Movements and oceanographic associations of large pelagic fishes in the North Atlantic Ocean

Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy at the Massachusetts Institute of Technology and the Woods Hole Oceanographic Institution September 2018Highly migratory marine fishes support valuable commercial fisheries worldwide. Yet, many target species have proven difficult to study due to long-distance migrations and regular deep diving. Despite the dominance of oceanographic features, such as fronts and eddies, in the open ocean, the biophysical interactions occurring at the oceanic (sub)mesoscale (< 100 km) remain poorly understood. This leads to a paucity of knowledge on oceanographic associations of pelagic fishes and hinders management efforts. With ever-improving oceanographic datasets and modeling outputs, we can leverage these tools both to derive better estimates of animal movements and to quantify fish-environment interactions. In this thesis, I developed analytical tools to characterize the biophysical interactions influencing animal behavior and species’ ecology in the open ocean. A novel, observation-based likelihood framework was combined with a Bayesian state-space model to improve geolocation estimates for archival-tagged fishes using oceanographic profile data. Using this approach, I constructed track estimates for a large basking shark tag dataset using a high-resolution oceanographic model and discovered a wide range of movement strategies. I also applied this modeling approach to track archival-tagged swordfish, which revealed affinity for thermal front and eddy habitats throughout the North Atlantic that was further corroborated by synthesizing these results with a fisheries-dependent conventional tag dataset. An additive modeling approach applied to longline catch-per-unit effort data further highlighted the biophysical interactions that characterize variability in swordfish catch. In the final chapter, I designed a synergistic analysis of high-resolution, 3D shark movements and satellite observations to quantify the influence of mesoscale oceanography on blue shark movements and behavior. This work demonstrated the importance of eddies in structuring the pelagic ocean by influencing the movements of an apex predator and governing the connectivity between deep scattering layer communities and deep-diving, epipelagic predators. Together, these studies demonstrate the breadth and depth of information that can be garnered through the integration of traditional animal tagging and oceanographic research with cutting-edge analytical approaches and high-resolution oceanographic model and remote sensing datasets, the product of which provides a transformative view of the biophysical interactions occurring in and governing the structure of the pelagic ocean.Supported by the NASA Earth and Space Science Fellowship, the MIT John S. Hennessy Fellowship, the MIT Martin Family Society of Fellows for Sustainability Fellowship, the WHOI Ocean Venture, Grassle, and James Stratton Fellowships and the WHOI Academic Programs Office. This research and its dissemination was supported by funds from National Geographic, Amazon Web Services, the Explorers Club, Rolex, Sigma Xi, the MIT Center for International Studies, WHOI Access to the Sea and Coastal Ocean Institute Funds, MIT Graduate Student Council, MIT Student Assistance Fund, WHOI Biology Department, American Fisheries Society, WHOI Academic Programs Offic

HMMoce : an R package for improved geolocation of archival-tagged fishes using a hidden Markov method

Author Posting. © The Author(s), 2017. This is the author's version of the work. It is posted here under a nonexclusive, irrevocable, paid-up, worldwide license granted to WHOI. It is made available for personal use, not for redistribution. The definitive version was published in Methods in Ecology and Evolution 9 (2018): 1212-1220, doi:10.1111/2041-210X.12959.Electronic tagging of marine fishes is commonly achieved with archival tags that rely on light levels and sea surface temperatures to retrospectively estimate movements. However, methodological issues associated with light-level geolocation have constrained meaningful inference to species where it is possible to accurately estimate time of sunrise and sunset. Most studies have largely ignored the oceanographic profiles collected by the tag as a potential way to refine light-level geolocation estimates. Open-source oceanographic measurements and outputs from high-resolution models are increasingly available and accessible. Temperature and depth profiles recorded by electronic tags can be integrated with these empirical data and model outputs to construct likelihoods and improve geolocation estimates. The R package HMMoce leverages available tag and oceanographic data to improve position estimates derived from electronic tags using a hidden Markov approach. We illustrate the use of the model and test its performance using example blue and mako shark archival tag data. Model results were validated using independent, known tracks and compared to results from other geolocation approaches. HMMoce exhibited as much as 6-fold improvement in pointwise error as compared to traditional light-level geolocation approaches. The results demonstrated the general applicability of HMMoce to marine animals, particularly those that do not frequent surface waters during crepuscular periods.This work was funded by awards to C. Braun 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 NASA Earth and Space Science Fellowship

Movements of the white shark Carcharodon carcharias in the North Atlantic Ocean

© The Author(s), 2017. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Marine Ecology Progress Series 580 (2017): 1-16, doi:10.3354/meps12306.In the western North Atlantic, much of what is known about the movement ecology of the white shark Carcharodon carcharias is based on historical fisheries-dependent catch records, which portray a shelf-oriented species that moves north and south seasonally. In this study, we tagged 32 white sharks (16 females, 7 males, 9 unknown), ranging from 2.4 to 5.2 m total length, with satellite-based tags to investigate broad-scale movements in the North Atlantic. Based on 10427 days of tracking data, we found that white sharks are more broadly distributed, both horizontally and vertically, throughout the North Atlantic than previously understood, exhibiting an ontogenetic shift from near-coastal, shelf-oriented habitat to pelagic habitat with frequent excursions to mesopelagic depths. During the coastal phase, white sharks migrated seasonally from the northeast shelf in the summer to overwintering habitat off the southeastern US and the Gulf of Mexico, spending 95% of their time at <50 m depth. During the pelagic phase, subadult and adult white sharks exhibited wide-ranging movements during the fall, winter, and spring into the broader Atlantic over a 30° latitudinal range and as far east as the Azores. These sharks moved daily to depths of up to 1128 m, spending significant time at specific mesopelagic depth zones through a temperature range of 1.6 to 30.4°C. We believe these movements are associated with offshore foraging facilitated by the thermal physiology of the species. Our findings extend the known essential habitat for the white shark in the North Atlantic beyond existing protection, with implications for future conservation.This research was funded by Federal Aid in Sport Fish Restoration, the National Science Foundation (OCE-0825148), the John J. Sacco and Edith L. Sacco Charitable Foundation, the Atlantic White Shark Conservancy, the Massachusetts Environmental Trust, Discovery Communications, National Geographic, and the Woods Hole Oceanographic Institution

Horizontal and vertical movement patterns and habitat use of juvenile porbeagles (Lamna nasus) in the Western North Atlantic

© The Author(s), 2021. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Skomal, G., Marshall, H., Galuardi, B., Natanson, L., Braun, C. D., & Bernal, D. Horizontal and vertical movement patterns and habitat use of juvenile porbeagles (Lamna nasus) in the Western North Atlantic. Frontiers in Marine Science, 8,(2021): 624158, https://doi.org/10.3389/fmars.2021.624158.The porbeagle (Lamna nasus) is a large, highly migratory endothermic shark broadly distributed in the higher latitudes of the Atlantic, South Pacific, and Indian Oceans. In the North Atlantic, the porbeagle has a long history of fisheries exploitation and current assessments indicate that this stock is severely overfished. Although much is known of the life history of this species, there is little fisheries-independent information about habitat preferences and ecology. To examine migratory routes, vertical behavior, and environmental associations in the western North Atlantic, we deployed pop-up satellite archival transmitting tags on 20 porbeagles in late November, 2006. The sharks, ten males and ten females ranging from 128 to 154 cm fork length, were tagged and released from a commercial longline fishing vessel on the northwestern edge of Georges Bank, about 150 km east of Cape Cod, MA. The tags were programmed to release in March (n = 7), July (n = 7), and November (n = 6) of 2007, and 17 (85%) successfully reported. Based on known and derived geopositions, the porbeagles exhibited broad seasonally-dependent horizontal and vertical movements ranging from minimum linear distances of 937 to 3,310 km and from the surface to 1,300 m, respectively. All of the sharks remained in the western North Atlantic from the Gulf of Maine, the Scotian Shelf, on George's Bank, and in the deep, oceanic waters off the continental shelf along the edge of, and within, the Gulf Stream. In general, the population appears to be shelf-oriented during the summer and early fall with more expansive offshore radiation in the winter and spring. Although sharks moved through temperatures ranging from 2 to 26°C, the bulk of their time (97%) was spent in 6-20°C. In the summer months, most of the sharks were associated with the continental shelf moving between the surface and the bottom and remaining < 200 m deep. In the late fall and winter months, the porbeagles moved into pelagic habitat and exhibited two behavioral patterns linked with the thermal features of the Gulf Stream: “non-divers” (n = 7) largely remained at epipelagic depths and “divers” (n = 10) made frequent dives into and remained at mesopelagic depths (200–1000 m). These data demonstrate that juvenile porbeagles are physiologically capable of exploiting the cool temperate waters of the western North Atlantic as well as the mesopelagic depths of the Gulf Stream, possibly allowing exploitation of prey not available to other predators.This research was funded by the Large Pelagics Research Center (Grant 06-125)

Movement patterns of juvenile whale sharks tagged at an aggregation site in the Red Sea

© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 9 (2014): e103536, doi:10.1371/journal.pone.0103536.Conservation efforts aimed at the whale shark, Rhincodon typus, remain limited by a lack of basic information on most aspects of its ecology, including global population structure, population sizes and movement patterns. Here we report on the movements of 47 Red Sea whale sharks fitted with three types of satellite transmitting tags from 2009–2011. Most of these sharks were tagged at a single aggregation site near Al-Lith, on the central coast of the Saudi Arabian Red Sea. Individuals encountered at this site were all juveniles based on size estimates ranging from 2.5–7 m total length with a sex ratio of approximately 1:1. All other known aggregation sites for juvenile whale sharks are dominated by males. Results from tagging efforts showed that most individuals remained in the southern Red Sea and that some sharks returned to the same location in subsequent years. Diving data were recorded by 37 tags, revealing frequent deep dives to at least 500 m and as deep as 1360 m. The unique temperature-depth profiles of the Red Sea confirmed that several whale sharks moved out of the Red Sea while tagged. The wide-ranging horizontal movements of these individuals highlight the need for multinational, cooperative efforts to conserve R. typus populations in the Red Sea and Indian Ocean.Financial support was provided in part by KAUST baseline research funds (to MLB), KAUST award nos. USA00002 and KSA 00011 (to SRT), and the United States National Science Foundation (OCE 0825148 to SRT and GBS)

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

Reef-fidelity and migration of tiger sharks, Galeocerdo cuvier, across the Coral Sea

© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS One 9 (2014): e83249, doi:10.1371/journal.pone.0083249.Knowledge of the habitat use and migration patterns of large sharks is important for assessing the effectiveness of large predator Marine Protected Areas (MPAs), vulnerability to fisheries and environmental influences, and management of shark–human interactions. Here we compare movement, reef-fidelity, and ocean migration for tiger sharks, Galeocerdo cuvier, across the Coral Sea, with an emphasis on New Caledonia. Thirty-three tiger sharks (1.54 to 3.9 m total length) were tagged with passive acoustic transmitters and their localised movements monitored on receiver arrays in New Caledonia, the Chesterfield and Lord Howe Islands in the Coral Sea, and the east coast of Queensland, Australia. Satellite tags were also used to determine habitat use and movements among habitats across the Coral Sea. Sub-adults and one male adult tiger shark displayed year-round residency in the Chesterfields with two females tagged in the Chesterfields and detected on the Great Barrier Reef, Australia, after 591 and 842 days respectively. In coastal barrier reefs, tiger sharks were transient at acoustic arrays and each individual demonstrated a unique pattern of occurrence. From 2009 to 2013, fourteen sharks with satellite and acoustic tags undertook wide-ranging movements up to 1114 km across the Coral Sea with eight detected back on acoustic arrays up to 405 days after being tagged. Tiger sharks dove 1136 m and utilised three-dimensional activity spaces averaged at 2360 km3. The Chesterfield Islands appear to be important habitat for sub-adults and adult male tiger sharks. Management strategies need to consider the wide-ranging movements of large (sub-adult and adult) male and female tiger sharks at the individual level, whereas fidelity to specific coastal reefs may be consistent across groups of individuals. Coastal barrier reef MPAs, however, only afford brief protection for large tiger sharks, therefore determining the importance of other oceanic Coral Sea reefs should be a priority for future research.Funding was provided by the the Agence Francaise de Développement (http://www.afd.fr), French Pacific Fund, the CRISP program (www.crisponline.info) and QLD Fisheries

Vertical movements of a pelagic thresher shark (Alopias pelagicus): insights into the species' physiological limitations and trophic ecology in the Red Sea

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Arostegui, M. C., Gaube, P., Berumen, M. L., DiGiulian, A., Jones, B. H., Rostad, A., & Braun, C. D. Vertical movements of a pelagic thresher shark (Alopias pelagicus): insights into the species' physiological limitations and trophic ecology in the Red Sea. Endangered Species Research, 43, (2020): 387-394, https://doi.org/10.3354/esr01079.The pelagic thresher shark Alopias pelagicus is an understudied elasmobranch harvested in commercial fisheries of the tropical Indo-Pacific. The species is endangered, overexploited throughout much of its range, and has a decreasing population trend. Relatively little is known about its movement ecology, precluding an informed recovery strategy. Here, we report the first results from an individual pelagic thresher shark outfitted with a pop-up satellite archival transmitting (PSAT) tag to assess its movement with respect to the species’ physiology and trophic ecology. A 19 d deployment in the Red Sea revealed that the shark conducted normal diel vertical migration, spending the majority of the day at 200-300 m in the mesopelagic zone and the majority of the night at 50-150 m in the epipelagic zone, with the extent of these movements seemingly not constrained by temperature. In contrast, the depth distribution of the shark relative to the vertical distribution of oxygen suggested that it was avoiding hypoxic conditions below 300 m even though that is where the daytime peak of acoustic backscattering occurs in the Red Sea. Telemetry data also indicated crepuscular and daytime overlap of the shark’s vertical habitat use with distinct scattering layers of small mesopelagic fishes and nighttime overlap with nearly all mesopelagic organisms in the Red Sea as these similarly undergo nightly ascents into epipelagic waters. We identify potential depths and diel periods in which pelagic thresher sharks may be most susceptible to fishery interactions, but more expansive research efforts are needed to inform effective management.This research was funded by a KAUST Center Part-nership Fund award (4107.3 to the Red Sea Research Cen-ter) and KAUST baseline funding (B.H.J. and M.L.B.).M.C.A. and P.G. acknowledge support from NOAA projectNA15OAR4320063. This study was conducted under a pro-tocol approved by the University of Washington’s Institu-tional Animal Care and Use Committee

Extreme diving behaviour in devil rays links surface waters and the deep ocean

© The Author(s), 2014. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Nature Communications 5 (2014): 4274, doi:10.1038/ncomms5274.Ecological connections between surface waters and the deep ocean remain poorly studied despite the high biomass of fishes and squids residing at depths beyond the euphotic zone. These animals likely support pelagic food webs containing a suite of predators that include commercially important fishes and marine mammals. Here we deploy pop-up satellite archival transmitting tags on 15 Chilean devil rays (Mobula tarapacana) in the central North Atlantic Ocean, which provide movement patterns of individuals for up to 9 months. Devil rays were considered surface dwellers but our data reveal individuals descending at speeds up to 6.0 m s−1 to depths of almost 2,000 m and water temperatures <4 °C. The shape of the dive profiles suggests that the rays are foraging at these depths in deep scattering layers. Our results provide evidence of an important link between predators in the surface ocean and forage species occupying pelagic habitats below the euphotic zone in ocean ecosystems.This research was partially supported by the Portuguese Foundation for Science and Technology/Ministry of Education and Science (FCT/MCTES-MEC) through individual support to P.A. (Cieˆncia 2008/POPH/QREN) and J.F. (SFRH/BPD/66532/2009) and the LARSyS Strategic Project (PEst/OE/EEI/LA00009/2011). This study was support by the US National Science Foundation (OCE 0825148 to S.R.T. and G.B.S.), The Harrison Foundation, Rodney and Elizabeth Berens, the King Abdullah University of Science and Technology (baseline research funds to M.L.B.) and the Woods Hole Oceanographic Institution

Remote marine protected area reveals unusual social behaviour in Chaetodon trifascialis

Author Posting. © The Author(s), 2016. This is the author's version of the work. It is posted here by permission of Springer for personal use, not for redistribution. The definitive version was published in Marine Biodiversity 48 (2018): 155-156, doi:10.1007/s12526-016-0531-0.The research expedition was funded by New England Aquarium, Woods Hole Oceanographic Institution and King Abdullah University of Science and Technology