Combining abundance and performance data reveals how temperature regulates coastal occurrences and activity of a roaming apex predator.

The redistribution of species has emerged as one of the most pervasive impacts of anthropogenic climate warming, and presents many societal challenges. Understanding how temperature regulates species distributions is particularly important for mobile marine fauna such as sharks given their seemingly rapid responses to warming, and the socio-political implications of human encounters with some dangerous species. The predictability of species distributions can potentially be improved by accounting for temperature's influence on performance, an elusive relationship for most large animals. We combined multi-decadal catch data and bio-logging to show that coastal abundance and swimming performance of tiger sharks Galeocerdo cuvier are both highest at ~22°C, suggesting thermal constraints on performance may regulate this species' distribution. Tiger sharks are responsible for a large proportion of shark bites on humans, and a focus of controversial control measures in several countries. The combination of distribution and performance data moves towards a mechanistic understanding of tiger shark's thermal niche, and delivers a simple yet powerful indicator for predicting the location and timing of their occurrences throughout coastlines. For example, tiger sharks are mostly caught at Australia's popular New South Wales beaches (i.e. near Sydney) in the warmest months, but our data suggest similar abundances will occur in winter and summer if annual sea surface temperatures increase by a further 1-2°C.

Strong trans-Pacific break and local conservation units in the Galapagos shark (Carcharhinus galapagensis) revealed by genome-wide cytonuclear markers.

The application of genome-wide cytonuclear molecular data to identify management and adaptive units at various spatio-temporal levels is particularly important for overharvested large predatory organisms, often characterized by smaller, localized populations. Despite being "near threatened", current understanding of habitat use and population structure of Carcharhinus galapagensis is limited to specific areas within its distribution. We evaluated population structure and connectivity across the Pacific Ocean using genome-wide single-nucleotide polymorphisms (~7200 SNPs) and mitochondrial control region sequences (945 bp) for 229 individuals. Neutral SNPs defined at least two genetically discrete geographic groups: an East Tropical Pacific (Mexico, east and west Galapagos Islands), and another central-west Pacific (Lord Howe Island, Middleton Reef, Norfolk Island, Elizabeth Reef, Kermadec, Hawaii and Southern Africa). More fine-grade population structure was suggested using outlier SNPs: west Pacific, Hawaii, Mexico, and Galapagos. Consistently, mtDNA pairwise ΦST defined three regional stocks: east, central and west Pacific. Compared to neutral SNPs (FST = 0.023-0.035), mtDNA exhibited more divergence (ΦST = 0.258-0.539) and high overall genetic diversity (h = 0.794 ± 0.014; π = 0.004 ± 0.000), consistent with the longstanding eastern Pacific barrier between the east and central-west Pacific. Hawaiian and Southern African populations group within the west Pacific cluster. Effective population sizes were moderate/high for east/west populations (738 and 3421, respectively). Insights into the biology, connectivity, genetic diversity, and population demographics informs for improved conservation of this species, by delineating three to four conservation units across their Pacific distribution. Implementing such conservation management may be challenging, but is necessary to achieve long-term population resilience at basin and regional scales.

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.

First tiger shark Galeocerdo cuvier bite in 75 years in French Polynesia (Eastern Central Pacific).

We analyzed a tiger shark (estimated 2.8 m total length) bite on a snorkeler. The removal of the terminal part of the leg suggests a predatory motivation for the bite. This is the first documented bite by a tiger shark in French Polynesia waters for the past 75 years.

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.

Suspected predatory bites on a snorkeler by an oceanic whitetip shark Carcharhinus longimanus off Moorea island (French Polynesia).

Understanding why sharks bite humans is essential for developing strategies to prevent these incidents. Here, we use bite wound characteristics and eye witness descriptions of shark behavior to determine the likely motivation for several bites perpetrated by an oceanic whitetip (OWT) shark Carcharhinus longimanus on an adult female snorkeler off Moorea island (French Polynesia) in October 2019. The victim was snorkeling with others in pelagic waters as part of an organized whale-watching tour when the shark-without any warning behavior-bit her at least three times resulting in severe injuries with substantial loss of soft tissue from the chest and both forearms. The victim survived these injuries thanks to rapid and effective first aid provided by her companions. The sudden, unprovoked and repeated bites with substantial tissue removal are consistent with predatory behavior although the dominance hypothesis cannot be fully ruled out. This would be the first case of a predatory shark bite ever documented in French Polynesia in over 70 years of data collection. Given the routine association of OWT sharks with cetaceans, in-water whale watching activities should adopt appropriate risk management strategies in regions hosting this species of shark.

Similar circling movements observed across marine megafauna taxa.

Advances in biologging technology have enabled 3D dead-reckoning reconstruction of marine animal movements at spatiotemporal scales of meters and seconds. Examining high-resolution 3D movements of sharks (Galeocerdo cuvier, N = 4; Rhincodon typus, N = 1), sea turtles (Chelonia mydas, N = 3), penguins (Aptenodytes patagonicus, N = 6), and marine mammals (Arctocephalus gazella, N = 4; Ziphius cavirostris, N = 1), we report the discovery of circling events where animals consecutively circled more than twice at relatively constant angular speeds. Similar circling behaviors were observed across a wide variety of marine megafauna, suggesting these behaviors might serve several similar purposes across taxa including foraging, social interactions, and navigation.

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.

Coral reef grazer-benthos dynamics complicated by invasive algae in a small marine reserve.

Blooms of alien invasive marine algae have become common, greatly altering the health and stability of nearshore marine ecosystems. Concurrently, herbivorous fishes have been severely overfished in many locations worldwide, contributing to increases in macroalgal cover. We used a multi-pronged, interdisciplinary approach to test if higher biomass of herbivorous fishes inside a no-take marine reserve makes this area more resistant to invasive algal overgrowth. Over a two year time period, we (1) compared fish biomass and algal cover between two fished and one unfished patch reef in Hawai'i, (2) used acoustic telemetry to determine fidelity of herbivorous fishes to the unfished reef, and (3) used metabarcoding and next-generation sequencing to determine diet composition of herbivorous fishes. Herbivore fish biomass was significantly higher in the marine reserve compared to adjacent fished reefs, whereas invasive algal cover differed by species. Herbivorous fish movements were largely confined to the unfished patch reef where they were captured. Diet analysis indicated that the consumption of invasive algae varied among fish species, with a high prevalence of comparatively rare native algal species. Together these findings demonstrate that the contribution of herbivores to coral reef resilience, via resistance to invasive algae invasion, is complex and species-specific.

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.

Unexpected Positive Buoyancy in Deep Sea Sharks, Hexanchus griseus, and a Echinorhinus cookei.

We do not expect non air-breathing aquatic animals to exhibit positive buoyancy. Sharks, for example, rely on oil-filled livers instead of gas-filled swim bladders to increase their buoyancy, but are nonetheless ubiquitously regarded as either negatively or neutrally buoyant. Deep-sea sharks have particularly large, oil-filled livers, and are believed to be neutrally buoyant in their natural habitat, but this has never been confirmed. To empirically determine the buoyancy status of two species of deep-sea sharks (bluntnose sixgill sharks, Hexanchus griseus, and a prickly shark, Echinorhinus cookei) in their natural habitat, we used accelerometer-magnetometer data loggers to measure their swimming performance. Both species of deep-sea sharks showed similar diel vertical migrations: they swam at depths of 200-300 m at night and deeper than 500 m during the day. Ambient water temperature was around 15°C at 200-300 m but below 7°C at depths greater than 500 m. During vertical movements, all deep-sea sharks showed higher swimming efforts during descent than ascent to maintain a given swimming speed, and were able to glide uphill for extended periods (several minutes), indicating that these deep-sea sharks are in fact positively buoyant in their natural habitats. This positive buoyancy may adaptive for stealthy hunting (i.e. upward gliding to surprise prey from underneath) or may facilitate evening upward migrations when muscle temperatures are coolest, and swimming most sluggish, after spending the day in deep, cold water. Positive buoyancy could potentially be widespread in fish conducting daily vertical migration in deep-sea habitats.

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.

The shark assemblage at French Frigate Shoals atoll, Hawai'i: species composition, abundance and habitat use.

Empirical data on the abundance and habitat preferences of coral reef top predators are needed to evaluate their ecological impacts and guide management decisions. We used longline surveys to quantify the shark assemblage at French Frigate Shoals (FFS) atoll from May to August 2009. Fishing effort consisted of 189 longline sets totaling 6,862 hook hours of soak time. A total of 221 sharks from 7 species were captured, among which Galapagos (Carcharhinus galapagensis, 36.2%), gray reef (Carcharhinus amblyrhynchos, 25.8%) and tiger (Galeocerdo cuvier, 20.4%) sharks were numerically dominant. A lack of blacktip reef sharks (Carcharhinus melanopterus) distinguished the FFS shark assemblage from those at many other atolls in the Indo-Pacific. Compared to prior underwater visual survey estimates, longline methods more accurately represented species abundance and composition for the majority of shark species. Sharks were significantly less abundant in the shallow lagoon than adjacent habitats. Recaptures of Galapagos sharks provided the first empirical estimate of population size for any Galapagos shark population. The overall recapture rate was 5.4%. Multiple closed population models were evaluated, with Chao M(h) ranking best in model performance and yielding a population estimate of 668 sharks with 95% confidence intervals ranging from 289-1720. Low shark abundance in the shallow lagoon habitats suggests removal of a small number of sharks from the immediate vicinity of lagoonal islets may reduce short-term predation on endangered monk seal (Monachus schauinslandi) pups, but considerable fishing effort would be required to catch even a small number of sharks. Additional data on long-term movements and habitat use of sharks at FFS are required to better assess the likely ecological impacts of shark culling.