World phylogeography and male-mediated gene flow in the sandbar shark, Carcharhinus plumbeus.

The sandbar shark, Carcharhinus plumbeus, is a large, cosmopolitan, coastal species. Females are thought to show philopatry to nursery grounds while males potentially migrate long distances, creating an opportunity for male-mediated gene flow that may lead to discordance in patterns revealed by mitochondrial DNA (mtDNA) and nuclear markers. While this dynamic has been investigated in elasmobranchs over small spatial scales, it has not been examined at a global level. We examined patterns of historical phylogeography and contemporary gene flow by genotyping 329 individuals from nine locations throughout the species' range at eight nuclear microsatellite markers and sequencing the complete mtDNA control region. Pairwise comparisons often resulted in fixation indices and divergence estimates of greater magnitude using mtDNA sequence data than microsatellite data. In addition, multiple methods of estimation suggested fewer populations based on microsatellite loci than on mtDNA sequence data. Coalescent analyses suggest divergence and restricted migration among Hawaii, Taiwan, eastern and western Australia using mtDNA sequence data and no divergence and high migration rates, between Taiwan and both Australian sites using microsatellite data. Evidence of secondary contact was detected between several localities and appears to be discreet in time rather than continuous. Collectively, these data suggest complex spatial/temporal relationships between shark populations that may feature pulses of female dispersal and more continuous male-mediated gene flow.

Comparative visual function in four piscivorous fishes inhabiting Chesapeake Bay.

Maintaining optimal visual performance is a difficult task in photodynamic coastal and estuarine waters because of the unavoidable tradeoffs between luminous sensitivity and spatial and temporal resolution, yet the visual systems of coastal piscivores remain understudied despite differences in their ecomorphology and microhabitat use. We therefore used electroretinographic techniques to describe the light sensitivities, temporal properties and spectral sensitivities of the visual systems of four piscivorous fishes common to coastal and estuarine waters of the western North Atlantic: striped bass (Morone saxatilis), bluefish (Pomatomus saltatrix), summer flounder (Paralichthys dentatus) and cobia (Rachycentron canadum). Benthic summer flounder exhibited higher luminous sensitivity and broader dynamic range than the three pelagic foragers. The former were at the more sensitive end of an emerging continuum for coastal fishes. By contrast, pelagic species were comparatively less sensitive, but showed larger day-night differences, consistent with their use of diel light-variant photic habitats. Flicker fusion frequency experiments revealed significant interspecific differences at maximum intensities that correlated with lifestyle and habitat. Spectral responses of most species spanned 400-610 nm, with significant day-night differences in striped bass and bluefish. Anadromous striped bass additionally responded to longer wavelengths, similar to many freshwater fishes. Collectively, these results suggest that pelagic piscivores are well adapted to bright photoclimates, which may be at odds with the modern state of eutrified coastal and estuarine waters that they utilize. Recent anthropogenic degradation of water quality in coastal environments, at a pace faster than the evolution of visual systems, may impede visually foraging piscivores, change selected prey, and eventually restructure ecosystems.

Bottom-up and climatic forcing on the worldwide population of leatherback turtles.

Nesting populations of leatherback turtles (Dermochelys coriacea) in the Atlantic and western Indian Oceans are increasing or stable while those in the Pacific are declining. It has been suggested that leatherbacks in the eastern Pacific may be resource limited due to environmental variability derived from the El Niño Southern Oscillation (ENSO), but this has yet to be tested. Here we explored bottom-up forcing and the responding reproductive output of nesting leatherbacks worldwide. We achieved this through an extensive review of leatherback nesting and migration data and by analyzing the spatial, temporal, and quantitative nature of resources as indicated by net primary production at post-nesting female migration and foraging areas. Leatherbacks in the eastern Pacific were the smallest in body size and had the lowest reproductive output due to less productive and inconsistent resources within their migration and foraging areas. This derived from natural interannual and multidecadal climate variability together with an influence of anthropogenic climate warming that is possibly affecting these natural cycles. The reproductive output of leatherbacks in the Atlantic and western Indian Oceans was nearly twice that of turtles in the eastern Pacific. The inconsistent nature of the Pacific Ocean may also render western Pacific leatherbacks susceptible to a more variable reproductive output; however, it appears that egg harvesting on nesting beaches is their major threat. We suggest that the eastern Pacific leatherback population is more sensitive to anthropogenic mortality due to recruitment rates that are lower and more variable, thus accounting for much of the population differences compared to Atlantic and western Indian turtles.

Critical assessment and ramifications of a purported marine trophic cascade.

When identifying potential trophic cascades, it is important to clearly establish the trophic linkages between predators and prey with respect to temporal abundance, demographics, distribution, and diet. In the northwest Atlantic Ocean, the depletion of large coastal sharks was thought to trigger a trophic cascade whereby predation release resulted in increased cownose ray abundance, which then caused increased predation on and subsequent collapse of commercial bivalve stocks. These claims were used to justify the development of a predator-control fishery for cownose rays, the "Save the Bay, Eat a Ray" fishery, to reduce predation on commercial bivalves. A reexamination of data suggests declines in large coastal sharks did not coincide with purported rapid increases in cownose ray abundance. Likewise, the increase in cownose ray abundance did not coincide with declines in commercial bivalves. The lack of temporal correlations coupled with published diet data suggest the purported trophic cascade is lacking the empirical linkages required of a trophic cascade. Furthermore, the life history parameters of cownose rays suggest they have low reproductive potential and their populations are incapable of rapid increases. Hypothesized trophic cascades should be closely scrutinized as spurious conclusions may negatively influence conservation and management decisions.

Dual annual spawning races in Atlantic sturgeon.

Atlantic sturgeon (Acipenser oxyrinchus oxyrinchus, Acipenseridae) populations in the United States were listed as either endangered or threatened under the Endangered Species Act in 2012. Because of the endangered/threatened status, a better understanding of Atlantic sturgeon life-history behavior and habitat use is important for effective management. It has been widely documented that Atlantic sturgeon reproduction occurs from late winter to early summer, varying clinally with latitude. However, recent data show Atlantic sturgeon also spawn later in the year. The group that spawns later in the year seems to be completely separate from the spring spawning run. Recognition of the later spawning season has drastically modified estimates of the population status of Atlantic sturgeon in Virginia. With the combination of new telemetry data and historical documentation we describe a dual spawning strategy that likely occurs in various degrees along most, if not all, of the Atlantic sturgeon's range. Using new data combined with historical sources, a new spawning strategy emerges which managers and researchers should note when determining the status of Atlantic sturgeon populations and implementing conservation measures.

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.

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 world's 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.

Comparative visual function in five sciaenid fishes inhabiting Chesapeake Bay.

Maintaining optimal visual performance is a difficult task in the photodynamic coastal and estuarine waters in which western North Atlantic sciaenid fishes support substantial commercial and recreational fisheries. Unavoidable tradeoffs exist between visual sensitivity and resolution, yet sciaenid visual systems have not been characterized despite strong species-specific ecomorphological and microhabitat differentiation. We therefore used electroretinographic techniques to describe the light sensitivities, temporal properties, and spectral characteristics of the visual systems of five sciaenids common to Chesapeake Bay, USA: weakfish (Cynoscion regalis), spotted seatrout (Cynoscion nebulosus), red drum (Sciaenops ocellatus), Atlantic croaker (Micropogonias undulatus) and spot (Leiostomus xanthurus). Benthic sciaenids exhibited higher sensitivities and broader dynamic ranges in white light V/logI experiments than more pelagic forms. Sensitivities of the former were at the lower (more sensitive) end of an emerging continuum for coastal fishes. Flicker fusion frequency experiments revealed significant interspecific differences at maximum intensities that correlated with lifestyle and habitat, but no specific differences at dimmer intensities. Spectral responses of most sciaenids spanned 400-610 nm, with significant diel differences in weakfish and Atlantic croaker. Weakfish, a crepuscular predator, also responded to ultraviolet wavelengths; this characteristic may be more useful under less turbid conditions. Collectively, these results suggest that sciaenids are well adapted to the dynamic photoclimate of the coastal and estuarine waters they inhabit. However, the recent anthropogenic degradation of water quality in coastal environments, at a pace faster than the evolution of visual systems, has amplified the importance of characterizing visual function in managed aquatic fauna.

Acoustic pressure and particle motion thresholds in six sciaenid fishes.

Sciaenid fishes are important models of fish sound production, but investigations into their auditory abilities are limited to acoustic pressure measurements on five species. In this study, we used auditory brainstem response (ABR) to assess the pressure and particle acceleration thresholds of six sciaenid fishes commonly found in Chesapeake Bay, eastern USA: weakfish (Cynoscion regalis), spotted seatrout (Cynoscion nebulosus), Atlantic croaker (Micropogonias undulatus), red drum (Sciaenops ocellatus), spot (Leiostomus xanthurus) and northern kingfish (Menticirrhus saxatilis). Experimental subjects were presented with pure 10 ms tone bursts in 100 Hz steps from 100 Hz to 1.2 kHz using an airborne speaker. Sound stimuli, monitored with a hydrophone and geophone, contained both pressure and particle motion components. Sound pressure and particle acceleration thresholds varied significantly among species and between frequencies; audiograms were notably flatter for acceleration than pressure at low frequencies. Thresholds of species with diverticulae projecting anteriorly from their swim bladders (weakfish, spotted seatrout, and Atlantic croaker) were typically but not significantly lower than those of species lacking such projections (red drum, spot, northern kingfish). Sciaenids were most sensitive at low frequencies that overlap the peak frequencies of their vocalizations. Auditory thresholds of these species were used to estimate idealized propagation distances of sciaenid vocalizations in coastal and estuarine environments.

Genetic polyandry and sexual conflict in the sandbar shark, Carcharhinus plumbeus, in the western North Atlantic and Gulf of Mexico.

To investigate patterns of polyandry in the sandbar shark (Carcharhinus plumbeus), 20 pregnant females were sampled from the western North Atlantic and Gulf of Mexico. Five species-specific microsatellite markers were used to genotype each shark and its litter. Of 20 litters, 17 (85%) were shown to have multiple sires. In multiply sired litters, the estimated minimum number of sires ranged from two to five with an average of 2.3 males per litter. Regression analysis did not demonstrate a significant relationship between female reproductive success and female body size or sire number and female body size. There was a high incidence of reproductive skew noted in litters, and two groups of males with significantly different mean reproductive success were observed. Analyses using Bateman's principles suggest that there is less direct benefit for females that acquire multiple mates than for males who bias paternity within litters. In light of past morphological and behavioural studies, these data suggest that patterns of polyandry in elasmobranchs may be determined by coercive mating, and that breeding behaviour has likely evolved in the context of sexual conflict.

Visual acuity thresholds of juvenile loggerhead sea turtles (Caretta caretta): an electrophysiological approach.

Visual evoked potentials measure dynamic properties of the visual system by recording transient electric responses of neural tissue identified to correspond to a specific visual stimulus, such as light or a striped grid. In this study, visual evoked potentials were used to test the visual acuity of juvenile loggerhead sea turtles (Caretta caretta) in water. Subject animals were fitted with a Plexiglas goggle filled with filtered seawater. Stimuli of black and white striped gratings were presented to the turtles using a slide projector directing an image onto a screen via a rotatable mirror that shifted the striped pattern laterally one-half cycle. Bioelectric activity was collected using a digital averaging computer and subdermal platinum electrodes, implanted under the head scutes directly above the optic nerve and the contralateral optic tectum. To isolate the response signal from the noise, signal averaging techniques were used when collecting visual evoked potentials. The resulting response waveforms included a robust positive-negative compound that was used to track the turtle's response to visual stimulation. Acuity thresholds for these sea turtles, which were derived from linear regressions analysis of the positive-negative compound amplitudes versus stripe size, ranged from 0.130 to 0.215. This acuity level is comparable to other inshore, shallow water marine species.

Uterine epithelial-sperm interaction, endometrial cycle and sperm storage in the terminal zone of the oviducal gland in the placental smoothhound, Mustelus canis.

The fate of spermatozoa deposited within the female reproductive tract has been described in the smoothhound, Mustelus canis. Evidence of uterine epithelial-sperm interaction is presented, as well as documentation of sperm storage specifically in the terminal zone of the oviducal gland. Sperm fate is correlated with morphology of the endometrial cycle and specificity of storage in the oviducal gland. The endometrium of M. canis undergoes dramatic tissue remodeling associated with gestation. In females harboring fertilized ova or preimplantation yolk-reliant embryos, the uterine epithelium is simple cuboidal with mucous droplets for lubrication. The presence of the embryo elicits a response from the uterus, which becomes modified for nutrient and respiratory exchange into vascular uterine attachment sites that abut the distal aspect of the yolk sac. Areas of the uterus adjacent to the uterine attachment sites are termed paraplacental sites. Uterine attachment sites are simple squamous while the paraplacental epithelium is simple columnar. Paraplacental cells have basal metachromatic vesicles and a dense array of apical cytoplasmic filaments. Immediately postpartum the uterine attachment sites, now termed uterine or placental scars, begin to remodel to a mucous epithelium for the next gestational cycle. Paraplacental cells slough off the apical filamentous portion, and sperm become embedded in the epithelium. Bundled sperm occur throughout gestation in the terminal zone of the oviducal gland. Sperm are not embedded in the terminal zone epithelium as in the uterus. Following sperm release from the uterus, the paraplacental epithelium reverts to a mucous epithelium for the next reproductive cycle. Fertilization is presumed to occur in the anterior oviduct above the oviducal gland. The physiological mechanisms that mediate sperm-uterus attachment, release, and storage in the terminal zone of the oviducal gland are currently under investigation.

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 (PhiST = 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.