Emily J. Southall

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.

Environmental context explains Lévy and Brownian movement patterns of marine predators.

An optimal search theory, the so-called Lévy-flight foraging hypothesis, predicts that predators should adopt search strategies known as Lévy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey. Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Lévy behaviour has recently been questioned. Consequently, whether foragers exhibit Lévy 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 Lévy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Lévy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Lévy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Lévy 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 Lévy-flight foraging hypothesis, supporting the contention that organism search strategies naturally evolved in such a way that they exploit optimal Lévy patterns.

Foraging success of biological Lévy 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 (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.

Annual social behaviour of basking sharks associated with coastal front areas

Comparatively little is known about reproductive behaviour in wild sharks as it has proved extremely difficult to study, especially in large pelagic sharks. Here we describe annual courtship–like behaviour in the second–largest fish species, the basking shark (Cetorhinus maximus), from 25 separate episodes observed and tracked during a five–year study period (1995–999) off south–west England. Social behaviours observed between paired, or three or four, sharks were consistent with courtship behaviours seen in other shark species, namely nose–to–tail following, close following, close flank approach, parallel and echelon swimming. Mature individuals between 5 and 8 m total body length ( L;T;) exhibited these behaviours whereas smaller sharks (3–4 m L;T;) did not. Lead individuals were identified as female on a number of occasions and interactions were prolonged; the longest continuous observation of socializing was 1.8 h, although intermittent track data indicates bouts may last for up to 5–6 h. Locations of courtship–like behaviour events were not distributed randomly and were significantly associated with thermal fronts. Our results indicate that putative courtship behaviour occurs between May and July along oceanographic fronts, probably as a consequence of individuals aggregating to forage in rich prey patches before initiating courtship. Thus, locating the richest prey patches along fronts may be important for basking sharks to find mates as well as food in the pelagic ecosystem. As courtship–like behaviours occur annually off south–west England we speculate that this region may represent an annual breeding area for this protected species, but mating itself probably takes place at depth as it was not seen at the surface.

Hierarchical random walks in trace fossils and the origin of optimal search behavior

Significance How best to search for food in heterogeneous landscapes is a universal problem facing mobile organisms. Diverse modern animals use a random search strategy called a Lévy walk, composed of many small move steps interspersed by rare long steps, which theoretically is optimal for locating sparse resources. Here, we find the first evidence, to our knowledge, that extinct animals, in this case 50 My-old sea urchins, used a Lévy-like search strategy. Our results are important because they indicate Lévy walks likely have an ancient origin and may arise from simple behaviors observed in much older fossil trails. This foraging strategy may have adapted in response to decreased food availability after productivity collapse associated with past climate change and mass extinctions. Efficient searching is crucial for timely location of food and other resources. Recent studies show that diverse living animals use a theoretically optimal scale-free random search for sparse resources known as a Lévy walk, but little is known of the origins and evolution of foraging behavior and the search strategies of extinct organisms. Here, using simulations of self-avoiding trace fossil trails, we show that randomly introduced strophotaxis (U-turns)—initiated by obstructions such as self-trail avoidance or innate cueing—leads to random looping patterns with clustering across increasing scales that is consistent with the presence of Lévy walks. This predicts that optimal Lévy searches may emerge from simple behaviors observed in fossil trails. We then analyzed fossilized trails of benthic marine organisms by using a novel path analysis technique and find the first evidence, to our knowledge, of Lévy-like search strategies in extinct animals. Our results show that simple search behaviors of extinct animals in heterogeneous environments give rise to hierarchically nested Brownian walk clusters that converge to optimal Lévy patterns. Primary productivity collapse and large-scale food scarcity characterizing mass extinctions evident in the fossil record may have triggered adaptation of optimal Lévy-like searches. The findings suggest that Lévy-like behavior has been used by foragers since at least the Eocene but may have a more ancient origin, which might explain recent widespread observations of such patterns among modern taxa.

Spatial distribution patterns of basking sharks on the European shelf: preliminary comparison of satellite-tag geolocation, survey and public sightings data

Current concerns about the population levels of the basking shark (Cetorhinus maximus) in the north-east Atlantic have prompted a need to understand population distribution, habitat preference and centres of abundance. In this study, spatial distribution maps derived from satellite-tag geolocations, boat surveys and public sightings data were compared. The broad distribution patterns revealed by these diierent methods are similar, but there are considerable diierences in density distributions. Surface sightings data show high densities, or ‘hotspots’ in the Hebridean Sea, Clyde Sea, Irish Sea and close inshore around Devon and Cornwall. Tag geolocations, in contrast, identi¢ed two areas where individuals spent considerable time outside the distributions indicated by surveys and public sightings: the Celtic Sea and Western Approaches of the English Channel. The reason for this disparity and its implications for population estimates for the species are discussed.

Scaling laws of ambush predator 'waiting' behaviour are tuned to a common ecology.

The decisions animals make about how long to wait between activities can determine the success of diverse behaviours such as foraging, group formation or risk avoidance. Remarkably, for diverse animal species, including humans, spontaneous patterns of waiting times show random ‘burstiness’ that appears scale-invariant across a broad set of scales. However, a general theory linking this phenomenon across the animal kingdom currently lacks an ecological basis. Here, we demonstrate from tracking the activities of 15 sympatric predator species (cephalopods, sharks, skates and teleosts) under natural and controlled conditions that bursty waiting times are an intrinsic spontaneous behaviour well approximated by heavy-tailed (power-law) models over data ranges up to four orders of magnitude. Scaling exponents quantifying ratios of frequent short to rare very long waits are species-specific, being determined by traits such as foraging mode (active versus ambush predation), body size and prey preference. A stochastic–deterministic decision model reproduced the empirical waiting time scaling and species-specific exponents, indicating that apparently complex scaling can emerge from simple decisions. Results indicate temporal power-law scaling is a behavioural ‘rule of thumb’ that is tuned to species’ ecological traits, implying a common pattern may have naturally evolved that optimizes move–wait decisions in less predictable natural environments.

Rapid voluntary stomach eversion in a free-living shark

video observation of oral gastric eversion in a free-living caribbean reef shark ( carcharhinus perezi ) shows voluntary gastric eversion followed by retraction not only occurs, but is extremely rapid (lasting ∼0.3 s). eversion may occur by stomach relaxation–oesophageal contraction coupled with increased abdominal pressures to enable prolapse, and retraction by a mechanism analogous to suction feeding. this behaviour provides a ‘cleansing’ function for removing indigestible food particles, parasites or mucus from the stomach lining. sharks, and possibly other animals with similar gut morphologies, may use this technique to help maintain a healthy alimentary tract.

Year‐round sexual harassment as a behavioral mediator of vertebrate population dynamics

Within-species sexual segregation is a widespread phenomenon among vertebrates, but its causes remain a topic of much debate. Female avoidance of male coercive mating attempts has the potential to influence the social structure of animal populations, yet it has been largely overlooked as a driver of sexual separation. Indeed, its potential role in long-term structuring of natural populations has not been studied. Here we use a comparative approach to examine the suitability of multiple hypotheses forwarded to account for sexual segregation (i.e., activity budget, predation risk, thermal niche–fecundity, and social factors) as drivers underlying sex-specific habitat use in a monomorphic model vertebrate, the small-spotted catshark, Scyliorhinus canicula. Using this hypothesis-driven approach, we show that year-round sexual habitat segregation in S. canicula can be accounted for directly by female avoidance of male sexual harassment. Long-term electronic tracking reveals that sperm-storing female catsharks ...