Some Aspects of the Biology of the Micronektonic Fish Cyclothone Pallida and C

Journal of the Oceanographical Society of Japan Vol.42, pp.473 to 480,1987

Some Aspects of the Biology of the Micronektonic Fish Cyclothone pallida and C. acclinidens (Pisces: Gonostomatidae) in Sagami Bay, Central Japan

Masaki Miya†and Takahisa Nemoto†

Abstract: Some aspects of the biology of the micronektonic fishes Cyclothone pallida and C. acclinidens are described on the basis of samples taken during a series of 20 cruises from December 1982 to November 1985 at a fixed station near the center of Sagami Bay, Central Japan. C. pallida is a regular component of the Cyclothone population in Sagami Bay, being found in more than 90% of the samples. On the other hand, C. acclinidens was encountered sporadically, being found in less than 25% of the samples. The depth range of C. pallida is estimated to be about 400-1,000 m. It spawns mainly during the spring and summer in Sagami Bay. C. pallida releases about 1,000-3,000 eggs and may spawn several times during its life span. On the average, it reaches 18.5 mm standard length (SL) in one year, 24 mm SL in two years and 29.5 mm SL in three years during its subadult stage. Extrapolation of the growth curve suggests that males and females attain first sexual maturity in three to four years at 30-35 mm and five to six years at 40-45 mm SL, respectively. Cyclothone pallida is concluded to have a regular life cycle in Sagami Bay. It remains uncertain whether or not C. acclinidens reproduces in this area.

1. Introduction 1973; Badcock, 1982). C. pallida ranks fourth Six species of the abundant meso- and bathy- in numerical abundance among Cyclothone in pelagic fish genus Cyclothone (family Gono- Japanese waters (Kawaguchi, 1969), occurring stomatidae) occur in Japanese waters (Kawa- mainly between 40•KN and S latitude in the guchi, 1971; Miya and Nemoto, 1987). Of these, Pacific Ocean. C. acclinidens is particularly three species, Cyclothone alba Brauer, C. pseudo- abundant in the lower latitudes of the eastern pallida Mukhacheva and C. atraria Gilbert, Pacific and its occurrence recorded up to now constitute more than 98% of the number of in Japanese waters is represented by only two Cyclothone caught (Kawaguchi, 1969). Patterns specimens (Kawaguchi, 1971). C. obscura is of the vertical distribution, reproduction and chiefly collected in the bathypelagic zones of growth of these three dominant species in Sagami equatorial waters, though Miya and Nemoto Bay have been revealed from the study of samples (1987) found a single specimen among over 19,000 taken during either part or all of 20 cruises Cyclothone from Sagami Bay. Thus Sagami Bay over three years (Miya and Nemoto, 1986a, b, is located either near or at the northern geo- 1987.). However, there is no information on graphical limits of these less abundant species. the biology of the less dominant Cyclothone Despite their abundance and ubiquity in the species, C. pallida Brauer, C. acclinidens Gar- subtropical and tropical waters, aspects of their man and C. obscura Brauer in Sagami Bay. biology, especially reproduction and growth, These less abundant Cyclothone are cosmo- remain poorly known (cf. Maynard, 1982). In politan species and their centers of abundance this paper we first examine the patterns of apparently lie in subtropical and tropical waters occurrence of Cyclothone pallida and C. acclini- (Mukhacheva, 1964, 1967, 1974; Kobayashi, dens in Sagami Bay, and then describe and

*Received 18 August 1986; in revised form 13 discuss vertical distribution, reproduction and

October 1986; accepted 30 October 1986. growth of C. pallida on the basis of samples collected near the center of Sagami Bay during †Ocean Research Institute, University of Tokyo, 1-15-1, Mimmidai, Nakano-ku, Tokyo 164, Japan. a series of 20 cruises from December 1982 to 474 Miya and Nemoto

November 1985. Some aspects of the biology nets, Motoda, 1971), which are equipped with of C. acclinidens are also noted on the basis of closing devices. Five to seven MTD nets with the same samples. a mouth diameter of 80 cm and a mesh opening of 0.68 mm were towed horizontally in a shallow

2. Materials and methods (ca. 200-600 m) and a deep (ca. 600-1,000 m) Since detailed description and discussion of series of hauls. A total of 13 day and 12 night the methods and sampling data were given in stratified samples were obtained during 2-3 Miya and Nemoto (1986b, 1987.), their outlines August 1983. are presented here. The samples were preserved in 5-10% buffered Samples were collected at a fixed station near formalin seawater. C. pallida and C. acclini- the center of Sagami Bay (35•‹00'N, 139•‹20'E, dens were separated, counted and standard ca. 1,500 m depth) from December 1982 to lengths (SL) were measured to the nearest 0.1 November 1985 during a series of 20 cruises of mm. All specimens except small ones of C. the R/V Tansei Maru of the Ocean Research pallida (<25_mm) were dissected, and a smear Institute, University of Tokyo. of a pair of whole gonads was examined under Fifty-nine oblique hauls were made during the a stereo microscope for sex determination. first 14 cruises from December 1982 to August Sexually indeterminate fishes were defined as 1984 using a large conical plankton net (ORI subadults. Ovaries were staged according to the net: mouth area, 2.0 m2; mesh opening, 0.69 mm, criteria used for Cyclothone alba (Miya and Omori, 1965). The net was towed three to Nemoto, 1986b) and diameters of at least 30 ova eight times during each cruise from the surface in the largest size class were measured to the down to an average depth of 1,056m. An nearest 10 tim using an ocular micrometer. Isaacs-Kidd plankton trawl (IKPT, Loeb, 1979) Mature males were distinguished on the basis with a mouth area of 7.3 m2 and a mesh open- of development of the nasal rosettes according ing of 0.5mm was used alternatively during the to Miya and Nemoto (1986b). last six cruises from December 1984 to November Analysis of age and growth was based on the 1985. The IKPT was towed obliquely two to length-frequency distributions in which data of eight times during each cruise from the surface the same months from different years were down to an average depth of 1,107 m. pooled for respective months. The probability The day and night vertical distributions were paper method of graphical analysis of polymodal investigated using Motoda horizontal nets (MTD distributions proposed by Cassie (1954) was used

MONTH Fig. 1. Changes of occurrence of (A) Cyclothone pallida and (B) C. acclinidens in Sagami Bay. Data of the same months from the same years were pooled for respective months. Vertical bars denote 1SD. Biology of Cyclothone pallida and C. acclinidens 475 to discriminate the modal lengths. among tows from the same month were greater than between-month variations. Whereas the 3. Results and discussion differences were significant for C. acclinidens 3.1. Seasonal occurrence of Cyclothone pallida (Kruskal-Wallis test, P<0.05) that occasionally and C. acclinidens occurs through the sampling series (Fig. 1). A total of 400 specimens of Cyclothone pallida Such significant differences were probably ref- and 28 specimens of C. acclinidens were collected erable to collections from some months (August during the 20 cruises. C. pallida was found in 1983 and 1984, and May 1985) when more than more than 90% of the oblique haul collections, half of the tows collected one to three C. accli- while catches with C. acclinidens were en- nidens specimens. countered sporadically, in less than 25 % of the 3.2. Vertical distribution of Cyclothone pallida samples from all oblique hauls. The MTD nets caught only five fish. Their Numerical abundance as indicated by the depth of capture was restricted to the depths number of fish under 100 m2 ocean surface of between about 550 and 950 m (Table 1). Be- C. pallida ranged from 11 to 50 with a mean cause the data are too few, presence or absence abundance of 29.8 fish, while that of C. acclini- of size stratification with depth and diel vertical dens ranged from 0 to 10 with a mean abundance migration cannot be inferred. of 2.6 fish. No definite seasonal tendencies Kawaguchi (1969) gave the depth range of were observed in the occurrence of either species

(Fig. 1). Mean numerical abundances of the Table 1. Cyclothone pallida catch three dominant species of Cyclothone in Sagami data by MTD horizontal hauls. Bay (C. alba, C. pseudopallida and C. atraria) based on the same samples are 472, 278 and 943 fish, respectively (Miya, unpublished data). Therefore among the six Cyclothone species that occur in Sagami Bay C. pallida and C. acclinidens rank fourth and fifth in numerical abundance, respectively. Monthly differences in numerical abundance were not significant for C. pallida (Kruskal- Wallis test, P>0.25), indicating that variations

Table 2. Monthly changes of maturation stages of female Cyclothone pallida. Arabic numerals in parentheses indicate the number of fish. Data of the same months from different years

were pooled for respective months. Data were not available for January and September. Asterisks denote females of late Stage III / V (mean ovum diameter >300 ƒÊm). 476 Miya and Nemoto

Table 3. Monthly changes in the number of mature males of Cyclothone pallida. Numbers in parentheses indicate the total number of males caught in each length category. Data were not available for January and September.

this species as 500-1,000 m in Sagami Bay, which Table 4. Fecundity counts of agrees with the present observation. Cyclothone Cyclothone pallida. pallida is a cosmopolitan species and its depth range varies greatly in different areas, from 400-700 m at 11•‹N, 20•‹W in the eastern North Atlantic (Badcock and Merrett, 1977) to 600- 1,300 m in Hawaiian waters (Maynard, 1982). Despite such variability, a pattern common to its vertical distribution is that C. pallida always occurs in the third layer within the genus' depth range regardless of the species composition

(Bond, 1974; Badcock and Merrett, 1976, 1977; VII/II appear in the size class between 40-45 Maynard, 1982). The top layers are occupied mm (Table 2), while all smaller mature males by either C. alba or C. braueri depending were found in the size class between 30 and on the area. C. pseudopallida and C. pallida 35 mm except for a single male of 28.9 mm SL always occur in the second and third layers, (Table 3). These facts indicate that female C. respectively, while the deeper-dwellers, if any, pallida matures and spawns at 40-45 mm, and such as C. livida, C. acclinidens or C. microdon, that males reach sexual maturity at 30-35 mm occupy the deepest layers. If such a pattern SL. The sizes of the smallest mature females applies to Sagami Bay, then the depth range of and males taken from other areas vary from 39 C. pallida would be about 400-1,000 m, a depth to 49 mm and from 25 to 28 mm, respectively range intermediate between that of C. pseudo- (Bond, 1974; Badcock and Merrett, 1976; May- pallida [400-600 m, Miya and Nemoto (1986a)] nard, 1982), which generally conform to those and C. atraria [450->1,000 m, Miya and of the present study. Nemoto (MS.)]. The occurrence of recovering spent females 3.3. Reproduction of Cyclothone pallida after the spawning season together with their Immature (Stage I+II) and maturing females size range (43.5-57.4 mm) which overlaps with

(Stage III/V) were collected throughout the those of the earlier stages (Table 2) suggest that year, but females nearly reaching ovulation (late C. pallida spawns more than once during its Stage III/V) were found only between March life span. Maynard (1982) also suggested the and August (Table 2). Although no ripe (Stage possibility of iteroparity of this species on the VI) or spent females (Stage VII) were found basis of his observation that size ranges of during this study, recovering spent females (Stage different developmental stages of females greatly VII/II) were collected between July and De- overlap one another. cember. These observations appear to reflect a The fecundity of females of late Stage III/V seasonal spawning of Cyclothone pallida, indi- (tagged with asterisks in Table 2) was estimated cating that it spawns mainly during the spring by counting the total number of eggs. Counts and summer months in Sagami Bay. Mature were made on a total of six females and the males, however, exhibit no clear seasonality in fecundity ranged from 1,840 (57.3 mm SL) to their occurrence (Table 3). 2,797 (54.4 mm SL) (Table 4). These values are The smallest females at Stages III/V and noticeably higher than those reported by Maynard Biology of Cyclothone pallida and C. acclinidens 477

(1982) on fishes from Hawaiian waters: 1,251 mm were discernible in the subadult length- (50.5 mm SL) to 1,454 (58.5 mm SL) (on the frequency distribution (Fig. 2). The smaller basis of his counts on fish with mean ovum number of the smallest modal length suggests diameter of >0.30 mm). No correlation between that recruitments have just appeared in this standard length and the number of eggs was month. found either in the present data or in those of On the assumption that each mode represents Maynard (1982). an year-class and that each year-class was born 3.4. Age and growth of Cyclothone pallida on 1 June which is the mid-point of the spawning Figure 2 shows the monthly length-frequency season, we can obtain an average growth curve distributions of Cyclothone Pallida. Almost all during the subadult stage of C. pallida (Fig. 3). fishes of < 30mm are subadults, while those A straight line was fitted arbitrarily to the >30mm are mostly either males or females. growth curve of C. pallida using a linear re- Sexual dimorphism is obvious, with the largest gression equation: male and female being 43.2 and 60.5 mm, respec- lt=12.9+ 5.58t (r2=0.999), tively; however, no evidence of protandry was where It is the standard length in millimeters found. at t years. The average growth curve indicates No increasing modal length with time was that C. pallida reaches 18.5 mm in one year, observed in its length-frequency distributions. 24 mm in two years and 29.5 mm in three years. This is probably because the sample size of each Since size of the smallest mature male (28.9 month except that of November was too small mm) approximates the size at age 3 (29.5 mm), (<50 specimens) to analyze polymodal length- male C. pallida probably attains sexual maturity frequency distributions. However, in November in three to four years. Thus a mode observed in when over 150 specimens were available, three males at 32-33 mm in November (Fig. 2) possibly modes at about 14-15 mm, 20-21 mm and 25-26 corresponds to a year-class that either has already attained or will attain sexual maturity. Further- more this mode apparently falls between the length-frequency distribution of subadults and that of females (Fig. 2), suggesting that the sexual dimorphism in smaller males and larger females results from lower growth rate in males as confirmed by Miya and Nemoto (1986a, b)for C. alba and C. pseudopallida. No distinct modes were observed in females, although if the growth continued at this rate (Fig. 3), age at 40-45 mm (size at maturity of

STANDARD LENGTH (mm)

Fig. 2. Monthly length-frequency distributions of Cyclothone pallida. Dotted areas, solid areas A G. E (years) and open areas represent the number of subadults, males and females, respectively. Data Fig. 3. Average growth curve during subadult

of the same months from different years were stage of Cyclothone pallida on the basis of the pooled for respective months. No data were average standard lengths of different age-groups available for January and September. in November. Vertical bars denote •} 1SD. 478 Miya and Nemoto

Table 5. Catch data of Cyclothone acclinidens. Standard length (mm), sex and maturity stages are shown. Data of the same months from different years are pooled for respective months. No fish was collected during February, March, April and July; Data were not available for January and September.

a Females of late Stage III / V b Mature males (males with enlarged nasal rosettes) females) would be about five to six years. If found in the stratified samples taken with MTD so the largest female (60.5 mm) may have nets. Sexual dimorphism of this species, with survived several spawning seasons. smaller males and larger females, was obvious There have been few studies on the age and as in other Cyclothone species. Mature males growth of Cyclothone pallida. Bond (1974) ex- (males with enlarged nasal rosettes) and mature amined seasonal changes of length-frequency females (Stages III/V and VI) greatly differ in distributions and maturity stages of this species size (25-29 mm vs 35-38 mm), but no evidence from Bermudan waters. Although no distinct of protandry was found in our specimens. modes were observed in its length-frequency It should be noted that despite the lower distributions, he assumed nevertheless that two abundance of C. acclinidens in Sagami Bay, as age-groups were present in adult females (22-56 many as three ripe females were found in a mm), which were assigned to age 1 and age 2, total of 28 specimens (Table 5). In the three respectively (Bond, 1974). However, his distinc- dominant species of Cyclothone (C. alba, C. tion between these age-groups is quite arbitrary. pseudopallida and C. atraria) that apparently Thus it is likely that more age-groups are con- have regular life cycles in Sagami Bay, ripe tained in the size range between 22 and 56 mm. females of each species rarely occurred (Miya Maynard (1982) examined length-frequency distri- and Nemoto, 1986a, b, MS.), comprising butions and gonadal development of this species only 0.1-0.4 % of the total number caught from Hawaiian waters, but found no temporal through the sampling series (Miya, unpublished patterns in these respects. He further attempted data). This is also true of the three dominant to determine age on the basis of adult otolith Cyclothone species in Hawaiian waters (C. alba, growth increments; however, he was unsuccess- C. pseudopallida and C. pallida); Maynard ful in correlating the number of growth incre- (1982) found few or even no ripe females among ments with other life history aspects (Maynard, over ten thousands specimens of the three species. 1982). Thus these studies have provided no Although we have no substantial evidence, it is clue to the estimation of the age and growth possible that if females of C. acclinidens reach of Cyclothone pallida. ovulation, they cannot encounter mature males 3.5. Cyclothone acclinidens because densities of ripe females and responsive A total of twelve subadults (16.5-26.9 mm SL), males will determine the chances of sexual en- eight males (25.5-29.7 mm SL) and eight females counter. If so the ripe females observed in this (25.0-38.0 mm SL) were collected by the series study would be unable to spawn in the absence of oblique hauls (Table 5), although no fish was of mature males. In contrast ripe females of Biology of Cyclothone pallida and C. acclinidens 479

the dominant species should have much more Kawaguchi, K.(1971): Gonostomatid fishes of the chances of sexual encounters than those of C. western North Pacific. Japan. J. Ichthyol., 18, acclinidens, and thus they will be spawning as 1-16. soon as they reach ovulation, resulting in the Kobayashi, B.N.(1973): Systematics, zoogeography apparent scarcity of ripe females in the samples. and aspects of the biology of the bathypelagic fish genus Cyclothone in the Pacific Ocean.Ph. D. dissertation, Univ. California, San Diego, 4. Concluding remarks 487pp. The present study demonstrates that Cyclo- Loeb, V.J.(1979): Larval fishes in the zooplankton thone pallida regularly occurs and spawns in community of the North Pacific central gyre. Sagami Bay. This indicates that C. pallida Mar. Biol., 53, 173-191. has a regular life cycle in Sagami Bay despite the Maynard, S.D.(1982): Aspects of the biology of fact that this area is located near the northern mesopelagic fishes of the genus Cyclothone(Pisces: geographical limits of this species. On the other Gonostomatidae) in Hawaiian waters. Ph. D. hand, C. acclinidens was collected sporadically in dissertation, Univ. Hawaii, Hawaii, 257 pp. Miya, M. and T. Nemoto(1986a): Reproduction, Sagami Bay and we have obtained no conclusive growth and vertical distribution of the meso- evidence concerning spawning of this species in pelagic fish Cyclothone pseudopallida (family this area. Therefore it remains uncertain whether Gonostomatidae).p.830-837. In: Indo-Pacific or not C. acclinidens reproduces in Sagami Bay. fish biology: Proceedings of the second inter- national conference on Indo-Pacific fishes, ed. by Acknowledgements T. Uyeno, R. Arai, T. Taniuchi and K. Matsu- We wish to thank Dr. R. Bieri, Antioch ura, Ichthyological Society of Japan, Tokyo. College, for his comments and suggestions on Miya, M. and T. Nemoto (1986b): Life history and the manuscript. We are also very grateful to vertical distribution of the mesopelagic fish the captain, officers and crew members of the Cyclothone alba (family Gonostomatidae) in Sagami Bay, Central Japan. Deep-Sea Res., 33, R/V Tansei Maru for their cooperation in col- 1053-1068. lecting samples. Miya, M. and T. Nemoto (1987): The bathypelagic gonostomatid fish Cyclothone obscura from Sagami References Bay, Central Japan. Japan. J. Ichthyol., 33. Badcock, J. (1982): A new species of the deep-sea (in press). fish genus Cyclothone Goode & Bean (Stomia- Miya, M. and T. Nemoto(1987.): Reproduction, toidei, Gonostomatidae) from the tropical Atlantic. growth and vertical distribution of the meso- J. Fish Biol., 20, 197-211. and bathypelagic fish Cyclothone atraria(Pisces: Badcock, J. and N. R. Merrett (1976): Midwater Gonostomatidae) in Sagami Bay, Central Japan. fishes in the eastern North Atlantic-I.Vertical Deep-Sea Res. (in press). distribution and associated biology in 30•‹N, 23•‹W, Motoda, S.(1971): Devices of simple plankton with developmental notes on certain myctophids. apparatus. V. Bull. Fac. Fisheries, Hokkaido Prog. Oceanogr., 7, 3-58. Univ., 22, 101-106. Badcock, J. and N.R. Merrett(1977): On the distri- Mukhacheva, V.A.(1964): The composition of species bution of midwater fishes in the Eastern North. of the genus Cyclothone (Pisces, Gonostomatidae) Atlantic. p. 249-282. In: Oceanic sound scatter- in the Pacific Ocean. Trudy Inst. Okeanol., 73, ing prediction, ed. by N.R. Andersen and B.J. 93-138. (in Russian with English summary). Zahuranec, Plenum Press, New York. Mukhacheva, V.A.(1967): Fishes of the genus Bond, G.W. (1974): Vertical distribution and life Cyclothone (Gonostomatidae).p. 150-164.In: histories of the gonostomatid fishes (Pisces: Biology of the Pacific Ocean, Vol.7, Book III, Gonostomatidae) off Bermuda . Ph. D.disserta- ed. by T.S. Rass, Ratisu, Tokyo.(in Japanese tion, Univ. Rhode Island, Rhode Island, 276 pp. translated from Russian). Cassie, R.M.(1954): Some uses of probability paper Mukhacheva, V.A.(1974):Cyclothones (gen. Cyclo- in the analysis of size frequency distributions . thone, fam. Gonostomatidae) of the World and Aust. J. mar. Freshwat. Res., 5, 513-522. their distributions. Trudy Inst. Okeanol., 96, Kawaguchi, K.(1969): Ecological studies on meso- 205-249. (in Russian with English summary) . and bathypelagic micronektonic fishes in the Omori, M. (1965): A 160-cm opening-closing plankton western North Pacific Ocean. Ph. D. dissertation, net. I. Description of the gear. J . Oceanogr. Univ. Tokyo, Tokyo, 218 pp . (in Japanese). Soc. Japan, 21, 212-220. 480 Miya and Nemoto

相模湾におけるヨコエソ科魚類ウスオニハダカとセンオニハダカの生物学

宮正樹*・根本敬久*

要旨:相模湾中央部の定点(北緯35度00分,東経139度た.本種は一産卵期におよそ1,000-3,000個の卵を生 20分,水深約1,500m)において,1982年12月から1985年み,一生に数回産卵すると考えられた.平均成長曲線か 11月にかけて計20回の航海により採集された試料から, ら,本種は未成魚期に1年で体長18.5mmに,2年でウスオニハダカ(Cyclothone pallida)とセンオニハダカ 24mmに,3年で29.5mmになることが示された.こ (C.acclinidens)に関するいくつかの生物学的知見が得の成長速度を外挿すると,雄は3-4年目に体長30-35mm られた.ウスオニハダカの分布深度は400-1,000mと推で,また雌は5-6年目に体長40-45mmで性的成熟に達定された.本種はほぼすべての試料中に見いだされ,相することになる.一方,センオニハダカが採集された試模湾では春から夏にかけて産卵することが明らかになっ料は全試料の25%に満たず,採集個体も28個体と少なか *東京大学海洋研究所ったため,本種が相模湾で繁殖しているかどうかは不明〒164東京都中野区南台1-15-1 であった.