John A. Musick

The Biology of Sea Turtles

Physiology as Integrated Systems Amanda Southwood Williard Vision Kerstin A. Fritsches and Eric J. Warrant Natal Homing and Imprinting in Sea Turtles Kenneth J. Lohmann, Catherine M.F. Lohmann, J. Roger Brothers, and Nathan F. Putman The Skeleton: An In Vivo View of Structure Jeanette Wyneken Age and Age Estimation in Sea Turtles Larisa Avens and Melissa L. Snover Molecular Genetics of Sea Turtles Michael P. Jensen, Nancy N. FitzSimmons, and Peter H. Dutton Oceanic Habits and Habitats: Dermochelys coriacea Vincent S. Saba Oceanic Habits and Habitats: Caretta caretta Katherine L. Mansfield and Nathan F. Putman Feeding Biology: Advances from Field-Based Observations, Physiological Studies, and Molecular Techniques T. Todd Jones and Jeffrey A. Seminoff Predators, Prey, and the Ecological Roles of Sea Turtles Michael R. Heithaus Exposure to and Effects of Persistent Organic Pollutants Jennifer M. Keller Fisheries Bycatch of Marine Turtles: Lessons Learned from Decades of Research and Conservation Rebecca Lewison, Bryan Wallace, Joana Alfaro-Shigueto, Jeff Mangel, Sara Maxwell, and Elliott Hazen Climate Change and Marine Turtles Mark Hamann, Mariana M.P.B. Fuentes, Natalie C. Ban, and Veronique J.L. Mocellin Free-Ranging Sea Turtle Health Mark Flint Sea Turtle Epibiosis Michael G. Frick and Joseph B. Pfaller Parasites of Marine Turtles Ellis C. Greiner Index

Extinction risk and conservation of the world’s sharks and rays

The rapid expansion of human activities threatens ocean-wide biodiversity. Numerous marine animal populations have declined, yet it remains unclear whether these trends are symptomatic of a chronic accumulation of global marine extinction risk. We present the first systematic analysis of threat for a globally distributed lineage of 1,041 chondrichthyan fishes—sharks, rays, and chimaeras. We estimate that one-quarter are threatened according to IUCN Red List criteria due to overfishing (targeted and incidental). Large-bodied, shallow-water species are at greatest risk and five out of the seven most threatened families are rays. Overall chondrichthyan extinction risk is substantially higher than for most other vertebrates, and only one-third of species are considered safe. Population depletion has occurred throughout the world’s ice-free waters, but is particularly prevalent in the Indo-Pacific Biodiversity Triangle and Mediterranean Sea. Improved management of fisheries and trade is urgently needed to avoid extinctions and promote population recovery. DOI: http://dx.doi.org/10.7554/eLife.00590.001

Biology of sharks and their relatives

Phylogeny and Zoogeography The Origin and Relationships of Early Chondrichthyans Eileen D. Grogan, Richard Lund, and Emily Greenfest-Allen Elasmobranch Phylogeny: A Mitochondrial Estimate Based on 595 Species Gavin J.P. Naylor, Janine N. Caira, Kirsten Jensen, Kerri A.M. Rosana, Nicolas Straube, and Clemens Lakner Phylogeny of Batoidea Neil C. Aschliman, Kerin M. Claeson, and John D. McEachran Phylogeny, Biology, and Classification of Extant Holocephalans Dominique A. Didier, Jenny M. Kemper, and David A. Ebert Form, Function, and Physiological Processes Biomechanics of Locomotion in Sharks, Rays, and Chimeras Anabela M.R. Maia, Cheryl A.D. Wilga, and George V. Lauder Prey Capture Behavior and Feeding Mechanics of Elasmobranchs Philip J. Motta and Daniel R. Huber Energetics, Metabolism, and Endothermy in Sharks and Rays Diego Bernal, John K. Carlson, Kenneth J. Goldman, and Christopher G. Lowe Food Consumption and Feeding Habits Bradley M. Wetherbee, Enric Cortes, and Joseph J. Bizzarro Integrative Multisensor Tagging: Emerging Techniques to Link Elasmobranch Behavior, Physiology, and Ecology Nicholas M. Whitney, Yannis P. Papastamatiou, Adrian C. Gleiss Reproductive Biology of Elasmobranchs Christina L. Conrath and John A. Musick Hormonal Regulation of Elasmobranch Physiology James Gelsleichter and Andrew N. Evans Sensory Physiology and Behavior of Elasmobranchs Jayne M. Gardiner, Robert E. Hueter, Karen P. Maruska, Joseph A. Sisneros, Brandon M. Casper, David A. Mann, Leo S. Demski Recent Advances in Elasmobranch Immunology Carl A. Luer, Catherine J. Walsh, and Ashby B. Bodine Ecology and Life History Assessing the Age and Growth of Chondrichthyan Fishes Kenneth J. Goldman, Gregor M. Cailliet, Allen H. Andrews, and Lisa J. Natanson Population Dynamics, Demography, and Stock Assessment Enric Cortes, Elizabeth N. Brooks, and Todd Gedamke Genetics of Sharks, Skates, and Rays Edward J. Heist Predator-Prey Interactions Michael R. Heithaus and Jeremy J. Vaudo An Updated Look at Elasmobranchs as Hosts of Metazoan Parasites Janine N. Caira, Claire J. Healy, and Kirsten Jensen Assessing Habitat Use and Movement Colin A. Simpfendorfer and Michelle R. Heupel Index

Global Conservation Priorities for Marine Turtles

Where conservation resources are limited and conservation targets are diverse, robust yet flexible priority-setting frameworks are vital. Priority-setting is especially important for geographically widespread species with distinct populations subject to multiple threats that operate on different spatial and temporal scales. Marine turtles are widely distributed and exhibit intra-specific variations in population sizes and trends, as well as reproduction and morphology. However, current global extinction risk assessment frameworks do not assess conservation status of spatially and biologically distinct marine turtle Regional Management Units (RMUs), and thus do not capture variations in population trends, impacts of threats, or necessary conservation actions across individual populations. To address this issue, we developed a new assessment framework that allowed us to evaluate, compare and organize marine turtle RMUs according to status and threats criteria. Because conservation priorities can vary widely (i.e. from avoiding imminent extinction to maintaining long-term monitoring efforts) we developed a “conservation priorities portfolio” system using categories of paired risk and threats scores for all RMUs (n = 58). We performed these assessments and rankings globally, by species, by ocean basin, and by recognized geopolitical bodies to identify patterns in risk, threats, and data gaps at different scales. This process resulted in characterization of risk and threats to all marine turtle RMUs, including identification of the worlds 11 most endangered marine turtle RMUs based on highest risk and threats scores. This system also highlighted important gaps in available information that is crucial for accurate conservation assessments. Overall, this priority-setting framework can provide guidance for research and conservation priorities at multiple relevant scales, and should serve as a model for conservation status assessments and priority-setting for widespread, long-lived taxa.

Regional Management Units for Marine Turtles: A Novel Framework for Prioritizing Conservation and Research across Multiple Scales

Background Resolving threats to widely distributed marine megafauna requires definition of the geographic distributions of both the threats as well as the population unit(s) of interest. In turn, because individual threats can operate on varying spatial scales, their impacts can affect different segments of a population of the same species. Therefore, integration of multiple tools and techniques — including site-based monitoring, genetic analyses, mark-recapture studies and telemetry — can facilitate robust definitions of population segments at multiple biological and spatial scales to address different management and research challenges. Methodology/Principal Findings To address these issues for marine turtles, we collated all available studies on marine turtle biogeography, including nesting sites, population abundances and trends, population genetics, and satellite telemetry. We georeferenced this information to generate separate layers for nesting sites, genetic stocks, and core distributions of population segments of all marine turtle species. We then spatially integrated this information from fine- to coarse-spatial scales to develop nested envelope models, or Regional Management Units (RMUs), for marine turtles globally. Conclusions/Significance The RMU framework is a solution to the challenge of how to organize marine turtles into units of protection above the level of nesting populations, but below the level of species, within regional entities that might be on independent evolutionary trajectories. Among many potential applications, RMUs provide a framework for identifying data gaps, assessing high diversity areas for multiple species and genetic stocks, and evaluating conservation status of marine turtles. Furthermore, RMUs allow for identification of geographic barriers to gene flow, and can provide valuable guidance to marine spatial planning initiatives that integrate spatial distributions of protected species and human activities. In addition, the RMU framework — including maps and supporting metadata — will be an iterative, user-driven tool made publicly available in an online application for comments, improvements, download and analysis.

Marine, Estuarine, and Diadromous Fish Stocks at Risk of Extinction in North America (Exclusive of Pacific Salmonids)

This initiative was supported by grants to AFS and the Virginia Institute of Marine Science by the Pew Charitable Trusts, NMFS Office of Protected Resources, National Fish and Wildlife Foundation, The Munson Foundation and the Homeland Foundation, J.A. Musick, Principal investigator.

Age and Growth of the Sandbar Shark, Carcharhinus plumbeus, before and after Population Depletion

Recent studies have shown that by 1991 the sandbar shark (Carcharhinus plumbeus) population along the Atlantic coast of the United States had declined in abundance to approximately 20% of its level in the late 1970s. This phenomenon allowed us to test the hypothesis that compensatory (density-dependent) growth occurred after severe population reduction. Age and growth of sandbar sharks were investigated by counting rings and back-calculating lengths at previous ages from vertebral samples collected in 1980-1981 and 1991-1992. The collections included 188 sharks from 1980-1981 and 412 sharks from 1990-1991 ranging in length from 51-172 cm precaudal length (PCL). All sharks were mature at lengths > 136 cm PCL. Minimum and maximum ring counts, which included a birth mark, were 1 and 25. Age at maturity was 15-16 years for both sample periods and both sexes. For sexes combined, the von Bertalanffy growth parameters were L,. = 199 cm PCL, K = 0.057, to = -4.9 years for the 1980-1981 sample and L,. = 164 cm PCL, K = 0.089, to = -3.8 years for the 1991-1992 sample. Statistical tests found significant differences between the two growth models. Significant differences in size at age and annual incremental growth of juveniles suggest a small increase in juvenile sandbar shark growth rate between the two sampling periods. However, age at maturity was unchanged between samples suggesting that any biological significance of a growth rate increase has not been realized.

Natal homing in juvenile loggerhead turtles (Caretta caretta)

Juvenile loggerhead turtles (Caretta caretta) from West Atlantic nesting beaches occupy oceanic (pelagic) habitats in the eastern Atlantic and Mediterranean, whereas larger juvenile turtles occupy shallow (neritic) habitats along the continental coastline of North America. Hence the switch from oceanic to neritic stage can involve a trans‐oceanic migration. Several researchers have suggested that at the end of the oceanic phase, juveniles are homing to feeding habitats in the vicinity of their natal rookery. To test the hypothesis of juvenile homing behaviour, we surveyed 10 juvenile feeding zones across the eastern USA with mitochondrial DNA control region sequences (N = 1437) and compared these samples to potential source (nesting) populations in the Atlantic Ocean and Mediterranean Sea (N = 465). The results indicated a shallow, but significant, population structure of neritic juveniles (ΦST = 0.0088, P = 0.016), and haplotype frequency differences were significantly correlated between coastal feeding populations and adjacent nesting populations (Mantel test R2 = 0.52, P = 0.001). Mixed stock analyses (using a Bayesian algorithm) indicated that juveniles occurred at elevated frequency in the vicinity of their natal rookery. Hence, all lines of evidence supported the hypothesis of juvenile homing in loggerhead turtles. While not as precise as the homing of breeding adults, this behaviour nonetheless places juvenile turtles in the vicinity of their natal nesting colonies. Some of the coastal hazards that affect declining nesting populations may also affect the next generation of turtles feeding in nearby habitats.

Is the collapse of shark populations in the Northwest Atlantic Ocean and Gulf of Mexico real

Abstract Increasing fishing pressure on sharks stocks over recent decades has resulted in declines of many populations and led to increasing concerns for their conservation. The extent of these declines, however, has been highly variable—the result of the level of fishing, ocean conditions, and the life history of individual species. Two recent articles have described the collapse and possible extirpation of shark populations in the northwest Atlantic Ocean and Gulf of Mexico. Herein, we examine the results of these two papers commenting on the data sets used, comparing them to other available data sets, and critically evaluating the analyses and conclusions. We argue that these conclusions have been overstated because: (1) the analyses were based on a limited number of data sets, (2) the data sets themselves are inadequate to describe the status of all shark populations in the northwest Atlantic Ocean and Gulf of Mexico reported in these studies, (3) available data sets that could produce different concl...

Feeding strategies of some demersal fishes of the continental slope and rise off the Mid-Atlantic Coast of the USA

Stomach contents of 729 fishes comprising 16 species were examined from the continental slope and rise off the Middle Atlantic States of the USA. Two main feeding modes among demersal deep-sea fishes were evident: those feeding primarily on pelagic food items, and those feeding on benthic invertebrates. Both pelagic and benthic predators were euryphagous. Most pelagic predators also fed on the epibenthos. These findings support Dayton and Hesslers (1972) suggestion that benthic predators should have a generalized diet which may be responsible for the high diversity found in the deep-sea infauna. The mesopelagic fauna is an important food source for some demersal fishes on the continental slope. Pelagic prey, which are also important to ecologically dominant demersal fishes on the lower slope and continental rise, may be nutritionally supported by suspended particulate organic matter in a nepheloid layer close to the bottom, and they may exist in much higher concentrations than in the bathypelagic zone above.