Sympathy for the devil: a conservation strategy for devil and manta rays

Scientific research and expertise on devil and manta rays

In order to examine trends in devil and manta ray scientific research, we extracted scientific papers from the ISI Web of Science Core Collection and Google Scholar on 30 May 2016. Our specific aim was to update the systematic literature search conducted up to the year 2011 by Couturier et al. (2012) and, as such, we searched the primary literature for titles that contained ‘mobula,’ ‘manta,’ or ‘devil ray’ published from 2012 to 2016. We exported these results and ‘false-positive’ papers unrelated to devil or manta rays were removed.

Range, fisheries, and protection mapping

Eleven geographic distribution maps of Extent of Occurrence (EOO) and Area of Occupancy (AOO) were generated prior to the workshop and refined during and following the workshop based on current species distribution knowledge. The EOO is defined as “the area contained within the shortest continuous imaginary boundary which can be drawn to encompass all the known, inferred or projected sites of present occurrence of a taxon” (IUCN, 2001; IUCN, 2012; IUCN, 2014). The AOO is defined as “the area within its ‘Extent of Occurrence’ that is occupied by a taxon for each country. The measure reflects the fact that a taxon will not usually occur throughout the area of its Extent of Occurrence, which may, for example, contain unsuitable habitats or may be beyond the maximum depth distribution” (IUCN, 2001; IUCN, 2012; IUCN, 2014). The AOO for devil and manta ray species was estimated by including only areas where the presence of a given species had been confirmed.

Devil ray and manta ray AOO distribution maps were grouped by genus in order to map and compare: (a) locations of known fishing pressure through target and incidental fisheries (from Croll et al., 2015), and (b) presence of international, regional, and national protection (detailed in Table 1). Information on known fisheries and protections was gathered primarily by consulting mobulid experts who participated in the conservation strategy workshop, and those who were part of the wider network of experts (detailed below). This information was supported by reviewing the devil and manta ray literature.

Development of a Global Devil and Manta Ray Conservation Strategy

The IUCN SSG Global Devil and Manta Ray conservation strategy workshop was attended by 18 experts who held knowledge from nine of the 19 Major Fishing Areas as recognized by the Food and Agriculture Organization of the United Nations (FAO; Fig. 2A). Fourteen more experts contributed to the conservation strategy through electronic correspondence, and an additional 16 experts provided knowledge during the 2015 Fisheries Society for the British Isles (FSBI) symposium in Plymouth, United Kingdom (27–31 July 2015; Fig. 2B). These additional collaborators helped to provide expertise for mobulids in the eastern Indian and the Atlantic Ocean, as no workshop participant self-identified as having knowledge specific to these Major Fishing Areas.

Through a series of workshop subgroup discussions and plenary sessions, participants at the strategy workshop developed a vision, goals, objectives, and actions (IUCN, 2008) aimed at rebuilding and conserving devil and manta ray populations. This process largely followed that for the Global Sawfish Conservation Strategy, the first of its kind for a group of elasmobranchs (Harrison & Dulvy, 2014). The devil and manta ray workshop participants included biologists and fisheries scientists, as well as representatives of organizations focused on tourism, education, and policy.

The group used Specific, Measurable, Achievable, Relevant/Realistic, and Time-Bound (SMART) criteria as a guide for setting objectives and actions. In some cases, workshop participants prioritized countries or regions based on known threats (i.e., those with large, expanding, and unregulated mobulid incidental or targeted catch). Following the workshop, experts revised the goals, objectives, and actions outlined in the strategy, and collaborated on the development of this paper to provide context for the strategy.

Scientific research and expertise on devil and manta rays

Since the literature review conducted by Couturier et al. (2012), which included all peer-reviewed literature from 1980 to 2011, the search term “mobula” returned 11 peer-reviewed publications, while “manta” returned 50 over the past 4.5 years from 2012 to 2016 (up to June 2016). The term “devil ray” was also searched for, and returned an additional 10 publications. Compared to Couturier et al. (2012), who reported 96 publications with either “manta” or “mobula” in the title over 31 years (1980–2011), our update identified a total of 71 additional publications with “manta,” “mobula,” or “devil ray” in the title over only the past 4.5 years. Couturier et al. (2012) identified 28 peer-reviewed studies focused on Mobula spp. from 1980 to 2011, whereas our study identified 21 novel peer-reviewed studies focused on Mobula spp. over the past four years (2012–2016).

For devil rays (21 studies), the research theme (as defined by Couturier et al., 2012) was dominated by “Occurrence” (10); followed by “Anatomy, biology, and morphology” (4), and “Bycatch and fisheries” (3). For manta rays (44 studies), the top two research themes were also “Occurrence” (15) and “Anatomy, biology, and morphology” (13), followed by “Life history and population” (7) and “Bycatch and fisheries” (4). Publications that referred to both devil and manta rays in the title (6 studies) were excluded in this research theme analysis. These results differ from Couturier et al. (2012)’s finding that across all devil and manta ray studies “Taxonomy” was the leading research theme, followed by “Occurrence” and “Bycatch and fisheries.”

Range, fisheries, and protection mapping

Novel reports on occurrence of mobulid species updated species-specific Area of Occupancy and Extent of Occurrence maps for the eleven species of devil and manta ray (Fig. 3). Compared to the previous IUCN Red List distribution maps (IUCN, 2015), these updated maps show larger AOO and EOOs for most mobulids, as new sightings and landings data have been reported. For example, the Chilean Devil Ray Mobula tarapacana (Philippi, 1892) is confirmed to be present throughout the Red Sea and Gulf of Aden, whereas previously it was only reported in the upper Red Sea. Generally, there have been range extensions across the central Atlantic with new sightings of the Bentfin Devil Ray Mobula thurstoni (Lloyd, 1908) in West Africa, ranging across the isolated Atlantic islands of the Canaries, Azores, and Ascension. Furthermore, there were significant new records in the Indo-west Pacific nations of the Philippines, Vanuatu (for the Bentfin Devil Ray), Fiji and Palau (for the Chilean Devil Ray).

The devil rays fall within three broad classes of geographical distribution. The three largest-bodied species—at least 1.8 m disc width—have near circumglobal tropical and subtropical geographic ranges: the Spinetail Devil Ray Mobula japanica (Müller & Henle, 1841), Chilean Devil Ray, and Bentfin Devil Ray. Three species are found only in the Atlantic Ocean and Mediterranean Sea. The Atlantic Devil Ray Mobula hypostoma (Bancroft, 1831) is found only in the western Atlantic and has an apparently disjunct distribution in the Caribbean and northern Gulf of Mexico and also in the South Atlantic continuous along the coastlines of Southern Brazil, Uruguay, and Northern Argentina. The eastern Atlantic counterpart is the Lesser Guinean Devil Ray Mobula rochebrunei (Vaillant, 1879) that was described from Guinea and is thought to be present in Mauritania, Senegal, Guinea-Bissau, and Angola. Finally, the largest species—the Giant Devil Ray—is apparently only found in the Mediterranean Sea. There are three smaller (approximately 1 m disc width) Indo-Pacific species: two found only in the Indian Ocean and western Pacific Ocean, the Pygmy Devil Ray Mobula eregoodootenkee (Bleeker, 1859) and the Shortfin Devil Ray Mobula kuhlii (Müller & Henle, 1841), and one species found only in the eastern Pacific, the Smoothtail Devil Ray Mobula munkiana Notarbartolo di Sciara, 1987. The larger of the two manta ray species, the Giant Manta Ray, has a near circumglobal distribution in tropical and subtropical waters and is most similar to those of the three largest devil ray species, whereas the Reef Manta Ray Manta alfredi (Krefft, 1868) has an Indo-West Pacific distribution.

Species-specific differences in international, national, and state/territory protection occur across the 11 mobulid species. The Giant Manta Ray has the largest number of international, national, and state/territory protection of any mobulid species, followed by the Reef Manta Ray (Table 1). Species-specific differences exist within the devil rays. The Giant Devil Ray has a small EOO that coincides with the Mediterranean Sea (Fig. 3B) yet it has been the subject of numerous national, regional, and international protection commitments from surrounding countries (Table 1). In contrast, the Chilean Devil Ray has a large EOO that overlaps with that of the Giant Manta Ray, but national protection is only afforded in six of the 31 countries in its recorded range (Table 1).

When grouped by genus, protections for devil rays under two key international agreements are now equal to those for manta rays (Fig. 4), yet national and state/territory legislation for devil rays still lags behind protection for manta rays (Fig. 5). Moreover, current national regulations leave devil rays unprotected and manta rays protected in areas where target and incidental fisheries for both genera are known to occur. For example, several mobulid target and incidental fisheries occur in the Indo-Pacific region and most protections in this region apply exclusively to manta rays (i.e., Indonesia, Peru, and the Philippines; see Fig. 5).

Development of a Global Devil and Manta Ray Conservation Strategy

Workshop participants agreed on an overall vision for the status of devil and manta rays, and three goals aimed at achieving this vision, as well as a series of sixteen objectives and associated actions to support the goals (see Table 2 for details)

Vision: Populations of devil and manta rays that flourish in resilient ocean ecosystems, harmoniously with human communities, through knowledge, sustainability, and education.

Goal A. The knowledge required to sustain devil and manta rays is generated and communicated.

Objectives:

1. Taxonomy: To resolve the taxonomy and define management units of devil and manta rays

2. Biology: To determine the productivity, life history, and demography of devil and manta ray populations

3. Ecology: To understand the spatial and temporal ecology of devil and manta rays

4. Public Communication: Communicate research on biology, ecology, status, threats and socio-economic value, of devil and manta rays to enhance conservation and management.

Goal B. Devil and manta ray populations are maintained at, or recovered to, ecologically relevant levels through managing fisheries, trade and demand.

Objectives:

1. Fisheries Management: Devil and manta ray populations and fisheries are monitored and sustainably managed

2. Trade Regulation: Ensuring that trade in all devil and manta ray products is traceable, regulated, and monitored

3. Socio-economics and Demand: Reduce the demand for devil and manta ray products and understand the socio-economic drivers to ensure demand does not drive unsustainable fishing.

Goal C. Educated and engaged communities support and benefit from devil and manta ray conservation and management through outreach, capacity building, and fundraising.

Objectives:

1. Tourism: A standardized best practice approach to tourism interaction with devil and manta rays is adopted by tourism operators globally

2. Community Engagement: Knowledgeable communities contribute to devil and manta ray conservation and management

3. Alternative Livelihoods: Empowered coastal communities benefit from alternative livelihoods that are developed to reduce overexploitation of devil and manta ray populations

4. Devil and Manta Ray Network: Commitments to plans and regulations are encouraged, prioritized, facilitated and fulfilled.

How did the charisma gap arise between manta and devil rays?

Tourism and related economic sectors have partially fuelled the conservation activities surrounding manta rays. Translating this success to devil rays, however, may be challenging because of biological differences that make devil rays harder for tourists to easily and reliably access. Both species of manta ray reach a large body size, form predictable aggregations, and are accessible to divers (O’Malley, Lee-Brooks & Medd, 2013). Some species of devil ray also reach a large body size, form predictable aggregations, and are accessible to divers, and as a result may be incorrectly identified as manta rays by tourism operators and tourists (RHL Walls & D Fernando, pers. obs., 2016). Other devil ray species, however, form unpredictable and sporadic aggregations and exhibit shy behaviour. For example, while aggregations of leaping Smoothtail Devil Ray (Fig. 1D) off Baja California provide great potential for boat-based tourism, they occur over short periods that can be difficult to predict. It is inevitable that sighting frequency and reliability will enable a larger segment of society to engage with manta rays, resulting in greater overall interest in conserving manta rays than for devil rays, despite similar threats across genera.

This is not the first charisma gap in species conservation, nor chondrichthyan conservation, and this pattern may be more widespread than is appreciated (McClenachan et al., 2012). For example, an apparent charisma gap occurs in the United States where the 2010 Shark Conservation Act prohibited removal of fins at sea for all sharks landed in United States waters, with an exception for the Atlantic Dusky Smooth-hound (Mustelus canis), which can be landed with their fins removed according to an exceptionally lenient fin-to-carcass ratio (United States Public Law 111–348, 2011). US Atlantic state bans on shark fins also make exceptions for smooth-hounds as well as the Spiny Dogfish (Squalus acanthias). In many places around the world, shark finning has been banned largely based on concerns over cruelty, yet few regulations prohibit the removal of wings from live skates. We caution that variation in public awareness, and care for a biased subset of chondrichthyans and other marine organisms, will lead to problematic asymmetries in scientific knowledge, conservation campaigns, and protective regulations (McClenachan et al., 2012). We suggest using well-established species conservation planning frameworks for a means of bridging the charisma gap.

How can we build upon manta ray protection to benefit devil rays?

Many countries still only apply protective measures to manta rays despite all mobulids being highly sensitive to overexploitation. Those countries offering protection for both devil and manta rays include Australia, Brazil, the Member States of the European Union, Israel, Mexico, Ecuador, New Zealand, and the Maldives (Camhi et al., 2009; Whitcraft, O’Malley & Hilton, 2014; Council Regulation (EU), 2015; CITES, 2015; Department of the Environment, 2016). National asymmetries in protection are still apparent in Peru, the Philippines, United Arab Emirates (UAE), and Indonesia, as these countries afford legal protection to one or both species of manta ray, but not yet to devil rays. We hope that a key outcome of our strategy development is a greater awareness of the need for matching protection and conservation of both devil and manta rays.

International protection for mobulids has expanded relatively rapidly in recent years, and following an initial lag in devil ray protection, the majority of international agreements now protect all mobulids. The first major international action for mobulids came in 2011 with the listing of just the Giant Manta Ray on Appendix I and II of the Convention on the Conservation of Migratory Species of Wild Animals (CMS), obligating the 122 Parties to strictly protect the species and collaborate toward regional conservation. In 2013, the two manta ray species were listed under CITES Appendix II, the world’s oldest and largest multilateral environmental agreement with the legal mechanisms in place to hold Parties accountable to trade restrictions. The 183 Parties are thus required to issue permits to export manta rays (or manta ray products) only after demonstrating that they are sourced from legal and sustainable fishing operations (CITES, 2013). In 2014, during the 11th Meeting of the CMS Parties, the remaining ten species of mobulid were listed on Appendix I and II (CMS, 2015). In 2016, during the 17th Meeting of the Conference of the Parties to CITES, all species of Mobula were listed under Appendix II (CITES, 2016; Action 6.10). In 2015, the General Fisheries Commission for the Mediterranean (GFCM) became the first Regional Fishery Management Organization (RFMO) to prohibit take of a mobulid species (the Giant Devil Ray). This was followed later that year by a binding measure adopted by the Inter-American Tropical Tuna Commission (IATTC). This IATTC measure aims to prevent targeting, retention, and discard mortality for all mobulid species taken in relevant Eastern Tropical Pacific fisheries, but includes notable exceptions for small-scale operations.

Can responsible trade and demand reduction help to decrease target fisheries for gill plates?

Trade regulation can lead to both positive and negative outcomes. Trade may cease, or continue at sustainable levels as a result of regulation; or trade may continue illegally, or continue without full regulatory compliance. Trade regulation, therefore, should be promoted and implemented with careful consideration of socio-economic drivers. Sometimes governments find it simpler to ban, rather than regulate, trade (Vincent et al., 2014). Regulatory obligations (such a CITES permit processing system) can be challenging to implement, particularly in countries with low capacity for management (Shepherd & Nijman, 2007; Rosen & Smith, 2010). Counter-intuitive to the intended purpose, complete bans can sometimes stimulate wildlife exploitation by driving it underground and creating circumstances for elevated value. An analysis of mainly terrestrial species policies that changed from allowing a regulated trade at sustainable levels to a complete ban on trade, found that trade volumes increased by 135% in the year prior to the ban (Rivalan et al., 2007). The price of rhino horn in Korea rose by 400% two years after a total ban, which fueled a sharp increase in poaching (Rivalan et al., 2007; Biggs et al., 2013).

One approach to preventing negative conservation outcomes from trade regulation involves attempting to understand relevant socio-economic drivers and associated stakeholder behaviour. Investigations into the mobulid gill plate trade found it to be centered in Guangzhou, China, and involve only a handful of large suppliers (Whitcraft, O’Malley & Hilton, 2014; O’Malley et al., 2016; Actions 7.3, 7.4, 7.5). Conservation campaigns aimed at consumer demand reduction in Guangzhou, along with stronger Chinese government policies that inadvertently affect wildlife trade, appear to be reducing demand for gill plates (O’Malley et al., 2016, Action 7.7); however, continued monitoring is needed to evaluate and track the success of such consumer behaviour change campaigns. Anecdotal information suggests that trade regulation specific to manta rays may unintentionally increase fishing and trade pressure on devil rays. For example, in Indonesia, where national protection exists for manta rays but not devil rays, fishers have begun to target devil rays to avoid penalties. In this case, fishers claim that devil rays are more challenging to catch than manta rays, and thus were less frequently targeted prior to national manta ray protection (D Adhiasto, pers. comm., 2016).

Another important consideration of regulating mobulid ray exploitation is the effect on livelihoods and food security of fishing communities. Human populations in many tropical coastal communities are growing rapidly, have low income, and rely heavily on fish for protein and income (Allison et al., 2009). Mobulids provide a source of income and protein in several developing countries, particularly Indonesia and Sri Lanka (Fernando & Stevens, 2011; Lewis et al., 2015). Developed nations can increase the effectiveness of conservation measures by helping to facilitate necessary social and economic transitions (McClanahan et al., 2008). Under CITES Appendix II, countries can independently assess the sustainability of exports and determine the allowable level of trade, if any. Countries may prohibit landings of mobulids from fisheries based on depletion, high vulnerability, or precaution, regardless of CITES listings. Some mobulid species may be able to support sustainable fisheries, but this has yet to be documented in practice, and would require robust management and enforcement. All fisheries that catch mobulids, including fisheries where catch is incidental, should be monitored, regulated, and minimized when necessary to ensure that these fisheries are sustainable.

How can the impact of incidental catch on mobulids be reduced?

Incidental catch in both large and small-scale fisheries is a key challenge to the conservation of mobulids, given mortality during capture, evidence for low rates of post-release survival (Francis & Jones, 2017), and increased incentives for fisheries to retain these species for the gill plate trade (Croll et al., 2015). The few available studies on post-release survival in devil rays show that handling following capture may strongly influence post-release survival (Action 5.8), although more research is needed (Action 5.9). In a study where small (142–238 cm disc width (DW), mean 200 cm DW) Spinetail Devil Rays were tagged without being removed from the water as part of a scientific study, post-release survival was relatively high (Croll et al., 2012). In contrast, when large individuals (215–265 cm DW) of the same species were brought on the deck of commercial fishing vessels prior to being tagged and released, post-release survival was low (Francis & Jones, 2017). Researchers found that removing these rays from the water caused significant physical strain with potential for post-release mortality. For tuna purse seine fisheries, releasing large rays directly from the brailer (scoopnet that removes the fish from the purse seine), or lifting them out of the brailer using a canvas sling or scoop, is considered best practice; small and medium rays landed on the fishing vessel deck can be carried by their wings to be released (Poisson et al., 2014).

The IATTC’s 2015 prohibition on the retention, transshipment, storage, landing, and sale of all devil and manta rays in large-scale, Eastern Tropical Pacific tuna fisheries is a significant step toward mobulid protection, but compliance has yet to be evaluated, and exceptions made for small-scale fisheries compromise the conservation goals that drove the original proposal (Action 5.13; IATTC, 2015). Effective implementation of associated requirements for reporting mobulid catch data and ensuring safe releases, as well as provisions for technical assistance and capacity building, is critical to improving the outlook for the species in this region (Action 5.3, 5.4, 5.5).

While the IATTC mobulid measure can be seen as progress for some purse seine fisheries, more attention to the incidental catch of mobulids in data-poor trawl fisheries, particularly midwater trawls, is needed. A study on the pelagic megafauna taken incidentally in large-scale European trawl fleets targeting sardinella, sardine, and horsemackerel off the Northwest Africa shelf found that approximately one mobulid is taken for every hour of trawling (Zeeberg, Corten & de Graaf, 2006). More research and management is urgently needed to address threats to mobulids from such trawling operations and from many other fisheries (Action 5.6).