Environmental DNA reveals tropical shark diversity in contrasting levels of anthropogenic impact
Increased and targeted fishing pressure has led to the collapse of shark populations around the world. According to worldwide estimates, a staggering 100 million sharks are killed each year (Worm et al., 2013). Modern research has shed light on the key role these oceanic predators play in maintaining healthy oceans, leading to the implementation of conservation actions in many parts of the world to reverse population collapse. Regular monitoring is key to assess the success of these efforts and to improve management strategies. Information about species abundance, migration patterns, habitat use and feeding and nursery grounds enables conservationists to prioritize conservation efforts, target threats and protect specific locations.
The lack of baseline data on the diversity and relative abundance of shark species in the Dutch Caribbean has been a significant barrier to their protection. In an effort to reduce this knowledge gap, a number of research projects that are part of DCNA’s Save Our Sharks Project (generously funded by the Dutch Postcode Lottery) have helped collect information on the occurrence of sharks, their relative and seasonal abundance, movements and behavior across different management zones in the Dutch Caribbean. These include BRUV (Baited Remote Underwater Video) monitoring, acoustic monitoring and the establishment of a shark sighting network. We now know thanks to these efforts that the Saba Bank has the highest shark abundance in the area and must therefore be prioritized for shark conservation, and that endangered shark species(Carcharhinus falciformis,Sphyrna mokarranand Galeocerdo cuvier)live in the waters of our islands.
While traditional monitoring survey methods based on acoustic and direct visual observation have helped garner important information on species abundance and richness, they are typically expensive, labor-intensive, time-consuming and dependent on professional taxonomic identification (Deiner et al., 2017; Littlefair et al., 2017). There has been much interest in recent years in the potential of eDNA metabarcodingas a rapid, cost-effective and non-invasive monitoring tool (Deiner et al., 2017) to complement existing methods.A new study by Bakker et al. (2017) looks into the possible application of this emerging research method for elasmobranch species.They piloted a “novel, rapid and non-invasive environmental DNA (eDNA) metabarcoding approach specifically targeted to infer shark presence, diversity and eDNA read abundance in tropical habitats” which will enhance the ability to assess and monitor sharks and therefore improve conservation strategies that depend on accurate population assessments(Bakker et al., 2017).
Environmental DNA (eDNA) metabarcoding was first used to detect rare and invasive species, and there is now much excitement over its potential to track the presence, richness and abundance of animal species within their natural environment in a fast, efficient and non-invasive way (Creer et al., 2016; Deiner et al., 2017). Animals leave behind DNA in their habitat through feces, gametes, skin cells, etc., and researchers are now able to isolate this DNA from environmental samples (water, soil), amplify and then sequence it to identify the taxonomic identity of the species (Deiner et al., 2017; Littlefair et al., 2017; Bakker et al. 2017). Because eDNA can only be detected in the water column for a few days, it is possible to know whether the species was recently in the area. Several studies have found eDNA metabarcoding to be more effective than traditional survey methods in detecting taxonomic diversity, including teleost fish in freshwater and marine ecosystems, as well as able to detect rare species that would not be detected through visual observations (Lim et al., 2016, O'Donnell et al., 2017; Port et al., 2013; Thomsen et al., 2012) However, because different animal species “have different rates of eDNA productionor “origin” and exhibit different “transport” rates from other locations, eDNA in an environmental sample could be inconsistent relative to a species’ true local and current abundance” (Deiner et al., 2017).Acoustic surveys of marine mammals were also found to detect greater species richness than eDNA metabarcoding (Foote et al., 2012).
The study by Bakker et al. (2017) is the first to investigate the application of eDNA metabarcoding to the study of elasmobranch abundance and diversity. Natural seawater samples were taken in the Caribbean (55) and New Caledonia (22) in 2015. Four different locations in the Caribbean were chosen that reflect varying levels of anthropogenic impact, from most (Jamaica and Belize) to least (The Bahamas, which is a shark sanctuary). In New Caledonia samples were collected in three locations: the pristine Chesterfield Atolls, New Caledonia North and the densely populated areas of Noumea. Bakker et al. (2017) used an elasmobranch specific COI primer for the amplification of eDNA metabarcoding markers. Caribbean reef sharks (Carcharhinus perezii)and Lemon sharks (Negaprion brevirostris) were abundant in Caribbean research sites while New Caledonian waters were dominated by Grey reef sharks (Carcharhinus amblyrhynchos)andWhitetip reef sharks (Triaenodon obesus)with the exception of the most impoverished locations (e.g. Belize, Jamaica and Noumea) (Bakker et al., 2017).
The main goal of the study was to examine whether patterns of species diversity reflect the known degree of anthropogenic impact. Previous studies within the Caribbean region have found that sharks are more abundant in areas where population density is low and where strong fishing regulations or conservation measures have been implemented (Ward-Paige et al., 2010). Bakker et al. (2017) also found that MOTU (Molecular Operational Taxonomic Unit) richness and abundance patterns are linked to the level of anthropogenic impact in each location: less remote and non-protected locations showed lower values for both diversity and abundance, while the more pristine/remote/protected locations had higher species richness and abundance. The Bahamas, which was declared a shark sanctuary in 2011, displayed the greatestelasmobranch diversity (11 MOTUs) while Jamaica and Belize displayed the least (2 and 1 MOTU respectively). In New Caledonia, the remote Chesterfield Atolls (11 MOTUs) had similar diversity to New Caledonia North (14 MOTUs) but displayed significantly higher abundance, meaning that read abundance may be correlated with remoteness (Bakker et al., 2017).
Based on the results of the Bakker et al. study (2017), there appears to be much potential for the application of eDNA metabarcoding to the assessment of elasmobranch species abundance and richness. Bakker et al. however site a number of concerns about the methodology that need to be addressed in future developments of elasmobranch eDNA metabarcoding approaches, including the choice of markers and primers. Certain elasmobranch species could also not be detected by the primer set selected by Bakker et al. (2017). The nurse shark (Ginglymostoma cirratum), which is known to be abundant in the Caribbean and was visually observed at the time of sampling was not detected by any of the eDNA sequence reads. The authors are however very optimistic about the use of eDNA metabarcoding as an objective and powerful elasmobranch assessment tool, from monitoring the success of shark sanctuaries to mapping differences in shark diversity (Bakker et al., 2017).