Dental Sexual Dimorphism and Food Habits in the Stingray ...

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 distributed in shallow coastal waters and bays of Japan from Hokkaido to Okinawa. It is utilized as a food fish in many places and particularly in Tokyo Bay, where its meat is deemed delicious from autumn to winter. In addition to its value as a commercial fish, it plays an important role as an apex predator in the demersal food network of coastal and bay areas. However, very little is known of its life-history traits, although taxonomic studies have been conducted in recent years.1-3) Only fragmentary information has been published on age and growth.4-6)

During the course of our life history studies on the stingray in Tokyo Bay, we found sexual

dimorphism in dentition. Dental sexual dimorphism has been reported frequently in many species of sharks7) and batoids.8) However, there have been no published accounts on dental sexual dimorphism in the stingray. There are two types of sexual dimorphism in general. One is that it occurs in the early developmental stage as seen in claspers of cartilaginous fishes. Another is that it develops as the animal becomes mature. In case of the stingray, there is little difference in dentition at the juvenile stage between sexes but sexual heterodonty is clearly observed as it grows larger.

This report attempts firstly to show dental sexual dimorphism, secondly to elucidate size at maturity and food habits based upon the specimens col

lected from Tokyo Bay, and lastly to examine which character is closely related to dental sexual dimorphism, sexual maturation, or food habits.

Materials and Methods

The stingrays were collected from Tokyo Bay during the period April 1988-May 1990. Most

of specimens were obtained in the Shiba Branch of Yokohama City Fishermen's Cooperative Association while a small number of specimens were captured by experimental fisheries. All the specimens were caught by bottom trawlers. Monthly numbers of specimens examined are shown in Table 1.

Measurement methods for disc width (DW) and clasper length are depicted in Fig 1. To examine the size when males begin to have a pointed cusp, we employed two methods: in the first case (1988 academic year), we divided the shape of teeth into two types, pointed and not-pointed; in the second case (1989 academic year), we measured the ratio of height to basal length in anterior teeth. Clasper length, testis weight, ovary and uterus weights were measured as indexes of maturity. The testis was found on both sides across the vertebrae whereas the ovary and uterus

were functional only on the left side.Food habits were indicated by percentage

frequency of occurrence (percentage occurrence), 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

Fig. 1. Measurement method of disc width and

clasper length for the stingray D. akajei.

stomachs with one or more individuals of prey

to the total of non-empty stomachs. Food items

were identified to species when possible. Food

items were categorized as unidentified when

identification to the family level was not possible.

Results

Difference in Dentition between SexesSEM 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 immature 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

mm and 400mm DW. The relationship between the ratio of height to basal length in anterior teeth and disc width is shown in the lower panel of Fig. 4. The ratio started to increase at over 350mm DW but stopped increments at over 400mm DW. The latter result showed fairly good agreement with the former. Therefore, we concluded that the cusp of teeth of males began to be pointed at about 350mm DW and completed their pointedness at over 400mm DW.

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.

Fig. 3. Microscopic photograph of teeth from a mature female of D. akajei, 665mm DW.

Bar indicates 2mm.

Size at Maturity

The relationship between disc width and clasper

length is shown in Fig. 5. Claspers grew rapidly when males reached about 350mm DW but

they did not show large increments at over 400mm 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 indicator for maturation than testis weight. Thus, it is estimated that males attained their maturity at about 350mm DW and almost all the males became mature at over 400mm DW.

The relationship between disc width and ovary weight is shown in Fig. 7. Some females showed a rapid increase in the weight of their ovary between 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. The same relationship was also observed between disc width and uterus weight (Fig. 8). Judging from abrupt increases in ovary and uterus weights, which are considered to be closely related to the maturation of females, it is estimated that females

may reach their first maturity between 500 and 550mm DW and most females over 600mm DW may be mature. Estimated sizes at maturity for females are much larger than those of males by

approximately 200mm DW.

Food HabitsFood habits expressed by percentage frequency

of occurrence are shown in Table 2. Food items are exhibited according to size at maturity, i.e. 350mm DW for males and 550mm for females. The higher prey category shows that Crustacea were the most frequently occurring

prey both by maturity stage and by sex, with more than 56% occurrence by frequency. Osteichthyes were next in importance showing 29 to 57 occurrence by frequency. Annelida also ocurred

in 10-20% of the stomachs examined. However, Bivalvia and Cephalopoda were seldom found in the stomachs. Thus, Crustacea and Osteichthyes were important food items for the stingray.

Among Crustacea, Macrura were important food items, with more than 33% occurrence by frequency. There seems to be a little difference in the percentage occurrence of Crangon affinis between sexes, i.e. high in males (11-19%) and low in females (3.1-4.1%). On the contrary, females showed a high percentage occurrence for Oratosquilla oratoria (33-56%) while males exhibited a low percentage (19-22%). Anisomysis ijimai occurred at the immature stage for both sexes, but was not found at the mature stage.

Regarding Osteichthyes, immature specimens of both sexes showed low occurrence in stomachs with less than 30 percent by frequency . Among fishes, Sardinops melanostictus was the most frequently occurring food item in mature specimens. Conger myriaster was next in importance . Other fishes identifiable to species were Re-

Table 2. Food habits of the stingray D. akajei collected in Tokyo Bay

pomucenus valenciennei, Amblychchaeturichthys hexanema, and A. sciistius, which were all

popular fishes in Tokyo Bay according to the experimental trawl fishing in 1988 and 1989. There does not seem to be a large difference in

percentage occurrence of fishes by frequency between mature males and females, although mature females tended to eat more O. oratoria than males.

Discussion

It is obvious that the dentition of the stingray does not differ between sexes at the juvenile stage but becomes quite different as it grows larger. The ratios of height to basal length in teeth reveal that dental sexual dimorphism occurred between 350 and 400mm DW for males. This length

range is closely related to size at maturity for males, estimated from relationships between disc width and clasper length or testis weight. It is necessary, of course, to estimate size at maturity based upon histological examination of the testis and the seminal vesicle. However, since clasper length is said to be a good indicator for male maturation in general, as was used in fact in dasyatids,9-11) size at maturity judged by abrupt increments in clasper length may not be greatly divergent from the true value.

There has been little information on the food habits of the stingray. It is said that benthic invertebrates such as Polychaeta and Bivalvia are the main food items.12) The stomach content

analysis in this study reveals that crustaceans are the most frequently occurring prey items.

Fishes were also found frequently in the stomachs

of stingray in Tokyo Bay. Analyses of food habits for other species of dasyatids also support the notion that crustaceans and fishes are im

portant food items.13) Although food items between sexes are not identical at the adult stage, no marked difference which could generate sexual heterodonty was observed between sexes in this study.

As to why dental sexual dimorphism occurs, there have been two speculations. Feduccia and Slaughter14) suggested that sexual dimorphism in dentition in lays is interpreted as a means of

making possible differential foraging by sexes to reduce intraspecific competition for food. On

the contrary, MacEachran15) found no significant difference in food consumed between sexes either for young or mature specimens based upon an examination of 1,600 stomachs of four species of rajids with sexually dimorphic teeth. Stomach content analysis in this study also supports the

notion that dental sexual dimorpnism occurs as males become mature. McCourt and Kerstitch16) suggested that sexually dimorphic dentition in Urolophus concentricus may help grip females during copulation. Males of the stingray have been reported to bite female pectoral fins during

copulation for D. akajei17,18) and for D. americana.19) Therefore, it is concluded that pointed

cusps in the teeth of mature males of the stingray are available for copulatory behavior rather than food habits.

Another form of sexual dimorphism was found for size at maturity in this study. Males matured at sizes between 350 and 400mm DW while females reached maturity at sizes between 550 and 600mm DW. An approximately size difference of 200mm DW was observed between sexes concerning size at maturity.

Acknowledgements

Thanks go to the former students of our laboratory, Messers K. Ishii and H. Haneda for their help in the examination of materials.

We acknowledge Mr. N. Koyama, Shiba Branch of Yokohama City Fishermen's Cooperative Association and colleagues of our laboratory for their cooperation in collecting specimens. This study was supported partly

by a Grant-in-Aid for Scientific Research from

the Ministry of Eduction, Science, and Culture,

Japan (No. 03660183).

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