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Conservation Physiology • Volume 3 2015
of 40 min, which is likely to provide a better representation
of the real stress response towards a human intrusion than
handling stress as in experiment 1. The stress response dif-
fered significantly between the two sub-colonies (Fig. 2), but
again CORT levels did not change significantly over time.
One possible explanation is that birds were already stressed
when the first sample (i.e. time 0) was taken. However, this
would not explain the flat response because, if the first sam-
ple was representing the peak, we would have expected a
decrease over the next 30 min. Alternatively, the weak
responsiveness found in both sub-colonies could be an adap-
tation to the reproductive phase/life-history stage to maintain
breeding activity. Flat stress responses have been reported for
other species in specific life-history stages (Romero, 2002,
2004; Partecke et al., 2006; Romero and Wikelski, 2010). It
should be remembered that our experiments were conducted
when storm petrels were brooding. Generally, birds adapt
their stress response according to their life-history stage and
they do so particularly when breeding, in order to avoid over-
reaction to mild stressors which could have serious conse-
quences on fitness (Wingfield et al., 1994; Romero et al.,
1997; Walker et al., 2002).
The life-history stage might explain the dampened stress
response, but it does not explain why tourist-exposed birds
had lower CORT concentrations than undisturbed ones. So
far, reduced stress responses in free-living animals have been
explained by habituation or adaptation to human disturbance
(Romero, 2004; Partecke et al., 2006; Romero and Wikelski,
2010; Dickens and Romero, 2013). Exposure to a repetitive
stressor modulates the stress response, which becomes less
sensitive to this particular stressor. In our study, boat traffic
might have modulated the stress response to this specific dis-
turbance. Our results are in line with studies conducted on
other species, such as tourist-exposed Galapagos iguanas,
which have lower baseline and stress-response CORT levels
than undisturbed iguanas (Romero and Wikelski, 2010).
Likewise, blackbirds living in an urban environment have
comparable baseline levels with, but lower stress-response lev-
els to acute stress than, those living in the forest (Partecke
et al., 2006). One could conclude that tourist-disturbed birds
in our study have a lower stress response than the non-dis-
turbed birds because they had reached a physiological exhaus-
tion, i.e. their adrenals were not able to produce CORT any
longer. This possibility, however, is ruled out by the results of centrations than disturbed birds in 2012. It is more likely that
the ACTH and DEX challenges. We obtained a clear increase
of CORT 30 min after ACTH injection in both sub-colonies,
with tourist-exposed storm petrels showing a significantly
stronger response than the control group. This indicates that
the adrenals of tourist-exposed storm petrels are fully func-
tional and not exhausted. These results are in agreement with
those of previous studies showing that in animals habituated
to a specific stressor, novel stressors will elicit a stronger
response than in non-habituated animals, a phenomenon
called ‘facilitation’ (Romero and Sapolsky, 1996; Romero,
2004; Cyr and Romero, 2009). An alternative interpretation
of our results is that birds breeding in tourist-exposed areas
Research article
were not habituated in a physiological sense but instead Downloaded from http://conphys.oxfordjournals.org/ by guest on March 12, 2016
showed a lowered responsiveness to stressors and had there-
fore chosen to breed in disturbed areas. If this was the case,
our results would indicate that there exist in the population
individual differences in the response to stressors, with birds
that are little responsive to human disturbance but are still
able to mount a stress response to other types of stressors.
The DEX test should induce the negative feedback that
leads to the termination of the stress response (Cyr and
Romero, 2009). As expected, we obtained a reduction of
CORT release 30 min after the DEX injection, but only in the
disturbed sub-colony. The absence of a reduced CORT
response in undisturbed individuals does not exclude the pos-
sibility that a negative feedback response would have occurred
later than 30 min. We are aware that the second blood sample
in our study was taken earlier after injection compared with
other studies (60–90 min; see Rich and Romero, 2005).
However, we had to limit the time in captivity because our
study birds were brooding and we could not keep them away
from their nests any longer. Nevertheless, our results suggest
that the disturbed group is more sensitive and reactive
towards stress stimuli, in line with the finding of a facilitated
stress response after ACTH challenge.
Body condition is often used as an indicator of chronic stress
(Bonier et al., 2009; D’Alba et al., 2011; Dickens and Romero,
2013). In the present study, we did not find any difference in
body condition between birds of the two sub-colonies, and the
samples were similarly composed of individuals of both sexes.
In summary, our results indicate strongly that the human-
disturbed storm petrels are not chronically stressed, either
because they are physiologically habituated or because they
have a reduced sensitivity specifically to humans. It remains
unclear why tourist-disturbed birds sampled in 2011 had a
lower maximal response than all others birds sampled in the
following year (see Fig. 1a and b). A possibility is that the
birds breeding in the outer cave became habituated to distur-
bance from researchers first in 2012. However, this is unlikely
because these caves have been visited by researchers since the
1980s (Massa and Catalisano, 1986; Massa and Sultana,
1991; Soldatini et al., 2014). Moreover, this hypothesis would
not explain why non-disturbed birds had higher CORT con-
small differences in the life-history stage during the experi-
ments affected the results. In the first year (experiments 1 and
2), storm petrels started their breeding activity about
15–20 days later than in the following year (experiment 3)
and were incubating eggs during the experiments, whereas in
the following year some already had hatchlings.
Overall, our results show that storm petrels breeding in a
tourist-exposed area are not chronically stressed. This might
mean that the birds have become habituated to mild
­disturbance, such as frequent boat and human noises, or alter-
natively, that birds breeding in the outer cave have a lower
responsiveness to human disturbance and can therefore breed
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