Dasyatis Sabina Research Articles

Network Analysis Reveals Species-Specific Organization of Microbial Communities in Four Co-Occurring Elasmobranch Species along the Georgia Coast

Comparing co-occurring species may provide insights into how aspects of ecology may play a role in influencing their microbial communities. During the 2019 commercial shrimp trawl season off coastal Georgia, swabs of skin, gills, cloaca, and gut were taken for three species of batoids (Butterfly Ray, Bluntnose Stingray, and Atlantic Stingray) and one shark species (Atlantic Sharpnose) for high-throughput sequencing of the V4 region of the bacterial 16S rRNA gene. White muscle was analyzed for stable isotopes (δ13C and δ15N) to evaluate potential niche overlap in these four sympatric mesopredators. Significant differences were found in both δ13C and δ15N signatures across species, suggesting a degree of resource partitioning. When examined within tissue type, the host species had a weak effect on β-diversity for cloaca and skin, with no differences found for gill and gut samples. However, network analysis metrics demonstrated a stronger species-specific effect and distinct microbial community relationships were apparent between the shark and batoids, with the former having tighter networks for both internally- and externally-influenced tissues (gut/cloaca and skin/gills, respectively). Despite overlapping habitat use, species’ microbiomes differed in their organizational structuring that paralleled differences in stable isotope results, suggesting a mediating role of species-specific ecology on bacterial microbiomes.

Diagnostic agreement between three point-of-care glucose and β-hydroxybutyrate meters and reference laboratory methods in stingrays.

Point-of-care (POC) glucose and β-hydroxybutyrate (β-HB) meters can potentially provide rapid insight into an elasmobranch's metabolic state in clinical and field research settings. This study evaluated the diagnostic agreement of three commercial POC meters against reference laboratory methods for glucose and β-HB concentrations in stingrays. Blood was collected during anesthetized exams from 28 stingrays representing four species: cownose rays (Rhinoptera bonasus), Atlantic stingrays (Hypanus sabina), southern stingrays (Hypanus americanus), and yellow stingrays (Urobatis jamaicensis). Glucose and β-HB concentrations were measured with each POC meter using whole blood and plasma; in parallel, plasma glucose and β-HB concentrations were measured via reference laboratory methods. Agreement between POC meters and reference laboratory methods was assessed using Bland-Altman methods, Passing-Bablok regression, observed total error, percent relative error, and linear mixed effect models. Plasma glucose and β-HB concentrations determined by reference laboratory methods ranged from <20-63 mg/dL to 0.05-5.38 mmol/L, respectively. One human POC meter-the Precision Xtra-showed the greatest agreement with reference laboratory methods when measuring glucose with whole blood [mean bias and 95% CI: 0 (-3-4) mg/dL] and β-HB with plasma [mean bias and 95% CI: 0.1 (-0.04-0.2) mmol/L]. Stingray sex, weight, buffy coat, and packed cell volume did not significantly affect the agreement between POC meters and reference laboratory methods. Across all three POC meters, mean bias and imprecision for plasma β-HB concentrations were relatively small (0-0.1 mmol/L and 0%, respectively). Utilizing POC meters to measure glucose and β-HB in stingrays may be viable when reference methods are unavailable.

Morphological and histochemical characterization of the pectoral fin muscle of batoids.

Batoids differ from other elasmobranch fishes in that they possess dorsoventrally flattened bodies with enlarged muscled pectoral fins. Most batoids also swim using either of two modes of locomotion: undulation or oscillation of the pectoral fins. In other elasmobranchs (e.g., sharks), the main locomotory muscle is located in the axial myotome; in contrast, the main locomotory muscle in batoids is found in the enlarged pectoral fins. The pectoral fin muscles of sharks have a simple structure, confined to the base of the fin; however, little to no data are available on the more complex musculature within the pectoral fins of batoids. Understanding the types of fibers and their arrangement within the pectoral fins may elucidate how batoid fishes are able to utilize such unique swimming modes. In the present study, histochemical methods including succinate dehydrogenase (SDH) and immunofluoresence were used to determine the different fiber types comprising these muscles in three batoid species: Atlantic stingray (Dasyatis sabina), ocellate river stingray (Potamotrygon motoro) and cownose ray (Rhinoptera bonasus). All three species had muscles comprised of two muscle fiber types (slow-red and fast-white). The undulatory species, D. sabina and P. motoro, had a larger proportion of fast-white muscle fibers compared to the oscillatory species, R. bonasus. The muscle fiber sizes were similar between each species, though generally smaller compared to the axial musculature in other elasmobranch fishes. These results suggest that batoid locomotion can be distinguished using muscle fiber type proportions. Undulatory species are more benthic with fast-white fibers allowing them to contract their muscles quickly, as a possible means of escape from potential predators. Oscillatory species are pelagic and are known to migrate long distances with muscles using slow-red fibers to aid in sustained swimming.

Changes in the composition of coelomic fluid in the Atlantic stingray, Hypanus sabina, upon dilution of the environmental salinity: osmoregulatory and pH implications

Changes in the composition of coelomic fluid in the Atlantic stingray, Hypanus sabina, upon dilution of the environmental salinity: osmoregulatory and pH implications

Caudal Spine Morphology and Puncture Performance of Two Coastal Stingrays

A diagnostic characteristic of stingrays in the family Dasyatidae is the presence of a defensive, partially serrated spine located on the tail. We assessed the contribution of caudal spine morphology on puncture and withdrawal performance from two congeneric, co-occurring stingrays, the Atlantic stingray, Hypanus sabinus, and the bluntnose stingray, Hypanus say. Spines exhibited a high degree of morphological variability. Stingray spines were serrated along 50.8% (H. sabinus) or 62.3% (H. say) of their length. Hypanus say had a greater number of serrations along each side of the spine (30.4) compared with H. sabinus (20.7) but the pitch did not differ between species. We quantified spine puncture and withdrawal forces using porcine skin as a model for human skin. Puncture and withdrawal forces did not differ significantly between species, or within H. say, but withdrawal force was greater than puncture force for H. sabinus. We incorporated micro-computed tomography scanning to quantify tissue mineral density and found that for both species, the shaft of the spine was more heavily mineralized than the base, and midway (50%) along the length of the spine was more heavily mineralized than the tip. The mineralization variability along the spine shaft may create a stiff structure that can fracture once embedded within the target tissue and act as an effective predator deterrent.

Positional and ontogenetic variation in vertebral centra morphology in five batoid species

An increasing number of studies on elasmobranchs have shown that band-pair counts in vertebral centra do not accurately reflect age. Research in sharks has indicated that the number of band pairs vary with body size and that centrum morphology is related to structural needs. A study of this kind has not been undertaken on batoids; thus, we examined the relationship between band-pair deposition and morphology of centra along the vertebral column, and ontogenetically, for five batoid species (little skate, Leucoraja erinacea, winter skate, Leucoraja ocellata, barndoor skate, Dipturus laevis, Atlantic stingray, Dasyatis sabina, and round ray, Urobatis halleri). Centrum morphology and band-pair count varied along the vertebral column in all individuals of all species, except in young of the year. Variation in band-pair counts among centra within individuals supports the hypothesis that band-pair formation is related to somatic growth and body shape rather than to an annual cycle.

Electrosensory Impairment in the Atlantic Stingray, Hypanus sabinus, After Crude Oil Exposure

Elasmobranchs are renowned for their extremely sensitive electrosensory system, which is used to detect predators, prey, and mates, and is possibly used for navigation. The proper functioning of the electrosensory system is thus critical to fitness. The objective of this study was to test whether exposure to crude oil impairs the electroreceptive capabilities of elasmobranch fishes. Electrosensory function was quantified from six stingrays before and after exposure to a concentration of oil that mimicked empirically measured concentrations along the coast of Louisiana following the Deepwater Horizon spill. Orientation distance (cm), and angle with respect to the dipole axis of a prey-simulating electric field were used to derive the electric field intensity that elicited a response. Oil exposed stingrays continued to exhibit feeding behavior, but they initiated orientations to prey-simulating electric fields from a significantly closer orientation distance. The mean orientation distance after oil exposure was 5.29 ± 0.41 SE cm compared to a pre-exposure orientation distance of 7.16 ± 0.66 SE cm. Stingrays required a mean electric field intensity of 0.596 ± 0.21 SE μV cm-1 to initiate a response after oil exposure, compared to a mean of only 0.127 ± 0.03 SE μV cm-1 in uncontaminated seawater. Oil exposed stingrays thus exhibited a response to a stimulus approximately 4.7 times greater than controls. Stingrays impacted by an oil spill appear to experience reduced electrosensory capabilities, which could detrimentally impact fitness. This study is the first to quantify the effects of crude oil on behavioral electrosensory function.

Elasmobranch Community Dynamics in Florida’s Southern Indian River Lagoon

Many elasmobranch species utilize estuaries as nurseries, parturition areas, and foraging grounds. Florida’s Indian River Lagoon (IRL), an “estuary of national significance,” has experienced many anthropogenic impacts in recent decades, such as habitat degradation and declining water quality, and there is a substantial data gap surrounding the status of elasmobranchs in this system. A fishery-independent survey (longline/gillnet) was implemented to characterize the elasmobranch community and understand distribution patterns and habitat use in the IRL (Sebastian to St. Lucie Inlet). From July 2016 to June 2018, 630 individuals of 16 species were caught and tagged, including two critically endangered smalltooth sawfish Pristis pectinata. Bull sharks Carcharhinus leucas and Atlantic stingrays Hypanus sabinus were the two most common species collected (47% of the total catch), and size differences by region were observed. The longline catch exhibited a significant difference in species composition among regions while the gillnet catch composition significantly varied among seasons. Although dependent on survey gear type, there was evidence of combinations of abiotic parameters (e.g., depth, salinity, water clarity, distance to a freshwater source, distance to an inlet) driving elasmobranch species composition. Bull sharks and Atlantic stingrays dominated areas with frequently low salinities while more diverse assemblages of species were apparent towards inlet passes. This study provides the first in-depth analysis of the elasmobranch community in the IRL and develops capacity to understand how these species may respond to further environmental changes in this highly impacted estuary.

Bioactive properties of crude venom isolated from Hypanus sabinus

Bioactive properties of crude venom isolated from Hypanus sabinus

A large-scale sustained fish kill in the St. Johns River, Florida: A complex consequence of cyanobacteria blooms

In the summer of 2010, a sustained multispecies fish kill, affecting primarily adult red drum (Sciaenops ocellatus) and Atlantic stingray (Dasyatis sabina), along with various baitfish such as menhaden (Brevoortia spp.) and shad (Dorosoma spp.), was documented for six weeks along 50 km of the Lower St. Johns River (LSJR), Florida. An Aphanizomenon flos-aquae bloom was present in the freshwater reaches before the fish kill. The kill was triggered by a significant reverse-flow event and sudden influx of high-salinity water in late May that contributed to the collapse of the bloom upstream and brought euryhaline fish downstream into the vicinity of the senescing bloom or its by-products. The decomposing bloom led to a sequence of events, including the release of small amounts of cyanotoxins, bacterial lysis of cyanobacterial cells, high organic loading, and changes in the diversity and dominance of the plankton community to include Microcystis spp., Leptolyngbya sp., Pseudanabaena spp., Planktolyngbya spp., and low concentrations of Heterosigma akashiwo. Dissolved oxygen levels were within normal ranges in the reach of the fish kill, although elevated ammonia concentrations and high pH were detected farther upstream. These conditions resulted in complex pathological changes in fish that were not consistent with acute cyanotoxin exposure or with poor water quality but were attributable to chronic lethal hemolysis. Potential sources of hemolytic activity included H. akashiwo, Microcystis spp., and Bacillus cereus, a hemolytic bacterium. The continued presence of A. flos-aquae in the LSJR could have significant environmental repercussions and ideally the causal factors contributing to bloom growth and maintenance should be fully understood and managed.

Performance of Two Survey Gears Targeting Elasmobranchs in a Shallow, Subtropical Estuary

AbstractFishery‐independent surveys have become increasingly prevalent in recent decades for monitoring the population trends of highly mobile species like elasmobranchs (sharks and rays). Despite the utility of gear evaluations for streamlining costs and increasing the efficiency of fishery‐independent surveys, these assessments are sparse for elasmobranch‐specific surveys. Catch data were examined from a fishery‐independent longline and gill‐net survey that targeted elasmobranchs in Florida's southern Indian River Lagoon from July 2016 to September 2018. The goal of the study was to assess the effects of the type of longline bait that is used (Striped Mullet Mugil cephalus versus Atlantic Mackerel Scomber scombrus) and the size of gill‐net mesh (15.2‐ versus 20.3‐cm stretch mesh) on the species composition, catch per unit effort (CPUE), and size distribution of captured elasmobranchs. Elasmobranchs were caught more often in the gill net than on the longline. Striped Mullet yielded a significantly higher CPUE of elasmobranchs than Atlantic Mackerel did. Although Striped Mullet caught more sharks than Atlantic Mackerel did, the mean length of the sharks did not differ between groups that were captured with the two bait types. Species composition differed with respect to bait type; significantly more Bull Sharks Carcharhinus leucas and Atlantic Sharpnose Sharks Rhizoprionodon terraenovae were caught with Striped Mullet. Elasmobranch abundances were similar between the two sizes of gill‐net mesh. However, species composition differed, with a greater abundance of both Atlantic Stingrays Hypanus sabinus and Bull Sharks caught in the 15.2‐cm mesh. Elasmobranchs that were caught in the 20.3‐cm mesh were significantly larger than those caught in the 15.2‐cm mesh. The length distributions for the common species (Bull Sharks, Atlantic Stingrays, and Bluntnose Stingrays H. say) differed significantly with respect to the two mesh sizes. This study is the first assessment of a standardized elasmobranch‐specific survey in this nationally significant estuary and increases our understanding of the performance of complementary gear types for targeting sharks and rays in a shallow lagoonal system.

Argulus from the Pascagoula River, MS, USA, with an Emphasis on Those of the Threatened Gulf Sturgeon, Acipenser oxyrinchus desotoi

Species of Argulus (Branchiura Thorell, 1864) are common ectoparasites of freshwater, estuarine, and marine fishes. Argulid identification and taxonomy is often confusing because many species are reported to parasitize multiple host species, have similar morphological characters, and come from various salinity regimes. Gulf sturgeon is an anadromous fish natal to drainages in the north-central Gulf of Mexico, and as with many endangered species, has a poorly documented parasite community. During Gulf sturgeon tagging and monitoring studies (2016–2019) in the Pascagoula River, MS, USA, species of Argulus were collected from Gulf sturgeon as well as other incidentally captured fishes. Argulus flavescens Wilson, 1916 was found on Gulf sturgeon and flathead catfish, Argulus americanus Wilson, 1902 on bowfin, and Argulus bicolor Bere, 1936 on Atlantic stingray. We provide morphological details and measurements for these species as well as the first confirmed 28S rDNA molecular data. Argulus flavescens was more abundant and prevalent on larger Gulf sturgeon and on sturgeon captured in freshwater rather than estuarine habitats. Our results indicate that A. flacescens may not tolerate estuarine salinities and that the anadromous life-history pattern of Gulf sturgeon could help rid them of A. flavescens when they emigrate from their riverine habitats.

THE MESOPTERYGIAL VEIN: A RELIABLE VENIPUNCTURE SITE FOR INTRAVASCULAR ACCESS IN BATOIDS.

Intravascular access in batoid species is commonly achieved using the ventral coccygeal or radial wing vessels. However, these approaches can be difficult because of the presence of cartilage, lack of specific landmarks, species variation, and small vessel size in many species. This study used postmortem contrast radiography and gross dissection to develop landmarks for a new, dependable vascular access in three Myliobatiform species commonly maintained in captivity: Atlantic stingray (Hypanus sabinus), cownose ray (Rhinoptera bonasus), and smooth butterfly ray (Gymnura micrura). The mesopterygial vein provides quick vascular access and is suitable for administration of large fluid volumes and intravascular drugs. It is located immediately ventrolateral to the metapterygium cartilage, which sits adjacent to the coelomic cavity and supports the caudal half of the pectoral fin. Using the pectoral girdle and cranial third of the metapterygium cartilage as landmarks, vascular access can be achieved by directing a needle medially at approximately a 30° (adult cownose rays) or 45° angle (Atlantic stingrays, juvenile cownose rays, smooth butterfly rays) toward the metapterygium cartilage. Differences in the degree of needle direction are due to species and age-specific shapes of the metapterygium cartilage. The mesopterygial vein is an alternate site of quick and reliable venous access in batoid species.

Correction to: Mercury accumulation, speciation, and temporal trends in Atlantic Stingrays (Hypanus sabinus).

The corrections are: In the 2nd sentence of the Statistical Analyses section, the current sentence lacks important statistical assumption wording.

Mercury accumulation, speciation, and temporal trends in Atlantic Stingrays (Hypanus sabinus)

Mercury (Hg) deposited into aquatic sediments can be converted into the more toxic methylmercury (MeHg) by microbial activity. Atlantic stingrays (Hypanus sabinus) are an estuarine and nearshore species found in coastal regions of the western North Atlantic, occurring in multiple habitat types, and feeding mainly on benthic invertebrates. Mercury dynamics and speciation in stingrays have not been well examined. This study quantified total Hg and Hg species (Hg (II) and MeHg) in Atlantic stingrays sampled from Florida's Indian River Lagoon (IRL) from 2012 to 2013. Tissues (muscle and liver) collected from 29 stingrays were lyophilized and homogenized before being analyzed using a direct mercury analyzer. Concentrations of total Hg in muscle were positively related to stingray disk width, but concentrations in liver were not. Mean (±SD) total Hg in muscle (0.56 ± 0.30 mg/kg dw) was significantly higher than mean total Hg in liver (0.23 ± 0.19 mg/kg dw). Within liver tissue, percent MeHg (of total Hg) ranged from 31 to 99%. The ratio between total Hg in liver and total Hg in muscle was <1 for nearly all individuals, suggesting a lack of active hepatic demethylation and sequestration mechanisms. Concentrations of Hg in IRL Atlantic stingrays fall below concentrations known to result in direct toxicity to fishes; however, effects thresholds are not well understood for elasmobranchs. Comparisons of Hg concentrations in IRL Atlantic stingrays sampled previously (37 individuals in 1994) indicate that total Hg concentrations in muscle of Atlantic stingrays have decreased over the past two decades, suggesting a reduction in the bioavailable Hg in the IRL ecosystem.

Effect of Deepwater Horizon Crude Oil Water Accommodated Fraction on Olfactory Function in the Atlantic Stingray, Hypanus sabinus

The Deepwater Horizon oil spill was the largest accidental marine oil spill in history, releasing nearly 5 million barrels of crude oil. Crude oil causes both lethal and sublethal effects on marine organisms, and sensory systems have the potential to be strongly affected. Marine fishes rely upon the effective functioning of their sensory systems for detection of prey, mates, and predators. However, despite the obvious importance of sensory systems, the impact of crude oil exposure upon sensory function remains largely unexplored. Here we show that olfactory organ responses to amino acids are significantly depressed in oil exposed stingrays. We found that the response magnitude of the electro-olfactogram (EOG) to 1 mM amino acids decreased by an average of 45.8% after 48 h of exposure to an oil concentration replicating that measured in coastal areas. Additionally, in oil exposed individuals, the EOG response onset was significantly slower, and the clearing time was protracted. This study is the first to employ an electrophysiological assay to demonstrate crude oil impairment of the olfactory system in a marine fish. We show that stingrays inhabiting an area impacted by an oil spill experience reduced olfactory function, which would detrimentally impact fitness, could lead to premature death, and could cause additional cascading effects through lower trophic levels.

Registros limnéticos de Hypanus sabinus (Myliobatiformes: Dasyatidae) en la cuenca del río Grijalva, sur del Golfo de México

Abstract: Hypanus sabinus is reported in the limnetic environments in the coastal plain of the Southern Gulf of Mexico. Eight specimens were collected 51 km away from the coastline in electric conductivity values less than 1,017 µS cm-1. One pregnant female and one male with two caudal spines are included. These findings represent the first limnetic records of this species in southern Mexico.

Community structure of elasmobranchs in estuaries along the northwest Gulf of Mexico

Estuaries promote high levels of productivity and biodiversity by providing habitat for many biological communities due to their wide range of environmental conditions. Estuarine systems serve as nurseries, areas for parturition, and feeding grounds for elasmobranchs. However, estuaries face an array of anthropogenic pressures, including overfishing, altered flow regimes, pollution, and habitat destruction. Given the vulnerability of estuarine ecosystems, observing long-term changes in community structure is essential to understanding the effects of anthropogenic stressors. Elasmobranch community structure was analyzed among eight estuaries in the northwest Gulf of Mexico to evaluate spatial and temporal variability in species abundance and diversity using bi-annual fisheries independent gillnet survey data over three decades (1985–2014). Ten species comprised 99.4% of elasmobranchs caught which included 35.3% bull sharks (Carcharhinus leucas), 18.1% bonnetheads (Sphyrna tiburo), 17.0% cownose rays (Rhinoptera bonasus), 13.4% blacktip sharks (Carcharhinus limbatus), 5.9% Atlantic stingrays (Dasyatis sabina), 3.1% Atlantic sharpnose sharks (Rhizoprionodon terraenovae), 2.7% spinner sharks (Carcharhinus brevipinna), 2.1% scalloped hammerheads (Sphyrna lewini), 1.7% finetooth sharks (Carcharhinus isodon), and 0.7% lemon sharks (Negaprion brevirostris). During the study period, elasmobranch community structure changed among estuaries and among decades. Bull sharks, bonnetheads, cownose rays, blacktip sharks, and spinner sharks all increased in abundance during the study period, whereas finetooth sharks and lemon sharks decreased over time. Higher latitude estuaries were dominated by bull sharks while lower latitude estuaries were dominated by cownose rays. Salinity was the most important environmental variable in predicting individual elasmobranch species abundance (deviance explained: 14.4 ± 6.5 SD), while temperature and depth also played a role in shaping community structure. Diversity was greatest in mid-latitudinal estuaries with spatially and temporally dynamic salinity regimes. As environmental change and human impacts persist across much of the world, understanding environmental drivers of community structure using long-term datasets will provide insight to how these changes influence coastal ecosystems, and enable more comprehensive and scale-independent models to be developed for the management and conservation of coastal ecotones.

The physiological stress response of the Atlantic stingray (Hypanus sabinus) to aerial exposure

Although secondary stress physiology of elasmobranchs is fairly well studied, gaps remain in our understanding of species differences, including stress recovery. We examined the physiological stress response to air exposure in Atlantic stingrays (Hypanus sabinus) using a serial sampling method requiring minimal handling. Many elasmobranch stress studies exclusively quantify glucose, although there is evidence that elasmobranchs are unusually reliant on ketone bodies. Therefore, we also tested the hypothesis that ketone bodies play a significant role in the elasmobranch stress response by examining plasma β-hydroxybutyrate. Plasma osmolality, urea, trimethylamine-N-oxide, and a suite of ions were also measured to characterize departures from homeostasis due to air exposure. H. sabinus were exposed to air for 30 min and serially sampled at 0, 15, and 30 min, as well as 48 h after the stressor to assess the extent of recovery. Blood lactate and acidosis increased significantly during the stressor and returned to basal levels by 48 h. Glucose values were significantly affected, with the highest values observed at 48 h, suggesting that animals were not fully recovered as initially indicated by other metrics. Average plasma β-hydroxybutyrate was unaffected by the stressor. This suggests that ketone bodies may not be a major fuel source used during acute stress, at least in the timeframe examined.

Tidal and diel movement patterns of the Atlantic stingray (Dasyatis sabina) along a stream-order gradient

The behaviour of the Atlantic stingray (Dasyatis sabina) is affected by environmental cues, including time of day and tide. The purpose of the present study was to determine whether these cycles and differences in creek geomorphology affected presence and movement patterns of Atlantic stingrays near Savannah, GA, USA. Forty-five stingrays were tagged with Vemco coded-acoustic transmitters and passively tracked in two creek systems between December 2012 and December 2014. The geomorphology of the creeks was classified using the Horton stream-order concept, with the smallest tributaries assigned to the first order. Stingrays moved most at dusk (0.26±0.09 movements day–1), followed by night (0.23±0.09 movements day–1). Stingrays were found in deeper water during the cold season than during the warm season. Patterns in creek usage across tidal stages were nearly consistent across seasons. However, the diel pattern varied; stingrays utilised all creek orders throughout the diel cycle in the warm seasons, but entered only shallow creeks during the day in the cold season. Because presence and movements of stingrays were affected by tidal and diel cycles, these environmental factors could also affect their foraging patterns and their influence as an ecosystem engineer.