Environmental DNA reveals tropical shark diversity in contrasting levels of anthropogenic impact

Abstract

Sharks are charismatic predators that play a key role in most marine food webs. Their demonstrated vulnerability to exploitation has recently turned them into flagship species in ocean conservation. Yet, the assessment and monitoring of the distribution and abundance of such mobile species in marine environments remain challenging, often invasive and resource-intensive. Here we pilot 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. We identified at least 21 shark species, from both Caribbean and Pacific Coral Sea water samples, whose geographical patterns of diversity and read abundance coincide with geographical differences in levels of anthropogenic pressure and conservation effort. We demonstrate that eDNA metabarcoding can be effectively employed to study shark diversity. Further developments in this field have the potential to drastically enhance our ability to assess and monitor elusive oceanic predators, and lead to improved conservation strategies.

Figure 1

Map of New Caledonian (a) and Caribbean (b) sampling locations. The intensity of dot shading in all panels indicates the level of anthropogenic impact from ‘severely impacted’ (light pink/blue) to ‘least impacted’ (dark pink/blue). The krona-like plots (c) show the complete taxonomic assignment for each of the sampling locations (with elasmobranchs in purple). The different taxonomic levels are represented by the layers of rings, starting with phylum, for the innermost layer, and subsequently class, order, family and genus radiating outwards. In the centre of each location plot, the number of elasmobranch reads compared to the total number of filtered reads, is displayed. The Principal Component Analysis (PCA) (d) depicts the scattering of the samples containing elasmobranch reads, across the two biogeographic areas. The six most discriminating taxa are labelled in full, while the rest are indicated by numbers (following alphabetical order from lines 27–50 in Supplementary Table S2), namely: 1 = C. acronotus, 2 = C. albimarginatus, 4 = C. amblyrhynchos/limbatus_Caribbean, 6 = C. brachyurus/perezii, 8 = C. melanopterus/cautus, 9 = C. leucas, 10 = C. obscurus/macloti/longimanus/galapagensis, 12 = C. perezii/falciformis_Pacific, 13 = C. plumbeus, 14 = C. plumbeus/altimus/sorrah, 15 = G. cuvier, 17 = N. brevirostris/acutidens_Pacific, 18 = R. porosus/terraenovae, 20 = S. mokarran, 21 = D. Americana, 22 = S. fasciatum. Maps made with Natural Earth. Free vector and raster map data @ naturalearthdata.com.

Figure 2

Bar plot showing the relative abundances of reads (fourth-root transformed) for every elasmobranch MOTU detected in the Caribbean and New Caledonian locations.

Figure 3

Violin plots showing (a) elasmobranch diversity (MOTU richness) and (b) abundance of reads per sample in the different locations from the Caribbean (green) and New Caledonia (blue). The shapes indicate the density distribution of the samples, extending from the minimum to the maximum observed values. The median values are indicated by the red dots. The thick black bars are the interquartile ranges. The thin black extending lines represent the 95% confidence intervals such that the values in the wider parts of the plots are more probable than those in the narrower parts. Per region, significant differences (P < 0.05) are indicated with asterisks. Asterisk significant codes: ***P < 0.001, **P < 0.01, *P < 0.05, ^•P < 0.1.

Figure 4

Species accumulation curves showing elasmobranch diversity (MOTU richness) as a function of the number of samples in the locations from the Caribbean (a) and New Caledonia (b). Error bars indicate standard errors after 100 permutations. Belize is absent from the plot as it contains only one elasmobranch MOTU.