Development of lateral line organs in leptocephali of the freshwater eel Anguilla japonica (Teleostei,Anguilliformes)

A study of the ontogeny of the lateral line system in leptocephali of the Japanese eel Anguilla japonica reveals the existence of three morphologically different types of lateral line organs. Type I is a novel sensory organ with hair cells bearing a single kinocilium, lacking stereocilia, distributed mainly on the head of larvae, and morphologically different from typical superficial neuromasts of the lateral line system. Its developmental sequence suggests that it may be a presumptive canal neuromast. Type II is an ordinary superficial neuromast, common in other teleost larvae, which includes presumptive canal neuromasts that first appear on the trunk and accessory superficial neuromasts that later appear on the head and trunk. Type III is a very unusual neuromast located just behind the orbit, close to the otic vesicle, with radially oriented hair cells, suggesting that these serve as multiple axes of sensitivity for mechanical stimuli. The behavior of larval eels suggests that the radially oriented neuromasts may act as the sole mechanosensory organ until the ordinary superficial neuromasts develop. The finding that larval eels possess a well-developed mechanosensory system suggests the possibility that they are also capable of perceiving weak environmental mechanical stimuli, like other teleost larvae.     

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.     

The lateral line system in larvalIchthyophis (Amphibia: Gymnophiona)

Summary The lateral line systems of larval caecilians of the genusIchthyophis possess two types of elements, free neuromasts and ampullary organs. Free mechanoreceptive neuromasts are typical of those found in other vertebrates, and are arranged in series roughly homologous to neuromast groups in many other fishes and amphibians. In contrast to other amphibians,Ichthyophis larvae possess only one paired, dorsal body series of neuromasts. Regional specialization of neuromasts is evident inIchthyophis. Premaxillary and anterior head neuromasts are the largest in size and total cell number. Overall, size and total cell numbers are correlated with depth of epidermis. Neuromasts on the anterior sides of the head occur in slight grooves and have apical tips situated farther below the level of the epidermis and with greater apical indentation. These features probably provide increased protection against abrasion. Apparently abnormal neuromasts are frequently found among the neuromast series. Such neuromasts contain fewer cells that lack normal apical extension, producing a sunken effect similar to that of the ampullary organ elements. The ampullary organs ofIchthyophis are morphologically similar to those found in various freshwater fishes and known to function as electroreceptors. These organs are not observed in the lateral line systems of members of other amphibian orders (Urodela and Anura), and we suggest that they function as electroreceptors. The sunken neuromasts of theIchthyophis lateral line system may parallel the possible evolutionary development of pit organs from normal neuromasts.     

中国大鲵侧线器官的研究

本文以光镜和扫描是镜手段研究了中国大鲵幼体，亚成体及成体头部及躯干部表皮中的侧线器官，即电接受壶腹器官，机械接受的表面神经丘和陷器官的分布，形态和发展变化。壶腹器管仅存于幼体头部，变态结束后消失，后两种终生存在，但前者按一定路线和方向排列，后者仅存于头部，陷在表皮中，文章探讨了壶腹器官的原始性，其消失与生活习性以及由水登陆进化的关系；对三种器官的形态及其它有尾类的侧线器官进行了比较。     

VISION AND SENSORY PHYSIOLOGY The lateral line systems of three deep-sea fish

The distribution and ultrastructure of the lateral line systems in three taxonomically dispersed deep-sea fish are described: Poromitra capito, Melanonus zugmayeri and Phrynichthys wedli. They are meso- to bathpelagic and are thought to feed on small crustaceans and fish. All possess highly developed lateral line systems, a feature associated with life in the deep sea. Poromitra capito and M. zugmayeri exhibit widened head canals which are connected to the outside by large pores and which contain around 60 large neuromasts. Each neuromast consists of a cupula, shield-shaped mantle and a sensory plate containing hundreds to thousands of hair cells. Direction of sensitivity is in the long axis of the canal (perpendicular to the long axis of the mantle). Depending on their position on the sensory plate, the hair cells have different morphologies. They fall into three basic classes which, from comparison with past work, may be tuned to different frequencies. Alternatively, the various hair cell morphologies could be interpreted as being members of a developmental or growth sequence. Phrynichthys wedli has no canal organs, these being replaced secondarily by many superficial neuromasts placed on prominent papillae in rows which cover much of the 'head' and body. Direction of sensitivity is along the axis of the neuromast row. An extreme proliferation of superficial neuromasts are also found on the heads of P. capito and M. zugmayeri and these are of a type not described before. They consist of stitches, raised on papillae in M. zugmayeri and several mm long in P. capito , in which continuous lines of hair cells, two to three cells wide, are embedded. Direction of sensitivity is perpendicular to the long axis of the stitch. Based on the structure and direction of sensitivity, possible functional implications of all the neuromast types described are compared and discussed.     

Organization of the superficial neuromast system in goldfish, Carassius auratus

Distribution, morphology, and orientation of superficial neuromasts and polarization of the hair cells within superficial neuromasts of the goldfish (Carassius auratus) were examined using fluorescence labeling and scanning electron microscopy. On each body side, goldfish have 1,800-2,000 superficial neuromasts distributed across the head, trunk and tail fin. Each superficial neuromast had about 14-32 hair cells that were arranged in the sensory epithelium with the axis of best sensitivity aligned perpendicular to the long axis of the neuromast. Hair cell polarization was rostro-caudal in most superficial neuromasts on trunk scales (with the exception of those on the lateral line scales), or on the tail fin. On lateral line scales, the most frequent hair cell polarization was dorso-ventral in 45% and rostro-caudal in 20% of the superficial neuromasts. On individual trunk scales, superficial neuromasts were organized in rows which in most scales showed similar orientations with angle deviations smaller than 45 degrees . In about 16% of all trunk scales, groups of superficial neuromasts in the dorsal and ventral half of the scale were oriented orthogonal to each other. On the head, most superficial neuromasts were arranged in rows or groups of similar orientation with angle deviations smaller than 45 degrees . Neighboring groups of superficial neuromasts could differ with respect to their orientation. The most frequent hair cell polarization was dorso-ventral in front of the eyes and on the ventral mandible and rostro-caudal below the eye and on the operculum.     

Evolution of electrosensory ampullary organs: conservation of Eya4 expression during lateral line development in jawed vertebrates

The lateral line system of fishes and amphibians comprises two ancient sensory systems: mechanoreception and electroreception. Electroreception is found in all major vertebrate groups (i.e. jawless fishes, cartilaginous fishes, and bony fishes); however, it was lost in several groups including anuran amphibians (frogs) and amniotes (reptiles, birds, and mammals), as well as in the lineage leading to the neopterygian clade of bony fishes (bowfins, gars, and teleosts). Electroreception is mediated by modified “hair cells,” which are collected in ampullary organs that flank lines of mechanosensory hair cell containing neuromasts. In the axolotl (a urodele amphibian), grafting and ablation studies have shown a lateral line placode origin for both mechanosensory neuromasts and electrosensory ampullary organs (and the neurons that innervate them). However, little is known at the molecular level about the development of the amphibian lateral line system in general and electrosensory ampullary organs in particular. Previously, we identified Eya4 as a marker for lateral line (and otic) placodes, neuromasts, and ampullary organs in a shark (a cartilaginous fish) and a paddlefish (a basal ray‐finned fish). Here, we show that Eya4 is similarly expressed during otic and lateral line placode development in the axolotl (a representative of the lobe‐finned fish clade). Furthermore, Eya4 expression is specifically restricted to hair cells in both neuromasts and ampullary organs, as identified by coexpression with the calcium‐buffering protein Parvalbumin3. As well as identifying new molecular markers for amphibian mechanosensory and electrosensory hair cells, these data demonstrate that Eya4 is a conserved marker for lateral line placodes and their derivatives in all jawed vertebrates.     

Metamorphosis-related changes in the lateral line system of lampreys, <Emphasis Type="Italic">Petromyzon marinus</Emphasis>

Lamprey metamorphosis leads to considerable changes in morphology and behavior. We have recently reported that larval lampreys possess a functional lateral line system. Here we investigated metamorphic morphological changes in the lateral line system using light and electron microscopy. Functional modifications were studied by recording the trunk lateral line nerve activity of larvae and adults while stimulating neuromasts with approximately sinusoidal water motion. We found a general re-patterning of neuromasts on the head and trunk including an increase in numbers, redistribution within the pit lines, and shifts of the pit lines relative to external features. The trunk lateral line nerve response was qualitatively similar in adults and larvae. Both showed two neuronal populations responding to opposite directions of water flow. Magnitude of the response increased monotonically with stimulus amplitude. At low frequencies, the response lag relative to the stimulus maximum was approximately 220°, and the gain depended approximately linearly on frequency, confirming that superficial neuromasts are velocity detectors. Changes in phase lag with increasing stimulus frequency were steeper in larvae, suggesting slower afferent conductance. The response gain with frequency was smaller for adults, suggesting a narrower frequency discrimination range and decreased sensitivity. These changes may be adaptations for the active lifestyle of adult lampreys.     

Morphogenesis of free neuromasts in the larvae of brown-marbled grouper Epinephelus fuscoguttatus

Newly hatched larvae had one pair of free neuromasts behind the eyes. As the larvae grew, free neuromasts increased in number. The apical surface of sensory epithelium widened and subsequently elongated. The number of sensory hair cells increased and the directions of maximum sensitivity became both anteroposterior and dorsoventral on the trunk. Before notochord flexion, only the anteroposterior type was observed. After notochord flexion, two types of neuromasts were observed on the trunk. On the head, the orientation of free neuromasts formed a tangential line to concentric circles around the eyes and nostrils. Free neuromasts on the head could therefore receive stimuli from various angles from predators or zooplanktons. This suggests that these free neuromasts play a role in compensating for a dead angle of vision, and an important role in detecting zooplankton under scotopic vision. Canal organs were observed on the head and operculum in 40-d-old animals.     

The behavioural role of pit organs in the epaulette shark

Epaulette sharks Hemiscyllium ocellatum in three treatments, pit organs (free neuromasts) ablated, sham-operated and normal ( n  = 8 for each treatment), showed a significant preference for facing upstream in a flume ( P  < 0·05). There were no significant differences in the mean angles or angular variances among treatments. Individuals with ablated pit organs, however, spent significantly less time moving around than controls ( P  < 0·05), suggesting that pit organs contributed to motivation for activity. Pit organs do not appear to make an important contribution to rheotaxis in H. ocellatum . It is suggested that this may be due to structural differences in the pit organs of H. ocellatum compared with other species.     

The lateral line receptor array of cyprinids from different habitats

The lateral line system of teleost fishes consists of an array of superficial and canal neuromasts (CN). Number and distribution of neuromasts and the morphology of the lateral line canals vary across species. We investigated the morphology of the lateral line system in four diurnal European cyprinids, the limnophilic bitterling (Rhodeus sericeus), the indifferent gudgeon (Gobio gobio), and ide (Leuciscus idus), and the rheophilic minnow (Phoxinus phoxinus). All fish had lateral line canals on head and trunk. The total number of both, CN and superficial neuromasts (SN), was comparable in minnow and ide but was greater than in gudgeon and bitterling. The ratio of SNs to CNs for the head was comparable in minnow and bitterling but was greater in gudgeon and ide. The SN‐to‐CN ratio for the trunk was greatest in bitterling. Polarization of hair cells in CNs was in the direction of the canal. Polarization of hair cells in SNs depended on body area. In cephalic SNs, hair cell polarization was dorso‐ventral or rostro‐caudal. In trunk SNs, it was rostro‐caudal on lateral line scales and dorso‐ventral on other trunk scales. On the caudal fin, hair cell polarization was rostro‐caudal. The data show that, in the four species studied here, number, distribution, and orientation of CNs and SNs cannot be unequivocally related to habitat. J. Morphol. 275:357–370, 2014. © 2013 Wiley Periodicals, Inc.     

The Sensory Canal Systems of the Living Coelacanth, Latimeria Chalumnae: A New Instalment

Entire sensory canal systems of the coelacanth, Latimeria chalumnae, are described: not only the course of principal canals with their primary and secondary collaterals, but also the course and branches of the pit-line and reticular canals. The number of pores on the left side of the head were found to be 296 in an early (yolksac) embryo, 321 in a late term fetus, 485 in a juvenile, and 2974 in adults. This means that in latimeria most of the lateral-line canal system develop after parturition. Pit lines of the living coelacanth are not rows of superficial neuromasts but canals covered by a thin epidermis like in other sensory canals of the lateral line. These pit-line canals, however, have a very specific structure and branching pattern: the medial dorsal pit-line canal is connected by fine branches on top of the head. The infra-dentary pit-line canal connects via these branches with canals deep inside the bones. Several fine and richly branched canaliculi of unknown function radiate from each quadratojugal pit-line canal. The gular plate pit-line canal has superficially branching arms as well as connections to numerous deeper canals inside the bone. These canals consist of fine branches that in turn lead to and open on the ventral surface of the gular plates as small pores. The system is reminiscent of the reticular (pore) canal system known only from some fossil agnathans and fishes. Thus latimeria combines the reticular system of ancient vertebrates with the lateral-line system of modern fishes. The significance of this gular (possibly electro-sensory) system for feeding by the coelacanth will be discussed.     

The lateral line system and its innervation in Champsodon snyderi (Champsodontidae): distribution of approximately 1000 neuromasts

The lateral line system and its innervation were studied in Champsodon snyderi (Champsodontidae). The lateral line system was composed of 43 canal and 935 superficial neuromasts, the former being arranged in 8 lines (7 on the head, 1 on the body). Tubular lateral line scales, clearly differing from the heart-shaped spinoid scales on the remaining parts of the head and body, were arranged dorsolaterally along the body, enclosing 19 canal neuromasts. Superficial neuromasts on the body were vertically aligned along 3 distinct body sections (comprising 19 dorsal, 26 lateral, and 20 ventrally positioned vertical lines), the lateral section being separated from the adjacent sections by single dorsolateral and ventrolateral horizontal lines of superficial neuromasts, respectively. All the canal neuromasts in the lateral line scales were included in the dorsal vertical lines. Accessory lateral rami, innervating most of the neuromasts on the body, were derived from the lateral ramus in a one-to-one relationship with the vertebrae.     

Neuromast formation in the prehatching embryos of the Japanese flounder (Paralichthys olivaceus)

The present paper clarifies the initial development of the lateral line organs in the embryonic Japanese flounder, Paralichthys olivaceus. The first appearances of lateral line primordia, and the proliferation, distribution and morphological development of the free neuromasts, including nerve ending formation: establishment of hair cell innervations via the formation of synapses, were examined by light microscopy, scanning and transmission electron microscopy. The first pair of neuromast primordia appeared in the otic region ≈ 30 h prior to hatching and subsequently differentiated into free neuromasts, otic neuromasts, after ≈ 8 h. At hatching, a pair of free neuromasts and three pairs of neuromast primordia were present on the head, and three pairs of neuromast primordia were present on the trunk. The hair cell polarity of the otic neuromast until just prior to hatching was radial, but not bi‐directional. The typical afferent and efferent nerve endings in the otic neuromasts had formed by the time of hatching, suggesting that the otic neuromasts are functional prior to hatching. The three neuromast primordia located on each side of the trunk were derived from a long, narrow ectodermal cell cluster and erupted through the epidermis after hatching.     

Sensory integration in the hydrodynamic world of rainbow trout

Water movements, of both abiotic and biotic origin, provide a wealth of information for fishes. They detect these water movements by arrays of hydrodynamic sensors located on the surface of the body as superficial neuromasts and embedded in subdermal lateral line canals. Recently, the anatomical dichotomy between superficial and canal neuromasts has been matched by demonstrations of a corresponding functional dichotomy. Superficial neuromasts are sensitive to water flows over the surface of the fish and are the sub-modality that participates in orientation to water currents, a behaviour known as rheotaxis. The canal neuromasts are sensitive to water vibration and it is this sub-modality that determines the localization of artificial prey. Recently, however, it has been shown that the complex behaviour of natural prey capture in the dark requires input from both lateral line sensory submodalities and here we show that the ability of trout to hold station behind a stationary object in fast flowing water also requires integration of information from both sub-modalities.     

Inter- and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays

The distribution of pit organs (free neuromasts) has previously been documented for several species of pelagic sharks, but is relatively poorly known for rays and bottom-dwelling (demersal) sharks. In the present study, the complete distribution of pit organs was mapped in the demersal sharks Heterodontus portusjacksoni, Orectolobus maculatus, Hemiscyllium ocellatum, Chiloscyllium punctatum, and Asymbolus analis, and the rays Rhinobatos typus, Aptychotrema rostrata, Trygonorrhina sp. A, Raja sp. A, and Myliobatis australis. All of these species had pit organs scattered over the dorsolateral surface. The sharks also had "mandibular" pit organs (and "umbilical" pit organs in C. punctatum and A. analis) on the ventral surface, while pit organs were sparse or absent on the ventral surface of rays. All of the species examined here, except for M. australis, also had a "spiracular" group of pit organs adjacent to the eye and/or spiracle. Spiracular pit organs were also recorded for the sawshark Pristiophorus sp. A and the skate Pavoraja nitida, although the remainder of pit organs were not mapped in these species. The distribution and number of pit organs varied both within and among species. Pit organ distribution was asymmetrical in each individual examined, but no particular trend towards left or right "handedness" was observed in any species. Although rays have been thought to have fewer pit organs than sharks in general, this was not the case in the present study. All of the species examined here had few pit organs compared to the pelagic sharks previously documented, but it is not clear whether this is due to ecological or phylogenetic causes.     

Electrosensory ampullary organs are derived from lateral line placodes in cartilaginous fishes

Ampullary organ electroreceptors excited by weak cathodal electric fields are used for hunting by both cartilaginous and non-teleost bony fishes. Despite similarities of neurophysiology and innervation, their embryonic origins remain controversial: bony fish ampullary organs are derived from lateral line placodes, whereas a neural crest origin has been proposed for cartilaginous fish electroreceptors. This calls into question the homology of electroreceptors and ampullary organs in the two lineages of jawed vertebrates. Here, we test the hypothesis that lateral line placodes form electroreceptors in cartilaginous fishes by undertaking the first long-term in vivo fate-mapping study in any cartilaginous fish. Using DiI tracing for up to 70 days in the little skate, Leucoraja erinacea, we show that lateral line placodes form both ampullary electroreceptors and mechanosensory neuromasts. These data confirm the homology of electroreceptors and ampullary organs in cartilaginous and non-teleost bony fishes, and indicate that jawed vertebrates primitively possessed a lateral line placode-derived system of electrosensory ampullary organs and mechanosensory neuromasts.     

Phylogenetic trends in the abundance and distribution of pit organs of elasmobranchs

Pit organs (free neuromasts of the mechanosensory lateral line system) are distributed over the skin of elasmobranchs. To investigate phylogenetic trends in the distribution and abundance of pit organs, 12 relevant morphological characters were added to an existing matrix of morphological data (plus two additional end terminals), which was then re-analysed using cladistic parsimony methods ( paup * 4.0b10). Character transformations were traced onto the most parsimonious phylogenetic trees. The results suggest the following interpretations. First, the distinctive overlapping denticles covering the pit organs in many sharks are a derived feature; plesiomorphic elasmobranchs have pit organs in open slits, with widely spaced accessory denticles. Second, the number of pit organs on the ventral surface of rays has been reduced during evolution, and third, spiracular pit organs have changed position or have been lost on several occasions in elasmobranch evolution. The concentrated-changes test in macclade (version 4.05) was used to investigate the association between a pelagic lifestyle and loss of spiracular pit organs (the only character transformation that occurred more than once within pelagic taxa). Depending on the choice of tree, the association was either nonsignificant at P  = 0.06 or significant at P  < 0.05. Future studies, using species within more restricted elasmobranch clades, are needed to resolve this issue.     

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.     

Development of the head skeleton and pectoral girdle in Esox.

A consideration of head development in two species of Esox, lucius and americanus (ssp. vermiculatus) representing the two subgenera Esox and Kenozoa respectively, focused on the significance of the variations of the latero-sensory canal system, its associated bones, and other skeletal elements. In living forms only aspects of "regression" or specialization can be studied. Canals tend to be reduced to pit lines first at their termini but can be broken in their course. Pit lines range from nearly canals to surface structures, or even fail to develop. The number of neuromasts varies. Canal bones develop from two centers: neuromast related and deeper membranous centers which may have no relationship to neuromasts. Tooth-bearing and non-canal-related dermal bones have only membranous (original) centers. The number of neuromasts associated with a bone usually does not affect its development or form. In the case of the circumorbital bones, the extrascapulars, and the nasal, a one to one relationship has developed by regression--towards the development of the latero-sensory component only. The idea that reductions in bone number are commonly traceable to fusion is rejected although examples of fusion are know. Most bones that disappear are simply lost (no blastema or other evidence of their presence seen in development). The relationship between dermal bone and chondral bone is examined and there is evidence of the former giving rise to the latter. The ontogenic order of appearances shows a feeding (functional) correlation.