The vulnerability of sharks, skates, and rays to ocean deoxygenation: Physiological mechanisms, behavioral responses, and ecological impacts.

Levels of dissolved oxygen in open ocean and coastal waters are decreasing (ocean deoxygenation), with poorly understood effects on marine megafauna. All of the more than 1000 species of elasmobranchs (sharks, skates, and rays) are obligate water breathers, with a variety of life-history strategies and oxygen requirements. This review demonstrates that although many elasmobranchs typically avoid hypoxic water, they also appear capable of withstanding mild to moderate hypoxia with changes in activity, ventilatory responses, alterations to circulatory and hematological parameters, and morphological alterations to gill structures. However, such strategies may be insufficient to withstand severe, progressive, or prolonged hypoxia or anoxia where anaerobic metabolic pathways may be used for limited periods. As water temperatures increase with climate warming, ectothermic elasmobranchs will exhibit elevated metabolic rates and are likely to be less able to tolerate the effects of even mild hypoxia associated with deoxygenation. As a result, sustained hypoxic conditions in warmer coastal or surface-pelagic waters are likely to lead to shifts in elasmobranch distributions. Mass mortalities of elasmobranchs linked directly to deoxygenation have only rarely been observed but are likely underreported. One key concern is how reductions in habitat volume as a result of expanding hypoxia resulting from deoxygenation will influence interactions between elasmobranchs and industrial fisheries. Catch per unit of effort of threatened pelagic sharks by longline fisheries, for instance, has been shown to be higher above oxygen minimum zones compared to adjacent, normoxic regions, and attributed to vertical habitat compression of sharks overlapping with increased fishing effort. How a compound stressor such as marine heatwaves alters vulnerability to deoxygenation remains an open question. With over a third of elasmobranch species listed as endangered, a priority for conservation and management now lies in understanding and mitigating ocean deoxygenation effects in addition to population declines already occurring from overfishing.

Can denticle morphology help identify southeastern Australian elasmobranchs?

Elasmobranchs are covered in scale-like structures called dermal denticles, comprising dentine and enameloid. These structures vary across the body of an individual and between species, and are frequently shed and preserved in marine sediments. With a good understanding of denticle morphology, current and historical elasmobranch diversity and abundance might be assessed from sediment samples. Here, replicate samples of denticles from the bodies of several known (deceased) shark species were collected and characterized for morphology before being assigned morphotypes. These data were used to expand the established literature describing denticles and to investigate intra- and interspecific variability, with the aim of increasing the viability of using sediment samples to assess elasmobranch diversity and abundance. Denticle morphology was influenced more by life-history traits than by species, where demersal species were largely characterized by generalized function and defense denticles, whereas pelagic and benthopelagic species were characterized by drag-reduction denticles. Almost all species possessed abrasion strength or defense denticles on the snout, precluding their utility for separating species. In a separate manipulative experiment, samples of denticles were collected from sediments in two aquaria with known elasmobranchs to determine their utility for reliably separating species. Visual examination of denticles, morphometric measurements, scaled photographs, and reference collections allowed for some precise identification, but not always to the species level. Ongoing work to develop denticle reference collections could help to identify past and present families and, in some cases, species.

Smooth muscle "microsphincters" in the gastric mucosa of stingrays (Elasmobranchii, Dasyatidae).

The occurrence of smooth muscle sphincters around gastric gland tubules in the cardiac stomach of some elasmobranch species is reported for the first time. These "microsphincters" took the form of a twisted torus, approximately 12-16 muscle fibres thick, that could fully constrict the gland tubules. However, their inconsistent positioning does not suggest a role in partitioning the tubules from the stomach lumen or in modulating secretory activity. Further research is required to ascertain the full taxonomic occurrence of these structures across the Elasmobranchii and to elucidate their function.

Visual discrimination and resolution in freshwater stingrays (Potamotrygon motoro).

Potamotrygon motoro has been shown to use vision to orient in a laboratory setting and has been successfully trained in cognitive behavioral studies using visual stimuli. This study explores P. motoro's visual discrimination abilities in the context of two-alternative forced-choice experiments, with a focus on shape and contrast, stimulus orientation, and visual resolution. Results support that stingrays are able to discriminate stimulus-presence and -absence, overall stimulus contrasts, two forms, horizontal from vertical stimulus orientations, and different colors that also vary in brightness. Stingrays tested in visual resolution experiments demonstrated a range of visual acuities from < 0.13 to 0.23 cpd under the given experimental conditions. Additionally, this report includes the first evidence for memory retention in this species.

Comparative study of cartilaginous fish divulges insights into the early evolution of primary, secondary and mucosal lymphoid tissue architecture.

Cartilaginous fish are located at a pivotal point in phylogeny where the adaptive immune system begins to resemble that of other, more-derived jawed vertebrates, including mammals. For this reason, sharks and other cartilaginous fish are ideal models for studying the natural history of immunity. Insights from such studies may include distinguishing the (evolutionarily conserved) fundamental aspects of adaptive immunity from the (more recent) accessory. Some lymphoid tissues of sharks, including the thymus and spleen, resemble those of mammals in both appearance and function. The cartilaginous skeleton of sharks has no bone marrow, which is also absent in bony fish despite calcified bone, but cartilaginous fish have other Leydig's and epigonal organs that function to provide hematopoiesis analogous to mammalian bone marrow. Conserved across all vertebrate phylogeny in some form is gut-associated lymphoid tissues, or GALT, which is seen from agnathans to mammals. Though it takes many forms, from typhlosole in lamprey to Peyer's patches in mammals, the GALT serves as a site of antigen concentration and exposure to lymphocytes in the digestive tract. Though more complex lymphoid organs are not present in agnathans, they have several primitive tissues, such as the thymoid and supraneural body, that appear to serve their variable lymphocyte receptor-based adaptive immune system. There are several similarities between the adaptive immune structures in cartilaginous and bony fish, such as the thymus and spleen, but there are mechanisms employed in bony fish that in some instances bridge their adaptive immune systems to that of tetrapods. This review summarizes what we know of lymphoid tissues in cartilaginous fishes and uses these data to compare primary and secondary tissues in jawless, cartilaginous, and bony fishes to contextualize the early natural history of vertebrate mucosal immune tissues.

The geographic distribution of reef and oceanic manta rays (Mobula alfredi and Mobula birostris) in Australian coastal waters.

The known distribution of manta rays in Australian waters is patchy, with records primarily centred around tourism hotspots. We collated 11,614 records of Mobula alfredi from photo-ID databases (n = 10,715), aerial surveys (n = 378) and online reports (n = 521). The study confirms an uninterrupted coastal distribution from north of 26°S and 31°S on the west and east coasts, respectively. More southerly M. alfredi records relate to warm-water events with a southernmost extent at 34°S. Coastal sightings of Mobula birostris were rare (n = 32), likely reflecting a preference for offshore waters, but encompass a wider latitudinal extent than M. alfredi of 10-40°S.

Contrasting life-history traits of two sympatric smooth-hound species: implication for vulnerability.

In this study, life-history traits (maximum and average size, size at maturity and fecundity) of two congeneric smooth-hounds, Mustelus mustelus and Mustelus punctulatus, which share a geographical distribution and experience a similar fishing exploitation, were estimated and compared between species. The results indicated a lower maximum and average size, a lower size at maturity and a higher fecundity in M. punctulatus compared with those in M. mustelus. Considering that these two species co-occur in the same areas and are caught by the same fishing gears, the results indicate a higher vulnerability to exploitation of M. mustelus compared with that of M. punctulatus.

Diet composition of starry smooth-hound Mustelus asterias and methodological considerations for assessing the trophic level of predatory fish.

The stomach contents of 640 starry smooth-hound Mustelus asterias from the north-east Atlantic were examined. The diet was dominated by crustaceans (98.8% percentage of index of relative importance, %IRI), with the two main prey species being hermit crab Pagurus bernhardus (34% IRI) and flying crab Liocarcinus holsatus (15% IRI). Ontogenetic dietary preferences showed that smaller individuals [20-69 cm total length (LT ) n = 283] had a significantly lower diversity of prey than larger individuals (70-124 cm LT , n = 348); however, 18 prey species were found exclusively in smaller individuals and eight prey taxa were found exclusively in larger individuals. Larger commercially important brachyurans such as edible crab Cancer pagurus and velvet swimming crab Necora puber were more prevalent in the diet of larger individuals. Specimens from the North Sea ecoregion had a lower diversity of prey types for a given sample size than fish from the Celtic Seas ecoregion. Whilst cumulative prey curves did not reach an asymptote, this was primarily due to the high taxonomic resolution utilized and 95% of the diet was described by just seven crustacean taxa. The trophic level (TL) was calculated as 4.34 when species-level prey categories were used. This fine-scale taxonomic resolution resulted in a TL estimate close to a whole level above that estimated using wider taxonomic groupings. This large bias has important methodological implications for TL studies based on categorized prey data, particularly those of predatory fish.

Social media posts reveal the geographic range of the Critically Endangered clown wedgefish, Rhynchobatus cooki.

The shark-like rays of the family Rhinidae (wedgefishes) are globally threatened with extinction. The poorly known clown wedgefish, Rhynchobatus cooki has historically been recorded only from fish markets in Singapore and Jakarta, Indonesia. Its natural geographic range has until now gone undocumented. Social media posts revealed the first wild records of this Critically Endangered species; six records were located between 2015 and 2020 from small-scale fisheries in Lingga and Singkep Islands, Indonesia. These results demonstrate the utility of social media searches to identify biogeographic records of cryptic and data-poor species.

Shearing overbite and asymmetrical jaw motions facilitate food breakdown in a freshwater stingray, Potamotrygon motoro.

Many species of fish process their prey with cyclic jaw motions that grossly resemble those seen in mammalian mastication, despite starkly different tooth and jaw morphologies. The degree of similarity between the processing behaviors of these disparate taxa has implications for our understanding of convergence in vertebrate feeding systems. Here, we used XROMM (X-ray reconstruction of moving morphology) to investigate prey processing behavior of Potamotrygon motoro, the ocellate river stingray, which has recently been found to employ asymmetrical, shearing jaw motions to break down its prey. We found that P. motoro modulates its feeding kinematics to produce two distinct types of chew cycles: compressive cycles and overbite cycles. The latter are characterized by over-rotation of the upper jaw relative to the lower jaw, past the expected occlusal limit, and higher levels of bilateral asymmetry as compared with compressive chews. We did not find evidence of the mediolateral shearing motions typical of mammalian mastication, but overbite cycles appear to shear the prey item between the upper and lower toothplates in a propalinal fashion. Additionally, comparison of hyomandibular and jaw motions demonstrates that the angular cartilages decouple jaw displacement from hyomandibular displacement in rostrocaudal and mediolateral directions. The multiple similarities between mammalian mastication and the dynamic processing behavior of P. motoro support the use of sub-family Potamotrygoninae as a model for studying evolutionary convergence of mastication-like processing.

Recombinant production of a bioactive peptide from spotless smooth-hound (Mustelus griseus) muscle and characterization of its antioxidant activity.

Bioactive peptides are short amino acid sequences with desirable health effects which are derived from animals, plants, and marine sources. In this study, recombinant production of a bioactive peptide (GIISHR) from spotless smooth-hound (Mustelus griseus) muscle and its antioxidant properties is discussed. A gene composed of 12 tandem copies of the peptide sequence was cloned in pET-28a and expressed as a His-tagged polypeptide in Escherichia coli. The recombinant polypeptide was then purified by Ni-NTA affinity chromatography, cleaved by Trypsin and purified by ultrafiltration. DPPH (1,1-diphenyl-2-picrylhydrazyl), ABTS (2,2'-azinobis-3-ethylbenzotiazoline-6-sulfonic acid) and hydroxyl radical scavenging activity assays, ferric reducing antioxidant power (FRAP) assay and ß-carotene bleaching test were used to characterize the antioxidant activity of the GIISHR. Liquid chromatography-mass spectrometry analysis revealed 60% purity for released bioactive peptide. Production yield was estimated as 60-80 mg GIISHR active peptide per 1 L bacterial culture. Antioxidant activity assays indicated that the antioxidant activity was increased with increase in peptide concentration. Though the DPPH radical scavenging activity, FRAP and ß-carotene bleaching power of the peptide were lower than those of the synthetic antioxidant tert-butylhydroquinone (TBHQ), the ABTS and hydroxyl radical scavenging activities of the peptide (at a concentration of 20 mg/mL) were similar to those of TBHQ (at a concentration of 0.1 mg/mL). The findings of the present study may be helpful in development of a process for production of the bioactive antioxidant peptides and its application in food industry.

First confirmed record of the Critically Endangered green sawfish Pristis zijsron from Bangladeshi waters.

In a study identifying the species composition of illegally traded elasmobranch products, evidence was collected of the presence of green sawfish Pristis zijsron in Bangladeshi waters of the Bay of Bengal. This is the first confirmed record of Pristis zijsron from this region, extending its known range > 1000 km to the north-west. This is an important record in a region where sawfish have declined significantly and are now rarely sighted; it highlights the urgency of further regional species-specific studies within the Indian Ocean.

Genetic and historical evidence of common sawsharks Pristiophorus cirratus in the waters of southern Queensland.

In 2011, a male pristiophorid was caught by a prawn trawler north east of Cape Moreton, Queensland, Australia. Molecular analyses confirmed the specimen to be the common sawshark Pristiophorus cirratus. Historical catch data indicate the occurrence of the species in the region but this is the first verified record of P. cirratus occurring in the waters of southern Queensland. Together, these records extend the recognised northern limit of P. cirratus by c. 500 km, which suggests that further investigation of its distribution is warranted.

Electroreception in marine fishes: chondrichthyans.

Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up-to-date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.

Contraception within an elasmobranch captive breeding programme: a case report on the eagle ray Aetobatus ocellatus using gonadotrophin-releasing hormone (GnRH) agonist deslorelin (Suprelorin).

This study describes the first case of contraception within a captive elasmobranch breeding programme where an implant of Suprelorin, containing a long-acting gonadotrophin-releasing hormone (GnRH) analogue Deslorelin, was implanted in an eagle ray Aetobatus ocellatus, which successfully halted breeding.

Kinematics of swimming of the manta ray: three-dimensional analysis of open-water maneuverability.

For aquatic animals, turning maneuvers represent a locomotor activity that may not be confined to a single coordinate plane, making analysis difficult, particularly in the field. To measure turning performance in a three-dimensional space for the manta ray (Mobula birostris), a large open-water swimmer, scaled stereo video recordings were collected. Movements of the cephalic lobes, eye and tail base were tracked to obtain three-dimensional coordinates. A mathematical analysis was performed on the coordinate data to calculate the turning rate and curvature (1/turning radius) as a function of time by numerically estimating the derivative of manta trajectories through three-dimensional space. Principal component analysis was used to project the three-dimensional trajectory onto the two-dimensional turn. Smoothing splines were applied to these turns. These are flexible models that minimize a cost function with a parameter controlling the balance between data fidelity and regularity of the derivative. Data for 30 sequences of rays performing slow, steady turns showed the highest 20% of values for the turning rate and smallest 20% of turn radii were 42.65±16.66 deg s-1 and 2.05±1.26 m, respectively. Such turning maneuvers fall within the range of performance exhibited by swimmers with rigid bodies.

Synthetic capacity does not predict elasmobranchs' ability to maintain trimethylamine oxide without a dietary contribution.

Trimethylamine oxide (TMAO) is an organic osmolyte and universal protein stabilizer. Its role as a cytoprotectant is particularly important in ureosmotic elasmobranchs that accumulate high levels of urea, a macromolecular perturbant. Feeding is a key component in the turnover and maintenance of these nitrogenous compounds. However, previous studies examining TMAO regulation have been largely completed using starved individuals, when nitrogen balance is altered. Here, under fed conditions, we test the importance of dietary TMAO on long-term maintenance in three elasmobranch species with differing endogenous synthetic capacities. Smoothhounds (Mustelus canis), spiny dogfish (Squalus acanthias), and little skates (Leucoraja erinacea) exhibited species- and tissue-specific differences in their ability to conserve TMAO when fed a low TMAO diet for 56days. Smoothhounds, a species with the capacity for endogenous production, exhibited a decrease in muscle TMAO. Spiny dogfish and little skates, species with no reported ability for synthesis, exhibited decreases in plasma and liver TMAO, respectively. Our findings are contrary to previous starvation studies demonstrating constant levels of TMAO for up to 56days in elasmobranchs. Further, the previously reported synthetic capacity of these species did not correlate with their ability to conserve TMAO and cannot be used to predict a species reliance on dietary contributions for prolonged maintenance. It is possible that all species rely to a degree on absorption of TMAO from the diet or that alternate synthetic or regulatory pathways play a larger role than previously thought.

Ultrasonography as a promising methodology to indicate captured-induced abortion in viviparous elasmobranchs.

This study aimed to characterize morphological aspects related to abortion through a non-lethal approach in the shortnose guitarfish Zapteryx brevirostris, an endemic and threatened species commonly caught by artisanal fisheries. Two females with signs of abortion and one female exhibiting external signs of pregnancy were purchased alive at a fish market during the period when this species has developing embryos in southern Brazil. Scans were conducted using a portable ultrasound. Females with signs of abortion revealed an absence of embryos despite having a similar morphology of the uterus when compared to the pregnant female. Examination of the pregnant female revealed the presence of two embryos, measuring c. 100 mm, each detected through their midline. This study presents new data on uterine macromorphology following successive abortive events in a viviparous elasmobranch species and validates ultrasonography as a diagnostic tool for the species. Ultrasonography is an effective, non-lethal and less-invasive methodology that is recommended for use in future studies of abortion and other reproductive events in elasmobranchs.

Biodiversity, Life History, and Conservation of Northeastern Pacific Chondrichthyans.

The sharks, batoids, and chimaeras, collectively the class Chondrichthyes, are one of the most successful groups of fishes, with over 1250 species globally. Recent taxonomic revisions have increased their diversity by about 20% over the past 17 years (2000-2016). The Northeast Pacific Ocean is one of the top 20 most diverse regions/countries on the globe with 77 chondrichthyan species, a number less than a quarter that of the most species-rich area (Australia) but that has increased by 10% since 2000 to include three new species (two skates and a chimaera). In this chapter we discuss the species richness of chondrichthyans occurring in the Northeast Pacific Ocean, characterize their life histories, briefly review several fisheries, and summarize the conservation status of those chondrichthyans occurring in the region. Detailed descriptions and evaluations of fisheries can be found in Chapter 7 of AMB Volume 78.

First insights into the function of the sawshark rostrum through examination of rostral tooth microwear.

Potential roles of the rostrum of sawsharks (Pristiophoridae), including predation and self-defence, were assessed through a variety of inferential methods. Comparison of microwear on the surface of the rostral teeth of sawsharks and sawfishes (Pristidae) show that microwear patterns are alike and suggest that the elongate rostra in these two elasmobranch families are used for a similar purpose (predation). Raman spectroscopy indicates that the rostral teeth of both sawsharks and sawfishes are composed of hydroxyapatite, but differ in their collagen content. Sawfishes possess collagen throughout their rostral teeth whereas collagen is present only in the centre of the rostral teeth of sawsharks, which may relate to differences in ecological use. The ratio of rostrum length to total length in the common sawshark Pristiophorus cirratus was found to be similar to the largetooth sawfish Pristis pristis but not the knifetooth sawfish Anoxypristis cuspidata. Analysis of the stomach contents of P. cirratus indicates that the diet consists of demersal fishes and crustaceans, with shrimp from the family Pandalidae being the most important dietary component. No prey item showed evidence of wounds inflicted by the rostral teeth. In light of the similarities in microwear patterns, rostral tooth chemistry and diet with sawfishes, it is hypothesised that sawsharks use their rostrum in a similar manner for predation (sensing and capturing prey) and possibly for self-defence.