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Changes in the spatial distribution of North Sea plaice (Pleuronectes platessa) and implications for fisheries management
Journal of Sea Research 57 (2007) 187 – 197 www.elsevier.com/locate/seares
Changes in the spatial distribution of North Sea plaice (Pleuronectes platessa) and implications for fisheries management O.A. van Keeken ⁎, M. van Hoppe, R.E. Grift, A.D. Rijnsdorp Wageningen IMARES, Institute for Marine Resources and Ecosystem Studies, P.O. Box 68, 1970 AB IJmuiden, The Netherlands Received 29 October 2005; accepted 25 September 2006 Available online 28 October 2006
Abstract To protect the main nursery area of plaice, an area called the ‘Plaice Box’ was closed to trawl fisheries with large vessels in 1989, with the expectation that recruitment, yield and spawning stock biomass would increase. However, since then the plaice population has declined and the rate of discarding outside the Plaice Box has increased, suggesting an offshore shift in spatial distribution of juvenile plaice. Using research vessel survey data collected since 1970, the change in distribution of juvenile age groups was analysed in relation to the distance to the coast. Further, a comparison of the distribution of different length classes of plaice between three historic periods was made (1902–1909; 1983–1987; 1999–2003). A shift towards deeper water of largersized plaice (20–39 cm) is apparent already before the 1980s and may be related to the decrease in the number of competitors or predators. An offshore shift in the distribution of young plaice occurred in the 1990s most likely in response to higher water temperatures that may have exceeded the maximum tolerance range or increased the food requirements above the available food resources. A decrease in competition with larger plaice offshore, possibly in combination with increased inshore predation by cormorants and seals, may also have played a role. The offshore shift in distribution has reduced the effectiveness of the Plaice Box as a technical measure to protect the under-sized plaice from discarding, since an increased proportion of the population of undersized plaice is moving to the more heavily exploited offshore areas. © 2006 Elsevier B.V. All rights reserved. Keywords: Plaice; Spatial distribution; North Sea; Plaice Box; Fisheries management
1. Introduction In the North Sea, plaice is exploited in a mixed fishery for flatfish. Due to the small mesh size used in the fishery to catch sole, large numbers of undersized plaice are caught and discarded (Rijnsdorp and Millner, 1996; Van Beek, 1998). In order to reduce discard mortality, the main distribution area of undersized plaice was closed to fishing in 1989 for vessels with an engine ⁎ Corresponding author. E-mail address: [email protected] (O.A. van Keeken). 1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2006.09.002
power of more than 300 hp (221 KW) (ICES, 1994, 1999). This area, the ‘Plaice Box’, was based on the spatial segregation between juvenile and adult fish (ICES, 1987, 1994). Plaice spawn in offshore waters, whereas the juveniles settle in the shallow waters of estuaries and sandy beaches. During ontogeny, plaice gradually leave the shallow coastal waters and move into deeper waters further offshore (Wimpenny, 1953; Rijnsdorp and Van Beek, 1991). In contrast to expectations, the recruitment, yield and spawning stock biomass of plaice decreased since the introduction of the Plaice Box (ICES, 1999). The rate of
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discarding in the waters outside the Plaice Box has increased (ICES, 1999; Pastoors et al., 2000), and plaice have been discarded at smaller lengths outside the Plaice Box in recent years (own obs.), suggesting that a change in the distribution pattern of plaice may have occurred. The distribution pattern of plaice is the result of the interaction between behaviour through directed migrations and small-scale (dispersive) movements, and the effect of fishing. Migratory behaviour between summer feeding areas and winter spawning areas develops when plaice becomes sexually mature (De Veen, 1978; Rijnsdorp, 1989; Rijnsdorp and Pastoors, 1995; Gibson, 1997; Hunter et al., 2003). Small-scale movements will occur in the juvenile and adult phase. Such small-scale movements may be random (Beverton and Holt, 1957), for example as a result of foraging behaviour, may have a directed component, for example in the tidal migrations (Kuipers, 1973; Gibson et al., 2002) or, when related to the evasive behaviour, may be directed away from adverse environmental conditions such as extreme temperatures or low oxygen concentrations (Beverton and Holt, 1957; Berghahn et al., 1993; Gibson, 1994, 1997). Beverton and Holt (1957) described the offshore movement of plaice as a dispersion process, thus driven by random movements. Small-scale directed movements were described by Berghahn et al. (1993), who recorded a mass exodus of 0-group plaice from the tidal flats in response to temperature. Also, the autumn offshore migration from the shallow inshore waters and the spring inshore migration may reflect a response to temperature and feeding conditions (De Veen, 1978). Fish may further respond to predation risk by changing migration behaviour (Burrows and Gibson, 1995; Manderson et al., 2004). Offshore movement could also be an effect of changed feeding conditions, caused by the introduction of the Plaice Box, since fishing efforts shifted to the border of the Plaice Box after its closure. Bottom trawling may increase the availability of the benthos in terms of suitable food for plaice (De Veen, 1978; Rijnsdorp and Van Beek, 1991; Rijnsdorp and Vingerhoed, 2001). A change in the distribution of undersized plaice may have a large impact on the management of the fisheries. Insight into the extent of the changes in distribution and the likely causes is of paramount interest for the evaluation of the effectiveness of the current management of the Plaice Box. This paper focuses on the offshore movement of plaice from the nursery grounds along the continental coast. These nursery areas produce 90% of the recruitment of North Sea plaice (ICES, 1985; Van Beek et al., 1989). Changes in distribution are analysed
in relation to the distance to the continental coast, using research vessel survey data collected since 1970. Further, a comparison is made of the distribution of different length classes of plaice between three historic periods: 1902–1909, 1983–1987 and 1999–2003, and implications of the change in distribution for fisheries management are discussed. 2. Methods 2.1. Comparing spatial distribution between three historic periods The spatial distributions of different size classes of plaice were compared between three periods: 1902– 1909, 1983–1987, 1999–2003. The periods analysed differed with respect to several of the factors that may affect distribution, such as water temperature, productivity, predation risk and the level and distribution of fishing effort. 2.1.1. Data Third quarter data for 1902–1909 were available from two different surveys: RV ‘Huxley’ and RV ‘Wodan’. References to these data can be found in Rijnsdorp et al. (1996). RV ‘Huxley’ used either a 26.5 m otter trawl (OT90) or a 13 m beam trawl (BT13) (Table 1). Tow duration varied between 1 and 3 h at a towing speed of 2 nm h− 1. Fish were grouped into 10 cm length classes. RV ‘Wodan’ used a 26.5 m otter trawl similar to that of RV ‘Huxley’. Haul duration was generally 1–2 h at a towing speed of 2 nm h− 1. Fish were grouped into 5 cm length classes. Mesh size was 63 mm and 68 mm for beam trawl and otter trawl, respectively. Table 1 Details of the gears used during 1902–1909, 1983–1987 and 1999– 2003 BT13 1902– 1909 Haul duration (min) Codend mesh Tickler chains Towing speed Sweep Swept area (1000 m2 h− 1) Relative catch effiency
OT90 1902– 1909
BT14 1983– 1987
BT12 1983– 1987
BT8 1983–1987 1999–2003
60–180 60–180 10–40
10–40
30
63 0 2 13 50
68 0 2 17 60
85 8 5–5.5 14 140
85 8 5–5.5 12 120
40 8 4 8 60
0.85
1
2.3
2
1
Relative catch efficiency rates were standardized to swept area per hour with OT90/BT8.
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Third quarter data for 1983–1987 were available from research cruises conducted with chartered commercial beam trawl vessels (‘KW34’ and ‘KW36’) in the offshore areas, and the RV ‘ISIS’ in the southeastern North Sea. ‘KW34’ collected data in 1983, 1985 and 1986, while ‘KW36’ collected data in 1987. Both vessels used a 12 m beam trawl (BT12), except for 1983 when ‘KW34’ used a 14 m beam trawl (BT14). Haul duration was 30 min, but occasionally varied between 10–40 min. Towing speed varied between 5 and 5.5 nm h− 1 and mesh size was 85 mm. Data for 1999–2003 were available from the BTS survey conducted by RV ‘ISIS’ and RV ‘Tridens’, using an 8 m beam trawl (BT8). The BTS survey was carried out in August and September. RV ‘ISIS’ covered the eastern part, while RV ‘Tridens’ covered the western part of the southern North Sea. Haul duration was 30 min at a towing speed of 4 nm h− 1. Mesh size was 40 mm. 2.1.2. Data analysis The number per haul was converted into the mean number per hour and corrected for the area swept. The swept areas for each gear were scaled to the swept area of the OT90/BT8 (Table 1). Because the ‘Wodan’ data reported numbers per 10 cm length class, these length classes were used in the analysis for all surveys (20– 29 cm, 30–39 cm, 40–49 cm, 50 and larger), except for the smallest length class which was restricted to 15–19 cm to prevent a bias in catch rates due to the smaller mesh size used in 1983–1987 and 1999–2003. Average catch rates were calculated per square of 0.5° longitude × 1° latitude (ICES rectangles). As we are particularly interested in the offshore movement of the size classes from their nursery grounds, the shortest distance of each haul to the continental coast was calculated. In the final analysis only hauls east of 2°E were included, because in the areas west of this line, plaice may originate from the nursery grounds along the British east coast. Intra-specific competition was quantified with the index of mean crowding (Lloyd, 1967). The index of mean crowding gives the average number of individuals with which an individual shares its spatial unit. Following Rijnsdorp and Van Beek (1991), the ICES rectangle was used as spatial unit and mean crowding of length group b on length group a was calculated as: X xaid xbi i X ð1Þ b ma ¼ xai i
where bma is the index of mean crowding by length group b on length group a, and xai and xbi are the catch
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rate of length group a and b respectively in the ith spatial unit. 2.2. Modelling catch rates to distance from the coast The offshore movement of plaice was studied in more detail by analyzing the slope of the decline in numbers with increasing distance from the coast for the juvenile age groups 0, 1 and 2. 2.2.1. Data For this analysis data from the Sole Net Survey (SNS) were used. The survey was initiated in 1969 and samples 10 fixed transects (parallel or perpendicular to the coastline) along the Dutch, German and Danish coasts in September – October before the autumn migration (Fig. 1). The survey used a 6 m beam trawl with a cod-end of 40 mm stretched mesh. Haul duration was 15 min at a towing speed of 4 nm h− 1. To investigate yearly differences in catch rates to the shortest distance from the coast, two transects were chosen, which are perpendicular to the coast: 601 and 666, combining transect 606 and 660. Temperature data and growth indices were used in the analysis to investigate the effect on the distribution of plaice. Monthly mean temperatures were available from a coastal station at Den Helder (Van Aken, 2003).
Fig. 1. Map of the transects of sampling stations of the SNS survey. Transect 601 is situated perpendicular of the Danish coast, transect 666 combines transect 660 and 606 off the Dutch coast. The heavy lines indicate the location of the Plaice Box, a protected area along the continental coast between 53° and 57°N.
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was performed on the slope of the log catch rate against distance for individual years in relation to the growth index or the temperature index. 3. Results 3.1. Comparing historic periods
Fig. 2. Growth index for age-2 female plaice obtained from backcalculated mean length at age (top), and mean and maximum monthly water temperature (July–September) measured daily at a coastal station (Den Helder, The Netherlands).
A time series of juvenile growth rate, annual length increment of plaice of 15–25 cm, was available for the cohorts 1950– 1994 from otolith back-calculations of female plaice (Rijnsdorp and Van Leeuwen, 1996), which was updated with samples up to 2003. Fig. 2 shows the temperature and growth indices used in the analysis. 2.2.2. Data analysis Numbers per haul were converted into numbers at age per hour using age length keys. Distance from the coast was calculated as shortest distance to the coastline. Log-transformed catch-rates (number h− 1) were modelled using GLM (SAS Institute Inc., 1999): logðCr þ 1ÞfA þ D þ YC þ A⁎D þ Y ⁎D þ A⁎Y ⁎D
The well-known pattern of a gradual movement away from coastal waters was apparent in all three periods (Fig. 3). Closer inspection, however, indicated that similar-sized plaice have spread further away from the coast in recent time. The analysis of the distribution of the different size classes over depth corroborated the changes in distribution (Fig. 4). The change in depth distribution of the two smallest size classes was already apparent between 1902–1907 and 1983–1987, although the major shift occurred between 1983–1987 and 1999– 2003. In the larger size classes, the change occurred between 1902–1907 and 1983–1987. In the former period, plaice N 30 cm were mainly restricted to depths of b 60 m, while in the two later periods they were caught to a depth of 90 m. The index of intra-specific competition showed that the total mean crowding on the 15–19 cm and 20–29 cm length classes was highest in the first period and decreased for both classes over the two following periods (Fig. 5). Total mean crowding in the last period was more than a factor of two lower than in the first period for both length classes. Also for the 30–39 cm length class, the total mean crowding showed a steady decline over the three periods, whereas that for the 40– 49 cm length class showed an increasing trend. Total crowding on the length class N 50 cm was higher in 1983–1987 than in the other two periods. The contribution of the various size classes to the total mean crowding is illustrated in Fig. 6. The contribution of the 15–19 cm length class to the mean crowding on other length groups increased over the last two periods.
ð2Þ where Cr is the catch rate (numbers h− 1) in transect r, A is age group, D is distance from coast (km), YC is year class and Y is year. A, Y and YC are included as class variables and D as continuous variable. A type I analysis was used to test whether the parameters included in the model significantly contributed to the explained variance in catch rates. The interaction term D⁎Y examines whether the slope of the catch rates has changed with distance over time. To test whether growth or temperature had a significant effect on the distribution, regression analysis
3.2. Modelling catch rates to distance from the coast The catch rate of plaice decreased with increasing distance (D) from the coast, and the relationship differed between the age groups (A). Table 2 shows that the variable D + A⁎D explained 24.7% and 15.3% of the variance for area 601 and 666, respectively. Other important variables were age (A) and year class (YC). The total model, including the variables distance (D), age (A), year class (YC) and their first and second order interactions, explained 63.2% of the variance for transect 601 and 60.3% for transect 666. The significant
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Fig. 3. Catch rates (number h− 1) per ICES square for plaice of length group 15–19 cm (left) and 20–29 cm (right) in the period 1902–1909 (upper panels), 1983–1987 (middle panels) and 1999–2003 (lower panels). x indicates a zero catch rate, whereas the size of the dot reflects catch rates increasing from 0.01–0.9; 1–4.9; 5–14.9; 15–49.9 and N = 50 plaice h− 1.
interactions Y⁎D and A⁎Y⁎D indicated that the relationship between catch rate and distance changed over time, and differed for the various age groups. The slope of the relationship, estimated for 0-, 1- and 2-group in individual years, revealed that the slopes did not change gradually over time, but that they varied
without a trend until the mid 1990s and then increased (Fig. 7). The change in slope was particularly clear in area 601 off the Danish coast. In area 666 off the Dutch coast, the slopes of 0- and 1-group showed some high values in the mid 1990s but the change in time was less clear.
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Fig. 4. Relative catch rate (number h− 1) of 15–19 cm, 20–29 cm, 30–39 cm and 40–49 cm length groups over 5 m depth classes for each period. Catch rates are expressed relative to the mean catch rate over all depth bands.
The slopes of the relationship between abundance and distance from the coast were regressed to water temperature and growth index. Water temperature showed a significant effect for age 1, but not for age 0 or age 2, and explained 20% and 13% of the variance in the slope for transect 601 and 666, respectively. The growth index did not show a significant relationship explaining less than 1 – 9% of the variance in slopes. 4. Discussion The available survey data clearly indicate a change in the spatial distribution of plaice. In the first decades of the 20th century, high concentrations of small plaice were observed in shallow coastal waters (Wimpenny, 1953). Since the mid 1980s, a gradual offshore movement has taken place, and consistent with this offshore movement, the population of 1-group plaice has left the Dutch Wadden Sea almost completely since the late 1990s (Bolle, pers. comm., 2005). The change in distribution was particularly pronounced in the 20–29 cm and the 30–39 cm length classes and off the Danish coast, but less clear off the Dutch coast. The timing of the change in distribution differed between these length classes. The 20–29 cm length class extended its distribution to offshore waters between the mid 1980s and the late 1990s, whereas the 30–39 cm length class already extended its distribution before the mid 1980s. In the two recent time periods, the 30–39 cm length class comprised mainly adult plaice, as the length at first maturity is 20–24 cm in males and 30–35 cm in females. In 1900, however, this length class would have
comprised both juvenile and adult plaice, as the length at first maturity ranged between 30–37 cm in males and 32–43 cm in females (Rijnsdorp, 1989). This may imply that the decrease in the size at first maturation in conjunction with the onset of a seasonal migration between feeding and spawning areas may have resulted in a more homogeneous distribution of the 30–39 cm length class over the North Sea. Beverton and Holt (1957) described the offshore movement of young plaice in terms of diffusion. The decrease in the slope of the relationship of the log catch rates against distance in the 1990 implies that the dispersion rate has increased. Such an increase may be due to an increase in small-scale undirected movements or a directed response to temperature, food availability,
Fig. 5. Change in the mean crowding on length classes 15–19 cm, 20– 29 cm, 30–39 cm, 40–49 cm and N = 50 cm between time periods 1902–1909, 1983–1987, 1999–2003.
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Fig. 6. Contribution of each length class to the mean crowding on length classes 15–19 cm, 20–29 cm, 30–39 cm, 40–49 cm and N = 50 cm in time periods (a) 1902–1909; (b) 1983–1987; (c) 1999–2003.
intra- or inter-specific competitors, or predators (Fig. 8). The scatter plot of the slope of the log catch rates and distance with summer temperature showed a significant effect for 1-group in both transects, but not for 0-group. In the 1990s, when maximum mean monthly temperatures reached and exceeded 20 °C (Fig. 2), temperatures above which growth rates of 0-group start to decline (Fonds et al., 1992), maximum temperatures on the hottest days must have been even higher. Newly settled plaice showed a mass ‘exodus’ from the intertidal pools in the Wadden Sea when temperatures exceeded the critical level of 24 °C (Van der Veer and Bergman, 1986; Berghahn et al., 1993). As the optimal temperature decreases with fish size (Imsland et al., 1996; Jonassen et al., 1999), it can be expected that the habitat choice is, at least partly, related to the available temperature field. If, due to the recent increase, the summer temperature exceeds the optimal value, a shift of plaice to deeper and cooler water further offshore can be expected. Small-scale undirected movement may have increased in the 1990s in response to an increase in
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temperature, which may enhance the activity level of fish. An increase in summer temperature will increase the food requirements of plaice that may then exceed the available food resources for a larger part of the growing season (Teal, pers. comm., 2005). Small-scale undirected movement may also have increased in the 1990s in response to a reduction in the productivity of the coastal waters. In the western Wadden Sea, a decrease in primary production was observed between 1994 and 2003 from a level of about 1200 to 600 mg C m− 2 d− 1 (Cadée and Hegeman, 2002), although there is at present no indication of decreased benthic biomass in recent years (Beukema et al., 2002). Nevertheless, changes in the benthic production of certain components may have occurred. Macoma balthica recruitment and biomass have decreased in recent years probably due to the mismatch in the timing of reproduction in relation to larval food as well as an increased predation by Crangon crangon (Philippart et al., 2003). The slightly shallower slopes in the early 1980s, in particular in area 601, may be affected by the reduction of oxygen concentrations to values below 2 mg l− 1 that were observed in 1981–1983 in the inner German Bight between 7° and 8° East (Von Westernhagen et al., 1986). As only one hypoxia event was recorded in the 1990s (in 1994, OSPAR, 2000), hypoxia does not seem to have played a role in the changes in plaice distribution since the mid 1990s. The offshore movement may also have been affected by changes in predation risk. Shifts of 0-group flatfish, bringing them into shallower water during the night, may serve as an anti-predator strategy (Burrows et al., 1994). Gibson et al. (1998, 2002) showed that 0-group plaice avoided predation risk by feeding predominantly in areas with few fish predators. Burrows and Gibson (1995) showed changes in patterns and types of behaviour and reduced activity of tank-kept juvenile plaice with predator presence. Changes in predation risk will certainly have occurred during the last century. Fisheries caused a considerable decrease in the abundance of larger predatory fish species (Rice and Gislason, 1996; Daan et al., 2005), resulting in a lower predation risk in deeper offshore waters. On the other hand, plaice faced an increased predation risk in coastal waters in the 1990s from seals and piscivorous birds (mainly cormorants). The number of seals has decreased in the 20th century due to hunting and pollution, dropping to a minimum of about 4000 animals in the mid 1970s and again in 1989 after a virus outbreak, but has recovered to more than 20 000 animals in 2002 (Reijnders et al., 2003). The numbers of cormorants, known to feed on plaice and other flatfish (Leopold
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Table 2 Statistical evaluation of the influence of age (A), distance (D), year-class (YC) and year (Y) on the catch rates in transects 601 and 666 Transect
Source
SS
%
df
MS
F
p
601
A D YC A⁎D Y⁎D A⁎Y⁎D Explained Unexplained Total A D YC A⁎D Y⁎D A⁎Y⁎D Explained Unexplained Total
1861.1 371.3 907.5 1580.6 98.4 182.2 5001.0 2912.4 7913.4 2053.3 290.2 568.1 648.3 47.3 86.0 3693.3 2428.2 6121.5
23.5 4.7 11.5 20.0 1.2 2.3 63.2 36.8 100.0 33.5 4.7 9.3 10.6 0.8 1.4 60.3 39.7 100.0
4 1 36 4 1 4 50 1265
465.3 371.3 25.2 395.1 98.4 45.5 100.0 2.3
202.1 161.3 10.9 171.6 42.7 19.8
b.0001 b.0001 b.0001 b.0001 b.0001 b.0001
4 1 36 4 1 4 50 1840
513.3 290.2 15.8 162.1 47.3 21.5 73.9 1.3
389.0 219.9 12.0 122.8 35.8 16.3
b.0001 b.0001 b.0001 b.0001 b.0001 b.0001
666
et al., 1998) in the Wadden Sea and the shallow coastal zone, has steadily increased from a few hundred birds in 1991 to more than 2000 birds in 2001 (Dijksen, pers. comm., 2005). A large-scale change in the spatial distribution of the fishing effort could also affect the distribution pattern of plaice due to spatial differences in mortality. The major change in the fisheries has been the introduction of larger vessels, resulting in a relative increase of fishing efforts in offshore areas. In addition to this, the coastal zone was extended from 3 to 12 nm in the 1970s and the Plaice Box was introduced in 1989 (Pastoors et al., 2000). A relative increase in offshore fishing will result in an apparent increase in the slope of the log catch rate against distance, opposite to the observed change. Another fisheries effect may occur if bottom trawling affects the productivity of the benthos in terms of suitable food for flatfish (De Veen, 1978; Rijnsdorp and Van Beek, 1991; Rijnsdorp and Vingerhoed, 2001). Such an effect might have occurred with the establishment of the Plaice Box (Pastoors et al., 2000). If trawling disturbance increases benthic productivity, at least in terms of the suitable food for plaice, it may be hypothesized that plaice will be attracted to the trawling grounds at the borders of the Plaice Box. This hypothesis, however, does not seem to play a dominant role, because: (1) changes in distribution occurred well before the establishment of the Plaice Box; (2) the offshore movement of the undersized plaice was not restricted to the Plaice Box but was also observed in the southern North Sea; (3) recent studies have not provided
support for the hypothesis that bottom trawling enhances benthic productivity, nor can they exclude that such an effect may occur (Collie et al., 2000; Jennings et al., 2001; Kaiser et al., 2000; Schratzberger and Jennings, 2002; Schratzberger et al., 2002).
Fig. 7. Estimated slopes of the relationship between catch rate and distance from coast in (a) transects 601 and (b) transect 666 for age groups 0 (x), 1 (▴) and 2 (⋄). A negative slope indicates that the abundance decreased with distance, a zero slope (dashed line) indicates that no relationship existed between distance and abundance and a positive slope indicates that abundance increased with distance. The grey lines show the change in the slope for three abundant year classes born in 1979, 1985 and 1996.
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Fig. 8. Schematic description of the changes in the relationship between environmental conditions and the distance to the coast between past and present periods. Solid lines indicate the current time period, dotted lines the period at the beginning of the 20th century. Upper left: summer and winter temperature; upper right: abundance of competitors; lower left: abundance of fish and bird predators; lower right: fishing effort. The Y-axis is expressed in arbitrary units.
We lack insight into the quantitative role of the various factors discussed above, but it seems unlikely that the observed changes can be ascribed to a single factor. The enhanced offshore movement of young plaice in the 1990s will primarily be a response to increased summer temperatures, either through a direct response to temperatures exceeding the tolerance range, or indirect through an increase in food requirement (Teal, pers. comm., 2005), although the decrease in predation risk and/or intra- or inter-specific competitive interactions in offshore areas may have allowed young plaice to disperse over a wider area than in a situation with a high abundance of predators or competitors. It is
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unlikely that a possible decline in the productivity of coastal waters in recent years plays a dominant role, because also in the early 20th century when the waters were still not enriched with nutrients, small plaice predominantly occurred in shallow coastal waters (Wimpenny, 1953). For the larger size classes (20– 39 cm), the change in distribution towards deeper water may be primarily related to the decreased abundance of competitors and predators, as there is no indication of a change in temperature or other factors. The offshore movement of plaice has important consequences for the management of the mixed flatfish fisheries. Most beam trawl vessels target mainly sole using a mesh size of 80 mm with a retention length for plaice of about 17 cm (Van Beek et al., 1981) well below the minimum landing size of 27 cm and discarding 50% or more of their plaice catch in numbers (Van Beek, 1998). As an increased proportion of the population of undersized plaice has moved from the relatively mildly fished coastal waters within the 12 nm zone and the Plaice Box to the more heavily exploited offshore areas, the Plaice Box has become less effective as a management measure to reduce the discarding of under-sized plaice. Our results are relevant for fisheries management, both in the evaluation of the effectiveness of previous management measures and the exploration of possibilities for improving the current management measures. Our results are also important to estimate inter-annual variations in discarding. In spite of the high discard rates in the flatfish fisheries, the stock assessments of North Sea plaice were based on landings at age only. Only recently have stock assessments been performed using reconstructed data (ICES, 2004). When discard rates are stable, the exclusion of discards will only affect the absolute estimate of the recruitment, but will not affect the relative trends in spawning stock biomass or recruitment (Rijnsdorp and Millner, 1996; ICES, 2002; Kell and Bromley, 2004). Variable discard patterns, however, will bias the time series of recruitment. The observed change in the distribution of the discard size classes of plaice implies that discard rates cannot be assumed constant. As the discard observer programme only covers a short period, a full time series of discards can only be estimated indirectly, for instance from data on growth rate and gear selectivity (Casey, 1993). Recently, we have embarked on a reconstruction of the inter-annual variations in plaice discards by extending Casey's method to accommodate for changes in spatial distribution (ICES, 2004). This is of prime importance since the reference points Blim, defined as the biomass below which recruitment is impaired, and Bpa, acting as a trigger to initiate management action to conserve the
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stock before biomass drops below critical limits, are derived from the historical relation between recruitment and spawning stock biomass and are therefore sensitive to assumptions on discarding (Kell and Bromley, 2004). References Berghahn, R., Bullock, A.M., Karakiri, M., 1993. Effects of solar radiation on the population dynamics of juvenile flatfish in the shallows of the Wadden Sea. J. Fish Biol. 42, 329–345. Beukema, J.J., Cadée, G.C., Dekker, R., 2002. Zoobenthic biomass limited by phytoplankton abundance: evidence from parallel changes in two long-term data series in the Wadden Sea. J. Sea Res. 48, 111–125. Beverton, R.J.H., Holt, S.J., 1957. On the dynamics of exploited fish populations. London, Her Majesty's Stationary Office. Fish. Invest. Ser. II XIX. Burrows, M.T., Gibson, R.N., 1995. The effects of food, predation risk and endogenous rhythmicity on the behaviour of juvenile plaice, Pleuronectes platessa L. Anim. Behav. 50, 41–52. Burrows, M.T., Gibson, R.N., Robb, L., Comely, C.A., 1994. Temporal patterns of movement in juvenile flatfishes and their predators: underwater television observations. J. Exp. Mar. Biol. Ecol. 177, 251–268. Cadée, G.C., Hegeman, J., 2002. Phytoplankton in the Marsdiep at the end of the 20th century; 30 years monitoring biomass, primary production, and Phaeocystis blooms. J. Sea Res. 48, 97–110. Casey, J., 1993. Estimating discards using selectivity data: the effects of including discard data in assessments of the demersal fisheries in the Irish Sea. J. Northwest Atl. Fish. Soc. 19, 91–102. Collie, J.S., Hall, S.J., Kaiser, M.J., Poiner, I.R., 2000. A quantitative analysis of fishing impacts on shelf-sea benthos. J. Anim. Ecol. 69, 785–798. Daan, N., Gislason, H., Pope, J.G., Rice, J.C., 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES J. Mar. Sci. 62, 177–188. De Veen, J.F., 1978. On selective tidal transport in the migration of North Sea plaice (Pleuronectes platessa) and other flatfish species. Neth. J. Sea Res. 12, 115–147. Fonds, M., Cronie, R., Vethaak, A.D., Van der Puyl, P., 1992. Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Neth. J. Sea Res. 29, 127–143. Gibson, R.N., 1994. Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth. J. Sea Res. 32, 191–206. Gibson, R.N., 1997. Behaviour and the distribution of flatfishes. J. Sea Res. 37, 241–256. Gibson, R.N., Pihl, L., Burrows, M.T., Modin, J., Wennhage, H., Nickell, L.A., 1998. Diel movements of juvenile plaice Pleuronectes platessa in relation to predators, competitors, food availability and abiotic factors on a microtidal nursery ground. Mar. Ecol., Prog. Ser. 165, 145–159. Gibson, R.N., Robb, L., Wennhage, H., Burrows, M.T., 2002. Ontogenetic changes in depth distribution of juvenile flatfishes in relation to predation risk and temperature on a shallow-water nursery ground. Mar. Ecol., Prog. Ser. 229, 233–244. Hunter, E., Metcalf, J.D., Reynolds, J.D., 2003. Migration route and spawning area fidelity by North Sea plaice. Proc. R. Soc. Lond., B 270, 2097–2103. ICES, 1985. Report of the 0-group North Sea flatfish Working Group, IJmuiden, 21–25 November 1983. ICES C.M. 1985/G:2.
ICES, 1987. Report of the ad-hoc Meeting of the North Sea flatfish Working Group, IJmuiden, 2–5 February 1987. ICES C.M. 1987/ Assess:14. ICES, 1994. Report of the Study Group on the Plaice Box, Charlottenlund, 12–15 April 1994. ICES C.M. 1994/Assess:14. ICES, 1999. Report of the Workshop on the Evaluation of the Plaice Box, IJmuiden, 22–25 June 1999. ICES C.M. 1999/D:6. ICES, 2002. Report of the Study Group on Discard and by-catch Information, Copenhagen, Denmark. ICES CM 2002/ACFM:09. ICES, 2004. Report of the Working Group on the Assessment of Demersal Stocks in the North Sea and Skagerrak, Bergen, Norway, 7–16 September 2004. ICES CM 2005/ACFM:07. Imsland, A.K., Sunde, L.M., Folkvord, A., Stefansson, S.O., 1996. The interaction of temperature and fish size on growth of juvenile turbot. J. Fish Biol. 49, 926–940. Jennings, S., Dinmore, T.A., Duplisea, D.E., Warr, K.J., Lancaster, J.E., 2001. Trawling disturbance can modify benthic production processes. J. Anim. Ecol. 70, 459–475. Jonassen, T.M., Imsland, A.K., Stefansson, S.O., 1999. The interaction of temperature and fish size on growth of juvenile halibut. J. Fish Biol. 54, 556–572. Kaiser, M.J., Ramsay, K., Richardson, C.A., Spence, F.E., Brand, A.R., 2000. Chronic fishing disturbance has changed shelf sea benthic community structure. J. Anim. Ecol. 69, 494–503. Kell, L.T., Bromley, P.J., 2004. Implications for current management advice for North Sea plaice (Pleuronectes platessa L.): Part II. Increased biological realism in recruitment, growth, densitydependent sexual maturation and the impact of sexual dimorphism and fishery discards. J. Sea Res. 51, 301–312. Kuipers, B.R., 1973. On the tidal migration of young plaice (Pleuronectes platessa) in the Wadden Sea. Neth. J. Sea Res. 6, 376–388. Leopold, M.F., Van Damme, C.F., Van der Veer, H.W., 1998. Diet of cormorants and the impact of cormorant predation on juvenile flatfish in the Dutch Wadden Sea. J. Sea Res. 40, 93–107. Lloyd, M., 1967. Mean crowding. J. Anim. Ecol. 36, 1–30. Manderson, J.P., Pessutti, J., Hilbert, J.G., Juanes, F., 2004. Shallow water predation risk for a juvenile flatfish (winter flounder; Pseudopleuronectes americanus, Walbaum) in a northwest Atlantic estuary. J. Exp. Mar. Biol. Ecol. 304, 137–157. OSPAR, 2000. Quality Status Report 2000. Region II. Greater North Sea. Ospar Commission for the Protection of the Marine Environment of the North-East Atlantic, London. Pastoors, M.A., Rijnsdorp, A.D., Van Beek, F.A., 2000. Effects of a partially closed area in the North Sea (“Plaice Box”) on stock development of plaice. ICES J. Mar. Sci. 57, 1014–1022. Philippart, C.J.M., Van Aken, H.M., Beukema, J.J., Bos, O.G., Cadée, G.C., Dekker, R., 2003. Climate-related changes in recruitment of the bivalve Macoma balthica. Limnol. Oceanogr. 48, 2171–2185. Reijnders, P.J.H., Brasseur, S.M.J.M., Siebert, K.F., Abt, U., Stede, M., Tougaard, S., 2003. The harbour seal population in the Wadden Sea as revealed by the aerial surveys in 2003. Wadden Sea Newsl. 29, 11–12. Rice, J., Gislason, H., 1996. Patterns of change in the size spectra of numbers and diversity of the North Sea fish assemblage, as reflected in surveys and models. ICES J. Mar. Sci. 53, 1214–1225. Rijnsdorp, A.D., 1989. Maturation of male and female North Sea plaice (Pleuronectes platessa L.). J. Cons. Int. Explor. Mer 46, 35–51. Rijnsdorp, A.D., Millner, R.S., 1996. Trends in population dynamics and exploitation of North Sea plaice (Pleuronectes platessa L.) since the late 1800s. ICES J. Mar. Sci. 53, 1170–1184.
O.A. van Keeken et al. / Journal of Sea Research 57 (2007) 187–197 Rijnsdorp, A.D., Pastoors, M.A., 1995. Modeling the spatial dynamics and fisheries of North Sea plaice (Pleuronectes platessa L.) based on tagging data. ICES J. Mar. Sci. 52, 963–980. Rijnsdorp, A.D., Van Beek, F.A., 1991. Changes in growth of plaice Pleuronectes platessa L. and sole Solea solea L. in the North Sea. Neth. J. Sea Res. 27, 441–457. Rijnsdorp, A.D., Van Leeuwen, P.I., 1996. Changes in growth of North Sea plaice since 1950 in relation to density, eutrophication, beam trawl effort, and temperature. ICES J. Mar. Sci. 53, 1199–1213. Rijnsdorp, A.D., Vingerhoed, B., 2001. Feeding of plaice Pleuronectes platessa L. and sole Solea solea (L.) in relation to the effects of bottom trawling. J. Sea Res. 45, 219–229. Rijnsdorp, A.D., Van Leeuwen, P.I., Daan, N., Heessen, H.J.L., 1996. Changes in abundance of demersal fish species in the North Sea between 1906–1909 and 1990–1995. ICES J. Mar. Sci. 53, 1054–1062. SAS Institute Inc., 1999. SAS/STAT Procedure Guide, Version 8. SAS Institute INC, Cary, NC, USA. Schratzberger, M., Jennings, S., 2002. Impacts of chronic trawling disturbance on meiofaunal communities. Mar. Biol. 141, 991–1000.
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Schratzberger, M., Dinmore, T.A., Jennings, S., 2002. Impacts of trawling on the diversity, biomass and structure of meiofauna assemblages. Mar. Biol. 140, 83–93. Van Aken, H.M., 2003. 140 years of daily observations in a tidal inlet (Marsdiep). ICES Mar. Sci. Symp. 219, 359–361. Van Beek, F.A., 1998. Discarding in the Dutch Beam Trawl Fishery. ICES CM 1998/BB:5. Van Beek, F.A., Rijnsdorp, A.D., Van Leeuwen, P.I., 1981. Results of Mesh Selection Experiments on North Sea Plaice with a Commercial Beam Trawler in 1981. ICES C.M. 1981/B:32. Van Beek, F.A., Rijnsdorp, A.D., De Clerck, R., 1989. Monitoring juvenile stocks of flatfish in the Wadden Sea and the coastal areas of the southern North Sea. Helgol. Meeresunters. 43, 461–477. Van der Veer, H.W., Bergman, M.J.N., 1986. Development of tidally related behaviour of a newly settled 0-group plaice (Pleuronectes platessa) population in the western Wadden Sea. Mar. Ecol., Prog. Ser. 31, 121–129. Von Westernhagen, H., Hickel, W., Bauerfeind, E., Niermann, U., Kroncke, I., 1986. Sources and effects of oxygen deficiencies in the south-eastern North Sea. Ophelia 26, 45–60. Wimpenny, R.S., 1953. The Plaice. Arnold, London. 144 pp.
Changes in the spatial distribution of North Sea plaice (Pleuronectes platessa) and implications for fisheries management O.A. van Keeken ⁎, M. van Hoppe, R.E. Grift, A.D. Rijnsdorp Wageningen IMARES, Institute for Marine Resources and Ecosystem Studies, P.O. Box 68, 1970 AB IJmuiden, The Netherlands Received 29 October 2005; accepted 25 September 2006 Available online 28 October 2006
Abstract To protect the main nursery area of plaice, an area called the ‘Plaice Box’ was closed to trawl fisheries with large vessels in 1989, with the expectation that recruitment, yield and spawning stock biomass would increase. However, since then the plaice population has declined and the rate of discarding outside the Plaice Box has increased, suggesting an offshore shift in spatial distribution of juvenile plaice. Using research vessel survey data collected since 1970, the change in distribution of juvenile age groups was analysed in relation to the distance to the coast. Further, a comparison of the distribution of different length classes of plaice between three historic periods was made (1902–1909; 1983–1987; 1999–2003). A shift towards deeper water of largersized plaice (20–39 cm) is apparent already before the 1980s and may be related to the decrease in the number of competitors or predators. An offshore shift in the distribution of young plaice occurred in the 1990s most likely in response to higher water temperatures that may have exceeded the maximum tolerance range or increased the food requirements above the available food resources. A decrease in competition with larger plaice offshore, possibly in combination with increased inshore predation by cormorants and seals, may also have played a role. The offshore shift in distribution has reduced the effectiveness of the Plaice Box as a technical measure to protect the under-sized plaice from discarding, since an increased proportion of the population of undersized plaice is moving to the more heavily exploited offshore areas. © 2006 Elsevier B.V. All rights reserved. Keywords: Plaice; Spatial distribution; North Sea; Plaice Box; Fisheries management
1. Introduction In the North Sea, plaice is exploited in a mixed fishery for flatfish. Due to the small mesh size used in the fishery to catch sole, large numbers of undersized plaice are caught and discarded (Rijnsdorp and Millner, 1996; Van Beek, 1998). In order to reduce discard mortality, the main distribution area of undersized plaice was closed to fishing in 1989 for vessels with an engine ⁎ Corresponding author. E-mail address: [email protected] (O.A. van Keeken). 1385-1101/$ - see front matter © 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.seares.2006.09.002
power of more than 300 hp (221 KW) (ICES, 1994, 1999). This area, the ‘Plaice Box’, was based on the spatial segregation between juvenile and adult fish (ICES, 1987, 1994). Plaice spawn in offshore waters, whereas the juveniles settle in the shallow waters of estuaries and sandy beaches. During ontogeny, plaice gradually leave the shallow coastal waters and move into deeper waters further offshore (Wimpenny, 1953; Rijnsdorp and Van Beek, 1991). In contrast to expectations, the recruitment, yield and spawning stock biomass of plaice decreased since the introduction of the Plaice Box (ICES, 1999). The rate of
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discarding in the waters outside the Plaice Box has increased (ICES, 1999; Pastoors et al., 2000), and plaice have been discarded at smaller lengths outside the Plaice Box in recent years (own obs.), suggesting that a change in the distribution pattern of plaice may have occurred. The distribution pattern of plaice is the result of the interaction between behaviour through directed migrations and small-scale (dispersive) movements, and the effect of fishing. Migratory behaviour between summer feeding areas and winter spawning areas develops when plaice becomes sexually mature (De Veen, 1978; Rijnsdorp, 1989; Rijnsdorp and Pastoors, 1995; Gibson, 1997; Hunter et al., 2003). Small-scale movements will occur in the juvenile and adult phase. Such small-scale movements may be random (Beverton and Holt, 1957), for example as a result of foraging behaviour, may have a directed component, for example in the tidal migrations (Kuipers, 1973; Gibson et al., 2002) or, when related to the evasive behaviour, may be directed away from adverse environmental conditions such as extreme temperatures or low oxygen concentrations (Beverton and Holt, 1957; Berghahn et al., 1993; Gibson, 1994, 1997). Beverton and Holt (1957) described the offshore movement of plaice as a dispersion process, thus driven by random movements. Small-scale directed movements were described by Berghahn et al. (1993), who recorded a mass exodus of 0-group plaice from the tidal flats in response to temperature. Also, the autumn offshore migration from the shallow inshore waters and the spring inshore migration may reflect a response to temperature and feeding conditions (De Veen, 1978). Fish may further respond to predation risk by changing migration behaviour (Burrows and Gibson, 1995; Manderson et al., 2004). Offshore movement could also be an effect of changed feeding conditions, caused by the introduction of the Plaice Box, since fishing efforts shifted to the border of the Plaice Box after its closure. Bottom trawling may increase the availability of the benthos in terms of suitable food for plaice (De Veen, 1978; Rijnsdorp and Van Beek, 1991; Rijnsdorp and Vingerhoed, 2001). A change in the distribution of undersized plaice may have a large impact on the management of the fisheries. Insight into the extent of the changes in distribution and the likely causes is of paramount interest for the evaluation of the effectiveness of the current management of the Plaice Box. This paper focuses on the offshore movement of plaice from the nursery grounds along the continental coast. These nursery areas produce 90% of the recruitment of North Sea plaice (ICES, 1985; Van Beek et al., 1989). Changes in distribution are analysed
in relation to the distance to the continental coast, using research vessel survey data collected since 1970. Further, a comparison is made of the distribution of different length classes of plaice between three historic periods: 1902–1909, 1983–1987 and 1999–2003, and implications of the change in distribution for fisheries management are discussed. 2. Methods 2.1. Comparing spatial distribution between three historic periods The spatial distributions of different size classes of plaice were compared between three periods: 1902– 1909, 1983–1987, 1999–2003. The periods analysed differed with respect to several of the factors that may affect distribution, such as water temperature, productivity, predation risk and the level and distribution of fishing effort. 2.1.1. Data Third quarter data for 1902–1909 were available from two different surveys: RV ‘Huxley’ and RV ‘Wodan’. References to these data can be found in Rijnsdorp et al. (1996). RV ‘Huxley’ used either a 26.5 m otter trawl (OT90) or a 13 m beam trawl (BT13) (Table 1). Tow duration varied between 1 and 3 h at a towing speed of 2 nm h− 1. Fish were grouped into 10 cm length classes. RV ‘Wodan’ used a 26.5 m otter trawl similar to that of RV ‘Huxley’. Haul duration was generally 1–2 h at a towing speed of 2 nm h− 1. Fish were grouped into 5 cm length classes. Mesh size was 63 mm and 68 mm for beam trawl and otter trawl, respectively. Table 1 Details of the gears used during 1902–1909, 1983–1987 and 1999– 2003 BT13 1902– 1909 Haul duration (min) Codend mesh Tickler chains Towing speed Sweep Swept area (1000 m2 h− 1) Relative catch effiency
OT90 1902– 1909
BT14 1983– 1987
BT12 1983– 1987
BT8 1983–1987 1999–2003
60–180 60–180 10–40
10–40
30
63 0 2 13 50
68 0 2 17 60
85 8 5–5.5 14 140
85 8 5–5.5 12 120
40 8 4 8 60
0.85
1
2.3
2
1
Relative catch efficiency rates were standardized to swept area per hour with OT90/BT8.
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Third quarter data for 1983–1987 were available from research cruises conducted with chartered commercial beam trawl vessels (‘KW34’ and ‘KW36’) in the offshore areas, and the RV ‘ISIS’ in the southeastern North Sea. ‘KW34’ collected data in 1983, 1985 and 1986, while ‘KW36’ collected data in 1987. Both vessels used a 12 m beam trawl (BT12), except for 1983 when ‘KW34’ used a 14 m beam trawl (BT14). Haul duration was 30 min, but occasionally varied between 10–40 min. Towing speed varied between 5 and 5.5 nm h− 1 and mesh size was 85 mm. Data for 1999–2003 were available from the BTS survey conducted by RV ‘ISIS’ and RV ‘Tridens’, using an 8 m beam trawl (BT8). The BTS survey was carried out in August and September. RV ‘ISIS’ covered the eastern part, while RV ‘Tridens’ covered the western part of the southern North Sea. Haul duration was 30 min at a towing speed of 4 nm h− 1. Mesh size was 40 mm. 2.1.2. Data analysis The number per haul was converted into the mean number per hour and corrected for the area swept. The swept areas for each gear were scaled to the swept area of the OT90/BT8 (Table 1). Because the ‘Wodan’ data reported numbers per 10 cm length class, these length classes were used in the analysis for all surveys (20– 29 cm, 30–39 cm, 40–49 cm, 50 and larger), except for the smallest length class which was restricted to 15–19 cm to prevent a bias in catch rates due to the smaller mesh size used in 1983–1987 and 1999–2003. Average catch rates were calculated per square of 0.5° longitude × 1° latitude (ICES rectangles). As we are particularly interested in the offshore movement of the size classes from their nursery grounds, the shortest distance of each haul to the continental coast was calculated. In the final analysis only hauls east of 2°E were included, because in the areas west of this line, plaice may originate from the nursery grounds along the British east coast. Intra-specific competition was quantified with the index of mean crowding (Lloyd, 1967). The index of mean crowding gives the average number of individuals with which an individual shares its spatial unit. Following Rijnsdorp and Van Beek (1991), the ICES rectangle was used as spatial unit and mean crowding of length group b on length group a was calculated as: X xaid xbi i X ð1Þ b ma ¼ xai i
where bma is the index of mean crowding by length group b on length group a, and xai and xbi are the catch
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rate of length group a and b respectively in the ith spatial unit. 2.2. Modelling catch rates to distance from the coast The offshore movement of plaice was studied in more detail by analyzing the slope of the decline in numbers with increasing distance from the coast for the juvenile age groups 0, 1 and 2. 2.2.1. Data For this analysis data from the Sole Net Survey (SNS) were used. The survey was initiated in 1969 and samples 10 fixed transects (parallel or perpendicular to the coastline) along the Dutch, German and Danish coasts in September – October before the autumn migration (Fig. 1). The survey used a 6 m beam trawl with a cod-end of 40 mm stretched mesh. Haul duration was 15 min at a towing speed of 4 nm h− 1. To investigate yearly differences in catch rates to the shortest distance from the coast, two transects were chosen, which are perpendicular to the coast: 601 and 666, combining transect 606 and 660. Temperature data and growth indices were used in the analysis to investigate the effect on the distribution of plaice. Monthly mean temperatures were available from a coastal station at Den Helder (Van Aken, 2003).
Fig. 1. Map of the transects of sampling stations of the SNS survey. Transect 601 is situated perpendicular of the Danish coast, transect 666 combines transect 660 and 606 off the Dutch coast. The heavy lines indicate the location of the Plaice Box, a protected area along the continental coast between 53° and 57°N.
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was performed on the slope of the log catch rate against distance for individual years in relation to the growth index or the temperature index. 3. Results 3.1. Comparing historic periods
Fig. 2. Growth index for age-2 female plaice obtained from backcalculated mean length at age (top), and mean and maximum monthly water temperature (July–September) measured daily at a coastal station (Den Helder, The Netherlands).
A time series of juvenile growth rate, annual length increment of plaice of 15–25 cm, was available for the cohorts 1950– 1994 from otolith back-calculations of female plaice (Rijnsdorp and Van Leeuwen, 1996), which was updated with samples up to 2003. Fig. 2 shows the temperature and growth indices used in the analysis. 2.2.2. Data analysis Numbers per haul were converted into numbers at age per hour using age length keys. Distance from the coast was calculated as shortest distance to the coastline. Log-transformed catch-rates (number h− 1) were modelled using GLM (SAS Institute Inc., 1999): logðCr þ 1ÞfA þ D þ YC þ A⁎D þ Y ⁎D þ A⁎Y ⁎D
The well-known pattern of a gradual movement away from coastal waters was apparent in all three periods (Fig. 3). Closer inspection, however, indicated that similar-sized plaice have spread further away from the coast in recent time. The analysis of the distribution of the different size classes over depth corroborated the changes in distribution (Fig. 4). The change in depth distribution of the two smallest size classes was already apparent between 1902–1907 and 1983–1987, although the major shift occurred between 1983–1987 and 1999– 2003. In the larger size classes, the change occurred between 1902–1907 and 1983–1987. In the former period, plaice N 30 cm were mainly restricted to depths of b 60 m, while in the two later periods they were caught to a depth of 90 m. The index of intra-specific competition showed that the total mean crowding on the 15–19 cm and 20–29 cm length classes was highest in the first period and decreased for both classes over the two following periods (Fig. 5). Total mean crowding in the last period was more than a factor of two lower than in the first period for both length classes. Also for the 30–39 cm length class, the total mean crowding showed a steady decline over the three periods, whereas that for the 40– 49 cm length class showed an increasing trend. Total crowding on the length class N 50 cm was higher in 1983–1987 than in the other two periods. The contribution of the various size classes to the total mean crowding is illustrated in Fig. 6. The contribution of the 15–19 cm length class to the mean crowding on other length groups increased over the last two periods.
ð2Þ where Cr is the catch rate (numbers h− 1) in transect r, A is age group, D is distance from coast (km), YC is year class and Y is year. A, Y and YC are included as class variables and D as continuous variable. A type I analysis was used to test whether the parameters included in the model significantly contributed to the explained variance in catch rates. The interaction term D⁎Y examines whether the slope of the catch rates has changed with distance over time. To test whether growth or temperature had a significant effect on the distribution, regression analysis
3.2. Modelling catch rates to distance from the coast The catch rate of plaice decreased with increasing distance (D) from the coast, and the relationship differed between the age groups (A). Table 2 shows that the variable D + A⁎D explained 24.7% and 15.3% of the variance for area 601 and 666, respectively. Other important variables were age (A) and year class (YC). The total model, including the variables distance (D), age (A), year class (YC) and their first and second order interactions, explained 63.2% of the variance for transect 601 and 60.3% for transect 666. The significant
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Fig. 3. Catch rates (number h− 1) per ICES square for plaice of length group 15–19 cm (left) and 20–29 cm (right) in the period 1902–1909 (upper panels), 1983–1987 (middle panels) and 1999–2003 (lower panels). x indicates a zero catch rate, whereas the size of the dot reflects catch rates increasing from 0.01–0.9; 1–4.9; 5–14.9; 15–49.9 and N = 50 plaice h− 1.
interactions Y⁎D and A⁎Y⁎D indicated that the relationship between catch rate and distance changed over time, and differed for the various age groups. The slope of the relationship, estimated for 0-, 1- and 2-group in individual years, revealed that the slopes did not change gradually over time, but that they varied
without a trend until the mid 1990s and then increased (Fig. 7). The change in slope was particularly clear in area 601 off the Danish coast. In area 666 off the Dutch coast, the slopes of 0- and 1-group showed some high values in the mid 1990s but the change in time was less clear.
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Fig. 4. Relative catch rate (number h− 1) of 15–19 cm, 20–29 cm, 30–39 cm and 40–49 cm length groups over 5 m depth classes for each period. Catch rates are expressed relative to the mean catch rate over all depth bands.
The slopes of the relationship between abundance and distance from the coast were regressed to water temperature and growth index. Water temperature showed a significant effect for age 1, but not for age 0 or age 2, and explained 20% and 13% of the variance in the slope for transect 601 and 666, respectively. The growth index did not show a significant relationship explaining less than 1 – 9% of the variance in slopes. 4. Discussion The available survey data clearly indicate a change in the spatial distribution of plaice. In the first decades of the 20th century, high concentrations of small plaice were observed in shallow coastal waters (Wimpenny, 1953). Since the mid 1980s, a gradual offshore movement has taken place, and consistent with this offshore movement, the population of 1-group plaice has left the Dutch Wadden Sea almost completely since the late 1990s (Bolle, pers. comm., 2005). The change in distribution was particularly pronounced in the 20–29 cm and the 30–39 cm length classes and off the Danish coast, but less clear off the Dutch coast. The timing of the change in distribution differed between these length classes. The 20–29 cm length class extended its distribution to offshore waters between the mid 1980s and the late 1990s, whereas the 30–39 cm length class already extended its distribution before the mid 1980s. In the two recent time periods, the 30–39 cm length class comprised mainly adult plaice, as the length at first maturity is 20–24 cm in males and 30–35 cm in females. In 1900, however, this length class would have
comprised both juvenile and adult plaice, as the length at first maturity ranged between 30–37 cm in males and 32–43 cm in females (Rijnsdorp, 1989). This may imply that the decrease in the size at first maturation in conjunction with the onset of a seasonal migration between feeding and spawning areas may have resulted in a more homogeneous distribution of the 30–39 cm length class over the North Sea. Beverton and Holt (1957) described the offshore movement of young plaice in terms of diffusion. The decrease in the slope of the relationship of the log catch rates against distance in the 1990 implies that the dispersion rate has increased. Such an increase may be due to an increase in small-scale undirected movements or a directed response to temperature, food availability,
Fig. 5. Change in the mean crowding on length classes 15–19 cm, 20– 29 cm, 30–39 cm, 40–49 cm and N = 50 cm between time periods 1902–1909, 1983–1987, 1999–2003.
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Fig. 6. Contribution of each length class to the mean crowding on length classes 15–19 cm, 20–29 cm, 30–39 cm, 40–49 cm and N = 50 cm in time periods (a) 1902–1909; (b) 1983–1987; (c) 1999–2003.
intra- or inter-specific competitors, or predators (Fig. 8). The scatter plot of the slope of the log catch rates and distance with summer temperature showed a significant effect for 1-group in both transects, but not for 0-group. In the 1990s, when maximum mean monthly temperatures reached and exceeded 20 °C (Fig. 2), temperatures above which growth rates of 0-group start to decline (Fonds et al., 1992), maximum temperatures on the hottest days must have been even higher. Newly settled plaice showed a mass ‘exodus’ from the intertidal pools in the Wadden Sea when temperatures exceeded the critical level of 24 °C (Van der Veer and Bergman, 1986; Berghahn et al., 1993). As the optimal temperature decreases with fish size (Imsland et al., 1996; Jonassen et al., 1999), it can be expected that the habitat choice is, at least partly, related to the available temperature field. If, due to the recent increase, the summer temperature exceeds the optimal value, a shift of plaice to deeper and cooler water further offshore can be expected. Small-scale undirected movement may have increased in the 1990s in response to an increase in
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temperature, which may enhance the activity level of fish. An increase in summer temperature will increase the food requirements of plaice that may then exceed the available food resources for a larger part of the growing season (Teal, pers. comm., 2005). Small-scale undirected movement may also have increased in the 1990s in response to a reduction in the productivity of the coastal waters. In the western Wadden Sea, a decrease in primary production was observed between 1994 and 2003 from a level of about 1200 to 600 mg C m− 2 d− 1 (Cadée and Hegeman, 2002), although there is at present no indication of decreased benthic biomass in recent years (Beukema et al., 2002). Nevertheless, changes in the benthic production of certain components may have occurred. Macoma balthica recruitment and biomass have decreased in recent years probably due to the mismatch in the timing of reproduction in relation to larval food as well as an increased predation by Crangon crangon (Philippart et al., 2003). The slightly shallower slopes in the early 1980s, in particular in area 601, may be affected by the reduction of oxygen concentrations to values below 2 mg l− 1 that were observed in 1981–1983 in the inner German Bight between 7° and 8° East (Von Westernhagen et al., 1986). As only one hypoxia event was recorded in the 1990s (in 1994, OSPAR, 2000), hypoxia does not seem to have played a role in the changes in plaice distribution since the mid 1990s. The offshore movement may also have been affected by changes in predation risk. Shifts of 0-group flatfish, bringing them into shallower water during the night, may serve as an anti-predator strategy (Burrows et al., 1994). Gibson et al. (1998, 2002) showed that 0-group plaice avoided predation risk by feeding predominantly in areas with few fish predators. Burrows and Gibson (1995) showed changes in patterns and types of behaviour and reduced activity of tank-kept juvenile plaice with predator presence. Changes in predation risk will certainly have occurred during the last century. Fisheries caused a considerable decrease in the abundance of larger predatory fish species (Rice and Gislason, 1996; Daan et al., 2005), resulting in a lower predation risk in deeper offshore waters. On the other hand, plaice faced an increased predation risk in coastal waters in the 1990s from seals and piscivorous birds (mainly cormorants). The number of seals has decreased in the 20th century due to hunting and pollution, dropping to a minimum of about 4000 animals in the mid 1970s and again in 1989 after a virus outbreak, but has recovered to more than 20 000 animals in 2002 (Reijnders et al., 2003). The numbers of cormorants, known to feed on plaice and other flatfish (Leopold
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Table 2 Statistical evaluation of the influence of age (A), distance (D), year-class (YC) and year (Y) on the catch rates in transects 601 and 666 Transect
Source
SS
%
df
MS
F
p
601
A D YC A⁎D Y⁎D A⁎Y⁎D Explained Unexplained Total A D YC A⁎D Y⁎D A⁎Y⁎D Explained Unexplained Total
1861.1 371.3 907.5 1580.6 98.4 182.2 5001.0 2912.4 7913.4 2053.3 290.2 568.1 648.3 47.3 86.0 3693.3 2428.2 6121.5
23.5 4.7 11.5 20.0 1.2 2.3 63.2 36.8 100.0 33.5 4.7 9.3 10.6 0.8 1.4 60.3 39.7 100.0
4 1 36 4 1 4 50 1265
465.3 371.3 25.2 395.1 98.4 45.5 100.0 2.3
202.1 161.3 10.9 171.6 42.7 19.8
b.0001 b.0001 b.0001 b.0001 b.0001 b.0001
4 1 36 4 1 4 50 1840
513.3 290.2 15.8 162.1 47.3 21.5 73.9 1.3
389.0 219.9 12.0 122.8 35.8 16.3
b.0001 b.0001 b.0001 b.0001 b.0001 b.0001
666
et al., 1998) in the Wadden Sea and the shallow coastal zone, has steadily increased from a few hundred birds in 1991 to more than 2000 birds in 2001 (Dijksen, pers. comm., 2005). A large-scale change in the spatial distribution of the fishing effort could also affect the distribution pattern of plaice due to spatial differences in mortality. The major change in the fisheries has been the introduction of larger vessels, resulting in a relative increase of fishing efforts in offshore areas. In addition to this, the coastal zone was extended from 3 to 12 nm in the 1970s and the Plaice Box was introduced in 1989 (Pastoors et al., 2000). A relative increase in offshore fishing will result in an apparent increase in the slope of the log catch rate against distance, opposite to the observed change. Another fisheries effect may occur if bottom trawling affects the productivity of the benthos in terms of suitable food for flatfish (De Veen, 1978; Rijnsdorp and Van Beek, 1991; Rijnsdorp and Vingerhoed, 2001). Such an effect might have occurred with the establishment of the Plaice Box (Pastoors et al., 2000). If trawling disturbance increases benthic productivity, at least in terms of the suitable food for plaice, it may be hypothesized that plaice will be attracted to the trawling grounds at the borders of the Plaice Box. This hypothesis, however, does not seem to play a dominant role, because: (1) changes in distribution occurred well before the establishment of the Plaice Box; (2) the offshore movement of the undersized plaice was not restricted to the Plaice Box but was also observed in the southern North Sea; (3) recent studies have not provided
support for the hypothesis that bottom trawling enhances benthic productivity, nor can they exclude that such an effect may occur (Collie et al., 2000; Jennings et al., 2001; Kaiser et al., 2000; Schratzberger and Jennings, 2002; Schratzberger et al., 2002).
Fig. 7. Estimated slopes of the relationship between catch rate and distance from coast in (a) transects 601 and (b) transect 666 for age groups 0 (x), 1 (▴) and 2 (⋄). A negative slope indicates that the abundance decreased with distance, a zero slope (dashed line) indicates that no relationship existed between distance and abundance and a positive slope indicates that abundance increased with distance. The grey lines show the change in the slope for three abundant year classes born in 1979, 1985 and 1996.
O.A. van Keeken et al. / Journal of Sea Research 57 (2007) 187–197
Fig. 8. Schematic description of the changes in the relationship between environmental conditions and the distance to the coast between past and present periods. Solid lines indicate the current time period, dotted lines the period at the beginning of the 20th century. Upper left: summer and winter temperature; upper right: abundance of competitors; lower left: abundance of fish and bird predators; lower right: fishing effort. The Y-axis is expressed in arbitrary units.
We lack insight into the quantitative role of the various factors discussed above, but it seems unlikely that the observed changes can be ascribed to a single factor. The enhanced offshore movement of young plaice in the 1990s will primarily be a response to increased summer temperatures, either through a direct response to temperatures exceeding the tolerance range, or indirect through an increase in food requirement (Teal, pers. comm., 2005), although the decrease in predation risk and/or intra- or inter-specific competitive interactions in offshore areas may have allowed young plaice to disperse over a wider area than in a situation with a high abundance of predators or competitors. It is
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unlikely that a possible decline in the productivity of coastal waters in recent years plays a dominant role, because also in the early 20th century when the waters were still not enriched with nutrients, small plaice predominantly occurred in shallow coastal waters (Wimpenny, 1953). For the larger size classes (20– 39 cm), the change in distribution towards deeper water may be primarily related to the decreased abundance of competitors and predators, as there is no indication of a change in temperature or other factors. The offshore movement of plaice has important consequences for the management of the mixed flatfish fisheries. Most beam trawl vessels target mainly sole using a mesh size of 80 mm with a retention length for plaice of about 17 cm (Van Beek et al., 1981) well below the minimum landing size of 27 cm and discarding 50% or more of their plaice catch in numbers (Van Beek, 1998). As an increased proportion of the population of undersized plaice has moved from the relatively mildly fished coastal waters within the 12 nm zone and the Plaice Box to the more heavily exploited offshore areas, the Plaice Box has become less effective as a management measure to reduce the discarding of under-sized plaice. Our results are relevant for fisheries management, both in the evaluation of the effectiveness of previous management measures and the exploration of possibilities for improving the current management measures. Our results are also important to estimate inter-annual variations in discarding. In spite of the high discard rates in the flatfish fisheries, the stock assessments of North Sea plaice were based on landings at age only. Only recently have stock assessments been performed using reconstructed data (ICES, 2004). When discard rates are stable, the exclusion of discards will only affect the absolute estimate of the recruitment, but will not affect the relative trends in spawning stock biomass or recruitment (Rijnsdorp and Millner, 1996; ICES, 2002; Kell and Bromley, 2004). Variable discard patterns, however, will bias the time series of recruitment. The observed change in the distribution of the discard size classes of plaice implies that discard rates cannot be assumed constant. As the discard observer programme only covers a short period, a full time series of discards can only be estimated indirectly, for instance from data on growth rate and gear selectivity (Casey, 1993). Recently, we have embarked on a reconstruction of the inter-annual variations in plaice discards by extending Casey's method to accommodate for changes in spatial distribution (ICES, 2004). This is of prime importance since the reference points Blim, defined as the biomass below which recruitment is impaired, and Bpa, acting as a trigger to initiate management action to conserve the
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stock before biomass drops below critical limits, are derived from the historical relation between recruitment and spawning stock biomass and are therefore sensitive to assumptions on discarding (Kell and Bromley, 2004). References Berghahn, R., Bullock, A.M., Karakiri, M., 1993. Effects of solar radiation on the population dynamics of juvenile flatfish in the shallows of the Wadden Sea. J. Fish Biol. 42, 329–345. Beukema, J.J., Cadée, G.C., Dekker, R., 2002. Zoobenthic biomass limited by phytoplankton abundance: evidence from parallel changes in two long-term data series in the Wadden Sea. J. Sea Res. 48, 111–125. Beverton, R.J.H., Holt, S.J., 1957. On the dynamics of exploited fish populations. London, Her Majesty's Stationary Office. Fish. Invest. Ser. II XIX. Burrows, M.T., Gibson, R.N., 1995. The effects of food, predation risk and endogenous rhythmicity on the behaviour of juvenile plaice, Pleuronectes platessa L. Anim. Behav. 50, 41–52. Burrows, M.T., Gibson, R.N., Robb, L., Comely, C.A., 1994. Temporal patterns of movement in juvenile flatfishes and their predators: underwater television observations. J. Exp. Mar. Biol. Ecol. 177, 251–268. Cadée, G.C., Hegeman, J., 2002. Phytoplankton in the Marsdiep at the end of the 20th century; 30 years monitoring biomass, primary production, and Phaeocystis blooms. J. Sea Res. 48, 97–110. Casey, J., 1993. Estimating discards using selectivity data: the effects of including discard data in assessments of the demersal fisheries in the Irish Sea. J. Northwest Atl. Fish. Soc. 19, 91–102. Collie, J.S., Hall, S.J., Kaiser, M.J., Poiner, I.R., 2000. A quantitative analysis of fishing impacts on shelf-sea benthos. J. Anim. Ecol. 69, 785–798. Daan, N., Gislason, H., Pope, J.G., Rice, J.C., 2005. Changes in the North Sea fish community: evidence of indirect effects of fishing? ICES J. Mar. Sci. 62, 177–188. De Veen, J.F., 1978. On selective tidal transport in the migration of North Sea plaice (Pleuronectes platessa) and other flatfish species. Neth. J. Sea Res. 12, 115–147. Fonds, M., Cronie, R., Vethaak, A.D., Van der Puyl, P., 1992. Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Neth. J. Sea Res. 29, 127–143. Gibson, R.N., 1994. Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth. J. Sea Res. 32, 191–206. Gibson, R.N., 1997. Behaviour and the distribution of flatfishes. J. Sea Res. 37, 241–256. Gibson, R.N., Pihl, L., Burrows, M.T., Modin, J., Wennhage, H., Nickell, L.A., 1998. Diel movements of juvenile plaice Pleuronectes platessa in relation to predators, competitors, food availability and abiotic factors on a microtidal nursery ground. Mar. Ecol., Prog. Ser. 165, 145–159. Gibson, R.N., Robb, L., Wennhage, H., Burrows, M.T., 2002. Ontogenetic changes in depth distribution of juvenile flatfishes in relation to predation risk and temperature on a shallow-water nursery ground. Mar. Ecol., Prog. Ser. 229, 233–244. Hunter, E., Metcalf, J.D., Reynolds, J.D., 2003. Migration route and spawning area fidelity by North Sea plaice. Proc. R. Soc. Lond., B 270, 2097–2103. ICES, 1985. Report of the 0-group North Sea flatfish Working Group, IJmuiden, 21–25 November 1983. ICES C.M. 1985/G:2.
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