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.

Can biochemical tracers reveal ontogenetic trophic shift and individual prey selection in white sharks from Guadalupe Island, Northeast Pacific?

Refining the role of apex predators in marine food webs is a necessary step in predicting the consequences of their global decline under the footprint of fishing activities. White sharks (Carcharodon carcharias) are vulnerable predators, performing large migrations and able to forage on a variety of prey in different habitats. In the Northeast Pacific, juvenile and adult white sharks are found seasonally at the same aggregation sites, such as Guadalupe Island off Mexico. While adults are thought to target local pinniped colonies, very few prey-predator interactions have been documented and the diet of juveniles in this area remains poorly understood. Here we used carbon/nitrogen stable isotopes and fatty acids to characterize the trophic ecology of white sharks at Guadalupe Island. In contrast to the ontogenetic trophic shift paradigm, we detected no influence of size on muscle stable isotope and fatty acid composition, revealing no significant dietary variation between juvenile and adult sharks. Stable isotopes did not allow definitive conclusions to be drawn regarding the diet of white sharks at Guadalupe Island, due to significant variability in the contribution of different potential prey depending on the trophic discrimination factors used. However, most sharks were rich in polyunsaturated fatty acids (such as long-chain omega 3), suggesting a local diet of mainly pelagic prey (potentially large fish or cephalopods). A few individuals appeared to show recent consumption of pinnipeds, with higher proportions of saturated and monounsaturated fatty acids. These individual differences in fatty acid composition could reflect an ecological trade-off between consumption of prey rich in fat (marine mammals) versus prey rich in polyunsaturated fatty acids (pelagic prey), respectively meeting the energetic and physiological needs of white sharks. Although ontogenetic trophic changes were not able to be discerned, our results thus provide new insights into the physiological drivers of predator-prey interactions, which can benefit the definition of conservation strategies in a changing ocean.

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.

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.

Social dynamics and individual hunting tactics of white sharks revealed by biologging.

Social foraging, where animals forage in groups, takes many forms but is less studied in marine predators as measuring social associations in the wild is challenging. We used biologging (activity, cameras and telemetry receivers) sensors to measure social associations and simultaneous behaviour, in white sharks (Carcharodon carcharias) off Guadalupe Island, Mexico. Animal-borne telemetry receivers revealed that sharks varied in the number of associations they formed and occurred most often when sharks were swimming in straight paths or when they were turning frequently. While many associations were likely random, there was evidence of some stronger associations. Sharks varied in the depths they used and their activity, with some individuals more active in shallow water while others were more active 200-300 m deep. We propose that white sharks associate with other individuals so they can inadvertently share information on the location or remains of large prey. However, there may be a wide range of individual variability in both behaviour and sociality. Biologging now enables social associations of animals to be measured, concurrent with measures of their behaviour, so that social foraging of large marine predators can be quantified in the wild.

Foraging plasticity diversifies mercury exposure sources and bioaccumulation patterns in the world's largest predatory fish.

Large marine predators exhibit high concentrations of mercury (Hg) as neurotoxic methylmercury, and the potential impacts of global change on Hg contamination in these species remain highly debated. Current contaminant model predictions do not account for intraspecific variability in Hg exposure and may fail to reflect the diversity of future Hg levels among conspecific populations or individuals, especially for top predators displaying a wide range of ecological traits. Here, we used Hg isotopic compositions to show that Hg exposure sources varied significantly between and within three populations of white sharks (Carcharodon carcharias) with contrasting ecology: the north-eastern Pacific, eastern Australasian, and south-western Australasian populations. Through Δ200Hg signatures in shark tissues, we found that atmospheric Hg deposition pathways to the marine environment differed between coastal and offshore habitats. Discrepancies in δ202Hg and Δ199Hg signatures among white sharks provided evidence for intraspecific exposure to distinct sources of marine methylmercury, attributed to population and ontogenetic shifts in foraging habitat and prey composition. We finally observed a strong divergence in Hg accumulation rates between populations, leading to three times higher Hg concentrations in large Australasian sharks compared to north-eastern Pacific sharks, and likely due to different trophic strategies adopted by adult sharks across populations. This study illustrates the variety of Hg exposure sources and bioaccumulation patterns that can be found within a single species and suggests that intraspecific variability needs to be considered when assessing future trajectories of Hg levels in marine predators.

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.

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.

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.

The complete mitochondrial DNA of white shark (Carcharodon carcharias) from Isla Guadalupe, Mexico.

The Isla Guadalupe white shark mitochondrial structure is similar to the one previously reported for a white shark individual from Taiwan with a total length of 16,745 and 16,742 bp respectively; the base composition of the genomes was as follow A (30.60%), T (28.67%), C (26.86%) and G (13.87%), contains 13 protein-coding genes and 24 tRNA genes and the non-coding control region. The tRNA genes range from 70-72 bp. Gene order is the same as in other vertebrates and teleosts.

Feeding and migration habits of white shark Carcharodon carcharias (Lamniformes: Lamnidae) from Isla Guadalupe inferred by analysis of stable isotopes delta15N and delta13C.

Stable isotope composition of marine top predator's tissues provides insight information of its trophic ecology and migratory behavior. Previous reports have shown that dermal tissues could record longer patterns of hunting and movement. Based on this, the aim of this study was to describe the feeding and migratory habits of the white shark from Isla Guadalupe, using stable isotopic analysis of dermis. We considered a small subset of many possible prey taxa that the sharks could have eaten throughout their migration: pinnipeds, squid and tuna. We grouped the data in five focal areas: Gulf of California, Coast of California, Isla Guadalupe, SOFA and Hawaii. We performed a Bayesian mixing model to study the trophic ecology of this top predator. Average isotopic values for dermis tissue of white shark were delta13C (-14.5 per thousand) and delta15N (19.1 per thousand). Corrected white shark dermal mean values to resemble muscle were delta13C (-16.6 per thousand) and delta15N (21.2 per thousand). Mixing model data from dermis showed predation in offshore areas such the SOFA and a main importance of pinnipeds as prey of the white shark in Isla Guadalupe.

Feeding and migration habits of white shark Carcharodon carcharias (Lamniformes: Lamnidae) from Isla Guadalupe inferred by analysis of stable isotopes δ15N and δ13C / Hábitos alimenticios y migratorios del tiburón blanco Carcharodon carcharias (Lamniformes: Lamnidae) de Isla Guadalupe inferidos por el análisis de isótopos estables de δ15N and δ13C

Stable isotope composition of marine top predator’s tissues provides insight information of its trophic ecology and migratory behavior. Previous reports have shown that dermal tissues could record longer patterns of hunting and movement. Based on this, the aim of this study was to describe the feeding and migratory habits of the white shark from Isla Guadalupe, using stable isotopic analysis of dermis. We considered a small subset of many possible prey taxa that the sharks could have eaten throughout their migration: pinnipeds, squid and tuna. We grouped the data in five focal areas: Gulf of California, Coast of California, Isla Guadalupe, SOFA and Hawaii. We performed a Bayesian mixing model to study the trophic ecology of this top predator. Average isotopic values for dermis tissue of white shark were δ13C (-14.5‰) and δ15N (19.1‰). Corrected white shark dermal mean values to resemble muscle were δ13C (-16.6‰) and δ15N (21.2‰). Mixing model data from dermis showed predation in offshore areas such the SOFA and a main importance of pinnipeds as prey of the white shark in Isla Guadalupe. Rev. Biol. Trop. 62 (2): 637-647. Epub 2014 June 01.

La composición isotópica de los tejidos de los depredadores tope en el ambiente marino provee información sobre su ecología trófica y su comportamiento migratorio. Estudios previos han mostrado que el tejido dérmico puede registrar patrones largos de movimiento y caza. El objetivo de este estudio fue describir los hábitos tróficos y migratorios de los tiburones blancos de Isla Guadalupe realizando un análisis de isótopos estables de su tejido dérmico. Consideramos un pequeño grupo de muchos posibles taxa que los tiburones pudieron haber comido a lo largo de su migración: pinípedos, calamares y atunes. Estas presas fueron agrupadas en cinco áreas focales: Golfo de California, Isla Guadalupe, Costa de California, SOFA y Hawái. Realizamos un modelo de mezcla bayesiano para estudiar la ecología trófica de este depredador tope. Los promedios del valor isotópico de la dermis del tiburón blanco fueron δ13C (-14.5‰) y δ15N (19.1‰). Los promedios del valor isotópico de la dermis transformada para semejar músculo fueron δ13C (-16.6 ‰) y δ15N (21.2‰). El modelo de mezcla mostró una probable depredación de los tiburones en áreas oceánicas como el SOFA y confirmó la importancia de los pinnípedos como presa principal del tiburón blanco en Isla Guadalupe.