Are Burrow Nesting Seabird Chicks Affected by Human Disturbance?

Author(s): Yuri V. Albores-Barajas, Cecilia Soldatini and Robert W. Furness

Source: Waterbirds: The International Journal of Waterbird Biology , December 2009,
Vol. 32, No. 4 (December 2009), pp. 572-578
Published by: Waterbird Society

Stable URL: https://www.jstor.org/stable/40660921

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Are Burrow Nesting Seabird Chicks Affected by Human Disturbance?
Yuri V. Albores-Barajas12*, Cecilia Soldatini2 and Robert W. Furness1
institute of Biomedicai and Life Sciences Graham Kerr Building, University of Glasgow, Glasgow, G12 8QQ, UK

2Dipartimento di Scienze Ambientali, Università Ca' Foscari di Venezia Campo della Celestia, Castello 2737/b,
30122, Venezia, Italy

*Corresponding author: E-mail: yalbores@unive.it

Abstract. - Many studies on the effects of human disturbance on birds have focused on adults and report mainly
negative effects. Few focus on effects on chicks. Here, an experimental approach was used to determine effects of
human disturbance on chick growth. Cassin's Auklet chicks were assigned to one of three groups (control, low and
high disturbance) . In experimental groups, a person walked close to the burrow entrance four times or eight times
a day, according to the disturbance level assigned. Growth (mass increment and wing length increase) was mea-
sured and compared between the three groups. Since adults are absent from the nest during the day, chicks, but
not their parents, experienced the disturbance regime. Body condition and experience (age) of the parents did not
influence peak or fledging mass of chicks subject to disturbance. Chicks were not affected by disturbance in the
early stages of growth, while chicks in the experimental groups stopped gaining weight sooner than controls and
fledged at lower weights (6 to 9% less) compared to chicks in the control group. Chicks in the high disturbance
group had a lower peak (F268 = 7.53, P< 0.001) and fledging mass (F268= 17.274, P< 0.001) compared to chicks in
the control group, while chicks in the low disturbance group had a lower fledging mass (F268 = 17.274, P< 0.001)
but similar peak mass. As subsequent survival of chicks is likely to be affected by their mass at fledging, the results
show that it is necessary to consider the chick growth stage when making management plans for areas with burrow-
nesting seabirds. Received 5 September 2008, accepted 2 July 2009.
Keywords. - Cassin's Auklets, chick growth, disturbance, fledging mass, islands, seabirds.
Waterbirds 32(4): 572-578, 2009

Disturbance is "the disruption of normal turbed, then it will move; but if the bird does
activity patterns" (Lord et al 1997) and in not have another undisturbed place to relo-
the case of bird populations has been stud- cate to, then it will stay, despite the distur-
ied for a long time (Robert and Ralph 1975; bance (Gill et al 2001). Disturbance can re-
Safina and Burger 1983). Disturbance can sult in a negative effect for the birds that can-
involve human presence itself, making birds not move, decreasing breeding success or
fly away, with consequences such as exposing body mass; the previous assumption is the
the nest to the weather. Disturbance can also
opposite of the general idea that a bird is not
disturbed if it remains in the same site de-
be more subtle, such as the effect of ecotour-
ism (Safina and Burger 1983). While seabird
spite human presence/activity.
ecotourism may focus on conservation of the Studies of the effects of disturbance have
species (Burger 2000) , visitors may alsofocused
dis- primarily on adults, with only a few
turb the birds by standing close to the studies
nest centered on the effects on chicks or
for too long (Klein et al 1995; Gossling
burrow-nesting species (Lord et al 1997;
1999). Giese and Riddle, 1999; Kitaysky et al 2003;
McClung et al 2004; Mullner et al 2004).
Birds do not all respond in the same way
Some of the research studies have found that
to disturbance; the responses vary according
to species' reproductive behavior, habitua-
a chick growing under conditions of severe
tion, degree of exposure and amount of disturbance
hab- will have its future compro-
itat available (Humphrey et al 1987; Gill mised
et al from an impaired immune system (Ki-
2001). The study of behavioral responses of
taysky et al 2003; Mullner et al 2004). An in-
birds to disturbance may not be the best crease
ap- in chick mortality was observed in a
Glaucous-winged Gull (Larus glaucescens)
proach to evaluate the effects of disturbance
(Gill et al 2001). For example, if a bird colony
has subject to disturbance (Gillet et al
an alternative nesting site to go to when1975);
dis- the increase was caused by prédation

572

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 Disturbance Effects on Chicks 573

On San
of conspecific neighbors as Benito
wellIslands, the
asfirst
theeggs areinabil-
laid in early
January and by the end of January most of the breeding
ity of the chicks to find their nest when dis-
birds are incubating. The peak of chick-hatching is in
placed as a consequence of
the first half of disturbance
February but there is considerable varia-
tion in hatching date within the colony (e.g. 35-43
(Robert and Ralph 1975).
days) . Chicks are left unattended in the burrow during
In the present study, the effects of distur-
the day, when only a few days old, and they are fed by
bance on Cassin's Auklet, Ptycoramphus
their parents aleuti-
until a few days before fledging. Fledging
starts in the first half of March.
cusy chicks, a burrow-nesting seabird species,
were addressed for two main reasons. First,
Experimental Setting
auklet chicks always remain inside their bur-
rows, are relatively easy to follow and the A total of 148 nestboxes had been installed in previ-
ous years. The nestboxes are distributed in several clus-
conditions inside the burrows are fairly con-ters around the island, in zones that have been
stant. Secondly, in a relatively short time occupied by pairs breeding in natural burrows. Breed-
chicks undergo development stages that fol- ing activity was monitored in all the nestboxes from the
beginning of the breeding season every five days until
low the same pattern for all the chicks, thus an adult was found incubating, then biometrics
differences in chick growth may indicate dif- (weight - to the closest 5g-, wing-length, tarsus, head,
ferent external pressures (Giese and Riddle bill length and width and egg length and width - to the
closest mm) and eye color were recorded. Eye color was
1999; Mullner et al 2004). Our objective wasused to establish if older and more experienced individ-
to determine if different levels of distur- uals perform better during the breeding season. Eye
color is a good predictor of the age of the individual in
bance provoke a different response from the
Cassin's Auklet, with juveniles having a dark brown iris
chicks in terms of growth. that fades until becoming completely white in the adult
(Manuwal 1978; Albores-Barajas 2007). As Cassin's
Methods Auklets exchange incubation duties daily, it is possible
to measure the partner the following day. After both
parents had been measured, the nestbox was left un-
Study Area checked for 35 days, the minimum incubation time, to
reduce disturbance to the breeding pair, and then nest-
Data collection was completed from January to boxes were checked every five days. Egg volume (V) was
March 2006 on West San Benito Island off the Pacific
estimated from egg length (L) and breadth (B): V =
coast of Mexico. The islands are located along the Gray
0.51LB2 (Preston 1974).
Whale migration route and are a stopover for whale- To measure the effect of disturbance on chick
watching boats that follow whales from January until growth, mass and wing length were measured in 75
late March. Boats visit the islands with a frequency of
chicks that were subjected to one of three treatments o
one-three boats per week (average of 40 people per
disturbance. Treatment was randomly assigned and
boat) . Tourists hike on the West island to observe native
there were 25 chicks in each group. Control and exper
flora and fauna. Cassin's Auklet burrows are located in
imental nest boxes were interspersed. Control grou
the lower areas of the island, where the tourists walk and
chicks were not subjected to experimental disturbance
it is possible for people walking close to a burrow and
en- other people present on the island were advised t
trance to disturb the adult or chick inside, or even tram-
stay away from these areas. Low disturbance group
ple the burrow. Boat traffic is likely to increase in
chicks were disturbed four times a day (at 08:00, 11:00,
coming years because of the Escalera Nautica project
14:00 and 16:00 hrs) by a person walking 1 m from th
which will build 24 marinas along the Baja Californian nestbox entrance, for approximately 5 s, while chicks i
coast (Alvarez-Castaneda et al 2006). Besides tourists
the high disturbance group were disturbed eight time
visiting the island, there is a fishing village with approx-
a day (at 07:00, 08:30, 10:00, 11:30, 13:00, 14:30, 16:00
imately 80 people living on West San Benito Island from and 1 7:30 hrs) , also by a person walking within 1 m from
September to February. The islands are not managedthe or nestbox entrance, for approximately 5 s. The tim
patrolled by conservation personnel. of the person walking close to the nestbox entrance was
set to 5 s as this is the approximate time it takes a walke
Study Species to move away at a normal pace. Disturbance protoco
was applied until the chicks fledged. Chicks from all
Cassin's Auklets breed in natural cavities, mainly in groups were measured (wing to the nearest mm -usin
rock slopes, or burrows excavated with their own feet. a wing-rule) and mass to the nearest g (using a pesóla
Cassin's Auklets lay single-egg clutches and have a mo- spring balance) every five days until they were fully
nogamous mating system (Manuwal 1979), with inten- feathered; then they were ringed and measured daily to
sive biparental care during incubation and chick- record peak mass and fledging mass. Hatching mass was
feeding (Manuwal and Thoresen 1993). defined as the mass recorded the first time the chick was
Cassin's Auklets are not included in the Red List of En-
left on its own during the day; peak mass was the maxi-
dangered Species (IUCN 2009) but a decline in the overall mum mass recorded for that chick and fledging weight
population has been observed (Ackerman et al 2004) and is the weight recorded the last time the chick was found
thought to be mainly caused by effects of climate changeinside the burrow.
(Hyrenbach and Veit 2003) , introduced species, and per- Adult body condition - As better quality parents are ca-
haps human disturbance (Albores-Barajas 2007) . pable of producing better offspring (Chastel et al

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 574 Waterbirds

1995), adult biometrics

0.8 r
- wing l
and width and head size - were
Components Analysis
0.6
(Tabachn
Factor one was used as a measu
one was plotted 0.4
against the weig
the residuals were used as an in
tion (Carry I 0.2
and Furness 1999), a

!•• 0.2 i I 1
used to establish if body conditi
effect on hatching, peak and fle
Older and more experienced a
at the breeding -0.2
grounds and hav
rows available. Parents were assi
groups (adults, -0.4 sub ■ adults
_L and fi
eye color (Nelson 1981) and %2 w
there was an effect of
Control Low High
age on gr
.0.6 I

A linear regression was

Disturbance run usin
pendent variable, and treatm
laying date, egg volume
Figure 1. Mean body condition index (±SE) and
of parents bo
the parents, as
from explanatory vari
each chick in the experimental groups. Body con-
Chick growth dition
- index was obtained from
The a PCA factor 1. Vari-
growth cur
as well as of ables are those shown in Table 1. Then
treatment Factor 1 was
groups,
taken every five days
plotted against weight anduntil
the residuals usedthe as an indi-
and then daily
cator of until fledging
body condition. Differences between the three
groups, the area
groups are not under the
significant (F(266) =2.71, cur
P = 0.073).
hatching until fledging) for eac
ware, then in subsequent analys
ered as an individual. Repeated
used to determine differences i
control and experimental
breeders to more experiencedgroup
breeders (71
dled for measuring, thus, alth
kept to the
pairs measured). The groups
minimum, our
did cont
not show
disturbed. any differences (%2 2 = 1.15, P= 0.43) in age
composition.
Results Chick growth - A total of 73 chicks were
followed (24 control and low disturbance
Adult body condition - Body sizeandof 25thehigh disturbance). One chick from
adults was estimated using PCA, where bill group died at the age of five days
the control
depth has the largest contribution (30%)
and to from the low disturbance group
a chick
the body size index of the individual,
died at fol-
the age of ten days, both by natural
lowed by head and tarsus, the totalcauses. There were no differences in hatch-
variance
explained by PCA1 is 33%. No correlation
ing mass between the chicks in all three ex-
was found when comparing body perimental
condition groups, indicating that results
index of the parents and chick growth
obtained(r =afterwards
- were not affected by
0.02, P = 0.27). Body condition of hatching
the par-mass or egg volume.
ents of the chicks from the three experimen-
There were no differences in growth dur-
tal groups was no different (Fig. 1;ingF266 = 25-30 days, but when chicks were
the first
2.71, P= 0.07), so it can be assumed fully
that feathered
sub- (i.e. after 30 days) chicks in
sequent results are not influencedthe by experimental
body groups started losing
condition of the parents. weight (Fig. 2). The area under the curve
Body condition of the parents did showed differences between the control
not de-
termine the volume of the egg (r= group and
-0.29, P = the two experimental groups
0.08) . Egg volume was estimated for CF268 = 6.09, P= 0.003).
43 eggs,
Chicks in the control group reached a
the rest of the eggs showed signs of hatching,
therefore measurements were not taken. mean peak mass (the maximum mass that a
Mean egg volume was 22.84 ± 0.28 (Mean chick±reaches before the parents stop feed-
SE) cm3. Egg volume did not influence ing the chick, three or four days before
chick
hatching weight (r= 0.204, P= 0.1). fledging) of 133 g before starting to lose
All three experimental groups had mass.
par-In comparison, chicks in the low dis-
ents from all age categories, from firstturbance
time group reached a lower mean peak

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 Disturbance Effects on Chicks 575

ar

1 130 -L T
1 128

!- 124 • -L i Í
124 • -L Í

I
120

118"

Control Low High

134 r
B

a'26 1I 1
: T
': 1 I
Figure 2. Chick growth curves in different treatments.
Chicks were measured every five days until fully feath-
ered, then daily to measure fledging mass. Chicks in the
114
control group had no extra J_
disturbance provided,
chicks in the low disturbance group were disturbed four
112

times a day and chicks in the highly disturbed group 110«

Control Low High

were disturbed eight times a day. Brackets indicate SE.
Disturbance level

Figure 3. A) Mean peak and B) fledging mass (±SE) of

chicks under different levels of disturbance (N = 24 con-
mass (128 g), and chicks that
trol, 25 low and 24 highwere disturbed
disturbance regime). Differences
more reached a mean
between peak mass
peak mass are only of control
significant between 124 g
(Fig. 3a) . The chicks and
in high disturbance
the highchicks (F(268) = 7.53, P < 0.001);
disturbance
while differences in mean chick fledging mass are signif-
group were different in
icantly peak
different betweenmass from
the control group the
and the two
chicks in the controlexperimental
group groups(F%68
(F(268) = 17.24, P= 7.53, P <
< 0.001).
0.001; Tukey test, P< 0.01) but the control
and low disturbance groups were similar in
mass (Tukey test, P ly > nest
0.05). Control
on islands. Our results show chicks that
had a mean fledging mass
chicks of nesting
from burrow 129species g, arecom-
af-
pared to the 120 g fected
of by the low
high levels disturbed
of disturbance. Al-
chicks and 117 g ofthough
the high
we studied disturbance
a single and peculiar spe-
group (Fig. 3b). Chicks in both
cies our findings treatment
can be applied to other bur-
groups had a significantly lower
row nesting seabird fledging
species. As the chick
weight than the control group
growth (F2
period is not long68 = for
enough 17.274,
chicks
P< 0.001; Tukey test:to P< 0.001
habituate for
to human both
presence, ex-
we assume
perimental groups). From
that the
the same results wouldregression
be obtained in
analysis, using a stepwise different method, theWhen
species and locations. only
pre-
variable that entered the model was distur-
paring management plans for islands where
bance level, but the variation explained is
burrow nesting seabirds are present, distur-
low (1? = 0.23, P< 0.001). bance effects on chicks should be taken into
consideration.

Discussion Body condition of the parents may affect

the output of a breeding season (Nager et al.
Burrow/ crevice nesting species repre-
2000; Quillfeldt et al 2006). Individuals with
sent a large proportion of seabirds and main-
better body condition may face adverse con-

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 576 Waterbirds

ditions or apossibility that experimental birds

stressful perlost
tion, betterweightthan
simply as a result individ
of higher levels of
condition locomotory activity caused by disturbance.
(Weimerskirch
2000; Walker et al
Mauck et(2002), found
al that2004;
newly
2006) The hatched Magellanic
age . of Penguin
the (Spheniscuspare
ma-
ence the gellanicus) chicks did not show succes
breeding a significant
experienced individuals
stress response to disturbance provided by
ability to tourists. The authors catch
locate, suggest the low re- an
ing to a sponse may occur to
higher avoid the negative ef-
amount o
the chick (Greig et al 1983; Reid 1988; fects of stress hormones at early stages of de-
Daunt et al 1999; Reid et al 2003). Our re- velopment. On the other hand, Mullner et al
sults suggest that the age of parents did not (2004) observed that younger Hoatzin
influence their output. 2006 was a year with chicks seemed to be relatively unaffected by
abundant resources (Goericke et al 2007) disturbance, while there was an increased
which allowed all parents to provide enough mortality in chicks ready to fledge. We did
food for their chicks and so permitted high not observe an increased mortality of the
success among all pairs, whether experi- older chicks, but the mass loss of 6-9% we ob-
enced or not. served may jeopardize the survival of the in-
We assumed that the low disturbance lev- dividual at sea, lacking enough reserves dur-
el group reflected the amount of distur- ing the first days before it learns where to
bance perceived by the birds under current catch prey.
conditions; however, disturbance is likely to Growth can also depend on the type of
increase as a result of an increase in tourism prey the parents provide to their chicks in
boat traffic. When comparing the growth different breeding seasons (Hedd et al 2002;
curve for the chicks under the three differ- Abraham and Sydeman 2006; Abraham
ent treatments, the control chicks showed2008).
an In our study, differences in growth
almost constant mass gain, until they cannot be caused by differences in food
reached a peak. The curve we obtained is a quality, as the experiment was conducted in
typical growth curve for Cassin's Auklets one breeding season, and there is no reason
(Morbey and Ydenberg 1997), and many to think that chicks in different groups were
other seabird species, especially nocturnal fed different diets. Adults performed one
burrow nesting birds (Masello and Quillfeldt food delivery each night and were absent
2002; Ritz et al 2005; Tobon and Osorno from the burrows when the disturbance oc-

curred, so adults were unlikely to change be-

2006) , as parents provision their chicks until
they are fully developed and capable of
havior in response to disturbance of the
flight. Once chicks are fully developed,chicks.
the
parents stop feeding them. Although we did not analyze metabolic
All groups grew at the same rate during
rate or stress hormones, there is a possibility
that
the first stage of growth, but chicks in the ex-the differences we found are the conse-
perimental groups began losing mass when
quence of a higher metabolic rate and an ac-
cumulation of stress hormones. Other fac-
they were fully feathered, probably as a result
of an increased metabolic rate causedtors by reported in literature to have an effect,
stress. If the weight loss was due to daily such
han- as body condition of the parents (Mol-
dling, all groups would have reacted ler
theand Erritzoe 2003), laying date (Ramos et
al 2004), hatching mass (Ramos et al 2004),
same way, however, the different experimen-
tal groups reacted differently. As it wasetc.,
not did not influence chick growth in the
possible to measure stress hormones in these
present study.
birds because of logistical problems we can The long-term effects of disturbance are
still poorly understood; however, our results
only infer that the loss of mass in the experi-
mental birds was caused by elevated levelsshow
ofthat there is an effect of disturbance on
stress hormones, but we cannot rule out the
chick growth. Therefore the chick growth

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 Disturbance Effects on Chicks 577

period should be necessarily considered

Gill, J. A., K. Norris and as
W.J. Sutherland. 2001. Why be- a
havioural responses may not reflect the population
period of high sensitivity to disturbance in
consequences of human disturbance? Biological
management plans. Conservation 97: 265-268.
In the case of the San Benito Islands,
Gillet, W. H., J. L. Haywardjr. and J. F. Stout. 1975. Ef-
fects of human activity on egg and chick mortality in
which are not protected under federal or re-a Glaucous-winged Gull colony. Condor 77: 492-495.
gional legislation and the presence of peo-
Goericke, R., E. Venrick, T. Koslow, W.J. Sydeman, F. B.
ple does not provide direct revenue for theSchwing, S. J. Bograd, W. T. Peterson, R. Emmett, R.
Lara Lara, G. Gaxiola-Castro, J. Gomez-Valdez, D.
protection of the island, there should be
Hyrenbach, R. W. Bradley, M. Weise, J. T. Harvey, C.
control of the number of people allowed on Collins and N. C. H. Lo. 2007. The state of the Cali-
the island, or exclusion of visitors from thefornia Current, 2006-2007: Regional and local pro-
immediate area around the auklet burrows. cesses dominate. California Cooperative Oceanic
Fisheries Investigations Reports 48: 33-66.
Gossling, S. 1999. Ecotourism: a means to safeguard
biodiversity and ecosystem functions? Ecological
Acknowledgments Economics 29: 303-320.
Greig, S. A., J. C. Coulson and P. Monaghan. 1983. Age-
related differences in foraging success in the Her-
This study was part of the Ph.D. research for Y.V.A,
ring Gull (Larus argentatus). Animal Behaviour 31:
funded by Consejo Nacional de Ciencia y Tecnologia,
1237-1243.
Mexico. We are grateful to Grupo de Ecologia y Conser-
Hedd, A., J. L. Ryder, L. L. Cowen and D. F. Bertram.
vación de Islas for support during study development
2002. Inter-annual variation in the diet, provisioning
and PNA Cedros for logistic support in the field.
and growth of Cassin's Auklet at Triangle Island,
British Columbia: responses to variation in ocean cli-
mate. Marine Ecology Progress Series 229: 221-232.
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