Morphology of the mechanosensory lateral line system in the Atlantic Stingray,Dasyatissabina: The mechanotactile hypothesis

The biological function of anatomical specializations in the mechanosensory lateral line of elasmobranch fishes is essentially unknown. The gross and histological features of the lateral line in the Atlantic stingray, Dasyatis sabina, were examined with special reference to its role in the localization and capture of natural invertebrate prey. Superficial neuromasts are arranged in bilateral rows near the dorsal midline from the spiracle to the posterior body disk and in a lateral position along the entire length of the tail. All dorsal lateral line canals are pored, contain sensory neuromasts, and have accessory lateral tubules that most likely function to increase their receptive field. The pored ventral canal system consists of the lateral hyomandibular canal along the disk margin and the short, separate mandibular canal on the lower jaw. The extensive nonpored and relatively compliant ventral infraorbital, supraorbital, and medial hyomandibular canals form a continuous complex on the snout, around the mouth, and along the abdomen. Vesicles of Savi are small mechanosensory subdermal pouches that occur in bilateral rows only along the ventral midline of the rostrum. Superficial neuromasts are best positioned to detect water movements along the transverse body axis such as those produced by tidal currents, conspecifics, or predators. The pored dorsal canal system is positioned to detect water movements created by conspecifics, predators, or possibly distortions in the flow field during swimming. Based upon the stingray lateral line morphology and feeding behavior, we propose the Mechanotactile Hypothesis, which states that the ventral nonpored canals and vesicles of Savi function as specialized tactile mechanoreceptors that facilitate the detection and capture of small benthic invertebrate prey. J. Morphol. 238:1–22, 1998. © 1998 Wiley-Liss, Inc.     

Information-processing demands in electrosensory and mechanosensory lateral line systems.

The electrosensory and mechanosensory lateral line systems of fish exhibit many common features in their structural and functional organization, both at the sensory periphery as well as in central processing pathways. These two sensory systems also appear to play similar roles in many behavioral tasks such as prey capture, orientation with respect to external environmental cues, navigation in low-light conditions, and mediation of interactions with nearby animals. In this paper, we briefly review key morphological, physiological, and behavioral aspects of these two closely related sensory systems. We present arguments that the information processing demands associated with spatial processing are likely to be quite similar, due largely to the spatial organization of both systems and the predominantly dipolar nature of many electrosensory and mechanosensory stimulus fields. Demands associated with temporal processing may be quite different, however, due primarily to differences in the physical bases of electrosensory and mechanosensory stimuli (e.g. speed of transmission). With a better sense of the information processing requirements, we turn our attention to an analysis of the functional organization of the associated first-order sensory nuclei in the hindbrain, including the medial octavolateral nucleus (MON), dorsal octavolateral nucleus (DON), and electrosensory lateral line lobe (ELL). One common feature of these systems is a set of neural mechanisms for improving signal-to-noise ratios, including mechanisms for adaptive suppression of reafferent signals. This comparative analysis provides new insights into how the nervous system extracts biologically significant information from dipolar stimulus fields in order to solve a variety of behaviorally relevant problems faced by aquatic animals.     

Comparative morphology of the electrosensory system of the epaulette shark Hemiscyllium ocellatum and brown-banded bamboo shark Chiloscyllium punctatum

We compared the electrosensory system of two benthic elasmobranchs Hemiscyllium ocellatum and Chiloscyllium punctatum. The distribution of the ampullary pores on the head was similar for both species, with a higher density of pores anteriorly and a lower density posteriorly, although C. punctatum generally possessed larger pores. Ampullary canals of the mandibular cluster were quasi-sinusoidal in H. ocellatum, a shape previously found in benthic rays only, whereas ampullary canals in C. punctatum were of a linear morphology as reported for many shark and ray species previously. The ampullae proper were of the lobular type, as occurs in most galean sharks. Chiloscyllium punctatum had six sensory chambers compared with the five per ampulla in H. ocellatum, which were generally smaller than those of C. punctatum. The sensory epithelium comprised flattened receptor cells, compared with the usual pear-shaped receptor cells encountered in other elasmobranchs and their apically nucleated supportive cells did not protrude markedly into the ampullary lumen, unlike those in benthic rays.     

A comparison of the electrosensory morphology of a euryhaline and a marine stingray

The electrosensory system is found in all chondrichthyan fishes and is used for several biological functions, most notably prey detection. Variation in the physical parameters of a habitat type, i.e. water conductivity, may influence the morphology of the electrosensory system. Thus, the electrosensory systems of freshwater rays are considerably different from those of fully marine species; however, little research has so far examined the morphology and distribution of these systems in euryhaline elasmobranchs. The present study investigates and compares the morphology and distribution of electrosensory organs in two sympatric stingray species: the (euryhaline) estuary stingray, Dasyatis fluviorum, and the (marine) blue-spotted maskray, Neotrygon kuhlii. Both species possess a significantly higher number of ventral electrosensory pores than previously assessed elasmobranchs. This correlates with a diet consisting of benthic infaunal and epifaunal prey, where the electrosensory pore distribution patterns are likely to be a function of both ecology and phylogeny. The gross morphology of the electrosensory system in D. fluviorum is more similar to that of other marine elasmobranch species, rather than that of freshwater species. Both D. fluviorum and N. kuhlii possess ‘macro-ampullae’ with branching canals leading to several alveoli. The size of the pores and the length of the canals in D. fluviorum are smaller than in N. kuhlii, which is likely to be an adaptation to habitats with lower conductivity. This study indicates that the morphology of the electrosensory system in a euryhaline elasmobranch species seems very similar to that of their fully marine counterparts. However, some morphological differences are present between these two sympatric species, which are thought to be linked to their habitat type.     

Comparative morphology of shark pectoral fins

Sharks vary greatly in morphology, physiology, and ecology. Differences in whole body shape, swimming style, and physiological parameters have previously been linked to varied habitat uses. Pectoral fin morphology has been used to taxonomically classify species and hypotheses on the functional differences in shape are noted throughout the literature; however, there are limited comparative datasets that quantify external and skeletal morphology. Further, fins were previously categorized into two discrete groups based on the amount of skeletal support present: (a) aplesodic, where less than half of the fin is supported and (b) plesodic where greater than half of the fin is supported. These discrete classifications have been used to phylogenetically place species, though the methodology of classification is infrequently described. In this study, we sampled fins from 18 species, 6 families, and 3 orders, which were also grouped into five ecomorphotype classifications. We examined the external morphology, extent of skeletal support, and cross-sectional shape of individual cartilaginous elements. Using phylogenetic comparative methods, we show that fin shape does not differ significantly between ecomorphotypes, suggesting there may be some mechanical constraint. However, we find that the internal anatomy of the fin does vary significantly between ecomorphotypes, especially the extent and distribution of calcification of skeletal support, suggesting that the superficial similarity of fin shapes across ecomorphotypes may belie differences in function. Finally, we find that a number of morphological variables such as number of radials, radial calcification and shape, and fin taper all correlate with the extent of skeletal support. Within these morphospaces, we also describe that some orders/families tend to occupy certain areas with limited overlap. While we demonstrate that there is some mechanical constraint limiting external variations in shark pectoral fin morphology, there are compounding differences in skeletal anatomy that occur within ecomorphotypes which we propose may affect function.     

Comparative squamation of the lateral line canal pores in sharks

The current study collected the first quantitative data on lateral line pore squamation patterns in sharks and assessed whether divergent squamation patterns are similar to experimental models that cause reduction in boundary layer turbulence. In addition, the hypothesis that divergent orientation angles are exclusively found in fast‐swimming shark species was tested. The posterior lateral line and supraorbital lateral line pore squamation of the fast‐swimming pelagic shortfin mako shark Isurus oxyrinchus and the slow‐swimming epi‐benthic spiny dogfish shark Squalus acanthias was examined. Pore scale morphology and pore coverage were qualitatively analysed and compared. In addition, pore squamation orientation patterns were quantified for four regions along the posterior lateral line and compared for both species. Isurus oxyrinchus possessed consistent pore scale coverage among sampled regions and had a divergent squamation pattern with multiple scale rows directed dorsally and ventrally away from the anterior margin of the pore with an average divergent angle of 13° for the first row of scales. Squalus acanthias possessed variable amounts of scale coverage among the sampled regions and had a divergent squamation pattern with multiple scale rows directed ventrally away from the anterior margin of the pore with an average angle of 19° for the first row of scales. Overall, the squamation pattern measured in I. oxyrinchus fell within the parameters used in the fluid flow analysis, which suggests that this pattern may reduce boundary layer turbulence and affect lateral line sensitivity. The exclusively ventral oriented scale pattern seen in S. acanthias possessed a high degree of divergence but the pattern did not match that of the fluid flow models. Given current knowledge, it is unclear how this would affect boundary layer flow. By studying the relationship between squamation patterns and the lateral line, new insights are provided into sensory biology that warrant future investigation due to the implications for the ecology, morphology and sensory evolution of sharks.     

Captive husbandry and bioenergetics of the spiny butterfly ray,Gymnura altavela (Linnaeus)

Historically, gymnurid rays have not done well in a captive environment. This report describes success in maintaining two specimens of the spiny butterfly ray, Gymnura altavela, in captivity. An aggressive husbandry protocol of tube feeding and force feeding maintained energy levels until the rays began to feed on their own. The rays used their pectoral fins to strike at food items, a behavior they may use in the wild to stun and capture prey. The first estimates of growth in captivity for any species of butterfly ray are given. Growth rates for the male averaged 0.063 mm/day (s.d.=0.030) and 10.253 g/day (s.d.=9.689), whereas growth rates for the female butterfly ray averaged 0.303 mm/day (s.d.=0.215) and 22.777 g/day (s.d.=15.2). Estimates of gross conversion efficiency (Kl) were calculated using the caloric values and known food intake. The estimates of Kl averaged 5.4% (s.d.=3.857) and 16.1% (s.d.=7.511) for the male and female, respectively, with a combined average of 10.8% (s.d.=7.95). These are the first estimates of Kl reported for any species of batoid using direct methods (growth rate and food intake). © 1996 Wiley-Liss, Inc.     

Representation of lateral line and electrosensory systems in the midbrain of the axolotl,Ambystoma mexicanum

Summary The study focussed on the representation of the electrosensory and lateral line units in the midbrain of the axolotl Ambystoma mexicanum. In addition, the responses to photic and acoustic/vibrational stimuli were determined. Unit properties were characterized with respect to baseline activity, sensitivity, latency, directional specificity and number of input modalities. The anatomical arrangement of the units was determined using stereotactic and histological measurements of the electrode positions.Of 106 units recorded, 29 units were unimodal, 77 units responded to more than one modality. Most units discharged only in response to stimuli. Thresholds of electrosensory units were about 100 V/cm field strength; lateral line units had thresholds below 5 m pp amplitude. The shortest latencies (8–17 ms) were found for responses to visual stimuli. Lateral line and vestibular units responded after 35–58 ms, electroreceptive units after 79–150 ms. All electrosensory and about 50% of the lateral line units were sharply tuned to definite stimulus directions.Electrosensory and lateral line units formed topographical maps in the tectum. The map in each tectal hemisphere contained information about the contralateral surroundings. The electrosensory, lateral line and visual representations were only partly in register; especially in the caudal areas of the midbrain the alignment was poor.     

A new genus and species of fossil myliobatoid ray from the Fishburne Formation (lower Eocene/Ypresian) of Berkeley County,South Carolina,USA

Elasmobranch fossils recovered from the Fishburne Formation (lower Eocene/Ypresian) of Berkeley County, South Carolina, USA, include species from four genera of sharks and six genera of rays. Of particular interest was the recovery of multiple isolated teeth from a new genus and species of the cownosed ray family Rhinopteridae, which is the focus of this study. The unique crown morphology separates this genus and species from Rhinoptera. Eorhinoptera grabdai, gen. et sp. nov., is represented by small, bar-shaped teeth in the shape of greatly elongated hexagons. These teeth are the isolated elements of a dental plate. The holotype, with 12 wide root lobes, is the most elongated in the sample being 1 cm long and 1.5 mm wide, indicating an origin in the central region of the plate. Paratypes are less elongated, have 4–8 root lobes and are from more lateral rows. The crown is smooth and has a distinctly convex occlusal surface. Eorhinoptera is only the second genus of cow-nosed ray. Its distinctive crown morphology may have allowed it to exploit different kinds of prey than those favoured by rays that lacked convex tooth crowns.     

Post‐embryonic development of canal and superficial neuromasts and the generation of two cranial lateral line phenotypes

The relatively simple structural organization of the cranial lateral line system of bony fishes provides a valuable context in which to explore the ways in which variation in post‐embryonic development results in functionally distinct phenotypes, thus providing a link between development, evolution, and behavior. Vital fluorescent staining, histology, and scanning electron microscopy were used to describe the distribution, morphology, and ontogeny of the canal and superficial neuromasts on the head of two Lake Malawi cichlids with contrasting lateral line canal phenotypes (Tramitichromis sp. [narrow‐simple, well‐ossified canals with small pores] and Aulonocara stuartgranti [widened, more weakly ossified canals with large pores]). This work showed that: 1) the patterning (number, distribution) of canal neuromasts, and the process of canal morphogenesis typical of bony fishes was the same in the two species, 2) two sub‐populations of neuromasts (presumptive canal neuromasts and superficial neuromasts) are already distinguishable in small larvae and demonstrate distinctive ontogenetic trajectories in both species, 3) canal neuromasts differ with respect to ontogenetic trends in size and proportions between canals and between species, 4) the size, shape, configuration, physiological orientation, and overall rate of proliferation varies among the nine series of superficial neuromasts, which are found in both species, and 5) in Aulonocara, in particular, a consistent number of canal neuromasts accompanied by variability in the formation of canal pores during canal morphogenesis demonstrates independence of early and late phases of lateral line development. This work provides a new perspective on the contributions of post‐embryonic phases of lateral line development and to the generation of distinct phenotypes in the lateral line system of bony fishes. J. Morphol. 277:1273–1291, 2016. © 2016 Wiley Periodicals, Inc.     

Brain morphology in large pelagic fishes: a comparison between sharks and teleosts

A quantitative comparison was made of both relative brain size (encephalization) and the relative development of five brain area of pelagic sharks and teleosts. Two integration areas (the telencephalon and the corpus cerebellum) and three sensory brain areas (the olfactory bulbs, optic tectum and octavolateralis area, which receive primary projections from the olfactory epithelium, eye and octavolateralis senses, respectively), in four species of pelagic shark and six species of pelagic teleost were investigated. The relative proportions of the three sensory brain areas were assessed as a proportion of the total 'sensory brain', while the two integration areas were assessed relative to the sensory brain. The allometric analysis of relative brain size revealed that pelagic sharks had larger brains than pelagic teleosts. The volume of the telencephalon was significantly larger in the sharks, while the corpus cerebellum was also larger and more heavily foliated in these animals. There were also significant differences in the relative development of the sensory brain areas between the two groups, with the sharks having larger olfactory bulbs and octavolateralis areas, whilst the teleosts had larger optic tecta. Cluster analysis performed on the sensory brain areas data confirmed the differences in the composition of the sensory brain in sharks and teleosts and indicated that these two groups of pelagic fishes had evolved different sensory strategies to cope with the demands of life in the open ocean.     

The comparative morphology of pit organs in elasmobranchs

The pit organs of elasmobranchs (sharks, skates and rays) are free neuromasts of the mechanosensory lateral line system. Pit organs, however, appear to have some structural differences from the free neuromasts of bony fishes and amphibians. In this study, the morphology of pit organs was investigated by scanning electron microscopy in six shark and three ray species. In each species, pit organs contained typical lateral line hair cells with apical stereovilli of different lengths arranged in an “organ‐pipe” configuration. Supporting cells also bore numerous apical microvilli taller than those observed in other vertebrate lateral line organs. Pit organs were either covered by overlapping denticles, located in open grooves bordered by denticles, or in grooves without associated denticles. The possible functional implications of these morphological features, including modification of water flow and sensory filtering properties, are discussed. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Anatomy of the mechanosensory lateral line canal system and electrosensory ampullae of Lorenzini in two species of sawshark (fam. Pristiophoridae)

It has long been assumed that the elongated rostra (the saws) of sawsharks (family: Pristiophoridae) and sawfish (family: Pristidae) serve a similar function. Recent behavioural and anatomical studies have shed light on the dual function of the pristid rostrum in mechanosensory and electrosensory prey detection and prey manipulation. Here, the authors examine the distributions of the mechanosensory lateral line canals and electrosensory ampullae of Lorenzini in the southern sawshark, Pristiophorus nudipinnis and the longnose sawshark, Pristiophorus cirratus. In both species, the receptive fields of the mechano- and electrosensory systems extend the full length of the rostrum indicating that the sawshark rostrum serves a sensory function. Interestingly, despite recent findings suggesting they feed at different trophic levels, minimal interspecific variation between the two species was recorded. Nonetheless, compared to pristids, the pristiophorid rostrum possesses a reduced mechanosensory sampling field but higher electrosensory resolution, which suggests that pristiophorids may not use their rostrums to disable large prey like pristids do.     

Head Morphology and Electrosensory Pore Distribution of Carcharhinid and Sphyrnid Sharks

Selection to maximize electroreceptive search area might have driven evolution of the cephalofoil head morphology of hammerhead sharks (family Sphyrnidae). The enhanced electrosensory hypothesis predicts that the wider head of sphyrnid sharks necessitates a greater number of electrosensory pores to maintain a comparable pore density. Although gross head morphology clearly differs between sphyrnid sharks and their closest relatives the carcharhinids, a quantitative examination is lacking. Head morphology and the distribution of electrosensory pores were compared between a carcharhinid, Carcharhinus plumbeus, and two sphyrnid sharks, Sphyrna lewini and S. tiburo. Both sphyrnids had greater head widths than the carcharhinid, although head surface area and volume did not differ between the three species. The raked head morphology of neonatal S. lewini pups, presumably an adaptation to facilitate parturition, becomes orthogonal to the body axis immediately post-parturition whereas this change is much less dramatic for the other two species. The general pattern of electrosensory pore distribution on the head is conserved across species despite the differences in gross head morphology. Sphyrna lewini has a mean of 3067 ± 158.9 SD pores, S. tiburo has a mean of 2028 ± 96.6 SD pores and C. plumbeus has a mean of 2317 ± 126.3 SD pores and the number of pores remains constant with age. Sphyrnids have a greater number of pores on the ventral surface of the head whereas C. plumbeus has an even distribution on dorsal and ventral surfaces. The greater number of pores distributed on a similar surface area provides S. lewini pups with a higher density of electrosensory pores per unit area compared to C. plumbeus pups. The greater number of ampullae, the higher pore density and the larger sampling area of the head combine to provide hammerhead sharks with a morphologically enhanced electroreceptive capability compared to comparably sized carcharhinids.     

Neuromast morphology and lateral line trunk canal ontogeny in two species of cichlids: an SEM study

A study of neuromast ontogeny and lateral line canal formation in Oreochromis aureus and Cichlasoma nigrofasciatum reveals the existence of two classes of neuromasts: those that arise just before hatching (presumptive canal neuromasts, dorsal superficial neuromasts, gap neuromasts, and caudal fin neuromasts) and pairs of neuromasts that arise on each lateral line scale lateral to each canal segment at the same time as canal formation. In the anterior trunk canal segment, each presumptive canal neuromast is accompanied by a dorsoventrally oriented superficial neuromast forming an orthogonal neuromast pair. It is suggested that each of these dorsoventrally oriented superficial neuromasts is homologous to the transverse superficial neuromast row described by Münz (Zoomorphology 93:73-86, '79) in other cichlids. It is further suggested that the longitudinal lines described by Münz (Zoomorphology 93:73-86, '79) are derived from the pair of superficial neuromasts that arise during canal formation. Distinct changes in neuromast topography are documented. Neuromast formation, scale formation, and lateral line canal formation are three distinct and sequential processes. The distribution of neuromasts is correlated with myomere configuration; there is always one presumptive canal neuromast on each myomere. A single scale forms beneath each presumptive canal neuromast. Canal segment formation is initiated with the enclosure of each presumptive canal neuromast by an epithelial bridge which later ossifies. The distinction of these three processes raises questions as to the causal relationships among them.     

Movement patterns of the round stingray Urobatis halleri(Cooper) near a thermal outfall

Fine‐scale movements and site fidelity of round stingrays Urobatis halleri at Seal Beach California, U.S.A., were examined using acoustic telemetry. Actively tracked fish generally exhibited limited nearshore movement, with greater distances travelled at night when the tide was ebbing than during the day with ebbing tides. Increases in round stingray activity were associated with increases in ambient temperature. Passively tracked fish showed seasonal patterns in their presence at Seal Beach. Males left Seal Beach during the autumn, returned the following spring, and remained in the area until the following autumn. Females spent far less time at Seal Beach, remaining in the area for a few weeks during June and July. Passively tracked round stingrays were recorded more often in the warm waters of the San Gabriel River mouth (the location of a thermal outfall from an electric‐generating station) than adjacent beaches, with fish often returning to Seal Beach after periods of absence. Anthropogenic effects resulting from coastal development may have created environmental conditions ( i.e . warmer water and finer sediments) that influence the movements and site fidelity of round stingrays.     

Renal water and solute excretion in the Atlantic stingray in fresh water

Freshwater, male Atlantic stingrays Dasyatis sabina , from Lake Jesup, Florida, U·S·A·, excreted a dilute urine similar in composition to freshwater teleosts and lampreys with the exception that urea was the primary osmolyte. Urine flow rate was 2·5 to 10 fold higher than that reported for freshwater teleosts resulting in high free-water clearance. Mass-specific free-water clearance values from euryhaline elasmobranchs inhabiting freshwater environments greatly exceed those for freshwater teleosts and are nearly equivalent to those of freshwater lampreys.     

Linking local movement and molecular analysis to explore philopatry and population connectivity of the southern stingray Hypanus americanus

Limited data pertaining to life history and population connectivity of the data-deficient southern stingray (Hypanus americanus) are available. To determine potential vulnerabilities of their populations, this study aimed to analyse their movement patterns and genetic variability. A population of southern stingrays encompassing nine sites around Cape Eleuthera, the Bahamas, has been monitored using mark-recapture, spanning a 2.5 year period. Out of 200 individual stingrays, more than a third were encountered again. The home range of the females appears to be restricted, which supports the notion of high site residency. As resident populations of stingrays could suffer from a lack of population connectivity and be predestined for genetic isolation and local extirpation, this study further investigated the genetic connectivity of four sample sites in the central and western Bahamas. A haplotype analysis from the mitochondrial D-loop region showed that no distinct population structure strictly correlated with the sample site. These findings were complemented by five microsatellite loci that revealed high degrees in genotypic variability and little population differentiation. The results suggest gene flow mediated by both males and females.     

Swim bladder and posterior lateral line nerve of the nurseryfish, Kurtus gulliveri (Perciformes: Kurtidae)

The morphology of the swim bladder and inner ear of the nurseryfish, Kurtus gulliveri, appear adapted for enhanced pressure wave reception. The saccule is enlarged and surrounded by very thin bone and two large fontanelles that would present reduced resistance to pressure waves. The swim bladder is elaborate, with six dorsolaterally projecting pairs of lobes that are tightly encased in ribs and an additional caudally projecting pair of lobes encased in the first hemal spine. The ribs and musculature surrounding the swim bladder laterally are very thin, so that four or five "rib windows" are readily apparent on back-lit specimens. This swim bladder-rib configuration would also present reduced resistance to pressure waves to enhance function as a peripheral auditory structure. However, high-resolution X-ray computed tomography and dissection reveal no anterior projections of the swim bladder that could serve as a mechanical coupling to the inner ear. The posterior lateral line nerve is well developed and lies directly over the tips of the ribs encasing the swim bladder lobes. This nerve is not, however, associated with a lateral line canal and a lateral line canal is absent on most of the body. We hypothesize that the posterior lateral line nerve transmits mechanosensory information from the swim bladder.