Ocean‐scale prediction of whale shark distribution

Aim Predicting distribution patterns of whale sharks (Rhincodon typus, Smith 1828) in the open ocean remains elusive owing to few pelagic records. We developed multivariate distribution models of seasonally variant whale shark distributions derived from tuna purse‐seine fishery data. We tested the hypotheses that whale sharks use a narrow temperature range, are more abundant in productive waters and select sites closer to continents than the open ocean. Location Indian Ocean. Methods We compared a 17‐year time series of observations of whale sharks associated with tuna purse‐seine sets with chlorophyll a concentration and sea surface temperature data extracted from satellite images. Different sets of pseudo‐absences based on random distributions, distance to shark locations and tuna catch were generated to account for spatiotemporal variation in sampling effort and probability of detection. We applied generalized linear, spatial mixed‐effects and Maximum Entropy models to predict seasonal variation in habitat suitability and produced maps of distribution. Results The saturated generalized linear models including bathymetric slope, depth, distance to shore, the quadratic of mean sea surface temperature, sea surface temperature variance and chlorophyll a had the highest relative statistical support, with the highest percent deviance explained when using random pseudo‐absences with fixed effect‐only models and the tuna pseudo‐absences with mixed‐effects models (e.g. 58% and 26% in autumn, respectively). Maximum Entropy results suggested that whale sharks responded mainly to variation in depth, chlorophyll a and temperature in all seasons. Bathymetric slope had only a minor influence on the presence. Main conclusions Whale shark habitat suitability in the Indian Ocean is mainly correlated with spatial variation in sea surface temperature. The relative influence of this predictor provides a basis for predicting habitat suitability in the open ocean, possibly giving insights into the migratory behaviour of the world’s largest fish. Our results also provide a baseline for temperature‐dependent predictions of distributional changes in the future.     

Feeding habits of the whale shark (<Emphasis Type="Italic">Rhincodon typus</Emphasis>) inferred by fatty acid profiles in the northern Mexican Caribbean

Whale shark (Rhincodon typus, Smith, 1828) is an endangered species with anthropogenic pressures due to increasing demand of encounter tourism activities. Research efforts to identify management and conservation strategies for this species are needed. The Northern Mexican Caribbean is one of the most important feeding aggregation sites of whale sharks worldwide. In this study, Mexican Caribbean whale shark feeding habits are assessed by means of fatty acid (FA) signature analysis, a biochemical non-destructive technique widely applied in trophic ecology studies. Sub-dermal tissue biopsies of 68 whale sharks and samples of their potential prey (zooplankton) were collected during 2010 and 2011 in two areas with high R. typus abundance. Zooplankton samples (n?=?17) were divided in two categories: mixed zooplankton (several groups of zooplankton) and fish eggs (> 95% of sample components were fish eggs). FA profiles of whale shark tissue sampled between years showed significant variability; while there was no intraspecific differences in FA signature related to sex, size and location. FA profiles of whale sharks and their potential prey were dominated by saturated fatty acids (SFA). R. typus FA signature was significantly different from that of mixed zooplankton; on the other hand, whale shark and fish egg FA profiles formed groups with overlapping values and registered high levels of oleic acid. PUFA average ω3/ ω6 ratio on whale shark FA profiles for both years was below 1. Arachidonic acid (ARA) percentage was higher in whale shark biopsies (13.2% in 2010, 6.8% in 2011) compared to values observed in fish eggs (2.0%) and mixed zooplankton (1.4%). Similarity between FA profiles of whale sharks and fish eggs, low levels of bacterial FA found in R. typus biopsies, as well as whale shark feeding behavior observations in the study area, suggest that R. typus is feeding mainly on surface zooplankton in Mexican Caribbean; however, elevated ARA percentages in whale shark samples may indicate that this species has complementary feeding sources, such as demersal zooplankton, which has been reported in other aggregation sites. Results obtained contribute to the knowledge of the whale shark trophic ecology in the area, but are inconclusive. Further studies are recommended to evaluate whale shark FA profiles from different tissues (muscle or blood); also, broader information is needed about zooplankton FA signature in the study area.     

Ensemble modeling of the potential distribution of the whale shark in the Atlantic Ocean

The whale shark (Rhincodon typus) is an endangered marine fish species which can be adversely affected by the fishing activities of the industrial purse seine fleet targeting tropical tuna. Tuna tend to aggregate around all types of floating objects, including whale sharks. We analyzed and modeled the spatial distribution and environmental preferences of whale sharks based on the presence and absence data from fishing observations in the Atlantic Ocean. We used a thorough multialgorithm analysis, based on a new presence–absence dataset, and endeavored to follow the most recent recommendations on best practices in species distribution modeling. First, we selected a subset of relevant variables using a generalized linear model that addressed multicollinearity, statistical errors, and information criteria. We then used the selected variables to build a model ensemble including 19 different algorithms. After eliminating models with insufficient performance, we assessed the potential distribution of whale sharks using the mean of the predictions of the selected models. We also assessed the variance among the predictions of different algorithms, in order to identify areas with the highest model consensus. The results show that several coastal regions and warm shallow currents, such as the Gulf Stream and the Canary and Benguela currents, are the most suitable areas for whale sharks under current environmental conditions. Future environmental projections for the Atlantic Ocean suggest that some of the suitable regions will shift northward, but current concentration areas will continue to be suitable for whale shark, although with less productivity, which could have negative consequences for conservation of the species. We discuss the implications of these predictions for the conservation and management of this charismatic marine species.     

Genetic structure of populations of whale sharks among ocean basins and evidence for their historic rise and recent decline

This study presents genetic evidence that whale sharks, Rhincodon typus, are comprised of at least two populations that rarely mix and is the first to document a population expansion. Relatively high genetic structure is found when comparing sharks from the Gulf of Mexico with sharks from the Indo‐Pacific. If mixing occurs between the Indian and Atlantic Oceans, it is not sufficient to counter genetic drift. This suggests whale sharks are not all part of a single global metapopulation. The significant population expansion we found was indicated by both microsatellite and mitochondrial DNA. The expansion may have happened during the Holocene, when tropical species could expand their range due to sea‐level rise, eliminating dispersal barriers and increasing plankton productivity. However, the historic trend of population increase may have reversed recently. Declines in genetic diversity are found for 6 consecutive years at Ningaloo Reef in Australia. The declines in genetic diversity being seen now in Australia may be due to commercial‐scale harvesting of whale sharks and collision with boats in past decades in other countries in the Indo‐Pacific. The study findings have implications for models of population connectivity for whale sharks and advocate for continued focus on effective protection of the world's largest fish at multiple spatial scales.     

Habitat suitability of Rhincodon typus in three localities of the Gulf of California: Environmental drivers of seasonal aggregations

The whale shark is an endangered species that usually feeds in coastal areas of highly productive seas such as the Gulf of California, Mexico. This study aims to describe the effect of sea surface temperature, chlorophyll a, bathymetry and slope on the habitat suitability of whale sharks in three important aggregation sites of the Gulf of California. A total of 2396 records of occurrence of whale sharks were obtained from international databases and scientific literature between 1996 and 2018. These records were used for the creation of a species distribution model using MaxEnt for each of the three aggregation sites. The concentration of chlorophyll a explained 71% of the habitat suitability, followed by bathymetry and slope with a combined 17%, and sea surface temperature constituting 10% of the model. Habitat suitability was related to areas where nontargeted fisheries may impact whale sharks through bycatch, entanglement and ship strikes. The implications for the conservation of whale sharks should be considered for management decisions in terms of marine protected areas, fishing refugees or bans, and other regulations regarding fisheries activities.     

Whale sharks Rhincodon typus get cleaned by the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in the Philippines

Cleaning interactions are essential for healthy marine ecosystem communities. This study reports the first documentation of the whale shark Rhincodon typus cleaning behaviour in the Indo-West Pacific by two wrasse species, the blue-streak cleaner wrasse Labroides dimidiatus and the moon wrasse Thalassoma lunare in Cebu, Philippines. This study documented 36 cleaning interactions with 14 individual whale sharks. The cleaning interactions appear opportunistic rather than targeted by the sharks, unlike that observed in other species of elasmobranchs. Further work should focus on understanding the drivers of these unique cleaning interactions.     

White Sharks (Carcharodon carcharias) Scavenging on Whales and Its Potential Role in Further Shaping the Ecology of an Apex Predator

Scavenging, a result of a temporary pulse of resources, occurs in virtually all ecosystems containing carnivores, and is an important energy transfer pathway that can impact ecosystem structure and function, and this ecological significance has largely been considered from a terrestrial standpoint; however, little is known about the role of scavenging in shaping the behavioral ecology of marine species, specifically apex predators. Here we present findings from multiple opportunistic observations of white sharks scavenging on whale carcasses in False Bay, South Africa. Observations of white sharks scavenging over successive days provided evidence of strategic and selective scavenging by this species. Moreover, extended daily observations permitted recordings of unique social, aggregative, and feeding behaviors. We further compare these data against observations of natural predation by sharks on seals in the study area. We discuss these data in relation to environmental conditions, shark social interactions, migration patterns, whale biology, and behaviorally-mediated trophic cascades. While the appearance of a whale carcass is largely a stochastic event, we propose that white shark scavenging on whales may represent an underestimated, yet significant component to the overall foraging ecology of this species, especially as individuals attain sexual maturity.     

Scarring patterns and relative mortality rates of Indian Ocean whale sharks

This study recorded the scarring rate and severity for whale sharks Rhincodon typus from three Indian Ocean aggregations (Australia, Seychelles and Mozambique), and examined whether scarring (mostly attributed to boat strikes and predator attacks) influences apparent survival rates using photo‐identification libraries. Identifications were based on spot‐and‐stripe patterns that are unique to individual whale sharks. Scarring was most prevalent in the Seychelles aggregation (67% of individuals). Predator bites were the most frequent source of scarring (aside from minor nicks and abrasions) and 27% of individuals had scars consistent with predator attacks. A similar proportion of whale sharks had blunt trauma, laceration and amputation scars, the majority of which appeared to be caused by ship collisions. Predator bites were more common (44% of individuals) and scars from ship collisions were less common at Ningaloo Reef than at the other two locations (probability of among‐site differences occurring randomly = 0·0007 based on a randomized multinomial contingency analysis). In all aggregations, scars occurred most often on the caudal fin, which may result from the fin being the body part closest to the surface when boats pass over, or they may provide a large target for predator attack. No evidence was found for an effect of scarring on apparent survival (φ; mean ±s .e .) for the Ningaloo (not scarred φ= 0·858 ± 0·033; scarred φ= 0·929 ± 0·033) or Seychelles populations (not scarred φ= 0·502 ± 0·060; scarred φ= 0·538 ± 0·070). The lower apparent survival of the Seychelles population may be attributed to a high number of transient whale sharks in this aggregation that might bias estimates. This study indicates that while scarring from natural predators and smaller vessels appears to be unrelated to whale shark survival, the effect of deaths related to ship strike need to be quantified to assist in future management of this species.     

Movement Patterns of Juvenile Whale Sharks Tagged at an Aggregation Site in the Red Sea

Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009–2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5–7 m total length with a sex ratio of approximately 1∶1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.     

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.     

The Seasonal Aggregation of Whale Sharks at Ningaloo Reef, Western Australia: Currents, Migrations and the El Niño/ Southern Oscillation

Whale sharks, Rhincodon typus, seasonally aggregate in coastal waters off Ningaloo Reef, Western Australia. We review the oceanographic setting of the region and present evidence that such aggregations form as a result of migratory behavior associated with climatic and oceanographic processes. We utilise records of whale shark abundance collected at Ningaloo Reef from dedicated searches by boat and aircraft and from log sheets recorded by the tourism industry. Measures of whale shark abundance derived from log sheet data sets were moderately correlated with the Southern Oscillation Index and weakly correlated with coastal sea level, an index of the strength of the Leeuwin Current, and sea surface temperature over the period 1993 to 1998. Abundances of whale sharks derived from boat searches from 1983 to 1992 were also correlated with fluctuations in the Southern Oscillation Index, except during a three year period from 1988 to 1990. We conclude that, at least in some years, there appears to be a link between the abundance of aggregating whale sharks and the physical and biological oceanography of the region, with greater whale shark numbers in La Niña years. The lack of correlation in other years may be due to a combination of uneven quality of data and/or aggregations occurring in response to a complex interaction between the physical and biological oceanography of the region.     

Stable isotope profiles in whale shark (<Emphasis Type="Italic">Rhincodon typus</Emphasis>) suggest segregation and dissimilarities in the diet depending on sex and size

We investigated the sex- and size-related differences in the diet of whale sharks from the Arabian Sea (north-western Indian Ocean) using carbon and nitrogen stable-isotope analyses in white muscle. The samples were collected during the commercial fishing season between April and May of 2001 in Veraval (Gujarat, India). The overall isotope signature was similar to that of the pelagic-neritic zooplanktivore Ilisha melastoma, which suggests that both species are feeding on similar prey. In whale sharks, a positive relationship was found between δ¹⁵N and δ¹³C. This, together with a significant enrichment of both heavy stable isotopes with total length indicates that the contribution to the diet of small fish and/or larger zooplankton of higher trophic level increases with the movement from offshore areas to coastal areas as they grow. Gender differences in the isotopic ratios were not statistically significant, but small sample size cannot rule out completely the existence of some degree of spatial or dietary segregation between sexes.     

Recent strandings and sightings of whale sharks in South Africa

Available information on whale shark strandings around the coast of South Africa during the period 1984–1995 was collated. Stranded animals ranged in size from 3–11 m TL, most were immature and the sex ratio was even. Aerial observations and sightings by divers indicate that whale sharks are most abundant in South African waters during the austral summer and autumn months. This revised version was published online in July 2006 with corrections to the Cover Date.     

Whale killers: Prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia

Reports of killer whales (Orcinus orca) preying on large whales have been relatively rare, and the ecological significance of these attacks is controversial. Here we report on numerous observations of killer whales preying on neonate humpback whales (Megaptera novaeangliae) off Western Australia (WA) based on reports we compiled and our own observations. Attacking killer whales included at least 19 individuals from three stable social groupings in a highly connected local population; 22 separate attacks with known outcomes resulted in at least 14 (64%) kills of humpback calves. We satellite‐tagged an adult female killer whale and followed her group on the water for 20.3 h over six separate days. During that time, they attacked eight humpback calves, and from the seven known outcomes, at least three calves (43%) were killed. Overall, our observations suggest that humpback calves are a predictable, plentiful, and readily taken prey source for killer whales and scavenging sharks off WA for at least 5 mo/yr. Humpback “escorts” vigorously assisted mothers in protecting their calves from attacking killer whales (and a white shark, Carcharodon carcharias). This expands the purported role of escorts in humpback whale social interactions, although it is not clear how this behavior is adaptive for the escorts.     

To go or not to go with the flow: Environmental influences on whale shark movement patterns

Seven whale sharks were tracked using satellite-linked tags from Ningaloo Reef, off northern Western Australia, following tagging in April and June 2002 and April-May 2005. We investigated how the movements of those whale shark tracks were influenced by geostrophic surface currents during sequential one-week periods by using a passive diffusion model parameterised with observed starting locations of the sharks and weekly maps of surface current velocity and direction (derived from altimetry). We compared the outputs from the passive diffusion model and maps of chlorophyll-a concentration (SeaWiFs/MODIS) and with the actual tracks of the sharks using GIS and generalized linear mixed-effects models (GLMM). The GLMM indicated very little support for passive diffusion with sea-surface ocean currents influencing whale shark distributions in the north eastern Indian Ocean. Moreover, the sharks' movements correlated only weakly with the spatial distribution of sea-surface chlorophyll-a concentrations. The seven whale sharks had average swimming speeds comparable with those recorded in other satellite tracking studies of this species. Swimming speeds of the seven sharks were similar to those reported in previous studies and up to three times greater than the maximum sea-surface current velocities that the sharks encountered while traversing into lower southerly latitudes (moving northward towards the equator). Our results indicate that whale sharks departing from Ningaloo travel actively and independently of near-surface currents where they spend most of their time despite additional metabolic costs of this behaviour.     

Multi-Year Impacts of Ecotourism on Whale Shark (Rhincodon typus) Visitation at Ningaloo Reef,Western Australia

In-water viewing of sharks by tourists has become a popular and lucrative industry. There is some concern that interactions with tourists with ecotourism operations might harm sharks through disruption of behaviours. Here, we analysed five years of whale shark (Rhincodon typus) encounter data by an ecotourism industry at Ningaloo Reef, Western Australia, to assess the impact of ecotourism interactions on shark visitation, within the context of the biological and physical oceanography of the region. Our data base consisted of 2823 encounter records for 951 individual whale sharks collected by ecotourism operators between 2007 and 2011. We found that total encounters per whale shark and encounters per boat trip increased through time. On average, whale sharks re-encountered in subsequent years were encountered earlier, stayed longer and tended to be encountered more often within a season than sharks that were only encountered in a single year. Sequential comparisons between years did not show any patterns consistent with disturbance and the rate of departure of whale sharks from the aggregation was negatively correlated to the number of operator trips. Overall, our analysis of this multi-year data base found no evidence that interactions with tourists affected the likelihood of whale shark re-encounters and that instead, physical and biological environmental factors had a far greater influence on whale shark visitation rates. Our approach provides a template for assessing the effects of ecotourism interactions and environmental factors on the visitation patterns of marine megafauna over multiple years.     

A review of the biology and ecology of the whale shark

The information available on the biology and ecology of the whale shark is reviewed, and is updated from material published since 1986. Research work carried out on the seasonal aggregation of whale sharks at the Ningaloo Reef in Western Australia is summarized. Future research studies on whale sharks in the Ningaloo Marine Park are discussed in the context of management of sustainable whale shark interaction tourism.     

Oceanographic and atmospheric phenomena influence the abundance of whale sharks at Ningaloo Reef, Western Australia

Seasonal observations of whale shark abundance recorded by ecotourist operators at Ningaloo Reef, Western Australia from 1999 to 2004 were compared with weekly regional and global oceanographic and atmospheric variables, including average sea surface temperatures, along-shelf wind shear, sea level and the Southern Oscillation Index (SOI). Estimates of these physical variables were derived from either ground-based data or from remote sensing instruments. A generalised linear mixed-effects modelling (GLMM) approach with random sampling and model simulation was used to determine the relationships between the number of whale sharks and all model variants of the environmental parameters, using information-theoretic weights of evidence to rank models. SOI and wind shear had the most support for explaining the deviance in weekly whale shark abundance at Ningaloo Reef during a season. The SOI and wind shear variables positively influenced whale shark abundance such that more sharks were sighted when the Southern Oscillation was stronger and along-shelf winds were increasingly prevalent. This may reflect changes in the strength of oceanographic processes such as the Leeuwin Current (in response to the Southern Oscillation) and wind/current driven upwelling which may affect the abundance of whale sharks transported to the region and/or the availability of their prey by driving productivity changes.     

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.     

The life and work of Eugenie Clark: devoted to diving and science

Synopsis Eugenie Clark is an ichthyologist with a talent for communicating about marine life. Her life had three principal periods, (1) studies under Charles Breder, Carl Hubbs, Lester Aronson and Myron Gordon, (2) directorship of the Cape Haze Marine Laboratory sponsored by the Vanderbilts, and (3) professorship and inspired teaching at the University of Maryland. Genie proved that sharks have surprising learning abilities and that, contrary to popular opinion, none are vicious killers. During her studies on reproductive behavior, territoriality, and ecology of tropical marine sand-dwelling fishes of the Caribbean and Red seas, among many other phenomena, she discovered the cross-fertilizing hermaphroditeSerranus subligarius, the Moses and peacock soles producing toxins that repel sharks and other predators, and sharks sleeping in underwater caves in Mexico and Japan. She combined a love for swimming and diving with the study of marine fishes - from hard-hat diving and snorkeling to using SCUBA and submersibles. Professor emerita since 1992, she has ridden whale sharks and participated in dives using submersibles to 3 600 m depths. She is a recipient of over 25 honors and awards, participated in 24 television specials, and the current IMAX film on sharks. She is the author of theLady with a Spear andThe Lady and the Sharks which are of considerable popular fame.