The diving behaviour of green turtles undertaking oceanic migration to and from Ascension Island: dive durations, dive profiles and depth distribution
1 School of Biological Sciences, University of Wales Swansea, Singleton Park, Swansea SA2 8PP, UK,
2 Department of Animal Ecology, Lund University, Ecology Building, SE-223 62 Lund, Sweden,
3 Dipartimento di Etologia, Ecologia, Evoluzione, University of Pisa, Via A. Volta 6, I-56126 Pisa, Italy and
4 The Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Lowestoft NR33 0HT, UK
*e-mail: g.hays{at}swan.ac.uk
Accepted September 11, 2001
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: satellite telemetry, turtle, Chelonia mydas, diving, migration.
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
While all these approaches have produced major advances in our knowledge, they all provide only integrated measures of processes occurring during migration and do not reveal any intricacies of temporal patterns within migration. Establishing how the behaviour and physiology of animals change within a long-distance migration is logistically challenging but has now started to be addressed through the advent of reliable telemetry and logging equipment. First, for example, satellite tracking using the Argos system has allowed the routes of long-distance migrants to be reconstructed in hitherto unimagined detail and has revealed that animals may follow very straight-line courses for hundreds of kilometres, presumably through the use of reliable biological compasses (Cochran, 1987; Gudmundsson et al., 1995
; Papi and Luschi, 1996
; Kjellén et al., 1997
). Second, some physical data (e.g. pressure, temperature, speed) can be relayed via satellite transmitters, allowing insights into the physiological ecology of animals in remote locations (Weimerskirsh et al., 1994
; Hays et al., 1999
; Hindell et al., 1999
; Pennycuick et al., 1999
). However, the limited available bandwidth of the Argos system severely constrains the amount of data that can be transmitted so that, for example, complete dive profiles cannot generally be obtained for marine animals. This constraint of the Argos system has led to the use of artificial displacements of animals carrying data loggers, rather than transmitters, so that their behaviour can be recorded in even more detail as they travel (Webb et al., 1998
).
A paradigmatic group of long-distance migrants are marine turtles, with both conventional mark/recapture and satellite tracking showing that several populations and species may move thousands of kilometres between breeding grounds and feeding areas. For example, the green turtles (Chelonia mydas) that nest at Ascension Island in the middle of the Atlantic migrate at the end of the nesting season to feeding grounds along the South American coast, over 2200 km distant (Luschi et al., 1998). These turtles are thought not to feed either during their oceanic crossings or while at Ascension Island (Mortimer and Carr, 1987
) and, hence, it might be hypothesised that during migration their behavioural repertoire would be very narrow, with individuals simply swimming continuously to attain their destination with the minimal energy consumption. However, limited dive information from five individuals has recently suggested that the behaviour during migration for this population is not invariant (Hays et al., 1999
). Here we use (i) information obtained from satellite transmitters and (ii) results from the first displacement experiments in which turtles have been allowed to migrate back to a starting point while carrying time/depth recorders to reveal the details of their diving behaviour while they are travelling across the ocean.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Time/depth recorder (TDR) studies
Beach patrols located turtles nesting early in the season at Ascension Island between December 1999 and February 2000. Once they had laid their clutch, turtles were placed into large, padded wooden crates before being transported by truck to the nearby Georgetown pierhead (<1 km). Then, using a forklift truck, cranes and barges, they were loaded onto the merchant ship MV Ascension and displaced between 60 and 270 km away from the island prior to release. Animals were kept shaded and moist at all times. Prior to deployment, a TDR (LTD_100, LOTEK Marine Technologies, St Johns, Newfoundland, Canada) was attached to the carapace using quick-setting epoxy resin. The TDR recorded the depth at 12 s intervals to a resolution of 4 cm.
To relocate the turtles, nesting beaches on Ascension Island were monitored. This was logistically challenging because of the very high numbers nesting on the island and involved over 20 island residents spending more than 200 man-nights patrolling beaches. When instrumented females were found, the TDR was removed and the dive data offloaded. In total, nine turtles were instrumented with TDRs, of which seven were re-sighted during subsequent nesting. Of these, the TDR was cracked and filled with sea water in two cases, while in five cases intact undamaged TDRs were recovered and all the depth data successfully offloaded. Dive data were analysed using bespoke software (MultiTrace, Jensen Software Systems, Laboe, Germany). To extract the dive variables for each long-duration dive (>5 min), dives were defined as starting when the rate of descent was greater than 0.3 m s1 and ending when both the rate of ascent was more than 0.3 m s1 and the depth was less than 10 % of the maximum for that dive. The time when turtles returned to Ascension Island was readily apparent in each dive record with the commencement of flat-bottomed U-shaped dives indicative of individuals remaining on the sea bed (Hays et al., 2000).
The height of nesting females was measured with a ruler (to the highest point on the carapace) when they were on compact level sand.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
|
|
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Although the diving behaviour of a number of air-breathing vertebrates has been documented, many species also survey the water column (for example, for food) while they are travelling, so that their dives are to tens or hundreds of metres. However, there is little or no food available for herbivorous green turtles (Chelonia mydas) while they are swimming across the ocean to their nesting beaches, and we would therefore expect that minimisation of their cost of transport, rather than foraging, would be the key factor driving their swimming depth. In this regard, the optimum strategy is not to swim at the surface, where surface drag is high, but instead to swim below the surface where drag is reduced (Hertel, 1966). Specifically, drag is minimised once the depth is approximately 2.53 times an animals body thickness. Our finding that migrating turtles spent much of their time at a depth of approximately 0.91.5 m is consistent with this prediction that they are swimming at the shallowest depth that minimises their cost of transport.
The two typical deep dive profiles that were identified have been recorded both for marine turtles during their internesting period in coastal waters and for sea snakes (Graham et al., 1975, 1987
; Minamikawa et al., 1997
, 2000
; Rubinoff et al., 1986
). During the gradual ascent phase, it is known (from the use of activity sensors) that individuals may remain almost motionless hanging in midwater, and these distinctive dive types are believed to minimise the energy expenditure of submerged animals, i.e. these may be midwater resting dives of some aquatic reptiles. In other cases individuals may swim during the gradual ascent phase (Graham et al., 1987
). The gradual ascent phase of these midwater dives has been attributed to a gradual loss of buoyancy as a result of removal of O2 from the lungs without a corresponding replacement of CO2 and, as such, individuals ascend very gradually to maintain neutral buoyancy.
The relatively deep excursions at the start of type 2 dives are enigmatic, although one suggestion is that these excursions represent the exploration of the water column (Graham et al., 1975, 1987
). This conclusion that turtles undertaking oceanic migration may dive relatively deeply is as exciting as it is unexpected. Many years ago, Archie Carr, the pioneer of sea turtle research, speculated that migrating turtles might rest during migration but logically reasoned that, being air-breathers, they might rest at the surface, where they would have continuous access to air (Carr, 1967
). Our results show that this is not the case and, in fact, that turtles spend very little time at the surface.
What are the ultimate and proximate reasons for turtles diving deeply during their trans-oceanic crossing? In some birds, there may be breaks during migration during which individuals feed and/or wait for favourable winds before continuing their journey (Weber et al., 1998; Åkesson and Hedenström, 2000
). However, neither of these conditions is likely to apply to green turtles since (i) being herbivorous, they are thought not to feed during migration and (ii) there is unlikely to be a short-term temporal change in the currents that help carry the turtles back to Brazil (Luschi et al., 1998
). The predominantly nocturnal pattern of deep diving that we observed has also been found during the inter-nesting period at Ascension Island (Hays et al., 2000
) and for other species of marine turtle while individuals are at their feeding grounds (van Dam and Diez, 1996
) and may be linked to why migrating turtles travel faster during the day than at night (Luschi et al., 1996
, 1998
). It might be that, as has been suggested for some migrating birds (Gudmundsson et al., 1995
), there is a physiological reason limiting the ability of turtles to maintain their optimum speed of travel throughout migration and so they must periodically rest, with these rest periods occurring at night because of an innate diurnal activity cycle in this group.
Deep diving clearly necessitates periods of ascent to the surface to breathe followed by descent, and so these vertical movements must come with some associated energetic cost. There is, therefore, presumably some counterbalancing advantage to deep diving. Although there are few predators of adult marine turtles, it is known that they may be attacked by large sharks (Stancyk, 1995; Fergusson et al., 2000
), and adults at Ascension Island are seen missing parts of flippers, presumably as a result of predatory attacks. By diving below the surface, turtles will reduce the extent to which they are silhouetted against the surface and, hence, their risk of being observed by foraging sharks. Indeed, the dorso-ventral countershading of green turtles (darker above, light below) is also presumably an evolutionary response to predatory risk. An analogous use of a sub-surface refuge to reduce the risk of predation has also been proposed for elephant seals (Mirounga angustirostris) when digesting and assimilating food (Le Boeuf et al., 1982
; Crocker et al., 1997
), suggesting that the surface may, in general, be a risky place for air-breathing marine animals.
However, while seals may rest a few hundred metres below the surface, the typical deep dive for green turtles was between approximately 13 and 21 m. This range for the mean depth of type 1 and 2 dives corresponds approximately to the depths at which green turtles rest on the sea bed during the internesting period at Ascension Island (Hays et al., 2000), i.e. the depth of pelagic/midwater and neritic/benthic dives is similar. This depth selection may be driven by the ability of turtles to achieve neutral buoyancy. We have argued that approximately 20 m is the maximum depth at which Ascension Island green turtles can attain neutral buoyancy after diving with fully inflated lungs (Hays et al., 2000
); i.e. if turtles were to dive any deeper, they would be negatively buoyant and would therefore (i) sink further during the dive if not resting on the sea bed and (ii) need to expend energy overcoming negative buoyancy to return to the surface. Therefore, green turtles presumably do not routinely dive any deeper as this would increase the energetic costs of descent and ascent.
In summary, we have shown, for the first time, the dive profiles and depth distribution of turtles undertaking oceanic migration and have identified a dichotomy between short, near-surface dives, which probably reflect travelling, and deeper, longer-dives.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Able, K. P. (1980). Mechanisms of orientation, navigation and homing. In Animal Migration, Orientation and Navigation (ed. S. Gauthreaux), pp. 283373. New York: Academic Press.
Åkesson, S. and Hedenström, A. (2000). Wind selectivity of migratory flight departures in birds. Behav. Ecol. Sociobiol. 47, 140144.
Åkesson, S., Karlsson, L., Pettersson, J. and Walinder, G. (1992). Body composition and migration strategies: a comparison between robins (Erithacus rubecula) from two stop-over sites in Sweden. Vogolwarte 36, 188195.
Alerstam, T. (1996). The geographic scale factor in orientation of migrating birds. J. Exp. Biol. 199, 919.
Carr, A. (1967). The Turtle: a Natural History. London: Cassell. 248pp.
Cochran, W. W. (1987). Orientation and other migratory behaviours of a Swainsons thrush followed for 1500 km. Anim. Behav. 35, 927929.
Crocker, D. E., Le Boeuf, B. J. and Costa, D. P. (1997). Drift diving in female northern elephant seals: implications for food processing. Can. J. Zool. 75, 2739.
Eckert, S. A., Eckert, K. L., Ponganis, P. and Kooyman, G. L. (1989). Diving and foraging behaviour of leatherback sea turtles (Dermochelys coriacea). Can. J. Zool. 67, 28342840.
Eckert, S. A., Nellis, D. W., Eckert, K. L. and Kooyman, G. L. (1986). Diving patterns of two leatherback turtles (Dermochelys coriacea) during internesting intervals at Sandy Point, St. Croix, U.S. Virgin Islands. Herpetologica 42, 381388.
Emlen, S. T. (1975). Migration: orientation and navigation. In Avian Biology, vol. 5 (ed. D. S. Farner and J. R. King), pp. 129219. New York: Academic Press.
Fergusson, I. K., Compagno, L. J. V. and Marks, M. A. (2000). Predation by white sharks Carcharodon carcharias (Chondrichthyes: Lamnidae) upon chelonians, with new records from the Mediterranean Sea and a first record of the ocean sunfish Mola mola (Osteichthyes: Molidae) as stomach contents. Env. Biol. Fish. 58, 447453.
Graham, J. B., Gee, J. H., Motta, J. and Rubinoff, I. (1987). Subsurface buoyancy regulation by the sea snake Pelamis platurus. Physiol. Zool. 60, 252261.
Graham, J. B., Gee, J. H. and Robison, F. (1975). Hydrostatic and gas exchange functions of the lung of the sea snake Pelamis platurus. Comp. Biochem. Physiol. 50A, 447482.
Gudmundsson, G. A., Alerstam, T., Benvenuti, S., Papi, F., Lilliendahl, K. and Åkesson, S. (1995). Examining the limits of flight and orientation performance: satellite tracking of brent geese migrating across the Greenland ice-cap. Proc. R. Soc. Lond. B 261, 7379.
Hays, G. C., Adams, C. R., Broderick, A. C., Godley, B. J., Lucas, D. J., Metcalfe, J. D. and Prior, A. A. (2000). The diving behaviour of green turtles at Ascension island. Anim. Behav. 59, 577586.[Medline]
Hays, G. C., Luschi, P., Papi, F., Del Seppia, C. and Marsh, R. (1999). Changes in behaviour during the internesting period and postnesting migration for Ascension Island green turtles. Mar. Ecol. Prog. Ser. 189, 263273.
Hertel, H. (1966). Structure, Form, Movement. New York: Reinhold.
Hindell, M. A., McConnell, B. J., Fedak, M. A., Slip, D. J., Burton, H. R., Reijnders, P. J. H. and McMahon, C. R. (1999). Environmental and physiological determinants of successful foraging by naive southern elephant seal pups during their first trip to sea. Can. J. Zool. 77, 18071821.
Kjellén, N., Hake, M. and Alerstam, T. (1997). Strategies of two Ospreys Pandion haliaetus migrating between Sweden and tropical Africa as revealed by satellite tracking. J. Avian Biol. 28, 1523.
Le Boeuf, B. J., Riedman, M. and Keyes, R. S. (1982). White shark predation on pinnipeds in California coastal waters. Fish. Bull. 80, 891895.
Luschi, P., Hays, G. C., Del Seppia, C., Marsh, R. and Papi, F. (1998). The navigational feats of green sea turtles migrating from Ascension Island investigated by satellite telemetry. Proc. R. Soc. Lond. B 265, 22792284.[Medline]
Luschi, P., Papi, F., Liew, H. C., Chan, E. H. and Bonadonna, F. (1996). Long-distance migration and homing after displacement in the green turtle (Chelonia mydas): A satellite tracking study. J. Comp. Physiol. A 178, 447452.
Minamikawa, S., Naito, Y., Sato, K., Matsuzawa, Y., Bando, T. and Sakamoto, W. (2000). Maintenance of neutral buoyancy by depth selection in the loggerhead turtle Caretta caretta. J. Exp. Biol. 203, 29672975.
Minamikawa, S., Naito, Y. and Uchida, I. (1997). Buoyancy control and diving behaviour of the loggerhead turtle, Caretta caretta. J. Ethol. 15, 109118.
Mortimer, J. A. and Carr, A. (1987). Reproduction and migrations of the Ascension island green turtles (Chelonia mydas). Copeia 1987, 103113.
Papi, F. and Luschi, P. (1996). Pinpointing Isla Meta: the case of sea turtles and albatrosses. J. Exp. Biol. 199, 6571.
Pennycuick, C. J., Bradbury, T. A. M., Einarsson, Ó. and Owen, M. (1999). Response to weather and light conditions of migrating Whooper Swans Cygnus cygnus and flying height profiles, observed with the Argos satellite system. Ibis 141, 434443.
Perdeck, A. C. (1958). Two types of orientation in migrating starlings, Sturnus vulgaris L. and chaffinches, Fringilla coelebs L., as revealed by displacement experiments. Ardea 46, 137.
Piersma, T. and Lindström, Å. (1997). Rapid reversible changes in organ size as a component of adaptive behaviour. Trends Ecol. Evol. 12, 134138.
Piersma, T., Gudmundsson, G. A. and Lilliendahl, K. (1999). Rapid changes in size of different functional organ and muscle groups in a long-distance migrating shorebird. Physiol. Biochem. Zool. 72, 405415.[Medline]
Rubinoff, I., Graham, J. B. and Motta, J. (1986). Diving of the sea snake Pelamis platurus in the Gulf of Panama. II. Horizontal movement patterns. Mar. Biol. 91, 181191.
Stancyk, S. E. (1995). Non-human predators of sea turtles and their control. In Biology and Conservation of Sea Turtles (ed. K. A. Bjorndal), pp. 139152. Washington: Smithsonian Institution Press.
van Dam, R. P. and Diez, C. E. (1996). Diving behavior of immature hawksbills (Eretmochelys imbricata) in a Caribbean cliff-wall habitat. Mar. Biol. 127, 171178.
Webb, P. W., Crocker, D. E., Blackwell, S. B., Costa, D. P. and Le Boeuf, B. J. (1998). Effects of buoyancy on the diving behaviour of northern elephant seals. J. Exp. Biol. 201, 23492358.
Weber, T. P., Alerstam, T. and Hedenström, A. (1998). Stopover decisions under wind influence. J. Avian Biol. 29, 552560.
Wehner, R. (1998). Navigation in context: grand theories and basic mechanisms. J. Avian Biol. 29, 370386.
Weimerskirch, H., Doncaster, C. P. and Cuenot-Chaillet, F. (1994). Pelagic seabirds and the marine environment: foraging patterns of wandering albatrosses in relation to prey availability and distribution. Proc. R. Soc. Lond. B 255, 9197.
Wiltschko, W. and Wiltschko, R. (1991). Magnetic orientation and celestial cues in migratory orientation. In Orientation in Birds (ed. P. Berthold), pp. 1637. Basel: Birkhäuser Verlag.