Attachment of the juvenile queen scallop (Aequipecten opercularis (L.)) to maerl in mesocosm conditions; juvenile habitat selection

Journal of Experimental Marine Biology and Ecology 306 (2004) 139 – 155 www.elsevier.com/locate/jembe

Attachment of the juvenile queen scallop (Aequipecten opercularis (L.)) to maerl in mesocosm conditions; juvenile habitat selection N.A. Kamenos *, P.G. Moore, J.M. Hall-Spencer

1

University Marine Biological Station Millport, Marine Parade, Isle of Cumbrae, KA28 0EG, Scotland, UK Received 11 June 2003; received in revised form 10 October 2003; accepted 16 October 2003

Abstract Substratum un-acclimated juvenile queen scallops (Aequipecten opercularis) ( < 18 mm and 18 – 30 mm shell height) were released in equal numbers onto pristine live maerl (PLM), impacted dead maerl (IDM), gravel and sand in choice chambers. Their habitat selection was monitored over a 4day period in control and predator treatments (utilising Asterias rubens L. and Carcinus maenas (L.)). Microhabitat use of PLM by juvenile queen scallops and the presence of cues in live maerl were also investigated. In control and predator treatments juvenile queen scallops were observed to attach preferentially to PLM than IDM, gravel or sand. Juvenile queen scallops were observed to maintain a more exposed attachment site in the absence of predators but sought refuge within and between maerl nodules in the presence of both predators. Smaller queen scallops ( < 18 mm shell height) were more efficient at utilising maerl thalli as a refuge. Juvenile A. opercularis showed hierarchical cue responses mediated by predator presence, i.e. responding favourably to a factor associated with live maerl presence irrespective of heterogeneity in the absence of predators but favourably to higher maerl heterogeneity in their presence. If they also preferentially attach to PLM in the field, at some sites where PLM grounds cover large areas, they may thus be considered to constitute ‘nursery areas’. Habitat attachment preference appears to be predetermined and not a result of localised predator avoidance; however, habitat usage changes in the presence of predators. Maerl beds have been shown to be easily damaged by scallop dredging in Scotland and if such nursery areas are

* Corresponding author. Tel.: +44-1475-530581; fax: +44-1475-530601. E-mail address: [email protected] (N.A. Kamenos). 1 Now at Department of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK. 0022-0981/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2003.10.013

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being destroyed extensively in the field, this could damage recruitment to localised adult populations. D 2003 Elsevier B.V. All rights reserved. Keywords: Attachment; Habitat selection; Maerl; Scallop; Micro-habitat use; Scotland

1. Introduction Maerl grounds are formed from loose-lying, normally nongeniculated coralline red algae (Corallinaceae) and are found in areas characterised by high water movements (tidal and/or wave action) in the photic zone. Grounds are composed of high numbers of individual thalli, with individual species showing growth form plasticity (Woelkerling, 1988). Maerl grounds form shallow marine biotopes of high biodiversity, analogous to kelp forests and sea grass beds (Birkett et al., 1998; BIOMAERL team, 1999). Maerl has a significantly higher heterogeneity than common adjacent substrata (Kamenos et al., 2003) and high heterogeneity is known to equate to high biodiversity in many marine systems (Menge et al., 1983; Gilinsky, 1984; Ormond et al., 1997; Himmelman and Guay, 2003). Maerl grounds are easily damaged by towed demersal fishing gears. A single impaction event significantly reduces the heterogeneity of maerl thalli to that of a gravel substratum by breakage and also kills the thalli due to burial (Hall-Spencer and Moore, 2000; Kamenos et al., 2003). A single impaction event can thus change a pristine live maerl (PLM) bed into an impacted live maerl (ILM) bed, which may subsequently die (impacted dead maerl (IDM) bed). The demands of aquaculture have been responsible for promoting a large body of research into natural and artificial surfaces conducive to pectinid spat settlement. Scallop spat attachment in the wild has been observed on rhodophytes (Le Pennec, 1974; Harvey et al., 1993), phaeophytes (Minchin, 1981), hydroids (Eggleston, 1962; Harvey et al., 1993), Bryozoa, tubicolous annelids (Eggleston, 1962) and shell gravels (Le Pennec, 1974). Conducive artificial substrata include monofilament, filter wool, polyethylene bags, AstroturfR, adult scallop shells (Pearce and Bourget, 1996) and NetronR with various chitin layerings (Wethey, 1986; Pawlik, 1992; Walters and Juanes, 1993; Harvey et al., 1995a,b, 1997). Juvenile queen (Aequipecten opercularis) and great (Pecten maximus) scallops have been observed attached primarily to various algae including Laminaria saccharina and Desmarestia aculeata but also to Bryozoa, hydroids, gravel, clean shell and general benthic epifauna (Eggleston, 1962; Paul, 1981; Minchin, 1992). Bay scallops (Argoopecten irradians) are known to use seagrass beds both as nursery areas and adult habitats (Garcia-Esquivel and Bricelj, 1993; Arnold et al., 1998; Bologna and Heck, 1999; Irlandi et al., 1999; Arnold et al., 2003; Goldberg and Tettelbach, 2003; Greenawalt et al., 2003). High numbers of juvenile Placopecten magellanicus (Brethes and Bourgeois, 2003) and Chlamys islandica (Himmelman and Guay, 2003) have been observed associated with scallop shells placed on the seabed in attempts to increase scallop production.

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No field or laboratory study has yet quantified the numbers of juvenile queen scallops using various natural substrata as juvenile habitats. There are reports that maerl grounds support large numbers of juvenile queen scallops and may thus be acting as nursery areas for this, and possibly other commercially important species (Birkett et al., 1998; BIOMAERL team, 1999); observations which prompted this study. It is often unclear whether observations made on juvenile queen scallop habitats to date relate to their initial settlement habitat or to a surface to which they have subsequently migrated. As there is no evidence that scallops preferentially settle on live maerl, it may be that they do not settle directly on maerl but migrate there from other settlement substrata that are either epiphytes on maerl or occur in close proximity to a maerl ground. Minchin (1992) suggested that dispersal from settlement areas to fished areas would explain an absence of P. maximus spat less than 1 year old from areas that are fished for scallops and it is thus likely that during the period between settlement and recruitment to adult populations, these elusive juvenile scallops are using particular habitats as nursery areas. No data are available on the stimuli governing post-settlement byssal attachments in juvenile A. opercularis. They are likely to involve a combination of physical and chemical factors which may or may not be similar to those settling (reviews by: Crisp, 1974; Pawlik, 1992; Eckman, 1996) and adult scallops (review by Brand, 1991) are known to respond to. Live maerl is known to act as a contact chemostimulant (Giraud and Cabioch, 1976; Morse et al., 1980; Morse and Morse, 1984) to a variety of organisms, (e.g. Haliotis rufescens Morse and Morse, 1984; H. laevigata Daume et al., 1999; Spirobis rupensis Gee, 1965; and other spirobids Crisp, 1974) due to a macromolecular fraction of GABA (g-aminobutyric acid) detectable only on the surface of live red coralline algae (Morse et al., 1980; Morse and Morse, 1984). Scallops are known to respond to chemical cues during metamorphosis and settlement (Pawlik, 1992; Harvey et al., 1997). In P. maximus metamorphosis can be induced by jacaranone extracted from the red algae Delesseria sanguinea (Yvin et al., 1985; Cochard et al., 1989). This study aims to investigate substratum byssal-attachment preferences of juvenile A. opercularis to PLM, IDM and other common substrata. The effect of predator presence on these preferences is also addressed and the stimuli that may be controlling the observed preferences considered.

2. Materials and methods 2.1. Scallop collection Juvenile A. opercularis were obtained from a commercial grower (Highland Aquaculture, Isle of Skye). The spat were collected on spat bags and grown-on in lantern nets, thus were not pre-acclimated to any particular natural substratum. Individuals between 18 and 30 mm shell height (settled in July 2001) were collected from the grower in May 2002. Scallops < 18 mm shell height (settled in July 2002) were collected in October 2002. Scallops were packed in NetlonR bags and placed in a polystyrene box lined with Fucus sp. for transport to Millport by road. Both batches were out of the water for < 6 h. All

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scallops were allowed a minimum of 1 week to acclimate in flow-through tanks with food supplements (as used in the experiments; see below) but no natural substratum, prior to experimental use. 2.2. Substratum collection Unimpacted pristine live maerl thalli were collected by SCUBA diving from Caol Scotnish (Loch Sween, 56j01.99VN, 5j36.13VW, 4 to 15 m CD). Impacted dead maerl thalli were collected with a naturalist’s dredge from Stravanan Bay (Isle of Bute, 55j45.36 VN, 5j04.29VW, 11 m CD). PLM thalli were larger (median rhodolith diameter 43.3 mm) than IDM thalli (median length 6 mm; median diameter 1.5 mm). Gravel (median length 7.3 mm) was collected from the HWM at Ballochmartin Bay, Isle of Cumbrae (55j47.09VN, 4j53.55VW), and fine grade sand (125 –250 Am diameter) from the HWM on Kames Bay, Isle of Cumbrae (55j45.16 VN, 4j54.57VW). The collected substrata were un-sorted to give results more representative of the natural environment. Live maerl was stored in a high flow (3000 l h 1) out-door seawater tank after collection until required; other substrata were stored in low flow (1000 l h 1) out-door seawater tanks. 2.3. Experimental tank set-up 2.3.1. Habitat selection experiments A circular tank (diameter 140 cm, depth 47 cm) with central overflow was set up in an isolation wet laboratory with four 90j, 3 cm high, segments on the base (area: 3843 cm2 each). PLM, IDM, gravel and sand were randomly assigned to each segment of the tank, with substratum depth of f 3 cm. Coarsely (2 mm) filtered seawater was supplied by four nozzles, just below the water level, producing a counter clockwise circulation. Each input nozzle corresponded to a base segment. Illumination was provided by low power daylight bulbs (75 W); the light regime followed ambient sunrise/sunset times. The experimental chamber was left for 12 days to allow biofilm development on each substratum prior to any experimentation. 2.3.2. Maerl microsite selection experiments PLM nodules were placed one layer deep on the base of circular tanks (diameter 12 cm, depth 20 cm). Coarsely (2 mm) filtered seawater was supplied by a single nozzle just below the water level, producing a counter clockwise circulation, water left each tank via overflow. The experiments were conducted under the same environmental conditions as the habitat selection experiment. The experimental tank was left for 7 days to allow biofilm development prior to any experimentation. 2.3.3. Cue utilisation experiments The base of similar tanks used in the maerl microsite experiments were separated into three equal segments (3 cm depth). PLM, impacted live maerl (ILM = crushed PLM) and IDM were randomly assigned to one of the segments. PLM had significantly higher heterogeneity than ILM and IDM, which did not differ (heterogeneity tested as in

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Kamenos et al., 2003). The experimental chambers were left for 7 days to allow biofilm development on each substratum prior to any experimentation. 2.4. Experimental protocol 2.4.1. Habitat selection experiments Two size groups of juvenile queen scallops were tested in the experiments ( < 18 mm shell height and 18– 30 mm shell height); the same protocol was followed for both groups. For each size group the control experiment was carried out first, to avoid predator excretory products affecting the control results. After the 18– 30-mm trial the experimental chamber was thoroughly flushed prior to the < 18-mm trials for the same reasons as order of treatment experimentation. In the control trial, at T0, 125 queen scallops were haphazardly distributed on each substratum and monitored bi-hourly for the first 12 h, then every 12 h for a further 72 h. Number of scallops in 95-cm2 quadrats (N = 5) on each substratum, total numbers on each substratum and associated tank sides were recorded at each observation period. The observation periods were distributed to allow (1) initial scallop dispersal rate observation, (2) day- and night-time observations (night-time observations were made using red light to reduce organism disturbance), (3) the prolonged observation of relative organism distributions. The coarsely filtered seawater was supplemented with 1 l of highly concentrated mixed Tetraselmis sp., Chaetoceros sp. and Skeletonema sp. culture twice daily at 09:00 h and 21:00 h after the corresponding observation periods. For each size group, the effect of certain predators on scallop attachment was investigated using the common starfish (Asterias rubens) and the green shore crab (Carcinus maenas). Experiments in the presence of a predator (A. rubens: 13.9 –14.2 mm for the 18 – 30-mm group and 11– 14 mm for the < 18-mm group as well as C. maenas (all male): 63.2– 65 mm (carapace diameter) for the 18– 30-mm group and 60.0 –63.5 mm for the < 18-mm group) were identical to the control, except that a single predator was added to each substratum directly prior to the addition of substratum un-acclimated scallops. Predators had been acclimated to the corresponding substratum in separate tanks for 1 week prior to the experimental sessions. Additionally, they were fed to satiation on Mytilus edulis L. 4 days prior to the experiment and then starved to avoid differences in feeding intensity (individuals were assumed to be satiated if they appeared uninterested in the ration offered 3 h after ration introduction). 2.4.2. Maerl microsite selection experiments In the control experiment, substratum unacclimated A. opercularis ( < 18 mm shell height) were placed haphazardly on PLM in the experimental tanks (N = 10). At T+ 24 the position of the scallops was noted and given a score for each of two position criteria. Internodule position relates to an individual scallop’s attachment position to maerl nodules; either on the exposed top surface or less exposed sides and base. Intra-matrix position relates to an individual scallop using either the intra-matrix spaces of an individual nodule or the external surface of an individual maerl nodule while attached. The term surface

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exposure will be used to indicate how unprotected the juvenile queen scallops are. For both criteria the higher the score the greater the degree of surface exposure demonstrated by each scallop (Table 1). Each experiment was repeated in the presence of a single A. rubens ( f 140 mm arm diameter) and then a male C. maenas ( f 45 mm carapace diameter). All the experiments were repeated with 18 – 30 mm shell height scallops (A. rubens 130 mm arm diameter, C. maenas 45 mm carapace diameter). For each experiment fresh unacclimated scallops and predators (fed to satiation 3 days prior to use) were used. 2.4.3. Cue utilisation experiments Ten substratum unacclimated A. opercularis ( < 18 mm shell height) were placed haphazardly on each substratum in an experimental tank (N = 3). At T+ 24 the number of scallops on each substratum was noted. The experiment was repeated in the presence of A. rubens ( f 130 mm diameter) placed in the centre of the tank prior to the queen scallops. Both treatments were repeated using 18 –30 mm shell height queen scallops. Predation rates in the presence of C. maenas were unnaturally high, an artefact of this experimental set-up, thus the data are not considered in the analyses. 2.5. Data analysis It is important to stress that where only one experimental chamber was used discussion of descriptive statistics was considered only for locations within that specific chamber (Hurlbert, 1984) as production of a measure of between tank variability was logistically not possible or necessary (much in the same way that data for substrata within a single bay would only relate to that bay). All analyses were performed using MinitabR V13 and ExcelR. One-way ANOVAs were used in cases where data were from one temporal point (e.g. T0) and also in scallop height comparisons. In analyses where all N were equal, normality assumptions were met but variance assumptions not tested as the ANOVA is robust enough to cope with deviations from variance (Sokal and Rohlf, 1981; Zar, 1999; Huck, 2000). To ascertain the general substratum preferences of post-acclimated juvenile queen scallops over the experimental period, rather than at any interim time, repeated measures ANOVAs were used, as successive censuses were taken during the same experiment at different times (i.e. T+ 24 – T96) with only time as the repeated measure (Neter et al., 1996). Subsequent pairwise comparisons were performed in two

Table 1 Scoring used to describe inter-nodule and intra-matrix position criteria for juvenile queen scallops (A. opercularis) in maerl microsite selection experiments Criterion/score

1

2

3

4

Inter-nodule position Intra-matrix position

Between or under nodules No part of scallop exposed

Upper surface exposed n/a Scallop < half exposed

n/a

n/a

Scallop >half exposed

Scallop fully exposed

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ways. Where no interactions occurred, a Tukey analysis grouping time level means was performed (Neter et al., 1996) using the subject MS, which is the denominator MS for substratum in the ANOVA with a 95% family confidence coefficient (method a). Where interactions were present, Tukey analyses were performed on densities at T+ 24 and T+ 96 individually for each treatment and size group (Sokal and Rohlf, 1981; Neter et al., 1996; Zar, 1999), using the Error MS which is the denominator MS of the interaction term, indicating where distribution differences lay at the end of the acclimation period as well as at the end of the experiment (method b). Frequency distributions ( G-Tests) were used to investigate the relative numbers of scallops on each substratum at a particular time. These allowed investigation of the effects of predator presence on the ratios of scallops present on each substratum. GTests were run as pairwise comparisons for pairs of treatments using Dunn –Sı˘da´k adjusted Chi-Square values and Williams corrected G statistics. The counts from T+ 24 were used (as trials showed that such a time period allowed the scallops to make a habitat choice). Additionally, this time was unaffected by high predation leading to very low numbers on any substratum due to the confined nature of the arena. The two position criteria from microhabitat experiments were added together giving an overall exposure score. Exposure score comparisons for each treatment were made as pairwise comparisons using a Mann –Whitney U Test. Nine pairwise comparisons were made: three within size-group treatment comparisons for each size group (i.e. control vs. starfish, control vs. crab and starfish vs. crab). Also three within treatment (between size-group) comparisons. Each of the comparisons was considered at a Dunn – Sı˘da´k adjusted P level for the nine comparisons of P = 0.0057.

3. Results 3.1. Habitat selection experiments At T0 the densities of queen scallops on each substratum within each treatment did not differ (Tables 2a and 2b). All substratum density comparisons for treatments in both size-classes after the acclimation period (T+ 24 to T+ 96) proved significant indicating that at least one mean density was significantly different from one other mean density within a size-class treatment (see below). Neither controls showed any interaction (substratum*time), thus Tukey method a (see above) was implemented for post hoc pairwise comparisons. All predator treatments showed an interaction (substratum*time), i.e. substratum densities responded differently to time, thus post hoc pairwise comparisons were carried out using Tukey method b (see above). 3.1.1. Size group: <18 mm shell height In the control treatment significantly higher queen scallop densities were observed on PLM than any of the other substrata tested at all times. Sand had significantly the lowest densities at any time. Gravel had significantly higher densities than IDM at any time ( F3 = 437.21, P < 0.0001). At T+ 24 and T+ 96 significantly more queen scallops were observed on PLM than any of the other substrata in ‘‘starfish’’ ( F3 = 632.1,

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Table 2a Mean (N = 5) densities of queen scallops (A. opercularis)/95 cm2 with associated standard deviations (SD) and 95% confidence intervals (95% CI) on pristine live maerl (PLM), impacted dead maerl (IDM), gravel (G) and sand (S) at T0, T+ 24 and T+ 96 for each size group and treatment. < 18 mm = < 18 mm shell height Size group

Time

Treatment

Substratum

Mean

SD

95% CI

< 18 mm

T0

Control

IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S

11 11 11.6 11.6 9.8 9.8 10.2 10 8.4 8.0 8.0 8.4 4 7.2 21.4 1 4 4.2 18.8 0.8 0.4 1.6 13.6 0.8 2.6 7.6 20.8 0.8 3.8 4 18.2 3.4 0 0 2.2 0

0.71 0.71 1.52 1.52 1.48 1.48 2.17 1.23 1.14 1.23 1.23 1.14 0.71 1.48 2.51 1.23 1.87 1.64 1.64 0.84 0.55 1.95 1.82 0.84 1.57 2.30 1.48 0.84 1.48 0.71 3.11 1.14 0.00 0.00 1.09 0.00

0.62 0.62 1.33 1.33 1.30 1.30 1.90 1.07 1.00 1.07 1.07 1.00 0.62 1.30 2.20 1.07 1.64 1.44 1.44 0.73 0.48 1.71 1.59 0.73 1.38 2.02 1.30 0.73 1.30 0.62 2.73 1.00 0.00 0.00 0.96 0.00

Starfish

Crab

< 18 mm

T+ 24

Control

Starfish

Crab

< 18 mm

T+ 96

Control

Starfish

Crab

P < 0.0001) and ‘‘crab’’ treatments ( F3 = 232.04, P < 0.0001). IDM, gravel and sand had equal juvenile queen scallop densities in the ‘‘starfish’’ and ‘‘crab’’ treatments (all: Table 2a and Fig. 1 for general trends). 3.1.2. Size group: 18 –30 mm shell height In the control treatment significantly higher queen scallop densities were observed on PLM than any of the other substrata tested at all times. Sand had significantly the lowest

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Fig. 1. Mean number of < 18 mm shell height juvenile queen scallops (A. opercularis) (pooled from all treatments) and 95% confidence intervals (C.I.), in 95-cm2 quadrats, on pristine live maerl (PLM), impacted dead maerl (IDM), gravel and sand at 12-h intervals (N = 15 for each mean).

densities at any time. Gravel and IDM had equal densities at all times ( F3 = 364.47, P < 0.0001). At T+ 24 significantly more juvenile queen scallops were observed on PLM than any of the other substrata in ‘‘starfish’’ ( F3 = 165.16, P < 0.0001) and ‘‘crab’’ treatments ( F3 = 251.23, P < 0). Sand had significantly the lowest densities in ‘‘starfish’’ and ‘‘crab’’ treatments. Gravel and IDM had equal densities in starfish and crab treatments (all: Table 2b and Fig. 2 for general trends). At T+ 96 significantly more juvenile queen scallops were observed on PLM than any of the other substrata in ‘‘starfish’’ ( F3 = 165.16, P < 0.0001) and ‘‘crab’’ treatments ( F3 = 251.23, P < 0.0001). Gravel and sand had equal scallop densities in the ‘‘starfish’’ treatment but IDM had significantly higher densities than sand. Sand had significantly the lowest densities in the ‘‘crab’’ treatment. IDM and gravel equal scallop densities in the ‘‘starfish’’ and ‘‘crab’’ treatments (all: Table 2b and Fig. 2 for general trends). 3.1.3. Frequency distributions between treatments (within size groups) In all comparisons the null hypothesis was accepted indicating that juvenile queen scallop distributions were independent of treatment ( G3 all>2.04, P all>0.05). Thus treatment had no effect on the proportions of scallops on each substratum within the size groups tested. For ease of viewing, data were therefore pooled by size group in Figs. 1 and 2 giving general trends.

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Table 2b Mean (N = 5) densities of queen scallops (A. opercularis)/95 cm2 with associated standard deviations (SD) and 95% confidence intervals (95% CI) on pristine live maerl (PLM), impacted dead maerl (IDM), gravel (G) and sand (S) at T0, T+ 24 and T+ 96 for each size group and treatment. 18 – 30 mm = 18 – 30 mm shell height Size group

Time

Treatment

Substratum

Mean

SD

95% CI

18 – 30 mm

T0

Control

IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S IDM G PLM S

11 11.6 11.6 11.8 9.6 9.8 9.4 9.8 9.6 9.4 9.6 9.6 5.4 6 20.8 1.8 7.2 8 16.6 2.2 9.4 6.8 17.4 0.8 4.6 6 18.8 0.8 6.8 6 18 2.6 9.4 8.2 15.2 4.4

1.58 2.19 2.30 1.92 1.14 0.45 1.14 1.30 1.14 1.52 0.55 1.14 1.67 2.74 5.50 0.84 1.30 2.74 4.22 1.48 1.95 1.48 1.14 0.87 0.98 3.39 2.78 0.84 2.05 2.35 1.87 1.14 1.14 1.79 1.64 1.52

1.39 1.92 2.02 1.69 1.00 0.39 1.00 1.14 1.00 1.33 0.48 1.00 1.47 2.40 4.82 0.73 1.14 2.40 3.70 1.30 1.71 1.30 1.00 0.77 0.86 2.97 2.43 0.73 1.80 2.06 1.64 1.00 1.00 1.57 1.44 1.33

Starfish

Crab

18 – 30 mm

T+ 24

Control

Starfish

Crab

18 – 30 mm

T+ 96

Control

Starfish

Crab

3.1.4. Scallops height comparison by substratum The shell heights of juvenile queen scallops remaining on each substratum at the end of each treatment were compared for each size class. Only queen scallops on IDM (14.42 mm shell height F 1 (95% CI)) were significantly larger ( F3 = 4.02, P = 0.01) than those on gravel (13 F 0.88) and PLM (12.33 F 0.88) in the ‘‘starfish’’ treatment for < 18 mm shell height scallops. However, the maximum mean size difference (2.09 mm) is probably too small to be ecologically significant. In all other treatments scallop heights did not differ between substrata.

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Fig. 2. Mean number of 18 – 30 mm shell height juvenile queen scallops (A. opercularis) (pooled from all treatments) and 95% confidence intervals (C.I.), in 95-cm2 quadrats, on pristine live maerl (PLM), impacted dead maerl (IDM), gravel and sand at 12-h intervals (N = 15 for each mean).

3.2. Maerl microsite utilisation In all the experiments live scallops attached to the maerl, none attached to the tank sides. In the treatments with a predator present some predation on A. opercularis occurred, so the distribution of the remaining live scallops only was considered. Dead shells were ignored (Fig. 3). In all control vs. predator comparisons, A. opercularis had significantly higher exposure scores in the control treatments. Both ‘‘starfish’’ vs. ‘‘crab’’ comparisons generated equal exposure scores. Between size-group control treatment comparisons also showed equal exposure scores, while ‘‘starfish’’ and ‘‘crab’’ comparisons showed significantly higher exposures for the 18 –30-mm shell height groups (Fig. 3). 3.3. Cue utilisation The proportions of A. opercularis on each substratum were significantly different in the presence of a predator for both < 18 mm shell height ( G2 = 7.34, P < 0.05) and 18 –30 mm shell height ( G2 = 6.90, P < 0.05) (Fig. 4). Interpretation of the data indicates that while there were similar proportions of juvenile queen scallops on PLM and ILM,

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Fig. 3. Mean exposure scores of juvenile A. opercularis utilising PLM as a habitat in control, starfish and crab treatments. < 18 = < 18 mm shell height scallops, 18 – 30 = 18 – 30 mm shell height scallops. Exposure score is comprised of the total scores for inter-nodule and intra-matrix scores where higher scores indicate greater physically exposed scallops. Error bars = SD. Horizontal lines at the same level indicate treatments that did not differ significantly ( P > 0.0057).

Fig. 4. Mean number of juvenile A. opercularis on pristine live mearl (PLM), impacted live maerl (ILM) and impacted dead maerl (IDM) at T+ 24 h in control and starfish treatments. < 18 = < 18 mm shell height scallops, 18 – 30 = 18 – 30 mm shell height scallops. Error bars = SD, N = 3 for all.

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both of which were higher than IDM in the control treatments; in the ‘‘starfish’’ treatment the proportion of juvenile queen scallops on PLM was greater than on the ILM and IDM which were similar to each other (Fig. 4).

4. Discussion PLM has been shown to attract juvenile A. opercularis (actively or accidentally) from adjacent substrata in our mesocosm experiment. PLM thus harboured significantly higher A. opercularis densities ( < 30 mm shell height) than IDM, gravel and sand substrata in the presence or absence of either A. rubens or C. maenas for the whole experimental period post-acclimation. With the < 18-mm control group secondarily preferring only gravel, while IDM and gravel or all three remaining substrata were selected secondarily by other treatment groups, there does not appear to be a defined ‘‘second choice substratum’’. Generally, IDM and gravel were selected preferentially to sand. Scallop-size induced, differential habitat selection within a size group was not the impetus behind the observed distributions. PLM had a higher substratum heterogeneity than the IDM or gravel, which did not differ, but was higher than sand (Kamenos et al., 2003). High habitat heterogeneities are known to equate to high biodiversities in many marine and terrestrial systems, due to direct factors such as the creation of more available habitats for colonisation as well as indirect factors such as stabilization of predator –prey relationships by refuge creation (Menge et al., 1983; Gilinsky, 1984; Ormond et al., 1997; Himmelman and Guay, 2003). It is unlikely that substratum heterogeneity is the only stimulus to which A. opercularis responded. Unlike the habitat selection experiments, a change in juvenile queen scallop distributions was observed for both size classes tested in the presence of A. rubens. Queen scallop numbers on ILM dropped to similar levels as those in IDM, while numbers on PLM increased. It is possible, therefore, that the juvenile queen scallops were responding to a series of hierarchical cues already known to occur in settling invertebrates, e.g. barnacles (Crisp, 1974; Chia, 1988) and hydroids (Williams, 1965). In the absence of a predator the queen scallops are attracted by a factor associated with the live maerl irrespective of its heterogeneity. In the presence of a predator, however, heterogeneity also became important and substrata possessing ‘‘live maerl’’ cues and high heterogeneities are likely to be selected preferentially. Bay scallops have been observed to swim towards seagrass beds using a combination of visual, chemical and acoustic cues. However, there is no direct evidence that relocating scallops rely solely on visual stimuli (Winter and Hamilton, 1985; Hamilton and Koch, 1996). In our experiment it was thus unlikely that juvenile queen scallops were using visual location in order to discriminate deep purple maerl against a dark green tank background. The queen scallops appeared to swim in random directions until landing on the PLM at which point they would stop swimming and bysally attach directly to the maerl. This behaviour is indicative of a tactile or very localised chemical or acoustical response to the presence of maerl. Live maerl is known to act as a tactile chemostimulant (Giraud and Cabioch, 1976; Morse et al., 1980; Morse and Morse, 1984) to a variety of settling invertebrates (Gee, 1965; Crisp, 1974; Morse and Morse, 1984; Daume et al., 1999) and as metamorphosing and settling scallops have been shown to respond to similar

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stimuli (Yvin et al., 1985; Cochard et al., 1989; Pawlik, 1992; Harvey et al., 1997) it is possible that attaching juvenile queen scallops are responding to the macromolecular fraction of GABA known to exist in live maerl. The presence and absence of some predatory species have been observed not to affect the relative distributions of A. opercularis on PLM, IDM, gravel or sand in laboratory conditions. This would suggest that juvenile queen scallops respond to a series of predetermined stimuli for habitat selection, which are not affected by predator presence or absence. Thus apparent habitat selection cannot be dismissed as a localised escape response to predators. Although the presence of predators does not affect general habitat selection by juvenile queen scallops, it has been found to affect microhabitat selection by juvenile queen scallops. Aequipecten opercularis were observed to recede into inter-nodule and intramatrix spaces in the presence of both A. rubens and C. maenas, utilising the protective calcareous structure as a refuge. The 18 – 30-mm shell height group could not use the intramatrix spaces as efficiently as the < 18-mm shell height group, which could be totally obscured by the branches of an individual maerl thallus due to their smaller size. Intramatrix positions offered better protection from C. maenas than inter-nodule positions. These crabs have been observed excavating between nodules to gain access to A. opercularis seeking refuge (Kamenos, pers. obs.). Foraging of the brachyuran crabs Ovalipes ocellatus and Callinectes sapidus on juvenile Mercenaria mercenaria was observed to be less efficient on more heterogeneous substrata leading to significantly lower predation rates (Sponaugle and Lawton, 1990). Our data thus suggests that maerl not only provides a refuge to attached A. opercularis but also reduces foraging success of potential crab and even possibly starfish predators. Similarly to juvenile A. opercularis, juvenile Argopecten irradians, Chlamys islandica and Placopecten magellanicus have been observed to utilise refuges from predators (Garcia-Esquivel and Bricelj, 1993; Brethes and Bourgeois, 2003; Himmelman and Guay, 2003). The use of specific substrata by juveniles allows (1) enhanced survival through avoidance of predators (Garcia-Esquivel and Bricelj, 1993); (2) enhancement of growth by positioning scallops in an optimum hydrodynamic regime that minimises exposure to re-suspended bottom sediments and maximises food capture. However, sea grasses, for instance, are known to reduce near bottom current velocities and water flux markedly while generating increased turbulence in the water canopy interface, thus creating steep vertical gradients in the flow regimes (Garcia-Esquivel and Bricelj, 1993; Eckman, 1996) which reduces the influx of food. Similar hydrographic characteristics are likely to be present in and around PLM beds, habitats known to have high heterogeneities (Kamenos et al., 2003) or (3) a combination of the above factors (Garcia-Esquivel and Bricelj, 1993).

5. Conclusions Although there is no present evidence that juvenile A. opercularis settled directly on maerl, significantly higher numbers were observed on PLM than other common substrata and, most importantly, on IDM. Similar distributions in the field (Kamenos; unpubl.)

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suggest A. opercularis either migrate to PLM from other primary settlement substrata or settle on maerl epiphytes and attach to maerl at a later stage. Thus individual juvenile queen scallops have been shown to bysally attach to PLM on a centimetre scale for protective purposes. If this is also the situation in the field, at some sites PLM grounds cover large areas, which may thus be considered to constitute ‘nursery areas’. Towed demersal gears have been found to easily reduce the heterogeneity of PLM (Hall-Spencer and Moore, 2000; Kamenos et al., 2003), possibly reducing recruitment to adult populations in areas where PLM beds are being heavily commercially impacted. The ‘‘ecosystem service’’ offered by PLM beds as nursery grounds for commercial species (see BIOMAERL team, 2003) needs to be taken seriously.

Acknowledgements The authors would like to thank Scottish National Heritage whose funding made this work possible, Rowardennan Field Station (University of Glasgow) for loan of the tanks and Dr. I.P. Smith for constructive statistical criticism. One of us (N.A.K.) was in receipt of a Sheina Marshall studentship from the University Marine Biological Station Millport. Additionally, we would like to thank Kenny Cameron and Stephen Muir (UMBSM divers) and the crew of the R.V. Aplysia for help with maerl collection.[RW]

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