Vulnerability of Eastern Tropical Pacific chondrichthyan fish to climate change.

Climate change is an environmental emergency threatening species and ecosystems globally. Oceans have absorbed about 90% of anthropogenic heat and 20%-30% of the carbon emissions, resulting in ocean warming, acidification, deoxygenation, changes in ocean stratification and nutrient availability, and more severe extreme events. Given predictions of further changes, there is a critical need to understand how marine species will be affected. Here, we used an integrated risk assessment framework to evaluate the vulnerability of 132 chondrichthyans in the Eastern Tropical Pacific (ETP) to the impacts of climate change. Taking a precautionary view, we found that almost a quarter (23%) of the ETP chondrichthyan species evaluated were highly vulnerable to climate change, and much of the rest (76%) were moderately vulnerable. Most of the highly vulnerable species are batoids (77%), and a large proportion (90%) are coastal or pelagic species that use coastal habitats as nurseries. Six species of batoids were highly vulnerable in all three components of the assessment (exposure, sensitivity and adaptive capacity). This assessment indicates that coastal species, particularly those relying on inshore nursery areas are the most vulnerable to climate change. Ocean warming, in combination with acidification and potential deoxygenation, will likely have widespread effects on ETP chondrichthyan species, but coastal species may also contend with changes in freshwater inputs, salinity, and sea level rise. This climate-related vulnerability is compounded by other anthropogenic factors, such as overfishing and habitat degradation already occurring in the region. Mitigating the impacts of climate change on ETP chondrichthyans involves a range of approaches that include addressing habitat degradation, sustainability of exploitation, and species-specific actions may be required for species at higher risk. The assessment also highlighted the need to further understand climate change's impacts on key ETP habitats and processes and identified knowledge gaps on ETP chondrichthyan species.

El cambio climático es una emergencia medioambiental que amenaza a especies y ecosistemas en todo el mundo. Los océanos han absorbido alrededor del 90% del calor antropogénico y entre el 20% y el 30% de las emisiones de carbono, lo que ha provocado su calentamiento, acidificación, desoxigenación, cambios en la estratificación de los océanos y en la disponibilidad de nutrientes, así como fenómenos extremos más pronunciados. Dadas las predicciones de cambios, hay una importante necesidad de entender cómo las especies marinas se verán afectadas. En este estudio utilizamos una Evaluación Integrada de Riesgos para evaluar la vulnerabilidad de 132 condrictios del Pacífico Tropical Oriental (PTO) a los impactos del cambio climático. Adoptando un enfoque preventivo, estimamos que la vulnerabilidad general al cambio climático es Alta para casi una cuarta parte (23%) de las especies de condrictios del PTO evaluadas y Moderada para gran parte del resto (76%). La mayoría de las especies altamente vulnerables son batoideos (77%), y una gran proporción de éstas (90%) son especies costeras o especies pelágicas que utilizan los hábitats costeros como áreas de crianza. Seis especies de batoideos tuvieron una vulnerabilidad Alta en los tres componentes de la evaluación. Esta evaluación indica que las especies costeras, en particular las que dependen de áreas de crianza costeras, son las más vulnerables al cambio climático. Es probable que el calentamiento de los océanos, junto con la acidificación y la posible desoxigenación, tenga efectos generalizados sobre las especies de condrictios del PTO, pero las especies costeras se verán también afectadas por los cambios en los aportes de agua dulce, la salinidad y el aumento del nivel del mar. Esta vulnerabilidad relacionada con el clima se ve agravada por otros factores antropogénicos que ya se están produciendo en la región, como la sobrepesca y la degradación del hábitat. La mitigación de los impactos del cambio climático sobre los condrictios del PTO implica medidas que incluyan abordar la degradación del hábitat y la sostenibilidad de la explotación pesquera, y acciones para las especies de mayor riesgo son necesarias. Esta evaluación también destaca la necesidad de comprender mejor los impactos del cambio climático en los hábitats y procesos clave del PTO y las lagunas de conocimiento identificadas en relación con las especies de condrictios del PTO.

Seasonal occurrence and individual variability of bull sharks, Carcharhinus leucas, in a marine reserve of the southwestern Gulf of California.

Background: Studying how the bull sharks aggregate and how they can be driven by life history traits such as reproduction, prey availability, predator avoidance and social interaction in a National Park such as Cabo Pulmo, is key to understand and protect the species. Methods: The occurrence variability of 32 bull sharks tracked with passive acoustic telemetry were investigated via a hierarchical logistic regression model, with inference conducted in a Bayesian framework, comparing sex, and their response to temperature and chlorophyll. Results: Based on the fitted model, occurrence probability varied by sex and length. Juvenile females had the highest values, whereas adult males the lowest. A strong seasonality or day of the year was recorded, where sharks were generally absent during September-November. However, some sharks did not show the common pattern, being detected just for a short period. This is one of the first studies where the Bayesian framework is used to study passive acoustic telemetry proving the potential to be used in further studies.

Heavy metal and trace element concentrations in the blood of scalloped hammerhead sharks (Sphyrna lewini) from La Paz Bay, México.

Sharks are particularly susceptible to bioaccumulation due to their life history characteristics and trophic position within marine ecosystems. Despite this, studies of bioaccumulation cover only a small proportion of extant species. In this study we report concentrations of trace elements and heavy metals in blood samples of Sphyrna lewini for the first time. We report high concentrations of several trace elements and heavy metals, with concentrations of some elements exceeding the limit determined safe for human consumption. High elemental concentrations may reflect biochemical differences between blood plasma and other tissues; however, they may also be symptomatic of high levels of exposure triggered by anthropogenic activities. We also provide evidence of elemental accumulation through ontogeny, the nature of which differs from that previously reported. Ultimately, this baseline study increases our understanding of interspecific and intraspecific variation in bioaccumulation and ecotoxicology in elasmobranchs which may prove important in ensuring adequate management.

Do marine protected areas influence mercury exposure? Insights from a shark community in the tropical Northeast Pacific.

Biomass depletion caused by overfishing is likely to alter the structure of food webs and impact mercury transfer to marine predators. Although marine protected areas (MPAs) are spared from fishing pressure, their influence on biota mercury levels is poorly understood. Here, we used carbon and nitrogen stable isotope compositions as well as mercury concentrations in fin clips to characterize foraging habitat and mercury exposure of a shark community composed of migratory and resident species of the Revillagigedo archipelago, an offshore MPA in the Northeast Pacific off Mexico. We found that the probability of finding migratory sharks in the isotopic niche of Revillagigedo-resident sharks was low, likely reflecting the use of habitats outside the archipelago by highly mobile species. Community-wide variations in mercury were primarily explained by shark length, revealing that bioaccumulation was the main driver of Hg concentrations. We failed to detect a clear effect of foraging habitat on shark mercury exposure, which may be related to migratory species using both exploited and protected areas when moving outside the Revillagigedo MPA. More similar studies on the potential mitigation of Hg contamination by MPAs are needed in the future if fishing pressure increases to satisfy the growing global human population.

From rivers to ocean basins: The role of ocean barriers and philopatry in the genetic structuring of a cosmopolitan coastal predator.

The Bull Shark (Carcharhinus leucas) faces varying levels of exploitation around the world due to its coastal distribution. Information regarding population connectivity is crucial to evaluate its conservation status and local fishing impacts. In this study, we sampled 922 putative Bull Sharks from 19 locations in the first global assessment of population structure of this cosmopolitan species. Using a recently developed DNA-capture approach (DArTcap), samples were genotyped for 3400 nuclear markers. Additionally, full mitochondrial genomes of 384 Indo-Pacific samples were sequenced. Reproductive isolation was found between and across ocean basins (eastern Pacific, western Atlantic, eastern Atlantic, Indo-West Pacific) with distinct island populations in Japan and Fiji. Bull Sharks appear to maintain gene flow using shallow coastal waters as dispersal corridors, whereas large oceanic distances and historical land-bridges act as barriers. Females tend to return to the same area for reproduction, making them more susceptible to local threats and an important focus for management actions. Given these behaviors, the exploitation of Bull Sharks from insular populations, such as Japan and Fiji, may instigate local decline that cannot readily be replenished by immigration, which can in turn affect ecosystem dynamics and functions. These data also supported the development of a genetic panel to ascertain the population of origin, which will be useful in monitoring the trade of fisheries products and assessing population-level impacts of this harvest.

Radiologic Sciences Student Perceptions of Advisement.

PURPOSE: To investigate student perceptions of a structured advisement program. METHODS: Using a mixed-methods approach, 24 radiologic sciences students were surveyed in the initial and final semesters of the program to capture their perceptions of advisement practices. Quantitative data were analyzed for percentages and descriptive statistics, and qualitative responses were analyzed for emergent themes. RESULTS: Qualitative data analyses identified 3 themes: building relationships, strengthening student performance, and determining best practices for advisement. Quantitative data demonstrated that students appreciated the advisement process and acknowledged improvements in communication skills and the feedback loop. DISCUSSION: Advisement sessions can serve an important role in identifying areas where students can improve their performance. To grow and develop, students must understand their own strengths and weaknesses. Structured forms of advisement can serve as important tools to guide advisement conversations toward specific topics. CONCLUSION: The results of this study indicate that student advising is a vital component of radiologic sciences programs. Participants indicated that the advisement process helped them build relationships with faculty members and improved their overall performance.

A priority nursery area for the conservation of the scalloped hammerhead shark Sphyrna lewini in Mexico.

This study describes the genetic diversity and level of genetic differentiation of the scalloped hammerhead shark Sphyrna lewini from eight putative nursery areas in the Mexican Pacific Ocean, using the mtDNA control region. Genetic analyses revealed a particular spatial divergence between La Reforma and all the remaining sites, with five exclusive haplotypes and the highest genetic diversity. This pattern may be interpreted as the signature of regional female philopatry, relatively to a particular female-mediated gene flow for La Reforma, which shows a strong subdivision in the Gulf of California.

The impact of climate change on the distribution of Sphyrna lewini in the tropical eastern Pacific.

Variability and climate change due to anthropic influence have brought about alterations to marine ecosystems, that, in turn, have affected the physiology and metabolism of ectotherm species, such as the common hammerhead shark (Sphyrna lewini). However, the impact that climate variability may have on this species' distribution, particularly in the Eastern Tropical Pacific Marine Corridor, which is considered an area with great marine biodiversity, is unknown. The purpose of this research was to evaluate the effect of derivate impact of climate change on the oceanographic distribution of the hammerhead shark (Sphyrna lewini) in the Eastern Tropical Pacific Marine Corridor, contrasting the present and future scenarios for 2050. The methodology used was an ecological niche model based on the KUENM R package software that uses the maximum entropy algorithm (MaxEnt). The modelling was made for the year 2050 under RCP2.6 and RCP8.5 scenarios. A total of 952 models were made, out of which only one met the statistical parameters established as optimal, for future scenarios. The environmental suitability for S.lewini shows that this species would migrate to the south in the Chilean Pacific, associated with a possible warming that the equatorial zone will have and the possible cooling that the subtropical zone of the South Pacific will have by 2050, the product of changes in oceanographic dynamics.

Diving deeper into the underlying white shark behaviors at Guadalupe Island, Mexico.

Fine-scale movement patterns are driven by both biotic (hunting, physiological needs) and abiotic (environmental conditions) factors. The energy balance governs all movement-related strategic decisions.Marine environments can be better understood by considering the vertical component. From 24 acoustic trackings of 10 white sharks in Guadalupe Island, this study linked, for the first time, horizontal and vertical movement data and inferred six different behavioral states along with movement states, through the use of hidden Markov models, which allowed to draw a comprehensive picture of white shark behavior.Traveling was the most frequent state of behavior for white sharks, carried out mainly at night and twilight. In contrast, area-restricted searching was the least used, occurring primarily in daylight hours.Time of day, distance to shore, total shark length, and, to a lesser extent, tide phase affected behavioral states. Chumming activity reversed, in the short term and in a nonpermanent way, the behavioral pattern to a general diel vertical pattern.

A first assessment of the distribution and abundance of large pelagic species at Cocos Ridge seamounts (Eastern Tropical Pacific) using drifting pelagic baited remote cameras.

Understanding the link between seamounts and large pelagic species (LPS) may provide important insights for the conservation of these species in open water ecosystems. The seamounts along the Cocos Ridge in the Eastern Tropical Pacific (ETP) ocean are thought to be ecologically important aggregation sites for LPS when moving between Cocos Island (Costa Rica) and Galapagos Islands (Ecuador). However, to date, research efforts to quantify the abundance and distribution patterns of LPS beyond the borders of these two oceanic Marine Protected Areas (MPAs) have been limited. This study used drifting-pelagic baited remote underwater video stations (BRUVS) to investigate the distribution and relative abundance of LPS at Cocos Ridge seamounts. Our drifting-pelagic BRUVS recorded a total of 21 species including elasmobranchs, small and large teleosts, dolphins and one sea turtle; of which four species are currently threatened. Depth of seamount summit was the most significant driver for LPS richness and abundance which were significantly higher at shallow seamounts (< 400 m) compared to deeper ones (> 400m). Distance to nearest MPA was also a significant predictor for LPS abundance, which increased at increasing distances from the nearest MPA. Our results suggest that the Cocos Ridge seamounts, specifically Paramount and West Cocos which had the highest LPS richness and abundance, are important aggregation sites for LPS in the ETP. However, further research is still needed to demonstrate a positive association between LPS and Cocos Ridge seamounts. Our findings showed that drifting pelagic BRUVS are an effective tool to survey LPS in fully pelagic ecosystems of the ETP. This study represents the first step towards the standardization of this technique throughout the region.

The use of an unoccupied aerial vehicle to survey shark species over sand and rocky-reef habitats in a marine protected area.

Cabo Pulmo National Park was established in 1995 and has since seen a large increase in fish biomass. An unoccupied aerial vehicle (UAV) was used to survey shallow coastal habitat in which lemon sharks (Negaprion brevirostris), bull sharks (Carcharhinus leucas) and Pacific nurse sharks (Ginglymostoma unami) were recorded. Sharks were more common in the afternoon, potentially using warmer shallow areas to behaviourally thermoregulate. This study highlights UAV surveying to be a viable tool for species identification, a limitation of previous terrestrial surveys conducted in the area.

Foraging depth depicts resource partitioning and contamination level in a pelagic shark assemblage: Insights from mercury stable isotopes.

The decline of shark populations in the world ocean is affecting ecosystem structure and function in an unpredictable way and new ecological information is today needed to better understand the role of sharks in their habitats. In particular, the characterization of foraging patterns is crucial to understand and foresee the evolution of dynamics between sharks and their prey. Many shark species use the mesopelagic area as a major foraging ground but the degree to which different pelagic sharks rely on this habitat remains overlooked. In order to depict the vertical dimension of their trophic ecology, we used mercury stable isotopes in the muscle of three pelagic shark species (the blue shark Prionace glauca, the shortfin mako shark Isurus oxyrinchus and the smooth hammerhead shark Sphyrna zygaena) from the northeastern Pacific region. The Δ199Hg values, ranging from 1.40 to 2.13‰ in sharks, suggested a diet mostly based on mesopelagic prey in oceanic habitats. We additionally used carbon and nitrogen stable isotopes (δ13C, δ15N) alone or in combination with Δ199Hg values, to assess resource partitioning between the three shark species. Adding Δ199Hg resulted in a decrease in trophic overlap estimates compared to those based on δ13C/δ15N alone, demonstrating that multi-isotope modeling is needed for accurate trophic description of the three species. Mainly, it reveals that they forage at different average depths and that resource partitioning is mostly expressed through the vertical dimension within pelagic shark assemblages. Concomitantly, muscle total mercury concentration (THg) differed between species and increased with feeding depth. Overall, this study highlights the key role of the mesopelagic zone for shark species foraging among important depth gradients and reports new ecological information on trophic competition using mercury isotopes. It also suggests that foraging depth may play a pivotal role in the differences between muscle THg from co-occurring high trophic level shark species.

Description of first nursery area for a pygmy devil ray species (Mobula munkiana) in the Gulf of California, Mexico.

Munk's pygmy devil rays (Mobula munkiana) are medium-size, zooplanktivorous filter feeding, elasmobranchs characterized by aggregative behavior, low fecundity and delayed reproduction. These traits make them susceptible to targeted and by-catch fisheries and are listed as Vulnerable on the IUCN Red List. Multiple studies have examined fisheries impacts, but nursery areas or foraging neonate and juvenile concentrations have not been examined. This study describes the first nursery area for M. munkiana at Espiritu Santo Archipelago, Mexico. We examined spatial use of a shallow bay during 22 consecutive months in relation to environmental patterns using traditional tagging (n = 95) and acoustic telemetry (n = 7). Neonates and juveniles comprised 84% of tagged individuals and their residency index was significantly greater inside than outside the bay; spending a maximum of 145 consecutive days within the bay. Observations of near-term pregnant females, mating behavior, and neonates indicate an April to June pupping period. Anecdotal photograph review indicated that the nursery area is used by neonates and juveniles across years. These findings confirm, for the first time, the existence of nursery areas for Munk's pygmy devil rays and the potential importance of shallow bays during early life stages for the conservation of this species.

The use of machine learning to detect foraging behaviour in whale sharks: a new tool in conservation.

In this study we present the first attempt at modelling the feeding behaviour of whale sharks using a machine learning analytical method. A total of eight sharks were monitored with tri-axial accelerometers and their foraging behaviours were visually observed. Our results highlight that the random forest model is a valid and robust approach to predict the feeding behaviour of the whale shark. In conclusion this novel approach exposes the practicality of this method to serve as a conservation tool and the capability it offers in monitoring potential disturbances of the species.

The Twilight Zone as a Major Foraging Habitat and Mercury Source for the Great White Shark.

The twilight zone contains the largest biomass of the world's ocean. Identifying its role in the trophic supply and contaminant exposure of marine megafauna constitutes a critical challenge in the context of global change. The white shark (Carcharodon carcharias) is a threatened species with some of the highest concentrations of neurotoxin methylmercury (MeHg) among marine top predators. Large white sharks migrate seasonally from coastal habitats, where they primarily forage on pinnipeds, to oceanic offshore habitats. Tagging studies suggest that while offshore, white sharks may forage at depth on mesopelagic species, yet no biochemical evidence exists. Here, we used mercury isotopic composition to assess the dietary origin of MeHg contamination in white sharks from the Northeast Pacific Ocean. We estimated that a minimum of 72% of the MeHg accumulated by white sharks originates from the consumption of mesopelagic prey, while a maximum of 25% derives from pinnipeds. In addition to highlighting the potential of mercury isotopes to decipher the complex ecological cycle of marine predators, our study provides evidence that the twilight zone constitutes a crucial foraging habitat for these large predators, which had been suspected for over a decade. Climate change is predicted to expand the production of mesopelagic MeHg and modify the mesopelagic biomass globally. Considering the pivotal role of the twilight zone is therefore essential to better predict both MeHg exposure and trophic supply to white sharks, and effectively protect these key vulnerable predators.

Shark movement patterns in the Mexican Pacific: A conservation and management perspective.

Marine animal tracking has become one of the major tools used to understand the behavior and ecology of a multitude of species in the ocean, thus there is an increasing body of knowledge about this subject worldwide, particularly for sharks. Nevertheless, little was known of the movement patterns of shark in the Mexican Pacific (MXP) and Gulf of California (GOC), except for the pioneering work carried out in the 1980s on the movements of scalloped hammerhead sharks in El Bajo Espiritu Santo and other islands in the region, as well as ongoing studies on white shark movements, migratory patterns and behavior off Isla Guadalupe. Here we present an overview of previous studies on the movements of sharks, as well as a comprehensive description of new studies currently being carried out by our research group at Pelagios Kakunjá on several species of sharks in the MXP. We show how information gleaned from these studies can be put to use to guide sustainable exploitation policies and promote effective conservation practices.

Trophic resources and mercury exposure of two silvertip shark populations in the Northeast Pacific Ocean.

Worldwide shark populations have experienced rapid declines over the last decades, mainly due to overfishing. Marine protected areas (MPAs) have thus become an indispensable tool for the protection of these marine predators. Two recently-created MPAs in the Northeast Pacific Ocean, the Revillagigedo National Park and Clipperton Atoll, are characterized by different trophic structures potentially influencing the trophic niche and contaminant exposure of resident sharks in these two sites. In this context, we used carbon (δ13C) and nitrogen (δ15N) stable isotope analyzes as well as total mercury concentrations ([THg]) to assess the effect of foraging site on the trophic niche and Hg levels of juvenile silvertip (ST) sharks Carcharhinus albimarginatus. Analyzing fin clip samples from Revillagigedo and Clipperton, we found that shark δ15N varied spatially in relation to δ15N baselines, suggesting similar trophic position in both MPAs. Moreover, δ13C values indicated that ST sharks from Revillagigedo would feed on different food webs (i.e. both benthic and pelagic) while individuals from Clipperton would only rely on benthic food webs. These differences between MPAs led to a weak overlap of isotopic niches between the two populations, highlighting the site residency of juvenile ST sharks. Within each population, [THg] was not correlated with trophic tracers (δ15N and δ13C) and was also similar between populations. This study revealed no influence of site or food web in [THg] and raises the question of the origin of Hg exposure for reef shark populations in the Northeast Pacific Ocean.

Residency and diel movement patterns of the endangered scalloped hammerhead Sphyrna lewini in the Revillagigedo National Park.

This study is the first description of the residency and diel movements of Sphyrna lewini at the Revillagigedo National Park, Mexico. Eleven adult scalloped hammerheads of total length 200-300 cm were monitored using acoustic telemetry during 2013-2015 at four sites at San Benedicto Island. Diel and residency patterns were described based on 58,055 detections by four autonomous receivers. The sharks displayed high daytime residency in two of the four sites, with movements away into the pelagic environment at night. This study generates a baseline for effective monitoring to improve the conservation and management of an iconic but endangered species at this marine reserve.

Shark ecology, the role of the apex predator and current conservation status.

Feeding studies, since traditional stomach content analysis to stable isotopes analyses, provides insights into the trophic relationship among the apex predators and the ecosystems they inhabit. The Pacific Coast of Mexico (PCM) is inhabited by 62 known species (or 12%) of living sharks, which belong to 21 families and 34 genera. We divide the Pacific Coast of Mexico (PCM) into four regions for consideration: (1) the western coast of Baja California (WcBJ), (2) the Gulf of California (GC), (3) the Central Pacific Mexican (CPM), and (4) the Gulf of Tehuantepec (GT). Biodiversity is highest in the GC, with 48 shark species, followed by the WcBJ with 44 species, then the CPM with 28 species and the GT with 26 species. Few large species (>2m in total length) function as top predators in any region, with a greater number of smaller shark species (<1.5m total length). Information about the trophic ecology of different shark species is included to know the ecological role and position of each shark species within a food web to understand the dynamics of marine communities and the impact that each species has on trophic net, which is critical to effective resource conservation and responsible exploitation. The different shark species predate mainly on coastal or oceanic waters. The coastal sharks feed mainly on crustaceans and small fishes; whereas the oceanic species predate mainly on squids and fishes from mesopelagic to epipelagic habits. Also is included a summary of the IUCN Red List category assigned to all shark species from the Mexican Pacific. Thirty-one percent (19 species) of sharks in the Mexican Pacific are considered as threatened (Critically Endangered, Endangered or Vulnerable). Of these, 4.9% (3 species) are Endangered and 26.2% (15 species) are Vulnerable. In addition, since 2012 the fishing of shark and rays has been closed between 1 May and 31 July in the Mexican Pacific as a conservative management measure.

Movements of scalloped hammerhead sharks (Sphyrna lewini) at Cocos Island, Costa Rica and between oceanic islands in the Eastern Tropical Pacific.

Many species of sharks form aggregations around oceanic islands, yet their levels of residency and their site specificity around these islands may vary. In some cases, the waters around oceanic islands have been designated as marine protected areas, yet the conservation value for threatened shark species will depend greatly on how much time they spend within these protected waters. Eighty-four scalloped hammerhead sharks (Sphyrna lewini Griffith & Smith), were tagged with acoustic transmitters at Cocos Island between 2005-2013. The average residence index, expressed as a proportion of days present in our receiver array at the island over the entire monitoring period, was 0.52±0.31, implying that overall the sharks are strongly associated with the island. Residency was significantly greater at Alcyone, a shallow seamount located 3.6 km offshore from the main island, than at the other sites. Timing of presence at the receiver locations was mostly during daytime hours. Although only a single individual from Cocos was detected on a region-wide array, nine hammerheads tagged at Galapagos and Malpelo travelled to Cocos. The hammerheads tagged at Cocos were more resident than those visiting from elsewhere, suggesting that the Galapagos and Malpelo populations may use Cocos as a navigational waypoint or stopover during seasonal migrations to the coastal Central and South America. Our study demonstrates the importance of oceanic islands for this species, and shows that they may form a network of hotspots in the Eastern Tropical Pacific.