Swimming kinematics of the Caribbean reef shark, Carcharhinus perezi.

The Caribbean reef shark, Carcharhinus perezi, is known to rest on the substrate, a behaviour not documented in any of its congeners. We quantified the swimming kinematics of C. perezi in the wild and found that the head yawed at a frequency 15% greater than the tail beat, but that the amplitude of the tail exceeded the head yaw by approximately 80% across the range of velocities measured. We found that C. perezi velocity, head yaw frequency, and tailbeat frequency were all less than its obligate ram ventilating congener C. limbatus.

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.

Adult blacktip sharks (Carcharhinus limbatus) use shallow water as a refuge from great hammerheads (Sphyrna mokarran).

A refuge can be any space that keeps an organism safe from danger. Prey usually seek protection in the closest refuge available to minimize cost while maximizing survival. Aerial drone footage of blacktip sharks, Carcharhinus limbatus, along the coast of southeast Florida, USA, shows adult blacktips fleeing to the shallow water adjacent to the beach when confronted with or chased by a predatory great hammerhead shark, Sphyrna mokarran. To authors' knowledge, this is the first evidence of adult C. limbatus using shallow waters as a refuge.

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.

Magnetic field discrimination, learning, and memory in the yellow stingray (Urobatis jamaicensis).

Elasmobranch fishes (sharks, skates, and rays) have been hypothesized to use the geomagnetic field as a cue for orienting and navigating across a wide range of spatial scales. Magnetoreception has been demonstrated in many invertebrate and vertebrate taxa, including elasmobranchs, but this sensory modality and the cognitive abilities of cartilaginous fishes are poorly studied. Wild caught yellow stingrays, Urobatis jamaicensis (N = 8), underwent conditioning to associate a magnetic stimulus with a food reward in order to elicit foraging behaviors. Behavioral conditioning consisted of burying magnets and non-magnetic controls at random locations within a test arena and feeding stingrays as they passed over the hidden magnets. The location of the magnets and controls was changed for each trial, and all confounding sensory cues were eliminated. The stingrays learned to discriminate the magnetic stimuli within a mean of 12.6 ± 0.7 SE training sessions of four trials per session. Memory probes were conducted at intervals between 90 and 180 days post-learning criterion, and six of eight stingrays completed the probes with a ≥75% success rate and minimum latency to complete the task. These results show the fastest rate of learning and longest memory window for any batoid (skate or ray) to date. This study demonstrates that yellow stingrays, and possibly other elasmobranchs, can use a magnetic stimulus as a geographic marker for the location of resources and is an important step toward understanding whether these fishes use geomagnetic cues during spatial navigation tasks in the natural environment.

Freezing behaviour facilitates bioelectric crypsis in cuttlefish faced with predation risk.

Cephalopods, and in particular the cuttlefish Sepia officinalis, are common models for studies of camouflage and predator avoidance behaviour. Preventing detection by predators is especially important to this group of animals, most of which are soft-bodied, lack physical defences, and are subject to both visually and non-visually mediated detection. Here, we report a novel cryptic mechanism in S. officinalis in which bioelectric cues are reduced via a behavioural freeze response to a predator stimulus. The reduction of bioelectric fields created by the freeze-simulating stimulus resulted in a possible decrease in shark predation risk by reducing detectability. The freeze response may also facilitate other non-visual cryptic mechanisms to lower predation risk from a wide range of predator types.

A physiological analysis of color vision in batoid elasmobranchs.

The potential for color vision in elasmobranchs has been studied in detail; however, a high degree of variation exists among the group. Evidence for ultraviolet (UV) vision is lacking, despite the presence of UV vision in every other vertebrate class. An integrative physiological approach was used to investigate color and ultraviolet vision in cownose rays and yellow stingrays, two batoids that inhabit different spectral environments. Both species had peaks in UV, short, medium, and long wavelength spectral regions in dark-, light-, and chromatic-adapted electroretinograms. Although no UV cones were found with microspectrophotometric analysis, both rays had multiple cone visual pigments with λ max at 470 and 551 nm in cownose rays (Rhinoptera bonasus) and 475, 533, and 562 nm in yellow stingrays (Urobatis jamaicensis). The same analysis demonstrated that both species had rod λ max at 500 and 499 nm, respectively. The lens and cornea of cownose rays maximally transmitted wavelengths greater than 350 nm and greater than 376 nm in yellow stingrays. These results support the potential for color vision in these species and future investigations should reveal the extent to which color discrimination is significant in a behavioral context.

Sensitivity and specificity of the olfactory epithelia of two elasmobranch species to bile salts.

Odor detection in vertebrates occurs when odorants enter the nose and bind to molecular olfactory receptors on the cilia or microvilli of olfactory receptor neurons (ORNs). Several vertebrate groups possess multiple, morphologically distinct types of ORNs. In teleost fishes, these different ORN types detect specific classes of biologically relevant odorants, such as amino acids, nucleotides and bile salts. For example, bile salts are reported to be detected exclusively by ciliated ORNs. The olfactory epithelium of elasmobranch fishes (sharks, rays and skates) is comprised of microvillous and crypt ORNs, but lacks ciliated ORNs; thus, it was questioned whether the olfactory system of this group of fishes is capable of detecting bile salts. The present investigation clearly indicates that the olfactory system of representative shark and stingray species does detect and respond to bile salts. Additionally, these species detect glycine-conjugated, taurine-conjugated and non-conjugated bile salts, as do teleosts. These elasmobranchs are less sensitive to the tested bile salts than reported for both agnathans and teleosts, but this may be due to the particular bile salts selected in this study, as elasmobranch-produced bile salts are commercially unavailable. Cross-adaptation experiments indicate further that the responses to bile salts are independent of those to amino acids, a major class of odorant molecules for all tested fishes.

A content analysis of 32 years of Shark Week documentaries.

Despite evidence of their importance to marine ecosystems, at least 32% of all chondrichthyan species are estimated or assessed as threatened with extinction. In addition to the logistical difficulties of effectively conserving wide-ranging marine species, shark conservation is believed to have been hindered in the past by public perceptions of sharks as dangerous to humans. Shark Week is a high-profile, international programming event that has potentially enormous influence on public perceptions of sharks, shark research, shark researchers, and shark conservation. However, Shark Week has received regular criticism for poor factual accuracy, fearmongering, bias, and inaccurate representations of science and scientists. This research analyzes the content and titles of Shark Week episodes across its entire 32 years of programming to determine if there are trends in species covered, research techniques featured, expert identity, conservation messaging, type of programming, and portrayal of sharks. We analyzed titles from 272 episodes (100%) of Shark Week programming and the content of all available (201; 73.9%) episodes. Our data demonstrate that the majority of episodes are not focused on shark bites, although such shows are common and many Shark Week programs frame sharks around fear, risk, and adrenaline. While criticisms of disproportionate attention to particular charismatic species (e.g. great whites, bull sharks, and tiger sharks) are accurate and supported by data, 79 shark species have been featured briefly at least once. Shark Week's depictions of research and of experts are biased towards a small set of (typically visual and expensive) research methodologies and (mostly white, mostly male) experts, including presentation of many white male non-scientists as scientific experts. While sharks are more often portrayed negatively than positively, limited conservation messaging does appear in 53% of episodes analyzed. Results suggest that as a whole, while Shark Week is likely contributing to the collective public perception of sharks as bad, even relatively small alterations to programming decisions could substantially improve the presentation of sharks and shark science and conservation issues.

The distribution of manta rays in the western North Atlantic Ocean off the eastern United States.

In 2018, the giant manta ray was listed as threatened under the U.S. Endangered Species Act. We integrated decades of sightings and survey effort data from multiple sources in a comprehensive species distribution modeling (SDM) framework to evaluate the distribution of giant manta rays off the eastern United States, including the Gulf of Mexico. Manta rays were most commonly detected at productive nearshore and shelf-edge upwelling zones at surface thermal frontal boundaries within a temperature range of approximately 20-30 °C. SDMs predicted highest nearshore occurrence off northeastern Florida during April, with the distribution extending northward along the shelf-edge as temperatures warm, leading to higher occurrences north of Cape Hatteras, North Carolina from June to October, and then south of Savannah, Georgia from November to March as temperatures cool. In the Gulf of Mexico, the highest nearshore occurrence was predicted around the Mississippi River delta from April to June and again from October to November. SDM predictions will allow resource managers to more effectively protect manta rays from fisheries bycatch, boat strikes, oil and gas activities, contaminants and pollutants, and other threats.

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.

Olfactory morphology and physiology of elasmobranchs.

Elasmobranch fishes are thought to possess greater olfactory sensitivities than teleost fishes due in part to the large amount of epithelial surface area that comprises their olfactory organs; however, direct evidence correlating the size of the olfactory organ to olfactory sensitivity is lacking. This study examined the olfactory morphology and physiology of five distantly related elasmobranch species. Specifically, we quantified the number of lamellae and lamellar surface area (as if it were a flat sheet, not considering secondary lamellae) that comprise their olfactory organs. We also calculated the olfactory thresholds and relative effectiveness of amino acid odorants for each species. The olfactory organs varied in both the number of lamellae and lamellar surface area, which may be related to their general habitat, but neither correlated with olfactory threshold. Thresholds to amino acid odorants, major olfactory stimuli of all fishes, ranged from 10⁻9·° to 10⁻6·9 mol l⁻¹, which indicates that these elasmobranch species demonstrate comparable thresholds with teleosts. In addition, the relative effectiveness of amino acid stimuli to the olfactory organ of elasmobranchs is similar to that previously described in teleosts with neutral amino acids eliciting significantly greater responses than others. Collectively, these results indicate parallels in olfactory physiology between these two groups of fishes.

Response of the hammerhead shark olfactory epithelium to amino acid stimuli.

Sharks and rays are highly sensitive to chemical stimuli in their natural environment but several hypotheses predict that hammerhead sharks, with their expanded head and enlarged olfactory epithelium, have particularly acute olfactory systems. We used the electro-olfactogram (EOG) technique to compare the relative response of the scalloped hammerhead shark (Sphyrna lewini) olfactory epithelium to 20 proteinogenic amino acids and determine the sensitivity for 6 amino acids. At micromolar concentrations, cysteine evoked the greatest EOG response which was approximately twice as large as that of alanine. The weakest response was obtained for proline followed by aspartic acid and isoleucine. The olfactory epithelium showed adaptation to sequential stimulation, and recovery was related to the inter-stimulus time period. Estimated EOG response thresholds were in the sub-nanomolar range for both alanine (9.2 x 10(-11) M) and cysteine (8.4 x 10(-10) M) and in the micromolar range for proline and serine. These thresholds from 10(-10) to 10(-6) M for the scalloped hammerhead shark are comparable or lower than those reported for other teleost and elasmobranch species. Future work should focus on binary and more complex compounds to test for competition and cross-adaptation for different classes of peripheral receptors, and their responses to molecules found in biologically relevant stimuli.

Functional consequences of structural differences in stingray sensory systems. Part I: mechanosensory lateral line canals.

Short range hydrodynamic and electrosensory signals are important during final stages of prey capture in elasmobranchs (sharks, skates and rays), and may be particularly useful for dorso-ventrally flattened batoids with mouths hidden from their eyes. In stingrays, both the lateral line canal and electrosensory systems are highly modified and complex with significant differences on ventral surfaces that relate to feeding ecology. This study tests functional hypotheses based on quantified differences in sensory system morphology of three stingray species, Urobatis halleri, Myliobatis californica and Pteroplatytrygon violacea. Part I investigates the mechanosensory lateral line canal system whereas part II focuses on the electrosensory system. Stingray lateral line canals include both pored and non-pored sections and differ in branching complexity and distribution. A greater proportion of pored canals and high pore numbers were predicted to correspond to increased response to water flow. Behavioral experiments were performed to compare responses of stingrays to weak water jets mimicking signals produced by potential prey at velocities of 10-20 cm s(-1). Bat rays, M. californica, have the most complex and broadly distributed pored canal network and demonstrated both the highest response rate and greater response intensity to water jet signals. Results suggest that U. halleri and P. violacea may rely on additional sensory input, including tactile and visual cues, respectively, to initiate stronger feeding responses. These results suggest that stingray lateral line canal morphology can indicate detection capabilities through responsiveness to weak water jets.

Functional consequences of structural differences in stingray sensory systems. Part II: electrosensory system.

Elasmobranch fishes (sharks, skates and rays) possess highly sensitive electrosensory systems, which enable them to detect weak electric fields such as those produced by potential prey organisms. Different species have unique electrosensory pore numbers, densities and distributions. Functional differences in detection capabilities resulting from these structural differences are largely unknown. Stingrays and other batoid fishes have eyes positioned on the opposite side of the body from the mouth. Furthermore, they often feed on buried prey, which can be located non-visually using the electrosensory system. In the present study we test functional predictions based on structural differences in three stingray species (Urobatis halleri, Pteroplatytrygon violacea and Myliobatis californica) with differing electrosensory system morphology. We compare detection capabilities based upon behavioral responses to dipole electric signals (5.3-9.6 microA). Species with greater ventral pore numbers and densities were predicted to demonstrate enhanced electrosensory capabilities. Electric field intensities at orientation were similar among these species, although they differed in response type and orientation pathway. Minimum voltage gradients eliciting feeding responses were well below 1 nVcm(-1) for all species regardless of pore number and density.

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.

Etmopterus lailae sp. nov., a new lanternshark (Squaliformes: Etmopteridae) from the Northwestern Hawaiian Islands.

A new species of lanternshark, Etmopterus lailae (Squaliformes: Etmopteridae), is described from the Northwestern Hawaiian Islands, in the central North Pacific Ocean. The new species resembles other members of the "Etmopterus lucifer" clade in having linear rows of dermal denticles, and most closely resembles E. lucifer from Japan. The new species occurs along insular slopes around seamounts at depths between 314-384 m. It can be distinguished from other members of the E. lucifer clade by a combination of characteristics, including a longer anterior flank marking branch, arrangement of dermal denticles on the ventral snout surface and body, flank and caudal markings, and meristic counts including number of spiral valve turns, and precaudal vertebrate. A key to species of the Etmopterus lucifer-clade is included.

Quantification of Massive Seasonal Aggregations of Blacktip Sharks (Carcharhinus limbatus) in Southeast Florida.

Southeast Florida witnesses an enormous seasonal influx of upper trophic level marine predators each year as massive aggregations of migrating blacktip sharks (Carcharhinus limbatus) overwinter in nearshore waters. The narrow shelf and close proximity of the Gulf Stream current to the Palm Beach County shoreline drive tens of thousands of sharks to the shallow, coastal environment. This natural bottleneck provides a unique opportunity to estimate relative abundance. Over a four year period from 2011-2014, an aerial survey was flown approximately biweekly along the length of Palm Beach County. A high definition video camera and digital still camera mounted out of the airplane window provided a continuous record of the belt transect which extended 200 m seaward from the shoreline between Boca Raton Inlet and Jupiter Inlet. The number of sharks within the survey transect was directly counted from the video. Shark abundance peaked in the winter (January-March) with a maximum in 2011 of 12,128 individuals counted within the 75.6 km(-2) belt transect. This resulted in a maximum density of 803.2 sharks km(-2). By the late spring (April-May), shark abundance had sharply declined to 1.1% of its peak, where it remained until spiking again in January of the following year. Shark abundance was inversely correlated with water temperature and large numbers of sharks were found only when water temperatures were less than 25 °C. Shark abundance was also correlated with day of the year but not with barometric pressure. Although shark abundance was not correlated with photoperiod, the departure of the sharks from southeast Florida occurred around the vernal equinox. The shark migration along the United States eastern seaboard corresponds spatially and temporally with the spawning aggregations of various baitfish species. These baseline abundance data can be compared to future studies to determine if shark population size is changing and if sharks are restricting their southward migration as global water temperatures increase.

Olfactory morphology of carcharhinid and sphyrnid sharks: does the cephalofoil confer a sensory advantage?

Many hypotheses have been advanced to explain the adaptive significance of the sphyrnid cephalofoil, including potential advantages of spacing the olfactory organs at the distal tips of the broad surface. We employed comparative morphology to test whether the sphyrnid cephalofoil provides better stereo-olfaction, increases olfactory acuity, and samples a greater volume of the medium compared to the situation in carcharhiniform sharks. The broadly spaced nares provide sphyrnid species with a significantly greater separation between the olfactory rosettes, which could lead to an enhanced ability to resolve odor gradients. In addition, most sphyrnid species possess prenarial grooves that greatly increase the volume of water sampled by the nares and thus increase the probability of odorant encounter. However, despite a much greater head width, and a significantly greater number of olfactory lamellae, scalloped hammerhead sharks do not possess a greater amount of olfactory epithelial surface area than the carcharhiniform sandbar sharks. Therefore, sphyrnid sharks might not possess any greater olfactory acuity than carcharhinids. Despite this, there are clear olfactory advantages to the cephalofoil head morphology that could have led to its evolution, persistence, and diversification. persistence, and diversification.

The sexually dimorphic cephalofoil of bonnethead sharks, Sphyrna tiburo.

Sexually dimorphic head shape is common in vertebrates from teleosts to mammals. Herein we document that cephalic sexual dimorphism is also found in the cartilaginous fishes (Chondrichthyes). Male bonnethead sharks develop a prominent bulge along the anterior margin of the cephalofoil at the onset of sexual maturity. This contrasts with the uniformly rounded anterior margin of adult females and juveniles and embryos of both sexes. The anterior cephalic bulge is produced by elongation of the rod-like rostral cartilages, and its appearance corresponds temporally with the elongation of the rod-like cartilages of the male intromittent organs (claspers). We propose that the rostral cartilage elongation is a byproduct of endocrinological changes at the onset of sexual maturity that stimulate growth of the clasper cartilages. The basal location of the chondrichthyan fishes within the vertebrate clade extends the earliest appearance of cephalic sexual dimorphism among the vertebrates.