Testing Cort-Fitness and Cort-Adaptation hypotheses in a habitat suitability gradient for roe deer

Research output: Journal contributionsJournal articlesResearchpeer-review

Authors

  • G. Escribano-Avila
  • Nathalie Pettorelli
  • E. Virgós
  • Carlos Lara-Romero
  • Jorge Lozano Mendoza
  • I. Barja
  • F.S. Cuadra
  • Marisa Puerta
According to the Cort-Fitness Hypothesis, higher stress levels (glucocorticoids) in vertebrates are correlated to lower fitness. However, recent studies have failed to validate this hypothesis. A proposed wider framework suggests that reproduction can be perceived as an overload adds up to other environmental challenges that individuals must adjust to. In this case, elevated glucocorticoids could help individuals to allocate resources to reproduction without comprising other functions, leading to the expectation of a positive cort-fitness relationship. This has been proposed as the Cort-Adaptation Hypothesis. Stress levels result from a complex interaction between the environment and the neuroendocrine system of animals. Accounting for physiological functions involved in how animals cope with their environment would help to clarify the relationship between glucocorticoids and animal performance. We used roe deer (. Capreolus capreolus) inhabiting diverse habitats in the Iberian Peninsula to: i) test the Cort-Fitness and Cort-Adaptation hypotheses by indexing fitness using a comprehensive physiological approach which takes into account fundamental physiological functions and their trade-offs; and ii) evaluate the link between primary productivity and individuals' condition in a seasonal environment. We evaluated spatial and temporal variation in stress levels, reproductive hormone levels, nutritional status and immune function from fecal samples collected in 2010. Lower stress levels were related to better condition in non-reproductive seasons but not to higher primary productivity. In contrast, stress levels were always positively related to reproductive condition, which was better in most productive habitats. Summer and winter were the less productive seasons and the more challenging for the species in the habitat gradient studied. In winter, reproductive condition traded off against immune function being biased toward immune function in less productive habitats. In summer reduced primary productivity limited roe deer nutritional and immunological condition but not reproductive condition. Overall our results match both the Cort-Fitness and Cort-Adaptation Hypotheses. © 2013 Elsevier Masson SAS.
Original languageEnglish
JournalActa Oecologica
Volume53
Pages (from-to)38-48
Number of pages11
ISSN1146-609X
DOIs
Publication statusPublished - 11.2013

Bibliographical note

Cited By :5

Export Date: 27 January 2017

CODEN: ACOEE

Correspondence Address: Escribano-Avila, G.; Departamento de Biología y Geología, Universidad Rey Juan Carlos, Departamental I. C/Tulipán s/n, E-28933 Móstoles, Madrid, Spain; email: gema.escribano@urjc.es

References: Abáigar, T., Domene, M.A., Palomares, F., Effects of fecal age and seasonality or steroid hormone concentration as a reproductive parameter in field studies (2010) Eur. J. Wildl. Res., 56, pp. 781-787; Acevedo, P., Delibes-Mateos, M., Escudero, M.A., Vicente, J., Marco, J., Gortazar, C., Environmental constraints in the colonization sequence of roe deer (Capreolus capreolus Linnaeus, 1758) across the Iberian Mountains, Spain (2005) J.Biogeogr., 32, pp. 1671-1680; Araujo, M.B., Rahbek, C., How does climate change affect biodiversity? (2006) Science, 313, pp. 1396-1397; Blanchard, P., Festa-Bianchet, M., Gaillard, J.M., Jorgenson, J.T., Atest of long-term fecal nitrogen monitoring to evaluate nutritional status in bighorn sheep (2003) J.Wildl. Manage, 67, pp. 477-484; Blanvillain, C., Berthier, J.L., Bomsel-Demontoy, M.C., Sempere, A.J., Olbricht, G., Schwarzenberg, F., Analysis of reproductive data and measurement of fecal progesterone metabolites to monitor the ovarian function in the Pudu, Pudu puda (Artiodactyla, Cervidae) (1997) Mammalia, 61, pp. 589-602; Blottner, S., Hingst, O., Meyer, H.H.D., Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus) (1996) Reproduction, 108, pp. 299-305; Bonier, F., Martin, P.R., Moore, I.T., Wingfield, J.C., Do baseline glucocorticoids predict fitness? (2009) Trends. Ecol. Evol., 24, pp. 634-642; Bonier, F., Moore, I.T., Robertson, R.J., The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods (2011) Biol. Lett., 7, pp. 944-946; Boonstra, R., Coping with changing northern environments: the role of the stress axis in birds and mammals (2004) Integr. Comp. Biol., 44, pp. 95-108; Brisbin, J.T., Gong, J., Shafit, S., Interactions between commensal bacteria and the gut-associated immune system of the chicken (2008) Anim. Health. Res. Rev., 9, pp. 101-110; Bubenik, G.A., Brown, R.D., Schams, D., Antler cycle and endocrine parameters in male axis deer (Axis axis) - seasonal levels of LH, FSH, testosterone and prolactin and results of GNRH and ACTH challenge tests (1991) Comp. Bicochem. Physiol. A-mol. Integr. Physiol., 99, pp. 645-650; Bubenik, G.A., Reyes, E., Schams, D., Lobos, A., Bartos, L., Seasonal levels of LH, FSH, testosterone and prolactin in adult male pudu (Pudu puda) (1996) Comp. Bicochem. Physiol. B - Biochem. Mol. Biol., 115, pp. 417-420; Busch, D.S., Hayward, L.S., Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables (2009) Biol. Conserv., 142, pp. 2844-2853; Busch, D.S., Robinson, W.D., Robinson, T.R., Wingfield, J.C., Influence of proximity to a geographical range limit on the physiology of a tropical bird (2011) J.Anim. Ecol., 80, pp. 640-649; Cerutti, A., Rescigno, M., The biology of intestinal immunoglobulin A responses (2008) Immunity, 28, pp. 740-750; Comrey, A.L., Lee, H.B., (1992) AFirst Course in Factor Analysis, , Lawrence Erlbaum Associates, Inc Publishers, Hillsdale, New Jersey; Cote, S.D., Festa-Bianchet, M., Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality (2001) Oecologia, 127, pp. 230-238; Creel, S., Fox, J.E., Hardy, A., Sands, J., Garrott, B., Peterson, R.O., Snowmobile activity and glucocorticoid stress responses in wolves and elk (2002) Conserv. Biol., 16, pp. 809-814; Davies, G., Stear, M.J., Bishop, S.C., Genetic relationships between indicator traits and nematode parasite infection levels in 6-month-old lambs (2005) Anim. Sci., 80, pp. 143-150; Demas, G.E., Drazen, D.L., Nelson, R.J., Reductions in total body fat decrease humoral immunity (2003) Proc. R. Soc. B - Biol. Sci., 270, pp. 905-911; Demas, G.E., Zysling, D.A., Beechler, B.R., Muehlenbein, M.P., French, S.S., Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts (2011) J.Anim. Ecol., 80, pp. 710-730; Dray, S., Dufour, A.B., The ade4 package: implementing the duality diagram for ecologists (2007) J.Stat. Softw., 22, pp. 1-20; Dumonceaux, G.A., Bauman, J.E., Camilo, G.R., Evaluation of progesterone levels in feces of captive reticulated giraffe (Giraffa camelopardalis reticulata) (2006) J.Zoo. Wildl. Med., 37, pp. 255-261; Dunn, P.O., Garvin, J.C., Whittingham, L.A., Freeman-Gallant, C.R., Hasselquist, D., Carotenoid and melanin-based ornaments signal similar aspects of male quality in two populations of the common yellowthroat (2009) Funct. Ecol., 24, pp. 149-158; Ezenwa, V.O., Stefan Ekernas, L., Creel, S., Unravelling complex associations between testosterone and parasite infection in the wild (2012) Funct. Ecol., 26, pp. 123-133; (2008) Ecología y caracterización genética de las poblaciones de corzo en la Comunidad de Madrid, , Madrid, FIDA; Flagstad, O., Roed, K., Stacey, J.E., Jakobsen, J.S., Reliable noninvasive genotyping based on excremental PCR of nuclear DNA purified with a magnetic bead protocol (1999) Mol. Ecol., 8, pp. 879-883; Garonna, I., Fazey, I., Brown, M.E., Pettorelli, N., Rapid primary productivity changes in one of the last coastal rainforests: the case of Kahua, Solomon Islands (2009) Environ. Conserv., 36, pp. 253-260; Garrott, R.A., Monfort, S.L., White, P.J., Mashburn, K.L., Cook, J.G., One-sample pregnancy diagnosis in elk using fecal steroid metabolites (1998) J.Wildl. Dis., 34, pp. 126-131; Gendreau, Y., Cote, S.D., Festa-Bianchet, M., Maternal effects on post-weaning physical and social development in juvenile mountain goats (Oreamnos americanus) (2005) Behav. Ecol. Sociobiol., 58, pp. 237-246; Gobush, K.S., Mutayoba, B.M., Wasser, S.K., Long-term impacts of poaching on relatedness, stress physiology, and reproductive output of adult female African Elephants (2008) Conserv. Biol., 22, pp. 1590-1599; Gomez, J.A., Garcia, A.J., Landete-Castillejos, T., Gallego, L., Effect of advancing births on testosterone until 2.5 years of age and puberty in Iberian red deer (Cervus elaphus hispanicus) (2006) Anim. Reprod. Sci., 96, pp. 79-88; Guillet, C., Bergström, R., Cederlund, G., Size of winter home range of roe deer Capreolus capreolus in two forest areas with artificial feeding in Sweden (1996) Wildl. Biol., 2, pp. 107-111; Hamel, S., Garel, M., Festa-Bianchet, M., Gaillard, J.M., Cote, S.D., Spring Normalized Difference Vegetation Index (NDVI) predicts annual variation in timing of peak faecal crude protein in mountain ungulates (2009) J.Appl. Ecol., 46, pp. 582-589; Hasselquist, D., Wasson, M.F., Winkler, D.W., Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows (2001) Behav. Ecol., 12, pp. 93-97; Hayward, L.S., Bowles, A., Ha, J.C., Wasser, S.K., Impacts of acute and long-term vehicle exposure on physiology and reproductive success of the northern spotted owl (2011) Ecosphere, 2, pp. 1-20; Hewison, A.J.M., Morellet, N., Verheyden, H., Daufresne, T., Angibault, J.M., Cargnelutti, B., Merlet, J., Cebe, N., Landscape fragmentation influences winter body mass of roe deer (2009) Ecography, 32, pp. 1062-1070; Hoffmann, B., Barth, D., Karg, H., Progesterone and estrogen levels in peripheral plasma of the pregnant and non-pregnant roe deer (Capreolus capreolus) (1978) Biol. Reprod., 19, pp. 931-935; Holand, Ø., Mysterud, A., Wannag, A., Linnell, J.D.C., Roe deer in northern environments: physiology and behaviour (1998) The European Roe Deer: the Biology of Success, pp. 117-138. , Scandinavian University Press, Oslo, R. Anderson, P. Duncan, J.D.C. Linnell (Eds.); Huber, S., Palme, R., Arnold, W., Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus) (2003) Gen. Comp. Endocrinol., 130, pp. 48-54; Huete, A., Didan, K., Miura, T., Rodriguez, E.P., Gao, X., Ferreira, L.G., Overview of the radiometric and biophysical performance of the MODIS vegetation indices (2002) Remote Sens. Environ., 83, pp. 195-213; Husak, J.F., Moore, I.T., Stress hormones and mate choice (2008) Trends. Ecol. Evol., 23, pp. 532-534; Kaiser, H.F., The application of electronic comptures to factor analysis (1960) Educ. Psychol. Meas., 20, pp. 141-151; Kamler, J., Homolka, M., Faecal nitrogen: a potential indicator of red and roe deer diet quality in forest habitats (2005) Folia Zool., 54, pp. 89-98; Kamler, J., Homolka, M., Cizmar, D., Suitability of NIRS analysis for estimating diet quality of free-living red deer Cervus elaphus and roe deer Capreolus capreolus (2004) Wildl. Biol., 10, pp. 235-240; Kapke, C.A., Arcese, P., Ziegler, T.E., Scheffler, G.R., Estradiol and progesterone metabolite concentration in white-tailed deer (Odocoileus virginianus) feces (1999) J.Zoo. Wildl. Med., 30, pp. 361-371; Knox, W.M., Miller, K.V., Collins, D.C., Bush, P.B., Kiser, T.E., Marchinton, R.L., Serum and urinary levels or reproductive hormones associated with the estrous cycle in white-tailed deer (Odocoileus virginianus) (1992) Zoo Biol., 11, pp. 121-131; Lambert, R.T., Ashworth, C.J., Beattie, L., Gebbie, F.E., Hutchinson, J.S., Kyle, D.F., Racey, P.A., Temporal changes in reproductive hormones and conceptus-endometrial interactions during embryonic diapauses and reactivation of blastocyst in European roe deer (Capreolus capreolus) (2001) Reproduction, 121, pp. 863-871; Lanctot, R.B., Hatch, S.A., Gill, V.A., Eens, M., Are corticosterone levels a good indicator of food availability and reproductive performance in a kittiwake colony? (2003) Horm. Behav., 43, pp. 489-502; Linnell, J.D.C., Andersen, R., Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus (1998) J.Zool., 244, pp. 497-504; Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P., Hector, A., Hooper, D.U., Wardle, D.A., Biodiversity and ecosystem functioning: current knowledge and future challenges (2001) Science, 294, pp. 804-808; Mateos-Quesada, P., Corzo - Capreolus capreolus (2011) Enciclopedia Virtual de los Vertebrados Españoles, , Museo Nacional de Ciencias Naturales, Madrid, L.M. Carrascal, A. Salvador (Eds.); McEwen, B.S., Wingfield, J.C., The concept of allostasis in biology and biomedicine (2003) Horm. Behav., 43, pp. 2-15; McNamara, J.M., Buchanan, K.L., Stress, resource allocation, and mortality (2005) Behav. Ecol., 16, pp. 1008-1017; Millennium E.A, (2005) Ecosystems and Human Well-being: Synthesis, , Island Press, Washington, D; Monfort, S.L., Martinet, C., Wildt, D.E., Urinary steroid metabolite profiles in female Pere-Davids deer (Elaphurus davidianus) (1991) J.Zoo. Wildl. Med., 22, pp. 78-85; Mormede, P., Andanson, S., Auperin, B., Beerda, B., Guemene, D., Malmkvist, J., Manteca, X., Veissier, I., Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare (2007) Physiol. Behav., 92, pp. 317-339; Navarro-Gonzalez, N., Verheyden, H., Hoste, H., Cargnelutti, B., Lourtet, B., Merlet, J., Daufresne, T., Serrano, E., Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape (2011) Eur. J. Wildl. Res., 57, pp. 639-645; Neish, A.S., Microbes in gastrointestinal health and disease (2009) Grastroenterology, 136, pp. 65-80; Parmesan, C., Yohe, G., Aglobally coherent fingerprint of climate change impacts across natural systems (2003) Nature, 421, pp. 37-42; Peters, I.R., Calvert, E.L., Hall, E.J., Day, A.J., Measurement of immunoglobulin concentrations in the feces of healthy dogs (2004) Clin. Diagn. Lab. Immunol., 11, pp. 841-848; Peterson, D.A., McNulty, N.P., Guruge, J.L., Gordon, J.L., IgA response to symbiotic bacteria as a mediator of gut homeostasis (2007) Cell Host Microbe, 2, pp. 328-339; Pettorelli, N., Mysterud, A., Yoccoz, N.G., Langvatn, R., Stenseth, N.C., Importance of climatological downscaling and plant phenology for red deer in heterogeneous landscapes (2005) Proc. R. Soc. B - Biol. Sci., 272, pp. 2357-2364; Pettorelli, N., Gaillard, J.M., Mysterud, A., Duncan, P., Stenseth, N.C., Delorme, D., Van Laere, G., Klein, F., Using a proxy of plant productivity (NDVI) to find key periods for animal performance: the case of roe deer (2006) Oikos, 112, pp. 565-572; Phalipon, A., Cardona, A., Kraehenbuhl, J.P., Edelman, L., Sansonetti, P.J., Secretory component: a new role in secretory IgA-mediated immune exclusion invivo (2002) Immunity, 17, pp. 107-115; Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D.R., (2012) nlme: Linear and Nonlinear Mixed effects Models, , 3.1.-104, R.D.C.T.R.p.v. (Ed.); Ramsay, E.C., Moran, F., Roser, J.F., Lasley, B.L., Urinary steroid evaluations to monitor ovarian function in exotic ungulates.10. Pregnancy diagnosis in perissodactyla (1994) Zoo Biol., 13, pp. 129-147; Roelants, H., Schneider, F., Goritz, F., Streich, J., Blottner, S., Seasonal changes of spermatogonial proliferation in roe deer, demonstrated by flow cytometric analysis of c-kit receptor, in relation to follicle-stimulating hormone, luteinizing hormone, and testosterone (2002) Biol. Reprod., 66, pp. 305-312; Romero, L.M., Physiological stress in ecology: lessons from biomedical research (2004) Trends. Ecol. Evol., 19, pp. 249-255; Romero, L.M., Wikelski, M., Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events (2001) Proc. Natl. Sci. U.S.A, 98, pp. 7366-7370; Ruiz, M., French, S.S., Demas, G.E., Martins, E.P., Food supplementation and testosterone interact to influence reproductive behavior and immune function in Sceloporus graciosus (2010) Horm. Behav., 57, pp. 134-139; Ryg, M., Physiological control of growth, reproduction and lactation in deer (1986) Rangifer, 1, pp. 261-266; Sapolsky, R.M., Romero, L.M., Munck, A.U., How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions (2000) Endocr. Rev., 21, pp. 55-89; Sempere, A.J., Lacroix, A., Temporal and seasonal relationships between LH, testosterone and antlers in fawn and adult mare roe deer (Capreolus capreolus) a longitudinal study from birth to 4 years of age (1982) Acta. Endocrinol., 99, pp. 295-301; Sempere, A.J., Mauget, R., Bubenik, G.A., Influence of photoperiod on the seasonal pattern of secretion of luteinizing hormone and testosterone and on the antler cycle in roe deer (Capreolus capreolus) (1992) Reproduction, 95, pp. 693-700; Sheldon, B.C., Verhulst, S., Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology (1996) Trends. Ecol. Evol., 11, pp. 317-321; Sheriff, M., Dantzer, B., Delehanty, B., Palme, R., Boonstra, R., Measuring stress in wildlife: techniques for quantifying glucocorticoids (2011) Oecologia, 166, pp. 869-887; Smith, W.D., Jackson, F., Jackson, E., Williams, J., Age Immunity to Ostertagia-circumcinta - comparison of the local immune-response of 4-1/2-month-old and 10-mont-old lambs (1985) J.Comp. Pathol., 95, pp. 235-245; Snoeck, V., Peters, I.R., Cox, E., The IgA system: a comparison of structure and function in different species (2006) Vet. Res., 37, pp. 455-467; Speakman, J.R., The physiological costs of reproduction in small mammals (2008) Philos. Trans. R. Soc. B - Biol. Sci., 363, pp. 375-398; Stoops, M.A., Anderson, G.B., Lasley, B.L., Shideler, S.E., Use of fecal steroid metabolites to estimate the pregnancy rate of a free-ranging herd of tule elk (1999) J.Wildl. Manage., 63, pp. 561-569; Taillon, J., Cote, S.D., Are faecal hormone levels linked to winter progression, diet quality and social rank in young ungulates? An experiment with white-tailed deer (Odocoileus virginianus) fawns (2008) Behav. Ecol. Sociobiol., 62, pp. 1591-1600; (2011) R: a Language and Environment for Statistical Computing, , R Foundation for Statistical Computing, Vienna, Austria, Team R.D.C; Telleria, J.L., Virgos, E., Distribution of an increasing roe deer population in a fragmented Mediterranean landscape (1997) Ecography, 20, pp. 247-252; Virgos, E., Telleria, J.L., Roe deer habitat selection in Spain: constraints on the distribution of a species (1998) Can. J. Zool. Rev. Can. Zool., 76, pp. 1294-1299; Vitousek, P.M., Beyond global warming: ecology and global change (1994) Ecology, 75, pp. 1861-1876; Wahlstrom, L.K., Kjellander, F., Ideal free distribution and natal dispersal in female roe deer (1995) Oecologia, 103, pp. 302-308; Wehausen, J.D., Ramey, R.R., Epps, C.W., Experiments in DNA extraction and PCR amplification from bighorn sheep feces: the importance of DNA extraction method (2004) J.Hered., 95, pp. 503-509; Williams, G.C., Natural Selection, the cost of reproduction, and a refinement of Lack's principle (1966) Am. Nat., 100, pp. 687-690; Wingfield, J.C., Comparative endocrinology, environment and global change (2008) Gen. Comp. Endocrinol., 157, pp. 207-216; Wingfield, J.C., Sapolsky, R.M., Reproduction and resistance to stress: when and how (2003) J.Neuroendocrinol., 15, pp. 711-724

    Research areas

  • Environmental change, Habitat quality, Immune function trade-off, Non-invasive, Stress, deer, environmental stress, fitness, habitat quality, immune system, physiology, reproductive productivity, steroid, trade-off
  • Sustainability Science