Telemetry and random-walk models reveal complex patterns of partial migration in a large marine predator.

Animals are often faced with complex movement decisions, particularly those that involve long-distance dispersal. Partial migrations, ubiquitous among all groups of vertebrates, are a form of long-distance movement that occurs when only some of the animals in a population migrate. The decision to migrate or to be a resident can be dependent on many factors, but these factors are rarely quantified in fishes, particularly top predators, even though partial migrations may have important implications for ecosystem dynamics and conservation. We utilized passive acoustic telemetry, with a Brownian bridge movement model and generalized additive mixed models, to explore the factors regulating partial migration in a large marine predator, the tiger shark, throughout the Hawaiian Islands. Although sharks tended to utilize a particular "core" island, they also demonstrated inter-island movements, particularly mature females that would swim from the northwestern Hawaiian Islands to the main Hawaiian Islands (MHI). Immigration to another island was a function of season, sea surface temperature (SST), and chlorophyll a concentration. Our results predict that 25% of mature females moved from remote French Frigate Shoals atoll to the MHI during late summer/early fall, potentially to give birth. Females with core home ranges within the MHI showed limited movements to the NWHI, and immigration to an island was better explained by SST and chlorophyll a concentration, suggesting a foraging function. Dispersal patterns in tiger sharks are complex but can be considered a mix of skipped-breeding partial migration by mature females and individual-based inter-island movements potentially linked to foraging. Therefore, sharks appear to use a conditional strategy based on fixed intrinsic and flexible extrinsic states. The application of Brownian bridge movement models to electronic presence/absence data provides a new technique for assessing the influence of habitat and environmental conditions on patterns of movement for fish populations.

"Breath holding" as a thermoregulation strategy in the deep-diving scalloped hammerhead shark.

Fish moving between different thermal environments experience heat exchange via conduction through the body wall and convection from blood flow across the gills. We report a strategy of preventing convective heat loss at the gills during excursions into deep, cold water by the tropical scalloped hammerhead shark (Sphryna lewini). Adult scalloped hammerhead sharks dive rapidly and repeatedly from warm (~26°C) surface waters to depths exceeding 800 meters with temperatures as low as 5°C. Biologgers attached to adult sharks show that warm muscle temperatures were maintained throughout the deepest portion of each dive. Substantive cooling only occurred during the latter stages of the ascent phase and, once initiated, was rapid. Heat transfer coefficient modeling indicated that convective heat transfer was suspended, probably by suppressing gill function during deep dives. This previously unobserved strategy has broad similarities to marine mammal "breath hold" diving.

Autonomous measurement of ingestion and digestion processes in free-swimming sharks.

Direct measurement of predator feeding events would represent a major advance in marine trophic ecology. To date, devices available for empirically quantifying feeding in free-swimming fishes have relied on measuring stomach temperature, pH or physical motility, each of which has major practical limitations. We hypothesized that the considerable physical changes that occur in the stomachs of carnivorous predators during the processes of ingestion and digestion should be quantifiable using bulk electrical impedance measured across paired electrodes. We used a prototype archival data logging tag to record changes in impedance inside the stomachs of captive free-swimming tiger and sandbar sharks over multiple, successive feeding events. Feeding and digestion events produced characteristic changes in electrical impedance of the stomach contents, identifiable as five successive phases: (1) pre-ingestion (empty stomach), (2) ingestion, (3) chemical 'lag', (4) mechanical 'chyme' and (5) stomach emptying. The duration of the chyme phase was positively related to meal size.

Energetics of the yo-yo dives of predatory sharks.

Sharks zigzag vertically through the water in a series of alternating ascending and descending segments, changing depth by a few tens of meters over a period of a few hundred seconds. This 'yo-yo' like behavior has several characteristic patterns, identifiable by the way the swimming and vertical velocities vary along the dive. We suggest that these patterns represent different optimal strategies minimizing the cost of locomotion under different constraints; moreover, these constraints can be inferred by matching the pattern of a dive with a (standard) optimal swimming strategy for which the constraints are known. We used three sets of constraints and two definitions of the 'cost of locomotion' to analytically generate four standard optimal strategies; we have used high resolution tracking data from four tiger sharks to identify two different yo-yo diving patterns. These patterns seem to match two of the standard strategies: one that maximizes range, given an alternating power supply (e.g., swimming actively on ascents and lazily on descents); and the other that maximizes range, given an alternating vertical velocity (implying an 'intentional' up-and-down motion).

Scales of orientation, directed walks and movement path structure in sharks.

1. Animal search patterns reflect sensory perception ranges combined with memory and knowledge of the surrounding environment. 2. Random walks are used when the locations of resources are unknown, whereas directed walks should be optimal when the location of favourable habitats is known. However, directed walks have been quantified for very few species. 3. We re-analysed tracking data from three shark species to determine whether they were using directed walks, and if so, over which spatial scales. Fractal analysis was used to quantify how movement structure varied with spatial scale and determine whether the sharks were using patches. 4. Tiger sharks performed directed walks at large spatial scales (at least 6-8 km). Thresher sharks also showed directed movement (at scales of 400-1900 m), and adult threshers were able to orient at greater scales than juveniles, which may suggest that learning improves the ability to perform directed walks. Blacktip reef sharks had small home ranges, high site fidelity and showed no evidence of oriented movements at large scales. 5. There were inter- and intraspecific differences in path structure and patch size, although most individuals showed scale-dependent movements. Furthermore, some individuals of each species performed movements similar to a correlated random walk. 6. Sharks can perform directed walks over large spatial scales, with scales of movements reflecting site fidelity and home range size. Understanding when and where directed walks occur is crucial for developing more accurate population-level dispersal models.

Diel patterns in swimming behavior of a vertically migrating deepwater shark, the bluntnose sixgill (Hexanchus griseus).

Diel vertical migration is a widespread behavioral phenomenon where organisms migrate through the water column and may modify behavior relative to changing environmental conditions based on physiological tolerances. Here, we combined a novel suite of biologging technologies to examine the thermal physiology (intramuscular temperature), fine-scale swimming behavior and activity (overall dynamic body acceleration as a proxy for energy expenditure) of bluntnose sixgill sharks (Hexanchus griseus) in response to environmental changes (depth, water temperature, dissolved oxygen) experienced during diel vertical migrations. In the subtropical waters off Hawai'i, sixgill sharks undertook pronounced diel vertical migrations and spent considerable amounts of time in cold (5-7°C), low oxygen conditions (10-25% saturation) during their deeper daytime distribution. Further, sixgill sharks spent the majority of their deeper daytime distribution with intramuscular temperatures warmer than ambient water temperatures, thereby providing them with a significant thermal advantage over non-vertically migrating and smaller-sized prey. Sixgill sharks exhibited relatively high rates of activity during both shallow (night) and deep (day) phases and contrary to our predictions, did not reduce activity levels during their deeper daytime distribution while experiencing low temperature and dissolved oxygen levels. This demonstrates an ability to tolerate the low oxygen conditions occurring within the local oxygen minimum zone. The novel combination of biologging technologies used here enabled innovative in situ deep-sea natural experiments and provided significant insight into the behavioral and physiological ecology of an ecologically important deepwater species.

Habitat geography around Hawaii's oceanic islands influences tiger shark (Galeocerdo cuvier) spatial behaviour and shark bite risk at ocean recreation sites.

We compared tiger shark (Galeocerdo cuvier) spatial behaviour among 4 Hawaiian Islands to evaluate whether local patterns of movement could explain higher numbers of shark bites seen around Maui than other islands. Our sample consisted of 96 electronically-tagged (satellite and acoustic transmitters) tiger sharks, individually tracked for up to 6 years. Most individuals showed fidelity to a specific 'home' island, but also swam between islands and sometimes ranged far (up to 1,400 km) offshore. Movements were primarily oriented to insular shelf habitat (0-200 m depth) in coastal waters, and individual sharks utilized core-structured home ranges within this habitat. Core utilization areas of large tiger sharks were closer to high-use ocean recreation sites around Maui, than around Oahu. Tiger sharks routinely visited shallow ocean recreation sites around Maui and were detected on more days overall at ocean recreation sites around Maui (62-80%) than Oahu (<6%). Overall, our results suggest the extensive insular shelf surrounding Maui supports a fairly resident population of tiger sharks and also attracts visiting tiger sharks from elsewhere in Hawaii. Collectively these natural, habitat-driven spatial patterns may in-part explain why Maui has historically had more shark bites than other Hawaiian Islands.

Insight into shark magnetic field perception from empirical observations.

Elasmobranch fishes are among a broad range of taxa believed to gain positional information and navigate using the earth's magnetic field, yet in sharks, much remains uncertain regarding the sensory receptors and pathways involved, or the exact nature of perceived stimuli. Captive sandbar sharks, Carcharhinus plumbeus were conditioned to respond to presentation of a magnetic stimulus by seeking out a target in anticipation of reward (food). Sharks in the study demonstrated strong responses to magnetic stimuli, making significantly more approaches to the target (p = < 0.01) during stimulus activation (S+) than before or after activation (S-). Sharks exposed to reversible magnetosensory impairment were less capable of discriminating changes to the local magnetic field, with no difference seen in approaches to the target under the S+ and S- conditions (p = 0.375). We provide quantified detection and discrimination thresholds of magnetic stimuli presented, and quantify associated transient electrical artefacts. We show that the likelihood of such artefacts serving as the stimulus for observed behavioural responses was low. These impairment experiments support hypotheses that magnetic field perception in sharks is not solely performed via the electrosensory system, and that putative magnetoreceptor structures may be located in the naso-olfactory capsules of sharks.

Sharks can detect changes in the geomagnetic field.

We used behavioural conditioning to demonstrate that sharks can detect changes in the geomagnetic field. Captive sharks were conditioned by pairing activation of an artificial magnetic field with presentation of food over a target. Conditioned sharks subsequently converged on the target when the artificial magnetic field was activated but no food reward was presented thereby demonstrating that they were able to sense the altered magnetic field. This strong response provides a robust behavioural assay that could be used to determine how sharks detect magnetic fields and to measure detection thresholds.

ECOLOGY. Aquatic animal telemetry: A panoramic window into the underwater world.

The distribution and interactions of aquatic organisms across space and time structure our marine, freshwater, and estuarine ecosystems. Over the past decade, technological advances in telemetry have transformed our ability to observe aquatic animal behavior and movement. These advances are now providing unprecedented ecological insights by connecting animal movements with measures of their physiology and environment. These developments are revolutionizing the scope and scale of questions that can be asked about the causes and consequences of movement and are redefining how we view and manage individuals, populations, and entire ecosystems. The next advance in aquatic telemetry will be the development of a global collaborative effort to facilitate infrastructure and data sharing and management over scales not previously possible.

Growth and maximum size of tiger sharks (Galeocerdo cuvier) in Hawaii.

Tiger sharks (Galecerdo cuvier) are apex predators characterized by their broad diet, large size and rapid growth. Tiger shark maximum size is typically between 380 & 450 cm Total Length (TL), with a few individuals reaching 550 cm TL, but the maximum size of tiger sharks in Hawaii waters remains uncertain. A previous study suggested tiger sharks grow rather slowly in Hawaii compared to other regions, but this may have been an artifact of the method used to estimate growth (unvalidated vertebral ring counts) compounded by small sample size and narrow size range. Since 1993, the University of Hawaii has conducted a research program aimed at elucidating tiger shark biology, and to date 420 tiger sharks have been tagged and 50 recaptured. All recaptures were from Hawaii except a single shark recaptured off Isla Jacques Cousteau (24°13'17″N 109°52'14″W), in the southern Gulf of California (minimum distance between tag and recapture sites  =  approximately 5,000 km), after 366 days at liberty (DAL). We used these empirical mark-recapture data to estimate growth rates and maximum size for tiger sharks in Hawaii. We found that tiger sharks in Hawaii grow twice as fast as previously thought, on average reaching 340 cm TL by age 5, and attaining a maximum size of 403 cm TL. Our model indicates the fastest growing individuals attain 400 cm TL by age 5, and the largest reach a maximum size of 444 cm TL. The largest shark captured during our study was 464 cm TL but individuals >450 cm TL were extremely rare (0.005% of sharks captured). We conclude that tiger shark growth rates and maximum sizes in Hawaii are generally consistent with those in other regions, and hypothesize that a broad diet may help them to achieve this rapid growth by maximizing prey consumption rates.

Global phylogeography with mixed-marker analysis reveals male-mediated dispersal in the endangered scalloped hammerhead shark (Sphyrna lewini).

BACKGROUND: The scalloped hammerhead shark, Sphyrna lewini, is a large endangered predator with a circumglobal distribution, observed in the open ocean but linked ontogenetically to coastal embayments for parturition and juvenile development. A previous survey of maternal (mtDNA) markers demonstrated strong genetic partitioning overall (global Φ(ST) = 0.749) and significant population separations across oceans and between discontinuous continental coastlines. METHODOLOGY/PRINCIPAL FINDINGS: We surveyed the same global range with increased sample coverage (N = 403) and 13 microsatellite loci to assess the male contribution to dispersal and population structure. Biparentally inherited microsatellites reveal low or absent genetic structure across ocean basins and global genetic differentiation (F(ST) = 0.035) over an order of magnitude lower than the corresponding measures for maternal mtDNA lineages (Φ(ST) = 0.749). Nuclear allelic richness and heterozygosity are high throughout the Indo-Pacific, while genetic structure is low. In contrast, allelic diversity is low while population structure is higher for populations at the ends of the range in the West Atlantic and East Pacific. CONCLUSIONS/SIGNIFICANCE: These data are consistent with the proposed Indo-Pacific center of origin for S. lewini, and indicate that females are philopatric or adhere to coastal habitats while males facilitate gene flow across oceanic expanses. This study includes the largest sampling effort and the most molecular loci ever used to survey the complete range of a large oceanic predator, and findings emphasize the importance of incorporating mixed-marker analysis into stock assessments of threatened and endangered shark species.

Electroreception in juvenile scalloped hammerhead and sandbar sharks.

The unique head morphology of sphyrnid sharks might have evolved to enhance electrosensory capabilities. The 'enhanced electroreception' hypothesis was tested by comparing the behavioral responses of similarly sized carcharhinid and sphyrnid sharks to prey-simulating electric stimuli. Juvenile scalloped hammerhead sharks Sphyrna lewini and sandbar sharks Carcharhinus plumbeus oriented to dipole electric fields from the same maximum distance (approximately 30 cm) and thus demonstrated comparable behavioral-response thresholds (<1 nV cm(-1)). Despite the similarity of response threshold, the orientation pathways and behaviors differed for the two species. Scalloped hammerheads typically demonstrated a pivot orientation in which the edge of the cephalofoil closest to the dipole remained stationary while the shark bent its trunk to orient to the center of the dipole. By contrast, sandbars swam in a broader arc towards the center of the dipole. The different orientation patterns are attributed to the hydrodynamic properties of the cephalofoil, which enables the hammerheads to execute sharp turns at high speed. The greater trunk width of the sandbar sharks prevented them from demonstrating the same degree of flexibility. Therefore, although the sphyrnid head morphology does not appear to confer a greater sensitivity to prey-simulating dipole electric fields, it does provide (1). a greater lateral search area, which may increase the probability of prey encounter, and (2). enhanced maneuverability, which may aid in prey capture.