Environmental context explains Lévy and Brownian movement patterns of marine predators

An optimal search theory, the so-called Levy-flight foraging hypothesis(1), predicts that predators should adopt search strategies known as Levy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey(2-4). Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Levy behaviour has recently been questioned(5,6). Consequently, whether foragers exhibit Levy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory's central predictions. Here we use maximum-likelihood methods to test for Levy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Levy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Levy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Levy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Levy-flight foraging hypothesis(1,7), supporting the contention(8,9) that organism search strategies naturally evolved in such a way that they exploit optimal Levy patterns.

Foraging success of biological Levy flights recorded in situ

It is an open question how animals find food in dynamic natural environments where they possess little or no knowledge of where resources are located. Foraging theory predicts that in environments with sparsely distributed target resources, where forager knowledge about resources’ locations is incomplete, Lévy flight movements optimize the success of random searches. However, the putative success of Lévy foraging has been demonstrated only in model simulations. Here, we use high-temporal-resolution Global Positioning System (GPS) tracking of wandering (Diomedea exulans) and black-browed albatrosses (Thalassarche melanophrys) with simultaneous recording of prey captures, to show that both species exhibit Lévy and Brownian movement patterns. We find that total prey masses captured by wandering albatrosses during Lévy movements exceed daily energy requirements by nearly fourfold, and approached yields by Brownian movements in other habitats. These results, together with our reanalysis of previously published albatross data, overturn the notion that albatrosses do not exhibit Lévy patterns during foraging, and demonstrate that Lévy flights of predators in dynamic natural environments present a beneficial alternative strategy to simple, spatially intensive behaviors. Our findings add support to the possibility that biological Lévy flight may have naturally evolved as a search strategy in response to sparse resources and scant information.

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 (16754km 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.

Seasonal movements and behaviour of basking sharks from archival tagging: No evidence of winter hibernation

Habitat selection processes in highly migratory animals such as sharks and whales are important to understand because they influence patterns of distribution, availability and therefore catch rates. However, spatial strategies remain poorly understood over seasonal scales in most species, including, most notably, the plankton-feeding basking shark Cetorhinus maximus. It was proposed nearly 50 yr ago that this globally distributed species migrates from coastal summer-feeding areas of the northeast Atlantic to hibernate during winter in deep water on the bottom of continental-shelf slopes. This view has perpetuated in the literature even though the 'hibernation theory' has not been tested directly. We have now tracked basking sharks for the first time over seasonal scales (1.7 to 6.5 mo) using 'pop-up' satellite archival transmitters. We show that they do not hibernate during winter but instead undertake extensive horizontal (up to 3400 km) and vertical (> 750 m depth) movements to utilise productive continental-shelf and shelf-edge habitats during summer, autumn and winter. They travel long distances (390 to 460 km) to locate temporally discrete productivity 'hotspots' at shelf-break fronts, but at no time were prolonged movements into open-ocean regions away from shelf waters observed. Basking sharks have a very broad vertical diving range and can dive beyond the known range of planktivorous whales. Our study suggests this species can exploit shelf and slope-associated zooplankton communities in mesopelagic (200 to 1000 m) as well as epipelagic habitat (0 to 200 m).