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Notes on the Gross Functional Morphology of the Ampullary System in Two Similar Species of Skates, Raja erinacea and R. ocellata
Abstract
The organization of the ampullae of Lorenzini in Raja erinacea is similar to earlier accounts of this system in other rajids. Variations in the number of ampullae were recorded in 30 specimens and were independent of either sex or body size. Somatic pore patterns for R. erinacea and a sibling species, R. ocellata, are similar, however, the number of individual pores is significantly greater in R. ocellata. The geometric center of the ventral pore pattern is closely associated with the mouth in both species and thought to aid in feeding. Ventral pore densities indicate a greater acuity in the electroreceptive system in R. erinacea. The possibility of this array of pores being useful in the identification of these two skates was also considered. Differences in the subsections of the pore patterns were compared and found to be a valuable field character.
... For example, the number of alveoli per ampulla may be an indicator of the number of sensory receptor cells, as an increase in alveoli represents a subsequent increase in surface area of the sensory epithelium that lines each alveolar bulb. Through extensive work on over 40 species of skates, Raschi (1978Raschi ( , 1986 was able to correlate the morphology of ampullary organs with habitat depth, and the distribution of pores with feeding preferences and the light environment in this isolated group. While similar morphological studies and subsequent ecological correlations have been made for a few species of ray (Jordan 2008;Wueringer and Tibbetts 2008) and shark (Fishelson and Baranes 1998;Raschi et al. 2001;Tricas 2001;Collin and Whitehead 2004;Atkinson and Bottaro 2006), it is unknown how well these previous correlations might apply to the diverse range of predatory behaviours and habitats that elasmobranchs occupy. ...
... Group E, located at the anterior of the head covering the nose, had the highest number of pores, followed by adjacent Groups C and F. Similar increases in pore density around the nasal region are seen in other species of shark (Chu and Wen 1979;Fishelson and Baranes 1998;Kajiura 2001;Collin and Whitehead 2004;Atkinson and Bottaro 2006). A higher concentration of pores implies finer spatial resolution of an electrical signal (Raschi 1978;Raschi 1986). Prey detection is an important function of the electrosense in elasmobranchs, and higher acuity in the anterior region of the head could aid in guiding the terminal mouth of wobbegongs towards a particular prey item, especially when that prey is obscured by the rest of the head (Raschi 1986). ...
... The total number of ampullary pores varies greatly between elasmobranch species, ranging from as low as 191 in the pluto skate, Gurgesiella plutonia (=Fenestraja plutonia) (see Raschi 1986), to 3067 in the scalloped hammerhead, Sphyrna lewini (see Kajiura 2001). While some carcharhinid species possess over 2000 pores (Kajiura 2001;Raschi et al. 2001;Collin and Whitehead 2004), the majority of elasmobranchs species have between 500 and 1500 pores (Daniels 1967;Raschi 1978;Raschi 1986;Fishelson and Baranes 1998;Raschi et al. 2001;Wueringer and Tibbetts 2008). Wobbegong sharks, therefore, have relatively low numbers of ampullary pores compared with most other elasmobranch species. ...
Electroreception is an ancient sense found in many aquatic animals, including sharks, which may be used in the detection of prey, predators and mates. Wobbegong sharks (Orectolobidae) and angel sharks (Squatinidae) represent two distantly related families that have independently evolved a similar dorso-ventrally compressed body form to complement their benthic ambush feeding strategy. Consequently, these groups represent useful models in which to investigate the specific morphological and physiological adaptations that are driven by the adoption of a benthic lifestyle. In this study, we compared the distribution and abundance of electrosensory pores in the spotted wobbegong shark (Orectolobus maculatus) with the Australian angel shark (Squatina australis) to determine whether both species display a similar pattern of clustering of sub-dermal electroreceptors and to further understand the functional importance of electroreception in the feeding behaviour of these benthic sharks. Orectolobus maculatus has a more complex electrosensory system than S. australis, with a higher abundance of pores and an additional cluster of electroreceptors positioned in the snout (the superficial ophthalmic cluster). Interestingly, both species possess a cluster of pores (the hyoid cluster, positioned slightly posterior to the first gill slit) more commonly found in rays, but which may be present in all benthic elasmobranchs to assist in the detection of approaching predators.
... Carcharhiniform and lamnid sharks possess three clusters on each body side, which are bilaterally symmetric, while rajids skates possess four [Ewart and Mitchell, 1891; Norris, 1929; Aadland, 1992], and rhinobatids and pristids possess five [Norris, 1929; Wueringer and Tibbetts, 2008; Wueringer et al., 2011]. Interestingly, the largest cluster present in batoids, namely the hyoid cluster [Raschi, 1978; Wueringer and Tibbetts, 2008; Wueringer et al., 2011] , is missing in carcharhiniform and lamniform sharks [Raschi, 1984] . Moreover , ampullae of a particular area of innervation are found loosely aggregated in sharks and clustered together within the same connective tissue capsule in skates [Raschi, 1984]. ...
... Somatic pores visible on the skin of elasmobranchs may be divided into several pore fields that are useful for comparisons between different taxa. One pore field may contain ampullary pores from more than one cluster [Raschi, 1978; Wueringer et al., 2011]. Ampullae from one cluster can project to more than one pore field, like the hyoid cluster, which projects to four to six pore fields in rhinobatids and three pore fields in pristids [Wueringer and Tibbetts, 2008; Wueringer et al., 2011]. ...
... Most morphological studies of the electroreceptors of elasmobranchs examine shifts in total ampullary pore numbers (and thus ampullae) between the dorsal and b a ventral surfaces, which can then be related to physical parameters of different marine zones [Raschi, 1978; Kajiura, 2000; Kajiura et al., 2010; Kempster et al., 2012]. Total ampullary pore numbers were recently reviewed for all species of sharks and rays assessed to date [Kajiura et al., 2010; Kempster et al., 2012] and will not be further discussed here. ...
The ampullae of Lorenzini are the electroreceptors of elasmobranchs. Ampullary pores located in the elasmobranch skin are each connected to a gel-filled canal that ends in an ampullary bulb, in which the sensory epithelium is located. Each ampulla functions as an independent receptor that measures the potential difference between the ampullary pore opening and the body interior. In the elasmobranch head, the ampullary bulbs of different ampullae are aggregated in 3-6 bilaterally symmetric clusters, which can be surrounded by a connective tissue capsule. Each cluster is innervated by one branch of the anterior lateral line nerve (ALLN). Only the dorsal root of the ALLN carries electrosensory fibers, which terminate in the dorsal octavo-lateral nucleus (DON) of the medulla. Each ampullary cluster projects into a distinctive area in the central zone of the DON, where projection areas are somatotopically arranged. Sharks and rays can possess thousands of ampullae. Amongst other functions, the use of electroreception during prey localization is well documented. The distribution of ampullary pores in the skin of elasmobranchs is influenced by both the phylogeny and ecology of a species. Pores are grouped in distinct pore fields, which remain recognizable amongst related taxa. However, the density of pores within a pore field, which determines the electroreceptive resolution, is influenced by the ecology of a species. Here, I compare the pore counts per pore field between rhinobatids (shovelnose rays) and pristids (sawfish). In both groups, the number of ampullary pores on the ventral side of the rostrum is similar, even though the pristid rostrum can comprise about 20% of the total length. Ampullary pore numbers in pristids are increased on the upper side of the rostrum, which can be related to a feeding strategy that targets free-swimming prey in the water column. Shovelnose rays pin their prey onto the substrate with their disk, while repositioning their mouth for ingestion and thus possess large numbers of pores ventrally around the mouth and in the area between the gills.
... For example, the number of alveoli per ampulla may be an indicator of the number of sensory receptor cells, as an increase in alveoli represents a subsequent increase in surface area of the sensory epithelium that lines each alveolar bulb. Through extensive work on over 40 species of skates, Raschi (1978Raschi ( , 1986 was able to correlate the morphology of ampullary organs with habitat depth, and the distribution of pores with feeding preferences and the light environment in this isolated group. While similar morphological studies and subsequent ecological correlations have been made for a few species of ray (Jordan 2008;Wueringer and Tibbetts 2008) and shark (Fishelson and Baranes 1998;Raschi et al. 2001;Tricas 2001;Collin and Whitehead 2004;Atkinson and Bottaro 2006), it is unknown how well these previous correlations might apply to the diverse range of predatory behaviours and habitats that elasmobranchs occupy. ...
... Group E, located at the anterior of the head covering the nose, had the highest number of pores, followed by adjacent Groups C and F. Similar increases in pore density around the nasal region are seen in other species of shark (Chu and Wen 1979;Fishelson and Baranes 1998;Kajiura 2001;Collin and Whitehead 2004;Atkinson and Bottaro 2006). A higher concentration of pores implies finer spatial resolution of an electrical signal (Raschi 1978;Raschi 1986). Prey detection is an important function of the electrosense in elasmobranchs, and higher acuity in the anterior region of the head could aid in guiding the terminal mouth of wobbegongs towards a particular prey item, especially when that prey is obscured by the rest of the head (Raschi 1986). ...
... The total number of ampullary pores varies greatly between elasmobranch species, ranging from as low as 191 in the pluto skate, Gurgesiella plutonia (=Fenestraja plutonia) (see Raschi 1986), to 3067 in the scalloped hammerhead, Sphyrna lewini (see Kajiura 2001). While some carcharhinid species possess over 2000 pores (Kajiura 2001;Raschi et al. 2001;Collin and Whitehead 2004), the majority of elasmobranchs species have between 500 and 1500 pores (Daniels 1967;Raschi 1978;Raschi 1986;Fishelson and Baranes 1998;Raschi et al. 2001;Wueringer and Tibbetts 2008). Wobbegong sharks, therefore, have relatively low numbers of ampullary pores compared with most other elasmobranch species. ...
The electrosensory capabilities of wobbegong sharks are of particular interest, partly because very little is known about
their behavioural ecology and specifically because of their unusual ambush predatory strategy and benthic lifestyle. While
several biological functions of electroreception have been proposed, less consideration has been given to the functional significance
of interspecific differences in the morphology and topographic distribution of the ampullary organs. The morphology of the
ampullary organs was examined in four species of wobbegong shark, and the distribution of electroreceptive pores was mapped
in two species. The ampullary systems of wobbegongs are similar in morphology to other marine elasmobranchs. The number of
alveoli per ampullae is not significantly different between the four species; however, differences are seen between ampullary
cell size in some species. Ampullary pore distribution patterns are relatively unique, with the majority of pores occurring
on the dorsal region of the head. Wobbegongs feed primarily on demersal teleost fishes, and as the benthic and well-camouflaged
wobbegong remains motionless, these fish could be easily detected by the dorsal pores when swimming within range.
... Bonnethead sharks also feed almost exclusively on benthic crustaceans, such as the blue crab, Callinectes sapidus (Cortes et al. 1996), whereas juvenile sandbar sharks feed on benthic crustaceans as well as small fishes in the water column (Medved et al. 1985 ). Therefore, it would be advantageous for sandbar shark pups to be able to detect potential prey items around the entire head whereas sphyrnids have the highest concentration of electroreceptors on the ventral surface of the head for detection of benthic prey. Despite the existence of pore pattern illustrations for several elasmobranch species (Daniels 1967, Gilbert 1967, Raschi 1978, Chu & Wen 1979 ), no quantitative comparisons have been performed to determine if sphyrnids have a greater number or density of electrosensory pores compared to carcharhinids. The first prediction of the enhanced electrosensory hypothesis is that sphyrnids should have a greater number of pores compared to carcharhinids to maintain a comparable pore density over the greater head width. ...
... The second prediction of the enhanced electrosensory hypothesis is that the sphyrnids should have a comparable, if not greater, density of pores compared to the carcharhinids. A higher pore density implies finer spatial resolution that enables the shark to determine the location of an electrical stimulus near the body surface (Raschi 1978 ). Although the scalloped hammerhead pups appear to have a greater pore density than the sandbar sharks this is likely an artifact of the size difference of the sampled 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.
... Since each ampulla functions independently (Waltman 1966), the density of electroreceptor pores is hypothesized to correlate with spatial resolution (Murray 1974;Raschi 1986) and the separation of the pores, with sensitivity (Kalmijn 1988). Canal length and skin thickness increase through ontogeny (Kajiura 2001b;Wueringer and Tibbetts 2008;Crooks 2011;Wueringer et al. 2011;Winther-Janson et al. 2012;Gauthier et al. 2018), but the number of pores is fixed (Raschi 1974(Raschi , 1984Aadland 1992;Kajiura 2001b;Raschi et al. 2001;Atkinson and Bottaro 2006;Wueringer and Tibbetts 2008;Marzullo et al. 2011;Theiss et al. 2011;Wueringer et al. 2011;Kempster et al. 2012;Winther-Janson et al. 2012; Moore and McCarthy 2014). Growth has therefore been proposed to result in a tradeoff between increased sensitivity and decreased spatial resolution (Kajiura 2001b). ...
During elasmobranch ontogeny, increasing body size has been proposed to result in a tradeoff between increased sensitivity and decreased spatial resolution of the electrosensory system, but this hypothesis has not previously been tested. Further, the sensitivity of the electrosensory system has not been examined in any large sharks. In the present study, we examined the behavioral electrosensitivity of large (likely adult) sandbar sharks to prey-simulating electric fields, compared with previously published results for small (juvenile) sandbar sharks. We found that the large sandbar sharks, which were approximately three times larger than the small juveniles previously tested, had lower minimum (0.002 nV/cm) and median (0.5 nV/cm) response thresholds. These represent the lowest sensitivity thresholds of any elasmobranch studied to date. Since electric field detection plays an important role in feeding behavior, increases in sensitivity of the electrosensory system and the corresponding increase in electric field detection distance with growth may be linked to ontogenetic dietary changes.
... In both pristids and pristiophorids the DSOC and the PNC extend along the length of the elongated rostrum. The VSOC in pristiophorids, unlike in other sharks or sawfish, loops back and forth between dorsum and ventrum (Kajiura et al., 2010;Raschi, 1978), but connects over a short distance to the DSOC. Similar to the posterior lateral line canal in teleosts, which often curves away from the pectoral fin to minimise the detection of water movement caused by the pectoral fin (Kasumyan, 2003), the reduction of the pristiophorid VSOC could aid in reducing the perception of mechanosensory noise created by the movement of the barbels. ...
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.
... Tactile cues are thought to be perceived by the non-pored canals of the lateral line system, free nerve endings in the skin (Roberts 1978), and by the vesicles of Savi, found in dasyatid, torpedinid, and narcinid batoids such as the lesser electric ray Narcine bancroftii (d). Based on Cornett (2006), Dider (1995, Johnson (1917), Maruska (2001), Raschi (1978), Tester and Nelson (1967) tory environments have been estimated to be detectable at distances from the source that vary from the mm to cm range for the wake of an individual plankter to over a hundred meters for a herring (Dehnhardt et al. 2001;Yen et al. 1998). ...
Fishes, and elasmobranchs in particular, are often described as “opportunistic” predators meaning that they will take advantage of feeding opportunities as they arise. The implication of this term is that elasmobranchs are not selective about what they eat, which is a gross oversimplification of the complex interactions that shape diet, many of which are driven by interactions of an organism’s physiology, ecology, and behavior.
... The nerve is located laterally to the entrance of the canals in the cluster, same as observed by Wueringer (2012). This is the largest cluster present in batoids (Raschi 1978, Wueringer and Tibbetts 2008, Wueringer et al. 2011) being absent in Carcharhiniformes and Lamniformes sharks (Raschi 1986. Guitarfish and sawfishes features five bilaterally symmetric clusters (Norris 1929cited Wueringer 2012, Wueringer and Tibbetts 2008, Wueringer et al. 2011. ...
The electrosensory system on elasmobranchs consists of subcutaneous electroreceptor organs known as ampullae of Lorenzini. The present study investigated the ampullae of Lorenzini morphology of the lesser guitarfish Zapteryx brevirostris, using light microscopy and scanning electron microscopy. The pore number found in the ventral skin surface is much higher than that found in the dorsal portion, characteristic of species that inhabit the euphotic zone. Under light microscopy it was possible to observe that the wall canal consists of a single layer of squamous epithelial cells. The canal features distal expansion, where the ampullae are located with up to six alveoli. The sensory epithelium of ampullae is composed by cubic cells, with oval nucleus, restricted to the interior of the alveoli. With analysis the clusters under scanning electron microscopy, it was possible to observe the structure and the random arrangement of individual ampullae, canals and nerves. The distribution of dorsal and ventral pores and ampullae in Z. brevirostris resembled those of the same family. The number of alveoli per ampullae was similar to that found in euryhaline elasmobranchs species, suggesting that the morphological organization in Z. brevirostris is linked to its possible evolutionary transitory position among batoids.
... Setiap saluran ini mengandungi bahan mukopolisakarida yang bertindak sebagai konduktor penghantaran denyutan kepada ampula. Polimer-polimer dalam hidrogel dikenal pasti memberi isyarat kepada aor yang berada di persekitaran (Pollack 2001). Polimer-polimer ini memberi isyarat kepada air, kemudian menyekat migrasi ion-ion, mengurangkan kecekapan mobiliti kepada setengah daripada keadaan asal atau neutral. ...
A study was carried to observe the morphology of electrosensory fine structure organ (Ampullae of Lorenzini) of Shark Fishes Carcharhinus melanopterus, C. limbatus and Chiloscyllium griseum. This organ is very sensitive to several kinds of stimulus especially with regard to prey location, direction and mating. In the laboratory, a section where the sensory organ can be found was isolated from dermis layer of the sharks's head. A scanning electron microscope (SEM) was used to observe and produce images of the sensory organ. Images that were obtained from Carcharhinus melanopterus, C. limbatus and Chiloscyllium griseum were in the form of cluster. Sensory canals connecting the ampullae and the pores were found to be different in length and arrangement for different species.
... The concentration of ampullae in sharks and rays on the ventral surface surrounding the mouth suggests that they function primarily in foraging and feeding (Raschi, 1978). Aspects of orientation behavior of these animals have been attributed to the fan-shaped structure of the ampullary canals (Murray, 1962;Kalmijn, 1974;Broun et al., 1979). ...
The ability to detect and locate prey solely on the basis of emitted bioelectric fields was tested in the stingray Dasyatis sabina. Two species of invertebrates common in the natural habitat of D. sabina were encased in electrically transparent agar chambers and buried in sand in an experimental pool. The responses of this stingray were observed and recorded. Goodness of fit analysis of these data indicate that D. sabina is electroreceptive. However, there was no evidence to suggest that the stingray was able to discriminate between the two types of animals by the use of its electrosensory system alone.
... Both systems develop from dorsolateral placodes, embryonic neuroectoderm in the widest sense, and development sites are closely adjacent, but show wide differences in ontogenesis, morphology and function (e.g., Ewart, 1892;Ewart and Mitchell, 1892;Holmgren, 1942;Disler, 1961;Fishelson and Baranes, 1998a;Gibbs and Northcutt, 2004). The investigation of the ampullae of Lorenzini has a long history (e.g., Ewart, 1892, Ewart andMitchell, 1892;Allis, 1901;Metcalf, 1915;Allis, 1923;Dot-terweich, 1932;dijkgraaf and Kalmijn, 1963;Kalmijn, 1966;Murray, 1974;Raschi, 1978Raschi, , 1986Raschi et al., 2002;Collin and Whitehead, 2004), but only few studies attempt to systematically describe the complex arrangement of the tripartite ampullary system (ampullary sac, tubuli, pore fields) (Chu and Meng, 1979;Fishelson and Baranes, 1998b). Most of the literature is fragmentary, describing separate elements of the total electroreceptive system (raschi and Mackanos, 1987). ...
ABSTRACT. - The heads of three scyliorhinid sharks (Scyliorhinus canicula, Galeus melastomus, Apristurus aphyodes)
were investigated histologically in order to clarify the anatomy of the electroreceptive system (ampullae of Lorenzini). Complexes of ampullae of Lorenzini were digitally 3D-reconstructed according to section series and superficial pore patterns belonging to the complexes were mapped. Neurocranial structures were reconstructed with computertomography. These investigations revealed that not all pore fields on the surface of the head inG. melastomus and A. aphyodes (Pentanchinae) are part of the electroreceptive system as generally assumed: mediorostral pore fields dorsally and ventrally as well as preorbital and supralabial pore fields in both species are part of a subdermal system of shallow solitary grooves, surrounded by the same dense connective tissue as the canalicular mechanoreceptive lateral line. Histological sections show digitiform protuberances and maculae similar to neuromast organs of the epithelia in the groove system in G. melastomus.
Accordingly, histology rather indicates a mechanoreceptive function. The exact function or biological role and the phylogenetic significance of this elaborate system in two pentanchine catsharks are by no means clear yet. A similar groove system was found in A. fedorovi, A. herklotsi and G. murinus. In S. canicula (Scyliorhininae) no comparable grooves or pores are found.
... Both species possess hyoid, supraorbital and mandibular ampullary clusters, with the hyoid cluster accounting for the highest abundance of ampullae. This arrangement is typical of marine batoids (Raschi, 1978;Wueringer and Tibbetts, 2008;Wueringer et al., 2011), whereas a similar grouping is absent in freshwater dasyatids (Szabo et al., 1972;Szamier and Bennett, 1980;Raschi et al., 1997). The majority of electrosensory pores in both D. fluviorum and N. kuhlii are found (c-f) The general structure and morphology of the ampullary organs are similar between D. fluviorum (c, transversal; e, sagittal) and N. kuhlii (d, transversal; f, sagittal); however, some variation does exist. ...
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.
... The majority of electrosensory pores of T. lymma are found on the ventral side of the body (associated with the hyoid cluster) and are most densely concentrated around the mouth (mandibular cluster), with very few pores located on the dorsal side ( fig. 1 ). This arrangement is typical of batoids [Raschi, 1978;Wueringer and Tibbetts, 2008;Kempster et al., 2012], as their depressed body shape facilitates prey localisation beneath the head [Last and Stevens, 2009], and therefore a ventral concentration of pores would enhance detection of infaunal and epifaunal prey items. This suggests that, in addition to ecological constraints, electrosensory pore distribution may also be a function of body morphology. ...
Quantitative studies of sensory axons provide invaluable insights into the functional significance and relative importance of a particular sensory modality. Despite the important role electroreception plays in the behaviour of elasmobranchs, to date, there have been no studies that have assessed the number of electrosensory axons that project from the peripheral ampullae to the central nervous system (CNS). The complex arrangement and morphology of the peripheral electrosensory system has a significant influence on its function. However, it is not sufficient to base conclusions about function on the peripheral system alone. To fully appreciate the function of the electrosensory system, it is essential to also assess the neural network that connects the peripheral system to the CNS. Using stereological techniques, unbiased estimates of the total number of axons were obtained for both the electrosensory bundles exiting individual ampullary organs and those entering the CNS (via the dorsal root of the anterior lateral line nerve, ALLN) in males and females of different sizes. The dorsal root of the ALLN consists solely of myelinated electrosensory axons and shows both ontogenetic and sexual dimorphism. In particular, females exhibit a greater abundance of electrosensory axons, which may result in improved sensitivity of the electrosensory system and may facilitate mate identification for reproduction. Also presented are detailed morphological data on the peripheral electrosensory system to allow a complete interpretation of the functional significance of the sexual dimorphism found in the ALLN. © 2013 S. Karger AG, Basel.
... Consequently, the ventral surface of the cephalic lobes is not evenly distributed across the substrate. Thus when searching for prey items, the area of the lobes closest to the substrate has the highest density of electrosensory pores, increasing the spatial resolution (Raschi, 1978) and distance of the field of detection from the body. ...
Many benthic batoids utilize their pectoral fins for both undulatory locomotion and feeding. Certain derived, pelagic species of batoids possess cephalic lobes, which evolved from the anterior pectoral fins. These species utilize the pectoral fins for oscillatory locomotion while the cephalic lobes are used for feeding. The goal of this article was to compare the morphology of the cephalic lobes and anterior pectoral fins in species that possess and lack cephalic lobes. The skeletal elements (radials) of the cephalic lobes more closely resembled the radials in the pectoral fin of undulatory species. Second moment of area (I), calculated from cephalic lobe radial cross sections, and the number of joints revealed greater flexibility and resistance to bending in multiple directions as compared to pectoral fin radials of oscillatory species. The cephalic lobe musculature was more complex than the anterior pectoral fin musculature, with an additional muscle on the dorsal side, with fiber angles running obliquely to the radials. In Rhinoptera bonasus, a muscle presumably used to help elevate the cephalic lobes is described. Electrosensory pores were found on the cephalic lobes (except Mobula japonica) and anterior pectoral fins of undulatory swimmers, but absent from the anterior pectoral fins of oscillatory swimmers. Pore distributions were fairly uniform except in R. bonasus, which had higher pore numbers at the edges of the cephalic lobes. Overall, the cephalic lobes are unique in their anatomy but are more similar to the anterior pectoral fins of undulatory swimmers, having more flexibility and maneuverability compared to pectoral fins of oscillatory swimmers. The maneuverable cephalic lobes taking on the role of feeding may have allowed the switch to oscillatory locomotion and hence, a more pelagic lifestyle. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.
... To date, all elasmobranchs tested for their response towards electric dipoles displayed either a biting response or produced suction feeding movements [1,89101115,28,343536, but freshwater sawfish also produce lateral swipes of their rostrum towards dipoles suspended in the water column [27] . Benthic skates are highly electro- receptive37383940, but Raja erinacea failed to react to the vertical component of an electric field: when presented with a dipole above the pectoral fins, the animals instead attacked a location on the substrate under the pectorals fin directly below the centre of the suspended dipole, apparently unable to interpret a signal with a vertical component [7]. Thus sawfish, which are generally considered to be sluggish benthic dwellers [41], may actually be agile, demersal predators. ...
In the aquatic environment, living organisms emit weak dipole electric fields, which spread in the surrounding water. Elasmobranchs detect these dipole electric fields with their highly sensitive electroreceptors, the ampullae of Lorenzini. Freshwater sawfish, Pristis microdon, and two species of shovelnose rays, Glaucostegus typus and Aptychotrema rostrata were tested for their reactions towards weak artificial electric dipole fields. The comparison of sawfishes and shovelnose rays sheds light on the evolution and function of the elongated rostrum ('saw') of sawfish, as both groups evolved from a shovelnose ray-like ancestor. Electric stimuli were presented both on the substrate (to mimic benthic prey) and suspended in the water column (to mimic free-swimming prey). Analysis of around 480 behavioural sequences shows that all three species are highly sensitive towards weak electric dipole fields, and initiate behavioural responses at median field strengths between 5.15 and 79.6 nV cm(-1). The response behaviours used by sawfish and shovelnose rays depended on the location of the dipoles. The elongation of the sawfish's rostrum clearly expanded their electroreceptive search area into the water column and enables them to target free-swimming prey.
... Ampullary pores are concentrated both on the ventral and dorsal surfaces of the rostrum in all pristids. Additionally, although the hyoid capsule is the largest ampullary capsule in pristids, and it is also the largest one in other batoids, namely rhinobatids [Wueringer and Tibbetts, 2008] and rajids [Raschi, 1978], pristids possess significantly fewer pores located around the mouth than along the rostrum. As the number of ampullary pores equals the number of ampullae, which function as independent electroreceptors, an increased number of elec-9 troreceptors provide increased resolution. ...
The distribution and density of the ampullary electroreceptors in the skin of elasmobranchs are influenced by the phylogeny and ecology of a species. Sensory maps were created for 4 species of pristid sawfish. Their ampullary pores were separated into pore fields based on their innervation and cluster formation. Ventrally, ampullary pores are located in 6 areas (5 in Pristis microdon), covering the rostrum and head to the gills. Dorsally, pores are located in 4 areas (3 in P. microdon), which cover the rostrum, head and may extend slightly onto the pectoral fins. In all species, the highest number of pores is found on the dorsal and ventral sides of the rostrum. The high densities of pores along the rostrum combined with the low densities around the mouth could indicate that sawfish use their rostrum to stun their prey before ingesting it, but this hypothesis remains to be tested. The directions of ampullary canals on the ventral side of the rostrum are species specific. P. microdon possesses the highest number of ampullary pores, which indicates that amongst the study species this species is an electroreception specialist. As such, juvenile P. microdon inhabit low-visibility freshwater habitats.
... The hyoid cluster of Aptychotrema rostrata is the largest cluster in rajids (Raschi 1978Raschi , 1986) and also in rhinobatids (Wueringer and Tibbetts 2008). As Aptychotrema rostrata is found in the marine environment and their ampullae of Lorenzini are macroscopic in the range of centimeters, the ampullary organs are classiWed as macroampullae sensu Andres and von Düring (1988) (Wueringer and Tibbetts 2008) , compared to the microampullae of Holocephali species and the miniampullae of freshwater elasmobranchs, as described in Potamotrygon laticeps (Garman, 1913) and Potamotrygon motoro (Müller and Henle, 1841) (Andres and von Düring 1988). ...
Small epidermal pores of the electrosensory ampullae of Lorenzini located both ventrally and dorsally on the disk of Aptychotrema rostrata (Shaw and Nodder, 1794) open to jelly-filled canals, the distal end of which widens forming an ampulla that contains 6 ± 0.7 alveolar bulbs (n = 13). The sensory epithelium is restricted to the alveolar bulbs and consists of receptor cells and supportive cells. The receptor cells are ellipsoid and their apical surfaces are exposed to the alveolar lumen with each bearing a single central kinocilium. Presynaptic bodies occur in the basal region of the receptor cell immediately proximal to the synaptic terminals. The supportive cells that surround receptor cells vary in shape. Microvilli originate from their apical surface and extend into the alveolar lumen. Tight junctions and desmosomes connect the supportive cells with adjacent supportive and receptor cells in the apical region. The canal wall consists of two cell layers, of which the luminal cells are squamous and interconnect via desmosomes and tight junctions, whereas the cells of the deeper layer are heavily interdigitated, presumably mechanically strengthening the canal wall. Columnar epithelial cells form folds that separate adjacent alveoli. The same cells separate the ampulla and canal wall. An afferent sensory nerve composed of up to nine myelinated nerve axons is surrounded by several layers of collagen fibers and extends from the ampulla. Each single afferent neuron can make contacts with multiple receptor cells. The ultrastructural characteristics of the ampullae of Lorenzini in Aptychotrema rostrata are very similar to those of other elasmobranch species that use electroreception for foraging.
... Each ampulla is connected to a surface pore by a single canal. The total number of pores of an elasmobranch remains constant throughout development (Raschi 1978(Raschi , 1984Aadland 1992;Kajiura 2000), whereas body size increases. In the present study, no correlation was found between body size and the number of either dorsal or ventral ampullary pores, indicating that in rhinobatids the number of ampullae remains constant throughout much of their development. ...
The anatomical characteristics of the mechanoreceptive lateral line system and electrosensory ampullae of Lorenzini of Rhinobatos typus and Aptychotrema rostrata are compared. The spatial distribution of somatic pores of both sensory systems is quite similar, as lateral line canals are bordered by electrosensory pore fields. Lateral line canals form a sub-epidermal, bilaterally symmetrical net on the dorsal and ventral surfaces; canals contain a nearly continuous row of sensory neuromasts along their length and are either non-pored or pored. Pored canals are connected to the surface through a single terminal pore or additionally possess numerous tubules along their length. On the dorsal surface of R. typus, all canals of the lateral line occur in the same locations as those of A. rostrata. Tubules branching off the lateral line canals of R. typus are
ramified, which contrasts with the straight tubules of A. rostrata. The ventral prenasal lateral line canals of R. typus are pored and possess branched tubules in contrast to the non-pored straight canals in A. rostrata. Pores of the ampullae of Lorenzini are restricted to the cephalic region of the disk, extending only slightly onto the pectoral fins in both species. Ampullary canals penetrate subdermally and are detached from the dermis. Ampullae occur clustered together, and can be surrounded by capsules of connective tissue. We divided the somatic pores of the ampullae of Lorenzini of R. typus into 12 pore fields (10 in A. rostrata), corresponding to innervation and cluster formation. The total number of ampullary pores found on the ventral skin surface of R. typus is approximately six times higher (four times higher in A. rostrata) than dorsally. Pores are concentrated around the mouth, in the abdominal area between the gills and along the rostral cartilage. The ampullae of both species of shovelnose ray are multi-alveolate macroampullae, sensu Andres and von Düring (1988). Both the pore patterns and the distribution of the ampullary clusters in R. typus differ from A. rostrata, although a basic pore distribution pattern is conserved.
The present work aimed to analyze the distribution of the electrosensory pores of the Daggernose Shark Carcharhinus oxyrhynchus identifying the organ's importance in the natural history of the species. By examining photographs and digital microscope videos, we found that C. oxyrhynchus possesses the highest abundance of pores among Carcharhiniformes. This suggests a well‐developed electroreceptor system, which may have maximized its evolutionary success in high turbidity environments. Furthermore, as a morphologically derived species, C. oxyrhynchus comprises a more complex and specialized electrosensory system. Notably, the species exhibits ontogenetic variation in pore abundance, highlighting the importance of a high‐resolution system for adults. The higher density of pores in the ventral region indicates a preference for benthic prey, despite also feeding on pelagic items. Moreover, the species has a high‐resolution electrosensory system and a high density of pores in the snout, which emphasizes the importance of the elongated snout that expands the electroreception search area coverage. Evolutionary convergence was observed in the development of the electrosensory system, as C. oxyrhynchus shares characteristics of pore distribution and abundance with phylogenetically unrelated species.
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A comparison of the ampullae of Lorenzini among 40 species of skates (Rajoidei) demonstrates a close relationship between inferred electroreceptive capabilities and feeding mechanisms. Three general lines of morphological modifications are noted. (1) Whereas the majority of ampullary pores are located on the ventral surface of the dorsoventrally flattened body, the relative proportion of ventral pores is significantly lower on species inhabiting aphotic waters. (2) The ventral pores on more piscivorous species are distributed over a larger portion of body surface than they are on those species that feed primarily on invertebrates. Ventral pores in this latter group are more noticeably concentrated around the mouth and their densities on the adult are inversely related to the overall mobility of preferred prey species. (3) The size of each ampulla and the number of alveoli associated with it are directly related to the habitat depth occupied by each species. Shallow-water species have smaller ampullae with fewer alveoli than deeper-dwelling (> 1,000 m) species.
The general distribution of ampullary pores on deep dwelling rajoids appears to compensate for reduced visual input, whereas their relative densities are a measure of the system's resolution and reflect major differences in feeding strategies. The increased ampullary size and complexity observed in deep-sea rajoids provides mechanisms to increase both the sensitivity and signal-to-noise ratios.
The laterally expanded head is the principal character distinguishing hammerhead sharks, and its morphology is important for interpreting their ontogeny and species diversity. Because their head shape changes during its ontogeny, it is vital to evaluate it in order to establish other taxonomical characteristics to correctly identify Sphyrna species. This study examines the distribution of electrosensorial pore regions on the ventral surface of the cephalofoil (VSC) in Sphyrna lewini, S. tiburo, S. tudes and S. zygaena from the Southwestern Atlantic Ocean. The pore distribution patterns in the VSC can distinguish these species. Use of those patterns, with the head shape, confirms the identification of the four most common species of hammerhead sharks in the Southwestern Atlantic.
This chapter focuses on the comparative anatomy of vertebrate electroreceptors. Electrosensitivity plays an important role in the biological activities of fish and amphibia for prey detection, feeding behaviour and social communication and its significance is reflected in the number of sensory cells and the amount of nerve supply that ranks in the order of other sensory systems. Two types of electroreceptors are characteristic in teleost as well as non-teleost fishes and in some amphibia: the ampullary and the tuberous receptor organs. Three types of ampullae can be distinguished in chondrichthyes with regard to the length of the canal and the size and differentiation of the alveolus: (1) macro-ampullae, (2) micro-ampullae, and (3) mini-ampullae. The macro-ampullae (known as the ampullae of Lorenzini) are macroscopically identified by large pores in the skin surface. Micro-ampullae occur in restricted areas of the maxillary and the mandibular processes of Holocephali and Hexanchidae. The mini-ampullae of freshwater rays, however, exhibit very short canals of about 300–500 μm length.
The dorsal octavolateral nucleus is the primary electrosensory nucleus in the elasmobranch medulla. We have studied the topographic organization of electrosensory afferent projections within the dorsal nucleus of the little skate, Raja erinacea , by anatomical (HRP) and physiological experiments.
The electrosensory organs (ampullae of Lorenzini) in skates are located in four groups on each side of the body, and each group is innervated by a separate ramus of the anterior lateral line nerve (ALLN). Transganglionic transport of HRP in individual rami demonstrated that electroreceptor afferents in each ramus project to a separate, nonoverlapping division of the central zone of the ipsilateral dorsal nucleus. These divisions, which are distinct areas separated by compact cell plates, are somatopically arranged. The volume of each division of the dorsal nucleus that is related to a single ramus is proportional to the number of ampullae innervated by the ramus, but not to the body surface area on which the receptors are distributed. Nearly one‐half of the nucleus is devoted to electrosensory inputs from the buccal and superficial ophthalmic ampullae concentrated in a small area on the ventral surface of the head rostral to the mouth. Multiple and single unit recordings demonstrated that adjacent cells in the nucleus have similar receptive fields on the body surface and revealed a detailed point‐to‐point somatotopy within the nucleus. With threshold stimuli most single units have ipsilateral receptive fields made up by excitatory inputs from 2–5 ampullary organs.
The somatotopy within the mechanosensory medial nucleus, also revealed by the HRP fills of individual ALLN rami, appears less rigid than that in the dorsal nucleus, as extensive overlap is present in the terminal fields of separate ALLN rami.
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