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This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright Author's personal copy 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. Author's personal copy 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 Author's personal copy 546 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 Author's personal copy 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. 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