Impact of juvenile growth on recruitment in flatfish

153

Netherlands Journal of Sea Research 32 (2): 153-173 (1994)

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH HENK W. VAN DER VEER ~, RODIGER BERGHAHN 2 and ADRIAAN D. RIJNSDORP3 1Netherlands Institute for Sea Research, P.O. Box 59, 1790AB Den Burg, Texel, The Netherlands 2EIbelabor, Universit~t Hamburg, Crosse Elbstrasse 268, 22767 Hamburg, Germany 3Netherlands Institute for Fisheries Research, P.O. Box 68, 1970AB IJmuiden, The Netherlands

ABSTRACT In this review, the impact of juvenile growth on subsequent recruitment in flatfish is discussed. Recruitment is defined as the number of specimens of a specific year class that survives to attain sexual maturity and Joins the reproductive population. Theoretically, variability in growth rate can have an Impact on recruitment either by means of size-selective mortality during Juvenile life and/or by means of size-dependent onset of maturation. In flatfish up to about 10 cm, growth depends on size in such a way that variability in size within a population increases during the first year of life, and decreases again in the subsequent part of Juvenile life. Temporal variability in size within local populations appears to be lower than spatial variability. Due to the prolonged spawning period, and hence period of settlement, variability in size of Juvenile flatfish increases with decreasing latitude. As a consequence of these patterns, size-selective mortality appears to be mainly restricted to the 0-group and to gain importance with decreasing latitude. A literature search for field data yielded only a few references suggesting size-selective mortality. In none of the studies was any relationship with ultimate recruitment studied or even suggested. Size-dependent onset of maturation has been found in some flatfish species, with slow-growing individuals or cohorts showing delayed maturation. Size-dependent onset of maturation has a clear effect on the level of recruitmenL However, in the species studied, the main traits in year-class strength still existed at the moment of recruitment to the reproducing stock. Size-dependant onset of maturation also appeared to affect the year-to-year variability in recruitment, but different effects were observed among species. It is argued that both size-selective mortality and size-dependent onset of maturation are more likely to dampen than to generate variability in recruitment. The study of the impact of Juvenile growth on recruitment in flatfish is hampered by the absence of long-term data sets on recruitment. Especially comparable series of (sub)tropical spaclea and of populations covering the total range of distribution of a species are lacking. 1. INTRODUCTION The juvenile stage of flatfish can be defined as the period between metamorphosis after larval settlement and the onset of maturation, when---by definition-they recruit to the adult stock. The ultimate annual level in recruitment of juveniles to the parent stock will therefore be affected by the variable combination of juvenile mortality and length of juvenile period. Mortality (Cushing, 1974; Rothschild, 1986; Zijlstra et aL, 1982) as well as the onset of maturation (Rijnsdorp, 1993a, 1993b)is directly determined by fish size. Both fish size and age at first maturity are functions of the growth rate and hence the environmental conditions during the juvenile phase. Therefore, juvenile growth may have an impact on both the level of recruitment and on recruitment variability. So far, the impact of variability in juvenile growth on recruitment has not been analysed in flatfish. This review attempts to quantify the importance of differences in juvenile growth in affecting mortality and the

onset of maturation and in determining level of and variability in recruitment of flatfish. Since most studies deal with growth expressed in length increase over time, this unit will be used in this study instead of instantaneous growth rates. No attempt is made to present a complete literature review. Only the basic principles will be illustrated. Most information available is from temperate species, and this may have biased the conclusions to some extent. The role of predation on juvenile flatfish by generating or dampening recruitment variability will be dealt with by Bailey (1994), while Gibson (1994) discusses the importance of habitat quality and quantity. Population processes operating in the adult phase are discussed by Rijnsdorp (1994). To prevent confusion, the principal terms used will be defined first, followed by the outline of the theoretical construct. Subsequently, the results of a literature review are analysed and discussed. Finally, some suggestions for future research will be made.

154

H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP 2. DEFINITIONS

In this paper the following definitions are used: Recruitment: The process whereby, in this case, juvenile flatfish survive to attain sexual maturity and join the reproductive population. Recruitment level: The ultimate number of a specific year class that survives to attain sexual maturity and joins the reproductive population. Recruitment variability: The variability in recruitment level over a number of years, expressed as coefficient of variation. Year-class strength: The estimate of the number of juveniles of a specific year class during their development between settlement and recruitment.

Variability-generating

factors

(controlling

factors):

Factors that generate the among-year variability in year-class strength and recruitment, which is illustrated by an increase in the coefficient of variation of abundance estimates over a number of years at a certain life stage compared with that of a previous stage. Variability-damping factors (regulating factors): Factors that reduce the among-year variability in yearclass strength and ultimate recruitment, which is illustrated by a decrease in the coefficient of variation of abundance estimates over a number of years at a certain life stage compared with that of a previous stage. Juvenile: The life history stage between the end of metamorphosis after larval settlement and the attainment of sexual maturity. Growth: The process of individual development, characterized by changes in individual weight and length. Variability in growth: The existence of different growth rates, between individuals, populations or years, ranging from starvation to the highest observed (and hence possible) growth rate under the conditions studied. Maturity: The 'juvenile-adult' transition, which means the end of the process of sexual development of individual immature juvenile fish, characterized by the development of the reproductive organs. In plaice the ripening of testis or ovaries to stage 2 are taken as indicator (Rijnsdorp, 1989). On the population level, length (Lmat) and mean age (Ama~ at first maturation are distinguished. They are defined as, respectively, the length and the mean age at which 50% of the population becomes mature. 3. THEORETICAL FRAMEWORK The number of juvenile flatfish that after settlement will ultimately recruit to the adult stock can be described by the familiar equation:

R = S*e

- (M1tl + M2t2 + ...Mit~)

in which R is the number of juveniles that becomes mature and recruits to the adult stock; S represents the number of settling and metamorphosing larvae, Mj is the instantaneous mortality rate at stage i and ti is the duration of stage L Ultimate recruitment is determined by the instantaneous mortality rates at the different stages, in combination with the stage durations. The sum of all stages is the time from settlement to the onset of maturation (tl + t2 + ... ti). Recruitment variability will be influenced by factors generating variability in M and/or t. Growth is one such factor. It affects both M and t by means of sizerelated mortality and of size-dependent onset of maturation. 3.1. GROWTH Annual growth rate decreases with fish size and this relationship of juvenile and adult (flat)fish growth both in weight and in length can be described by the Von Bertalanffy growth equation (e.g. Beverton & Holt, 1957). Laboratory studies have shown that the key factors determining the daily growth in length of individual flatfish are size of the fish, food availability and temperature (e.g. Fonds, 1979; Fonds et aL, 1992; Jobling, 1993). Growth rate can be affected by both density-independent and density-dependent processes. Densityindependent processes are thought to act mainly by variability in water temperature and by differences n food quality and quantity. Density-dependent processes will be induced by competition for food among the individual flatfish. Food quality and quantity vary spatially and temporally, as does temperature. Therefore, food availability and temperature will differ over time among individuals and populations. As a consequence, in the field, differences in growth rate of juvenile flatfish can always be observed among individuals m a population, among populations, and among years, which will ultimately be reflected in differences in the mean size and in its variability. 3.2. SIZE-RELATED MORTALITY Size-related mortality was first described by Sund (1911, in Ricker, 1969) in relation to what later became known as Lee's phenomenon: the observation of greater mortality among larger individuals than among smaller ones of a given age (Ricker, 1969). Size-selective mortality was thought to arise either from natural mortality or size-selective catchability. This principle of size-selective mortality has later been applied in an inverse way for the early life stages by for instance Ware (1975). If predation decreased with increasing fish size, then survival would be directly related to growth. Ware (1975) especially applied size-selective mortality to the larval stages, and this was referred to as the 'growth-mortality hypothesis' by Anderson (1988). Conover

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH (1992) suggested that size-dependent mortality might be a key factor determining the winter survival of especially juveniles. Size-related mortality will furthermore be affected by prevailing water temperature and the predator field (Van der Veer & Bergman, 1987). In general, mortality during the juvenile stage will decrease with fish size, until the juveniles become available to the fisheries. From this stage onwards an increase of mortality with size will occur, which means that size-selective mortality is a function of the growth rate. 3.3. SIZE-DEPENDENT ONSET OF MATURATION Maturation is a developmental process that is coupled to the physiology of energy acquisition and hormone kinetics. According to the conventional view, a fish becomes sexually mature when it has passed some fixed size- or age-threshold (Nikolskii, 1969; Roff, 1982, 1983, 1991). However, in a more general representation, fish mature according to a trajectory in the length-age space (MacKenzie et aL, 1983; Stearns & Crandall, 1984; Reznick, 1992; Rijnsdorp, 1993a). In this model, which includes the fixed sizeor age-threshold as special cases, both length and age at first maturity are functions of the growth rate and the environmental conditions during the juvenile phase. The shape of the trajectory will be speciesspecific as such shapes evolved in response to the environmentally determined scope for growth and mortality rates in both the juvenile and adult phases (Stearns & Crandall, 1984; Stearns & Koella, 1986). Above, length and age at first maturity were used as proxies for the average juvenile-adult transition points for the population. However, the process of ovarian maturation starts well before the spawning period (Barr, 1963; Deniel, 1981; Rijnsdorp, 1989; Fargo & Tyler, 1994). There are even indications that ovarian maturation could span a period of several years (Dunn & Tyler, 1969; Burton & Idler, 1984; Rijnsdorp, 1993b). The maturation trajectories, therefore, should not be considered constant because they may be a function of growth rate. 4. FIELD DATA Table 1 presents an overview of field studies comparing juvenile growth of flatfish in different areas and years. Most studies selected fulfilled the requirements set by Miller et aL (1992). Only the most important growth aspects will be discussed below. 4.1. GROWTH Variability in growth can be studied on an individual basis by tagging of individual fish, or by means of back-calculation from otolith microstructure analysis (for a review see Stevenson & Campana (1992)), and for populations by shifts in size-frequency distribu-

155

tions, or by comparison of mean or median size among populations and/or years. Tagging of individual fish and otolith microstructure analysis are the only methods that result in unbiased estimates of individual growth. As soon as estimates of population growth are made, it cannot be excluded that they will be biased by processes such as size-selective mortality, irrespective of whether they are based on otolith analysis or on shifts in size-frequency distributions. Back-calculations of growth by means of otolith microstructure analysis result in variability in growth estimates between individuals (e.g. Karakiri et aL, 1989), which is generally thought to be caused by (slight) variability in (a)biotic factors in the environment, although genetic differences may be involved as well. At the individual level, variability in growth is considered to be a natural phenomenon and has been accepted more or less as an axiom. The most important factors determining growth are temperature, fish size and food quality and quantity. The basic principles will be illustrated in the following without going into detail. 4.1.1. IMPACT OF TEMPERATURE Since fishes are cold-blooded animals, all processes will be directly affected by prevailing temperature, and hence fish growth will (among other factors) be a function of temperature. Extensive studies have been carried out on the bioenergetics of fish; only the main principles will be discussed. For further details see e.g. Jobling (1993) and Neill et aL (1994). The general equation describing fish energetics is: ING = LOSSFAE + LOSSEx c + META + PROD

in which ING is the amount of energy ingested; LOSSFAE is the energy lost in faeces, LOSSExc is the loss in excretory products; META is the energy spent on metabolism and PROD is the fish production in body growth. Ultimate fish growth will mainly be determined by the balance between ingestion and metabolism, which are the major factors. Both ingestion and metabolism are temperature dependent, though in a different way (Jobling, 1993). Metabolism will continuously increase with rising temperatures. Ingestion will also increase at rising temperature, but as soon as temperature approaches the upper lethal temperature of the species, ingestion rate will decrease (Fig. 1). As a consequence, the relationship between temperature and growth will be a skewed dome-shaped curve in the form of Fig. lb. The ultimate shape of the growth curve and the optimal temperature for growth will be species-specific. Fig. 2 shows the growth curves for some temperate and some subtropical flatfish species. In all species, the shape of the growth curve was rather similar. The optimal temperature for growth was

156

H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP

TABLE 1 Field studies comparing growth of juvenile flatfish in different areas and/or years. AG: age group: 0= 0-group; I= I-group; I1= II-group. Method: I= comparison of growth in different areas, based on length increase of fietd population; I1= comparison of growth in different years, based on length increase of field population; II1=comparison of growth !n different areas, based on otolith microstructure analysis; IV= comparison of growth in different years, based on otoli{h microstructure analysis; V= comparison to growth in the laboratory; VI= field experiment (cages, transplantation, food intake, tagging); VII-- before/after drastic changes in fishing effort.

Ammotretis rostratus Citharichthys spilopterus Etropus crossotus Glyptocephalus cynoglossus Hippoglossus stenolepis Limanda limanda

Paralichthys califomicus Platichthys flesus

Pleuronectes platessa

Pseudopleuronectes americanus Rheinhardtius hippoglossoides Rhombosolea tapidna Solea solea Solea lascaris Symphurus plagiusa

AG

region

method

0 0 0 >0 >0 >0 >0 >0 >0 >0 0 0 >0 >0 >0 0 >0 >0 >0 >0 >0 >0 >0 >0 0 0 >0 0 >0 0 >0 0 0 >0 >0 0 >0 0 0 >0 >0 >0 0 >1 0 0 >0 0 >11 >0 >0 >0 0

Australia Georgia Georgia Newfoundland Kamchatka Pacific ICES subdiv. 22 North Sea North Sea French coast San Diego Loch Craiglin Loch Kyle Lake Grevelingen Baltic Sea Ba!gzand North Sea North Sea North Sea North Sea North Sea Loch Craiglin Loch Kyle North Sea Loch Ewe Filey Bay Balgzand Balgzand Lake Grevelingen Balgzand Danish fjord German Wadden Sea German Wadden Sea North Sea ICES subdiv. 22 German Wadden Sea French coast North Sea Dutch Wadden Sea North Sea Port Erin North Sea Dutch Wadden Sea Nova Scotia New Jersey New Jersey NE Atlantic Australia North Sea French coast North Sea French coast Georgia

III,V V V VII II I, II I I II I I VI VI I I, II II,V I II,Vll I,Vl I,VI II,VII VI VI II II,V II II II,V II,V VI I,V II,V II,V I I11, IV t lI,V III,V II II,VI II,IV I,V I,VII V III III, IV III,V II I II I V

reference Jenkins, 1987 Reichert & Van der Veer, 1991 Reichert & Van der Veer, 1991 Bowering, 1989 D'aykov, 1977 McCaughran & Summerfelt, 1987 Bagge & Nielsen, 1989 Lozan, 1989 Lozan, 1989 Deniel, 1990 Kramer, 1991 Gross, 1947 Gross, 1950 Doornbos & Twisk, 1984 Berner et aL, 1989 Van der Veer et aL, 1991 Borley, 1909 Borley, 1923 Carruthers, 1924 Hickling, 1938 Beckmann, 1944 Gross, 1947 Gross, 1950 Kotthaus, 1956 Steele 8, Edwards, 1970 Lockwood, t972 Kuipers, 1977 Zijlstra et aL, 1982 Doornbos & Twisk, 1984 Van der Veer, 1986 Hoffmann & Degel, 1987 Berghahn, 1987 Berghahn, 1987 Bergman etaL, 1988 Bagge & Nielsen, 1989 Karakiri et aL, 1989 Deniel, 1990 Van der Veer et aL, 1990 Karakiri et aL, 1991 Rijnsdorp & Van Beek, 1991 Nash etaL, 1992 Rijnsdorp & Van Leeuwen, 1992 Van der Veer & Witte, 1993 Dickie & Mc'Cracken, 1955 Sogard, 1992 Sogard & Able, 1992 Boje & J~rgensen, 1991 Jenkins, 1987 Nielsen, 1973 Deniel, 1990 Rijnsdorp & Van Beek, 1991 Deniel, 1990 Reichert & Van der Veer, 1991

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH

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Temperature(oc) Fig. 1. Theoretical relationship between temperature and fish energetics, a. Relationship between temperature and intake (solid line) and metabolism (broken line), b. Relationship between temperature and fish growth. For more information see text. Redrawn after Jobling (1993). higher in the subtropical species than in the temperate species. However, in all species, maximum growth rate in length was similar, 1 mm'd 1. With increasing fish size, the optimal water temperature for maximum growth appeared to decrease, as has been found in plaice (Pleuronectes platessa) and flounder (Platichthys flesus) by Fonds et aL (1992). It may be expected that in other flatfish species, the relationship between temperature and growth will show a similar pattern. At present there is no information whether maximum growth in all species is similar (~1 mm.d-1). 4.1.2. IMPACT OF FISH SIZE The effect of fish size on growth rate has been studied in North Sea plaice (Pleuronectes platessa) and

157

sole (Solea solea). For these two species, growth was positively related with size during the first part of the juvenile stage up to a size of about 10 to 15 cm (Fonds, 1979), whereas in the later juvenile stage a negative relationship between growth and size develops (Fonds, 1979; Rijnsdorp & Van Beek, 1991), until they join the adult population at a size of about 15 to 35 cm (Zijlstra, 1972). It is expected that this relationship will be a common feature of growth in all flatfish species. The initial positive relationship between size and growth means that the variability in sizes within the population increases from the start of the growing season after settlement. At some point in the juvenile stage, this process will stop and subsequently a reduction in the variability in size will occur. Fig. 3 shows the growth of plaice in the Dutch Wadden Sea during its juvenile stage. Three growing seasons could be distinguished. The impact of growth on variability in size can be seen from the trends in standard deviation (S.D.) and in the coefficient of variation (C.V.) of the size-frequency distributions with time. The S.D. increased during the first year of life (0-group), remained more or less constant during the second year (I-group) and decreased during the third year (ll-group). This increase in S.D. during the first year of life reflected the positive influence of size on growth in the smallest difference in size range, whereas in the II-group the reverse situation was observed. The C.V. showed a more or less similar trend. After a slight increase directly after settlement, there was a continuous decrease during the juvenile stage. This suggests that the variability in size is largest during the early juvenile stage in the O-group. 1.25

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impact of food quality and quantity on growth of 0group plaice in the western Dutch Wadden Sea. In both the intertidal area and in the sublittoral they found a positive relationship between potential food abundance and growth of 0-group plaice (Fig. 5). Furthermore, a consistent difference in growth could be observed between the intertidal and the sublittoral. At a similar food abundance growth was higher in the intertidal. This difference could be attributed to food quality. Lugworms, Arenicola marina, were only present in the intertidal, where their tail-tips are an important food item in the stomachs of 0-group plaice (Kuipers, 1977; De Vlas, 1979; Van der Veer & Witte, 1993). In the intertidal, growth of 0-group plaice was

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Fig. 3. Courses of mean length and its variability in juvenile plaice (Pleuronectes platessa) in the Balgzand intertidal area during the first years of life in 1975 (rq), 1976 (0) and 1977 (A). a. Mean length (Mean; cm); b. Variability in size (S.D.; cm); c. Coefficient of variation (C.V.=S.D./Mean). Data from Kuipers (1977) and Dapper (1979).

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IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH 4.2.2. SPATIAL VARIABILITY

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Spatial variability in growth and size is presented for a number of 0-group plaice populations in the Dutch Wadden Sea studied simultaneously (Fig. 8). Spatial variability in growth appeared to be higher than temporal variability. At the end of the growing season in autumn, the year-to-year differences in mean length of the populations were about 20 to 25 mm (Fig. 8a). The trends in S.D. were similar in all subpopulations, although the variability among areas (Fig. 8b) was higher than that among years (Fig. 8b). Despite this spatial variability in growth and size, the C.V. values showed a similar pattern in all areas. After a period of

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Fig. 8. Growth of 0-group plaice (Pleuronectes p/atessa) at a number of intertidal areas in the Dutch Wadden Sea in 1986. rq=Balgzand; 0=Wadden; O=Lutjeswaard; A=Vtie; O=Ballastplaat, a. Mean length (Mean; ram); b. Variability of length (S.D.; mm); c. Coefficient of variation (C.V.=S.D./Mean). Data from Van der Veer & Witte (1993). slight increase, the C.V. started to drop and reached low values in autumn (Fig. 8c). In conclusion, in the 0-group spatial and temporal variability did not affect the general pattern of an increase in variability in size directly after settlement. Over short periods, spatial variability appears to be larger than temporal variability. 4.2.3. LATITUDINAL GRADIENTS Growth rates for cohorts of some temperate, subtropical and tropical 0-group flatfish species are compared in Fig. 9. Despite large differences in water tempera-

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Week Fig. 9. Changes in mean lengths of cohorts of some temperate, subtropical and tropical 0-group flatfish species in the course of the growing season, a. Mean length (Mean; mm); b. Variability of length estimates (S,D.; mm); c. Coefficient of variation (C.V.=S.DJMean) Data from: temperate species (O=Pteuronectes platessa; R=Limanda limanda): Van der Veer (1986); subtropical species (O=Citharichthys spilopterus; O=Symphurus plagiusa): Reichert & Van der Veer (1991); tropical species (ill =Cyclopsetta chittendeni; E) = Citharichthys stampliO: Pauly (1994) and Van der Veer (unpubl.). ture, the growth rate of the various flatfish species was rather similar (Fig. 9a). The variability in size (S.D.) increased in almost all species (Fig. 9b), indicating size-dependent growth also in (sub)tropical species. The C.V. increased after settlement or remained stable, and decreased in the course of the growing season (Fig. 9c). There is a latitudinal gradient in the period of larval settling whose duration increases with decreasing latitude (Fig. 10). At low

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH latitudes, more cohorts are settling each year. Fig. 11 shows the mean length and variability in size of some temperate, subtropical and tropical species. Although the growth patterns of individual species did not differ (Fig. 9), the variability in size of their members increased in (sub)tropical species at low latitudes (Fig. 11 b), due to the prolonged period of larval settlement. As a consequence the overall size-frequency distributions are broader at low latitudes. Although the C.V. decreased in individual cohorts of (sub)tropical species (Fig. 11c), this pattern disappeared when the whole 0-group population was considered. In conclusion, the variability in size appears to increase from temperate towards subtropical and tropical areas; the widest range was observed in tropical juvenile flatfish. 4.2.4. IMPACT OF FISHERIES Pre-recruit surveys of exploited populations offer the opportunity to study the variability in length-at-age during the juvenile phase over longer periods (Fig. 12). Records of exploited populations in various areas also show variability in juvenile growth which is a multitude of the interannual variations of local populations. An increase in the mean length-at-age of recruiting age groups has been observed in a number of flatfish since exploitation started (Table 2). For example, the length-at-age relationship of Baltic plaice and flounder showed an increase in both the

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Fig. 11. Mean size of some temperate, subtropical and tropical 0-group flatfish populations in the course of the growing season, a. Mean length (Mean; mm); b. Variability of length estimates (S.D.; mm); c. Coefficient of variation (C.V.=S.D./ Mean). For meaning of symbols see legend of Fig. 9. Data from: temperates species: Van der Veer (1986); subtropical species: Re•chert & Van der Veer (1991); tropical species: Pauly (1994) and Van der Veer (unpubl.).

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Fig. 10. Latitudinal variation in timing of settlement of various groups of flatfish, as indicated by the time (month) of the spawning season. Redrawn after Minami & Tanaka (1992).

intercept and the slope after exploitation started at the beginning of this century. Although the age(s) at which the increase in growth occurred cannot be determined from such data, the increase may be related to the decline in population density due to exploitation in those species that show an overlap in spatial distribution between the juveniles and the exploited part of the population. Examples are some flatfish species in the northwest Atlantic. Nursery areas of American plaice (Hippoglossoides plates-

162

H.W. VAN DER VEER, R. B E R G H A H N & A.D. RIJNSDORP

TABLE 2 Age (Amat) and length (Lmat) at first sexual maturity in flatfish in a period of low level of exploitation compared to a period with a high level of exploitation, nc - no change over the time period of study.

period Plaice, Pleuronectes platessa L. 1904-10 1927-28

area

Baltic Sea Baltic Sea North Sea German Bight German Bight Southern Bight Southern Bight Flamborough Flamborough

1904-11 1985-86 1904-11 1985-86 1904-11 1985-86 Flounder, Platichthys flesus L. 1920-30 Baltic Sea 1948-49 Baltic Sea Sole, Solea solea (L.) 1892 North Sea 1934 North Sea 1964-68 North Sea 1966-88 North Sea Yeilowfin sole, Limanda asper 1961 Kamchatka 1969 Kamchatka 1959-64 Bering Sea 1973 Bering Sea 1990 Bering Sea American plaice, Hippoglossoides platessoides 1961-65 NW Atl. 3L 1969-72 3L 1957-64 3N 1971 3N Witch flounder, Glyptocephalus cynoglossus 1959-64 NW Atl. 4T 1975-79 4T 1959-64 4Vn 1975-79 4Vn 1959-64 4Vs 1975-79 4Vs 1959-64 4W 1975-79 4W 1959-64 4X 1975-79 4X 1950-59 3Ps 1980-86 3Ps 1973-78 3K 1979-83 3K 1968-78 3L 1979-83 3L 1973-78 2J 1979-83 2J Pacific halibut, Hippoglossus stenolepus 1949-59 East Pacific area 2 1960-77 area 2 1949-59 area 3 1960-77 area 3

male

female

Lmat Arnat

Lmat Amat

source

16 23

3 3

22 28

3 3

Johansen, 1929 Molander; 1955

37 24 30 20

6.5 3 5.5 2

42 35 36 33 40 34

7.5 5 6.5 4 6.5 4.5

Rijnsdorp, 1989

3 3

18

2

17 13 20.3

3 3 27.5 27.2 27.5 27.0

3

29.9 27.2 31 25 28.8

8.5 7.2

Rijnsdorp, 1989

Molander, 1955

Holt, 1892 B0ckmann, 1934 De Veen, 1976 Van Beek, 1985 Tikhonov, 1978 Wilderbruer et aL, 1992

23.5 23.9 24.0 25.6

7.6 6.4 5.3 4.7

42.1 40.4 43.3 41.5

14~0 10.6 11.1 8.8

34.2 33.0 36.9 32.9 36.4 30.8 35.7 29.2 33.8 30.1 32.2 33.0 30.5 29.8 30.0 32.6

7.8 8.0 7.8 9.2 6.9 6.1 7.7 5.8 7.7 5.1 7.2 7.3 4.6 4.9 6.0 3.5

42.5 33.4 43.9 33.0 43.4 33.5 42.4 33.1 43.9 34.3 46.0 42.9 41.9 43.4 44.8 41.5 47.0 44.2

12.6 8.8 10~5 8.8 9.2 7.6 9.2 7.1 10.2 7.2 10.2 7.9 7.6 9.8 7.8 10.4 7.5

nc nc 120 125

12.4 12.1 11.8 10.9

-

Rijnsdorp, 1989

Pitt, 1975 Pitt, 1975

Beacham, 1983 Beacham, 1983 Beacham, 1983 Beacham, 1983 Beacham, 1983 Bowering, 1989 Bowering, 1987 Bowering, 1987 Bowering, 1987

Schmitt & Skud, 1978 Schmitt & Skud, 1978

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH

163

TABLE 2 (continued) Age (Area~ and length (Lmat)at first sexual maturity in flatfish in a period of low level of exploitation compared to a period with a high level of exploitation, nc - no change over the time period of study. period area male female source

Lmat Amat Atlantic halibut,

Lmat Amat

Hippoglossus hippoglosaus 1956-60 1981-85

north Atlantic north Atlantic

soides) and probably witch flounder (Glyptocephalus cynoglossus) overlap with the adult distribution areas (Walsh, 1991). In species with nursery grounds in shallow waters, such as sole, plaice and flounder in the North Sea and the Baltic (K~.ndler, 1932; Rijnsdorp & Van Beek, 1991), the increase in juvenile growth is most probably related to other factors than the abundance of the exploited population. Obviously, competition with both large and small plaice and other animals is important apart from prey size and density. Rijnsdorp & Van Leeuwen (1992) studied the changes in somatic growth of female North Sea plaice during the period 1930o1985 by means of otolith back-calculations. In this way, growth could be reconstructed for a number of age- and size-classes. A significantly retarded growth was found in the outstandingly strong 1963 year-class up to size class 15 to 20 cm (ll-group). This decrease in growth coincided with the build-up of competitive biomass (Rijnsdorp & Van Beek, 1991), suggesting the occurrence of density-dependent growth in the I- and/or IIgroup, but not in the 00group. From otolith analysis of 26 year classes (1953-1978) in the Pacific halibut (Hippoglossus stenolepis), Hagen & Quinn (1991) concluded that density-dependent growth did not appear to be a factor accounting for variability in juvenile growth. 4.3. SIZE-RELATED MORTALITY

12 7

13.5 8

Haug & Tjemsland, 1986

factor in the early life phase of this species. Field observations on size-selective mortality in juvenile flatfish are even more scarce. Predation by crustaceans has only been found in temperate areas, such as British waters (Edwards & Steele, 1968), the Dutch Wadden Sea (Van der Veer & Bergman, 1987) and Swedish bays (Pihl, 1990). Only Van der Veer & Bergman (1987) presented a detailed analysis of the predation by the brown shrimp on juvenile plaice. Based on otoliths found in the stomachs, the size spectrum of the 0-group plaice consumed was reconstructed and compared with the size-distribution of the 0-group plaice population in the field (Fig. 15). At the beginning of the settlement of larval plaice, there was no size-selective predation by the brown shrimp. However, from the end of April onwards, only the smaller size classes of 0-group plaice were preyed upon resulting in size-selective mortality (Table 3).

a

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Only few studies deal with size-selective mortality in juvenile flatfish. A few laboratory experiments have 25.0 been carried out in which predation pressure among newly settled flatfish was studied in relation to prey and predator size (Van der Veer & Bergman, 1987; Seikai et aL, 1993; Witting & Able, 1993). Newly-settled plaice were sensitive to predation by crusta- "~ 15.0" ceans, such as the brown shrimp Crangon crangon and the shore crab Carcinus maenas. Both predators 10.0. were able to prey upon a specific size range of 00 group plaice (Fig. 13). Predation rate decreased with 5.0 increasing size of prey. On the other hand, mortality was also affected by the size of the predator. A simi1 5 1970 1975 1980 1985 1990 lar size-dependent prey-predator system was observed in a flatfish species of warmer waters, the Fig. 12. Mean length (cm) in autumn of juvenile flatfish (a. Japanese flounder, Paralichthys olivaceus (Fig. 14). plaice, b. sole) from pre-recruit surveys (sexescombined) in Seikai et aL (1993) concluded that predation by the the North Sea, after Rijnsdorp et aL (1991). 13 = 0-group; shrimp Crangon affinis might be a significant mortality • = I-group. |

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164

H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP

Predation rate may also have been related to temperature (Fig. 16), but the analysis of Van der Veer & Bergman (1987) was not detailed enough to prove this. Size-dependent winter mortality has so far not been found in juvenile flatfish. Laboratory studies on summer flounder, Paralichthys dentatus, gave indications that at least in this species it might play only a minor role (Malloy &Targett, 1991; Szedlmayer et aL, 1992). In conclusion, size-selective mortality has been found in juvenile flatfish. Predation rate appears to be affected by the size of both the prey and the predator, as well as by the prevailing water temperature. The observations are restricted to the early demersal stages and to temperate waters. 4.4. SIZE,DEPENDENT ONSET OF MATURATION The relationship between size and maturation has been studied by Rijnsdorp (1993b) for North Sea plaice. Juvenile growth has a clear influence on matu-

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Predator size (mm) Fig. 14. Size-selective mortality of O-group J a p a n e s e flounder (Paralichthys olivaceus) by various size groups of the

crangonid shdmp Crangon affinis as predator under laboratory conditions. Data from Seikai et aL (1993). ration. Slow-growing plaice reach maturity at a smaller length, but higher age than fast-growing plaice. The proportion of mature female plaice increases with size and with age (Fig. 17). For plaice and a number of other flatfish species, there is ample evidence that the onset of maturation has also changed since exploitation started (Table 2), which is likely to be related to a corresponding increase in juvenile growth rate. In general, fish tend to mature at a younger age in exploited stocks than in lightly or unexploited stocks. Changes in maturation, however, do not necessarily reflect a trend in time since a substantial interannual variation in age (Amat) and length (Lmat) at first maturity may occur (Table 4; Fig. 18). 5. DISCUSSION

Predator size (mm)

5.1. THE THEORY o

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From a theoretical point of view, variability in growth of juvenile flatfish can have an impact on ultimate recruitment, either by affecting survival in case of

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Fig. 13. Size-selective mortality of O-group plaice (Pleuronectes platessa) by crustaceans as predators under laboratory conditions, a. Predation by various size groups of the brown shrimp Crangon crangon, b. Predation by various size groups of the shore crab Carcinus meanas. Data from Van der Veer & Bergman (1987).

TABLE 3 X2 test of goodness of fit between the size-frequency of 0group plaice in the field at Balgzand, and the reconstructed size-distribution of plaice consumed by shrimps, based on stomach analysis (otoliths) for the period of settlement in 1980. Data from Van der Veer (1986) and Van der Veer & Bergman (1987). date )~2 p< 005 28 February 1.33 n.s. 10 March 5.08 n.s. 24 March 3.24 n.s. 9 April 7.55 n.s. 21 April 16.24 6 May 16.17

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH

165

% 80 25-28/2

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size-selective mortality or by affecting the length of the juvenile stage. Both processes, size-selective mortality and size-dependent onset of maturation, have been found in flatfish field studies. Therefore, juvenile growth can in principle have an impact on recruitment in flatfish. The theoretical prediction that growth (by affecting size-selective mortality) plays a significant role in population dynamics (Beyer, 1989; Parma & Deriso, 1990), has so far not falsified by field observations on juvenile flatfish. The impact of variability in growth on recruitment was analysed in relation to its effect on mortality (m) and on juvenile stage duration (t). However, in commercially exploited populations juveniles become available to the fisheries before the onset of maturation. For these species, not only natural mortality (M) occurs, but also fishery mortality (F) will operate: R = S * e -(F+~t

in which R is the number of juveniles that become mature and recruit to the adult stock; S represents the number of settling and metamorphosing larvae, M is natural mortality and F is fishery mortality. All factors affecting t will have an impact on recruitment. There will be a minimum duration of the juvenile stage. At low densities, there will be no relation between density and t. However, if growth is reduced at high abundance, t will become positively related with S (Fig. 19). A relationship between density and stage duration will prolong the period of predation at high densities and therefore act in a negatively density-dependent way, damping the year-to-year varia0.15 -

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30 mm 0 10 Size class Fig. 15. Predation on various size groups of O-group plaice Pleuronectes platessa by the brown shrimp Crangon crangon in the Dutch Wadden Sea during the period of settlement, as revealed by means of analysis of otoliths found in shrimp stomachs (block columns) The actual size-frequency distributions of the plaice in the field are also shown (white columns). Data from Van der Veer & Bergman (1987).

2

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i

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4

6

8

10

12

Water temperature (°C)

Fig. 16. Relationship between rates of predation (expressed as instantaneous mortality rate; d "1) of O-group plaice P/euronectes platessa by the brown shrimp Crangon crangon in the Dutch Wadden Sea during the period of settlement and prevailing water temperature. Data from Van der Veer & Bergman (1987).

166

H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP

I

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5.2. IMPACT ON RECRUITMENT

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5.3. RECRUITMENT TO THE FISHERIES

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The impact of variability in growth on 'recruitment' to the fisheries (by being caught in the nets) will only be through flatfish size. Since emigration of some flatfish species, e.g.

.,"

25

Any discussion on the ultimate impact of variability in on recruitment strongly depends on the definition of recruitment itself. By definition, recruitment is the process whereby (flat)fish survive to attain sexual maturity and join the reproductive population (see also Heath, 1992; Gibson, 1994). The term 'recruitment' is (ab)used in several other senses, such as the number of individuals colonizing a nursery; or the surviving number of a cohort or year class which enters the fishery. The colonization of a nursery by juveniles is actually an immigration process instead of recruitment. In most time series, recruitment is considered the estimate of a cohort or year class which enters the fishery (see e.g. Rijnsdorp et al., 1991,1992). For this reason, the impact of variability in juvenile growth on recruitment will be discussed in the light of both 'recruitment to the fisheries' and 'recruitment to the reproductive population'.

......... growth

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petition for food by adults. In this way, the introduction of fishery will reduce the adult population and at low stock sizes also the recruitment, i.e. fishery may be able to remove density-dependent regulating (damping) processes. Other regulating mechanisms in the juvenile phase (by predation) and in the adult phase are discussed by Bailey (1994) and Rijnsdorp (1994), respectively.

/ .t ~

30

35

40

45

35.0 -

Mean length (cm) Fig. 17. Maturity proportions of female plaice, Pleuronectes platessa, in relation to ultimate length and to the back-calculated length at previous ages for individuals sampled at a. age III; b. age IV and c. age V. Data from Rijnsdorp (1993b). bility in recruitment. Variability in recruitment will be introduced by variability in t which is under the influence of density-independent processes such as water temperature and food quality and quantity. This means that with increasing population density there will be a shift from variability-generating factors towards damping factors. In unexploited populations, population regulation (damping) will occur at high densities by means of density-dependent processes, as for instance negatively density-dependent growth prolonging the juvenile stage. In species with an overlap in distribution of juveniles and adults, such as the yellowtait flounder Limanda ferruginea (Walsh, 1991), density-dependent processes might also operate by means of com-

0 32.5 -

30.0

-

27.5 -

¢: 25.0 19'60

19'65

19'70

19'75

19'80

19'85

19'90

Fig. 18. Mean length (cm) at which 50% of the females were mature in various years during the 1963-1988 period in two species of North Sea flatfish • = 4 year old plaice, Pleuronectes platessa; O = 3-year old sole, Solea solea. Data from Rijnsdorp et aL (1991).

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH

167

TABLE 4 Interannual variability as coefficient of variation (CV; %) in the age (Amat) and length (Lmat) at first maturity of male (m) and female (f) flatfish. Source: 1: Rijnsdorp et aL, 1991; 2: Beacham, 1983. species area time period CV% n source Age at first maturity (Area~ plaice f North Sea 1963-85 22.4 31 1 sole f North Sea 1966-85 9.3 23 1 witch flounder m Gulf of St. Lawrence 1975-81 15.4 6 2 f Gulf of St. Lawrence 1975-81 16.1 6 2 Length at first maturity (Lmat) plaice sole witch flounder

f f m f

North Sea North Sea Gulf of St. Lawrence Gulf of St. Lawrence

plaice from the nurseries towards the deep, is linked to total length (Heincke's law; Heincke, 1905), different scenarios can be made for the likelihood of a higher size-selective mortality with regard to possible temporal and spatial overlaps with fisheries that have flatfish as (by-)catch (Van Beek et aL, 1990). This implies that the assumption of a decreasing mortality rate with flatfish size (e.g. Cushing, 1974; Rothschild, 1986; Zijlstra et aL, 1982; Beverton & lies, 1992) is only correct for the pre-recruit period. As soon as juvenile flatfish migrate towards deeper water and/or become available to the fisheries, mortality rate will increase with size. The first analysis of the relationship between mean size of the population and year-class strength was done by Rauck & Zijlstra (1978) for plaice (Fig. 20). They observed an inverse relationship between mean length of the population and year-class strength at the end of the first year of life. Differences in the pattern of larval settlement between strong and weak years resulted in this relationship. Size-selective mortality appeared to be relatively unimportant: the mortality of smaller individuals was not high enough to completely reduce the strong year class to a normal one. Unfortunately, such data sets are not optimally suited for this type of analysis. Juvenile growth can also be back-calculated from otoliths of adult flatfish (Fig. 21). In both North Sea plaice and sole, there was no relationship between mean length of the 0-group population in autumn and subsequent year-class strength of the cohort. In plaice, a number of exceptionally strong year classes were observed of more than 10~individuals, but they corresponded with a variety of mean lengths of the population, from about 7 to 10 cm. In sole, one exceptionally strong year class was observed in 1963. However, the mean size of the 0-group soles at the end of the growing season was within the normal range of mean lengths observed. Size-selective mortality would have operated the other way round and would have resulted in a positive relationship between mean size and year-class strength.

1963-88 1966-85 1975-81 1975-81

3.6 3.8 4.5 4.6

23 23 6 6

1 1 2 2

Although according to Heincke's law (Heincke, 1905) there is an inverse relationship between flatfish size and depth, it is unknown whether variability in juvenile growth affects the timing of emigration of juveniles to deeper water. A more rapid growth would mean an earlier migration towards deeper water, where they would become available to the fisheries. A reduced (negatively density-dependent) growth would retard this migration. Such a mechanism would result in an inverse relationship between size and mortality, and hence generate variability in recruitment. In North Sea plaice this has not been observed. The variability in year-class strength remained similar during the juvenile period from 0-group until recruitment (Van der Veer, 1986). In this species, variability in growth does not seem to affect the variability in recruitment.

II

I

II

!

!

Fig. 19. Theoretical relationship between (S) year-class strength of flatfish at settlement and (t) duration of juvenile stage until maturity. See text for details.

168

H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP

!0-

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m

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I

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10

20

30

40

50

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•

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iability in plaice. With log-transformed data, however, recruitment variability increases. In sole, both transformed and untransformed data show an increase in the recruitment variability due to inter-annual variability in Amab This means that inter-annual variability in growth can affect the year-to-year variability in recruitment. The absolute level of recruitment will also be affected by variability in growth and hence in age of maturation. However, for both North Sea plaice and sole, the general patterns remained the same: Strong year classes showed a delayed growth and maturation, and hence a higher overall mortality until maturity. Nevertheless, strong year classes remained strong at recruitment to the reproductive population (Fig. 22), but due to a longer period of mortality the ultimate level was reduced. In the field also size-selective mortality will operate, and its effect should be added to that of size-dependent onset of maturation on recruitment. However, at present no quantitative information is available. From the theoretical point of view, the relationship between growth and duration of the juvenile stage will act as a damping factor, reducing the year-to-year variability in 1250"

a

7-

0

0

!

80

i

120

I000-

i

160

750-

Density (n. 1000m -e) Fig. 20. Relationship between the abundance and mean length of 0-group plaice in the Wadden Sea in autumn of various years a: in the German Wadden Sea in the years 1955 - 1973 (Rauck & Zijlstra, 1978); b: in the western part of the Dutch Wadden Sea in the years 1973 - 1979 (Zijlstra et al., 1982).

500• mmnlmm • ml

m

5

5.4. RECRUITMENT TO THE REPRODUCTIVE POPULATION As the onset of sexual maturation depends on growth rate, variations in growth will affect the duration of the juvenile stage and hence the period over which mortality processes operate. How the combination of size-selective mortality and size-dependent onset of maturation affects ultimate recruitment to the reproductive population can only be addressed in an indirect way. The time-series data of North Sea plaice and sole (Rijnsdorp et aL, 1991) were used to explore the effects of size-dependent onset of maturation. The numbers of recruits at the age of maturation (Amat) were calculated from the number of 1-year-old fish estimated by VPA (Virtual Population Analysis), assuming an average juvenile instantaneous mortality rate between age 1 and the onset of sexual maturity of M=0.1 and F=0.4 y-1 in plaice and sole. The untransformed data show that the growth-related variability in Areat results in a decrease in recruitment var-

m@

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7

8

9

10

11

12

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14

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b

4OO300.~

200•

lO0-

• •m

m m m

mm am

9

• •

•

1

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12

Mean length (nun) Fig. 21. Relationship between mean size (mm) at the end of the first growing season and recruitment (in million individuals, at age It) of a. North Sea plaice (Pleuronectes platessa) and b. sole (Solea solea). Data from Rijnsdorp et al. (1991) and Rijnsdorp & Van Leeuwen (1992).

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH recruitment. Note that these results may be biased since all data are from (heavily) exploited populations in which regulating (damping) mechanisms are probably removed. 5.5. GENERAL CONCLUSIONS In their study of age- and size-selective predation on larval fish, Litvak & Leggett (1992) argue that predation will be determined by the combined interacting probabilities of encounter, attack and capture. It is possible that the impact of size-selective mortality is masked by such simultaneously operating factors as variability in predator abundance, in temperature and in juvenile flatfish density. There are many hypotheses dealing with growth and survival. Recently, Anderson (1988) and Leggett & DeBIois (1994) summarized most of them for fish species in general. They conclude that the growthmortality hypothesis provides the best rational framework for future research. However, one may wonder whether this is also true for flatfish species. One of the underlying assumptions is that food availability is generally limiting for growth. One of the main characteristics of the life cycle of flatfish is that at least after settlement, food conditions are rather stable. Food limitation in the sense of starvation has not been observed so far, nor has negatively density-dependent growth in the 0-group. Available information on temperate flatfish species indicates that year-class strength is established already during the planktonic stages (Zijlstra et aL, 1982; Van der Veer, 1986; Van der Veer et aL, 1991), or in the early demersal stage (Rijnsdorp et aL, 1992). This implies that processes 250" 200" 150"

I00"

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Recruitment at age I ( * 10-6) Fig. 22. Relationship between year-class strength at age 1 (-10-6) and ultimate recruitment to the mature population (. 10- 6 ) in North Sea plaice, Pleuronectes platessa. Data from Rijnsdorp et aL (1991).

169

operating during the juvenile stages will mainly dampen variability in year-class strength and ultimate recruitment. This assumption is supported by the observation that during the period of size-selective predation in just-settled 0-group plaice in the intertidal, the between-year variability in year-class strength was reduced, despite simultaneously acting density-independent factors such as water temperature (Van der Veer, 1986). Further, Beverton & lies (1992) showed that in the 0- and I-group phase of plaice mortality showed a density-dependent component. Moreover, the two available long-term data sets on recruitment in temperate flatfish species, sole and plaice, also do not imply any relationship between growth and ultimate recruitment. If a growth-mortality relationship exists in flatfish, it only appears to dampen variability in recruitment. Any study on how variability in growth affects ultimate recruitment is hampered by the absence of basic ecological information on the range of distribution of flatfish. Especially data for subtropical and tropical waters are lacking. Furthermore, there are hardly any long-term data sets on year-class strength in flatfish during specific life stages and on ultimate recruitment. As long as such information is not available, any review should be considered preliminary. However, at present the growth/mortality hypothesis is not supported for flatfish. 5.6. FUTURE RESEARCH Hardly any progress has been made in the study of recruitment since the first hypotheses were formulated. The literature on recruitment is biased with an overwhelming amount of references dealing only with side issues or processes other than defined in this study: recruitment is the process whereby juvenile flatfish survive to attain sexual maturity and join the reproductive population. Except for the increase in growth of juvenile flatfish after the start of commercials exploitation, and the decrease in juvenile growth of a strong year class, our study provides hardly any support for negatively density-dependent growth in juvenile flatfish. This suggests that in most nurseries, juvenile flatfish are not food-limited and that the carrying capacity of the areas is never exceeded. Under such conditions, larval immigration will be the limiting factor, which is in accordance with the suggestion for 0-group plaice in the Wadden Sea (Bergman et al., 1989). Although in their study of recruitment in marine fishes, Wooster & Bailey (1989) argue that there will be no simple unifying hypothesis to explain recruitment variability in all species under all conditions, they also suggest that larval transport might be a key factor in some species, including flatfish. New and promising is the 'basin model' of densitydependent habitat selection as developed by MacCall (1990). This model offers a framework for the rela-

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H.W. VAN DER VEER, R. BERGHAHN & A.D. RIJNSDORP

tionship between habitat quality and quantity on the one hand and distribution, growth and survival on the other. In combination with the ecophysiological framework provided by Neill et aL (1994) and the information about the impact of habitat quality and quantity (Gibson, 1994), predation (Bailey, 1994) and latitude (Pauly, 1994), this might result in a new approach. However, a major problem is that most research concentrates on the process of recruitment without long-term data sets to validate the 'new' theories or hypotheses. As a consequence, the publication of new hypotheses and theories about recruitment is completely out of balance with the amount of effort put into monitoring recruitment of a (flat)fish species itself. The past has proved that new theories hardly contribute to solving the problem of recruitment. More energy should be put into establishing long-term data sets on recruitment, and especially in low latitudinal areas. Without this type of information, establishing new hypotheses seems to be rather a waste of time and energy. Acknowledgement.--Special thanks are due to Kevin M. Bailey, Robin N. Gibson and John M. Miller for their valuable suggestions on earlier drafts of the manuscript. 6. REFERENCES Anderson, J., 1988. A review of size dependent survival during pre-recruit stages in relation to recruitment.~. Northw. Atl. Fish. Sci. 8: 55-66. Bailey, K.M., 1994. Predation on juvenile flatfish and recruitment variability.--Neth. J. Sea Res. 32: 175-189. Bagge, O. & E. Nielsen, 1989. Changes in abundance and growth of plaice and dab in Subdivision 22 in 19621985.--Rapp. P.-v. R~un. Cons. perm. int. Explor. Mer 190: 183-192. Barr, W.A., 1963. The endocrine control of the sexual cycle in the plaice (Pleuronectes platessa L.). I. Cyclical changes in the normal o v a r y . ~ e n . Comp. Endoc. 3: 197-204. Beacham, T.D., 1983. Variability in size and age at sexual maturity of witch flounder Glyptocephalus cynoglossus, in the Canadian maritime region of the northwest Atlantic Ocean.--Can. Field-Nat. 97: 409-422. Berghahn, R., 1987. Effects of tidal migration on growth of 0group plaice (Pleuronectes platessa L.) in the North Frisian Wadden Sea.--Meeresforsch. 31: 209-226. Bergman, M.J.N., H.W. van der Veer & J.J. Zijlstra, 1988. Plaice nurseries: effects on recruitment.--J. Fish. Biol. 3,3 (Suppl. A): 201-218. Bergman, M.J,N., H.W. Van der Veer, A. Stam & D. Zuidema, 1989. Transport mechanisms of larval plaice (Pleuronectes platessa L.) from the coastal zone into the Wadden Sea nursery area.--Rapp. P.-v. R~un. Cons. perm. int. Explor. Mer 191: 43-49. Berner, M., G. Sager & R. Sammler, 1989. Untersuchungen zu L&ngen- und Massewachstum, Zuwachs und L&ngen/Masse-Relation der Flunder (Platichthys flesus L.) des Breeger und Breetzer Boddens.--Fischerei-Forschung 27: 44-50. Beverton, R.J.H. & S.J. Holt, 1957. On the dynamics of exploited populations.--Fishery Invest. (Ser. 2) 19: 1-

533. Beverton, R.J.H. & T.C. lies, 1992. Mortality rates of 0-group plaice (Pleuronectes platessa L.), dab (Limanda limanda L.) and turbot (Scophthalmus maximus L.) in European waters III. Density-dependence of mortality rates of 0-group plaice and some demographic implications.--Neth. J. Sea Res. 29: 61-79. Beyer, J.E., 1989. Recruitment stability and survival-simple size-specific theory with examples from the early life dynamics of marine fish.--Dana 7: 45-147. Boje, J. & O.A. Jergensen, t991. Growth of Greenland halibut in the northwest Atlantic. ICES C.M. 1991/G:40:1-7 (mimeo). Borley, J.O., 1909. A comparison of the condition of the plaice of different regions as to weight.--Intern. Invest. Mar. biol. Ass. Report II1:81-105. Borley, J.O., 1923. The plaice fishery and the war.--Fishery Invest. (Ser. 2) 5 (3): 1-56. Bowering, W.R., 1987. Distribution of witch flounder (Glyptocephalus cynoglossus) in the southern Labrador and eastern New Foundland area and changes in certain biological parameters after 20 years of exploitation.Fish. Bull. U.S. 85:611-629. , 1989. Witch flounder distribution off southern Newfoundland, and changes in age, growth, and sexual maturity patterns with commercial exploitation.--Trans. Am. Fish. Soc. 118: 659-669. B[~ckmann, A., 1934. Untersuchungen eber die Naturgeschichte der Seezunge, die SeezungenbevSlkung und den Seezungenfang in der Nordsee.--Ber. dt. Kommn. Meeresforsch. 7 (2]; 1-66. - - , 1944. Die SchotfenbevSIkerung der Helgot&nder Bucht und die Einschr~nkung der Fischerei w&hrend der Kriegsjahre 1914-18 und 1939-1942.--Rapp. P.-v. R~un. Cons. perm. int. Explor. Mer 114:1-114. Burton, M.P. & D.R. Idler, 1984. The reproductive cycle in winter flounder Pseudopleuronectes americanus (Walbaum).---Can. J. ZooL 62: 2563-2567. Carruthers, J.N., 1924. Report on the English post-war plaice marking and transplantation experiments.-Fishery Invest. (Ser. 2) 6: 1-22. Conover, D.O., 1992. Seasonality and the scheduling of life history at different latitudes.---J. Fish Biol. 41: 161-178. Creutzberg, F., A.Th.G.W. Ettink & G.J. Van Noort, 1978. The migration of plaice larvae Pleuronectes platessa into the western Wadden Sea. In: DiS. McLusky & A.J. Berry. Physiology and behaviour of marine organisms. Proc. 12th EMBS, Pergamon Press, New York: 243251. Cushing, D.H., 1974. The possible density-dependance of larval mortality and adult mortality in fishes. In: J.H.S. Blaxter. The early life history of fish. Springer-Verlag, Berlin: 103-112. Dapper, R., 1979. De aantallen van I- en II-groep schol op het Balgzand in de jaren 1975, 1976, 1977, 1978. Interne Verslagen Nederlands Instituut voor Onderzoek der Zee, Texel, 1979-12: 1-93. D'aykov, Y., 1977. The growth rate of Pacific halibut from the western Kamchatka shelf.--Biol. Morya 1977 (3) (in Russian): 80-82. Deniel, C., 1981. Les poissons plats (Teleosteens, Pleuronectiformes) en Bale de Douarnenez. Ph.D. thesis, Universit~ de Bretagne Occidentale: 1-481. - - , 1990. Comparative study of growth of flatfishes on the west coast of Brittany.--J. Fish Biol. 37:149-166.

IMPACT OF JUVENILE GROWTH ON RECRUITMENT IN FLATFISH

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