THE ANATOMY OF THE FEEDING MECHANISM AND THE FOOD HABITS OF MICROSPATHODON CHRYSURUS (PISCES: POMACENTRIDAE)J ALEJANDRO CIARDELLF Institute of Marine Sciences, University of Miami

ABSTRACT The morphology and action of the bones, ligaments and muscles involved in feeding is described. Tooth replacement is explained. The gastrointes- tinal tract is described. An analysis of the food habits is presented. The ecology of the juveniles and adults is discussed in terms of their feeding habits.

INTRODUCTION The yellowtail demoiselle, Microspathodon chrysurus, is an abundant fish in the coral reef environment of southeastern Florida and the Florida Keys. It is widespread through the tropical western Atlantic, extending as far south as Brazil. Reports of its occurrence in Afro-Atlantic waters need confirmation. Microspathodon chrysurus is reputedly an algal browser (Longley, in Longley & Hildebrand, 1941: 186; Jordan & Evermann, 1898: 1565). This is true for the adults, but the juveniles are mainly carnivorous. The juveniles also differ sufficiently from the adults in body color that they were thought by Poey (1875: 102) to represent a distinct species which he named Pomacentrus niveatus. The adults are uniformly dark brown, generally with a yellow caudal fin. The conspicuous juveniles are violet black, with sky-blue spots located mainly dorsally on the body; their caudal fin is transparent. Observations by Walter A. Stark, 11, and Alan Roy Emery (personal communication) indicate that the young remove parasites from other fishes, at least occasionally. Its contribution to the biomass of shallow coral reefs and its seemingly specialized feeding make Microspathodon chrysurus an important subject for study. The anatomy of the feeding mechanism is described in detail, with comments on function, and the diet and ecology of the species are discussed. This study stems from a research program on food habits and feeding mechanisms of coral-reef fishes supported by the National Science Foundation (NSF-GB-1450), C. Richard Robins, principal investigator, and constitutes a technical report from the program. I am especially indebted to Dr. C. Richard Robins, for his advice and encouragement throughout the study and for his editing of the manuscript. I am also indebted to Dr. Frederick M. Bayer and to William N. Eschmeyer, for

1 Contribution No. 844 from the Institute of Marine Sciences, University of Miami. This paper is pan of a thesis which was submitted in partial fulfillment of the degree of Master of Science, Uni- versity of Miami. Cornl Gables, Florida. o Present address: Depto. de Investigaciones Jctiol6gicas y faunisticas, CVM, and Universidad de Carlagena, Cartagena, Colombia. 846 Bulletin of Marine Science [17(4) aid in the preparation of the illustrations and for the review of the manuscript. I thank Drs. Leonard J. Greenfield and C. P. Idyll for sug- gestions concerning the manuscript. I wish also to thank Dr. James C. Tyler of the Academy of Natural Sciences of Philadelphia, for the loan of West Indian specimens. In this study, I have received advice at various times, and help in collecting, from my fellow graduate students. I wish especially to thank Ray S. Birdsong, William P. Davis, and Henry A. Feddern. Special thanks are due to Gregorio Reyes-Vasquez and Charles D'Asaro for the identification of the gastrointestinal contents, and to Dr. Charles E. Lane for confirming the identification of the nematocysts. Dr. Reinaldo Pfaff advised me to come to the University of Miami to study Marine Science, and he has encouraged me throughout the study. I wish to thank Drs. German Covo and Luis H. Arraut of the University of Cartagena for their support, and my family for their encouragement. Through my first three years (1962-65) at the University of Miami, I was supported by the University of Miami which furnished my tuition, and by the University of Cartagena (Colombia) which provided living expenses and books. During the last year (1965-66), I was supported by scholarship No. 8284 from the Pan American Union. Finally, I would like to thank the Person-to-Person Committee of Coral Gables, Florida (Cartagena's sister city) which made it possible for me to study at the University of Miami.

MATERIAL The specimens of Microspathodon chrysurus used in this study are all from the inshore waters of southern Florida and the Bahama Islands. All preserved material is in the collection of the Institute of Marine Sciences, University of Miami (UMML). Additional material from various regions of the western Atlantic was referred to, but was of no direct interest in this study and is not listed below. Preserved material.- The number of specimens and their range in standard length are given in parentheses. UMML 2639 (1, 38 mm) Alligator Reef, Monroe County, Florida; UMML 2933 (4, 37-49 mm) Alligator Reef, Monroe County, Florida; UMML 6435 (7, 19-52 mm) Alligator Reef, Monroe County, Florida; UMML 7234 (2, 34-45 mm) Ajax Reef, Dade County, Florida; UMML 1770 (8, 26-50 mm) S. side of Pigeon Cay, Bahama Islands. Cleared and stained material.-UMML 8877 (2 adults) Alligator Reef, Monroe County, Florida. Material for dissection.-Material for dissection preserved in Vin d'Alsace was from field station CRR-F-374, at Ajax Reef, Dade County, Florida. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 847 Some of this material was destroyed in the course of this study, but the remainder is catalogued as UMML 19841. Non-preserved material.-Freshly-collected, non-preserved material from the large populations of Microspathodon chrysurus at Ajax, Triumph, and Alligator reefs in Dade and Monroe counties, Florida, was used to supple- ment the preserved material, particularly in connection with muscle attach- ments, bone motion, and analysis of stomach contents.

METHODS The illustrations of bones are based largely on the head bones of two large adults, more than 90 mm in standard length, collected at Alligator Reef. The bones of these adults were compared with those of two smaller specimens less than 50 mm in standard length to find morphological differ- ences, but none of importance was found. The material was photographed and the negatives projected onto glass and the image copied. All the bones illustrated are from the left side of the head. A 2-mm scale in each illustration indicates size. The illustrations of the teeth were made by the use of a dissecting microscope with camera lucida. Illustrations of the muscles were made by the use of a dissecting microscope with camera lucida, and by using a Goodkin enlarger. Illustra- tions of the gastrointestinal tract and of the mouth are based on photo- graphs, from which outlines were traced. The stomach and the intestine were removed to facilitate the study of their contents, by means of both dissecting and compound microscope. All measurements were taken with calipers. Measurements of standard length were recorded to the nearest millimeter.

FOOD ANALYSIS Analysis of gastrointestinal contents shows a change in the quality of food ingested by juveniles and adults. Such a change of diet is common in fishes. Hunt & Carbine (1950: 71) recorded as many as three changes in the diet of young pikes. Vasisht (1959) showed a change from carnivo- rous to omnivorous diet for some commercial fishes of the Punjab region, and Robins & Deubler (1955: 14) showed changes in food with age and season for the burbot, Lota Iota lacustris. Gregorio Reyes-Vasquez and Charles N. D'Asaro identified the food items from the stomach and intestines of Microspathodon chrysurus. These contents are analyzed below. I. Diatoms: a. Planktonic: Amphiprora, Asterionel/a, Coscinodiscus, Cymbel/a, Diploneis, Eunotia, Leptocylindrus, Melosira, Navicula, Nitzschia, Pleurosigma, Rhabdonema, Skeletonema, Synedra, Triceratium, Thalassiotrix, Tropidoneis. 848 Bulletin of Marine Science [17(4) TABLE 1 FREQUENCY OF OCCURRENCE OF FOOD ITEMS IN GASTROINTESTINAL CONTENTS OF Microspathodon chrysurus BY SIZE CLASS1 Standard length (mm) 40 40-80 80 Sample size (Nos. of fish) 15 14 13 Diatoms a. Pelagic 0(0) 7 (50) 10(77) b. Epontic 0(0) 6 (43) 9 (69) Chlorophyceae 4 (27) 1 (7) 4 (30) Cyanophyceae 2 (13) 3 (21) 9 (69) Rhodophyceae 2 (13) 3 (21) 5 (38) Dinoflagellates 1 (7) 5 (36) 4 (30) Zooxanthellae 6 (40) 7 (50) 0(0) Nematocysts 10 (67) 8 (57) 0(0) Unidentified animal food 2 (13) 2 (14) 8 (61) Sand, spicules, etc. 2 (13) 3 (21) 5 (38)

1 Numbers indicate number of individuals in which the food item was found (per cent frequency of occurrence is given parenthetically). Although the Zooxanthellae are dinoflagellates, they were sep- arated as a food item because of their symbiotic relations with corals.

b. Epontic: Amphora, Climaeosphenia, Grammatophora, lsthmia, Lie- mophora, Mastogloia, Striatella, Surirella, Tropidoneis. The term epontic (epi = on, ontos = being) is used here as defined by Wood (1965: 4). 2. Chlorophytes: unicellular and filamentous. 3. Cyanophytes: filamentous. 4. Rhodophytes: filamentous. 5. Dinoflagellates: Great numbers of Zooxanthellae were found in the juveniles. 6. Animal food: mainly copepods and some red gelatinous matter in the adults, and nematocysts in the juveniles. 7. Sand, Foraminifera, sponge spicules, teeth of Sagitta. As is shown by Table 1, the main materials found in the gut of juveniles are nematocysts and Zooxanthellae. This leads the author to believe that their principal food is the hydrozoan Millepora, though anthozoans may be ingested (see section on ecology, below). The adults eat large amounts of blue-green algae (cyanophytes), showing some selectivity in the choice of their food. However, if there is any other kind of food available in large amounts they will ingest it. This is shown by the fact that some specimens contained large quantities of planktonic diatoms of the genus Asterionella, which they probably ingested during a planktonic bloom of this diatom. Two specimens were found with their stomachs full of a gelatinous matter of animal origin. This matter was elongate, red, and contained a number of copepods and other small crustaceans. Other 1967J Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 849 specimens had ingested large numbers of copepods. The large numbers of specimens in which some animal food occurs, and the large amount of animal food found in three specimens, indicate that this material is not accidentally ingested. Coral fragments and other hard material varying from three to five millimeters in diameter were found in the oral cavity of many specimens, but not in the gastrointestinal tract. This suggests the existence of a selective mechanism that eliminates such particles from the food. Probably this mechanism is operated by the action of the pharyngeal apparatus.

NOTES ON THE FEEDING ECOLOGY Corals are an important part of a reef community (Odum & Odum, 1955: 297). Hiatt & Strasburg (1960: 113) noted that it would be strange if some provision had not been made to take advantage of this food source. They found during the course of their study of Pacific reefs that some species of fishes of the families Chaetodontidae, Scaridae, Balistidae (including Monacanthidae), and Tetraodontidae are coral eaters. The species of the family Pomacentridae that they examined were found to be omnivorous or herbivorous, but they did not list any of them as being a coral eater. The author has found that the juveniles of Microspathodon chrysurus are specialized coral eaters. The morphology of tooth attachment in the upper jaw of Microspathodon chrysurus is very similar to that described by Norris & Prescott (1959: 276) for Girella nigricans and, as they point out (p. 282), such structure appears to be a complex adaptation for grazing and scraping. Further specialized adaptations in Microspathodon chrysurus are the pads located in front of the oral valve and at the comers of the mouth (Fig. 29). These pads may be used to discharge the nematocysts of the coral polyps. Although Hyman (1940: 386) points out that the nematocysts can be used as a basis for the identification of the coelenterates, no existent key suffices for this purpose. However, direct comparison of the nematocysts from the gastrointestinal contents with those of Millepora, and with the figures of nematocysts shown by Hyman (J940: 384) and by Weill (1934a & b), suggests that most are from Millepora. Although according to Yonge (1930: 54), only a few corals seem to extend their polyps during the day, and although Hyman (J 940: 450) notes that Millepora feeds at night, field observations show that they extend their polyps during the day. This may explain the selective association of the juveniles of Microspathodon chrysurus with Millepora, and also their shallow-water distribution, since, as can be seen from the studies of Almy & Carri6n- Torres (1963), Goreau (1959), Storr (1964), and Wells (1957), Millepora is a shallow-water genus. 850 Bulletin of Marine Science [17(4)

FIGURE 1. Microspathodon chrysurus. Anteroventral view of the premaxilla.

Apparently only the juveniles of Microspathodon chrysurus eat corals, since no nematocysts have been found in the adults. The adults are vegetarians, though they will take animal food occasionally. The adult selects its food from rocky areas, using the upper jaw. Here the mobility of the teeth is of use, since it allows the teeth to follow the irregularities of the rock's surface. The adults can also select bottom food, as can be inferred from the amounts of sand, sponge spicules, and Foraminifera found in the gastrointestinal contents. In feeding on the bottom, they take advantage of the shape and immobility of the teeth in the lower jaw, since they use it in very much the same way that a grab is used. From the analysis of gastrointestinal contents, it seems that the adults especially select blue-green algae (Cyanophyceae). Since the distribution of algae is related directly to the wave length of the light (Engelman, discussed in Wald, 1959: 99), and to the type of substrate (Gilmartin, 1960: 210), these two factors probably determine, at least in part, the ecological dis- tribution of the adults. In Florida waters, the adults of Microspathodon chrysurus occur mainly in shallow waters on reefs and in the rocky and sandy areas that surround the reefs.

DESCRIPTION OF BONES Premaxilla.-(Figs. 1, 2, 18, 21, 26, 28.) The premaxilla is a lamellar bone with the ventral surface concave and the dorsal convex (Figs. 1, 2). The 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 851

FIGURE 2. Microspathodon chrysurus. Posterodorsal view of the premaxilla. ventral concavity is closed to the lateral end (Fig. 2). Mesially, a small lamellar surface projects ventrally (Figs. 1, 2); the rest of the concavity is open mesially (Figs. 1, 2). The posterior surface of the concavity presents a series of ridges. The anteroventral surface of the convexity bends posteriorly and also presents a series of ridges (Fig. 1). The dorsal surface is thick, becoming thinner towards the anterior and posterior edges so that the edges are almost transparent. On the dorsal surface, mesially, and almost immediately posterior to the anterior edge is located the sharply pointed ascending or nasal process (Figs. 1, 2, 18, 26). It is narrow anteriorly, and is about six times wider from front to back than from side to side. Dorsally it has a posterior mesial concavity (Fig. 1), and an anterior convexity (Fig. 2), looking like the mirror image of an "S." The length of the ascending process is about one-half the distance from the base of the process to the posterior end of the premaxilla. Posterior to the ascending process and for about one-third the length from the base of the process to the posterior end of the premaxilla is located a swollen surface (Fig. 2), oval in shape, whose mesial end coincides with the bending of the dorsal surface (Fig. 2). Dorsally, this protrusion extends slightly above the level of the dorsal surface to form a concavity in front of the ascending process (Fig. 1); this swollen surface occupies three- quarters of the posterior part of the premaxilla (Fig. 2). At the posterior end of the premaxilla, there is, dorsally, a triangular process, which starts sharply at about the quarter mark along the pre- maxilla, and diminishes gradually towards the posterior end of the bone (Figs. 1, 2). 852 Bulletin of Marine Science [17(4)

FIGURE 3. Microspathodon chrysurus. Dorsoanterior view of the maxilla.

The ventral fossa of the premaxilla houses connective tissue that In turn bears the teeth (Figs. 18, 21); the teeth do not attach directly to the bone. Maxilla.-(Figs. 3, 4, 21, 22, 28.) The maxilla is elongated, twisted, and can be divided into two sections at the level of a small dorsal process situated at about one-third the way from the anterior (mesial) end (Fig. 3). The first section, situated anteriorly and mesially, is broad and sheet-like, but curved anteroposteriorly to form a ventral concavity (Fig. 4), and a dorsal convexity (Fig. 3). From above, it is roughly quadrangular, with the anterior side longer than the posterior (Fig. 3). Anteriorly it has an expanded surface, whose edge is almost circular in shape. This surface extends from the mesial plane about one-third the length of the maxilla (Fig. 3), and turns dorsomesially slightly laterad to the small dorsal process (Fig. 3), to join the main body of the bone ventrally at the level of the small dorsal process (Fig. 3). On this anterior surface, mesially, is located a thin transparent concavity in the shape of two-thirds of an ellipse. This transparent area is situated about one-half the way from the ventral edge of the maxilla (Figs. 3, 4), and against this area abuts the anterior end of the palatine (Fig. 28). Starting at the mesiodorsal end of the transparent concavity, a thicker area arises, triangular in shape, rounded anteroposteriorly, and divided by the height of the triangle into two almost equal surfaces, the mesial surface being higher (Fig. 3). The lateral side of this triangle drops sharply to form a triangular concavity, one vertex of which ends shortly before the small dorsal process of the 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 853

FIGURE 4. Microspathodon chrysurus. Ventroposterior view of the maxilla. maxilla; the anterior vertex ends almost at the point in which the first triangle described arises (Fig. 3). The posterodorsal surface ends in a roughly teardrop-shaped process (Fig. 4). The second section of the maxilla extends laterally and is slightly arched from above (Fig. 3). It is thick, almost round, with a terminal lamellar surface that forms a posterior concavity (Figs. 3, 4); this surface extends ventrally in mesial direction to end at the level of the small dorsal process. Dorsally, it extends mesially about one-third the way from the dorsal process to the lateral end, ending mesially in a small process that bends in a lateroposterior direction (Fig. 3). The maxilla overlies the premaxilla at the level of the lateral end of the posterior swollen surface of the premaxilla (Fig. 28). Dentary.-(Figs. 5, 6, 21, 23-27.) The dentary is elongate, shaped like the mirror image of an "L," and tubular; it can be divided at the level of the angle into a lateromesial and an anteroposterior section or dentary process, the first being wider and thicker than the latter. Dorsally, both parts bear teeth. The lateromesial section has a deep ventral concavity (Figs. 5, 20), on the posterior part of which the teeth are situated (Figs. 5,6,20,21,23-27). Ventrolaterally on the anterior surface of the bone are located a series of orifices (Fig. 5); these are the preoperculo-mandib- ular pores. Dorsolaterally, another orifice (Fig. 5) opens to a large cavity situated ventrolaterally (Figs. 5, 6, 27); this cavity extends slightly into the lateromesial section, forming on the anterior surface of the bone 854 Bulletin of Marine Science [17(4)

FIGURE 5. Microspathodon chrysurus. Anterolateral view of the dentary. a rather round swollen surface, with a mesial depression. The mandibular pores are situated immediately mesial to this depression. The swollen surface slopes very gradually dorsally, and disappears at the level of the dorsal orifice (Fig. 5). The concavity situated ventrolaterally opens posteriorly (Fig. 6). A process that is directed posteriorly is located ventromesial to the concavity (Figs. 5, 24, 25, 27). The articular (Figs. 21, 23-25) joins the space between this process and the dentary process, which is tubular in shape. The teeth located on the dentary process are smaller than those of the lateromesial section. Articular.-(Figs. 7, 21, 23-25.) The articular is flattened in cross section, and nearly quadrate when observed from the side (Fig. 7), with the longest edges directed anteroposteriorly and the shortest ventrodorsally, the pos- terior one being rounded and the anterior one having a ventroanterior inclination. The mesial surface of this process has a shallow concavity, situated posteriorly, which serves as the area of attachment for two branches of the adductor mandibulae (Figs. 24, 25). Anterior to the area of muscle attachment, the mesial surface of the articular is concave and receives the posterior ventromesial process of the dentary (Figs. 21, 25). The dorsal edge of the articular's process receives the ventral edge of the dentary process. The angular is fused to the anterior part of the articular (Fig. 7). A concavity located ventrally provides for the articulation of the condyle of the quadrate. The angular is pyramidal in shape and projects mesially and ventrally from the articular (Fig. 7). Palatine.-(Figs. 8,21,28.) The palatines are thick, tubular bones, arched 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 855

FIGURE 6. Microspathodon chrysurus. Posteromesial view of the dentary. in shape, with the ventral edge smooth and nearly semicircular in outline, and the dorsal edge three-sided. The three sides of the dorsal edge are unequal, the anterior being the longest, the posterior the shortest. The ventral end of the palatine is more mesial and thicker than the anterior end which articulates with the elliptical concavity situated on the anterior surface of the maxilla (Figs. 21, 28). Ventrally, the palatine has three projections: the first is small; the second is thick, short, and articulates ventrally with the parethmoid and the vomer at the point of contact of those two bones; and the third is long and directed lateroventrally (Fig. 8) to articulate with the quadrate in the H-shaped process of that bone (Fig. 9). The dorsal edge has two shallow, posterodorsal concavities (Fig. 8); these serve as contact points for a special notch of the parethmoid (Figs. 21, 28). Quadrate.-(Fig. 9.) The flattened quadrate is roughly triangular. Dor- sally, the quadrate is united to the pterygoid, and posteriorly to the symplectic. Anteroventrally, the quadrate has a large round condyle (Fig. 9) for the articulation with the ventral concavity of the articular (Fig. 8); this articulation was illustrated by Gregory (1933: 254, Fig. 128). The anterior dorsal part of the quadrate has an H-shaped process (Fig. 9) that receives the posterior ventral part of the palatine as noted above. Symplectic.-(Fig. 9.) The nearly circular and flattened symplectic is situated posterior to the quadrate, and ventral to the pterygoid and metapterygoid, and is united to them. Posteriorly, it is in contact with the hyomandibular. The symplectic has an almost central orifice. 856 Bulletin of Marine Science [17(4)

FIGURE 7. Microspathodon chrysurus. Mesial view of the articular.

Metapterygoid.-(Fig. 9.) The metapterygoid is lamellar, and shaped like a cleaver whose handle points ventrally to contact the symplectic. Ante- riorly, the metapterygoid connects with the pterygoid. The posterior edge is in contact with the hyomandibular. Pterygoid.-(Fig. 9.) The pterygoid is quadrangular in outline, with a dorsal depression at the level of the H-shaped process of the quadrate. The ventral edge is in contact with the symplectic, the anterior with the quadrate, and the posterior with the meta pterygoid. Its anterodorsal end contributes to the dorsal formation of the H-shaped articulation of the quadrate for the palatine. Hyomandibular.-(Fig. 10.) The elongate hyomandibular is slightly arched anteriorly. Its dorsal end is provided with two articular heads by which the entire jaw and hyal apparatus attaches to the skull. The anterior of the two condyles articulates with the sphenotic, the posterior with the pterotic. On the mesial surface of the hyomandibular, at about one-third the way from the dorsal end, a third head articulates with and supports the opercular bone. Laterally and externally, the hyomandibular presents two flat surfaces separated by a ridge. The anterior surface is enlarged dorsally, and supports over most of its area branches of the adductor mandibulae, as does the posterior surface. The posterior surface has an opening toward its ventral end. A spiny process that projects dorsally and posteriorly near the dorsal end of the hyomandibular provides an attach- ment site for the adductor arcus palatini. The anteromesial surface is larger at its dorsal edge, becoming more inclined towards the mesial plane; 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 857

FIGURE 8. Microspathodon chrysurus. Mesial view of the palatine. this surface is almost transparent. The posterior edge of the hyomandibular bears the preopercular bone. Anteriorly and ventrally the hyomandibular joins the metapterygoid, symplectic, and quadrate. Gregory (1933: 254, Fig. 128) illustrated the relationships of the hyomandibular to the surround- ing bones. Vomer.-(Fig. 11.) The vomer is elongate, and may be divided for convenience into an anterior head and a posterior shaft. The dorsal surface of the head is attached to the parethmoid. The head is triangular when viewed from above. Its lateral surface curves outward to form a shield that is concave posteriorly. The lateral edge of the shield has dorsally a posterior sharp projection at each ventral corner. One of the ventral processes of the palatine joins the posterior concave surface of the shield. The ventral surface of the vomer lacks teeth, but its head is slightly concave to receive the tongue when it is pressed dorsally. Preopercle.-(Fig. 12.) The preopercIe is scythe-shaped, essentially flat- tened laterally, but with a raised flange that runs along the middle of the lateral surface for nearly the entire length of the bone. This flange houses posteriorly the preoperculomandibular sensory canal. Anterior to the flange, the lateral surface is very flat and receives the posterior edge of the hyomandibular. The ventral leg of the preopercIe attaches to the quadrate. Glossohyal.-(Fig. 13.) The glossohyal can be divided into two sections. The first is situated on the mesial plane, and the second, flattened, section extends laterally in the floor of the mouth. There is a small round cartilage anteriorly (not shown in Fig. 13). In plane view, the glossohyal resembles 858 Bulletin of Marine Science [17(4)

FIGURE 9. Microspathodon chrysurus. Lateral view of the quadrate, symplec- tic, metapterygoid, and pterygoid. an arrowhead; in lateral view, it is arched toward the anterior end which projects into the mouth and provides support for the tongue. Urohyal.-(Fig. 14.) The urohyal is bladelike, triangular in outline, with its anterior edge rounded. Anterodorsally it has two winglike projections that end in a sharp point. Two other small processes, rectangular in outline, start at the base of the lateral projections and extend dorsally; they enclose a U-shaped concavity. To them and to the concave area immediately behind them attaches the glossohyal. The dorsal edge of the urohyal has two concavities, the first being smaller than the second. The anterior edge extends dorsoventrally and has an indentation towards its lower end. The curved anterior edge has a bladelike lateral projection along all but its posterior end. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 859

FIGURE 10. Microspathodon chrysurus. Lateral view of the hyomandibular. 860 Bulletin of Marine Science [17(4)

FIGURE 11. Microspathodon chrysurus. Ventral view of the vomer.

Epihyal.-(Fig. 15.) The epihyal is broad, roughly triangular in outline, and joins anteriorly the ceratohyal. The interhyal attaches to the posterior dorsal end of the epihyal and is responsible for the suspension of the entire hyal apparatus. The lateral surface (which is inclined so that it points somewhat ventrally) of the epihyal has a concavity on its dorsal third. Below this concavity are located the posterior two branchiostegal rays. Ceratohyal.-(Fig. 15.) The ceratohyal is broad and elongate. Posteriorly it is attached to the epihyal, and anteriorly and dorsally it is attached to the basihyal. Posteriorly, the ceratohyal is expanded ventrally; this ventral projection is concave laterally, and below it attach the third and fourth branchiostegal rays. The anterior two branchiostegal rays are reduced in size and attach to the shaft of the ceratohyal. A groove runs posteriorly along the dorsal part of the lateral face of the ceratohyal, originating on the epihyal and ending in an opening through the basihyal. Basihyal.-(Fig. 15.) The basihyal is triangular in outline, with a dorsal projection at its base. Because of the downward tilt of the hyal series, this projection that originates anteromesially fits under the wings of the anterior end of the urohyal. Lower Pharyngeals.-(Fig. 16.) Most fishes have paired lower pharyn- geals, but in Microspathodon chrysurus, as in all of the pomacentrids, the lower pharyngeals are fused basally. In this, they resemble the closely related cichlids, except that the cichlids retain the median suture. The labroids also have fused pharyngeals (Jordan & Evermann, 1898: 1571), but they are of a very different type. In Microspathodon chrysurus the 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 861

FIGURE 12. Microspathodon chrysurus. Lateral view of the preoperc1e. fused lower pharyngeal is Y-shaped, with the single arm of the "Y" directed anteriorly and the paired arms directed lateroposteriorly. At the union, the fused lower pharyngeal is broad and roughly triangular in outline. The paired arms are flattened distal to the point of union. The anterior or basal arm does not bear teeth. Small canine teeth are attached to the triangular area and are continuous with the single row of teeth along the dorsal surface of each lateral arm. Jordan (1907: 28) termed such teeth cardiform. Upper Pharyngeals.-Three bones form the upper pharyngeal complex. As a unit, they are elongated and directed lateromesially, with a posterior inclination of approximately 45\ the lateral end being broader. The lateral bone has a small process, which is located dorsoanteriorly and is pyramidal in shape. It joins the central bone on its mesial surface. 862 Bulletin of Marine Science [17(4)

FIGURE 13. Microspathodon chrysurus. Ventral view of the glossohyal.

The central bone has two small mesial processes, tubular in shape, on its dorsal surface; they are separated from the pyramidal process of the lateral bone by a concavity. The third and most mesial bone starts at the level of the paired processes, is cylindrical in outline, and extends anteromesially a short distance, ending in a dull point. The teeth attached to the ventral surface of the upper pharyngeal complex are cardiform.

FIGURE 14. Microspathodon chrysurus. Lateral view of the urohyal. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 863

FIGURE 15. Microspathodon chrysurus. Anterodorsal view of the epihyal, ceratohyal and basihyal.

DESCRIPTION OF TEETH Teeth.-(Figs. 17-21, 23-26.) The teeth of the upper jaw differ from those of the lower jar in structural details, as well as in size. However, I cannot agree with the statement of Jordan & Evermann (1898: 1567) that the teeth of the lower jaw are twice the size of those of the upper

FIGURE 16. Microspathodon chrysurus. Dorsal view of the fused lower pharyngeals. 864 Bulletin of Marine Science [17(4)

FIGURE 17. Microspathodon chrysurus.-a & c, premaxillary tooth: a, posterior view; c, lateral view.-b & d, dentary tooth: b, posterior view; d, lateral view. jaw; the teeth of both jaws are approximately of the same size, as is shown in Figure 17, in which they are drawn at the same scale. All of the jaw teeth are incisors. Jordan (1907: 24) stated that such a dentition indicates a diet of crustaceans or snails; Norman & Greenwood (1963: 29) indicated that such a dentition is used for a mixed diet; neither supposition applies very well to Microspathodon chrysurus (see section on food above). Premaxillary Teeth.-(Figs. 17a, c; 18b; 19; 21; 26.) The distal end of each tooth is divided into two approximately equal zones (Fig. 17a). The terminal zone is brown, elongated lateromesially, and ends anteriorly in a sharp edge (Fig. 17c). The second zone is yellowish, and is rounded in cross section (Fig. 17a, c). Basally from this zone, the tooth's surface is

a

o •

FIGURE 18. Microspathodon chrysurus. a, frontal view of the premaxilla (dots show position of teeth, with larger dots indicating the teeth shown in b); b, mesial view of the premaxilla, showing position of teeth. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 865

FIGURE 19. Microspathodon chrysurus. Position of the teeth of the premaxilla when they are to be replaced (lower tooth about to be shed). expanded so that it is T-shaped in cross section. This narrow ventral ridge extends basally for about half the tooth's length, where it ends in a ventral, small process (Fig. 17a, c). From the process basally, the tooth is ovoid in cross section. Laterally, the anterior edge of the tooth is convex (Fig. 17c). Posteriorly it is triple concave. The tooth's cutting surface is bent posteriorly. Dentary Teeth.-(Figs. 17b, d; 20; 21; 23-27.) Compared to the pre- maxillary teeth, the dentary teeth are wider, and they are provided with a posterior ridge that is larger than the ventral ridge of the premaxillary teeth, traversing most of the tooth. The ridge has a sharply pointed process near the midpoint of the tooth (Fig. 17d). In lateral view, the posterior edge of the dentary tooth has four concavities (Fig. 17d). The anterior edge of the tooth is more evenly convex.

NOTES ON THE POSITION AND REPLACEMENT OF TEETH Position and Replacement on the Premaxi/la.-(Figs. 18, 19, 21, 26.) The teeth are imbedded in connective tissue, and arranged in a semicircle. The

FIGURE 20. Microspathodon chrysurus. Position of the growing teeth in the dentary. 866 Bulletin ot Marine Science [17(4) tissue is continuous across the premaxillary symphysis. The manner of protrusion of the premaxillary teeth is shown in Figure 18b. The teeth start growing at the anterior surface of the premaxillary concavity, and grow in a posteroventral direction (Fig. 18b) until they replace the older teeth, the tip finally protruding through the anterior edge of the premaxillary tissue. This direction of growth is completely different from that described by Norman & Greenwood (1963: ] 02) for sharks, and from that described by Eaton (1935a: 162, Fig. 2) for the loricariid fish, Plecostomus. In Plecostomus, the teeth grow in a postero-anterior direction-an out-folding. Apparently, not all the teeth in Microspathodon chrysurus are shed simultaneously; the position of several teeth representing apparent stages of replacement can be seen in Figure ] 8a. The arrangement suggests a certain regularity in tooth replacement. Figure ]9 shows the position of a tooth that is about to replace an older one. The replacement of premaxillary teeth just described for Microspathodon chrysurus is similar to that described for the premaxillary teeth of Cire/La nigricans by Norris & Prescott (1960: 276). They also pointed out that this type of tooth replacement is found in Microspathodon bairdi (an east- ern Pacific relative of M. chrysurus) and in Ophioblennius steindachneri (a blenny). Position and Replacement ot Teeth on the Dentary.-(Figs. 5,6,20,23-27.) The dentary bone has two sets of teeth. The anterior ones, located on the ventra] concavity of the dentary, adjoin the bone basally from the sharply pointed ventral process of the teeth; these teeth are illustrated in Figures ] 7b, d, and 20. The teeth situated on the dentary process are continuous with the anterior ones, are conic basally, and have the conic section inserted in special sockets of the bone itself; they are apparently fixed teeth, and whether they are replaced, is unknown. The cutting surface provided by the dentary teeth is U-shaped. The growing tooth originates at the base of the old tooth (Fig. 20), and the dorsal surface of the tooth extends first anteriorly and then dorsally (Fig. 20). As on the premaxilla, teeth are not replaced all at the same time, but periodically, as shown by the growing teeth in Figure 20. A tooth broken or lost through accident apparently is replaced rapidly.

MUSCLES The morphology of the muscles of the cheek varies with the species of fish studied, as shown by Souche (1932a, b, c, d, e, f, g, & h; 1933; 1935a & c; 1936) for more than three hundred species of fishes; furthermore, the adductor mandibulae may have only two branches as shown by Thomas (1956: 17) for Hilsa ilisha, or can be very branched as shown by Tchern- avin (1953: 48) for Chauliodus s/oani. The adductor mandibu/ae has 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 867

FIGURE 21. Position of premaxilla, maxilla, palatine, dentary, articular, levator arcus palatini (a), adductor mandibulae: maxillaris (b), adductor mandibulae: mandibularis (c), adductor mandibulae: Al (d), and adductor mandibulae: A2 (e). four branches in Microspathodon chrysurus; these branches are described below. A cheek muscle termed pterygo-maxillaire, that has been studied by Souche (1932b, d; 1935b) in several fishes, is absent in Microspathodon chrysurus. Levator Arcus Palatini.-(Fig. 21a.) This muscle is short, square, and covered by a thick layer of connective tissue between the muscle and the skin. It is situated immediately posterior to the eye and occupies the space between the sphenotic, on which it originates, and the heads of the hyo- mandibular, on which it inserts. Its fibers are directed dorsoventrally. Its contraction, as indicated by Girgis (1952: 299) and AI-Hussaini (1949: 115), raises the hyomandibular, using its heads as a fulcrum; thus it becomes possible for other bones to enlarge the mouth cavity. Its main function is to participate in the complex movements of swallowing. 868 Bulletin of Marine Science [17(4)

FIGURE 22. Microspathodon chrysurus. Insertion of the maxillaris muscle on the maxilla.

Adductor Mandibulae: Maxillaris.-(Figs. 2Ib, 22.) It is a thick tri- angular muscle, situated superficially, immediately under the skin of the cheek. This muscle originates on the dorsolateral surface of the preopercle and partially on the hyomandibular, and occupies the space between the ventral surface of the suborbital bones and the inner part of the preopercle (Fig. 21b ). It is completely separated from the adductor mandibulae: mandibularis which runs along its ventral edge. The general placement of the maxillaris is seen in Figure 21. It is thicker anteriorly, where it is round in cross section, while posteriorly, toward its origin, it is thinner and more elliptical in cross section. The anterior part ends in a strong aponeurosis that inserts in the posteroventral surface of the lateral part of the maxilla (Fig. 22). Contraction of the maxillaris turns the maxilla down by pulling it back (see discussion of mechanical action, below). Adductor Mandibulae: Mandibularis.-(Figs. 21c, 23.) This portion is thick, almost rectangular in outline, with the posteroventral angle

FIGURE 23. Microspathodon chrysurus. Insertion of the mandibularis muscle on the dentary. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 869

FIGURE 24. Microspathodon chrysurus. Insertion of the A] muscle on the articular. rounded. It occupies the space left between the maxillaris and the outer part of the preopercle. It originates in the surface formed by the angle of the preopercle and partially on the hyomandibular. Its dorsal limit runs parallel to the ventral limit of the maxillaris; the ventral limit is partially covered by the lateral part of the maxilla, and runs in ventrodorsal direction. The mandibularis is thinner than the maxillaris. Its dorsoante- rior vertex ends in a strong aponeurosis which is attached laterally to the dentary process on its posterior lower surface, near its point of contact with the articular (Fig. 23). Contraction of the mandibularis lowers the poste- rior part of the dentary process, and raises the anterior part, pushing its teeth against the premaxillary teeth. Adductor Mandibulae: A].-(Figs. 2Id, 24.) This muscle is fan-shaped and occupies the space between the mesial surfaces of the maxillaris and mandibularis, and the lateral surface of the adductor mandibulae: A 2'. It originates on the lateral surface of the hyomandibular, and inserts by way of an aponeurosis on the upper part of the mesial concavity of the posterior section of the articular (Fig. 24). Anteroposteriorly, it overlaps in part the levator arcus palatinus (Fig. 21). Its dorsal limit is the circumorbital flange; its anterior limit is slightly anterior to that of the mandibularis.

FIGURE 25. Microspathodon chrysurus. Insertion of the A2 muscle on the articular. 870 Bulletin of Marine Science [17(4)

The fibers of the adductor mandibulae: Al and A:l anastomose at their point of contact. Contraction of Al rotates the articular, raising the dentary, and closing the mouth.

Adductor Mandibulae: A2.-(Figs. 21e, 25.) This muscle is fan-shaped, and it is thicker dorsally than ventrally. It occupies the space between the mesial surface of the adductor mandibulae: Al and the lateral surfaces of the adductor arcus palatini. Its ventrolateral surface contacts the lateral surfaces of the metapterygoid, pterygoid, symplectic and quadrate; it is ventral to the circumorbital series. A2 originates on the mesioanterior surface of the hyomandibular, and inserts by way of a strong aponeurosis on the lower part of the mesial concavity of the posterior section of the articular. Its action is the same as that described for Al' Adductor Arcus Palatini.- This muscle occupies the space between the mesial surface of the adductor mandibulae: A:l and the ventral surface of the parasphenoid. It is situated under the subocular shelf, and extends for the whole length of it in posteroanterior direction. It is composed of three branches situated in succession, the largest being the middle one. The first one, the palatine of Takahashi (1925: 25), originates in the ventrolateral surface of the parasphenoid; it inserts on the lateral surface of the pterygoid, and on the posteroventral surface of the palatine. The middle branch, the pterygoid of Takahashi (1925: 25), originates on the ventrolateral surface of the parasphenoid and inserts on the dorsolateral surface of the pterygoid and metapterygoid. The posterior branch, the hyomandibular of Takahashi ( 1925: 25), originates in the ventrolateral surface of the parasphenoid and inserts at about the midpoint of the edge of the mesial surface of the hyomandibular. The fibers of the hyomandibular branch run in antero- posterior direction. The fibers of the pterygoid branch run in dorsoventral direction, changing slowly to acquire a posteroanterior direction. The fibers of the palatine branch run in an anteroventral direction. Mesially, this muscle is covered by the tissue that lines the oral cavity. This muscle thus forms part of the dorsal wall of the oral cavity. Its contraction raises the bones of the palatine arc that connect to the hyomandibular, thus enlarg- ing the oral cavity. Geniohyoideus.-(Figs. 26a, b.) This muscle is located laterally on the ventral side of the head. It originates at the ventral edge of the anterior concavity of the epihyal and ceratohyal (Fig. 26), and on the second branchiostegal ray. It is trapezoidal in outline and is directed anteromesially (Fig. 26a), and finally anteriorly (Fig. 26b). It inserts anteriorly by way of a strong aponeurosis in the ventromesioposterior part of the dentary (Figs. 26, 27). In cross section, the geniohyoideus is semicircular, being deepest mesially. Its contraction lowers the dentary, thus opening the mouth. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 871

FIGURE 26. Microspathodon chrysurus. a = the mesioanteriorly directed por- tion of geniohyoideus muscle; b = the posteroanteriorly directed portion of geniohyoideus muscle; c = the central pad (note the position with respect to premaxilla and vomer); d = the ligament that unites the ascending process of the premaxilla to the dermethmoid bone.

CARTILAGE AND LIGAMENTS OF THE PREMAXILLA The ascending or nasal process of the premaxilla, viewed from the front, is covered, starting at its base and extending for all its length, by a hemispherical cartilage, the dermethmoid cartilage; the flat surface of the cartilage is against the mesial plane. From a dorsal view, it can be seen that the dermethmoid cartilage prolongates posteriorly to contact the dermethmoid bone (Fig. 28). Posteriorly, the cartilage covers a ligament (Fig. 26d) that links the ascending process of the premaxilla with the deep part of the dermethmoid bone. A similar, but single, ligament in cyprinids is called the rostral or sigmoid ligament by Eaton (1935b: 167) and Harrington (1955: 281). Four other ligaments attach to the dermeth- maid cartilage, two on each side. A fifth ligament runs along the front edge of the cartilage and connects to the dorsoposterior surface of the palatine on each side (Fig. 28); this is the thickest ligament associated with the dermethmoid cartilage. Of the two other ligaments on each side, 872 Bulletin of Marine Science [17(4)

FIGURE 27. Miscrospathodon chrysurus. Insertion of the geniohyoideus on the dentary. the first originates from the posteroventral part of the dermethmoid cartilage and inserts ventrolaterally on the anteroventral part of the palatine (Fig. 28). The second ligament originates at approximately the same place on the dermethmoid cartilage, but is directed posterolaterally, inserting on the parethmoid bone slightly above the articular notch for the palatine (Fig. 28).

MECHANICAL ACTION OF THE JAWS Connections and Relations of the Bones.-Each premaxilla is connected to the maxilla by very strong tissue located mainly on its dorsal surface. This type of connection allows the premaxillae to have some movement. Their position is illustrated in Figure 28. Each maxilla connects in a rather loose way to the anteroventral part of the palatine, and is held in place by connective tissue; this type of connection allows the maxillae to pivot around the point of contact. Their position is illustrated in Figure 28. The articular is held firmly in place by strong connective tissue situated

FIGURE 28. Microspathodon chrysurus. Ligaments of the upper jaw. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 873

FIGURE 29. Microspathodon chrysurus. Positions of the pads in the mouth. within the posterior concavity of the dentary. Inside this concavity is also found Meckel's cartilage (see Figs. 23-25). The ventral concavity of the articular articulates with the condyle of the quadrate and is held in place by connective tissue. The quadrate is situated peculiarly in Microspathodon chrysurus. This was illustrated by Gregory (1933: 254, Fig. 128), who also discussed this peculiarity, stating (p. 255): "The position of the quadrate-articular joint in Microspathodon is remarkably far forward in front of the anterior border of the orbit; but on account of the downward prolongation of the snout and the mouth, and of the raising of the quadrate joint, the mouth points forward instead of upward." The dentary is mesial to the lateral part of the maxilla. Gregory (1933: 254, Fig. 128) illustrated its position. A ligament that starts at the dorsoposterior end of the dentary process connects it with the maxilla and premaxilla by branching into two parts, one to each bone. The insertion on the premaxilla is on the triangular process of the lateral end of the dorsal surface. The insertion on the maxilla is near the insertion of the aponeurosis of the maxillaris. In addition to the ligaments, there are connections of fibrous connective tissue between the maxilla and the dentary; this tissue forms pads in front of the corners of the mouth. 874 Bulletin of Marine Science [17(4)

_LIVER 13 SWIM BLADDER mil INTESTINE • STOMACH

IIIGONADS lljJITIJ SPLEEN

[III ESOPHAGUS ~ PYLORIC CAECA FIGURE 30. Microspathodon chrysurus. Positions of the internal organs.

Movements of the Jaws and Associated Muscles.-OPENING OF THE JAWS: Tchernavin (1953: 44) cited three methods used by fishes to open the mouth, and based these methods on the kinds of muscles involved. The method here described corresponds to the first described by Tchernavin, "depressing of the mandible by pulling its anterior end downwards and backwards." The muscle that does the most to open the mouth is the geniohyoideus (Figs. 26a, b; 27). Its contraction depresses the anterior part of the dentary, and at the same time makes the articular rotate on the condyle of the quadrate. The same rotary movement is imposed on the dentary process, and this motion is transmitted to the maxilla and premaxilla by way of the ligament that links them to the dentary; the real motion trans- mitted by the ligament is a pulling forward of the maxilla and premaxilla. The forward movement of the maxilla, by way of its attachment to the palatine, is transformed into a rotary motion, with the maxilla pivoting around the anteroventral end of the palatine. A similar movement is described by Eaton (1943: 184) for some cichlids. The forward move- 1967J Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 875

• LIVER ~ SWIM BLADDER mlNTESTINE • STOMACH

IIGONADS [j] SPLEEN

[I[] ESOPHAGUS ~ PYLORIC CAECA FIGURE 31. Microspathodon chrysurus. Positions of internal organs, with the left portion of the liver removed. ment transmitted to the premaxilla is also transformed into a rotary motion by way of its connections to the maxilla and by way of the anterior ligament that unites the palatines passing anterior to the dermethmoid cartilage (Fig. 28). The rotary motion of the premaxilla is also assisted by the pre- maxilla-dermethmoid ligament. This ligament also limits the motion of the premaxilla, just as dose the analogous rostral or sigmoid ligament in Rutilus (AI-Hussaini, 1949: 117), a cyprinid. The movement is also helped by the posterior push of the posterodorsal surface of the first section of the maxilla. The other ligaments (Fig. 28) are probably used to main- tain the position of the premaxilla. CLOSING OF THE JAWS: The maxilla and premaxilla are retracted by the action of the maxil/aris (Figs. 21 b, 22). Its contraction exerts a back- ward pull on the maxilla, this backward motion being transformed into a rotary motion by the pivoting of the maxilla against the palatine. The premaxilla is pulled back in rotary motion by way of its attachment (described above) to the maxilla. 876 Bulletin of Marine Science [17(4)

:>.;. •••• 0:-: •••: ••••••• •• ...::::-••••••• .r

'~" .,•..... ;,&:.,::.::':' :~::::'. ' .• ". '. '." . •.••• :::=:.:..

BLiVER E3 SWIM BLADDER lmllNTESTINE • STOMACH

IIGONADS [W SPLEEN

[[j] ESOPHAGUS ~ PYLORIC CAECA FIGURE 32. Microspathodon chrysurus. Positions of the internal organs, with the left portion of the liver removed, showing relative length of the intestine.

The dentary is closed by the action of the mandibularis (Figs. 2Ic, 23). The contraction of this muscle acts on the dcntary, pulling back the posterior part of the dentary process. The closing of the lower jaw is helped further by the action of the adductor mandibulae: Al and A:: (Figs. 2Id, e, 24, 25).

MORPHOLOGY OF THE ALIMENTARY TRACT Microspathodon chrysurus has thick, fleshy lips. A rough pad is located inside each corner of the mouth (Fig. 29). Another and larger pad is located anterior to the oral valve, in front of the vomer, and slightly posterior to the premaxillary teeth (Figs. 26c, & 29); its anterior part 1967) Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 877 is semicircular and free from the roof of the mouth, the attachment being only along its posterior part, just in front of the oral valve. The oral cavity is triangular in sagittal section (Figs. 30-32); it is expanded laterally and ventrally, in posterior direction, to reach a maximum expansion at the level of the pharynx. The oral valve, as pointed out by Gudger (1946: 274), is formed only by the maxillary breathing valve, a crescentic membrane. The mandibular portion is absent. The function of oral valves as respiratory mechanisms was reported on by Dahlgren (1898). The roof of the mouth posterior to the maxillary breathing valve is rugose, and it presents a recess against which the tongue fits. The tongue is short (Figs. 26, 29-31); its dorsal surface is triangular and rugose. The pharynx can be divided into two parts: the respiratory and the masticatory pharynx. The respiratory portion is formed by four gill arches. The gill rakers, situated mesially on the arches, vary in number from 21 to 25, but the usual number is 24. They are short, and are equal in length to about one-third the diameter of the eye. The masticatory part is formed by the upper and lower pharyngeals. The lower, fused pharyngeal element (Fig. 16) has a pad between the arms. Posteriorly, this pad reaches the border of the esoph- agus. The esophagus (Fig. 31) is a short muscular tube whose function, as stated by Angelescu & Gneri (1949: 221) for a similar esophagus in Prochilodus lineatus, is simply the conduction and lubrication of food. The liver (Fig. 30) is anterior to the stomach, below and at the sides of the esophagus, and is situated against the anterior surface of the coelom. It is large, with the lobes expanded to the left and the right, the left lobe being the larger. The gall bladder is located dorsomesially on the right lobe. The spleen is located slightly below the gall bladder, and at about the same level as the stomach; it is wing-shaped, and extends along the ventral surface of the stomach. The swim bladder is located dorsally and posteriorly in the body cavity; it is wide anteriorly, tapering posteriorly (Figs. 30-32). The gonads are located anterior to the posterior part of the swim bladder. The kidneys are located retroperitoneally. The stomach (Figs. 30-32) is a simple muscular sac whose blind end projects toward the left side of the body. The esophageal and intestinal openings are located next to each other at the right. Immediately ventral to the stomach and connected to the anterior end of the intestine are three pyloric caeca (Fig. 31), the largest being anterior. In Microspathodon chrysurus the pyloric caeca contained food; they also have the inner surface covered with villi, and possibly have a digestive function, as has been suggested frequently by authors (e.g., Rahimullah, 1945). The intestines, located on the ventral part of the visceral cavity (Figs. 30, 31), are very long (Figs. 32, 33). The large intestine or rectum (Barrington, 1957: 124) is short and nearly straight, and the small 878 Bulletin of Marine Science [17(4)

1100 • 1000 •

900 - •

...... 800 • ~ z 700 • I- ~ • ; 600 ~ r • I- 500- ~ o • % 400- I- o ~z ..J 300 •

200 • ," 100 ,..• •• •

o 10 20 30 40 50 60 70 80 80 '00 110 120 130 STANDARD LENGTH ( mm)

FIGURE 33. Microspathodon chrysurus. Standard length against intestinal length. intestine is very long and coiled. The relationship of the length of the intestines to the food ingested has been discussed by Churchill & Mitchell (1937: 76) and by Angelescu & Gneri (1949: 177). Generally, herbivo- rous species have longer intestines. The relation between length of the intestines and the standard length of Microspathodon chrysurus is shown in Figures 32 and 33.

SUMMARY The studies conducted on the food and feeding of Microspathodon chrysurus show that the peculiar shape of the jaws, as well as the disposi- tion of the teeth, allows it to feed on rocks, corals and sandy bottoms. The premaxilla of Microspathodon chrysurus is ventrally hollow, and toothless; it houses in the cavity a connective tissue which in turn bears movable teeth. The maxilla also has a ventral concavity that overlies the premaxilla; it moves by pivoting around the anterior tip of the palatine. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 879

The dentary has an anterior concavity which bears connective tissue; it has two different sets of teeth, one set located against the posterior part of the concavity, not imbedded in the bone, and one set on the dentary process imbedded in the bone. The articular bone articulates with the quadrate on its ventral portion, and the peculiarities of this joint have been discussed above. The lower pharyngeals are fused basally to form a Y -shaped bone. The teeth of the dentary are not only different mor- phologically from those in the connective tissue of the premaxilla, but they are replaced differently. On the premaxilla the teeth primordia originate at the anterior surface of the concavity and move backwards as the teeth grow, while on the dentary the new teeth originate at the base of the older tooth and move in a somewhat elliptical way around a fixed base. The cranial muscles studied were the levator arcus palatini, the adductor arcus palatini and the adductor mandibulae. The function of the levator arcus palatini and of the adductor arcus palatini is to enlarge the oral cavity, the first by raising the hyomandibular, the second by raising the palatine arch. The adductor mandibulae closes the mouth by acting on the maxillary, dentary, and articular bones. The geniohyoideus muscle, located ventrally on the head, opens the mouth by depressing the dentary, pulling the anterior end down and back- wards. The maxilla and premaxilla are then opened by the action of a ligament connecting them to the dentary. Three pads are located in the mouth of Microspathodon chrysurus. There are two small ones at the corners of the mouth, and a large one between the teeth of the premaxillary tissue and the oral valve (only the maxillaris oral valve is present); they probably serve to discharge the nematocysts of the corals upon which the juveniles feed. The pharyngeal apparatus is probably used to select the size of the particles to be ingested. The esophagus is a short muscular tube. The liver is located anteriorly against the coelomic wall; the gall bladder is located dorsally on its right lobe, and slightly below the gall bladder is situated the spleen. The sac-like stomach is dorsal to the visceral mass. The swim bladder is broad ante- riorly, tapering posteriorly; near its posterior end are located the gonads. The kidneys are retroperitoneal. The number of pyloric caeca is always three; they apparently have digestive functions. The small intestine is long and very coiled. The large intestine is nearly straight. Microspathodon chrysurus is omnivorous, showing a gradual change from mainly carnivorous as juveniles, to mostly vegetarian as adults. The distribution of Microspathodon chrysurus is related to its feeding habits, the juveniles being found in large numbers around patches of Millepora, the adults in the rocky and sandy areas within or around the reefs. 880 Bulletin of Marine Science [17(4)

SUMARIO

ANATOMIA DEL MECANISMO DE AUMENTACION Y HABITOS AUMENTICIOS DE Microspathodon crysurus (PECES: POMACENTRIDAE) Los estudios realizados sobre los habitos alimenticios de Microspathodon chrysurus demuestran que la conformaci6n particular de sus mandibulas, as! como la distribuci6n y caracteristicas morfol6gicas de sus dientes, estan destinados a facilitar la ingesti6n de alimentos, tanto en los ambientes rocosos 0 coralinos, como en los fondos arenosos. La premaxila, en su parte ventral, presenta una concavidad rellena de tejido conjuntivo en el cual estan imbuidos los dientes, que son m6viles. La maxila, que tambien tiene una concavidad ventral, cubre la convexidad dorsal de la premaxila y se mueve apoyandose sobre el extrema anterior del palatino. En la parte anterior del dentario existe una concavidad dorsal IIena de tejido conjuntivo, imbuidos en el y apoyandose en la parte anterior del borde posterior del hueso estan situados los dientes. Tanto en la premaxila como en el dentario los dientes se renuevan peri6dicamente con crecimiento anteroposterior. El hueso articular se une al cuadrado en la parte ventral y las carac- teristicas de esta uni6n se describen ampliamente. Los huesos faringeos se fusionan en su parte basal, formando una estructura en forma de "Y". Los dientes del dentario no s610 se diferencian morfol6gicamente de los de la premaxila, sino que, adem as, tienen un proceso de renovaci6n distinto. En la premaxila los dientes primordiales se originan en la superficie anterior de la cavidad y se desplazan hacia atras al crecer; en cambio, en el dentario los nuevos dientes giran en forma eHptica alrededor de su base. Se estudian y describen las funciones de los siguientes musculos: levator arcus palatini, adductor arcus palatini, adductor mandibulae y geniohyoi- deus. Dos de los tres cojinetes que presenta la boca estan situados en sus comisuras laterales y el tercero y mas grande, esta situado entre los dientes del tejido premaxilar y la valvula oral (se observa s610 la valvula oral maxilar). La funci6n de los cojinetes es probablemente la de absorber las descargas de los nematocistos de los corales que hacen parte de su regimen alimenticio en la etapa juveniI. El Microspathodon chrysurus es un pez omnivoro, que cambia gradual- mente los habitos predominantemente carnivoros de la edad juvenil hasta volverse predominantemente herbivoro en la edad adulta. La distribuci6n del Microspathodon chrysurus se relaciona con sus habitos alimenticios, encontrandose los ejemplares j6venes, en gran numero, en los alrededores de las zonas donde hay concentraciones de Millepora, mientras que los adultos se encuentran en los sitios rocosos 0 arenosos de los arrecifes 0 en sus alrededores. 1967] Ciardelli: Feeding Mechanisms of Microspathodon chrysurus 881

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