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

Acta Oecologica

Volumn 53, Issue , 2013, Pages 38-48

  Escribano Avila, Gema ^a   Pettorelli, Nathalie ^b   Virgós, Emilio ^a   Lara Romero, Carlos ^a   Lozano, Jorge ^a   Barja, Isabel ^c   Cuadra, Felipe S ^d   Puerta, Marisa ^d  

^a UNIVERSIDAD REY JUAN CARLOS   (Spain)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

^c UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Environmental change; Habitat quality; Immune function trade off; Non invasive; Stress

Indexed keywords

DEER; ENVIRONMENTAL STRESS; FITNESS; HABITAT QUALITY; IMMUNE SYSTEM; PHYSIOLOGY; REPRODUCTIVE PRODUCTIVITY; STEROID; TRADE-OFF;

EID: 84884236636     PISSN: 1146609X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.actao.2013.08.003     Document Type: Article

References (91)

1. Abáigar T., Domene M.A., Palomares F. Effects of fecal age and seasonality or steroid hormone concentration as a reproductive parameter in field studies. Eur. J. Wildl. Res. 2010, 56:781-787.
2. 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. J.Biogeogr. 2005, 32:1671-1680.
3. Araujo M.B., Rahbek C. How does climate change affect biodiversity?. Science 2006, 313:1396-1397.
4. 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. J.Wildl. Manage 2003, 67:477-484.
5. 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). Mammalia 1997, 61:589-602.
6. Blottner S., Hingst O., Meyer H.H.D. Seasonal spermatogenesis and testosterone production in roe deer (Capreolus capreolus). Reproduction 1996, 108:299-305.
7. Bonier F., Martin P.R., Moore I.T., Wingfield J.C. Do baseline glucocorticoids predict fitness?. Trends. Ecol. Evol. 2009, 24:634-642.
8. Bonier F., Moore I.T., Robertson R.J. The stress of parenthood? Increased glucocorticoids in birds with experimentally enlarged broods. Biol. Lett. 2011, 7:944-946.
9. Boonstra R. Coping with changing northern environments: the role of the stress axis in birds and mammals. Integr. Comp. Biol. 2004, 44:95-108.
10. Brisbin J.T., Gong J., Shafit S. Interactions between commensal bacteria and the gut-associated immune system of the chicken. Anim. Health. Res. Rev. 2008, 9:101-110.
11. 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. Comp. Bicochem. Physiol. A-mol. Integr. Physiol. 1991, 99:645-650.
12. 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). Comp. Bicochem. Physiol. B - Biochem. Mol. Biol. 1996, 115:417-420.
13. Busch D.S., Hayward L.S. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol. Conserv. 2009, 142:2844-2853.
14. 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. J.Anim. Ecol. 2011, 80:640-649.
15. Cerutti A., Rescigno M. The biology of intestinal immunoglobulin A responses. Immunity 2008, 28:740-750.
16. Comrey A.L., Lee H.B. AFirst Course in Factor Analysis 1992, Lawrence Erlbaum Associates, Inc Publishers, Hillsdale, New Jersey. second ed.
17. Cote S.D., Festa-Bianchet M. Birthdate, mass and survival in mountain goat kids: effects of maternal characteristics and forage quality. Oecologia 2001, 127:230-238.
18. Creel S., Fox J.E., Hardy A., Sands J., Garrott B., Peterson R.O. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv. Biol. 2002, 16:809-814.
19. Davies G., Stear M.J., Bishop S.C. Genetic relationships between indicator traits and nematode parasite infection levels in 6-month-old lambs. Anim. Sci. 2005, 80:143-150.
20. Demas G.E., Drazen D.L., Nelson R.J. Reductions in total body fat decrease humoral immunity. Proc. R. Soc. B - Biol. Sci. 2003, 270:905-911.
21. Demas G.E., Zysling D.A., Beechler B.R., Muehlenbein M.P., French S.S. Beyond phytohaemagglutinin: assessing vertebrate immune function across ecological contexts. J.Anim. Ecol. 2011, 80:710-730.
22. Dray S., Dufour A.B. The ade4 package: implementing the duality diagram for ecologists. J.Stat. Softw. 2007, 22:1-20.
23. Dumonceaux G.A., Bauman J.E., Camilo G.R. Evaluation of progesterone levels in feces of captive reticulated giraffe (Giraffa camelopardalis reticulata). J.Zoo. Wildl. Med. 2006, 37:255-261.
24. 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. Funct. Ecol. 2009, 24:149-158.
25. Ezenwa V.O., Stefan Ekernas L., Creel S. Unravelling complex associations between testosterone and parasite infection in the wild. Funct. Ecol. 2012, 26:123-133.
26. FIDA Ecología y caracterización genética de las poblaciones de corzo en la Comunidad de Madrid 2008, Madrid.
27. 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. Mol. Ecol. 1999, 8:879-883.
28. 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. Environ. Conserv. 2009, 36:253-260.
29. 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. J.Wildl. Dis. 1998, 34:126-131.
30. Gendreau Y., Cote S.D., Festa-Bianchet M. Maternal effects on post-weaning physical and social development in juvenile mountain goats (Oreamnos americanus). Behav. Ecol. Sociobiol. 2005, 58:237-246.
31. 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. Conserv. Biol. 2008, 22:1590-1599.
32. 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). Anim. Reprod. Sci. 2006, 96:79-88.
33. 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. Wildl. Biol. 1996, 2:107-111.
34. 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. J.Appl. Ecol. 2009, 46:582-589.
35. Hasselquist D., Wasson M.F., Winkler D.W. Humoral immunocompetence correlates with date of egg-laying and reflects work load in female tree swallows. Behav. Ecol. 2001, 12:93-97.
36. 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. Ecosphere 2011, 2:1-20.
37. Hewison A.J.M., Morellet N., Verheyden H., Daufresne T., Angibault J.M., Cargnelutti B., Merlet J., Picot D., Rames J.L., Joachim J., Lourtet B., Serrano E., Bideau E., Cebe N. Landscape fragmentation influences winter body mass of roe deer. Ecography 2009, 32:1062-1070.
38. Hoffmann B., Barth D., Karg H. Progesterone and estrogen levels in peripheral plasma of the pregnant and non-pregnant roe deer (Capreolus capreolus). Biol. Reprod. 1978, 19:931-935.
39. Holand Ø., Mysterud A., Wannag A., Linnell J.D.C. Roe deer in northern environments: physiology and behaviour. The European Roe Deer: the Biology of Success 1998, 117-138. Scandinavian University Press, Oslo. R. Anderson, P. Duncan, J.D.C. Linnell (Eds.).
40. Huber S., Palme R., Arnold W. Effects of season, sex, and sample collection on concentrations of fecal cortisol metabolites in red deer (Cervus elaphus). Gen. Comp. Endocrinol. 2003, 130:48-54.
41. 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. Remote Sens. Environ. 2002, 83:195-213.
42. Husak J.F., Moore I.T. Stress hormones and mate choice. Trends. Ecol. Evol. 2008, 23:532-534.
43. Kaiser H.F. The application of electronic comptures to factor analysis. Educ. Psychol. Meas. 1960, 20:141-151.
44. Kamler J., Homolka M. Faecal nitrogen: a potential indicator of red and roe deer diet quality in forest habitats. Folia Zool. 2005, 54:89-98.
45. 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. Wildl. Biol. 2004, 10:235-240.
46. Kapke C.A., Arcese P., Ziegler T.E., Scheffler G.R. Estradiol and progesterone metabolite concentration in white-tailed deer (Odocoileus virginianus) feces. J.Zoo. Wildl. Med. 1999, 30:361-371.
47. 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). Zoo Biol. 1992, 11:121-131.
48. 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). Reproduction 2001, 121:863-871.
49. 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?. Horm. Behav. 2003, 43:489-502.
50. Linnell J.D.C., Andersen R. Timing and synchrony of birth in a hider species, the roe deer Capreolus capreolus. J.Zool. 1998, 244:497-504.
51. Loreau M., Naeem S., Inchausti P., Bengtsson J., Grime J.P., Hector A., Hooper D.U., Huston M.A., Raffaelli D., Schmid B., Tilman D., Wardle D.A. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 2001, 294:804-808.
52. Mateos-Quesada P. Corzo - Capreolus capreolus. Enciclopedia Virtual de los Vertebrados Españoles 2011, Museo Nacional de Ciencias Naturales, Madrid. L.M. Carrascal, A. Salvador (Eds.).
53. McEwen B.S., Wingfield J.C. The concept of allostasis in biology and biomedicine. Horm. Behav. 2003, 43:2-15.
54. McNamara J.M., Buchanan K.L. Stress, resource allocation, and mortality. Behav. Ecol. 2005, 16:1008-1017.
55. Millennium E.A Ecosystems and Human Well-being: Synthesis 2005, Island Press, Washington, D.
56. Monfort S.L., Martinet C., Wildt D.E. Urinary steroid metabolite profiles in female Pere-Davids deer (Elaphurus davidianus). J.Zoo. Wildl. Med. 1991, 22:78-85.
57. Mormede P., Andanson S., Auperin B., Beerda B., Guemene D., Malmkvist J., Manteca X., Manteuffel G., Prunet P., van Reenen C.G., Richard S., Veissier I. Exploration of the hypothalamic-pituitary-adrenal function as a tool to evaluate animal welfare. Physiol. Behav. 2007, 92:317-339.
58. Navarro-Gonzalez N., Verheyden H., Hoste H., Cargnelutti B., Lourtet B., Merlet J., Daufresne T., Lavin S., Hewison A.J.M., Morand S., Serrano E. Diet quality and immunocompetence influence parasite load of roe deer in a fragmented landscape. Eur. J. Wildl. Res. 2011, 57:639-645.
59. Neish A.S. Microbes in gastrointestinal health and disease. Grastroenterology 2009, 136:65-80.
60. Parmesan C., Yohe G. Aglobally coherent fingerprint of climate change impacts across natural systems. Nature 2003, 421:37-42.
61. Peters I.R., Calvert E.L., Hall E.J., Day A.J. Measurement of immunoglobulin concentrations in the feces of healthy dogs. Clin. Diagn. Lab. Immunol. 2004, 11:841-848.
62. Peterson D.A., McNulty N.P., Guruge J.L., Gordon J.L. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2007, 2:328-339.
63. 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. Proc. R. Soc. B - Biol. Sci. 2005, 272:2357-2364.
64. Pettorelli N., Gaillard J.M., Mysterud A., Duncan P., Stenseth N.C., Delorme D., Van Laere G., Toigo C., Klein F. Using a proxy of plant productivity (NDVI) to find key periods for animal performance: the case of roe deer. Oikos 2006, 112:565-572.
65. Phalipon A., Cardona A., Kraehenbuhl J.P., Edelman L., Sansonetti P.J., et al. Secretory component: a new role in secretory IgA-mediated immune exclusion invivo. Immunity 2002, 17:107-115.
66. Pinheiro J., Bates D., DebRoy S., Sarkar D.R. nlme: Linear and Nonlinear Mixed effects Models 2012, 3.1.-104. R.D.C.T.R.p.v. (Ed.).
67. 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. Zoo Biol. 1994, 13:129-147.
68. 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. Biol. Reprod. 2002, 66:305-312.
69. Romero L.M. Physiological stress in ecology: lessons from biomedical research. Trends. Ecol. Evol. 2004, 19:249-255.
70. Romero L.M., Wikelski M. Corticosterone levels predict survival probabilities of Galapagos marine iguanas during El Nino events. Proc. Natl. Sci. U.S.A 2001, 98:7366-7370.
71. 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. Horm. Behav. 2010, 57:134-139.
72. Ryg Morten Physiological control of growth, reproduction and lactation in deer. Rangifer 1986, 1:261-266.
73. Sapolsky R.M., Romero L.M., Munck A.U. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 2000, 21:55-89.
74. 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. Acta. Endocrinol. 1982, 99:295-301.
75. 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). Reproduction 1992, 95:693-700.
76. Sheldon B.C., Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends. Ecol. Evol. 1996, 11:317-321.
77. Sheriff M., Dantzer B., Delehanty B., Palme R., Boonstra R. Measuring stress in wildlife: techniques for quantifying glucocorticoids. Oecologia 2011, 166:869-887.
78. 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. J.Comp. Pathol. 1985, 95:235-245.
79. Snoeck V., Peters I.R., Cox E. The IgA system: a comparison of structure and function in different species. Vet. Res. 2006, 37:455-467.
80. Speakman J.R. The physiological costs of reproduction in small mammals. Philos. Trans. R. Soc. B - Biol. Sci. 2008, 363:375-398.
81. 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. J.Wildl. Manage. 1999, 63:561-569.
82. 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. Behav. Ecol. Sociobiol. 2008, 62:1591-1600.
83. Team, R.D.C R: a Language and Environment for Statistical Computing 2011, R Foundation for Statistical Computing, Vienna, Austria.
84. Telleria J.L., Virgos E. Distribution of an increasing roe deer population in a fragmented Mediterranean landscape. Ecography 1997, 20:247-252.
85. Virgos E., Telleria J.L. Roe deer habitat selection in Spain: constraints on the distribution of a species. Can. J. Zool. Rev. Can. Zool. 1998, 76:1294-1299.
86. Vitousek P.M. Beyond global warming: ecology and global change. Ecology 1994, 75:1861-1876.
87. Wahlstrom L.K., Kjellander F. Ideal free distribution and natal dispersal in female roe deer. Oecologia 1995, 103:302-308.
88. 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. J.Hered. 2004, 95:503-509.
89. Williams G.C. Natural Selection, the cost of reproduction, and a refinement of Lack's principle. Am. Nat. 1966, 100:687-690.
90. Wingfield J.C. Comparative endocrinology, environment and global change. Gen. Comp. Endocrinol. 2008, 157:207-216.
91. Wingfield J.C., Sapolsky R.M. Reproduction and resistance to stress: when and how. J.Neuroendocrinol. 2003, 15:711-724.