Population genetics is essential for understanding and managing marine ecosystems, but sampling remains challenging. We demonstrate that high-throughput sequencing of seawater environmental DNA can provide useful estimates of genetic diversity in a whale shark (Rhincodon typus) aggregation. We recover similar mitochondrial haplotype frequencies in seawater compared to tissue samples, reliably placing the studied aggregation in a global genetic context and expanding the applications of environmental DNA to encompass population genetics of aquatic organisms.
The whale shark is an ideal flagship species for 'citizen science' projects because of its charismatic nature, regular presence at numerous coastal aggregation sites and a growing number of ecotourism ventures focusing on the species. An online database of Whale Shark encounters, identifying individuals based on their unique skin patterning from 1992 to 2014 captured almost 30,000 whale shark encounter reports, comprising more than 6000 individuals identified from 54 countries. In this time the number of known whale shark aggregation sites increased from 13 to 20. Examination of encounters revealed a skewed sexratio bias towards males (overall >66%), high site fidelity amongst individuals with limited movements of sharks between neighbouring countries/regions but no records confirming 2 large, ocean basin-scale migrations. Citizen science has been vital in amassing large spatial and temporal datasets to elucidate key aspects of whale shark life-history and demographics and will continue to provide substantial long-term value.
Article impact statement: Environmental DNA provides habitat-characteristic molecular signatures and can be used efficiently to map marine biodiversity at large spatial scales.
ABSTRACT-The effect of burial due to sudden sediment loading was examined in a mixed Philippine seagrass meadow through the experimental deployment of sediment (0. 2. 4 , 8, and 16 cm deposited over the experimental plots). The responses in shoot density, vertical growth, and branching of the species present were assessed 2. 4, and 10 mo following disturbance. Shoot density responses were strongly species-specific. The large Enhalus acoroides maintained shoot density at all burial treatments, and only showed evidence of decline by the end of the expenment. Thalassia hempnchiiand, to a lesser extent. Cymodocea rotundata showed a sharp decllne In shoot density even at moderate burial treatments, from which they faded to recover. The accompanying species (Halodule uninervis, Syringodiurn isoetifolium, and Cyrnodocea serrulata) showed an initial decline In shoot density followed by recovery. The small Halophila ovalis showed an opportunistic growth in plots receiving intermediate (buried by 4 and 8 cm sediment) disturbance, reaching shoot densities well in excess of those on control plots. The results suggest a pattern of species loss following disturbance by sediment burial corresponding to the sequence, T hemprichii + (C. rotundata. S. isoetifolium, H uninervis) + C. serrulata + E. acoroides. Vertical growth increased significantly for all species with differentiated vertical shoots, except C, serrulata. The examination of the time course of vertical growth imprinted on the shoots of the dominant species, T hemprichii, revealed a rapid response to bunal through increased internodal length, which was maintained over 8 mo following the disturbance. The resulting cumulative vertical growth along the experiment was linearly correlated with the degree of burial in~posed on the plants. Branching of vertical shoots also increased significantly (73 to 96%, depending on the species) with burial. Experimental burial induced changes in shoot age distribution of some of the species, involving rearrangements, through selective mortality or recruitment, of the contribution of young shoots to the populations. The results obtained show major differences in species response to small-scale disturbance, closely linked to predictions derived from consideration of species growth rate and size, and provide evidence of the importance of small-scale disturbance in the maintenance of multispecific seagrass meadows.
The Arabian Gulf is the warmest sea in the world and is host to a globally significant population of the whale shark Rhincodon typus. To investigate regional whale shark behaviour and movements, 59 satellite-linked tags were deployed on whale sharks in the Al Shaheen area off Qatar from 2011–14. Four different models of tag were used throughout the study, each model able to collect differing data or quantities of data. Retention varied from one to 227 days. While all tagged sharks crossed international maritime boundaries, they typically stayed within the Arabian Gulf. Only nine sharks dispersed through the narrow Strait of Hormuz into the Gulf of Oman. Most sharks stayed close to known or suspected feeding aggregation sites over summer months, but dispersed throughout the Arabian Gulf in winter. Sharks rarely ventured into shallow areas (<40 m depth). A single, presumably pregnant female shark was the sole animal to disperse a long distance, crossing five international maritime boundaries in 37 days before the tag detached at a distance of approximately 2644 km from the tagging site, close to the Yemeni-Somali border. No clear space-use differentiation was evident between years, for sharks of different sizes, or between sexes. Whale sharks spent the most time (~66%) in temperatures of 24–30°C and in shallow waters <100 m depth (~60%). Sharks spent relatively more time in cooler (X2 = 121.692; p<0.05) and deeper (X2 = 46.402; p<0.05) water at night. Sharks rarely made dives deeper than 100 m, reflecting the bathymetric constraints of the Gulf environment. Kernel density analysis demonstrated that the tagging site at Al Shaheen was the regional hotspot for these sharks, and revealed a probable secondary aggregation site for whale sharks in nearby Saudi Arabian waters. Analysis of visual re-sightings data of tagged sharks revealed that 58% of tagged individuals were re-sighted back in Al Shaheen over the course of this study, with 40% recorded back at Al Shaheen in the year following their initial identification. Two sharks were confirmed to return to Al Shaheen in each of the five years of study.
Data on the occurrence of whale sharks, Rhincodon typus, in the Arabian Gulf and Gulf of Oman were collected by dedicated boat surveys and via a public-sightings scheme during the period from 2011 to 2014. A total of 422 individual whale sharks were photo-identified from the Arabian Gulf and the northern Gulf of Oman during that period. The majority of sharks (81%, n = 341) were encountered at the Al Shaheen area of Qatar, 90 km off the coast, with the Musandam region of Oman a secondary area of interest. At Al Shaheen, there were significantly more male sharks (n = 171) than females (n = 78; X2 = 17.52, P < 0.05). Mean estimated total length (TL) for sharks was 6.90 m ± 1.24 (median = 7 m; n = 296). Males (7.25 m ± 1.34; median = 8 m, n = 171) were larger than females (6.44 m ±1.09; median = 7 m, n = 78; Mann-Whitney U test, p < 0.01). Of the male sharks assessed for maturity 63% were mature (n = 81), with 50% attaining maturity by 7.29 m and 100% by 9.00 m. Two female sharks of >9 m individuals were visually assessed as pregnant. Connectivity among sharks sighted in Qatari, Omani and UAE waters was confirmed by individual spot pattern matches. A total of 13 identified sharks were re-sighted at locations other than that at which they were first sighted, including movements into and out of the Arabian Gulf through the Strait of Hormuz. Maximum likelihood techniques were used to model an estimated combined population for the Arabian Gulf and Gulf of Oman of 2837 sharks ± 1243.91 S.E. (95% C.I. 1720–6295). The Al Shaheen aggregation is thus the first site described as being dominated by mature males while the free-swimming pregnant females are the first reported from the Indian Ocean.
Environmental DNA (eDNA) provides a promising supplement to traditional sampling methods for population genetic inferences, but current studies have almost entirely focused on short mitochondrial markers. Here, we develop one mitochondrial and one nuclear set of target capture probes for the whale shark (Rhincodon typus) and test them on seawater samples collected in Qatar to investigate the potential of target capture for eDNA‐based population studies. The mitochondrial target capture successfully retrieved ~235× (90× − 352× per base position) coverage of the whale shark mitogenome. Using a minor allele frequency of 5%, we find 29 variable sites throughout the mitogenome, indicative of at least five contributing individuals. We also retrieved numerous mitochondrial reads from an abundant nontarget species, mackerel tuna (Euthynnus affinis), showing a clear relationship between sequence similarity to the capture probes and the number of captured reads. The nuclear target capture probes retrieved only a few reads and polymorphic variants from the whale shark, but we successfully obtained millions of reads and thousands of polymorphic variants with different allele frequencies from E. affinis. We demonstrate that target capture of complete mitochondrial genomes and thousands of nuclear loci is possible from aquatic eDNA samples. Our results highlight that careful probe design, taking into account the range of divergence between target and nontarget sequences as well as presence of nontarget species at the sampling site, is crucial to consider. eDNA sampling coupled with target capture approaches provide an efficient means with which to retrieve population genomic data from aggregating and spawning aquatic species.
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