In a world of limited funding, conservation priorities are often based on immediacy of extinction, the value of biodiversity and conservation opportunity (Marris, 2007). In this study, we provide the first estimates of the threat status and hence risk of extinction of chondrichthyans. Our systematic global assessment of the status of this lineage that includes many iconic predators reveals a risky combination of high threat (17% observed and 23.9% estimated), low safety (Least Concern, 23% observed and >37% estimated), and high uncertainty in their threat status (Data Deficient, 46% observed and 8.7% estimated). Over half of species are predicted to be threatened or Near Threatened (n = 561, 53.9%, Table 1). While no species has been driven to global extinction—as far as we know—at least 28 populations of sawfishes, skates, and angel sharks are locally or regionally extinct (Dulvy et al., 2003; Dulvy and Forrest, 2010). Several shark species have not been seen for many decades. The Critically Endangered Pondicherry shark (Carcharhinus hemiodon) is known only from 20 museum specimens that were captured in the heavily-fished inshore waters of Southeast Asia: it has not been seen since 1979 (Cavanagh et al., 2003). The now ironically-named and Critically Endangered Common skate (Dipturus batis) and Common angel shark (Squatina squatina) are regionally extinct from much of their former geographic range in European waters (Cavanagh and Gibson, 2007; Gibson et al., 2008; Iglésias et al., 2010). The Largetooth sawfish (Pristis pristis) and Smalltooth sawfish (Pristis pectinata) are possibly extinct throughout much of the Eastern Atlantic, particularly in West Africa (Robillard and Séret, 2006; Harrison and Dulvy, 2014).

Our analysis provides an unprecedented understanding of how many chondrichthyan species are actually or likely to be threatened. A very high percentage of species are DD (46%, 487 species); that is one of the highest rates of Data Deficiency of any taxon to date (Hoffmann et al., 2010). This high level of uncertainty in status further elevates risk and presents a key challenge for future assessment efforts. We outline a first step through our estimation that 68 DD species are likely to be threatened based on their life histories and distribution. Numerous studies have retrospectively explained extinction risk, but few have made a priori predictions of risk (Dulvy and Reynolds, 2002; Davidson et al., 2012). Across many taxa, extinction risk has been shown to be a function of an extrinsic driver or threat (Jennings et al., 1998; Davies et al., 2006) and the corresponding life history and ecological traits: large body size (low intrinsic rate of population increase, high trophic level), small geographic range size, and ecological specialization. Maximum body size is an essential predictor of threat status, we presume because of the close relationship between body size and the intrinsic rate of population increase in sharks and rays (Smith et al., 1998; Frisk et al., 2001; Hutchings et al., 2012). Though we note that this proximate link may be mediated ultimately through the time-related traits of growth and mortality (Barnett et al., 2013; Juan-Jordá et al., 2013). Our novel contribution is to show that depth-related geographic traits are more important for explaining risk than geographic range per se. The shallowness of species (minimum depth limit) and the narrowness of their depth range are important risk factors (Figure 3). We hypothesize that this is so because shallower species are more accessible to fishing gears and those with narrower depth ranges have lower likelihood that a proportion of the species distribution remains beyond fishing activity. For example, the Endangered Barndoor skate (Dipturus laevis) was eliminated throughout much of its geographic range and depth distribution due to bycatch in trawl fisheries, yet may have rebounded because a previously unknown deepwater population component lay beyond the reach of most fisheries (Dulvy, 2000; Kulka et al., 2002; COSEWIC, 2010). We find that geographic range (measured as Extent of Occurrence) is largely unrelated to extinction risk. This is in marked contrast to extinction risk patterns on land (Jones et al., 2003; Cardillo et al., 2005; Anderson et al., 2011a) and in the marine fossil record (Harnik et al., 2012a, 2012b), where small geographic range size is the principal correlate of extinction risk. We suggest that this is because fishing activity is now widespread throughout the world’s oceans (Swartz et al., 2010), and even species with the largest ranges are exposed and often entirely encompassed by the footprint of fishing activity. By contrast, with a few exceptions (mainly eastern Atlantic slopes, Figure 7E), fishing has a narrow depth penetration and hence species found at greater depths can still find refuge from exploitation (Morato et al., 2006; Lam and Sadovy de Mitcheson, 2010).

The status of chondrichthyans is arguably among the worst reported for any major vertebrate lineage considered thus far, apart from amphibians (Stuart et al., 2004; Hoffmann et al., 2010). The percentage and absolute number of threatened amphibians is high (>30% are threatened), but a greater percentage are Least Concern (38%), and uncertainty of status is lower (32% DD) than for chondrichthyans. Our discovery of the high level of threat in freshwater chondrichthyans (36%) is consistent with the emerging picture of the intense and unmanaged extinction risk faced by many freshwater and estuarine species (Darwall et al., 2011).

Our threat estimate is comparable to other marine biodiversity status assessments, but our findings caution that ‘global’ fisheries assessments may be underestimating risk. The IUCN Global Marine Species Assessment is not yet complete, but reveals varying threat levels among taxa and regions (Polidoro et al., 2008, 2012). The only synoptic summary to-date focused on charismatic Indo-Pacific coral reef ecosystem species. Of the 1,568 IUCN-assessed marine vertebrates and invertebrates, 16% (range: 12–34% among families) were threatened (McClenachan et al., 2012). This is a conservative estimate of marine threat level because although they may be more intrinsically sensitive to extinction drivers, charismatic species are more likely to garner awareness of their status and support for monitoring and conservation (McClenachan et al., 2012). The predicted level of chondrichthyan threat (>24%) is distinctly greater than that provided by global fisheries risk assessments. These studies provide modeled estimates of the percentage of collapsed bony fish (teleost) stocks in both data-poor unassessed fisheries (18%, Costello et al., 2012) and data-rich fisheries (7–13%, Branch et al., 2011). This could be because teleosts are generally more resilient than elasmobranchs (Hutchings et al., 2012), but in addition we caution that analyses of biased geographic and taxonomic samples may be underestimating risk of collapse in global fisheries, particularly for species with less-resilient life histories.

Our work relies on consensus assessments by more than 300 scientists. However, given the uncertainty in some of the underlying data that inform our understanding of threat status, such as fisheries catch landings data, it is worth considering whether these uncertainties mean our assessments are downplaying the true risk. While there are methods of propagating uncertainty through the IUCN Red List Assessments (Akcakaya et al., 2000), in our experience this approach was uninformative for even the best-studied species, because it generated confidence intervals that spanned all IUCN Categories. Instead it is worth considering whether our estimates of threat are consistent with independent quantitative estimates of status. The Mediterranean Red List Assessment workshop in 2005 prompted subsequent quantitative analyses of catch landings, research trawl surveys, and sightings data. Quantitative trends could be estimated for five species suggesting they had declined by 96% to >99.9% relative to their former abundance suggesting they would meet the highest IUCN Threat category of Critically Endangered (Ferretti et al., 2008). By comparison the earlier IUCN regional assessment for these species, while suggesting they were all threatened, was more conservative for two of the five species: Hammerhead sharks (Sphyrna spp.)—Critically Endangered, Porbeagle shark (Lamna nasus)—Critically Endangered, Shortfin mako (Isurus oxyrinchus)—Critically Endangered, Blue shark (Prionace glauca)—Vulnerable, and Thresher shark (Alopias vulpinus)—Vulnerable.

We can also make a complementary comparison to a recent analysis of the status of 112 shark and ray fisheries (Costello et al., 2012). The median biomass relative to the biomass at Maximum Sustainable Yield (B/B MSY ) of these 112 shark and ray fisheries was 0.37, making them the most overfished groups of any of the world’s unassessed fisheries. Assuming B MSY occurs at 0.3 to 0.5 of unexploited biomass then the median biomass of shark and ray fisheries had declined by between 81% and 89% by 2009. These biomass declines would be sufficient to qualify all of these 112 shark and ray fisheries for the Endangered IUCN category if they occurred within a three-generation time span. By comparison our results are considerably more conservative. Empirical analyses show that an IUCN threatened category listing is triggered only once teleost fishes (with far higher density-dependent compensation) have been fished down to below B MSY (Dulvy et al., 2005; Porszt et al., 2012). Hence, our findings are consistent with only around one-quarter of chondrichthyan species having been fished down below the B MSY target reference point. While there may be concern that expert assessments may overstate declines and threat, it is more likely that our conservative consensus-based approach has understated declines and risk in sharks and rays.

For marine species, predicting absolute risk of extinction remains highly uncertain because, even with adequate evidence of severe decline, in many instances the absolute population size remains large (Mace, 2004). There remains considerable uncertainty as to the relationship between census and effective population size (Reynolds et al., 2005). Therefore, Red List categorization of chondrichthyans should be interpreted as a comparative measure of relative extinction risk, in recognition that unmanaged steep declines, even of large populations, may ultimately lead to ecosystem perturbations and eventually biological extinction. The Red List serves to raise red flags calling for conservation action, sooner rather than later, while there is a still chance of recovery and of forestalling permanent biodiversity loss.

Despite more than two decades of rising awareness of chondrichthyan population declines and collapses, there is still no global mechanism to ensure financing, implementation and enforcement of chondrichthyan fishery management plans that is likely to rebuild populations to levels where they would no longer be threatened (Lack and Sant, 2009; Techera and Klein, 2011). This management shortfall is particularly problematic given the large geographic range of many species. Threat increased only slightly when geographic range is measured as the Extent of Occurrence; however, geographic range becomes increasingly important when it is measured as the number of countries (legal jurisdictions) spanned by each species. The proportion of species that are threatened increases markedly with geographic size measured by number of Exclusive Economic Zones (EEZs) spanned; one-quarter of threatened species span the EEZs of 18 or more countries (Figure 10). Hence, their large geographic ranges do not confer safety, but instead exacerbates risk because sharks and rays require coherent, effective international management.

Figure 10 Download asset Open asset Elevated threat in chondrichthyans with the largest geographic ranges, spanning the greatest number of national jurisdictions. Frequency distribution of number of jurisdictions spanned by all chondrichthyans (black, n = 1,041) and threatened species only (red, n = 174), for (A) country EEZs, and (B) the overrepresentation of threatened species spanning a large number of country EEZs, shown by the log ratio of proportion of threatened species over the proportion of all species. The proportion of threatened species is greater than the proportion of all species where the log ratio = 0, which corresponds to range spans of 16 and more countries. https://doi.org/10.7554/eLife.00590.019

With a few exceptions (e.g., Australia and USA), many governments still lack the resources, expertise, and political will necessary to effectively conserve the vast majority of shark and rays, and indeed many other exploited organisms (Veitch et al., 2012). More than 50 sharks are included in Annex I (Highly Migratory Species) of the 1982 Law of the Sea Convention, implemented on the high seas under the 1992 Fish Stocks Agreement, but currently only a handful enjoy species-specific protections under the world’s Regional Fishery Management Organizations (Table 6), and many of these have yet to be implemented domestically. The Migratory Sharks Memorandum of Understanding (MoU) adopted by the Parties to the Convention on Migratory Species (CMS) so far only covers seven sharks, yet there may be more than 150 chondrichthyans that regularly migrate across national boundaries (Fowler, 2012). To date, only one of the United Nations Environment Programme’s Regional Seas Conventions, the Barcelona Convention for the Conservation of the Mediterranean Sea, includes chondrichthyan fishes and only a few of its Parties have taken concrete domestic action to implement these listings. Despite two decades of effort, only ten sharks and rays had been listed by the Convention on International Trade in Endangered Species (CITES) up to 2013 (Vincent et al., 2014). A further seven species of shark and ray were listed by CITES in 2013—the next challenge is to ensure effective implementation of these trade regulations (Mundy-Taylor and Crook, 2013). OSPAR (the Convention for the Protection of the marine Environment of the North-East Atlantic) lists many threatened shark and ray species, but its remit excludes fisheries issues. Many chondrichthyans qualify for listing under CITES, CMS, and various regional seas conventions, and should be formally considered for such action as a complement to action by Regional Fisheries Management Organizations (RFMOs) (Table 6).

Table 6 Progress toward regional and international RFMO management measures for sharks and rays https://doi.org/10.7554/eLife.00590.020 1. Bans on ‘finning’ (the removal of a shark’s fins and discarding the carcass at sea) through most RFMOs (Fowler and Séret, 2010); 2. North East Atlantic Fisheries Commission (NEAFC) bans on directed fishing for species not actually targeted within the relevant area (Spiny dogfish [Squalus acanthias], Basking shark [Cetorhinus maximus], Porbeagle shark [Lamna nasus]) (NEAFC, 2009); 3. Convention on the Conservation of Antarctic Marine Living Resources bans on ‘directed’ fishing for skates and sharks and bycatch limits for skates (CCMLR, 2011); 4. A Northwest Atlantic Fisheries Organization (NAFO) skate quota (note: this has consistently been set higher than the level advised by scientists since its establishment in 2004) (NAFO, 2011); 5. International Commission for the Conservation of Atlantic Tunas (ICCAT) bans on retention, transshipment, storage, landing, and sale of Bigeye Thresher (Alopias superciliosus), and Oceanic whitetip shark (Carcharhinus longimanus), and partial bans (developing countries excepted under certain circumstances) on retention, transshipment, storage, landing, and sale of most hammerheads (Sphyrna spp.), and retention, transshipment, storage, and landing (but not sale) of Silky shark (Carcharhinus falciformis) (Kyne et al., 2012); 6. An Inter-American Tropical Tuna Commission (IATTC) ban on retention, transshipment, storage, landing, and sale of Oceanic whitetip sharks (IATTC, 2011); 7. An Indian Ocean Tuna Commission (IOTC) ban on retention, transshipment, storage, landing, and sale of thresher sharks-with exceptionally low compliance and reportedly low effectiveness (IOTC, 2011); and, 8. A Western and Central Pacific Fisheries Commission ban on retention, transshipment, storage, and landing (but not sale) of Oceanic whitetip sharks (Clarke et al., 2013).

Bans on ‘finning’ (slicing off a shark’s fins and discarding the body at sea) are the most widespread shark conservation measures. While these prohibitions, particularly those that require fins to remain attached through landing, can enhance monitoring and compliance, they have not significantly reduced shark mortality or risk to threatened species (Clarke et al., 2013). Steep declines and the high threat levels in migratory oceanic pelagic sharks suggest raising the priority of improved management of catch and trade through concerted actions by national governments working through RFMOs as well as CITES, and CMS (Table 7).

Table 7 Management recommendations: the following actions would contribute to rebuilding threatened chondrichthyan populations and properly managing associated fisheries https://doi.org/10.7554/eLife.00590.021 Fishing nations and regional fisheries management organizations (RFMOs) are urged to: 1. Implement, as a matter of priority, scientific advice for protecting habitat and/or preventing overfishing of chondrichthyan populations; 2. Draft and implement Plans of Action pursuant to the International Plan Of Action (IPOA–Sharks), which include, wherever possible, binding, science-based management measures for chondrichthyans and their essential habitats; 3. Significantly increase observer coverage, monitoring, and enforcement in fisheries taking chondrichthyans; 4. Require the collection and accessibility of species-specific chondrichthyan fisheries data, including discards, and penalize non-compliance; 5. Conduct population assessments for chondrichthyans; 6. Implement and enforce chondrichthyan fishing limits in accordance with scientific advice; when sustainable catch levels are uncertain, set limits based on the precautionary approach; 7. Strictly protect chondrichthyans deemed exceptionally vulnerable through Ecological Risk Assessments and those classified by IUCN as Critically Endangered or Endangered; 8. Prohibit the removal of shark fins while onboard fishing vessels and thereby require the landing of sharks with fins naturally attached; and, 9. Promote research on gear modifications, fishing methods, and habitat identification aimed at mitigating chondrichthyan bycatch and discard mortality. National governments are urged to: 10. Propose and work to secure RFMO management measures based on scientific advice and the precautionary approach; 11. Promptly and accurately report species-specific chondrichthyan landings to relevant national and international authorities; 12. Take unilateral action to implement domestic management for fisheries taking chondrichthyans, including precautionary limits and/or protective status where necessary, particularly for species classified by IUCN as Vulnerable, Endangered or Critically Endangered, and encourage similar actions by other Range States; 13. Adopt bilateral fishery management agreements for shared chondrichthyan populations; 14. Ensure active membership in Convention on International Trade in Endangered Species (CITES), Convention for the Conservation of Migratory Species (CMS), RFMOs, and other relevant regional and international agreements; 15. Fully implement and enforce CITES chondrichthyan listings based on solid non-detriment findings, if trade in listed species is allowed; 16. Propose and support the listing of additional threatened chondrichthyan species under CITES and CMS and other relevant wildlife conventions; 17. Collaborate on regional agreements and the CMS migratory shark Memorandum of Understanding (CMS, 2010), with a focus on securing concrete conservation actions; and, 18. Strictly enforce chondrichthyan fishing and protection measures and impose meaningful penalties for violations.

A high proportion of catch landings come from nations with a large number of threatened chondrichthyans and less-than-comprehensive chondrichthyan fishery management plans. Future research is required to down-scale these global Red List assessments and analyses to provide country-by-country diagnoses of the link between specific fisheries and specific threats to populations of more broadly distributed species (Wallace et al., 2010). Such information could be used to focus fisheries management and conservation interventions that are tailored to specific problems. There is no systematic global monitoring of shark and ray populations and the national fisheries catch landings statistics provide invaluable data for tracking fisheries trends in unmanaged fisheries (Newton et al., 2007; Worm et al., 2013). However, the surveillance power of such data could be greatly improved if collected at greater taxonomic resolution. While there have been continual improvements, catches are under-reported (Clarke et al., 2006), and for those that are reported only around one-third is reported at the species level (Fischer et al., 2012). To complement improved catch landings data, we recommend the development of repeat regional assessments of the Red List Status of chondrichthyans to provide an early warning of adverse changes in status and to detect and monitor the success of management initiatives and interventions. Aggregate Red List Threat indices for chondrichthyans, like those available for mammals, birds, amphibians, and hard corals (Carpenter et al., 2008) would provide one of the few global scale indicators of progress toward international biodiversity goals (Walpole et al., 2009; Butchart et al., 2010).

Our global status assessment of sharks and rays reveals the principal causes and severity of global marine biodiversity loss, and the threat level they face exposes a serious shortfall in the conservation management of commercially-exploited aquatic species (McClenachan et al., 2012). Chondrichthyans have slipped through the jurisdictional cracks of traditional national and international management authorities. Rather than accept that many chondrichthyans will inevitably be driven to economic, ecological, or biological extinction, we warn that dramatic changes in the enforcement and implementation of the conservation and management of threatened chondrichthyans are urgently needed to ensure a healthy future for these iconic fishes and the ecosystems they support.