SUISANZOSHOKU 50(1), 47-54 (2002)

Relative Growth and Feeding Habits of Halfbeak, Hyporhamphus sajori, Larvae and Juveniles in Toyama Bay of the Japan Sea

Futami OYA*1, Toshihiro TSUJI*2, and Shinobu FUJIWARA*1

(AcceptedDecember 12, 2001)

Abstract: Relative growth and feeding habits of larvae and juveniles of the Japanese half beak, Hyporhamphus sajori, was assessed from data collected during a field survey in the summer of 1999. The lower jaw started to elongate from about 10 mm TL. In the allometric relationship between lower jaw length and total length, a turning point was calculated from the intersection of regression equations at 28 mm TL. This point corresponds with the total length completed at metamorphosis. Halfbeak larvae smaller than 30 mm TL fed mainly on copepod nauplii such as Oithona spp. and Paracalanus type. Larvae larger than 60 mm TL fed on larger items such as insects, harpacticoid copepods and organic detritus. In specimens beyond 57 mm TL, the rate of body weight increase with total length was greater and was apparently due to a change in dietary items.

Key words: Hyporhamphus sajori; allometric growth; food; Toyama Bay

The Japanese half beak, Hyporhamphus sajori, Another paper described that larvae less than 10 is widely distributed throughout coastal waters mm TL fed on copepod nauplii and copepodid, of Japan and is an important species for and those more than 10 mm TL fed on adult inshore fisheries. The half beak catch by two- copepoda and cladocera6). The earlier growth boat seines in Ishikawa Prefecture rapidly stage of half beak larvae has been studied in the decreased after recording a peak catch of 612 laboratory3,7,8),and in the natural environment9). tons in 1979. Sadakata et al.1) and Tsuji and This paper describes the relative growth in the Sadakata2) suggested that the major reasons for earlier stage, with an emphasis on the relative the decrease in catch were due to the increase growth of the lower jaw and body weight to total in the fishing pressure and the high efficiency length and the type of prey items consumed. of fishing by two-boat seines. Currently, the half beak stock is low, so it is necessary to Materials and Methods research the stock recovery potential of the half beak fishery in Toyama Bay. 1. Collection of larvae and plankton In previous studies, half beak larvae have Fish samples were collected at 13 stations been studied in the wild, and reared in the in the northwest area of Toyama Bay and at laboratory. Fertilized eggs of this species were five stations in Nanao Bay (Fig. 1) using a fish- easily caught and the larvae developed without larvae net (130 cm mouth diameter, 0.33 mm difficulty. In the laboratory, they could be mesh aperture, 6.8 open area ratio). There were cultured only with Artemia sauna nauplii until two sampling periods: 3rd and 4th of June, and they reached 64 mm in total length (TL)3,4. In 25th and 28th of June, 1999. The ship towed the natural environment, the larvae of 8.5•`19.0 the net horizontally along the surface layer for mm TL fed chiefly on nauplii and copepodid, but about 10 minutes at a speed of two knots. At the larvae of 22.5 mm TL fed on adult copepods5). Ushitsu Port, the samples were collected using *1M arine Biological Research Institute of Japan, Co. Ltd., Yutaka-cho, Shinagawa, 142-0042, Japan. *2lshika wa Prefecture Fisheries Research Center, Ushitsushinkou, Notomachi, Fugeshigun Ishikawa 927-0435, Japan. 48 F. Oya, T. Tsuji, and S. Fujiwara a hand net (35 cm mouth diameter, 2.5 mm jaw to the tip of the upper jaw. mesh aperture) on the 14th of July, 1999.

Zooplankton samples were collected at two 3. Gut content analysis stations (stations 2 and 7) in the northwest area The guts of 42 larvae from the early June of Toyama Bay and at two stations (stations 11 sample, three from the late June sample and 36 and 14) in Nanao Bay using a Kitahara net (30 from the Ushitsu sample were dissected in order cm mouth diameter, 0.09 mm mesh aperture, to examine the food organisms. The guts of

4.2 open area ratio) towed from 20 m depth to the half beak larvae were removed and dissected the surface, at the same time as larvae were with needles. Food organisms in the gut were collected (Fig. 1) . In order to make comparisons identified and counted, and copepod nauplii between plankton and gut contents, copepod were identified to family and genus levels. nauplii were identified to family and genus levels by the number and arrangement of spine and/or Results setae on the caudal armature as described by Bjð±rnberg10) and Koga11) 1. Hydrography

. After collection, all the samples were preserved The transparency (m) in the northwest area in 5-10% formalin seawater solution. of Toyama Bay in early June was from 16 to 21

The following measurements were taken at m, and in Nanao Bay it was from 6 to 9 m. In each station: transparency, water temperature late June, the former was from 8 to 16 m, and the and salinity using an STD meter (AST-500, Alec latter was from 4 to 7 m.

Electronics, Co.). Water temperature (•Ž) of the surface layer

in early June ranged between 18.6 and 20.0•Ž

2. Measurement of specimens in the northwest area of Toyama Bay and

The sorted half beak larvae were weighed (0.1 between 18.2 and 20.7•Ž in Nanao Bay. In late mg) and measured for total length (from the June, the former was between 19.6 and 20.9•Ž, tip of the upper jaw to the end of the tail fin; the latter was between 21.1 and 22.7•Ž.

0.1 mm). The lower jaw length was measured, to Salinity of the surface layer in early June the nearest 0.1 mm, from the tip of the lower ranged between 33.62 and 34.26 in the northwest

area of Toyama Bay, and between 32.51 and

33.79 in Nanao Bay. In late June, the former

was between 33.62 and 34.26, and the latter was

between 29.26 and 32.81.

The hydrography of the study site can be

described as follows: in early and late June, the

warm Tsushima Current influenced the whole

study site, but in Nanao Bay, low salinity and

stagnant water influenced the inner bay.

2. Relative growth

In early June, 54 halfbeak larvae were caught,

and about 80% of those were caught at stations

1 and 10. In late June, only one half beak larva was collected from three stations: stations 2,8

and 13. Thirty-six individuals of half beak larvae were caught in Ushitsu Port in mid-July.

The ranges of total length, lower jaw length

Fig. 1. Map showing field stations for collection of half and body weight of halfbeak larvae were 7.8- - beak larvae and plankton samples. 94.3mm, 0.2•`17.9 mm and 1.8-1654 mg, respec- Growth and Feeding Habits of Halfbeak Larvae 49

Fig. 2. Relationships between total length (TL) and body weight (BW), and lower jaw length (LL) of all collected halfbeak larvae and juveniles.

tively Table 1. The value of constant a and logb on the allometric . In early June, the smallest specimen that equation between total length (TL) and lower jaw length (LL), and body weight (BW) of all the corresponded to a newly hatched larva3), was halfbeak larvae and juveniles caught at station 12, located in Nanao Bay. At

station 1, 32 specimens of 12.8•}3.4mm (mean

•} SD) TL were collected, and at station 10,

11 specimens of 12.5•}5.0 mm (mean•}SD) TL

were collected. Three or less individuals smaller

than 20 mm TL were collected at the other stations. In late June, specimens larger than beyond 60 mm TL, a was 3.7. Despite a lack of 60 mm TL were collected at station 8. All the larvae and juveniles between 30-60 mm TL in half beak larvae collected from Ushitsu Port, in our samples, a turning point at ca. 60 mm TL mid July, grew to be larger than 60 mm (81.9 was calculated at the intersection of the two •} 7.6; mean•}SD) TL. regression equations calculated for BW and TL. Figure 2 shows the relationships between lower jaw length (LL) and body weight (BW) 3. Gut contents of the half beak larvae to total length (TL) for all larvae and juveniles In early June, copepods were the dominant collected in the study. In general, the allometry food items at stations 1 and 10, especially is presented by the equation: y=bxƒ¿. The nauplii of Oithona sp. (perhaps O. similis) and constants of the allometry equations are given Paracalanus type. The pollen of pine trees was in Table 1. The lower jaw started to elongate eaten only at station 1. On the other hand, at at around 10 mm TL. The growth of the lower stations 11 and 12 in Nanao Bay, cladocera were

jaw in relation to total length up to 30 mm TL dominant; and at station 15, approximately only had highly positive allometry (ƒ¿=3.0), but beyond one copepod species, O. davisae was found in 60 mm TL, the allometry was negative (ƒ¿=0.7), the gut contents. although the correlation coefficient was low In late June, copepods were also dominant,

(R2=0.69). A turning point was suggested at ca. especially Pontellidae (this species was identified 20•`30 mm TL. On the other hand, body weight with Pontella chierchiae in the plankton to total length had more positive allometry with specimens of the fish larvae sample, but its growth. That is, up to 30 mm TL, a was 2.4, and presence was extremely rare) nauplii, which 50 F.Oya, T. Tsuji, and S. Fujiwara were eaten dominantly at station 2. At station were similar to the samples at station 8: they 8, although total length was longest of all the were also comprised of organic detritus, larger June samples, these fish did not feed so much. insects, Harpacticoida, Bivalvia (veliger larva) Their gut contents were comprised of organic and Balanomorpha (nauplius larva). detritus and/or larger insects. The amount of Table 2 gives the results of the gut content gut contents was greatest at station 13, where O analysis of the half beak larvae as ranges of total . davisae and Acartia omorii were the dominant length. As categorized by total length ranges, the food items. At Ushitsu Port, the gut contents following food items were abundant: 7.8•`10.0

Table 2. Number of individuals for each species of gut contents on the range of total length of the halfbeak larvae and juveniles Growth and Feeding Habits of Halfbeak Larvae 51 mm: Oithona spp. nauplius; Evadne nordmanni, warm water species such as Salpid Dolioletta pollen of pine trees; Paracalanus type nauplius; gegenbauri, Salpa fusiformis and Copepod O. and Favella ehrenbergii,10.1•`20.0 mm: Oithona plumifera. On the other hand, at the stations in spp. nauplius, pollen of pine trees, Paracalanus Nanao Bay (stations 11 and 14), the abundance type nauplius, and O. davisae, copepoda eggs; was three to four times greater than that of the

20.1•`30.0 mm: O. davisae, A. omorii, Acartia northwest area (1.0•~104•`1.5•~104 finds./haul) spp. nauplius, and O. plumifera; 60.1•`70.0 mm: and the species which are observed in eutrophic

Bivalvia larvae, Balanomorpha nauplius, and area (i.e. copepod O. davisae and appendicularia

Harpacticoida; 70.1•`80.0 mm: Brachyura zoea, Oikopleura dioica) distinguished Nanao Bay from

Penilia avirostris, Bivalvia larvae, Harpacticoida, the northwest area. In late June, the abundance and Paracalanus parvus; 80.1•`90.0 mm: Insects, was greater than in early June, especially at

Harpacticoida, and Bivalvia larvae; 90.1•`94.3 station 14 where the abundance of O. davisae was mm: Insects, Bivalvia larvae, and P. parvus. about ten times greater than at other stations.

The main food of the smaller halfbeak larvae The amounts of the copepod nauplii such as was Oithona spp. nauplii and Paracalanus type Paracalanus type, Oithona spp., Acartia sp. at nauplii, and that of the larger larvae was Insects, this station were not as great as at other

Harpacticoida and Bivalvia larvae. stations, and other copepod nauplii were

dominant. Oithona spp. nauplii may have been

4. Field survey of zooplankton underestimated because the nauplii size of the

The zooplankton fauna observed in early dominant O. davisae is too small to collect

June, around the northwest area of Toyama Bay completely.

(stations 2 and 7), was composed mainly of Figure 3 shows the percentage of the main

Fig. 3. Comparison between gut contents of halfbeaks and plankton items collected at stations 2 and 11 in early June 1999. Left side represents gut contents and right side represents plankton organisms; upper side is station 2 and lower side is station 11. 52 F. Oya, T. Tsuji, and S. Fujiwara taxonomic groups that appeared in both the that until 30 mm TL, the constant ƒ¿ is smaller gut contents of half beak larvae and in plankton (ƒ¿=2.4) . However, beyond 60 mm TL, ƒ¿ (3.7) is samples collected at the same time, at the larger than it was in the rearing study. There same sampling stations. Although there was are several studies on the growth of larvae under some problem of plankton sampling method, we natural conditions, but there are no studies attempted to compare these results. At station on earlier stage larvae. Kuniyuki and Koide8)

2, although Bivalvia (52%) dominated the gut observed growth based on the relationship content, more than 90% of the plankton samples between body length (L cm) and body weight were Copepods. At station 11, there was a similar (W g) of the fish from about 70 mm body length inconsistent tendency. Cladocera was the most to adult. They obtained a regression equation dominant species in the gut contents (61%), of W=0.00141 L3.25. This equation was regressed but Copepods comprised 63% of the plankton by a single equation and had no turning point. samples. Thus, we conjecture that food availability in

the natural environment was insufficient during

Discussion the earlier growth stages, but after a change in diet, growth increased as indicated by the

A turning point in allometric growth was constant ƒ¿. derived at ca. 30 mm TL for the halfbeak larvae The smallest specimen was 7.8 mm TL, which and juvenile specimens examined in this study. corresponds to a newly hatched larva3). It was

Below this length, the lower jaw grew obviously caught at station 12, in Nanao Bay. Half beaks in a positive allometric relationship with total make use of drifting seaweeds as spawning length (Fig. 2; Table 1) . This turning point was beds, although in the case of a large standing calculated at 28.3 mm TL from the intersection stock, they spawn at seaweed beds along the of two allometric equations. Yamamoto and coast12). There is an anti-clockwise tidal current

Nishioka7 showed that metamorphosis is in Toyama Bay13), and it has been observed completed at 22-28 mm TL. Thus, the total length that drifting seaweeds reach the inner-bay area at the turning point corresponds to their length of Toyama Bay on this current. The origin of range. The value of constant ƒ¿ in the allometric these seaweeds is recognized as Okinoshima equation beyond the obtained TL was 0.69. The Island14). Although it is considered that the lower jaw does not grow proportionally with body smallest specimen hatched in Nanao Bay, we length. could not determine whether it was spawned

A turning point was derived at ca. 60 mm TL in drifting seaweeds or at the seaweed beds. from the allometric relationship between BW Therefore, we have to clarify the location of the and TL. The intersection was calculated at spawning ground in Toyama Bay.

56.7 mm TL from two allometric regression The food environments of several fish larvae equations. Food items of these two groups living in estuaries or coastal areas have been which were above and below 60 mm TL were studied. Because it is difficult to distinguish very different: the smaller group fed mainly on detritus from digested matter, those papers copepods including nauplii, copepodid and adult, probably deal with detritus as digested matter6). and the bigger group consumed mainly organic Unfortunately, we have no methods to evaluate detritus and larger insect with Bivalvia etc. the amount of detritus in larval stomachs and/

In the laboratory study, under the condition or intestines, because the amount of detritus is of abundant food availability, the relationship so low that we cannot weigh it. If the amount between BW and TL had a high constant ƒ¿ (3.3), of matter in the gut is recorded by weight and no turning point beyond 60 mm TL, derived from a calculation, it is possible that throughout the rearing period4). When the data the feeding intake is under-estimated due to of this study is compared with data collected neglected amounts of organic detritus. Although under laboratory rearing conditions, we found halfbeak larvae larger than 60 mm TL ate lesser Growth and Feeding Habits of Halfbeak Larvae 53

amounts than those smaller than 30 mm TL per Paracalanus type. As these facts show, copepod

individual, it was shown that the growth rate nauplii such as Oithona spp. and Paracalanus

of the former is higher than that of latter. This type play an important role as the main food

indicates that detritus is an important source of items in the earlier stage larvae of fish. food, in addition to other prey items. Detritus plays an important role as a food source especially Acknowledgements for young fish and/or fish larvae growing in

estuaries or coastal areas. Half beak larvae reared We are grateful to the captain and crew of the to 9 mm TL did not feed on detritus7). Our results R/V•gRokkou-Mare•h of the Ishikawa Prefecture

also show that larvae less than 30 mm TL do not Fisheries Research Center for assistance with feed on detritus, and those less than 20 mm TL the field sampling. We thank two anonymous

do not consume it at all. We have to give thought referees for valuable comments, and also Ms. to methods that can assess very small amounts Linda Worland for reviewing the English of our

of detritus. manuscript. The main food items of halfbeak larvae

are reported in several studies: Yamamoto References and Nishioka7) report that the larvae take

small crustaceans, especially copepodite and 1) Sadakata, T., T. Tsuji, and T. Shikata (1998): Analysis nauplii of copepods, and mollusca larvae. Wada of catches of halfbeak Hyporhamphus sajori by two- and Kuwahara6) report the copepod Euterpina boat seine in Ishikawa Prefecture. Bull. lshikawa Pref. Fish. Res. Center, 1, 1-7 (in Japanese).

acutifrons, and cladocera such as Penilia 2) Tsuji, T. and T. Sadakata (2000): Present status of the avirostriis, E. tergestina and Podon polyphemoides. halfbeak fisheries in Japan. Bull. Ishikawa Pref. Fish. Both papers noted that the halfbeak larvae did Res. Center, 2, 1-11(in Japanese). not consume the protozoans Noctiluca scintillans 3) Oya, F, and K. Oka (1981): Cultivation of the halfbeak larva in the laboratory-with special reference to

and Favella spp. In our results, tintinnid ciliates allometric growth. Aquaculture (Suisanzoshoku), 29(1), such as Parafavella sp., Favella ehrenbergii were 57-61 (in Japanese). eaten by larvae less than 20 mm TL, although N. 4) Nakata, H., K. Oka, and F. Oya (1982): Cultivation of the half beak larva in the laboratory-with special refer- scintillans were not eaten. These facts indicate ence to feeding habits. Aquaculture (Suisanzoshoku), that early stage halfbeak larvae do not have 30(1), 28-32 (in Japanese). strong food preferences in comparison to gadoid 5) Yokota, T., M. Toriyama, F. Kanai, and S. Nomura larvae15).Fig. 3 shows discordance between gut (1961): Studies on the feeding habit of fishes. Rep. Nankai Reg. Fish. Res. Lab., 14, 1-231 (in Japanese). contents and plankton composition, but using 6) Wada, Y. and A. Kuwahara (1994): Feeding habits of the only this data, we cannot estimate whether they halfbeak Hemiramphus sajori larvae in Kumihama Bay have food preferences. However, as mentioned and the adjacent waters, Japan Sea. Research reports of above, it has been observed that half beak larvae Kyoto Marine Center, 17, 59-65 (in Japanese). 7) Yamamoto, G. and C. Nishioka (1947): On the rearing selectively consume Pontellidae nauplii or O. of the larvae of Japanese halfbeak, Hyporampus sajori

davisae as individuals. (Temminck & Schlegel). Seibutu, 2(5), 136-140 (in Hirakawa et al.16) studied the dietary compo- Japanese). sition of anchovy larvae in Toyama Bay. The 8) Kuniyuki, K. and T. Koide (1962): An ecological study of the Hemiramphus sajori (Temminck et Schlegel). anchovy larvae (SL.: 4.1-8.0 mm) took mainly Rep. Naikai Reg. Fish. Res. Lab., 18, 1-9 (in Japanese). copepod nauplii with some species. Among 9) Uchida, K. (1930): Life history of halfbeak. Nippon these, nauplii cyclopoid (Oithona spp.) were the Gakujutu Kaihou, 6, 557-580 (in Japanese). most important dietary component, with calanoid 10) Bjð±rnberg, T. K. S. (1972): Developmental stages of some tropical and subtropical planktonic marine (mainly Paracalanus type) second. The study on copepods. Stud. Fauna Curacao, 40, 1-185. the diet of larval sardine, also in Toyama Bay, 11) Koga, F. (1973): Life history of copepods especially of showed a similar tendency17).Our results indicate nauplius larvae ascertained mainly with cultivation of that the main foods of halfbeak larvae, smaller animals. Bull. Plankton Soc. Japan, 20(1), 30-40 (in than 20 mm TL, are nauplii of Oithona spp. and Japanese). 54 F. Oya, T. Tsuji, and S. Fujiwara

12) Sobajima, N. and H. Funata (1988): Fisheries biology 15) Last, J. M. (1978): The food of three species of Gadoid on halfbeaks, Hyporhamphus sajori (T. et S.), in the larvae in the eastern English Channel and southern western Wakasa Bay, Japan Sea I. Spawning aspects. North Sea. Max Biol., 48, 377-386. Bull. Kyoto Ocea. Fish. Sci.,11, 51-60 (in Japanese). 16) Hirakawa, K., T. Goto, and M. Hirai (1997): Diet 13) Uchiyama, I. (1993): Mean geostrophic currents in composition and prey size of larval anchovy, Engraulis Toyama Bay and adjacent waters. Bull. Toyama Pre. japonicus, in Toyama Bay, southern Japan Sea. Bull. Fish. Exp. Stn., 4, 11-30 (in Japanese). Japan Sea Natl. Fish. Res. Inst., 47, 67-78. 14) Fujita, D. (1999): Drifting seaweeds and the related 17) Hirakawa, K. and T. Goto (1996): Diet of larval sardine, fish resources along the Sea of Japan coast of central Sardinops melanostictus in Toyama Bay, southern Japan Honshu: Review and perspective. Aquabiology, 21(5), Sea. Bull. Japan Sea Natl. Fish. Res. Inst., 46, 65-75. 421-426 (in Japanese).

富 山湾 に お け る サ ヨ リ仔 稚 魚 の相 対 成 長 と摂 餌 生 態

大屋二三・辻 俊宏 ・藤原 しのぶ

サ ヨ リHyporhamphus sajoriの 相 対成 長 と摂餌 生 態 の調査 が富 山湾 の石 川県 沿 岸 で行 わ れた。 全長 10mmか らサ ヨ リの特 徴 で ある下 顎が伸 張 しだ し,全 長 と下 顎 の間 の比成 長 関係 に は全 長28mm付 近 に不 連 続点 が あ る と推 察 され,こ の付 近が 変態 完 了の全 長 に相 当す る もの と思 わ れ た。全長30mm以 下 の仔魚 は主 としてOithona spp.やPaRacalanus typeの か いあ し類 の ノー プ リウス幼生 を摂 餌 してお り,全 長60mm以 上 の稚魚 は昆虫 や有機 デ トリタス を摂餌 して いた。 成長 初期 には選択 性 が認 め られ たが,成 長 が進 む につれ餌 料 に対 す る選択 性 は弱 ま る もの と推察 された 。全長 に対 す る体重 の増 加率 が全 長57mmを 超 える と大 き くなるが,こ れ は食 物 の変化 に よる もの と思 われ た。