Fisheries Science 65(1), 117-122 (1999)

Age and Growth of Japanese Whiting Sillago japonica in Tateyama Bay

Sulistiono, Masashi Yokota, Shuichi Kitada, and Seiichi Watanabe

Department of Aquatic Biosciences, Tokyo University of Fisheries, Konan, Minato, Tokyo 108-8477. Japan (Received August 6, 1998)

Age and growth of the Japanese whiting Sillago japonica were examined from 908 fish specimens collected from October 1993 to January 1995 in Tateyama Bay, and growth curves were estimated by us ing a new method. Monthly changes in percentage of the otolith with opaque and translucent zones in the outer margin indicated that growth ring was formed once a year. Marginal increments of otolith formed annual rings from March and April. Ages of the fish were estimated to be 2, 3 and 4 years for both sexes. Using otoliths of 532 fish, growth in total length was expressed by the combined equation of the relative growth in total length and the radius, and the growth of ring radius as Lt=602.5(1-e-0.125(t-0.02)) for male and Lt=530.2(1-e-0.149(t-0.04)) for female,

where Lt is total length in mm and t time in year. Growth in female and male were similar. The growth equations of the new and back-calculation methods were compared, and the difference of the parameter estimates, discussed. Key words: age, growth, otolith, Tateyama Bay, Sillago japonica

The Japanese whiting Sillago japonica, is distributed in otolith. The ring marks in this study were defined as the the waters of Japan, Taiwan, Korea and South east Asia boundaries from the outer margin of the translucent zone where it is commercially fished using beach seines, gill net to the opaque one. All age assessments were made follow and trammel net in coastal waters, and in nearshore deeper ing the methods of Bowler 4) and Mio.5) The time of annu waters using beam and otter trawl nets.1) lus formation was determined by monthly changes in per Drops in catches of this fish have been attributed to centage occurrence of the otoliths with opaque margins. changes in the environment and overfishing, and further This was calculated by dividing the number of fish with an decreases in the availability of this family in nature are an opaque zone at its otolith margin divided by total number ticipated. However, sillaginids have a great potential for of fish examined for age determination: opaque/(opa fish culture including economic opportunities in Asia as que+ translucent). they are known for their "delicious eating".2) When the otolith ring radius growth fits the von Ber The objective of the present study is to clarify the age talanffy growth curve, and the observed ith ring radius of and growth of S. japonica using specimens collected in j th fish is rij, ring growth can be expressed by Tateyama Bay, and to propose a new growth curve which is obtained by a combination of the otolith ring growth curve and the relationship between otolith radius and total where R•‡ is maximum ring radius, k is growth rate, and io length. A comparison of the back-calculation procedure is the hypothetical number of rings when the ring radius is by the method considered here along with a discussion on zero. Assuming a normal error distribution, the likelihood the difference in parameter estimates is given. function is

Materials and Methods

A total of 908 specimens (male =475, female =433) were where m is maximum number of rings in collected speci caught during monthly collections in Tateyama Bay using mens, ni is the total number of i-th ring fish and V(ri) is an encircling trammel net and hand line from October the estimated variance of i-th ring radius. Maximizing log 1993 to January 1995. All fish were sexed by observation L numerically, R., k and io can be estimated. Standard er of the gonads, measured to the nearest mm of total length rors of these parameters are also obtained from the Hessi and weighed to the nearest gram. an matrix numerically. The left otolith was removed from the specimens and Here, assume a following linear relationship between fixed in glycerin. Opaque and translucent rings of the otolith radius and total length otolith (Fig. 1) were observed under reflected light using a L=ƒÀR. (3) binocular microscope,3) usually at 10 •~ magnification. The otolith radius and ring radii were measured at the shortest By combining Eqs. (1) and (3), we get a von Bertalanffy axis which was from the focus to the longest width of the growth equation 118 Sulistiono et al. these fish. The otolith is oval shaped, anterior portion Lt =ƒÀR. {1-e-k(t-to)}, (4) being more sharply defined than the posterior (Fig. 1). where to=io-tadj, and tad] is a scale parameter which ad Monthly changes in percentage occurrence of otoliths with justs the number of ring marks to the actual age. opaque margins were observed (Fig. 2). Specimens collect ed during spring and summer showed an increase during Results May and remained high between April and August, then decreased sharply in September. This data suggests that Appearance of Opaque Zone and Ring Mark Formation the ring mark was formed once a year from March to Otoliths of the 532 fish that could be clearly measured April, and thus can be considered as an annual mark. under microscope were observed to estimate the ages of

Fig. 1. A, Photomicrogroph showing opaque and translucent zones; B, Method of radius length measurement of otolith in Sillago japonica.

Fig. 2. Monthly percentage of opaque zone appearance at the edge of the otolith in Sillago japonica. Age and Growth of Japanese Whiting Sillago japonica in Tateyama Bay 119

Fig. 3. Relationship between total length and otolith annual radius (ri) represented by age group. •¢ : 1 ring, •£: 2 rings, •ü: 3 rings, •œ: 4 rings.

Age Composition and Size Frequency Distribution hood estimation (Fig. 5). Estimates and standard errors Age determination made by counting the number of an are given in Table 1. nual rings of the otolith showed that the fish included 4 Male: groups (Fig. 3). Mean annulus radii (ri) are: the first class ri=8.63{1-e-0.125(i-0.436)} (5) at 0.58 mm, second at 1.53 mm, third at 2.37 mm and the fourth at 3.1 mm in male and 0.59, 1.54, 2.38 and 2.9 mm, Female: respectively in female. r;=7.52{1-e-0.149(i-0.457)} (6) The specimens collected exhibited 2, 3 and 4 otolith ring formation. Most of the fish had 2 rings (68.5% in males The relationship between the otolith radius and the total and 71.3% in females). Three rings were shown in 30.7% length (Eq. (3)) was estimated separately by sex as follows of the males and 27.9% of the females. Four rings were (Fig. 6): found in less than 1% of the total fish collected. Male: Size frequency distribution of total length and the age L=69.788 (r=0.790, n=265). (7) composition were changed seasonally in both sexes (Fig. 4). The smaller fish with 2 rings (black bar) might begin to Female: grow from April or May (with total length around 140 L=70.55R (r=0.839, n=267). (8) mm). This group of fish continued to grow from June to October (with total length around 170 mm). From Oc The time lag between hatching (in summer: Sulistiono tober, these fish show somewhat stagnant growth the win and S. Watanabe unpub. data) and ring formation ter season (from January to March) in which the maxi (March: Fig. 2) is about seven months. So, we determine mum size of the same age fish was found both in males and tad;as females to be around 175 mm. Fishes with 3 rings (spotted bar) started also to grow during May (with total length around 190 mm) through June, July until December. As with the fish with 2 rings formed on the otolith, those with Using Eqs. (5) and (7) for male (Eqs. (6) and (8) for 3 rings also seemed to be stagnant during the winter sea female), and Eq. (9), total length growth equations for son. both sexes were obtained as follows: Male: Growth Curve Using ring radius in Fig. 3, the growth of the otolith was Lt=602.5{1-e-0.125(r-0.02)} (10) fit to the von Bertalanffy growth curve by maximum likeli- Female: Lt=530.2{1-e-0.149(t-0.04)} (11)

Table 1. Estimates and standard errors for von Bertalanffy growth The total lengths calculated from the above equations model of ring radius and measured total lengths are shown in Fig. 7.

Discussion

In the study, four age groups could be determined from reflected light examination of the annuli found in otoliths dissected from the sample specimens. Comparison be- 120 Sulistiono et al.

Fig. 4. Length frequency distribution of Sillago japonica collected from Tateyama Bay. M, F and n denote male, female and number of samples respectively. tween ring analysis and the length frequency distribution method was developed. First, otolith ring growth was fit (Fig. 4) showed monthly growth in total length could be ted to the von Bertalanffy growth equation using a maxi predicted. Sampling done in April 1994 suggests a new mum likelihood procedure. Second, linear equations were recruitment for one age group (2 rings) with a mode at used to relate fish total length to the otolith radius. Fi around 140 mm. This fish group grew to be 160 mm at nally, total length growth curves were expressed by the June and July 1994. The growth of that group continued, combination of both equations . Results using this method and reached 180 mm at October and November 1994, but seem to be a good estimation because the season of otolith little or stagnant growth was observed after December. Be ring formation is constant (the ring formation of Japanese cause of the limited length frequency distribution data of whiting is around March or April, Fig. 2) and the large the fish collected during this study, and the non-random number of data can be used. Although the measurements sampling, a straight estimate of the growth was considered of otolith radius in the Japanese whiting are difficult be- to be inaccurately applied. cause otolith morphology is variable, this growth equa To more correctly estimate total length growth, a new tions well fit the actual data (Fig. 5). Age and Growth of Japanese Whiting Sillago japonica in Tateyama Bay 121

Table 2. Estimates and standard errors for von Bertalanffy growth model of Total length by back-calculation method

Table 3. Comparison of von-Bertalanffy growth parameters esti mated from the method considered in this study (I) and the back-calculation procedure given in Appendix (‡U)

Fig. 5. Growth curve of otlith in Sillago japonica.

Table 4. Growth of three sillaginid fishes in Japanese and Indian waters

Fig. 6. Relationship between total length and otolith radius. Note: M, F, and T are male, female and total (male and female) respectively; TL, FL and SL are total length, fork length and standard length respectively; a) and b) are present study using new method and back-calculated procedures respectively. * As S.sihama5,6) were collected outside the known distribution of this species12), they were probably S. japonica.

mum total length was equal or larger than those in other areas and species. On the other hand, the estimated growth coefficient k in this study was smaller than the others. In Kyushu, maximum length (around 290 mm) was smaller than the fish in Tateyama Bay which was around 342 mm in male and 469 mm in female. The size of the Japanese whiting in Tateyama Bay was larger than that of S. japonica observed in Hiroshima, but smaller than S. japonica7) and observed in Kyushu5) and S. sihama in In Fig. 7. Growth of total length in Sillago japonica. dia 4) of the same age. In Hiroshima, Kyushu, and Karwar Circle: observed data; solid curve: growth curve obtained by the Waters (India) the S. sihama were 69.5, 110, and 140.5 new calculation method of this study; dotted curve: growth curve ob mm; 132, 191, and 232 mm; and 148, 190, and 224 mm for tained by back-calculation. 1, 2, and 3 year olds, respectively.4-6) Same age in S. robus ta collected in Australia were of smaller size, but similar in total length with S. bassensis.9) The size of S. japonica at Most studies to describe the growth of body size have 1, 2, 3, and 4 years old seems smaller than that of S. par used back-calculation procedures. Back-calculation using visquamis of the same age, which reached 184, 246, 291, the maximum likelihood method was also applied to this and 311 mm in male, and 165, 222, 246, and 270 mm in fe data (Table 2, see Appendix). Although the standard er male at 1, 2, 3, and 4 years old, respectively.8) rors of the parameters in the back-calculation method Comparing estimated length by our method and back- were large for both sexes, the estimates were compared calculated length, both methods produced equivalent with those of other studies of the genus Sillago obtained results in female (Fig. 7). However, at age 4 in males, the by back-calculation (Table 4). For both sexes, the maxi- back-calculated estimate was smaller, but not significantly 122 Sulistiono et al. than that of our method. Therefore the estimates of both methods appear to fit well. Estimates of growth parameters were different between the two methods in spite of the similar estimating procedures (Table 3). Larger We can estimate mean L for each ring by L. and smaller k and to were estimated by our method, compared to the back-calculation procedure. In particu lar, L. by our method was much larger than that of the where rj is the sample mean of ith ring radius, which is back-calculation method in male. This difference in L. given by might be caused by a bias in the otolith samples at age 4 in males. Several earlier studies.10,11) have suggested that back-calculation lengths disagreed with observed length at several ages because of biased sampling, calculation error, The variance of Li is given by etc. In this study, the sample size at age 4 was small, and V(Li)=r-2iV(ƒÀ)+ƒÀ2V(ri)+2riƒÀCov(ƒÀ,ri) the 4th ring radii in male were smaller than the estimated one (Fig. 5). We speculate that these would result in un We can assume Cov (ƒÀ, ri)=0, V(Lj) is estimated derestimation in the back-calculation procedure. Although the estimated total lengths by our method generally corresponded with observed total lengths, ob where served ones were greater than estimated ones around age 2 (Fig. 7). This might be because due to net selectivity we couldn't collect a large number of fish under 150 mm. From the growth curve derived by the new calculation Using Li and V (Li) at each ring, and adjusting the num method, the Japanese whiting was growing until age 4. ber of ring marks to the actual age by Eq. (9), we estimate During the first year S. japonica reached 70 mm in total von Bertalanffy growth curve by maximum likelihood length in male and 71 mm in female. In the second year, procedure. The likelihood function is as follows: the fish grew to be 133 mm in males and 134 mm in fe males. Through the third year, the fish was also growing, and the fish at 4 years old reached 237 mm in males and 236 mm in females.

Acknowledgments We thank Mr. Kyusuke Ito for his assistance during References sample collection, Mr. Neal Teitler for his English correction, Dr. Shinji Tsuchida for their advice during the study, and two anonymous reviewers 1) R. J. McKay: Sillaginid Fishes of the World, FAO-UN, Rome, for helpful comments and suggestions on the manuscript. 1992, p. 87. 2) A. Wheeler: Fishes of the World. Macmillan Pub., New York, Appendix 1975, p. 366. 3) G. M. Cailliet, M. S. Love, and A. W. Ebeling: Fishes. A Field and Back-calculation procedure by maximum likelihood Laboratory Manual on Their Structure, Identification and Natural method. Given relationship between total length and History, Wadsworth Publishing Company, Belmonth, California, 1986, p. 194. otolith radius as 4) N. Radhakrishnan: A contribution to the biology of Indian sand whiting-Sillago sihama (Forskdl). Indian J. Fish., 4, 254-283 (1957). ƒÀis estimated by 5) S. Mio: The Determination of the age and growth of Sillago sihatna Forsskaal. Bull. Japan Sea Reg. Fish. Lab., 14, 1-8 (1965). 6) S. Kakuda: Studies on the ecology and fishing stock of Sillago siha ma (Forskal) through the analysis of its bottom drift-net fishery. J. Fac. Fish. Anim. Husb. Hiroshima Univ., 9, 1-55 (1970). 7) S. Ito and H. Uchida: Study on age and growth of shirogisu in Chikuzen Sea. Seikai Block gyoruikenkyukaiho, 7, 39-44 (1990) (in Japanese). where j refers to individual fish and n is the sample size 8) H. Imoto,N. Yoshioka,C. Kitajima,and S. Matsui:The Age and (n=ƒ°mi=1 ni). The variance of ƒÀ is given by growthof bluewhiting, Sillago parvis quamis distributed in the coastalwaters of NorthernKyushu. Nippon SuisanGakkaishi, 63(6),892-898 (1977). 9) G. A. Hyndesand I. C. Potter:Comparisons between the age struc tures, growthand reproductivebiology of two cooccurringsil laginids,Sillago robusta and S. Bassensis,in temperaturecoastal V(ƒÀ) is estimated watersof Australia.J. Fish.Biol., 49, 14-32(1996) . 10) C. L. Pierce,J. B.Rasmussen, and W . C.Leggett: Back-calculation of fish lengthfrom scale: Empirical comparation of proportional methods.Trans. Am. Fish. Soc., 125,889-896 (1996) . 11) W. E. Ricker:Back-calculated of fish length based on proportionali ty betweenscale and lengthincrement. Can. J. Fish. Aquat.Sci., where 49, 1018-1026(1992). 12) M. Sano,and K. Moshizuki:A revisionof the JapaneseSillaginid fishes.Japan(J. Ich., 31, 136-149(1984).

V(Li)=r-2iV(ƒÀ)+ƒÀ2V(ri)