marimón, and E. Aracil (Centres Científics i Tecnològics, Universitat de Barcelona) for their help in SIA, C. Sanpera, R. Moreno, F.J. Ramírez, J. Cotín and M. García (Departament de Biologia Animal, Universitat de Barcelona) for technical support with material and protocols in isotopic analysis, and D.G. Lupiáñez, R. Jiménez (Departamento de Genética e Instituto de Biotecnología, Universidad de Granada), M.E. Esteban, P. Moral, M.A. Arnedo, E. Planas, G. Estrada, V. Opatova, E. Mora, L. Pita and A. García (Departament de Biologia Animal, Universitat de Barcelona) for their support in the laboratory. We also thank G. Viscor for comments that greatly improved this manuscript and M. Lockwood who revised the English. Permission to handle eagles in Catalonia was granted by the “Servei de Biodiversitat i Protecció dels Animals” (Generalitat de Catalunya), and in Andalusia by the “Gobierno de Andalucía”. J. Resano-Mayor was supported by a predoctoral grant from the “Departamento de Educación, Gobierno de Navarra; Plan de Formación y de I+D 2008–2009”. Funding for this work was provided by projects CGL2007-64805 and CGL2010-17056 from the “Ministerio de Ciencia e Innovación, Gobierno de España”, the “Àrea d’Espais Naturals de la Diputació de Barcelona” and Miquel Torres S.A. We are indebted to two anonymous referees for helpful suggestions that notably improved the original version of the manuscript.

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Author notes

  1. Jaime Resano-Mayor

    Present address: Division of Conservation Biology, Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, 3012, Bern, Switzerland

  2. Marcos Moleón

    Present address: Departamento de Biología de la Conservación, Estación Biológica de Doñana-CSIC, C/Américo Vespucio, s/n, 41092, Seville, Spain

  3. Manuel E. Ortiz-Santaliestra

    Present address: Institute for Environmental Sciences, University of Koblenz-Landau, Fortstrasse 7, 76829, Landau, Germany

Authors and Affiliations

  1. Equip de Biologia de la Conservació, Departament de Biologia Animal, Universitat de Barcelona, Av. Diagonal 643, 08028, Catalonia, Barcelona, Spain

    Jaime Resano-Mayor, Antonio Hernández-Matías, Joan Real & Francesc Parés

  2. Departamento de Biología Aplicada, Univeridad Miguel Hernández, Ctra. Beniel km 3.2, 03312, Orihuela, Alicante, Spain

    Marcos Moleón

  3. Instituto de Investigación en Recursos Cinegéticos (IREC) CSIC-UCLM-JCCM, Rda Toledo s/n, 13071, Ciudad Real, Spain

    Rafael Mateo & Manuel E. Ortiz-Santaliestra

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All applicable international, national, and institutional guidelines for the care and use of animals were followed.

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This study was funded by projects CGL2007-64805 and CGL2010-17056 from the “Ministerio de Ciencia e Innovación, Gobierno de España”, the “Àrea d’Espais Naturals de la Diputació de Barcelona” and Miquel Torres S.A. J. Resano-Mayor was supported by a predoctoral grant from the “Departamento de Educación, Gobierno de Navarra; Plan de Formación y de I+D 2008–2009”.

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Resano-Mayor, J., Hernández-Matías, A., Real, J. et al. The influence of diet on nestling body condition of an apex predator: a multi-biomarker approach. J Comp Physiol B 186, 343–362 (2016). https://doi.org/10.1007/s00360-016-0967-3

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