Journal of the Oceanographical Society of Japan Vol.41, pp.89 to 97, 1985

The Diet of Mesopelagic Fish from the

Pacific Coast of Hokkaido, Japan*

J.D.M. Gordon•õ, S. Nishida•ö and T. Nemoto•ö

Abstract: The diet of at least 28 species of mesopelagic fish from the Pacific coast of

Hokkaido was examined. The dominant family was the Gonostomatidae (42%) which was represented by five species. The most abundant species was Cyclothone atraria which together with the other species of this genus preyed predominantly on copepods. Euphausiids and

copepods were dominant in the diet of Gonostoma gracile. The next most abundant family

was the Myctophidae (32%) which was represented by seven species. The dominant species, Stenobrachius nannochir, preyed mainly on copepods. Copepods were also the dominant food

item of the other myctophids except for Lampanyctus jordani which fed mainly on euphausiids. The other important family was the Bathylagidae (21%). Leuroglossus schmidti was the

dominant species and its diet was more diverse with ostracods, copepods, molluscs and larva- ceans being the most important food items. Bathylagus ochotensis had a similar diet. Copepods were the most important food items for all but a few species and their occurrence in the fish stomachs was related to the known vertical distribution of both predators and prey.

Ostracods and euphausiids were also important prey items, the latter especially in large fish

species. Molluscs and larvaceans were restricted to the two species of the family Bathylagidae.

1.Introduction coast of Japan to the south of Hokkaido. Much of the early work on the feeding of mesopelagic fish in the North Pacific has been 2. Materials and methods reviewed by Hopkins and Baird (1977) and more The fish were collected by oblique tows with recently the food of the Hawaiian mesopelagic a 3-m Isaacs-Kidd midwater trawl during Cruise fish has been studied in some detail(Clarke, KH-82-2 of the R/V Hakuho Maru, Ocean 1978, 1980, 1982; Maynard, 1982). Gorelova Research Institute, University of Tokyo, in late and Tselyin (1979) and Gorelova (1980) have April and early May 1982. The locations of the investigated the feeding of gonostomatid fish of stations are shown in Fig. 1. Most of the fish the genus Cyclothone in the tropical Pacific. Although there have been many studies of the taxonomy and distribution of micronektonic fish in the waters around Japan there have been few studies on the food and feeding of these fish with the exception of the work of Okiyama (1971) on Maurolicus muelleri in the Japan Sea, Kawaguchi (1969) on Gonostoma gracile in the Kuroshio area and Suruga Bay and Ozawa et al. (1977) on Vinciguerria nimbaria to the south of Japan. In this paper we report on the food of a collection of mesopelagic fish from the Pacific

* Received 1 October 1984; in revised form 20 December 1984; accepted 21 January 1985.

†Scottish Marine Biological Association, P.O. Box 3, Oban, Argyll, Scotland.

‡Ocean Research Institute, University of Tokyo, Fig. 1. Sampling stations for Hakacho Maru 1-15-1, Minamidai, Nakano, Tokyo 164, Japan. cruise KH-82-2 in 1982. 90 Gordon, Nishida and Nemoto from Station 1-2 were used for biochemical instances the wet weight of the stomach contents analysis and no fish were obtained from Station was recorded. The results were expressed as. 2-4 which was a shallow tow from 0-40m during the percentage frequency of occurrence (F), which the day. Times of sunrise and sunset during is the number of stomachs containing a particular the sampling period were 04.12 and 18.08 h, food item expressed as a percentage of the total respectively, and except for two tows (Stations number of stomachs containing food, and also 2-5 and 2-6) at night the rest were during the as Cn, the number frequency of each food item daytime. expressed as a percentage of the total number The fish, which had been preserved in 5% of food items. Unidentified tissue or unidentified formalin/seawater, were identified, measured Crustacea was treated as one food item in the (standard length) and the stomach contents were calculation of Cn. removed. The prey items were identified and counted as far as possible after rejecting those 3.Results which were the result of net feeding. In some The species composition and the number of

Table 1. The species composition and the number of individuals of each species collected by IKMT during Cruise KH-82-2 of the R/V Hakuho Maru. The numbers of stomachs containing food are shown in parenthesis.

a Larval and juvenile specimens not examined . The Diet of Mesopelagie Fish 91 specimens of each species at each station and for the juveniles of Nectoliparis pelagicus, Oneirodes all stations combined are given in Table 1. sp. and Lampanyctus steinbecki were not ex- A total of 615 fish belonging to at least 28 amined. The six juvenile macrourid specimens species were collected. The dominant family were not identified further. All the specimens was the Gonostomatidae (42%) and of these of Alepocephalus sp., Tarletonbeania crenularis 77% were Cyclothone atraria. Next in im- and Stenobrachius sp. had empty stomachs. portance was the family Myctophidae (32%) of GjOsaeter and Kawaguchi (1980) in their review which Stenobrachius nannochir accounted for of the world resources of mesopelagic fish divide 74% of the total number. The other important the northwest Pacific into three regions with family was the Bathylagidae (21%) of which different biomass distributions and the present 79% were Leuroglossus schmidti, but a large sampling area is included in the subarctic region. proportion of these were postlarval or meta- The dominant myctophid and gonostomatid fish morphosing stages. The mean number, length of the subarctic area noted by Gjcbsaeter and and length range for the species of these families Kawaguchi (1980), the species lists given by are given in Table 5. The number of stomachs Ueno (1971) for this area off Hokkaido and by containing food is given in parenthesis, but for Pearcy et al. (1979b) for the Bering Sea and reasons mentioned above all the specimens of the adjacent North Pacific all show similarities G. gracile, Bathylagus pacificus, Protomycto- to the faunal composition as shown in Table 1. phum thompsoni, Lampanyctus jordani and S. 3.1. Family Gonostomatidae nannochir from Station 1-2 were not examined. Previous feeding studies on the fish of the The stomach contents of a metamorphosing speci- genus Cyclothone in the Pacific have shown that men of Opostomias mitsuii, the larval speci- a high proportion of fish have empty stomachs mens of Alectrias sp. and Lycodapus sp. and and those that have been feeding generally con-

Table2. The diet of Cyclothone atraria, C. pseudopallida and Gonostoma gracile for all stations combined. F is the number of stomachs containing a food item expressed as a percentage of the total number of stomachs containing food and Cn is the number frequency of each food item expressed as a percentage of the total number of food items. 92 Gordon, Nishida and Nemoto tain only one food organism, usually a copepod about equal importance. The mean number of or an ostracod (Gorelova, 1980; Maynard 1982). prey items per stomach was 1.3 with a range Most of the published information concerns the from 1 to 4. Gorelova (1980) examined 91 speci- species C. alba, C. pallida and C. pseudopallida mens of C. atraria but she only found two which were not abundant in this collection. individuals with food. The diet of C. pseudo- The detailed diet of C. atraria, C. pseudo- pallida was similar to that of C. atraria except pallida and G. gracile is given in Table that all the identified copepods belonged to the 2. Copepods were the dominant food of C. genus Gaidius. The mean number of prey atraria with species of the genera Gaidius and items was 1.2 with a range from 1 to 3. Gore- Pleuromamma being most common. Ostracods lova (1980) also found that copepods were the and unidentified crustacean fragments were of dominant food of C. pseudopallida although

Table 3. The diet of Stenobrachius nannochir, S. leucopsarus, Protomyctophum thompsoni, Lampanyctus jordani and Diaphus theta. For explanation of F and Cn see Table 2. The Diet of Mesopelagic Fish 93 ostracods and occasionally amphipods, euphausiids siids were the most important food items. and fish were recorded. Maynard (1982) found The diet of P. thompsoni was dominated that copepods were the dominant food of C. by copepods and unidentified crustacean pseudopallida followed by crustacean remains fragments. The copepods were all highly and ostracods. 96% of the copepods were cala- digested and could not be identified to species. noids and of these 53% were Pleuromamma sp. The stomach content weights from Station 2-5, Only two of the eight specimens of C. alba which was the only station where this species. contained food, one having an unidentified was caught at night, were considerably greater copepod and the other crustacean fragments. than those of any other station which may The single stomach of C. pallida which contained suggest that the species feeds at dusk. Ten. food had an unidentified copepod. of the 15 specimens of L. jordani contained. The food of G. gracile was usually highly food but all the stomachs were partially digested and although there were no signs everted, digested food in the mouth being treated. of eversion of the stomach regurgitated food as stomach contents. The stomachs of the was frequently found in the entrance of the remaining fish were completely everted. Euphau- oesophagus. If this food showed obvious signs siids were the dominant species consumed and. of digestion it was included with the stomach one stomach contained 12 specimens. Although. contents. Euphausiids were the dominant food. the frequency of occurrence of copepods was. item followed by crustacean remains and cope- high, there were never more than two specimens. pods. Kawaguchi (1969) examined 90 specimens per stomach. The mean number of prey items. of G. gracile from Suruga Bay and 126 from per stomach was 4.4 with a range from 1 to 12. the Kuroshio area and found that copepods were Copepods dominated in the diet of Diaphus the dominant food items at a frequency of theta and in some stomachs they were very occurrence of 50 and 28 %, respectively, com- numerous. The dominant species were Metridia- pared with euphausiids which accounted for 3 and 16%, respectively. Other food items which Table 4. The diet of metamorphosed Leuro- were rare in their occurrence were amphipods, glossus schmidti and Bathylagus ochotensis. mysids, chaetognaths and fish. For explanation of F and Cn see Table 2. 3.2. Family Myctophidae The details of the diets of five species of mycto- phid are given in Table 3. Copepods were the most important constituent of the diet of S. nannochir and although many species were consumed the species of the genera Gaidius and Pleuromamma were the most abundant, Ostracods and to a lesser extent chaetognaths were important in the diet while amphipods and mysids were rare. The mean number of food items per stomach was 1.7 with a range from 1 to 8. Although only 9 S. leucopsarus contained food, copepods were the dominant prey with species of the genera Metridia and Pleuromamma being the most common. Euphausiids were the next most important food item while ostracods and amphipods were of minor importance. The mean number of food items per stomach was 2.4 with a range from 1 to 14. Previous studies on the food of S. leucopsarus by Collard (1970) and Tyler and Pearcy (1975) off the Pacific coast of North America have shown that copepods and euphau- 94 Gordon, Nishida and Nemoto okhotensis and M. pacifica and in the stomach that of copepods and ostracods, in terms of of a 57 mm fish there were 42 and 15 individuals, volume they were of considerable significance. respectively, while that of a 69mm fish con- The molluscan material in the stomachs was tained 48 M. okhotensis, 16M. pacifica and 22 ascribed to two species and by examining plank- Metridia sp. The mean number of prey items ton samples from Stations 1-1 and 1-2 collected per stomach was 27.6 with a range of 3 to 106. by the finer meshed ORI net, they were identi- Tyler and Pearcy (1975) observed that the copepod fied as the pteropods Limacina helioina and Metridia lucens was important in the diet of ? Clio pyramidata. The mean number of prey this species but of 129 fish containing food the items was 2.5 with a range from 1 to 6. average number of copepods per stomach was 1.6. Bathylagus ochotensis had a similar diet to L. 3.3. Family Bathylagidae schmidti (Table 4). Molluscs, probably of the L. schmidti was the most abundant bathy- same two species, and larvaceans dominated the lagid fish but of the 101 specimens collected. diet in terms of frequency of occurrence although only 27 were fully metamorphosed. The re- in terms of numbers copepods were dominant. mainder were either postlarvae which had only The mean number of prey items per stomach a few melanophores or metamorphosing fish with was 4.4 with a range from 1 to 14. The single a pigmented peritoneum. Sixty stomachs of specimen of B. pacificus examined had unidenti- postlarvae or metamorphosing fish were examined fied tissue in its stomach. and all were found to be empty. 70.4% of the 3.4. Other Families metamorphosed fish had food in their stomachs Chauliodus macouni (Chauliodontidae) was re- and their diet is given in Table 4. Copepods, presented in the collection by 7 fish ranging ostracods, crustacean fragments, molluscs, lar- from 98 to 142 mm in length. Unidentifiable vaceans and unidentified tissue were the most fish fragments were found in the stomachs of important food items. The texture of the un- two specimens. Two specimens of Tactostorna identified tissue suggested that it was mainly macropus (Melanostomiidae) with standard molluscan and although the Cn value for molluscs, lengths of 123 and 129 mm were collected. The larvaceans and unidentified tissue are lower than former contained highly digested remains of the

Table 5. The total number, the mean length and the length range of fish belonging to the families Gonostomatidae, Myctophidae and Bathylagidae. The values of F and Cn of the major taxa of food organisms are summarised. A "-" indicates that all or most of the stomachs examined were empty. The Diet of Mesopelagic Fish 95 headr egion of afish and the same stomach also most abundant species were the copepodite stages contained crustacean remains which may have of Calanus plumchrus, C. cristatus and Eucalanus been derived from the prey fish. The postlarva bungii bungii and the copepodites and adult of Theragra chalcogramma (Gadidae) had un- females of Metridia pacifica (=M. lucens in identifiable crustacean remains in its stomach. Furuhashi, 1966; Morioka, 1972), Pseudocalanus The two juvenile Melamphaes sp. (Melamp- minutus and Scolecithricella minor. The mid haidae) contained copepod fragments. One of layers (ca. 300 to 700 m) are occupied by the the two postlarvae of Hemilepidotus (Cottidae) adults of C. plumchrus and C. cristatus which contained copepods and a larval euphausiid and do not vertically migrate. The adult males of the other contained unidentified tissue. Three M. pacifica remain in this layer by day and specimens of N. pelagicus (Cyclopteridae) were night but the copepodites and adult females examined and two contained food. A fish of migrate into this layer during the day. The 49mm standard length contained 5 copepods dominant species of the mid layer also include and a large mass of unidentified tissue and one Gaidius spp., Gaetanus spp., Pleuromamma of 48mm contained the fragmented remains scutulata and the adult females of M. okhotensis. of 2 copepods. The deeper layers (below 700m) were inhabited by Lucicutia spp., adult males and females of 4. Discussion C. cristatus and C. pacificus (= C. finmarchicus The diets of some of the more abundant fish in Furuhashi, 1966; Morioka, 1972), Spinocalanus species in this collection are summarized by abyssalis and other bathypelagic species. major prey taxa in Table 5. The importance Identified copepods in fish stomach contents of copepods in the diets of all species is obvious. were dominated by species from the mid and Euphausiids were absent from smaller species deep layers. Adult copepods accounted for 73% such as Cyclothone atraria, C. pseudopallida and of all copepods identified. Broken down into P. thompsoni but were an important dietary genera, adults accounted for 91, 67 and 74% component in large species such as G. gracile and of Pleuromamma, Gaidius and Metridia, re- L. jordani. Molluscs and larvaceans occurred only spectively. Because C. atraria and C. pseudopal- in the food of the bathylagid species. Cailliet lida inhabit the mid layers and are non-mig- (1972) found that Leuroglossus stilbius collected ratory (Willis and Pearcy, 1982), the predominance off Southern California fed predominantly on lar- of copepods such as Gaidius and Pleuromamma vaceans and salps with ostracods, small copepods spp. is to be expected. The myctophid and zoea larvae as minor food items. He con- Stenobrachius leucopsarus has a complex depth sidered that it was morphologically adapted to distribution off the coast of Oregon (Pearcy, et eat relatively inactive small organisms. The al., 1979a). They showed that part of the popu- morphology of L. schmidti shows that it is lation vertically migrates and the rest remains poorly equipped to consume or capture active at depth. An analysis of the diets suggested prey because the teeth and swimming muscles that the migrators fed in the upper layers during are more poorly developed than in other meso- the night and in the middle layers during the pelagic fishes (Okiyama : personal communi- day. Although only a few fish were examined cation). Although euphausiids were consumed in this study they contained copepods represent- by both B. ochotensis and L. schmidti the ative of both the upper and mid layers. S. euphausiids were either Euphausia pacifica, the nannochir is a nonmigratory species (Willis and smallest species collected, or the larval stages of Pearcy, 1982). Its diet consisted of at least 12 other species. different species of copepod which either perma- The overall dominance of copepods makes it nently inhabited the middle and deep layers or of interest to consider this group in more detail. were vertical migrators. Diaphus theta and The vertical distribution of copepods in this area B. ochotensis are vertically migrating species during the spring and early summer has been (Pearcy, et al., 1977). The importance of investigated by Furuhashi (1966), Morioka (1972) Metridia spp, in their diets may indicate that and Hattori and Nishizawa (personal communi- they feed both in the upper and mid layers. cation). In the upper layer (O to ca. 200 m) the L. schmidti also feeds on Metridia spp. and 96 Gordon, Nishida and Nemoto

may also be a vertical migrator. In: Oceanic Sound Scattering Prediction ed. by N. R. Andersen, and B. J. Zahuranec, Marine Acknowledgements Science, Vol.5, Plenum Press, New York and The authors gratefully acknowledge the assis- London, pp.325-360. tance of Drs. K. Kawaguchi and M. Okiyama Kawaguchi, K.(1969): Ecological study of the and Mr. M. Miya of the Ocean Research Insti- micronektonic fishes of the western Pacific Ocean. Ph. D. Dissertation, The University of Tokyo, tute for their help in identifying the fish and Japan, 218 pp. the useful discussions on their ecology. We also Maynard, S. D.(1982): Aspects of the biology of thank Dr. Y. Hirota of the Japan Sea Regional mesopelagic fishes of the genus Cyclothone (Pisces: Fisheries Research Laboratory, for identifying Gonostomatidae) in Hawaiian waters. Ph. D. the euphausiids and Dr. T. Okutani of the Dissertation, University of Hawaii, Hawaii. Tokyo University of Fisheries for identifying 257 pp. the pteropods. One of us (JDMG) gratefully ac- Morioka, Y.(1972): The vertical distribution of knowledges the financial support of the Ministry calanoid copepods off the southeast coast of of Education, Science and Culture, and the Hokkaido. In: Biological Oceanography of the Director of the Ocean Research Institute of the Northern North Pacific Ocean, ed. by A. Y. Takenouchi, Idemitsu Shoten, Tokyo, pp.309- University of Tokyo, Professor N. Nasu and 321. his staff for all the help during his visit to the Okiyama, M.(1971): Early life history of the gono- Ocean Research Institute. stomatid fish Maurolicus muelleri (Gmelin) in the Japan Sea. Bull. Japan Sea Regional Fisheries References Laboratory, 23, 21-53. Cailliet, G. M.(1972): The study of feeding habits Ozawa, T. K., Fujii, K. and Kawaguchi, K.(1977): of two marine fishes in relation to plankton Feeding chronology of the vertically migrating ecology. Trans. Amer. Micros. Soc., 91, 88-89. gonostomatid fish Vinciguerria nimbaria (Jordan Clarke, T. A.(1978): Diel feeding patterns of 16 and Williams) of southern Japan. J. Oceanogr. species of mesopelagic fishes in Hawaiian waters. Soc. Japan., 33, 320-327. Fish. Bull. U. S., 76, 495-513. Pearcy, W. G., Krygier, E. E., Mesecar, R. and Ram- Clarke, T. A.(1980): Diets of fourteen species of say, F.(1977): Vertical distribution and mig- vertically migrating mesopelagic fishes in Hawaii- ration of oceanic plankton off Oregon. Deep-Sea an waters. Fish. Bull. U. S., 78, 619-640. Res., 24, 223-245. Clarke, T. A.(1982): Feeding habits of stomiatoid Pearcy, W. G., Lorz, H. V. and Peterson, W.(1979a): fishes from Hawaiian waters. Fish. Bull. U. S., Comparison of the feeding habits of migratory 80, 287-304. and non-migratory Stenobrachius leucopsarus Collard, S. B.(1970): Forage of some eastern Pacific (Myctophidae). Mar. Biol., 51, 1-8. midwater fishes. Copeia, 1970 (2), 348-354. Pearcy, W. G., Nemoto, T. and Okiyama, M.(1979b): Furuhashi, K.(1966): Studies on the vertical distri- Mesopelagic fishes of the Bering Sea and the bution of copepods in the Oyashio region east of adjacent northern North Pacific Ocean. J. Oceano- Japan and in the Kuroshio region south of Japan. gr. Soc. Japan., 35, 127-135. Publ. Seto Mar. Biol. Lab., 14, 295-322. Tyler, H. R. and Pearcy, W. G.(1975): The feeding Gjosaeter, J. and Kawaguchi, K.(1980): A review habits of three species of lanternfishes (Family of the world resources of mesopelagic fish. FAO Myctophidae) off Oregon, USA. Mar. Biol., 32, Fisheries Technical Paper, No.193, FAO, Rome, 7-11. 1980. Ueno, T.(1971): List of the marine fishes from the Gorelova, T. A.(1980): Feeding of deep-sea fish of waters of Hokkaido and its adjacent regions. Sci. the genus Cyclothone (Gonostomatidae, Pisces). Rep. Hokkaido Fish. Experimental Station, 13, Oceanology, 20, 209-213. 61-102. Gorelova, T. A. and Tselyin, N. B.(1979): Feeding Willis, J. M. and Pearcy, W. G.(1982): Vertical of mesopelagic fish of the genus Cyclothone. distribution and migration of fishes of the lower Oceanology, 19, 736-739. mesopelagic zone off Oregon. Mar. Biol., 70, 87- Hopkins, T. L. and Baird, R. C.(1977): Aspects of 98. the feeding ecology of oceanic midwater fishes. The Diet of Mesopelagic Fish 97

太平洋北海道沖 にお け る中層 性魚類 の食 性

J. D. M. Gordon*, 西 田 周 平**,根 本 敬 久**

要 旨:太 平洋 北 海道 沖 で採 集 され た,28種 を含 む 中 層 性 た が,Lampanyctus jordaniの み は主 と して お きあ み 類 魚 類 の食 性 を 調査 した。 卓 越 した科 は ヨ コエ ソ科(5種, を 摂 食 して い た 。 そ の他 の重 要 な科 は ソ コイ ワ シ科(3 42%)で あ った 。 卓 越種 はCyclothone atrariaで あ り, 種,21%)で あ っ た。 卓 越 種Leuroglossus schmidtiの 本 属 の他 の種 と と もに主 と して か い あ し類 を 摂 食 して い 餌 料 は他 の魚 種 に比 べ 多様 で,介 形 類,か い あ し類,軟 た 。 お きあ み類 とかい あ し類 はGonostoma gmcileの 主 体 類 お よ び幼 形 類 が 本 種 の 主 要 な 餌 生 物 で あ った. 要 な餌 料 で あ った。 つ ぎ に卓 越 した 科 は ハ ダ カ イ ワ シ科 Bathylagus ochotensisも 同 様 の 餌 料 を 摂 食 して い た 。 (7種,32%)で あ った。 卓 越 種 のStenobrachius nanno- か い あ し類 は大 部 分 の魚 種 に お い て最 も重 要 な 餌 料 で ehirは 主 と して か い あ し類 を 摂食 して い た 。 か い あ し類 あ り,そ の魚 類 胃 内容 物 へ の 出 現 と,捕 食 者 と餌 生 物 の は他 のハ ダ カ イ ワ シ科魚 類 に おい て も主要 な餌 料 で あ っ 鉛 直 分 布 に関 す る従 来 の知 見 につ い て 論 議 した.介 形 類 と お き あ み類 も重要 な餌 生 物 で あ り,と くに 後 者 は大 型 * Scottish Marine Biological Association, の魚 種 に おい て重 要 で あ った.軟 体 類 と幼 形 類 は ソ コ イ P. O. Box 3, Oban, Argyll, Scotland. ** 東 京 大 学 海 洋 研 究 所 ワ シ科 の2種 に特 異 的 に 摂 食 され て い た.

〒164東 京 都 中 野 区 南 台1-15-1