Global collision-risk hotspots of marine traffic and the world's largest fish, the whale shark.

Marine traffic is increasing globally yet collisions with endangered megafauna such as whales, sea turtles, and planktivorous sharks go largely undetected or unreported. Collisions leading to mortality can have population-level consequences for endangered species. Hence, identifying simultaneous space use of megafauna and shipping throughout ranges may reveal as-yet-unknown spatial targets requiring conservation. However, global studies tracking megafauna and shipping occurrences are lacking. Here we combine satellite-tracked movements of the whale shark, Rhincodon typus, and vessel activity to show that 92% of sharks' horizontal space use and nearly 50% of vertical space use overlap with persistent large vessel (>300 gross tons) traffic. Collision-risk estimates correlated with reported whale shark mortality from ship strikes, indicating higher mortality in areas with greatest overlap. Hotspots of potential collision risk were evident in all major oceans, predominantly from overlap with cargo and tanker vessels, and were concentrated in gulf regions, where dense traffic co-occurred with seasonal shark movements. Nearly a third of whale shark hotspots overlapped with the highest collision-risk areas, with the last known locations of tracked sharks coinciding with busier shipping routes more often than expected. Depth-recording tags provided evidence for sinking, likely dead, whale sharks, suggesting substantial "cryptic" lethal ship strikes are possible, which could explain why whale shark population declines continue despite international protection and low fishing-induced mortality. Mitigation measures to reduce ship-strike risk should be considered to conserve this species and other ocean giants that are likely experiencing similar impacts from growing global vessel traffic.

First insights into the vertical habitat use of the whitespotted eagle ray Aetobatus narinari revealed by pop-up satellite archival tags.

The whitespotted eagle ray Aetobatus narinari is a tropical to warm-temperate benthopelagic batoid that ranges widely throughout the western Atlantic Ocean. Despite conservation concerns for the species, its vertical habitat use and diving behaviour remain unknown. Patterns and drivers in the depth distribution of A. narinari were investigated at two separate locations, the western North Atlantic (Islands of Bermuda) and the eastern Gulf of Mexico (Sarasota, Florida, U.S.A.). Between 2010 and 2014, seven pop-up satellite archival tags were attached to A. narinari using three methods: a through-tail suture, an external tail-band and through-wing attachment. Retention time ranged from 0 to 180 days, with tags attached via the through-tail method retained longest. Tagged rays spent the majority of time (82.85 ± 12.17% S.D.) within the upper 10 m of the water column and, with one exception, no rays travelled deeper than ~26 m. One Bermuda ray recorded a maximum depth of 50.5 m, suggesting that these animals make excursions off the fore-reef slope of the Bermuda Platform. Individuals occupied deeper depths (7.42 ± 3.99 m S.D.) during the day versus night (4.90 ± 2.89 m S.D.), which may be explained by foraging and/or predator avoidance. Each individual experienced a significant difference in depth and temperature distributions over the diel cycle. There was evidence that mean hourly depth was best described by location and individual variation using a generalized additive mixed model approach. This is the first study to compare depth distributions of A. narinari from different locations and describe the thermal habitat for this species. Our study highlights the importance of region in describing A. narinari depth use, which may be relevant when developing management plans, whilst demonstrating that diel patterns appear to hold across individuals.

Androgen receptors in the bonnethead, Sphyrna tiburo: cDNA cloning and tissue-specific expression in the male reproductive tract.

As demonstrated in past studies, androgens appear to play critical roles in regulating reproduction in male sharks. However, little is known about the cell-specific actions of androgens in these fishes. To address this, this study examined androgen targets in reproductive organs of a seasonally reproducing shark, the bonnethead (Sphyrna tiburo). A partial bonnethead AR cDNA clone was isolated and found to exhibit strong homology with known vertebrate ARs. Using RT-PCR and in situ hybridization, AR was found to be expressed in multiple cell types in the male bonnethead testis (premeiotic germ cells, Leydig-like interstitial cells, Sertoli cells, peritubular myoid cells, and mature spermatozoa) and gonadal ducts (stromal cells, luminal epithelial cells, mature spermatozoa). Furthermore, AR expression in these organs was found to vary temporally in relation to the seasonal reproductive cycle. Based on immunocytochemistry, the presence of AR protein in male bonnethead reproductive organs was largely consistent with patterns of AR gene expression with the single exception of mature spermatozoa, which exhibited consistently strong mRNA expression but only inconsistent and weak AR protein immunoreactivity. These results suggest important roles for androgens in regulating germ cell proliferation, hormone production, spermatid elongation, spermiation, and gonadal duct function in male bonnetheads. In addition, high abundance of AR mRNA in bonnethead spermatozoa suggest the potential for de novo protein synthesis following spermiation/copulation and/or a role for AR mRNA in early embryonic development, both of which have been proposed to explain the occurrence of mRNA transcripts in spermatozoa from various vertebrates.

The sexually dimorphic cephalofoil of bonnethead sharks, Sphyrna tiburo.

Sexually dimorphic head shape is common in vertebrates from teleosts to mammals. Herein we document that cephalic sexual dimorphism is also found in the cartilaginous fishes (Chondrichthyes). Male bonnethead sharks develop a prominent bulge along the anterior margin of the cephalofoil at the onset of sexual maturity. This contrasts with the uniformly rounded anterior margin of adult females and juveniles and embryos of both sexes. The anterior cephalic bulge is produced by elongation of the rod-like rostral cartilages, and its appearance corresponds temporally with the elongation of the rod-like cartilages of the male intromittent organs (claspers). We propose that the rostral cartilage elongation is a byproduct of endocrinological changes at the onset of sexual maturity that stimulate growth of the clasper cartilages. The basal location of the chondrichthyan fishes within the vertebrate clade extends the earliest appearance of cephalic sexual dimorphism among the vertebrates.

Vertical Movements and Patterns in Diving Behavior of Whale Sharks as Revealed by Pop-Up Satellite Tags in the Eastern Gulf of Mexico.

The whale shark (Rhincodon typus) is a wide-ranging, filter-feeding species typically observed at or near the surface. This shark's sub-surface habits and behaviors have only begun to be revealed in recent years through the use of archival and satellite tagging technology. We attached pop-up satellite archival transmitting tags to 35 whale sharks in the southeastern Gulf of Mexico off the Yucatan Peninsula from 2003-2012 and three tags to whale sharks in the northeastern Gulf off Florida in 2010, to examine these sharks' long-term movement patterns and gain insight into the underlying factors influencing their vertical habitat selection. Archived data were received from 31 tags deployed on sharks of both sexes with total lengths of 5.5-9 m. Nine of these tags were physically recovered facilitating a detailed long-term view into the sharks' vertical movements. Whale sharks feeding inshore on fish eggs off the northeast Yucatan Peninsula demonstrated reverse diel vertical migration, with extended periods of surface swimming beginning at sunrise followed by an abrupt change in the mid-afternoon to regular vertical oscillations, a pattern that continued overnight. When in oceanic waters, sharks spent about 95% of their time within epipelagic depths (<200 m) but regularly undertook very deep ("extreme") dives (>500 m) that largely occurred during daytime or twilight hours (max. depth recorded 1,928 m), had V-shaped depth-time profiles, and comprised more rapid descents (0.68 m sec-1) than ascents (0.50 m sec-1). Nearly half of these extreme dives had descent profiles with brief but conspicuous changes in vertical direction at a mean depth of 475 m. We hypothesize these stutter steps represent foraging events within the deep scattering layer, however, the extreme dives may have additional functions. Overall, our results demonstrate complex and dynamic patterns of habitat utilization for R. typus that appear to be in response to changing biotic and abiotic conditions influencing the distribution and abundance of their prey.

Horizontal movements, migration patterns, and population structure of whale sharks in the Gulf of Mexico and northwestern Caribbean sea.

Whale sharks, Rhincodon typus, aggregate by the hundreds in a summer feeding area off the northeastern Yucatan Peninsula, Mexico, where the Gulf of Mexico meets the Caribbean Sea. The aggregation remains in the nutrient-rich waters off Isla Holbox, Isla Contoy and Isla Mujeres, Quintana Roo for several months in the summer and then dissipates between August and October. Little has been known about where these sharks come from or migrate to after they disperse. From 2003-2012, we used conventional visual tags, photo-identification, and satellite tags to characterize the basic population structure and large-scale horizontal movements of whale sharks that come to this feeding area off Mexico. The aggregation comprised sharks ranging 2.5-10.0 m in total length and included juveniles, subadults, and adults of both sexes, with a male-biased sex ratio (72%). Individual sharks remained in the area for an estimated mean duration of 24-33 days with maximum residency up to about 6 months as determined by photo-identification. After leaving the feeding area the sharks showed horizontal movements in multiple directions throughout the Gulf of Mexico basin, the northwestern Caribbean Sea, and the Straits of Florida. Returns of individual sharks to the Quintana Roo feeding area in subsequent years were common, with some animals returning for six consecutive years. One female shark with an estimated total length of 7.5 m moved at least 7,213 km in 150 days, traveling through the northern Caribbean Sea and across the equator to the South Atlantic Ocean where her satellite tag popped up near the Mid-Atlantic Ridge. We hypothesize this journey to the open waters of the Mid-Atlantic was for reproductive purposes but alternative explanations are considered. The broad movements of whale sharks across multiple political boundaries corroborates genetics data supporting gene flow between geographically distinct areas and underscores the need for management and conservation strategies for this species on a global scale.

Feeding anatomy, filter-feeding rate, and diet of whale sharks Rhincodon typus during surface ram filter feeding off the Yucatan Peninsula, Mexico.

The feeding anatomy, behavior and diet of the whale shark Rhincodon typus were studied off Cabo Catoche, Yucatan Peninsula, Mexico. The filtering apparatus is composed of 20 unique filtering pads that completely occlude the pharyngeal cavity. A reticulated mesh lies on the proximal surface of the pads, with openings averaging 1.2mm in diameter. Superficial to this, a series of primary and secondary cartilaginous vanes support the pads and direct the water across the primary gill filaments. During surface ram filter feeding, sharks swam at an average velocity of 1.1m/s with 85% of the open mouth below the water's surface. Sharks on average spent approximately 7.5h/day feeding at the surface on dense plankton dominated by sergestids, calanoid copepods, chaetognaths and fish larvae. Based on calculated flow speed and underwater mouth area, it was estimated that a whale shark of 443 cm total length (TL) filters 326 m(3)/h, and a 622 cm TL shark 614 m(3)/h. With an average plankton biomass of 4.5 g/m(3) at the feeding site, the two sizes of sharks on average would ingest 1467 and 2763 g of plankton per hour, and their daily ration would be approximately 14,931 and 28,121 kJ, respectively. These values are consistent with independently derived feeding rations of captive, growing whale sharks in an aquarium. A feeding mechanism utilizing cross-flow filtration of plankton is described, allowing the sharks to ingest plankton that is smaller than the mesh while reducing clogging of the filtering apparatus.