Can Thermoclines Be a Cue to Prey Distribution for
Marine Top Predators? A Case Study with Little Penguins
Laure Pelletier1,2*, Akiko Kato1,2, André Chiaradia3, Yan Ropert-Coudert1,2
1 Université de Strasbourg, IPHC, Strasbourg, France, 2 CNRS, UMR7178, Strasbourg, France, 3 Research Department, Phillip Island Nature Parks, Cowes, Victoria, Australia
Abstract
The use of top predators as bio-platforms is a modern approach to understanding how physical changes in the environment
may influence their foraging success. This study examined if the presence of thermoclines could be a reliable signal of
resource availability for a marine top predator, the little penguin (Eudyptula minor). We studied weekly foraging activity of
43 breeding individual penguins equipped with accelerometers. These loggers also recorded water temperature, which we
used to detect changes in thermal characteristics of their foraging zone over 5 weeks during the penguin’s guard phase.
Data showed the thermocline was detected in the first 3 weeks of the study, which coincided with higher foraging
efficiency. When a thermocline was not detected in the last two weeks, foraging efficiency decreased as well. We suggest
that thermoclines can represent temporary markers of enhanced food availability for this top-predator to which they must
optimally adjust their breeding cycle.
Citation: Pelletier L, Kato A, Chiaradia A, Ropert-Coudert Y (2012) Can Thermoclines Be a Cue to Prey Distribution for Marine Top Predators? A Case Study with
Little Penguins. PLoS ONE 7(4): e31768. doi:10.1371/journal.pone.0031768
Editor: Howard Browman, Institute of Marine Research, Norway
Received July 27, 2011; Accepted January 18, 2012; Published April 20, 2012
Copyright: ß 2012 Pelletier et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was funded by grants from the Japan Society for Promotion of Science, the Région Alsace, the Centre National de la Recherche Scientifique
(CNRS) and the BHP-Billiton. Note that Phillip Island Nature Park is a not-for profit organization dedicated to the protection and conservation of little penguins.
The Park is controlled by a Board of Management appointed by the Minister for Environment of Victoria, Australia. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors received funding from BHP-Billiton in the form of donations to support their research. The company did not participate in or
interfere with the design, data collection and analysis, or output of this research. This does not alter the authors’ adherence to all the PLoS ONE policies on sharing
data and materials. All data are available at the National Ecological Meta Database (Australia) http://www.bom.gov.au/jsp/bmrc/NEMDSearch/
NemdSearch?lookup_id = 81&submit = Submit. YRC is one of approximately 1,000 academic editors for PLoS ONE and as such had no access to the peer
review or acceptance process for this manuscript (which was conducted with no regard to his position on the board). PLoS ONE academic editors are volunteers
and receive no compensation for their services.
* E-mail: laure.pelletier@iphc.cnrs.fr
as shown, for example, in Argentine anchovies (Engraulis anchoita),
which distribute preferentially in the layer immediately above the
thermocline [9]. This is probably because thermoclines are rich in
nutrients where the different levels of the food web concentrate
[10,11,12]. For instance, the foraging behaviour of thick-billed
murres (Uria lomvia) varies with the vertical distribution of prey,
which is associated with annual variation in the intensity of the
thermocline and water temperature at different depths [13].
Another seabird, Rhinoceros auklets (Cerorhinca monocerata) usually
dive above or around the thermocline, indicating that either the
distribution of their prey is constrained by this shift in temperature
[14] or that the escape speed of the ectothermic prey is slowed
down by the sudden change in temperature, making them easier
targets to predators.
Here, we studied the foraging behaviour of the little penguin
(Eudyptula minor), a marine diving seabird in which case the link
between thermocline and foraging success has also been reported
[15]. These authors found that a reduction in thermal stratification
in the water detected by data loggers in a weak El Niño year (2006)
was associated with reduced foraging success of little penguins.
Thus, the increase in the mixing of the water column could have
resulted from an increase in the wind force and in the number of
storms [15], although other physical factors may lead to a similar
mixing. The foraging patterns of penguins suggested that their
prey were dispersed widely in the presence of poorly stratified
waters [15]. In these studies [13–15], the absence of the
Introduction
During reproduction, parents have to make decisions to
optimise energy acquisition to simultaneously address their own
needs and that of their offspring [1]. To this end, breeding animals
should optimally match their peak of food requirements with the
seasonal peak of resource availability [2]. A mismatching of these
peaks can cause a decrease in the current reproductive output, as
well as a reduction in the animal’s long-term fitness [3,4]. The
impact of this match-mismatch is particularly significant in marine
ecosystems. The open ocean is a heterogeneous environment that
is characterized by patchy prey distribution over a large time and
spatial scale. As a consequence, top predators target places of high
prey abundance, the hot spots which are a result of physical
processes, such as up-wellings, eddies, gyres or sea-ice edges [5].
These places often change seasonally, annually or on a decadal
basis [6]. Prey availability in these places can be affected by
changes in oceanographic conditions, which could affect foraging
success of marine top predators. These changes taking place at
local foraging zones are generally influenced by large-scale
processes [7] and can trigger a mismatch between predators and
their prey.
For diving marine animals, oceanographic conditions of the
water column, such as the presence of a thermocline, can also be
important for the distribution of prey [8]. Clupeids, an abundant
food source for top predators, can aggregate around thermoclines
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Thermocline Affects Penguin Foraging Behaviour
the signal using purpose-written macro in Igor Pro (Wavemetrics
Inc., USA, Version 4.02) [24]. The acceleration data were
separated into low and high frequency components using the
IFDL package from Igor [22]. Each propulsive stroke was
recorded on the heaving axis resulting in a forward acceleration
recorded on the surging axis. The amplitude of each stroke was
analysed using the heaving acceleration, which is the most
sensitive signal to detect frequency of strokes [22]. We could then
identify periods of higher than the normal amplitude values
observed during diving periods. Those periods of high amplitude
were used as a proxy of prey encounter and pursuit [23]. Note
this method does not provide a direct measure of prey
consumption but prey encounter, which gives an estimate of
food available to a bird during a trip. We calculated the ratio of
the number of dives with prey encounter to the total number of
dives during the foraging trip, as an index of hunting efficiency
[24]. We determined prey encounter rates for depths .10 m
because the high buoyancy of the birds in ,10 m depth
influences the flipper beating activity [15,23].
Given that temperature sensors have a delayed time response
(T0.9 < 15 sec) [14], we corrected the temperature associated to
depth following Daunt et al. [25]. Within a day trip, we determined
a single thermal profile of the water column for each bird. For
each hour of the day, we obtained a temperature profile by
grouping temperatures from the same depth from both the descent
and the ascent phase of the dive [15] during the course of the
deepest dive (.25 m) [14]. From the several profiles obtained
from a given bird, we calculated a mean temperature every
2 meters. This resulted in one thermal profile for each penguin
that we then used to determine the presence or absence of a
thermocline, defined as a zone of rapid decrease of temperature in
the water column [26] in the five weeks of this study. The depth of
the thermocline was visually detected from the vertical profile of
temperature.
Statistical analysis of dive parameters was performed using the
R software (version 2.8.1) [27]. For the hunting efficiency
analyses, the sample size was only 39 birds due to missing data
or excluding birds, which did not dive deeper than 10 m. We
tested for normality and applied a logarithmic transformation
when necessary. We used a generalized linear mixed model
(GLMM) [28] with individuals as a random factor. For
proportions, a binomial distribution was used, while a Poisson
distribution was used for other variables. Subsequently, multiple
comparisons were undertaken using the Tukey’s post hoc test.
Unless otherwise stated, values are presented as mean 6 SE with
significance at 0.05.
thermocline reduced their foraging success during chick rearing,
leading to a decrease in reproductive success. While previous
studies [13–15] have looked at a composite of breeding/foraging
success in relation to predominant oceanographic conditions over
a whole season [16], no study, to our knowledge, has investigated
the rate of prey encounter in relation to oceanographic conditions
over short time scale (i.e. within a season).
In this study, we examined changes in the foraging activity and
efficiency of breeding little penguins, while simultaneously
monitoring changes in the vertical thermal characteristics of the
water in their foraging zone. Since thermoclines can act as a
boundary to prey distribution seasonally [15], we hypothesised
that the presence of a thermocline could be a reliable signal of
resource availability. We deployed miniature accelerometers on
little penguins at early chick-rearing phase in a single season of
high breeding success, when food supply was probably not a
limiting factor [17]. We expect the ability of penguins to match the
energetically demanding chick-rearing phase [18] with the
presence of a thermocline to be critical to the foraging behaviour
of these diving seabirds.
Materials and Methods
The study was conducted on the little penguin breeding colony
at Phillip Island (38u319S, 145u099E), Victoria, Australia. We
deployed data loggers on 43 adult penguins at guard phase,
tending chicks aged 1 to 2 weeks. At guard phase penguins make
one-day foraging trips within 20 km from the colony [19]. The
study period spanned 5 weeks, from 13 November to 17
December 2005. We used 12-bit, 52615 mm, four-channel data
loggers that weighed 16 g (M190L-D2GT, Little Leonardo,
Tokyo, Japan) to record depth (resolution 0.05 m) and temperature (0.01uC) every second. This logger also recorded two axis
accelerations along the longitudinal body axis (surging) and the
dorso-ventral axis (heaving) of the bird, between 230 and
30 m s22 at 32 Hz. The accelerometer measured both specific
acceleration (e.g. movement) and gravity-related acceleration (e.g.
posture).
Penguins were captured in their artificial nest box and loggers
were attached on the lower back of the bird with Tesa tape [20].
All birds were recaptured in their nest boxes, the logger retrieved
and the tape completely removed. Attachment and removal of the
logger was completed within 5 min from the capture, and birds
were returned to their nest-boxes. All equipped birds were
monitored until the end of breeding [21]. Fieldwork protocol
was approved by the Animal Experimentation Ethics Committee,
Phillip Island Nature Park (PINP AEEC, number PINP AEEC
2.2004) with a research permit issued by the Department of
Sustainability and Environment, Flora and Fauna (number
10003419) of Victoria, Australia.
Data were downloaded from the loggers into a computer and
analysed using Igor Pro (Wavemetrics Inc., USA, 2008, Version
6.04). Given the low accuracy of the depth sensors at surface, only
dives .1 m were considered for analysis [22]. Dive depth, total
number of dives, time spent underwater, defined as the sum of all
dive durations, and proportion of time at the bottom phase were
calculated for each individual. A dive started and ended when
birds departed and returned to the water surface. Start and end of
bottom phases were defined as the first and last time the depth
change rate became ,0.25 m s21 during a dive [22]. It is during
the bottom phase of dives that little penguins encounter most of
their prey (75.4%) [23].
We measured foraging efficiency using frequency and amplitude of flipper beatings, which were automatically extracted from
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Results
All equipped birds made one-day trips and succeeding in raising
their chicks until fledging. During the five weeks of the study,
significant changes in the thermal profiles were observed in the
water column (Figure 1). A thermocline was visible in the first
three weeks, but not detected in the last two weeks. The
thermocline was higher in the water column during the second
week (24–40 m) compared with the first (44–56 m) and third
weeks (38 m - the end of the thermocline being not detected).
During the third week, the thermocline disappeared gradually
from temperature profiles.
The mean number of dives performed by penguins during a
foraging trip varied on a weekly basis (Table 1). Birds foraging
during the second week made significantly less dives than
individuals from other weeks (Tukey’s post hoc test: all p-values
,0.05, Table 1). Moreover, deep dives (.25 m) were more
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Thermocline Affects Penguin Foraging Behaviour
Figure 1. Changes of the thermal profiles of the water column in Bass Strait, Australia. During five weeks in November-December 2005, as
measured by little penguins equipped with data loggers during one-day trips at their guard phase of breeding. Each temperature profile corresponds
to a mean water temperature (6SD) every 2 meters calculated from several profiles obtained from each given bird (identified by date and nest
number). The thermocline is framed in bold. The seabed is situated between 60 m (dotted, horizontal grey line) to 80 m (solid, horizontal grey line).
We only represented the dive/temperature profiles of those birds that dived deeper than 25 m (see Materials and Methods for details).
doi:10.1371/journal.pone.0031768.g001
frequent in the first two weeks (between 10 and 15% dives) than in
the subsequent three weeks (4% of dives). A reduction in the mean
dives depth was observed after the third week (Table 1).
The total time spent underwater also differed weekly (Table 1).
During the first week,birdsspent significantly morehours underwater
than individuals in all other weeks (Tukey’s post hoc test: all p-values
,0.05). For the second week, birds spent on average less time
underwater, but also less time (in proportion) at the bottom phase of
dives (Table 1). The time spent at the bottom phase of dives was
equivalent for birds foraging the other four weeks (Table 1, Tukey’s
post hoc test: all p-values .0.05). The hunting efficiency was higher
for the first three weeks than for the last two (Figure 2), although the
average efficiency of individuals from week 2 and week 5 was not
significantly different (p-value = 0.056).
Table 1. Comparison of different diving parameters of little
penguins during one-day trips at guard phase of breeding.
Nb of dive
Week 1
Week 2
Week 3
Week 4
Week 5
(n = 6 )
(n = 12 )
(n = 10 )
(n = 7 )
(n = 8 )
8926127a 600637b
a
a
9796140c 11656140a 14416149a
Dive depth (m)
10.960.1
10.960.1
8.260.1a,b 6.360.1c
Time underwater
(h)
6.660.4a
4.460.3b
4.860.6c,d 4.960.6b,c 5.860.3d
Discussion
6.160.1b
The thermal stratification of the water column in the foraging
zone of little penguins changed over the course of the chick-rearing
phase. These changes coincided with a decrease in foraging
performance over time. Penguins showed higher hunting efficiency
in the first 3 weeks when the thermocline was detected in the water
column. Hunting efficiency declined while the total number of dives
Bottom phase (%) 35.261.8a 28.361.4b 34.262.4a 35.762.2a 3760.7a
Values expressed in mean 6SE over the five weeks. a, b, c, d: letters indicate
significant differences (at 0.05). n = number of birds.
doi:10.1371/journal.pone.0031768.t001
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Thermocline Affects Penguin Foraging Behaviour
capture them. In contrast, penguins increased the number of
dives in the last two weeks reflecting an increase in birds’
foraging effort. Despite of greater number of dives, the prey
encounter was lower than the first three weeks. This lower
foraging efficiency coincided with absence of a thermocline in
the foraging zone of the penguins towards the end of guard
phase. In the absence of a thermocline, prey were likely to be
more dispersed in a mixed water column so penguins were
exploiting a less optimal environment.
Many seabird species can increase their foraging range and
decline foraging success as the breeding season progresses. This
change in foraging behaviour can be explained by prey depletion
within the foraging zones close to the colony, the so-called
Ashmole’s halo effect [33–36]. However, this energy-limitation
hypothesis does not always find support in the literature [37]. Our
results suggest an alternative explanation for a shift in foraging
behaviour of diving birds during breeding. The lower prey
encounter rate in the foraging area as the breeding season
progresses could be explained by changes in oceanographic
conditions that limit access to prey. For little penguins and
perhaps for most diving marine animals, the presence and
abundance of prey is not only associated with their distance from
the central place and prey depletion but also with factors that
affect prey distribution and availability in the water column, such
as a thermocline and its change over time.
The absence of the thermocline late in the breeding season
indeed led to an increase in diving effort while reducing hunting
efficiency. We know that earlier breeding onset of little penguins
has been related to an increase in sea surface temperature (SST) 3–
6 months prior to breeding [38]. An increase in SST is precisely
what can lead to the formation of a thermocline because
stratification is initiated when the water surface warms up and
separates from much colder deep water [39]. We propose here
that if individuals are indeed adjusting the onset of breeding using
SST information before the reproduction, then these individuals
could be in a position to match their peak of food demand to peaks
of food availability, as defined by the presence of thermoclines in
their foraging zone. One main condition for this would be the
ability of these individuals to relate those thermal regimes with
prey availability and this can come through the accumulation of
breeding attempts, i.e. experience [24,40].
In this context, future work should examine how individual’s
characteristics, such as age or experience, influence the ability of
penguins to match their peak of food requirement to the presence of
a thermocline in their foraging environment. These are important
parameters to assess climatic scenarios, such as the predicted
increase in El Niño events in the next decades [41]. El Niño events
could lead to a greater mixing of the water column and
disappearance of thermocline, affecting the foraging patterns of
marine predators that depend, as shown in this study, on these
thermal structures to forage more successfully.
Figure 2. Changes of the hunting efficiency during the five
weeks. Mean hunting efficiency 6SE (see Materials and Methods) of
penguins for each week is represented. Letters a, b and c indicate
significant differences (0.05) following GLMM-binomial and Tukey’s post
hoc tests. n = number of birds.
doi:10.1371/journal.pone.0031768.g002
tended to increase when the thermocline weakened or was no longer
detected.
No thermocline was detected in the temperature profiles recorded
by the data loggers in the last two weeks of our study. A possible
explanation for this is that the thermocline was deeper and not
reached by penguins in the last two weeks. This is, however, unlikely
given that little penguin can dive up to 70 m [29], implying that they
are capable of foraging throughout the whole water column of Bass
Strait with the mean depth between 60–80 m [30]. In week 5 for
instance, birds dived as deep as 70 m, without detecting a
thermocline. In fact, it would be surprising if the thermocline is
located below 70 m, i.e. only 10 m above the maximum seabed
depth in the penguin’s foraging zone. In any case, .70 m depth
would be beyond the penguin’s reach. Secondly, birds could be
foraging above the thermocline so that changes in water temperature were not detected by the data loggers. However, our biological
data do not support that since penguins had lower hunting efficiency
in weeks 4 and 5, suggesting that their foraging conditions were
similar to those observed when thermoclines were absent. For these
reasons, we suggest that the temperature profile recorded by the
loggers were a close to real representation of the thermal structure in
penguins foraging area over the course of our study (Figure 1).
When the thermocline was present in the water column, birds
showed a higher hunting efficiency than when the thermocline was
absent. Thermoclines are known to aggregate marine life. For
example, anchovies, a common prey for little penguins [31], are
known to concentrate around thermoclines [9]. While we believe
prey can still be found sporadically distributed in the water column,
the thermocline may act as a physical barrier, preventing prey from
dispersing. The ectothermic nature of fish could be one possible
explanation for this behaviour. The abrupt cooling when crossing
the thermocline would reduce prey metabolism and consequently
their maximum escape speeds, thus making them easy prey to
predators [15,32]. Alternatively, a high concentration of fish above
the thermocline could be as consequence of phytoplankton being
concentrated in the upper water mass [10,11,12].
Interestingly, birds foraging during week 2 had a high prey
encounter with the smallest diving effort (few dives, little time
spent underwater, short bottom time), which coincided with the
period where the thermocline was the shallowest in the water
column. This suggests that prey were probably concentrated at
shallow waters on week 2 so penguins had less diving effort to
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Acknowledgments
We thank the continuing support from the Phillip Island Nature Parks and
its staff, in particular to people from the Research Department: P. Dann,
L. Renwick, P. Wasiak, R. Kirkwood and M. Salton. P. Fallow assisted in
the field and I. Zimmer provided invaluable input during the analysis. We
also thank P. Gaspar for his comments and help to improve our manuscript
and P. Wasiak for proof-reading the final version.
Author Contributions
Conceived and designed the experiments: LP AK AC YRC. Performed the
experiments: AK AC YRC. Analyzed the data: LP AK. Wrote the paper:
LP AK AC YRC.
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