The distribution and population structure of the bivalve Arctica islandica L. in the North Sea: what possible factors are involved?

Journal of Sea Research 50 (2003) 11 – 25 www.elsevier.com/locate/seares

The distribution and population structure of the bivalve Arctica islandica L. in the North Sea: what possible factors are involved? R. Witbaard *, M.J.N. Bergman Royal Netherlands Institute for Sea Research, PO Box 59, 1790 AB den Burg, Texel, The Netherlands Received 4 September 2002; accepted 4 February 2003

Abstract The present paper summarises observations on the distribution, abundance and population structure of the bivalve Arctica islandica in the North Sea between 1970 and 2000, and demonstrates that Arctica has a widespread distribution in the North Sea north of 53j30VN. Along its southern and eastern borders the distribution seems to be limited to depths beyond 30 m. A comparison between distribution patterns of Arctica in 1972 – 1994 and in 1996 – 2000 suggests slight changes along its southernmost border in the Oyster Ground. In the south-eastern North Sea, the average density of Arctica (>10 mm) was 7 individuals per 100 m2 and the population was dominated by full-grown specimens exceeding 50 mm shell height. The highest abundance of spat, juveniles and adults was found in the deeper central section of the Oyster Ground that is stratified during summer. There, the mean density was 21 individuals (>10 mm) per 100 m2. These densities were much lower than in the northern North Sea (Fladen Ground), where abundance was one to two orders of magnitude higher and peaked at 28 600 individuals per 100 m2. In the Fladen Ground, the population structure was bimodally shaped and dominated by juveniles. In the Oyster Ground, the skewed size class distribution suggests that the recruitment to larger size classes is hampered. An insufficiently dense stock of reproducing adults generating less dense spatfalls, possibly in combination with limited survival of spat and juveniles, prevents successful recruitment. Although natural processes may contribute to the skewed population structure, intensive bottom trawling is thought to have a major effect as well. It is therefore questionable whether under presentday conditions the population of Arctica in the SE North Sea can be considered sustainable in the long term. D 2003 Elsevier B.V. All rights reserved. Keywords: Arctica islandica; North Sea; Population structure; Recruitment; Fisheries impact

1. Introduction Arctica islandica L. is the only living species of a bivalve genus that originates in the early Cretaceous (Nicol, 1951). Arctica is known under various com* Corresponding author. Tel.: +31-222-369537; fax: +31-222319674. E-mail address: [email protected] (R. Witbaard).

mon names such as ‘Iceland Cyprina’, ‘Ocean Quahog’ and ‘Mahogany Clam’. The latter name is derived from the golden brown colour of the periostracum present on the shells of young specimens. The periostracum becomes black when the animal grows older because of the deposition of iron complexes (Brey et al., 1990). Arctica has been studied for its anatomy (Salleudin, 1964; Palmer, 1979), behaviour (Taylor, 1976)

1385-1101/03/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S1385-1101(03)00039-X

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and physiology (Bayne, 1971; Oescher and Story, 1993; Tschischka et al., 2000). Since the 1980s, ecological aspects of Arctica have become a subject of study after the species became commercially important along the American east coast (Kennish et al., 1994), in Icelandic waters (Thorarinsdottir and Steingrimsson, 2000) and likely in British waters (S. Davis, Cornwall Sea Fisheries, pers. comm., 2001). For the North Sea, however, knowledge of the distribution, abundance and population structure remains scarce because commercial exploitation has never initiated such research. Arctica is now seen as an indicator organism for environmental health (Rees and Dare, 1993; Aquasense, 2001) and therefore proper distribution maps, reliable density estimates and insight into the population structure and its controlling factors are urgently needed. Only when such basic knowledge is available will its use as an indicator make sense. Throughout the last century the species has been recorded in faunal studies of the North Sea (Petersen, 1915, 1918; Davis, 1923, 1925; Hunt, 1925; Holme, 1953; Dyer et al., 1983, Høsaeter, 1986), yet distribution maps constructed so far (Seaward, 1990) reveal little detail or deal with only a section of the North Sea (Basford et al., 1989). A first map of its distribution in the southern and central North Sea with a higher spatial resolution (see Witbaard et al., 1994) was obtained from the ICES Benthic Survey in 1986 and based on boxcore samples and trawl catches (Duineveld et al., 1990). Although specimens of less than 10 mm (spat) were regularly found in the boxcore samples, larger animals were seldom retained, even in the catches of the fine-meshed beamtrawl. Therefore, the map merely reflects the distribution and density of spat rather than the distribution of adults. The present paper compiles data from surveys between 1970 and 2000, including quantitative records on all size classes, and describes the distribution, abundance and population structure of Arc-

tica in the North Sea in relation to environmental variables.

2. Material and methods Primary data sources are reports of NIOZ research cruises with RV ‘Tyro’, RV ‘Aurelia’ and RV ‘Pelagia’, containing data on the occurrence of Arctica collected during various research programs since the early seventies. A second source of information is data series from field surveys with governmental research vessels (RV ‘Tridens’, RV ‘Mitra’, RV ‘Zirfaea’) and commercial trawlers from the local fishing fleet. Records from the literature have been used as the third data source. The entire data set encompass 1520 sampling stations in the North Sea south of 60j00VN (Fig. 1). No attempts have been made to include literature records of Arctica along the east coast of the UK nor from the Norwegian fjords or Skagerrak. The diverse origin of the data implies that a variety of sampling gear and methods were involved. The most frequently used gears were van Veen grabs (0.2 m2), boxcorers (0.07 m2) and both scientific (5 m wide, stretched mesh size in cod end of 2 cm) and commercial (12 m wide, stretched mesh size in the cod end of 8 cm) beam trawls. Density estimates derived from such diverse types of gear are often not quantitative and difficult to compare. In large parts of the southern North Sea, the abundance of juveniles and adults is too low to be sampled properly by means of a single grab sample. Because of their low catch efficiency and size selectivity, beamtrawls do not allow reliable density estimates either (Witbaard and Klein, 1994; Craeymeersch et al., 1998; Groenewold and Bergman, unpubl. ms). Such problems are circumvented by the Triple-D benthos dredge (Bergman and Van Santbrink, 1994), which collects infaunal species quantitatively by sampling a maximum of 20 m2 seabed to a depth

Fig. 1. Presence-absence data of Arctica islandica (>10 mm) within the North Sea. Filled dots represent stations where one or more specimens were found in a grab, trawl or Triple-D dredge sample. Open circles represent stations where, despite sampling, no living Arctica were found. The map is based on 1520 records from NIOZ sampling operations between 1972 and 2000 as well as on records from the literature (Van Noort et al., 1979a,b,c,d, 1982, 1983, 1984, 1986; Van Noort and Creutzberg, 1981; Basford et al., 1989; Duineveld et al., 1990; Ku¨nitzer, 1990; Van Moorsel and Waardenburg, 1991; Holtmann and Groenewold, 1992, 1994; Van Moorsel, 1993, 1994; Lavaleye et al., 2000). Inset gives geographical names mentioned in the text.

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of 12 to 18 cm. The dredge has a stretched mesh size of 1.4 cm and retains animals larger than f 10 mm, i.e. juveniles and adults. Therefore, it was not until the Triple-D benthos dredge became operational in 1995 that reliable abundance estimates could be obtained for areas, such as the Oyster Ground, where Arctica is less abundant. From 1995 onwards, 158 single (non-replicated) hauls of 16 to 20 m2 were taken from the Dutch continental shelf. In July 2000 the dredge was used for a detailed survey in the Fladen Ground (northern North Sea), where samples of 4 to 20 m2 were collected from 30 stations. Of all specimens caught in the various sampling campaigns, shell dimensions were measured and age-size relationships (Witbaard et al., 1999) were used to convert shell height to age. Where possible the data have been used to make spatiotemporal comparisons of the population structures. Special attention has been given to the differences in the distribution, abundance and frequency of spat ( < 10 mm), juveniles (10 – 50 mm) and adults (>50 mm) in the south-eastern North Sea (Oyster Ground).

A comparison of the relative abundance of juveniles and adults (>10 mm) obtained from finemeshed beam trawls between 1972 and 1986 (Fig. 2a) (Van Noort et al., 1979a,b,c,d, 1982, 1983, 1984, 1986; Van Noort and Creutzberg, 1981) with those estimated with the same type of gear between 1990 and 1994 (Fig. 2b) (Witbaard, 1997) and the quantitative data obtained by the recent Triple-D hauls in 1995 – 2000 (Fig. 3) suggests a change in the distribution in the south-eastern North Sea. The early data (Fig. 2) show that Arctica occurred in relatively dense patches just north of the 30-m depth line, i.e. between 1972 and 1986 dense patches were found west of 04j48VE and between 1990 and 1994 such patches were observed east of 04j48VE. In recent years (>1995), a similar distribution pattern was obtained with hauls by the Triple-D dredge although

3. Results 3.1. Distribution Records of Arctica compiled from non-quantitative grab and trawl samples since 1972, similar records from the literature, and from the quantitative Triple-D dredge samples were used to construct a comprehensive map on the occurrence of juvenile and adult Arctica within the North Sea (Fig. 1). This map shows that Arctica is widely distributed over the entire North Sea north of the 30 m depth contour at 53j30VN. Despite the intensive sampling programs in the Dutch continental sector, living Arctica have never been reported from the Southern Bight, south of this latitude (Van Noort et al., 1979a,b,c,d, 1982, 1983, 1984, 1986; Van Noort and Creutzberg, 1981; Holtmann and Groenewold, 1992, 1994; Daan and Mulder, 2000; Lavaleye et al., 2000). Along the Danish coast the 30-m depth contour similarly seems to limit coastward extension.

Fig. 2. A comparison of non-quantitative density estimates of Arctica islandica (>10 mm) in the Oyster Ground based on 5-m beam trawl catches (fine-meshed nets with a stretched mesh size of 2 cm in the cod end). Density is given in numbers per 10 000 m2. Open circles indicate the absence despite sampling. (a) Abundance as estimated by Van Noort et al. (1979a,b,c,d, 1982, 1983, 1984, 1986) Van Noort and Creutzberg (1981) between 1972 and 1986; (b) densities determined from cruises with RV ‘Aurelia’ and RV ‘Pelagia’ between 1990 and 1994 (Witbaard, 1997).

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Fig. 3. The distribution and abundance (n 100 m 2) of Arctica islandica (shell size >10 mm) in and around the Oyster Ground as sampled by the Triple-D benthos dredge in 158 single hauls of 16 – 20 m2 between 1995 and 2000. The shaded area accommodates the highest densities of juvenile and adult Arctica. Dotted line indicates the border of the Dutch continental shelf.

the data suggest that the southernmost distribution limit east of 04j48VE has shifted slightly to the north since 1994. Although the sampling effort in the central and northern North Sea was less intensive than in the southern section, the station grid used for the ICES benthic survey (Duineveld et al., 1990, Basford and Eleftheriou, 1988; Basford et al., 1989) and that of De Wilde et al. (1986) nevertheless gives an indication of the scattered and patchy distribution in these northern waters (Fig. 1). Whether this scattered distribution always reflects the actual situation is questionable because at least the larger but less abundant size classes of this bivalve are easily

missed with small-sized grab samplers. This is illustrated by the fact that neither McIntyre (1961) nor Hartwig et al. (1983) reported full-grown Arctica in their earlier grab surveys in the Fladen Ground (northern North Sea), whereas De Wilde et al. (1986) found high numbers of adults in boxcores in the same area in 1983. The age and size structure of these specimens (Witbaard et al., 1999) indicated that these adults must have been there for tens of years, and thus were apparently missed in the earlier surveys. In 1983 the survey of De Wilde et al. (1986) along the 00j30VE transect revealed that Arctica occurred in at least two clusters of stations, one at

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58j42VN and another at 59j20VN. Later, the boxcorer sampling by Basford et al. (1989) confirmed these results, although their coarse sampling grid could not add much detail. In July 2000, the area was re-sampled by means of the quantitative Triple-D benthos dredge, to cover the gaps in the foregoing sampling programs (Fig. 4). The results confirmed the earlier findings, viz. relatively high densities of Arctica in the two clusters of stations as mentioned above, whereas the densities at the intermediate stations were much lower. Moreover, the

Fig. 4. Distribution and abundance (n m 2) of Arctica islandica (>10 mm) in the Fladen Ground along the 00j30VE transect in the northern North Sea as measured during a cruise with RV ‘Pelagia’ in July 2000. Samples of 4 to 20 m 2 were taken with the Triple-D benthos dredge.

results demonstrated that the geographical distribution of Arctica in the Fladen Ground had been stable for almost 20 years. 3.2. Density In extensive areas of the North Sea, densities of adult Arctica are so low that they are rarely found in traditional grab samples. It is only in the central Fladen Ground (northern North Sea) that almost every boxcore sample yields one or more adult specimens (De Wilde et al., 1986). For this area, they found an average density of 12 ind m 2, and hence, Arctica comprised up to 75% of the total biomass locally. In 1991 beam trawling confirmed the presence of Arctica patches with high densities (Witbaard, 1996; Witbaard et al., 1997). The quantitative sampling with the Triple-D dredge in July 2000, which catches all specimens larger than 10 mm, estimated local densities up to 286 individuals m 2 in the northern cluster of stations and 23 individuals m 2 in the southern cluster (Figs. 4 and 6). Hauls of the Triple-D dredge in the south eastern North Sea covering the entire Oyster Ground from the southern border up to the Dogger Bank showed that here the average density was generally low (Fig. 3), viz. 7 ind 100 m 2. Relatively high densities were found just north of the Dogger Bank, with 14 to 27 ind 100 m 2. In the central Oyster Ground (shaded area in Fig. 3) maximum densities up to 35 ind 100 m 2 were found. Outside these two areas densities were an order of magnitude lower. In the central parts of the Oyster Ground (shaded area in Fig. 3) the mean density was 21 ind 100 m 2 and the variance-to-mean ratio (cv), which is considered to be a measure of dispersion, was as low as 0.47, suggesting a rather uniform distribution on this scale which would imply that the density estimates based on single hauls can be considered to be reliable. Dispersion patterns over wider scales i.e., covering the entire Oyster Ground, appear to be more patchy with a mean density of 7 ind 100 m 2 and a cv of 1.27. 3.3. Population size structure Size frequency distributions were constructed for several parts of the North Sea (see Fig. 1), viz. the

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Fladen Ground, Oyster Ground, and Silverpit (Fig. 5). A bimodal size distribution was found for both the Fladen Ground (Fig. 5a and b) and Silverpit (Fig. 5c). Such bimodality was less pronounced or even absent in the Oyster Ground samples (Fig. 5d, e, f). In May 1983, the population in the Fladen Ground was numerically dominated by specimens

Fig. 5. The size frequency distributions of Arctica islandica populations in the North Sea. (a) Fladen Ground sampled by boxcorer in 1983 (50 individuals); (b) Fladen Ground sampled by the Triple-D dredge in July 2000 (5859 individuals); (c) North edge of the Silverpit (54j08VN, 02j12VE) sampled by 5-m beam trawl with fine-meshed net in 1993 (65 individuals); (d) Oyster Ground sampled by 5-m-wide fine-meshed beam trawl between 1990 and 1994 (975 individuals; (e) Oyster Ground sampled by the Triple-D dredge between 1996 and 2000 (430 individuals); (f), central Oyster Ground, i.e. shaded area in Fig. 3, sampled in 1997 by the Triple-D benthos dredge (61 individuals). In each panel a vertical dotted line indicates the minimum shell size under which the sampling gear used is expected to have underestimated the size classes due to mesh size selection. In (a) and (b) the year in which the largest cohorts settled is indicated.

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with shell heights of approximately 35 mm (Fig. 5a) which must have settled in the late 1960s. This cohort was still recognisable in the samples taken in July 2000, 17 years later. In July 2000 newly settled small specimens with shell heights between 10 and 20 mm were dominant (Fig. 5b). The agesize relationship (Witbaard et al., 1999) of these specimens suggests that they settled in 1995. Over the last 30 years, successful recruitment apparently occurred only twice with an interval of about 25 years. Fig. 6 depicts the spatial variation in size frequency distributions in the Fladen Ground, and indicates that not all sampled stations had the same size class distribution. The stations north of 59jN are dominated by the recently (1995) settled cohort, whereas this cohort is less abundant at more southern stations. In contrast to the population in the Fladen Ground, the Arctica population in the Oyster Ground was dominated by adult specimens with shell heights above 50 mm (Fig. 5d, e, f). Specimens with shell heights less than 50 mm are not only extremely rare, but seem to be concentrated in the most central parts of the Oyster Ground (c.f. Fig. 5e and f). This central area (shaded area in Fig. 3) accommodates 68% of all individuals in this size class, whereas only 39% of all animals larger than 50 mm were found in this area. The fraction of specimens smaller than 50 mm in this central area was significantly higher than would have been expected if the size classes had had an even distribution over the Oyster Ground (p = 0.01; Pearson’s m2-test). However, despite the relatively high abundance of smaller individuals in the central area, the population structure is still strongly skewed towards the larger size classes (Fig. 5f). The relative absence of animals smaller than 50 mm in the Oyster Ground could be due to a lack of settlers. To study this relationship we compiled abundance data of f 1-y-old Arctica spat ( < 10 mm) as recorded in the monitoring program BIOMON with boxcore samples taken each spring between 1995 and 2000 (Holtmann et al., 1996, 1997, 1998, 1999; Daan and Mulder, 2000, 2001). The emerging pattern (Fig. 7) shows that spat was found most frequently and in the highest densities in the same central area of the Oyster Ground which

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Fig. 7. The mean abundance and frequency of settlement of Arctica islandica spat ( < 10 mm) in single boxcore samples from the southern North Sea collected each spring between 1995 and 2000 (Holtmann et al., 1996, 1997, 1998, 1999; Daan and Mulder, 2000, 2001). Numbers within each circle indicate average density (n m 2) of spat over the 6-year period. Greyscale of each circle indicates the frequency of settlement within the 6-year period. The shaded area accommodates the highest densities of juvenile and adult Arctica.

contains the highest densities of juveniles and adults (shaded area in Fig. 3).

4. Discussion 4.1. Methodological remarks One of the greatest difficulties in comparing (historical) abundance data of rare and sparsely distributed macro-benthic species such as Arctica islandica is that the data have been collected with various types of gear. A. islandica lives in a variety of sediment

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types just buried beneath the sediment-water interface. The potential depth penetration of most bottom-samplers is sufficiently large to sample Arctica. Grab performance is, however, highly dependent on sediment type. It is often reduced in hard sediments, and this may lead to a biased data-set, viz. an underestimation of the abundance in hard sandy sediments. Another problem associated with the use of grabs is the scale difference between the small sample size and the actual density. Density differs between areas and often correlates with the age structure of the populations studied. The abundance of spat and occasionally of juveniles is often high enough to be sampled by a few grab samples, but in large areas the abundance of adults may be so low that hundreds of replicate grab samples would be needed to estimate density reliably. In practice, this is hardly feasible in view of the limited resources (ship time) of field programs. Bottom trawls are frequently used as an alternative to estimate densities of such sparsely distributed species. Trawls sample considerably larger bottom surface areas but have the disadvantage of a low catch efficiency for infaunal organisms and, depending on the mesh size of the net, are highly size selective. In view of the low catch efficiency of even heavy commercial beamtrawls (only 5 – 8% for adults; Fonds, 1991; Witbaard and Klein, 1994; Craeymeersch et al., 1998; Groenewold and Bergman, unpubl. ms), the fine-meshed trawl surveys (Fig. 2) may similarly have underestimated the densities and thus yielded conservative estimates. But these finemeshed trawls at least retained the smaller size-classes down to f 2 cm and thus would have given a more complete picture of the population structure. These methodological problems initiated the development of the Triple-D dredge. Extensive testing of this equipment showed that the dredge combines the quantitative character of a bottom grab with the advantage of sampling over relatively large bottom surface areas (4– 20 m2) (Bergman and Van Santbrink, 1994). Because the dredge is equipped with a 0.7  0.7 cm net, it retains all specimens larger than

Fig. 6. The size frequency distribution of Arctica islandica (>10 mm) at several stations in the Fladen Ground on basis of Triple-D dredge samples collected in July 2000. Vertical axes give the percentage of specimens in corresponding 5-mm size classes. Numbers between brackets are the total numbers of animals retained from each sample. Numbers in italics are estimated densities in numbers per m2. Latitudes of sampling stations are given on the right-hand side of the graph. The central axis of stations was projected at the 00j30VE longitude. See Fig. 4 for geographical setting of the stations.

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10 mm. Hence the results obtained from this gear yield the best density estimates that can be obtained for less abundant infaunal bivalves such as Arctica islandica. In combination with boxcore samples, the Triple-D data would give a good insight into the population structure. The comparison of the distribution pattern obtained from the recent Triple-D dredge data with the earlier obtained distribution maps on the basis of the combination of trawls and grabs (Fig. 1) yielded similar distribution patterns in the southern North Sea. This indicates that the various methodologies that were used to collect the older data sets supplemented each other adequately to give an overview of the North Sea wide distribution of Arctica. 4.2. Distribution and density The fact that during the last decades hundreds of boxcores and trawls taken from the shallow sandy area south of f 53j30VN did not yield a single specimen of Arctica islandica convinced us that this bivalve is really absent from the Southern Bight. The southern limit coincides with the 30 m depth contour (Fig. 1), which borders the southernmost limit of the summer stratified water mass of the Oyster Ground with bottom water temperatures never exceeding 16 jC and similarly marks the transition to the shallow tidally mixed southern waters with coarser, less silty sands. The reasons for the sharp delimitation in the presence of Arctica could thus be manifold. Bearse (1976) showed that the fine sediment fractions were more useful to differentiate between absence and presence of Arctica than organic matter content or water depth. Although the derived discriminatant functions had a high predictive power, they did not yield consistent results for different areas. Hence, (part of) the observed relationship between sediment characteristics and Arctica abundance could be noncausative. The Arctica distribution in the North Sea supports this conclusion, since, although the highest densities of Arctica are found in areas with fine sediments (Figs. 1 and 3), they also occur in sandy and gravel bottoms (south-western corner of Dogger Bank (54j55VN, 01j72E), Monkey Bank (56j30VN 06j00VE), Cleaver Bank (54j08VN 03j14VE), or the northern edge of the Silverpit (Outer Well Bank

(54j08VN, 02j12VE)). Apparently, their occurrence is positively correlated, but not exclusively determined, by the presence of fine-grained sediments. It remains unexplained why fine sediments favour high densities because growth rates of Arctica seem to be depressed in areas with fine sediments, suggesting sub-optimal food conditions (Witbaard et al., 1999, 2001). Other experimental studies indeed demonstrated adverse effects of high loads of resuspended sediment on bivalve growth because the admixture of fine silty particles lowered the quality of the food particles (Grizzle and Morin, 1989; Cranford et al., 1998; Gremare et al., 1998). The high densities of Arctica in the fine-grained sediments thus do not necessarily reflect the best sites for growth and one might wonder why Arctica is not a common inhabitant of the more southern sandy North Sea, where food conditions in terms of quality tend to be better (Duineveld and Boon, 2002). One plausible reason for the absence of Arctica in the shallow southern Bight could be that the high water temperatures in summer exceed their upper limit (16 – 18jC, Merrill et al., 1969) for survival. Another possible explanation for the predominant occurrence of Arctica in fine-grained sediments can be found in the dispersion of pelagic larvae and their survival as settlers. Once the pelagic larvae are present in the water column, either produced by a local parent stock or by a distant one, their spatial distribution is dependent on hydrography, ontogenetic larval development and associated behavioural traits. Water temperature is a major factor in their development. In experiments, the veliger stage is best reared at temperatures between 10 and 15 jC (Landers, 1976), and a successful metamorphosis into a shelled veliger requires temperatures above 10 jC (Lutz et al., 1982). At temperatures between 8.5 and 10 jC, development becomes prolonged and metamorphosis questionable (Lutz et al., 1982), so that it may take as long as 55 days before settlement takes place (Landers, 1976). Mann and Wolf (1983) furthermore showed that the swimming larvae respond to changes in water temperature and changes in pressure (depth). They demonstrated that the thermal structure of the water masses on the southern New England shelf (Western Atlantic) at the time of spawning gave rise to an accumulation of the larvae in or below the thermocline. This accumulation originated from the effects of temperature on development and larval

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behaviour. The interaction between hydrography and species specific responses would thus determine the geographical extension and distribution of viable settlers. The water temperature in the central Oyster Ground (Tomczak and Goedecke, 1964) during the period of spawning remains within the limits for proper larval development, and the thermal structure of the area is very similar to that described by Mann and Wolf (1983) for the southern New England shelf. We therefore assume that the stratified water column in the Oyster Ground similarly leads to an accumulation and aggregation of larvae in or below the seasonal thermocline. The seasonally stratified waters overlying the deeper central parts of the area have summer temperatures generally between 12 and 20 jC. There, the larvae successfully develop and survive, while conditions for development and survival deteriorate along the (southern) margins of this stratified area. This would also hold for survival of early settlers, which might particularly suffer from high water temperatures and high bottom currents outside the stratified area. The abundance of spat ( < 10 mm) in sediment cores collected in spring 1986 from all over the south-eastern North Sea (Duineveld et al., 1990, 1991; c.f. map in Witbaard et al., 1994) as well as the mean abundance and frequency of larval settlement in six recent years (Fig. 7) indeed points to coinciding distributions of settlers and the area for summer stratification of the deeper central Oyster Ground. The relatively high abundance of juveniles with heights between 10 and 50 mm in the central Oyster Ground (Figs. 3 and 5f) similarly suggests a more regular settlement in this area and thus supports the proposed link between stratification and settlement as postulated by Mann and Wolf (1983). 4.3. Population size structure The inter-annual variability in the spatial extent of the stratification will give rise to spatial differences in the distribution of yearly spatfalls, but it is doubtful whether these differences alone could lead to the odd size and age structures found in the Oyster Ground (Fig. 5e). That natural processes can be responsible for the temporal variability in bivalve settlers and especially Arctica is well known (see Zettler et al.,

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2001). This is also illustrated by the Triple-D data from the hydrographically stable Fladen Ground (Fig. 5b), where years with strong cohorts have alternated with long periods without such extremely successful settlement events. Unfortunately we have no data on the frequency (over years) and abundance of spat ( < 10 mm) in the Fladen Ground. But Fig. 5 (a and b) suggests that despite the occurrence of irregular and extremely successful settlements, less abundant spatfalls in intermediate years can result in a dense population with a large proportion of juveniles. The skewed size distribution in the Oyster Ground, where animals under 14 years of age were almost completely lacking, could similarly be due to an erratic but natural variability in settlement. It should, however, be admitted that the skewness of the population in the Oyster Ground as based on the Triple D catches (Fig. 5e, f) is rather extreme in view of the regular spatfalls as suggested by Fig. 7. Apparently the recruitment of this spat to the juvenile and adult phase is negligible, which suggests that these average spat densities are insufficient to compensate for the high mortality rates during this first phase of life. The mean density of spat (Fig. 7) in the Oyster Ground is indeed low, as it is only 5% of the densities measured in settlement experiments in the Baltic (Arntz and Rumohr, 1982) or those which would be needed to sustain the densities of juveniles as found in the Fladen Ground (Fig. 6). The extent to which the magnitude of the adult population plays a role in the occurrence of sufficiently strong year classes is hard to assess but an obvious explanation for the low abundance of spat in the Oyster Ground could be the low density of reproductively active adults (Fig. 3). Low adult densities would lower the fertilisation success and thus the number of available larvae. One of the factors that have controlled the size of the adult stock in the Oyster Ground over the last decades is the intensive beam trawl fisheries for flatfish (Witbaard and Klein, 1994; Bergman and Lindeboom, 1999). Several studies demonstrated that beam trawl fisheries affect Arctica populations by inducing direct mortality due to physical damage either in the trawl net or in the trawl track (Bergman and Van Santbrink, 2000; Groenewold and Bergman, unpubl. ms). The overall annual fishing mortality in adult Arctica populations on the Dutch continental shelf inflicted by commercial beam

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trawl fleets is calculated at 11% for 1994 (Bergman and Van Santbrink, 2000). This additional mortality would have been enough to decimate the population of adults in the Oyster Ground within ca 25 years, resulting in present-day densities of only 10 ind 100 m 2, which are low compared to those in the Fladen Ground. The frequent, but small, settlement in the central parts of the Oyster Ground in recent years (Fig. 7) did not result in a dense population of juveniles (Fig. 5f). Closer inspection of the data suggests that this spat must have died before they reached an age of f 2 years, i.e. a height of 10 mm, since they were rarely caught with boxcores (Daan and Mulder, 2001). As with adults, bottom trawling could be a cause of increased mortality of spat. Bergman and Hup (1992) estimated that the direct mortality due to a single haul of a beamtrawl for 2 –3 mm large Arctica is at least as high as for adults (20%). It is feasible that juveniles (10 – 50 mm) endure an even higher direct mortality because they live shallower within the sediment, have thinner shells and are thus more easily hit and broken than adults (Witbaard and Klein, 1994), but on the other hand they are not so easily blown away by the bow wave of the trawl as spat (Bergman and Van Santbrink, 2000). Besides the direct fishing mortality, spat and juveniles in particular may suffer from the indirect effects of trawling. Changes in habitat structure, e.g. sediment stability, could decrease their survival rates, whereas changes in food web structure, favouring specialised predators such as Astropecten or Buccinum (Nielsen, 1975) might enhance rates of predation upon them. The direct and indirect impacts of beam trawl fisheries in controlling the population structure of Arctica is supported by several field observations. In the Fladen Ground, which is a hydrographically stable and a less intensely fished area, Arctica populations tend to be stable over long periods of time (Fig. 5a, b) which contrasts with our observations for the intensely fished south-eastern North Sea. The observations that Arctica decreased in abundance at some of the locations along its southernmost border in the Oyster Ground as suggested by the comparison of Figs. 2 and 3 coincide with the designation of the ‘Plaice Box’ just south of this region in 1995. The closure of that area for trawlers of >300 Hp probably led to locally increased fishing

intensity at the border between the ‘Plaice Box’ and the Oyster Ground as already suggested by Lavaleye (1999) on the basis of maps recently published in Rijnsdorp et al. (2001). We similarly observed the abrupt disappearance of an Arctica patch from the northern edge of the Silverpit. In 1993 this population was successfully sampled and had a size class distribution (Fig. 5c) in which smaller adults were well represented. An attempt to resample this population in 1998 was unsuccessful: only damaged and empty shells were collected. This disappearance was most probably caused by fishery disturbance, since we would have expected intact empty doublets if a natural catastrophic event had been responsible. The data presented here indicate that the Oyster Ground is actually the southernmost border of the distribution of Arctica in the North Sea, which could imply that conditions for survival are marginal. The data for the Mecklenburg Bight (Baltic) presented by Zettler et al. (2001), however, suggest that conditions on the margins of distributional range do not necessarily lead to low densities. We therefore think that, for the southern North Sea, the chronically increased mortality rate due to bottom trawling, in addition to the natural variability in settlement and mortality, may have (had) a disproportionally large impact on the population. Given the skewed age structure in the Oyster Ground, the low numbers present seem to be a remnant of what once was a thriving population. The first data on the genetic structure of Arctica populations in the North Sea suggest a high degree of reproductive isolation (Holmes et al., 2003) and it is thus questionable whether the population in the Oyster Ground is fed by larval supply from elsewhere. The likely absence of an external source of larvae will have major consequences for the longterm survival of the decimated population in the Oyster Ground under present day conditions. To secure the survival of such a population, the impact of fisheries should be diminished either by changing fishery methods or by designation of protected areas, but even then it is doubtful whether the population in the Oyster Ground will be viable and able to recover in the future. At present we can only speculate on the future development of this population in the absence of fisheries.

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Acknowledgements This paper could not have been presented without the assistance of colleagues, friends, and crews from research vessels and commercial trawlers. We would especially like to thank A.R. Boeyen for the supply of many samples from the North Sea and the crew of RV ‘Pelagia’ for their major contribution in collecting Arctica. Dr A. Eleftheriou and D. Basford deserve special thanks for their supply of distribution data of Arctica in the northern North Sea. G.C.A. Duineveld and I. Williams are acknowledged for their helpful comments on the manuscript. Part of this work has been made possible by NWO grant no 750-700-02.

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