Environmental Biology of Fishes 67: 191–201, 2003. © 2003 Kluwer Academic Publishers. Printed in the Netherlands.
Seasonal ichthyodiversity and growth patterns of juvenile flatfish on a nursery ground in the Southern Bight of the North Sea (France) Rachid Amara Universit´e du Littoral Cˆote d’Opale, UMR 8013 ELICO CNRS, Avenue Foch, 62930 Wimereux, France (e-mail:
[email protected]) Received 24 November 2002
Accepted 25 May 2003
Key words: flatfish nursery, demersal fish composition, juvenile, growth pattern Synopsis The demersal fish community on a flatfish nursery ground, of the Southern Bight of the North Sea, was sampled monthly between May 1998 and 1999. The studied coastal area is a multispecific nursery area. Although 32 fish species were caught, only nine species had a major influence on the variation in total densities through the year and can be considered as key species. Juvenile sole and plaice exhibited similar seasonal growth patterns with rapid growth during late spring and summer, a growth arrest during autumn and winter and a restart of growth in March. Comparisons of observed growth in length with predicted maximal growth under optimal food conditions suggested that during the summer, growth of 0-group sole and plaice was only determined by prevailing mean water temperature. During autumn and winter, while growth in length of sole followed model predictions, observed length of plaice was less than model predictions, suggesting growth limitation. Analyses of the factors that may be responsible for differences between observed and expected length growth indicated that autumn and winter growth arrest of plaice was not only related to low winter water temperature. It is suggested that for visual feeders such as plaice, the interaction of decreasing food availability and day length during autumn and winter can reduce the access to food resource and therefore feeding success and growth. Introduction Use of shallow marine coastal zones and estuaries as nursery areas is an important phase of the life history of many marine organisms, including many commercially valuable species. The temporal structure of species communities in these areas is often the result of seasonal settling or consecutive migration waves of young stages. The shallow marine coastal zones of the Eastern Channel and the North Sea provide important nursery habitat for juvenile flatfish. In these areas, juvenile flatfish generally play a key role in structuring the inshore community (Riou et al. 2001, Beyst et al. 2001). For flatfish, there is a general consensus that yearclass strength is determined primarily in the larval or early post-settlement stage (Leggett & Deblois 1994, Van der Veer et al. 2000). However, numerous studies suggest that processes operating during the nursery
ground phase are also important in regulating recruitment (Phil 1990, Van der Veer et al. 1994). A positive relationship between the recruitment and the available surface area of the nursery grounds was observed for some flatfish species (e.g. sole Rijnsdorp et al. 1992, plaice Van der Veer et al. 2000). This positive relationship raises the question as to whether nursery areas may ever become saturated with settling larvae and reaches their carrying capacity. Studies on juveniles flatfish concluded that growth rates of 0-group in the nursery were generally maximal and that food was constantly available and therefore never growth limiting (e.g. Van der Veer et al. 1991, Rogers 1994, Phil et al. 2000, Amara et al. 2001). However, in some areas there is evidence that food availability and quality is an important factor in determining growth, essentially for newly settled individuals (Van der Veer & Witte 1993, Berghahn et al. 1995, Amara & Paul 2003).
192 Although there was no evidence that growth of juvenile flatfish was density-dependent (Phil et al. 2000, Sogard et al. 2001), the use of the nursery ground by numerous other species may entail interspecific competition for food. Modin & Phil (1994) concluded that competitive effects generating density dependence in juvenile plaice are likely unimportant until extremely high densities are attained. Numerous recent studies have focused on the ecology of juvenile flatfish but, many of them have concentrated either on the recently settled fish or sampling was limited primarily to the spring–autumn period. Although growth has a direct influence on mortality rate and survival (Van der Veer et al. 1994), there is little quantitative information on winter juvenile growth. Few studies analysed the influence of both biotic (food availability and interspecific competition for food) and abiotic factors on the seasonal growth patterns of wild juvenile flatfish. Hence, our understanding of seasonal growth patterns in wild juvenile fish and the factors influencing or controlling their growth are still unclear. Sole, plaice and dab are the most common fish and the most abundant flatfish of the shallow waters of the North Sea (Daan et al. 1990). These species contribute to commercially important demersal fisheries and also play an important role in the structuring of the epibenthic community both as predators and prey.
The main objective of this paper is to analyse the seasonal growth patterns of 0 and 1-group sole, plaice and dab in order to test whether growth conditions on the nursery are optimal throughout the year. First, I describe the seasonal bentho-demersal species composition of the flatfish nursery ground in terms of diversity and abundance. This analysis is essential to understand the seasonal occupation of the nursery and the possible interactions between the flatfish and other species. The biotic and abiotic factors that may influence the seasonal growth patterns will be analysed and discussed later. Material and methods Study area The study area is located in the lower part of the Southern Bight of the North Sea near Gravelines (France) (Figure 1). The hydrodynamics of the area are strong. The studied area is a high productive region for primary and secondary production, as well as for fishing activities. It lies at the end of a continuous chain of nursery grounds for flatfish, which are scattered all along the eastern shore of the Southern Bight. The bottom of the subtidal zone studied consisted of fine
Figure 1. Study area with location of the demersal fish sampling stations and the benthos sampling station ‘B’.
193 sand (70–90%) and mud (1–12%) (Carpentier et al. 1997).
where Hmax is the maximum value of H obtained when all species are equally abundant.
Sampling
Growth of juvenile flatfish
Demersal fish were collected monthly between May 1998 and 1999 (10 surveys), from six stations at around 5–10 m depth (Figure 1). Sampling was done with a 3-m beam trawl equipped with one tickler chain and fitted with a fine 20 mm mesh liner and a 6 mm cod-end liner. Fish were preserved in a 7% formaldehyde–sea water solution or in 95% ethanol (for later otolith analyses). In the laboratory, all fish were identified (except for goby species of the genus Pomatoschistus which were not distinguished) and counted to determine the density and to analyse fish community composition. The densities were standardized to a number of individuals per 1000 m2 . All fish individuals were measured to the nearest mm TL, without a correction for shrinkage. Data on benthos (density and biomass (ash free dry weight)) were obtained from the ‘station B’ during all seasons in 1998 and 1999 (Dewarumez unpubl. data). The sampling procedure is described in Amara et al. (2001). Water temperatures and salinity were measured on every sampling occasion at each station. These data were combined with bi-weekly measurements at the ‘station B’ (Dewarumez unpubl. data).
Three species of flatfish, sole, plaice and dab, were separated into age groups based on their length-frequency distribution and when necessary confirmed by otolith annual rings analysis. The growth in length was studied by analysing the mean length of the 0 and 1-groups fish at each sampling date. The 0-group is defined as metamorphosed individuals that have not experienced a new calendar year: on the January 1 they became 1-group. Growth conditions of juvenile plaice and sole were analysed by comparing observed increases in length of the population in the field with predicted maximum growth, using experimentally established growth models obtained under unlimited food supply describing maximal growth in relation to temperature. For plaice, we used the model developed by Fonds et al. (1992)
Data analyses The fish community was characterized using either Margalef’s index (D), which is a measure of species richness diversity D = (S − 1)/ loge N where ‘S’ is the number of species and ‘N’ is the total number of individuals, or the Shannon–Wiener diversity index (H )
H =−
S
pi · ln(pi)
i=1
where pi is the proportion of individuals in the i-th species. Distribution of individuals was measured by the uniformity or ‘evenness’ index. J = H /Hmax = H / loge S
L = 0.0136 · T1.5 − 6.10−9 · T6 where L is the predicted growth in length (mm d−1 ) and T is the mean water temperature (◦ C). This equation was obtained with wild-caught juvenile (5–15 cm) reared at temperatures ranging from 2◦ C to 22◦ C and fed with fresh mussel meat (Mytilus edulis). For sole, two growth models were used: the relationship between the mean water temperature (T, ◦ C) and the mean length (L, cm) developed by Fonds (1979). L = (0.14T + 0.036L − 1.2) where L is the predicted growth in length (cm month−1 ). This equation was obtained with wildcaught juvenile (1–15 cm) reared for over a year at temperatures ranging from 10◦ C to 20◦ C and fed daily on fresh mussel meat, M. edulis and occasionally on live lugworm, Arenicola marina. The second growth model (Irvin 1973 in Howell 1997) describes maximal growth in relation to temperature. L = 2.7T − 21.9 where L is the predicted growth in length (cm month−1 ). This relationship was obtained from hatchery reared juvenile sole reared at five temperatures
194 ranging from 11◦ C to 27◦ C and fed ad libitum on the oligochaete worm, Lumbricillus rivalis.
using the shallow coast as a nursery ground. Flatfish species were well represented with seven species (plaice, dab, flounder, sole, solenette, turbot and brill). There was seasonal variation in the density of bentho-demersal fish with highest values in summer (about 200 ind. 1000 m−2 ) and lowest in winter (about 30 ind. 1000 m−2 ) (Figure 2). The summer rise in density was due to the essential settlement of juvenile flatfish and the presence of sand gobies. Although occurring in all seasons, these species represented more than 86% of the total fish catch by number during summer. During autumn, callionyme dominated the catch, whereas plaice and lesser weever dominated spring catches. In winter, catches were dominated by sand gobies representing 62% of the total catch by number. Diversity index followed an opposite pattern with lowest values during summer and highest during winter
Results Ichthyodiversity and species composition A total of 10 954 fish belonging to 32 species was collected from 53 trawl samples (Table 1). Nine species were ‘resident’ species since they were present throughout the year and had a major influence on the variation in total densities throughout the year and therefore can be considered as key species (Table 1). All other species were recorded ‘seasonally’ or ‘occasionally’. Most of the sampled fish were juveniles, many with an offshore distribution as adults,
Table 1. Occurrence and densities (no. 1000 m−2 ) of fish species collected at different season. Key species of the fish community are marked with an ∗ . Density (no, 1000 m2 )
Occurrence (%)
Raja clavata Scyliorhinus canicula Petromyzon marinus Engraulis encrasicolus Sprattus sprattus Clupea harengus Osmerus eperlenus Enchelyopus cimbrius Ciliata mustela Triglops murrayi Trisopterus luscus∗ Merlangius merlangus Gadus morhua Syngnathus acus Trigla lucerna Agonus cataphractus∗ Dicentrarchus labrax Chelon labrosus Pholis gunellus Echiichthys vipera∗ Parablennius gattorugine Hyperoplus lanceolatus Callionymus lyra∗ Pomataschistus spp.∗ Scophthalmus maximus Scophthalmus rhombus Limanda limanda∗ Pleuronectes platessa∗ Platichthys flesus∗ Solea solea∗ Buglossidium luteum
Thornback ray Lesser spotted dogfish Lamprey European anchovy Sprat Herring Smelt Four-bearded rockling Five-bearded rockling Moustache sculpin Bib Whiting Cod Greater pipefish Tub gurnard Pogge Bass Thick lipped mullet Butterfish Lesser weever Tompot blenny Sand eel Dragonnet Sand goby family Turbot Brill Dab Plaice Flounder Sole Solenette
Summer
Autumn
Winter
Spring
Summer
Autumn
Winter
Spring
6.67 0.00 0.00 0.00 51.67 0.00 0.00 0.00 0.00 0.00 66.67 30.00 0.00 28.33 41.67 60.00 0.00 0.00 0.00 28.33 0.00 15.00 41.67 85.00 15.00 0.00 93.33 100.00 38.33 91.67 0.00
0.00 10.00 0.00 20.00 60.00 0.00 0.00 0.00 0.00 20.00 30.00 30.00 50.00 50.00 60.00 40.00 20.00 0.00 10.00 40.00 0.00 30.00 80.00 100.00 0.00 20.00 70.00 90.00 20.00 90.00 0.00
8.33 16.67 16.67 0.00 75.00 33.33 0.00 16.67 33.33 16.67 58.33 83.33 66.67 16.67 0.00 25.00 66.67 25.00 25.00 33.33 0.00 58.33 75.00 100.00 0.00 0.00 66.67 83.33 8.33 58.33 0.00
22.22 0.00 0.00 0.00 16.67 27.78 5.56 5.56 50.00 0.00 83.33 83.33 16.67 33.33 38.89 44.44 38.89 5.56 0.00 83.33 11.11 44.44 88.89 88.89 0.00 11.11 66.67 100.00 38.89 88.89 22.22
0.02 0.00 0.00 0.00 4.47 0.00 0.00 0.00 0.00 0.00 5.83 0.29 0.00 0.27 0.26 2.87 0.00 0.00 0.00 4.28 0.00 0.07 2.23 94.10 0.06 0.00 10.18 27.61 0.30 11.98 0.00
0.00 0.04 0.00 0.35 2.55 0.00 0.00 0.00 0.00 0.07 2.26 0.27 0.67 0.29 1.53 0.61 0.17 0.00 0.03 0.55 0.00 0.24 14.27 38.93 0.00 0.17 3.68 8.49 0.07 4.50 0.00
0.03 0.06 0.05 0.00 1.20 0.16 0.00 0.12 0.35 0.08 0.71 1.79 0.56 0.25 0.00 0.10 0.99 0.11 0.11 0.65 0.00 0.28 1.62 14.83 0.00 0.00 0.60 2.89 0.02 1.71 0.00
0.13 0.00 0.00 0.00 0.78 0.11 0.02 0.02 0.64 0.00 1.63 4.08 0.15 0.15 0.39 0.56 0.36 0.02 0.00 10.55 0.04 0.56 4.79 5.52 0.00 0.04 2.50 8.33 0.15 4.81 0.14
195 and spring (Figure 2). The number of species during summer was 16 and 24–25 during winter and spring (Table 1). Flatfish population dynamics
Figure 2. Monthly fluctuations in (a) the density (no. 1000 m−2 ), (b) species richness (D), (c) Shannon diversity index (H ) and (d) evenness (J).
Sole, dab and plaice were the most abundant flatfish species and represented 29% of the total fish catch. Juveniles belonging to the 0-group constituted the majority of the flatfish catches. Settlement of juvenile plaice, sole and dab was observed from the first sampling at the beginning of May. The highest densities of 0-group plaice were observed at the beginning of the sampling period (36 ind. 1000 m−2 in May) and during July for 0-group sole and dab (18 and 15 ind. 1000 m−2 , respectively). After the peak of settlement, a gradual decline of densities occurred. During autumn and winter, densities of juvenile sole, plaice and dab remained low (about 3–5 ind. 1000 m−2 ) and increased again in late spring. Juvenile sole and plaice exhibited similar seasonal growth patterns with rapid growth during late spring and summer, a growth arrest during autumn and winter and a restart of growth in March (Figure 3). At the end of the growing season (September), sole and plaice reached a total length of 117 and 110 mm, respectively. For dab, the growth pattern was different; fish length increasing continuously over the year. The rates of increase in length during summer, winter and spring were respectively 0.68, −0.07 and 0.44 mm day−1 for sole; 0.59, 0.09 and 0.64 mm day−1 for plaice and 0.21, 0.19 and 0.17 mm day−1 for dab. Although some differences occurred between observed length in the field and maximum predicted length for sole (Figure 3), the seasonal growth patterns followed the model’s predictions. It appeared that growth of the 0 and 1-group sole was maximal and was only conditioned by prevailing water temperature. For plaice, there was high similarity between observed and simulated lengths during summer, suggesting that growth was not food-limiting during this period. However, differences occurred during autumn and winter when the growth model predicted continuous growth, whereas a complete cessation of growth was observed in the field. Considering the hypothesis that the maximum predicted growth is only determined by prevailing mean water temperature, a difference between the two patterns implied the existence of an underlying process of growth limitation. Growth of juvenile flatfishes can be affected by a number of
196 (a)
(b)
(c)
Figure 3. Mean total length (open circles) ±1 standard deviation (mm) of 0- and 1-group (a) sole, (b) plaice and (c) dab. For sole and plaice, growths in length were compared with simulated maximal growth according to growth models obtained under optimal food conditions in the laboratory (see text). For sole Fond’s (1979) model (solid squares) and Irvin’s (1973) model (open squares); for plaice Fonds et al. (1992) model (solid squares).
factors in the nursery habitat. Salinity, which did not vary significantly during the year (about 34.5%) due to the high hydrodynamics, is not likely to affect the growth pattern. Temperature, day length and benthic fauna (food availability), the main factors affecting fish growth, were analysed (Figure 4).
As in other temperate areas, temperature showed a classical seasonal pattern. From May, water temperature increased to reach a maximum in late July–early August (about 20◦ C) and then decreased to a minimum of about 5–6◦ C in late January/early February (Figure 4). Day length duration at the latitude of our
197
Figure 4. Seasonal fluctuations of (a) water temperature, (b) day length (h) and (c) density (straight line, no. m−2 ) and biomass (bar charts, g m−2 , ash free dry weight) of the benthic fauna in the studied area in 1998 and 1999.
study area also showed a seasonal pattern: it was maximum in summer (about 16 h) and minimum in winter (about 8 h). The study area can be classified as a rich benthic fauna, which is dominated by annelids, molluscs and crustaceans (Dewarumez unpubl. data),
constituting the major diet of juvenile flatfish in this area (Amara et al. 2001). The density and biomass of the benthic fauna were maximum in summer and minimum in winter and spring (Figure 4).
198 Discussion and conclusion The accuracy of the data presented in this paper depends, to a large extent, on the effectiveness with which the juvenile populations are sampled by the beam trawl. The efficiency of the 3 m beam trawl used in this study is discussed in Amara et al. (2001) and it is assumed that juvenile flatfish are effectively sampled in our study. Another factor that can affect the results is size-selective migration. Unlike in other areas where winter distributions are notably deeper than those in summer or autumn (Gibson 1997), juvenile flatfish distributions in the studied area are coastal all year round (Riou et al. 2001, Amara unpubl. data). These authors found that below a depth of 20 m, there were almost no juveniles and, the higher densities were found in less than 8-m depth for sole and less than 12-m depth for plaice. This stability in the juvenile distribution can be explained by the hydrodynamic properties of the area. Due to strong tidal currents and moderate depths (
