Julian D. Metcalfe

Scaling laws of marine predator search behaviour

Many free-ranging predators have to make foraging decisions with little, if any, knowledge of present resource distribution and availability. The optimal search strategy they should use to maximize encounter rates with prey in heterogeneous natural environments remains a largely unresolved issue in ecology. Lévy walks are specialized random walks giving rise to fractal movement trajectories that may represent an optimal solution for searching complex landscapes. However, the adaptive significance of this putative strategy in response to natural prey distributions remains untested. Here we analyse over a million movement displacements recorded from animal-attached electronic tags to show that diverse marine predators—sharks, bony fishes, sea turtles and penguins—exhibit Lévy-walk-like behaviour close to a theoretical optimum. Prey density distributions also display Lévy-like fractal patterns, suggesting response movements by predators to prey distributions. Simulations show that predators have higher encounter rates when adopting Lévy-type foraging in natural-like prey fields compared with purely random landscapes. This is consistent with the hypothesis that observed search patterns are adapted to observed statistical patterns of the landscape. This may explain why Lévy-like behaviour seems to be widespread among diverse organisms, from microbes to humans, as a ‘rule’ that evolved in response to patchy resource distributions.

Tracking fish with electronic tags

The distributions of many species of fish show pronounced seasonal changes as a result of migration. We are using long-term electronic tagging to study the migratory behaviour of fish in the North Sea. Using simple measurements of depth and temperature, we have found that we can reconstruct the tracks of plaice (Pleuronectes platessa) migrating between the southern North Sea and their spawning areas in the eastern English Channel or northeast coast of England. In this way we show that fish can visit more than one spawning area within a single spawning season and that rates of movement are often ten times faster than those deduced from conventional mark-recapture experiments.

FLEXIBLE FORAGING MOVEMENTS OF LEATHERBACK TURTLES ACROSS THE NORTH ATLANTIC OCEAN

Some marine species have been shown to target foraging at particular hotspots of high prey abundance. However, we show here that in the year after a nesting season, female leatherback turtles (Dermochelys coriacea) in the Atlantic generally spend relatively little time in fixed hotspots, especially those with a surface signature revealed in satellite imagery, but rather tend to have a pattern of near continuous traveling. Associated with this traveling, distinct changes in dive behavior indicate that turtles constantly fine tune their foraging behavior and diel activity patterns in association with local conditions. Switches between nocturnal vs. diurnal activity are rare in the animal kingdom but may be essential for survival on a diet of gelatinous zooplankton where patches of high prey availability are rare. These results indicate that in their first year after nesting, leatherback turtles do not fit the general model of migration where responses to resources are suppressed during transit. However, their behavior may be different in their sabbatical years away from nesting beaches. Our results highlight the importance of whole-ocean fishing gear regulations to minimize turtle bycatch.

Migration route and spawning area fidelity by North Sea plaice

Data from plaice, Pleuronectes platessa L., tagged with electronic data storage tags, were used to test whether these fishes exhibited migration route and spawning area fidelity in successive spawning seasons. Depth and temperature data were recorded for each fish over 365–512 days in the central North Sea and this information was used to reconstruct movements based on tidal locations. We discovered highly directed seasonal migrations from the winter spawning area south of a major topographical feature, Dogger Bank Tail End, to summer feeding grounds 250 km to the north in deep, cold, thermally stratified water. Our results show synchronous timing of migration, repeated pre– and post–spawning migration routes and 100% spawning area fidelity, including two individuals that returned to within 20 km of their previous seasons spawning location. This is the first study to provide a complete reconstruction of annual migrations by individual fishes, showing strong homing behaviour along consistent migration routes.

Encounter success of free-ranging marine predator movements across a dynamic prey landscape

Movements of wide-ranging top predators can now be studied effectively using satellite and archival telemetry. However, the motivations underlying movements remain difficult to determine because trajectories are seldom related to key biological gradients, such as changing prey distributions. Here, we use a dynamic prey landscape of zooplankton biomass in the north-east Atlantic Ocean to examine active habitat selection in the plankton-feeding basking shark Cetorhinus maximus. The relative success of shark searches across this landscape was examined by comparing prey biomass encountered by sharks with encounters by random-walk simulations of ‘model’ sharks. Movements of transmitter-tagged sharks monitored for 964 days (16 754 km estimated minimum distance) were concentrated on the European continental shelf in areas characterized by high seasonal productivity and complex prey distributions. We show movements by adult and sub-adult sharks yielded consistently higher prey encounter rates than 90% of random-walk simulations. Behavioural patterns were consistent with basking sharks using search tactics structured across multiple scales to exploit the richest prey areas available in preferred habitats. Simple behavioural rules based on learned responses to previously encountered prey distributions may explain the high performances. This study highlights how dynamic prey landscapes enable active habitat selection in large predators to be investigated from a trophic perspective, an approach that may inform conservation by identifying critical habitat of vulnerable species.

The diving behaviour of green turtles at Ascension Island

For six green turtles, Chelonia mydas, that had nested on Ascension Island in the South Atlantic, we used time-depth recorders to examine their diving behaviour during the subsequent internesting interval (10-12 days). All the turtles performed dives where they remained at a fixed depth for a long period, surfaced briefly and then dived to the same depth again. It is generally believed these dive profiles are caused by the turtles resting on the sea bed. The maximum depth that turtles routinely reached on these resting dives was between 18 and 20 m, with resting dives deeper than 20 m being extremely rare. Resting dive duration increased significantly with deeper dives. From this relationship, and assuming that turtles with fully inflated lungs at the surface need to dive to 19 m to achieve negative buoyancy, we estimated for two turtles that the oxygen consumption during resting dives was 0.016 and 0.020 litres O(2)/kg per h, respectively. This is similar to the value predicted from the allometric scaling relationship for the minimal oxygen consumption of turtles. We calculated that the energy conserved by resting during the internesting period may appreciably increase the reproductive output of females. Copyright 2000 The Association for the Study of Animal Behaviour.

THE IMPLICATIONS OF LUNG-REGULATED BUOYANCY CONTROL FOR DIVE DEPTH AND DURATION

Among air-breathing divers, control of buoyancy through lung volume regulation may be most highly developed in marine turtles. In short, the turtle lung may serve a dual role as both an oxygen store and in buoyancy control. A simple model is developed to show that, for turtles diving up to the maximum depth at which they can still use their lungs to attain neutral buoyancy, the total oxygen store will increase greatly with dive depth, and hence a corresponding increase in dive duration is predicted. Time–depth recorders attached to free-living green turtles (Chelonia mydas) at Ascension Island confirmed a marked increase in dive duration with depth, with the gradient of this relationship being >10 times that seen in diving birds and mammals. Consistent with the prediction that the lungs serve a dual role, we found that, when lead weights were added to some turtles to increase their specific gravity, the mean depth of dives decreased, but for dives to the same depth, weighted animals dived for longer. The depth distribution of green turtles seems to be generally constrained by the maximum depth at which they can still attain close to neutral buoyancy.

Water temperature and internesting intervals for loggerhead (Caretta caretta) and green (Chelonia mydas) sea turtles

Temperature loggers were attached to the carapace of green turtles (Chelonia mydas) at Ascension Island and Cyprus and to loggerhead turtles (Caretta caretta) at Cyprus, in order to record the ambient temperature experienced by individuals during the internesting interval, i.e. the period between consecutive clutches being laid. Internesting intervals were relatively short (10–14 days) and mean ambient temperatures relatively warm (27–281C), compared to previous observations for these species nesting in Japan, although a single internesting interval versus temperature relationship described all the data for these two species from the different areas. The implication is that water temperature has both a common and a profound effect on the length of the internesting interval for these two species: internesting intervals are shorter when the water is warmer. r 2002 Elsevier Science Ltd. All rights reserved.

Fisheries: Different behaviour of North and Irish Sea cod

Cod (Gadus morhua) are bottom-living, predatory fish of considerable commercial importance, but surprisingly little is known of what cod do for most of their time because it is difficult and costly to study the behaviour of fish at sea. Here we use electronic data-storage tags to investigate the behaviour of cod in the North Sea and in the Irish Sea and find that there are marked differences in the activity of fish in the two regions. This difference could be explained by dissimilar foraging ecology and may have implications for the future management of severely depleted cod stocks.

Migratory behaviour of the thornback ray, Raja clavata, in the southern North Sea

Although depleted throughout the European continental shelf, the relatively high density of thornback rays Raja clavata, in the Thames Estuary (UK) makes it an important stock centre and potential focus for species management. To describe spatial and temporal distribution, 197 thornback rays were tagged with electronic data storage tags (DSTs) and released in theThames Estuary in October 1999 and 2000, and 100 rays tagged with conventional tags in 2000. Fifty-one per cent of DSTs and 48% of conventional tags were returned. Fishery-independent estimates of position (‘geolocations’) between the time of release and recapture using the tidal location method were possible using 75 individual data records of between 31 and 423 days. Ninety-six per cent of rays were recaptured within the Thames Estuary. The rays were located in water of 20^35 m depth during the autumn and winter, then migrated into shallower water (520 m depth) during the spring. Fishery-independent analysis of distribution demonstrated that the rays were more widely distributed in the southern North Sea during the autumn and winter. The range contracted in spring, when the ¢sh moved into the inner Thames Estuary. No gross behaviour diierences were observed between males and females. Displacement and dispersion coe⁄cients calculated from geolocation data demonstrated clear annual cycles, indicative of migration. These movements were not apparent from the mark ^ recapture data, a ¢shery-related eiect. The extent of migration as determined from experiments with DSTs was approximately three times greater than that suggested by conventional tagging data alone.