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.

Environmental context explains Levy 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.

Environmental context explains Lévy and Brownian movement patterns of marine predators

An optimal search theory, the so-called Lévy-flight foraging hypothesis1, 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 prey2, 3, 4. Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Lévy behaviour has recently been questioned5, 6. 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 hypothesis1, 7, supporting the contention8, 9 that organism search strategies naturally evolved in such a way that they exploit optimal Lévy patterns.

Monitoring the Prey-Field of Marine Predators: Combining Digital Imaging With Datalogging Tags

There is increasing interest in the diving behavior of marine mammals. However, identifying foraging among recorded dives often requires several assumptions. The simultaneous acquisition of images of the prey encountered, together with records of diving behavior will allow researchers to more fully investigate the nature of subsurface behavior. We tested a novel digital camera linked to a time-depth recorder on Antarctic fur seals (Arctocephalus gazella). During the austral summer 2000-2001, this system was deployed on six lactating female fur seals at Bird Island, South Georgia, each for a single foraging trip. The camera was triggered at depths greater than 10 m. Five deployments recorded still images (640 x 480 pixels) at 3-sec intervals (total 8,288 images), the other recorded movie images at 0.2-sec intervals (total 7,598 frames). Memory limitation (64 MB) restricted sampling to approximately 1.5 d of 5-7 d foraging trips. An average of 8.5% of still pictures (2.4%-11.6%) showed krill (Euphausia superba) distinctly, while at least half the images in each deployment were empty, the remainder containing blurred or indistinct prey. In one deployment krill images were recorded within 2.5 h (16 km, assuming 1.8 m/sec travel speed) of leaving the beach. Five of the six deployments also showed other fur seals foraging in conjunction with the study animal. This system is likely to generate exciting new avenues for interpretation of diving behavior.

Scale-dependent foraging ecology of a marine top predator modelled using passive acoustic data

1.Understanding which environmental factors drive foraging preferences is critical for the development of effective management measures, but resource use patterns may emerge from processes that occur at different spatial and temporal scales. Direct observations of foraging are also especially challenging in marine predators, but passive acoustic techniques provide opportunities to study the behaviour of echolocating species over a range of scales. 2.We used an extensive passive acoustic data set to investigate the distribution and temporal dynamics of foraging in bottlenose dolphins using the Moray Firth (Scotland, UK). Echolocation buzzes were identified with a mixture model of detected echolocation inter-click intervals and used as a proxy of foraging activity. A robust modelling approach accounting for autocorrelation in the data was then used to evaluate which environmental factors were associated with the observed dynamics at two different spatial and temporal scales. 3.At a broad scale, foraging varied seasonally and was also affected by seabed slope and shelf-sea fronts. At a finer scale, we identified variation in seasonal use and local interactions with tidal processes. Foraging was best predicted at a daily scale, accounting for site specificity in the shape of the estimated relationships. 4.This study demonstrates how passive acoustic data can be used to understand foraging ecology in echolocating species and provides a robust analytical procedure for describing spatio-temporal patterns. Associations between foraging and environmental characteristics varied according to spatial and temporal scale, highlighting the need for a multi-scale approach. Our results indicate that dolphins respond to coarser scale temporal dynamics, but have a detailed understanding of finer-scale spatial distribution of resources.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Identifying predictable foraging habitats for a wide-ranging marine predator using ensemble ecological niche models

Aim: Ecological niche modelling can provide valuable insight into species' environmental preferences and aid the identification of key habitats for populations of conservation concern. Here, we integrate biologging, satellite remote-sensing and ensemble ecological niche models (EENMs) to identify predictable foraging habitats for a globally important population of the grey-headed albatross (GHA) Thalassarche chrysostoma. Location: Bird Island, South Georgia; Southern Atlantic Ocean. Methods: GPS and geolocation-immersion loggers were used to track at-sea movements and activity patterns of GHA over two breeding seasons (n = 55; brood-guard). Immersion frequency (landings per 10-min interval) was used to define foraging events. EENM combining Generalized Additive Models (GAM), MaxEnt, Random Forest (RF) and Boosted Regression Trees (BRT) identified the biophysical conditions characterizing the locations of foraging events, using time-matched oceanographic predictors (Sea Surface Temperature, SST; chlorophyll a, chl-a; thermal front frequency, TFreq; depth). Model performance was assessed through iterative cross-validation and extrapolative performance through cross-validation among years. Results: Predictable foraging habitats identified by EENM spanned neritic (<500 m), shelf break and oceanic waters, coinciding with a set of persistent biophysical conditions characterized by particular thermal ranges (3–8 °C, 12–13 °C), elevated primary productivity (chl-a > 0.5 mg m−3) and frequent manifestation of mesoscale thermal fronts. Our results confirm previous indications that GHA exploit enhanced foraging opportunities associated with frontal systems and objectively identify the APFZ as a region of high foraging habitat suitability. Moreover, at the spatial and temporal scales investigated here, the performance of multi-model ensembles was superior to that of single-algorithm models, and cross-validation among years indicated reasonable extrapolative performance. Main conclusions: EENM techniques are useful for integrating the predictions of several single-algorithm models, reducing potential bias and increasing confidence in predictions. Our analysis highlights the value of EENM for use with movement data in identifying at-sea habitats of wide-ranging marine predators, with clear implications for conservation and management.

Identifying optimal feeding habitat and proposed Marine Protected Areas (pMPAs) for the black-legged kittiwake (Rissa tridactyla) suggests a need for complementary management approaches

Marine Protected Areas (MPAs) are an important conservation tool. For marine predators, recent research has focused on the use of Species Distribution Models (SDMs) to identify proposed sites. We used a maximum entropy modelling approach based on static and dynamic oceanographic parameters to determine optimal feeding habitat for black-legged kittiwakes (Rissa tridactyla) at two colonies during two consecutive breeding seasons (2009 and 2010). A combination of Geographic Positioning System (GPS) loggers and Time-Depth Recorders (TDRs) attributed feeding activity to specific locations. Feeding areas were <30 km from the colony, <40 km from land, in productive waters, 25–175m deep. The predicted extent of optimal habitat declined at both colonies between 2009 and 2010 coincident with declines in reproductive success. Whilst the area of predicted optimal habitat changed, its location was spatially stable between years. There was a close match between observed feeding locations and habitat predicted as optimal at one colony (Lambay Island, Republic of Ireland), but a notable mismatch at the other (Rathlin Island, Northern Ireland). Designation of an MPA at Rathlin may, therefore, be less effective than a similar designation at Lambay perhaps due to the inherent variability in currents and sea state in the North Channel compared to the comparatively stable conditions in the central Irish Sea. Current strategies for designating MPAs do not accommodate likely future redistribution of resources due to climate change. We advocate the development of new approaches including dynamic MPAs that track changes in optimal habitat and non-colony specific ecosystem management.

Determining trends and environmental drivers from long-term marine mammal and seabird data : examples from Southern Australia

Climate change is acknowledged as an emerging threat for top-order marine predators, yet obtaining evidence of impacts is often difficult. In south-eastern Australia, a marine global warming hotspot, evidence suggests that climate change will profoundly affect pinnipeds and seabirds. Long-term data series are available to assess some species' responses to climate. Researchers have measured a variety of chronological and population variables, such as laying dates, chick or pup production, colony-specific abundance and breeding success. Here, we consider the challenges in accurately assessing trends in marine predator data, using long-term data series that were originally collected for other purposes, and how these may be driven by environmental change and variability. In the past, many studies of temporal changes and environmental drivers used linear analyses and we demonstrate the (theoretical) relationship between the magnitude of a trend, its variability, and the duration of a data series required to detect a linear trend. However, species may respond to environmental change in a nonlinear manner and, based on analysis of time-series from south-eastern Australia, it appears that the assumptions of a linear model are often violated, particularly for measures of population size. The commonly measured demographic variables exhibit different degrees of variation, which influences the ability to detect climate signals. Due to their generally lower year-to-year variability, we illustrate that monitoring of variables such as mass and breeding chronology should allow detection of temporal trends earlier in a monitoring programme than observations of breeding success and population size. Thus, establishing temporal changes with respect to climate change from a monitoring programme over a relatively short time period requires careful a priori choice of biological variables. © 2014 Springer-Verlag Berlin Heidelberg.

Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion

Despite global declines in the abundance of marine predators, knowledge of foraging ecology, necessary to predict the ecological consequences of large changes in marine predator abundance, remains enigmatic for many species. Given that populations suffering severe declines are of conservation concern, we examined the foraging ecology of southern sea lions (SSL) (Otaria flavescens)-one of the least studied otariids (fur seal and sea lions)-which have declined by over 90 % at the Falkland Islands since the 1930s. Using a combination of biologging devices and stable isotope analysis of vibrissae, we redress major gaps in the knowledge of SSL ecology and quantify patterns of individual specialization. Specifically, we revealed two discrete foraging strategies, these being inshore (coastal) and offshore (outer Patagonian Shelf). The majority of adult female SSL (72 % or n = 21 of 29 SSL) foraged offshore. Adult female SSL that foraged offshore travelled further (92 ± 20 vs. 10 ± 4 km) and dived deeper (75 ± 23 vs. 21 ± 8 m) when compared to those that foraged inshore. Stable isotope analysis revealed long-term fidelity (years) to these discrete foraging habitats. In addition, we found further specialization within the offshore group, with adult female SSL separated into two clusters on the basis of benthic or mixed (benthic and pelagic) dive behavior (benthic dive proportion was 76 ± 9 vs. 51 ± 8 %, respectively). We suggest that foraging specialization in depleted populations such as SSL breeding at the Falkland Islands, are influenced by foraging site fidelity, and could be independent of intraspecific competition. Finally, the behavioral differences we describe are crucial to understanding population-level dynamics, impediments to population recovery, and threats to population persistence.

Regional variability in diving physiology and behavior in a widely distributed air-breathing marine predator, the South American sea lion Otaria byronia

Our understanding of how air-breathing marine predators cope with environmental variability is limited by our inadequate knowledge of their ecological and physiological parameters. Due to their wide distribution along both coasts of the sub-continent, South American sea lions (Otaria byronia) provide a valuable opportunity to study the behavioral and physiological plasticity of a marine predator in different environments. We measured the oxygen stores and diving behavior of South American sea lions throughout most of its range, allowing us to demonstrate that diving ability and behavior vary across its range. We found no significant differences in mass-specific blood volumes of sea lions among field sites and a negative relationship between mass-specific oxygen storage and size, which suggests that exposure to different habitats and geographical locations better explains oxygen storage capacities and diving capability in South American sea lions than body size alone. The largest animals in our study (individuals from Uruguay) were the most shallow and short duration divers, and had the lowest mass-specific total body oxygen stores, while the deepest and longest duration divers (individuals from Southern Chile) had significantly larger mass-specific oxygen stores, despite being much smaller animals.Our study suggests that the physiology of air-breathing diving predators is not fixed, but that it can be adjusted, to a certain extent, depending on the ecological setting and or habitat. These adjustments can be thought of as a "training effect" as the animal continues to push its physiological capacity through greater hypoxic exposure, its breath holding capacity increases.

New information from fish diets on the importance of glassy flying squid (Hyaloteuthis pelagica) (Teuthoidea: Ommastrephidae) in the epipelagic cephalopod community of the tropical Atlantic Ocean

Squids of the family Ommastrephidae are a vital part of marine food webs and support major fisheries around the world. They are widely distributed in the open ocean, where they are among the most abundant in number and biomass of nektonic epipelagic organisms. In turn, seven of the 11 genera of this family (Dosidicus, Illex, Martialia, Nototodarus, Ommastrephes, Sthenoteuthis, and Todarodes) are heavily preyed upon by top marine predators, i.e., birds, mammals, and fish, and currently support fisheries in both neritic and oceanic waters (Roper and Sweeney, 1984; Rodhouse, 1997). Their commercial importance has made the large ommastrephids the target of many scientific investigations and their biology is consequently reasonably well-known (Nigmatullin et al., 2001; Zuyev et al., 2002; Bower and Ichii, 2005). In contrast, much less information is available on the biology and ecological role of the smaller, unexploited species of ommastrephids (e.g., Eucleoteuthis, Hyaloteuthis, Ornithoteuthis, and Todaropsis).

Validating the use of intrinsic markers in body feathers to identify inter‑individual differences in non‑breeding areas of northern fulmars

Many wildlife studies use chemical analyses to explore spatio-temporal variation in diet, migratory patterns and contaminant exposure. Intrinsic markers are particularly valuable for studying non-breeding marine predators, when direct methods of investigation are rarely feasible. However, any inferences regarding foraging ecology are dependent upon the time scale over which tissues such as feathers are formed. In this study, we validate the use of body feathers for studying non-breeding foraging patterns in a pelagic seabird, the northern fulmar. Analysis of carcasses of successfully breeding adult fulmars indicated that body feathers moulted between September and March, whereas analyses of carcasses and activity patterns suggested that wing feather and tail feather moult occurred during more restricted periods (September to October and September to January, respectively). By randomly sampling relevant body feathers, average values for individual birds were shown to be consistent. We also integrated chemical analyses of body feather with geolocation tracking data to demonstrate that analyses of δ13C and δ15N values successfully assigned 88 % of birds to one of two broad wintering regions used by breeding adult fulmars from a Scottish study colony. These data provide strong support for the use of body feathers as a tool for exploring non-breeding foraging patterns and diet in wide-ranging, pelagic seabirds.

Foraging behaviour and habitat utilisation of Australasian gannets determined using GPS loggers

Australasian gannets (Morus serrator) breed in the cool temperate waters of south-eastern Australia and also at several localities around New Zealand, where they are a major marine predator feeding on commercially-exploited pelagic fish. This study investigated the foraging behaviour and habitat utilization of gannets at Pope’s Eye Marine Reserve during the 2005-2005 breeding period using GPS-depth-loggers. GPS data were recorded for a total of 45 foraging trips from 20 individuals. Gannets were found to forage at average maximum distances of 52.7 km (± 29.6 km) from the colony, with total foraging path lengths of 177.1 km (± 93.4 km) and foraging trip durations of 16.5 h (± 9.9 h). During foraging trips gannets spent on average 31.5% (± 11.4) of the time flying at an average flight speed of 47.3 km h-1 (± 2.9 km h-1). Gannets made an average of 39.8 (± 35.2) dives per trip and 3.8 (± 5.6) dives per daylight hour. Dives had an average depth of 3.5 m (± 1.1 m) and a mean maximum depth of 7.0 m (± 3.0 m), lasting for a mean dive duration of 5.3 sec (± 1.3 sec). Gannets foraged predominantly in shallow coastal waters and there was some evidence for foraging site fidelity. Considerable individual variation in foraging strategies was also observed. The results highlight the potential of GPS technology to reveal the fine-scale foraging behaviour of marine predators, thereby improving our understanding the interaction between marine predator populations, commercially exploited fish stocks and the marine environment.

Foraging behaviour and habitat selection of the little penguin Eudyptula minor during early chick rearing in Bass Strait, Australia

Knowledge of the foraging areas of top marine predators and the factors influencing them is central to understanding how their populations respond to environmental variability. While there is a large body of literature documenting the association of air-breathing marine vertebrates with areas of high marine productivity, there is relatively little information for species restricted to near-shore or continental-shelf areas. Differences in foraging range and diving behaviour of the little penguin Eudyptula minor were examined from 3 breeding colonies (Rabbit Island, Kanowna Island and Phillip Island) in central northern Bass Strait, southeast Australia, during the chick-guard stage using electronic tags (platform terminal transmitters, PTTs, and time-depth recorders, TDRs). Although there were large overall differences between individuals, the mean maximum foraging range (16.9 to 19.8 km) and mean total distance travelled (41.8 to 48.0 km) were similar between the 3 colonies, despite different bathymetric environments. Individuals from all 3 colonies selected foraging habitats within a narrow sea surface temperature (SST) range (16.0 to 16.4°C). While there were significant differences in mean dive depths (5.4 to 10.9 m) and mean durations (13.2 to 28.6 s) between the different colonies, the mean diving effort (vertical distance travelled: 936.3 to 964.3 m h–1) was similar. These findings suggest little penguins from the 3 colonies employ relatively similar foraging efforts yet are plastic in their foraging behaviours.