The Pharyngeal Bones and Teeth of Catostomid Fishes

Examination of the pharyngeal apparatus of 22 species of catostomids reveals three types of bones and teeth associated with different dietary habits. The mollusk feeders Moxostoma hubbsi and M . carinatum have 21-42 large, molariform teeth on each of the heavy pharyngeal bones. The teeth occlude with a chewing pad borne by the basioccipital and are well-adapted for crushing shells. Most catostomids (other Moxostoma, Cycleptus, Hypentelium, Lagochila, Catostomus, Chasmistes, Erimyzon, Xyrauchen and Minytrema) have 43-90 moderately compressed teeth arranged in comblike fashion on each bone. These species feed primarily on benthic macroinvertebrates including aquatic insect larvas and small mollusks. In addition to mastication, the teeth of this group probably serve to manipulate and hold food during the rejection of inorganic matter inadvertently taken in with the food. The teeth of Ictiobus and Carpiodes are extremely small and numerous (134184)., and the pharyngeal bones are correspondingly delicate. These specle5 are microphagous filtm feeders with a well-developed selectory apparatus consisting of gill rakers, gill arches and palatal organ. The teeth are capable of masticating small food items and may also function as strainers. An analytical key based only on pharyngeal bone and tooth characteristics is provided, and the bones and teeth of several species are illustrated. Catostomid pharynqeal bones and teeth have some limited use in specimen identification. They are usually reliable at the tribe or genus level. In certain trophically specialized forms (Moxostoma hubbsi, M . carinatum and Ictiobus cyprinellus) they are significant at the species level. INTRODUCTION Freshwater fishes of the family Catostomidae, commonly known as suckers, are represented by 11 genera with about 63 species in North and Central America and the single relict genus Myxocyprinus in China. Catostomids probably diverged from a cyprinid ancestor sometime before the Eocene (Uyeno and Smith, 1972). Most are suctorial bottom-feeders with small, extensible, ventroterminal mouths. These fishes lack both oral teeth and a stomach. They do, however, possess pharyngeal teeth arranged in a single row on each of the two pharyngeal bones located posterior to the fourth pair of gill arches. Certain aspects of catostomid morphology are well-documented; for example, osteological information for some species has been provided by Sagemehl (1891 ) , Edwards (1926), Gregory (1933), Nelson (1948, 1949, 1955), Ramaswami (1957), Weisel (1960, 1967a), Branson (1962), Smith (1966) and Smith and Koehn (1971). However, catostomid pharyngeal bones and teeth, of considerable trophic and possible taxonomic significance, have never been adequately treated. Le Sueur (1817) was aware of the existence of catostomid pharyngeal bones and teeth, but only later did ichthyologists begin to recognize the potential taxonomic value of these structures (Agassiz, 1855; Bleeker, 1860; Cope, 1870; Jordan, 1878). More recently, fossilized catostomid pharyngeal bones and teeth have been found in several localities in the southwestern United States (C. L. Smith, 1954, 1958; G. R. Smith, 1963). This family represents the second-most abundant fish group in North American Pleistocene deposits, and most of these fossils are osteologically indistinguishable from living species (Miller, 1965). Therefore, descriptions of pharyngeal structures from Recent species provide valuable information for interpreting material from archaeological (Trautman, 3 957:262) and paleontological (cf. Rutte, 1962, for Old World cyprinids) sites. With the exception of comments by Forbes (1888: 440-441) and Forbes and Richardson (1908 :63-64), the structural diversity of catostomid pharyngeal bones and teeth has generally not been appreciated by ichthyologists, nor has their form in the various species been related to diet or to specializations in ancillary pharyngeal structures. I undertook this investigation to rectify this situation as well as to assess the utility of pharyngeal bones and teeth in specimen identification. All 11 American genera are represented in the study. Special emphasis is accorded to Moxostoma carinatum, Catostomus commersoni and Carpiodes cyprinus because the pharyngeal morphology of each of these species is considered typical of one of the three levels of trophic adaptation seen in the pharyngeal complex. MATERIALS METHODS AND For the most part, the 22 species (135 specimens) used in this study represent a typical Great Lakes assemblage of catostomids (Table I ) . Many were collected from the waters of Minnesota with a 0.25-inch mesh seine. Most of the Moxostoma, Ictiobur and Carpiodes cyprinus were netted in Lake St. Croix, Washington Co., Minn., by a commercial fisherman. Other northern species were borrowed from the James Ford Bell Museum of Natural History at the University of Minnesota. Rare species were obtained from Cornell University (CU) ; Museum of Comparative Zoology, Harvard University (MCZ) ; University of Michigan Museum of Zoology (UMMZ) ; University of Oklahoma Museum of Zoology (UOMZ) ;and National Museum of Natural History, Washington, D. C. (USNM). Pharyngeal bones were removed, thoroughly cleaned of adhering tissue, dehydrated in ethanol, and degreased in acetone. The number of teeth per bone was counted with the aid of a dissecting microscope. Broken and missing teeth were included in the count. In addition, the pharyngeal region was dissected in representatives of all but the rare species (Moxostoma hubbsi, M. valenciennesi, Ictiobus niger, Xyrauchen texanus and Lagoclzila lacera). Most specimens studied were sexually mature adults. Whenever possible, gut contents were examined and major groups of food items were identified. For rare species, however, it was necessary to refer to the literature (Forbes. 1888; Forbes and Richardson, 1908; Carlander, 1969) for dietary information. Illustrations were prepared with the use of a drawing tube attachment on a Wild M-7 stereomicroscope. The pharyngeal bones of some species were too large to be drawn by this method; in such cases, the specimens were photographed and a tracing was made from a print. In order to assure uniformity in illustrative procedures, the bones were positioned so that the surface facing posteriorly in life, Chu's (1935) ventral surface, was nearest the illustrator. I n many species the presence of numerous small, dorsal teeth made it impossible for the illustrations to reflect the correct tooth count as given in Table 1. Illustrations of the most ventral tooth of each species are also provided. Many catostomid teeth bear conical projections or hooks on their anterior (inner) margins; these are subject to wear, however, and are shown only when they are a constant and diagnostic feature in a given species. The catostomid classification used in this paper is that of Hubbs (1930). This was amended by Nelson (1948, 1949) and subsequently employed by Miller (1958). Figures 8-21 are arranged according to this sequence. Skull bone nomenclature is that of Harrington (1955) with the exception that the pharyngobranchials are referred to as infrapharyngobranchials (Nelson, 1969). Weisel's (1960) work on the skull of Catostomus macrocheilus was also helpful. Although the pharyngeal bone nomenclature proposed by Chu (1935) was formulated with respect to cyprinids, it is employed here because it is easily adaptable to catostomid bones. Pharyngeal tissues studied histologically were fixed in 10% formalin with subsequent dehydration in ethanol, clearing in xylene, and embedding in paraffin. Sections were cut to a thickness of 6 pm and then stained with hematoxylin and eosin or Weigert's elastica (for sirnultaneous demonstration of collagen, elastin and muscle). Mounting was in Permount. GENERALANATOMY THE REGION OF PHARYNGEAL The pharyngeal bones and teeth.-Fish teeth are generally involved in the seizing, manipulating, masticating and swallowing of food. Catostomid pharyngeal teeth participate in all but the first of these actions. The teeth are arranged in a single row on each of the two pharyngeal bones. These falcate bones, representing fifth ceratobranchials, are joined at their ventral tips to each other and to ventral gill arch elements by means of a cartilaginous copula. There are only muscular connections between the pharyngeal bones and the skull, vertebral column and pectoral girdle. Cyprinoid pharyngeal teeth are unusual among vertebrate teeth in that the "enamel organs" are of endodermal rather than ectodermal origin, developing from the deeper columnar layer of the pharyngeal epithelium representing the endoderm of the primitive foregut (Edwards, 1929). The crowns of the teeth are probably composed entirely of dentin (Cheprakova, 1958). This material, termed modified dentin by Peyer (1968), functionally substitutes for enamel in most teleost teeth. Bony ankyloses, several millimeters long, unite the crowns to the pharyngeal bone. The ankyloses are partially resorbed by osteoclasts prior to tooth loss and reformed during tooth replacement. ~atostomid pharyngeal teeth are replaced continuously throughout life. Weisel's (196713) study of the form and attachment sequence of the teeth in larval and juvenile Catostomus indicates that the replacement is rapid at these stages of life with at least the first and second generations of replacement teeth resembling the conical hooked teeth of immature cyprinids. .In most catostomids the form of the teeth varies with their position on the bone. The more dorsally situated teeth are generally more distinctly hooked on the anterior (inner) margin than are the ventral teeth. Masticatory activity, however, may sometimes obliterate the hooks. Conversely, recently ankylosed crowns may not have worn sufficiently to exhibit the flat masticatory surfaces characteristic of, for example, the teeth of Moxostoma hubbsi and M . carinatum (Figs. 14-