Content uploaded by Gabriel E Machovsky-Capuska
Author content
All content in this area was uploaded by Gabriel E Machovsky-Capuska on Jan 01, 2014
Content may be subject to copyright.
1 23
Animal Cognition
ISSN 1435-9448
Anim Cogn
DOI 10.1007/s10071-013-0716-x
The contribution of private and public
information in foraging by Australasian
gannets
Gabriel E.Machovsky-Capuska, Mark
E.Hauber, Eric Libby, Christophe Amiot
& David Raubenheimer
1 23
Your article is protected by copyright and
all rights are held exclusively by Springer-
Verlag Berlin Heidelberg. This e-offprint is
for personal use only and shall not be self-
archived in electronic repositories. If you wish
to self-archive your article, please use the
accepted manuscript version for posting on
your own website. You may further deposit
the accepted manuscript version in any
repository, provided it is only made publicly
available 12 months after official publication
or later and provided acknowledgement is
given to the original source of publication
and a link is inserted to the published article
on Springer's website. The link must be
accompanied by the following text: "The final
publication is available at link.springer.com”.
ORIGINAL PAPER
The contribution of private and public information in foraging
by Australasian gannets
Gabriel E. Machovsky-Capuska •Mark E. Hauber •
Eric Libby •Christophe Amiot •David Raubenheimer
Received: 24 September 2013 / Revised: 11 November 2013 / Accepted: 25 November 2013
ÓSpringer-Verlag Berlin Heidelberg 2013
Abstract Predators that forage on foods with temporally
and spatially patchy distributions may rely on private or
public sources of information to enhance their chances of
foraging success. Using GPS tracking, field observations,
and videography, we examined potential sites and mecha-
nisms of information acquisition in departures for foraging
trips by colonially breeding Australasian gannets (Morus
serrator). Analyses of the bill-fencing ceremony between
mated pairs of breeding gannets did not detect correlations
between parameters of this reciprocal behavior and forag-
ing trips, as would have been predicted if gannets used this
behavior as a source of private information. Instead, 60 %
of the departing birds flew directly to join water rafts of
other conspecific en route to the feeding grounds. The
departure of solitary birds from the water rafts was syn-
chronized (within 60 s) with the arrival of incoming for-
agers and also among departing birds. Furthermore, solitary
departing birds from the rafts left in the same directional
quadrant (908slices) as the prior arriving (67 %) and also
prior departing forager (79 %). When associated plunge
dives of conspecific were visible from the colony, provid-
ing a public source of information, gannets more often
departed from the water rafts in groups. Our study thus
provides evidence for the use of water rafts, but not the nest
site, as locations of information transfer, and also confirms
the use of local enhancement as a strategy for foraging
flights by Australasian gannets.
Keywords Decision making Information-centre
hypothesis Local enhancement Morus serrator
Seabirds Water rafts
Introduction
Patchily distributed marine pelagic resources can present
considerable challenges to predatory seabirds. For a pred-
ator to be successful, a long-range foraging strategy can
contribute to decisions about when to depart, whether to
forage solitarily or in groups, and how to acquire infor-
mation about the locality and quality of food resources.
Among seabirds, several hypotheses of the sources and
mechanisms of information acquisition about food sources
have been suggested and tested (Richner and Heeb 1995;
Wakefield et al. 2013). Colonies may serve as centers for
information transfer of feeding sources (ICH: information-
center hypothesis) in which nesting birds gain information
from successfully returning birds on the nature and
G. E. Machovsky-Capuska (&)D. Raubenheimer
The Charles Perkins Centre and Faculty of Veterinary Science
and School of Biological Sciences, University of Sydney,
Sydney, Australia
e-mail: g.machovsky@sydney.edu.au
G. E. Machovsky-Capuska
Coastal-Marine Research Group, Institute of Natural
and Mathematical Sciences, Massey University,
Auckland, New Zealand
M. E. Hauber
Department of Psychology, Hunter College and the Graduate
Center of the City University of New York, New York,
NY, USA
E. Libby
New Zealand Institute for Advanced Study, Institute of Natural
and Mathematical Sciences, Massey University, Auckland,
New Zealand
C. Amiot
Human-Wildllife Interaction Research Group, Institute
of Natural and Mathematical Sciences, Massey University,
Auckland, New Zealand
123
Anim Cogn
DOI 10.1007/s10071-013-0716-x
Author's personal copy
whereabouts of resources (Horn 1968; Ward and Zahavi
1973; Krebs 1974; Brown 1986; Waltz 1987). More
recently, Weimerskirch et al. (2010) suggested that infor-
mation transfer occurs through compass water rafts near
the colony in which social aggregations of rafting birds
acquire information on the direction of food sources from
the angle of bearing of arriving birds. Finally, another form
of cueing, called local enhancement (LE), describes how a
foraging group (‘‘flock’’) attracts individuals to the feeding
patch by its visual conspicuousness (Po
¨ysa
¨1992; Buckley
1997; Gru
¨nbaum and Veit 2003; Weimerskirch 2007) and
also by vocalizations and other acoustic cues associated
with prey capture (Valone 1993).
Predictions in regard to information sources and
exchanges of the whereabouts of food in a closely related
group of seabirds, the gannets (Morus spp.), are also
diverse. Based on the gregariousness of gannets, some
authors suggested that the transfer of information may
occur in gannet colonies (called ‘‘gannetries’’), as per the
ICH (Mock et al. 1988; Richner and Heeb 1995). Others
highlight social flock formations and the conspicuous white
plumage coloration to indicate the use of LE (McGillivray
1842; Nelson 1978; Hamer et al. 2001; Tickell 2003;
Davoren et al. 2003; Adams and Navarro 2005; Bellier
et al. 2005). Both of these processes are considered as
public sources of information, available to all members of
the colony without restriction.
However, as previously shown in honeybees (Apis
mellifera; Zhang et al. 2005; Zeil 2008), memory could
also serve as a private source of information for orientation
in patch detection, a mechanism that has been proposed to
be important to Atlantic gannets (M. bassanus; Drury 1959;
Garthe et al. 2007; Hamer et al. 2007; Pettex et al. 2010)
and Cape gannets (M. capensis; Gre
´millet et al. 2004;
Lewis et al. 2006). Less is known about the at-sea foraging
strategies and the factors driving departures from the col-
ony of Australasian gannets (M. serrator). However, con-
sidering that these gannets have a high divorce rate (43 %;
Ismar et al. 2010a), and that they forage under the risk of
predation (Stephenson 2005) and injury due to accidental
collisions (Machovsky-Capuska et al. 2011a), there is a
strong potential benefit to breeding pairs to engage in
cooperation to maximize foraging efficiency for the current
breeding attempt. An effective way of doing so would be
for the returning bird to privately transfer to its mate cur-
rent information on the nature and whereabouts of
resources during changes of guard at the nest.
An example of a species that transfers private information
about foraging in this way are honeybees whose workers
only signal to nest mates the direction, distance, and quality
of foods in a ritual known as the ‘‘waggle dance’’ (von Frisch
1967). Three socioecological factors may help to explain the
evolution of this unusual form of signaling: (1) the highly
colonial conditions in which honeybees can readily and
efficiently exchange information between genetically clo-
sely related colony members (King and Cowlishaw 2007);
(2) the honeybees within a colony have a close genetic
relatedness, and therefore the evolutionary interests of sig-
naler and receiver are tightly aligned (Hamilton 1963); and
(3) the foods for which honeybees forage are typically
patchily distributed and quickly exhausted, and in these
conditions the timely sharing of information increases for-
aging efficiency (Beekman and Lew 2008).
Gannets have a characteristic pair-greeting ceremony
behavior as part of changing guard at the nest, known as
‘‘bill fencing’’ (BF; Fig. 1); this is a sustained bout of bill
clashing and facial contact that almost invariably takes
place in the critical period separating the return of one
parent to the nest and the departure of the other (Nelson
1978; Machovsky-Capuska 2012; Fig. 1). Although bill
fencing has been suggested to serve as a courtship display
(Cunningham 1866; Townsend 1920), mate recognition
(Meseth 1975), and a form of pair bond consolidation
(Nelson 1978), its functional roles remain unclear. Based
on socioecological similarities with the ‘‘waggle dance’’ in
honeybees (criteria 1–3 above), we considered that bill
fencing could potentially serve in the private exchange of
foraging information.
Australasian gannets are the second rarest member of
the seabird group Sulidae and breed exclusively in south-
eastern Australia and New Zealand (Nelson 2005). Gannets
Fig. 1 Australasian gannets bill fencing. Photo by David
Raubenheimer
Anim Cogn
123
Author's personal copy
feed mainly on pelagic fish and squid (Robertson 1992;
Schuckard et al. 2012). These highly successful marine
predators have been reported to travel for food as far as
388.5 km (Machovsky-Capuska et al. 2013a) with a highly
effective foraging technique (72 % feeding success per
attempt, Machovsky-Capuska et al. 2011b; Machovsky-
Capuska 2012).
Here we use GPS data loggers, behavioral observations,
and videography to examine possible mechanisms of infor-
mation acquisition and the use of navigational cues in Aus-
tralasian gannets while departing for foraging. In particular,
we addressed three questions to test the prediction that
gannets use conspecific as well as abiotic factors as navi-
gational cues while departing for foraging: (a) Do Austral-
asian gannets privately transfer information about food
sources between members of the same couple using bill-
fencing ceremonies? (b) Are the bearings of the departing
birds influenced by the arrivals of conspecific at the water
rafts? and (c) Do wind speed and duration influence the
direction of arrivals and departures for foraging? We predict
that if food sources are not visible from the colony, gannets
will obtain information from their partners during bill-
fencing ceremonies and also cue the whereabouts of food
sources from the bearing of incoming birds at the water rafts.
Alternatively, if associated conspecific foraging activities
(e.g., plunge diving: Machovsky-Capuska et al. 2011a) are
visible near the colony, then gannets will rely on the infor-
mation gained in seeing conspecific foraging. Furthermore,
we predict that wind direction will serve as an important
navigational cue to the departure bearing of gannets
embarking on foraging trips and also facilitates flight when
the birds return with heavy prey loads. These analyses allow
for a better understanding of the sources of information and
decision-making process in Australasian gannets while for-
aging in a complex marine environment.
Materials and methods
Study area
The study was conducted during chick-rearing periods in
December and January 2009–2010 and 2010–2011 on the
Beach Colony of Cape Kidnappers gannetry, New Zealand
(39°3804800S, 177°0503600E). The Beach Colony is one of the
four gannetries at Cape Kidnappers and is located at sea level
with around 1,000 breeding pairs (Machovsky-Capuska 2012).
GPS deployment and video footage collection
Both members of a breeding pair of adult Australasian
gannets rearing 2- to 5-week-old chicks were captured at
the same nest located at the periphery of the colony and
equipped with GPS data loggers manufactured by e-obs
digital telemetry, Germany (http://www.e-obs.de, more
details in Machovsky-Capuska et al. 2013a). The devices
weighed 45 g, which represents 2 % of the adult body
weight (Nelson 1978). Data on position (latitude, longi-
tude, and altitude), speed, and time were recorded at 1 s
intervals. The data loggers were attached using Tesa tape to
the four central tail feathers as recommended by Ismar
et al. (2010b). The first bird in a pair observed to be
departing from the nest was captured immediately after
adopting the sky-pointing posture (Nelson 1978), then
released after the data logger was fitted [approximately
10 min as defined by Machovsky-Capuska et al. (2013a)].
The second bird in the pair was captured the following day
while nesting, at a time predicted to be within a range of
1–5 h prior to the arrival of its partner. This estimate was
based on Machovsky-Capuska et al. (2013a) suggesting
that in this colony, the average duration of foraging trips
was approximately 24 h. In all cases, human interference
during nest changeover was avoided.
Upon arrival of the first gannet tracked with the GPS
data logger, high-resolution video footage of the BF cere-
mony during nest changeover was recorded using a Canon
XH A1S handycam with 20 mm zoom. After observing the
adults feeding their chicks, the recently arrived bird was
captured, the data logger and tape strips completely
removed, and birds were thereafter released at the edge of
the colony. Following Machovsky-Capuska (2012),
behavioral components of BF ceremonies were analyzed
frame by frame using Adobe Premiere Pro CS4. Consid-
ering the problems of accurately extracting angles from 2D
video footage, we decided to use the number of bill touches
during bill-fencing ceremonies for behavioral comparisons.
Following Gre
´millet et al. (2004), the recorded GPS trips
were analyzed to determine distance travelled, speed, and
time away from the colony. To conduct comparisons with
the dance of the honeybees, following von Frisch (1967),
relationships between bill touches during BF ceremonies
and data collected from GPS data loggers were tested using
Pearson’s correlations. Bonferroni’s correction (Curtin and
Schulz 1998) was used to correct for multiple comparisons,
based on which we adopted a threshold probability level of
P=0.005. Since the flight paths of Australasian gannets
were not direct and involved a combination of foraging
sites, we calculated the average bearing location of the
dives from the colony to represent the intended destination
(Pettex et al. 2010; Machovsky-Capuska et al. 2013a). For
each gannet pair from which BF was recorded, we com-
puted the average bearing location to quantify the differ-
ence in their bearing angle from the colony. Following
Machovsky-Capuska et al. (2013a), we randomly permuted
these angles between pairs 100,000 times to evaluate the
probability that the observed distribution of vectors would
Anim Cogn
123
Author's personal copy
occur randomly and thus corrected for biases due to geo-
graphic constraint. Data from the GPS units were analyzed
using MATLAB 2009 and PASW Statistics version 18.
Data were initially tested using Levene’s test for homo-
scedasticity and Shapiro–Wilk’s test for normality, and two
tailed t-tests were used for seasonal comparisons.
Departures and behaviors of gannets from the colony
During December and January 2009–2011 austral breeding
seasons, population-level departures were observed every
hours from dawn to dusk. A single observer conducted
scans at a constant focal duration that covered 180°view at
30 s intervals. Scans aimed to record the departure time
from the colony and behavior of breeding adult gannets,
systematically conducted from the same site on a cliff 40 m
above the breeding colony using a 10 950 reticulated
binoculars and compass (Waltz 1982). Considering that the
colony is located at the base of a 60-m flat cliff, scans
allowed a complete 180°view subdivided for the purposes
of initial data collection into four sectors of 45°within
a 1 km range from the colony. Following Burger (1997),
departure behaviors were recorded as follows: (1) direct
departure (DD, when birds departed from the colony to
foraging), (2) landing near conspecific (LC, when birds
departed from the colony and landed near another con-
specific), and (3) splashdown (S, when birds bathe, preen
and head dip while floating on the water alone). In addition,
departing behaviors were also related to the presence of
associated plunge-diving foraging activity of other gannets
visible from the colony (Machovsky-Capuska et al. 2011a).
Frequencies of departure behaviors were compared using
v
2
and Z-tests, and an increase in direct departures from the
colony with associated plunge-diving foraging activity was
considered to reflect the use of local enhancement by the
departing bird (Buckley 1997; Gru
¨nbaum and Veit 2003;
Bellier et al. 2005).
Water raft analysis
We defined a water raft as an aggregation of Australasian
gannets floating in the water with a spacing of less than
3 m between conspecifics, which had either arrived directly
from the colony en-route to foraging or had returned from a
foraging trip (Burger 1997). Following Weimerskirch et al.
(2010), a second observer recorded the angle of bearing of
gannet water rafts every hour from dawn to dusk in paralell
to the departures from the colony. For our observations,
only the most populated water raft was followed. Thus,
rafts were subdivided into sectors of 90°from which flock
size and behavior of arriving and departing birds were
coded as in Davoren et al. (2003) and Montevecchi et al.
(2009). In this procedure, departure behaviors were
recorded as follows: (1) indirect departure (ID, when birds
departed from the raft to foraging), (2) landing near con-
specific (LC, when birds departed from the raft and landed
near another conspecific), and (3) colony (C, when birds
departed from the raft and landed at the colony). The
arrival and departure bearings of Australasian gannets from
the water rafts were calculated and corrected to 90°of the
observer following Batschelet (1981).
We conducted circular correlations between arrival and
subsequent departures (60 s—follower) bearings to test
whether departing birds follow the same bearing of the
previous arrival bird using correlation coefficient for
angular variables and Watson two-sample tests of unifor-
mity (Package circular version 0.4-3 of the software R). In
parallel with behavioral observations, a third observer
collected a total of 50 h of high-resolution video footage of
Australasian gannets rafting using a Canon XH A1S
handycam with 20 mm zoom from the same area and
altitude of the cliff as previously described. For time-of-
the-day comparisons, we separated the day into three
segments—early morning, midday, and afternoon—and
compared frequencies using the v
2
test. In addition, hourly
measurements of wind direction and speed were down-
loaded from the National Climate Database from New
Zealand’s National Institute of Water and Atmospheric
Research (NIWA) http://cliflo.niwa.co.nz, with the station
selected as Cape Kidnappers WxT Aws (D97601;
39°3804200S, 177°05031.200E). Correlation coefficient for
angular variables and Watson’s two-sample test of uni-
formity (Package circular version 0.4-3 of the software R)
were also used to test the influence of wind direction and
the angle of bearing of the arriving and departing birds.
Data were initially tested using Levene’s tests for homo-
scedasticity and Shapiro–Wilk for normality. For statistical
comparisons, data were analyzed using PAWS Statistics,
version 18. We report data as mean ±SE.
Results
Exchange of foraging information at the colony
We succeeded in deploying GPS data loggers on both
partners of a nesting pair and filming BF during the nest
changeover for the same pairs in 6 couples out of 35
(17 %) attempts, this amounting to approximately 600 h of
effort. The major challenge was to capture in our obser-
vations the arrival time of foraging Australasian gannets at
the colony, which was highly unpredictable, in order to
film the BF at changeover and relate it to the foraging trips
of both putative signaler and receiver.
A total of 12 individual foraging trips (n=2 in 2010
and n=10 in 2011) from chick-rearing gannets were
Anim Cogn
123
Author's personal copy
recorded. Gannets foraged over average distances of
63.2 km (±25.9 km), with a mean foraging path length of
310.9 km (±132.2 km) and a mean foraging trip duration
of 27.3 h (±8.9 h). During foraging trips, gannets travelled
an average speed of 11.6 km h
-1
(±3.9 km h
-1
, Table 1).
Foraging trip performance was highly consistent between
the two consecutive breeding seasons studied, with no
significant differences in any of the variables analyzed
(maximum distance from colony, t-test, t=0.38, df =10,
P=0.71, two-tailed; foraging path length t-test, t=1.03,
df =10, P=0.32, two-tailed; foraging trip duration t-test,
t=0.54, df =10, P=0.60, two-tailed; and speed t-test,
t=0.43, df =10, P=0.67, two-tailed).
The analysis of foraging trips (n=12) collected from
GPS data loggers, after Bonferroni correction for multiple
comparisons, showed no significant correlations between
distance travelled, time away from the colony, travel
speed, BF duration, bill touches, and the length of time the
couple spent together during nest changeovers (Table 2).
Furthermore, the distribution of the bearing of foraging
trips in the GPS deployments assembled from 100,000
permutations (see ‘‘Methods’’) revealed that the average
angular difference between directions of Australasian
gannets in BF pairs was not significantly less than expected
by chance (P[0.05).
Departures and behaviors of gannets from the colony
When no plunge-diving foraging activity was visible from
the colony, 60 % (n=1,230) of breeding Australasian
gannets departing from CK colony landed in water rafts
between 50 and 70 m from the colony, whereas 21 %
(n=430) landed alone in a splashdown and 19 %
(n=390) departed directly for foraging sites (v
2
=721.3;
df =2; P\0.0001, Fig. 2a). The majority of the colony
departures were made by solitary gannets (v
2
=57.0;
df =3; P\0.0001, Fig. 2a). However, when plunge-div-
ing conspecific foraging activity was observed within
500 m of the colony (Fig. 2b), DD (60 %, n=191) was
higher than LC (30 %, n=95, Fig. 2b). This frequency of
DD is significantly higher than when plunge-diving con-
specific foraging activity or food sources were not seen near
the colony (19 %, n=361, Z=15.4, P\0.0001), sug-
gesting the use of local enhancement by foraging gannets.
Thus, the number of departed birds was also larger when
associated plunge-diving conspecific foraging activity was
observed near to the colony (v
2
=135.4, df =3,
P\0.0001, Fig. 2b).
Water raft analysis
During our behavioral and video footage analysis, we
observed that Australasian gannets formed water rafts near
Table 1 Bill-fencing ceremony characteristics and foraging parameters for six breeding couples of Australasian gannets fitted with GPS data loggers
Code Year Bird A Bill fencing Bird B
Sex Maximum
distance from
colony (km)
Foraging
path length
(km)
Foraging
trip
duration
(h)
Speed
(km h
-1
)
Duration
(s)
Couple
time (s)
Duration
(s)/couple
time (s)
Bill
touches
(s
-1
)
Sex Maximum
distance from
colony (km)
Foraging
path length
(km)
Foraging
trip
duration
(h)
Speed
(km h
-1
)
1 2010 F 45.45 267.02 23.40 11.41 15.64 156.36 0.10 1.92 M 94.21 530.90 37.73 14.07
2 2011 M 63.46 389.16 34.73 11.21 31.92 760.80 0.04 0.31 F 76.09 177.83 25.84 6.88
3 2011 M 76.64 301.03 46.24 6.51 15.14 466.68 0.03 0.46 F 68.13 393.28 27.16 14.48
4 2011 M 19.80 220.54 24.99 8.82 14.52 55.00 0.26 0.48 F 69.68 553.09 25.61 21.59
5 2011 F 63.44 239.75 23.08 10.39 56.24 277.80 0.20 0.39 M 44.53 192.65 16.58 11.62
6 2011 F 27.58 152.02 13.35 11.39 39.90 60.68 0.66 0.80 M 109.88 314.00 29.53 10.63
Bird A =first arriving adult, Bird B =second arriving adult
Anim Cogn
123
Author's personal copy
the colony, varying in the number of birds and also in
location with respect to the colony. We recorded a total of
248 water rafts with a mean of 35.4 ±15.5 gannets (range
15–71 birds). For the time-of-the-day comparisons (see
methods), the largest number of gannets observed rafting at
any one time (956 birds) was in the early morning period
(v
2
=9.7, df =2, P\0.05). Upon arrival at a raft, gannets
began to preen, bathe and head dip, and lounged on the
water for statistically similar periods in the middle of the
day with a mean of 5.0 ±0.4 min (range 0.1–14.3 min), in
early morning (3.5 ±0.3 min, range 0.06–10.1 min), and
in the afternoon periods (4.2 ±0.4 min, range
0.3–14.6 min; v
2
=9.9, df =2, P=0.06). The mean
duration of time gannets spent in the raft was
4.4 ±0.20 min (range 0.06–14.6 min), based on a total of
225 rafting birds recorded.
The frequency of gannets arriving at the water raft
directly from foraging (58 %) was similar to that of the
colony (42 %), as this difference was not significant
(v
2
=3.4; df =2; P=0.16). Individual gannets accoun-
ted for a significantly greater proportion of raft arrivals
(68 %) and departures (55 %) than did groups of two or
more birds (v
2
=27.3, df =3, P\0.0001). There were
significantly more departures from the rafts toward the
foraging sites than directly to the colony (v
2
=882.1,
df =2, P\0.0001).
We found evidence of an association between birds
departing indirectly to the foraging sites and others arriving
at the water raft from foraging. Seventy percent of
departures toward the foraging sites from the raft took
place within 60 s of an arrival (v
2
=103.2, df =2,
P=0.001), and the majority of the departing birds (67 %)
departed within the same directional quadrant from which
the previous bird had arrived (v
2
=67.6, df =1,
P\0.0001). Sixty nine percent of departures toward the
foraging sites from the raft took place within 60 s of a
departure (v
2
=83.7; df =2; P\0.0001), and the
majority of the birds (79 %) departed within the same
directional quadrant from which the previous bird had
departed (v
2
=71.2; df =1; P\0.0001).
Arrivals at the water rafts from foraging were positively
correlated with wind bearing (Table 3). However, there were
no significant correlations for either arrival or departure
bearings and wind speed\20 and[20 km h
-1
(Table 3).
Discussion
The use of sensory information by animals is critical in
locating and exploiting food resources (Stevens 2013).
Birds have evolved complex visual systems that play an
important role in orientation and foraging (Aidala et al.
2012). Although gannets are visual predators (Cunningham
1866; Machovsky-Capuska et al. 2011c,2012,2013b),
very little is known about the source of the sensory cues
involved in their foraging habitat recognition (Greif and
Siemers 2010). Information on the location of food can be
acquired privately (from memory and environmental cues)
Table 2 Correlation coefficients for relationships between times of absence from the nest, speed during the trip, flight distance, bill-fencing
duration, bill touches, and couple duration for different breeding adults of Australasian gannets fitted with GPS data loggers (n=12)
Bill-fencing
duration (s)
Couple time
(s)
Bill touches
(s
-1
)
Bird B
Maximum distance
from colony (km)
Foraging path
length (km)
Speed
(km h
-1
)
CPCPCPC P C P C P
Bird A
Maximum distance from colony (km) 0.60 0.21 0.32 0.83 -0.30 0.57 -0.37 0.47 0.10 0.85 -0.71 0.12
Foraging path length (km) -0.46 0.36 0.16 0.76 -0.39 0.45 -0.10 0.85 0.45 0.37 -0.73 0.10
Foraging trip duration (h) -0.40 0.43 0.57 0.23 -0.76 0.08 0.19 0.72 0.64 0.17 -0.90 0.01
Speed (km h
-1
)-0.25 0.64 -0.25 0.63 0.14 0.79 -0.27 0.60 0.05 0.93 -0.18 0.73
Bird B
Maximum distance from colony (km) -0.28 0.59 -0.31 0.55 0.55 0.25
Foraging path length (km) -0.77 0.07 -0.28 0.60 -0.12 0.82
Foraging trip duration (h) -0.91 0.01 0.24 0.64 -0.43 0.40
Speed (km h
-1
) 0.54 0.27 -0.65 0.16 0.62 0.19
Couple time (s) 0.06 0.92
Bill-fencing duration (s) 0.40 0.44
Bird A =first arriving adult, Bird B =second arriving adult. CPearson correlation coefficient, PSignificance level, with Bonferroni correction
a\0.005
Anim Cogn
123
Author's personal copy
or publically (from the behavior of conspecific; Danchin
et al. 2004; Hauber and Zuk 2010). Our study provides
evidence of the use of public rather than private informa-
tion during foraging in Australasian gannets.
Private information
How do gannet partners know how much to invest in
parental care? Results about the duration of bill-fencing
ceremonies and number of bill touches in relation to dis-
tance, duration, and angle of bearing of foraging trips did
not provide evidence for the exchange of foraging infor-
mation between partners.
Instead, individual ecological and social context may
have an effect through exposure to wind speed and
direction, as has been shown to have a strong effect on the
flight behavior of other seabirds and their energy invest-
ment while searching for food (Birt-Friesen et al. 1989;
Pennycuick 1989). Our analysis of the relationship between
arrival and departure bearing with wind direction revealed
that the majority of Australasian gannets used tail winds
while arriving from foraging, as previously shown in
Atlantic and Cape gannets (Gre
´millet et al. 2004; Garthe
et al. 2007).
Public information
It has been suggested that colonies may act as centers for
transfer of information (ICH; Ward and Zahavi 1973), and
gannet colonies of other species in particular have been
Fig. 2 Frequency of departures and flock size of breeding Austral-
asian gannets. Departure behaviors from the colony, when associated
plunge-diving conspecific foraging activity was not visible, and when
associated plunge-diving conspecific foraging activity was visible
nearby. ** and *** represent statistically significant results
(P\0.0001). Photos by Gabriel Machovsky-Capuska
Anim Cogn
123
Author's personal copy
identified as candidates to test this hypothesis (Mock et al.
1988; Richner and Heeb 1995). The ICH predicts that birds
would leave directly for foraging, to maximize the proba-
bility that information about food sources is current. We
found that 80 % of the birds did not head directly to the
feeding grounds when food sources were not visible from
the colony, but stopped near the colony in a water raft or by
itself before departing for foraging. Our results found that
gannets formed water rafts with the highest concentration
of birds early in the morning when most started their for-
aging trips. This is similar to previous findings on common
murres (Uria aalge) gathering near the colony prior to
departing for foraging (Burger 1997).
The evidence for the use of water rafts during both the
initiation and completion of foraging trips, in addition to
the synchrony between the directional bearing of incoming
and subsequent outgoing gannets and also between
departing foragers, suggests that water rafts play an
important role in updating social information concerning
food resources in gannets. These results are consistent with
the formation of water rafts to detect conspecifics returning
from foraging (Burger 1997) and the use of these rafts as
arenas for social information exchange in Guanay cormo-
rants (Phalacrocorax bougainvillii) (Weimerskirch et al.
2010). The variation in the bearing location of these water
aggregations of gannets with respect to the colony was
continuously adjusted to the bearing of the arrival foragers
as previously observed in cormorants by Weimerskirch
et al. (2010).
Acquiring information from cues and signals of foraging
conspecifics, a process called local enhancement (Thorpe
1963), is widespread among seabirds. When plunge-diving
foraging activity was observed from the colony within a
range of 200–700 m, direct departures (DD) were signifi-
cantly increased relative to when plunge-diving activity
was not visible nearby, supporting the claim that the
gannets we observed used local enhancement while for-
aging, as previously suggested for other gannet species
(Nelson 1978; Gre
´millet et al. 2004). Foraging in this way,
gannets have access to more accurate information and can
make better-informed decisions by observing and follow-
ing the behavior of foraging conspecifics (King and
Cowlishaw 2007; Conradt 2011). During these events, we
have also observed an increase in the number of birds
departing from the rafts and the colony. This is likely
related to the opportunity to capture food near the colony
and possibly also increased feeding success with larger
flock size (Ferna
´ndez-Juricic et al. 2004), something which
remains unstested for gannets.
The present study highlights the importance of water
rafts as arenas for information exchange for foraging
gannets. The results have also provided evidence of the use
of a combination of several strategies, including synchro-
nization between arriving and departing birds and among
departing foragers, the use of local enhancement and an
influence of the wind on foraging by Australasian gannets.
Further studies are needed to gain a better understanding of
the use of navigational and sensory cues in these marine
predators, and its role in generating colony level coordi-
nation of foraging departures and paths, while searching
and capturing food in complex marine environments.
Acknowledgments We acknowledge T. Fettermann, S. Clements,
G. Greyling, A. Boyer, L. Meynier, L. van Zonneveld, T. Greenawalt,
E. Martı
´nez, K. & S. Machovsky, and S. Ismar for assistance in the
field. We also thank the Napier Department of Conservation office for
the permission to use the ranger’s house during field work and the
Cape Kidnappers’ landowners and farm managers for access to their
property. We thank E. Martı
´nez, S. Dwyer and L. Pichegru for helpful
comments on early versions of the manuscript and I. Couzin for his
assistance during the funding application. This research was funded
by National Geographic Waitt Grant and the Massey University
Research Fund.
Ethical standards The experiments in the present study were
conducted under Massey University Animal Ethics (09/76) and New
Zealand Department of Conservation (DoC) permits (ECHB-23237-
RES).
Conflict of interest The authors declare that they have no conflict
of interest.
References
Adams N, Navarro R (2005) Foraging of a coastal seabird: flight
patterns and movements of breeding Cape gannets Morus
capensis. Afr J Mar Sci 27:239–248
Aidala Z, Huynen L, Brennan PLR, Musser J, Fidler A, Chong N,
Machovsky-Capuska GE, Anderson MG, Talaba A, Lambert D,
Hauber ME (2012) Ultraviolet visual sensitivity in three distinct
avian lineages: paleognaths, parrots, and songbirds. J Comp
Physiol A 198:495–510
Batschelet E (1981) Circular statistics in biology. Academic Press,
New York
Table 3 Circular correlation coefficients for relationships between
arrival and departure angles from e water rafts by Australasian
gannets
Wind Coefficient Statistic P
Bearing
Arrival 0.22 1.85 0.05
Indirect departure 0.26 1.22 0.08
Speed
Arrival (km/h)
\20 0.20 1.64 0.10
[20 -0.001 -0.005 0.99
Indirect departure (km/h)
\20 0.23 1.79 0.07
[20 -0.11 -0.32 0.74
Bold statistically significant
Anim Cogn
123
Author's personal copy
Beekman M, Lew JB (2008) Foraging in honeybees-when does it pay
to dance? Behav Ecol 19:255–261
Bellier E, Cetain G, Chadoeuf J, Monestiez P, Bretagnolle V (2005)
Spatial pattern in seabirds’ distribution: testing for influence of
foraging strategies. The case of Northern gannets in the Bay of
Biscay. ICES CM 2005/L:13
Birt-Friesen VL, Montevecchl WA, Calms DK, Macko SA (1989)
Activity-specific metabolic rates of free-living Northern gannets
and other seabirds. Ecology 70:357–367
Brown CR (1986) Cliff swallow colonies as information centers.
Science 234:83–85
Buckley N (1997) Spatial-concentration effects and the importance of
local enhancement in the evolution of colonial breeding in
seabirds. Am Nat 149:1091–1112
Burger AE (1997) Arrival and departure behavior of common Murres
at colonies: evidence of an information Halo? Colon Waterbird
20:55–65
Conradt L (2011) When it pays to share decisions. Nature 471:40–41
Cunningham RO (1866) On the Solan Goose, or Gannet (Sula
Bassana, Lim.). Ibis 8:1–22
Curtin F, Schulz P (1998) Multiple correlations and Bonferroni’s
correction. Biol Psychiatry 44:775–777
Danchin E, Giraldeau LA, Valone TJ, Wagner RH (2004) Public
information: from nosy neighbours to cultural evolution. Science
305:487–491
Davoren G, Montevecchi W, Anderson J (2003) Search strategies of a
pursuit-diving marine bird and the persistence of prey patches.
Ecol Monogr 73:463–481
Drury WH Jr (1959) Orientation of gannets. Bird-Banding
30:118–119
Ferna
´ndez-Juricic E, Siller S, Kacelnik A (2004) Flock density, social
foraging and scanning: an experiment with starlings. Behav Ecol
15:371–379
Garthe S, Montevecchi W, Davoren G (2007) Flight destinations and
foraging behaviour of northern gannets (Sula bassana) preying
on a small forage fish in a low-Arctic ecosystem. Deep-Sea Res
Part II 54:311–320
Greif S, Siemers BM (2010) Innate recognition of water bodies in
echolocating bats. Nat Commun 1:107
Gre
´millet D, Dell’Omo G, Ryan P, Peters G, Ropert-Coudert Y,
Weeks S (2004) Offshore diplomacy, or how seabirds mitigate
intra-specific competition: a case study based on GPS tracking of
Cape gannets from neighbouring colonies. Mar Ecol Prog Ser
268:265–279
Gru
¨nbaum D, Veit RR (2003) Black-browed albatrosses foraging on
Antarctic krill: density-dependence through local enhancement?
Ecology 84:3265–3275
Hamer K, Phillips R, Hill J, Wanless S, Wood AG (2001) Contrasting
foraging strategies of gannets Morus bassanus at two North
Atlantic colonies: foraging trip duration and foraging area
fidelity. Mar Ecol Prog Ser 224:283–290
Hamer KC, Humphreys EM, Garthe S, Hennicke J, Peters G,
Gre
´millet D, Phillips RA, Harris MP, Wanless S (2007) Annual
variation in diets, feeding locations and foraging behaviour of
gannets in the North Sea: flexibility, consistency and constraint.
Mar Ecol Prog Ser 338:295–305
Hamilton WD (1963) Evolution of altruistic behavior. Am Nat
97:354–356
Hauber ME, Zuk M (2010) Chapter 8: social influences on
communication signals: from honesty to exploitation. In: Szek-
ely T, Moore AJ, Komdeur J (eds) Social behaviour: genes,
ecology and evolution. Cambridge University Press, New York,
pp 185–199
Horn HS (1968) The adaptive significance of colonial nesting in the
Brewer’s Blackbird (Euphagus cyanocephalus). Ecology 49:
682–694
Ismar SMH, Daniel C, Stephenson BM, Hauber ME (2010a) Mate
replacement entails a fitness cost for a socially monogamous
seabird. Naturwissenschaften 97:109–113
Ismar SMH, Hunter C, Lay K, Ward-Smith T, Wilson PR, Hauber
ME (2010b) A virgin flight across the Tasman Sea? Satellite
tracking of postfledging movement in the Australasian Gannet
Morus serrator. J Ornithol 151:755–759
King AJ, Cowlishaw G (2007) When to use social information: the
advantage of large group size in individual decision making. Biol
Lett 3:137–139
Krebs JR (1974) Colonial nesting and social feeding as strategies for
exploiting food resources in the great blue heron (Ardea
herodias). Behaviour 51:99–134
Lewis S, Gre
´millet D, Daunt F, Ryan P, Crawford R, Wanless S
(2006) Using behavioural and state variables to identify prox-
imate causes of population change in a seabird. Oecol
147:606–614
Machovsky-Capuska GE, Dwyer SL, Alley MR, Stockin KA, Rauben-
heimer D (2011a) Evidence for fatal collisions and kleptoparasit-
ism while plunge diving in Gannets. Ibis 153:631–635
Machovsky-Capuska GE, Vaughn RL, Wu
¨rsig B, Katzir G, Rauben-
heimer D (2011b) Dive strategies and foraging effort in the
Australasian gannet Morus serrator revealed by underwater
videography. Mar Ecol Prog Ser 442:255–261
Machovsky-Capuska GE, Huynen L, Lambert D, Raubenheimer D
(2011c) UVS is rare in seabirds. Vision Res 51:1333–1337
Machovsky-Capuska GE (2012) Hunting between the air and the
water: the Australasian gannet (Morus serrator). PhD thesis,
Massey University, New Zealand
Machovsky-Capuska GE, Howland HC, Vaughn RL, Wu
¨rsig B,
Raubenheimer D, Hauber ME, Katzir G (2012) Visual accom-
modation and active pursuit of prey underwater in a plunge
diving bird: the Australasian gannet. Proc R Soc Lond B Biol
279:4118–4125
Machovsky-Capuska GE, Hauber ME, Libby E, Wikelski MC,
Schuckard R, Melville D, Cook W, Houston M, Raubenheimer
D (2013a) Foraging behaviour and habitat use of chick-rearing
Australasian gannets in New Zealand. J Ornithol. doi:10.1007/
s10336-013-1018-4
Machovsky-Capuska GE, Vaughn-Hirshorn RL, Wu
¨rsig B, Rauben-
heimer D (2013b) Can gannets define their diving profile prior to
submergence? Notornis 60:255–257
McGillivray J (1842) Account of the Island of St Kilda, chiefly with
reference to its natural history. Edinb New Philos J 32:47–70
Meseth EH (1975) The dance of the Laysan albatross (Diomedea
immutabilis). Behaviour 54:217–257
Mock D, Lamey T, Thompson D (1988) Falsifiability and the
information centre hypothesis. Ornis Scand 19:231–248
Montevecchi WA, Benvenuti S, Garthe S, Davoren GK, Fifield D
(2009) Flexible foraging tactics by a large opportunistic seabird
preying on forage and large pelagic fishes. Mar Ecol Prog Ser
385:295–306
Nelson JB (1978) The Sulidae: gannets and boobies. Oxford
University Press, Oxford
Nelson JB (2005) Pelicans, cormorants and their relatives. Oxford
University Press, Oxford
Pennycuick CJ (1989) Bird flight performance: a practical calculation
manual. Oxford University Press, Oxford
Pettex E, Bonadonna F, Enstipp MR, Siorat F, Gre
´millet D (2010)
Northern gannets anticipate spatio-temporal occurrence of their
prey. J Exp Biol 213:2365–2371
Po
¨ysa
¨H (1992) Group foraging in patchy environments: the
importance of coarse-level local enhancement. Ornis Scand
23:159–166
Richner H, Heeb P (1995) Is the information center hypothesis a flop?
Adv Study Behav 24:1–45
Anim Cogn
123
Author's personal copy
Robertson D (1992) Diet of the Australasian gannet Morus serrator
(G.R. Gray) around New Zealand. N Z J Ecol 16:77–81
Schuckard R, Melville D, Cook W, Machovsky-Capuska GE (2012)
Diet of the Australasian gannet (Morus serrator) at Farewell
Spit, New Zealand. Notornis 59:66–70
Stephenson B (2005) Variability in the breeding ecology of Austral-
asian gannets (Morus serrator) at Cape Kidnappers, New
Zealand. PhD thesis, Massey University, New Zealand
Stevens M (2013) Sensory ecology, behaviour, and evolution. Oxford
University Press, Oxford
Thorpe WH (1963) Learning and instinct in animals. Methuen,
London
Tickell WLN (2003) White plumage. Waterbirds 26:1–12
Townsend CW (1920) Courtship in birds. Auk 37:380–393
Valone TJ (1993) Patch information and estimation—a cost of group
foraging. Oikos 68:258–266
von Frisch K (1967) The dance language and orientation of bees
28–235. Harvard University Press, Harvard
Wakefield ED, Bodey TW, Bearhop S, Blackburn J, Colhoun K,
Davies R, Dwyer RG, Green JA, Gre
´millet D, Jackson AL,
Jessopp MJ, Kane A, Langston RH, Lescroe
¨l A, Murray S, Le
Nuz M, Patrick SC, Pe
´ron C, Soanes LM, Wanless S, Votier SC,
Hamer KC (2013) Space partitioning without territoriality in
gannets. Science 341:68–70
Waltz E (1982) Resource characteristics and the evolution of
information centers. Am Nat 119:73–90
Waltz E (1987) A test of the information centre hypothesis in two
colonies of common terns, Sterna hirundo. Anim Behav
35:48–59
Ward P, Zahavi A (1973) The importance of certain assemblages of
birds as ‘‘Information Centres’’ for food finding. Ibis
115:517–534
Weimerskirch H (2007) Are seabirds foraging for unpredictable
resources? Deep-Sea Res Part II 54:211–223
Weimerskirch H, Bertrand S, Silva J, Marques JC, Goya E (2010) Use
of social information in seabirds: compass rafts indicate the
heading of food patches. PLoS ONE 5:e9928. doi:10.1371/
journal.pone.0009928
Zeil J (2008) Orientation, navigation and searching. In: Jorgensen SE,
Fath BD (eds) Behavioral ecology (vol 3) of encyclopedia of
ecology. Elsevier, Oxford
Zhang S, Bock F, Si A, Tautz J, Srinivasan MV (2005) Visual
working memory in decision making by honey bees. Proc Natl
Acad Sci USA 102:5250–5255
Anim Cogn
123
Author's personal copy
