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.

The rostral micro-tooth morphology of blue marlin, Makaira nigricans.

Billfish rostra potentially have several functions; however, their role in feeding is unequivocal in some species. Recent work linked morphological variation in rostral micro-teeth to differences in feeding behavior in two billfish species, the striped marlin (Kajikia audax) and the sailfish (Istiophorus platypterus). Here, we present the rostral micro-tooth morphology for a third billfish species, the blue marlin (Makaira nigricans), for which the use of the rostrum in feeding behavior is still undocumented from systematic observations in the wild. We measured the micro-teeth on rostrum tips of blue marlin, striped marlin, and sailfish using a micro-computed tomography approach and compared the tooth morphology among the three species. This was done after an analysis of video-recorded hunting behavior of striped marlin and sailfish revealed that both species strike prey predominantly with the first third of the rostrum, which provided the justification to focus our analysis on the rostrum tips. In blue marlin, intact micro-teeth were longer compared to striped marlin but not to sailfish. Blue marlin had a higher fraction of broken teeth than both striped marlin and sailfish, and broken teeth were distributed more evenly on the rostrum. Micro-tooth regrowth was equally low in both marlin species but higher in sailfish. Based on the differences and similarities in the micro-tooth morphology between the billfish species, we discuss potential feeding-related rostrum use in blue marlin. We put forward the hypothesis that blue marlin might use their rostra in high-speed dashes as observed in striped marlin, rather than in the high-precision rostral strikes described for sailfish, possibly focusing on larger prey organisms.

Movement and population dispersal of dolphinfish (Coryphaena hippurus) across the Eastern Tropical Pacific inferred from carbon and nitrogen stable isotope analyses.

The dolphinfish (Coryphaena hippurus) is a globally distributed marine predator that supports one of the most important coastal fisheries along the Eastern Tropical Pacific (ETP), but its spatial movements in this area are poorly understood. Stable isotope values (δ13 C and δ15 N) of white muscle from dolphinfish (n = 220) captured at different locations across the ETP (i.e., Mexico, Costa Rica, Ecuador, Peru and oceanic areas) were normalized to copepod baseline stable isotope values to estimate dolphinfish trophic position, movements and population dispersal. Movement or residence patterns were inferred from the difference in δ15 N values (Δ15 Ndolphinfish-copepod ‰) between copepods and dolphinfish muscle. Baseline corrected isotope values (δ13 Cdolphinfish-copepod and δ15 Ndolphinfish-copepod ) of dolphinfish muscle were used to estimate isotopic niche metrics and infer population dispersal across isoscapes. Values of δ13 C and δ15 N differed between juvenile and adult dolphinfish and across the ETP. Trophic position estimates ranged from 3.1 to 6.0 with a mean of 4.6. Adults and juveniles had similar trophic position estimates, whereas isotopic niche areas (SEA ‰2 ) of adults were greater relative to juveniles in every location. Adult dolphinfish showed "moderate movement by some individuals" in all locations based on Δ15 Ndolphinfish-copepod values, except for Costa Rica where adults were classified with "high degree of movement by some individuals" whereas juveniles showed "limited movement" in all areas except Mexico. Population dispersal based on Δ15 Ndolphinfish-copepod values showed "moderate" and "high" dispersal for adults and "no dispersal" for most juveniles, except for Mexico. This study provides insight into potential dolphinfish spatial mobility across an area of interest for multiple nations, which can help to improve stock assessments and management of the species.

Persistent Organic Pollutants in Whale Shark (Rhincodon typus) Skin Biopsies from Bahía de Los Ángeles, Mexico.

The whale shark (Rhincodon typus) is a filter-feeding organism that can be considered a sentinel species, and Bahía de los Ángeles (BLA) in the Gulf of California is an important sighting site for these elasmobranchs. This filter-feeding organism can be considered a pollutant sampler from the marine environment. Persistent organic pollutants are toxic compounds with high mobility and environmental persistence, bioaccumulation and trophic transfer. Among these are polycyclic aromatic hydrocarbons (PAHs) and organochlorine pesticides (OCPs). The present work aimed to determine concentrations of PAHs and OCPs in whale shark skin biopsies, collected in 2021 at BLA. Mean detected levels of PAHs and OCPs were 279.4 ng/g dw (dry weight) and 1478.1 ng/g dw, respectively. Analysis of similarities between the ordered sizes (4.2-7.6 m) and the concentrations of PAHs and OCPs indicated no significant differences. Individual PAHs detected indicate pyrogenic and petrogenic sources; the presence of pesticides at levels higher than those of hydrocarbons may be related to agricultural activity in the areas surrounding the Baja California peninsula. This study is the first report of PAH levels in R. typus for the Gulf of California and Mexico.

Little Sharks in a Big World: Mitochondrial DNA Reveals Small-scale Population Structure in the California Horn Shark (Heterodontus francisci).

The California horn shark (Heterodontus francisci) is a small demersal species distributed from southern California and the Channel Islands to Baja California and the Gulf of California. These nocturnal reef predators maintain small home-ranges as adults and lay auger-shaped egg cases that become wedged into the substrate. While population trends are not well documented, this species is subject to fishing pressure through portions of its range and has been identified as vulnerable to overexploitation. Here, we present a survey of 318 specimens from across the range, using mtDNA control region sequences to provide the first genetic assessment of H. francisci. Overall population structure (ΦST = 0.266, P < 0.001) is consistent with limited dispersal as indicated by life history, with two distinct features. Population structure along the continuous coastline is low, with no discernable breaks from Santa Barbara, CA to Bahia Tortugas (Baja California Sur, Mexico); however, there is a notable partition at Punta Eugenia (BCS), a well-known biogeographic break between tropical and subtropical marine faunas. In contrast, population structure is much higher (max ΦST = 0.601, P < 0.05) between the coast and adjacent Channel Islands, a minimum distance of 19 km, indicating that horn sharks rarely disperse across deep habitat and open water. Population structure in most elasmobranchs is measured on a scale of hundreds to thousands of kilometers, but the California Horn Shark has population partitions on an unprecedented small scale, indicating a need for localized management strategies which ensure adequate protection of distinct stocks.

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.

Reproductive biology of the swell shark Cephaloscyllium ventriosum (Carcharhiniformes: Scyliorhinidae).

The Cephaloscyllium ventriosum shark is present in the artisanal fisheries of elasmobranchs on the western coast of Baja California Sur, Mexico. The main characteristics of the sexual maturation of this species based on individuals captured from off north-west Mexico in 2013-2016 are described. The size at maturity of this species was determined for the first time (total length 82 cm for females and 76 cm for males). Most females had one egg case per one uterus, and two per one uterus was an isolated event of low incidence. From the histological analysis of females, it was possible to show sperm storage in the oviducal gland. Fully developed sperm in immature organisms were identified in the testes. The main indicator of the maturity stage of males and their mating activity is the clasper. The present study provides evidence for a reliable estimation of the sexual maturity of these organisms, demonstrating the need for the combination of macroscopic and microscopic methods.

Reproductive biology of the Rasptail skate Rostroraja velezi (Rajiformes: Rajidae).

The Rasptail skate Rostroraja velezi is commercially exploited in artisanal elasmobranch fisheries along the west coast of Baja California Sur, Mexico, but information on its life history is limited. This study aimed to investigate the reproductive biology of R. velezi. A total of 105 specimens were caught from April 2008 to May 2012, including the largest reported specimen with 121 cm total length, 96 cm disc width (DW ). Females attained larger sizes than males. Males and females presented functional gonads. There was an asymmetry in the testes of males, with the left testis being larger. Histological analysis of the reproductive biology of R. velezi was performed here for the first time. The presence of sperm storage in females and spermatogenic development beginning at the first stages of maturity in males was recorded. It was possible to identify the development of secretions in the club, baffle and terminal zone of the oviducal gland. DW at maturity, defined as the DW at which 50% of the population is mature, was estimated at 68-72 cm for females and 65.1 cm for males. Egg-bearing females caught in April and May presented one egg capsule per uterus. Furthermore, a description of the egg capsule of R. velezi is provided. Elucidating the reproductive cycle, the type of reproductive strategies, and the fecundity of R. velezi will allow us to understand the impact of fisheries on this species.

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.

General descriptions of the dermis structure of a juvenile whale shark Rhincodon typus from the Gulf of California.

The aim of this study is to provide preliminary observations on the microanatomy of Rhincodon typus skin using histology and electron microscopy analyses. Skin biopsies were obtained from a deceased juvenile male shark (548 cm total length) stranded in La Paz, Mexico, during February 2018. The results of this study evidenced the basic structure of the dermal denticles in the epidermis of the trunk of the shark, as well as the composition of the connective tissue in the hypodermis. Histological images of the hypodermis showed a high concentration of collagen fibres, formed by a large number of fine and wavy fibres of compact shape and little intercellular substance.

Isotopic (δ15 N) relationship of pregnant females and their embryos: Comparing placental and yolk-sac viviparous elasmobranchs.

Nitrogen stable isotopes ratios (δ15 N) were determined for selected tissues (muscle, liver, blood and yolk) of pregnant females and their embryos of a placental viviparous species, the Pacific sharpnose shark (Rhizoprionodon longurio), and a yolk-sac viviparous species, the speckled guitarfish (Pseudobatos glaucostigmus). The R. longurio embryo tissues were 15 N enriched compared to the same tissues in the pregnant female, using the difference in δ15 N (Δδ15 N) between embryo and adult. Mean Δδ15 N was 2.17‰ in muscle, 4.39‰ in liver and 0.80‰ in blood. For P. glaucostigmus, embryo liver tissue was significantly 15 N enriched in comparison with liver of the pregnant female (Δδ15 N mean = 1.22‰), whereas embryo muscle was 15 N depleted relative to the muscle of the pregnant female (Δδ15 N mean = -1.22‰). Both species presented a significant positive linear relationship between Δδ15 N and embryo total length (LT ). The results indicated that embryos have different Δδ15 N depending on their reproductive strategy, tissue type analysed and embryo LT .

Concentrations of Silver, Chrome, Manganese and Nickel in Two Stranded Whale Sharks (Rhincodon typus) from the Gulf of California.

Concentrations of Ag, Cr, Mn and Ni were measured in tissues of two whale sharks (Rhincodon typus) stranded in La Paz Bay (LAP) and Punta Bufeo (PB), Gulf of California, during 2017 and 2018. The concentration range of Ni (0.012-1.12 µg/g ww) and Cr (0.16-5.21) in the epidermis of both specimens was lower compared to the concentrations found in the epidermis of whale sharks from East Africa. The whale shark from LAP exhibited higher levels of Mn (4.45 µg/g ww), Ni (0.284 µg/g ww) and Cr (5.21 µg/g ww) in the muscle compared to another filter feeder shark, the megamouth, from Taiwan and from Brazil. The highest concentrations of Ag were found in the heart (3.70) of the individual from LAP and in the filtering pads (1.93) of the shark from PB. Chromium in all selected tissues and the Mn found in the skeletal muscle, testicles (0.50), liver (Right lobe, 1.28; Left lobe, 1.63) and gills (1.54) of both sharks exceeded the limit established by the FAO/WHO for fish products.

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.

An estimate of the number of white sharks Carcharodon carcharias interacting with ecotourism in Guadalupe Island.

The aim of the present study is to provide an estimate of the number of white sharks Carcharodon carcharias that seasonally interact with ecotourism boats in Guadalupe Island using Schnabel's mark-recapture method and 6316 records of white sharks during 2012-2014. The results of the estimation highlight an abundance of 78 white sharks 95% C.I. (62.1, 105.6) interacting with ecotourism. The regulations regarding the number of tourists, boats and the monitoring of white sharks should be assessed to improve management decisions regarding the conservation and sustainable use of this threatened species.

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.

A new genus and two new species of trypanorhynch cestodes (Tentaculariidae) from the sharksCarcharhinus sorrah(Müller & Henle) andSphyrna lewini(Griffith & Smith) from off the coasts of Malaysia and Mexico.

Two new tentaculariid species were found infecting carcharhiniform sharks from off the coasts of Malaysian Borneo and the southwestern coast of the Baja California Sur, Mexico. Both new species exhibit a homeoacanthous heteromorphous basal and a homeoacanthous homeomorphous metabasal armature. Since this hook arrangement is unique within the tentaculariids and the taxonomy in this group deeply depends on the tentacular armature, Reimeriella n. g. is erected to accommodate R. varioacantha n. sp. ex Carcharhinus sorrah (Müller & Henle) and R. mexicoensis n. sp. ex Sphyrna lewini (Griffith & Smith). Unlike R. mexicoensis n. sp., R. varioacantha n. sp. has a pars bothrialis not overlapping the pars bulbosa and the number of testes is higher. Reimeriella mexicoensis n. sp. possesses very large uncinate to falcate hooks in the basal armature, while in R. varioacantha n. sp. these hooks are almost the same in size as the remaining hooks in both the basal and metabasal armature. The latter species is the first tentaculariid species where the metabasal armature very closely resembles an eutetrarhynchid with a heteroacanthous typical homeomorphous metabasal armature and a high number of spiniform hooks per half spiral row (10-11 vs 6-7 in R. mexicoensis n. sp.) in the metabasal and apical armature. This pattern provides further morphological evidence for the close relationship of the Eutetrarhynchoidea and the Tentacularioidea. Reimeriella varioacantha n. sp. enriches the trypanorhynch fauna from off the coast of Malaysian Borneo while R. mexicoensis n. sp. is a novel record of a tentaculariid trypanorhynch from the Mexican Pacific.

Trophic Structure and Biomagnification of Total Mercury in Ray Species Within a Benthic Food Web.

Stable isotopes of C (δ13C) and N (δ15N) were used to explore the trophic structure and evaluate mercury (Hg) biomagnification in the food web of muscle of three commercially important ray species from the Pacific coast of Baja California Sur (PCBCS): the shovelnose guitarfish (Pseudobatos productus), banded guitarfish (Zapteryx exasperata), and bat ray (Myliobatis californica). The food web of these ray species predominately consisted of zooplankton, three species of fish, and five species of invertebrates. Mean δ15N values in all species ranged from 10.54 ± 0.18‰ in zooplankton to 17.84 ± 0.81‰ in the shovelnose guitarfish. Mean δ13C values ranged from - 22.05 ± 0.75‰ in the red crab to - 15.93 ± 0.78‰ in the bat ray. Mean total Hg concentration ([THg]) in all species ranged from 0.0009 ± 0.0002 mg kg-1 ww in zooplankton to 0.24 ± 0.19 mg kg-1 ww in the banded guitarfish. The food web magnification factor was 6.38 and significantly greater than 1.0. The present study describes [THg] biomagnification in the benthic food web of three ray species of the PCBCS. This provides an important baseline knowledge of the biomagnification dynamics and pathways of Hg in this environment for these multiple interacting species.

Whale shark Rhincodon typus strandings in the Gulf of California, Mexico.

The present study analyses whale shark Rhincodon typus stranding in the Gulf of California, Mexico, reported by the public, scientists, authorities and artisanal fishermen. A total of 14 strandings were documented during the period 2001-2018. The total length of R. typus ranged from 350-1,102 cm, with a sex ratio of 3.5:1 (males: females). This study highlights potential stranding areas, the need for better stranding protocols to assist R. typus recovery and the importance of samples from dead animals for scientific research.

Seasonal trends in whale shark Rhincodon typus sightings in an established tourism site in the Gulf of California, Mexico.

The number of individual whale shark Rhincodon typus sightings registered October 2015-March 2018 in Bahia de La Paz, Mexico, ranged from 73 to 129 animals per season (total 1662), with the majority of them identified as males. Density plot maps showed high correlations in sightings between sample seasons and revealed potential hotspot areas. Our study provides an essential baseline of information for the management of whale shark conservation and the associated touristic activities in the region.

Reproductive characteristics and reproductive tract anatomy of the California butterfly ray Gymnura marmorata (Myliobatiformes: Gymnuridae).

The California butterfly ray Gymnura marmorata is frequently caught by artisanal fisheries in north-western Mexico (Baja California Sur; BCS). The aim of this study was to estimate reproductive characteristics and describe the micro and macroscopic reproductive structures of female and male G. marmorata. Sampling was carried out at two fisheries landing sites located on the west coast BCS, from 2008 to 2012. The largest disc width (WD ) ever recorded for this species was 131.0 cm and females were larger than males. The male sample was composed exclusively of adult specimens, with a median size at 50% maturity (WD50 ) estimated at 44.9 cm WD . For females, size at onset of maturity was estimated at 63.0 cm WD ; WD50 , at 64.7 cm WD ; and size at pregnancy at 80.1 cm WD . Gonadal asymmetry was observed for the first time in this species. Indeed, in males only the left testis was functional (testicular asymmetry), while in females, only the left ovary was functional (ovarian asymmetry).