A comparative analysis of recruitment variability in North Atlantic flatfishes — testing the species range hypothesis

In Collaboration with the Netherlands Institute for Sea Research

ELSEVIER

Journal of Sea Research

37 ( 1997) 28 l-299

A comparative analysis of recruitment variability in North Atlantic flatfishes - testing the species range hypothesis William C. Leggett a,*, Kenneth T. Frank b a OfJice of the Principal and Department of Biology, Queen’s University, Kingston, ON K7L 3N6, Canada b Department of Fisheries and Oceans, Marine Fish Division, l?O. Box 1006, Dartmouth, NS B2Y 4A2, Canada Received

15 January

1997; accepted

22 April 1997

Abstract The hypothesis that recruitment variation in flatfishes should be most variable at the northern edge of the species range, least near the centre of the range, and intermediate near the southern limit was tested using stock and recruitment data generated from sequential population analysis for several different flatfish stocks involving four species (plaice Pleuronectes platessa, sole Solea vulgaris from the eastern Atlantic, American plaice Hippoglossoides platessoides, and yellowtail flounder Limandaferruginae from the western Atlantic). Several groundfish species have been found to conform to this so-called species range hypothesis with the suggestion that density-independent processes predominate at the edges of the distributional range and density-dependent processes dominate in the centre of the range. Our results were generally inconsistent with the hypothesis: the coefficient of variation (CV) of recruitment for plaice in the eastern Atlantic was independent of latitude, the CV of recruitment for sole exhibited a dome-shaped relationship with latitude with the highest CVs occurring at the mid-point of the range, and the CV of recruitment for the western Atlantic stocks exhibited a monotonic decrease with latitude. We extended our latitudinal analyses by assessing both the degree of dependency of recruitment on spawning stock biomass and the spatial and temporal scales of variability in recruitment and pre-recruit survival for the eastern Atlantic stocks. In general our analysis revealed no evidence of a strong stock and recruitment relationship for any of the stocks examined, and previously published analyses revealed no such patterns with latitude. Analysis of both de-trended recruitment and pre-recruit survival time series over the species ranges of sole and plaice revealed strong positive correlations among adjacent stocks and inverse correlations among stocks at the extremes of the range. Recruitment variation in the flatfish stocks examined appears to be dominated by density-independent factors, operating at a local scale, on the egg and larval stages. Keywords: recruitment;

latitudinal

variation; pre-recruit survival; density independence/dependence;

flatfishes; North

Atlantic

1. Introduction Miller et al. (1991) hypothesised that recruitment variation in flatfishes should vary with latitude in * Corresponding author: E-mail: [email protected] 1385-I 101/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved. PII S1385-1101(97)00023-3

response to differences in the relative importance of biotic and abiotic regulators. More specifically, they predicted that recruitment would be most variable at the northern edge of the species range, least near the centre of the range, and intermediate near the southem limit (i.e. a skewed, convex pattern of recruitment

WC. Leggett, K.T. Frank/Journal

282

Middle

South

North

b)

of Sea Research 37 (1997) 281-299

The hypotheses advanced by Miller et al. (op tit) deserve careful evaluation because, if correct, they could provide valuable insight into those species and locations having the greatest potential for rigorous . tests of hypotheses related to controls on recruitment in the flatfishes generally. At the time Miller et al. (1991) published their work, they acknowledged that the data required to test their hypotheses were inadequate. Since that time Myers et al. (1995a) have compiled and published an extensive body of stock and recruitment time series for flatfishes and other species worldwide. We used these data to contrast the patterns of recruitment variation in flatfishes with those prevailing in non-flatfish species, to evaluate elements of the hypotheses proposed by Miller et al. (op. cit.), and to examine the spatial and temporal scales of covariation in recruitment time series for selected flatfish species. 2. Materials and methods

South Fig. 1. Schematic

Middle representation

North

of the species range hypothesis.

variation should prevail; see Fig. la). This hypothesis is generally consistent with that of McCall (1990). Both hypothesised that at the edges of the distributional range density-independent (abiotic environmental) processes should predominate, whereas near the centre of the range density-dependent processes would dominate (Fig. lb). Miller et al. (op. cit.) based their predictions on analyses of patterns in life histories within the flatfishes, and on general observations on the latitudinal variability in biotic factors, specifically food and predation, which are likely to act more as regulators than as controls of recruitment because of their density-dependent characteristics. Bijnsdorp et al. (1992) working with sole (Solea solea) and Myers (1991), working with cod (Gadus morhua), haddock (Melanogrammus aeglejinus) and herring (Clupea harengus), reported patterns of recruitment variation that are generally consistent with these predictions (Fig. 2, adapted from Myers, 1991).

The estimate of recruitment variability used in our analysis was the coefficient of variation, defined as the standard deviation of the population numbers at age expressed as a percentage of mean. Frequency distributions of the coefficient of variation (CV) of recruitment were constructed for three species groups: flatfish, groundfish (cod and haddock), and pelagics (herring). The data were obtained from statistical summaries computed by Myers et al. (1995a) for 28 stocks of flatfish mainly from the North Atlantic but with some Pacific stocks included, for 35 stocks of cod mainly from the Atlantic but with a few Pacific stocks, and for 41 herring stocks mainly from the Atlantic but with some Pacific stocks included. An alternative estimate of recruitment variability, the standard deviation of the logarithmically transformed (base 10) numbers at age, was also used in our analysis. The results were similar in all cases so we report only the analysis involving the CVs. Estimates of flatfish recruitment and spawning stock biomass were obtained from sequential population analyses (SPA) compiled by Myers et al. (1995a) in his summary of worldwide spawner and recruitment data. Time series of data were available for eight stocks of plaice Pleuronectesplatessa from the eastern Atlantic spanning almost 10“ of latitude

283

WC. Leggett, K.T Frank/Journal of Sea Research 37 (1997) 281-299

s

1Cod, eastern Atlantic]

1

0.6

t

0.6 0.4 0

a

00

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.a

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40

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65

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66

66

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0 40

70

41

42

43

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46

46

IHerrIng, westamAttantk] 0.6

0.6

Fig. 2. The standard deviation of detrended log-transformed recruitment time series vs the latitude herring stocks in the eastern and western Atlantic. Figure adapted from Myers (1991).

(49.5 to 58”N). For sole Solea vulgaris seven stocks from the eastern Atlantic were included in the analysis ranging from 46 to 58”N. In the western Atlantic,

of spawning

for cod, haddock

and

data were available for three stocks of American plaice Hippoglossoides platessoides (range of latitude: 41 to 48”N) and three stocks of yellowtail

284

WC. Leggett, K.Z Frank/Journal

flounder Limanda ferruginae (range of latitude: 40 to 46”N). The data sources, age at recruitment and other pertinent information for each stock are given in Appendix A. Because SPA estimates of recruitment have potential fishery-dependent biases they are not the ideal source of data. Pre-recruit surveys, if they were readily available for all of the stocks under investigation, could provide an alternative data source for future investigations of spatial correlations in recruitment. An index of pre-recruit survival was calculated as the ratio of recruits divided by the spawning stock biomass (SSB) in a manner similar to that of Sinclair et al. (1985) and Sinclair (1994). As suggested by Sinclair (1994) the index includes both density-dependent and density-independent sources of mortality as well as any associated measurement error. Because there are no strong relationships between stock and recruitment for any of the flatfish stocks examined (see Section 3), the index primarily represents variations in extrinsic effects on year-class size. While SSB is not the best proxy for the reproductive output of the spawning stock in a given year, it is the most widely available and only a few stocks have more exact measures of annual egg production. Trends in the recruitment data and survival index were compared using correlation analysis. Such time series tend to be autocorrelated and we followed the recommendation of Cohen et al. (1991) to de-trend such data using the technique of first differencing. First differencing results in the creation of a new series by taking the difference between successive points. Prior to differencing, a natural logarithmic transformation was used to stabilise the variance. Correlations were performed using the longest common time period for each pair of stocks. The recruitment series are from 12 to 35 years for plaice, 7 to 37 years for sole, 12 to 26 years for American plaice, and 19 to 21 years for yellowtail flounder. No adjustments to the degrees of freedom were made for possible autocorrelation and in so doing, the number of statistically significant correlations would be maximised favouring large-scale effects (Cohen et al., 1991).

of Sea Reseamh 37 (1997) 28I-299

3. Results 3.1. Recruitment variation injlatjbh, cod and herring

We examined data for 28 flatfish stocks, 35 cod and haddock stocks and 41 herring stocks (Fig. 3). These indicate the CVs of recruitment to be greatest in the herring, intermediate in groundfish (cod and haddock) and lowest in the flatfishes. This finding is consistent with that of Bailey (1994). 3.2. Latitudinal variation in recruitment inJEa@sh To evaluate the Miller et al. (1991) hypothesis that recruitment variability should show a skewed, concave relationship to latitude of spawning with highest variance in the north, lowest at intermediate latitudes, and intermediate variance in the south, we examined the CV of recruitment in yellowtail flounder, American plaice, sole and European plaice. The CV of recruitment for yellowtail flounder and American plaice from the western Atlantic varied inversely with latitude of spawning. American plaice exhibited a lower overall CV of recruitment at all latitudes (Fig. 4). The CV of recruitment for sole in the eastern Atlantic exhibited a domed-shaped relationship with latitude with the highest CVs occurring at the midpoint of the range (Fig. 5). The data point at latitude 58”N is based on a restricted time series (7 years). If excluded the series suggested an increase in the CV of recruitment with latitude. This conforms to the pattern reported by Rijnsdorp et al. (1992). An analysis of the relationship between the CV of recruitment and time series length revealed no significant pattern (series length 7-37 years, r = 0.58, p > 0.05). Therefore, we have no reason to delete any of the data and conclude that the relationship is domed. The CV of recruitment for plaice in the eastern Atlantic was independent of latitude (Fig. 6). The patterns of the CV of recruitment in these species in relation to latitude, whether individually or collectively, do not conform to the expectations of the Miller et al. (1991) hypothesis nor do they follow the convex relationship reported for cod, haddock and herring by Myers (1991).

NC. Leggett, K.‘I: Frank/Journal

285

of Sea Research 37 (1997) 281-299

/NW Atlantic Flatfish 1

?? mmpl

o-9

ax?9

40-49

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8088

LNbdZ-

10&199120.12914&149

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a

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50

Fig. 4. CV of recruitment for northwest Atlantic stocks of yellowtail flounder (Yt 11) and American plaice (Am pl) vs latitude of spawning.

CV of Recruitment [Gadbrmas (cd andhad&& only) 1 0.4

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t

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04

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a.99

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CV of Recruitment

45

Fig. 5. CV of recruitment for northeast Atlantic stocks of sole vs latitude of spawning. Data labels refer to ICES stock management unit (see Appendix A for details).

~Clupeiformas(herring only) 1 0.4 --

8

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“1

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40.49

w.99

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1oQ109120.12914&149

CV of Recruitment

20

Fig. 3. Frequency distributions of the coefficient of variation (CV) for 28 flatfish stocks, 35 cod and haddock stocks, and 41 herring stocks primarily from the North Atlantic but with some Pacific stocks included. Data obtained from statistical summaries computed by Myers et al. (1995a).

3.3. Stock and recruitment We sought evidence sity of density-dependent

relationships

75” 8

1

,L., 45

L 1:

.--_

liilUdDd_

___

55

A 60

Fig. 6. CV of recruitment for northeast Atlantic stocks of plaice vs latitude of spawning. Data labels refer to ICES stock management unit (see Appendix A for details).

injlatjishes

for variation in the intenregulation of recruitment

with latitude of spawning through an analysis of the relationship between spawning stock biomass and recruitment in sole and European plaice for which

286

WC. Leggett, K.T. Frank/Journal

of Sea Research 37 (1997) 281-299

Sole llla

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WC. Leggett, K.7: Frank/Journal

the number of stocks was greatest. The Miller et al. (1991) hypothesis generates the prediction that density dependence should be strongest near the midpoint of the ranges for these species, and should decline toward the limits of the ranges as density-independent regulation intensifies. Visual inspection of the scatter plots of spawning stock biomass and recruitment for these species (Figs. 7 and 8) revealed no evidence of a latitudinal variation in this relationship. Indeed there was no evidence of a strong stock recruitment relationship for any of the stocks examined. This finding is consistent with that of Myers and Barrowman (1996), who reported that the Pleuronectidae and the Solidae showed the weakest relationship between recruitment and spawner abundance of nine fish families investigated. Iles (1994) reported evidence of weak stock dependence in five of twelve North Sea and west English Channel (ICES VIIe) stocks of plaice and sole. His data, too, revealed no pattern with latitude (Fig. 9). Myers and Barrowman (1996) note that the weak relationship between spawning stock biomass and recruitment evident in the Pleuronectidae and Solidae could result from strong density-dependent juvenile mortality in this group (see also Myers and Cadigan, 1993; Iles, 1994). We conclude that the evidence available from spawning stock biomass-recruitment analyses does not support the hypothesis of a consistent latitudinal pattern in the intensity of densitydependent regulation of recruitment in these species. We note, however, that other approaches to the investigation of density-dependent processes do exist (see Myers and Cadigan, 1993). In addition, if we assume that recruitment is dependent on spawning stock biomass at all latitudes, then the relationship would be obscured at the extremes of the species range due to environmental effects and not so at intermediate latitudes. This pattern did not appear in data. 3.4. Spatial scale of recruitment variation

of Sea Research 37 (1997) 281-299

287

dynamics of the flatfish stocks we investigated. In the absence of environmental data against which to evaluate this hypothesis directly, we chose to examine the spatial scales of correlations in the recruitment time series. This analysis was based on the assumption that broad-scale similarities in the recruitment time series would suggest forcing at large spatial scales, presumably in response to atmospheric forcing, whereas correlations on a more local scale would suggest that smaller-scale processes (upwelling, wind, onset of stratification, etc.) predominate. 3.4.1. European plaice Recruitment time series for the stocks investigated, segregated into three geographic areas (north, middle, south. of range), are given in Fig. 10. Nine statistically significant correlations (out of 28 stock pairings) occurred in the differenced recruitment time series. Positive correlations occurred among three stocks at the northern end of the range (latitude 57-58”N) and four stocks ranging in latitude from 49.5 to 53”N (southern to mid-point of species range). Significant negative correlations occurred between stocks at the extremes of the range (i.e. Celtic Sea vs ICES IIIa and Kattegat; Table 1). Pre-recruit survival time series (differenced In WSSB), again segregated into north, middle and southern components of range, are provided in Fig. 11. Eight of twenty-eight pairings were significantly correlated. As with the recruitment time series, positive correlations were clustered (three stocks at latitude 57-58”N and five at 49.5-53.5”N). Again negative correlations occurred between stocks at the extremes of the range (ICES VIIe and Kattegat; Table 2). In both series the remaining correlations, while non-significant, were predominately negative in sign between stocks in the northern areas and those located in the middle and southern regions (Tables 1 and 2).

Our analyses suggest that non-density-dependent factors predominate in regulating the recruitment

Fig. 7. Scatter plots of recruitment and spawning stock biomass for sole stocks in the northeast Atlantic. Stocks are arranged in descending order from those occurring at the northern extreme of the species range (ICES IIIa at 58”N) to the southern extreme (ICES VIII at 46”N). Stock management unit and length of each time series is also provided.

WC. Leggett, K.7: Frank/Journal

288

of Sea Research 37 (1997) 281-299

Plaice North Sea

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of Sea Research 37 (1997) 281-299

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Fig. 9. Stock and recruitment plots for sole and plaice stocks examined by Iles (1994) arranged by latitude of spawning. Relationships differing from either constant recruitment or a proportional line are shown together with 95% confidence intervals.

Fig. 8. Scatter plots of recruitment and spawning stock biomass for plaice stocks in the northeast Atlantic. Stocks are arranged in descending order from those occurring at the northern extreme of the species range (ICES IIIa at 58”N) to the southern extreme (ICES VIIe at 49S”N). Stock management unit and length of each time series is also provided.

WC. Leggett, K.?: Frank/Journal

290 +

Kattegat(57N)

+

lrish(53.5 N)

+

Vlld(50 N)

of Sea Research 37 (1997) 281-299 + Kattegat(57N) ---0.. Skaggerak(56 N) -A Ma (56 N)

+_

P North(53N) 1.51 -.- A

1.5,

Irish (53.5N) --a_North(53N)

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-1.5’ I I I I I II I 1960

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1965

1970

I

1975

7 8 8 11 r r 9 I a 8 8 8 II 8 1960

1965

1990

Fig. 10. Recruitment time series for plaice. Stocks were separated into three geographic areas (north, middle, south of range) based on latitude of spawning.

3.4.2. Sole Recruitment time series for seven sole stocks (range of latitude 46-58”N) are given in Fig. 12. Five of twenty-one pairings showed significant correlations. Four stocks ranging in latitude from 49.5 to 53S”N were positively correlated. These were negatively correlated with the Bay of Biscay stock (ICES VIII, latitude 46“N). There was no correlation between either of these and the northernmost stock (ICES IIIa), perhaps due to the shorter time series (n = 6) of the latter (Table 3). Pre-recruit survival time series for these stocks are given in Fig. 13. Of 21 pairings assessed, 5 significant correlations, all positive, occurred. These were clustered in the intermediate portion of the range (latitude 49.5-53.5”N). No correlations occurred between these stocks and the stocks located

A 1965

1990

Fig. 11. Pre-recruit survival index for plaice. Stocks were separated into three geographic areas (north, middle, south of range) based on latitude of spawning.

in the northern and southern portions of the range (Table 4). In both time series the remaining correlations, while non-significant, were predominately positive. Negative non-significant correlations in the prerecruit series occurred exclusively between the Bay of Biscay (ICES VIII) stock and the others tested (Tables 3 and 4). For both species positive correlations occurred primarily among stocks that were closely associated geographically (i.e. northern, mid-range, southern). Negative correlations occurred exclusively between mid-range and northern or southern stocks. These findings suggest that factors influencing recruitment and pre-recruit survival in these species/stocks operate at local rather than large scales. This finding is consistent with those of Hollowed et al. (1987) for 28 species from 5 regions in the NE Pacific, and Cohen et al. (1991) for cod and haddock in the NW Atlantic.

WC. Lqgett, K.7: Frank/Jound Table 1 Correlation Atlantic

coefficients

Latitude

Stock

58

IIIa

(r), probability

SK

51

KA

53.5

IS

53

NS

51

cs

50

VIId

49.5

We

291

levels (p). and sample sizes (n) for plaice (Pleumnectes Plafessa) recruitment

in the northeast

Stock IIIa

58

of Sea Research 37 (1997) 281-299

r

1.ooo

P n r P n r P n r P n

13 0.93825 0.0001 II 0.87276 0.0001 13 -0.00859 0.9778 13

r P n r P n r P n r P n

0.19990 0.5126 13 -0.54972 0.0516 13 -0.09608 0.7918 10 -0.34225 0.2523 13

For data sources see Appendix

SK

KA

IS

NS

cs

VIId

We

1.000

I1 0.80703 0.0027 11 -0.0507 0.8823 11 0.10051 0.7687 11 -0.45109 0.1637 11 -0.14949 0.7239 8 0.255 11 0.4490 11

1.000 22 -0.27808 -0.2102 22 -0.25847 0.2455 22 -0.60823 0.0274 13 -0.44918 0.2136 10 -0.44918 0.1071 14

l.ooO 28 0.5 1269 0.0053 28 0.50036 0.0684 14 0.54762 0.0812 II 0.70520 0.0033 15

1.000 34 0.02042 0.9447 14 0.89204 0.0002 11 0.41634 0.1227 15

1.000 14 0.20416 0.547 1 11 -0.34225 -0.2523 13

l.OGO II 0.76423 0.0062 11

1.000 15

A.

3.5. Between species correlations within areas Sole and plaice co-occur in several management units. These species spawn at different times. We assessed correlations between the time series of recruitment and pre-recruit survival for the two species where they co-occur in an effort to gain insight into the temporal scale of factors influencing recruitment. Our operating assumption was that positive correlations would be indicative of factors operating at longer temporal scales (> sum of spawning times for the two species) whereas negative and non-significant correlations would suggest forces operating at shorter scales (i.e. at the scale of spawning times of the individual species). Plaice and sole co-occurred in six management units. The differenced recruitment series was significantly correlated in only one of these regions (North Sea, n = 34, r = 0.455, p < 0.05). The differenced survival index was insignificant in all cases.

For these species, we conclude that factors influencing recruitment variation within regions operate principally at time scales approximating the duration of spawning. 4. Discussion and conclusions Flatfishes exhibit significant year to year variation in recruitment as is characteristic of all marine fishes. When contrasted with gadoids and herring, however, recruitment variation in the flatfishes is modest. Recruitment variation is generally assumed to result from the combination of spawning stock effects and stochastic abiotic and biotic processes which influence the survival of early life stages. Density-dependent processes, operating at the population or stock level, and throughout the pre-recruit phase of the life cycle, are generally believed to moderate the intensity of the overall variation in recruitment. Our analyses suggest that recruitment variation in

292

WC. Leggett, K.Z Frank/Journal

Table 2 Correlation coefficients northeast Atlantic Latitude

(r), probability

Stock

58

57

53.5

53

51

50

49.5

sizes (n) for plaice (Pleumnectes platessa) pre-recruit

survival

in the

Stock IIIa

58

levels (p), and sample

of Sea Research 37 (1997) 281-299

IIIa

r

SK

P n r

KA

P n r

IS

P n r

NS

P n r

cs

P n r

VIId

P n r

VIIe

P n r P n

For data sources see Appendix

SK

KA

IS

NS

cs

VIId

VIIe

1.ooo 11 0.93687 0.0002 9 0.9002 1 0.0002 11 -0.09478 0.7816 11 0.12727 0.7092 11 -0.40277 0.2194 11 -0.13207 0.7348 9 -0.5 1653 0.1038 11

1.000 9 0.86265 0.0028 9 0.01937 0.9606 9 0.04876 0.9009 9 -0.3255 0.3926 9 -0.28694 0.5327 7 0.31475 0.4094 9

1.ooo 21 -0.19553 0.3957 21 -0.19796 0.3897 21 -0.52291 0.0811 12 -0.32150 0.3989 9 -0.68321 0.0100 13

1BOO 27 0.29889 0.1299 27 0.5445 1 0.0544 13 0.37877 0.2804 10 0.66078 0.0101 14

1.000 34 0.05532 0.8576 13 0.82221 0.0035 10 0.41861 0.1363 14

1.000 13 0.02204 0.9518 10 0.61956 0.0239 13

1.000 10 0.53042 0.1147 10

1.000 14

A.

the flatfishes is dominated by density-independent factors operating on the egg and larval stages. This conclusion is based on the finding that the stocks investigated showed little or no evidence of spawning stock (stock-recruitment) effects, and is consistent with that of Beverton and Iles (1992), Myers and Cadigan (1993), Iles (1994) and Myers and Barrowman (1996). Our analyses also indicate that the density-independent regulation of pre-recruit survival in plaice and sole operates principally at the local (stock) scale rather than at large geographic scales. This conclusion is based on the fact that positive, between-stock correlations in the recruitment time series occurred only among neighbouring stocks (i.e. those in close geographic proximity to one another). Our results are consistent with those of Myers et al. (1996) who demonstrated that the spatial scale of interannual recruitment variation for marine species is typically

500 km. These authors suggested wind or sea surface temperature as influential forcing factors of coherent recruitment fluctuations because only these variables exhibited correlations at similar spatial scales. However, care should be taken in assessing the biological meaning of the positive correlations observed at local scales (e.g. Skagerrak, ICES IIIa, Kattegat for plaice: ICES VIIIa,b,c,d for sole). Such correlations could result from movement of pre-recruits among and between stocks either as a consequence of egg and larval drift, or in response to density effects at the local stock level. Inter-stock exchange has in fact been demonstrated for some groundfish stocks in the North Atlantic including haddock stocks on the Scotian Shelf and the Iceland/West Greenland/Labrador Shelf cod stocks (Frank, 1992; Dickson and Brander, 1993). This caveat does not impact on our overall conclusion, however, because correlations between more distant stocks, where pre-recruit mixing is un-

WC. Leggett, K.Z Frank/Journal 3_

-e-

of Sea Research 37 (1997) 281-299

llla (58 N)

31

+

293

llla(56 N)

2B = I 2 5

lo-1-2

II~JI.II,II~I,I~I.,.III,.,I,,,III,II 1960 1965 1970 1975 1980 +

1965

PI,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,,, 1965 1970 1975 1960

1990

North(53.5N) 31

+,_ Celtic (51 N) -0 Vlld(50N) -A-.Vlle(49.5N)

3-

2g T ; f

1965

1990

+ North(53.5N) ..A.. Irish (;3.5N)

J'.,,,,...,,,,.,.,,,,..,,,,,,,,,,,.. 1965 1970 1975 1960

3_

1960

1960

1965

1990

+ Cekic(51 N) e--Vlld(50N) -*- 'Ale(49.5N)

P2 0 I lt

lo-

w ?

-i-

o-

f-l-z',..,,...,,...,....,....,....,..,.,., 1960 1965 1970 1975 1960 3-

+

1965

1990

VIII(46 N)

31

2e n B 4 C

+

Vlll(46N)

lo-1-2

,,,,,,,,,,,,,,,,,,,,,,,,,'-Tyl-lrrl 1960 1965 1970 1975 1960

Fig. 12. Recruitment into four geographic

1965

1990

time series for sole. Stocks were separated areas based on latitude of spawning.

likely to occur, were either non-significant or negative, as was the case in several widely separated stocks. It should also be noted that we did not adjust the statistical significance levels for multiple comparisons. If we had done so, e.g. by using the Bonferroni approach where the probability level is divided by the number of comparisons, the p level for plaice would have been 0.05/28 or 0.0018 and for sole 0.05/21 or 0.0024. Using this criterion the number of significant correlations drop: three for plaice recruitment, two for plaice pre-recruit survival, one

_Z',,,,~,,,,,,,,,,,,,~,,,,,,,,,,,,,,,, 1965 1970 1975 1960

1960

1965

1990

Fig. 13. Pre-recruit survival index for plaice. Stocks were separated into four geographic areas based on latitude of spawning.

for sole recruitment and none for sole pre-recruit survival. In light of our pre-conditioning of each of the original time series to remove autocorrelation (1st differencing) further statistical adjustments were considered overly stringent. In fact, adjustment for multiple comparisons in recruitment synchrony studies is uncommon (see e.g. Hollowed et al., 1987; Cohen et al., 1991; Rijnsdorp et al., 1992; Sinclair, 1994; Myers et al., 1995b). Our analyses also indicate that pre-recruit survival in plaice and sole occurs on temporal scales equivalent to the approximate duration of the species/stock

294

WC. Leggett, K.7: Frank/Journal

of Sea Research 37 (1997) 281-299

Table 3 Correlation coefficients (r), probability levels (p), and sample sizes (n) for sole (Solea solea) recruitment in the northeast Atlantic Latitude

Stock

Stock IIIa

58

IIIa

53.5

IS

53.5

NS

51

cs

50

VIId

49.5

VIIe

46

VIII

IS

NS

VIId

cs

VIIe

VIII

1.oo 6

0.19408 0.7125 6 0.25558 0.625 6 -0.6088 0.1996 6 0.53326 0.2759 6 0.5329 0.2763 6 -0.07 135 0.8932 6

1.00 22 0.27537 0.2148 22 0.312 0.1935 19 0.10716 0.6529 20 0.24867 0.2645 22 0.30078 0.3688 11

1.00 36 0.08314 0.7351 19 0.75065 0.0001 20 0.49351 0.0196 22 -0.52823 0.0775 12

1.00 19 -0.05583 0.8204 19 0.47301 0.0408 19 -0.37887 0.2803 10

1.00 20 0.63746 0.0025 20 0.59462 0.0537 11

1.00 22 0.41088 0.2094 11

I .oo 12

For data sources see Appendix A. spawning interval. This conclusion is based on the absence of correlations in the recruitment time series for plaice and sole within the same management unit. This finding supports our conclusion (see above) that the primary forces inducing inter-annual variability in recruitment in these species are operating at the egg and early larval stages. Were the temporal duration of these effects longer, and therefore influential on survival in later larval and early juvenile stages, we would expect to observe correlations in recruitment series for the two species in spite of the temporal separation in their spawning times.

The results of our investigations into the pattern and intensity of latitudinally (species range) based correlations in recruitment time series lead us to reject the Miller et al. (1991) hypothesis. Recruitment variation in the flatfishes we investigated, which included both eastern and western Atlantic species, did not exhibit a consistent pattern as proposed by the hypothesis. Philippart et al. (1997) report a similar result. Strong latitudinal patterns were evident in the recruitment variability of American plaice, yellowtail flounder and sole, but in all cases these patterns

were inconsistent range hypothesis

with the predictions of the species (Miller et al., 1991). Moreover, the

patterns of variability in recruitment of American plaice and yellowtail flounder were distinct from that exhibited by sole. An important assumption underlying the evaluation of the species range hypothesis is that the data set covers the whole range of distribution of the various species. This does in fact appear to be true for most of the species we examined with the possible exception of plaice in the eastern Atlantic. The northern limit of distribution of plaice extends to the Barents Sea; however, data from Myers et al. (1995a) were available only to latitude 58”N (ICES Statistical area IIIa). While this stock does not appear to support a commercial fishery, trawl surveys conducted from 1972 to 1989 give some indication of its recruitment variability - the CV of recruitment was 75% (based on abundance at age 4; see data contained in table 2 of Kovtsova and Boitsov, 1995). This value is lower than the CV obtained for the plaice stock in the Kattegat (latitude of spawning 57”N) and the CV is likely to be inflated given that

WC. L.eggett, K.T. Frank/Journal Table 4 Correlation Atlantic

coefficients

Latitude

Stock

58

IIIa

(r). probability

levels (p).

IS

53.5

NS

51

cs

50

VIId

49.5

VIIe

46

VIII

sizes (n) for sole (Solea solea) pre-recruit

295

survival

in the northeast

Stock IIIa

53.5

and sample

of Sea Research 37 (1997) 281-299

r

1.00

P n r P n r P n r P n r P n r P n r P n

4 0.36558 0.6344 4 0.296 0.704 4 -0.28005 0.72 4 0.669 0.331 4 0.31521 0.6848 4 -0.07944 0.9206 4

For data sources see Appendix

IS

NS

cs

VIId

VIIe

VIII

1.00 20 0.1033 0.6646 20 0.57088 0.0167 17 0.0457 0.8523 19 0.17619 0.4575 20 0.21738 0.5208 11

1.00 35 0.12596 0.630 17 0.60252 0.0063 19 0.49084 0.0239 21 -0.55367 0.0618 12

1.00 17 0.00152 0.9954 17 0.51712 0.0335 17 -0.03049 0.9334 10

1.00 19 0.63861 0.0033 19 0.24244 0.4726 11

1.00 21 0.00142 0.9967 11

1.00 12

A.

trawl survey estimates of recruitment are generally more variable than the estimates obtained from virtual population analysis. Our conclusions regarding geographic patterns in plaice recruitment variability in the eastern Atlantic remain unchanged. The time series of recruitment used in our analyses included all available data for each stock and was not restricted to the converged part of the SPA (i.e. those data that are well estimated and unlikely to change due to the results of new survey or fishery data). We felt that further reduction of already short time series for some of the plaice and sole stocks was not warranted. We did, however, examine the effect of excluding the estimate of recruitment in the most recent year on the CV of recruitment from each stock. This had little effect on the CVs with the exception of sole in the Celtic Sea, where the value dropped from 127% to 30%. The range of difference for all other species fell between 0 and 11% (mean = 2%). The effect of this re-calculation of the CV was to flatten the geographic pattern of recruitment variability in sole (Fig. 5) and there was no change

in either eastern Atlantic plaice or the NW Atlantic flatfish. Recruitment variation in the flatfishes we investigated differed from that of gadoids and herrings in two fundamental ways: first, recruitment was markedly less variable in the flatfishes; second, as noted above, the pattern of recruitment variation in the flatfishes differed from the expectations of the ‘species range hypothesis’ (Figs. 4-6) whereas the patterns evident in both gadoids and herring were generally consistent with expectations (Fig. la and Fig. 2). We infer from these differences that the factors influencing recruitment variation in these groups must differ in fundamental ways. Several investigators (Leggett, 1977; Peterman et al., 1988; Leggett and Deblois, 1994) have noted that the strength of correlations between early life stages and recruits to the reproductive or harvestable stock increases when abundance data of progressively later life stages are used as the basis of the independent variable. There is, clearly, a purely statistical basis for this increase in the strength of the correlation coefficient. How-

296

WC. Leggett, K.T. Frank/Journal

ever, it is also likely that the increase experienced as one progresses through the egg, larval, and early juvenile stages in these correlations is due, at least in part, to the damping effects of density-dependent mortality during the juvenile stage on recruitment variation induced by stochastic factors operating principally at the egg and larval stages. Van der Veer (1986), Van der Veer and Bergman (1987), and Van der Veer et al. (1990) have shown this to be true in plaice. In the Wadden Sea the coefficient of variation in plaice abundance declined from 62% to 30% during the settlement stage when density-dependent mortality is most severe (for a complete review see Bailey, 1994). The magnitude of these losses are likely to be influenced by the density of the newly settled juveniles in the environment (Beverton, 1984; Beverton and Iles, 1992). In theory density-dependent modulation could also occur as a consequence of competition between juveniles for food and space but empirical support for such processes is lacking (Van der Veer et al., 1990; Beverton, 1995). Flatfishes differ from gadoids and herring in that their early juveniles occupy a two-dimensional environment in which the potential for density-dependent effects on survival is likely to be amplified relative to the three-dimensional environment occupied by equivalent life stages of gadoids and herring. We conclude that the reduced recruitment variability and the absence of consistent latitudinal patterns in recruitment variation in flatfishes result from the strong and apparently species-specific modulation of recruitment variability by density-dependent mortality operating primarily at the juvenile stage. We concur with Sharp (1994) that a fuller understanding of the processes regulating recruitment in this group, and in particular the geographic and temporal patterns of variability of individual species will require that future research focus on developing a much better understanding of the predator-prey relations and physiologically significant environmental variables that combine to determine recruitment in the flatfishes. The individual-based modelling of recruitment and recruitment processes in winter flounder undertaken by Chambers et al. (1995) provides a worthwhile template for defining the key questions to be addressed.

of Sea Research 37 (1997) 281-299

Acknowledgements We are pleased to acknowledge our debt to Dr. R. Myers, Department of Fisheries and Oceans, St. John’s, Newfoundland, who provided the data upon which the analyses contained in this paper are based. Appendix A Date sources for time series of recruitment and spawning stock biomass generated by VPA for flat&h species from the eastern and western Atlantic. Data were supplied by R. Myers Species:

Plaice (Pleuronectes platessa)

Stock: Source:

ICES VIId Anon., 1993. Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES Dot. C.M. 1993/Assess: 5. VPA, 1 year olds in actual numbers

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Thousands/tonnes 1 ICES VIIe Anon., 1993. Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES Dot. CM. 1993/Assess: 3. VPA Thousands/tonnes 1 Celtic Sea Anon., 1993. Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES Dot. C.M. 1993/Assess: 3. VPA, 1 year olds in actual numbers Thousands/tonnes 1 ICES IIIa Anon., 1993. Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES Dot. C.M. 1993/Assess: 5. VPA, 1 year olds in actual numbers

2 Irish Sea Anon., 1993. Report of the Working Group on the Assessment of Northern Shelf Demersal stocks. ICES Dot. C.M. 1993/Assess: 20.

WC. Leggett, K.‘I: Frank/Journal

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments: Recruitmenti SSB units: Age at recruitment:

VPA, 1 year olds in actual numbers, REC from 1990 to 1991 uses weighted ave. prediction. Thousands/tonnes

of Sea Research 37 (1997) 281-299

Recruitment/ SSB units: Age at recruitment: Stock: Source:

Kattegat Anon., 1987. Report of the Division IIIa Demersal Stocks Working Groups. ICES Dot. C.M. 1987/Assess: 16. Anon., 1990. Report of the Division IIIa Demersal Stocks Working Groups. ICES Dot. C.M. 1990/Assess: 20. Anon., 1991. Report of the Division IIIa Demersal Stocks Working Groups. ICES CM. Dot. 199UAssess: 9. Anon., 1992. Report of the Division IIIa Demersal Stocks Working Groups. ICES C.M. Dot. 1992/Assess: 9. Thousands/tonnes

Recruitment/ SSB units: Age at recruitment: Stock: Source:

North Sea Anon., 1988. Report of the North Sea Flatfish Working Group. ICES Dot. C.M. 1988/Assess: 9. Anon., 1991. Report of the North Sea Flatfish Working Group. ICES C.M. 199UAssess: 5. Anon., 1992. Report of the North Sea Flatfish Working Group. ICES C.M. 1992/Assess: 6. Anon., 1993. Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES Dot. CM. 1993/Assess: 5. VPA, I year olds in actual numbers Millions/thousand

Recruitment/ SSB units: Age at recruitment: Stock: Source:

tonnes

Skagetmk Anon., 1990. Report of the Division IIIa Demersal Stocks Working Group. ICES Dot. C.M. 1990/Assess: 10. Anon., 1991. Report of the Division IIIa Demersal Stocks Working Group. ICES Dot. C.M. 199UAssess: 9. None Thousands/tonnes 2

Species:

Sole (Solea vulgaris)

Stock: Source:

Celtic Sea Anon., 1993. Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES Dot. C.M. 1993/Assess: 3. VPA, 2 year olds in actual numbers

Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

Comments:

291

Thousands/tonnes 2 ICES IIIa Anon., 1987. Report of the Division IIIa Demersal Stocks Working Groups. ICES Dot. C.M. 1987/Assess: 16. Anon., 1990. Report of the Division IIIa Demersal Stocks Working Groups. ICES Dot. CM. 1990/Assess: 10. Anon., 1991. Report of the Division IIIa Demersal Stocks Working Groups. ICES C.M. 199UAssess: 9. Anon., 1992. Report of the Study Group on Division IIIa Demersal Stocks. ICES Dot. CM. 1992/G: 2. Thousands/tonnes 2 Irish Sea Anon., 1993. Report of the Working Group on the Assessment of Northern Shelf Demersal stocks. ICES Dot. CM. 1993/Assess: 20. SPA, 2 year olds in actual numbers, REC from 1989 to 1990 uses weighted ave. prediction. Thousands/tonnes 2 North Sea ICES Symposium on the Changes in the North Sea Stocks and their causes. No. 30.; Anon., 1982. Report of the North Sea Flatfish Working Group ICES Dot. C.M. 1982/Assess: 3.; Anon., 1988. ICES Dot. C.M. 1988.; Anon., 1991. ICES Dot. C.M. 199UAssess: 5.; Anon., 1992. Report of the North Sea Flatfish Working Group. ICES Dot. CM. 1992/Assess: 6.; Anon., 1993. Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES Dot. C.M. 1993/Assess: 5. VPA, 1 year olds in (000 000’s) Millions/thousand

tonnes

ICES VIId Anon., 199 1. Report of the North Sea Flatfish Working Group. ICES Dot. C.M. 199UAssess: 5. Anon., 1992. Report of the North Sea Flattish Working Group. ICES Dot. C.M. 1992/Assess: 6. Anon., 1993. Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak. ICES Dot. C.M. 1993/Assess: 5. VPA, 1 year olds in (000’s)

298

WC. Leggett, K.T. Frank/Journal

Source:

Recruitment/ SSB units: Thousands/tonnes Age at recruitment: Stock: Source:

ICES VIIe Anon., 1993. Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES Dot. CM. 1993/Assess: 3. VPA, 1 year olds in (000’s)

Comments: Recruitment/ SSB units: Thousands Age at recruitment: Stock: Source:

Bay of Biscay (VIII) Anon., 1993. Report of the Working Group on the Assessment of Southern Shelf Demersal Stocks. ICES Dot. C.M. 1993/Assess: 3. None

Comments: Recruitment/ SSB units: Thousands/tonnes Age at recruitment: 0 Species:

American plaice (Hippoglossoides

Stock: Source:

NAFO 3LN0 Brodie, W.B., Bowering, W.R., Baird, J.W., 1990. An assessment of the American plaice stocks in division 3LN0. NAFO SCR Dot. 90/80, 32 pp. SPA, 6 year olds in (000’s)

platessoides)

Comments: Recruitment/ Thousands/tonnes SSB units: Age at recruitment: 6 Stock: Source: Comments: Recruitment/ SSB units: Age at recruitment: Stock: Source:

of Sea Research 37 (1997) 281-299

Thousands/nil 6 NAFO 5YZ Anon., 1992. Report of the Fourteenth Northeast Regional Stock Assessment Workshop (14th SAW). Northeast Fisheries Science Center Reference Document 92-07. SPA, 6 year olds in (000’s)

Comments: Recruitment/ SSB units: Millions/thousand tonnes Age at recruitment: YellowtailJIounder

stock:

NAFO 3LN0

Comments: Recruitment/ SSB units: Thousands/tonnes Age at recruitment: 4 Stock: Source: Comments: Recruitment/ SSB units: Age at recruitment:

NAFO 5Z Woods Hole Ref. Dot. 91-03. RV (1 + 2)

Stock: Source: Comments: Recruitment/ SSB units: Age at recruitment:

Southern New England Woods Hole Ref. Dot. 91-03. RV (1 + 2), F is the median

Millions/thousand tonnes 1

Millions/thousand tonnes 1

References

NAFO 3Ps Brodie, W.B., 1991. CAFSAC Res. Dot. 91/72. SPA, 6 year olds in (000’s); no SSB data.

Species:

Brodie, W.B., 1986. An assessment of yellowtail flounder in NAFO div. 3LN0. NAFO SRC Dot. 86/40, 20 pp. Brodie, W.B., Walsh, S.J., Bowering, W.R., 1990. Yellowtail flounder in NAFO div. 3LN0 - an assessment of stock status. NAFO SCR Dot. 90/86, 24 pp. Paz, J., Larra, M.G. Neta, 1990. Year-class variations of American plaice and yellowtail flounder in div. 3LN0 and the abundance of other commercial fish. NAFO SCR Dot. 90/l 14, 10 pp. SPA, 5 year olds in (000’s)

(Limanda ferruginae)

Bailey, K.M., 1994. Predation on juvenile flatfish and recruitment variability. Neth. J. Sea Res. 32, 175-189. Beverton, R.J.H., 1984. Dynamics of single species. In: May, R.M. (Ed.), Exploitation of Marine Communities. Life Sci. Res. Rep. 32, Springer-Verlag. Berlin, pp. 13-58. Beverton, R.J.H., 1995. Spatial limitation of population size: the concentration hypothesis. Neth. J. Sea Res. 34, l-6. Beverton, R.J.H., Iles, T.C., 1992. Mortality rates of O-group plaice (Pleuronectes platessa L.), dab (Lima&a fimanda) and turbot (Scophthalmus maximus L.) in European waters. III. Density-dependence of mortality rates of O-group plaice and some demographic implications. Neth. J. Sea Res. 29, 61-79. Chambers, R.C., Rose, K.A., Tyler, J.A., 1995. Recruitment and recruitment processes of winter flounder Pleumnectes americanus, at different latitudes: implications of an individualbased simulation model. Neth. J. Sea Res. 34, 10-43. Cohen, E.B., Mountain, D.G., O’Boyle, R., 1991. Local-scale versus large-scale factors affecting recruitment. Can. J. Fish. Aquat. Sci. 48, 1003-1006. Dickson, R.R., Brander, K.M., 1993. Effects of a changing windfield on cod stocks of the North Atlantic. Fish. Oceanogr. 2, 124-153. Frank, K.T., 1992. Demographic consequences of age-specific

WC. Leggett, K.Z Frank/Journal dispersal in marine fish populations, Can. J. Fish. Aquat. Sci. 49,2222-2231. Hollowed, A.B., Bailey, K.M., Wooster, W.S., 1987. Patterns in recruitment of marine fishes in the northeast Pacific Ocean. Biol. Oceanogr. 5, 99-131. Iles, T.C., 1994. A review of stock-relationships with reference to flatfish populations. Neth. J. Sea. Res. 32, 399-420. Kovtsova, M.V., Boitsov, K.D., 1995. Recruitment of the Barents Sea plaice (Pleuronectes platessa L.). Neth. J. Sea Res. 34, 229-235. Leggett, W.C., 1977. Density dependence, density independence, and recruitment in the American Shad (Absa sapidissima) population of the Connecticut River. In: Van Winkle, W. (Ed.), Assessing the Effects of Power Plant Induced Mortality on Fish Populations. Pergamon Press, New York, pp. 3-17. Leggett, W.C., Deblois, E., 1994. Recruitment in marine fishes: is it regulated by starvation and predation in the egg and larval stages?. Neth. J. Sea. Res. 32, 119-134. McCall, A.D., 1990. Dynamic Geography of Marine Fish Populations. Washington University Press, Washington, 153 pp. Miller, J.M., Burke, J.S., Fitzhugh, G.R., 1991. Early life history patterns of Atlantic North American flatfish: likely (and unlikely) factors controlling recruitment. Neth. J. Sea. Res. 27, 261-275. Myers, R.A., 1991. Population variability and range of a species, NAFO Sci. Count. Stud. 16, 21-24. Myers, R.A., Barrowman, N.J., 1996. Is fish recruitment related to spawner abundance?. Fish Bull. 94, 707-724. Myers, R.A., Cadigan, N.G., 1993. Density-dependent juvenile mortality in marine demersal fish. Can. J. Fish. Aquat. Sci. 50, 1576-1590. Myers. R.A., Bridson, J., Barrowman. N.J., 1995a. Summary of worldwide spawner and recruitment data. Can. Tech. Rep. Fish. Aquat. Sci. 2024, l-274; and appendices. Myers, R.A., Barrowman, N.J., Thompson, K.R., 1995b. Synchrony of recruitment across the North Atlantic: an update.

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(Or, ‘now you see it, now you don’t!‘). ICES J. Mar. Sci. 52. 103-l IO. Myers, R.A., Murtz, G., Bridson, J., 1996. Spatial scales of interannual recruitment variations of marine, anadromous, and freshwater fish. ICES C.M. 1996/O, 18. Peterman, R.M., Bradford, M.J., Lo, N.C.H., Methot, R.D., 1988. Contribution of early life stages to interannual variability in recruitment of northern anchovy (Engraulis mm&x). Can. J. Fish. Aquat. Sci. 45, S-16. Philippart, C.J.M., Henderson, PA., Johannessen, T., Rijnsdorp, A.D.. Rogers, S.I., 1997. Latitudinal variation of fish recruits in Northwest Europe. J. Sea Res. (in press). Rijnsdorp, A.D., Van Beek, EA., Flatman, S., Millner, R.M., Riley, J.D., Giret, M., De Clerck, R., 1992. Recruitment of sole stocks, Solea solea (L.), in the northeast Atlantic. Neth. J. Sea. Res. 29, 173-192. Sharp, G.D., 1994. Recruitment in flatfish: lines for future research. Neth. J. Sea Res. 32, 227-230. Sinclair, A., 1994. Recent declines in cod stocks in the Northwest Atlantic. NAFO SCR Dot. 94/73, I- 17. Sinclair, M., Tremblay, M.J., Bernal, P., 1985. El Nifio events and variability in a Pacific mackerel (Scomber japonicus) survival index: support for Hjort’s second hypothesis. Can. J. Fish. Aquat. Sci. 42, 602-608. Van der Veer, H.W., 1986. Immigration, settlement and densitydependent mortality of a larval and early post-larval O-group plaice (Pleuronectes platessa) population in the western Wadden Sea. Mar. Ecol. Prog. Ser. 29, 233-236. Van der Veer, H.W., Bergman, M.J.N., 1987. Predation by crustaceans on a newly settled O-group plaice Pleuronectes platessa population in the western Wadden Sea. Mar. Ecol. Prog. Ser. 35, 203-215. Van der Veer, H.W., Pihl, L., Bergman, M.J.N., 1990. Recruitment mechanisms in North Sea plaice Pleumnectes platessu Mar. Ecol. Prog. Ser. 64, I-12.