Fisheries Science 63(1), 15-21 (1997)

Spawning Cycle of Two Dragonet Species, Calliurichthys japonicus and Repomucenus huguenini, in Tosa Bay, Southern Japan

Benjamin Jareta Gonzales,*1,*3 Nobuhiko Taniguchi,*1,•õ and Osamu Okamura*2 *1Department of Fisheries , Faculty of Agriculture, Kochi University, Nankoku, Kochi 783, Japan *2Department of Biology , Faculty of Science, Kochi University, 2-5-1 Akebono-cho, Kochi 780, Japan *3State Polytechnic College of Palawan -Institute of Marine Sciences , Puerto Princesa City 5300, Philippines

(Received February 9, 1996)

The spawning cycle of Calliurichthys japonicus and Repomucenus huguenini was investigated from March 1992 to February 1993 in a wild population in Tosa Bay, Kochi Prefecture. Calliurichthys japonicus is an annual spawner, having high reproductive activity in summer. The species appears to spawn mainly between 90-120m water depth and extends its spawning ground to shallower waters of the Bay during the peak reproductive period in July. Maturity of females occurs at 12.5cm in SL and 17.7 cmSL in male. Repomucenus huguenini is a biannual spawner, spawning within its normal distri bution range of 15-30m water depth during spring (May) and autumn (October to December with a

peak in November). This species matures and reproduces from an early age with maturity estimated to occur at 4.5cm SL in both sexes. The temperature in 45-120m when the GI of C. japonicus samples was at its peak in July, ranged from 17.4-21.6•Ž and salinity from 34.6-35.0. During the peak reproductive season of R. huguenini in November, the temperature ranged from 22.4-22.8•Ž and salini ty from 34.4-34.6in 15 to 30m water depth.

Key words: spawning, length at maturity, dragonet, Tosa Bay

Information on the ecological interactions of fish spe Research on dragonets has determined the age and cies is a prerequisite for their effective management and growth of Callionymus lyra;3) the general biology and ecol conservation. Conservation efforts for fish species should ogy of Foetorepus altivelis,4) Callionymus belcheri,5) and consider not only those species of fishery or of economic Diplogrammus xenicus;6) the life-history of Repomucenus importance, but other ecologically important species as beniteguri;7) and the spawning of Repomucenus valencien well.1) Fish catch compositions during trawling surveys in nei and R. richardsonii8) and Paradiplogrammus enneac Tosa Bay reveal a high catch percentage of a diverse array tis.9) However, no reports are available on the spawning of of dragonet fishes. Calliurichthys japonicus and two predominant dragonets Calliurichthys japonicus and Repomucenus huguenini are the two dragonet species Repomucenus huguenini occurring in Tosa Bay. which predominantly occur among these fish catches. Because of their abundance, these two species are likely to Materials and Methods play an important ecological role in the benthic communi ty of the Bay. Samples were collected monthly in Tosa Bay from eight Life history strategies of fishes can be deduced by depth zones of 15, 30, 45, 60, 90, 120, 150, and 190m dur studying or comparing similar species in the same or simi ing the period from March 1992 to February 1993 (Fig. 1). lar environments.2) It is also important to understand Sampling of fish specimens was carried out using a beam which of the life history characteristics and environmental trawl (7m beam length, 10m total net length with 10mm factors covary. In the present paper, we detail the spawn cod end mesh). The net was towed for about 30 minutes at ing season and length at maturation of C. japonicus and each depth zone. The gear was operated on board the 20 R. huguenini to clarify the dynamics of the benthic com ton R/V Toyohata Maru of the Usa Marine Biological munity of Tosa Bay. In addition, since C. japonicus and Institute of Kochi University. The bottom water was sam R. huguenini are both abundant and are benthic ver pled with a Nansen bottle sampler at each station. A revers tebrates in the Bay, they can also be useful as biological in ing type thermometer mounted on the water sampling bot dicators to detect environmental changes that may occur tle and a conduction type salinometer were used to analyze in the Bay. Therefore, any basic information on the the proximate environmental parameters. seasonal reproductive timing and length at maturation of Fish specimens were temporarily stored on ice while on both species may assist in detecting or forecasting the vari board the vessel and were preserved in 10% formalin solu ous impacts of human-induced changes on the benthic tion immediately after sorting. In the laboratory, standard ecosystem of Tosa Bay. length (SL) and body weight (BW) of the fish were meas

•õ Corresponding author. 16 Gonzales et al.

ured to the nearest 0.1cm and 0.1g, respectively. The gonads were removed and weighed to the nearest 0.01mg. The monthly mean gonad index (GI) of both species were determined, and the maturation stage of the oocytes of adult fish specimens collected during the peak spawning months were observed under a microscope. The sex of small individuals (C. japonicus, <9cm SL; R. huguenini, <6cm SL) was determined initially by such morphological characters as the relatively longer length of the filamentous finrays on the first dorsal fin in male R. huguenini, the relatively longer tail length to body length of male C. janonicus, and the relatively elongated genital organ of males in both species. Sex was finally confirmed by the shape and color of the testis (elongated and dark color) and the ovary (rounded and milky white). The GI was calculated using the formula: Gl=gonad weight (g) •~ 104/ SL3(cm). In C. japonicus, only female specimens of length ? 12.1cm SL and male specimens ?17.0cm SL were used for GI analysis, while in R. huguenini, male and female specimens with length sizes ? 4.5cm in SL were used (Fig. 2). To accurately discern the spawning ground of C. japonicus, which has a wider depth distribution range than R. huguenini, we analyzed Fig. 1. Map of study area and location of trawling survey sites (dotted the samples collected from different depths and months portion). separately (Fig. 4).

Fig. 2. Monthly changes in gonad indices (GI) of Calliurichthys japonicus (A, female; B, male) and Repomucenus huguenini (C , female; D, male) collected from Tosa Bay, March 1992-February 1993 (Mean•}SE). In C. japonicus, no female specimens ? 12.1 or male specimens ? 17.0cm in SL were collected in March, May, and October (indicated by dotted lines). Spawning in Two Dragonet Species 17 All females were reproductively inactive, having low GI Results values from March to April, while from May larger ones (approximately 10.0 cm mean SL) with a maximum GI Spawning Season of C. japonicus value of 10.2 appeared (Fig. 5). Smaller females (7.0-9.0 The mean monthly GI of female C. japonicus started to cm in SL) began to show higher GIs in July, and these in increase from January (Fig. 2A). No large individuals creased continuously until the peak in November. The (? 12.0cm in SL) were caught in either March or May, but most active female spawning cohort in November had a in April, the mean GI value showed a continuation of this mean SL of 7.0cm, while a larger cohort with a mean SL trend. A significant increase in female GI was observed it of 12.0cm showed a decreasing GI in the same month. June (Fig. 2A), and the mean monthly GI of female C, Testes began to ripen earlier than the ovaries in April (Fig. japonicus (? 12.0 cm in SL) peaked in July, having high 5). Comparatively high male GI values occurred from values over the summer, from June to September (Fig. 2A). April to May and from September to November. The male No large male C. japonicus (? 17.0cm in SL) were col. GI gradually decreased from December to February of the lected in March or May. The mean monthly GI of male C. following year. During the high spawning activity of R. japonicus was relatively high in April (Figs. 2B, 3). The huguenini from October to December, 26% of the total fe male GI increased in June, while a slight decrease was ob male specimens with relatively high GI values (10.3-17.9) served in July (Fig. 2B). The GI of large males (? 17.cm. had a size range of 4.5-7.2cm SL, while in males, 24% of SL) increased significantly in August reaching the peak it the total specimens with relatively high GI values (0.3-0.9) September (Fig. 2B). Mean monthly GI values of both sex. had a size range of 4.1 to 7.3cm SL. The smallest length es were low in winter (Figs. 2A, B and 3). size with a high GI value was 4.5cm SL for both male and A sligt increase in the GI valuu of both males and fe female R. huguenini. males (> 14.0cm SL) was observed in April (Fig. 3). Only During the peak reproductive season of R. huguenini in smaller-sized male (8.5-12.6cm) and female (8.0-11.9cm November, the temperature range was 22.4-22.8•Ž and SL) cohorts were collected in May and all showed low GIs. the salinity 34.4-34.6 at 15 to 30 m depths, where samples As larger female individuals were sampled in June, a were collected. marked increase in GI occurred (Fig. 3). Individual Most of the oocytes observed in adult specimens of C. females (13.0-17.0 cm SL) with the highest GI and larger japonicus in July, and R. huguenini during May and males (17.0-21.7cm SL) with high GI values occurred in November were characterized by a very narrow previtelline July. These large individuals with relatively high GIs con space (vitellogenic stage). tinued to appear until September, while thereafter their GI markedly decreased and remained low till February of the Discussion following year (Fig. 3). The smallest size of females with a high GI value was 12.5cm SL and that of males was 17.7 Spawning of Calliurichthys japonicus cm SL. Of the total female specimens with high GI values Although we lack data for March and May, the GI (5.0-10.8), 74% were collected from 90m water depth. values of C. japonicus increase from February to June, Samples of C. japonicus were collected between 45 and reaching a peak in July. The mean monthly GI value (Fig. 120m depths of the Bay (Fig. 4). Large female individuals 2A) and the presence of large individuals with high GI were distributed mostly in deeper waters (90-120m), values (Fig. 3) suggest that female C. japonicus spawn in throughout the year. Some large females, however, were the summer, from June to September with the highest collected between 45 and 60m depths in June and July reproductive condition being in July. (Fig. 4A). The GI values of these fish samples were highest Calliurichthys japonicus may be classified with the in the 120m depth zone in August (Fig. 4B). While speci group of dragonets that spawn once a year (annual mens also with high GIs were observed in 45-120m water spawner). The peak of its reproductive effort is the same as depths during June through September. In July, large that of Callionymus enneactis, spawning in July.9) The an females with high GIs appeared between 45 and 60m nual reproductive frequency of C. japonicus is similar to depths. Large males of C. japonicus were collected in deep Callionymus belcheri, spawning once a year. However, C. er waters (90-120m) in almost all months of the year (Fig. belcheri spawns between March and May,5) occurring earli 4C). Some large males, however, were also observed in 45 er than C. japonicus. These two species were described by - 60m depths in July and also a few relatively large males Fricke10) as belonging to the same genus-Callionymus. were collected in 45-60m depths in January. However, The annual reproductive frequency occurrence of C. large males with high GIs were collected only in 90m japonicus coincides with that of Synchiropus altivelis, depth in August and September (Fig. 4D). which spawns annually between late winter and early The temperature at 45-120m, when the GI of C. japoni spring.4) However, the spawning season of the former cus samples collected was at its peak in July, ranged from differs from that of the latter by occurring in summer. The 17.4-21.6•Ž and salinity from 34.6-35.0. Synchiropus species groups are easily distinguished from the Callionymus species by their generic differences.11) Spawning Season of R. huguenini Furthermore, Fricke10) classified Calliurichthys japonicus, The mean monthly GI values of R. huguenini (?4.5cm Callionymus enneactis (Paradiplogrammus enneactis in SL) in both sexes were relatively low from March to Sep Nakabo,12)) and Callionymus belcheri in one genus-Cal tember, but a significant increase occurred from Septem lionymus. In our result, these three species are separated ber to October, reaching a peak in November (Fig. 2C, D). from Synchiropus altivelis by spawning annually in either Thereafter, it markedly decreased until February. spring or summer, while the latter species spawns during 18 Gonzales et al.

Fig. 3. Relationship between standard length (SL) and gonad index (GI) of Calliurichthys japonicus in Tosa Bay for March 1992 to February 1993.

the colder months of late winter and early spring. Added spawn once a year. to this, Synchiropus altivelis is distributed in relatively deeper water (180m) than C. enneactis (0-1m),9,13) C. bel Spawning of Repomucenus huguenini cheri (3-33 m),5) and C. japonicus (45-120). On the other The mean monthly GI value shows that R. huguenini hand, Synchiropus altivelis, Callionymus enneactis, and spawned from October to December with a peak in Novem C. belcheri have a similar geographic distribution (from ber. The appearance of individuals with high GI values the waters of Australia to the waters around Japan, 5,12,14)) (Fig. 5) indicates that spawning also occurs in May. while Calliurichthys japonicus has a relatively wider ge Repomucenus huguenini is therefore a biannual spawner, ographical distribution, occurring from the Western which also includes species such as Callionymus sublaevis; Pacific to Western Australia and the Southeast coast of spawning in March and October; C. calcaratus, May Africa.10,15)Despite their taxonomic and geographical or through June and from October to November;16) and bathymetrical distribution differences, these dragonets all Repomucenus richardsonii, April and November.17) Spawning in Two Dragonet Species 19

Fig. 4. Monthly average standard length (top) and average GI (bottom) of all samples of female (A, B) and male (C, D) Calliurichthys japonicus collected from different zones within its distributional range (45-120m depth).

Repomucenus huguenini, besides belonging in the same ge huguenini. In C. belcheri, the first discharge of follicles oc nus with R. richardsonii, also has a similar geographic dis curred during the peak of the female GI.5) Repomucenus tribution, the former from Hokkaido to the Fast China huguenini spawned spontaneously in a tank from late Sep Sea and the latter from Niigata, Sendai Bay, southward to tember to late November,19) coinciding with the significant the South China Sea.14)On the other hand, the congeneric increase of male and female GI in the present study. Fur species Callionymus sublaevis and C. calcaratus are also thermore, Takita et al.,9) based on ovarian histological ex similarly distributed in Australia.16) Despite their taxonom aminations, confirmed that the (predicted) spawning ic and geographical distribution differences, these drago period in nature of the dragonet Paradiplogrammus en nets all spawn twice a year and have a very similar neactis and that which occurred in the tank were syn reproductive timing, occurring either in spring and au chronous. These results support the validity of our esti tumn, or in summer and autumn. In contrast, though C. mates of the spawning seasons of C. japonicus and R. enneactis, C. belcheri, C. sublaevis, and C. calcaratus are huguenini in the wild, using the GI method. congeneric species, they exhibit different annual reproduc tive frequencies and seasons. These facts suggest that the Spawning grounds seasonal reproductive timing and frequency of breeding The depth distribution of C. japonicus has a tendency per year in dragonets may not be influenced by their taxo for larger specimens to occur in deeper waters (Fig. 4A, C). nomic relationships and geographical or bathymetrical dis Such phenomena are widespread in the demersal fishes of tributions, but may depend on an endogenous reproduc Tosa Bay.20)Both large male and female C. japonicus were tive cycle, which is under genetic control, synchronized to collected from the deeper part of its distributional range, the environmental conditions of their respective habitats. 90-120m, throughout the year. The high GI values (Fig. The oocytes in the vitellogenic stage observed in adult 4B, D) of large individuals (Fig. 4A, C) between 90-120m specimens of C. japonicus in July, and R. huguenini dur depths indicate that this depth range is their main spawn ing May and November, also suggest that both species ing ground. The appearance of large males and females were ready to spawn during those periods. In other fish, with high GIs in 45 and 60m depths in July, during the like Nibea mitsukurii, actual spawning in a tank occurred peak reproductive period, suggest that some of the spawn two months later than the spawning period estimated from ing individuals migrate to shallower waters (45-60m) to GI and microscopic observations of oocytes sampled from spawn. Such spawning migration may occur to allow the the wild.18) This finding is inconsistent with those of the exploitation of wider habitat ranges. On the other hand, dragonets Callionymus belcheri and Repomucenus the narrow depth distribution (15-30m) of the R. hugueni 20 Gonzales et al.

Standard length (cm)

Fig. S. Relationship between standard length (SL) and gonad index (GI) of Repomucenus huguenini in Tosa Bay for March 1992 to February 1993.

ni implies that no spawning migration occurs and that the Length at Sexual Maturity species spawn within its distributional range: in the shal The relative size at maturation between sexes of C. low waters of Tosa Bay. Adult male and female R. japonicus was similar to that of other dragonets;4,16,17,21) huguenini collected from 15m and 30m water depths of smaller in females and larger in males. In R. huguenini, Tosa Bay spawned in a tank from late September through the relative size at maturation was similar to that of C. bel late November. 19) cheri 5)being the same in both sexes. Early life-history theo The difference in the seasonal reproductive timing and ry suggests that high mortality caused by density-indepen the spawning depth between C. japonicus and R. hugueni dent effects selects for early reproduction and this strategy ni show that there is no space competition during spawn would be expected in harsh or unpredictable environ ing between these two species. ments.22)The early maturation of R. huguenini, is presuma bly influenced by the environmental changes in the shallow Spawning in Two Dragonet Species 21 waters of Tosa Bay and is therefore environmentally less cal notes. Japan J. Ichthyol., 29, 253-259 (1982). stable. On the contrary, C. japonicus thrives in deeper 7) T. Takai and T. Yoshioka: The life history of the dragonet, Cal waters, which are a relatively stable environment, and lionymus beniteguri in the Seto Inland Sea-I. Egg, larvae and shows a more delayed maturation. juvenile. J. Shimonoseki Univ. Fisher., 27, 147-154 (1979) (in Life history traits are relative to the productivity of their Japanese). 8) T. Takita and E. Okamoto: Spawning behavior of the two drago habitats; in high-productivity streams, there tends to be nets, Callionymus flagris and C. richardsoni, in an aquarium. several spawnings in a season, early age at maturity and a Japan J. Ichthyol., 26, 282-288 (1979) (in Japanese). short life span. In low-productivity streams, the tendency 9) T. Takita, T. Iwamoto, S. Kai, and 1. Sogabe: Maturation and is for a single spawning in a breeding season, delayed spawning of the dragonet Callionymus enneactis, in an aquarium. maturity and long life spans.22) These circumstances agree Japan J. Ichthyol., 30, 221-226 (1983). with the results of our study. Repomucenus huguenini, 10) R. Fricke: Indo-Pacific Callionymidae. Verlag Von J. Cramer Braunschweig, Germany, 1983, p. 774. presumably living in a high productivity environment, 11) R. Fricke: The Kaianus-group of the genus Callionymus (Pisces: spawned twice a year, matured early, and has a short life Callionymidae) with descriptions of six new species. Proc. Calif. span (about 1 year and 4 months*4). In contrast, C. japoni Acad. Sci., 42: 349-377 (1981). cas lives in an environment with lower productivity, 12) T. Nakabo: Fishes of Japan with pictorial keys to the species. Tokai spawns once a year, and has a delayed maturation and lon Univ. Press, Tokyo, 1993, p. 1474. ger life span (?3 years; Gonzales, unpublished). 13) B. Gonzales and O. Okamura: Rare occurrence of Bathycalliony mus formosanus (Teleostei: Callionymidae) in Tosa Bay, southern Japan with ecological notes and recent list of callionymids in the Acknowledgments Thanks are due to Associate Professor Kunio Sasaki Bay. SPCP-Inst. Mar. Sci. Res. J., 2, 28-36 (1995). and his students, and the captain and crew of Toyohata Maru for the 14) T. Nakabo: Family Callionymidae, in "The fishes of the Japanese field assistance. We also thank Associate Professor Tetsuji Nakabo of Archipelago" (ed. by H. Masuda, K. Amaoka, C. Araga, T. Uyeno Kyoto University for providing us with valuable references. We are grate and T. Yoshino), Tokai Univ. Press, Tokyo, 1984, pp. 342-346. ful to Dr. Ambok Bolong Abul Munafi for his assistance on fish maturi 15) J. L. B. Smith: Fishes of the families Draconettidae and Callionymi ty, to the anonymous reviewers and Chris Norman for their helpful com dae from the Red Sea and Western Indian Ocean. Rhodes Univ., ments on this manuscript. Ichthyol. Bull., 28, 547-564 (1963). 16) C. R. Johnson: The systematics and biology of the Australian References species of the genus Callionymus (Pisces: Callionymidae). Ph. D. thesis, University of Queensland, Australia, 1972, p. 217. 1) FAO: Report of the expert consultation on utilization and conserva 17) H. Eda: Life history of callionymid fishes in Omura Bay. Ph. D. tion of aquatic genetic resources. FAO Fisheries Report No. 491. thesis, Nagasaki University, Nagasaki, 1994, p. 151 (in Japanese). Food and Agriculture Organization of the United Nations. Rome, 18) N. Taniguchi and Y. Okada: Study on the maturation and spawn Italy, 1993, pp. 3-15. ing of the nibe-croaker collected from Tosa Bay. Reps. Usa Mar. 2) D. A. Roff: Reproductive uncertainty and the evolution of iteropari Biol. Inst., 1, 41-49 (1979). ty: why don't flatfish put all their eggs in one basket? Can. J. Fish. 19) B. Gonzales, O. Okamura, and N. Taniguchi: Spawning behavior Aquat. Sci., 38, 968-977 (1981). of laboratory-reared dragonet, Repomucenus huguenini, and de 3) H. Chang: Age and growth of Callionymus lyra L. J. Mar. Biol. velopment of its eggs and prolarvae. Suisanzoshoku, 44, 7-15 Ass. U.K., 30, 281-296 (1951). (1996). 4) M. Akazaki: Biological studies on a dragonet, Synchiropus altivelis 20) H. Horikawa, M. Toriyama, and S. Kishida: Ontogenetic habitat shifts of demersal fishes along depth gradient. Rept. Fish. Res. In (Temminck et Schlegel). Japan. J. Ichthyol., 5, 145-152 (1957) (in Japanese). vest. Japan. Gov., 27, 61-78 (1991) (in Japanese). 5) C. R. Johnson: Biology and ecology of Callionymus belcheri 21) T. Takita: Embryonic and larval development of the callionymid fish, Callionymus calliste. Japan. J. Ichthyol., 29, 441-445 (1983). (Pisces: Callionymidae). Copeia, 3, 461-470 (1972). 6) R. Fricke and M. Zaiser: Redescription of Diplogrammus xenicus 22) R. J. Wootton: Ecology of teleost fishes. Chapman and Hall, New York, 1990, p. 404. (Teleostei: Callionymidae) from Miyake-jima, Japan, with ecologi

*4 B . J. Gonzales: Ecological studies on the callionymid fishes in Tosa Bay, southern Japan. M. Sc. thesis, Kochi University, Kochi, 1994, p. 80.