Mesoscale eddies release pelagic sharks from thermal constraints to foraging in the ocean twilight zone

Author Posting. © National Academy of Sciences, 2019. This article is posted here by permission of National Academy of Sciences for personal use, not for redistribution. The definitive version was published in Proceedings of the National Academy of Sciences 116 (35), (2019): 17187-17192, doi:10.1073/pnas.1903067116.Mesoscale eddies are critical components of the ocean’s “internal weather” system. Mixing and stirring by eddies exerts significant control on biogeochemical fluxes in the open ocean, and eddies may trap distinctive plankton communities that remain coherent for months and can be transported hundreds to thousands of kilometers. Debate regarding how and why predators use fronts and eddies, for example as a migratory cue, enhanced forage opportunities, or preferred thermal habitat, has been ongoing since the 1950s. The influence of eddies on the behavior of large pelagic fishes, however, remains largely unexplored. Here, we reconstruct movements of a pelagic predator, the blue shark (Prionace glauca), in the Gulf Stream region using electronic tags, earth-observing satellites, and data-assimilating ocean forecasting models. Based on >2,000 tracking days and nearly 500,000 high-resolution time series measurements collected by 15 instrumented individuals, we show that blue sharks seek out the interiors of anticyclonic eddies where they dive deep while foraging. Our observations counter the existing paradigm that anticyclonic eddies are unproductive ocean “deserts” and suggest anomalously warm temperatures in these features connect surface-oriented predators to the most abundant fish community on the planet in the mesopelagic. These results also shed light on the ecosystem services provided by mesopelagic prey. Careful consideration will be needed before biomass extraction from the ocean twilight zone to avoid interrupting a key link between planktonic production and top predators. Moreover, robust associations between targeted fish species and oceanographic features increase the prospects for effective dynamic ocean management.We thank D. McGillicuddy, G. Lawson, and G. Flierl for helpful discussions while developing this work and 2 anonymous reviewers whose feedback significantly improved the manuscript. We also thank C. Fischer and the OCEARCH team for their support of this research. This work was funded by awards to C.D.B. from the Martin Family Society of Fellows for Sustainability Fellowship at the Massachusetts Institute of Technology; the Grassle Fellowship and Ocean Venture Fund at the Woods Hole Oceanographic Institution; and the National Aeronatics and Space Administration (NASA) Earth and Space Science Fellowship. C.D.B. and P.G. acknowledge support from the NASA New Investigator Program Award 80NSSC18K0757, and P.G. acknowledges support from NSF Award OCE-1558809. This research is partially supported by funding to S.R.T. as part of the Audacious Project, a collaborative endeavor, housed at TED. We thank donors to the Woods Hole Oceanographic Institution (WHOI) ProjectWHOI crowdfunding campaign: The Secret Lives of Sharks. Computational support was provided by the Amazon Web Services Cloud Credits for Research program. Funding for the development of HYCOM has been provided by the National Ocean Partnership Program and the Office of Naval Research.2020-02-0

Gut microbial communities of hybridising pygmy angelfishes reflect species boundaries

Hybridisation and introgression of eukaryotic genomes can generate new species or subsume existing ones, with direct and indirect consequences for biodiversity. An understudied component of these evolutionary forces is their potentially rapid effect on host gut microbiomes, and whether these pliable microcosms may serve as early biological indicators of speciation. We address this hypothesis in a field study of angelfishes (genus Centropyge), which have one of the highest prevalence of hybridisation within coral reef fish. In our study region of the Eastern Indian Ocean, the parent fish species and their hybrids cohabit and display no differences in their diet, behaviour, and reproduction, often interbreeding in mixed harems. Despite this ecological overlap, we show that microbiomes of the parent species are significantly different from each other in form and function based on total community composition, supporting the division of parents into distinct species, despite the confounding effects of introgression acting to homogenize parent species identity at other molecular markers. The microbiome of hybrid individuals, on the other hand, are not significantly different to each of the parents, instead harbouring an intermediate community composition. These findings suggest that shifts in gut microbiomes may be an early indicator of speciation in hybridising species

Comparative phylogeography of reef fishes from the Gulf of Aden to the Arabian Sea reveals two cryptic lineages

Arabian Sea is a heterogeneous region with high coral cover and warm stable conditions at the western end (Djibouti), in contrast to sparse coral cover, cooler temperatures, and upwelling at the eastern end (southern Oman). We tested for barriers to dispersal across this region (including the Gulf of Aden and Gulf of Oman), using mitochondrial DNA surveys of 11 reef fishes. Study species included seven taxa from six families with broad distributions across the Indo-Pacific and four species restricted to the Arabian Sea (and adjacent areas). Nine species showed no significant genetic partitions, indicating connectivity among contrasting environments spread across 2000 km. One butterflyfish (Chaetodon melannotus) and a snapper (Lutjanus kasmira) showed phylogenetic divergences of d = 0.008 and 0.048, respectively, possibly indicating cryptic species within these broadly distributed taxa. These genetic partitions at the western periphery of the Indo-Pacific reflect similar partitions recently discovered at the eastern periphery of the Indo-Pacific (the Hawaiian and the Marquesan Archipelagos), indicating that these disjunctive habitats at the ends of the range may serve as evolutionary incubators for coral reef organisms. © 2017 Springer-Verlag Berlin HeidelbergTh

Data from: Assessing the utility of eDNA as a tool to survey reef-fish communities in the Red Sea

Relatively small volumes of water may contain sufficient environmental DNA (eDNA) to detect target aquatic organisms via genetic sequencing. We therefore assessed the utility of eDNA to document the diversity of coral reef fishes in the central Red Sea. DNA from seawater samples was extracted, amplified using fish-specific 16S mitochondrial DNA primers, and sequenced using a metabarcoding workflow. DNA sequences were assigned to taxa using available genetic repositories or custom genetic databases generated from reference fishes. Our approach revealed a diversity of conspicuous, cryptobenthic, and commercially relevant reef fish at the genus level, with select genera in the family Labridae over-represented. Our approach, however, failed to capture a significant fraction of the fish fauna known to inhabit the Red Sea, which we attribute to limited spatial sampling, amplification stochasticity, and an apparent lack of sequencing depth. Given an increase in fish species descriptions, completeness of taxonomic checklists, and improvement in species-level assignment with custom genetic databases as shown here, we suggest that the Red Sea region may be ideal for further testing of the eDNA approach

Conspicuous and cryptic reef fishes from a unique and economically important region in the northern Red Sea.

Al Wajh Bank in the northern Red Sea contains an extensive coral reef system that potentially supports a novel fish community. The large (1500km2) and shallow (< 40m depth) lagoon experiences greater temperature and salinity fluctuations, as well as higher turbidity, than most other Red Sea reefs. Since these conditions often influence coral community structure and introduce physiological challenges to its resident organisms, changes in reef-associated fishes are expected. We present critical baseline data on fish biodiversity and benthic composition for the Al Wajh Bank. Underwater visual census of conspicuous fishes and standardized collections of cryptobenthic fishes were combined to provide a comprehensive assessment of these fish communities. We documented 153 fish species and operational taxonomic units, including undescribed species, within 24 families on reefs largely dominated by hard coral and soft sediment (39% and 32% respectively). The families Pomacentridae and Gobiidae contributed the most towards fish diversity and abundance. Bray-Curtis dissimilarity distances among sampled sites suggest a distinctive fish community within the lagoon, and coefficients of variation for each species show high variation in their distribution across the lagoon. Species accumulation curves predict that additional sampling would document many more species throughout Al Wajh. Our findings provide the most extensive biodiversity survey of fishes from this region to date and record the condition of the reef prior to major coastal development planned to occur in the near future

Comparative demography of commercially important species of coral grouper, Plectropomus leopardus and P. laevis, from Australia's great barrier reef and Coral Sea marine parks

Understanding the spatial and environmental variation in demographic processes of fisheries target species, such as coral grouper (Genus: Plectropomus), is important for establishing effective management and conservation strategies. Herein we compare the demography of Plectropomus leopardus and P. laevis between Australia's Great Barrier Reef Marine Park (GBRMP), which has been subject to sustained and extensive fishing pressure, and the oceanic atolls of Australia's Coral Sea Marine Park (CSMP), where there is very limited fishing for reef fishes. Coral grouper length‐at‐age data from contemporary and historical otolith collections across 9.4 degrees of latitude showed little difference in lifetime growth between GBRMP and CSMP regions. Plectropomus laevis populations in GBRMP reefs had significantly higher rates of total mortality than populations in the CSMP. Mean maximum lengths and mean maximum ages of P. laevis were also smaller in the GBRMP than in the CSMP, even when considering populations sampled within GBRMP no‐take marine reserves (NTMRs). Plectropomus leopardus, individuals were on average smaller on fished reefs than NTMRs in the GBRMP, but all other aspects of demography were broadly similar between regions despite the negligible levels of fishing pressure in the CSMP. Similarities between regions in growth profiles and length‐at‐age comparisons of P. laevis and P. leopardus suggest that the environmental differences between the CSMP and the GBRMP may not have significant impacts on lifetime growth. Our results show that fishing may have influenced the demography of coral grouper on the GBR, particularly for the slower growing and longer lived species, P. laevis

Regional versus latitudinal variation in the life-history traits and demographic rates of a reef fish, Centropyge bispinosa, in the Coral Sea and Great Barrier Reef Marine Parks, Australia

Environmental temperature is an important determinant of physiological processes and life histories in ectotherms. Over latitudinal scales, variation in temperature has been linked to changes in life-history traits and demographic rates, with growth and mortality rates generally being greatest at low latitudes, and longevity and maximum length being greater at higher latitudes. Using the two-spined angelfish, Centropyge bispinosa, as our focal species, we compared growth patterns, growth rates, longevity, mortality, asymptotic length and maximum length across 22 reefs that span 13° of latitude within the Great Barrier Reef Marine Park (GBRMP) and the Coral Sea Marine Park (CSMP), Australia. We found no predictable latitudinal variation in mortality rates, growth patterns, growth rates, asymptotic or maximum length of C. bispinosa at regional to biogeographic scales. However, C. bispinosa consistently exhibited reduced longevity at lower, warmer latitudes within the CSMP. The greatest differences in mean maximum length of C. bispinosa were between continental (GBRMP) and oceanic (central CSMP) reefs of similar latitude, with individuals being larger on average on continental versus oceanic reefs. The lack of predictable life-history and demographic variation in C. bispinosa across a 13° latitudinal gradient within the CSMP, coupled with differences in mean maximum length between continental and oceanic reefs at similar latitudes, suggest that local environmental conditions have a greater influence than environmental temperature on the demographic rates and life-history traits of C. bispinosa

Unfiltered 16S fish mitochondrial DNA sequences amplified from seawater samples collected in the Red Sea

Unfiltered 16S fish mitochondrial DNA sequences amplified from seawater samples collected at inshore, midshore, and offshore coral reefs, as well as a boat harbor along the central Red Sea coastline near Thuwal, Saudi Arabia. File names are structured as follows: sequencingrun_gene_samplesource_sitename_sampleID_forwardMIDtag_reverseMIDtag. Example: FTP77_Fish16S_Water_TahlaNorthExposed_AWFSF151469_F750_R637

Data from: Acoustic telemetry reveals cryptic residency of whale sharks

Although whale sharks (Rhincodon typus) have been documented to move thousands of kilometres, they are most frequently observed at a few predictable seasonal aggregation sites. The absence of sharks at the surface during visual surveys has led to the assumption that sharks disperse to places unknown during the long ‘off-seasons’ at most of these locations. Here we compare 2 years of R. typus visual sighting records from Mafia Island in Tanzania to concurrent acoustic telemetry of tagged individuals. Sightings revealed a clear seasonal pattern with a peak between October and February and no sharks observed at other times. By contrast, acoustic telemetry demonstrated year-round residency of R. typus. The sharks use a different habitat in the off-season, swimming deeper and further away from shore, presumably in response to prey distributions. This behavioural change reduces the sharks' visibility, giving the false impression that they have left the area. We demonstrate, for the first time to our knowledge, year-round residency of unprovisioned, individual R. typus at an aggregation site, and highlight the importance of using multiple techniques to study the movement ecology of marine megafauna