BULLETIN OF MARINE SCIENCE, 71(1): 515–534, 2002
BIOLOGICAL VARIATION OF LOLIGO VULGARIS (CEPHALOPODA: LOLIGINIDAE) IN THE EASTERN ATLANTIC AND MEDITERRANEAN
A. Moreno, J. Pereira, C. Arvanitidis, J.-P. Robin, D. Koutsoubas, C. Perales-Raya, M. M. Cunha, E. Balguerias and V. Denis
ABSTRACT The biological characteristics of the squid Loligo vulgaris from north France, north- west Portugal, the Saharan Bank, and the Greek Seas were analyzed to describe large- scale biological patterns and to evaluate geographical variation in the Atlantic and the Mediterranean. In northwest Portugal and on the Saharan Bank population length struc- tures are more complex due to extended spawning and recruitment periods. Squid spawn only between November and April in north France and the Greek Seas. Gonadosomatic indices decreased with decreasing latitude in the Atlantic, while the highest indices were found in the Mediterranean. Full maturity occurred at smaller size in northwest Portugal than in other areas of the Atlantic, and at similar size to Mediterranean squid. Length- weight relationship slopes increased from the north to the south in the Atlantic and in the Mediterranean. Multivariate analysis of seasonal biological indices demonstrated sig- nificant biological differences between squid of different areas, mainly in terms of size at maturity, male GSI and average body size and weight. Biological variability between areas was considered related to plasticity of responses to large-scale geographic environ- mental conditions.
Loligo vulgaris Lamark, 1798 is a neritic species living in temperate waters in the eastern Atlantic, from the North Sea and around the British Isles (55°N) to the western African coast (20°S), and throughout the Mediterranean Sea (Roper et al., 1984). L. vul- garis and L. forbesi are the main targets of squid fisheries on the Atlantic European coasts. Catches of commercial importance are taken mainly by the United Kingdom, France, Spain and Portugal (Boyle and Pierce, 1994). Separate landings statistics for the two species are not recorded. In the northeast Atlantic Loligo species are mainly a by-catch of the multi-species bottom trawl fisheries, although some directed small-scale hand-jig fisheries exist in Spain (Guerra et al., 1994) and Portugal (Coelho et al., 1994). However, L. forbesi is known to be more abundant in the northern areas, being replaced southwards by L. vulgaris. In the Mediterranean, Loliginid populations, mostly made up of L. vul- garis, are not targeted, but are heavily fished by Spain and Italy (Worms, 1983). Pub- lished cephalopod fishery and abundance studies from the eastern Mediterranean are very limited, in particular with reference to L. vulgaris (e.g., D’Onghia et al., 1996; Lefkaditou et al., 1998). Unlike the northeast Atlantic and Mediterranean fisheries, L. vulgaris is an important secondary target species in the Saharan Bank cephalopod trawl fishery (Raya et al., 1999). Research on aspects of the life-cycle of L. vulgaris from various parts of its distribu- tion, includes studies from the northeast Atlantic: the Dutch coast (Tingbergen and Verwey, 1945), the Galician coast (Guerra and Rocha, 1994; Rocha, 1994; Rocha and Guerra, 1996), and the Portuguese coast (Coelho et al., 1994; Moreno et al., 1994, 1996; Bettencourt et al., 1996; Villa et al., 1997); from the central-east Atlantic (Baddyr 1988, 1991; Bravo de Laguna, 1988; Arkhipkin, 1995; Raya et al, 1999); and from the western Mediterra-
515 516 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002 nean (Mangold-Wirz, 1963, Worms, 1980, 1983; Natsukari and Komine, 1992). There are no published studies on the population biology of L. vulgaris in the eastern Mediter- ranean. Moreover, most studies were undertaken in distinct periods within a range of 50 yrs. Nevertheless, a certain degree of consistency can be found for some of the biological characteristics of L. vulgaris across its range. The following aspects can be considered typical of the species: a 1:1 sex ratio, a complex population structure driven by protracted recruitment and spawning periods, spawning in the colder seasons, spring and summer recruitment, lower size at maturity in males, and a one year life span (estimated from statolith analysis). Recently a multinational European research project (FAIR CT96 1520) provided sup- port for new biological data collection and a new analysis of historical data on L. vul- garis. The surveyed areas (the English Channel, the Portuguese coast, the Saharan Bank, and the Greek Seas) have different environmental conditions, namely temperature re- gimes and food availability. This paper aims to describe broad-scale biological patterns of L. vulgaris populations and to evaluate the geographic variation, based on similar sampling at the limits of its distribution: from northern (English Channel) and southern areas (Portugal) in the north- east Atlantic, from the central-east Atlantic (Saharan Bank) and from the eastern Mediter- ranean (Greece). Furthermore, this paper examines the relationships between biological and environmental variation.
MATERIAL AND METHODS
BIOLOGICAL SAMPLING.—Samples of L. vulgaris were collected monthly from the northeast At- lantic (English Channel and Portuguese waters) and the eastern Mediterranean (Greek Seas), be- tween January 1997 and June 1999. Available historical data from the central east Atlantic (Saharan Bank) were re-analysed and used for comparisons, when appropriate. Fishery data (landings of L. vulgaris from all fishing gears) from the four areas were analysed for the period 1997–1998. Samples from the English Channel (hereafter referred to as north France) were collected from trawl fishery landings at the Port-en-Bessin fish market between January 1997 and May 1999 (1475 specimens), during the periods when this species is present in the catches. The offshore bottom trawlers use nets with 80 mm cod-end stretched mesh size. The fishing grounds are located at a depth range of 50 to 150 m (49.5–50.5°N, 1°E–5°W). Portuguese samples (hereafter referred to as northwest Portugal) were taken from the trawl fish- ery landings in Peniche and Nazaré markets, between January 1997 and June 1999 (3040 speci- mens). Here, the fishing grounds are located off the coast (39–40.5°N, 9°W) at a depth range of 60 to 90 m. The stretched trawl mesh is approximately 65 mm long. Samples of all commercial size categories from the Saharan Bank (hereafter referred to as Sa- haran Bank) were obtained from the Spanish commercial trawl fishery (881 specimens) in June, September, November and December 1993, and January 1994 (21–28°N, 13–17°W). The trawlers use nets with a stretched mesh of 60 mm. Additional samples were collected during a research cruise onboard the Moroccan research vessel CHARIF AL IDRISSI in April 1994 (377 specimens). In this area, fishing grounds are located between 50 and 100 m depth. L. vulgaris was also sampled from the trawl fishery in Greece (hereafter referred to as Greek Seas), between October 1997 and May 1999 (35–41°N, 21–26°E) (880 specimens). Commercial bottom trawlers use cod-end stretched mesh sizes of 26 mm. Fishery samples were not taken from June to September as this period is closed for the trawl fishery, but additional samples were collected when possible during research cruises in the RV PHILIA by means of a commercial net: in July 1997 and May 1998 (162 speci- mens). MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 517
Squid sampling methods were similar within and between localities. Dorsal mantle length (ML) was recorded in all specimens. The monthly sampled specimens were sexed, body weight (BW) recorded, and maturity assessed (maturity scale after Lipinski, 1979 in the Saharan Bank and after Boyle and Ngoile, 1993 in the other areas). Gonad weight (testis or ovary) (GW) was recorded for sub-samples of the monthly samples. DATA ANALYSIS.—Variables of ML, BW, recruitment, maturity, size at maturity and sex ratio (22 biological indices) were computed for each time period, for each area and for the whole area. Average ML, overall (AvgML, mm) and by sex (AvgMLM and AvgMLF), and average BW, overall (AvgBW, g) and by sex (AvgBWM and AvgBWF) were estimated. The averages by sex were compared between geographic areas for the period October 1998–June 1999 (Saharan Bank, October 1993–June 1994) by two-factor ANOVA (area and trimester as factors). Individual mea- sures (ML and BW) by sex were used in the analysis as replicates within trimesters. Since the F test is remarkably robust to deviations from normality and violation of homogeneity of variances (Lindman, 1974), only the correlation between variances and means was tested as a criterium for the applicability of ANOVA. A Scheffé test was performed to evaluate differences between pairs. The recruitment season in each area was determined by a Recruitment Index (RI) computed to standardised sample sizes between months and between areas (to 100 squid by sampled month in each area). The computation of the RI assumes that recruits are animals with ML < T. The species threshold T was defined as the modal ML of the size frequency distribution, thus:
Rm = number of recruits observed in month m
R = ΣRm (all the recruits observed in a fishing season — from July to June next year)
R RI = m R
Sex ratios were estimated as the ratio of males to females (SR) in standardized sample sizes. Significant deviations from 1:1 were tested (each quarter within each area and for the whole sam- pling period and area) by Chi-square tests. The spawning season was determined by evaluating the monthly proportion of mature males (%matM) and females (%matF) in standardized sample sizes, and the average Gonadosomatic Index. The Gonadosomatic indices were calculated for maturing and mature males (GSIallM) and females (GSIallF), and for mature males (GSImatM) and mature females only (GSImatF), with 95% confidence interval as:
n ∑GWi i=1 GSI = n ∑()BWii− GW i=1
The minimum size at maturity was defined as the ML of the smallest mature squid (MLmim, mm), male (MLminM, mm) or female (MLminF, mm) found in each period. Maturity curves were fitted using a logistic function (Sparre et al., 1989) for the percentage of mature animals in length class l,
Pmax Pl = []1+ e−()abl+ 518 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Assuming Pmax = 1 it is possible to use a linear transformation of the same model, in the form:
⎛ Pl ⎞ ln⎜ ⎟ =+abl ⎝ PPmax − l ⎠
Intercepts and slopes of the linear model were compared for each sex between geographic area by the method in Campell and Madden (1990). The size at which 50% of males (ML50M, mm) or females (ML50F, mm) are found mature, was derived as the ratio of the parameters of the linear model above (ML50 = a/b), when a significant fit was obtained (least squares regression, P < 0.05). Length-weight relationships by trimester (power model: BW = a*MLb) were statistically com- pared for each area, by analyzing the similarity between intercepts and slopes (SlopeM and SlopeF) of the log transformed model, using the method suggested by Campell and Madden (1990). A selection of variables from those above, computed by trimester and grouped by location, to include in the multivariate analysis was achieved by the following procedure: (a) a preliminary analysis of variance (one-factor ANOVA) was performed on the scores of the 22 variables. Missing values were replaced by within location arithmetic mean and the correlation between variances and means evaluated, (b) when the separation by location was significant, i.e., when the variance was greater inter-location than intra-location, and no significant correlation between variances and means was detected, the variable was selected. The selected variables were subsequently standardised (mean subtracted from each variable and the result divided by the standard deviation) and a dis- criminant analysis performed using the routines implemented in the Statistica ver. 5 software.
RESULTS
FISHERIES.—In the Atlantic and Mediterranean L. vulgaris is caught mainly as a by- catch of the multi-species trawl fishery. The seasonal pattern of L. vulgaris landings is somewhat similar across the range with higher landings in autumn or winter (Fig. 1). As it is mainly a by-catch fishery and catches are usually landed, the seasonal pattern of landings produces a good picture of the seasonal pattern of abundance in each area. The main geographic differences are the low landings of squid in February in the Saharan Bank, and the high landings in late summer in northwest Portugal, contrasting with the very low landings or absence of squid in north France and the Greek Seas, in late spring and summer months. The total absence of squid landings in north France in summer may not indicate total absence of the species, but presence of specimens below recruitment size. In the Greek Seas the low landings in late spring and summer may reflect the low catches of other fishing gears, at the time when the trawl fishery is closed, on a population of mostly small squid. SIZE AND RECRUITMENT.—The range of mantle lengths (ML) sampled was between 29 and 640 mm and that of body weights (BW) between 1 and 2302 g. This species is sexu- ally dimorphic, with males attaining greater lengths and weights than females (Table 1). Averages for the whole area were similar between sexes, 160 mm and 180 g. Squid from the four geographic areas differ significantly in ML and BW (two-factor ANOVA ‘area’ P << 0.001), independently of season. Detailed analysis of differences between areas showed that: north France was not significantly different from the Saharan Bank (except for males ML), northwest Portugal was not significantly different from the Greek Seas (except for female BW), north France and Saharan Bank ML and BW of each MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 519
Figure 1. Monthly landings of Loligo vulgaris in the Atlantic and Mediterranean, average over 2 yrs (1997 and 1998) from all fishing gears. Absence of some monthly data corresponds to closed fishing seasons.
Table 1. Mean and maximum mantle length (ML, mm) and body weight (BW, g) of males and females recorded in each geographic area and in the whole area.
MWL B Amverage Meaximu Amverag Maximu N9France 200 434 238 1,49 N8W Portugal 104 403 150 1,26 Mkales S4aharan Ban 200 664 320 2,30 G5reek Seas 103 497 901,52 W6hole area 106 624 128 2,30
N7France 108 336 204 1,32 N0W Portugal 185 362 192 82 Fkemales S9aharan Ban 127 326 201 1,06 G0reek Seas 155 287 104 57 W2hole area 126 346 107 1,32 520 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Figure 2. Size frequency distributions of Loligo vulgaris in the studied geographic areas, from commercial and research samples: Saharan Bank = June 1993 to April 1994, 1258 specimens; north France, northwest Portugal = January 1997 to June 1999, respectively 1475 and 3040 specimens; Greek Seas = July 1997 to May 1999, 1042 specimens. (A) Overall size frequency distribution. (B) Seasonal length frequency distributions. sex were significantly higher than those from northwest Portugal and Greek Seas (Scheffé test, P < 0.05). The combined effect of both ‘area’ and ‘trimester’ was also significant (two-factor ANOVA ‘area’ and ‘trimester’: P << 0.001) indicating geographic differences in the seasonality of the population dynamics. The smallest individuals were found in the Greek Seas, probably as a consequence of the finer mesh size used by trawlers (commer- cial and research) in this area. The largest squid and the heaviest male were found on the Saharan Bank, while the heaviest female was found in north France. Some of the geographic differences in size and weight may be related to fishing gear selectivity, namely the lower size and weight limits. Other differences, such as the larger and heavier animals of the Saharan Bank in relation to those in northwest Portugal, clearly represent geographic differences. Modes of the length frequency distributions, which determine the fishery recruitment threshold, were the same in northwest Portugal, the Saharan Bank and the Greek Seas, 120 mm, although a smaller second mode (40 mm) appears in the Greek length distribu- tion. In north France the modal ML was larger, 170 mm ML (Fig. 2A). Seasonally, length frequency distributions varied by area. In north France small squid entered the fishery in autumn (4th trimester) and the modal size increased until spring (2nd trimester, Fig. 2B). The recruitment peak was in October (Fig. 3), coincident with MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 521
Figure 3. Monthly variation of the recruitment index (RI) in north France, northwest Portugal and Greek Seas. the first presence of squid in landings after the summer absence (see Fig. 1). In Greek Seas the modal size increased from summer to spring, when the length distribution be- comes clearly bimodal due to the recruitment of very small squid (Fig. 2B). The recruit- ment in Greek Seas was high at intervals throughout the year between April 1997 and April 1998 (Fig. 3). The lack of samples in summer months complicates the analysis of the general pattern. If the peaks in April and October indicate the visible ends of a con- tinuous period of recruitment, then it possibly extends from spring to autumn. In northwest Portugal the length structure was more complex (Fig. 2B), modal size remained constant from winter to summer, and an increase was only apparent from au- tumn to winter. Recruitment was more continuous throughout the year than in the above areas (Fig. 3). Peak recruitment was observed in the spring and summer of 1998, however the proportion of recruits was low in the summer of 1997 and in the spring of 1999. Secondary peaks in December 1997 and March 1999 were also observed. In the Saharan Bank the smaller squid were found in winter and spring along with the largest, and modal progression can be more easily followed from summer 1993 to winter 1994 (Fig. 2B). However, the stratified sampling by size categories makes the establishment of conclu- sions from size frequencies in this area more difficult. SEX RATIO.—In spite of the 1:1 sex ratio for this species in the area overall, in north France (χ2, SR = 0.48, P < 0.05) and northwest Portugal (χ2, SR = 0.43, P < 0.001) females were found in significantly greater numbers than males. The proportion of fe- males in north France was significantly higher only in winter 1998 (χ2, SR = 0.39, P < 0.001) and spring 1999 (χ2, SR = 0.38, P < 0.001). In northwest Portugal significant deviations from the 1:1 sex ratio showed higher inter annual variation. The proportion of females was the highest in the same periods as in north France (χ2, SR = 0.35, SR = 0.23, 522 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
and males (C and D).
Figure 4. Monthly percentage of mature squid and GSI in north France, northwest Portugal and Greek Seas, for females (A and B) MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 523
P < 0.001, respectively in winter 1998 and spring 1999), but it was also significantly higher in summer (χ2, SR = 0.42, P < 0.001) and autumn 1997 (χ2, SR = 0.42, P < 0.001). Higher numbers of females were also found on the Saharan Bank but the sex ratio for the whole sampling period was not significantly different from 1:1 (χ2, SR = 0.48, P > 0.05). Significantly more females than males were only observed in summer 1993 (χ2, SR = 0.42, P < 0.001). On the contrary more males than females were often found in the Greek Seas (χ2, SR = 0.57, P < 0.001). Seasonally, significant deviations from a sex ratio of 1:1 were verified in winter 1998 (χ2, SR = 0.58, P < 0.001), spring 1998 (χ2, SR = 0.81, P < 0.001), and winter 1999 (χ2, SR = 0.66, P < 0.001). MATURITY.—Except in north France, where half of the males and females were mature, the percentage of mature females was much lower (27–31%) than that of mature males (48–51%). Differences in the female spawning season, as indicated by the high propor- tion of mature females, were noted between areas (Fig. 4A). In north France, females spawned between November and April. Peaks in February 1998 and March 1999 in north France took place 1 mo later than in northwest Portugal to the south. However, in the latter area females spawned throughout the year and a secondary peak was present in late spring. In Greek Seas, as in north France, females spawned only in a restricted period of the year, from November until April or May. Female maturity peaks were later than any- where else, in April 1998, and 1999. The observation of the annual progression of female GSI (GSIallF) (Fig. 4C) reveals peaks in winter/early spring and troughs in early autumn in north France, northwest Portugal, and the Greek Seas and earlier maturation in north- west Portugal than in other areas. In northwest Portugal, where the population structure is more complex due to extended recruitment, the analysis of GSIallF, which was calcu- lated without immature specimens, more accurately describes the maturation pattern and the spawning season length (high values during a great part of the year), than does the proportion of mature females. In north France mature males (like females) appeared from November until March or April, with maturity peaks in March 1998 and January 1999 (Fig. 4C). In this area male GSI peaked earlier (Fig. 4D) than male maturity, indicating that big mature males die earliest and/or late maturing males have smaller GSI. In northwest Portugal two annual male maturity peaks were observed: October and March 1997/98 and December and April 1998/99 (Fig. 4C). The spring GSI peaks were more pronounced than the autumn ones (Fig. 4D). The mating season was extended, with mature males (like mature fe- males) collected throughout the year. In the Greek Seas mature males were observed between November and May, with peaks in February 1998 and March 1999 (Fig. 4C). High GSI values were found throughout the mating season (Fig. 4D). The highest proportion of mature males on the Saharan Bank was recorded in Novem- ber (1993) and that of females in January (1994). Within each area, male maturity peaked (%matM) earlier than female maturity. However, in northwest Portugal, the peak of male GSI occurred 2 to 4 mo after that of females. Geographic differences in the maturity pattern between north France and the Greek Seas were less evident in males than in females. The highest GSI of mature females was found in the Mediterranean (Greek Seas). In the Atlantic this index tended to decrease with decreasing latitude (Fig. 5) but the highest GSI of males was observed in northwest Portugal. SIZE AT MATURITY.—Overall (Atlantic and Mediterranean) estimated ML50 of females was 188 mm, higher than that of males, which was 168 mm. Table 2 presents minimum ML and ML at which 50% of the specimens are mature for each geographic area, and the 524 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Figure 5. Geographic variation of the gonadosomatic index calculated with only mature squid (GSImat). N = North and S = South. Marker = mean, ascending and descending lines = 95% confidence limits. areas significantly different in size at maturity by the statistical comparison of the matu- rity ogives. The MLmin was lower in northwest Portugal and the Greek Seas than in the other two areas and the ML50 increased with decreasing latitude in the Atlantic (both sexes). The ML50M was lower in the Mediterranean than in the Atlantic, and in the Atlantic it was lower in northwest Portugal, than in the other areas. The comparison of maturity ogives also showed that size at maturity of males is significantly different be- tween the Mediterranean and Atlantic, and in the Atlantic between north France and north- west Portugal. The ML50F is the highest on the Saharan Bank, but significant differences were only found between the north France female maturity ogive and the other Atlantic areas. Geographic differences were more pronounced in males due to the more complex pattern of size at maturity. In general, maturation seems to occur at smaller sizes in north- west Portugal, than in other areas of the Atlantic, and at similar sizes to those inside the Mediterranean. In spite of the greater maximum ML attained by males, MLmin and ML50 were generally higher in females, the only exception being that of the animals from the Saharan Bank, where females have smaller ML50’s than males. Seasonal variation in size at maturity was observed in all geographic areas (Fig. 6). In north France females matured at the smallest size in winter and males in autumn (earlier). In northwest Portugal female MLmin occurred in spring and that of males in winter (ear-
Table 2. Minimum size at maturity (MLmin) and size of 50% mature (ML50) males and females within each geographic area. Comparison of the maturity ogives (Mat ogives) between geographic areas: the areas listed, F (= N France), P (= NW Portugal), SB (= Saharan Bank) and G (= Greek Seas) correspond to those which are significantly different (P < 0.05) from each of the ones specified in the first column.
Msales Female MMLminM MsL50 MFaturity ogive MFLmin MsL50 Maturity ogive N0France 192 1G7 P0, 114 1B8 P, S N0W Portugal 861G6 F0, 122 1F8 S4aharan Bank 180 2G2 106 8 2F2 G5reek Seas 951B3 F9, P, S 191 1–8 MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 525
Figure 6. Seasonal variation in the size at maturity by geographic area. A = Minimum ML at maturity of females (MLminF), B = Minimum ML at maturity of males (MLminM), C = ML50 of females (ML50F). lier). On the Saharan Bank, female MLmin occurred in autumn, similar to that of males (not shown). Females in the Greek Seas matured at the smallest size in autumn and males in winter (later). The estimation of seasonal ML50 was not always significant, in particular for males. From the comparison between seasonal variation in the values of ML50F and the spawn- ing pattern of females, a single trend emerges: lower sizes at maturity were found in winter and spring (see Fig. 6B) coincident with the spawning periods in all areas but in the Greek Seas. Size at maturity was negatively correlated with the proportion of mature 526 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Table 3. Length-weight relationships by sex for each geographic area. Power model BW = a*MLb, intercepts (a) and slopes (b) estimated from the linearly transformed models.
Fsemales Male Prower model 2 NlPrower mode 2 N NWFrance B = 0.0008*ML2.38 01.95 8W0 B = 0.0019*ML2.20 04.95 67 NWW Portugal B = 0.0003*ML2.54 02.98 1W,44 B = 0.0006*ML2.41 02.97 1,15 SWaharan Bank B = 0.0003*ML2.56 05.98 5W6 B = 0.0004*ML2.47 08.97 52 GWreek Seas B = 0.0001*ML2.81 02.97 3W9 B = 0.0002*ML2.59 09.97 50 squid in the Atlantic areas (r = −0.99, P < 0.001 in north France; r = −0.62, P < 0.05 in northwest Portugal; r = −1, P < 0.001 in the Saharan Bank). This correlation was also negative in females from the Greek Seas, but the correlation coefficient was not signifi- cant (r = −0.68, P > 0.05). LENGTH-WEIGHT RELATIONSHIP.—The geographic variation in the slope of the length- weight relationships (Table 3) showed that growth in weight with length increased from the north to the south in the Atlantic and from the Atlantic to the Mediterranean. This was true for both males and females, which displayed negatively allometric growth in all areas of the range. These length-weight relationship coefficients were statistically com- pared between areas. Paired within sex tests, demonstrated that each area had coefficients significantly different from all others, except females in northwest Portugal compared to those in the Saharan Bank, therefore the increase in weight with length can not be mod- elled by a single equation for squid from the whole area. MULTIVARIATE COMPARISONS.—The preliminary analysis of variance performed on 22 variables obtained from the four sampling sites (trimester data series) indicated that only 10 (from those without significant correlation between variances and means) showed greater inter-group than intra-group variance: GSImatM, AvgMLM, MLmin, AvgBW, GSIallM, AvgML, MLminF, ML50F, AvgBWF and SR (in decreasing order of between group variation). These variables were then subjected to a Linear Discriminant Analysis to determine whether any significant difference could be found between sites. Significant overall discrimination was found between geographic areas (Wilks’ Lambda = 0.01186, P < 0.0001), and three discriminant functions (axis) were estimated, all sig- nificant (Chi-square, P < 0.05). The most clear and significant discrimination was pos- sible by the first discriminant function (axis 1 where 62% of the variance is explained) for squid from northwest Portugal (high positive mean of the canonical variables), Saharan Bank (high negative mean), and from north France and the Greek Seas combined (Fig. 7). This axis can be interpreted as a size at maturity and GSI of mature males function, with higher axis-variable correlation of MinML, MinMLF, and ML50F (negative correlation), and GSImatM (positive correlation). Thus the higher the size at maturity and the lower the GSImatM by trimester, the less likely that squid belong to northwest Portugal, as well as the lower the size at maturity and the higher the GSImatM, the less likely that squid are from the Saharan Bank. North France and the Greek Seas populations show small varia- tion regarding those variables. On the other hand, north France (high positive mean of the canonical variables) and the Greek Seas (high negative mean) are separated along the second axis (which explains 23% of the variance). The second axis can be interpreted as growth (size and weight) function, with higher correlation of the variables AvgML, AvgBWF, AvgMLM, and AvgBW (positive correlation). Thus, the higher the average size and weight by trimester the less MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 527
Figure 7. Plot of the canonical scores of the four groups of samples representing squid from north France, northwest Portugal, the Saharan Bank and the Greek Seas (results of the linear discriminant analysis). (a) axis 1 vs axis 2, (b) axis 2 vs axis 3, * - group centroids. likely that squid are from the Greek Seas, as well as the lower the average size and weight the less likely that squid belong to north France. Between northwest Portugal and the Saharan Bank there is smaller variation in what concerns average body size and weight. Finally, the Saharan Bank is separated from the other areas along the third axis (which explains 15% of the variance). The third axis can be interpreted as the GSI function, with higher correlation of variables GSIallM and GSImatM (positive correlation), indicating that the higher those variables the less likely that squid belong to Saharan Bank. Overall, the differences between areas were all significant (P < 0.05), with the variables related to size at maturity and male GSI displaying the strongest discriminant power, followed by the variables related to average size and weight. WATER TEMPERATURE REGIMES.—In north France the surface water temperatures are colder. During the study period this was on average 4°C less than in northwest Portugal and 9°C less than on the Saharan Bank (Fig. 8). Minimum and average SST’s in the 528 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Figure 8. SST range (line) and average (marker) in the sampling period in each area (Saharan Bank = June 1993 to May 1994, other areas = July 1997 to June 1999).
Greek Seas were similar to those of northwest Portugal, but in Greece the maximum temperatures were much higher in summer (up to more than 6°C). Average monthly SST varies by 8°C in N France. This variation decreases with latitude: 6°C in northwest Por- tugal and only 4°C on the Saharan Bank. The variation in average monthly SST in the Greek Seas (12°C) is higher than in the Atlantic areas. Most of the biological variables analysed appear to have cycles similar and out-of- phase with the temperature cycles associated to seasons. One exception was the RI, which increases with increasing SST, possibly as an indication of better juvenile development conditions during the warmer season.
DISCUSSION
BROAD-SCALE PATTERNS AND GEOGRAPHIC VARIATION.—Seasonal patterns of abundance inferred from seasonal landing patterns indicate the existence of some geographic differ- ences related to population dynamics. In north France landings abruptly rise from Sep- tember to October, continue to increase until March and drop again sharply until May. The species is not landed during summer. This pattern clearly illustrates a population of small juveniles (pre-recruits) growing during summer, fully recruiting by autumn, then growing, maturing, and finally dying after spawning in winter/early spring. It is well known, from egg mass recovery, that at least some spawning takes place in the English Channel. Thus in summer, the juvenile population born from that, must be made up of individuals too small to be recruited to the fishery. Research surveys confirm that pre- recruits are present in coastal waters in the eastern part of the English Channel in summer (Robin et. al., 1998). On the other hand, easterly migrations can also contribute to the sudden absence of L. vulgaris in the English Channel in May–June. According to Tinbergen and Verwey (1945), L. vulgaris undergo reproductive migrations in spring, entering the North Sea along the Belgian, Dutch, northwest German, and Danish coasts, where they appear only in late summer. The rise in catches from September to October can also be due to the behavior of the fishing fleet, which moves eastward in autumn. However, the possibility that some squid migrate from the Bay of Biscay or from more southern areas (Northwest Portugal and Spain) to the English Channel to be recruited there, can not be excluded. MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 529
The population dynamics in the Greek Seas appears to be similar to that of north France. Higher landings are observed in autumn, composed mainly of small squid. Although landings decrease thereafter, modal length and GSI increase until spring, and all spawn- ers disappear from catches in May or June. The spawning season is restricted to a rela- tively short period (November–May), lasting just 1 or 2 mo more than in north France. The fine mesh size used by trawlers in Greece enables catches of very small squid only a few months old (from the autumn spawning) as early as May. In north France and Greek Seas some differences were observed in the length of the recruitment and spawning sea- sons, but no significant differences in inter-annual variation were detected. The population structure of L. vulgaris in northwest Portugal is more complex. Re- cruitment generally takes place throughout the year. In 1998, there was a main recruit- ment season between May and August and several other peaks in autumn and winter, showing high inter-annual variation. Spawning animals are also found every month with two maturity peaks (proportion of mature and GSI) observed in both sexes. Inter-annual variation in the spawning and recruitment seasonal trends seems to be common in L. vulgaris from Portuguese waters. Coelho et al. (1994) and Moreno et al. (1994) reported the same for 1990 to 1992. The extensive spawning season and some horizontal migra- tions are the factors most likely to contribute to the complex population structure ob- served in northwest Portugal. An indication of horizontal migration is the occurrence of late winter/early spring recruitment peaks locally unmatched by previous spawning peaks. A late summer spawning peak on the south coast, reported by Bettencourt et al.(1996), could result in a northwest coast recruitment peak. The spawning and recruitment trends in the Saharan Bank were not analysed in detail, as available data is not contemporaneous with data from the other areas. Raya et al. (1999) described the trends, indicating that spawning occurs throughout the year, but mainly from November until January, with a main recruitment season from June to September. Secondary spawning peaks in May and recruitment peaks in November-December occur in some years. These population features and a high inter-annual variability result in a complex population structure similar to what is found in northwest Portugal. Other studies undertaken in several localities across the distribution range of L. vul- garis also show geographic variability in the seasonality of spawning. A restricted spawning period was observed in the North Sea (Tinbergen and Verwey, 1945). Spawning through- out the year was reported further south in the eastern Atlantic, from the northwest Span- ish coast to the western Sahara (Baddyr, 1988; Coelho et al., 1994; Guerra and Rocha, 1994; Moreno et al., 1994; Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996; Villa et al., 1997). Mangold-Wirz (1963) and Worms (1983) also observed year round spawn- ing in the western Mediterranean, different from the restricted period in the eastern Medi- terranean (present study). Geographic differences in the spawning seasons reported in the literature (Tinbergen and Verwey, 1945; Mangold-Wirz, 1963; Worms, 1983; Bravo de Laguna, 1988; Coelho et al., 1994; Guerra and Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996) and observed in the present study, reveal a clear latitudinal/longitudinal trend. In the Atlantic, only one spawning peak was observed from the North Sea to the north- west Spanish coast, and two peaks were observed towards the south, from northwest Portugal to the Saharan Bank. In the Mediterranean, two spawning peaks were observed in western areas, but only one peak in eastern waters. The timing of the spawning peaks is also different: spawning peaks earlier in the south than in the north in Atlantic waters and earlier in all the Atlantic areas than in the Mediterranean. 530 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
Geographic differences in the sex ratio between Atlantic and Mediterranean areas were found. In north France and northwest Portugal more females than males were generally found specially during the main spawning season, suggesting that males disappear first from the fishery. Since mating takes place before spawning, it is possible that some males die prior to the main spawning event of the females. However, the opposite occurs in the Greek Seas, where males outnumber females around the year. These observations sug- gest geographic differences in population dynamics. In addition, it is possible that some of the differences found may be the result of inappropriate sampling by the commercial fishery. Presently we do not have sufficient information on migratory movements, but alterations in sex ratio may reflect differential migratory strategies between sexes. Geographic differences were also observed in the mean and maximum ML and BW of specimens. Fishing gear selectivity may account for some of these differences, namely lower mean ML and BW in the Greek Seas where the small sampling mesh size allows catches of very small squid. Differences and similarities between Atlantic areas in mean ML and BW most likely reflect a combination of geographic differences in the popula- tion structure, and differential growth rates. Comparison of the growth rates estimated for other areas (Natsukari and Komine, 1992; Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996), support the hypothesis that L. vulgaris grow at higher rates in lower latitudes. The growth in weight with length increased from north to south, in the Atlantic and from the Atlantic to the Mediterranean. In agreement with this, the slopes of the length- weight relationships determined in squid from Northwest Spanish (Guerra and Rocha, 1994) and south Portuguese waters (Coelho et al., 1994), are similar to the ones estimated for squid in northwest Portugal. The highest GSI (maturing and mature) was found in the Mediterranean, and decreas- ing GSI was shown from north to south in the Atlantic. These differences are not related to the relative proportions of maturing or mature squid between areas but reflect a higher reproductive investment in relation to body growth in the Greek Seas and north France. On the other hand, GSI values of mature males do not follow that trend, since the highest is found in northwest Portugal. In this area high male GSI is more related to the very small minimum size at maturity and ML50. Across its geographic distribution L. vulgaris males mature at a lower minimum size than females (e.g., Mangold-Wirz, 1963; Baddyr, 1991; Coelho et al., 1994; Guerra and Rocha, 1994; Moreno et al., 1994; present study). Age studies confirm that in fact, males mature earlier in life than females, and that small mature squid are younger than large mature squid (Rocha, 1994; Arkhipkin, 1995; Bettencourt et al., 1996; Moreno et al., 1996). Females show smaller ML50’s than males in the Saharan Bank. However, in this area there were two male size modes at maturity (which biases the estimation of ML50), the first lower than that of females (Raya et al., 1999). The size at maturity of each sex shows great geographic variation and can be a reflex either of differences in growth or maturity rates. The minimum sizes at maturity observed in our analysis and earlier stud- ies in other areas (Coelho et al., 1994; Guerra and Rocha, 1994; Rocha, 1994; Bettencourt et al., 1996) support the hypothesis that Atlantic L. vulgaris mature at a smaller size in northwest Portugal. A decreasing tendency was generally detected from north France through northwest Spain to northwest Portugal and an increase from this area through south Portugal to the Saharan Bank. The ML50 of females was similar in north France, northwest Spain and northwest Portugal, and was higher in south Portugal and the Sa- MORENO ET AL.: BIOLOGICAL DIVERSITY IN LOLIGO VULGARIS 531 haran Bank. Minimum age at maturity was lower in northwest Portugal (Moreno et al., 1996) than on the Saharan shelf (Arkhipkin, 1995). In most cases lower size at maturity was observed during the main spawning seasons. In addition, there was a significant negative correlation between the trends of proportion mature and size at maturity. It seems that squids are induced to mature and spawn in a given period of the year, independent of size and age (with a minimum threshold). This is particularly evident in males, which can be found very young in mating condition. It seems also that the main factors inducing early maturation are exogenous, although matu- ration may be primarily regulated by endogenous stimuli. Studies on L. vulgaris reynaudii in South Africa, also showed that size at maturity is highly variable between geographic areas and times of the year (Augustin et al., 1992). BIOLOGICAL AND ENVIRONMENTAL VARIATION.—Between the areas analysed, there are im- portant environmental differences related to latitude, one of which is the water tempera- ture regime. The univariate and multivariate analysis indicated that squid were signifi- cantly different between areas, in particular with respect to size at maturity, male GSI and average body size and weight by trimester. Some of these differences may be a combined effect of temperature in growth and maturation rates. Growth at different temperatures can result in squid of markedly different size at age, introducing a high degree of variabil- ity in growth-related parameters (Carvalho and Nigmatullin, 1998), namely in more com- plex population dynamics. Maturation rate is also known to be very responsive to changes in temperature (Jackson et al., 1997). On the other hand, similarities were also observed between areas located at distinct latitudes and subject to different mean water tempera- ture (northwest Portugal and the Saharan Bank or north France and the Greek Seas), so other environmental factors must equally play an important role. Northwest Portugal and the Saharan Bank are located within an area characterized by the upwelling of cold sub-surface waters during most of the year. Consequently, the sea- sonal productivity cycle, closely related to the upwelling events, supports high zooplank- ton biomass for a long period (Wooster et al., 1976). The main biological similarities between L. vulgaris from northwest Portugal and the Saharan Bank: seasonality and long duration of mating, spawning, and recruitment seasons, are probably related to parallels in productivity regimes. Moreover, the seasonal productivity cycle is greatly affected by irregular temporal and local processes (Wooster et al., 1976), which likely accounts for the high inter-annual variability in the spawning and recruitment peaks within the two areas. The shorter spawning and recruitment periods found in north France and the Greek Seas may also reflect life-cycle strategies related to productivity patterns, since in these areas, zooplankton abundance is high during a short period of the year. Furthermore, the seasonality of mating, spawning and recruitment indicate that the early growth of most squid occurs during the short period of highest food availability, which is from June to August in the English Channel (Robinson et al., 1986) and July to October in the Aegean Sea (Siokou-Frangou, 1996). On a broad scale the four areas present differences and similarities concerning produc- tivity cycles and temperature regimes and this environmental variation may account for the biological differences and similarities observed between areas. 532 BULLETIN OF MARINE SCIENCE, VOL. 71, NO. 1, 2002
CONLUSION
It is clear that L. vulgaris has a high degree of biological variation across its geographic distribution. Most of the biological indices analysed showed a geographic trend implying species adaptation to large-scale environmental geographic trends. Squid living at differ- ent water temperature regimes evidenced geographic variability in reproductive and growth-related parameters. Squid living in areas which differ in the productivity cycles showed distinct spawning/recruitment patterns and consequent population complexity (north France~Greek Seas vs northwest Portugal~Saharan Bank). We consider that this collection of biological parameters across a range of fishing grounds is a step towards more extensive comparisons of life-traits similar to what has been done in Teleost fishes (e.g., Rochet, 1998; Cornillon and Rochet, 1999). More in-depth studies relating life- history strategies to environmental conditions are desirable to achieve a better under- standing of the population dynamics and provide adequate background for the establish- ment of conservation regulation.
ACKNOWLEDGMENTS
We would like to express our gratitude to A. Kapantagakis and E. Pallikara for providing Greek fisheries data, P. Koulouri, E. Hatziyanni, K. Sevastou, and A. Chatzyspirou for technical assis- tance (IMBC, Greece); Dr. D. Vafidis (NAGREF, Greece) and P. Mendonça (IPIMAR, Portugal) for assistance with sampling; and M. Azevedo (IPIMAR, Portugal) for statistical advise. This manu- script benefited from the scientific discussions during the CEPHVAR project meetings, for which we thank project colleagues, notably Prof. P. Boyle and Dr. G. Pierce. This work was partially funded by the Commission of the European Communities (FAIR-CT96-1520).
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ADDRESSES: (A.M., J.P., M.M.C.) Instituto de Investigação das Pescas e do Mar (IPIMAR), Algés, 1449-006 Lisboa, Portugal. E-mail: (A.M.)