Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 303-310. 1989

Lunar-phased immigration and settlement of metamorphosing Japanese flounder larvae into the nearshore nursery ground

Masaru Tanaka, Tsuneo G oto, Minoru Tomiyama, Hiroyuki Sudo, and Mikio Azuma

Tanaka, Masaru, Goto, Tsuneo, Tomiyama, Minoru, Sudo, Hiroyuki, and Azuma, Mikio 1989. Lunar-phased immigration and settlement of metamorphosing Japanese flounder larvae into the nearshore nursery ground. - Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 303-310.

Japanese flounder, Paralichthys olivaceus, larvae migrate from offshore spawning- grounds to nearshore nursery areas, where they settle on the bottom during the completion of metamorphosis. Passive transport combined with tidal currents have been inferred as indispensably important for immigration to the nursery areas for such poor swimmers as larval pleuronectiforms. To verify this, newly-immigrated flounder larvae and juveniles were sampled on 41 days with a 2 m beam trawl in the nearshore nursery area of Shijiki Bay, Hirado Island, from 18 April to 28 May 1985. The time series sampling record showed four peaks of catch, three of which corresponded well with the spring-tide phase. Vertical movement of metamorphosing pelagic larvae directly followed the tidal rhythm; upward migration was observed during flood, and downward during ebb tide. Such behaviour has already been recognized in flounders which were newly settled on the nursery ground. Combined effects of the flood tide and upward movement of larvae with the development of inshore tidal currents during spring tides accelerated the transport of larvae, resulting in a semi-lunar rhythm of immigration. Mysid larvae, the major food item for newly- settled flounders, appeared to be abundant around spring tides on the nursery ground. Thus, lunar-phased immigration and settlement are considered to be of adaptive significance in survival of flounders just metamorphosed. These hypothetical specu­lations are also discussed in relation to lunar effects on the physiology of meta­morphosis.

M. Tanaka, T. Goto, and M. Tomiyama: Department o f Fisheries, Faculty o f Agri­culture, Kyoto University, Kyoto 606, Japan. H. Sudo: Seikai Regional Fisheries Research Laboratory, Kokubuchyo, Nagasaki 850, Japan. M. Azuma: Department o f Biology, Faculty o f Education, Nagasaki University, Bunkyo-chyo, Nagasaki 852, Japan.

Introduction

The Japanese flounder, Paralichthys olivaceus, is one of the highest-priced commercial fish in Japanese coastal fisheries with an annual catch of approximately 6000- 80001. This species is distributed around the coastal areas of Japan, Korea and China, but is most abundant off the northwestern coast of Japan. Several major spawning-grounds are located around the Japan Sea and the adjacent East China Sea (Goto et al., 1989). Spawning starts in the early spring and continues until early summer, depending on locality. The pelagic stage of egg and larvae varies between one and two months dependent on temperatures (Seikai et al., 1986; Goto et al., 1989). Metamorphosing larvae then migrate into near-shore shallow areas to settle on the sandy beaches. During metamorphosis, flounders undergo a

change of habitat and diet synchronized with marked morphological changes, all suggesting that this phase might be of great significance in survival.

In near-shore areas, tidal rhythm is considered an important environmental factor affecting the life of intertidal organisms, particularly reproductive cycles and patterns of movement. Tide-related behaviour has been reported in juvenile plaice (Gibson, 1973, 1978; van der Veer and Bergman, 1986); however, patterns of immigration and settlement directly related to lunar- phase and its adaptive significance have been poorly understood.

The purpose of this study is to describe the temporal nature of metamorphosis and settlement in flounder larvae and to test hypotheses about lunar periodicity in the magnitude of immigration to the nursery areas.

303

Shiom i\ b a n a

x/Tanoura

129° 20'E

- '-A jika s h i m a ^

y 4 0

o

0 H ira d o Is.

GOTO NADA

JJ < Y M 1 ; 11/ / v - ' f 3 0 v i 11/ K a s h i r a n o ( I i :

/ s h i m a ^ J ^ ) ; / :

i w L » i i à2b \

N a g a te ^ i \ ( " N n o h a n a i

O g am i a^_ sh im a .N -.'.

2 0 ^

5 0 —

i___

Figure 1. Map showing the area surveyed with depth contour in metres. The larva-net surveys were done near the mouth of the bay, a closed triangle indicating the discrete-depth horizontal sampling position and a closed circle the anchored-net sampling position. The beam-trawl tows were made at Tanoura beach, indicated by x, located in the innermost part of the bay.

Based on these results, we discuss the possible mech­anisms involved and the adaptive significance of lunar rhythm.

Materials and methods

The study was performed in Shijiki Bay, Hirado Island, situated in the western part of Japan (Fig. 1). This bay is about 5 km long and 2 km wide with a tidal range of about 1.0 m at neap tides to about 2.8 m at spring tides. The shoreline consists of a reef and a boulder-shingle zone with a well-developed cover of macrophytes. Small-scale sandy beaches are distributed in the inner half of the bay. The main research site, named Tanoura (x in Fig. 1), is the widest beach, with an area of ca. 19 300-36 700 m 2 depending upon the tidal phase. The beach is completely enclosed by densely vegetated

Zostera and Sargassum beds (Fig. 2). Our preliminary research has shown that pelagic flounder larvae aggre­gate near the mouth of the bay, whereas settling and settled juveniles concentrate on the sandy beaches located in the innermost part of the bay.

The vertical distribution of pelagic larvae at the mouth of the bay was examined by two different methods. Discrete-depth horizontal tows of 10 min duration were taken at near-surface, mid-(15 m) and near bottom (30 m) layers, with a 1.3 m ring-net (6 m long, 0.5 mm mesh aperture) designed after Smith et al. (1968). Five series of diel sampling were made in late April or early May of 1977, 1982 and 1983, each consisting of three- layer tows once every 2 or 3 h. A 2-m ring anchored- net sampling system (10 m long, 1.5 mm mesh aperture) was deployed once every year in mid-May of 1982, 1983 and 1985. 1-h collections were made every 6h ,

304

Figure 2. Map of Tanoura beach, showing three lines for beam- trawl tows (A, B, C) and distribution of bottom types.

coinciding with flood and ebb on near-surface and near­bottom (30 m) layers during the entire day.

Settling and settled juveniles were collected with a 2- m beam trawl of 0.3 m height and 3 mm cod end mesh aperture designed after Kuipers (1975). Fishing efficiency of this gear is 26.7% for flounder juveniles less than 50mm SL (Fujii et al., 1989). The net was pulled 30 m by hand in an anchored boat along the three lines illustrated in Figure 2 at depths of about 0.2-1.5 m, 1.0-2.5 m, 1.5-3.5 m (lines A , B, C, respectively). In 1983, diel sampling at 2 to 3 h intervals was conducted on 11 to 12 May. In 1985, daily sampling for newly- immigrated flounders was performed over 41 d from 18 April through 28 May; these tows were mainly taken around the daytime high tides.

The flounder larvae and juveniles were classified into the developmental stages described by Minami (1982): A to E are pre-metamorphic, F to H are early-, mid- and late-metamorphosing, respectively, and I is the metamorphosed stage. The latter stage was subdivided into I[ to I4 according to development of the pectoral fins (Goto et al., 1989); Ij to I3 are settling and nearly metamorphosed, and I4 is settled and completely jneta- morphosed.

Mysids were collected by a sledge-type epibenthic sampler (0.5 m wide, 0.25 m height, 1.2 m long and 0.5 mm mesh aperture) along the same three lines as for flounder juveniles during the period of 18 April to 28 May, 1985. Larval mysids, which were sieved first through 1.0 mm mesh then retained on 0.5 mm mesh, were divided into three developmental categories: early

larvae hatched from the egg membrane (I), late-moulted larvae with eyes (II) and newly-emerged juveniles (III). The former two are equivalent to the stages II and III illustrated in Mauchline (1980).

Results

D iel changes in vertical distribution o f pelagic larvae

Vertical distribution of the pelagic larvae in late April 1977 is shown in Figure 3. The larvae appeared to be mainly distributed near the bottom in daytime. A considerable part of the larval population moved upward at night, as shown by increased densities in mid­water layers at dusk and at near-surface at night, and moved back at dawn. In the 1982 diel sampling, the total catch was low, but relatively large numbers of mid- and late-metamorphosing larvae were collected in the near-surface layer at night. Thus, the extent of vertical movement varied with the days sampled, but meta­morphosing larvae were usually found to exhibit a more prominent upward nocturnal migration.

Tide-related vertical m ovem ent of m etamorphosing larvae

The anchored-net sampling system, which caught larvae flowing in with the tidal currents, showed that more larvae were collected during flood than ebb tides (Fig.4). Metamorphosing F to H stage larvae, in particular,

0 100:_________ I

mI 1 Sandy bottom

l l l l l l l l l Zostera zone

ËS83 Sargassum zone

Reef Bouldershingle zone

305

12-13TIME 18-19 20-21 22-23 0 0 -0 1 0 4 - 0 5 0 6 -0 7 0 8 - 0 9 10-1

( B o t to m )D AYN IG H T D a w nDusk

2-13 14-15 16-17

50 100

Figure 3. Vertical distribution of pelagic flounder larvae and its diel change at the mouth of Shijiki Bay, 29-30 April 1977. The density scale (bottom right) is number of larvae 1000 m~3 and the top scale shows time. Samples were taken at 0 m, 15 m and 30 m with a towed ring net. Coarse-dotted, fine-dotted and open portions indicate the twilight, night-time and daytime vertical profiles, respectively.

were carried into the surface net during flood tides, but seldom during ebb tides. The evening phase was before sunset at which illumination the larvae usually inhabit rather deeper strata, as demonstrated in Figure 4, never­theless they mainly occurred at near-surface. A dif­ference is between daytime and nighttime ebb phases, thus demonstrating the effect of light intensity on depth distribution. Although the results obtained in other years were not as clear as in 1983, tide-related vertical movement of metamorphosing larvae was still apparent.

D iel sampling for settling and settled flounders

In order to clarify the sampling fluctuations of settled flounders related to tidal phases, diel sampling was conducted at 2- to 3-h intervals with the beam trawl. A total of 686 flounders was collected in 31 tows. The body lengths ranged from 10.0 to 103.0 mm with 87% being between 10 and 13 mm. The average numbers collected exhibited a cyclic change related to tidal phase, with the largest numbers at low tide, a decrease during the flood, with the smallest numbers at high tide and a subsequent increase during the ebb.

These catch fluctuations might be caused only by density changes derived from the areal fluctuations dur­ing the ebb and flood. Therefore, the number of indi­viduals, each G-H and I stage, were converted into total population estimates within the entire nursery area, using the depth-area relationship and 26.7% of fishing efficiency. As shown in Figure 5, there was no clear trend of settled I stage juvenile abundance, whereas cyclic changes in population size that were synchronized with tidal phases were observed in settling G and H stage larvae; numbers increase during the ebb and decrease during the flood tide.

Settlement pattern o f m etam orphosing-settling flounders

Time-series of the numbers of individuals collected dur­ing 18 April through 28 May 1985 are shown in Figure 6. Average numbers of individuals collected per haul varied daily from 1.0 to 32.5. Unusually large numbers of juveniles were caught on 24 April. The 24th day sampling was done exceptionally at low-tide when settled juveniles were more densely aggregated around

0 4 2 0 - 0 5 2 0 1215-1315

SURFACE

EBBFLOOD10oo

>

0

. BOTTOM5

ABC DEF GH A B C D E F G H

1 7 2 0 -1 8 2 0

- FLOOD [3

1 1 1

2 3 0 5 - 2 3 5 0

EBB

i l l ................................... J___1__ I__ I___1__ I__ 1__ I___I I__ I__ I__ I___L_1___I___I___I

DEVELOPMENTAL STAGE

Figure 4. Abundance and developmental stage of pelagic flounder larvae carried into the anchored 2-m larval nets during flood and ebb tides. Sampling was done on 8-9 May 1983 at the mouth of Shijiki Bay. The upper section shows the result obtained in the surface net, and lower section the near-bottom net.Open and dotted bars indicate the pre-metamorphic and metamorphosing stages.

306

Figure 5. Changes in estimated population of settling and settled flounders at Tanoura beach, showing tidal-phase related change of G and H stage larvae but no changes related to tides in settled I stage juveniles. Each population size was calculated from flounder density, fishing efficiency of the sampler and area of the beach. Dotted part shows the nighttime.

Stage

Stage

7

C e£ * 5

< z /

3 2 Q- * Oa- 1

0

'•— •. '° ............o— — ° '- ° ~ - - - O ------- - ° —-o '

3E

08 10 120620 22 00 02 0416 1812 14

TIME OF DAY

line C, resulting in a larger catch. Figure 7, showing the daily catch of settling larvae (G-H) and newly settled juveniles ( I 1-I2 ), demonstrated that there were four groups of days when relatively large numbers of floun­ders were collected, namely around 19 April, 29 April, 6 May and 20 May. Except 29 April, these groups of days closely coincided with spring tides. The 29 April sample contained the largest number of pre-settlement stage larvae and coincided with the neap tides.

Semi-lunar settlement periodicity of the flounder that was synchronized with spring tides was also confirmed from weekly sampling coinciding with spring and neap tides in Tanoura beach in 1986 (Goto et al., 1989).

Larval mysid abundance

Daily changes of larval mysid abundance during the period of 19 April to 28 May 1985 are shown in Figure 8. Since daily catches fluctuated greatly, each value is expressed in average number of individuals per haul

during three successive days. Abundance of groups I and II mysids fluctuated in nearly the same way, but there was no simple correlation with tidal cycles. On the other hand, total abundance, combining groups I, II and III, seemed to exhibit a cyclic change with higher abundance occurring during spring tides.

Discussion

Lunar-phase related immigration to nursery grounds has been suggested in some other fish species (Pollock et at., 1983; McFarland et al., 1984; Tzeng, 1985). For Japanese flounder, Imabayashi (1980a) postulated semi- lunar immigration that was correlated with spring-tides which he based on length-composition analysis of settled demersal juveniles. In the present study, long­term regular daily sampling demonstrated that the immi­gration and settlement of metamorphosing flounder lar­vae predominantly occurs during spring tides (Fig. 7).

Fig. 6. Results of 41 days of successive sampling from 18 April to 28 May 1985, along with moon phase (top), tidal range, water temperature (W.T.) and salinity (Sal.). Number of individuals per haul is expressed in mean (open circle) and maximum (bar) value.

C O C

^ 0 0

Szioo*-<a: 0

20

18 20 APRIL

301 5MAY

SAMPLING DATE

10 25 28

307

o_ zH- <O

15(~~| newly-settled juveniles

■ s e t t l in g larvae

LJi 53Z

OAPRIL

20 25 28

SAMPLING DATE

Figure 7. Daily changes in number of individuals of settling larvae (F-H stage) and newly- settled juveniles (I r I3 stage) collected at line C during the 41- day sampling period. Lunar phase and tidal range are shown in the upper section.

Several factors may be considered as potentially caus­ing the semi-lunar rhythm of flounder immigration and settlement: these include spawning synchronized with the semi-lunar cycle, hydrographic conditions related to tidal range, semi-lunar related aggregation of meta­morphosing larvae at pelagic nursery areas, vertical migration synchronized with tidal phase, lunar effects on the physiology of metamorphosis, and endogenous semi-lunar rhythms. Among these factors, we consider the vertical movement of larvae as the most important biological factor. A diagnosis of body structure of meta­morphosing flounder larvae suggests that swimming ability is rather poorly developed (Yasunaga, 1985; Fukuhara, 1986). However, even such poor swimmers are likely to be able to move between the near-surface and near-bottom layers in a rather short time. As shown

in Figure 3, pelagic flounder larvae usually shift their main habitat from deeper to near-surface layers at night, the nocturnal migration developing more clearly with advances in metamorphosis. This implies that night-time flood tidal currents would transport the larvae landward, as found in stone flounder (Tsuruta, 1978) and English sole (Boehlert and Mundy, 1987). This transport pro­cess, however, can have a vulnerable phase if the larvae are flushed out to seaward during ebb tides.

Another type of vertical movement related to the tidal phase may be of great significance in transporting larvae to near-shore areas. The flood-upward and ebb- downward vertical movement, as confirmed in pelagic larvae (Fig. 4), can lead to selective tidal stream trans- port (Arnold, 1969). If this behaviour commonly occurs, metamorphosing larvae would be transported longer

350

G r o u p I II III

G r o u p I

G r o u p II30 0

< 25 0

UJ

200

150 o-o>

u_ 100

o-o'^50

0 010 20 28

SAMPLING DATE

Figure 8. Time-series changes in abundance of larval mysids at line C during the period of 40- days’ sampling from 19 April to 28 May 1985. Mysid abundance is expressed in average number of individuals per haul during the successive three days. I, II, and III indicate early larvae, late larvae, and newly-emerged juveniles, respectively. Lunar phases are illustrated on the top.

308

distances by more developed landward tidal currents during spring tides. Moreover, the vertical movement caused by larval reactions to environmental cues may develop with the strength of the tidal flux. The meta­morphosing flounder larvae would thus be transported more effectively to near-shore areas during spring tides, resulting in a semi-lunar immigration pattern.

Tide-related vertical movement has been suggested in Paralichthys spp. (Weinstein et al., 1980), but direct field investigations of the factors inducing tidal rhythmic activity have not been made (Boehlert and Mundy, 1988). In the present study, settling larvae, which have already been transported to the nursery area, are also likely to show such tide-related vertical movement (Fig.5). Four series of diel samplings for settling and settled flounders were conducted in Tanoura beach in April and May 1985. Total catch of 587 flounders by 108 tows showed a negligible difference between the daytime and night-time (Sudo et al., unpublished). Therefore, tide- related changes in the estimated population of settling G-H stage larvae (Fig. 5) are considered as a function of vertical movement: most of the larvae swim up the water column, resulting in catch decreases during the high tides and vice versa during the low tides.

Although the detailed mechanism by which larvae time their vertical movement is unknown, it seems to be definitely significant in migrating to near-shore nursery areas in flounder larvae. Selective tidal stream transport has been suggested as the most effective immi­gration mechanism in various pleuronectiform larvae: including plaice (Creutzberg et al., 1978; Zijlstra et al., 1982; Rijnsdorp et al.. 1985; van der Veer, 1986), stone flounder (Tsuruta, 1978), Paralichthys spp. (Weinstein eta l., 1980), marbled sole (Takahashi eta l., 1986) and English sole (Boehlert and Mundy, 1987). In the present species, Kiyono etal. (1978) preliminarily suggested the possibility of night-flood transport. A majority of these works, excluding Rijnsdorp et al. (1985) and van der Veer (1986), who regarded the process as entirely pass­ive, superimpose the tide-related vertical movement of larvae on the mechanism of tidal stream transport.

In our research field, various earlier larval stages were found to be distributed around the mouth of the bay, whereas migration into the near-shore nursery appeared to occur only in metamorphosing larvae. This suggests that immigration is fundamentally an active process caused by larval reactions to tidal-flux changes as Boehlert and Mundy (1988) stressed in their review of estuarine recruitment. During metamorphosis of Jap­anese flounder, major changes occur in morphology and behaviour; e.g. body form (Okiyama, 1967; Minami, 1982; Takahashi, 1985; Seikai et al., 1986; Fukuhara, 1986), skeletal ossification (Balart, 1985), sensory organs (Kawamura and Ishida, 1985), swimming behav­iour (Fukuhara, 1986) and settling behaviour (Seikai, 1985; Seikai et al., 1986). Seikai (1985) observed that settlement occurred during the early phase of meta­

morphosis in the laboratory. This type of “pseudo­settlement” may occur when the larvae are transported to shallower areas, particularly at the time of ebb phases, so playing an important role in preventing flush- out. These developmental events lead us to consider that metamorphosing larvae may react to environmental variables that facilitate effective orientation.

The Japanese flounder shifts its habitat from pelagic to demersal and its diet from planktonic zooplankters to benthic mysids (Imabayashi, 1980b; Minami, 1982). Recent stomach content analysis reveals that the early larval mysids, ranging about 1.5 to 2.0 mm in length, were the dominant item of diet for newly-settled flounders (Hirota and Noguchi, unpublished). The reproduction of intertidal organisms is frequently synch­ronized with full moon and/or new moon (Korringa, 1947; Neumann, 1975; Naylor, 1976; Saigusa, 1980a, 1980b). However, the relation between larval release and lunar phase has never been examined (Mauchline, 1980). Our preliminary analysis for daily changes in larval abundance of mysids reveals that mysids remain at rather high level around spring tides. Thus, newly- settled flounder juveniles may have a better food supply at spring tides, resulting in greater chances of survival.

Although the immigration and settlement of meta­morphosing flounder larvae occur around spring tides, rather large surges of immigration may occur during neap tides (Fig. 7, 29 April). These surges seem to be correlated with strong onshore winds. Thus, total immigration may be attributed both to components derived from lunar effects and in addition, occasional events caused by meteorological effects. Such effects combine with hydrographic conditions in inshore migration of postlarval sole in the Vilaine estuary (Marchand and Masson, 1989). Which component is more significant in the survival of newly-immigrated juveniles must be an important further research target.

Acknowledgements

We would like to thank the personnel of the Seikai Regional Fisheries Research Laboratory and staff of RV “Yoko” for providing facilities. We wish to acknowl­edge the invaluable discussion we had with M. Azeta and helpful assistance rendered by F. Kato, Y. Morioka, K. Kimoto, J. Nakashima, R. Ikemoto, H. Yoshiwara and S. Kuriyama. We are also grateful to A. Rossiter and J. B. Tanangonan for reviewing the manuscript, and to G. W. Boehlert and J. H. S. Blaxter for critical review and invaluable comments.

ReferencesArnold, G. P. 1969. The orientation of pelagic larvae

Pleuronectes platessa in water currents. J. Exptl. Biol., 50: 785-801.

309

Balart, E. F. 1985. Development of median and paired fin skeleton of Paralichthys olivaceus (Pleuronectiformes: Para- lichthydae). Japan. J. Ichthyol., 31 (4): 398-410.

Boehlert, G. W., and Mundy, B. C. 1987. Recruitment dynamics of metamorphosing English Sole, Parophrys vet- ulus, to YaquinaBay, Oregon. Estuar. Coast. Shelf Sei., 25: 261-281.

Boehlert, G. W., and Mundy, B. C. 1988. Roles of behavioral and physical factors in larval and juvenile fish recruitment to estuarine nursery areas. Am. Fish. Soc. Symp., 3: 51-67.

Creutzberg, F., Eltink, A. T. G. W., and van Noort, G. W. 1978. The migration of plaice larvae Pleuronectes platessa into the western Wadden Sea. In Physiology and behaviour of marine organisms, pp. 243-251. Ed. by D. S. McLusky and A. J. Berry. Pergamon Press, New York. 388 pp.

Fujii, T., Sudo, H., Azeta, M., and Tanaka, M. 1989. Settling process of a flounder, Paralichthys olivaceus, larvae and juveniles in Shijiki Bay, Hirado Island. Nippon Suisan Gak- kaishi, 55 (1): 17—23.

Fukahara, O. 1986. Morphological and functional devel­opment of Japanese flounder in early life stage. Nippon Suisan Gakkaishi, 52: 81-91.

Gibson, R. N. 1973. Tidal and circadian rhythm in juvenile plaice, Pleuronectes platessa. Mar. Biol., 22: 379-386.

Gibson, R. N. 1978. Lunar and tidal rhythms in fish. In The rhythmic activity of fishes, pp. 201-214. Ed. by J. E. Thorpe, Academic Press, New York.

Goto, T., Sudo, H., Tomiyama, M., and Tanaka, M. 1989. Settling period of a flounder, Paralichthys olivaceus, larvae and juveniles in Shijiki Bay, Hirado Island. Nippon Suisan Gakkaishi, 55 (1): 9-16.

Imabayashi, H. 1980a. Settling mechanism of larvae of bastard halibut, Paralichthys olivaceus, in the nursery ground, esti­mated from the size of distribution. Bull. Jap. Soc. Sei. Fish., 46: 419-426.

Imabayashi, H. 1980b. Feeding activities of juvenile and young bastard halibut, Paralichthys olivaceus, in the benthic com­munity - 1. Intraspecific relationship in the population. Bull. Jap. Soc. Sei. Fish., 46: 427—435.

Kawamura, G., and Ishida, K. 1985. Changes in the sense organ morphology and behaviour with growth in the flounder Paralichthys olivaceus. Bull. Jap. Soc. Sei. Fish., 51: 155- 165.

Kiyono, S., Sakano, Y., and Hamanaka, Y. 1978. Studies on the stock of the flounder, Paralichthys olivaceus in the Wakasa Bay - IV. Transport mechanism of the larval fish. Rep. Kyoto Inst. Ocean. Fish. Sei., (1977): 16-26.

Korringa, P. 1947. Relations between the moon and periodicity in the breeding of marine animals. Ecol. Monogr., 17: 349- 381.

Kuipers, B. 1975. On the efficiency of a two-meter beam trawl for juvenile plaice (Pleuronectes platessa). Neth. J. Sea Res., 9: 69-85.

Marchand, J., and Masson, G. 1989. Factors of estuarine colonization by 0-group sole (Solea vulgaris): hydrological conditions, behaviour, and feeding activity in the Vilaine estuary. Rapp. P.-v. Réun. Cons. int. Explor. Mer, 191: 287-295 (this volume).

McFarland, W. N., Brothers, E. B., Ogden, J. C., Shulman, M. J., Bermingham, E. L., and Kotchian-Prentiss, N. M.1984. Recruitment patterns in young French grunts, Hae- mulon flavolineatum (Family Haemulidae), at St Croix, Vir­gin Island. Fish. Bull., 83: 413-426.

Mauchline, J. 1980. The biology of mysids and euphausiids. Adv. Mar. Biol., 18: 1-681.

Minami, T. 1982. The early life history of a flounder Para­lichthys olivaceus. Bull. Jap. Soc. Sei. Fish., 48: 1581-1588.

Naylor, E. 1976. Rhythmic behaviour and reproduction in marine animals. In Adaptation to the environment: essays on the physiology of marine animals, pp. 393-429. Ed. by R. C. Newell. Butterworths, London.

Neumann, D. 1975. Lunar and tidal rhythm in the development and reproduction of an intertidal organism. In Physiological adaptation to the environment, pp. 451-463. Ed. by F. J. Vemberg. Intext Educational Publishers, New York.

Okiyama, M. 1967. Study on the early life history of a flounder, Paralichthys olivaceus (Temminck et Schlegel). I. Descrip­tion of postlarvae. Bull. Japan Sea Reg. Fish. Res. Lab., 17: 1- 12 .

Pollock, B. R., Weng, H., and Morton, R. M. 1983. The seasonal occurrence of postlarval stages of yellowfin bream, Acanthopagrus australis (Günther), and some factors affect­ing their movement into an estuary. J. Fish Biol., 22: 409- 415.

Rijnsdorp, A. D., van Starlen, M., and van der Veer, H. W.1985. Selective tidal transport of North Sea plaice larvae Pleuronectes platessa in coastal nursery areas. Trans. Am. Fish. Soc., 114: 461-470.

Saigusa, M. 1980a. Lunar and semilunar rhythm in repro­duction (1). Aquabiology, 9: 248-254.

Saigusa, M. 1980b. Lunar and semilunar rhythm in repro­duction (2). Aquabiology, 10: 372-377.

Seikai, T. 1985. Metamorphosing and settling processes of flatfish larvae analysed from rearing experiments. Bull. Jap. Soc. Fish. Oceanogr., 47/48: 81-84.

Seikai, T., Tananagonan, J. B.. and Tanaka. M. 1986. Tem­perature influence on larval growth and metamorphosis of the Japanese flounder Paralichthys olivaceus in the labora­tory. Nippon Suisan Gakkaishi, 52: 977-982.

Smith, P. E., Count, R. C., and Clutter, R. I. 1968. Changes in filtering efficiency of plankton nets due to clogging under tow. J. Cons. int. Explor. Mer, 32: 232-248.

Takahashi, Y. 1985. Morphological and behavioural changes with growth in reared larvae and juveniles of a flounder, Paralichthys olivaceus. Aquiculture, 33: 43-52.

Takahashi, K., Hoshiai, G., and Abe, H. 1986. Distribution and migration of Limanda yokohamae (Günther) larvae in Ishinomaki Bay and Mangoku Bay. Aquiculture, 34: 1-8.

Tsuruta, Y . 1978. Field observations on the immigration of larval stone flounder into the nursery ground. Tohoku J. Agr. Res., 29: 136-145.

Tzeng, W. N. 1985. Immigration timing and activity rhythms of the eel, Anguilla japonica, elvers in the estuary of northern Taiwan, with emphasis on environmental influences. Bull. Jap. Soc. Fish. Oceanogr., 47/48: 11-28.

Veer, H. W. van der. 1986. Immigration, settlement, and density-dependent mortality of a larval and early postlarval 0-group plaice (Pleuronectes platessa) population in the west­ern Wadden Sea. Mar. Ecol. Prog. Ser., 29: 223-236.

Veer, H. W. van der, and Bergman, M. J. N. 1986. Devel­opment of tidally-related behaviour of a newly-settled 0- group plaice (Pleuronectes platessa) population in the west­ern Wadden Sea. Mar. Ecol. Prog. Ser., 31: 121-129.

Weinstein, M. P., Weiss, S. L., Hodson, R. G., and Gerry, L. R. 1980. Retention of three taxa of postlarval fishes in an intensively flushed tidal estuary, Cape Fear River, North Carolina. Fish. Bull., 78: 419-436.

Yasunaga, Y. 1985. Measurement of swimming speed of flounder larvae Paralichthys olivaceus with a small straight channel. Bull. Jap. Soc. Sei. Fish., 51: 227-231.

Zijlstra, J. J., Dapper, R., and Witte, J. J. 1982. Settlement, growth and mortality of post-larval plaice (Pleuronectes pla­tessa) in the western Wadden Sea. Neth. J. Sea Res., 15: 250-272.

310