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This article appeared in a journal published by Elsevier. The attached
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Animal Behaviour 78 (2009) 543–548
Contents lists available at ScienceDirect
Animal Behaviour
journal homepage: www.elsevier.com/locate/yanbe
Social preferences of juvenile lemon sharks, Negaprion brevirostris
T.L. Guttridge a, b, *, S.H. Gruber b,1, K.S. Gledhill b,1, D.P. Croft c, 2, D.W. Sims d, e, 3, J. Krause a
a
Institute for Integrative and Comparative Biology, University of Leeds
Bimini Biological Field Station
c
Centre for Research in Animal Behaviour, University of Exeter
d
Marine Biological Association of the United Kingdom
e
Marine Biology and Ecology Research Centre, University of Plymouth
b
a r t i c l e i n f o
Article history:
Received 12 March 2009
Initial acceptance 4 May 2009
Final acceptance 9 June 2009
Published online 17 July 2009
MS. number: 09-00166R
Keywords:
elasmobranch
group dynamics
lemon shark
Negaprion brevirostris
predator
schooling
shoaling
Group living in sharks is a widespread phenomenon but relatively little is known about the composition
and organization of these groups. In binary choice field experiments juvenile lemon sharks were
attracted to conspecifics presumably to form groups. Experiments investigating size assortment preferences indicated that lemon sharks aged 2–3 years (but not 0–1 years) preferred to spend more time
with a group of size-matched individuals than unmatched ones. Furthermore, in species association tests
lemon sharks spent significantly more time associating with conspecifics than with a sympatric heterospecific, the nurse shark, Ginglymostoma cirratum. These findings enhance our knowledge of groupjoining decisions in sharks indicating that active mechanisms can play a role in the formation and
composition of shark groups.
Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
Group living among wild animals is a widespread phenomenon
that can provide distinct behavioural advantages such as in
foraging, social learning or by reducing individual risk to predation
(Krause & Ruxton 2002). While diverse terrestrial and aquatic
animals have been the subject of numerous studies to date,
considerably less is known about group living in sharks, even
though this is an ancient lineage comprising top predators that at
certain times appear predominantly solitary in their nature. Many
shark species are known to form groups or loose aggregations
(Klimley & Brown 1983; Ebert 1991; Castro 2000; Sims et al. 2000).
Some of the potential functions of these groupings have been discussed (Sims 2003; Heupel & Simpfendorfer 2005), and include
communication (i.e. transfer of social information, Klimley &
Nelson 1981), courtship (Sims et al. 2000), predatory behaviour
* Correspondence and present address: T. L. Guttridge, Institute for Integrative
and Comparative Biology, L.C. Miall Building, University of Leeds, Leeds LS2 9JT, U.K.
E-mail address: [email protected] (T.L. Guttridge).
1
S. H. Gruber and K. S. Gledhill are at the Bimini Biological Field Station, South
Bimini, Bahamas.
2
D. P. Croft is at the Centre for Research in Animal Behaviour, University of
Exeter, Perry Road, Exeter EX4 4QG, U.K.
3
D. W. Sims is at the Marine Biological Association, Citadel Hill, Plymouth PL1
2PB, U.K.
(i.e. cooperative hunting, Ebert 1991), and group protection or
avoidance of sexual harassment (Holland et al. 1992; Economakis &
Lobel 1998; Wearmouth & Sims 2008). Little systematic information is available, however, on the size and composition of these
groups, or the underlying mechanisms that determine group
composition. It is widely accepted that many shark species show
ontogenetic and sex-based shifts in habitat use and diet composition (reviewed in Wetherbee & Cortes 2004) and these passive
sorting mechanisms may contribute to the formation of size- and
sex-segregated groups (Sims 2003; Hulbert et al. 2005; Wearmouth
& Sims 2008). However, whether sharks are capable of choosing
their social partners through active choice, like many other animals,
remains to be determined.
Our aim in this study was to conduct controlled, captive, choice
experiments to quantify the social preferences of juvenile lemon
sharks. In Bimini, Bahamas, two species of shark occupy the
mangrove habitat extensively during their early life, giving the
opportunity for social interactions to occur between members of
different species. Lemon sharks and nurse sharks, Ginglymostoma
cirratum, in Bimini are slow growing (Barker et al. 2005) and are
known to show site-specific spatial use and long-term residency
(Morrissey & Gruber 1993; Pratt & Carrier 2001; Franks 2007). Both
shark species are occasionally observed in pairs or small groups
(Gruber et al. 1988; Castro 2000). Lemon sharks have been
0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.anbehav.2009.06.009
Author's personal copy
544
T.L. Guttridge et al. / Animal Behaviour 78 (2009) 543–548
observed in small groups performing social behaviours such as
‘follow’ and ‘circle’ (Gruber et al. 1988; Reyier et al. 2008). Nurse
sharks often rest together under rock crevices or mangrove roots
(Castro 2000; Pratt & Carrier 2001) but there has been no
systematic investigation of their grouping behaviour.
Our first experiment investigated juvenile lemon shark sociality; do they have a preference to associate with other sharks
rather than be solitary? A number of studies on juvenile sharks
have indicated that grouping at this vulnerable early life history
stage may be critical to countering the effects of predation and
starvation within a nursery habitat (Holland et al. 1992; Heupel &
Simpfendorfer 2005). This, coupled with the knowledge that
juvenile lemon sharks have extensively overlapping home ranges
(Morrissey & Gruber 1993; Franks 2007) and are often observed
associating in small groups (Gruber et al. 1988), led us to our first
prediction that juvenile lemon sharks prefer to be social. There is
also anecdotal evidence to suggest that sharks form size-segregated
groups (Klimley & Brown 1983; Hulbert et al. 2005). Body size
matching has been described for a number of fresh and salt water
fish species (Peuhkuri et al. 1997; Svensson et al. 2000) and confers
numerous antipredator and foraging benefits (Landeau & Terborgh
1986; Krause 1994). Numerous shark studies have also noted
evidence for size segregation from telemetry and long-line data
(Heupel & Simpfendorfer 2005; Hulbert et al. 2005). Accordingly,
our second prediction was that sharks prefer to associate with
sharks of the same size class. Finally, many juvenile shark species
are highly sympatric, sharing habitat and prey preferences in
nursery areas (Heithaus 2008). In Bimini, Bahamas, juvenile nurse
and lemon sharks are regularly observed to use the same shallow
water habitat and often come in close contact, swimming with each
other or resting close together (T. L. Guttridge, unpublished data);
however, to what extent they associate socially is unknown. Mixedspecies groups are observed in elasmobranchs (Semenuik & Dill
2005) and are also common in other marine taxa (Au 1991).
Differences in social behaviour, daily routine and feeding physiology (Gruber 1982; Castro 2000) led to our final prediction that
these two species will segregate with conspecifics, despite sharing
the same habitat extensively.
METHODS
(5 5 cm diamond-shaped holes) which exposed the sharks to
natural ambient environmental conditions (tidal/lunar cycles,
changes in salinity, temperature, light). Sharks were fed to satiation
every 3 days on a mixed diet of fresh and frozen local fish (no live
prey was used). Each shark was used only once in each trial and
once the trials were completed all were released in their location of
capture. No sharks died during the experiments.
Preference Experiments
Binary choice experiments comprised social and size preference
trials. Sharks were tested in a separate square test pen (10 10 m),
physically divided into three compartments, two outer ones
(2 10 m) and a central area (6 10 m). The central compartment
was further separated into three zones (2 10 m); zones A, B and
the control zone were each demarked by vinyl hose pipe laid on the
sand across the compartment (Fig. 1). Each zone was 2 m wide
corresponding to between two and four body lengths of all sharks
used in this study. A wooden tower 4 m high was used as an
observation post, providing a full view of the pen (Fig. 1).
During each trial, a group of four sharks or a single shark was
allocated at random to the outer compartments. These provided
a stimulus for the test shark to respond to while it was free to move
throughout the three zones of the central compartment. The pen
mesh separating the compartments allowed for visual and olfactory
communication between the test and the ‘stimulus’ sharks. The
cumulative time spent in the association zones was recorded as
a measure of each test shark’s social preference (Pitcher & Parrish
1993) for a particular stimulus. All sharks were given 24 h to
acclimatize to the experimental pen. Each trial lasted 6 h, divided
into two separate 3 h periods, morning and afternoon. Sharks were
recorded as having entered a zone once their head and first dorsal
fin had crossed the demarcation line. At the start of each trial, two
observers would allow 15 min for the sharks to acclimatize to their
presence. Water temperature and depth were also recorded at
10 min intervals throughout the trials as these are thought to
influence shark behaviour (Morrissey & Gruber 1993; Hight & Lowe
2008). Additionally both experiments were based on a balanced
design. This ensured that both sides of the experimental pen
received the same number of experimental replicates, preventing
any bias from occurring.
Study Site and Sharks
This study was conducted in Bimini, Bahamas (25 440 N,
79 160 W), a small chain of islands approximately 85 km east of
Miami, Florida, U.S.A. Lemon and nurse sharks were our test
subjects because of their abundance in Bimini, renowned hardiness
in captivity, relatively small body size, extensively overlapping
home ranges and known heterospecific encounters (Gruber 1982;
Gruber et al. 1988; Castro 2000; Pratt & Carrier 2001; T. L. Guttridge,
unpublished data).
Social preference experiment
We first investigated sociality of the juvenile lemon shark. In
treatment 1 (control), the test shark was given a choice between
two empty compartments; this was to ensure there was no
preference for either side (N ¼ 15). Treatment 2 tested one sizematched shark versus no sharks (N ¼ 8) and treatment 3 considered four size-matched sharks versus no sharks (N ¼ 14). Sharks
were deemed size matched if they were within 5 cm PCL of the test
shark. This size range was selected to ensure that individuals were
the same age (Barker et al. 2005).
Behavioural Experiments
A total of 42 juvenile lemon sharks (X SE ¼ 55:4 7:6 cm,
N ¼ 20 females and 22 males) and 10 juvenile nurse sharks
(X SE ¼ 65:5 7:2 cm, N ¼ 8 females and 2 males) were used for
the behavioural trials. Sharks were captured using gillnets and
transported immediately to a large holding pen in a 100-litre plastic
box. On arrival each shark was restrained while briefly placed in
a trough (10 100 cm) to allow sex determination and precaudal
(PCL) measurement (see Barker et al. 2005 for further details). All
sharks used in the behavioural trials were housed outdoors in two
circular (10 m diameter) holding pens built just offshore in shallow,
sand-bottom flats. The pens were constructed of plastic mesh
Size preference experiment
The second binary choice experiment tested for active preference of size-matched conspecifics versus unmatched conspecifics.
Stimulus and test sharks were assigned to one of two groups based
on body length (group 1: PCL 45–55 cm, age 0–1 years; group 2:
PCL 65–75 cm, age 2–3 years (Barker et al. 2005)). Four stimulus
sharks from each size class were then used in this experiment with
single test sharks. Association behaviour was recorded as above.
Overall, 18 sharks were tested: group 1 (N ¼ 8) and group 2
(N ¼ 10). Stimulus and test sharks were kept in separate holding
pens to prevent any size bias preferences from occurring prior to
each trial.
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T.L. Guttridge et al. / Animal Behaviour 78 (2009) 543–548
545
10 m
Association
zone
A
Control
zone
Association
zone
B
2m
Stimulus
sharks
10 m
Test shark
Observation
post
Figure 1. Semicaptive binary choice experimental set-up.
Heterospecific Experiment
The third experiment investigated species preferences of the
juvenile lemon and nurse sharks. Ten lemon (X SD ¼ 65 7 cm)
and 10 nurse (X SD ¼ 70 9 cm) sharks were caught over a 48 h
period and moved to a holding pen. All sharks were kept in this pen
for 3 days before the experiment, and fed once to satiation. In these
trials, two lemon sharks and two nurse sharks, randomly selected,
were moved from their mixed-species holding pen to an experimental pen (diameter 10 m), where they could freely interact. After
1 h acclimatization, sharks were observed for a 1 h test period. We
recorded at 1 min intervals whether each of the sharks was solitary
or interacting in a group with others as well as whether it was
swimming or resting. Groups were defined within both behavioural
states: a swimming group was when two sharks were within one
body length of each other performing a social behaviour such as
follow, parallel or circle (see Myrberg & Gruber 1974 for details);
a stationary group was when two sharks were resting within one
body length. Environmental conditions were also monitored as
above. Over a period of 5 days, 10 trials were conducted twice daily.
Individual sharks were reused for trials, but never with the same
conspecific or heterospecific.
Data Analysis
To investigate social and size preferences, we compared the total
time spent in each zone to an expected value, calculated by dividing
the total time spent in both zones by 2. A matched-pair t test was
used to test the null hypothesis that there would be no difference
between the observed result and the expected one. For heterospecific groupings an expected value for the frequency of heterospecific groups was also calculated. A total of six test pairs can be
generated from four individuals (there were no triplet or quadruple
associations observed), with the probability of a conspecific pair
being two out of six and a heterospecific pair being four out of six.
Totalling the number of 1 min intervals where sharks were
observed in pairs for each trial and calculating 4/6 of this number
gave an expected value for each trial. This value was then compared
to the observed value using a Wilcoxon signed-ranks test. In
addition, temperature and depth data for all trials were correlated
with time spent in the association zones using a linear model (LM)
from the R stats package (The R Foundation for Statistical
Computing, Vienna, Austria). All data were checked for normality
and heteroscedasticity; if non-normal, data were log transformed.
All statistical tests were two tailed.
RESULTS
Social Preference Experiment
All test sharks used in the binary choice experiments visited
both compartments of the experimental pen. In treatment 1 (no
sharks versus no sharks) juvenile lemon sharks indicated no preference for either side of the experimental pen (paired t test:
t14 ¼ 0.665, P ¼ 0.517). In treatment 2 (one shark versus zero
sharks) and treatment 3 (four sharks versus zero sharks), juvenile
lemon sharks showed a significant preference for the compartment
with the shark/s present based on cumulative time spent in the
stimulus zones (Fig. 2). There was no significant effect of temperature or depth on time spent in the association zones for either
treatment (LM: all P > 0.05).
Size Preference Experiment
Two- to three-year-old lemon sharks demonstrated a preference
for size-matched conspecifics versus unmatched sharks, spending
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T.L. Guttridge et al. / Animal Behaviour 78 (2009) 543–548
Age 2-3 test shark
*
12 500
*
7500
5000
2500
0
Age 0-1 test shark
*
10 000
Mean association time (s)
Mean association time (s)
12 500
1
0
4
0
10 000
7500
5000
2500
Stimulus sharks
Figure 2. Mean time SE spent by juvenile lemon sharks near either one stimulus
shark versus zero or four stimulus sharks versus zero. *P < 0.05, matched-pair t test.
a significant amount of time with size-matched individuals (Fig. 3).
For 0–1-year-old sharks, on the other hand, we detected no such
preference for size-matched or unmatched sharks based on time
(paired t test: t7 ¼ 1.178, P ¼ 0.277; Fig. 3). There were no significant effects of temperature or depth on time spent in the association zones for both shark sizes (LM: all P > 0.05).
Heterospecific Experiment
To test whether nurse and lemon sharks associated with
conspecifics over heterospecifics it was important to demonstrate
first that the shark species did not differ in their degree of sociality
(i.e. the number of 1 min intervals they were observed in a group,
either stationary or mobile). No significant difference was found
(paired t test: t9 ¼ 0.58, P ¼ 0.57; Fig. 4a). Our main result was that
far fewer heterospecific pairs were observed than expected
(Fig. 4a). Furthermore, a significant difference was found for the
context of associations, with lemon sharks preferring to interact
while mobile and nurse sharks while stationary (Fig. 4b). A significant relationship was also found between depth and nurse shark
sociality; as depth decreased sociality increased (LM: Rs ¼ 0.51,
F8 ¼ 8.928, P ¼ 0.017). No such relationship was found for nurse
sharks with temperature or lemon sharks with temperature and
depth (LM: all P > 0.05).
DISCUSSION
This study demonstrates that juvenile lemon sharks actively
prefer to be social. Test sharks chose to spend more time in an
association zone that was adjacent to a compartment with one or
four stimulus sharks present versus an empty one. Although
widely recognized in many shark species (Heupel & Simpfendorfer
2005; Hight & Lowe 2008), grouping behaviour has yet to receive
the attention that it has been given in other taxa such as cetaceans
(Lusseau 2003), primates (Strier et al. 2002) and teleost fish (Croft
et al. 2004). However, an active social preference such as that
found here suggests that it may be important for the survival and
development of juvenile sharks. Previous hypotheses for juvenile
shark grouping behaviours have included association as a means
to reduce predation risk (Holland et al. 1992) or to forage more
efficiently (Heupel & Simpfendorfer 2005). However, most of these
studies have simply inferred group formation between sharks
0
Age 2-3
Age 0-1
Age 2-3
Stimulus groups
Age 0-1
Figure 3. Mean time SE spent by juvenile lemon sharks near either four sizematched stimulus sharks versus four unmatched ones. *P < 0.05, matched-pair t test.
based on simultaneous detections on underwater tracking devices
or captures on long lines. With these techniques there is no way of
identifying for certain whether the sharks were actually associating in social groups (animals drawn to one another) or whether
they were aggregations (animals drawn together because of
a common attractive resource or constraint, e.g. food or shelter). At
our study site, juvenile lemon sharks have been observed in the
wild associating in small groups and have even been seen to corral
small bait fish together in the shallow flats (Morrissey & Gruber
1993). So we know that these sharks have been observed to group
in the wild, but how strong is the attraction? Our first finding
confirms and emphasizes that juvenile lemon sharks are attracted
to associate with conspecifics, even when the stimulus is reduced
to one individual. Future group-living studies on sharks should
now consider that, in addition to passive factors, such as habitat or
prey preferences, contributing to the formation of groups, sharks
are actively associating with conspecifics. This may lead to studies
investigating the potential for individual recognition and cooperation. Juvenile lemon sharks in Bimini grow slowly (Barker et al.
2005), show site-specific spatial use and long-term residency and
have extensively overlapping home ranges in their early life
history (Morrissey & Gruber 1993; Franks 2007). This evidence
and the tendency to associate in small groups or pairs could
promote the formation of persistent associations within this
population of juvenile lemon sharks. Co-occurrence of particular
individuals with one another seems to occur in many taxa
including marine and freshwater fish (Klimley & Holloway 1999;
Croft et al. 2004) and marine and terrestrial mammals (Christal &
Whitehead 2001), including primates (Strier et al. 2002). This type
of associative pattern has been linked to the evolution of cooperation and may also have implications for the flow of information
through a population and social learning (Brown & Laland 2003;
Croft et al. 2008).
Teleost fish research has demonstrated that information is
transferred more effectively between familiar individuals (Swaney
et al. 2001) and that familiar fish shoals have improved coordination of antipredator behaviour (Chivers et al. 1995). Future studies
on juvenile sharks should address whether social partner
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T.L. Guttridge et al. / Animal Behaviour 78 (2009) 543–548
0.8
**
(a)
0.7
Proportion of 1 h trial
0.6
0.5
0.4
0.3
0.2
0.1
0
LL
NN
LN
L
N
Group or solitary behaviours
0.8
Median proportion of pair behaviours
(b)
**
Lemon
Nurse
0.7
**
0.6
0.5
0.4
0.3
0.2
0.1
0
Mobile
Stationary
Pair behaviour
Figure 4. (a) Mean proportion of time SE spent either solitary, in a conspecific pair
or with a heterospecific by juvenile lemon and nurse sharks. LL: lemon shark pair; NN:
nurse shark pair; L: lemon solitary; N: nurse solitary. *P < 0.01, matched-pair t test. (b)
Median proportion of time spent by juvenile lemon and nurse sharks in either
a stationary or mobile pair. Error bars show upper and lower quartiles. **P < 0.01,
Wilcoxon signed-ranks test.
547
Motta 2008). For teleost fishes, assorting with size-matched
conspecifics is thought to be adaptive as it reduces predation risk
through the ‘oddity effect’ and increases foraging efficiency
through avoidance of larger, more competitive individuals (Peuhkuri et al. 1997). Similar factors may account for the preferences in
2–3-year-old sharks and provide an interesting field for future work
on shoaling behaviour in sharks.
Although sociality has many advantages, this may not necessarily extend to social groups forming between species. In our
mixed-species trial, both lemon and nurse sharks interacted almost
exclusively with conspecifics. Mixed-species groups in other
animals are usually made up of closely related, sympatric species
that have similar behavioural and phenotypic traits (Krause &
Ruxton 2002). Lemon and nurse sharks are from different shark
families, Carcharhinidae and Ginglymostomatidae, respectively,
and vary in coloration (Gruber 1982; Castro 2000). They also have
differing daily activity budgets and social behaviour. In the wild,
juvenile lemon sharks patrol the mangrove fringes and sand flats
(Morrissey & Gruber 1993; Franks 2007) performing mobile social
behaviours (e.g. follow and parallel, Gruber et al. 1988) indicative of
schooling fish (Pitcher & Parrish 1993). In contrast, juvenile nurse
sharks, although frequenting similar habitats, spend long periods of
the day resting, often in aggregations (Castro 2000). This is very
much like some species of insects and crustaceans that are primarily
social when they roost (Childress & Herrnkind 2001; Jeanson &
Deneubourg 2007). In this study, while both sharks showed similar
levels of sociality with conspecifics, the context of interactions was
different, with lemon sharks interacting while mobile (>95%) and
nurse sharks while stationary (>95%). The segregation found in this
study is probably attributable to passive and active mechanisms
that prevent mixed-species group benefits from occurring. Nurse
and lemon sharks may overlap spatially while searching for
productive food patches and avoiding dangerous areas rather than
searching for individuals to group with.
Sharks’ relative brain mass overlaps with that of mammals and
birds (Northcutt 1977). Numerous studies in mammals and birds
have correlated complex social behaviours with brain size
(reviewed in Striedter 2005). Shark species that are known to
school and group have the largest relative brain size (Yopak et al.
2007). Our study shows that sharks actively associate with each
other, creating the potential for social learning and cooperation
between individuals. These topics are of huge interest in other taxa
(Brown & Laland 2003) and could have important implications for
sharks in the context of fisheries and ecotourism (Fernö et al. 2006;
Laroche et al. 2007) which provide a fruitful field for future studies.
Acknowledgments
preferences are indeed observed and maintained through familiarity and/or individual recognition.
Anecdotal reports of size-segregated groups are common in
many shark species (Klimley & Brown 1983; Hulbert et al. 2005).
However, no experimental preference test has ever been conducted. Our 2–3-year-old sharks showed a preference for sizematched groups, indicating that juvenile sharks, like many marine
and freshwater teleost fishes, assort by size (Peuhkuri et al. 1997;
Svensson et al. 2000). In contrast, for sharks aged 0–1 years our
results detected no such preference for either size-matched or
unmatched stimulus groups. We hypothesize that the observed
asymmetry in preferences might be because larger sharks accumulate more information about the habitat, predators and local
prey, so associating with these individuals could allow for the
transfer of this information. Recent studies on shark feeding
behaviour have identified that experience can reduce the time
taken to locate, capture and consume prey (Ciaccio 2008; Lowry &
The study was supported by a Leverhulme study abroad
studentship awarded for postgraduate work to T.L.G., J.K. and D.P.C.
were supported by grants from the EPSRC and the NERC (NE/
E001181/1), respectively. We also thank the numerous volunteers
and staff members at the Bimini Biological Field Station who
worked so hard to obtain the necessary data set. The study would
not have been possible without financial support from the Bimini
Biological Field Station, Lacy Hoover, Earthwatch Institute, National
Science Foundation (NSF-OCE 97-12793) and Department of
Education, State of Florida (FLORIDA 8749703000001).
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