Seasonally mediated niche partitioning in a vertically compressed pelagic predator guild.

Niche partitioning among closely related, sympatric species is a fundamental concept in ecology, and its mechanisms are of broad interest for understanding ecosystem functioning and predicting the impacts of human-driven environmental change. However, identifying mechanisms by which top marine predators partition available resources has been especially challenging given the difficulty of quantifying resource use of large pelagic animals. In the eastern tropical Pacific (ETP), three large, highly mobile and ecologically similar pelagic predators (blue marlin (Makaira nigricans), black marlin (Istiompax indica) and sailfish (Istiophorus platypterus)) coexist in a vertically compressed habitat. To evaluate each species' ecological niche, we leveraged a decade of recreational fisheries data, multi-year satellite tracking with high-resolution dive data, and stable isotope analysis. Fishery interaction and telemetry-based three-dimensional seasonal utilization distributions suggested high spatial and temporal overlap among species; however, seasonal and diel variability in diving behaviour produced spatial partitioning, leading to low trophic overlap among species. Expanding oxygen minimum zones will reduce the available vertical habitat within predator guilds, likely leading to increases in interspecific competition. Thus, understanding the mechanisms of habitat partitioning among predators in the vertically compressed ETP can provide insight into how predators in other ocean regions may respond to vertically limited habitats.

Patrolling the border: Billfish exploit the hypoxic boundary created by the world's largest oxygen minimum zone.

Pelagic predators must contend with low prey densities that are irregularly distributed and dynamic in space and time. Based on satellite imagery and telemetry data, many pelagic predators will concentrate horizontal movements on ephemeral surface fronts-gradients between water masses-because of enhanced local productivity and increased forage fish densities. Vertical fronts (e.g. thermoclines, oxyclines) can be spatially and temporally persistent, and aggregate lower trophic level and diel vertically migrating organisms due to sharp changes in temperature, water density or available oxygen. Thus, vertical fronts represent a stable and potentially energy rich habitat feature for diving pelagic predators but remain little explored in their capacity to enhance foraging opportunities. Here, we use a novel suite of high-resolution biologging data, including in situ derived oxygen saturation and video, to document how two top predators in the pelagic ecosystem exploit the vertical fronts created by the oxygen minimum zone of the eastern tropical Pacific. Prey search behaviour was dependent on dive shape, and significantly increased near the thermocline and hypoxic boundary for blue marlin Makaira nigricans and sailfish Istiophorus platypterus, respectively. Further, we identify a behaviour not yet reported for pelagic predators, whereby the predator repeatedly dives below the thermocline and hypoxic boundary (and by extension, below the prey). We hypothesize this behaviour is used to ambush prey concentrated at the boundaries from below. We describe how habitat fronts created by low oxygen environments can influence pelagic ecosystems, which will become increasingly important to understand in the context of global change and expanding oxygen minimum zones. We anticipate that our findings are shared among many pelagic predators where strong vertical fronts occur, and additional high-resolution tagging is warranted to confirm this.

Hunting behavior of a solitary sailfish Istiophorus platypterus and estimated energy gain after prey capture.

Foraging behavior and interaction with prey is an integral component of the ecological niche of predators but is inherently difficult to observe for highly mobile animals in the marine environment. Billfishes have been described as energy speculators, expending a large amount of energy foraging, expecting to offset high costs with periodic high energetic gain. Surface-based group feeding of sailfish, Istiophorus platypterus, is commonly observed, yet sailfish are believed to be largely solitary roaming predators with high metabolic requirements, suggesting that individual foraging also represents a major component of predator-prey interactions. Here, we use biologging data and video to examine daily activity levels and foraging behavior, estimate metabolic costs, and document a solitary predation event for a 40 kg sailfish. We estimate a median active metabolic rate of 218.9 ± 70.5 mgO2 kg-1 h-1 which increased to 518.8 ± 586.3 mgO2 kg-1 h-1 during prey pursuit. Assuming a successful predation, we estimate a daily net energy gain of 2.4 MJ (5.1 MJ acquired, 2.7 MJ expended), supporting the energy speculator model. While group hunting may be a common activity used by sailfish to acquire energy, our calculations indicate that opportunistic individual foraging events offer a net energy return that contributes to the fitness of these highly mobile predators.

Baseline Health and Nutritional Parameters of Wild Sand Tigers Sampled in Delaware Bay.

Species-specific hematological reference values are essential for diagnosis and treatment of disease and maintaining overall health of animals. This information is lacking for many species of elasmobranchs maintained in zoos and aquaria, thus reducing the effectiveness of care for these animals. Descriptive statistics and reference intervals were calculated for hematocrit and complete blood cell counts, biochemistry and protein electrophoresis parameters, trace minerals, vitamins, heavy metals, reproductive hormones, and fatty acids in the blood of 153 wild Sand Tigers Carcharias taurus of both sexes and a range of sizes caught in Delaware Bay (Delaware, USA). Mean hematocrit, total white blood cell counts, lymphocyte differentials, glucose, phosphorus, amylase, and aspartate aminotransferase levels were significantly higher in juveniles than in adults. Levels of estradiol, progesterone, testosterone, and differences in selenium and eicosapentaenoic acid (a polyunsaturated fatty acid) between males and females suggest that they are important parameters for improving Sand Tiger breeding success in managed care. Finally, blood metal levels for arsenic, cadmium, lead, and mercury suggest low levels of contaminant exposure for Sand Tigers during their summer residence in Delaware Bay. The results of this study provide baseline health parameters for wild Sand Tigers that will aid in effective maintenance of aquarium animals and contribute to a greater understanding of the biology of these sharks and efforts to accomplish sustainable management of their populations.

First insights into the vertical habitat use of the whitespotted eagle ray Aetobatus narinari revealed by pop-up satellite archival tags.

The whitespotted eagle ray Aetobatus narinari is a tropical to warm-temperate benthopelagic batoid that ranges widely throughout the western Atlantic Ocean. Despite conservation concerns for the species, its vertical habitat use and diving behaviour remain unknown. Patterns and drivers in the depth distribution of A. narinari were investigated at two separate locations, the western North Atlantic (Islands of Bermuda) and the eastern Gulf of Mexico (Sarasota, Florida, U.S.A.). Between 2010 and 2014, seven pop-up satellite archival tags were attached to A. narinari using three methods: a through-tail suture, an external tail-band and through-wing attachment. Retention time ranged from 0 to 180 days, with tags attached via the through-tail method retained longest. Tagged rays spent the majority of time (82.85 ± 12.17% S.D.) within the upper 10 m of the water column and, with one exception, no rays travelled deeper than ~26 m. One Bermuda ray recorded a maximum depth of 50.5 m, suggesting that these animals make excursions off the fore-reef slope of the Bermuda Platform. Individuals occupied deeper depths (7.42 ± 3.99 m S.D.) during the day versus night (4.90 ± 2.89 m S.D.), which may be explained by foraging and/or predator avoidance. Each individual experienced a significant difference in depth and temperature distributions over the diel cycle. There was evidence that mean hourly depth was best described by location and individual variation using a generalized additive mixed model approach. This is the first study to compare depth distributions of A. narinari from different locations and describe the thermal habitat for this species. Our study highlights the importance of region in describing A. narinari depth use, which may be relevant when developing management plans, whilst demonstrating that diel patterns appear to hold across individuals.

Seasonal patterns in stable isotope and fatty acid profiles of southern stingrays (Hypanus americana) at Stingray City Sandbar, Grand Cayman.

Ecotourism opportunities in the marine environment often rely heavily on provisioning to ensure the viewing of cryptic species by the public. However, intentional feeding of wildlife can impact numerous aspects of an animals' behavior and ecology. Southern stingrays (Hypanus americana) provisioned at Stingray City Sandbar (SCS) in Grand Cayman have altered diel activity patterns and decreased measures of health. This study looked at seasonal changes in stable isotope (SI) and fatty acid (FA) profiles of provisioned stingrays at SCS. Plasma δ15N was higher in male stingrays (11.86 ± 1.71‰) compared to females (10.70 ± 1.71‰). Lower values for δ15N in males and females were measured in October during low tourist season, suggesting stingrays may be forced to rely on native prey items to supplement the decreased amount of provisioned squid available during this time. Plasma FA profiles were significantly different between sexes and across sampling time points, with FAs 22:6n3, 16:0, 20:5n3, 18:1n3C, 18:0 and 18:1n9T contributing to dissimilarity scores between groups. Dietary FAs primarily contributed to differences between males and females lending further evidence to differences in foraging patterns at SCS, likely due to intraspecific competition. Further, canonical analysis of principal coordinates (CAP) analysis of FA profiles suggest similar diets during peak tourist season and differences in diet between males and females during the low season. This study demonstrates alterations in feeding ecology in stingrays at SCS which is of critical importance for effective management of the SCS aggregation.

Satellite telemetry reveals higher fishing mortality rates than previously estimated, suggesting overfishing of an apex marine predator.

Overfishing is a primary cause of population declines for many shark species of conservation concern. However, means of obtaining information on fishery interactions and mortality, necessary for the development of successful conservation strategies, are often fisheries-dependent and of questionable quality for many species of commercially exploited pelagic sharks. We used satellite telemetry as a fisheries-independent tool to document fisheries interactions, and quantify fishing mortality of the highly migratory shortfin mako shark (Isurus oxyrinchus) in the western North Atlantic Ocean. Forty satellite-tagged shortfin mako sharks tracked over 3 years entered the Exclusive Economic Zones of 19 countries and were harvested in fisheries of five countries, with 30% of tagged sharks harvested. Our tagging-derived estimates of instantaneous fishing mortality rates (F = 0.19-0.56) were 10-fold higher than previous estimates from fisheries-dependent data (approx. 0.015-0.024), suggesting data used in stock assessments may considerably underestimate fishing mortality. Additionally, our estimates of F were greater than those associated with maximum sustainable yield, suggesting a state of overfishing. This information has direct application to evaluations of stock status and for effective management of populations, and thus satellite tagging studies have potential to provide more accurate estimates of fishing mortality and survival than traditional fisheries-dependent methodology.

Biogeophysical and physiological processes drive movement patterns in a marine predator.

BACKGROUND: Blue sharks (Prionace glauca) are among the most abundant and widely distributed of oceanic elasmobranchs. Millions are taken annually in pelagic longline fisheries and comprise the highest component of auctioned fin weight in the international shark fin trade. Though studies of blue sharks outnumber those of other large pelagic sharks, the species' complicated and sexually segregated life history still confound current understanding of Atlantic movement patterns. Lack of detailed information regarding movement and vertical behavior continues to limit management efforts that require such data for stock assessment and sustainable catch modeling. Therefore, this study aims to describe behavioral and ecological patterns distinct to aggregating and migrating blue sharks, and compare the findings to existing Atlantic movement models. RESULTS: Data collected from 23 blue sharks instrumented with pop-up satellite archival tags were used in statistical predictive regression models to investigate habitat use during a localized aggregation in the northwest Atlantic, while undergoing seasonal migrations, and with respect to environmental variables. Deployment durations ranged from 4 to 273 days, with sharks inhabiting both productive coastal waters and the open ocean, and exhibiting long-distance seasonal movements exceeding 3700 km. While aggregating on the continental shelf of the northwest Atlantic, blue sharks displayed consistent depth use independent of sex and life stage, and exhibited varied response to environmental (temperature and chlorophyll a) factors. As sharks dispersed from the aggregation site, depth use was influenced by bathymetry, latitude, demography, and presence in the Gulf Stream. Mature females were not observed at the New England tagging site, however, two mature females with recent mating wounds were captured and tagged opportunistically in The Bahamas, one of which migrated to the Mid-Atlantic Ridge. CONCLUSIONS: Vertical behaviors displayed by blue sharks varied greatly among locales; depth use off the continental shelf was significantly greater, and individuals exhibited a greater frequency of deep-diving behavior, compared to periods of aggregation on the continental shelf. Sexual segregation was evident, suggesting mature and immature males, and immature females may be subjected to high levels of anthropogenic exploitation in this region during periods of aggregation. Analysis of the spatio-temporal tracks revealed that nine individuals traveled beyond the United States EEZ, including a mature female captured in The Bahamas that migrated to the Mid-Atlantic Ridge. These results reflect and augment existing Atlantic migration models, and highlight the complex, synergistic nature of factors affecting blue shark ecology and the need for a cooperative management approach in the North Atlantic.

Etmopterus lailae sp. nov., a new lanternshark (Squaliformes: Etmopteridae) from the Northwestern Hawaiian Islands.

A new species of lanternshark, Etmopterus lailae (Squaliformes: Etmopteridae), is described from the Northwestern Hawaiian Islands, in the central North Pacific Ocean. The new species resembles other members of the "Etmopterus lucifer" clade in having linear rows of dermal denticles, and most closely resembles E. lucifer from Japan. The new species occurs along insular slopes around seamounts at depths between 314-384 m. It can be distinguished from other members of the E. lucifer clade by a combination of characteristics, including a longer anterior flank marking branch, arrangement of dermal denticles on the ventral snout surface and body, flank and caudal markings, and meristic counts including number of spiral valve turns, and precaudal vertebrate. A key to species of the Etmopterus lucifer-clade is included.

Global population genetic dynamics of a highly migratory, apex predator shark.

Knowledge of genetic connectivity dynamics in the world's large-bodied, highly migratory, apex predator sharks across their global ranges is limited. One such species, the tiger shark (Galeocerdo cuvier), occurs worldwide in warm temperate and tropical waters, uses remarkably diverse habitats (nearshore to pelagic) and possesses a generalist diet that can structure marine ecosystems through top-down processes. We investigated the phylogeography and the global population structure of this exploited, phylogenetically enigmatic shark by using 10 nuclear microsatellites (n = 380) and sequences from the mitochondrial control region (CR, n = 340) and cytochrome oxidase I gene (n = 100). All three marker classes showed the genetic differentiation between tiger sharks from the western Atlantic and Indo-Pacific ocean basins (microsatellite FST  > 0.129; CR ΦST  > 0.497), the presence of North vs. southwestern Atlantic differentiation and the isolation of tiger sharks sampled from Hawaii from other surveyed locations. Furthermore, mitochondrial DNA revealed high levels of intraocean basin matrilineal population structure, suggesting female philopatry and sex-biased gene flow. Coalescent- and genetic distance-based estimates of divergence from CR sequences were largely congruent (dcorr  = 0.0015-0.0050), indicating a separation of Indo-Pacific and western Atlantic tiger sharks <1 million years ago. Mitochondrial haplotype relationships suggested that the western South Atlantic Ocean was likely a historical connection for interocean basin linkages via the dispersal around South Africa. Together, the results reveal unexpectedly high levels of population structure in a highly migratory, behaviourally generalist, cosmopolitan ocean predator, calling for management and conservation on smaller-than-anticipated spatial scales.

Comparative Use of a Caribbean Mesophotic Coral Ecosystem and Association with Fish Spawning Aggregations by Three Species of Shark.

Understanding of species interactions within mesophotic coral ecosystems (MCEs; ~ 30-150 m) lags well behind that for shallow coral reefs. MCEs are often sites of fish spawning aggregations (FSAs) for a variety of species, including many groupers. Such reproductive fish aggregations represent temporal concentrations of potential prey that may be drivers of habitat use by predatory species, including sharks. We investigated movements of three species of sharks within a MCE and in relation to FSAs located on the shelf edge south of St. Thomas, United States Virgin Islands. Movements of 17 tiger (Galeocerdo cuvier), seven lemon (Negaprion brevirostris), and six Caribbean reef (Carcharhinus perezi) sharks tagged with acoustic transmitters were monitored within the MCE using an array of acoustic receivers spanning an area of 1,060 km2 over a five year period. Receivers were concentrated around prominent grouper FSAs to monitor movements of sharks in relation to these temporally transient aggregations. Over 130,000 detections of telemetered sharks were recorded, with four sharks tracked in excess of 3 years. All three shark species were present within the MCE over long periods of time and detected frequently at FSAs, but patterns of MCE use and orientation towards FSAs varied both spatially and temporally among species. Lemon sharks moved over a large expanse of the MCE, but concentrated their activities around FSAs during grouper spawning and were present within the MCE significantly more during grouper spawning season. Caribbean reef sharks were present within a restricted portion of the MCE for prolonged periods of time, but were also absent for long periods. Tiger sharks were detected throughout the extent of the acoustic array, with the MCE representing only portion of their habitat use, although a high degree of individual variation was observed. Our findings indicate that although patterns of use varied, all three species of sharks repeatedly utilized the MCE and as upper trophic level predators they are likely involved in a range of interactions with other members of MCEs.

Repeated, long-distance migrations by a philopatric predator targeting highly contrasting ecosystems.

Long-distance movements of animals are an important driver of population spatial dynamics and determine the extent of overlap with area-focused human activities, such as fishing. Despite global concerns of declining shark populations, a major limitation in assessments of population trends or spatial management options is the lack of information on their long-term migratory behaviour. For a large marine predator, the tiger shark Galeocerdo cuvier, we show from individuals satellite-tracked for multiple years (up to 1101 days) that adult males undertake annually repeated, round-trip migrations of over 7,500 km in the northwest Atlantic. Notably, these migrations occurred between the highly disparate ecosystems of Caribbean coral reef regions in winter and high latitude oceanic areas in summer, with strong, repeated philopatry to specific overwintering insular habitat. Partial migration also occurred, with smaller, immature individuals displaying reduced migration propensity. Foraging may be a putative motivation for these oceanic migrations, with summer behaviour showing higher path tortuosity at the oceanic range extremes. The predictable migratory patterns and use of highly divergent ecosystems shown by male tiger sharks appear broadly similar to migrations seen in birds, reptiles and mammals, and highlight opportunities for dynamic spatial management and conservation measures of highly mobile sharks.

Intraspecific variation in vertical habitat use by tiger sharks (Galeocerdo cuvier) in the western North Atlantic.

Tiger sharks (Galeocerdo cuvier) are a wide ranging, potentially keystone predator species that display a variety of horizontal movement patterns, making use of coastal and pelagic waters. Far less, however, is known about their vertical movements and use of the water column. We used pop-up satellite archival tags with two data sampling rates (high rate and standard rate tags) to investigate the vertical habitat use and diving behavior of tiger sharks tagged on the Puerto Rico-Virgin Islands platform and off Bermuda between 2008 and 2009. Useable data were received from nine of 14 sharks tagged, tracked over a total of 529 days. Sharks spent the majority of their time making yo-yo dives within the upper 50 m of the water column and considerable time within the upper 5 m of the water column. As a result, sharks typically occupied a narrow daily temperature range (∼2°C). Dives to greater than 200 m were common, and all sharks made dives to at least 250 m, with one shark reaching a depth of 828 m. Despite some similarities among individuals, a great deal of intraspecific variability in vertical habit use was observed. Four distinct depth distributions that were not related to tagging location, horizontal movements, sex, or size were detected. In addition, similar depth distributions did not necessitate similar dive patterns among sharks. Recognition of intraspecific variability in habitat use of top predators can be crucial for effective management of these species and for understanding their influence on ecosystem dynamics.

Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana.

Southern stingrays, Dasyatis americana, have been provided supplemental food in ecotourism operations at Stingray City Sandbar (SCS), Grand Cayman since 1986, with this site becoming one of the world's most famous and heavily visited marine wildlife interaction venues. Given expansion of marine wildlife interactive tourism worldwide, there are questions about the effects of such activities on the focal species and their ecosystems. We used a combination of acoustic telemetry and tag-recapture efforts to test the hypothesis that human-sourced supplemental feeding has altered stingray activity patterns and habitat use at SCS relative to wild animals at control sites. Secondarily, we also qualitatively estimated the population size of stingrays supporting this major ecotourism venue. Tag-recapture data indicated that a population of at least 164 stingrays, over 80% female, utilized the small area at SCS for prolonged periods of time. Examination of comparative movements of mature female stingrays at SCS and control sites revealed strong differences between the two groups: The fed animals demonstrated a notable inversion of diel activity, being constantly active during the day with little movement at night compared to the nocturnally active wild stingrays; The fed stingrays utilized significantly (p<0.05) smaller 24 hour activity spaces compared to wild conspecifics, staying in close proximity to the ecotourism site; Fed stingrays showed a high degree of overlap in their core activity spaces compared to wild stingrays which were largely solitary in the spaces utilized (72% vs. 3% overlap respectively). Supplemental feeding has strikingly altered movement behavior and spatial distribution of the stingrays, and generated an atypically high density of animals at SCS which could have downstream fitness costs for individuals and potentially broader ecosystem effects. These findings should help environmental managers plan mitigating measures for existing operations, and develop precautionary policies regarding proposed feeding sites.

Population size and survivorship for juvenile lemon sharks (Negaprion brevirostris) on their nursery grounds at a marine protected area in Brazil

Sharks face a number of obstacles for surviving their first several years of life and many species occupy nursery areas. Although estimates of survival, particularly for young age classes, are essential for assessing, monitoring and effectively managing animal populations, there have been relatively few calculations of survival within shark populations and even fewer estimates based on direct methods for sharks on their nursery grounds. We used tag-recapture methods to estimate the population size and survival of juvenile lemon sharks (Negaprion brevirostris) on their nursery grounds at Atol das Rocas, a marine protected area in Brazil. Sharks were sampled from 1999 to 2003. Population size estimates ranged from 12 to 100 juvenile sharks and survival estimates ranged between 24-54% with a mean of 44.6% over the most robust sampling periods. The population of juvenile lemon sharks declined over the course of our study, whereas survival rates may have increased over the same time period. Even a modest level of fishing and removal of mature females in adjacent areas may dramatically affect small populations of sharks within a small and isolated nursery such as Atol das Rocas. The lower survival rates and population size at Atol das Rocas could be the result of differences in physical characteristics of this nursery in comparison to others used by lemon sharks in the northwestern Atlantic. Such comparatively lower populational parameters suggest that the population of young lemon sharks is fragile at the Atol das Rocas nursery.

Os tubarões enfrentam muitos obstáculos para sobreviver nos primeiros anos de vida e muitas espécies ocupam áreas de berçário. Embora estimativas de sobrevivência, particularmente para jovens, sejam essenciais para acessar, monitorar e manejar efetivamente populações animais, existem poucos cálculos destas estimativas para populações de tubarões e poucas estimativas baseadas em métodos diretos para estes animais em suas áreas de berçário. Métodos de marcação e recaptura foram utilizadosno presente estudo para estimar o tamanho populacional e a sobrevivência de jovens tubarões-limão (Negaprion brevirostris) em uma área de berçário na Reserva Biológica do Atol das Rocas, Brasil. Os indivíduos foram amostrados entre 1999 e 2003 e as estimativas de tamanho populacional variaram entre 12 a 100 indivíduos jovens e a taxa de sobrevivência entre 24 e 54%, com média de 44,6% durante o período de amostragem mais robusto. A população destes tubarões jovens diminuiu ao longo de nosso estudo, ainda que as taxas de sobrevivência tenham aumentado durante o mesmo período. Mesmo um nível moderado de pesca e a remoção de fêmeas maduras em áreas adjacentes podem afetar dramaticamente pequenas populações de tubarões num berçário pequeno e isolado como o Atol das Rocas. As taxas de sobrevivência e tamanho populacional relativamente mais baixos em Rocas podem ser resultado das diferenças nas características físicas deste berçário, comparadas a outros utilizados pela espécie no Atlântico norte-ocidental. Tais parâmetros comparativamente mais baixos no Atol das Rocas sugerem a fragilidade da população jovem de tubarões-limão neste berçário.