Feeding behavior and kinematics of the lesser electric ray, Narcine brasiliensis (Elasmobranchii: Batoidea)

Jaw protrusion is a major functional motif in fish feeding and can occur during mouth opening or closing. This temporal variation impacts the role that jaw protrusion plays in prey apprehension and processing. The lesser electric ray Narcine brasiliensis is a benthic elasmobranch (Batoidea: Torpediniformes) with an extreme and unique method of prey capture. The feeding kinematics of this species were investigated using high-speed videography and pressure transduction. The ray captures its food by protruding its jaws up to 100% of head length (approximately 20% of disc width) beneath the substrate and generating negative oral pressures (< or = 31 kPa) to suck worms into its mouth. Food is further winnowed from ingested sediment by repeated, often asymmetrical protrusions of the jaws (> 70 degrees deviation from the midline) while sand is expelled from the spiracles, gills and mouth. The pronounced ram contribution of capture (jaw protrusion) brings the mouth close enough to the food to allow suction feeding. Due to the anatomical coupling of the jaws, upper jaw protrusion occurs in the expansive phase (unlike most elasmobranchs and similar to bony fishes), and also exhibits a biphasic (slow-open, fast-open) movement similar to tetrapod feeding. The morphological restrictions that permit this unique protrusion mechanism, including coupled jaws and a narrow gape, may increase suction performance, but also likely strongly constrain dietary breadth.     

Functional morphology of jaw trabeculation in the lesser electric ray Narcine brasiliensis, with comments on the evolution of structural support in the Batoidea

The design of minimum-weight structures that retain their integrity under dynamic loading regimes has long challenged engineers. One solution to this problem found in both human and biological design is the optimization of weight and strength by hollowing a structure and replacing its inner core with supportive struts. In animals, this design is observed in sand dollar test, avian beak, and the cancellous bone of tetrapod limbs. Additionally, within the elasmobranch fishes, mineralized trabeculae (struts) have been reported in the jaws of durophagous myliobatid stingrays (Elasmobranchii: Batoidea), but were believed to be absent in basal members of the batoid clade. This study, however, presents an additional case of batoid trabeculation in the lesser electric ray, Narcine brasiliensis (Torpediniformes). The trabeculae in these species likely play different functional roles. Stingrays use their reinforced jaws to crush bivalves, yet N. brasiliensis feeds by ballistically protruding its jaws into the sediment to capture polychaetes. In N. brasiliensis, trabeculae are localized to areas likely to experience the highest load: the quadratomandibular jaw joints, hyomandibular-cranial joint, and the thinnest sections of the jaws immediately lateral to the symphyses. However, the supports perform different functions dependent on location. In regions where the jaws are loaded transversely (as in durophagous rays), "load leading" trabeculae distribute compressive forces from the cortex through the lumen of the jaws. In the parasymphyseal regions of the jaws, "truss" trabeculae form cross-braces perpendicular to the long axes of the jaws. At peak protrusion, the jaw arch is medially compressed and the jaw loaded axially such that these trabeculae are positioned to resist buckling associated with excavation forces. "Truss" trabeculae function to maintain the second moment of area in the thinnest regions of the jaws, illustrating a novel function for batoid trabeculation. Thus, this method of structural support appears to have arisen twice independently in batoids and performs strikingly different ecological functions associated with the distribution of extreme loading environments.     

Electric organ morphology and function in the lesser electric ray,Narcine brasiliensis

The lesser electric ray, Narcine brasiliensis, is a small, demersal ray capable of generating electricity through its main and accessory electric organs. Although closely related to the large piscivorous torpedo rays, it differs in size, habitat, and prey. Based on these differences, we hypothesized that the main electric organs are used for predator defense rather than feeding and that the accessory electric organs, specific to this species, are used for intraspecific communication. We found that the mass of the main and accessory electric organs were both significantly smaller in females than in males. Whereas the main electro-somatic index does not change with growth, the accessory electro-somatic index increases, providing support for the accessory electric organs’ use in intraspecific communication. We characterized the discharge properties of the main electric organ throughout ontogeny by simulating a predation attempt on the ray. Rays always responded by generating electric organ discharges (EODs) and by flexing the tail dorsoventrally and laterally. The main EOD amplitude, measured directly at the source, increased logarithmically with disc width to a maximum measured amplitude of 56 V. Minimum amplitude was more variable, but followed a positive power relationship with disc width. Neonates produced trains comprised of significantly more EODs than the adults. Over the course of the first set of discharges, all age classes showed a decrease in fundamental frequency and an increase in train duration. In contrast to these defensive responses, the rays did not generate EODs while foraging or feeding on live prey.     

Tooth reorientation affects tooth function during prey processing and tooth ontogeny in the lesser electric ray, Narcine brasiliensis

The dental anatomy of elasmobranch fishes (sharks, rays and relatives) creates a functional system that is more dynamic than that of mammalian dentition. Continuous dental replacement (where new teeth are moved rostrally to replace older ones) and indirect fibrous attachment of the dentition to the jaw allow teeth to reorient relative to the jaw over both long- and short-term scales, respectively. In this study, we examine the processing behavior and dental anatomy of the lesser electric ray Narcine brasiliensis (Olfers, 1831) to illustrate that the freedom of movement of elasmobranch dentition allows a functional flexibility that can be important for complex prey processing behaviors. From static manipulations of dissected jaws and observations of feeding events in live animals, we show that the teeth rotate during jaw protrusion, resulting in a secondary grasping mechanism that likely serves to hold prey while the buccal cavity is flushed free of sediment. The function of teeth is not always readily apparent from morphology; in addition to short-term reorientation, the long-term dental reorientation during replacement allows a given tooth to serve multiple functions during tooth ontogeny. Unlike teeth inside the mouth, the cusps of external teeth (on the portion of the tooth pad that extends past the occlusal plane) lay flat, such that the labial faces act as a functional battering surface, protecting the jaws during prey excavation.     

Ecomorphology of the digestive tract of the brazilian electric ray Narcine brasiliensis (Olfers, 1831) (Torpediniformes: Narcinidae)

Elasmobranchii shows particular characteristics that make them susceptible to the impacts caused by fishing pressure, especially bottom trawling, which mostly affect rays, as they have demersal habits. Based on food availability and feeding ability, Polychaeta and Sipunculiforme are the bases of Brazilian electric ray Narcine brasiliensis diet. Morphologically, the digestion starts in the oesophagus with acid mucines action. The existence of acid and neutral mucines in the posterior intestine prevents lesions in the mucosa and favours the passage of faeces and shell residues. Thus, this study shows the interaction between their habitat, the organisms and their morphophysiology.     

Growth and derived life-history characteristics of the Brazilian electric ray Narcine brasiliensis

The majority of batoids are listed as Threatened (20.4%) or Data Deficient (41%) by the IUCN Red List. A key challenge to assessing Data-Deficient species is obtaining estimates of key life-history characteristics. Here, a Bayesian approach was used to estimate derived life-history characteristics from a growth model applied to the Data-Deficient Brazilian electric ray Narcine brasiliensis. The age of 170 specimens (107 females, 63 males) was estimated from vertebral centra, and total length, disc width, total weight and birth size were used in a joint estimation of sex-specific length-weight models and two-dimensional von Bertalanffy growth models. Estimates of age at length zero, age at maturity, longevity and mortality at age were derived simultaneously. The Bayesian joint modelling approach was robust to small sample sizes by adding a likelihood to constrain L₀ and sharing parameters, such as Brody growth coefficient between length measurements. The median growth parameter estimates were a shared L₀ = 38.8 mm, female L_∞ = 515 mm, 𝑘 = 0.125 and male L_∞ = 387 mm, 𝑘 = 0.194. Age at maturity was estimated to be 7.40–7.49 years for females and 4.45–4.47 years for males, whereas longevity was 22.5–22.6 years for females and 14.2 years for males depending on length measurement. Age-1 natural mortality was estimated to be 0.199–0.207 for females and 0.211–0.213 for males. The derived life-history characteristics indicate N. brasiliensis is earlier maturing, but slower growing relative to other Torpediniformes. These characteristics along with the species’ endemism to southern Brazil and high by-catch rates indicate that one of the IUCN Red List threatened categories may be more appropriate for the currently Data-Deficient status. The Bayesian approach used for N. brasiliensis can prove useful for utilizing limited age-growth data in other Data-Deficient batoid species to inform necessary life characteristics for conservation and management.     

Sexual, ontogenetic, temporal and spatial effects on the diet of Urotrygon rogersi (Elasmobranchii:Myliobatiformes)

The food habits and trophic ecology of Urotrygon rogersi were analysed to ascertain sexual, ontogenetic, temporal and spatial effects on the diet. These effects were examined with contingency tables, simple correspondence analysis and MANOVA. The trophic relationships of the species were determined with Levin's niche amplitude index and Pianka's diet overlap index. Urotrygon rogersi is a predator of benthic organisms, especially shrimp and polychaetes. Analysis of sex and time showed no significant differences, but differences among class sizes were found. A strong trend towards diet specialization and a strong overlap between sexes and between class sizes were found. Finally, fishing activity on shrimps in the study area could force U. rogersi to change its trophic spectrum over time as an adaptation to the considerable reduction in its principal prey.     

Anatomy of the feeding apparatus of the nurse shark,Ginglymostoma cirratum

The anatomy of the feeding apparatus of the nurse shark, Ginglymostoma cirratum, was investigated by gross dissection and computer axial tomography. The labial cartilages, jaws, jaw suspension, muscles, and ligaments of the head are described. Palatoquadrate cartilages articulate with the chondrocranium caudally by short, laterally projecting hyomandibulae and rostrally by ethmoorbital articulations. Short orbital processes of the palatoquadrates are joined to the ethmoid region of the chondrocranium by short, thin ethmopalatine ligaments. In addition, various ligaments, muscles, and the integument contribute to the suspension of the jaws. When the mouth is closed and the palatoquadrate retracted, the palatine process of the palatoquadrate is braced against the ventral surface of the nasal capsule and the ascending process of the palatoquadrate is in contact with the rostrodorsal end of the suborbital shelf. When the mandible is depressed and the palatoquadrate protrudes slightly rostroventrally, the palatoquadrate moves away from the chondrocranium. A dual articulation of the quadratomandibular joint restricts lateral movement between the mandible and the palatoquadrate. The vertically oriented preorbitalis muscle spans the gape and is hypothesized to contribute to the generation of powerful crushing forces for its hard prey. The attachment of the preorbitalis to the prominent labial cartilages is also hypothesized to assist in the retraction of the labial cartilages during jaw closure. Separate levator palatoquadrati and spiracularis muscles, which are longitudinally oriented and attach the chondrocranium to the palatoquadrate, are hypothesized to assist in the retraction of the palatoquadrate during the recovery phase of feeding kinematics. Morphological specializations for suction feeding that contribute to large subambient suction pressures include hypertrophied coracohyoideus and coracobranchiales muscles to depress the hyoid and branchial arches, a small oral aperture with well‐developed labial cartilages that occlude the gape laterally, and small teeth. J. Morphol. 241:33–60, 1999. © 1999 Wiley‐Liss, Inc.     

Evidence of a counter-current heat exchanger in the ray, Mobula tarapacana (Chondrichthyes: Elasmobranchii: Batoidea: Myliobatiformes)

A vascular network, or rete, has been found in the pectoral fin of the mobulid ray, Mobula tarapacana. This rete appears to be a counter-current heat exchanger which, in conjunction with a high level of red muscle, indicates that this ray is warm-bodied. Preliminary results on other closely related rays indicate that retia may be more common amongst the rays than previously thought.     

Functional morphology of the feeding apparatus,feeding constraints,and suction performance in the nurse shark Ginglymostoma cirratum

The nurse shark, Ginglymostoma cirratum, is an obligate suction feeder that preys on benthic invertebrates and fish. Its cranial morphology exhibits a suite of structural and functional modifications that facilitate this mode of prey capture. During suction‐feeding, subambient pressure is generated by the ventral expansion of the hyoid apparatus and the floor of its buccopharyngeal cavity. As in suction‐feeding bony fishes, the nurse shark exhibits expansive, compressive, and recovery kinematic phases that produce posterior‐directed water flow through the buccopharyngeal cavity. However, there is generally neither a preparatory phase nor cranial elevation. Suction is generated by the rapid depression of the buccopharyngeal floor by the coracoarcualis, coracohyoideus, and coracobranchiales muscles. Because the hyoid arch of G. cirratum is loosely connected to the mandible, contraction of the rectus cervicis muscle group can greatly depress the floor of the buccopharyngeal cavity below the depressed mandible, resulting in large volumetric expansion. Suction pressures in the nurse shark vary greatly, but include the greatest subambient pressures reported for an aquatic‐feeding vertebrate. Maximum suction pressure does not appear to be related to shark size, but is correlated with the rate of buccopharyngeal expansion. As in suction‐feeding bony fishes, suction in the nurse shark is only effective within approximately 3 cm in front of the mouth. The foraging behavior of this shark is most likely constrained to ambushing or stalking due to the exponential decay of effective suction in front of the mouth. Prey capture may be facilitated by foraging within reef confines and close to the substrate, which can enhance the effective suction distance, or by foraging at night when it can more closely approach prey. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

New data on the systematics and interrelationships of sawfishes (Elasmobranchii, Batoidea, Pristiformes)

New characters based on the arrangement and morphology of dermal denticles show that sawfishes can be divided into two distinctive groups. The first group, comprising the knifetooth sawfish Anoxypristis cuspidata , is characterized by tricuspid denticles variably located on both dorsal and ventral parts of the body. The second group is represented by species of the genus Pristis , showing an uniform and homogenous dermal covering of monocuspidate denticles on both dorsal and ventral sides of the body and within the buccopharyngeal cavity. Pristis is further divided into two subgroups: the first comprises species with denticles lacking any keels and furrows (the smalltooth sawfish Pristis pectinata , the green sawfish Pristis zijsron and the dwarf sawfish Pristis clavata ); the second comprises species with denticles presenting keels and furrows well differentiated on their anterior part (the common sawfish Pristis pristis , the largetooth sawfish Pristis perotteti and the greattooth sawfish Pristis microdon ). This investigation of the dermal covering provides results which agree with studies that separate the same two species groups of Pristis on the basis of other morphological data.     

Anatomy ofTrigonognathus kabeyai,with comments on feeding mechanism and phylogenetic relationships (Elasmobranchii,Squalidae)

The skeleton and musculature ofTrigonognathus kabeyai are described in detail. The particular jaw dentition suggests thatTrigonognathus has a clutching-type feeding action. Several characters that might serve this function are discussed from the point of the functional morphology. The phylogenetic relationships ofTrigonognathus are not fully resolved, but it possesses three of the four synapomorphies of the Etmopterinae, i.e., two separate labial cartilages, no supraotic shelf, and prespinal radiais. Furthermore, three equally probable hypotheses ofTrigonognathus relationships, a sister relationship with all etmopterine genera,Etmopterus+Miroscyllium, andAculeola+Centroscyllium, are discussed.     

A new species of Branchellion Savigny, 1822 (Hirudinida: Piscicolidae), a marine leech parasitic on the giant electric ray Narcine entemedor Jordan & Starks (Batoidea: Narcinidae) off Oaxaca,Mexico

Branchellion spindolaorum n. sp. (Hirudinida: Piscicolidae) is described based on specimens found parasitising the giant electric ray Narcine entemedor Jordan & Starks off the coast of Oaxaca, Mexico. The new species can be clearly distinguished from the other species of Branchellion Savigny, 1822 by the presence of 30 pairs of lateral branchiae and 10 pairs of pulsatile vesicles. The definition of the genus Branchellion is expanded to include species with either 30, 31 or 33 pairs of foliaceous (plate-like) lateral branchiae in the urosome. In addition, we provide for the first time for the genus, scanning electron micrographs of the secondary suckers located on the ventral surface of the posterior sucker. Additionally, partial DNA sequences of the mitochondrial cytochrome c oxidase subunit 1 (cox1) were generated and compared with homologous sequences of other species of the genus. Branchellion spindolaorum n. sp. represents the fourth species of the genus known in the Eastern Pacific and the first record of a leech parasitising N. entemedor.

     

Occurrence of the Chilean devil ray Mobula tarapacana (Elasmobranchii: Batoidea: Myliobatiformes) in the Sea of Okhotsk: first record from cold temperate waters

The northernmost record for Chilean devil ray Mobula tarapacana, a circumglobal species that occurs in tropical, subtropical and limited warm temperate waters, is described. An adult female was caught incidentally in the Sea of Okhotsk on 17 September 2011. This specimen is the first confirmed occurrence of devil rays Mobula spp. in cold temperate waters.     

New genera,species and records of rhinebothriidean cestodes (Platyhelminthes) parasitic in Australian stingrays (Elasmobranchii: Batoidea)

Collections of rhinebothriidean cestodes (Platyhelminthes) from Australian batoid elasmobranchs revealed the presence of a number of new genera and species. Ruptobothrium louiseuzeti n. g., n sp. is described from the reticulate whipray, Himantura australis Last, Naylor & Manjaji-Matsumoto, from off the Northern Territory and Mixobothrium queenslandense n. g., n sp. is described from the green sawfish, Pristis zijsron Bleeker, from off north-eastern Queensland. Two new species of Rhabdotobothrium Euzet, 1953 are described: Rhabdotobothrium meridionale n. sp. from the southern eagle ray Myliobatis tenuicaudatus Hector from off South Australia and Rhabdotobothrium anoxypristidis n. sp. from the narrow sawfish, Anoxypristis cuspidatus (Latham) from off north Western Australia. A new species of Scalithrium Healy & Reyda, 2016, Scalithrium australiense n. sp., is described from the reticulate whipray, Himantura australis Last, Naylor & Manjaji-Matsumoto, from off northern Western Australia. Scalithrium smitii (Shinde, Deshmukh & Jadhav, 1981) n. comb. is reported from Australian waters for the first time in the black spotted stingray Maculabatis toshi (Whitley) from off northern Western Australia. New host and geographical records are provided for Stillabothrium jeanfortiae Forti, Aprill & Reyda, 2016 from the brown whipray Maculobatis toshi (Whitley) and the black-spotted whipray, Maculabatis cf. astra (Last, Manjaji-Matsumoto & Pogonoski) from Moreton Bay in southern Queensland.

     

Systematic implications of brain morphology in potamotrygonidae (Chondrichthyes: Myliobatiformes)

The gross brain morphology, brain proportions, and position of cranial nerves in all four genera (Potamotrygon, Plesiotrygon, Paratrygon, and Heliotrygon) and 11 of the species of the Neotropical stingray family Potamotrygonidae were studied to provide new characters that may have a bearing on internal potamotrygonid systematics. The brain was also studied in four other stingray (Myliobatiformes) genera (Hexatrygon, Taeniura, Dasyatis, and Gymnura) to provide a more inclusive phylogenetic context for the interpretation of features of the brain in potamotrygonids. Our results indicate, based on neuroanatomical characters, that the genera Paratrygon and Heliotrygon are sister groups, as are the genera Potamotrygon and Plesiotrygon, agreeing with previous morphological and molecular phylogenetic studies. Both groups of genera share distinct conditions of the olfactory tracts, telencephalon and its central nuclei, hypophysis and infundibulum, morphology and orientation of the metencephalic corpus cerebelli, orientation of the glossopharyngeal nerve, and overall encephalic proportions. The corpus cerebelli of Paratrygon and Heliotrygon is interpreted as being more similar to the general batoid condition and, given their phylogenetic position highly nested within stingrays, is considered secondarily derived, not plesiomorphically retained. Our observations of the corpus cerebelli of stingrays, including Hexatrygon, corroborate that the general stingray pattern previously advanced by Northcutt is derived among batoids. The morphology of the brain is shown to be a useful source of phylogenetically informative characters at lower hierarchical levels, such as between genera and species, and thus, has significant potential in phylogenetic studies of elasmobranchs. J. Morphol. 277:252–263, 2016. © 2015 Wiley Periodicals, Inc.     

Taxonomic assessment of sharks,rays and guitarfishes (Chondrichthyes: Elasmobranchii) from south‐eastern Arabia,using the NADH dehydrogenase subunit 2 (NADH2) gene

An 829‐bp fragment of the NADH dehydrogenase subunit 2 (NADH2) gene was used to assess the taxonomic status of 1487 elasmobranch specimens, representing 52 putative species. Strong evidence was found for the existence of an undescribed Echinorhinus species and for cryptic speciation within Rhynchobatus djiddensis. The results also provide strong molecular support for the existence of two previously reported, but undescribed, guitarfish species. Potential, but less conclusive, cryptic lineage diversification was also noted in Carcharhinus leucas, Loxodon macrorhinus, Iago omanensis and Gymnura poecilura. A complex situation was found in the genus Himantura, with potentially three distinct lineages evident, one of which is probably an undescribed species, in the H. gerrardi complex. One dasyatid specimen could not be identified, but appears to be closely related to Dasyatis ushiei, while Himantura leoparda and Carcharhinus longimanus are reported from Oman for the first time. The results of the present study also reinforce previously reported geographical divisions within certain putative species, which has important implications for fishery management and conservation. © 2015 The Linnean Society of London     

Dentition of the apron ray Discopyge tschudii (Elasmobranchii: Narcinidae)

The present study provides quantitative and qualitative analyses of the dentition of Discopyge tschudii. Overall, 193 individuals (99 males and 94 females) of D. tschudii were collected on scientific trawl surveys conducted by the National Institute for Fisheries Research and Development (INIDEP) and commercial vessels in Argentina. Discopyge tschudii has rhombic‐shaped teeth, arranged in a semipavement‐like dentition; each tooth has an erect cusp slightly inclined posteriorly and holaulachorized root. Mature males have greater tooth lengths than females and immature specimens. Discopyge tschudii exhibits dignathic homodonty and gradient monognathic heterodonty where teeth of the commissural row are shorter than those of the symphyseal and internal rows.     

Evidence of brain-warming in the mobulid rays, Mobula tarapacana and Manta birostris (Chondrichthyes: Elasmobranchii: Batoidea: Myliobatiformes)

The presence of cranial retia mirabilia in rays of the genus Mobula is well established. Although previously regarded as consisting exclusively of arteries, the presence of veins has now been established in gross dissections of the rete in the mobulid, Manta birostris. Histological examination of the retia in Manta birostris and Mobula tarapacana confirms the presence of veins. These findings suggest the presence of a counter-current heat-exchanger that warms the brain.