The Social Organization of the Lemon Shark, Negaprion brevirostris
Tristan Guttridge & Dr. Samuel H. Gruber
In recent years our understanding of social interactions within and between animal populations has advanced considerably, largely due to the application of network analysis to wild populations of free-ranging teleost fish1 and dolphins2, which has provided a framework to study sociality and enabled the quantification of inter-individual associations. This has revealed that organisms from taxa, such as fish, which were at first thought to be socially primitive and simple3, actually have highly complex and structured social networks4.
Photo by Walt Stearns
Sharks are another group of marine animals that are often observed in groups, scalloped hammerheads (Sphyrna lewini) swim in polarized schools5 whilst grey reef sharks (Carcharhinus amblyrhynchos) aggregate in female only refuges6. Their relative brain-body ratios are comparable to those of birds and mammals7, suggesting that they might be capable of complex cognitive behaviours, analogous to that of larger brained vertebrates. For example, various species of sharks have been shown to form dominance hierarchies, in the wild8 and in captivity9 and in addition to this they are capable of adaptive learning10.
Previous research has developed numerous theories for the functions of these shark aggregations11-12 but very little is known about: (1) the interactions between individuals of the group; (2) the mechanisms underlying social recognition; (3) the factors (morphological, behavioural or ecological) that affect these associations and (4) the influence that these interactions have on the overall organization, structure, and complexity of the group/population. So the next logical step is to investigate the organisation of shark aggregations, determining whether social interactions are characterized by non-random partner selection, as in some teleost fishes13 exploring the factors that influence these interactions. Network analysis can then be used to quantify the interactions and enable the development of a social network, providing information both locally and globally about population structure, organisation, complexity and connectedness.
The lemon shark is a large Atlantic coastal species that has been studied extensively for the past 20yrs by Prof. Gruber and his colleagues at Bimini, Bahamas. Research has indicated that juvenile lemon sharks exhibit high site fidelity with distinctly overlapping home ranges14. Furthermore sharks are often observed in small groups performing socially interactive behaviours, such as 'circle-head-to-tail' and 'follow' 15 and during population surveys, using gillnets, there are peaks in numbers captured and sharks are rarely caught singly. This evidence and the recent discovery of two winter aggregations of juvenile and adult lemon sharks, at Cape Canaveral and Jupiter inlet, Florida, respectively, has added to the growing view that lemon sharks are highly sociable animals. To protect these vulnerable concentrations of sharks from overexploitation by commercial and recreational fishing, it is imperative to learn more about why aggregations are formed and the mechanisms underlying their structure and formation.
1. Investigate whether lemon sharks prefer to associate with conspecifics to being solitary and if so determine a) what factors influence these social interactions e.g. body size, sex, familiarity etc and b) the underlying mechanism behind such a preference i.e. use of visual, acoustic and olfactory cues.
2. Investigate if sharks are capable of recognizing individual conspecifics and determine if they show active-partner preference.
3. Apply network analysis to populations of adult and juvenile lemon sharks investigating information about social structure, complexity and organisation.
Methodology Study organism and field sites:
The lemon shark makes an excellent experimental subject for quantitative studies due to its size, abundance, generalised structure and good survival in captivity16. Intensive research since 1963 by Prof. Gruber has developed the lemon shark into an important 'model species' for both management and conservation of large coastal sharks.
Bimini Biological Field Station
Bimini consists of two mangrove-fringed islands that supply warm, shallow protected lagoons - ideal nursery grounds for a population of juvenile lemon sharks to grow up in. The sharklab has been running for 20yrs under Prof. S.H.Gruber (collaborator/advisor) and will provide both scientific and logistics support for this project including: scientific equipment, vessel hire, maintenance/fuel and the services of staff and other volunteers to assist in data collection.
Lemon Shark Aggregation - Jupiter Inlet, Florida, USA
For the past 5yrs an aggregation of 100+ lemon sharks has been observed annually at a location just off the East coast of Florida. Here the sharks rest on the seabed in great numbers differing in size and sex, for the winter months. Work investigating social behaviour in the adult phase of the lemon shark will be undertaken here alongside Prof. Gruber and his colleagues.
Behavioural pen-based experiments:
To investigate the theory behind social behaviour a series of pen-based experiments will be conducted in the shallow protected mangrove waters of Bimini, Bahamas. Here a population of 300 juvenile lemon sharks are easily accessible to capture and once caught very manageable/maintainable in small mesh constructed pens.
Experiment 1. - Shark association preferences
Binary choice tests will be used to investigate preferences for associating with conspecifics. Size, sex, familiarity, satiation and other variables will be tested along with the mechanisms that mediate these choices (visual, acoustic and olfaction).
Experiment 2. - Shark conspecific recognition and active partner preference.
A series of reward/recognition experiments will investigate a shark's ability to recognise individual conspecifics. Again many factors will be varied and the mechanisms enabling this discrimination will be identified. Furthermore to investigate active partner preference a nearest neighbour experiment will be set up using familiar and non-familiar individuals to determine any partner preference.
Preliminary visual surveys at both of the field sites to determine temporal and spatial periodicity of juvenile and adult lemon shark group interactions, sex ratio and animal orientation.
In situ behavioural observations/interactions - paralleling, circling, following etc will be recorded through a combination of aerial (microlite or tower) and underwater surveys.
Stereophotography used to determine adult lemon shark size, sex and nearest neighbour distance.
Tag and capture - enabling the attachment of acoustic tracking devices and conventional tags, along with obtaining information on size, sex, maturity, parasite load, weight, condition etc.
Acoustic tracking used to investigate the local movements of individual members of the adult lemon shark aggregation. Questions such as; "Are there sub-groups? Do sharks show active partner-preference?" will be considered.
Finally the results of the behavioural experiments along with the wild observations will be used to build an individual profile for each shark, allowing any consistent behavioural traits to be identified. These can then be used to determine if sharks differ individually i.e. are some sharks more sociable than others (do they have stable personality traits)? Finally once data on inter-individual interactions has been collected network analysis can be used to investigate how these interactions affect the organisation/structure of a semi-wild captive juvenile lemon shark population and a wild adult lemon shark population.
To capture juvenile and adult lemon sharks gill nets and rod and reel fishing will be used, respectively. These techniques have proved to be successful for numerous studies14, 16 and have been used for many years at Bimini, with low mortality rates, <5%17.
Significance and Originality
Sharks are of great importance both economically, through tourism and the fishing industry, and ecologically, through their role as a top predator in the marine ecosystem. However, recent uncontrolled exploitation18 has put many species at great risk from extinction, especially those that form large aggregations.
The aforementioned lemon shark aggregation at Jupiter inlet, Florida is an unknown phenomenon for any shark species in US continental waters, making it potentially a very attractive, but vulnerable resource to disturbance from ecotourism operations, such as diving and recreational fishing, as well as exploitation from commercial fisheries. Recent legislation has given limited protection to lemon sharks in US waters but the IUCN (International Union for Conservation of Nature and Natural Resources) still classifies them as near endangered. Furthermore tag and recapture research has suggested that they are wide-ranging, moving in and out of international waters, confirming that protection and unified effort is needed on a more global scale in order to ensure their survival.
So what this research aims to do is to investigate the mechanisms underlying the formation of such aggregations, assessing social interactions between individuals and determining the key factors that affect these associations. Social encounters between individuals play an important role in the transfer of information, but also in the transmission of disease. As inter-group contact increases so does the rate at which an infective agent can spread through a population. Therefore to control/predict or simply understand this spread it is imperative to unravel structure and organisation of a group/population, which will in turn help us to develop/identify strategies in fisheries management.
Finally, predators such as sharks are beginning to discard the 'mindless feeding machine' tag that they are so often labelled with. Understanding more about shark social behaviour will hopefully encourage people to relate to them on a more objective level, increasing both respect and awareness.
References 1Croft D.P., Krause. J., James. R. (2004). Social networks in the guppy (Poecilia reticulata). Proc. R. Soc. Lond. Biol. Lett. 271:516-519. 2Lusseau, D. (2003). The emergent properties of a dolphin social network. Proc. R. Soc. Lond. Ser. B. Biol. Sci. 270:S186-S188. 3Laland, K.L., Brown, C., Krause, J. (2003). Learning in fishes: from three-second memory to culture. Fish and Fisheries 4, 199-202. 4Croft, D. P., R. James, A. J. W. Ward, M. S. Botham, D. Mawdsley and Krause, J. (2005). Assortative interactions and social networks in fish. Oecologia. 143: 211-219. 5Klimley, A.P. and Nelson, D.R. (1984). Diel movement patterns of the scalloped hammerhead shark (Sphyrna lewini) in relation to El Bajo Espiritu Santo: a refuging central-position social system. Behav. Ecol. Sociobiol. 15:45-54. 6Economakis, A. E. and Lobel, P.S. (1998). Aggregation behaviour of the grey reef shark Carcharhinus amblyrhynchos, at the Johnston Atoll, Central Pacific Ocean. Env. Biol. Fish 51:129-139. 7Northcutt, R.G. (1977) Elasmobranch central nervous system organization and its possible evolutionary significance. Am. Zool. 17, 411-29 8Klimley, A. P. (1985). Schooling in Sphyrna lewini, a species with Low Risk of Predation: a Non-egalitarian State. Zoological Tierpsychology 70:297-319. 9Myrberg, A. A. and Gruber, S. H. (1974). The behaviour of the bonnethead shark, Sphyrna tiburo. Copeia 1974 (2):358-373. 10Clark, E. (1959). Instrumental conditioning of lemon sharks. Sci. New Series 130, 3369, 217-218.
11Heupel, M.R. & Simpfendorfer, C.A. (2005). Quantitative analysis of aggregation behaviour in juvenile blacktip sharks. Mar. Biol. 147: 1239-1249. 12Sims, D. W., Nash J. P. & Morritt, D. (2001). Movements and activity of male and female dogfish in a tidal sea lough: alternative behavioural strategies and apparent sexual segregation. Mar. Bio. 139, 1165-1175. 13Krause, J., Butlin, R.K., Peuhkuri, N and Pritchard, V.L. (2000). The social organization of fish shoals: a test of the predictive power of laboratory experiments for the field. Biol. Rev 75, 477-501. 14Morrissey, J. F. and Gruber, S. H. (1993). Habitat selection of juvenile lemon sharks, Negaprion brevirostris. Env. Biol. Fish 60:131-156. 15Gruber, S.H., D.R. Nelson & J.F. Morrissey. (1988). Patterns of activity and space utilization of lemon sharks, Negaprion brevirostris, in a shallow Bahamian lagoon. Bull. Mar. Sci. 43:61-76. 16Gruber, S.H. (1982). Role of the lemon shark, Negaprion brevirostris (Poey), as a predator in the tropical marine environment: a multidisciplinary study. Fla. Sci. 45: 46-75. 17Gruber, S. H., De Marignac, J. R. C., and Hoenig, J. M. (2001). Survival of juvenile lemon sharks at Bimini, Bahamas, estimated by mark-depletion experiments. Trans. Am. Fish. Soc. 130:376-384. 18Baum, J.K., Myers, R.A., Kehler, D.G., Worm, B., Harley, S.J., Doherty, P.A. 2003. Collapse and conservation of shark populations in the Northwest Atlantic. Science 299(5605):389-392.