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Morphology of the Mechanosensory Lateral Line System in the Atlantic Stingray, Dasyatis Sabina: the Mechanotactile Hypothesis

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Morphology of the Mechanosensory Lateral Line System in the Atlantic Stingray, Dasyatis Sabina: the Mechanotactile Hypothesis JOURNAL OF MORPHOLOGY 238:1–22 (1998) Morphology of the Mechanosensory Lateral Line System in the Atlantic Stingray, Dasyatis sabina: The Mechanotactile Hypothesis KAREN P. MARUSKA* AND TIMOTHY C. TRICAS Department of Biological Sciences, Florida Institute of Technology, Melbourne, Florida ABSTRACT 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 infraor- bital, 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 swim- ming. 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 mechano- receptors that facilitate the detection and capture of small benthic inverte- brate prey. J. Morphol. 238:1–22, 1998. ௠ 1998 Wiley-Liss, Inc. KEY WORDS: elasmobranch; lateral line; mechanosensory; neuromast; mechanotactile The mechanosensory lateral line occurs in sent to processing centers in the brain. For all fishes and aquatic amphibians (Dijkgraff, example, the spatial distribution of neuro- ’63; Lannoo, ’87; Webb, ’89; Northcutt, ’92) masts defines the receptive field on the body and detects near field water movements rela- (Denton and Gray, ’83), innervation patterns tive to the skin surface (Harris and Van influence system sensitivity, and provide in- Bergeijk, ’62; Kalmijn, ’89; Coombs, ’94; formation on peripheral processing mecha- Coombs et al., ’96). The functional unit of the nisms (Munz, ’89), and neuromast morphol- lateral line system is the neuromast, com- ogy determines which component of water posed of mechanosensory hair cells and sup- motion (e.g., acceleration or velocity) is en- port cells covered by a gelatinous cupula. coded (Kalmijn, ’89; Kroese and Schellart, Displacement of this cupula by viscous drag modulates the hair cell receptor potential and associated primary afferent neural dis- charges (Hoagland, ’33). Morphological fea- *Correspondence to: Karen P. Maruska, Dept. of Biological Sciences, Florida Institute of Technology, 150 W. University tures of the peripheral lateral line system Blvd., Melbourne, FL 32901–6988. E-mail:maruska@fit.edu or determine the characteristics of information E-mail: tricas@fit.edu ௠ 1998 WILEY-LISS, INC. 2 K.P. MARUSKA AND T.C. TRICAS ’92). Assessment of characteristics such as The Atlantic stingray, Dasyatis sabina,is neuromast morphology, distribution, and the most abundant and widely distributed patterns of innervation are essential to batoid elasmobranch in estuarine waters of evaluate the functional organization of the the southeastern United States. It feeds al- lateral line system. most exclusively on small benthic infaunal With the exception of the review by Boord invertebrates (e.g., amphipods, mysids, iso- and Campbell (’77) on shark lateral line pods, ophiuroids, polychaetes, and bivalves) systems, studies on the organization of the that it excavates from the sand substrate lateral line periphery in elasmobranchs are (Turner et al., ’82; Cook, ’94) and feeds al- generally incomplete and make little refer- most continuously throughout the day and ence to function. Three types of neuromasts night (Bradley, ’96). We used this species to occur in most elasmobranchs. Superficial examine the gross anatomy, morphology, spa- tial organization, and innervation patterns neuromasts (SN), or pit organs, are located of lateral line mechanoreceptors to interpret on the skin surface with the cupula directly the function of these different receptor types exposed to the water. Canal neuromasts (CN) with special emphasis on their role in preda- are situated in dermal or subdermal canals tion. As a result of this analysis, we propose that are in contact with the water via pores the Mechanotactile Hypothesis to explain at on the skin. Vesicles of Savi (VS) are isolated least one function for the unique, nonpored mechanoreceptors situated in subdermal lateral line canals found in elasmobranch pouches primarily on the ventral surface of fishes. some torpediniform and dasyatid batoids. Lateral line canals are generally described MATERIALS AND METHODS separately (Garman, 1888; Tester and Ken- dall, ’69; Chu and Wen, ’79; Puzdrowski and General morphology, distribution, and in- nervation patterns of the mechanosensory Leonard, ’93) from superficial neuromasts lateral line system were examined in the (pit organs) in elasmobranchs (Tester and Atlantic stingray, Dasyatis sabina. Canal Nelson, ’69) and are considered together only topography and neuromast distribution, in- in the skate, Raja batis (Ewart and Mitchell, nervation and axon characteristics, and dis- 1892). Thus complete descriptions of the tribution of cutaneous nerve endings were anatomy of the peripheral mechanosensory examined by gross dissection and standard system within a single elasmobranch spe- histological techniques. Observations on cies are extremely limited. stingray feeding behavior were conducted in The lateral line system in teleosts func- the field and used in conjunction with mor- tions in the detection of water flow across phological data to formulate hypotheses on the skin, and facilitates schooling behavior the possible function of lateral line mechano- (Partridge and Pitcher, ’80), localization of receptors in the detection and capture of stationary objects (Campenhausen et al., ’81; benthic invertebrate prey. Hassan, ’89), social communication (Satou et al., ’91, ’94), and prey detection (Hoekstra Canal topography and neuromast and Janssen, ’85, ’86; Montgomery and Saun- distribution ders, ’85; Montgomery et al., ’88; Montgom- Mature adult Atlantic stingrays, Dasyatis ery, ’89; Montgomery and Milton, ’93; Jans- sabina, of both sexes were collected with a 1’’ sen et al., ’95). However, use of lateral line- mesh seine net from the Banana River (FL). mediated mechanoreception for these Rays were anesthetized (MS222) and pithed, functions in elasmobranch fishes is pres- fixed in 10% formalin, and stored in 50% ently uninvestigated. The organization of isopropyl alcohol. Superficial neuromasts the lateral line system in elasmobranchs were stained in six live rays by immersion in differs from that of all teleosts primarily in a 0.05% methylene blue-seawater solution the location of multiple neuromasts between for 4–6 h. Superficial neuromasts are lo- adjacent pores and the existence of exten- cated on raised areas of epidermis (termed sive nonpored canals on the head (Chu and papillae) that contain a central groove with Wen, ’79; Webb and Northcutt, ’97; Webb, a sensory epithelium that sits at the groove ’89). These morphological differences likely base. Immersion of the ray in methylene represent unique transduction mechanisms blue solution stains the edges of the papillae between teleost and elasmobranch lateral grooves light blue. Each superficial neuro- line systems that may be related to function. mast papilla was marked with colored latex STINGRAY MECHANOSENSORY LATERAL LINE 3 paint and counted under a dissecting micro- Innervation and axon characteristics scope. Orientation of the superficial neuro- Innervation patterns of neuromasts were mast papilla groove was recorded as the determined by dissection and application of angular deviation from the rostrocaudal body 99% isopropyl alcohol saturated Oil red O axis and midsagittal plane. stain to nerve fibers and surrounding tissue. Locations of the dorsal and ventral hyo- Connective and muscle tissue was then mandibular, supraorbital, infraorbital, pos- destained with 70% alcohol and rinsed with terior lateral line, and mandibular canals tap water. Nerves stained a darker red than were mapped after pressure injection of a the surrounding connective and muscle tis- 0.5% methylene blue solution into the ca- sues. Nerve fibers were traced distally to the nals. Vesicles of Savi and canal neuromasts canal or neuromast base by dissecting away were located by injection of 0.5% toluidine connective and muscle tissue. blue stain into the lateral branches of each Nerves that innervate individual canal canal and visualized under a dissecting mi- neuromasts, superficial neuromasts, or croscope. Classification of the canals as hyo- vesicles of Savi were removed at the mecha- noreceptor
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