Nippon Suisan Gakkaishi 59(1), 53-60 (1993)

Dental Sexual Dimorphism and Food Habits in the Stingray Dasyatis akajei from Tokyo Bay, Japan

Toru Taniuchi* and Makoto Shimizu* (Received July 15, 1992)

Dental sexual dimorphism was observed in the stingray Dasyatis akajei. There was no dif ference between sexes in dentition at the juvenile stage. However, mature males had a pointed cusp for each tooth while mature females had virtually flat teeth with irregular surfaces. Sexual dental dimorphism occurred between a disc width of 350 and 400mm for males collected in Tokyo Bay, Japan. This size range was almost identical to the size at maturity for males, estimated from abrupt increments in clasper length and testis weight. Food habits expressed by frequency of occurrence of prey items showed no large difference between sexes. The main food items were crustaceans and fishes. The findings suggest that sexual heterodonty is closely related to the mating behavior of male stingrays. Another form of sexual dimorphism was found in size at maturity, i.e. smaller in males than females by a disc width of approximately 200mm.

The stingray Dasyatis akajei is commonly lected from Tokyo Bay, and lastly to examine distributed in shallow coastal waters and bays which character is closely related to dental sexual of Japan from Hokkaido to Okinawa. It is dimorphism, sexual maturation, or food habits. utilized as a food fish in many places and particu larly in Tokyo Bay, where its meat is deemed Materials and Methods delicious from autumn to winter. In addition to its value as a commercial fish, it plays an impor The stingrays were collected from Tokyo Bay tant role as an apex predator in the demersal food during the period April 1988-May 1990. Most network of coastal and bay areas. However, of specimens were obtained in the Shiba Branch very little is known of its life-history traits, al of Yokohama City Fishermen's Cooperative though taxonomic studies have been conducted Association while a small number of specimens in recent years.1-3) Only fragmentary informa were captured by experimental fisheries. All tion has been published on age and growth.4-6) the specimens were caught by bottom trawlers. During the course of our life history studies Monthly numbers of specimens examined are on the stingray in Tokyo Bay, we found sexual shown in Table 1. dimorphism in dentition. Dental sexual dimor Measurement methods for disc width (DW) and phism has been reported frequently in many clasper length are depicted in Fig 1. To examine species of sharks7) and batoids.8) However, the size when males begin to have a pointed there have been no published accounts on dental cusp, we employed two methods: in the first case sexual dimorphism in the stingray. There are (1988 academic year), we divided the shape of two types of sexual dimorphism in general. One teeth into two types, pointed and not-pointed; is that it occurs in the early developmental stage in the second case (1989 academic year), we as seen in claspers of cartilaginous fishes. An measured the ratio of height to basal length in other is that it develops as the animal becomes anterior teeth. Clasper length, testis weight, mature. In case of the stingray, there is little ovary and uterus weights were measured as indexes differencein dentition at the juvenile stage between of maturity. The testis was found on both sides sexes but sexual heterodonty is clearly observed across the vertebrae whereas the ovary and uterus as it grows larger. were functional only on the left side. This report attempts firstly to show dental sexual Food habits were indicated by percentage dimorphism, secondly to elucidate size at maturity frequency of occurrence (percentage occurrence), and food habits based upon the specimens col which means the percentage of the number of

* Department of Fisheries, Faculty of Agriculture, The University of Tokyo, Yayoi, Bunkyo, Tokyo 113, Japan(谷 内 透,清 水 誠:東 京 大 学 農 学 部). Table 1. Number of specimens of the stingray D. akajei collected in Tokyo Bay for each month Results Differencein Dentition between Sexes SEM photographs of teeth for four specimens are shown in Fig. 2. The teeth of an immature male of 210mm DW (Fig. 2B) were closely crowded in the quincunx or hexagonal. The teeth did not overlap on the outer part of the lip but lay one upon another slightly toward the inner part. Each functional tooth had a deeply hollow surface. Similarly, the teeth of an im mature female of 195mm DW (Fig. 2A) were nearly identical in shape to those of the immature male, although the former seemed to be more rounded in their general form than the latter. Thus, no marked difference in dentition between sexes was observed when the rays were quite young. However, the teeth of a female of 410mm DW (Fig. 2C), though not yet mature, were different from those of young ones. There was no hollow surface on the teeth but a ridge crossing the central part of the surface. Each tooth was rhomboid in shape and was closely corwded without gaps between the teeth. A sexual mature male of 415mm DW, conversely, had quite different dentition from the above specimens. The SEM photograph (Fig. 2D) indicates that the cusp of each tooth was hooked rather than slender. The teeth clearly overlapped each other with the outer edge pointed. A sexually mature female of 665mm DW had quite different teeth from the male. A microscopic photograph (Fig. 3) shows that the surface of the teeth was irregular. Each tooth was closely crowded without a pointed cusp. Thus, dental sexual dimorphism occurred as the stingrays grew larger. Plots of pointed and not-pointed types of teeth against disc width are shown in the upper panel of Fig. 4. Males less than 350mm DW had non-pointed teeth while all the specimens over 400mm DW had pointed teeth. The teeth of males seemed to become pointed between 350mm mmand 400mm DW. The relationship between the ratio of height to basal length in anterior teeth and disc width is shown in the lower panel Fig. 1. Measurement method of disc width and of Fig. 4. The ratio started to increase at over clasper length for the stingray D. akajei. 350mm DW but stopped increments at over 400mm DW. The latter result showed fairly stomachs with one or more individuals of prey good agreement with the former. Therefore, we to the total of non-empty stomachs. Food items concluded that the cusp of teeth of males began were identified to species when possible. Food to be pointed at about 350mm DW and completed items were categorized as unidentified when their pointedness at over 400mm DW. identification to the family level was not possible. Fig. 2. SEM photographs of teeth for four specimens of the stingray D. akajei. Bars indicate 500ƒÊm. A, teeth of an immature female 195mm DW; B, teeth of an immature male, 210mm DW; C, teeth of an immature female, 410mm DW; D, teeth of a mature male, 415mm DW.

length is shown in Fig. 5. Claspers grew rapidly when males reached about 350mm DW but they did not show large increments at over 400 mm DW. Similarly, the relationship between disc width and testis weight also indicates that testes increased in weight rapidly between 350mm and 450mm DW (Fig. 6). The variance of testis weight was larger than that of clasper length, reflecting the nature of its seasonal variation. In this regard, clasper length may be a better indi cator for maturation than testis weight. Thus, it is estimated that males attained their maturity at about 350mm DW and almost all the males Fig. 3. Microscopic photograph of teeth from a became mature at over 400mm DW. mature female of D. akajei, 665mm DW. The relationship between disc width and ovary Bar indicates 2mm. weight is shown in Fig. 7. Some females showed Size at Maturity a rapid increase in the weight of their ovary be The relationship between disc width and clasper tween 500mm and 550mm DW, while all females Fig. 4. Degree of pointedness in anterior teeth against disc width in male stingrays. Upper panel shows two types of cusp, pointed and not-pointed, against disc width in 1988. Lower panel shows the ratio of height to basal length against disc width in 1989.

Fig. 5. Relationship between disc width and clasper length in the stingray. Fig. 6. Relationship between disc width and testis weight in the stingray.

Fig. 7. Relationship between disc width and ovary weight in the stingray. Fig. 8. Relationship between disc width and uterus weight in the stingray. Quadrates indicate an ovary weight of over 200g.

over 600mm DW had ovaries of more than 40g. in 10-20% of the stomachs examined. However, The same relationship was also observed between Bivalvia and Cephalopoda were seldom found disc width and uterus weight (Fig. 8). Judging in the stomachs. Thus, Crustacea and Osteich from abrupt increases in ovary and uterus weights, thyes were important food items for the stingray. which are considered to be closely related to the Among Crustacea, Macrura were important maturation of females, it is estimated that females food items, with more than 33% occurrence by may reach their first maturity between 500 and frequency. There seems to be a little difference 550mm DW and most females over 600mm DW in the percentage occurrence of Crangon affinis may be mature. Estimated sizes at maturity for between sexes, i.e. high in males (11-19%) and females are much larger than those of males by low in females (3.1-4.1%). On the contrary, approximately 200mm DW. females showed a high percentage occurrence for Oratosquilla oratoria (33-56%) while males Food Habits exhibited a low percentage (19-22%). An Food habits expressed by percentage frequency isomysis ijimai occurred at the immature stage of occurrence are shown in Table 2. Food for both sexes, but was not found at the mature items are exhibited according to size at maturity, stage. i.e. 350mm DW for males and 550mm for Regarding Osteichthyes, immature specimens females. The higher prey category shows that of both sexes showed low occurrence in stomachs Crustacea were the most frequently occurring with less than 30 percent by frequency . Among prey both by maturity stage and by sex, with more fishes, Sardinops melanostictus was the most than 56% occurrence by frequency. Osteichthyes frequently occurring food item in mature speci were next in importance showing 29 to 57 mens. Conger myriaster was next in importance . occurrence by frequency. Annelida also ocurred Other fishes identifiable to species were Re- Table 2. Food habits of the stingray D. akajei collected in Tokyo Bay

pomucenus valenciennei, Amblychchaeturichthys range is closely related to size at maturity for hexanema, and A. sciistius, which were all males, estimated from relationships between disc popular fishes in Tokyo Bay according to the width and clasper length or testis weight. It is experimental trawl fishing in 1988 and 1989. necessary, of course, to estimate size at maturity There does not seem to be a large difference in based upon histological examination of the testis percentage occurrence of fishes by frequency and the seminal vesicle. However, since clasper between mature males and females, although length is said to be a good indicator for male mature females tended to eat more O. oratoria maturation in general, as was used in fact in than males. dasyatids,9-11) size at maturity judged by abrupt increments in clasper length may not be greatly Discussion divergent from the true value. There has been little information on the food It is obvious that the dentition of the stingray habits of the stingray. It is said that benthic does not differ between sexes at the juvenile stage invertebrates such as Polychaeta and Bivalvia but becomes quite different as it grows larger. are the main food items.12) The stomach content The ratios of height to basal length in teeth reveal analysis in this study reveals that crustaceans that dental sexual dimorphism occurred between are the most frequently occurring prey items. 350 and 400mm DW for males. This length Fishes were also found frequently in the stomachs of stingray in Tokyo Bay. Analyses of food by a Grant-in-Aid for Scientific Research from habits for other species of dasyatids also support the Ministry of Eduction, Science, and Culture, the notion that crustaceans and fishes are im Japan (No. 03660183). portant food items.13) Although food items between sexes are not identical at the adult stage, References no marked difference which could generate sexual heterodonty was observed between sexes in this 1) K. Nishida and K. Nakaya: Taxonomy of the genus Dasyatis (Elasmobranchii, Dasyatididae) from the North Pacific, in study. "Elasmobranchs as Living Resources: Advances in the As to why dental sexual dimorphism occurs, Biology, Ecology, Systematics, and the Status of the Fisheries" there have been two speculations. Feduccia (ed. by H. L. Pratt, Jr., S. H. Gruber and T. Taniuchi), U.S. Dep. Commer. NOAA Tech. Rep. NMFS 90, 1990, pp. 327- and Slaughter14) suggested that sexual dimorphism 346. in dentition in lays is interpreted as a means of 2) K. Nishida: Phylogeny of the suborder Myliobatidoidei. making possible differential foraging by sexes Mem. Fac. Fish. Hokkaido Univ., 37, 1-108 (1990). 3) K. Nishida: Taxonomy of Japanese myliobatidoids. Rep. to reduce intraspecific competition for food. On Japan. Soc. Elasmobranch Stu., 27, 1-18 (1990). the contrary, MacEachran15) found no significant 4) T. Yokota: Studies on the stocks of sharks and rays II. difference in food consumed between sexes Age composition of the ray, Dasyatis akajei (Muller et Henle), as observed in the catch by trawlers landed at Totoro, Miya either for young or mature specimens based upon zaki Prefecture during a period September, 1949 to May, an examination of 1,600 stomachs of four species 1950. Nippon Suisan Gakkaishi, 16(11), 188-189 (1951). of rajids with sexually dimorphic teeth. Stomach 5) T. Yokota: Studies on the stocks of sharks and rays I. A method of age estimation. Nippon Suisan Gakkaishi, 17, content analysis in this study also supports the 321-324, 3 tables (1952). notion that dental sexual dimorpnism occurs 6) R. Ishiyama and K. Okada: Age determination of batoids. Rakusui, 4, 99-105 (1952) (in Japanese). as males become mature. McCourt and Kers 7) L. J. V. Compagno: Sharks of the Order Carcharhiniformes. titch16) suggested that sexually dimorphic dentition Princeton Univ. Press, Princeton, 1988, p. 34. in Urolophus concentricus may help grip females 8) H. B. Bigelow and W. C. Schroeder: Order Batoidei. Mem. Sears Fnd. Mar. Res., 1(2), 4-514 (1953). during copulation. Males of the stingray have 9) F. F. Snelson, Jr., S. E. Williams-Hooper and T. H. Schmid: been reported to bite female pectoral fins during Reproduction and ecology of the Atlantic stingray, Dasyatis copulation for D. akajei17,18) and for D. ameri scobina, in Florida coastal lagoons. Copeia, 1988(3), 729- 739 (1988). cana.19) Therefore, it is concluded that pointed 10) F. F. Snelson, Jr., S. E. Williams-Hooper and T. H. Schmid: cusps in the teeth of mature males of the stingray Biology of the bluntnose stingray, Dasyatis sayi, in Florida are available for copulatory behavior rather than coastal lagoons. Bull. Mar. Sri., 45, 15-25 (1989). 11) T. B. Thorson: Observation on the morphology and life food habits. history of the euryhaline stingray Dasyatis guttata (Bloch and Another form of sexual dimorphism was found Schneider) 1801. Acta Biol. Venez., 11(4), 95-125 (1983). for size at maturity in this study. Males matured 12) R. Ishiyama: Akaei, in "New Illustrated Encyclopedia of the Fauna of Japan" (supervised by Y. Okada, S. Uchida, and T. at sizes between 350 and 400mm DW while Uchida), Vol. 3, Hokuryukan, Tokyo, 1965, p. 167. females reached maturity at sizes between 550 13) P. Devadoss: On the food of rays, Dasyatis uarnak (Forskal), D. alcockii (Annandale) and D. sephen (Forskal). Indian J. and 600mm DW. An approximately size Fish., 25, 9-13 (1978). difference of 200mm DW was observed between 14) A. Feduccia and B. H. Slaughter: Sexual dimorphism in sexes concerning size at maturity. skates and its possible role in differential niche utilization. Evolution, 28, 164-168 (1974). 15) J. D. MacEachran: Reply to "Sexual dimorphism in skates (Rajidae)." Evolution, 31, 218-220 (1977). Acknowledgements 16) R. M. McCourt and A. N. Kerstitch: Mating behavior and sexual dimorphism in dentition in the stingray, Urolophus Thanks go to the former students of our la concentricus from the Gulf of California. Copeia, 1980(4), boratory, Messers K. Ishii and H. Haneda for 900-901 (1980). 17) T. Tsutsumi: Life of Fishes. Momozono Shobo , Tokyo, their help in the examination of materials. 1977, p. 25 (in Japanese). We acknowledge Mr. N. Koyama, Shiba 18) S. Tasaka: Mating behavior of rays. Uminoyokocho, Branch of Yokohama City Fishermen's Shimoda Underwater Aquarium, 1986(2), 6 (1986) (in Japanese). 19) F. W. Brockman: An observation on mating behavior of Cooperative Association and colleagues of our the southern stingray, Dasyatis americana . Copeia, 1975(3), laboratory for their cooperation in collecting 784-785 (1975). specimens. This study was supported partly