Please cite this article in press as: Navarro-Castilla, Á., et al., Are degraded habitats from agricultural crops associated with elevated faecal
glucocorticoids in a wild population of common vole (Microtus arvalis)? Mammal. Biol. (2013), http://dx.doi.org/10.1016/j.mambio.2013.08.004
ARTICLE IN PRESS
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MAMBIO-40628; No. of Pages 8
Mammalian Biology xxx (2013) xxx–xxx
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Mammalian Biology
j ourna l ho me page: www.elsevier.com/locate /mambio
Original Investigation
Are degraded habitats from agricultural crops associated with
elevated faecal glucocorticoids in a wild population of common vole
(Microtus arvalis)?
Álvaro Navarro-Castilla
a,∗
, Isabel Barja
a
, Pedro P. Olea
b
, Ana Pi˜ neiro
a
,
Patricia Mateo-Tomás
b
, Gema Silván
c
, Juan Carlos Illera
c
a
Departamento Biología, Unidad Zoología, Facultad Ciencias, Universidad Autónoma de Madrid, 28049 Madrid, Spain
b
Instituto de Investigación en Recursos Cinegéticos (IREC), CSIC-UCLM-JCCM, Ronda de Toledo s/n, 13071 Ciudad Real, Spain
c
Departamento de Fisiología (Fisiología Animal), Facultad de Veterinaria, Universidad Complutense de Madrid, 28040 Madrid, Spain
a r t i c l e i n f o
Article history:
Received 30 January 2013
Accepted 13 August 2013
Available online xxx
Keywords:
Anthropogenic disturbance
Faecal corticosterone metabolites
Field margins
Managed landscapes
Small mammals
a b s t r a c t
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 disturb-
ance from agricultural practices and a lesser vegetation cover in crops compared with field margins.
© 2013 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
Introduction
Agriculture is considered to be a major cause of global change
and biodiversity loss. While it is widely known that agricul-
ture affects the composition and abundance of species (Tucker
et al., 1994; Krebs et al., 1999; Donald et al., 2001; Robinson and
Sutherland, 2002; Benton et al., 2003; Brotons et al., 2004), its
effects on other more subtle components such as physiological
changes in wild animals are largely unknown.
Agricultural activities are human-made interventions that
involve the modification of the original natural ecosystems which
are replaced by a series of degraded habitats that are exposed to
continuous modifications such as tilling, harvesting or crop rotation
(Ammann, 2004). Since habitat change may act as stressor in wild
animals (Wingfield et al., 1997), the environmental changes and
∗
Corresponding author at: Unidad de Zoología, Departamento de Biología, Uni-
versidad Autónoma de Madrid, C/ Darwin 2, Campus Universitario de Cantoblanco,
28049 Madrid, Spain. Tel.: +34 914 978287.
E-mail address: alvaro.navarrocastilla@uam.es (Á. Navarro-Castilla).
disturbing factors caused by agriculture may act as potential stress-
ors for natural populations. Among the responses to physiological
stressors, there is an increase in the synthesis and secretion of glu-
cocorticoids (GC) (Melmed and Kleinberg, 2003; Stewart, 2003).
Thus, GC levels have been used as physiological indicators of ani-
mal stress in several species (Möstl and Palme, 2002; Stewart, 2003)
including small mammals (Harper and Austad, 2001; Hayssen et al.,
2002; Good et al., 2003; Fletcher and Boonstra, 2006; Ylönen et al.,
2006; Götz and Stefanski, 2007). Although short-term GC secretion
is related to animal adaptive responses (Wingfield and Romero,
2001), chronically elevated and prolonged high GC levels can be
harmful to individuals and produce an array of pathological con-
sequences such as reproductive disruption, suppression of the
immune function, inhibition of growth, survival and decline in fit-
ness (Munck et al., 1984; Sapolsky, 1992; Sapolsky et al., 2000;
Möstl and Palme, 2002; Sapolsky, 2002; Stewart, 2003; Romero,
2004).
Assessing GC concentrations in blood plasma samples has
traditionally been considered as one of the accepted indicators
of quantitative measurements of physiological stress conditions
(Broom and Johnson, 1993). However, this technique is an
1616-5047/$ – see front matter © 2013 Deutsche Gesellschaft für Säugetierkunde. Published by Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.mambio.2013.08.004