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Are degraded habitats from agricultural crops associated with elevated faecal glucocorticoids in a wild population of common vole (Microtus arvalis)?

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Abstract

The severe impact of agriculture on species’ abundance and diversity is widely recognized. However, its effects on the physiology of wild animal populations are poorly known. We analyzed faecal glucocorti¬coids levels in wild common voles (Microtus arvalis) living in a farmland landscape to test whether living in degraded habitats, such as crops, is correlated with increased glucocorticoids. Other factors such as sex, reproductive status, and population density were also considered. We captured voles with Sherman traps in crops and in their field margins which were comprised of semi-natural vegetation. We collected fresh faecal samples from captured individuals and quantified their levels of faecal corticosterone metabolites (FCM) in the laboratory. The quantification of FCM concentrations was performed by competitive enzyme immunoassay. Individuals captured within the crops had higher levels of FCM than those in field margins; females and breeding individuals exhibited higher FCM levels. In addition, FCM concentrations positively correlated with abundance of voles. Our results suggest that degraded habitats in agricultural landscapes are associated with increased glucocorticoid levels on common voles likely caused by a higher disturbance from agricultural practices and a lesser vegetation cover in crops compared with field margins.

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References

  • Ammann, K., 2004. Biosafety in agriculture: is it justified to compare directly with natural habitats? In: Wolfenbarger, L.L, Andow, DA, Hilbeck, A., et al (Eds.), Frontiers in Ecology, Forum: GM Crops: Balancing Predictions of Promise and Peril. ESA Ecological Society of America, Washington, pp. 154–160.

    Google Scholar 

  • Arlettaz, R., Krähenbühl, M., Almasi, B., Roulin, A., Schaub, M., 2010. Wildflower areas within revitalized agricultural matrices boost small mammal populations but not breeding Barn Owls. J. Ornithol. 151, 553–564.

    Article  Google Scholar 

  • Balmelli, L, Nentwig, W., Airoldi, J.P., 1999. Food preferences of the common vole Microtus arvalis in the agricultural landscape with regard to nutritional components of plants. Z. Säugetierkd. 64, 154–168.

    Google Scholar 

  • Bamberg, E., Palme, R., Meingassner, J.G., 2001. Excretion of corticosteroid metabolites in urine and faeces of rats. Lab. Anim. 35, 307–314.

    Article  CAS  PubMed  Google Scholar 

  • Barja, I., Escribano, G., Lara, C, Virgós, E., Benito, J., Rafart, E., 2012. Non-invasive monitoring of adrenocortical activity in European badgers (Meles meles) and effects of sample collection and storage on faecal cortisol metabolite concentrations. Anim. Biol. 62, 419–432.

    Article  Google Scholar 

  • Barja, I., Silván, G., Rosellini, S., Piñeiro, A., Illera, M.J., Illera, J.C., 2008. Quantification of sexual steroid hormones in faeces of Iberian wolf (Canis lupus signatus): a non-invasive sex typing method. Reprod. Domest. Anim. 43, 701–707.

    Article  CAS  PubMed  Google Scholar 

  • Barja, I., Silván, G., Rosellini, S., Piñeiro, A., González-Gil, A., Camacho, L., Illera, J.C., 2007. Stress physiological responses to tourist pressure in a wild population of European pine marten. J. Steroid Biochem. 104, 136–142.

    Article  CAS  Google Scholar 

  • Bauman, D.E., 2000. Regulation of nutrient partitioning during lactation: homeostasis and homeorhesis revisited. In: Cronjé, P.B. (Ed.), Ruminant Physiology: Digestion, Metabolism and Growth and Reproduction. CAB Publishing, New York, pp. 311–327.

    Chapter  Google Scholar 

  • Benton, T.G., Vickery, J.A., Wilson, J.D., 2003. Farmland biodiversity: is habitat heterogeneity the key? Trends Ecol. Evol. 18, 182–188.

    Google Scholar 

  • Boonstra, R., Hik, D., Singleton, G.R., Tinnikov, A., 1998. The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 79, 371–394.

    Article  Google Scholar 

  • Boyce, C.C.K., Boyce, J.L., 1988. Population biology of Microtus arvalis II. Natal and breeding dispersal of females. J. Anim. Ecol. 57, 723–736.

    Google Scholar 

  • Briner, T., Nentwig, W., Airoldi, J.P., 2005. Habitat quality of wildflower strips for common voles (Microtus arvalis) and its relevance for agriculture. Agric. Ecosyst. Environ. 105, 173–179.

    Article  Google Scholar 

  • Broom, D.M., Johnson, K.G., 1993. Stress and Animal Welfare. Chapman & Hall, London, UK.

    Book  Google Scholar 

  • Brotons, L, Mañosa, S., Estrada, J., 2004. Modelling the effects of irrigation schemes on the distribution of steppe birds in Mediterranean farmland. Biodivers. Conserv. 13, 1039–1058.

    Article  Google Scholar 

  • Brown, J.L., Wildt, D.E., 1997. Assessing reproductive status in wild felids by noninvasive faecal steroid monitoring. Int. Zoo Yearb. 35, 173–191.

    Article  Google Scholar 

  • Brown, R.W., 1999. Margin/field interfaces and small mammals. Aspects Appl. Biol. 54, 203–210.

    Google Scholar 

  • Burnham, K.P., Anderson, D.R., 2002. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, New York, USA.

    Google Scholar 

  • Busch, D.S., Hayward, L.S., 2009. Stress in a conservation context: a discussion of glucocorticoid actions and how levels change with conservation-relevant variables. Biol. Conserv. 142, 2844–2853.

    Article  Google Scholar 

  • Byrom, A.E., Karels, T.J., Krebs, C.J., Boonstra, R., 2000. Experimental manipulation of predationand food supply of arctic ground squirrels in the boreal forest. Can. J. Zool. 78, 1309–1319.

    Article  Google Scholar 

  • Carobrez, S.G., Gasparotto, O.C., Buwalda, B., Bohus, B., 2002. Long-term consequences of social stress on corticosterone and IL-1ß levels in endotoxin-challenged rats. Physiol. Behav. 76, 99–105.

    Article  CAS  PubMed  Google Scholar 

  • Cook, C.J., Mellor, D.J., Harris, P.J., Ingram, J.R., Matthews, L.R., 2000. Hands-on and hands-off measurement of stress. In: Moberg, G.P., Mench, J.A. (Eds.), The Biology of Animal Stress: Basic Principles and Implications for Animal Welfare. CABI Publishing, New York, pp. 123–146.

    Chapter  Google Scholar 

  • Crawley, M.J., 2007. The R Book. John Wiley & Sons, Chichester, UK.

    Book  Google Scholar 

  • Creel, S., Winnie, J.A., Christianson, D., 2009. Glucocorticoid stress hormones and the effect of predation risk on elk reproduction. Proc. Natl. Acad. Sci. U.S.A. 106, 12388–12393.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Creel, S., Fox, J.E., Hardy, A., Sands, J., Garrott, B., Peterson, R.O., 2002. Snowmobile activity and glucocorticoid stress responses in wolves and elk. Conserv. Biol. 16, 809–814.

    Article  Google Scholar 

  • Dehnhard, M., Clauss, M., Lechner-Doll, M., Meyer, H.H.D., Palme, R., 2001. Noninvasive monitoring of adrenocortical activity in roe deer (Capreolus capreolus) by measurement of fecal cortisol metabolites. Gen. Comp. Endocrinol. 123, 111–120.

    Article  CAS  PubMed  Google Scholar 

  • Donald, P.F., Green, R.E., Heath, M.F., 2001. Agricultural intensification and the collapse of Europe’s farmland bird populations. Proc. R. Soc. B 268, 25–29.

    Article  Google Scholar 

  • Fletcher, Q.E., Boonstra, R., 2006. Do captive male meadow voles experience acute stress in response to weasel odour? Can. J. Zool. 84, 583–588.

    CAS  Google Scholar 

  • Good, T., Khan, M.Z., Lynch, J.W., 2003. Biochemical and physiological validation of a corticosteroid radioimmunoassay for plasma and fecal samples in oldfield mice (Peromyscus polionotus). Physiol. Behav. 80, 405–411.

    Article  CAS  PubMed  Google Scholar 

  • Götz, A.A., Stefanski, V., 2007. Psychosocial maternal stress during pregnancy affects serum corticosterone, blood immune parameters and anxiety behaviour in adult male rat offspring. Physiol. Behav. 90, 108–115.

    Article  PubMed  CAS  Google Scholar 

  • Goymann, W., 2005. Noninvasive monitoring of hormones in bird droppings: physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann. N. Y. Acad. Sci. 1046, 35–53.

    Article  CAS  PubMed  Google Scholar 

  • Goymann, W., Wingfield, J.C., 2004. Allostatic load, social status and stress hormones: the costs of social status matter. Anim. Behav. 67, 591–602.

    Article  Google Scholar 

  • Goymann, W., East, M.L., Wachter, B., Höner, O.P., Möstl, E., Van’t Holf, T.J., Hofer, H., 2001. Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. Proc. R. Soc. B 268, 2453–2459.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graham, L.H., Brown, J.L., 1996. Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids. Zoo Biol. 15, 71–82.

    Article  CAS  Google Scholar 

  • Gurnell, J., Flowerdew, J.R., 1994. Live Trapping Small Mammals. A Practical Guide. The Mammal Society, London, UK.

    Google Scholar 

  • Halle, S., 1993. Diel pattern of predation risk in microtine rodents. Oikos 68, 510–518.

    Article  Google Scholar 

  • Harper, J.M., Austad, S.N., 2000. Fecal glucocorticoids: a noninvasive method of measuring adrenal activity in wild and captive rodents. Physiol. Biochem. Zool. 73, 12–22.

    Article  CAS  PubMed  Google Scholar 

  • Harper, J.M., Austad, S.N., 2001. Effect of capture and season on fecal glucocorticoid levels in deer mice (Peromyscus maniculatus) and red-backed voles (Clethrionomys gapperi). Gen. Comp. Endocrinol. 123, 337–344.

    Article  CAS  PubMed  Google Scholar 

  • Harper, J.M., Austad, S.N., 2004. Fecal corticosteroid levels in free-living populations of deer mice (Peromyscus maniculatus) and southern red-backed voles (Clethrionomys gapperi). Am. Midl. Nat. 152, 400–409.

    Article  Google Scholar 

  • Hayssen, V., Harper, J.M., DeFina, R., 2002. Fecal corticosteroids in agouti and non-agouti deer mice (Peromyscus maniculatus). Comp. Biochem. Phys. A 132, 439–446.

    Article  CAS  Google Scholar 

  • Heroldová, M., Jánová, E., Bryja, J., Tkadlec, E., 2005. Set-aside plots—source of small mammal pests? Folia Zool. 54, 337–350.

    Google Scholar 

  • Jacob, J., 2000. Populationsökologische Untersuchungen an Kleinnagern auf unterschiedlich bewirtschafteten Flächen der Unstrut-Aue. Friedrich-Schiller-University, Jena, Germany (Ph.D. thesis).

    Google Scholar 

  • Jacob, J., Brown, J.S., 2000. Microhabitat use, giving-up densities and temporal activity as short-and long-term anti-predator behaviors in common voles. Oikos 91, 131–138.

    Article  Google Scholar 

  • Krebs, J.R., Wilson, J.D., Bradbury, R.B., Siriwardena, G.M., 1999. The second silent spring? Nature 400, 611–612.

    Article  CAS  Google Scholar 

  • Lemen, C.A., Clausen, M.K., 1984. The effects of mowing on the rodent community of a native tall grass prairie in eastern Nebraska. Prairie Nat. 16, 5–10.

    Google Scholar 

  • Lepschy, M., Touma, C, Hruby, R., Palme, R., 2007. Non-invasive measurement of adrenocortical activity in male and female rats. Lab. Anim. 41, 372–387.

    Article  CAS  PubMed  Google Scholar 

  • Louch, CD., Higginbotham, M., 1967. The relation between social rank and plasma corticosterone levels in mice. Gen. Comp. Endocrinol. 8, 441–444.

    Article  CAS  PubMed  Google Scholar 

  • Mackin-Rogalska, R., 1981. Spatial structure of rodent populations co-occurring in different crop fields. Pol. Ecol. Stud. 7, 213–227.

    Google Scholar 

  • Mateo-Tomás, P., Olea, P.P., 2009. Combining scales in habitat models to improve conservation planning in an endangered vulture. Acta Oecol. 35, 489–498.

    Article  Google Scholar 

  • Melmed, S., Kleinberg, D., 2003. Anterior pituitary. In: Larsen, P.R., Kronenberg, H.M., Melmed, S., Polonsky, K.S. (Eds.), Williams Textbook of Endocrinology. Saunders, Philadelphia, pp. 177–279.

    Google Scholar 

  • Millspaugh, J.J., Washburn, B.E., Milanick, M.A., Slotow, R., van Dyk, G., 2003. Effects of heat and chemical treatments on fecal glucocorticoid measurements: implications for sample transport. Wildl. Soc. B. 31, 399–406.

    Google Scholar 

  • Millspaugh, J.J., Woods, R.J., Hunt, K.E., Raedeke, K.J., Brundige, G.C., Washburn, B.E., Wasser, S.K., 2001. Fecal glucocorticoid assays and the physiological stress response in elk. Wildl. Soc. B. 29, 899–907.

    Google Scholar 

  • Moen, A.N., Whittemore, S., Buxton, B., 1982. Effects of disturbance by snow-mobilies on heart rate of captive white-tailed deer. N. Y. Fish Game J. 29, 176–183.

    Google Scholar 

  • Monclús, R., Palomares, F., Tablado, Z., Martínez-Fontúrbel, A., Palme, R., 2009. Testing the threat-sensitive predator avoidance hypothesis: physiological responses and predator pressure in wild rabbits. Oecologia 158, 615–623.

    Article  PubMed  Google Scholar 

  • Monfort, S.L., Mashburn, K.L., Brewer, B.A., Creel, S.R., 1998. Evaluating adrenal activity in African wild dogs (Lycaon pictus) by fecal corticosteroid analysis. J. Zoo Wildl. Med. 29, 129–133.

    CAS  PubMed  Google Scholar 

  • Monfort, S.L., Wasser, S.K., Mashburn, K.L., Burke, M., Brewer, B.A., Creel, S.R., 1997. Steroid metabolism and validation of noninvasive endocrine monitoring in the African wild dog (Lycaon pictus). Zoo Biol. 16, 533–548.

    Article  CAS  Google Scholar 

  • Morrow, C.J., Kolver, E.S., Verkerk, G.A., Matthews, L.R., 2002. Fecal glucocorticoid metabolites as a measure of adrenal activity in dairy cattle. Gen. Comp. Endocrinol. 126, 229–241.

    Article  CAS  PubMed  Google Scholar 

  • Möstl, E., Palme, R., 2002. Hormones as indicators of stress. Domest. Anim. Endocrin. 23, 67–74.

    Article  Google Scholar 

  • Munck, A., Guyre, P.M., Holbrook, N.J., 1984. Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. Endocr. Rev. 5, 25–48.

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa, S., Schielzeth, H., 2012. A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142.

    Article  Google Scholar 

  • Nováková, M., Palme, R., Kutalová, H., Jansky, L., Frynta, D., 2008. The effects of sex, age and commensal way of life on levels of fecal glucocorticoid metabolites in spiny mice (Acomys cahirinus). Physiol. Behav. 95, 187–193.

    Article  PubMed  CAS  Google Scholar 

  • Olea, P.P., 2009. Analysing spatial and temporal variation in colony size: an approach using autoregressive mixed models and information theory. Popul. Ecol. 51, 161–174.

    Article  Google Scholar 

  • Olea, P.P., Sánchez-Barbudo, I.S., Viñuela, J., Barja, I., Mateo-Tomás, P., Pineiro, A., Mateo, R., Purroy, F.J., 2009. Lack of scientific evidence and precautionary principle in massive release of rodenticides threatens biodiversity: old lessons need new reflections. Environ. Conserv. 36, 1–4.

    Article  Google Scholar 

  • Orrock, J.L., Danielson, B.J., Brinkerhoff, R.J., 2004. Rodent foraging is affected by indirect, but not by direct, cues of predation risk. Behav. Ecol. 15, 433–437.

    Article  Google Scholar 

  • Palme, R., Robia, C, Messmann, S., Möstl, E., 1998. Measuring faecal cortisol metabolites: a non-invasive tool to evaluate adrenocortical activity in mammals. Adv. Ethol. 33, 27–46.

    Google Scholar 

  • Pineiro, A., Barja, I., Silván, G., Illera, J.C., 2012. Effects of tourist pressure and reproduction on physiological stress response in wildcats: management implications for species conservation. Wildl. Res. 39, 532–539.

    Article  Google Scholar 

  • Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., The R Development Core Team, 2013. NLME: Linear and Nonlinear Mixed Effects Models, https://doi.org/CRAN.R-project.org/package=nlme. R package version 3.1-109.

  • Place, N.J., Kenagy, G.J., 2000. Seasonal changes in plasma testosterone and glucocorticoids in free-living male yellowpine chipmunks and response to capture and handling. J. Comp. Physiol. B 170, 245–251.

    Article  CAS  PubMed  Google Scholar 

  • Preston, C.R., 1990. Distribution of raptor foraging in relation to prey biomass and habitat structure. Condor 92, 107–112.

    Article  Google Scholar 

  • R Development Core Team, 2013. R: a language and environment for statistical computing. In: R Foundation for Statistical Computing, Vienna, Austria.

    Google Scholar 

  • Raouf, S.A., Smith, L.C., Brown, M.B., Wingfield, J.C., Brown, C.R., 2006. Glucocorticoid hormone levels increase with group size and parasite load in cliff swallows. Anim. Behav. 71, 39–48.

    Article  Google Scholar 

  • Reeder, D.M., Kramer, K.M., 2005. Stress in free-ranging mammals: integrating physiology, ecology, and natural history. J. Mammal. 86, 225–235.

    Article  Google Scholar 

  • Robinson, R.A., Sutherland, W.J., 2002. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176.

    Article  Google Scholar 

  • Rogovin, K., Randall, J.A., Kolosova, I., Moshkin, M., 2003. Social correlates of stress in adult males of the great gerbil, Rhombomys opimus, in years of high and low population densities. Horm. Behav. 43, 132–139.

    Article  PubMed  Google Scholar 

  • Romero, L.M., 2004. Physiological stress in ecology: lessons from biomedical research. Trends Ecol. Evol. 19, 249–255.

    Article  PubMed  Google Scholar 

  • Sapolsky, R.M., 1992. Neuroendocrinology of the stress-response. In: Becker, J.B., Breedlove, S.M., Crews, D. (Eds.), Behavioral Endocrinology. MIT Press, Cambridge, pp. 287–324.

    Google Scholar 

  • Sapolsky, R.M., 2002. Endocrinology of the stress-response. In: Becker, J.B., Breedlove, S.M., Crews, D., McCarthy, M.M. (Eds.), Behavioral Endocrinology. MIT Press, Cambridge, pp. 409–450.

    Google Scholar 

  • Sapolsky, R.M., Romero, L.M., Munck, A.U., 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr. Rev. 21, 55–89.

    CAS  PubMed  Google Scholar 

  • Schradin, C, 2008. Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent. Horm. Behav. 53, 573–579.

    Article  CAS  PubMed  Google Scholar 

  • Sheffield, L.M., Crait,J.R., Edge, W.D., Wang, G., 2001. Response of American kestrels and gray-tailed voles to vegetation height and supplemental perches. Can. J. Zool. 79, 380–385.

    Article  Google Scholar 

  • Silvan, G., Martinez-Mateos, M.M., Blass, A., Camacho, L., Gonzalez-Gil, A., Garcia-Partida, P., Illera, J.C., 2007. The effect of long-term exposure to combinations of growth promoters in Long Evans rats, part 1: endocrine adrenal function. Anal. Chim. Acta 586, 246–251.

    Article  CAS  PubMed  Google Scholar 

  • Stewart, P.M., 2003. The adrenal cortex. In: Larsen, P.R., Kronenberg, H.M., Melmed, S., Polonsky, K.S. (Eds.), Williams Textbook of Endocrinology. Saunders, Philadel¬phia, pp. 491–551.

    Google Scholar 

  • Strier, K.B., Lynch, J.W., Ziegler, T.E., 2003. Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypox-anthus). Am. J. Primatol. 61, 85–99.

    Article  CAS  PubMed  Google Scholar 

  • Sullivan, T.P., Hogue, E.J., 1987. Influence of orchard floor management on vole and pocket gopher populations and damage in apple orchards. J. Am. Soc. Hortic. Sci. 112, 972–977.

    Google Scholar 

  • Tataranni, PA, Larson, D.E., Snitker, S., Young, J.B., Flatt, J.P., Ravussin, E., 1996. Effects of glucocorticoids on energy metabolism and food intake in humans. Am. J. Physiol-Endoc. M 271, 317–325.

    Google Scholar 

  • Thiel, D., Jenni-Eiermann, S., Palme, R., Jenni, L., 2011. Winter tourism increases stress hormone levels in the capercaillie Tetrao urogallus. Ibis 153, 122–133.

    Article  Google Scholar 

  • Touma, C, Palme, R., 2005. Measuring fecal glucocorticoid metabolites in mammals and birds: the importance of validation. Ann. N. Y. Acad. Sci. 1046, 54–74.

    Article  CAS  PubMed  Google Scholar 

  • Touma, C, Palme, R., Sachser, N., 2004. Analyzing corticosterone metabolites in fecal samples of mice: a noninvasive technique to monitor stress hormones. Horm. Behav. 45, 10–22.

    Article  CAS  PubMed  Google Scholar 

  • Touma, C, Sachser, N., Möstl, E., Palme, R., 2003. Effects of sex and time of day on metabolism and excretion of corticosterone in urine and feces of mice. Gen. Comp. Endocrinol. 130, 267–278.

    Article  CAS  PubMed  Google Scholar 

  • Tucker, G., Heath, M.F., Tomialojc, L., 1994. Birds in Europe: Their Conservation Status. BirdLife Conservation Series, Cambridge.

    Google Scholar 

  • van Meter, P.E., French, J.A., Dloniak, S.M., Watts, H.E., Kolowski, J.M., Holekamp, K.E., 2009. Fecal glucocorticoids reflect socio-ecological and anthropogenic stressors in the lives of wild spotted hyenas. Horm. Behav. 55, 329–337.

    Article  PubMed  CAS  Google Scholar 

  • von der Ohe, C.G., Wasser, S.K., Hunt, K.E., Servheen, C, 2004. Factors associated with fecal glucocorticoids in Alaskan brown bears (Ursus arctos horribilis). Physiol. Biochem. Zool. 77, 313–320.

    Article  PubMed  Google Scholar 

  • Washburn, B.E., Millspaugh, J.J., 2002. Effects of simulated environmental conditions on glucocorticoid metabolite measurements in white-tailed deer feces. Gen. Comp. Endocrinol. 127, 217–222.

    Article  CAS  PubMed  Google Scholar 

  • Wingfield, J.C, Romero, L.M., 2001. Adrenocortical responses to stress and their modulation in free-living vertebrates. In: McEwen, B.S., Goodman, H.M. (Eds.), Handbook of Physiology - Coping with the Environment: Neural and Endocrine Mechanisms. Oxford University Press, New York, pp. 211–234.

    Google Scholar 

  • Wingfield, J.C, Hunt, K., Breuner, C, Dunlap, K., Fowler, G.S., Freed, L, Lepson, J., 1997. Environmental stress, field endocrinology, and conservation biology. In: Clemmons, J.R., Buchholds, R. (Eds.), Behavioral Approaches to Conservation in the Wild. Cambridge University Press, Cambridge, pp. 95–131.

    Google Scholar 

  • Ylönen, H., Eccard, J.A., Jokinen, I., Sundell, J., 2006. Is the antipredatory response in behaviour reflected in stress measured in faecal corticosteroids in a small rodent? Behav. Ecol. Sociobiol. 60, 350–358.

    Article  Google Scholar 

  • Young, K.M., Walker, S.L., Lanthier, C, Waddell, W.T., Monfort, S.L., Brown, J.L., 2004. Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. Gen. Comp. Endocrinol. 137, 148–165.

    Article  CAS  PubMed  Google Scholar 

  • Zwijacz-Kozica, T., Selva, N., Barja, I., Silván, G., Martínez-Fernández, L, Illera, J.C, Jodłowski, M., 2013. Concentration of fecal cortisol metabolites in chamois in relation to tourist pressure in Tatra National Park (South Poland). Acta Theriol. 58, 215–222.

    Article  Google Scholar 

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  1. Departamento Biología, Unidad Zoología, Facultad Ciencias, Universidad Autónoma de Madrid, 28049, Madrid, Spain

    Álvaro Navarro-Castilla, Isabel Barja & Ana Piñeiro

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

    Pedro P. Olea & Patricia Mateo-Tomás

  3. Departamento de Fisiología (Fisiología Animal), Facultad de Veterinaria, Universidad Complutense de Madrid, 28040, Madrid, Spain

    Gema Silván & Juan Carlos Illera

  4. Unidad de Zoología, Departamento de Biología, Universidad Autónoma de Madrid, C/ Darwin 2, Campus Universitario de Cantoblanco, 28049, Madrid, Spain

    Álvaro Navarro-Castilla

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Navarro-Castilla, Á., Barja, I., Olea, P.P. et al. Are degraded habitats from agricultural crops associated with elevated faecal glucocorticoids in a wild population of common vole (Microtus arvalis)?. Mamm Biol 79, 36–43 (2014). https://doi.org/10.1016/j.mambio.2013.08.004

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