Scale formation in selected western North Atlantic flatfishes

Transcription

1 Journal of Fish Biology (2006) 68, doi: /j x, available online at Scale formation in selected western North Atlantic flatfishes K. W. ABLE* AND J. C. LAMONACA Rutgers University, Institute of Marine and Coastal Sciences, Marine Field Station, 800 c/o 132 Great Bay Blvd, Tuckerton, NJ , U.S.A. (Received 16 February 2005, Accepted 19 October 2005) Patterns of scale formation (onset, completion and spatial pattern) were examined for five species of flatfishes in four families (Paralichthyidae: summer flounder Paralichthys dentatus, smallmouth flounder Etropus microstomus, Scophthalmidae: windowpane Scophthalmus aquosus, Pleuronectidae: winter flounder Pseudopleuronectes americanus and Soleidae: hogchoker Trinectes maculatus, to determine if the patterns are a useful indicator for the transition from the larval to the juvenile periods. In all species (except T. maculatus in which samples were limited), the ontogenetic pattern was very similar with onset of scale formation occurring on the lateral surface of the caudal peduncle, then spreading anteriorly along the presumptive lateral line, then laterally over the body, on to the head, and eventually on to the median fins. The timing of scale formation, relative to fish size, was late relative to other morphological and behavioural characters (i.e. fin ray formation, eye migration and settlement). The onset of scale formation, across all species, occurred at mm total length (L T ), at the same approximate size as eye migration and settlement. Completion of scale formation on the body occurred at mm L T but completion of scale formation on the fins did not occur until mm L T. Thus completion of scale formation in these flatfishes is apparently the last external morphological change to occur during the larval to juvenile transition and, as a result, is not completed until approximately one third (S. aquosus and P. dentatus) to one fourth (P. americanus) or about the same time (E. microstomus and T. maculatus) as the size at first reproduction. This character may have relevance to defining the end of the larval period and the beginning of the juvenile period in flatfishes and other fishes. In addition, the pattern of scale formation may be useful in enhancing understanding of systematics, functional morphology and habitat use. # 2006 The Fisheries Society of the British Isles Key words: flatfishes; juveniles; larvae; morphology; scales. INTRODUCTION Scales of teleosts are flexible, calcified plates lying within shallow envelopes, or scale pockets, in the upper layers of the dermis (Bullock & Roberts, 1974). Scales provide multiple functions, including protection of the lateral line, storage area for minerals and nutrients (van Oosten, 1957), drag reduction (Videler, 1994) and a useful means of ageing (Jerald, 1983; Busacker et al., 1990), and identifying *Author to whom correspondence should be addressed. Tel.: þ ext.230; fax: þ able@marine.rutgers.edu # 2006 The Fisheries Society of the British Isles 1679

2 1680 K. W. ABLE AND J. C. LAMONACA fishes (Batts, 1964; DeLamater & Courtenay, 1974; Daniels, 1996). Despite these multiple functions and uses relatively little is known about the patterns of scale formation in teleosts, especially marine taxa. It is known that scales have their origin in dermal papilla formed by the multiplication of fibroblasts (Elson, 1939; van Oosten, 1957) that develop into papillae (Elson, 1939; Waterman, 1970; Lindsey, 1988) that originate in one or several loci on the surface of the body (Andrews, 1970; Armstrong, 1973; Sire, 1981; Sire & Arnulf, 1990). For many species, scales originate at a single locus on the lateral midline of the caudal peduncle (Andrews, 1970; White, 1977) and the formation of scales often occurs between the larval to juvenile periods (Ahlstrom et al., 1976; Kendall et al., 1984; Gozlan et al., 1999; Webb, 1999; Urho, 2002). As a result, the completion of scale formation may be a useful indicator of the completion of the larval period and the beginning of the juvenile period (Fuiman, 1997; Fuiman et al., 1998). In order to test this possibility in flatfishes, the size and variation in size at scale formation (onset, completion and spatial pattern) were compared in five flatfishes in four families (Paralichthyidae, Pleuronectidae, Scophthalmidae and Soleidae; Chapleau, 1993) from the western North Atlantic. SOURCES OF SPECIMENS MATERIALS AND METHODS Specimens for examination of the patterns of scale formation were collected, with a variety of techniques (plankton nets, beam trawls, otter trawls and seines), primarily in Great Bay-Little Egg Harbor estuaries (c N; W) and on the adjacent continental shelf off New Jersey, U.S.A. An effort was made to examine a length series from prior to eye migration to full coverage of scales as occurs in the adult condition. Sample sizes examined varied between species (Table I). SCALE TECHNIQUES Because scale formation was examined in wild-caught specimens (Table I), care was taken during all stages of collection, preservation and examination to prevent damage of the integument or scale loss. Individuals to be stained were first preserved in 95% ethyl alcohol (ETOH) for at least 48 h, then treated with a solution containing alizarin red S to elucidate scales, as adapted from Taylor (1967) and Pothoff (1983). Stock solutions consisted of alizarin red S powder ad libitum plus a 05% KOH solution diluted 1 : 10 in 50% ETOH solution. Individuals were immersed in alizarin red S solution for c. 30 s and rinsed with deionized water or ETOH. Stained individuals were then transferred to 95% ETOH for final preservation. These specimens were visually examined with an Olympus stereomicroscope and patterns of scale formation were illustrated on blank templates for individual species adapted from illustrations in Able & Fahay (1998). Additional individual variation was determined for one species [winter flounder, Pseudopleuronectes americanus (Walbaum)] for which there were a large number of individuals over the appropriate size range. In all cases, the illustrations were then transferred to a digital medium via illustration in Adobe Photoshop. The area covered by scales was calculated from these illustrations using the Image J software package (Rasband, 2003) and expressed as per cent of body covered relative to the adult condition of scale coverage (100%). The adult condition was based on the smallest size at which scales were no longer being formed.

3 SCALE FORMATION IN FLATFISHES 1681 TABLE I. Scale formation characteristics in representative flatfishes from the Middle Atlantic Bight. Observations of onset and completion of scale formation on the body and fins are original observations; the other information is based on the literature sources provided Species L T (mm) at hatch LT (mm) at completion of adult complement of fin rays LT (mm) at settlement / metamorphosis L T (mm) at onset of scale formation on body LT (mm) at completion of scale formation on body L T (mm) at onset of scale formation on fins L T (mm) at completion of adult complement of scales Per cent body covered by scales LT (mm) at first reproduction Sample size for scale formation LT (mm) range examined for scale formation Reference Etropus microstomus Scophthalmus aquosus Paralichthys dentatus Pseudopleuronectes americanus Trinectes maculatus 20? ,2,3, ,5,6,3, 4, , , 12, 8, 5, 9, 10, 3, c , 13, 5, 3, ?? < and , 2, 3, 4 L T, total length. 1, Richardson & Joseph (1973); 2, Martin & Drewry (1978); 3, Able & Fahay (1998); 4, Collete & Klein-MacPhee (2002); 5, O Brien et al. (1993); 6, Morse & Able (1995); 7, Neuman & Able (2002); 8, Able et al. (1990); 9, Keefe & Able (1994); 10, Able & Kaiser (1994); 11, Hildebrand & Cable (1938); 12, Merriman & Sclar (1952); 13, Laroche (1981).

4 1682 K. W. ABLE AND J. C. LAMONACA The illustrations of representative stages of scale formation were standardized across all species. For example, the location of the lateral line is shown with a thin line, even before it is formed, to provide a local landmark. In addition, the margin of the dorsal and anal pterygiophores is also noted with a thin line. The area behind the pectoral fins is not shaded to indicate the location of the pectoral fins in order to provide another local landmark. The darkly shaded areas indicate scale formation on the body; the grey shaded areas indicate where scales occur on the fins. For selected species [P. americanus and windowpane Scophthalmus aquosus (Mitchill)] both sides of the fishes were compared because blind and ocular side scale formation can differ in some flatfishes (Ahlstrom et al., 1984). For all species, no differentiation was made between ctenoid (typically on the ocular side) and cycloid (typically on the blind side) scales (Norman, 1934; Ginsburg, 1952; Gutherz, 1967). Neither were occurrences of accessory scales noted, which typically occur later in development on summer flounder Paralichthys dentatus (L.) and smallmouth flounder Etropus microstomus (Gill) (Ginsburg, 1952; Gutherz, 1967). RESULTS PATTERNS OF SCALE FORMATION In all flatfish species examined, the onset of scale formation began after eye migration and attainment of the general asymmetrical, flattened shape of the adult. Scale formation, as generally depicted for the ocular side, shared the same general sequence in scale formation. For all species that could be examined, progression of scale formation began on the caudal peduncle, and extended anteriorly and then laterally, with no obvious differences between bothid, paralichthyid, pleuronectid and scophthalmid species (Figs 1 3). Specimens of the appropriate size were lacking to determine the pattern for hogchoker Trinectes maculatus (Bloch & Schneider). In the adult condition scales covered 82 84% of the entire body and fins (Table I). The exception was T. maculatus, in which the scales covered 96% of the body. There are some species specific differences in the size at onset and completion of scale formation. The patterns depicted in Figs 1 3 are representative of the larger sample sizes examined for this study (Table I). Etropus microstomus Scale formation occurs over the size range of c. 33 mm (Figs 1 and 3). The onset of scale formation probably occurs between mm because specimens slightly larger (113 mm) have a fully scaled lateral line (Fig. 1). By c. 13 mm the area covered by the scales has expanded laterally both above and below the lateral line and this continues at 15 mm. By mm the body is completely covered and other scales have begun to develop on the operculum. By c. 22 mm scales cover the head, except for the snout, (as in the adult condition) and small areas of the operculum. At larger sizes, scales begin forming on the dorsal, anal and caudal fins and they reach the adult condition, i.e. scale formation is complete, by c. 43mmL T, when the scales cover all except the tips of the median fins. This size is very close to the size at first reproduction (599 mml T ) (Table I). Scophthalmus aquosus Scale formation occurs over a relatively large size range from mm (Figs 1 and 3). Scale formation begins with a few scales on the midline of the

5 SCALE FORMATION IN FLATFISHES 1683 (a) (b) (c) mm 27 6 mm 17 0 mm 11 3 mm 33 8 mm 19 8 mm 13 8 mm 36 5 mm 20 5 mm 15 5 mm 41 1 mm 31 0 mm 22 1 mm 46 5 mm 48 0 mm 43 6 mm 80 0 mm 88 5 mm FIG. 1. Description of scale formation relative to total length in selected flatfishes: (a) Etropus microstomus, (b) Scophthalmus aquosus and (c) Paralichthys dentatus. caudal peduncle where the lateral line will eventually form (Fig. 1). By 33 mm scale formation has extended along the lateral line to the posterior edge of the operculum and has also expanded laterally. By c. 36 mm scales have extended anteriorly beyond the pectoral fins but not on the operculum or head. By 41 mm, the lateral extent of scale formation has continued with new locations for scale development occurring at the dorsal and ventral margins of the body near the middle of the dorsal and anal fins. By c mm the body is completely scaled and scales are beginning to form on the operculum. Between sizes of mm, scales are beginning to form on the median fins. By 80 mm scales have formed on the dorsal, anal and caudal fins and scale formation has reached the adult condition. This size is a little more than approximately one third of the size at first reproduction (Table I). In an attempt to determine if the extent or rate of development differed between the ocular and blind sides of this species, scale formation on both sides were examined (Fig. 3). Based on these observations, the blind side may have lagged slightly behind the eyed side at sizes between mm L T but at larger sizes they appear similar. Paralichthys dentatus Scale formation occurs over a larger size range than the other species, i.e mm (Figs. 1 and 3). By mm, scales are present along the lateral line from the

6 1684 K. W. ABLE AND J. C. LAMONACA (a) 13 5 mm 16 1 mm 18 1 mm (b) 23 3 mm 25 0 mm 33 0 mm 46 2 mm 66 2 mm 58 1 mm FIG. 2. Description of scale formation relative to total length in (a) Pseudopleuronectes americanus and (b) Trinectes maculatus. origin of the caudal fin to behind the pectoral fin. By c. 20 mm, the scales have expanded laterally but not anteriorly. By 22 mm the scales have expanded further laterally and also anteriorly to the posterior margin of the operculum. By 31 mm scale formation has extended to the dorsal and ventral limits of the body and extended anteriorly, to the dorsal portion of the head behind the eyes. By 40 mm all the scales are formed on the body and some are beginning to form on the median fins. By c. 88 mm all the scales are formed on the dorsal, anal and

7 SCALE FORMATION IN FLATFISHES (a) * 100 (b) * * * Adult scale coverage (%) (c) * 100 (d) * 100 (e) * L T (mm) FIG. 3. Variation in areal coverage of scales (means S.E., where the sample size is sufficient) by length during development presented as per cent of the adult condition of scale coverage in (a) Etropus microstomus (n ¼ 62 ocular), (b) Scophthalmus aquosus (n ¼ 55 ocular and n ¼ 17 blind), (c) Paralichthys dentatus (n ¼ 49 ocular), (d) Pseudopleuronectes americanus (n ¼ 117 ocular and n ¼ 22 blind) and (e) Trinectes maculatus (n ¼ 62 ocular). *, size examined in which scales have not formed.

8 1686 K. W. ABLE AND J. C. LAMONACA caudal fins and scale formation has reached the adult condition. This size is approximately one third of the size attained at first reproduction (Table I). Pseudopleuronectes americanus The duration of scale formation occurred over c. 53 mm (Figs 2 and 3). Scale formation begins with a few small scales in the middle of the caudal peduncle at c. 13 mm. By mm scales are formed along the entire lateral line. By mm the scales rows have expanded dorsally and ventrally but not to the ventral margin of the body. At c. 23 mm the scales have expanded to cover a broader area extending to the base of the dorsal and anal pterygiophores. Scales begin to form on a small area of the operculum between mm. Between mm new scales begin forming at several locations over the base of the dorsal and anal pterygiophores. By 44 mm, scales are forming on the median fins. By 66 mm scale formation has reached the adult condition because scales extend midway on to the dorsal and anal fins and slightly further on the caudal fin. This size is approximately one fourth the size of first reproduction (Table I). In a comparison between the eyed and the blind sides, the blind side seemed to lag slightly behind the eyed side at sizes between mm and at sizes <60 mm. The latter may be the adult condition for the blind side. There were a large number of specimens of this species, of the appropriate sizes, to examine scale formation in more detail and as a result it was possible to determine how much variation occurs at similar sizes. As an example, specimens that ranged from mm(n ¼ 5) varied in areal coverage of scales from 3 13%. In another example, individuals ranging from mm (n ¼ 4) varied from 13 40%. At larger sizes, an individual at 316 mm had new scales forming over the dorsal and anal pterygiophores while an individual at 318 mm did not. Trinectes maculatus There is an incomplete series for scale formation of this species and thus less is known of the pattern of scale formation especially between sizes of 5 20 mm (Figs 2 and 3). Individuals <5 mm have no scales. By 25 mm the scales cover almost all of the body with the exception of a patch just anterior to the approximate location of the pectoral fin. At this same size some scales are beginning to form on the proximal portions of the dorsal, anal and caudal fins. By mm scales on the body are complete and the scales on the fins are more extensive. This pattern continues until mm at which size the scales almost completely cover the fins, more so than any of the other flatfishes examined (Figs 1 3), and achieve the adult condition. The size is approximately the same size as that at first reproduction (Table I). DISCUSSION DEVELOPMENTAL CONSIDERATIONS The onset of scale formation is variable for the western North Atlantic flatfishes examined here. It occurs at the same length or at greater lengths than that at which most major morphological features have been completed (Table I). For

9 SCALE FORMATION IN FLATFISHES 1687 example, while the onset of scale formation occurs at approximately the same length as completion of the adult complement of fin rays for some species (E. microstomus and P. americanus) for others it occurs at larger lengths (S. aquosus and P. dentatus) (Table 1). This difference is especially marked for S. aquosus in which the fin rays are complete at 85 mm while the onset of scale formation does not occur until 270 mm. The onset of scale formation on the body occurred at sizes of mm for the five species for which data are available (Table I). This is at the same approximate size (E. microstomus) or larger than the size (S. aquosus, P. dentatus and P. americanus) at which the general adult body forms (flattened and asymmetral) and eye migration occurs for these species (Table I). Thus, all median fin rays have already been formed (Martin & Drewry, 1978), a common character for discerning the end of transformation and metamorphosis (Kendall et al., 1984; Fuiman, 1994; 1997; Fuiman & Higgs, 1997; Fuiman et al., 1998; Urho, 2002). The completion of scale formation in these flatfishes occurs at larger sizes in development, relative to other morphological changes, than is typically considered for most fishes (Table I). Scale formation of these same flatfishes was not complete until mm L T, depending on the species. Completion of the adult complement of scales, including on the fins, did not occur until mm L T. The sizes at completion of the adult complement of scales, including the fins, are overlapping or one third to one quarter the size at first reproduction, another indication that completion of scale formation occurs relatively late in development. The completion of scale formation has been identified as a useful ontogenetic index for the end of the larval period and the beginning of the juvenile period [although Balon (1999) considers scales less vital characters ]. This length based character (Armstrong, 1973; Fuiman 1997) undergoes transition late in development and after the completion of the last sensory system to be developed, i.e. the lateral line (Webb, 1989, 1999; Fuiman et al., 1998; Higgs & Fuiman, 1998). The length based nature of scale formation was not specifically examined in the present study but in other groups of fishes (cyprinodontid and fundulids) the length at scale formation was similar in field captured and laboratory reared specimens (Sakowicz, 2003, K.W. Able, unpubl. data). Further considerations for S. aquosus (Neuman & Able, 2002), based on a comparison of a variety of morphological characters, has also suggested the completion of scale formation as a good indicator for the end and beginning of the larval and juvenile periods, respectively. This has been suggested for non-flatfish species as well (Copp & Kovac, 1996; Fuiman & Higgs, 1997; Fuiman et al., 1998; Urho, 2002). Thus, one possibility to consider, as an ontogenetic index for flatfishes and perhaps other fishes, is that the larval period ends when scale formation begins and the juvenile period begins when scale formation, on the body, is complete. Those individuals in the intervening period could be defined as transitional or transforming (Kendall et al., 1984) individuals. This approach may be an advantage to those working on development and ecology of the early life history of flatfishes and other fishes. The benefit would be that instead of using the numerous terms that have been applied to individuals that have not completed development including postlarvae, pterygiolarvae, prejuveniles (Kendall et al., 1984) and metalarvae (Snyder, 1976) the single term transforming could be applied. A

10 1688 K. W. ABLE AND J. C. LAMONACA potential difficulty in the broad use of this metric is that some species and families of fishes lack scales (van Oosten, 1957). PATTERNS OF SCALE FORMATION Variation in scale formation within species was relatively small, based on the small measures of S.E. about mean values at different sizes based on the data for some species (Fig. 3). Most often the highest variability occurred for the smallest specimens examined. Some of this variation may simply be due to variability in shrinkage upon preservation, which commonly occurs in many small fishes (Fowler & Smith, 1983; Kruse & Dalley, 1990). Some variations may also be due to type of preservative. This may be especially important when assembling a length series from multiple sources. There are few accounts of scale formation for flatfishes in the literature with which to compare with the present observations. For one species, however, the patterns in timing appear different but these differences in timing are the result of different approaches. A prior examination of scale formation in S. aquosus divided up the surface of the ocular side into regions and determined the onset and end of scale formation in each region separately based simply on the presence or absence of scales in each region (Neuman & Able, 2002). The approach used here (Figs 1 and 2), in general, provides a more accurate description of the pattern of scale formation. In another study of scale formation for Paralichthys olivaceus (Temminck & Schlegel), completion was reported at a relatively large size (540 mm) (Seikai, 1980). In the present examination of a congener, P. dentatus, scale formation on the body was completed at 405 mm L T but scale formation on the fins was not complete until 885 mm L T. Curiously, Seikai (1980) did not mention or illustrate scale formation on the fins of P. olivaceus. Perhaps the focus on scales on the body, and not the fins accounted for this. A similar reason may account for the description of a fully scaled T. maculatus of 18 mm (Hildebrand & Cable, 1938) while the present observations indicate that scale formation, on the fins, is not complete until much larger (Fig. 2). Prior studies of P. olivaceus noted that anomalously coloured individuals appeared to form scales at a slower rate than normally coloured individuals raised in a hatchery (Seikai, 1980). Asymmetry in the general morphology of the ocular v. the blind side in flatfishes, including scales, is not uncommon (Norman, 1934; Ginsburg, 1952; Ahlstrom et al., 1984) but the differences in the areal coverage of scales do not appear to be large in the two species examined in this study. While the pattern of scale formation on the blind side occasionally lags behind that of the ocular side, the pattern is generally similar, at least for S. aquosus. InP. americanus, the areal extent of the scales on the blind side seems to lag behind late in development. Larger fish would need to be examined to determine if the blind side achieves the same amount of areal coverage of scales as occurs on the ocular side. The general pattern of scale formation between flatfish species was similar with scales first forming at a single locus on the caudal peduncle and then extending anteriorly to cover the lateral line, then laterally and on to the head and fins until the adult condition was achieved, although Fukuhara & Fushimi, (1984) described an exception for a non-flatfish species. The pattern of onset of

11 SCALE FORMATION IN FLATFISHES 1689 scale formation on the caudal peduncle is similar to that for other fishes in other families although the number of species for which there is detailed information is small and is biased toward freshwater families (Andrews 1970, White 1977). As a further example of the limited information available, of the 66 marine species with scales on the east coast of the U.S. treated in Able & Fahay (1998), only 31 (47%) species have information on either onset or completion of scale formation and none describe the pattern of scale formation as completely as is provided here for the flatfishes. All flatfishes examined have scales on the fins (dorsal, anal and caudal) (Figs 1 and 2), a pattern shared with all known Pleuronectiformes (Norman, 1934). This observation and differences between flatfishes and other families suggest that the pattern of scale formation (number of loci at onset, size at onset, duration and size at completion) and per cent body coverage may provide some insights into the taxonomy and phylogeny of fishes as has been observed for scale morphology (Roberts, 1993; Daniels, 1996) and lateral line development (Webb, 1989, 1999). The value of the pattern of scale formation will only become apparent as this information becomes available for a larger number of species and from other families of fishes. ECOLOGICAL CORRELATES The functional significance of teleost scales is largely unknown although it has been suggested that they play a role in protection and a storage area for minerals and nutrients (van Oosten, 1957) and drag reduction (Videler, 1994). In the species of flatfish examined here, the onset of scale formation begins at or after settlement (Table I), thus scales may play a role in the movement from the water column to the benthos and interactions with the substratum. Prior studies with S. aquosus lead to the suggestion that the timing of complete scale formation on the body (46 54 mm L L ) corresponded with the ability to bury ( mm L T ) (Neuman & Able, 2002). This correspondence between completion of scale formation and burial does not apply to other flatfishes. For P. dentatus, size at first (partial) burial in laboratory experiments occurred at 174 mml T, a size at which eye migration is complete (Keefe & Able, 1994) but scales are just beginning to form (Fig. 1). Complete burial (all parts of body except head) occurs at >22 mm L T (Keefe & Able, 1993, 1994) although completion of scale formation does not occur until 405 mm (on body) to 885 mm (on fins) (Table 1). Scale formation in flatfishes also may correspond to habitat use such that completion of scale formation may be related to the selection of habitats in general (Gibson, 1994). Clearly, more details of scale formation relative to behaviour are required for a better understanding of how this change in morphology influences the behavior and ecology of flatfishes and other fishes. We thank the staff at the Rutgers University Marine Field Station many of whom assisted in making collections of fishes for this analysis. M.P. Fahay and G.P. Sakowicz provided comments on an earlier draft. Support for this project was provided by Rutgers University Marine Field Station. This paper is Rutgers University Institute of Marine and Coastal Sciences Contribution No

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