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Comparative Morphology of Spined Scales and Their Phylogenetic Significance in the Teleostei

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Comparative Morphology of Spined Scales and Their Phylogenetic Significance in the Teleostei BULLETIN OF MARINE SCIENCE, 52(1): 60-1 L3, 1993 COMPARATIVE MORPHOLOGY OF SPINED SCALES AND THEIR PHYLOGENETIC SIGNIFICANCE IN THE TELEOSTEI Clive D. Roberts ABSTRACT The organization and morphology of spined scales are described from a broad-based survey of body scales of teleost fishes using scanning electron microscopy and light microscopy. Three general types of spined scale are recognized (I) crenate: simple marginal indentations and projections, (2) spinoid: spines continuous with the main body of the scale, and (3) ctenoid: spines separate from the main body of the scale, in two common configurations of transforming or peripheral ctenoid and a rare configuration of whole ctenoid. Crenate scales occur widely in the Elopocephala; spinoid scales occur widely in the Euteleostei; peripheral ctenoid scales have a restricted distribution in the Euteleostei, occurring probably indepen- dently in the Ostariophysi, Paracanthopterygii, and Percomorpha; transforming ctenoid scales are a unique specialized form of spined scale, and are a synapomorphic character diagnosing the Percomorpha; whole ctenoid scales are known from only two percomorph genera. The greatest diversity of spined scales is found in the Ostariophysi and the Percomorpha. Spined scales show great evolutionary plasticity, and it is suggested that changes in ontogenetic trajectory, as well as the evolution of new characters, contribute to the diversity of spinal structures observed. The value of scale morphology in fish classification was recognized almost 160 years ago by Louis Agassiz who classified fishes on the basis of four scale types: "Les Placoides" (e.g., "Pastenagues, Raies, Squales") with spine-like denticles of enamel and dentine, "Les Ganoides" (e.g., "Esturgeons, Polypteres, Lepisostes, Goniodontes, Silures, Scleroderms, Lophobranches") with thick plates ofganoine and bone, "Les Ctenoides" (e.g., "Mugiloides, Gobiodes, Cottoides, Scienoides, Sparoides, Scorpenoides, Percoides, Pleuronectides, Chaetodontes, Polyacanthes, Aulostomes") having thin plates with comb-like posterior borders, and "Les Cy- cloides" (e.g., "Cyprinoides, Clupes, Salmones, Esocides, Gadoides, Anguilli- formes, Blennoids, Atherines, Scomberoides, Labroides") having thin plates with smooth borders (Agassiz, 1834, in Baudelot, 1873,100 and Patterson 1977,581). Although this classification was short-lived and unnatural, the nomenclature in- troduced by Agassiz has been fully incorporated into ichthyology. Since that time, the use of teleost scale morphology in fish systematics has generally been confined to notations of scales as simply either "cycloid" or "ctenoid," with little or no analysis and comparison of scale structure; with a few notable exceptions, it was widely believed that scales had "limited use in fish systematics" (Van Oosten, 1957,204). Contrary to this view, light microscope studies on scales by Williamson (1851); Baudelot (1873); Timms (1905); Cockerell (1910, 1913, 1914, 1915); Chu (1935); Lagler (1947); Kobayasi (1951, 1952, 1953, 1954, 1955); McCully (1961) and others, have demonstrated their high value in systematic studies, and have contributed significantly to our knowledge of scale morphology. More recently, the use of the scanning electron microscope (SEM) has revealed many new features of scale morphology as well as providing information on scale growth and development. SEM studies by workers such as DeLamater and Cour- tenay (1973,1974) and particularly Hughes (1981) have shown that the complex microstructure of ctenoid scales contains a wealth of potentially valuable, but largely unutilized, phylogenetic information (Johnson, 1984). In addition to their rich information content, scales have great utility in systematic research because 60 ROBERTS: PHYLOGENETIC SIGNIFICANCE OF SPINED SCALES 61 they are usually readily accessible in live, fresh, preserved, and fossilized material. Unfortunately, this utility has not often been realized. Despite the wide use of the term, or perhaps because of it, there is considerable variation in the literature concerning the meaning of ctenoid. Many authors (often implicitly) apply a broad definition of ctenoid to all scales with spine-like pro- jections in the posterior field, with all other scale types being considered cycloid. Other authors apply a much stricter definition which only includes scales with spines that are separate from the scale (e.g., the "true" cteni of Johnson, 1984, and Starnes, 1988). The confusing corollary of ctenoid sensu stricto is that the alternative state of cycloid can include scales with spines (e.g., macrourids, Mar- shall and Iwamoto, 1973, 500, and Iwamoto, 1990, 90; priacanthids, Starnes, 1988, 120; Champsodon and Chiasmodon, Pietsch, 1989). Johnson (1984) rec- ognized the inadequacy of the two terms cycloid and ctenoid, and identified in the Percoidei two basic types of ctenoid scales: "Ct'" (scales with continuous spiny projections from the lateral surface and posterior margin) and "Ct" (scales with separate bony plates, or scalelets, that are continually added with growth). How- ever, these two types of cteni are generally not distinguished in systematic works. Percomorph fishes are ideal subjects for a study of comparative scale mor- phology because of the wide range of spined scale types exhibited together with the problematic nature ofpercomorph classification. The problems in percomorph phylogeny are largely due to the great morphological diversity and the limited num ber of descriptions and analyses of character complexes with which to generate corroborated hypotheses of monophyly, including the Series Percomorpha itself (see Johnson, 1993, and others in this issue). A survey of spined scales by the author began during an investigation into the relationships of the basal percomorph genus Polyprion (Roberts, 1986), and was expanded into a comprehensive broad-based study carried out on the extensive fish collection of the Smithsonian Institution during tenure of a Postdoctoral Fellowship. This paper reports the main results of the study, and shows that scale morphology is a valuable tool in the investigation of percomorph (and teleost) evolution. MATERIALS AND METHODS Scales were removed from the body taking care not to damage the posterior field. Unless otherwise dictated by the condition of the specimen, about six scales were removed from the right side of the body, either above or below the lateral line in the region of the pectoral fin. Lateral line scales and replacement scales were avoided where possible. Scales from recently preserved specimens were chosen in preference to older specimens which often have either damaged scales or an excess of foreign material adhering to their surfaces, although scales from specimens that had been in preservative for over 100 years were prepared successfully. In a pilot study, no difference was found in the quality of scale preparation between scales sampled from fresh or preserved specimens of the percoids Perea flaveseens and Lepomis maeroehirus. Therefore, preserved specimens were used throughout the study. Scales were examined with the light microscope (LM) and scanning electron microscope (SEM). Two types of examination were carried out: cursory study and detailed study. Cursory study was designed to quickly assess and identify scale morphology in a large number and wide phyletic distri- bution of fish taxa, and involved examination of unprocessed scales by transmitted light under a binocular dissecting LM. Detailed study was designed to investigate and identify the different types of spines and scale morphologies in key teleost lineages using both LM and SEM. Fish species sampled and type of scale preparation carried out on them are listed in Appendix I. Methods of scale preparation were initially modified from DeLamater and Courtenay (1974, 142), and involved bleaching in a solution of 9 parts 0.5% potassium hydroxide and I part 3% hydrogen peroxide followed by cleaning in a borax-trypsin solution for 2-5 days, and sonication in an ultrasonic water bath for about 10 sec. Although this initial method produced satisfactory preparations, it was time consuming and, therefore, the following quicker technique described by Hughes (1981), was used routinely for most of the study. Scales were cleaned by immersion in a 1% solution of sodium 62 BULLETIN OF MARINE SCIENCE, VOL. 52, NO. I, ]993 hypochlorite for 5-30 min (Hughes, 1981, recommended using a cold solution, but a solution at room temperature worked equally well). Tissue adhering to both faces of the scale was gently teased off under a dissecting microscope using two small short-bristled nylon paint brushes (natural bristle was quickly damaged by the sodium hypochlorite). Time of immersion was critical because ifleft for too long the scale started to disarticulate. Cleaned scales were washed in 50% ethanol. Scales to be viewed with SEM were partly dried in air and mounted on a numbered aluminum specimen stub using double-sided sticky tape. Drying continued in air and was completed in a vacuum during coating. Curling was reduced by sticking scales on to a stub before they became completely dry, and was less severe when the scales were dried from 50% ethanol, rather than from distilled water or 100% ethanol. When dry, the scales and specimen stubs were sputter coated with gold to a thickness of 25-30 nm in a vacuum of about 40 x 10-3 torr. It was not necessary to coat them with carbon (as recommended by DeLamater and Courtenay, 1974, 142) prior to coating with gold. Scales were viewed
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