The diving behaviour of green turtles undertaking oceanic migration to and from Ascension Island: dive durations, dive profiles and depth distribution

Satellite telemetry was used to record the submergence duration of green turtles (Chelonia mydas) as they migrated from Ascension Island to Brazil (N=12 individuals) while time/depth recorders (TDRs) were used to examine the depth distribution and dive profiles of individuals returning to Ascension Island to nest after experimental displacement (N=5 individuals). Satellite telemetry revealed that most submergences were short (<5 min) but that some submergences were longer (>20 min), particularly at night. TDRs revealed that much of the time was spent conducting short (2–4 min), shallow (approximately 0.9–1.5 m) dives, consistent with predictions for optimisation of near-surface travelling, while long (typically 20–30 min), deep (typically 10–20 m) dives had a distinctive profile found in other marine reptiles. These results suggest that green turtles crossing the Atlantic do not behave invariantly, but instead alternate between periods of travelling just beneath the surface and diving deeper. These deep dives may have evolved to reduce silhouetting against the surface, which would make turtles more susceptible to visual predators such as large sharks.

Convergent evolution in locomotory patterns of flying and swimming animals

Locomotion is one of the major energetic costs faced by animals and various strategies have evolved to reduce its cost. Birds use interspersed periods of flapping and gliding to reduce the mechanical requirements of level flight while undergoing cyclical changes in flight altitude, known as undulating flight. Here we equipped free-ranging marine vertebrates with accelerometers and demonstrate that gait patterns resembling undulating flight occur in four marine vertebrate species comprising sharks and pinnipeds. Both sharks and pinnipeds display intermittent gliding interspersed with powered locomotion. We suggest, that the convergent use of similar gait patterns by distinct groups of animals points to universal physical and physiological principles that operate beyond taxonomic limits and shape common solutions to increase energetic efficiency. Energetically expensive large-scale migrations performed by many vertebrates provide common selection pressure for efficient locomotion, with potential for the convergence of locomotory strategies by a wide variety of species.

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.

Asynchrony and regional differences in the reproductive cycle of the greenback stingaree Urolophus viridis from south-eastern Australia

Determining the periodicity of the reproductive cycle in chondrichthyan species when the population is recruiting asynchronously, as found for Urolopus viridis, can be problematic. The reproductive cycle generally requires distinguishable trends in reproductive indices across the population. The present study utilised other similar and sympatric urolophid species with synchronous reproductive cycles. Through data collected in the present study and comparisons of maximum total length (TL), periodicity of egg and embryo in utero, ovarian cycles, largest ovarian follicle diameter, and matrotrophic contribution (percentage increase from egg to embryo after maternal histotroph supplement) from similar studies, an annual reproductive cycle can be hypothesised. Sampling across two separate regions of Lakes Entrance (LE) and Western Bass Strait (WBS), U. viridis also showed regionality in several of the reproductive indices. Maximum TL and mass for females, mean size-at-birth, and female size-at-maturity and size-at-maternity in LE were markedly smaller than in WBS. In both regions litter size (1–2) increased with TL, with an exception of one female in WBS producing a litter of 3 which could be attributed to the larger TL. The implication of U. viridis producing such few young annually is they have the lowest biological productivity of any urolophid species in south-eastern Australia.

Protected species use of a coastal marine migratory corridor connecting marine protected areas

The establishment of protected corridors linking the breeding and foraging grounds of many migratory species remains deficient, particularly in the world's oceans. For example, Australia has recently established a network of Commonwealth Marine Reserves, supplementing existing State reserves, to protect a wide range of resident and migratory marine species; however, the routes used by mobile species to access these sites are often unknown. The flatback marine turtle (Natator depressus) is endemic to the continental shelf of Australia, yet information is not available about how this species uses the marine area. We used a geospatial approach to delineate a coastal corridor from 73 adult female flatback postnesting migratory tracks from four rookeries along the north-west coast of Australia. A core corridor of 1,150 km length and 30,800 km2 area was defined, of which 52 % fell within 11 reserves, leaving 48 % (of equivalent size to several Commonwealth Reserves) of the corridor outside of the reserve network. Despite limited data being available for other marine wildlife in this region, humpback whale migratory tracks overlapped with 96 % of the core corridor, while the tracks of three other species overlapped by 5-10 % (blue whales, olive ridley turtles, whale sharks). The overlap in the distribution ranges of at least 20 other marine vertebrates (dugong, cetaceans, marine turtles, sea snakes, crocodiles, sharks) with the corridor also imply potential use. In conclusion, this study provides valuable information towards proposing new locations requiring protection, as well as identifying high-priority network linkages between existing marine protected areas. © 2014 Springer-Verlag Berlin Heidelberg.

Use of long-distance migration patterns of an endangered species to inform conservation planning for the world's largest marine protected area

Large marine protected areas (MPAs), each hundreds of thousands of square kilometers, have been set up by governments around the world over the last decade as part of efforts to reduce ocean biodiversity declines, yet their efficacy is hotly debated. The Chagos Archipelago MPA (640,000 km2) (Indian Ocean) lies at the heart of this debate. We conducted the first satellite tracking of a migratory species, the green turtle (Chelonia mydas), within the MPA and assessed the species' use of protected versus unprotected areas. We developed an approach to estimate length of residence within the MPA that may have utility across migratory taxa including tuna and sharks. We recorded the longest ever published migration for an adult cheloniid turtle (3979 km). Seven of 8 tracked individuals migrated to distant foraging grounds, often ≥1000 km outside the MPA. One turtle traveled to foraging grounds within the MPA. Thus, networks of small MPAs, developed synergistically with larger MPAs, may increase the amount of time migrating species spend within protected areas. The MPA will protect turtles during the breeding season and will protect some turtles on their foraging grounds within the MPA and others during the first part of their long-distance postbreeding oceanic migrations. International cooperation will be needed to develop the network of small MPAs needed to supplement the Chagos Archipelago MPA.

How small-scale variation in oyster reef patchiness influences predation on bivalves

As oyster fishing continues to degrade reef habitat along the US Atlantic coast, oyster reefs appear increasingly fragmented on small spatial scales. In outdoor mesocosms, experiments tested how consumption of representatives of 4 different bivalve guilds by each of 3 mesopredators varies between continuous and fine-scale patches of oyster reef habitat. The mesopredator that fed least (stone crab) exhibited no detectable change in consumption on any bivalve (ribbed mussel, bay scallop, hard clam, and 3 size classes of eastern oyster). Consumption of bay scallops by both blue crabs and sheepshead fish was greater in small patches than in continuous oyster reef habitat. Of the bivalve guilds tested, only the scallop possesses swimming motility sufficient to reduce predation, an escape response that would likely leave the bivalve protected within structured habitat in larger continuous oyster reefs. Sheepshead consumed more small oysters in the continuous habitat than in the fine patches, while no other predator-prey interaction exhibited differential feeding as a function of habitat patchiness. Consequently, predation by mesopredators on bivalves can vary with the scale of oyster reef patchiness, but this process may depend upon the bivalve guild. Understanding the role of habitat patchiness on fine scales may be increasingly important in view of the declines in apex predatory sharks leading to mesopredator release, and global climate change directly and indirectly enhancing stone crab abundances, thereby increasing potential predation on bivalves.

A new method for resolving uncertainty of energy requirements in large water breathers: The 'mega-flume' seagoing swim-tunnel respirometer

Body size is a key determinant of metabolic rate, but logistical constraints have led to a paucity of energetics measurements from large water-breathing animals. As a result, estimating energy requirements of large fish generally relies on extrapolation of metabolic rate from individuals of lower body mass using allometric relationships that are notoriously variable. Swim-tunnel respirometry is the 'gold standard' for measuring active metabolic rates in water-breathing animals, yet previous data are entirely derived from body masses <10 kg - at least one order of magnitude lower than the body masses of many top-order marine predators. Here, we describe the design and testing of a new method for measuring metabolic rates of large water-breathing animals: a c. 26 000 L seagoing 'mega-flume' swim-tunnel respirometer. We measured the swimming metabolic rate of a 2·1-m, 36-kg zebra shark Stegostoma fasciatum within this new mega-flume and compared the results to data we collected from other S. fasciatum (3·8-47·7 kg body mass) swimming in static respirometers and previously published measurements of active metabolic rate measurements from other shark species. The mega-flume performed well during initial tests, with intra- and interspecific comparisons suggesting accurate metabolic rate measurements can be obtained with this new tool. Inclusion of our data showed that the scaling exponent of active metabolic rate with mass for sharks ranging from 0·13 to 47·7 kg was 0·79; a similar value to previous estimates for resting metabolic rates in smaller fishes. We describe the operation and usefulness of this new method in the context of our current uncertainties surrounding energy requirements of large water-breathing animals. We also highlight the sensitivity of mass-extrapolated energetic estimates in large aquatic animals and discuss the consequences for predicting ecosystem impacts such as trophic cascades.

Examining the functional role of current area closures used for the conservation of an overexploited and highly mobile fishery species

Protecting essential habitats through the implementation of area closures has been recognized as a useful management tool for rebuilding overfished populations and minimizing habitat degradation. School shark (Galeorhinus galeus) have suffered significant stock declines in Australia; however, recent stock assessments suggest the population may have stabilized and the protection of closed nursery areas has been identified as a key management strategy to rebuilding their numbers. Young-of-The-year (YOY) and juvenile G. galeus were acoustically tagged and monitored to determine ontogenetic differences in residency and seasonal use of an important protected nursery area (Shark Refuge Area or SRA) in southeastern Tasmania. BothYOYand juvenile G. galeus showed a distinct seasonal pattern of occurrence in the SRAwith most departing the area during winter and only a small proportion of YOY (33%) and no juveniles returning the following spring, suggesting areas outside the SRA may also be important during these early life-history stages. While these behaviors confirm SRAs continue to function as essential habitat during G. galeus early life history, evidence of YOY and juveniles emigrating from these areas within their first 1-2 years and the fact that few YOY return suggest that these areas may only afford protection for a more limited amount of time than previously thought. Determining the importance of neighbouring coastal waters and maintaining the use of traditional fisheries management tools are therefore required to ensure effective conservation of G. galeus during early life history.

Markov models and network analysis reveal sex-specific differences in the space-use of a coastal apex predator

Understanding the links between external variables such as habitat and interactions with conspecifics and animal space-use is fundamental to developing effective management measures. In the marine realm, automated acoustic tracking has become a widely used method for monitoring the movement of free-ranging animals, yet researchers generally lack robust methods for analysing the resulting spatial-usage data. In this study, acoustic tracking data from male and female broadnose sevengill sharks Notorynchus cepedianus, collected in a system of coastal embayments in southeast Tasmania were analyzed to examine sex-specific differences in the sharks' coastal space-use and test novel methods for the analysis of acoustic telemetry data. Sex-specific space-use of the broadnose sevengill shark from acoustic telemetry data was analysed in two ways: The recently proposed spatial network analysis of between-receiver movements was employed to identify sex-specific space-use patterns. To include the full breadth of temporal information held in the data, movements between receivers were furthermore considered as transitions between states of a Markov chain, with the resulting transition probability matrix allowing the ranking of the relative importance of different parts of the study area. Both spatial network and Markov chain analysis revealed sex-specific preferences of different sites within the study area. The identification of priority areas differed for the methods, due to the fact that in contrast to network analysis, our Markov chain approach preserves the chronological sequence of detections and accounts for both residency periods and movements. In addition to adding to our knowledge of the ecology of a globally distributed apex predator, this study presents a promising new step towards condensing the vast amounts of information collected with acoustic tracking technology into straightforward results which are directly applicable to the management and conservation of any species that meet the assumptions of our model.

Integrating acoustic telemetry into mark-recapture models to improve the precision of apparent survival and abundance estimates

Capture-mark-recapture models are useful tools for estimating demographic parameters but often result in low precision when recapture rates are low. Low recapture rates are typical in many study systems including fishing-based studies. Incorporating auxiliary data into the models can improve precision and in some cases enable parameter estimation. Here, we present a novel application of acoustic telemetry for the estimation of apparent survival and abundance within capture-mark-recapture analysis using open population models. Our case study is based on simultaneously collecting longline fishing and acoustic telemetry data for a large mobile apex predator, the broadnose sevengill shark (Notorhynchus cepedianus), at a coastal site in Tasmania, Australia. Cormack-Jolly-Seber models showed that longline data alone had very low recapture rates while acoustic telemetry data for the same time period resulted in at least tenfold higher recapture rates. The apparent survival estimates were similar for the two datasets but the acoustic telemetry data showed much greater precision and enabled apparent survival parameter estimation for one dataset, which was inestimable using fishing data alone. Combined acoustic telemetry and longline data were incorporated into Jolly-Seber models using a Monte Carlo simulation approach. Abundance estimates were comparable to those with longline data only; however, the inclusion of acoustic telemetry data increased precision in the estimates. We conclude that acoustic telemetry is a useful tool for incorporating in capture-mark-recapture studies in the marine environment. Future studies should consider the application of acoustic telemetry within this framework when setting up the study design and sampling program.

Integrating network analysis, sensor tags, and observation to understand shark ecology and behavior

Group living in animals is a well-studied phenomenon, having been documented extensively in a wide range of terrestrial, freshwater, and marine species. Although social dynamics are complex across space and time, recent technological and analytical advances enable deeper understanding of their nature and ecological implications. While for some taxa, a great deal of information is known regarding the mechanistic underpinnings of these social processes, knowledge of these mechanisms in elasmobranchs is lacking. Here, we used an integrative and novel combination of direct observation, accelerometer biologgers, and recent advances in network analysis to better understand the mechanistic bases of individual-level differences in sociality (leadership, network attributes) and diel patterns of locomotor activity in a widespread marine predator, the lemon shark (Negaprion brevirostris). We found that dynamic models of interaction based on Markov chains can accurately predict juvenile lemon shark social behavior and that lemon sharks did not occupy consistent positions within their network. Lemon sharks did however preferentially associate with specific group members, by sex as well as by similarity or nonsimilarity for a number of behavioral (nonsimilarity: leadership) and locomotor traits (similarity: proportion of time swimming "fast," mean swim duration; nonsimilarity: proportion of swimming bursts/transitions between activity states). Our study provides some of the first information on the mechanistic bases of group living and personality in sharks and further, a potential experimental approach for studying fine-scale differences in behavior and locomotor patterns in difficult-to-study organisms.