Abstract
We studied the factors that determined kidney fat stores (KFs) and kidney stores (Ks)—defined as the residuals from the linear regression of kidney mass and kidney fat, respectively, on body weight—in 463 Iberian wild goats (Capra pyrenaica) from the Sierra Nevada (southern Spain). Despite the fact that body stores in both sexes were highest during the warmest months of the year and lowest during the coldest months when food resources are limited, the observed pattern was sex- and age-dependent. The KFs of male goats fell more than those of females in winter, and the yearlings of both sexes needed one season more than young or adults to restore their KFs. Goats of all age classes showed the same seasonal patterns in their Ks, although Ks were lower in females than in males throughout the yearly cycle. In addition, we found strong delayed effects of both snowfalls and population density on body stores, and in years with a lot of snow, goats' KFs reached their lowest levels in the current winter–spring, but the highest in the following summers and autumns. This pattern was less noticeable in the Ks. Population density negatively affected the body stores of wild goats, especially in winter, and the amount of snow fallen in the year of birth (cohort effect) did not seem to influence the body stores in our data set. In addition, we assessed the accuracy of the residuals from the regression between body size and body mass for monitoring body condition of live wild goats and concluded that, although it poorly indicates fat stores, it could be used as a general proxy of body condition. Finally, we discuss the expected effects of climate warming on body stores in this Mediterranean Caprinae species.
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References
Anderson DR, Burnham KP, White GA (2001) Kullback–Leibler information in resolving natural resource conflicts when definitive data exist. Wildl Soc Bull 29:1260–1270
Andersson MB (1994) Sexual selection. Princeton University Press, Princeton, New York, USA
Barboza PS, Hume ID (2006) Physiology of intermittent feeding: integrating responses of vertebrates to nutritional deficit and excess. Physiol Biochem Zool 79:250–264
Barboza PS, Parker KL (2008) Allocating protein to reproduction in Artic reindeer and caribou. Physiol Biochem Zool 81:835–855
Bishop CJ, Unsworth JW, Garton EO (2005) Mule deer survival among adjacent populations in southwest Idaho. J Wildl Manage 69:311–321
Brown RD, Hellgre EC, Abbott M, Ruthven DC, Bingham RL (1995) Effects of dietary energy and protein restriction on nutritional indices of female white-tailed deer. J Wildl Manage 59:595–609
Buckland ST, Anderson DR, Burnham KP, Laake JL, Borchers DL, Thomas L (2001) Introduction to distance sampling: estimating abundance of biological populations. Oxford University Press, USA
Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer-Verlag, New York, USA
Burrin DG, Britton RA, Ferrell CL, Bauer ML (1992) Level of nutrition and synthetic capacity and nucleic acid content in sheep. J Anim Sci 70:1137–1145
Burrin DG, Ferrel CL, Britton RA, Bauer ML (1990) Level of nutrition and visceral organ size and metabolic activity in sheep. Br J Nutr 64:439–448
Chen X (1996) Studying school size effects in line transect sampling using the kernel method. Biometrics 52:1283–1294
Choquenot D (1991) Density-dependent growth, body condition, and demography in feral donkeys: testing the food hypothesis. Ecology 72:805–813
Christians JK (1999) Controlling for body mass effects: is part–whole correlation important? Physiol Biochem Zool 72:250–253
Clutton-Brock TH, Albon SD, Guinness FE (1981) Parental investment in male and female offspring in polygynous mammals. Nature 289:478–489
Consejería de Medio Ambiente (2004) Sierra Nevada: basic data. Grupo Entorno, Granada, Spain
Crampe JP, Gaillard J-M, Loison A (2002) Winter snowfall: a variable factor in recruitment by isard populations (Rupicapra pyrenaica pyrenaica). Can J Zool 80:1306–1312
Dailey TV, Hobbs NT (1989) Travel in Alpine terrain: energy expenditures for locomotion by mountain goats and bighorn sheep. Can J Zool 67:2368–2375
Fandos P (1991) La cabra montés (Capra pyrenaica) en el Parque Natural de las sierras de Cazorla Segura y las Villas. ICONA-CSIC, Madrid, Spain
Fandos P, Vigal CR, Fernandez-Lopez JM (1987) Weight estimation of Spanish ibex, Capra pyrenaica, and chamois, Rupicapra rupicapra (Mammalia, Bovidae). Mamm biol (formerly Zeitschrift für Säugetierkunde) 54:239–242
Ferguson MAD, Messier F (2000) Mass emigration of arctic tundra caribou from a traditional winter range: population dynamics and physical condition. J Wildl Manage 64:168–178
Ferrel CL, Jenkins TG (1985) Cow type and the nutritional environment: nutritional aspects. J Anim Sci 61:725–741
Festa-Bianchet M, Jorgenson J, King WJ, Smith KG, Wishart WD (1996) The development of sexual dimorphism, seasonal and lifetime mass changes in bighorn sheep. Can J Zool 74:330–342
Festa-Bianchet M, Jorgenson JT, Réale D (2000) Early development, adult mass, and reproductive success in bighorn sheep. Behav Ecol 11:633–639
Flydal K, Reimers E (2002) Relationship between calving time and physical condition in three wild reindeer Rangifer tarandus populations in southern Norway. Wildl Biol 8:145–151
Forsyth DM, Duncan RP, Tustin KG, Gaillard J-M (2005) A substantial energetic cost to male reproduction in a sexually dimorphic ungulate. Ecology 86:2154–2163
García-Berthou E (2001) On the misuse of residuals in ecology: testing regression residuals vs. the analysis of covariance. J Anim Ecol 70:708–711
Garroway CJ, Broders HG (2005) The quantitative effects of population density and winter weather on the body condition of white-tailed deer (Odocoileus virginianus) in Nova Scotia, Canada. Can J Zool 83:1246–1256
Goodson AD, Stevens DR, Bailey JA (1991) Effects of snow on foraging ecology and nutrition of bighorn sheep. J Wildl Manage 55:214–222
Granados JE, Fandos P, Márquez FJ, Soriguer RC, Pérez JM (2001) Allometric growth in the Spanish ibex, Capra pyrenaica. Folia Zool 50:234–238
Granados JE, Pérez JM, Soriguer RC, Fandos P, Ruiz-Martinez I (1997) On the biometry of the Spanish ibex Capra pyrenaica, from Sierra Nevada (Southern Spain). Folia Zool 46:9–14
Green AJ (2001) Mass/length residuals: measures of body condition or generators of spurious results? Ecology 82:1473–1483
Hjeljord O, Histøl T (1999) Range-body mass interactions of a northern ungulate: a test of hypothesis. Oecologia 119:326–339
Hurrell JW, van Loo NH (1997) Decadal variations in climate associated with the North Atlantic oscillation. Clim Chang 36:301–326
Igota H, Sakuragi M, Uno H, Kaji K, Kaneko M, Akamatsu R, Maekawa K (2004) Seasonal migration patterns of female sika deer in eastern Hokkaido, Japan. Ecol Res 19:169–178
Jensen PG, Pekins PJ, Holter JB (1999) Compensatory effect of the heat increment of feeding on thermoregulation costs of white-tailed deer fawns in winter. Can J Zool 77:1474–1485
Johnson JB, Omland KS (2004) Model selection in ecology and evolution. Trends Ecol Evol 19:101–108
Jönsson KI (1997) Capital and income breeding as alternative tactics of resource use in reproduction. Oikos 78:57–66
Kabbali A, Johnson WL, Goodrich RD, Allen CE (1992a) Effects of undernutrition and refeeding on weights of body parts and chemical components of growing Moroccan lambs. J Anim Sci 70:2859–2865
Kabbali A, Johnson WL, Johnson DW, Goodrich RD, Allen CE (1992b) Effects of compensatory growth on some body component weights and on carcass and noncarcass composition of growing lambs. J Anim Sci 70:2852–2858
King JR, Murphy ME (1985) Periods of nutritional stress in the annual cycle of endotherms: fact or fiction? Am Zool 25:955–964
Lesage L, Crête M, Ouellet J-P (2001) Evidence for trade-off between growth and body reserves in northern white-tailed deer. Oecologia 126:30–41
Levins R (1968) Evolution in changing environments: some theoretical explorations. Princeton University Press, Princeton, USA
Lindström Å, Piersma T (1993) Mass changes in migrating birds: the evidence for fat and protein storage re-examined. Ibis 135:70–78
Loison A, Langvatn R (1998) Short- and long-term effects of winter and spring weather on growth and survival of red deer in Norway. Oecologia 116:498–500
Martínez T (2000) Diet selection by Spanish ibex in early summer in Sierra Nevada. Acta Theriol 45:335–346
Mech LD, McRoberts RE, Peterson RO, Page RE (1987) Relationship of deer and moose populations to previous winters' snow. J Anim Ecol 56:615–627
Mitchell B, McCowan D, Nicholson IA (1976) Annual cycles of body weight and condition in Scottish red deer, Cervus elaphus. J Zool 180:107–127
Mysterud A, Langvetn R, Stenseth NC (2004) Patterns of reproductive effort in male ungulates. J Zool 264:209–215
Parker KL, Barboza PS, Gillinngham MP (2009) Nutrition integrates environmental responses of ungulates. Func Ecol 23:57–69
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Syst 37:637–669
Patterson B, Power V (2002) Contributions of forage competition, harvest, and climate fluctuation to changes in population growth of northern white-tailed deer. Oecologia 130:62–71
Pélabon C, Gaillard J-M, Loison A, Portier C (1995) Is sex biased maternal care limited by total maternal expenditure in polygnous ungulates. Behav Ecol Sociobiol 37:311–319
Pérez JM, Alpizar-Jara R (2008) Towards the use of distance sampling to monitorize mountain ungulates numbers. In: J Chen, C Guo (eds) Ecosystem Ecology Reserch Trends. Nova Science Publishers. 9–20
Pérez JM, Granados JE, Soriguer RC (1994) Population dynamic of the Spanish ibex Capra pyrenaica in Sierra Nevada Natural Park (southern Spain). Acta Theriol 39:289–294
Pérez JM, Granados JE, Soriguer RC, Fandos P, Márquez FJ, Crampe JP (2002) Distribution, status and conservation problems of the Spanish Ibex, Capra pyrenaica (Mammalia: Artiodactyla). Mammal Rev 32:26–39
Pérez JM, Ruiz-Martinez I, Granados JE, Soriguer RC, Fandos P (1997) The dynamics of sarcoptic mange in the ibex population of Sierra Nevada in Spain: the influence of climatic factors. J Wildl Res 2:86–89
Pérez-Barbería FJ, Mutuberría G, Nores C (1998) Reproductive parameters, kidney fat index, and grazing activity relationships between the sexes in Cantabrian chamois Rupicapra pyrenaica parva. Acta Theriol 43:311–324
Pettorelli N, Pelletier F, von Hardenberg A, Festa-Bianchet M, Côté SD (2007) Early onset of vegetation growth vs rapid green-up: impacts on juvenile mountain ungulates. Ecology 88:381–390
Piersma T, Drent J (2003) Phenotypic flexibility and the evolution of organismal design. Trends Ecol Evol 18:228–233
Post E, Stenseth NC (1999) Climatic variability, plant phenology, and northern ungulates. Ecology 80:1322–1339
R Development Core Team 2. 9. 2 (2009) A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: http://www.R-project.org, Accessed on: 15/12/2009
Riney T (1955) Evaluating condition of free-ranging red deer (Cervus elaphus), with special reference to New Zealand. N Z Jl Sci Technol 36:430–463
Ruckstuhl KE, Festa-Bianchet M, Jorgenson JT (2003) Bite rates in Rocky Mountain bighorn sheep (Ovis canadensis): effects of season, age, sex and reproductive status. Behav Ecol Sociobiol 54:167–173
Sæther BE, Gravem AJ (1988) Annual variation in winter body condition of Norwegian moose calves. J Wildl Manage 52:333–336
Sarasa M, Serrano E, Pérez J, Soriguer R C, Gonzalez G, Joachim J, Granados J E (2010) Effect of season, age and body condition on allocation to testis mass in Iberian ibex. J Zool. doi: 10.1111/j.1469-7998.2009.00689.x:
Schulte-Hostedde AI, Millar JS, Hickling GJ (2001) Evaluating body condition in small mammals. Can J Zool 79:1021–1029
Schulte-Hostedde AI, Zinner B, Millar JS, Hickling GJ (2005) Restitution of mass-size residuals: validating body condition indices. Ecology 86:155–163
Scmidt-Nielsen B, O'Dell R (1961) Structure and concentrating mechanism in the mammalian kidney. Am J Physiol 200:1119–1124
Serrano E, Alpizar-Jara R, Morellet N, Hewison AJM (2008a) A half a century of measuring ungulate body condition using indices: is it time for a change? Eu J Wildl Res 54:675–680
Serrano E, González FJ, Granados JE, Moço G, Fandos P, Soriguer RC, Pérez JM (2008b) The use of total serum proteins and tryglycerides for monitoring body condition in the Iberian wild goat (Capra pyrenaica). J Zoo Wild Med 39:646–649
Serrano E, Pérez JM, Christiansen P, Gállego L (2006) Sex-difference in the ossification rate of the appendicular skeleton in Capra pyrenaica Schinz, 1838, and its utility in the sex identification of long bones. Anat Histol Embryol 35:69–75
Stamps JA (1993) Sexual size dimorphism in species with asymptotic growth. Biol J Linn Soc 50:123–145
Stewart KM, Bowyer RT, Dick BL, Johnson BK, Kie JG (2005) Density-dependent effects on physical condition and reproduction in North American elk: an experimental test. Oecologia 143:85–93
Thomas L, Laake JL, Bishop JRB, Marques FFC, Buckland ST, Borchers DL, Anderson DR, Burnham KP, Hedley SL, Pollard JH, Bishop JRB, Marques TA (2005) Distance 5.0. beta 4. Research Unit for Wildlife Population Assessment; University of St. Andrews. Available at: http://www.ruwpa.st-and.ac.uk/distance/Accessed on 12/04/2009
Toïgo C, Gaillard J-M, Festa-Bianchet M, Largo E, Michaellet J, Maillard D (2007) Sex- and age-specific survival of the highly dimorphic Alpine ibex: evidence for a conservative life-history tactic. J Anim Ecol 76:679–686
Torbit SC, Carpenter LH, Swift DM, Alldredge AW (1985) Differential loss of fat and protein by mule deer during winter. J Wildl Manage 49:80–85
Tyler NJC (1986) The relationship between fat content of Svalbard reindeer in autumn and their death from starvation in winter. Rangifer 1:311–314
Varios A (1987) La vegetación de España. Universidad de Alcalá de Henares, Alcalá de Henares, Spain
Verme LJ, Ozoga JJ (1980) Effects of diet on growth and lipogenesis in deer fawns. J Wildl Manage 44:315–324
Vincent JP, Hewison AJM, Angibault J-M (1995) The influence of increasing density on body weight, kid production, home range and winter grouping in roe deer (Capreolus capreolus).-Journal of Zoology, London 236:371–382.
Visscher DR, Merrill EH, Fortin D, Frair JL (2006) Estimating woody browse availability for ungulates at increasing snow depths. For Ecol Manage 222:348–354
Walker MD, Webber PJ, Arnold EH, Eberte-May D (1994) Effects of interannual climate variation on aboveground phytomass in Alpine vegetation. Ecology 75:393–408
Wood S (2006) Generalized additive models: an introduction with R. CEC Statistic, Boca Raton, USA
Yokoyama M, Onuma M, Suzuki M, Kaji K (2001) Seasonal fluctuations of body condition in northern sika deer on Hokkaido Island, Japan. Acta Theriol 46:419–428
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM (2009) Mixed effects models and extension in ecology with R. Springer, New York, USA
Acknowledgments
We are grateful to J. Navarro, M. A. López, A. R. Huete, M. C. Pérez and J. García for their help with the field and laboratory work. We would also like to thank David Forsyth, John P. Ball, A. J. M. Hewison, G. Gonzalez, J. F. Gerard and Sandro Lovari for helpful comments on previous drafts of this manuscript. Marco Festa-Bianchet, G. Hilton and A. Schulte-Hostedde participated in stimulating discussions on the best way of estimating wild goat body stores. Special thanks go to Marcus Clauss and Jean Michel-Gaillard for their constructive criticism on the manuscript. E. Serrano is supported by the Juan de la Cierva Postdoctoral Programme of the MICINN (Spain) and M. Sarasa by a MENRT grant (France). Research activities were also partially supported by the Plan Andaluz de Investigación, Junta de Andalucía (RNM–118). Climatologic data were kindly provided by Cetursa, Sierra Nevada, S.A.
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Table S1
Reference values in grammes for kidney fat (KF) and fat-free kidney mass (KM) in female and male Iberian wild goats from the Sierra Nevada mountains. Yearlings (1 ≤ 2 years), prime-age females and growing males (2 ≤ age < 5 years), adults (≥5 years) (DOC 51 kb)
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Serrano, E., Granados, J.E., Sarasa, M. et al. The effects of winter severity and population density on body stores in the Iberian wild goat (Capra pyrenaica) in a highly seasonal mountain environment. Eur J Wildl Res 57, 45–55 (2011). https://doi.org/10.1007/s10344-010-0398-5
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DOI: https://doi.org/10.1007/s10344-010-0398-5