Community composition and diversity of two Limaria ...

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polychaetes Sabellaria alveolata, S. spinulosa and Serpula ver- micularis ..... ecology of reefs of Serpula vermicularis L. (Polychaeta: Serpulidae) in Scotland.
Journal of the Marine Biological Association of the United Kingdom, page 1 of 10. doi:10.1017/S0025315410002158

# Marine Biological Association of the United Kingdom, 2011

Community composition and diversity of two Limaria hians (Mollusca: Limacea) beds on the west coast of Scotland colin trigg1, dan harries2, alastair lyndon2 and colin g. moore2 1 Scottish Natural Heritage, Great Glen House, Leachkin Road, Inverness, IV3 8AW Scotland, UK, 2Heriot-Watt University, Riccarton, Edinburgh, EH14 4AS Scotland, UK

Limaria hians functions as a keystone species in construction of a highly diverse biogenic habitat. An investigation to quantify the biodiversity of two L. hians beds was carried out during the winter and summer seasons at two sites on the west coast of Scotland. Cores were taken semi-randomly through 100% L. hians nest material, organisms removed, identified and enumerated. Univariate and multivariate analyses of the data were used to establish temporal and locational differences. A total of 7275 individuals were found representing 282 species from 16 phyla. Univariate analysis revealed significant differences between the species richness of the two populations, whilst multivariate analysis illustrated differences in the assemblage compositions between sites and times. This study showed that in terms of richness and diversity these beds are among the most important biogenic habitats in the UK. Keywords: Limaria, biogenic reef, bivalve, biodiversity, associated community, keystone, Scotland Submitted 6 September 2010; accepted 18 November 2010

INTRODUCTION

It is generally the case that the more structurally complex a habitat the greater its biodiversity (Tilman, 1999; Cocito, 2004). In the tropics coral reefs are the archetypal representation of habitat complexity containing rich assemblages of invertebrates (Cornell & Karlson, 2000; Cocito, 2004). Corresponding complex structures in temperate seas are typified by biogenic reefs and maerl beds (Holt et al., 1998; Hall-Spencer & Moore, 2000a, b; Cranfield et al., 2004). Biogenic reefs have a number of effects on the physical environment, including stabilization of mobile sediment and the provision of suitable substrate for the attachment of sessile organisms. Consequently this leads to a community of biota that is more rich and diverse than the surrounding area (see Holt et al., 1998). Many mobile animals and their juveniles use upright structures to shelter from currents or predators, e.g. juvenile hake (Auster et al., 1997). Tupper & Boutilier (1995) showed that juvenile cod (Gadus morhua) are more likely to avoid predation in structurally complex habitats leading to better rates of survival. In UK inshore waters several biogenic reef forming species have been considered to be of special importance, namely the polychaetes Sabellaria alveolata, S. spinulosa and Serpula vermicularis and the bivalves Mytilus edulis and Modiolus modiolus (Holt et al., 1998; Moore et al., 1998; Rees et al., 2008). However, as highlighted by Hall-Spencer & Moore (2000b), the homologous bivalve beds of Limaria hians (Gmelin) are

Corresponding author: C. Trigg Email: [email protected]

currently omitted from the biogenic reef classification and have only recently been included as a priority habitat for conservation action under the UK Biodiversity Action Plan (Biodiversity Reporting and Information Group, 2007). Work on L. hians beds has indicated a diverse assemblage of organisms; however, the sensitivity of L. hians and the susceptibility of their beds to anthropogenic impacts has resulted in dwindling numbers and a drop in their coverage throughout the UK, with only their shells found in areas where several decades ago they were recorded as common (Ansell, 1974; Tebble, 1976; Minchin et al., 1987; Wood, 1988; Seaward, 1990; Minchin, 1995; Trigg & Moore, 2009). Limaria hians secretes byssal threads which it then attaches to surrounding material, eventually creating a cocoon-like structure (Merrill & Turner, 1963; Gilmour, 1967). Under the right environmental conditions, specifically areas subject to strong tidal currents, large aggregations of L. hians give rise to a layer of continuous nest carpeting the seabed (Ansell, 1974; Minchin et al., 1987; Minchin, 1995). These beds contain high densities of L. hians with as many as 700 ind. m2 recorded (e.g. Hall-Spencer & Moore, 2000b). The provision of a stable substrate overlying the mobile sediment allows colonization by epibionts, thus enabling an array of sessile and sedentary organisms to inhabit regions normally unsuitable for their attachment (Minchin, 1995; HallSpencer & Moore, 2000b). The bed also acts as a nursery ground for species such as Gadus morhua (Minchin, 1995; Collie et al., 1997; Hall-Spencer & Moore 2000b; Bradshaw et al., 2003). Along with the considerable numbers of species on and inside the byssal bed Hall-Spencer & Moore (2000b) found a high infaunal biomass directly below. Despite the acknowledged conservation importance of L. hians beds (Biodiversity Reporting and Information 1

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Group, 2007) no quantitative data exist on the associated community of L. hians beds. Understanding the contribution of this keystone species towards marine biodiversity in UK waters is a prerequisite for establishing sound conservational guidance, in addition to providing more detailed information on this habitat’s ecology. This paper describes an investigation carried out on the macrobenthos of L. hians beds on the west coast of Scotland during the winter and summer periods, in order to characterize the community and to determine the nature of temporal and spatial variation in community composition and diversity.

MATERIALS AND METHODS

Limaria hians beds were investigated at two sites in Argyll on the west coast of Scotland: Appin in Loch Linnhe (56833.794′ N 5824.819′ W, 9.1 m depth) and Shian in Loch Creran (56831.745′ N 5823.630′ W, 10.0 m depth) (Figure 1). Five replicate 10 cm diameter core samples were taken by diver at each site within areas of 100% nest cover on 17 June 2006. The coring tubes were pushed through the nest material and into the underlying sediment to a total depth of 15 cm. Nest thickness at each core location was measured by ruler. Core sample location was randomized by the diver swimming for 1 –5 kick cycles towards one of the four cardinal points, the number of kick cycles and the cardinal point being determined using a pseuso-random number generator. Core samples were initially preserved in 10% formosaline in 5 l containers before transfer to 70% ethanol for storage. Sampling was repeated at both sites on 13 –14 February 2007. Prior to examination of the core samples rose Bengal was added to each of the samples and left for a minimum of 24 hours. Freshwater was then added to the buckets and the

samples gently stirred to elutriate the lighter organisms. The supernatant was then drained through a 0.5 mm sieve. This process was repeated several times until very few organisms were being collected. The organisms retained in the sieve were washed into a sorting tray and, using forceps, sorted into major taxonomic groupings. The residue left in the sample container, comprising sediment and nest material, was then sieved in small amounts, the material retained being placed in a sorting dish where the nest material was teased apart and the biota sorted into major taxonomic groupings. Once sorted all the organisms were stored in 70% ethanol solution. These were then identified to the lowest possible taxon and enumerated; however, algae and colonial organisms (i.e. sponges, hydroids, bryozoans and some ascidians) were recorded as present or absent. Due to its extremely small size the polychaete Spirorbis spirorbis was recorded as present or absent. Nomenclature and authorities for all flora and fauna were obtained using the World Register of Marine Species (WoRMS) database (SMEBD, 2010). Two species abundance data matrices were produced. The minimum species richness matrix excluded taxa that did not necessarily represent additional species (such as unidentified juveniles); taxa recorded as present were given the nominal abundance of 1. In the quantitative-only data matrix such taxa were omitted. For each core replicate, total abundance (N) was taken as the sum of abundances of all quantitatively-recorded taxa. Species richness (S) was taken as the number of taxa included in the minimum species richness data matrix. The Shannon–Wiener index (H′ ) and Pielou’s evenness index (J) were obtained from the quantitative-only data matrix (with the exclusion of possible multispecies taxa such as Nematoda) using Primer 5.1 (Clarke & Warwick, 2001). Temporal and locational differences in mean N, S, H′ and J values were assessed by two-way analysis of variance

Fig. 1. Arrows indicate locations of the study sites at Appin, in Loch Linnhe and at Shian, in Loch Creran.

biodiversity of limaria hians reefs

(ANOVA), following confirmation of homoscedasticity using Levene’s test. Temporal and locational differences in community composition were examined using multivariate analysis tools in Primer 5.1 (Clarke & Warwick, 2001). Non-metric multidimensional scaling (n-MDS) was carried out on log(x + 1) transformed abundances in the minimum species richness data matrix, employing the Bray – Curtis index. Temporal and locational differences in community composition were tested by two-way analysis of similarities (ANOSIM), and the species contributing mostly to any differences identified using the SIMPER routine.

RESULTS

The results of two-way ANOVAs investigating seasonal and locational effects on mean values of the univariate parameters of abundance and diversity are given in Table 1. Abundance was significantly greater at Appin than at Shian; however, no temporal difference was identified. Overall, the abundance was dominated by molluscs, annelids, nematodes and crustaceans, together representing 93% of the total of 7275 enumerated animals (Table 2). A total of 306 taxa were identified from all 20 cores at both sites (Appendix). However, because the taxa list had more entries than could be confirmed as separate species, the minimum species richness total (S) was 282 (40 algae and 242 faunal taxa). For individual 79 cm2 core samples S ranged between 56 and 108, whilst pooling data for each location produced S values of 227 for Shian and 211 for Appin. The biota collected was represented by 3 algal and 13 faunal phyla with the richest groups being annelids, crustaceans, molluscs and rhodophytes (Table 2). Within each of the 3 richest phyla the dominant groups were errant polychaetes, amphipods and bivalves respectively. Of particular interest is the polychaete Lysilla nivea which was found at Shian. Originally described from Madeira, the presence of this worm is of geographical interest having only been found in UK waters within the southern Irish Sea fairly recently (Mackie et al., 1995). Mean species richness was found to be significantly greater in summer than in winter, though no locational effect was identified (Table 1). On the other hand, no seasonal change in the mean Shannon – Wiener or Pielou evenness indices was recorded, whilst means of both were significantly greater at Shian (Table 1). As these diversity indices were

Table 2. Composition of benthos in all 20 cores. Total abundance of individuals (in 0.16 m2) found in all samples per phylum. N/A indicates a phylum with species identified in binary. Phylum

No. of species

% of composition

Abundance

Annelida Crustacea Mollusca Rhodophyta Bryozoa Cnidaria Porifera Tunicata Echinodermata Phaeophyta Chlorophyta Nemertina Sipuncula Pycnogonida Nematoda Platyhelminthes

94 52 43 33 17 10 7 6 5 4 3 2 2 2 1 1

33.3 18.4 15.2 11.7 6.0 3.5 2.5 2.1 1.8 1.4 1.1 0.7 0.7 0.7 0.4 0.4

2357 812 2753 N/A N/A 8 N/A 13 241 N/A N/A 17 229 5 837 3

strongly influenced by the numerically dominant species, Modiolula phaseolina, the ANOVA was repeated omitting this species. This revealed significantly enhanced evenness in winter and at Shian. Temporal and locational patterns in species composition are illustrated in the n-MDS plot (Figure 2) which shows distinct separation of the replicate samples from each site and for the samples from different seasons at Shian. Both seasonal and locational differences were confirmed by two-way ANOSIM (P , 0.01 in both cases). A similarity percentages (SIMPER) analysis on log(x + 1) transformed data identified which species contributed most to the temporal and locational differences. It showed that the top 14 taxa contributed a cumulative percentage of 21% of the average dissimilarity between sites (49.72%; Table 3). The largest single contributor to the dissimilarity was Verruca stroemia. However, this only has a value of 1.96% and therefore indicates that the differences identified are from broad changes in the assemblage composition rather than from one or a few species. A similar result was found when assessing dissimilarity between times (Table 4). The top 16 taxa contributed a combined percentage of

Table 1. Mean of univariate measures: species number (S), abundance (N), Pielou’s evenness (J) and Shannon–Wiener diversity (H′ ) from Shian and Appin Limaria hians beds during summer 2006 and winter 2007. The measures represent mean values per 0.0079 m2 core. H1′ and J1 are excluding Modiolula phaseolina. Significant differences (P ≤ 0.05) are in bold. Shian

N S H′ J H1′ J1

Appin

P

P

Summer

Winter

Summer

Winter

Season

Location

307 93 4.83 0.83 4.96 0.85

266 74 5.02 0.88 5.01 0.88

417 80 4.29 0.73 4.61 0.79

466 74 3.68 0.64 5.00 0.86

0.94 0.02 0.37 0.53 0.10 ,0.01

,0.01 0.17 < 0.01 ,0.01 0.17 0.02

Fig. 2. Two-dimensional non-metric multidimensional scaling plot plot of biota, taken from the minimum species richness data set, found within a Limaria hians bed at 2 different sites and times (stress 0.15). The symbols W and † represent Shian 2006 and 2007 respectively; A and B represent Appin 2006 and 2007 respectively.

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Table 3. Similarity percentages analysis showing the dissimilarity between the associated community found on a Limaria hians bed at 2 different sites (Shian and Appin).

Verruca stroemia Modiolula phaseolina Musculus discors Cressa dubia Minuspio cirrefera Golfingia vulgaris Nereimyra punctata Leptochiton asellus Nucula nucleus Thracia villosiuscula Onoba semicostata Glycera lapidum Sphaerosyllis tetralix Prionospio banyulensis

Abundance at Shian

Abundance at Appin

Contribution %

Cumulative %

4.6 26.5 2.7 7.3 0.1 0.7 11.1 0.4 1.7 1.5 6.6 0.5 0.6 0.8

28.4 139.2 17.6 0.7 5.9 6.3 3.0 4.2 6.7 6.2 12.6 3.8 3.7 4.3

1.96 1.89 1.79 1.67 1.60 1.49 1.42 1.34 1.33 1.30 1.29 1.28 1.19 1.14

1.96 3.85 5.64 7.31 8.92 10.41 11.84 13.17 14.51 15.80 17.09 18.38 19.57 20.71

21% of the average dissimilarity between times (46.71%). Verruca stroemia has the greatest contribution (2.18%), the low value again indicating that no particular taxon has a large influence on the dissimilarity. Ten taxa were found in all the samples including the bivalve Musculus discors and the polychaetes Kefersteinia cirrata and Mediomastus fragilis. Using SIMPER found that 13 and 14 individual taxa, in Shian and Appin respectively, contributed over 50% to the similarity. Three of the 5 most dominant taxa at each site were the same: Nematoda spp., Modiolula phaseolina and Pholoe inornata. Just over 55% (N ¼ 156) of the total number of species were found at both sites.

DISCUSSION

This study represents the first comprehensive quantitative examination of the associated community found in a L. hians bed. A qualitative study in Loch Fyne on the west coast of Scotland recorded more than 280 taxa from 6 L. hians nests (Hall-Spencer & Moore, 2000b). Although the total number of species recorded in the present investigation was virtually identical to the Loch Fyne study, a maximum

of 227 taxa were found at a single site (Shian) when data from both the summer and winter sampling periods were pooled. The Loch Fyne study used 6 discrete nests of 25 cm diameter, equating to an estimated area of 0.29 m2, each about 10 cm in height. By comparison, the present study examined an area of 0.16 m2 in total (0.08 m2 at each location). Therefore, the larger area covered and the greater height of the nests in Loch Fyne could explain why more species were found, even though the sieve mesh size was 1 mm compared to 0.5 mm in this study. Furthermore, the Loch Fyne samples included small kelp plants living on the nests (Hall-Spencer, personal communication). Kelp have their own diverse communities living within the holdfasts and attached to the stipe (e.g. Christie et al., 2003), thus quite possibly enhancing the total species richness of a L. hians bed. More than half of the species collected in this study were found at both Appin and Shian. This is probably unsurprising considering their close geographical locations. Interestingly approximately 43% of the species found in the Loch Fyne study (Hall-Spencer & Moore, 2000b) were also found on the L. hians beds in this investigation; however, the composition of the benthos was quite different. Molluscs dominated the Loch Fyne samples (N ¼ 74) followed by Crustacea (N ¼ 63) and Polychaeta (N ¼ 52).

Table 4. Similarity percentages analysis showing the dissimilarity between summer and winter seasons of Limaria hians beds.

Verruca stroemia Onoba semicostata Cressa dubia Modiolula phaseolina Minuspio cirrefera Musculus discors Golfingia vulgaris Pholoe inornata Enchytraeidae spp. Nereimyra punctata Nucula nucleus Leptochiton asellus Syllidia armata Thracia villosiuscula Pomatoceros triqueter Sphaerosyllis tetralix

Abundance in summer

Abundance in winter

Contribution %

Cumulative %

28.8 15.1 1.4 60.2 1.1 9.2 4.0 35.1 0.8 5.2 4.7 1.6 3.8 3.9 1.6 1.4

4.2 4.1 6.6 105.5 4.9 11.1 3.0 14.7 4.1 8.9 3.7 3.0 1.6 3.8 3.5 2.9

2.18 1.65 1.47 1.46 1.33 1.31 1.30 1.27 1.24 1.19 1.18 1.11 1.09 1.09 1.05 1.03

2.18 3.83 5.30 6.76 8.09 9.39 10.69 11.96 13.21 14.4 15.58 16.69 17.79 18.87 19.92 20.95

biodiversity of limaria hians reefs

Differences in the assemblage composition between sites were clearly illustrated by the n-MDS plot (Figure 2) and confirmed by the two-way ANOSIM. Differences between the Shian and Appin communities were also revealed by Pielou’s evenness, the Shannon –Weiner diversity index and faunal abundance, which were all found to have significant site effects when examined by two-way ANOVA. A number of differences in the locations were discernible in situ and are thought to contribute towards the variations observed in the ordinations and univariate measures. For example, the bed at Shian was close to a rocky reef and was fairly homogeneous with a consistent 100% nest cover extending over a large area. In addition the thickness of the bed here was 5 cm with a density of L. hians of .600 ind. m22. In contrast the bed at Appin was in the middle of a kelp park, averaged 4 cm thick, had a L. hians population of approximately 350 ind. m22 and contained frequent patches within the bed devoid of nest material. The two sites are only separated by a distance of 4 km and display similar underlying heterogeneous sediments of gravelly sand. Current strengths are unknown but both sites are clearly tideswept, attaining spring rates in excess of 1 knot. There are, however, a number of known environmental differences between the sites that may contribute to the observed community differences. The narrow sill at the entrance to Loch Creran significantly reduces tidal flushing of the loch (see Landless & Edwards, 1976), which will influence larval supply and recruitment at the Shian site. Adjacent to a Modiolus modiolus bed, the Appin site is pockmarked by holes in the byssal carpet. On several occasions the abundant kelp here was observed to have pulled free sections of the Limaria hians bed; the drag from the currents eventually becoming too strong, resulting in the ‘uprooting’ of kelp holdfasts and subsequent tearing of attached nest material from the surrounding bed. This natural destruction of the beds was also recorded at a L. hians bed in Mulroy Bay, Ireland (Minchin, 1995) and clearly adds an extra dynamic quality to the Appin bed not seen at Shian. Significant time effects on species richness were found by two-way ANOVA and on species composition by two-way ANOSIM. However, no significant time differences were shown by J or H′ . Yet it should be noted that many of the organisms which exhibit seasonal changes were excluded from the univariate calculations, as they were not quantifiable (e.g. hydrozoans, bryozoans and algae) and species richness of algae was found to be significantly greater during the summer. A number of algal species were only recorded in the summer (e.g. Brongniartella byssoides, Colaconema daviesii, Audouinella purpurea and Halurus flosculosus), and when a two-way ANOVA was repeated without the algae the temporal change disappeared. Limaria hians beds have been recorded to depths of 30 m (Connor et al., 2004) so at this depth, where light is severely limited, seasonal differences in their community composition may not be significant. The recognized biogenic reefs in UK coastal waters are constructed by the mytilids Modiolus modiolus and Mytilus edulis the sabellids Sabellaria alveolata and S. spinosa and the serpulid Serpula vermicularis (Holt et al., 1998). The richest and most diverse of these are M. modiolus and S. vermicularis reefs (Holt et al., 1998) and are compared in detail with the present study. Studies on the biodiversity of the sabellid and M. edulis reefs have found considerably fewer taxa. For example, work by Svane & Setyobudiandi (1996) on a

M. edulis reef recorded a total of 39 species using a 0.5 mm sieve from an area of 0.029 m2. Although little work has been carried out on the sabellid reefs, in recent years an investigation by Sousa Dias & Paula (2001) on a S. alveolata reef in Portugal recorded 107 taxa from an area of 0.32 m2, using a 0.5 mm sieve. Studies undertaken on the M. modiolus reefs around the UK have found this habitat to be extremely diverse. Holt & Shalla (in Holt et al., 1998) found 270 invertebrate taxa in a M. modiolus reef off the Isle of Man, whilst in Strangford Lough 119 and 90 taxa were recorded on horse mussel clumps by Roberts et al. (2004) and Brown & Seed (1977) respectively. Surveys carried out by Mair et al. (2000), Moore et al. (2006) and Rees et al. (2008) on M. modiolus reefs allow comparisons with the present study as biota was retained on a 0.5 mm sieve and univariate measures calculated. These studies recorded a mean number of taxa of 84, 96 and 108 respectively, compared with a mean of 93 taxa per replicate for the L. hians bed at Shian. Greater areas were sampled per replicate in the M. modiolus studies, 0.03 m2 for the first 2 surveys and 0.06 m2 in the last, compared to a considerably lower 0.0079 m2 for the L. hians bed. A study on a S. vermicularis reef in Loch Creran recorded 71 taxa for a similar area (0.007 m2) and gave estimates of 12756 ind. 0.1 m22 for total fauna (Chapman, 2004). This compares with 2290 ind. 0.1 m22 for a Modiolus reef in Pen Llyˆn, North Wales (Rees et al., 2008) and 3886 ind. 0.1 m22 and 5894 ind. 0.1 m22 for the L. hians reefs in Shian and Appin respectively. The L. hians faunal assemblage is dominated by the same groups (Annelida, Crustacea and Mollusca) as in the study by Chapman (2004), although many more species of Mollusca were found on the serpulid reef than the L. hians bed (N ¼ 70 compared to N ¼ 43). The mean Shannon – Wiener diversity figures of the L. hians bed at Shian (4.83 in the summer and 5.02 in the winter) are similar to those of M. modiolus reefs also found in Loch Creran (4.9 and 5.2 for Mair et al. (2000) and Moore et al. (2006) respectively), and those recorded for the serpulid reefs (5.0) Chapman (2004). The similar diversity index values along with the high number of species found in the present study place L. hians beds among, what are considered (Holt et al., 1998), the most rich and diverse biogenic reefs in UK waters. Of the 16 phyla found in this investigation almost a third of all species were annelids, and of these all except one species were polychaetes. Within this group the presence of a large number of hesionids (7 species) and syllids (17 species) further highlights the diversity and complexity of the beds. A typical L. hians nest covers a variety of sediments (e.g. shell, gravel and muddy mixed sediments) which can also be bound to the L. hians beds by byssal attachment. In this investigation the rich polychaete assemblage may thus be a reflection of the varying sediments and microhabitats found on these beds. In this study 19 out of 20 cores recorded at least a single Flabelligera affinis worm. Interestingly a concurrent study (Trigg et al., unpublished) found that when cages containing L. hians nest material were brought to the surface, every gallery (.70) contained one or more F. affinis. Hall-Spencer & Moore (2000b) propose that F. affinis could be a commensal inhabitant of L. hians nests and future work should investigate whether a possible relationship exists between these species. Despite the high numbers of species found at the 2 L. hians beds investigated it is thought that these values are an

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underestimation of the total species using the habitat. The meiofaunal community were not investigated by this study; although a preliminary examination did not show a particularly well developed community in terms of abundance, and large motile organisms observed at each site (e.g. Necora puber, Gadus morhua and Asterias rubens) were not sampled. Several entries in the taxa list probably contained more than one species (e.g. Nemertina, Enchytraeidae and Nematoda) but could not be identified in the time available. Likewise the preponderance of high numbers of juveniles without clear defining features may have also reduced the total species found. The natural damage inflicted upon L. hians beds (see above), indicates that although the bed is generally stable, under certain conditions parts of the L. hians nest are subject to a reduction in nest cover. Following these or anthropogenic impacts the disturbed community may be significantly different from the community found on the original bed. The disturbed community possibly consisting of a less diverse assemblage, with opportunistic species taking advantage of the dislodged material and an increase in epifaunal scavengers, such as juvenile Gadus morhua, as food becomes available (Hall, 1994; Kaiser & Spencer, 1994; Hall-Spencer & Moore, 2000b). Over time it is thought that the community will establish a group of organisms partly typifying the adjacent environment in addition to some characteristic species for the surrounding habitat. Despite the beds being recognized as a relatively long-lived and stable environment if undisturbed (see Minchin, 1995) it has been observed that they are continuously assimilating new material onto the surface and edges of the bed (Trigg, personal observation). Thus it is believed that the beds are in a constant state of flux. Svane & Setyobudiandi (1996) state how species diversity and abundance of the community assemblage on a Mytilus edulis bed could be significantly influenced by its dynamic nature, this is also considered true of L. hians beds. The rapid production of nests and binding of passing and surrounding material by L. hians has been observed in situ (Trigg, personal observation) and in aquaria (Merrill & Turner, 1963). Moreover, the regular process of the animal secreting and attaching threads will provide new habitats such as the interstitial, allowing animals, for example hesionid and syllid worms, to colonize. This development is thought to constantly add organisms to the community, by provision of a suitable living space. In summary, the L. hians beds investigated in this study showed comparable levels of species richness and diversity with those found on the most diverse and rich biogenic reefs in UK waters. The results indicate that the associated community of these shallow L. hians beds are subject to temporal and geographical variations, the summer containing a significantly richer community than the winter period. However, before it can be concluded that temporal changes occurring on a particular L. hians bed are a result of regular seasonal patterns, it is advised that future studies be carried out over several years. The complex dynamic nature of the beds means a number of factors should be considered, i.e. the continual assimilation of material and organisms to the bed, the stochastic variability associated with settlement of invertebrates and the damage to beds from natural occurrences. The geographical differences seen in this investigation show that rather than considering all L. hians beds to be a similar entity each bed should be assessed individually.

These are important points when determining the habitat’s conservational significance and thus how it might be protected by future legislation.

ACKNOWLEDGEMENTS

The authors thank the Esme´e Fairbairn Foundation and SPLASH programme for their support. We would also like to thank S. Hamilton for providing taxonomic expertise (Polychaeta) and the referees for their comments.

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Gilmour T.H.J. (1967) The defensive adaptations of Lima hians (Mollusca, Bivalvia). Journal of the Marine Biological Association of the United Kingdom 47, 209–221.

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Hall S.J. (1994) Physical disturbance and marine benthic communities: life in unconsolidated sediments. Oceanography and Marine Biology: an Annual Review 32, 179–239.

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Hall-Spencer J.M. and Moore P.G. (2000a) Scallop dredging has profound long-term impacts on maerl habitats. ICES Journal of Marine Science 57, 1407–1415.

Tebble N. (1976) British bivalve seashells: a handbook for identification. London: British Museum (Natural History), 212 pp.

Hall-Spencer J.M. and Moore P.G. (2000b) Limaria hians (Mollusca: Limacea): a neglected reef forming keystone species. Aquatic Conservation: Marine and Freshwater Ecosystems 10, 267–277. Holt T.J., Rees E.I., Hawkins S.J. and Seed R. (1998) Biogenic reefs (Volume IX). An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scottish Association for Marine Science (UK Marine SACs Project), 170 pp. Kaiser M.J. and Spencer B.E. (1994) Fish scavenging behaviour in recently trawled areas. Marine Ecology Progress Series 112, 41–49. Landless P.J. and Edwards A. (1976) Economical ways of assessing hydrography for fish farms. Aquaculture 8, 29–43. Mackie A.S.Y., Oliver P.G. and Rees E.I.S. (1995) Benthic biodiversity in the southern Irish Sea. Studies in Marine Biodiversity and Systematics ˆ R Reports 1, 263 pp. from the National Museum of Wales, BIOMO Mair J.M., Moore C.G., Kingston P.F. and Harries D.B. (2000) A review of the status, ecology and conservation of horse mussel Modiolus modiolus beds in Scotland. Edinburgh: Scottish Natural Heritage, Commisioned Report No. F99PA08, 64 pp. Merrill A.S. and Turner R.D. (1963) Nest building in the bivalve genera Musculus and Lima. Veliger 6, 55–59. Minchin D. (1995) Recovery of a population of the flame shell, Lima hians, in an Irish bay previously contaminated with TBT. Environmental Pollution 90, 259–262. Minchin D., Duggan C.B. and King W. (1987) Possible effects of organotins on scallop recruitment. Marine Pollution Bulletin 18, 604–608. Moore C.G., Saunders G.R. and Harries D.B. (1998). The status and ecology of reefs of Serpula vermicularis L. (Polychaeta: Serpulidae) in Scotland. Aquatic Conservation: Marine and Freshwater Ecosystems 8, 645 –656. Moore C.G., Saunders G.R., Harries D.B., Mair J.M., Bates C.R. and Lyndon A.R. (2006) The establishment of site condition monitoring of the subtidal reefs of Loch Creran Special Area of Conservation. Edinburgh: Scottish Natural Heritage, Commissioned Report No. F02AA409, 119 pp. Rees E.I.S., Sanderson W.G., Mackie A.S.Y. and Holt R.H.F. (2008) Small-scale variation within a Modiolus modiolus (Mollusca: Bivalvia) reef in the Irish Sea. III. Crevice, infauna and epifauna from targeted cores. Journal of the Marine Biological Association of the United Kingdom 88, 151–156. Roberts D., Davies C., Mitchell A., Moore H., Picton B., Portig A. and Preston J. (2004) Strangford Lough Ecological Change Investigation (SLECI). 2. The current status of Strangford Lough Modiolus beds. Report to Environment and Heritage Service by the Queen’s University, Belfast, 76 pp. Seaward D.R. (1990) Distribution of the marine molluscs of North West Europe. Peterborough: Nature Conservancy Council, 114 pp. SMEBD (Society for the Management of European Biodiversity Data) (2010) The world register of marine species. http://www.marinespecies.org (accessed 3 March 2010).

Tilman D. (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474. Trigg C. and Moore C.G. (2009) Recovery of the biogenic nest habitat of Limaria hians (Mollusca: Limacea) following anthropogenic disturbance. Estuarine, Coastal and Shelf Science 82, 351–356. Tupper M. and Boutilier R.G. (1995) Effects of habitat on settlement, growth, and postsettlement survival of Atlantic cod (Gadus morhua). Canadian Journal of Fisheries and Aquatic Sciences 52, 1834–1841. and Wood E. (1988) Sea life of Britain and Ireland. London: Immel Publishing, 240 pp.

Correspondence should be addressed to: C. Trigg Scottish Natural Heritage Great Glen House Leachkin Road, Inverness, IV3 8AW Scotland, UK email: [email protected]

APPENDIX

Taxa recorded from two Limaria hians beds on the west coast of Scotland during June 2006 and January 2007. Phyla are depicted in bold lettering and authorities are listed alongside entries. Note that Syllis sp. H is currently without a species name (Hamilton, personal communication). RHODOPHYTA Phycodrys rubens (Linnaeus) Batters, 1902 Dasya hutchinsiae Harvey, 1833 Heterosiphonia plumose (Ellis) Batters, 1902 Brongniartella byssoides (Goodenough & Woodward) Schmitz, 1893 Colaconema daviesii (Dillwyn) Stegenga, 1985 Polysiphonia stricta (Dillwyn) Greville, 1824 Pterosiphonia parasitica (Hudson) Falkenberg, 1901 Audouinella microscopica (Na¨geli in Ku¨tzing) Woelkerling Audouinella purpurea (Lightfoot) Woelkerling, 1973 Bonnemaisonia asparagoides (Woodward) C. Agardh, 1822 Bonnemaisonia hamifera (as Trailliella intricata) Hariot, 1891 Palmaria palmata (Linnaeus) Kuntze, 1891 Peyssonnelia spp. Decaisne, 1841 Hildenbrandia sp. Nardo, 1834 Lithothamnion glaciale Kjellman, 1883 Melobesia membranacea (Esper) Lamouroux, 1812 Phymatolithon lenormandii (Areschoug) Adey, 1966 Erythrotrichia carnea (Dillwyn) J. Agardh, 1883 Plocamium cartilagineum (Linnaeus) Dixon, 1967 Rhodophyllis divaricata (Stackhouse) Papenfuss, 1950 Cruoria pellita (Lyngbye) Fries, 1836 Aglaothamnion bipinnatum (P. Crouan & H. Crouan) Feldmann-Mazoyer, 1941

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Appendix. Continued

Appendix. Continued Aglaothamnion tenuissimum (syn. A. byssoides) (Bonnemaison) Feldmann-Mazoyer, 1941 Callithamnion tetragonum (Withering) S.F. Gray, 1821 Compsothamnion thuyoides (J.E. Smith) Na¨geli, 1862 Halurus flosculosus (Ellis) Maggs & Hommersand, 1993 Plumaria plumosa (Hudson) Kuntze, 1891 Pterothamnion plumula (Ellis) Na¨geli, 1855 Ptilota gunneri P. Silva, Maggs & L. Irvine, 1993 Porphyra umbilicalis (Linnaeus) Ku¨tzing, 1843 Cryptopleura ramosa (Hudson) Kylin ex L. Newton, 1931 Delesseria sanguinea (Hudson) Lamouroux, 1813 Haraldiophyllum bonnemaisonii (Kylin) A. Zinova, 1981 PHAEOPHYTA Pseudolithoderma extensum (P. Crouan et H. Crouan) S. Lund, 1959 Sphacelaria plumosa Lyngbye, 1819 Desmarestia aculeate (Linnaeus) Lamouroux, 1813 Hincksia sandriana (Zanardini) P. Silva, 1987 CHLOROPHYTA Ulothrix flacca (Dillwyn) Thuret, 1863 Ulothrix subflaccida Wille, 1901 Ulothrix speciosa (Carmichael) Ku¨tzing, 1849 PORIFERA Suberites domuncula Olivi, 1792 Leucosolenia sp. Bowerbank, 1864 Sycon ciliatum Fabricius, 1780 Terpios fugax Duchassaing & Michelotti, 1864 Cliona celata Grant, 1826 Mycale spp. J.E. Gray, 1867 Mycale subclavata (syn. Mycale similaris) Bowerbank, 1866 Clathria (Microciona) atrasanguinea Bowerbank, 1862 CNIDARIA Alcyonium digitatum Linnaeus, 1758 Hexacorallia spp. Edwardsia claparedii (Panceri, 1869) Eudendrium sp. Ehrenberg, 1832 Eudendrium ramosum (Linnaeus, 1758) Calycella syringa (Linnaeus, 1767) Opercularella lacerata (Johnston, 1847) Halecium undulatum Billard, 1921 Kirchenpaueria pinnata (Linnaeus, 1758) Abietinaria abietina (Linnaeus, 1758) Hydrallmania falcata (Linnaeus, 1758) Sertularia argentea Linnaeus, 1758 PLATYHELMINTHES Turbellaria spp. NEMERTINA Nemertina spp. Cerebratulus spp. Renier, 1804 NEMATODA Nematoda spp. SIPUNCULA Golfingia elongata (Keferstein, 1862) Golfingia margaritacea/sp. juv. (M. Sars, 1851) Golfingia vulgaris (de Blainville, 1827) ANNELIDA Harmothoe spp. juv./indet. Kinberg, 1856 Harmothoe extenuata (Grube, 1840) Harmothoe impar (Johnston, 1839) Lepidonotus squamatus (Linnaeus, 1758) Pholoe inornata Johnston, 1839 ¨ rsted, 1843 Pholoe baltica O Eteone longa (Faricius, 1780) Pseudomystides limbata (Saint-Joseph, 1888) Phyllodocinae spp.

Eulalia viridis (Johnston, 1829) ¨ rsted, 1843) Eumida sanguinea (O Eumida/Eulalia sp. juv/indet. Glycera lapidum Quatrefages, 1866 Goniadella gracilis (Verrill, 1873) Sphaerodorum gracilis (Rathke, 1843) Amphiduros fuscescens (Marenzeller, 1875) Gyptis rosea Marion, 1875 Hesiospina similis (Hessle, 1925) Kefersteinia cirrata (Keferstein, 1862) Nereimyra punctata (O.F. Mu¨ller, 1788) Ophiodromus pallidus (Clapare`de, 1864) Syllidia armata Quatrefages, 1866 Eurysyllis tuberculata Ehlers, 1864 Syllis cornuta (Rathke, 1843) Syllis sp. H. Savigny, 1818 Trypanosyllis coeliaca Clapare`de, 1868 Syllis armillaris (Mu¨ller, 1776) Eusyllis blomstrandi Malmgren, 1867 Syllides benedicti Banse, 1971 Syllides japonicus Imajima, 1966 Brania sp. Quatrefages, 1866 Exogone (Parexogone) hebes (Webster & Benedict, 1884) ¨ rsted, 1845 Exogone naidina O Sphaerosyllis bulbosa Southern, 1914 Erinaceusyllis erinaceus Clapare`de, 1863 Sphaerosyllis taylori Perkins, 1981 Prosphaerosyllis tetralix Eliason, 1920 Autolytus sp. Grube, 1850 Proceraea sp. Ehlers, 1864 Nereididae spp. juv. Johnston, 1865 Nereis pelagica Linnaeus, 1758 Platynereis dumerilii (Audouin & Milne-Edwards, 1833) Nephtys kersivalensis McIntosh, 1908 ¨ rsted, 1843 Euphrosine borealis O Nematonereis hebes Verrill, 1900 Lumbrineris gracilis (Ehlers, 1868) Protodorvillea kefersteini (McIntosh, 1869) Schistomeringos neglecta (Fauvel, 1923) Paradoneis lyra (Southern, 1914) Spionidae sp. indet. G.O. Sars, 1872 Aonides oxycephala (Sars, 1862) Laonice bahusiensis Soderstrom, 1920 Minuspio cirrifera (Wiren, 1883) Polydora spp. juv. Bosc, 1802 ¨ rsted, 1843) Polydora caeca (O Dipolydora caulleryi Mesnil, 1897 Prionospio sp. indet. Malmgren, 1867 Prionospio banyulensis Laubier, 1966 Microspio mecznikowianus Clapare`de, 1870 Caulleriella alata (Southern, 1914) Cirratulus cirratus (O.F. Mu¨ller, 1776) Cirriformia tentaculata (Montagu, 1808) Aphelochaeta sp. Blake, 1991 Flabelligera affinis M. Sars, 1829 Pherusa plumosa (O.F. Mu¨ller, 1776) Macrochaeta caroli Westheide, 1981 Macrochaeta clavicornis (M. Sars, 1835) Capitella capitata (Fabricius, 1780) Mediomastus fragilis Rasmussen, 1973 Notomastus latericeus M. Sars, 1851 Polyophthalmus pictus (Dujardin, 1839) Asclerocheilus intermedius (Saint-Joseph, 1894) ¨ rsted, 1843) Polyphysia crassa (O Scalibregma celticum Mackie, 1991

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biodiversity of limaria hians reefs

Appendix. Continued

Appendix. Continued Scalibregma inflatum Rathke, 1843 Sabellaria spinulosa Leuckart, 1849 Melinna palmata Grube, 1869 Trichobranchidae spp. juv. Malmgren, 1865 Terebellides stroemi M. Sars, 1835 Trichobranchus glacialis Malmgren, 1866 Amphitrite cirrata O.F. Mu¨ller, 1771 in 1776 Axionice maculate (Dalyell, 1853) Eupolymnia nebulosa (Montagu, 1819) Eupolymnia nesidensis (Delle Chiaje, 1828) Lanassa venusta (Malm, 1874) ¨ rsted, 1844) Nicolea zostericola (O Phisidia aurea Southward, 1956 Pista cristata (O.F. Mu¨ller, 1776) Lysilla nivea Langerhans, 1884 Polycirrus spp. juv./indet. Grube, 1850 Polycirrus medusa Grube, 1850 Polycirrus norvegicus Wollebaek, 1912 Sabellidae sp. indet. Branchiomma bombyx (Dalyell, 1853) Jasmineira elegans Saint-Joseph, 1894 Serpulidae sp. indet. Rafinesque, 1815 Hydroides norvegicus Gunnerus, 1768 Pomatoceros lamarcki (Quatrefages, 1866) Pomatoceros triqueter (Linnaeus, 1767) Serpula vermicularis Linnaeus, 1767 Janua pagenstecheri (Quatrefages, 1865) Paradexiospira vitrea (Fabricius, 1780) Spirorbis spirorbis (Linnaeus, 1758) Tubificoides amplivasatus (Erse´us, 1975) Enchytraeidae spp. PYCNOGONIDA Achelia echinata Hodge, 1864 Callipallene sp. Flynn, 1929 CRUSTACEA Verruca stroemia (O.F. Mu¨ller, 1776) Balanus balanus (Linnaeus, 1758) Balanus crenatus Bruguie`re, 1789 Praunus inermis (Rathke, 1843) Hemimysis lamornae (Couch, 1856) Gammaridea sp. indet. Latreille, 1802 Apherusa bispinosa (Bate, 1857) Perioculodes longimanus (Bate & Westwood, 1868) Parapleustes assimilis (Sars, 1882) Amphilochus manudens Bate, 1862 Amphilochus neapolitanus Della Valle, 1893 Gitana sarsi Boeck, 1871 Cressa dubia (Bate, 1857) Stenothoidae spp. Boeck, 1871 Metopa pusilla Sars, 1892 Stenothoe marina (Bate, 1856) Stenothoe monoculoides (Montagu, 1815) Urothoe elegans (Bate, 1857) Metaphoxus fultoni (Scott, 1890) Acidostoma obesum (Bate & Westwood, 1861) Lysianassa ceratina (Walker, 1889) Perrierella audouiniana (Bate, 1857) Tryphosella sarsi Bonnier, 1893 Iphimedia obesa Rathke, 1843 Liljeborgia kinahani (Bate, 1862) Liljeborgia pallida (Bate, 1857) Dexamine thea Boeck, 1861 Ampelisca spinipes Boeck, 1861 Melitidae spp. 1 Bousfield, 1973 Ceradocus semiserratus (Bate, 1862)

Cheirocratus sundevalli (Rathke, 1843) Maera othonis (Milne-Edwards, 1830) Gammaropsis nitida (Stimpson, 1853) Ischyroceridae spp. Stebbing, 1899 Aoridae spp. Walker, 1908 Leptocheirus pectinatus (Norman, 1869) Microdeutopus spp. Costa, 1853 Corophium bonnellii (Milne-Edwards, 1830) Caprella spp. Guilding, 1824 Gnathia dentata G.O. Sars, 1872 Anthura gracilis (Montagu, 1808) Janira maculosa Leach, 1814 Munna sp. Kro¨yer, 1839 Munna minuta Hansen, 1916 Pseudoparatanais batei (G.O. Sars, 1882) Tanaopsis graciloides (Liljeborg, 1864) Vaunthompsonia cristata Bate, 1858 Nannastacus unguiculatus (Bate, 1859) Hippolyte varians Leach, 1814 Thoralus cranchii (Leach, 1817) Crangon crangon (Linnaeus, 1758) Pisidia longicornis (Linnaeus, 1767) Inachus dorsettensis (Pennant, 1777) Eurynome aspera (Pennant, 1777) Pilumnus hirtellus (Linnaeus, 1761) Copepoda spp. MOLLUSCA Polyplacophora spp. indet. Gray, 1821 Leptochiton asellus (Gmelin, 1791) Tonicella marmoreal (Fabricius O., 1780) Emarginula fissura (Linnaeus, 1758) Tectura virginea (O.F. Mu¨ller, 1776) Ansates pellucida (Linne´, 1758) Gibbula umbilicalis (da Costa, 1778) Dikoleps pusilla (Jeffreys, 1847) Tricolia pullus (Linnaeus, 1758) Lacuna vincta (Montagu, 1803) Rissoa interrupta (J. Adams, 1800) Rissoa parva (da Costa, 1778) Pusillina inconspicua (syn. Rissoa) (Alder, 1844) Alvania beani (Hanley in Thorpe, 1844) Alvania punctura (Montagu, 1803) Crisilla semistriata (Montagu, 1808) Cingula trifasciata (Adams J, 1800) Onoba semicostata (Montagu, 1803) Trophonopsis muricatus (Montagu, 1803) Odostomia eulimoides (syn. Brachystomia) (Hanley,1844) Onchidoris muricata (O.F. Mu¨ller, 1776) Nucula nucleus (Linnaeus, 1758) Mytilidae spp. juv. Rafinesque, 1815 Mytilus edulis (Linnaeus, 1758) Crenella decussata (Montagu, 1808) Musculus discors (Linnaeus, 1767) Modiolus modiolus (Linnaeus, 1758) Modiolula phaseolina (Philippi, 1844) Limaria hians (Gmelin, 1791) Chlamys varia (Linne´, 1758) Aequipecten opercularis (Linnaeus, 1758) Anomia ephippium Linnaeus, 1758 Pododesmus patelliformis (Linnaeus, 1761) Heteranomia squamula (Linnaeus, 1758) Galeommatoidea spp. indet. J.E. Gray, 1840 Kurtiella bidentata (Montagu, 1803) Neolepton sulcatulum (Jeffreys, 1859)

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Appendix. Continued

Appendix. Continued Parvicardium ovale (G.B. Sowerby II, 1840) Parvicardium scabrum (Philippi, 1844) Abra alba (W. Wood, 1802) Dosinia lupinus (Linnaeus, 1758) Tapes rhomboides (Pennant, 1777) Venerupis juv./indet. Lamarck, 1818 Mya truncata (Linnaeus, 1758) Hiatella arctica (Linnaeus, 1767) Thracia villosiuscula (Macgillivray, 1827) Chamelea gallina (syn. Venus striatula) (Linnaeus, 1758) ECHINODERMATA Antedon bifida (Pennant, 1777) Ophiothrix fragilis (Abildgaard, 1789) Ophiocomina nigra (Abildgaard, in O.F. Mu¨ller, 1789) Amphipholis squamata (Delle Chiaje, 1828) Psammechinus miliaris (P.L.S. Mu¨ller, 1771) TUNICATA Ciona intestinalis (Linnaeus, 1758) Ascidia mentula O.F. Mu¨ller, 1776 PLEUROGONA juv./indet. Botryllus schlosseri (Pallas, 1766)

Botrylloides leachii (Savigny, 1816) Pyura microcosmus (Savigny, 1816) Didemnum maculosum (Milne-Edwards, 1841) BRYOZOA Crisidia cornuta (Linnaeus, 1758) Disporella hispida (Fleming, 1828) Alcyonidium diaphanum (Hudson, 1778) Cribrilina cryptooecium Norman, 1903 Escharella immersa (Fleming, 1828) Tubulipora spp. Lamarck, 1816 Microporella ciliata (Pallas, 1766) Fenestrulina malusii (Audouin, 1826) Haplopoma graniferum (Johnston, 1847) Chorizopora brongniartii (Audouin, 1826) Eucratea loricata (Linnaeus, 1758) Electra pilosa (Linnaeus, 1767) Pyripora catenularia (Fleming, 1828) Callopora dumerilii (Audouin, 1826) Callopora lineata (Linnaeus, 1767) Amphiblestrum spp. J.E. Gray, 1848 Scrupocellaria scruposa (Linnaeus, 1758)

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