The lateral line system and its innervation in Champsodon snyderi (Champsodontidae): distribution of approximately 1000 neuromasts Masanori Nakae*, Shinji Asai, and Kunio Sasaki Laboratory of Marine Biology, Faculty of Science, Kochi University, 2-5-1 Akebono-cho, Kochi 780-8520, Japan (e-mail: MN,
[email protected]; KS,
[email protected]) Received: May 12, 2005 / Revised: February 1, 2006 / Accepted: February 6, 2006
Ichthyological Research ©The Ichthyological Society of Japan 2006
Ichthyol Res (2006) 53: 209–215 DOI 10.1007/s10228-006-0335-5
Abstract 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 oneto-one relationship with the vertebrae. Key words Champsodontidae · Champsodon snyderi · Lateral line system · Nerves · Neuromasts
C
omprising a single genus Champsodon with 13 species, the Champsodontidae is widespread throughout the temperate to tropical Indo-Pacific (Nemeth, 1994). Although the morphology of the family has been well studied osteologically and myologically (Mooi and Johnson, 1997), little is known of its neuroanatomy, despite the recognition that the numerous superficial neuromasts on the head and body are unusual (Johnson, 1993). In this article, the lateral line system and its innervation are described and illustrated for the first time in Champsodon snyderi. The innervation patterns of the lateral line system provide essential information for determining the homology or nonhomology of aspects of the system among related taxa, including the presence of superficial neuromasts. However, such information is available only for a limited number of species (see Coombs et al., 1988, for review), making sound utilization of the lateral line system in phylogenetic studies difficult. Although Freihofer (1972) considered the innervation patterns of the trunk neuromasts in atheriniform, mugilid, and percoid fishes, he failed to distinguish between canal and superficial neuromasts, thereby limiting the comparative valve of his study. Accordingly, the present article provides a basis for comparisons with other taxa having superficial neuromasts, the Kurtoidei, Apogonidae, and Gobioidei being cited by Mooi and Johnson (1997) as candidates for comparison with the Champsodontidae. The lateral line system is also important functionally, its variability being related to both habitats and habits. Champsodontids are diurnal migrators, shuttling between
benthic and pelagic environments (Morohoshi and Sasaki, 2003), the lateral line system in C. snyderi being discussed by them from a functional point of view. Mooi and Johnson (1997) argued that champsodontids are members of the Scorpaenoidei (sensu Mooi and Gill, 1995) on the basis of their sharing in common an opening at the base of the parietal spine as a passage for the supratemporal lateral line. However, Imamura and Yabe (2002) questioned this view on the basis of the ontogenetic pattern of the canal formation. The validity of the character is also discussed neuroanatomically.
Materials and Methods Champsodon snyderi specimens examined in this study were all collected from Tosa Bay, southern Japan, and are deposited at the Laboratory of Marine Biology, Faculty of Science, Kochi University (BSKU). Bones were observed from specimens stained with alizarin red S, and nerves on cleared and stained specimens prepared by the Sihler technique (Fraser and Freihofer, 1971), with modifications of Nakae and Sasaki (2004), and the Sudan black B protocol (Filipski and Wilson, 1984). The illustrations and description given are based on about ten specimens, from which the neuromast distribution and innervation were determined, because we were unable to observe all neuromasts and lateral line nerves in a single specimen. Although some intraspecific variations were recognized in the number and position of superficial neuromasts, typically associated with
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Fig. 1. Neuromast distribution, lateral line system (A) and innervation (B) in Champsodon snyderi. Black dots and open circles indicate superficial and canal neuromasts, respectively; canal-bearing lateral line is shaded. Posterior half of caudal fin omitted. DHL, dorsal horizontal line; DVL, dorsal vertical line; IOL, infraorbital line; LVL, lateral vertical line; MDL, mandibular line; OTL, otic line; POL, postotic line; PRL, preopercular line; SOL, supraorbital line; STL, supratemporal line; TRL, trunk line; VHL, ventral horizontal line; VVL, ventral vertical line
variations in vertebral number, only “typical” conditions were illustrated and described. Terminology generally follows Webb (1989) for lateral line system and Northcutt et al. (2000) for neuroanatomy.
Results Lateral line system (Figs. 1A, 2). The lateral line system was composed of both canal and superficial neuromasts (CN and SN, respectively) (Fig. 1A). CN were included in the supraorbital line (SOL), infraorbital line (IOL; note that IOL was incomplete owing to the incomplete infraorbital series; see following), preopercular line (PRL), mandibular line (MDL), otic line (OTL), postotic line (POL), supratemporal line (STL), and trunk line (TRL; note that TRL was incomplete owing to wide separation of the lateral line scales; Fig. 2). A supratemporal commissure connecting the left and right STL was absent. SN developed on the skin free from scales and on the caudal fin, vertical and horizontal lines of SN forming a ladder-like network on the body. A description of the lateral line system involving SN is given next.
Fig. 2. Lateral line scale (arrow) in Champsodon snyderi
Innervation (Figs. 1, 3, 4; Tables 1, 2). SOL (Fig. 1A) was innervated by the superficial ophthalmic ramus (SOR; Fig. 3A,B), which emerged from the trigeminal foramen in the prootic; at the posterior margin of the frontal, a dorsomedial
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Table 1. Number of neuromasts innervated by their respective lateral line rami in Champsodon snyderi Neuromasts Superficial Canal Total
SOR
BR
MDR
9 6
29 4
41 (+6?) 2
15
33
43 (+6?)
DMDR
SMDR
OTR
STR
LR
Total
5 7
60 0
1 1
11 (-6?) 3
779 20
935 43
12
60
2
14 (-6?)
799
978
SOR, superficial ophthalmic ramus; BR, buccal ramus; MDR, mandibular ramus; DMDR, deep subdivision of mandibular ramus; SMDR, superficial subdivision of mandibular ramus; OTR, otic ramus; STR, supratemporal ramus; LR, lateral ramus
Table 2. Neuromasts innervated by the lateral ramus (LR) in Champsodon snyderi, showing the number included in respective lateral lines Neuromasts
Superficial
Canal
Dorsal vertical lines Lateral vertical lines Ventral vertical lines Dorsal horizontal line Ventral horizontal line Others
144 198 167 99 98 73
19 0 0 0 0 0
Total
779
19
branch of SOR innervated 3 SN on the lateral (2) and dorsal (1) surfaces of the bone; along the posterodorsal margin of the orbit, 4 branches were derived dorsally from SOR, each innervating a single CN (all within a longitudinal canal following the orbital margin of the frontal); anteriorly, SOR innervated 6 SN on the nasal, in addition to 2 CN enclosed within that bone. IOL (Fig. 1A) was innervated by the buccal ramus (BR; Fig. 3A); after its emergence from the cranium through the trigeminal foramen, BR was divided into the dorsomedial and ventrolateral branches. The former, after passing below the eye and along the lateral surface of the snout, curved upward and posteriorly near the snout tip to innervate 6 SN overlying the mesoethmoid and frontal; en route, it innervated 2 CN in infraorbital 1 and 3 clusters of SN associated with infraorbital 1 (5 SN on the posterodorsal margin, 7 along the lateral to anterior surface, and 4 immediately anterior to that bone). The ventrolateral branch was fused with the dorsomedial branch anteriorly, 6 short branches arising before the fusion: 2 posterior branches each innervated 1 CN in a canal-bearing ossicle, and the posteriormost and 3 anterior branches innervated 1 and 2 SN each, respectively, along the ventral margin of the eye. PRL and MDL (Fig. 1A) were innervated by the mandibular ramus (MDR; Fig. 3A,C), which emerged from the facial foramen in the prootic; MDR passed downward along the anterior margin of the preoperculum (innervating PRL) and thence extended anteriorly to the lower jaw tip (innervating MDL); MDR comprised 4 major branches: opercular ramus (OPR; Fig. 3A), median mandibular ramus (MMDR; Fig. 3A), superficial ramus (SMDR; Fig. 3A,C), and deep ramus (DMDR; Fig. 3A,C). OPR (Fig. 3A) was directed
posteriorly, branching off at the dorsal end of the preoperculum; it included branches innervating 2 SN (or 8 SN?—branch fused with a branch of the supratemporal ramus innervating 6 SN), 7 SN (arranged horizontally on the operculum), 16 SN (vertically on the preoperculum), 11 SN (on the suboperculum), and 2 CN (within the upper preoperculum). MMDR (Fig. 3A) coursed dorsally to innervate 5 SN, the dorsalmost being located on the pterotic. Immediately below MMDR, MDR branched into superficial (SMDR; Fig. 3A,B) and deep subdivisions (DMDR; Fig. 3A,B); SMDR innervated 2 oblique (12 and 6 SN, respectively) and 1 horizontal (10 SN) line on the anterior to posterior cheek, 6 SN (2 and 4 SN forming a cluster, respectively) on the posteroventral cheek, and 27 SN along the junction of PRL and MDL to the lower jaw tip; DMDR innervated 3 CN (within the lower preoperculum) and 4 CN and 5 SN (along the lower jaw). OTL (Fig. 1A), comprising 1 CN in the pterotic, was innervated by the otic ramus (OTR; Fig. 3A,B), which shared the trigeminal foramen with SOR and BR for its emergence from the cranium. STL, POL, and the temporal portion of TRL (Fig. 1A) were innervated by the supratemporal ramus (STR; Fig. 3A,B), which emerged from the cranium through a foramen at the exoccipital. STR formed 2 major branches (STR1 and STR2) immediately after emergence. STR1 formed dorsal and ventral branches (STR1a and STR1b); STR1a innervated 1 CN enclosed in an opening at the base of the parietal spine (indicated by an arrow in Fig. 3B) and anteriorly 2 SN on the posterodorsal surface of the frontal; STR1b innervated 1 CN in the extrascapular (this bone only formed POL) and 9 SN (or 3 SN?) (3 in front of the extrascapular and 6 in a vertical line from the bone to pterotic; the branch innervating the latter was fused with MDR; see above). The supratemporal commissure was absent, the opening of the parietal spine forming a continuous canal with the extrascapular laterally, but being sealed medially by the skin. STR2 innervated 1 CN housed anteriorly on the dorsal tubular structure of the posttemporal, that structure forming the temporal portion of TRL. The structure also included 1 CN posteriorly, the branch innervating it [dorsal fin longitudinal ramus of Freihofer (1972)] being derived from the lateral ramus (LR; see below) medial to the operculum; the branch also innervated 5 SN along the posterior cranium to the inner rim of the posttemporal (2 anteriormost SN being medial to 1 CN at the opening of the parietal; see Fig. 3B) and 6 SN arranged in a line from the nape to the dorsal fin origin.
Fig. 3. Innervation in head and anterior body in Champsodon snyderi. A Lateral view; B dorsal view; C ventral view. Black dots and open circles indicate superficial and canal neuromasts, respectively; arrow indicates canal neuromast enclosed in opening at base of parietal spine (see text). ADB, anterodorsal branch; ALR 1, accessory lateral ramus 1; BR, buccal ramus; DB, dorsal branch; DHB, dorsal horizontal branch; DMDR, deep subdivision of mandibular ramus; LR, lateral ramus; MDR, mandibular ramus; MMDR, median mandibular ramus; OPR, opercular ramus; OTR, otic ramus; PLB, posterolateral branch; SMDR, superficial subdivision of mandibular ramus; SOR, superficial ophthalmic ramus; STR, supratemporal ramus and its branches
Champsodontid lateral line system and innervation
The main portion of TRL (see Fig. 1A) comprised 19 canal-bearing tubular scales with 3 or 4 spinules posteriorly (= lateral line scales), which differed significantly from the heart-shaped spinoid scales on other parts of the head and body (see Fig. 2); the lateral line scales were separated from one another, being arranged high on the body along the dorsal fin base. In addition to TRL, 3 series of vertically arranged SN (i.e., dorsal, lateral, and ventral vertical lines; Fig. 1A) and 2 series of horizontally arranged SN (i.e., dorsal and ventral horizontal lines; Fig. 1A) were present, all lateral line scales being included in the dorsal vertical lines. Some additional SN series also occurred on the body and caudal fin. TRL and all SN on the body and caudal fin (Fig. 1A) were innervated by the lateral ramus (LR; Figs. 1B, 3A,B), which shared the same foramen with STR for its emergence from the cranium and detached 26 accessory (regularly segmental) lateral rami (ALR; Fig. 4) along its length (except on the caudal peduncle); LR (Fig. 3B) was positioned deep in the body, being closely associated with the vertebrae. ALR coursed posterolaterally in the horizontal septum between the epaxial and hypaxial muscles, occurring singly in each segment (corresponding to each vertebra), the last ALR (26th) being derived from the lateral surface of the 26th vertebra; each ALR detached from LR had a common root and gave off several branches upon approaching the skin. The following descriptions of ALR 1 and 12 are given as representative of the overall pattern of ALR. ALR 1 (see Fig. 3A,B) was derived from LR medial to the operculum and coursed posterodorsally, where it ramified into 4 branches under the skin on the dorsal surface of the body: the anterodorsal branch (ADB) innervated 2 lines of neuromasts (the upper line transversely on the nape including 8 SN and the lower oblique high on the body including 7 SN) and 1 CN (associated with the 1st lateral line scale), the latter being defined as the 1st dorsal vertical line); the dorsal branch (DB) curved backward and formed an arch confluent with ALR 2, en route innervating the 2nd dorsal vertical line (8 SN and 1 CN associated with the 2nd lateral line scale); the dorsal horizontal branch (DHB) given off at the root of the dorsal branch, fused with ALR 2 posteriorly, innervating 4 SN that formed the anteriormost part of the dorsal horizontal line; the posterolateral branch (PLB) innervated the 1st lateral vertical line, including 9 SN. The structure of ALR 12 (Fig. 4) was basically similar to that of ALR 1, but differed as follows: ramification of the common root into the dorsal (DB) and posterolateral (PLB) branches occurred under the skin on the lateral surface of the body (ALR 1 occurred under the skin on the dorsal surface); the anterodorsal branch (ADB) innervating 2 vertical lines of neuromasts was absent; the ventral branch (VB) innervating a ventral vertical line of neuromasts (9 SN) (11th ventral vertical line) was present, the 1st and 2nd equivalent lines being innervated by ALR 2 (Fig. 3A); the ventral horizontal branch (VHB), innervating a part of the ventral horizontal line (4 SN including 1 at the joint of ALR 13), was continuous with the approximate midpoint of the ventral branch (VB), the anteriormost equivalent
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Fig. 4. Innervation in middle part of body in Champsodon snyderi. Black dots and open circles indicate superficial and canal neuromasts, respectively. ALR 12, accessory lateral ramus 12; DB, dorsal branch; DHB, dorsal horizontal branch; LHB, lateral horizontal branch; LR, lateral ramus; PLB, posterolateral branch; VB, ventral branch; VHB, ventral horizontal branch
branch interconnecting ALR 3 and 4 (Fig. 3A); a lateral horizontal branch (LHB), interconnecting ALR 12 and 13 in the midlateral region of the body, was present, the anteriormost equivalent branch interconnecting ALR 7 and 8 (Fig. 1B). The numbers of dorsal, lateral, and ventral vertical lines were 19 (involving 19 lateral line scales), 26, and 20, respectively, all ALR involving the lateral vertical lines (on a oneto-one basis), but some not involving dorsal (e.g., ALR 11) or ventral vertical lines (e.g., ALR 13) (Fig. 4). Some nerves also occurred that were not included in the basic ALR branching pattern. Four vertically arranged SN immediately below the 2nd dorsal fin spine (see Fig. 3A) were innervated by a branch derived from ALR 2; a horizontal line comprising 11 SN along the 1st dorsal fin base (Figs. 1B, 3A) was innervated by a branch derived from ALR 5, the branch appearing homologous with the dorsal branches of the other ALR. On the caudal peduncle, including the 27th to 30th (urostyle) vertebrae, and caudal fin, the nerve pattern was modified (Fig. 1B): 6 SN in a line on the dorsal surface of the caudal peduncle were innervated by ALR 26; 5 SN in a line on the ventrolateral surface of the caudal peduncle formed the posteriormost part of the ventral horizontal line, being innervated by ALR 26; vertical lines of SN on the 29th (10 SN) and 30th (10 SN) vertebrae, and caudal fin (13 SN) were innervated by 2 (vertebrae) or 3 (caudal fin) branches, respectively, the correspondence of those branches to those of ALR being unknown.
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Discussion The lateral line system in Champsodon snyderi comprised both CN (43) and SN (935) (Table 1). The high number of SN relative to CN is not surprising, the canal structures providing limited space for development of the latter, whereas such constraints are not imposed on the development of the former, although several distinct lines or patterns of SN, defined by their topographic position and innervation, can be recognized in actinopterygian taxa (Coombs et al., 1988). However, because the infraorbital and trunk lateral line canals are incomplete, owing to separation of the elements (i.e., infraorbitals and tubular lateral line scales), as opposed to the typical continuous condition, it is suggested that a decrease in CN number has occurred in the family. The arrangement of the CN-bearing lateral line system was basically identical with that commonly found in teleosts, comprising 7 lines on the head and 1 on the body (Webb, 1989). However, in the Champsodontidae, the infraorbital series has a greatly reduced number of elements, including large infraorbital 1 and 2 or 3 posterior ossicles only, all being separated from one another (Mooi and Johnson, 1997; this study). Despite the loss of canal-bearing elements, the buccal ramus was present, innervating both CN and SN along the lower margin of the eye, suggesting that the loss involved replacement of CN by SN, such being common in teleosts (Coombs et al., 1988). Mooi and Johnson (1997) could not determine whether the posterior elements represented infraorbitals or modified scales. Because the two elements each enclose 1 CN innervated by the buccal ramus, and 1 CN in a posterior infraorbital element is a common condition in teleosts (see Freihofer, 1978: table 1), they are here identified as posterior infraorbitals owing to their innervation pattern. Moreover, the relatively large sizes of the elements favors such identification. Because the scales on the head and body are very small in champsodontids, the “modified scale” hypothesis requires both loss of the infraorbitals and a size increase in the modified scales, being less parsimonious compared with our “preservation” hypothesis. CN in the trunk lateral line were widely separated from one another, being folded in canal-bearing scales (= lateral line scales) that differed clearly from the spinous, heartshaped scales dominating exclusively the other parts of the head and body (Fig. 2). Despite the small size of the lateral line scales and relatively numerous vertebrae [modally 31according to Nemeth (1994); 30 in the Fig. 1], the scale number was only 19, being the reverse to the general trend in teleosts in which the number increases in accordance with decreasing scale size and increasing number of vertebrae. For example, in Bothidae, lateral line scales number 53–54 in the large-scaled Asterorhombus intermedius (36 vertebrae) compared with 74–108 in the small-scaled Bothus myriaster (37–39 vertebrae) (Amaoka, 1969). The number increases to 152–185 in the family (Chascanopsetta lugubris), accompanying an increase in vertebral number (53–57) (Amaoka, 1969). Therefore, the lateral line scales in Champsodon snyderi can be recognized as representing a
reduced condition. In C. snyderi, each ALR innervates a single CN. As an ancestral condition, we suggest that each ALR innervated a greater number of CN along its dorsally arched portion, having continuous lateral line scales (i.e., a continuous trunk lateral line) as is common in teleosts (see following). The lateral line scales were arranged high on the body, being closely associated with the dorsal fin base along its entire course, such being considered as adaptive for the sand-burying behavior of this species (Morohoshi and Sasaki, 2003: Fig. 1). On the other hand, however, the degenerated trunk lateral line with a low number of CN (19) does not appear to be an “important (or primary)” sense organ, especially when the 779 SN on the body are considered (Table 1). Because the 19 CN were always included in the dorsal vertical lines (144 SN; Table 2), it is most likely that the lateral line scales (and CN) are relictual, having been incorporated into “new” vertical lines. Equally developed SN on the dorsal and ventral surface of the body (144 and 167 SN in the dorsal and ventral vertical lines, respectively; Table 2) do not correlate to a benthic habitat, the ventral half of the body being buried under sand. We suggest that utilization of the pelagic habitat during diurnal vertical migration in this species (Morohoshi and Sasaki, 2003) is functionally related to the equal development of SN. Well-developed SN over the body should be critical for nocturnal activities in champsodontids, which are characterized by relatively small eyes. Freihofer (1972) recognized a dorsal longitudinal collector lateral line nerve in 20 or so acanthopterygian families (sensu Greenwood et al., 1966), and Nakae and Sasaki (2005) in the perciform Malakichthys and tetraodontiform Triacanthodes. Although in C. snyderi the dorsally arched parts of ALR are continuous with one another (= collector), ALR are regularly segmental, corresponding to the number of vertebrae. This condition differs clearly from the typical collector nerve that is composed of only about 3–5 rami (= ALR), derived dorsally from LR (see Freihofer, 1972: Fig. 7). Freihofer (1978) described the lateral line innervation in a percoid Polycentrus schomburgkii as having a number of vertical SN lines on the dorsal surface of the body, as in Champsodontidae. In that species, however, the vertical lines are innervated by branches given off from the typical collector nerve, suggesting strongly that the lines are not homologous between the two. Freihofer (1972) listed Umbra, Percopsis, and Aphreoderus as having ALR, 1 each per segment, with dorsal, lateral, and ventral branches that are ramified from a common root under the skin. Although this pattern is similar to the champsodontid condition, the relationships of those genera to Champsodontidae are improbable. Mooi and Johnson (1997) argued that champsodontids were members of the Scorpaenoidei (sensu Mooi and Gill, 1995), based largely on the synapomorphy of a parietal spine with an opening for passage of the supratemporal sensory canal, Shinohara (1994) having previously recognized the parietal supporting a sensory canal as a synapomorphy of his traditional “Scorpaeniformes.” However, Imamura and Yabe (2002), in demonstrating polyphyly
Champsodontid lateral line system and innervation
of the “Scorpaeniformes,” showed that the canal evolved convergently in the scorpaenoid (parietal spine present) and cottoid (spine absent) lineages, based on observations of ontogenetic development of the canal, and argued that homology of the canal between Champsodontidae and the scorpaenoid lineage is unclear. It was seen in this study that the opening encloses the uppermost CN innervated by the supratemporal ramus (STR) in C. snyderi. Our examination of Scorpaena neglecta (BSKU 76486) to evaluate the homology of the opening between the two groups showed the canal to extend medially below the parietal spine, the left and right canals forming the supratemporal commissure, with 1 CN in each canal being innervated by a branch of STR. In C. snyderi, however, an opening is present, but sealed medially by the skin, the commissure thus being absent. Accordingly, the two groups are identical in having a CN on the parietal, but differ in presence or absence of the commissure. The homology of the opening has yet to be studied in the light of other characters, including the presence of a percoid-type collector nerve (comprising 4 ALR) in S. neglecta (personal observation). Acknowledgment G. Hardy (Ngunguru, New Zealand) read the manuscript and offered helpful comments.
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