The pattern of the mechanosensory lateral line on the caudal fin of the two deep‐water gobiid fishes Deltentosteus collonianus and Deltentosteus quadrimaculatus (Teleostei: Gobiidae)

The most common pattern of the lateral line system on the caudal fin of Gobiidae is characterized by three longitudinal rows of free neuromasts. Deltentosteus collonianus and Deltentosteus quadrimaculatus are two benthic Atlantic–Mediterranean gobiid fishes with additional rows on the caudal fin. In these species the caudal fin is more densely covered by the lateral line system compared to the usual status in Gobiidae. An increase of longitudinal neuromast rows occurs rarely in gobiid fishes and is only known in a few species of Gobiidae with a pelagic lifestyle. Both Deltentosteus species show numbers of neuromast rows on the caudal fin between the plesiomorphic three and the advanced eight rows of pelagic gobies. This intermediate position allows discussion of the existence and the characteristics of an underlying pattern in the increase of the number of longitudinal neuromast rows and adaptation to habitat conditions in Gobiidae.


Introduction
During past years the physiology of the lateral line system of teleost fishes has been studied extensively (e.g. Engelmann et al. 2000;Coombs et al. 2001;Mogdans et al. 2003;Carton and Montgomery 2004). Nevertheless, besides the physiological functions of the neuromasts, the primary importance for detecting hydrodynamic stimuli is their arrangement on the body of the fish (Dijkgraaf 1962;Coombs et al. 1988;Webb 1989).
The pattern of the mechanosensory lateral line is decisive for the location of important stimuli. It is adapted to the various lifestyles of fishes (e.g. Coombs et al. 1988;Popper and Platt 1993) and is closely related to the habitat (Hofer 1907;Dijkgraaf 1962;Disler and Smirnov 1977;Coombs et al. 1988Coombs et al. , 2001Montgomery et al. 1997). This is seemingly also true for the total number of neuromasts, which is typically some hundreds (Carton and Montgomery 2004) but can reach some thousands in gobiid fishes. Such extremely high numbers of free neuromasts are found in pelagic gobies such as Aphia minuta (Risso, 1810) and Leucopsarion petersii Hilgendorf, 1880 (Mortara 1918;Scattolin 2003).
Gobiidae are characterized by a specialized mechanosensory lateral line which is dominated by free neuromasts on the head, the trunk, and the caudal fin. Lateral line canals are developed, if at all, only on the head, a canal on the trunk is lacking (Sanzo 1911;Iljin 1930;Ahnelt and Bohacek 2004). The topography of the lateral line system on the head has been widely used for the classification of gobiid fishes (e.g. Takagi 1988;Gill et al. 1992;Larson 2001). Recently, more attention has been paid to the pattern of the free neuromasts on the trunk and the caudal fin (Ahnelt and Duchkowitsch 2001;Shibukawa et al. 2001;Gö schl 2003, 2004;Ahnelt and Scattolin 2003).
The pattern of the lateral line system on the caudal fin of Gobiidae is very conservative (Ahnelt and Gö schl 2004). Environmental pressure and adaptation to new habitats seemingly favour (sometimes drastic) changes of its arrangement on the head and the trunk but less distinct changes, if any, on the caudal fin. In particular, an increase of the number of neuromast rows on the caudal fin is rarely observed (Mortara 1918;De Buen 1923;Scattolin 2003) and is possibly linked to hydrodynamic conditions in the open water column and in deep waters, two environments secondarily inhabited by Gobiidae.
The genus Deltentosteus Gill 1863 has a unique position within the north-eastern Atlantic and Mediterranean gobiid fish fauna (De Buen 1923;Miller 1986). The lateral line system of the two species, Deltentosteus collonianus (Risso, 1820) and Deltentosteus quadrimaculatus (Valenciennes, 1837), is characterized by specialized features. Its arrangement on the head and the trunk has been described by Sanzo (1911) andDe Buen (1923), but information on the pattern of the caudal fin is incomplete.
We describe the unusual pattern of the free neuromasts on the caudal fin of the two benthic deep-water gobies D. collonianus and D. quadrimaculatus. Based on these data and on the arrangement of the lateral line system of pelagic gobies it is possible to postulate in which order neuromast rows are increased from the plesiomorphic three to the apomorphic eight rows on the caudal fin of Gobiidae. In addition, we discuss if the increase of neuromasts and neuromast rows in these two gobiid species is possibly linked to the adaptation to a low-noise habitat.

Material and methods
The lateral line system on the caudal fin of Gobiidae is formed by rows of free (superficial) neuromasts (summarized in Ahnelt and Gö schl 2004). These neuromasts (sensory papillae) run in longitudinal and transversal rows and are generally arranged in two patterns: pattern 1 is characterized by three longitudinal rows and pattern 2 by two longitudinal rows. In both cases generally a transversal row occurs anterior to the longitudinal rows (Ahnelt and Gö schl 2004). The nomenclature of the longitudinal rows of free neuromasts on the caudal fin follows Ahnelt and Duchkowitsch (2001): dorsal (lcd), median (lcm), and ventral (lcv) longitudinal rows. The median longitudinal row lcm extends in elongation of the median trunk lateral line (a series of free neuromasts in Gobiidae) whereas lcd and lcv are accessory lateral lines (Sanzo 1911;Ahnelt and Duchkowitsch 2001;Shibukawa et al. 2001;Ahnelt and Bohacek 2004). These three rows are arranged in a characteristic pattern: lcm is separated from lcd by three and from lcv by two fin rays. This pattern is characteristic for Gobioidei with three longitudinal neuromast rows developed on the caudal fin and seemingly represents the plesiomorphic type for Gobioidei (Ahnelt and Gö schl 2004) (Figure 1A). This characteristic arrangement allows the identification of these three longitudinal neuromast rows in species with more than three rows developed. The position of the neuromast rows compared to the branched caudal fin rays is compared only in adult specimens. In juveniles the number of the branched fin rays is usually not completely developed (H. Ahnelt, unpublished data). The topography of the free neuromasts was studied using a binocular microscope (Wild M-8) with oblique lighting.
The following preserved specimens were examined (collection number, number of specimens, standard length, sampling site).

Results
The lateral line system on the caudal fin in both species is formed by free neuromasts arranged in longitudinal rows. A distinct transversal row, developed in many Gobioidei (compare Ahnelt and Gö schl 2004), does not occur. The longitudinal rows extend on the interradial membranes from the base of the caudal fin rearwards. The neuromasts are large and have the shape of oblong, laterally compressed papillae with a broad base and narrowing distally.

Deltentosteus collonianus
Six longitudinal rows of free neuromasts are developed on the caudal fin. In adult specimens the dorsal-most longitudinal row extends between the third and the fourth (3/4) branched caudal fin rays, the following rows between 5/6, 6/7, 7/8, 8/9 and 9/10 branched caudal fin rays. The neuromast rows are separated by only one caudal fin ray, except for the two dorsalmost rows which are separated by two fin rays. Fifty-nine of 64 specimens show six longitudinal rows developed on each side of the caudal fin. In two specimens six rows occur on the left and five rows on the right side. In three specimens five rows occur on both sides of the caudal fin. Compared with the typical pattern of gobiid fishes exhibiting three longitudinal rows (lcd, lcm, and lcv), three additional rows occur on the caudal fin of this species. From ventral to dorsal: one additional row below the ventral row lcv, a second between lcv and the median row lcm and a third between the dorsal row lcd and lcm, immediately dorsal to the latter. Therefore typically two longitudinal neuromast rows occur dorsal and three rows ventral to lcm. In specimens with five rows the ventral-most row is absent on one or on both sides of the caudal fin, respectively.
Four longitudinal rows of free neuromasts are developed on the caudal fin. In adult specimens the dorsal-most longitudinal row extends between the third and the fourth (3/4) branched caudal fin rays, the following rows between 6/7, 8/9 and 9/10 branched caudal fin rays. The neuromast rows lcd, lcm, and lcv are arranged in the plesiomorphic pattern of Gobiidae: lcd is separated from lcm by three, lcm from lcv by two, and the additional fourth row from lcv by one caudal fin rays. Thirty-four of 39 specimens have developed four longitudinal rows on each side of the caudal fin. In three specimens only three rows occur on both sides of the fin. A specimen with three longitudinal rows is figured in Sanzo (1911, Plate 9, Figure 6). Compared with the typical pattern of gobiid fishes with three longitudinal rows (lcd, lcm, and lcv), one additional row, ventral to lcv, occurs on the caudal fin. No further rows have been found between lcd, lcm, and lcv. Therefore typically one longitudinal neuromast row occurs dorsal and two rows ventral to lcm. In specimens with three longitudinal rows the ventral-most row is absent in two specimens and in one lcv is lacking.
Deltentosteus collonianus and D. quadrimaculatus are the only Gobioidei known with six or four longitudinal rows of free neuromasts on the caudal fin, respectively. Both species are the only benthic gobies known so far with a number of neuromast rows on the caudal fin higher than the plesiomorphic three rows. Three longitudinal lateral lines on the caudal fin are also known from basal perciform fishes (Jakubowski 1966(Jakubowski , 1967Greenwood 1976;Collette and Banarescu 1977). Springer (1983), who identified this feature on Rhyacichthys, classified these three lateral lines on the caudal fin as primitive for percoid and gobioid fishes. [Note: Springer (1983) mentions three lateral lines on the caudal fin of Rhyacichthys, Ahnelt and Gö schl (2004) describe four lateral lines as typical for Rhyacichthyidae. The triple lateral line system on the caudal fin of Rhyacichthys as mentioned by Springer (1983) refers to the longitudinal lateral lines. Nevertheless, the typical pattern of Rhyacichthys aspro consists of four lateral lines on the caudal fin (Ahnelt and Gö schl 2004). The fourth lateral line is formed by a discontinuous transversal row of free neuromasts on the base of the caudal fin. This arrangement of the lateral line system on the caudal fin, a transversal row and three longitudinal rows, was identified as the plesiomorphic pattern for Gobioidei by Ahnelt and Gö schl (2004). The longitudinal lateral lines are formed by three rows of free neuromasts each preceded by a short lateral line canal in Rhyacichthyidae.] From their results Ahnelt and Gö schl (2004) concluded that the decrease of the number of longitudinal neuromast rows on the caudal fin of Gobioidei follows a certain order. A reduction in the number of neuromast rows first affects the ventral row (lcv) and in a next step the dorsal row (lcd). Finally, lcm is the only remaining row (e.g. in the odontobutid Perccottus glenii Dybowski, 1877). A further reduction is known from the blind goby Typhlogobius californiensis (Steindachner, 1879). In most specimens of this species, the only known blind fish with a reduced lateral line system (Ahnelt and Scattolin 2003), a few neuromasts are irregularly scattered over the central and dorsal part of the caudal fin. These neuromasts are the rest of two longitudinal rows (lcd and lcm). In gobioid fishes with two longitudinal lateral lines (lcd and lcm) on the caudal fin, these are also separated by three fin rays.

Discussion
As a deviation from the plesiomorphic pattern with three longitudinal lateral lines the number of neuromast rows on the caudal fin of a few Gobiidae is secondarily increased to four (De Buen 1923;present data), six (Fage 1918;present data), or eight longitudinal rows (Mortara 1918;Scattolin 2003), making it difficult to identify the three basic longitudinal rows. In the plesiomorphic state these three rows cover the dorsal, central and ventral part of the caudal fin of Gobioidei and are arranged in a characteristic pattern. The dorsal row (lcd) is separated from the median (lcm) by three and lcm from the ventral row (lcv) by two fin rays (Ahnelt and Gö schl 2004). Therefore the gap between lcm and lcd is wider than between lcm and lcv, a pattern already noted by Sanzo (1911) (Figure 1A). This arrangement allows the identification of these three basic neuromast rows in species with more than three rows ( Figure 1) and also allows the identification of additional rows relative to lcd, lcm, and lcv. To date only a few gobiid species are known with an increased number of longitudinal rows on the caudal fin, e.g. A. minuta and L. petersii (Mortara 1918;Scattolin 2003), with each neuromast row separated from the other by only one fin ray. These species can be considered as derived forms and are characterized by paedomorphic features such as the lack of lateral line canals, transparent bodies, and pelagic lifestyle. Ahnelt and Gö schl (2004) suggested that not only the decrease but also the increase of longitudinal neuromast rows follows a scheme, but contrary to the reduction of the neuromast rows on the caudal fin the manner in which their number increased was not completely understood. The two species of Deltentosteus display two different patterns of the lateral line system. With six rows D. collonianus is seemingly more specialized than D. quadrimaculatus with four rows. This different number of rows allows postulation on the order in which such neuromast rows are increased from the plesiomorphic three to the apomorphic eight rows found on the caudal fin of pelagic gobies: 1. Deltentosteus quadrimaculatus is characterized by only one longitudinal neuromast row above the plesiomorphic three rows of Gobiidae ( Figure 1B). This fourth row occurs in the first interradial space ventral to lcv, possibly as the result of a doubling of lcv. The typical gobiid pattern with three fin rays between lcd and lcm and two between lcm and lcv is not affected. 2. Three additional neuromast rows are developed on the caudal fin of D. collonianus ( Figure 1C). As in D. quadrimaculatus one longitudinal row occurs in the interradial space immediately ventral to lcv, the next in the free interradial space between lcv and lcm, and the third immediately dorsal to lcm. All neuromast rows except lcd are separated from each other by only one fin ray. The typical pattern of Gobiidae is changed distinctly. The gap between lcv and lcm is closed completely, those between lcm and lcd partly. But a somewhat asymmetrical pattern with lcd separated from the next row by two fin rays is still retained. 3. In some pelagic Gobiidae (e.g. A. minuta, L. petersii) the number of longitudinal rows is increased to eight rows ( Figure 1D). As a result the last gap immediately ventral to lcd is closed. Additionally, an eighth row occurs in the interradial space dorsal to lcd. In these species the arrangement of the neuromast rows is symmetrical, i.e. the longitudinal rows are separated from each other by one fin ray. In A. minuta and L. petersii the dorsalmost neuromast row extends between the second and third (2/3) and the ventralmost row between 9/10 branched fin rays (Scattolin 2003). This corresponds well with the less complete pattern of D. collonianus. In combination with a pelagic lifestyle eight longitudinal rows of free neuromasts on the caudal fin is the most advanced pattern in the Gobioidei and so far is only known in Gobiidae.
The pattern of the lateral line system on the caudal fin of D. collonianus and D. quadrimaculatus differs from each other and each represents a derived condition. Nevertheless, the sister taxa of Deltentosteus are not identified yet. Therefore the increase of the number of neuromast rows on the caudal fin in these two Deltentosteus species is obviously an apomorphic feature but we have no evidence that this is an autapomorphy. Additionally, it is unlikely that the above-mentioned species with eight longitudinal neuromast rows on the caudal fin could be regarded as sister taxa. These species differ distinctly from D. collonianus and D. quadrimaculatus by a series of paedomorphic features such as the lack of lateral line canals, transparent bodies, and pelagic lifestyle.
To date no gobiid species is known with seven neuromast rows and the ontogeny of the lateral line system of species with eight rows is not investigated. Therefore it is not clear how the number of neuromast rows is increased from six to eight. Nevertheless, concluding from the three above-mentioned types of arrangement of the lateral line system on the caudal fin of Gobiidae, the number of longitudinal neuromast rows is seemingly increased from ventral to dorsal: additional rows occur first in the ventral third of the caudal fin, a further increase of the neuromast rows covers the central and finally the dorsal part of the fin.
Seemingly at least two basic pathways developed during gobioid phylogeny. Originating from the plesiomorphic pattern with three neuromast rows on the caudal fin either (1) the number of neuromast rows decreased or (2) the number of neuromast rows increased. Deviations from the plesiomorphic pattern obviously occurred several times and independently within the Gobioidei (Ahnelt and Gö schl 2004).
Virtually nothing is known about the lifestyle of the two Deltentosteus species. Both are benthic, are usually collected during dredging on soft bottom (mud, muddy sand, or sand), and occur inshore to a depth of 120-160 m (Miller 1986;Ahnelt and Dorda 2004). Deltentosteus collonianus and D. quadrimaculatus are so far the only benthic gobies described with an increased number of longitudinal neuromast rows on the caudal fin. Therefore an increase of neuromast rows on the caudal fin of Gobiidae, reported from several pelagic species (Mortara 1918;Scattolin 2003), is not necessarily linked to a pelagic lifestyle. We assume that the increase of neuromast rows on the caudal fin is possibly linked to the adaptation to a low-noise habitat in deep habitats.
Extensive proliferation of free neuromasts is characteristic of many fishes inhabiting lownoise environments (Coombs et al. 1988;Webb 1989;Mogdans et al. 2003;Kasumyan 2003). Such an elaborated lateral line system occurs on the trunk and the caudal fin of D. collonianus and D. quadrimaculatus (Sanzo 1911, Plate 9, Figure 6; De Buen 1923, Figure 27). Surprisingly, the number of free neuromasts on the head is only slightly increased, if at all, and head canals, generally reduced or lacking in species inhabiting lownoise habitats are still developed. A feature such as lateral line canals is on first sight contradictory to the postulated increase of free neuromasts as a result of adaptation to a low-noise habitat. But in D. collonianus and D. quadrimaculatus these canals are perforated by an unusually high number of additional pores (Sanzo 1911;De Buen 1923, Figures 31, 37;Miller 1986) allowing a better and multidirectional instead of linear exposure of the canal neuromasts to water movements. Besides the complete loss of head canals and replacement of the canal neuromasts by free neuromasts, the extensive perforation of these canals is seemingly another but uncommon pathway of the evolutionary transformation of the head lateral line system in gobiid fishes.
The number of neuromast rows on the caudal fin (and also the increase in the total number of free neuromasts) in D. collonianus and D. quadrimaculatus is obviously linked to the high number of neuromasts on the trunk and to the extensively perforated head canals. This combination of features of the mechanosensory lateral line could be regarded as an indication of a specialized lifestyle in a low-noise habitat, a hypothesis which needs to be tested.