Inferred global connectivity of whale shark Rhincodon typus populations

Ten years have passed since the last synopsis of whale shark Rhincodon typus biogeography. While a recent review of the species' biology and ecology summarized the vast data collected since then, it is clear that information on population geographic connectivity, migration and demography of R. typus is still limited and scattered. Understanding R. typus migratory behaviour is central to its conservation management considering the genetic evidence suggesting local aggregations are connected at the generational scale over entire ocean basins. By collating available data on sightings, tracked movements and distribution information, this review provides evidence for the hypothesis of broad‐scale connectivity among populations, and generates a model describing how the world's R. typus are part of a single, global meta‐population. Rhincodon typus occurrence timings and distribution patterns make possible a connection between several aggregation sites in the Indian Ocean. The present conceptual model and validating data lend support to the hypothesis that R. typus are able to move among the three largest ocean basins with a minimum total travelling time of around 2–4 years. The model provides a worldwide perspective of possible R. typus migration routes, and suggests a modified focus for additional research to test its predictions. The framework can be used to trim the hypotheses for R. typus movements and aggregation timings, thereby isolating possible mating and breeding areas that are currently unknown. This will assist endeavours to predict the longer‐term response of the species to ocean warming and changing patterns of human‐induced mortality.     

Population structure of a whale shark Rhincodon typus aggregation in the Red Sea

The presence of whale sharks Rhincodon typus were recorded around Shib Habil, a small, coastal reef off the Red Sea coast of Saudi Arabia, from 2010 to 2015. A total of 267 suitable photographs resulting in the identification of 136 individuals, were documented from 305 encounters. Sharks were divided evenly between the sexes with no evidence of temporal or spatial segregation. All individuals were immature based on size estimates and, for males, juvenile clasper morphology. Scars were reported for 57% of R. typus with 15% showing evidence of propeller trauma. Estimates of population size and patterns of residency were calculated by modelling the lagged identification rate. Multiple models were run simultaneously and compared using the Akaike information criterion. An open population model was found to best represent the data and estimates a daily abundance between 15 and 34 R. typus during the aggregation season, with local residence times ranging from 4 to 44 days. Residence times away from Shib Habil range from 15 to 156 days with a permanent emigration–death rate between 0·07 and 0·58 individuals year^?1. These results are broadly similar to those from other aggregations of R. typus, although the observed sexual parity and integration found at this site is unique for the species and needs further study.     

Population genetic structure of Earth's largest fish, the whale shark (Rhincodon typus)

Large pelagic vertebrates pose special conservation challenges because their movements generally exceed the boundaries of any single jurisdiction. To assess the population structure of whale sharks (Rhincodon typus), we sequenced complete mitochondrial DNA control regions from individuals collected across a global distribution. We observed 51 single site polymorphisms and 8 regions with indels comprising 44 haplotypes in 70 individuals, with high haplotype (h = 0.974 +/- 0.008) and nucleotide diversity (pi = 0.011 +/- 0.006). The control region has the largest length variation yet reported for an elasmobranch (1143-1332 bp). Phylogenetic analyses reveal no geographical clustering of lineages and the most common haplotype was distributed globally. The absence of population structure across the Indian and Pacific basins indicates that oceanic expanses and land barriers in Southeast Asia are not impediments to whale shark dispersal. We did, however, find significant haplotype frequency differences (AMOVA, Phi(ST) = 0.107, P < 0.001) principally between the Atlantic and Indo-Pacific populations. In contrast to other recent surveys of globally distributed sharks, we find much less population subdivision and no evidence for cryptic evolutionary partitions. Discovery of the mating and pupping areas of whale sharks is key to further population genetic studies. The global pattern of shared haplotypes in whale sharks provides a compelling argument for development of broad international approaches for management and conservation of Earth's largest fish.     

Segregation and foraging ecology of whale sharks, Rhincodon typus, in the southwestern Gulf of California

Sharks segregate by sex and size, but few studies have attempted to explain such behaviors. To address this, we examined aggregations and the foraging ecology of whale sharks in Bahía de La Paz (BLP) with aerial and ship surveys and direct observation. Zooplankton abundance and composition, and hydrographic conditions were analyzed in relation to whale shark occurrence to explore underlying factors causing segregations. We observed large aggregations of juveniles (<9 m total length, TL) inshore, comprised by 60 % male individuals, and small aggregations of adults (>9 m TL) offshore, composed of 84 % females. Juvenile sharks were associated to turbid shallow waters in BLP, where they performed stationary and dynamic suction feeding on dense copepod swarms. Adults occurred in oceanic waters and fed by ram-filtering on diffuse patches of euphausiids, with no association to oceanographic conditions. Such segregation may be advantageous to juvenile R. typus utilizing shallow coastal waters to find abundant preferred prey needed for their fast growth rates. Our studies suggest that the main driving forces of whale shark segregation by sex and size in BLP may be diet preference for juveniles and habitat preference for adult sharks.     

Patterns in composition, abundance and scarring of whale sharks Rhincodon typus near Holbox Island, Mexico

Photo-identification and conventional tagging were used to estimate population size and structure of the whale shark Rhincodon typus near Holbox Island, Mexico. From 2005 to 2008, photographs of spot patterns behind the last gill slit and in a lateral view on the left side of each animal were used to identify individuals. Additionally, 578 R. typus were tagged using conventional marker tags. Of these and the 350 R. typus that were identified from 1184 photographs, 65% were male; 27%, female and 8%, indeterminate sex. Photographed R. typus ranged in size from 2·5 to 9·5 m total length. Size was bimodal with a large peak at 6 m and a smaller peak at 7 m. Photo-identification showed that there was considerable loss of marker tags. Few of these remained on the animals for more than a year, so that interannual re-sights using tagging could not be used in population modelling. Forty six interannual re-sightings were found in the photographic library; the interval between these re-sightings was typically 1 year. It was estimated that the R. typus aggregation near Holbox Island ranged from 521 to 809 individuals, based on mark-recapture models. From 13 to 33% of R. typus photographed had scars that were attributable to boat strikes. This study provides a baseline for assessing the status of R. typus near Holbox Island. This information is useful to understand drivers of local population size and distribution and potential concerns about increasing effects of tourism on R. typus in this area and for designing better management programmes for R. typus conservation.     

Young whale sharks, Rhincodon typus, feeding on a copepod bloom near La Paz, Mexico

Seven small (3.2 to 5.2 m total length) whale sharks were observed suction feeding on patches of surface plankton in the Bay of La Paz within 1 km of shore and 2 km N of the phosphate dock at San Juan de la Costa, on 1–2 November 1993. The sharks were photographed and videotaped from the boat and by snorkelers in the water. When actively feeding the shark turned its head from side to side, part of the head was lifted out of the water, and the mouth opened and closed 7 to 28 times per minute (x=17, N=13). These suction gulps were synchronized with the opening and closing of the gill slits. This feeding behavior occurred only in the patchy areas of densely cloudy water, a layer 10 to 30 cm thick at the surface containing an immense concentration of copepods, 95% of which were identified as Acartia clausi. Remoras accompanying the whale sharks also fed on the plankton bloom. This revised version was published online in July 2006 with corrections to the Cover Date.     

An unprecedented aggregation of whale sharks, Rhincodon typus, in Mexican coastal waters of the Caribbean Sea

Whale sharks, Rhincodon typus, are often perceived as solitary behemoths that live and feed in the open ocean. To the contrary, evidence is accumulating that they are gregarious and form seasonal aggregations in some coastal waters. One such aggregation occurs annually north of Cabo Catoche, off Isla Holbox on the Yucatán Peninsula of Mexico. Here we report a second, much denser aggregation of whale sharks (dubbed "the Afuera") that occurs east of the tip of the Yucatán Peninsula in the Caribbean Sea. The 2009 Afuera event comprised the largest aggregation of whale sharks ever reported, with up to 420 whale sharks observed in a single aerial survey, all gathered in an elliptical patch of ocean approximately 18 km(2). Plankton studies indicated that the sharks were feeding on dense homogenous patches of fish eggs, which DNA barcoding analysis identified as belonging to little tunny, Euthynnus alletteratus. This contrasts with the annual Cabo Catoche aggregation nearby, where prey consists mostly of copepods and sergestid shrimp. Increased sightings at the Afuera coincide with decreased sightings at Cabo Catoche, and both groups have the same sex ratio, implying that the same animals are likely involved in both aggregations; tagging data support this idea. With two whale shark aggregation areas, high coastal productivity and a previously-unknown scombrid spawning ground, the northeastern Yucatán marine region is a critical habitat that deserves more concerted conservation efforts.     

Regional movements of satellite‐tagged whale sharks Rhincodon typus in the Gulf of Aden

To gain insight into whale shark (Rhincodon typus) movement patterns in the Western Indian Ocean, we deployed eight pop‐up satellite tags at an aggregation site in the Arta Bay region of the Gulf of Tadjoura, Djibouti in the winter months of 2012, 2016, and 2017. Tags revealed movements ranging from local‐scale around the Djibouti aggregation site, regional movements along the coastline of Somaliland, movements north into the Red Sea, and a large‐scale (>1,000 km) movement to the east coast of Somalia, outside of the Gulf of Aden. Vertical movement data revealed high occupation of the top ten meters of the water column, diel vertical movement patterns, and deep diving behavior. Long‐distance movements recorded both here and in previous studies suggest that connectivity between the whale sharks tagged at the Djibouti aggregation and other documented aggregations in the region are likely within annual timeframes. In addition, wide‐ranging movements through multiple nations, as well as the high use of surface waters recorded, likely exposes whale sharks in this region to several anthropogenic threats, including targeted and bycatch fisheries and ship‐strikes. Area‐based management approaches focusing on seasonal hotspots offer a way forward in the conservation of whale sharks in the Western Indian Ocean.     

Acoustic telemetry reveals cryptic residency of whale sharks

Although whale sharks (Rhincodon typus) have been documented to move thousands of kilometres, they are most frequently observed at a few predictable seasonal aggregation sites. The absence of sharks at the surface during visual surveys has led to the assumption that sharks disperse to places unknown during the long ‘off-seasons’ at most of these locations. Here we compare 2 years of R. typus visual sighting records from Mafia Island in Tanzania to concurrent acoustic telemetry of tagged individuals. Sightings revealed a clear seasonal pattern with a peak between October and February and no sharks observed at other times. By contrast, acoustic telemetry demonstrated year-round residency of R. typus. The sharks use a different habitat in the off-season, swimming deeper and further away from shore, presumably in response to prey distributions. This behavioural change reduces the sharks'' visibility, giving the false impression that they have left the area. We demonstrate, for the first time to our knowledge, year-round residency of unprovisioned, individual R. typus at an aggregation site, and highlight the importance of using multiple techniques to study the movement ecology of marine megafauna.     

Observations of stranded and swimming whale sharks Rhincodon typus in Khor Al-Zubair,NW Arabian Gulf and Shatt Al-Arab Estuary,Iraq

This study is the first record of a whale shark Rhincodon typus in Iraqi waters and the second record from the Arabian (Persian) Gulf portion of the north-west Indian Ocean. The stranding and sighting events were documented by photos of three individuals: the stranded specimen was 6.5 m total length (L_T) and the free-swimming individuals were c. 1–2 and 2–3 m L_T respectively_. An appeal is made for Iraqi policy makers to participate in regional and international organizations for the conservation of this endangered species.     

Distribution and feeding habitat characterization of whale sharks Rhincodon typus in a protected area in the north Caribbean Sea

The relationship between the distribution of the whale shark Rhincodon typus and hydrobiological variables in the Caribbean Sea during 2005–2009 was analysed. Monthly trips were made to the R. typus aggregation area during the months when this species is present in the region (May to September) to record sightings and hydrological data and to collect samples to determine nutrients, chlorophyll a (Chl a) and zooplankton biomass. A total of 2104 R. typus were counted and three zones of high abundance were identified: Cabo‐Catoche, Contoy (both within the Whale Shark Biosphere Reserve, WSBR) and the zone knows as Afuera. The zones of greatest R. typus density within the WSBR were characterized by high Chl a concentrations (median: 1·1 mg m^?3, interpercentile range: 0·5–1·8 mg m^?3) and high nutrient concentrations, such as ammonium (median: 2·5 µmol l^?1, interpercentile range: 0·5–6·4 µmol l^?1), due to the influence of local upwelling. A generalized additive model (GAM) was used to explore the relationship between R. typus distribution and the environmental variables inside WSBR. Zooplankton biomass was the most influential environmental variable, supporting the close relationship between R. typus distribution and biological productivity. Copepods were the dominant zooplankton group within the WSBR. In the Afuera zone, there were large R. typus aggregations (>80 individuals) associated with zooplankton dominated by fish eggs and significantly higher mean ± s.d. biomass (3356·1 ± 1960·8 mg m^?3) compared with that recorded inside the WSBR (103·5 ± 57·2 mg m^?3). The differences among zones generated changes in R. typus distribution patterns and provided opportunities to develop local management strategies for this species.     

Fisheries, management and conservation of the whale shark Rhincodon typus in Taiwan

The Taiwanese government introduced a catch-and-report system for the whale shark Rhincodon typus in 2001, and in the following year limited the total allowable catch (TAC) to 80 individuals. This limit was reduced over the following years, reaching a low of 30 individuals in 2007. In November 2007, a comprehensive ban on R. typus fishing came into effect and protection measures were adopted for the species. This study measured and recorded the total length (L(T) ), body mass and sex of 810 R. typus, using fisheries and other released data for the period 1995-2008. The mean L(T) of individuals caught from June to October was smaller than that for individuals caught from November to May. Mean annual catches in set nets were higher in south-western Taiwan than in other regions of Taiwan. The sex ratio showed that males were caught more frequently than females in Taiwanese waters, indicating sex segregation. For the first time, the stock structure, conservation and management regulation of R. typus in the north-west Pacific Ocean have been reviewed. The results provide a useful resource for future assessment of the possible development of R. typus ecotourism in Taiwan.     

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 1.2 mm 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 1.1 m/s with 85% of the open mouth below the water's surface. Sharks on average spent approximately 7.5 h/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 m³/h, and a 622 cm TL shark 614 m³/h. With an average plankton biomass of 4.5 g/m³ 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.     

A review of the biology, fisheries and conservation of the whale shark Rhincodon typus

Although the whale shark Rhincodon typus is the largest extant fish, it was not described until 1828 and by 1986 there were only 320 records of this species. Since then, growth in tourism and marine recreation globally has lead to a significant increase in the number of sightings and several areas with annual occurrences have been identified, spurring a surge of research on the species. Simultaneously, there was a great expansion in targeted R. typus fisheries to supply the Asian restaurant trade, as well as a largely un-quantified by-catch of the species in purse-seine tuna fisheries. Currently R. typus is listed by the IUCN as vulnerable, due mainly to the effects of targeted fishing in two areas. Photo-identification has shown that R. typus form seasonal size and sex segregated feeding aggregations and that a large proportion of fish in these aggregations are philopatric in the broadest sense, tending to return to, or remain near, a particular site. Somewhat conversely, satellite tracking studies have shown that fish from these aggregations can migrate at ocean-basin scales and genetic studies have, to date, found little graphic differentiation globally. Conservation approaches are now informed by observational and environmental studies that have provided insight into the feeding habits of the species and its preferred habitats. Notwithstanding these advances, there remain notable gaps in the knowledge of this species particularly with respect to the life history of neonates and adults who are not found in the feeding aggregations.     

The first record,tagging and release of a neonatal whale shark Rhincodon typus in Taiwan

On 27 October 2013, a Rhincodon typus was apparently chased by a group of Caranx ignobilis into nearshore waters near Green Island (Ludao), east of Taiwan. A fisherman brought it back to port where it was kept in a small sea pen until release. The R. typus was 78 cm total length, and was tagged and released on 29 October 2013.     

Isolation and characterization of microsatellite loci in the whale shark (Rhincodon typus)

In preparation for a study on population structure of the whale shark (Rhincodon typus), nine species-specific polymorphic microsatellite DNA markers were developed. An initial screening of 50 individuals from Holbox Island, Mexico found all nine loci to be polymorphic, with two to 17 alleles observed per locus. Observed and expected heterozygosity per locus ranged from 0.200 to 0.826 and from 0.213 to 0.857, respectively. Neither statistically significant deviations from Hardy-Weinberg expectations nor statistically significant linkage disequilibrium between loci were observed. These microsatellite loci appear suitable for examining population structure, kinship assessment and other applications.     

Population structure,spatial distribution and life‐history traits of blacktip reef sharks Carcharhinus melanopterus

During a survey of the population of blacktip reef shark Carcharhinus melanopterus in Moorea (French Polynesia) between 2007 and 2011, population structural characteristics were estimated from 268 individuals. Total length (L_T) ranged from 48 to 139 cm and 48 to 157 cm for males and females, respectively, demonstrating that the average L_T of females was larger than that of males. The C. melanopterus population at Moorea showed an apparent spatial sexual segregation with females preferentially frequenting lagoons and males the fore‐reefs. Mean growth rate was c. 6 cm year^?1. Males reached sexual maturity at 111 cm L_T. This study reports on the population characteristics of this widespread carcharhinid shark species and makes comparisons with other locations, confirming high geographic variability in the population structure of the species.