Abstract

The unsustainable slaughter of millions of sharks for their fins continues unabated even in EU waters, threatening the survival of several species. Meanwhile, new discoveries about the ecology of the top predators illustrate how much we still have to learn about the life we are about to destroy. Michael Gross reports. The unsustainable slaughter of millions of sharks for their fins continues unabated even in EU waters, threatening the survival of several species. Meanwhile, new discoveries about the ecology of the top predators illustrate how much we still have to learn about the life we are about to destroy. Michael Gross reports. Shark fin soup is a traditional dish in China, but the slaughter of sharks, including endangered species, for their fins is a global problem. This was highlighted in August when a report commissioned by Greenpeace UK revealed that the UK exported 50 tonnes of shark fins over the last two years. Spanish vessels are mostly responsible for the sharks caught in European waters. If they land the catch in UK ports before sending the fins to Spain for further export to Asia, the fins get accounted for as exports by the financial authorities. This explains how the UK ended up exporting £300,000 worth of shark fins in 2017–2018, without having any cultural heritage to excuse the activity. Fins are not the only parts of sharks that end up on our dinner plates, however. Catherine Hobbs of the University of Exeter, UK, and colleagues recently used DNA barcoding to analyse fish products from takeaway fish and chip shops, fishmongers and wholesalers (Sci. Rep. (2019) 9, 1028). They found that the majority of the fish steaks sampled from takeaways could be identified as spiny dogfish (Squalus acanthias), a shark species that is endangered in the Northeast Atlantic and thus illegal to catch. The barcoding alone, however, cannot rule out the possibility that the fish was imported from outside the EU, so more transparency and traceability would be needed all along the supply chain to ensure consumers know what they are eating. The study also included a small number of shark fin products, some of which were also identified as endangered species illegally traded, such as the endangered scalloped hammerhead (Sphyrna lewini). The authors highlight the historic practice of using umbrella terms instead of species names, making it impossible for consumers to make sustainable choices. In the UK, for instance, six different, legally allowed designations can be used for a large number of different shark species. Conservation concerns aside, health issues such as allergies should be reason enough to ensure that consumers can always be sure which species they are buying. DNA barcoding, which has also uncovered fraudulent mislabelling of fish products in previous studies (Curr. Biol. (2012) 22, R73–R76), could help to address these problems if it were applied more widely. As the apex predators of marine ecosystems, sharks are ecologically important, but many are highly vulnerable to human activities (Curr. Biol. (2017) 27, R565–R572). Marine biologists have long warned of the threats they face (Curr. Biol. (2014) 24, R341–R344), but the killing continues and is already affecting the distribution and ecology of many shark species. Together with the skates and rays, they form the subclass of elasmobranchs, which is one of the most endangered groups of vertebrates, as a quarter of its species are threatened with extinction. In December 2018, the international conservation charity ZSL (Zoological Society of London) added a list of cartilaginous fish species (the class of Chondrichthyes, including sharks, rays and chimaera) to its EDGE of Existence programme, which ranks endangered species by a combination of Evolutionarily Distinctiveness (ED) and Global Endangerment (GE), following similar lists for amphibians, birds, corals, mammals and reptiles (Curr. Biol. (2018) 28, R581–R584). The idea behind these rankings is to provide a basis for setting priorities in conservation. Among the species threatened with extinction, the loss of one of the highly distinctive species would hit current biodiversity harder than the extinction of a species that has many close relatives. The top places of the Chondrichthyes list are occupied by four species of sawfish. These are rays with the characteristic tooth-bearing rostrum reminiscent of a saw, which makes them vulnerable to becoming entangled in nets aimed at other species and thus ending up as bycatch. They also have the disadvantages of growing quite large and having a slow life history, making them even more vulnerable to environmental change and external threats.Size matters: The whale shark (Rhincodon typus), the largest fish on our planet, has remained mysterious in many ways. (Photo: EliasSch/Pixabay.)View Large Image Figure ViewerDownload Hi-res image Download (PPT) Leading the field is largetooth sawfish (Pristis pristis), which also holds the record of highest-EDGE score determined so far for any kind of species. The species is critically endangered and highly unique. It occurs in shallow tropical waters. Intriguingly, it can cope with a range of different salinities, and has also been observed in rivers and in Lake Nicaragua. It has been exploited over many centuries — even the Maya had ornaments made of sawfish teeth. In May 2019, ZSL’s EDGE of Existence programme selected conservation researcher Alifa Haque as one of its EDGE Fellows to work with coastal communities in Bangladesh on the conservation of the largetooth sawfish. “The largetooth sawfish is threatened by the sale of its meats in prejudice of having curative properties locally and fins for trade, entanglement of its rostra in gill and demersal trawl nets, and loss of its critical mangrove and coastal native habitats,” Haque explains. “I will be working closely with the local fishers to harness their knowledge and identify critical habitats for the sawfish so we can prioritise areas for its protection and assess fishers barriers for a live release program for future conservation actions.” The highest-ranking sharks on the list are three angel shark species, including the species Squatina squatina. The once widespread angel shark family (Squatinidae) is now considered the second most threatened family of cartilaginous fish, after the sawfish family. Angel sharks typically live in coastal waters as bottom-dwelling camouflaged ambush predators that wait for passing prey. Pressure from fisheries that interact with the seabed and habitat loss from coastal development are threatening these species. In the framework of the Angel Shark Conservation Network (www.angelsharknetwork.com), organisations across the East Atlantic and Mediterranean Sea are working in partnership to safeguard the future of angel sharks across their range. Among the more widely known shark species, the endangered whale shark (Rhincodon typus) weighs in at 17 in the EDGE ranking. With its conspicuous pattern of bright spots reminiscent of a night sky, and as the largest fish species alive, the whale shark is popular with wildlife tourists, yet poorly understood, as we will see below. It is closely followed by two other popular favourites, the endangered great hammerhead (Sphyrna mokarran) and the basking shark (Cetorhinus maximus). Further down the list, the great white shark (Carcharodon carcharias), whose cinematic exploits have ruined the reputations of cartilaginous fish for all eternity, also makes an appearance, although its Red List status is only ‘vulnerable’. As shark enthusiasts and conservationists like to remind us, however, the number of humans killed by sharks in a given year tends to be a single digit, while the number of sharks killed by humans in the same time amounts to millions. Sharks and rays represent one of the deepest branches of the vertebrate phylogenetic tree — they went their separate ways some 400 million years ago, after the invention of jaws, but before the rest of us started to grow skeletons made of bone rather than cartilage. Accordingly, their biology can be quite different from ours. The vertebrate immune system was still in its infancy at that point, and that of sharks has some intriguing differences to ours, including the presence of single-domain antibodies of interest for biotechnology. The incomplete understanding of the life of sharks is bad news for conservation, however, as we insufficiently understand their behaviour, ecological relations, and how they might respond to the ecological crisis we are inflicting on them. Some discoveries made in the last few months may demonstrate how much humans can still learn about sharks. The blue shark (Prionace glauca), for instance, was thought to be limited to foraging in warmer waters near the surface, due to its inability to regulate its body temperature in colder waters. However, Camrin Braun from the Woods Hole Oceanographic Institution (WHOI), USA, and colleagues have tagged 15 blue sharks in the eddy field of the Gulf stream off the east coast of the USA, to enable observation of their whereabouts via satellite (Proc. Natl. Acad. Sci. USA (2019) https://doi.org/10.1073/pnas.1903067116). With extended tracking of these tagged animals, the researchers established that these sharks use a certain type of eddy, the anticyclonic eddy containing water corresponding to the surface temperature, as a climatised path into the biomass-rich twilight zone of the ocean at a depth of between 200 and 1,000 metres. There they used to forage for around an hour before returning to surface waters to warm up again. White sharks, by contrast, are warm blooded and can also use anticyclonic eddies where the water is colder. This finding came as a surprise as the warm anticyclonic eddies had previously been considered a marine desert with little importance for marine ecology. Now they turn out to provide a crucial link between the surface waters and the deeper twilight zone. Some shark species living in deep waters are also known to display biofluorescence, absorbing the ambient blue light and converting it to green light. While such phenomena are well characterised in invertebrates, where the discovery of green fluorescent protein (GFP) in the luminescent hydromedusa Aequorea victoria led to the development of widely used laboratory techniques, there was nothing known about how sharks fluoresce. The groups of David Gruber at City University of New York and Jason Crawford at Yale University, both in the USA, have now analysed the skin of two species of catshark that display green biofluorescence, namely the swell shark (Cephaloscyllium ventriosum) from the east Pacific and the chain catshark (Scyliorhinus retifer) from the western Atlantic, which are both ‘of least concern’ according to the IUCN Red List (iScience (2019) https://doi.org/10.1016/j.isci.2019.07.019). Both have large-scale patterns dividing the skin into lighter and darker areas. In the lighter areas, the researchers discovered a group of small-molecule fluorescent pigments that have never before been associated with biofluorescence, namely the bromo-tryptophan kynurenines. Some variants of these molecules also show antimicrobial properties, raising interesting questions about the biofluorescence, which may have evolved as a by-product of the shark’s defence against microbes. In addition, the authors also discovered denticles in the skin of the chain catshark that can serve as light guides for the luminescence. These surprising discoveries, which may well lead to applications in medicine or biotechnology, illustrate once more how much there is still to learn about sharks. The above-mentioned whale shark, despite its conspicuous size and appearance and its popularity with wildlife spotters, is also too little understood. For instance, there is no reliable data on its population size. The IUCN has listed it as endangered based on the losses due to bycatch and collisions with vessels, combined with small population sizes and the slow life history which tends to make species vulnerable. Even the diet of the world’s largest fish is still subject to debate. Alex Wyatt from the University of Tokyo and colleagues developed a new comprehensive method to calibrate isotope measurements to the diet of a few individuals in captivity (Ecol. Monogr. (2019) 89, e01339). Applying the method to eight whale sharks in the wild, all of which they liberated from fishing nets, they found that some of the individuals they tested may have gone hungry for weeks, and many have consumed considerable amounts of algae, although the species was believed to feed mainly on krill and small fishes. Knowing too little about cartilaginous fish also means that we are not sufficiently aware of the many ways in which we are already harming them and driving some of the species to extinction. In a recent analysis of populations and body sizes of sharks as a function of their distance from human activities, Tom B. Letessier of ZSL’s Institute of Zoology and colleagues showed a clear gradient (PLoS Biol. (2019) 17, e3000366.). Close to port towns with fishing vessels, there are fewer sharks and predators in general are smaller. The safe distance, beyond which there was no measurable effect, was 1,250 kilometres — much further than estimated in previous studies. This finding may suggest that fishing vessels now tend to travel further. These conclusions are based on the analysis of footage from more than 1,000 cameras equipped with bait and deployed in a wide range of different environments in the Pacific and Indian Oceans. Overall, the researchers recorded visits from 841 individual sharks of 19 different species. Letessier said: “Human activity is now the biggest influence on sharks’ distribution, overtaking every other ecological factor. Just 13% of the world’s oceans can be considered ‘wilderness’ but sharks and other predators are much more common and significantly larger at distances greater than 1,250 kilometres from people. This suggests that large marine predators are generally unable to thrive near to people and is another clear example of the impact of human overexploitation on our seas.” Knowing the location of the fish is also the objective of the decade-long tracking programme Tagging of Pacific Predators (TOPP), which ran from 2000 to 2010 and included Pacific bluefin tuna, yellowfin tuna, albacore tuna, white shark, shortfin mako shark, salmon shark and blue shark. In a recent analysis, Timothy White from Stanford University, USA, and colleagues have combined the TOPP data with recent satellite-based tracking of fishing vessels (Science (2018) 359, 904–908) to find out where fisheries and the habitats of sharks and tuna overlap (Sci. Adv. (2019) 5, eaau3761). “We may protect a species near the coastline of North America, but that same species may be exposed to a high level of international fishing in the open ocean. By increasing the transparency of where fish and ship fleets meet, we can identify hot spots where international protection may be required,” said Barbara Block, a senior co-author of the work. She also took part in the global assessment following the same principles which was published as this feature went to press (Nature (2019) 572, 461–466). Combining these two datasets to identify flashpoints, the researchers are hoping to inform the ongoing debate about how to protect marine wildlife in the high seas. The United Nations are currently debating a high-seas treaty due to be ready for signing in 2020, which could regulate the fisheries in the high seas, currently a largely unregulated global commons. Marine conservationists hope that the treaty will enable the UN to set aside large marine protected areas (MPAs) in the high seas. Some fisheries experts like Daniel Pauly at the University of British Columbia at Vancouver, Canada, have even called for a total ban of fishing in the high seas, arguing that it would reduce the take only marginally and could well improve productivity by offering space for fish stocks to recover. Moreover, much of the high-sea fishing is only economical thanks to subsidies covering the high cost of travelling far from shore. As these are in effect subsidies for burning fossil fuels, member states may want to consider abandoning this approach. While the UN may not go as far as following Pauly’s suggestion of a total ban, it is clear that more needs to be done to save the marine megafauna, including those much-misunderstood sharks.

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