Ecophysiology of juvenile flatfish in nursery grounds

Journal of Sea Research 45 (2001) 205±218

www.elsevier.com/locate/seares

Ecophysiology of juvenile ¯at®sh in nursery grounds Yoh Yamashita a,*, Masaru Tanaka b, John M. Miller c b

a Tohoku National Fisheries Research Institute, Shiogama, Miyagi 985-0001, Japan Division of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kyoto 606-8502, Japan c Zoology Department, North Carolina State University, Campus Box 7617, Raleigh, NC 27695, USA

Received 15 February 2000; accepted 25 June 2000

Abstract Relationships between biotic and abiotic factors and the ecological performance of late larval and juvenile ¯at®sh in nursery grounds are examined from ecophysiological viewpoints. The ®rst events in the nursery are metamorphosis and settlement. Development of organs, osmoregulation and behavioural changes during metamorphosis, and size at metamorphosis are regulated by environmental factors. Various hormones play critical roles in this regulation. Effects of environmental conditions on individual growth in the nursery grounds are described on the basis of Fry's ®ve environmental factors: limiting, controlling, masking, directive and lethal factors. The main limiting factors are food and dissolved oxygen; controlling factors are temperature and body size; masking factors are salinity and pollutants; lethal factors are extreme environments; and directive factors are food, predators and dissolved oxygen. In addition to temperature, it has been indicated that dissolved oxygen seems to be relatively important for ¯at®sh of the eastern US and northern European countries, while food abundance appears to be more critical for Japanese ¯ounder. The feasibility is discussed of ecophysiological modelling to predict individual growth and subpopulation production based on the assessment of the role of environmental variability using the above classi®cation, which organises and integrates environmental effects. q 2001 Elsevier Science B.V. All rights reserved. Keywords: Ecophysiology; Flat®sh; Juvenile; Growth; Environment; Modelling

1. Introduction The habitats of ®shes vary temporally and spatially, so ®shes must survive, grow and reproduce in conditions of a changing balance of biotic and abiotic environmental factors. Ecophysiology forms the interface between ecology and physiology which is affected by and regulated in response to environmental changes (Rankin and Jensen, 1993). Differences in ecological responses of individual ®sh to environmental conditions through physiological mechanisms may result in * Corresponding author. E-mail address: [email protected] (Y. Yamashita).

variability in growth, survival and thus subpopulation production and recruitment. Although recruitment has been extensively studied, especially focusing on the early life stages, there is no simple hypothetical mechanism to explain recruitment variability. Recruitment variation is too complex to be resolved by conventional empirical correlation or regression type analyses (Neill et al., 1994). Occasionally, these analyses may function in a restricted area, but they cannot be extended outside the system from which they were derived, because this would lack a mechanistic basis (Miller et al., 2000). In order to understand the complexity of population production and recruitment variability problems,

1385-1101/01/$ - see front matter q 2001 Elsevier Science B.V. All rights reserved. PII: S 1385-110 1(01)00049-1

206

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

analysis from an ecophysiological point of view may be applicable. Flat®sh occur throughout the world seas from the subarctic to the tropics (Pauly, 1994) having a wide range of spawning seasons, habitat requirements and life history strategies (Minami and Tanaka, 1992; Gibson, 1994). This leads to complex relationships between environmental factors and performance of populations. This study examines the relationships between biotic and abiotic factors and the ecological performance of late larval and juvenile ¯at®shes in nursery grounds. The ®rst events in the nursery are metamorphosis and settlement. Mortality may be highly variable at this stage, affecting year-class strength in some species (Tanaka et al., 1989a; Miller et al., 1991; Bradford, 1992; Furuta, 1996). First we summarise the ecophysiological characteristics with regard to metamorphosis and settlement focusing on the Japanese ¯ounder Paralichthys olivaceus. Then we examine the relationship between environmental factors and individual growth of ®sh in nursery grounds. Finally, the feasibility of ecophysiological modelling to predict individual growth and sub-population production is discussed. We adopted the scienti®c names of pleuronectid species after Cooper and Chapleau (1998). 2. Ecophysiological framework The general approach adopted is that presented by Fry (1947, 1971), who classi®ed environmental factors into ®ve functional categories depending upon their effects on metabolism: ² controlling factors set the pace of both maximum and maintenance rates; ² limiting factors constrain the maximum rate; ² masking factors increase or load the maintenance rate, by increasing obligatory work; ² directive factors either unload (reduce) the maintenance rate or release the active rate by putting ®sh in a microhabitat or physiological state where it is better (pre) adapted; ² lethal factors cause individual death. Fry (1947, 1971) de®ned the difference between active metabolism and standard metabolism as meta-

bolic scope, denoting the energy available for swimming, growth, and other activities. Active metabolism is equivalent to the maximum or potential rate and standard metabolism approximate maintenance rate. Analogous to Fry's metabolic scope for activity, the difference between maximum assimilated energy and maintenance energy losses indicates the scope for growth at an individual level, and the difference between sub-population growth and production losses is the scope for production at the subpopulation level (Neill et al., 1994; Miller, 1997; Miller et al., 1997). Fry's classi®cation suggests an integrated way to interpret environmental factors in an ecological scope such as growth and sub-population production (Neill and Bryan, 1991; Neill et al., 1994; Miller, 1997; Miller et al., 1997). Environmental factors interact and the effects of factors are additive only within the same factor class (Miller et al., 2000). 3. Ecophysiology of metamorphosing and settling larvae Many ¯at®sh species spawn in oceanic waters, pelagic larvae are transported inshore and settle in shallow inshore and estuarine habitats, e.g. plaice Pleuronectes platessus (Rijnsdorp et al., 1985; Van der Veer, 1986), English sole Parophorys vetula (Boehlert and Mundy, 1987), sole Solea solea (Fonds, 1979; Marchand and Masson, 1989), summer ¯ounder Paralichthys dentatus and southern ¯ounder Paralichthys lethostigma (Warlen and Burke, 1990; Burke et al., 1991), Japanese ¯ounder (Tanaka et al., 1989a,b), and stone ¯ounder Platichthys bicoloratus (Yamashita et al., 1996). Abundance of juveniles recruiting to the nursery ground is a limiting factor in juvenile sub-population production. However, if abundance is higher than optimal, density-dependent growth and survival may occur and operate as a controlling factor. Substantial changes in morphology, physiology and ecology of juvenile ¯at®shes occur during metamorphosis, when the shift from pelagic to benthic habitats occurs (e.g. Youson, 1988; Minami and Tanaka, 1992; Inui et al., 1994; Tanaka et al., 1996). Environmental factors may be crucial in determining the recruitment to nursery grounds (Tanaka et al., 1989a) via their

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

METAMORPHIC STAGE EVENT

Eye migration start Pre-metamorphic MET onset

Body transformation symmetry to asymmetry Metamorphic MET climax

207 Eye migration finish Post-metamorphic MET finish

SETTLEMENT Plankton feeder FOOD HABITS

DEVELOPMENT

Larval system Gastric gland Retinal rod cell twin cones

non-feeding

Benthos feeder

(resting) Gall bladder inflation Transforming Adult system Pyloric Hepatic pancreatic Gut epithelium caeca involution transformation Muscle transformation to Shift of red blood cell adult type to adult type

Fig. 1. Summary of the metamorphic (MET) process in Japanese ¯ounder (redrawn from Tanaka et al., 1996).

effects on growth and mortality during the metamorphosis-settlement period. 3.1. Development of organs The development of the digestive system in Japanese ¯ounder around the time of metamorphosis and settlement has been described by Tanaka et al. (1996) (Fig. 1). Oropharynx, esophagus, rudimentary stomach, intestine, liver, gall bladder, and pancreas differentiate before and during yolk absorption. This incompletely developed, but functional, system meets the requirements for ®rst feeding. The second prominent change in the digestive system occurs during metamorphosis. Gastric glands appear at the onset of metamorphosis and become functional around mid-metamorphosis, following the separation of the cardia, diverticulum and pylorus, and the formation of the pyloric caeca. By the end of the climax metamorphosing stage, the basic adult-type digestive system, characterised by a functional stomach and pyloric caeca, is established. The differentiation and functional development of gastric glands are directly controlled by, or under the in¯uence of thyroid hormones (Miwa et al., 1992; Inui et al., 1995; Tanaka et al., 1995). During metamorphosis larval-type muscle is transformed into adult-type muscle, the latter being characterised by thick muscle ®bres with abundant myo®brils (Yamano et al., 1991, 1994; Inui et al., 1995). Similarly there is a shift from primitive erythrocytes to de®nitive erythrocytes in red blood cell populations (Miwa and Inui, 1991; Inui et al., 1995). Both phenomena are regulated by thyroid

hormones. Morphological changes in skeletal muscle are linked to increases in maximum swimming speed (Fukuhara, 1986), and the transformation to de®nitive erythrocytes may increase the metabolic capability to support swimming. In addition to the development of digestive organs and muscle, the development of visual capability is closely associated with changes of foraging behaviour and feeding ecology. Kitamura (1990) reported that photosensitivity of larval Japanese ¯ounder increases 100-fold at the early-metamorphosing stage with the development of retinal rod cells and twin cones (Kawamura and Ishida, 1985). Similarly in plaice, the threshold intensity for visual feeding decreases from 1 to 10 m candles in young larvae to 0.01 m candles in metamorphic larvae when rods appear in the retina (Blaxter, 1968). An increase in visual sensitivity is crucial for juveniles which ambush food organisms associated with sand substrate. These morphological developments and completion of differentiation of the digestive system with metamorphosis lead to improved foraging and feeding on epibenthic and benthic organisms. Irreversible settlement is characterised by the disappearance of the pectoral ®n membrane and consequent reduction of the pectoral ®n size (Yamashita et al., 1996), and this occurs just after the completion of metamorphosis. 3.2. Ecology and physiology of settlement The most pronounced ecological change during metamorphosis is the shift from a pelagic to a benthic life. This change in habitat induces a feeding shift from zooplankton to benthic animals, and in foraging

208

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

behaviour from searching in the water column to ambushing prey on the bottom. Many species settle in areas shallower than 15 m, and settlement should occur in areas where the chances for subsequent growth and survival are high (Gibson, 1994); that is, where food is abundant and predation risk is low (Gibson, 1999). When newly settled Japanese ¯ounder juveniles encounter poor food conditions they tend to temporarily return to pelagic life and migrate elsewhere (Tanaka et al., 1989a); this may also occur in plaice (Creutzberg et al., 1978). Settlement in Japanese ¯ounder is usually established during the period of several days after the ®rst contact with the bottom, which occurs at the metamorphic climax stage (Tanaka et al., 1989a). A prominent phenomenon associated with metamorphosis and settlement is the temporary cessation of feeding; newly settled ¯ounder may rest on the bottom without displaying any active feeding behaviour for about two days (Tanaka et al., 1989a, 1996). Absence of feeding and growth around the time of the completion of metamorphosis has also been observed in marbled sole Pseudopleuronectes yokohamae (Fukuhara, 1988), English sole (Laroche, 1982) and plaice (Lockwood, 1984; Hamerlynck et al., 1989). During the non-feeding phase, hepatic and pancreatic involution, a signi®cant reduction of intestinal and rectal epithelium heights and gall bladder in¯ation are observed (Tanaka et al., 1996; Gwak et al., 1999). In addition, recalibration of binocular vision is required after the eye migration (Osse and Van den Boogaart, 1997). This non-feeding resting period may be necessary for the structural and functional reorganisation of the digestive system and body morphology, as a completion of the ®nal stage of metamorphosis and adaptation to the benthic environment. During this resting period, larvae may utilise energy earlier stored in the liver (Tanaka et al., 1996). Although the non-feeding resting period has been suggested to in¯uence survival, studies on this subject are scarce. 3.3. Osmoregulation The tolerance of Japanese ¯ounder to low salinity increases during metamorphosis (Higano and Yasunaga, 1986; Hiroi et al., 1997). For example, survival of pre-metamorphic larvae (18 days after hatching) in

S ˆ 4 psu was 0%, while at metamorphic climax (33 days) it was 100% (Hiroi et al., 1997). Cutaneous chloride cells are common in the skin of premetamorphic larvae, but these disappear in metamorphicclimax larvae and the branchial chloride cell number increases during metamorphosis (Hiroi et al., 1998). However, the role of the branchial chloride cells in osmoregulation in hypo-osmotic environments is not fully clari®ed. Tolerance of low salinity conditions is important for ¯at®sh which migrate to inshore areas during metamorphosis, because they may encounter low-salinity waters. Prolactin is a hormone implicated in freshwater adaptation (Evans, 1979; Hirano, 1986; Hirano et al., 1987). The changes that occur in prolactin secreting cells up to metamorphosis, and following transfer of Japanese ¯ounder to hypotonic water indicate that prolactin is involved in the development of low-salinity tolerance in this species during metamorphosis (De Jesus et al., 1994; Hiroi et al., 1997). 3.4. Size at metamorphosis and settlement Body size at metamorphosis varies widely among ¯at®sh, from less than 5 to 140 mm TL depending upon species (Osse and Van den Boogaart, 1997). The settlement season of Japanese ¯ounder is from spring to early summer, and the standard length (SL) at metamorphosis (climax stage) decreases with an increase in ambient temperature and advancement of season. For example SL at metamorphosis declines from 13 mm in late April (water temperature about 138C) to 9 mm by late May (about 188C), and this results in early larvae being three times heavier than late larvae (Goto et al., 1989; Noichi et al., 1997; Tanaka et al., 1998). Results of laboratory rearing experiments revealed a negative relationship between metamorphic size and ambient water temperature (Seikai et al., 1986; Minami and Tanaka, 1992; Tanaka et al., 1998). Concentrations of thyroid hormones (thyroxine and triiodothyronine) and the number of thyroid follicles are higher at higher temperature at the same SL (Tanangonan et al., 1989; Tanaka et al., 1995). Higher concentration of thyroid hormones accelerates larval metamorphosis (Miwa and Inui, 1987) relative to growth at higher temperatures so this may result in shorter larval duration and smaller metamorphic size. In plaice more rapid development at higher

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

209

environmental abiotic factors such as temperature, dissolved oxygen (DO) and salinity and their complex interactions. 4.1. Controlling factors

Fig. 2. Scope model for growth and environmental factors. Limiting factors depress assimilated energy and masking factors raise energy for metabolism. Locomotion indicates forced activities such as avoidance behaviour from predator.

temperatures results in metamorphosis at an earlier age, but not at smaller size (Hovenkamp and Witte, 1991), providing a contrast with observations made on Japanese ¯ounder. Because temperature is closely associated with pelagic life length, the size at metamorphosis, size speci®c susceptibility to predation and feeding success, further studies of its effects on subsequent survival are crucial. Metamorphosis of Japanese ¯ounder is mainly under endocrine control (Inui and Miwa, 1985; Miwa et al., 1988; De Jesus et al., 1991; Inui et al., 1994; Tanaka et al., 1995), but the roles of the various hormones, their interactions, and the relationship with environmental factors remain to be elucidated.

The dominant controlling factor for individual growth is temperature. Body size is not included in Fry's classi®cation of external environmental factors. We think body size becomes an intrinsic controlling factor when we apply the Fry paradigm at the individual level or at a higher level. 4.1.1. Temperature Temperature acts as a controlling factor by setting the pace of anabolism and catabolism. The components of the energy budget (ingestion, metabolism, and excretion) are known to be affected by temperature, and the relationship between temperature and these energy budget terms was summarised by Jobling (1993). When food is unlimited, ingestion increases with increasing temperature to a peak at the optimum temperature before declining steeply as the temperature approaches the upper thermal limit. Within the normal temperature range of the species, metabolism (M, standard metabolism in this case) and nitrogen excretion (E) increase with temperature, and the effect of temperature on both can be described by a semilogarithmic plot Ln…M or E† ˆ c 1 kT;

4. Ecophysiology of juvenile growth as

The general energy budget for juvenile ®sh is given

I ˆ G 1 M 1 F 1 E; where I is the ingested energy, G the growth, M the energy lost in metabolism (standard metabolism 1 metabolism for speci®c dynamic action 1 metabolism for activity), F and E represent energy losses in faeces and excretory products, respectively. Growth is determined by the difference between assimilated energy (I±F±E) and metabolic losses (M). This is equivalent to the metabolic scope for growth as de®ned in Fry's paradigm (Neill and Bryan, 1991; Neill et al., 1994; Miller, 1997; Miller et al., 1997) (Fig. 2). The energy budget is strongly affected by

where c is a constant (Ln(M or E) at T ˆ 08C) and k represents the temperature coef®cient. The temperature coef®cient can also be expressed as Q10 ˆ e…10k† : The scope for growth is de®ned as the difference between the assimilated energy which increases with temperature to a peak and then declines and the energy losses for metabolism which continue to increase with temperature. Consequently, the relationship between temperature and the scope for growth will be skewed in a dome-shaped curve (Fig. 2). The relationships between ingestion or growth rate and temperature have sometimes been described using polynomial regressions, but these have no more than an empiric basis. The optimum temperature, at which growth is maximal when food availability is not limiting, was found to be 10±158C for Atlantic halibut Hippoglossus hippoglossus (BjoÈrnsson and

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

4.1.2. Body size Body size in¯uences all components of the energy budgets, and the relationships between ingestion (I), routine metabolism (M), nitrogenous excretion (E), growth (G) and body weight (W) can usually be described by allometric equations (Jobling, 1993) I or M or E or G ˆ aW b ; where a and b are constants, with b representing the weight exponent. The weight exponent has sometimes been reported to be dependent on temperature (Table 1). For example, Fonds and Saksena (1977) and Fonds et al. (1992) reported a decrease in the weight exponent for ingestion and growth with increasing temperature for sole and plaice, indicating that there is a decrease of the optimum temperature for feeding and growth with increasing size. This would tally with observations that larger sole and plaice leave shallow coastal nurseries and migrate to deeper offshore waters where temperatures are lower. Weight exponents for resting (routine) metabolic rate in juvenile ¯at®shes have been found to range from 0.6 to 0.8 (Table 1), values that are lower than the 0.8 (Winberg, 1956) and the 0.86 (Brett and Groves, 1979) reported as the averages for ®shes. Flat®sh have a relatively smaller respiratory surface (Hughes, 1966; De Jager et al., 1977), spend less energy on metabolism and convert relatively more of the assimilated food energy into growth compared with more active round ®sh (Fonds et al., 1992). The growth rates of Japanese ¯ounder are very high

25 20 15 10 5 30 0.25

20

40 Body w eight (g

20

60 )

80

10

rature

0

Tempe

TryggvadoÂttir, 1996; Jonassen et al., 1999), 16±208C for turbot Scophthalmus maximus (Burel et al., 1996; Imsland et al., 1996), 208C for plaice and European ¯ounder Platichthys ¯esus (Fonds et al., 1992), 20± 258C for Japanese ¯ounder (Fig. 3), 23±258C for sole (Fonds, 1975; Howell, 1997) and above 308C for summer and southern ¯ounder (Peters and Angelovic, 1973; Peters and Kjelson, 1975). This relationship is affected by ®sh size, with larvae and juveniles often having a higher optimum temperature for growth than their larger conspeci®cs (Fonds and Saksena, 1977; Fonds et al., 1992; Jobling, 1993; BjoÈrnsson and TryggvadoÂttir, 1996; Imsland et al., 1996; Jonassen et al., 1999). The effect of temperature on the weight exponent for growth is discussed in next section.

Daily growth rate (% wet weight)

210

Fig. 3. Effects of temperature and body size on growth rate in Japanese ¯ounder juveniles, calculated and drawn from Iwata et al. (1994, 1995) and Seikai et al. (1997) and T. Targett, unpublished.

during the early juvenile period in the laboratory (1.9 mm d 21 in SL and 21.2% d 21 in wet weight for 25±43 mm SL ®sh, Seikai et al., 1997), compared with juveniles of other ¯at®sh such as plaice and European ¯ounder (ca. 1 mm d 21 of maximum growth rate, Fonds et al., 1992). Such a high growth rate of juvenile Japanese ¯ounder has also been reported from ®eld-collected juveniles (Fujii and Noguchi, 1996). The weight exponents for ingestion and growth in the Japanese ¯ounder calculated from data by Iwata et al. (1995) are 0.648 and 0.516, respectively. These weight exponents for Japanese ¯ounder are lower than those estimated for other ¯at®sh species (Table 1), indicating the decrease of growth rates with body size is rapid in this species (Fig. 3). The effects of temperature and size on metabolism (M) and excretion (E) over the normal temperature range can be expressed using multiple regressions Ln…Y† ˆ Ln a 1 bLn W 1 kT

…Y ˆ aW b e…kT† †;

where Y is the rate function of interest, a a constant, b the weight exponent and k is the temperature coef®cient. 4.2. Limiting factors Limiting factors for individual growth are resources used to power metabolism. The main limiting factors are food and dissolved oxygen.

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

211

Table 1 Weight exponent for ingestion, growth, respiration and excretion rates in juvenile ¯at®shes Species

Size range (g)

Temp. (8C)

Weight a exponent

Difference b between temps.

Source

Ingestion (satiation feeding) Limanda limanda Paralichthys olivaceus Platichthys ¯esus Pleuronectes platessus Pleuronectes platessus Solea solea Solea solea

1.1±150.7 4±251 1±378 2±301 0.7±9.2 10±1000 8±178

13 15±25 2±22 2±22 14 10±26 20

0.88 0.648 0.767±0.859 (0.798) 0.683±0.920 (0.743) 0.697 0.402±0.938 (0.691) 0.772

± NS NS ? S ± S ±

Pandian (1970) Iwata et al. (1995) c Fonds et al. (1992) Fonds et al. (1992) Kirk and Howell (1972) Fonds and Saksena (1977) Fonds et al. (1989)

Growth (on unlimited rations) Hippoglossus hippoglossus 10±5000

9±14

0.54

±

Paralichthys olivaceus Pleuronectes platessus Platichthys ¯esus Scophthalmus maximus Solea solea

15±25 2±22 6±22 14.4±17.8 20

0.516 0.703±1.081 (0.816) 0.781 0.671 0.736

NS S? NS ± ±

BjoÈrnsson and TryggvadoÂttir (1996) Iwata et al. (1995) c Fonds et al. (1992) Fonds et al. (1992) Iglesias et al. (1987) c Fonds et al. (1989)

Respiration (resting or routine) Limanda limanda 0.1±10 Paralichthys olivaceus 2.4±67.5 Platichthys ¯esus 1±418 Pleuronectes platessus 4±47 Pleuronectes platessus 0.05±10 Pleuronectes platessus 1±326

10 20 2±22 10±20 10 2±22

0.666 0.643 0.782 0.626 0.721 0.782

± ± NS NS ± NS

Edwards et al. (1969) Liu et al. (1997) Fonds et al. (1992) Jobling (1982) Edwards et al. (1969) Fonds et al. (1992)

Nitrogenous excretion (endogenous) Pleuronectes platessus 5±90 Paralichthys olivaceus 1.6±575

5±20 20

0.67 0.716

NS ±

Jobling (1981) Kikuchi et al. (1990,1992) c

a b c

4±251 1±131 1±378 5.7±106 8±178

Geometric mean in parentheses. Difference in b between temperature. S: signi®cant NS: not signi®cant. Weight exponents were calculated from data.

4.2.1. Food quality and quantity Both food quality and quantity act as limiting factors. For example, Seikai et al. (1997) showed that the speci®c growth rate of Japanese ¯ounder juveniles fed live mysids was approximately 1.1±2.7 times higher than that of ®sh fed formula feed or frozen mysids. Similarly, natural food (mussel meat) is better for growth of juvenile sole than formulated dry food in a laboratory (Fonds et al., 1989). Although their cause is not known, differences in nutritional components such as n3-HUFA may be important because such components have a signi®cant effect on larval survival, growth and behaviour (Watanabe, 1993; Seikai et al., 1997; Masuda et al., 1998; Masuda and Tsukamoto, 1999). Frozen and thawed mysid may

lose some nutrients such as lipids (Fonds et al., 1995) and the biochemical composition of frozen mysids may change, affecting their value as a food. In the wild, food quality has also been suggested to in¯uence juvenile growth: mysids appear to be better than amphipods as a food for Japanese ¯ounder (Tanaka et al., 1989a) and tail tips of lugworm better than bivalve siphons as a food for plaice (Van der Veer and Witte, 1993). Food availability has profound effects on growth, as demonstrated for Japanese ¯ounder (Fujii and Noguchi, 1996), stone ¯ounder (Malloy et al., 1996), plaice (Karakiri et al., 1989; Van der Veer and Witte, 1993; Berghahn et al., 1995) and greenback ¯ounder Rhombosolea tapirina (Shaw and Jenkins, 1992).

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

4.2.2. Dissolved oxygen Dissolved oxygen may act as a limiting factor through the restrictions imposed on feeding below a critical threshold. Decreases in DO reduce food intake (food digestion), conversion ef®ciency and metabolic rate and also increase ventilation costs, leading to reduced growth (Brett, 1979; Kramer, 1987; Neill and Bryan, 1991; Jobling, 1994). Generally an oxygen concentration of around 5±6 ppm is critical for optimal growth, below which suppression of the growth rate is proportional to the O2 concentration. Juvenile ¯at®sh such as winter ¯ounder Pseudopleuronectes americanus (Bejda et al., 1992), summer ¯ounder (Szedlmayer and Able, 1993), sole (e.g. Dalla Via et al., 1997), plaice (Petersen and Pihl, 1995 and European ¯ounder (Tallqvist et al., 1999), which use shallow estuaries or enclosed bays as nursery grounds, experience hypoxic conditions particularly on warm summer nights. Bejda et al. (1992) reported a 37% reduction in daily ration and a 54% reduction in growth rate in juvenile winter ¯ounder exposed to a DO concentration of 2.2 ppm compared with 6.7 ppm. Southern ¯ounder showed avoidance behaviour when DO fell below 3.7 ppm (Deubler and Posner, 1963). Avoidance responses may vary depending on the season, temperature, food availability and shelter (Kramer, 1987; Bejda et al., 1992) and are probably undertaken in an attempt to improve survival and growth. 4.3. Masking factors Masking factors, which result in increased metabolic losses and lead to reduced growth, include salinity and other environmental stressors. Many species of juvenile ¯at®sh utilise estuaries as their nursery grounds and are therefore exposed to variable salinity conditions. Post-larvae and juveniles of species within the genus Paralichthys show a euryhaline tendency. Japanese ¯ounder, summer ¯ounder and southern ¯ounder juveniles survive in hypotonic environments above S ˆ 4±8 psu during and after metamorphosis (Hiroi et al., 1997; Smith et al., 1999; Specker et al., 1999) and tolerance to freshwater increases with size (Yasunaga and Koshiishi, 1980; Smith et al., 1999). However there are species-speci®c differences in the utilisation of nursery habitats. Southern ¯ounder seem to prefer low salinity conditions at the estuary head,

120

P.olivaceus Growth (% of maximum)

212

100

S. maximus 80

P. flesus

P. dentatus

60

GH, Cortisol

P. lethostigma Prolactin isosmotic

40 0

10

20 Salinity (psu)

30

40

Fig. 4. Schematic ®gure showing effects of salinity on growth of various ¯at®sh species as a percentage of the maximum rate. Sources are in the text.

while summer ¯ounder are more often found in the high salinity estuary mouth or in salt marshes (Powell and Schwartz, 1977; Burke et al., 1991), juveniles of Japanese ¯ounder utilise exposed open inshore areas more often than closed brackish estuaries. It is likely that there is an optimum range of salinity for growth which is species- and life-stage speci®c (Brett, 1979). Southern ¯ounder (Peters and Kjelson, 1975), European ¯ounder (Gutt, 1985), and turbot (Gaumet et al., 1995) juveniles grow well at low salinity, whereas Japanese ¯ounder (T.E. Targett, M. Tanaka, unpublished data) and summer ¯ounder (Peters and Angelovic, 1973) grow better at high salinities (Fig. 4). Because osmoregulation can represent a major proportion of the maintenance metabolism (Morgan and Iwama, 1991; Ron et al., 1995) its cost may affect the energy available for growth. Consequently it could be hypothesised that growth rate should be highest at the salinity where the metabolic cost for osmoregulation is lowest. Higher growth rates and lower metabolism of juvenile turbot in S ˆ 10 and S ˆ 19 psu than in S ˆ 27 and S ˆ 35 psu (Waller, 1992; Gaumet et al., 1995) are consistent with this hypothesis. However, the relationship between metabolic rate and salinity is complex and may differ between species and developmental stages (e.g. Table 4 in Morgan and Iwama, 1991; Abud, 1992). The hormone prolactin is important for freshwater adaptation (e.g. Hirano, 1986; Hirano et al., 1987), and cortisol and growth hormone play roles in

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

seawater adaptation (e.g. Sakamoto et al., 1993, 1997. Growth-promoting effects of these three hormones in teleosts have also been reported (Nishioka et al., 1985; Shepherd et al., 1997), but this remains to be investigated for euryhaline ¯at®shes. Pollutants such as ammonia which are sometimes closely associated with reduced oxygen will act antagonistically on growth (Rasmussen and Korsgaard, 1996; Person-Le Ruyet et al., 1997). 4.4. Lethal factors Lethal factors in extreme environments kill ®sh. For example, summer ¯ounder larvae are thought to suffer increased mortality when exposed to the low temperatures of the eastern coast of the US for a long period. Exposure to a water temperature of less than 2±38C can kill transforming larvae and newly settled summer ¯ounder juveniles (Malloy and Targett, 1991, 1994; Szedlmayer et al., 1992) and mortality was signi®cantly greater at ,48C than at a higher (108C) temperature (Keefe and Able, 1993). A similar case was reported for sole in the North Sea (Woodhead, 1964; Fonds, 1975). Mortality at low temperature is size-speci®c with the smallest ®sh experiencing the highest mortality rates (Malloy and Targett, 1991). In the Wadden Sea area with a high tidal range, high temperature and solar radiation may be lethal to juvenile plaice in the shallow residual waters on the higher tidal ¯ats (Berghahn et al., 1993). In addition to extreme temperatures, depletion of DO, which commonly occurs in estuarine and inshore habitats (Whitledge, 1985), may act as a lethal factor for benthic ®shes (Bejda et al., 1992). The recent expansion of DO-depleted areas resulting from anthropogenic activities may have had a marked in¯uence on the life cycle of estuarine-dependent ¯at®sh species. 4.5. Directive factors The roles of directive factors are poorly understood. They cue or signal the ®sh to select or respond to particular characteristics of the environment (Brett, 1979). Many environmental factors including food, predator, DO, temperature, salinity, tidal ¯ow, light intensity, and photoperiod, can act as directive factors. Movements induced by or responses initiated by these factors enhance survival and growth.

213

The movements include diel, seasonal and ontogenetic migrations. For example, at night juvenile plaice migrate into shallower areas to feed where food is abundant and the risk of predation by larger ®sh is reduced (Burrows et al., 1994; Gibson et al., 1996, 1998). Such movements also ensure that the ®sh avoid the suboptimal high temperatures which may occur in shallow waters during the day (Gibson et al., 1998; Gibson, 1999). In areas with large tidal ranges, juvenile plaice may follow the tide and utilise shallow areas both for feeding and as refuges from predation during high tide (Kuipers, 1977; Van der Veer and Bergman, 1986; Berghahn, 1987). Age-0 summer ¯ounder also undergo tidal movements feeding in creeks during high tides and leaving there to avoid high temperature, low salinity and low DO during the low tides (Rountree and Able, 1992; Szedlmayer and Able, 1993). Selective tidal stream transport may play an important role in tidal migrations to allow movements with minimum energy costs (Metcalfe et al., 1990; Szedlmayer and Able, 1993; Burrows et al., 1994). Fonds et al. (1992) attempted to explain the differences in seasonal and ontogenetic migrations between plaice and European ¯ounder from an ecophysiological point of view. Weight exponents for food consumption and growth decreased with temperature in plaice, but not in European ¯ounder. This indicates that there is a decrease of the optimum temperature for feeding and growth with increasing ®sh size for plaice, but no change for ¯ounder. Temperature coef®cients for feeding, growth and metabolism were higher for European ¯ounder than for plaice, indicating relatively greater activity of ¯ounder at high temperatures. These characteristics seemed to be re¯ected in differences in distribution and migration patterns of plaice and ¯ounder. Two-year-old plaice appear to emigrate to deeper offshore water to avoid high summer temperatures in shallow inshore areas, whereas adult ¯ounder are able to feed and grow in shallow coastal waters during the summer. Directive factors act as cues for transitional changes in life history. The transformations are realised through hormonal responses stimulated by the directive environmental factors. Hormonal responses also play an important role in the acclimation to environmental changes such as low salinity. Therefore secretion of hormones such as thyroxine,

214

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

prolactin, cortisol and growth hormones are thought to be directive. 5. Future perspectives Neill et al. (1994) proposed a conceptual framework of ecophysiological modelling to study performance relationships by integrating responses of individual ®sh into community concepts. Michaelis± Menten kinetics may be useful to describe the relationship between substrate (e.g. food, carrying capacity) and product (e.g. growth, sub-population production), thereby giving convenient indices of performance. In this type of modelling, a scope for performance at level n 2 1 becomes a controlling factor at level n (Miller, 1997; Miller et al., 1997). Miller et al. (2000) developed an ecophysiology model incorporating physiological responses to assess the role of abiotic variability on the growth of red drum juveniles and delineated the importance of temperature and DO. Yamashita et al. (2000) reformed this model for Japanese ¯ounder and expanded it to a sub-population production study in an attempt to predict the stocking level above which release of hatchery-raised juveniles would restrict the growth of wild ®sh as food (a limiting factor at the individual level) began to limit production. To understand the performance of sub-populations, or any other level of biological organisation, it is necessary to integrate and quantify the effects of several key factors. For example, in addition to temperature, DO seems to be an important determinant of ¯at®sh growth and production in the shallow coastal waters of the eastern US and Europe, whereas food abundance seems to be more critical for the production of Japanese ¯ounder juveniles. Acknowledgements We would like to express our gratitude to Drs. R.N. Gibson, T.E. Targett, J.S. Burke, K.A. Duchon, O. Tominaga, T. Yada, T. Sakamoto, who supplied useful information on ecology and physiology of ¯at®shes. We would also like to thank Dr. W.H. Neill for helpful comments on the manuscript. Y. Yamashita was supported by a fellowship under the OECD Cooperative Research Programme: Biological Resource

Management for Sustainable Agriculture Systems. J.M. Miller was supported by Grant NA90AA-DSGO62 from the National Sea Grant College Program, National Oceanic and Atmospheric Administration, to the North Carolina Sea Grant College Program.

References Abud, E.O.A., . Effects of salinity and weight on routine metabolism in the juvenile croaker Micropogonias furnieri (Desmarest 1823). J. Fish Biol. 40, 1992471±472. Bejda, A.J., Phelan, B.A., Studholme, A.L., 1992. The effect of dissolved oxygen on the growth of young-of-the-year winter ¯ounder Pseudopleuronectes americanus. Env. Biol. Fish. 34, 321±327. Berghahn, R., 1987. Effects of tidal migration on growth of 0-group plaice (Pleuronectes platessa L.) in the North Frisian Wadden Sea. Meeresforsch. 31, 209±226. Berghahn, R., Bullock, A.M., Karakiri, M., 1993. Effects of solar radiation on the population dynamics of juvenile ¯at®sh in the shallows of the Wadden Sea. J. Fish Biol. 42, 329±345. Berghahn, R., Ruth, M., LuÈdemann, K., 1995. Differences in growth of 0-group plaice (Pleuronectes platessa L.) in neighbouring Wadden Sea areas. Neth. J. Sea Res. 34, 131±138. BjoÈrnsson, B., TryggvadoÂttir, S.V., 1996. Effects of size on optimal temperature for growth and growth ef®ciency of immature Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 142, 33±42. Blaxter, J.H.S., 1968. Light intensity, vision, and feeding in young plaice. J. Exp. Mar. Biol. Ecol. 2, 293±307. Boehlert, G.W., Mundy, B.C., 1987. Recruitment dynamics of metamorphosing English sole Parophorys vetulus, to Yaquina Bay, Oregon. Estuar. Coast. Shelf Sci. 25, 261±281. Bradford, M.J., 1992. Precision of recruitment predictions from early life stages of marine ®shes. Fish. Bull. US 90, 439±453. Brett, J.R., 1979. Environmental factors and growth. In: Hoar, W.S., Randall, D.J., Brett, J.R. (Eds.). Fish Physiology VIII. Academic Press, New York, pp. 599±675. Brett, J.R., Groves, T.D.D., 1979. Bioenergetics and growth. In: Hoar, W.S., Randall, D.J., Brett, J.R. (Eds.). Fish Physiology VIII. Academic Press, New York, pp. 279±352. Burel, C., Person-Le Ruyet, J., Gaumet, F., Le Roux, A., SeÂveÁre, A., Boeuf, G., 1996. Effects of temperature on growth and metabolism in juvenile turbot. J. Fish Biol. 49, 678±692. Burke, J.S., Miller, J.M., Hoss, D.E., 1991. Immigration and settlement pattern of Paralichthys dentatus and P. lethostigma in an estuarine nursery ground, North Carolina, USA. Neth. J. Sea Res. 27, 393±405. Burrows, M.T., Gibson, R.N., Robb, L., Comely, C.A., 1994. Temporal patterns of movement in juvenile ¯at®shes and their predators: underwater television observations. J. Exp. Mar. Biol. Ecol. 177, 251±268. Cooper, J.A., Chapleau, F., 1998. Monophyly and intrarelationships

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218 of the family Pleuronectidae (Pleuronectiforms), with a revised classi®cation. Fish. Bull. US 96, 686±726. Creutzberg, F., Eltink, A.T.G.W., Van Noort, G.J., 1978. The migration of plaice larvae Pleuronectes platessa into the western Wadden Sea. In: McLusky, D.S., Berry, A.J. (Eds.). Physiology and Behaviour of Marine Organisms. Proceedings of the 12th European Marine Biology Symposium. Pergamon Press, Oxford, pp. 243±251. Dalla Via, J., Van den Thillart, G., Cattani, O., Cortesi, P., 1997. Environmental versus functional hypoxia/anoxia in sole Solea solea: the lactate paradox revisited. Mar. Ecol. Prog. Ser. 154, 79±90. De Jager, S., Smit-Onel, M.E., Videler, J.J., Van Gils, B.J.M., Uf®nk, E.M., 1977. The respiratory surface of the gills of some teleost ®shes in relation to their mode of life. Bijdr. Dierk. 46, 199±205. De Jesus, E.G., Hirano, T., Inui, Y., 1991. Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese ¯ounder, Paralichthys olivaceus. Gen. Comp. Endocrinol. 82, 369±376. De Jesus, E.G., Hirano, T., Inui, Y., 1994. The antimetamorphic effect of prolactin in the Japanese ¯ounder. Gen. Comp. Endocrinol. 93, 44±50. Deubler Jr, E.E., Posner, G.S., 1963. Response of postlarval ¯ounders, Paralichthys lethostigma, to water of low oxygen concentrations. Copeia (2), 312±317. Edwards, R.R.C., Finlayson, D.M., Steele, J.H., 1969. The ecology of 0-group plaice and common dabs in Loch Ewe II. Experimental studies of metabolism. J. Exp. Mar. Biol. Ecol. 3, 1±17. Evans, D.H., 1979. Fish. In: Maloiy, D.M.D. (Ed.). Comparative Physiology of Osmoregulation in Animals. Academic Press, New York, pp. 305±390. Fonds, M., 1975. The in¯uence of temperature and salinity on growth of young soles, Solea solea L. In: Persoone, G., Jaspers, E. (Eds.). Proc. 10th Europ. Mar. Biol. Symp. Vol. 1. Mariculture. Universal Press, Wetteren, pp. 109±125. Fonds, M., 1979. Laboratory observations on the in¯uence of temperature and salinity on development of the eggs and growth of the larvae of Solea solea (Pisces). Mar. Ecol. Prog. Ser. 1, 91±99. Fonds, M., Saksena, V.P., 1977. The daily food intake of young soles (Solea solea L.) in relation to their size and the water temperature. Actes Coll. C.N.E.X.O. 4, 51±58. Fonds, M., Drinkwaard, B., Resink, J.W., Eysink, G.G.J., Toet, W., 1989. Measurements of metabolism, food intake and growth of Solea solea (L.) fed with mussel meat or with dry food. In: De Pauw, N., Jaspers, E., Ackefors, H., Wilkins, N. (Eds.). Aquaculture Ð A Biotechnology in Progress. European Aquaculture Society, Bredene, pp. 851±874. Fonds, M., Cronie, R., Vethaak, A.D., Van der Puyl, P., 1992. Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and ¯ounder (Platichthys ¯esus) in relation to ®sh size and temperature. Neth. J. Sea Res. 29, 127±143. Fonds, M., Tanaka, M., Van der Veer, H.W., 1995. Feeding and growth of juvenile Japanese ¯ounder Paralichthys olivaceus in relation to temperature and food supply. Neth. J. Sea Res. 34, 111±118.

215

Fry, F.E.J., 1947. Effects of the environment on animal activity. Univ. Toronto Stud., Biol. Ser. 55, 1±62. Fry, F.E.J., 1971. The effect of environmental factors on the physiology of ®sh. In: Hoar, W.S., Randall, D.J. (Eds.). Fish Physiology VI. Academic Press, New York, pp. 1±98. Fujii, T., Noguchi, M., 1996. Feeding and growth of Japanese ¯ounder (Paralichthys olivaceus) in the nursery ground. In: Watanabe, Y., Yamashita, Y., Oozeki, Y. (Eds.). Survival Strategies in Early Life Stages of Marine Resources. Balkema, Rotterdam, pp. 141±151. Fukuhara, O., 1986. Morphological and functional development of Japanese ¯ounder in early life stage. Bull. Jpn. Soc. Sci. Fish. 52, 81±91. Fukuhara, O., 1988. Morphological and functional development of larval and juvenile Limanda yokohamae (Pisces: Pleuronectidae) reared in the laboratory. Mar. Biol. 99, 271±281. Furuta, S., 1996. Predation on juvenile Japanese ¯ounder (Paralichthys olivaceus) by diurnal piscivorous ®sh: Field observations and laboratory experiments. In: Watanabe, Y., Yamashita, Y., Oozeki, Y. (Eds.). Survival Strategies in Early Life Stages of Marine Resources. Balkema, Rotterdam, pp. 285±294. Gaumet, F., Boeuf, G., SeÂveÁre, A., Le Roux, A., Mayer-Gostan, N., 1995. Effects of salinity on the ionic balance and growth of juvenile turbot. J. Fish Biol. 47, 865±876. Gibson, R.N., 1994. Impact of habitat quality and quantity on the recruitment of juvenile ¯at®shes. Neth. J. Sea Res. 32, 191±206. Gibson, R.N., 1999. The ecology of the early life stages of the plaice, Pleuronectes platessa L.: a review. Bull. Tohoku Natl. Fish. Res. Inst. 62, 16±48. Gibson, R.N., Robb, L., Burrows, M.T., Ansell, A.D., 1996. Tidal, diel and longer term changes in the distribution of ®shes on a Scottish sandy beach. Mar. Ecol. Prog. Ser. 130, 1±17. Gibson, R.N., Pihl, L., Burrows, M.T., Modin, J., Wennhage, H., Nickell, L.A., 1998. Diel movements of juvenile plaice Pleuronectes platessa in relation to predators, competitors, food availability and abiotic factors on a microtidal nursery ground. Mar. Ecol. Prog. Ser. 165, 145±159. Goto, T., Sudo, H., Tomiyama, M., Tanaka, M., 1989. Settling period of larvae and juveniles of Japanese ¯ounder Paralichthys olivaceus in Shijiki Bay, Hirado Island. Nippon Suisan Gakkaishi 55, 9±16 (in Japanese with English abstract). Gutt, J., 1985. The growth of juvenile ¯ounders (Platichthys ¯esus L.) at salinities of 0, 5, 15, and 35½. Z. Angew. Ichthyol. 1, 17± 26. Gwak, W.S., Seikai, T., Tanaka, M., 1999. Evaluation of starvation status of laboratory-reared Japanese ¯ounder Paralichthys olivaceus larvae and juveniles based on morphological and histological characteristics. Fish. Sci. 65, 339±346. Hamerlynck, O., Janssen, C.R., Van Landtschoote, E., 1989. Fasting and feeding in late larval and early post-larval plaice (Pleuronectes platessa L.). Rapp. P.-v. ReÂun. Cons. Int. Explor. Mer 191, 465. Higano, J., Yasunaga, Y., 1986. Tolerance to low salinity of the larva of ¯ounder Paralichthys olivaceus, considered from the change of oxygen consumption. Aquat. Fish. Port Engineer., Natl. Res. Inst. Fish. Eng. 7, 33±39 (in Japanese with English abstract).

216

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

Hirano, T., 1986. The spectrum of prolactin action in teleosts. In: Ralph, C. (Ed.). Development and Directions. Alan Liss, New York, pp. 53±74. Hirano, T., Ogasawara, T., Bolton, J.P., Collie, N.L., Hasegawa, S., Iwata, M., 1987. Osmoregulatory role of prolactin in lower vertebrates. In: Lahlou, B., Kirsch, R. (Eds.). Comparative Physiology of Environmental Adaptations. Karger, Basel, pp. 112±124. Hiroi, J., Sakakura, Y., Tagawa, M., Seikai, T., Tanaka, M., 1997. Developmental changes in low-salinity tolerance and responses of prolactin, cortisol and thyroid hormones to low-salinity environment in larvae and juveniles of Japanese ¯ounder, Paralichthys olivaceus. Zool. Sci. 14, 987±992. Hiroi, J., Kaneko, T., Seikai, T., Tanaka, M., 1998. Developmental sequence of chloride cells in the body skin and gills of Japanese ¯ounder (Paralichthys olivaceus) larvae. Zool. Sci. 15, 455±460. Hovenkamp, F., Witte, J.I.J., 1991. Growth, otolith growth and RNA/DNA ratios of larval plaice Pleuronectes platessa in the North Sea 1987 to 1989. Mar. Ecol. Prog. Ser. 70, 105±116. Howell, B.R., 1997. A re-appraisal of the potential of the sole Solea solea (L.), for commercial cultivation. Aquaculture 155, 355± 365. Hughes, G.M., 1966. The dimensions of ®sh gills in relation to their function. J. Exp. Biol. 45, 177±195. Iglesias, J., Olmedo, M., Otero, J.J., Peleteiro, J.P., SoloÂrzano, M.R., 1987. Growth, under laboratory conditions, of turbot, Scophthalmus maximus, from the Ria de Vigo (north-west Spain). Mar. Biol. 96, 11±17. Imsland, A.K., Sunde, L.M., Folkvord, A., Stefansson, S.O., 1996. The interaction of temperature and ®sh size on growth of juvenile turbot. J. Fish Biol. 49, 926±940. Inui, Y., Miwa, S., 1985. Thyroid hormone induces metamorphosis of ¯ounder larvae. Gen. Comp. Endocrinol. 60, 450±454. Inui, Y., Miwa, S., Yamano, K., Hirano, T., 1994. Hormonal control of ¯ounder metamorphosis. In: Davey, K.G., Peter, R.E., Tobe, S.S. (Eds.). Perspectives in Comparative Endocrinology. NRC, Canada, pp. 408±411. Inui, Y., Yamano, K., Miwa, S., 1995. The role of thyroid hormone in tissue development in metamorphosing ¯ounder. Aquaculture 135, 87±98. Iwata, N., Kikuchi, K., Honda, H., Kiyono, M., Kurokura, H., 1994. Effects of temperature on the growth of Japanese ¯ounder. Fish. Sci. 60, 527±531. Iwata, N., Kikuchi, K., Kurokura, H., 1995. Growth of the Japanese ¯ounder Paralichthys olivaceus at different temperatures. Isr. J. Aquat. -Bamidgeh 47, 178±184. Jobling, M., 1981. Some effects of temperature, feeding and body weight on nitrogenous excretion in young plaice Pleuronectes platessa L. J. Fish Biol. 18, 87±96. Jobling, M., 1982. A study of some factors affecting rates of oxygen consumption of plaice, Pleuronectes platessa L. J. Fish Biol. 20, 501±516. Jobling, M., 1993. Bioenergetics: feed intake and energy partitioning. In: Rankin, J.C., Jensen, F.B. (Eds.). Fish Ecophysiology. Chapman & Hall, London, pp. 1±44. Jobling, M., 1994. Fish Bioenergetics. Chapman & Hall, London 309pp.

Jonassen, T.M., Imsland, A.K., Stefansson, S.O., 1999. The in¯uence of temperature and ®sh size on growth of juvenile halibut. J. Fish Biol. 54, 556±572. Karakiri, M., Berghahn, R., Von Westernhagen, H., 1989. Growth differences in 0-group plaice Pleuronectes platessa as revealed by otolith microstructure. Mar. Ecol. Prog. Ser. 55, 15±22. Kawamura, G., Ishida, K., 1985. Changes in sense organ morphology and behaviour with growth in the ¯ounder Paralichthys olivaceus. Bull. Jpn. Soc. Sci. Fish. 51, 155±165. Keefe, M., Able, K.W., 1993. Patterns of metamorphosis in summer ¯ounder Paralichthys dentatus. J. Fish. Biol. 42, 713±728. Kikuchi, K., Takeda, S., Honda, H., Kiyono, M., 1990. Oxygen consumption and nitrogenous excretion of starved Japanese ¯ounder Paralichthys olivaceus. Nippon Suisan Gakkaishi 56, 1891. Kikuchi, K., Takeda, S., Honda, H., 1992. Nitrogenous excretion of juvenile and young Japanese ¯ounder. Nippon Suisan Gakkaishi 58, 2329±2333. Kirk, R.G., Howell, B.R., 1972. Growth rates and food conversion in young plaice Pleuronectes platessa L. fed on arti®cial and natural diets. Aquaculture 1, 29±34. Kitamura, S., 1990. Changes in the retinal photosensitivity of ¯ounder Paralichthys olivaceus during metamorphosis. Nippon Suisan Gakkaishi 56, 1007. Kramer, D.L., 1987. Dissolved oxygen and ®sh behavior. Env. Biol. Fish. 18, 81±92. Kuipers, B.R., 1977. On the ecology of juvenile plaice on a tidal ¯at in the Wadden Sea. Neth. J. Sea Res. 11, 56±91. Laroche, J.L., 1982. Growth during metamorphosis of English sole Parophrys vetulus. Fish. Bull. US 80, 150±153. Liu, H., Sakurai, Y., Munehara, H., Shimazaki, K., 1997. Diel rhythms of oxygen consumption and activity level of juvenile ¯ounder Paralichthys olivaceus. Fish. Sci. 63, 655±658. Lockwood, S.J., 1984. The daily food intake of 0-group plaice (Pleuronectes platessa L.) under natural conditions: changes with size and season. J. Cons. Int. Explor. Mer 41, 181±193. Malloy, K.D., Targett, T.E., 1991. Feeding, growth and survival of juvenile summer ¯ounder Paralichthys dentatus: experimental analysis of the effects of temperature and salinity. Mar. Ecol. Prog. Ser. 72, 213±223. Malloy, K.D., Targett, T.E., 1994. Effects of ration limitation and low temperature on growth, biochemical condition, and survival of juvenile summer ¯ounder from two Atlantic coast nurseries. Trans. Am. Fish. Soc. 123, 182±193. Malloy, K.D., Yamashita, Y., Yamada, H., Targett, T.E., 1996. Spatial and temporal patterns of juvenile stone ¯ounder Kareius bicoloratus growth rates during and after settlement. Mar. Ecol. Prog. Ser. 131, 49±59. Marchand, J., Masson, G., 1989. Process of estuarine colonization by 0-group sole (Solea solea): hydrological conditions, behaviour, and feeding activity in the Vilaine estuary. Rapp. P.-v. ReÂun. Cons. Int. Explor. Mer 191, 287±295. Masuda, R., Tsukamoto, K., 1999. School formation and concurrent developmental changes in carangid ®sh with reference to dietary conditions. Env. Biol. Fish. 56, 243±252. Masuda, R., Takeuchi, T., Tsukamoto, K., Ishizaki, Y., Kanematsu, M., Imaizumi, K., 1998. Critical involvement of dietary

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218 docosahexaenoic acid in the ontogeny of schooling behaviour in the yellowtail. J. Fish Biol. 53, 471±484. Metcalfe, J.D., Arnold, G.P., Webb, P.W., 1990. The energetics of migration by selective tidal stream transport: an analysis for plaice tracked in the southern North Sea. J. Mar. Biol. Ass. UK 70, 149±162. Miller, J.M., 1997. Opening address of the Third Flat®sh Symposium. J. Sea Res. 37, 183±186. Miller, J.M., Burke, J.S., Fitzhugh, G.R., 1991. Early life history patterns of Atlantic North American ¯at®sh: likely (and unlikely) factors controlling recruitment. Neth. J. Sea Res. 27, 261±275. Miller, J.M., Neill, W.H., Duchon, K.A., 1997. An ecophysiological model for predicting performance of released ®sh. Bull. Natl. Res. Inst. Aquacult., Suppl. 3, 87±91. Miller, J.M., Neill, W.H., Duchon, K.A., Ross, S.W., 2000. Ecophysiological determinants of secondary production in salt marshes: A simulation study. In: Weinstein, M.P., Litvin, D. (Eds.). Concepts and Controversies in Tidal Marsh Ecology. Kluwer Academic Press, Dordrecht, pp. 309±325. Minami, T., Tanaka, M., 1992. Life history cycles in ¯at®sh from the northeastern Paci®c, with particular reference to their early life histories. Neth. J. Sea Res. 29, 35±48. Miwa, S., Inui, Y., 1987. Effects of various doses of thyroxine and triiodothyronine on the metamorphosis of ¯ounder (Paralichthys olivaceus). Gen. Comp. Endocrinol. 67, 356±363. Miwa, S., Inui, Y., 1991. Thyroid hormone stimulates the shift of erythrocyte populations during metamorphosis of the ¯ounder. J. Exp. Zool. 259, 222±228. Miwa, S., Tagawa, M., Inui, Y., Hirano, T., 1988. Thyroxine surge in metamorphosing ¯ounder larvae. Gen. Comp. Endocrinol. 70, 158±163. Miwa, S., Yamano, K., Inui, Y., 1992. Thyroid hormone stimulates gastric development in ¯ounder larvae during metamorphosis. J. Exp. Zool. 261, 424±430. Morgan, J.D., Iwama, G.K., 1991. Effects of salinity on growth, metabolism, and ion regulation in juvenile rainbow and steelhead trout (Oncorhynchus mykiss) and fall Chinook salmon (Oncorhynchus tshawytscha). Can. J. Fish. Aquat. Sci. 48, 2083±2094. Neill, W.H., Bryan, J.D., 1991. Responses of ®sh to temperature and oxygen, and response integration through metabolic scope. In: Brune, D.E., Tomasso, J.R. (Eds.). Aquaculture and Water Quality, Advances in World Aquaculture. The World Aquaculture Society, Baton Rouge, pp. 30±57. Neill, W.H., Miller, J.M., Van der Veer, H.W., Winemiller, K.O., 1994. Ecophysiology of marine ®sh recruitment: a conceptual framework for understanding interannual variability. Neth. J. Sea Res. 32, 135±152. Nishioka, R.S., Grau, E.G., Bern, H.A., 1985. In vitro release of growth hormone from the pituitary gland of Tilapia Oreochromis mossambicus. Gen. Comp. Endocrinol. 60, 90±94. Noichi, T., Noichi, T., Senta, T., 1997. Comparison of ages, morphology and osteology by birth months of larval Japanese ¯ounder settling at Yanagihama Beach, Nagasaki Prefecture, Japan. Fish. Sci. 63, 169±174. Osse, J.W.M., Van den Boogaart, J.G.M., 1997. Size of ¯at®sh

217

larvae at transformation, functional demands and historical constraints. J. Sea Res. 37, 229±239. Pandian, T.J., 1970. Intake and conversion of food in the ®sh Limanda limanda exposed to different temperatures. Mar. Biol. 5, 1±17. Pauly, D., 1994. A framework for latitudinal comparisons of ¯at®sh recruitment. Neth. J. Sea Res. 32, 107±118. Person-Le Ruyet, J., Galland, R., Le Roux, A., Chartois, H., 1997. Chronic ammonia toxicity in juvenile turbot (Scophthalmus maximus). Aquaculture 154, 155±171. Peters, D.S., Angelovic, J.W., 1973. Effects of temperature, salinity, and food availability on growth and energy utilization of juvenile summer ¯ounder, Paralichthys dentatus. In: Nelson, D.J. (Ed.). Proceedings of the Third National Symposium of Radioecology. US Atomic Energy Commission, Oak Ridge, pp. 545± 554. Peters, D.S., Kjelson, M.A., 1975. Consumption and utilization of food by various postlarval and juvenile ®shes of North Carolina estuaries. Estuar. Res. 1, 448±472. Petersen, J.K., Pihl, L., 1995. Responses to hypoxia of plaice, Pleuronectes platessa, and dab, Limanda limanda, in the south-east Kattegat: distribution and growth. Env. Biol. Fish. 43, 311±321. Powell, A.B., Schwartz, F.J., 1977. Distribution of paralichthid ¯ounders (Bothidae: Paralichthys) in North Carolina estuaries. Chesapeake Sci. 18, 334±339. Rankin, J.C., Jensen, F.B., 1993. Fish ecophysiology: The comparative physiologist's viewpoint. In: Rankin, J.C., Jensen, F.B. (Eds.). Fish Ecophysiology. Chapman & Hall, London, pp. xvi±xix. Rasmussen, R.S., Korsgaard, B., 1996. The effect of external ammonia on growth and food utilization of juvenile turbot (Scophthalmus maximus L.). J. Exp. Mar. Biol. Ecol. 205, 35±48. Rijnsdorp, A.D., Van Stralen, M., 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. Ron, B., Shimoda, S.K., Iwama, G.K., Grau, E.G., 1995. Relationships among ration, salinity, 17a-methyltestosterone and growth in the euryhaline tilapia, Oreochromis mossambicus. Aquaculture 135, 185±193. Rountree, R.A., Able, K.W., 1992. Foraging habits, growth, and temporal patterns of salt-marsh creek habitat use by young-ofthe-year summer ¯ounder in New Jersey. Trans. Am. Fish. Soc. 121, 765±776. Sakamoto, T., McCormick, S.D., Hirano, T., 1993. Osmoregulatory actions of growth hormone and its mode of action in salmonids: a review. Fish Physiol. Biochem. 11, 1±6. Sakamoto, T., Shepherd, B.S., Madsen, S.S., Nishioka, R.S., Siharath, K., Richman III, N.H., Bern, H.A., Grau, E.G., 1997. Osmoregulatory actions of growth hormone and prolactin in an advanced teleost. Gen. Comp. Endocrinol. 106, 95±101. Seikai, T., Tanangonan, J.B., Tanaka, M., 1986. Temperature in¯uence on larval growth and metamorphosis of the Japanese ¯ounder Paralichthys olivaceus in the laboratory. Bull. Jpn. Soc. Sci. Fish. 52, 977±982. Seikai, T., Takeuchi, T., Park, G.S., 1997. Comparison of growth, feed ef®ciency, and chemical composition of juvenile ¯ounder

218

Y. Yamashita et al. / Journal of Sea Research 45 (2001) 205±218

fed live mysids and formula feed under laboratory conditions. Fish. Sci. 63, 520±526. Shaw, M., Jenkins, G.P., 1992. Spatial variation in feeding, prey distribution and food limitation of juvenile ¯ounder Rhombosolea tapirina GuÈnther. J. Exp. Mar. Biol. Ecol. 165, 1±21. Shepherd, B.S., Sakamoto, T., Nishioka, R.S., Richman III, N.H., Mori, I., Madsen, S.S., Chen, T.T., Hirano, T., Bern, H.A., Grau, E.G., 1997. Somatotropic actions of the homologous growth hormone and prolactins in the euryhaline teleost, the tilapia, Oreochromis mossambicus. Proc. Natl. Acad. Sci. USA 94, 2068±2072. Smith, T.I.J., Denson, M.R., Heyward, L.D., Jenkins, W.E., Carter, L.M., 1999. Salinity effects on early life stages of southern ¯ounder Paralichthys lethostigma. J. World Aquacult. Soc. 30, 236±244. Specker, J.L., Schreiber, A.M., McArdle, M.E., Poholek, A., Henderson, J., Bengtson, D.A., 1999. Metamorphosis in summer ¯ounder: effects of acclimation to low and high salinities. Aquaculture 176, 145±154. Szedlmayer, S.T., Able, K.W., 1993. Ultrasonic telemetry of age-0 summer ¯ounder, Paralichthys dentatus, movements in a southern New Jersey estuary. Copeia (3), 728±736. Szedlmayer, S.T., Able, K.W., Rountree, R.A., 1992. Growth and temperature-induced mortality of young-of-the-year summer ¯ounder (Paralichthys dentatus) in southern New Jersey. Copeia (1), 120±128. Tallqvist, M., Sandberg-Kilpi, E., Bonsdorff, E., 1999. Juvenile ¯ounder, Platichthys ¯esus (L.), under hypoxia: effects on tolerance, ventilation rate and predation ef®ciency. J. Exp. Mar. Biol. Ecol. 242, 75±93. Tanaka, M., Goto, T., Tomiyama, M., Sudo, H., 1989a. Immigration, settlement and mortality of ¯ounder (Paralichthys olivaceus) larvae and juveniles in a nursery ground, Shijiki Bay, Japan. Neth. J. Sea Res. 24, 57±67. Tanaka, M., Goto, T., Tomiyama, M., Sudo, H., Azuma, M., 1989b. Lunar-phased immigration and settlement of metamorphosing Japanese ¯ounder larvae into the nearshore nursery ground. Rapp. P.-v. ReÂun. Cons. Int. Explor. Mer 191, 303±310. Tanaka, M., Tanangonan, J.B., Tagawa, M., de Jesus, E.G., Nishida, H., Isaka, M., Kimura, R., Hirano, T., 1995. Development of the pituitary, thyroid and interrenal glands and applications of endocrinology to the improved rearing of marine ®sh larvae. Aquaculture 135, 111±126. Tanaka, M., Kawai, S., Seikai, T., Burke, J.S., 1996. Development of the digestive organ system in Japanese ¯ounder in relation to metamorphosis and settlement. Mar. Fresh. Behav. Physiol. 28, 19±31. Tanaka, M., Seikai, T., Yamamoto, E., Furuta, S., 1998. Signi®cance of larval and juvenile ecophysiology for stock enhancement of the Japanese ¯ounder, Paralichthys olivaceus. Bull. Mar. Sci. 62, 551±571. Tanangonan, J.B., Tagawa, M., Tanaka, M., Hirano, T., 1989. Changes in tissue thyroxine level of metamorphosing Japanese

¯ounder Paralichthys olivaceus reared at different temperatures. Nippon Suisan Gakkaishi 55, 485±490. Van der Veer, H.W., 1986. Immigration, settlement, and densitydependent 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. Van der Veer, H.W., 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. Van der Veer, H.W., Witte, J.I.J., 1993. The maximum growth/ optimal food condition hypothesis: a test for 0-group plaice Pleuronectes platessa in the Dutch Wadden Sea. Mar. Ecol. Prog. Ser. 101, 81±90. Waller, U., 1992. Factors in¯uencing routine oxygen consumption in turbot, Scophthalmus maximus. J. Appl. Ichthyol. 8, 62±71. Warlen, S.M., Burke, J.S., 1990. Immigration of larvae of fall/ winter spawning marine ®shes into a North Carolina estuary. Estuaries 13, 453±461. Watanabe, T., 1993. Importance of docosahexaenoic acid in marine larval ®sh. J. World Aquacult. Soc. 24, 152±161. Whitledge, T.E., 1985. Nationwide review of oxygen depletion and eutrophication in estuarine and coastal waters: Northeast Region. Brookhaven National Laboratory, Upton, 718pp. Winberg, G.G., 1956. Rate of metabolism and food requirements of ®sh. Fish. Res. Bd. Can. Transl. Ser. 194 (1960), 202pp. Woodhead, P.J.M., 1964. The death of North Sea ®sh during the winter of 1962/63 particularly with reference to the sole Solea vulgaris. HelgolaÈnder Wiss. Meeresunters. 10, 283±300. Yamano, K., Miwa, S., Obinata, T., Inui, Y., 1991. Thyroid hormone regulates developmental changes in muscle during ¯ounder metamorphosis. Gen. Comp. Endocrinol. 81, 464±472. Yamano, K., Takano-Ohmuro, H., Obinata, T., Inui, Y., 1994. Effect of thyroid hormone on developmental transition of myosin light chains during ¯ounder metamorphosis. Gen. Comp. Endocrinol. 93, 321±326. Yamashita, Y., Tsuruta, Y., Yamada, H., 1996. Transport and settlement mechanisms of larval stone ¯ounder, Kareius bicoloratus, into nursery grounds. Fish. Oceanogr. 5, 194±204. Yamashita, Y., Yamada, H., Neill, W.H., Miller, J.M., 2000. Ecophysiology model for evaluating carrying capacity and appropriate stocking level for Japanese ¯ounder juveniles. Abstracts for Meeting of the Japanese Society of Fisheries Science, 1±5 April 2000, p. 54 (in Japanese). Yasunaga, Y., Koshiishi, Y., 1980. Basic studies of problems on the propagation of plaice, Paralichthys olivaceus I. Acclimation to low salinity, feeding and gathering behaviour. Bull. Jpn. Sea Reg. Fish. Res. Lab. 31, 17±31 (in Japanese with English abstract). Youson, J.H., 1988. First metamorphosis. In: Hoar, W.S., Randall, D.J. (Eds.). Fish Physiology Vol. XI (Part B). Academic Press, London, pp. 135±196.