Would adding scallop shells (Chlamys islandica) to the sea bottom enhance recruitment of commercial species?

Journal of Experimental Marine Biology and Ecology 312 (2004) 299 – 317 www.elsevier.com/locate/jembe

Would adding scallop shells (Chlamys islandica) to the sea bottom enhance recruitment of commercial species? Martin Guay*, John H. Himmelman De´partement de biologie, Universite´ Laval, Que´bec City, Canada G1K 7P4 Received 31 March 2004; received in revised form 20 June 2004; accepted 17 July 2004

Abstract We examined the impact of adding scallop shells (byproduct of the fisheries) to sandy and rocky sea bottoms in the northern Gulf of St. Lawrence. The effect of adding shells was greatest on sandy bottoms where species richness increased 3.7-fold and species diversity 1.9-fold. The increase in most species was due to immigration rather than new settlement. Trials examining the effect of different densities of shells in plots of the same size (4 m2) showed that species diversity increased rapidly with shell abundance and levelled off when shells covered half of the bottom, whereas species richness only levelled off when shells almost completely covered the bottom. Trials examining the effect of the size of the shell patches (shell density being kept constant) showed that species diversity was already maximal in 1-m2 plots, whereas species richness only attained a plateau at 4 m2. Our small-scale trials indicate that the addition of shells would have a positive impact, increasing numerous invertebrates, including commercial species (scallops, whelks and urchins). D 2004 Elsevier B.V. All rights reserved. Keywords: Chlamys islandica; Commercial species; Sea bottom; Immigration

1. Introduction Species richness, diversity and abundance in marine benthic communities generally increase with substratum heterogeneity (Emson and Faller-Fritsch, 1976; Raffaelli and * Corresponding author. E-mail addresses: [email protected] (M. Guay)8 [email protected] (J.H. Himmelman). 0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2004.07.008

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Hughes, 1978; Menge et al., 1983, 1985; Chapman and Underwood, 1994). One reason for this is that larval settlement is often favoured where the bottom is more complex (Butman, 1987; Eckman, 1990; Johnson, 1994; Jacobi and Langevin, 1996; Lemire and Bourget, 1996) because of the increased surfaces for settlement (Dean, 1981; Bell, 1985; Bros, 1987) and increased larval retention related to the decrease in current velocity caused by heterogeneity (Breitburg et al., 1995). Another reason is that the thicker boundary layer created by heterogeneity may increase the availability of suspended food particles for filter feeding species (Jumars and Nowell, 1984; Frechette et al., 1989). Heterogeneity may also provide refuges for invertebrates from predators (Menge and Sutherland, 1976; Vince et al., 1976, Brock, 1979; Nelson, 1979; Russ, 1980; Coen et al., 1981; Heck and Thoman, 1981; Crowder and Cooper, 1982; Peterson, 1982; Coull and Wells, 1983; Gillinsky, 1984; Marinelli and Coull, 1987; Russo, 1987; Ryer, 1988; Gotceitas and Colgan, 1989), and stress from strong currents (Guichard and Bourget, 1998), or reduce interspecific competition (Buss and Jackson, 1979; Walters and Wethey, 1986). Many studies have evaluated community changes resulting from artificially increasing heterogeneity (Emson and Faller-Fritsch, 1976; Raffaelli and Hughes, 1978; Bros, 1987). The results of these studies have also been applied, as when artificial habitats are created (e.g., adding concrete blocks and lobster shelters to the bottom) to increase recreational or commercial fishing yield (Bohnsack, 1989; Butler and Hernnkind, 1997; Briones-Fourzan and Lozano-Alvarez, 2001). Unfortunately, human activities more often decrease bottom heterogeneity, a major example being the use of trawls and dredges to harvest benthic species. Such practices flatten the bottom (Currie and Gregory, 1996; Robinson et al., 2001) and often destroy the physical structures provided by benthic organisms, such as emergent worm tubes, empty and living bivalve shells and algal assemblages (Eleftheriou and Robertson, 1992; Auster, 1998). The disappearance of such structures and the destruction of organisms decrease the diversity and production of benthic communities (Langton and Robinson, 1990, Eleftheriou and Robertson, 1992, Thrush et al., 1995; Collie et al., 1997). In the northern Gulf of St. Lawrence, a scallop fishery using dredges has existed since the mid-1960s and 205 metric tons were taken in 2001 (MPO, 2002). The fishery mainly harvests the Iceland scallop, Chlamys islandica (O.F. Mqller). Most of the scallops are shucked to harvest the muscle and the remaining tissues and shells are thrown overboard, 30–40% being discarded far from scallop beds. In some cases, the scallops are shucked at port and this leads to piles of shells along wharves. Removing scallops and potential shell litter from beds could have a negative impact on scallop populations for several reasons. First, the shells often support the growth of filamentous hydrozoans and red algae (Magee et al., 2000), both favourable substrata for scallop settlement (Harvey et al., 1993; Arsenault and Himmelman, 1996a). Second, the empty shells provide juvenile Iceland scallops with refuge from benthic predators, particularly from crabs (Arsenault and Himmelman, 1996a, b). Finally, shell litter may be advantageous as scallops grow faster under shells than on exposed surfaces (Arsenault et al., 1997). The latter is because Iceland scallop beds are usually found in areas with strong tidal currents (Gilkinson, 1991), and as shown for giant scallops (Wildish et al., 1987; Wildish and Saulmier, 1992), the reduction in current velocity in crevices and under shells results in longer periods when feeding is not inhibited by high current speeds.

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Given the possible advantages of shell litter for scallop populations, it may be beneficial if the shells of scallops taken by the fishery were returned to specific locations, e.g., by shucking all the scallops over scallop beds. It is also possible that the heterogeneity provided by scallop shells would benefit other commercial species. For example, Bros (1987) showed that the addition of barnacle shells to benthic communities in Florida increased species richness as a result of new settlement and immigration. The present study evaluates the impact of adding Iceland scallop shells to different types of sea bottoms in the Mingan Islands in the northern Gulf of St. Lawrence. To this end, we added a given quantity of shells to experimental plots on sandy and rocky bottoms and 1 year later compared the shell addition plots with plots where no shells had been added. To obtain indications of the generality of our results, we also ran experiments to examine the effect of varying the density of shells in an experimental area, and the effect of changes in size of the shell plots when the density was maintained constant. Our study aimed to provide information pertinent to habitat and fishery management.

2. Methods 2.1. Study sites Our study was conducted during 1999 and 2000 in the Mingan Islands in the northern Gulf of St. Lawrence, eastern Canada (Fig. 1). The various experiments on the impact of adding Iceland scallop shells to the bottom were set up at a depth of 13–20 m at 10 sites (Fig. 1), five with sandy bottoms (N90% of the bottom was covered with substratum particles measuring b1 mm) and five with rocky bottoms (N50% of the bottom was covered with particles measuring 1–10 mm). One of the rocky bottom sites was at the upper edge of a scallop bed at the southern side of Iˆle du Fantoˆme (the bed studied by Arsenault and Himmelman, 1996a, b; 1998). This scallop bed is unusual because of its shallow depth. 2.2. Impact of adding shells to sandy and rocky bottoms We tested the impact of adding shells to the sea bottom by comparing the characteristics of 4-m2 plots (1.2 m in diameter) where we added shells with 4-m2 control plots where no shells were added. At each of 10 sites, four pairs of shell addition and control plots (considered as blocks in the statistical analysis) were placed at 10-m intervals along a transect line. The paired plots were separated by 4 m on opposite sides of the transect lines. The experiment was initiated in July and August 1999 by covering one plot in each pair (chosen at random) with 50-l volume of Iceland scallop shells (700–900 valves with a mean height of ~80 mm). One year later, in June to August 2000, we returned to characterize the experimental and control plots, except for those at one sandy site where the shell plots had almost completely disappeared (site 10; Fig. 1). Each plot was sampled with two 0.25 m2 quadrats (5050 cm) to record the number and size of all macroinvertebrates present, except for the

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Fig. 1. Location of study sites on rocky bottoms: (1) northern Grosse Iˆle au Marteau, (2) northeastern Grosse Iˆle au Marteau, (3) southern Iˆle au Fantoˆme, (4) southwestern Iˆle au Fantoˆme, (5) western Iˆle au Fantoˆme, and sandy bottoms, (6) eastern Petite Iˆle au Marteau, (7) southeastern Petite Iˆle au Marteau, (8) northern Iˆle aux Goe´lands, (9) eastern Iˆle aux Goe´lands and (10) southern Iˆle du Havre.

ophiuroid, Ophiopholis aculeata. Given the limited time we could spend doing the underwater sampling (due to cold temperatures and the limited time we could spend diving), we chose to focus on the other species for which patterns were less evident. O. aculeata is absent on sandy bottoms where there is no debris but is always abundant as soon as there are rocks and shell litter. In each quadrat, we carefully turned over every rock and shell, to not overlook any organisms. Furthermore, we noted the position of each organism (under or upper side of shells). In the same quadrat sampling, we also quantified the percentage cover of three substratum categories (sand, b1 mm; pebbles, b10 cm; and cobbles, 10–30 cm). Boulders (N30 cm) and bedrock were absent. 2.3. Impact of shell density and size of the shell patches To test the effect of shell density and plot size, we set up additional experiments in 1999 at a site with a sandy bottom (sites 8, Fig. 1). We ran trials with four densities (0, 250, 500 and 1000 shells per 4-m2 circular plot) and also with three sizes of plot (1, 4, and 8 m2). Each series of treatments (the four densities, or the three plot sizes) was grouped and repeated four times. In 2000, the density trial plots were sampled with two 0.25-m2 quadrats, in the same way as the trials on sandy and rocky bottoms. For the plot size trials, the control, and the 4-m2 plots were also sampled with two 0.25-m2 quadrats, but the 1-m2 plots were sampled with only one quadrat and the 8-m2 plots were sampled with four quadrats, two near the centre and two near the edge.

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2.4. Statistics The data on species diversity and richness, as well as on abundance of each common invertebrate, for the four sandy bottom sites and the five rocky bottom sites were analysed using mixed model ANOVAs. The factors were Bottom type, Site (nested in Bottom type), Block (nested in SiteBottom type) and Shells or not. Post hoc comparisons were made using LSD tests. Species diversity was calculated using Shannon’s Index (HV= Ap i lnp i , where p i is the relative abundance of the ith species). We used ANOVAs with four randomised blocks to analyse the data on species richness and diversity, and on the density of each common invertebrate from the shell density and plot size experiments. The factors examined were either shell density (four levels: the three densities of shells added, plus control plots where no shells were added) or the size of the shell patches (five levels: 1, 4, 8 m2 edge, 8 m2 center, plus a control where no shells were added).

3. Results 3.1. Effect of adding shells to sandy and rocky bottoms Sampling of bottom sediment types showed the sandy bottom sites were quite homogeneous, 95% or more of the substratum being sand. The rocky bottom sites were more variable. Gravel and cobbles together always accounted for N55% of the substratum, but sand was always present (10–45%). The density of shells in the shell plots in 2000 (1 year after the addition of shells) varied from 84 to 263 m 2 for the sandy bottom sites and from 130 to 214 m 2 for the rocky bottom sites. In most cases, the shells covered the 4-m2 plots with about one layer of shells. The analysis applied to the data from the quadrat sampling of the 4-m2 experimental plots, first showed a major effect of bottom type. This factor affected both species richness and diversity and also the density of all the common species recorded (Table 1). Overall, the analyses also showed a significant effect of adding shells on species richness, diversity, and on the density of all common species (Fig. 2), and the effect of adding shells varied with the type of bottom, except for Margarites groenlandicus (Table 1). Species richness almost quadrupled with the addition of shells on sandy bottoms (and became similar to that normally found on rocky bottoms), whereas it only increased by 35% on rocky bottoms. Species diversity almost doubled with the addition of shells on sandy bottoms, whereas it only increased slightly on rocky bottoms. The most frequently encountered species in our study can be grouped into potentially commercial species, predatory species, and other species. For the three species of potential commercial value, the Iceland scallop C. islandica, the common whelk Buccinum undatum, and the green sea urchin Strongylocentrotus droebachiensis, we observed a positive effect of the addition of shells. Shell addition caused a ninefold increase in the density of scallops on rocky bottom (Fig. 2). However, on sandy bottoms no significant increase was observed (scallops were present in low numbers in shell addition plots, and not encountered in control plots). Wallace (1982) and Thorarinsdo´ttir (1991) indicate that 1-year-old C.

304

Table 1

Results of mixed model ANOVAs evaluating the effect of the addition of scallop shells to sandy and rocky bottoms on species richness, species diversity and the density of the common invertebrates df

MS

F

P

MS

F

P

MS

Bottom type Site Shells or not Bottom typeShells or not Shells or notSite Error

1 7 1 1 7 67

Species richness 386.3 4.9 283.9 31.3 2.7 2.3

164.0 2.1 120.5 13.3 1.1

b0.001 0.082 b0.001 0.001 0.37

Diversity 2.7 0.1 1.8 0.5 0.03 0.02

163.9 6.5 112.7 30.9 2.0

b0.001 b0.001 b0.001 b0.001 0.091

Chlamys islandica 1.8 6.5 0.7 2.5 5.2 18.3 1.5 5.4 0.6 2.0 0.3

0.02 0.04 b0.001 0.03 0.09

Bottom type Site Shells or not Bottom typeShells or not Shells or notSite Error

1 7 1 1 7 67

Leptasterias polaris 29.4 67.2 12.7 29.2 8.6 19.7 3.9 9.0 1.8 4.1 0.4

b0.001 b0.001 b0.001 0.006 0.004

Abietinaria abietina 29.1 42.2 3.6 5.2 24.9 36.0 16.9 24.5 1.8 2.6 0.7

b0.001 0.001 b0.001 b0.001 0.04

Margarites groenlandicus 228.3 45.8 27.2 5.5 112.6 22.6 13.1 2.6 4.3 0.9 5.0

b0.001 b0.001 b0.001 0.11 0.54

Bottom type Site Shells or not Bottom typeShells or not Shells or notSite Error

1 7 1 1 7 67

Hyas araneus 3.4 1.0 21.8 1.2 0.7 0.2

b0.001 b0.001 b0.001 0.015 0.007

Buccinum undatum 36.8 40.4 2.6 2.8 73.7 81.1 39.4 43.3 1.7 1.9 0.9

b0.001 0.03 b0.001 b0.001 0.11

Strongylocentrotus droebachiensis 3.3 15.7 b0.001 1.3 6.3 b0.001 24.3 115.2 b0.001 17.3 82.1 b0.001 0.8 4.0 0.005 0.2

Bottom type Site Shells or not Bottom typeShells or not Shells or notSite Error

1 7 1 1 7 67

Lepidonotus squamatus and Harmothoe imbricata 109.0 78.0 b0.001 22.5 16.1 b0.001 40.1 28.7 b0.001 14.4 10.3 0.004 5.6 3.4 0.005 1.4

Acmaea testudinalis 1074.2 138.2 192.9 24.8 58.6 7.5 149.2 19.2 23.8 3.1 7.8

b0.001 b0.001 0.01 b0.001 0.02

Tonicella marmorea 542.3 70.5 119.1 15.5 45.0 5.9 60.0 7.8 20.0 2.6 7.7

19.5 5.9 125.8 6.8 3.7

F

P

b0.001 b0.001 0.02 0.001 0.04

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Fig. 2. Species richness, species diversity, and the density of the common invertebrates, in plots on sandy and rocky bottoms 1 year after the addition of scallop shells (filled bars), and in control plots (open bars) where shells were not added. The error bars are standard errors, and the values above the bars are probabilities from LSD tests comparing shell addition and control plots for each bottom type.

islandica measure 6–10 mm in shell height. Most of the increase in scallops on rocky sites was due to immigration as 73% of the individuals measured N10 mm in shell height. Seventy-seven percent of the b30-mm scallops were found under shells, 14% under rocks compared to only 10% exposed on the bottom. Most adult scallops (N30 mm) in the sampling were from southern Iˆle au Fantoˆme (85%, site 3), the site located in a scallop bed.

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The addition of shells resulted in a significant increase in density of whelks and urchins on sandy bottoms (14- and 20-fold increases, respectively), but only for whelks on rocky bottoms. The increase in whelks was due to immigration, since egg laying occurs from June to mid-July (Martel et al., 1986); thus, before we added the shells, and no egg capsules were present in the experimental plots where we added shells. The increase in urchins with addition of shells on the sandy bottoms was due to both adults and juveniles (84% measured N5 mm and were not recently settled individuals). We observed two main predatory species, the spider crab Hyas araneus, and the sea star, Leptasterias polaris. Overall, the addition of shells resulted in a significant and marked increase in crabs on both sandy and rocky bottoms. The increase on sandy bottoms was almost entirely due to small crabs (90% measured b20 mm in carapace length). A second crab species, Cancer irroratus, was only found in five plots where shells were added, and all were juveniles (20–35 mm in carapace width). For L. polaris, shell addition only caused a significant increase on rocky bottoms (a twofold increase), and sizes reflected those in the control plots. The increase in L. polaris was mainly due to immigration, since only 72% of the individuals measured N5 mm in diameter, and could not have been part of the 1999 brood (L. polaris spawns in autumn and the females brood until April to July; Boivin et al., 1986). A second sea star, Asterias vulgaris, also tended to increase with the addition of shells on rocky bottoms, but the increase was not significant. A number of other invertebrates showed changes in response to the addition of shells. The small herbivorous snail, M. groenlandicus, showed a marked increase on both sandy (eightfold) and rocky (2.3-fold) bottoms, and increases were due to both small (b5 mm in length) and large (N5 mm) snails. Scale worms, Lepidonotus squamatus and Harmothoe imbricata, only showed a significant increase (27-fold) on sandy bottoms. The sizes of the new individuals on the sandy bottoms were similar to those found on the rocky bottom

Table 2

Results of the ANOVAs evaluating the effect of the addition of shells to sandy bottom on species richness, species diversity and the density of the common invertebrates Factor Block Density Error

Block Density Error

df

MS

3 3 9

Species richness 8.8 3.2 0.078 53.8 19.4 b0.001 2.8

Diversity 0.1 1.1 2.6 42.4 0.1

Buccinum undatum

Juvenile Strongylocentrotus droebachiensis 12.9 1.2 0.35 204.7 19.6 b0.001 10.4

Adult Strongylocentrotus droebachiensis 47.2 2.0 0.19 170.4 7.1 0.009 24.0

Leptasterias polaris

Lepidonotus squamatus and Harmothoe imbricata 0.8 0.2 0.88 25.8 7.0 0.010 3.7

3 3 9

11.7 52.6 6.0

F

1.9 8.7

P

0.19 0.005

Hyas araneus Block Density Error

3 3 9

2.4 46.6 5.5

0.4 8.5

0.74 0.005

MS

1.0 2.2 0.5

F

2.3 5.0

P

MS

0.38 b0.001

Chlamys islandica 1.7 1.9 3.6 4.0 0.9

0.15 0.026

F

P 0.21 0.046

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Fig. 3. Relation of species diversity, species richness and the density of common invertebrates to shell density for trials conducted on sandy bottom at the northern side of Iˆle aux Goe´lands (site 8). The error bars are the standard errors, and bars not sharing the same letter are different ( Pb0.05, LSD tests).

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sites. The hydrozoan, Abietinaria abietina, showed a fourfold increase with the addition of shells on rocky bottom but no change on sandy bottoms (Fig. 2). Finally, the limpet, Acmaea testudinalis, and the chiton, Tonicella marmorea, showed an unusual pattern: an increase with the addition of shells on sandy bottoms (only significant for limpets) in contrast to a decrease on rocky bottoms (Fig. 2). The others species encountered, except for O. aculeata (not sampled), were too rare to permit adequate statistical comparisons of their abundance between shell addition and control plots. 3.2. Effect of adding different densities of shells to sandy bottom In the trials examining the effect of changes in shell density on 4-m2 experimental plots conducted at northern Iˆle aux Goe´lands (site 8), the mean density of shells remaining after 1 year was 81 m 2 (S.E.=17.2) for plots where ~400 valves were added, 173 m 2 (10.4) where ~800 valves were added, and 304 m 2 (20.8) where ~1600 valves were added. Valve density was 7 m 2 (2.0) for the control plots where no shells were added due to the presence of shells of bivalves, Spisula polynyma, Mya truncata and Mya arenaria, which occurred naturally at this site. The substratum at this site was 100% sand. The trials showed an increase in species richness with increasing shell density up to a density of 173 shells m 2, the number required to completely cover the 4-m2 plots (Table 2; Fig. 3). The highest shell density (304 m 2) did not result in a further increase in richness. Species diversity increased more rapidly and a plateau was attained at about 80 shells m 2 (Fig. 3). Examination of the effects of shell density on the various species revealed two general patterns (Fig. 3). The first was a progressive increase in numbers with shell density with no evidence of a plateau, as observed for the scallop, C. islandica, juvenile sea urchins, S. droebachiensis, the sea star, L. polaris, the spider crab H. araneus and scale worms, L. squamatus and H. imbricata. The second was a rapid increase in

Table 3

Results the ANOVAs evaluating the effect of the addition of different size of shell patch to sandy bottom on species richness, species diversity and the density of the common invertebrates Factor

df

MS

Block Patch size Error

3 4 12

F

MS

F

P

MS

Species richness 4.6 1.2 0.34 41.6 11.1 b0.001 3.8

Diversity 0.1 1.2 0.1

1.7 18.6

0.21 b0.001

Buccinum undatum 2.44 0.6 0.64 30.83 7.3 0.003 4.22

Hyas araneus

Strongylocentrotus droebachiensis

2.1 13.2

P

Block Patch size Error

3 4 12

2.2 14.4 1.1

0.16 b0.001

Block Patch size Error

3 4 12

Margarites groenlandicus 1.0 0.5 0.68 12.2 6.1 0.006 2.0

11.8 120.3 8.7

1.4 13.9

0.30 b0.001

F

P

Lepidonotus squamatus and Harmothoe imbricata 0.15 4.5 0.024 0.20 6.2 0.006 0.03

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abundance with shell density to a maximum at the first or second experimental level of shell density, and then no further increase, as observed for the whelk, B. undatum, and adult sea urchins, S. droebachiensis. Three molluscs, M. groenlandicus, A. testudinalis, T. marmorea, and the hydrozoan, A. abietina (data not shown), showed no significant effect of changes in shell density.

Fig. 4. Relation of species diversity, species richness and the density of common invertebrates to the size of shell plots for trials conducted on sandy bottom at the northern side of Iˆle aux Goe´lands (site 8). The error bars are the standard errors, and bars not sharing the same letter are different ( Pb0.05, LSD tests).

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3.3. Effect of adding shell patches of different sizes to sandy bottom In the patch size experiment, the mean density of shells was 137 m 2 (S.E.=22.0) for the 1-m2 plots and 263 m 2 (46) for the 4-m2 plots. The density of the 8-m2 plots was 387 m 2 (27.6) in the centre and 190 m 2 (22) adjacent to the edge. In all shell-addition plots the shells still covered the surface. The mean density of naturally occurring shells in the control plots where no shells were added was 7 m 2 (2.4). The trials showed an increase in species richness with increasing plot size up to a plateau at 4 m2 (Table 3; Fig. 4). Species diversity increased more rapidly and was already maximal at the smallest plot size (1 m2, Fig. 4). Examination of the effect of plot size on the density of the different species revealed two general patterns (Fig. 4). The first, observed for the crab, H. araneus, was a rapid increase in density at the first plot size (1 m2) and no further increase in larger plots. The second, observed for the scallop, C. islandica, the whelk, B. undatum, and the gastropod, M. groenlandicus, was an increase up to a plot size of 4 m2, with no further increase in 8-m2 plot. No significant effect of changes in plot size was observed for M. groenlandicus, A. testudinalis, T. marmorea, L. polaris, and A. abietina (Fig. 4 shows data for the limpet and chiton only). Comparison of the samples taken in the centre and at the edge of the 8-m2 plots showed that scale worms (twofold) and urchins (threefold) were less abundant at the edge than in the centre of the plots. The density of the chiton, T. marmorea, was more than twofold greater at the edge than in the centre, but the difference was not significant (data not shown). No differences between the edge and centre were noted for species richness and diversity, or for the density of the other species sampled. Although we began the experiment by adding the same density of shells to the different sized plots, the density 1 year later was 137 m 2 in the 1-m2 plots, 263 m 2 in the 4-m2 plots and 387 m 2 in the 8-m2 plots (in the center). Shell density was thus a confounding factor. Thus, the changes in the various species between the 1- and 4-m2 plots could have been due to shell density as well as plot size. However, as the shell density trials showed that for 4 out of 10 species, the benefits of shells plateaued at a density 173 shells m 2, the increase to 387 shells m 2 shells in the 8-m2 plots possibly had little effect. None of the species showed an increase between the 4- and 8-m2 plots, in spite of the increase in both plot size and shell density.

4. Discussion Our experimental additions of Iceland scallop shells to sandy and rocky bottoms in the Mingan Islands increased the species richness and diversity of benthic invertebrates. These observations are consistent with the previous studies showing that increasing heterogeneity increases diversity (Menge et al., 1983, 1985; Chapman and Underwood, 1994). The community changes were greater on sandy bottoms, which was likely because the increase in heterogeneity with the addition of shells was greater on sandy than on rocky bottoms. As most of the species in our study have a planktonic larval phase, the increases in the invertebrates with the addition of shells could be due to both larval settlement and

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immigration. An increase in settlement might have been predicted, as the decrease in current by the shells could enhance larval retention (Wright et al., 1990). However, our data show that only a small proportion of the increase in invertebrates could be attributed to newly settled individuals. Most of the individuals were more than a year old and thus had settled prior to the addition of shells. Thus, immigration was the main factor leading to the increase in invertebrates in the shell plots. The ability of biological structures to enhance recruitment through immigration of motile species has been also demonstrated by Dean (1981) and Bros (1987). Many of the invertebrates probably aggregated in the shell patches because these structures provided refuge from predators. In addition, in areas with strong current the Iceland scallop grows more rapidly when it is located under shells, likely because of reduced exposure to high velocity currents that inhibit feeding (Arsenault et al., 1997). The impact of adding shells varied among the different invertebrates according to the type of bottom. For the scallop, the much greater increase on rocky bottoms was probably because scallops are present in rocky habitats whereas they are virtually absent on sandy bottoms. Iceland scallops usually occur on rocky bottoms (Gilkinson, 1991) where there are suitable settlement substrata (hydrozoans and red algae; Harvey et al., 1993; Arsenault and Himmelman, 1996a) and also refuges to protect juveniles from predators such as crabs (Arsenault and Himmelman, 1996a, b). The movement of scallops into our artificial shell patches provides further evidence of the importance of refuges to their survival and abundance. Although scallop numbers did not increase on sandy bottoms in our main shell addition experiment, we did observe a significant increase at the highest shell density in the shell density experiment on sandy bottom. Given that scallops are extremely rare on sandy bottoms, these individuals had probably immigrated from rocky areas. This would mean covering considerable distances over sand, as the nearest rocky habitats were at least 40 m from the shell plots on sandy bottoms. The increase in whelks on both sandy and rocky bottoms was mainly due to juveniles (78% measured b20 mm in shell length). Small whelks are highly vulnerable to predators (Rochette and Himmelman, 1996), and the shell plots likely provided refuge from predators. The marked increase on sandy bottom is not surprising since small individuals are concentrated on sand–mud substratum (Jalbert et al., 1989), although they emerge from egg capsules laid in rocky habitats (Martel et al., 1986). Two herbivores, the small gastropod, M. groenlandicus and the green urchin, S. droebachiensis (urchins b20 mm), may have moved into shell plots to feed as well as to avoid predators, given that algal debris often accumulated on shell patches on sandy bottoms (most frequently Ptilota serrata). The numbers of predatory scale worms, L. squamatus and H. imbricata, sea stars, L. polaris, and crabs, H. araneus, also increased in artificial shell patches. Scale worms only increased on sand, and this was likely because the addition of shells to sand provided a major increase in suitable substrata for attachment and shelter (suitable substrata and refuges are already present on rocky bottoms). As most of the scale worms on the shell patches on sand were not recently settled individuals, they must have migrated from their usual habitat on rocky bottoms, or were transported there by currents. The increase in small L. polaris with the addition of shells to rocky bottoms was possible because the

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shells provided refuge from predators. Small L. polaris are normally found in shallow rocky zones where they feed on small bivalves Mytilus edulis and Hiatella arctica (Himmelman and Dutil, 1991, Gaymer et al., 2001) and they possibly avoid moving onto sand due to increased predation risk or lack of suitable prey. For the crab H. araneus, the increase in abundance in the shell patches was likely the result of both immigration and new settlement. About 55% measured b10 mm in carapace length and may have been recruits of the year (K. Anger, Alfred-Wegener Institut, personal communication). Dumbauld et al. (1993) reported that adding shells to the bottom in an intertidal area in Washington State increased the density of juvenile Dungeness crab, Cancer magister. Ferna´ndez et al. (1993a,b) also reported an increase in C. magister following the addition of shells to mud bottoms. In our region, artificial shell patches may have similarly increased survival of H. araneus. The addition of shells to rocky bottoms resulted in increased abundance of the hydrozoan, A. abietina. Hydrozoans often colonise scallop shells on scallop beds in eastern Canada (Magee et al., 2000). However, we did not observe an increase of A. abietina on sandy bottoms. As the hydrozoan can only recruit by settlement, factors explaining the difference in settlement, or post settlement survival, between the two bottom types remain to be elucidated. The chiton, T. marmorea, and the limpet, A. testudinalis, were the only common invertebrates that were negatively affected by the addition of shells on rocky bottoms. A negative effect of shells on chitons and limpets was also suggested by the density and plot size trials on a sandy bottom. Their densities tended to decrease at the highest density (304 compared to 172 shells m 2) in shell density trials (Fig. 3) and at the largest plot size (8 m2 compared to 4 m2) in the plot size trials (Fig. 4). As these grazers normally live with their ventral foot firmly attached to hard rock surfaces, the addition of shells may have limited their movement and even created barriers. Moreover, both species graze on microalgae films and the shading caused by the overlapping shells likely decreased food abundance over many surfaces (e.g., undersides of shells) and thus rendered foraging less efficient. Both grazers tended to increase with the addition of shells to sandy bottoms (but only significantly for limpets), where the shells represented rare hard substratum for attachment. It is not clear how they immigrated to shell patches on sand, as they are not adapted for crawling on sand. They were possibly transported there by currents. Although we did not quantify the abundance of the ophiuroid O. aculeata in our study, we did note that they were present on shell patches on sand, but absent on sandy bottoms without rocks or shells. Ophiuroids were always common in the many crevices on rocky bottoms, and we did not note a change with the addition of shells. Although our data show that the addition of shells from the scallop fisheries to the sea bottom would increase the abundance of most epibenthic invertebrates, the impact on infaunal species remains unknown. Iribarne et al. (1995) showed that adding oyster shells to a muddy bottom in Grays Harbor Estuary, Washington State, increased mortality of the infaunal bivalve, Macoma balthica, and they attributed this to increased predation by Dungeness crabs. At the same location, Feldman et al. (1997) revealed that a cover of oyster shells reduced recruitment of the ghost shrimp, Neotrypaea californiensis, and attributed this to the reduction in the mud surfaces (selected by the post larvae), and to an

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increase in juvenile mortality from crab predation. Infaunal clams (e.g., Mya truncata and Spisula polynyma) were common on our sandy bottom sites and could have been affected by shell cover. Studies on larger spatial and temporal scales are required to explore the impact of a massive addition of the shells from the scallop fishery to sea bottoms. Our trials on shell density showed that species richness, diversity, and the abundance of most common invertebrates attain a plateau once the bottom is covered by a single layer of shells. In addition, we showed that only a small patch size (1–4 m2) is needed to obtain most of the benefits of the addition of shells. However, the plot density and size trials were only performed on sandy bottoms and should be done for rocky bottoms as well. Moreover, quantitative assessments of shell additions to extensive areas are needed prior to recommending widespread disposal of shells on the sea bottom. Studies must also examine changes over time scales that would reflect the outcome of interspecific interactions among key recruiting species. Shell additions lead to increases in two predatory species, the crab, H. araneus, and the sea star, L. polaris, in just 1 year. Whereas the small size of these predators likely limited their impact, their effectiveness as predators could improve as they grow. On the other hand, some prey species, such as the Iceland scallop (Arsenault and Himmelman, 1996b), may have an increased ability to escape predation as they increase in size. The impact of predation could also change with increased availability of alternative prey (Kean-Howie et al., 1988; Gotceitas and Brown-Joseph, 1993). Finally, some predators may themselves become vulnerable to predators once they outgrow the size of refuges (e.g., fish predation on crabs; Pihl, 1982). A critical question for the scallop fishery is whether disposing of shells in specific locations would increase commercial fisheries yield. Adding the shells to specific sites could involve additional manipulations of shells and costs of transporting shells to disposal sites. These costs would be minimised if all the shells were thrown overboard on the scallop beds before leaving the beds, or if the dumping zones were near return routes to ports. The major bottleneck of Iceland scallop populations is the loss of juveniles to predators (Arsenault and Himmelman, 1998), and the addition of shells to scallop beds could enhance juvenile survival ultimately increasing the yield to the fishery. This improvement could be off set, however, by handling time for the fishers. A pilot program is needed to assess if the increase in scallop stocks (from increased juvenile survival) would outweigh the costs of adding the shells to appropriate areas and sorting the catch from shell litter. Given that many shells will likely be transported away or buried, the fate of shells in different situations should be a major concern in habitat management programs. There are likely few advantages to dumping shells in some sandy bottom locations where the shell would disappear (as at site 10 in our study), and shells might similarly disappear on some muddy bottom areas. Most of our sandy bottom sites retained sufficient shells to cover the bottom and shell transport appeared to be somewhat less on rocky bottoms than on sandy bottoms. Our plot size studies on a sandy bottom also showed that shell disappearance decreases with increasing plot size. Our experiments demonstrate that disposal sites should take into account the species targeted, e.g., sandy sites would be best for whelks and rocky sites for scallops.

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Up until now, the Iceland scallop fishery in the northern Gulf of St. Lawrence, regularly disposes tons of shells with little concern for habitat management. Our small-scale trials indicated that the addition of scallop shells would have a positive impact on sea bottoms, in that they would likely increase the numbers of numerous invertebrates, including several commercial species (scallops, whelks and urchins).

Acknowledgements We dedicate this paper to L.-V. St-Hilaire Gravel who helped with all of the diving work and who later tragically died during voluntary work in Africa. We also thank V. Messier, B. Laberge, P. Gauthier, P. Gagnon, J-F. Raymond, C. Gaymer, M. Dionne for their aid with the field work, and L.E. Johnson and H.E. Guderley for helpful comments on the manuscript. The study was supported by an operating grant from NSERC (National Sciences and Engineering Research Council of Canada) to J.H. Himmelman and M. Guay received support by Que´bec Oce´ans. [SS]

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