Page 2 - Soldatini_etal2015

Research article
So far, the impact of human disturbance on wild bird popu-
lations has been measured using behavioural parameters, such
as nest abandonment (Vleck and Vleck, 2002; Spee et al.,
2010) or flight initiation (Beale and Monaghan, 2004). While
early studies resulted in apparently contradictory results (see
Duffy, 1979; Anderson and Keith, 1980; Parsons and Burger,
1982), it became evident later that identical stressors can cause
opposite reactions depending on the individual’s life-history
stage. For example, during the early breeding season human
presence causes nest abandonment in penguins (Hockey and
Hallinan, 1981), but once breeding has started, most penguins
will not respond behaviourally to human disturbance (Culik
et al., 1990; Culik and Wilson, 1991). The latter behaviour is a
result of the strong commitment to complete reproduction
once breeding has started. Nevertheless, it is likely that these
breeding penguins perceive human disturbance as a stress stim-
ulus even though they do not show behavioural responses.
Indeed, more recent studies show that penguins exposed to
human presence have increased heart rates compared with
undisturbed penguins (Viblanc et al., 2015).
The mechanisms that underlie physiologically mediated
responses to anthropogenic disturbance have been studied
only recently. Human disturbance can act as a generic stress
factor and lead to a physiological stress response by activating
the hypothalamic–pituitary–adrenal (HPA) axis, with resulting
increased secretion of glucocorticoids [GCs; in birds, corticos-
terone (CORT)] within a few minutes and peaking after
30–60 min. Circulating GCs act on different target tissues to
induce an appropriate response to a given stressor. This stress
response is critical for survival because it suppresses all ‘unnec-
essary’ ongoing activities and allocates energetic resources to
functions that are essential for immediate survival (Sapolsky,
1992; Sapolsky et al., 2000; Rodrigues et al., 2009). Physiological
stress responses thus have the beneficial function of adjusting
physiological and behavioural reactions to sudden environmen-
tal changes (Gross and Siegel, 1988; Wingfield and
Ramenofsky, 2011; Cohen et al., 2012). For instance, all repro-
ductive functions will be shut down in order to favour immedi-
ate energy requirements of other systems and increase
awareness (Goymann and Wingfield, 2004; Bonier, 2012).
Different stressors will induce different stress responses and
thus might induce different behaviours (Vos et al., 1985;
Canoine et al., 2002). As soon as the stressor disappears, the
stress response goes back to baseline levels, thanks to negative
feedback on the HPA axis via GC receptors in different brain
regions. However, if a stressor persists and an individual
becomes chronically stressed, the physiological alterations will
become noxious, causing irreversible damage or dysfunction of
the HPA axis (McEwen and Sapolsky, 1995). Most studies on
chronic stress and its physiological consequences have been
carried out in captivity, and little is known about chronic stress
in free-living animals. Physiological studies in the field present
limitations because experimental conditions cannot be con-
trolled fully (see Fusani et al., 2005), but are essential to gain a colonies, and climate change, with peculiar constraints owing
better understanding of what happens in nature. Captivity and
laboratory conditions, particularly in wild animals, can have
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Conservation Physiology • Volume 3 2015
non-negligible effects on chronic stress (Boonstra, 2013). For Downloaded from http://conphys.oxfordjournals.org/ by guest on March 12, 2016
instance, dysfunctions of the HPA axis discovered in labora-
tory animals are rare in free-living animals, because natural
selection will act immediately on them (see Boonstra, 2013).
To what extent is chronic stress visible in nature? Elevated
GC levels have often been associated with chronic stress, but
this is not always the case, and it is generally difficult to define
the endocrine profile of chronic stress in wild animals (Dickens
and Romero, 2013). The few studies conducted in the field
have shown that chronic stress causes inhibition of the
immune response, reduction of reproductive activity and/or
fitness and poor body condition (Silverin, 1986; Wingfield and
Silverin, 1986; Creel et al., 2002, 2013; Tarlow and Blumstein,
2007; Ouyang et al., 2012).
Recently, a number of ecological studies have started to use
measurements of GCs as a means to investigate whether
anthropogenic disturbance might cause chronic stress in ani-
mal populations (Partecke et al., 2006; Romero and Wikelski,
2010). But to interpret GC levels as biomarkers of the stressed
condition of individuals and/or populations exposed to a spe-
cific stressor (Wingfield et al., 2008; Hau et al., 2010) often
requires additional experiments (see Cyr and Romero, 2009).
For example, an individual might have normally low GC
baseline levels and a reduced stress response only because its
adrenals suffer from exhaustion of CORT production or a
habituation to GCs in higher brain areas (Sapolsky et al.,
2000; Cyr and Romero, 2009; Dickens and Romero, 2013). In
this case, specific physiological tests can be helpful to evaluate
HPA axis responsiveness.
The adrenocorticotrophic hormone (ACTH) challenge test
simulates the brain response to a stressor, which sends a spe-
cific signal (ACTH) to the adrenals. If the adrenals are fully
functional, we expect to see an increase of GC release. If the
adrenals are exhausted, we expect to see a reduced GC
response. The dexamethasone (DEX) challenge test simulates
the negative feedback resulting after a stress response, because
DEX mimics GC action. In this case, the brain should show a
negative feedback response dampen the stress response. An
intact HPA axis should thus reduce GC release, whereas in the
case of dysfunction GC production remains high.
Here, we investigated the impact of anthropogenic stress
on a breeding population of the Mediterranean subspecies of
the European storm petrel (Hydrobates pelagicus melitensis).
The Mediterranean population is morphologically and behav-
iourally different from the Atlantic populations and is endemic
to the Mediterranean (Cagnon et al., 2004); although taxons
are not yet considered as separated by IUCN, and the species,
facing a generally decreasing trend, is still considered of least
concern (IUCN, 2015). Threats to the Mediterranean popula-
tion are disturbance and catastrophic events affecting the
to the geographical characteristics of the basin that does not
allow expansion northward. In this study, we investigated
whether storm petrels breeding in areas exposed to tourism