ICES Journal of Marine Science, 57: 1077–1090. 2000
doi:10.1006/jmsc.2000.0702, available online at http://www.idealibrary.com on
Megrim (Lepidorhombus whiffiagonis) growth in the
North-eastern Atlantic based on back-calculation of otolith rings
J. Landa, and C. Piñeiro
Landa, J., and Piñeiro, C. 2000. Megrim (Lepidorhombus whiffiagonis) growth in the
North-eastern Atlantic based on back-calculation of otolith rings. — ICES Journal of
Marine Science, 57: 1077–1090.
Megrim, Lepidorhombus whiffiagonis, growth in waters of the north-eastern Atlantic
from 1991 to 1995 was analyzed using back-calculation of otolith rings. A significantly
higher growth rate longer lengths and older ages were observed in females. A
north-south gradient growth was found, with greater lengths and ages in northern
areas. The greatest variation in growth was found in the first three age classes, with a
higher growth rate in southern areas. Differences in spawning seasons among areas
may be one of the causes.
2000 International Council for the Exploration of the Sea
Key words: megrim, Lepidorhombus whiffiagonis, otolith, age reading, growth, east
Atlantic.
Received 23 March 1998; accepted 8 March 2000.
J. Landa: Instituto Español de Oceanografı́a, P.O. 240, 39080 Santander, Spain.
C. Piñeiro: Instituto Español de Oceanografı́a, P.O. 1552. 36280 Vigo, Spain.
Correspondence to: J. Landa: e-mail: [email protected]
Introduction
The pleuronectid species, Lepidorhombus whiffiagonis is
caught together with hake, anglerfish and Nephrops in
the multispecific trawl fisheries in the waters of ICES
Subareas VI to IX, mainly by Spain, France, Ireland,
Great Britain, Belgium and Portugal. In the period
1991–1995, mean annual landings of this species totalled
14 902 t in Divisions VII and VIIIab, and 442 t in
Divisions VIIIc and IXa. Spain caught 45% and 89% of
the respective totals (Anon., 1997).
This species is assessed annually by ICES, which
distinguishes two stocks, the northern stock (Sub-area
VII and Divisions VIIIab) and the southern stock
(Divisions VIIIc and IXa). This differentiation was made
more on the basis of differences in fishing yields of the
countries involved than differences found regarding their
biology.
The growth of L. whiffiagonis has been studied by
several authors (Dwivedi, 1964; Conan et al., 1981;
Rodrı́guez and Iglesias, 1985; Aubin-Ottenheimer, 1986;
Moguedet and Pérez, 1988; Peronnet and Rivoalen,
1989; Alperi, 1990; Peronnet, 1990); Dawson, 1991a;
Alperi, 1992; Landa et al., 1996). Most authors determined the age-length relationship directly, using length
at capture and age from otoliths; only Rodrı́guez and
Iglesias (1985) used back-calculation to study growth.
1054–3139/00/041077+14 $30.00/0
Very few papers have compared megrim growth
throughout its area of distribution.
The main aim of this study is to improve knowledge of
the growth of this species comparing the estimated
growth from back-calculation with that estimated
directly from length and age at capture. We also compare growth between different areas and sexes. Furthermore, this paper presents, for the first time, values of
mean lengths at age and growth parameters for the
north-western coast of the Iberian Peninsula (Subdivision IXa2), which is considered as the southern limit
of the distribution of this species (Cardador, 1983; Silva
and Azevedo, 1994).
Material and methods
A total of 746 whole sagittal otoliths of L. whiffiagonis
were studied. This material was collected from landings
of catches in north-eastern Atlantic waters (ICES
Divisions VIIchjk, VIIIab, VIIIc and IXa) (Fig. 1) made
by the Spanish commercial fleet between 1991 and 1995.
Also included in the study were specimens collected in
five previous fishery surveys organized by the Instituto
Español de Oceanografı́a and carried out aboard the
R/V ‘‘Cornide de Saavedra’’ in ICES Divisions VIIIc
and IXa in September and October, between 1991 and
2000 International Council for the Exploration of the Sea
1078
J. Landa and C. Piñeiro
Main L. whiffiagonis fishing zones
Studied zones
18° 16° 14° 12° 10°
8°
6°
4°
2°W 0°
61°N
59°
VIb
57°
55°
VIIc
VIIb
53°
51°
VIIk
VIIj
49°
VIIh
47°
VIIIa
VIIIb
45°
VIIIc1
VIIIc2
43°
IXa2
41°
39°
The preparation and examination of samples was the
same as that used in Landa et al. (1996), under reflected
light, on a black background. Measurements were taken
using an image analysis computer programme: optical
pattern recognition system (OPRS). The radius of the
left otolith from each pair was measured along the
longitudinal axis of the anterior surface. The distances
of all the hyaline rings to the centre of the otolith were
also measured, along the same longitudinal axis. From
all these hyaline rings, those which were considered as
being annual, by their general width and clarity, were
distinguished and their respective distances to the centre
of the otolith were measured and placed in one file, while
another file was created in which all the rings (those
assumed to be annual plus others) were placed.
The criteria used to interpret age were the same as
that used in the workshop on megrim, L. whiffiagonis,
of Subarea VII age determination (Anon., 1991). All
otoliths were examined by two readers and the annual
hyaline rings on both otoliths of each pair were counted.
To corroborate that otolith use is valid for L. whiffiagonis age determination, it is fundamental to demonstrate that there is a season of the year in which the
otolith forms a hyaline edge; that the frequency distribution of distances from the centre of the otolith to the
presumed annulus are unimodal and increase with the
age of the fish; that there is correlation between fish
length and otolith size, and fish length and the number
of rings. The season in which the annual hyaline rings
form was determined by examination of the frequency
distribution of otolith edge types throughout the year.
To establish that the rings are formed annually,
the frequency distribution of all rings observed was
examined, along with the frequency distribution of each
annual ring.
To determine the relationship between total fish
length and the radius of the otolith, different fits were
tried for each area and sex, and the potential model was
selected:
Lt =aRbt,
37°
Figure 1. Location of commercial fishing and study zones for
L. whiffiagonis.
1995. In Division VIIIc, two Subdivisions were distinguished, VIIIc1 and VIIIc2, with the aim of analyzing
the possible differences in growth between them. In
Division IXa, the area studied corresponds to the
Spanish part (Subdivision IXa2).
The study was carried out independently for each sex,
taking into account the differential sexual growth of this
species (Landa et al., 1996).
(1)
where:
Lt =total fish length when caught
Rt =otolith radius when caught
a,b=parameters of the regression.
To estimate the back-calculated lengths, many
authors have described the allometric nature of the
relationship of L on R, noting a phase of greater growth
of the hard part with respect to the fish, at younger
ages, a phenomenon that generates errors in the backcalculated lengths of young fish (Lee’s phenomenon,
Lee, 1912). Other new techniques related to the
intercept, such as the biological intercept procedure
(Campana, 1990), eliminate the presence of Lee’s
phenomenon. Campana (1990) and Ricker (1990)
Megrim growth in the North-eastern Atlantic
discussed the problem of departure from reality in
relation to choosing a method for determination of
values affecting the results of corrections of backcalculated fish lengths at age. As Ricker (1990) suggested, we selected the more widely-used Fraser-Lee
(Fraser, 1916; Lee, 1920) procedure (2) (Carlander,
1981) to obtain the back-calculated total length distributions from the measurements of the radii of otolith
rings and from lengths and radii of otoliths when fish
were caught. In this model the line of regression does not
pass through the origin, and includes the intercept value
(am) for the power regression of fish length and otolith
radius (Bartlet et al., 1984). The use of this model was
considered more suitable than that of Lea (1910), which
described a linear regression of fish length and otolith
radius which passed through the origin. This model (2) is
intercept-corrected because it incorporates the regression intercept and, although it does not incorporate the
regression slope directly, the value of the regression
intercept is influenced by the slope (Campana, 1990).
The growth parameters were estimated by using backcalculated lengths by age class. The theoretical model to
which growth was fitted was von Bertalanffy’s (1938)
growth equation:
Lt =L` (1e0k(tt)),
where:
Lt =length at age class t.
L` =maximum length the species can reach.
K=instantaneous growth coefficient.
t=age.
t0 =point at which the Von Bertalanffy curve intersects
the abcisas axis.
Marquardt’s algorithm (1963) for minimum-squares
regression was used for the fit. Different values of L`
were tested to determine how the remaining parameters
would respond. Initially, the values of the three parameters were estimated without restricting the value of
L`. Next, three possible values of L` were assigned
for each ICES division and each sex, corresponding
to:
where:
Li =total fish length when otolith radius was Ri
Ri =radius of the i-th ring
Lt =total fish length when caught
Rt =otolith radius when caught
am =intercept value for the power regression of L on R
(natural logarithm of a).
Some assumptions are present in the back-calculation
of growth. The Fraser-Lee procedure is sensitive to age
sample-dependent variations in the intercept of the fish
otolith length relationship used (Campana, 1990). It
must also be taken into consideration that the FraserLee procedure carries the assumption that the fish
otolith length relationship does not vary with growth
rate in a systematic way, and furthermore, that the
regression parameters can be accurately estimated from
random samples of the population (Campana, 1990).
Smale and Taylor (1987) describe sources of error in the
back-calculation procedure due to the truncation of the
sample and an undefinable dependent variable.
The comparisons between the back-calculated length
distributions of the same ring in different aged otoliths
were carried out using Kruskal-Wallis non-parametric
analyses, as we had previously determined that the
homoscedasticity criteria (Cochran and Bartlet’s test)
necessary to use parametric ANOVAS were not satisfied. In these, the length distributions from backcalculation of a single specimen were not included in the
comparison. The back-calculated length distributions
for each age among the different areas and between both
sexes were also compared using Kruskal-Wallis and
Kolmogorov-Smirnov non-parametric analyses.
1079
the greatest lengths observed in samples from the
commercial landings during the last seven years (=L
maximum)
L maximum/0.95
L maximum0.95
From these three possible values for each area and
year, the last was chosen in each of the cases, as it was
the one that showed a higher coefficient of determination
in practically all areas and years analyzed. For Subdivisions VIIIc1 and VIIIc2, the same L`-value was
taken, since these two areas were not distinguished in the
commercial landing data.
Growth estimated by other authors for the same areas
was also compared to see whether the differences in
growth found some areas in the present paper were also
observed in other papers.
Results
Annual hyaline rings were easily identifiable in otoliths
belonging to small-sized and, thus, young specimens. In
larger specimens, however, the identification of the last
annual rings was more difficult, due to slower growth,
making the rings closer together and closer to the edge,
where identification is more difficult.
The season of annual hyaline ring formation can
be inferred from the frequency distribution of the
otolith edges throughout the annual period. Figure 2
shows the percentage of otoliths which have an opaque
edge throughout the year (no data are available for
December). The hyaline edge is present in the first four
months of the year, while the opaque edge predominates
1080
J. Landa and C. Piñeiro
Opaque edges (%)
100
80
60
40
20
0
1
2
3
4
5
6 7
Month
8
9
10 11 12
Figure 2. Percentage of opaque edge otoliths by month.
in the rest of the year. April is the month in which the
annual hyaline ring formation terminates.
Figure 3 shows the frequency distributions, by area
and sex, for the individual, annual, hyaline rings and for
all of the hyaline rings combined. In all cases the
distribution of all rings combined is polymodal, whereas
the distribution of each annual ring is generally unimodal. Furthermore, the distribution of each annual
ring tends to correspond to a mode of the distribution
of all the rings combined. Therefore, although many
hyaline rings may appear on the surface of the otolith, it
is generally possible to identify and differentiate the
annual rings.
In the distribution of all the rings combined (Fig. 3), a
mode was observed before the first annual ring, which
was present in all areas/sexes and which did not correspond to any unimodal annual distribution. This ring is
seen more clearly in the otoliths belonging to young
fishes, it is obscured in older individuals, hidden below
layers of bicarbonate deposited in later years.
Another periodic structure was located within the first
annual ring, but at a greater distance from the centre
than the ring just described. In contrast with the previously described ring, this ring was only observed in
certain areas/sexes (Fig. 3). It was more common in
females and was more pronounced towards the south of
the area of study (Subdivisions VIIIc1 and IXa2). As in
the previous case, it corresponds to a non-annual ring
and it is more difficult to see in the otolith than the
previous non-annual ring.
Division VIIchjk was generally observed to have the
lowest otolith growth rate, while higher rates are found
further south in the study area. Similarly, Figure 3
shows that the number of annual rings also diminished
progressively, with a great range of ages being observed
in the north (Division VIIchjk and Division VIIIab) and
a minimum range in the south (Subdivision IXa2).
In the relationship between total fish length and
otolith radius, the power and linear models gave the best
adjusted coefficient of determination (r2) and the best
general fit to all points throughout the whole range of
values (Fig. 4), as has been observed in regression
relationships of the same variables by other authors (i.e.
Conan, 1981, and Rodrı́guez and Iglesias, 1985 with L.
whiffiagonis in Subareas VII, and also Alperi, 1992 in
Subdivision VIIIc2). Nevertheless, all of those studies
used linear models and a better fit might have been
obtained using a different formulation. Härkönen (1986)
observed that linear models provided the best fit in most
of the cases of 97 species studied in the north-eastern
Atlantic. However, in most of the cases, juvenile individuals were not considered. Manooch et al. (1987)
related both variables for each sex through a potential
relationship for Scomberomorus cavalla. In our case, the
potential model (1) was also selected to explain the
relationship, since it presented the highest adjusted
coefficient of determination and best fits throughout the
range of values, in addition to showing more homoscedastic residual error distributions than the linear
model, for all areas/sexes studied (Table 1). In a study
on another pleuronectiforme, plaice, Draganik and
Kuczynski (1993) found, like us, that the power model
gave the best fit and a more homoscedastic residual error
distribution than the linear model.
Table 1 shows the values of the parameters of the
equation for each area and sex. This fit was somewhat
poorer for Division VIIIab than for the other areas,
owing to the absence of data on small sizes (Fig. 4).
For Subdivisions VIIIc1 and IXa2, the size range
represented was limited with respect to the other areas
due to the lower abundance of this species in these
areas.
The values of mean-lengths of the back-calculated
total length distributions using the Fraser-Lee model
(Fraser, 1916; Lee, 1920) for the power regression for
each ring separated by area and sex were estimated.
The results of the comparisons between length distributions back-calculated from a single ring in otoliths of
different ages showed that, in general, there were no
significant differences (p<0.05). Significant differences
(p<0.05) only appear in one or two ages in some areas.
In ages showing significant differences between length
distributions back-calculated from the same ring, such
as areas IXa2 and VIIIc1 (females), differences may be
explained by the low level of abundance, small age range
and, consequently, few age classes (2 to 4 classes) which
could be compared for each ring in these areas. In other
areas, the differences are due to the presence of some
extreme ring size, and thus extreme back-calculated
length, in some age group (e.g. age group 13 in females
of Division VIIchjk, age group 8 in females of Division
VIIIab or age group 2 in females of Subdivision VIIIc2).
Nevertheless, in general, there is a minimal number of
ages in which differences appear compared with those in
which they do not.
50
VIIchjk males
40
30
20
10
0
50
VIIchjk females
90
80
70
60
50
40
30
20
10
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
VIIIab males
0
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
VIIIab females
60
40
50
30
40
30
20
20
10
0
60
10
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
VIIIc2 males
40
30
20
10
0
0
40
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
VIIIc2 females
80
70
60
50
40
30
20
10
50
Frequency
0
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
VIIIc1 males
VIIIc1 females
60
50
30
40
20
30
20
10
10
0
30
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
IXa2 males
0
IXa2 females
60
25
50
20
40
15
30
10
20
5
10
0
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
0
0.5 1 1.5 2 2.5 3 3.5 4 4.5 5 5.5 6 6.5 7
Ring measurement (mm)
Figure 3. Otolith focus-to-ring measurements, for all the rings and for the annual rings, by zone and sex.
1082
J. Landa and C. Piñeiro
VIIchjk males
70
60
50
40
30
20
10
0
1
2
Lt (cm)
1
2
1
2
1
2
7
3
4
3
4
3
4
1
2
3
4
0
1
2
5
6
7
0
1
2
6
7
0
1
2
6
7
0
1
2
6
7
0
Rt (mm)
6
7
3
4
5
6
7
3
4
5
6
7
3
4
5
6
7
5
6
7
IXa2 females
70
60
50
40
30
20
10
5
5
VIIIc1 females
70
60
50
40
30
20
10
5
4
VIIIc2 females
70
60
50
40
30
20
10
5
3
VIIIab females
70
60
50
40
30
20
10
IXa2 males
70
60
50
40
30
20
10
0
6
VIIIc1 males
70
60
50
40
30
20
10
0
5
VIIIc2 males
70
60
50
40
30
20
10
0
4
VIIIab males
70
60
50
40
30
20
10
0
3
VIIchjk females
70
60
50
40
30
20
10
1
2
3
4
Figure 4. Relationship between total length (Lt) and otolith radius (Rt) described by power function for L. whiffiagonis by zone and
sex.
Megrim growth in the North-eastern Atlantic
1083
Table 1. Relationship between total length and otolith radius described by power functions for L.
whiffiagonis by zone and sex.
Zone
r2
d.f.
F
p-value
a
b
VIIchjk
VIIIab
VIIIc2
VIIIc1
IXa2
VIIchjk
VIIIab
VIIIc2
VIIIc1
IXa2
0.945
0.882
0.948
0.948
0.913
0.951
0.895
0.965
0.948
0.927
77
62
82
53
31
138
78
118
76
43
1311.43
463.10
1504.64
962.49
324.25
2666.55
667.07
3282.46
1389.34
545.46
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
0.000
6.851
7.717
6.999
7.524
7.787
6.498
7.903
6.997
7.269
8.057
1.118
0.999
1.094
1.059
1.111
1.233
1.077
1.159
1.196
1.122
Sex
Males
Females
Table 2. Results of Kolmogorov–Smirnov test comparing back-calculated length distributions of each
age between both sexes, of L. whiffiagonis. (p<0.05: *; p<0.01: **; p<0.001: ***).
Age (years)
Zone
VIIchjk
VIIIab
VIIIc2
VIIIc1
IXa2
1
2
3
4
5
6
7
8
9
10
**
**
***
*
***
n.s.
***
***
***
**
***
***
***
***
—
***
***
***
*
—
***
***
***
n.s.
—
***
***
***
n.s.
—
***
***
***
—
—
***
***
*
—
—
n.s.
**
—
—
—
n.s.
*
—
—
—
Unimodal distributions of annual rings (Fig. 3), as in
the case of mean lengths back-calculated from the first
three rings (Fig. 5), varied among areas, lower in the
north (Division VIIchjk) and increasing progressively
in Divisions VIIIc2, VIIIab and VIIIc1, to reach
maximum levels in the south-western most area studied
(Subdivision IXa2).
The results of the Kolmogorov-Smirnov analysis,
which compares back-calculated length distributions
between both sexes for each age class, showed that high
significant differences (p<0.001) exist for practically all
of them (Table 2). For ages 1 and 2 in some areas, the
levels of significance are not as high as for later ages,
which indicates that growth in these first two ages was
not clearly differentiated between the two sexes, in some
areas. These results are consistent with the findings of
Landa et al. (1996), in which it was observed that the
differences in mean lengths between the two sexes were
evident from age 2 onwards. Fewer significant differences (p<0.05) were also evident for the older ages in
each area. However, examination of the mean lengths of
these older ages revealed even greater differences in
growth between the two sexes. As in the comparison
between areas, the absence of significant differences for
the older ages reflects the small sample size for these age
groups.
The use of samples from different years permitted us
to obtain back-calculated mean values of lengths that
can be considered distinctive of each area and sex. This
leads to better comparison among these areas and
between sexes, and incorporates interannual variations.
The results of the Kruskal-Wallis analyses to compare
back-calculated length distributions among all areas for
each age class, show that significant differences (p<0.05)
exist in many of them (Table 3). Kolgomorov-Smirnov’s
tests show significant differences (p<0.05) in the backcalculated length distributions of the first three ages in
almost all the pairs of areas compared. These differences
between areas for the first three ages are also apparent in
Figure 5. In these first ages, greater growth was observed
in zone IXa2, followed by zones VIIIc1, VIIIab, VIIIc2
and VIIchjk. Growth in the first two areas appears to be
more asymptotic, while growth in the latter two seems to
be more linear in its progression. Growth rates in the
two areas most distant from one another, Divisions
VIIchjk and IXa2, appear to be the most dissimilar.
Furthermore, the reduced size range of specimens from
Subdivision VIIIc1 and, above all, from Subdivision
IXa2, reflects a smaller length range and the lowest
number of annual rings found (Fig. 3). This fact is
related to the progressive fall in the abundance of this
species, as Sánchez et al. (1998) described, as we move
towards the west (Subdivision VIIIc1) and south (Subdivision IXa2) of the study area. Subdivision IXa2
represents the limit for the distribution of this species, to
the south of which its abundance is minimal (Cardador,
1084
J. Landa and C. Piñeiro
Table 3. Results of Kolmogorov–Smirnov and Kruskal–Wallis tests comparing back-calculated length distributions of each age
between different zones, of L. whiffiagonis. (p<0.05: *; p<0.01: **; p<0.001: ***).
Age (years)
Zones
Test
Sex
1
2
3
4
5
6
7
8
9
10
11
12
All zones
K-W
VIIchjk-VIIIab
K-S
VIIchjk-VIIIc2
K-S
VIIchjk-VIIIc1
K-S
VIIchjk-IXa2
K-S
VIIIab-VIIIc2
K-S
VIIIab-VIIIc1
K-S
VIIIab-IXa2
K-S
VIIIc2-VIIIc1
K-S
VIIIc2-IXa2
K-S
VIIIc1-IXa2
K-S
m
f
m
f
m
f
m
f
m
f
m
f
m
f
m
f
m
f
m
f
m
f
***
***
***
***
***
***
***
***
***
***
***
*
n.s.
n.s.
***
***
***
***
***
***
***
***
***
***
***
***
n.s.
***
***
***
***
***
*
*
n.s.
***
***
***
**
***
***
***
**
**
***
***
*
***
n.s.
***
**
***
*
—
*
*
n.s.
***
n.s.
—
**
***
*
—
n.s.
—
n.s.
***
n.s.
**
n.s.
n.s.
n.s.
n.s.
—
—
*
*
n.s.
n.s.
—
—
n.s.
n.s.
—
—
—
—
*
*
*
n.s.
n.s.
n.s.
n.s.
n.s.
—
—
**
**
n.s.
n.s.
—
—
n.s.
n.s.
—
—
—
—
**
*
n.s.
n.s.
n.s.
*
n.s.
n.s.
—
—
**
***
n.s.
n.s.
—
—
n.s.
n.s.
—
—
—
—
*
***
n.s.
n.s.
n.s.
**
—
n.s.
—
—
*
**
—
n.s.
—
—
—
n.s.
—
—
—
—
*
***
n.s.
n.s.
n.s.
**
—
—
—
—
n.s.
n.s.
—
—
—
—
—
—
—
—
—
—
*
**
n.s.
*
—
*
—
—
—
—
—
n.s.
—
—
—
—
—
—
—
—
—
—
n.s.
**
n.s.
*
—
*
—
—
—
—
—
n.s.
—
—
—
—
—
—
—
—
—
—
—
n.s.
—
—
—
n.s.
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
n.s.
—
—
—
n.s.
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
—
Females
55
50
50
45
45
40
40
Back-calculated Lt (cm)
Back-calculated Lt (cm)
Males
55
35
30
25
20
15
35
30
25
20
15
10
10
5
5
0
1
2
3
4
5
6 7 8 9 10 11 12 13 14
Age (years)
VIIchjk
VIIIab
0
VIIIc2
1
2
3
4
5
6 7 8 9 10 11 12 13 14
Age (years)
VIIIc1
IXa2
Figure 5. Back-calculated mean lengths (cm) at age in studied zones.
1983; Silva and Azevedo, 1994). In contrast, Division
VIIchjk shows a wide age range and the smallest lengths
for the first age classes and represents the area with
the highest abundance level (Poulard et al., 1993) of
the areas studied. Zones VIIIab, VIIIc1 and VIIIc2
exhibited mean lengths at age and age ranges that lay
between those of Divisions IXa2 and VIIchjk. The
similarity between Divisions VIIIc1 and VIIIab is clear
Megrim growth in the North-eastern Atlantic
1085
Table 4. Von Bertalanffy’s growth parameters estimated with back-calculated total lengths (cm) for L. whiffiagonis by zone and sex.
Parameter
Males
VIIchjk R2 =0.91
L`
K
t0
No restriction
Estimate
Std Error
Lower
Upper
Restriction: L` =0.95Lmax. by zone
Parameter
Estimate
Std Error
Lower
Upper
Males
VIIchjk R2 =0.90
L`
K
t0
43.70
0.16
0.15
2.63
0.02
0.11
38.53
0.13
0.36
48.87
0.20
0.05
35.78
0.25
0.16
1.29
0.02
0.08
33.24
0.21
0.01
38.32
0.29
0.32
VIIab R2 =0.95
L`
K
t0
50.20
0.13
0.83
2.29
0.01
0.11
45.69
0.10
1.04
54.72
0.15
0.61
VIIab R2 =0.95
L`
K
t0
42.75
0.17
0.49
1.33
0.01
0.09
40.13
0.15
0.67
45.37
0.20
0.31
VIIIc2 R2 =0.95
L`
K
t0
38.23
0.20
0.35
1.74
0.02
0.10
34.80
0.16
0.55
41.66
0.23
0.16
VIIIc2 R2 =0.95
L`
K
t0
36.10
0.22
0.25
1.41
0.02
0.09
33.33
0.18
0.43
38.87
0.26
0.07
VIIIc1 R2 =0.85
L`
K
t0
36.22
0.24
0.38
4.65
0.07
0.25
27.00
0.11
0.87
45.44
0.37
0.11
VIIIc1 R2 =0.85
L`
K
t0
36.10
0.24
0.37
4.59
0.07
0.25
27.00
0.11
0.87
45.20
0.37
0.12
22.73
1.34
0.66
1.19
0.43
0.17
20.34
0.47
0.33
25.12
2.21
1.00
IXa2 R2 =0.83
L`
K
t0
35.15
0.32
0.21
12.50
0.24
0.46
10.06
0.16
1.14
60.24
0.79
0.73
Females
VIIchjk R2 =0.95
L`
K
t0
62.70
0.14
0.40
1.65
0.01
0.04
59.46
0.13
0.32
65.94
0.16
0.49
IXa2 R2 =0.86
L`
K
t0
Females
VIIchjk R2 =0.95
L`
K
t0
74.24
0.11
0.23
2.67
0.01
0.05
68.99
0.10
0.13
79.49
0.12
0.33
VIIab R2 =0.96
L`
K
t0
59.79
0.14
0.38
2.22
0.01
0.08
55.43
0.12
0.53
64.15
0.16
0.24
VIIab R2 =0.96
L`
K
t0
56.05
0.16
0.28
1.79
0.01
0.07
52.53
0.14
0.41
59.57
0.18
0.14
VIIIc2 R2 =0.96
L`
K
t0
61.96
0.12
0.48
2.31
0.01
0.07
57.41
0.10
0.62
66.51
0.14
0.33
VIIIc2 R2 =0.95
L`
K
t0
50.35
0.18
0.13
1.22
0.01
0.06
47.96
0.16
0.25
52.74
0.20
0.00
VIIIc1 R2 =0.91
L`
K
t0
35.61
0.45
0.30
1.22
0.05
0.08
33.20
0.36
0.15
38.02
0.54
0.46
VIIIc1 R2 =0.88
L`
K
t0
50.35
0.19
0.30
4.95
0.04
0.16
40.56
0.12
0.61
60.14
0.27
0.01
IXa2 R2 =0.90
L`
K
t0
30.50
0.72
0.40
4.86
0.33
0.23
20.80
0.05
0.06
40.19
1.38
0.85
IXa2 R2 =0.91
L`
K
t0
45.60
0.30
0.01
20.37
0.23
0.33
4.91
0.17
0.66
86.29
0.76
0.65
for practically the whole age range, with growth in
Sub-division VIIIc1 being somewhat higher for females
aged 2 and 3. Division VIIIab was characterized by a
somewhat higher growth rate than that of the neighbouring Subdivision VIIIc2, and for most of the ages
compared the significance levels are not as high as
between other areas. In turn, Subdivision VIIIc2 had
slightly higher growth than that of Division VIIchjk.
Nevertheless, females over 7 years of age from Division
VIIchjk reached the highest mean lengths by age class of
all the areas studied.
If the growth curve is estimated without restricting
any of its parameters, L` and K undergo great variations as a function of the area studied (Table 4). These
values are often very different from those observed
experimentally. Fixing a value of L` =0.95L maximum (maximum value of landed length in each area),
and estimating the rest of the parameters using
1086
J. Landa and C. Piñeiro
Marquardt’s (1963) algorithm, values are obtained
which fit more closely to the experimental data
(Table 4). The results show that the values of maximum
lengths diminish as we move to the south (from Division
VIIchjk towards IXa2). However, values of K increase
progressively in the same direction, as the lengths at age
in the first ages also increase slightly, to form curves with
steeper slopes. Furthermore, the inverse relationship
between L` and K produces the condition in which a
decrease in L` results in an increase in the slope.
Discussion
Rodrı́guez and Iglesias (1985) are the only authors to
have described the evolution of the otolith edge of
L. whiffiagonis throughout the whole year. Their study,
which was carried out in Subarea VII, obtained similar
results including the identification of April as the month
in which hyaline ring formation comes to an end.
Fuertes (1978), in a study of the other species of megrim,
L. boscii, in Subdivisions VIIIc1 and IXa2, obtained
similar results.
The presence of the two small non-annual rings in the
otolith of L. whiffiagonis is related to the events taking
place in the first months of life of the fish until reaching
one year of age. The one which appears first, more
common and marked, may represent a pelagic ring. The
second non-annual ring, less common and marked, is
probably related to changes occurring during the switch
from pelagic to demersal life.
In a study of the other species of megrim, L. boscii, in
the same areas of study, Landa et al. (unpublished data)
found significant differences (p<0.05) between lengths at
age among different years, related to cohorts with
extreme growth. Here, samples from different years were
used together, and so the back-calculated mean lengths
for each ring within a single age correspond to mean
inter-annual values and not to values of any specific year.
In this way, the possible inter-annual variability in the
sizes of rings was incorporated in the comparison. After
obtaining the results it was observed that, in general,
when a group of multiple cohorts is taken, there are no
significant differences (p<0.05) in the sizes of the ring
corresponding to each age among fish of different ages.
The different growth patterns between sexes noted in
this study (Table 2, Fig. 5), with lesser mean lengths at
age in males, and females reaching older ages, corresponds to that observed in the study by Landa et al.
(1996) for the same study area, using observed lengths at
age. Thus, greater and faster growth in females than in
males is once more confirmed, which is common to
many pleuronectiform species. This phenomenon may
be related to differences in metabolism between the
sexes, such as differences in oxygen consumption (Pauly,
1994a, b) and/or to differences in the level of surplus
energy between reproduction and somatic growth, which
Rijnsdorp and Ibelings (1989) found in plaice, and/or
differential food ingestion, such as that found by Lozán
(1992) in another species of flatfish, Limanda limanda.
Landa et al. (1996), using direct otolith readings,
observed higher growth in the first ages in Subdivision
VIIIc1. Here, megrim growth is estimated for the first
time in Subdivision IXa2, and the observation by Landa
et al. (1996) is not only confirmed in Subdivision VIIIc1,
but this higher growth is found throughout Subdivisions
VIIIc1 and IXa2.
Feeding and temperature are the two most important
parameters conditioning growth. Latitudinal variations
in temperature may directly affect the maintenance
metabolism (Pauly, 1994b), or indirectly provoke early
spawning (Overholtz et al., 1991; Provotorova and
Berebejm, 1993), permitting a longer feeding period, and
thus growth. Therefore, the influence of differential
feeding between areas on growth must also be taken into
account.
Dawson (1991b) observed that the spawning season in
the western mackerel stock occurs sooner than that of
the North Sea stock, situated more to the north. Therefore, the growth season of the stock situated more to the
south begins earlier and lasts longer, bringing about
higher growth. Arbault and Lacroix (1975) found that
mean lengths of the first ring of this species are greater in
Division VIIIc (southern area) of the western stock than
those found in the western stock as a whole. They relate
this with the fact that the spawning season in Division
VIIIc starts earlier with respect to the whole stock
(Lockwood et al., 1981a, b), thus making its period of
growth also somewhat longer.
In L. whiffiagonis a very similar phenomenon was
observed. Dawson (1991c) described a latitudinal succession in the spawning season among Divisions VIIg,
VIIh, VIIj and VIIIa, with an earlier season in VIIIa
(more southerly situated), and a gradually later season
moving towards Division VIIg (more northerly
situated). These results are complemented by those of
Dwivedi (1964), who carried out a study in Subarea
VIII, and found, as in the case of mackerel, that the
beginning of the spawning season was earlier than
in areas further north. Studies are not available on
Division IXa, but in L. boscii, Dwivedi (1964) and Costa
(1986) documented earlier spawning in Division IXa,
which gets progressively later moving towards Division
VIIIab. Therefore, the greatest growth of the first ring in
the southernmost areas seems to be entirely explained by
the earlier spawning season. Nevertheless, differences in
growth are not only reflected in the first ring, but rather
extend to the first three years, with a progressive reduction. It may be that the differences in growth in the first
ring are not put down until the following year, and are
maintained in later years, although growth in these years
is very similar between areas.
Megrim growth in the North-eastern Atlantic
1087
Table 5. Summary of L. whiffiagonis growth parameters by ICES Divisions.
Div.
VII
Author
Conan et al. (1981)
Rodrı́guez & Iglesias (1985)
Aubin-Ottenheimer (1986)
Moguedet & Pérez (1988)
Peronnet (1990)
Peronnet & Rivoalen (1989)
Peronnet (1990)
Dawson (1991)
Landa et al. (1996)
Landa et al. (1996)
Present work
VIIab Landa et al. (1996)
Landa et al. (1996)
Present work
VIIIc2 Alperi (1990)
Alperi (1990)
Alperi (1992)
Landa et al. (1996)
Landa et al. (1996)
Present work
VIIIc1 Landa et al. (1996)
Present work
IXa2 Present work
Data
Period
year
Males
L`
K
t0
Females
n
2
r
L`
K
t0
n
r2
1981
Mar.–Aug. 29.74 0.25 1.59
6
67.65 0.12 0.51 210
1984
Annual
39.36 0.29
0.14 181
63.13 0.11 0.07 444
1985
Annual
38.40 0.34 0.06 72
60.20 0.14 0.05 190
1987
Annual
43.67 0.14 1.76 184
65.20 0.09 1.87 342
1987
Annual
50.31 0.10 1.88 204
66.80 0.11 0.33 726
1988
Annual
44.80 0.14 1.76 230
66.80 0.11 0.33 888
1989
Annual
53.92 0.09 2.12 387
69.92 0.10 1.08 1287
1990
March
34.40 0.16 1.65 74 0.82 64.90 0.08 2.40 192 0.99
1991
Annual
66.00 0.11 0.31 463 0.98
1992
Annual
46.00 0.14 1.25 171 0.99 66.00 0.13
0.38 256 0.98
1991–1995
Annual
43.70 0.16 0.15 79 0.90 62.70 0.14
0.40 135 0.95
1991
Annual
45.00 0.14 1.85 54 0.99 59.00 0.12 1.34
54 0.96
1992
Annual
45.00 0.23
0.29 180 0.99 59.00 0.19
0.92 128 0.99
1991–1995
Annual
42.75 0.17 0.49 64 0.95 56.05 0.16 0.28
80 0.96
1983
Nov.–Dec. 32.27 0.38 0.77 81
52.25 0.17 1.58 124
1984
June
34.29 0.26 0.72 112
49.59 0.17 0.82 156
1990
September 32.44 0.24 2.20 148
51.52 0.12 2.68 224
1991
October 38.00 0.21 0.91 122 0.93 53.00 0.17 0.59 181 0.98
1992
October 38.00 0.20 1.19 181 0.98 53.00 0.20
0.23 338 0.95
1991–1995
Annual
36.10 0.22 0.25 68 0.95 50.35 0.18 0.13 103 0.95
1991
Sep.–Oct. 38.00 0.27 0.22 24 0.98 53.00 0.26
0.17
37 0.99
1991–1995
Annual
36.10 0.24 0.37 44 0.85 50.35 0.19 0.30
67 0.88
1991–1995
Annual
35.15 0.32 0.21 32 0.83 45.60 0.30 0.01
44 0.91
The case of Divisions VIIIab and VIIIc2 is particularly interesting. Although the former is situated more to
the north, it has somewhat higher mean lengths than
Subdivision VIIIc2. Specific studies showing a possible
earlier spawning in Division VIIIab are not available.
Both continental shelves of the Bay of Biscay present
well-differentiated characteristics which affect productoin phenomena. As a mechanism of fertilization in the
Spanish continental shelf (Subdivision VIIIc2), Sánchez
and Gil (1999) propose vertical forcing by Ekman drag
by north-east winds in spring-summer in the Spanish
continental shelf. Also, the greater width of the French
continental shelf (Divisions VIIIab) favours tidallyinduced vertical mixing. Thus, the continental run-off
and dynamic of nutrients associated with estuaries play
an important role in the fertilization of the photic area
(Le-Fèvre, 1986). All of this may favour a higher primary production in Divisions VIIIab than in Subdivision VIIIc2 (Sournia et al., 1990; Poulet et al., 1996).
This greater availability of food in the trophic chain may
explain the higher growth found in the east of the Bay of
Biscay with respect to that of the southern part.
Concerning the higher growth in Subdivision VIIIc1,
with respect to Subdivision VIIIc2 at the same latitude,
it must be mentioned that this has also been found in
other species, such as sardine larvae (Sardina pilchardus)
(Alvarez and Alemany, 1992). In the spawning season of
this species, Moreno-Ventas (pers. comm.) also observed
earlier warming of waters in Subdivisions IXa2 and
VIIIc1 than in Subdivision VIIIc2, which may provoke
an earlier spawning season. It has also been observed
that upwelling phenomena appearing in Subdivisions
VIIIc1 and IXa2 favour a higher primary production
(Cabanas et al., 1992; Varela, 1992). Similarly, in Subdivision VIIIc1 (Fraga, 1982; Lavı́n et al., 1992)
observed mixing of water masses which did not occur in
neighbouring areas. Thus, an earlier start of the spawning season, together with differing oceanographic
characteristics may influence the trophic chain of
megrim and so have repercussions in a different diet
and longer feeding period favouring higher growth in
Subdivisions VIIIc1 and IXa2 than in Subdivision
VIIIc2.
Pauly (1994b) observed that the latitudinal increase in
temperature influences on length and maximum age of a
species, this latter value increasing as temperature falls.
The age ranges and maximum lengths estimated for each
area both in Landa et al. (1996) and in the present paper
confirm this phenomenon.
In comparison with the paper of Landa et al. (1996),
which discussed growth in megrim in part of the same
area studied in this paper, and which was elaborated
from direct readings, in most cases both the mean
lengths at age and the parameters obtained by backcalculation were similar (Table 5). The greatest differences in growth parameters between both papers were
observed for area VIIIc1, owing to the differences in
mean lengths at age and the small age range from
1088
J. Landa and C. Piñeiro
Table 6. Mean values of K by author using the same value of L` (males: 43.7 cm; females: 62.7 cm)
for the whole area and age range of 1(2)–7 years.
Div.
VII
VIIIab
VIIIc2
VIIIc1
Author
Rodrı́guez & Iglesias (1985)
Aubin-Ottenheimer (1986)
Moguedet & Pérez (1988)
Peronnet & Rivoalen (1989)
Peronnet & Rivoalen (1989)
Dawson (1991)
Landa et al. (1996)
Present work
Mean of all authors
Landa et al. (1996)
Present work
Alperi (1990)
Alperi (1990)
Landa et al. (1996)
Landa et al. (1996)
Present work
Mean of all authors
Present work
which the parameters were estimated using direct
reading.
In Subarea VII, the papers of Conan et al. (1981)
in the case of females, Moguedet and Pérez (1988),
Peronnet and Rivoalen (1989), Peronnet (1990) and
Landa et al. (1996) showed very similar mean lengths at
age and growth parameters in all areas (Table 5). For
males, L` varied between 30 and 54 cm with K between
0.10 and 0.34. In females, L` varied between 60 and
70 cm with K between 0.08 and 0.14. Other authors
presented certain differences: Rodriguez and Iglesias
(1985) for females and Dawson (1991a) estimated slower
growth than the rest of the authors. Aubin-Ottenheimer
(1986), however, estimated faster growth for males.
Conan et al. (1981) and Rodrı́guez and Iglesias (1985)
underestimated L` due to lack of age range coverage,
giving rise to a greater value of the slope.
Subdivision VIIIc2 is quite uniform both in mean
lengths by age class and in the growth parameters
estimated throughout all the authors. The differences
observed in the parameters of males in the papers of
Alperi (1990, 1992) are not due to great differenes in
mean lengths of age, but rather to the fact that, as with
some authors on Subarea VII, there is a lack of coverage
of the age range, which produces a lower value of L`
and a greater slope of the curve.
In most of the studies carried out within each area,
great differences were not observed in mean lengths
estimated by age class. Thus, in many cases nor were
great differences found between the parameters estimated from these values. Only in these cases are the
differences in the age range coverage what bring about a
greater variation in the parameters.
Data
year
1984
1985
1987
1989
1987–1989
1990
1991–1992
1991–1995
1991–1992
1991–1995
1983
1984
1991
1992
1991–1995
1991–1995
Males
Females
0.08
0.22
0.14
0.14
0.14
0.12
0.15
0.17
0.15
0.19
0.16
0.15
0.13
0.11
0.14
0.15
0.14
0.17
0.07
0.13
0.13
0.09
0.10
0.08
0.12
0.13
0.11
0.14
0.13
0.11
0.11
0.11
0.13
0.12
0.11
0.13
The mean lengths estimated by other authors in
different areas come from different seasons of the year
and the comparison of these values is not easy. Neither
is the comparison of parameters L` and K presented in
Table 5 easy, given the inter-relation between the two.
To check whether the differences in mean lengths at first
ages among areas of our paper were also appreciable in
the values of the parameter K, the value of K was
estimated for each year, area and author, using the
same, fixed value of L` for the whole study area. The
highest value of L` estimated here for each sex was:
43.7 cm for males and 62.7 cm for females. As seen in
Table 5, the value of K varied interannually, in part
influenced by the age range and therefore by the abundance of that year. To avoid this influence, a common
age range was taken for all areas such that the possible
growth differential could be compared in the greatest
number of areas possible. All mean lengths between 1 (2)
and 7 were taken. Area IXa2 was not included in the
comparison given its scarce age range.
If we compare the values of the slope obtained in the
present work with those obtained by other authors for
the same areas (Table 6), we see that they are similar. On
comparing the mean values of the areas in which several
studies have been carried out (Division VIIchjk and
Division VIIIc2), it is observed that estimated growth is
very similar, confirming the similarities between mean
lengths by age class between the two areas (Table 3, Fig.
5). Furthermore, the differences in growth observed in
the first ages, higher growth being observed in Division
VIIIc2, are compensated by greater length in older ages.
In general it seems evident that the differences in
growth among areas in the first ages (1, 2 and 3) do not
Megrim growth in the North-eastern Atlantic
follow the same shape, but tend to even out in older ages
(4, 5 and 6).
It can also be seen that there is a latitudinal variation
in growth, with a greater age range and maximum
lengths in the north (Division VIIchjk), intermediate in
the Bay of Biscay (Division VIIIa,b,c2), less in the north
of the Galician continental shelf (Division VIIIc1) and
least in the south of the Galician continental shelf
(Division IXa2), where the species is very scarce.
There also seems to be a latitudinal variation in
growth of the first ages, with lower mean lengths at age
in the north (Division VIIchjk), intermediate in the
south of the Bay of Biscay (Division VIIIc2), greater in
the north of the Bay of Biscay (Division VIIIab) and
north of the Galician continental shelf (Division VIIIc1)
and maximum to the south of the Galician continental
shelf (Division IXa2). Furthermore, differences in mean
lengths seem to exist in all ages in the Bay of Biscay,
with higher growth in Division VIIIab (north) than in
Subdivision VIIIc2 (south).
Knowledge of these growth differences observed in the
areas which make up in the northern and southern
stocks of this species will be useful to improve the
assessment of the species and, at the same time, may
serve to progress in the differentiation of stocks on the
basis of biological criteria.
Acknowledgements
Thanks are extended to Ricardo Sánchez, Xabier
Moreno-Ventas, Pablo Abaunza and Luis Valdés for
their suggestions, to the whole Demersal fisheries team
of the IEO in Vigo and the teams which participated in
the IEO fishing surveys ‘‘Demersales 0991, 0992, 0993,
0994 and 0995’’ for their help in otolith sampling and
material preparation. We would also like to thank The
Basque Government for their support in funding the
project through a grant provided within the ‘‘Programa
de Formación de Investigadores del Departamento de
Educación, Universidades e Investigación’’. Finally, we
are grateful for our stay and time spent in the IEO in
Vigo.
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