Effect of disturbance on assemblages: an example using porifera.
The development of any community (e.g., mature or young) is controlled by a suite of biological and physical factors that may be closely related and interlinked (Buss and Jackson, 1979). In some marine environments, such as caves, communities (all species) are well developed (mature); in others, such as ice-scoured polar shores, all communities tend to be poorly developed (young). Yet there are other localities that contain communities in various stages of development in proximity to one another. Lough Hyne is such an example, where adjacent communities may experience some similar conditions (e.g., flow rate, temperature, food concentration) but are at different stages of development. For example, rocks in areas with fast currents, where disturbance is high, may have less well-developed communities than rocks in areas experiencing slight current flow, where disturbance is reduced (Maughan and Barnes, 2000a), even though they are separated by less than 300 m. The same may be true for sublittoral cliff habitats where climax community states may be achieved only under certain environmental conditions. In the case of rocks, size may also be important to community development because smaller rocks are more likely to be moved than larger rocks, causing differences in community (all species) and assemblage (component phyla) composition (Barnes et al., 1996). Unstable or highly disturbed (e.g., small rocks) habitats are often colonized by fast-growing, opportunistic, and r-strategic species that are able to quickly take advantage of newly created habitats or space (Lilly et al., 1953; Osman, 1977; Sousa, 1979; Barnes et al., 1996; McCook and Chapman, 1997).
Sponges are an important component of hard-substratum communities throughout most polar (e.g., Dayton, 1978), temperate (e.g., Hiscock et al., 1983; Bell and Barnes, 2000a), and tropical regions (e.g., Alcolado, 1990). There is a wide body of literature that considers the influence of environmental parameters on the composition of sponge assemblages (e.g., Wilkinson and Cheshire, 1989; Alcolad, 1990; Alvarez et al., 1990; Diaz et al., 1990; Schmahl, 1990; Witman and Sebens, 1990). There are also examples of studies comparing sponge assemblages on large (100-1000 km) spatial scales (Maldonado and Uriz, 1995; Hooper et al., 2002) and on smaller scales (2-20 km) between sponges inhabiting mangrove pools (Rutzler et al., 2000). However, comparisons between different habitat types (e.g., between loose rock and cliffs) under fixed environmental conditions or on local scales (hundreds of meters) where confounding effects are reduced are less common.
Studies of sponge assemblages suggest that a number of physical factors control species distributions; these factors include water flow rate (Bell and Barnes, 2000a), sedimentation (Konnecker, 1973), nutrient levels (Storr, 1976), depth (Alvarez et al., 1990; Witman and Sebens, 1990), light (Sara. et al., 1978; Cheshire and Wilkinson, 1991), and habitat availability (Konnecker, 1973; Barthel and Tendal, 1993). Habitats classified within these physical parameters (e.g., fast water flow at a depth of 20 m) often contain many smaller or cryptic habitats with their own predefined physical characteristics. For example, at a site of slight water flow, where sedimentation is high, the amount of sediment falling on inclined, vertical, or overhanging cliff surfaces varies considerably, resulting in different assemblages on each surface type (see Bell and Barnes, 2000b, c). Although not as well studied, biological factors are also known to influence the composition of sponge assemblages (see Paine, 1974; Wulff, 1995, 2000), and predation may also limit the local distribution of sponge species (Dunlap and Pawlik, 1996; Wulff, 2000; Bell, 2001). Rich sponge assemblages on sublittoral cliffs at Lough Hyne have been the focus of recent studies, but abundant and diverse sponge populations also occur on the undersides of loose rocks (Lilly et al., 1953; van Soest and Weinberg, 1980; van Soest et al., 1981). At many sites within Lough Hyne, these two habitats can be separated by less than 1 m, providing the opportunity to investigate differences between sponge assemblages occurring in habitats experiencing different levels of stability, without the confounding effects created by larger spatial scales.
The high overall diversity and richness found on hard substrata within Lough Hyne, coupled with the large range of local habitat stability, results in assemblages at various stages of development existing in proximity. Such environmental characteristics provide opportunities to examine the contribution of certain taxa (in this case sponges) to the overall community. This study investigates assemblages inhabiting three substratum types--artificial panels (the most ephemeral), rocks, and cliffs (the most stable)--which represent a qualitative series in terms of habitat stability (i.e., amount of disturbance). The degree of development of sponge assemblages at different levels of habitat stability can be investigated within a particular environmental regime (e.g., fast flow rates). Also, the use of a common substratum (i.e., panel, rock, and cliff) between sites with different environmental conditions (flow regime) gives a second environmental gradient based on flow-rate-generated disturbance (rather than habitat stability). This study attempts to answer four questions: (1) How do sponge assemblages vary with environmental conditions and habitat stability? (2) How does the composition of sponge assemblages vary with water flow rate compared with different rock sizes; both are surrogate measures of disturbance, so do they have similar consequences? (3) Are there discriminating species for (local) habitats of differing stability and flow rates? (4) Are there consistent similarities or differences in assemblage composition in extremes of flow rate and habitat stability?
Materials and Methods
Lough Hyne Marine Nature Reserve (Fig. 1) is a small (0.5 [km.sup.2]) temperate sea lough on the southwest coast of Ireland (51[degrees]29'N, 9[degrees]18'W). It is characterized by a large number of habitats within a small area (Kitching, 1987). Habitats range from current-swept cliff faces to soft-sediment basins where water currents are slight. The lough is connected to the adjacent Atlantic coast by a shallow and narrow channel (The Rapids). This constriction results in an unusual tidal regime whereby water flows into Lough Hyne for about 4 h and out for 8 h. The squeeze causes fast current velocities (>250 cm [s.sup.-1]) in the eastern parts of the lough during inflow, but only slight surface currents in the vicinity of the rapids during outflow (Bassindale et al., 1957). As water moves from east to west across the lough, there is a quick reduction in current flow rate with a corresponding increase in sedimentation.
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The small size of Lough Hyne means that communities are only separated on small spatial scales (hundreds of meters). Nevertheless, these communities are discrete because cliff and rock habitats in different parts of the lough are separated by soft sediments. Sponge assemblages are thus isolated and predictable, rather than occurring along a continuous gradient. Different substratum types (i.e., rocks, cliffs, and panels) within a specific environment were separated by less than several meters and therefore not discrete. Panels were sited at Labhra Cliff and Whirlpool Cliff, and rock habitats were sampled at West Cliff and Whirlpool Cliff (Fig. 1). West Cliff and Labhra Cliff have similar sedimentation and rates of water flow, and the sponge assemblages are also similar. Both sites are characterized by slight current flow rates (<5 cm [s.sup.-1]) and heavy sediment accumulation, which increases with depth. Hard substratum extends more than 30 m at both of these sites. Rocks were not sufficiently abundant at Labhra Cliff to sample. Whirlpool Cliff experiences a very fast (>200 cm [s.sup.-1]), unidirectional flow regime, resulting in high disturbance. This site extends to about 18 m, and current flow rates decrease with depth, falling to 100 cm [s.sup.-1] at 18 m (Fig. 2). Some data were taken from the literature (Bell and Barnes, 2000a) to enable greater comparison between sponge assemblages from different habitats within Lough Hyne. These data, which were included in the analysis, concerned sponge assemblages inhabiting vertical and inclined surfaces on sublittoral cliffs at Labhra Cliff, West Cliff, Whirlpool Cliff, and Bullock Island (an adjacent Atlantic coastal site with a turbulent flow regime). The tidal range within Lough Hyne is about 1.5 m.
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Sampling and observation methods
The artificial substrata (panels) used were square machined slate panels (15 x 15 cm), prepared and assembled as for Turner and Todd (1994). They were used to investigate an early pioneer stage in community succession. A blue square (10 cm x 10 cm) was drawn in the center of each panel with a permanent blue marker pen. Panels were placed in running water for 24 h and then dried; this process was repeated twice more prior to deployment. The blue background makes it easier to identify recruits that are small or translucent. Three panels (forming one panel array) were attached by cable ties to welded steel bars. The panel array was positioned with the blue surfaces facing down (to simulate the undersides of a boulder). Bolts at the corner of each steel frame allowed the panels to be adjusted so they were 20 mm above the substratum. Panel arrays were deployed at depths of 0 m, 6 m, and 12 m at Labhra Cliff and Whirlpool Cliff. The first panels were deployed at the start of October 1997 and were replaced bimonthly until March 2001. Before panels were replaced, they were cleaned using a razor blade. Each panel was examined under a binocular microscope, and the number of sponge recruits was recorded. Spicule preparations of sponge recruits were made to confirm identification. Additional panel arrays were placed at the same depths, but were not replaced bimonthly. Each panel was photographed 1, 2, 6, and 12 months after the date of deployment. Photographs were then projected onto a grid composed of 400 random dots, and the percentage cover of sponges on each panel was estimated. The mean percent cover was calculated for panels submerged at each time interval.
Twenty-five rocks were randomly selected within three size classes--small (10-150 [cm.sup.2]), medium (151-500 [cm.sup.2]), large (501-1000 cm [s.sup.-1]), and very large (1001-2000 cm [s.sup.-1]) such that equal numbers of boulders of each size were examined (i.e., this does not represent the true boulder size distribution). The surface areas of both upper and lower rock surfaces were measured using a transparent cloth marked in square centimeters. The number of sponges (number of patches) for each species on each rock was recorded. Each species was photographed, and samples were taken for spicule analysis to confirm identification. Sponge samples were dissolved in concentrated nitric acid, or bleach as required, and were examined through a compound microscope at high power (x400). All observations were made between October 1999 and February 2000, which eliminated faunistic inter-site differences caused by seasonal growth or tissue retraction over the study period.
The morphologies of all sponges observed on rocks were classified within the following groups (after Boury-Esnault and Ruizler, 1997; Bell and Barnes, 2000d): encrusting (EN), flabellate (FL), clathrate (CL), massive (MA), arborescent (AR), repent (RE), tubular (TU), ficiform (FI), massive globulose (MG), and papillate (PA).
Data visualization and statistical procedures
Data were subjected to Bray-Curtis similarity analysis using hierarchical agglomerative group-average clustering for all habitats and depths (including data from Bell and Barnes, 2000a). This analysis was performed using the unweighted pair group method using arithmetic averages (UPGMA) with the PRIMER program (ver. 5.2.8, Plymouth Marine Laboratory, Plymouth, England). Data were log (x + 1) transformed to reduce the importance of extreme values (rare species). Ordination by non-metric Multi-Dimensional Scaling (MDS in PRIMER) was undertaken on a dissimilarity matrix created from Bray-Curtis similarity analysis. SIMPER analysis (in PRIMER) was used to determine the contribution of each species to the average Bray-Curtis dissimilarity between habitats and sites. This method of analysis determines which species are responsible for any differences that occur. Data were transformed as for Bray-Curtis analysis. Because sampling areas differed between habitat types, the area of each habitat and the abundance of each species were scaled up or down to standardize sampling areas between sites, depths, and habitats (sponges [m.sup.-2]).
Patterns of species diversity for sponge assemblages on rocks were described with the Shannon and Weiner (Krebs, 1989) information function H' = [SIGMA][p.sub.i]ln [p.sub.i]. Paired Student's t tests were used to examine differences between rock surface types. A general linear model analysis of variance (GLM ANOVA) was used to compare logarithmically (Logl0) transformed sponge species diversity, richness, and rock surface area relationships between West Cliff and Whirlpool Cliff. The same method was used to compare the untransformed relationship between sponge density and rock surface area. This method compares the average linear relationship to an average linear relationship fitted to all the data. Kruskall-Wallis tests were used to compare the differences between percentage cover on submerged panels after 1, 2, 6, and 12 months.
A total of 96 species were reported during this study, 44 of which were found on rocks and 76 from cliff habitats (Table 1). Twenty-five sponge species were shared between rock and cliff habitats. All but two of the species (Hymeniacidon perlevis and Halichondria bowerbanki) of sponge found on rocks occurred oil the undersides. These two species were often found growing on the fronds of algae as well as on rock surfaces. Although sponge assemblages varied considerably between habitat types, there was little variation between rock sponge assemblages inhabiting the different sites (extremes of water flow rate) (Table 2). Of the 44 species inhabiting rocks, only 7 (16%) differed between West Cliff and Whirlpool Cliff, with only 1 of these species (Mycale rotalis) being found exclusively at Whirlpool Cliff'. The remaining 6 species were only found at West Cliff. Nineteen of the 44 species found on rocks were exclusive to rock habitats, illustrating the high degree of species exclusivity within this habitat type. The panels at Labhra Cliff and Whirlpool Cliff showed no exclusive species, and only 7 species of sponge were reported (Table 1). Therefore, no juvenile settlement was recorded for the majority of sponge species reported during this study despite the nearly 4-year duration of panel deployment. All species found on panels occurred in both rock and cliff habitats. Because panels can be considered a similar habitat to rocks (but younger in terms of community development), community age was the most likely determinant of the composition of the sponge assemblage. Of the total 76 species of sponge reported from cliff habitats, 31 species (data included from Bell and Barnes, 2000a) were found at Bullock Island, compared to 40 species at Whirlpool Cliff and 52 from both Labhra Cliff and West Cliff (Table 3). Although many of these species were shared between cliff habitats, only 10 of the total 76 species were shared between all cliff habitats. Environmental parameters, therefore, proved important in determining the sponge assemblage in cliff habitats. A much higher proportion of species were shared within the same habitat than between different habitat types (Table 3). However, the proportion of species shared between sites was higher for rock and panel habitats (>85% than for cliff habitats (<50%).
On rocks, encrusting morphologies were the most abundant form (20 of 44 species), followed by massive (15 of 44 species) and repent forms (7 of 44 species) (all pooled rock data). The remaining species exhibited cylindrical (Scypha ciliatum) and clathrate forms (Clathrina coriacea). On cliff surfaces, 30 species were encrusting, 19 were massive, and 6 exhibited repent forms (pooling cliff data). Sponge species on panels had a wide range of morphologies (given the small number of species), including tubular, repent, encrusting, massive, and clathrate forms. Differences were observed between the proportions of sponge morphologies between certain habitats and sites (Table 4). There was a considerable difference between the proportion of morphologies between cliff sites (Table 3). Encrusting forms were more abundant at the high-energy cliff sites (Bullock Island and Whirlpool Cliff) than at low-energy sites (Labhra Cliff and West Cliff), where they were replaced by arborescent and papillate forms. In rock habitats, high proportions of enerusting and massive forms were found, with no differences between sites. Panel assemblages were also very similar in the proportions of morphologies between sites.
Identification of different sponge assemblages
Small sponges were difficult to identify, (particularly on panels) and potentially represent an error in the analysis. However, this problem was reduced by the transformation of the data prior to analysis, which decreased the importance of extreme values or apparent rare species.
Bray-Curtis similarity analysis and Multi-Dimensional Scaling (MDS) (Fig. 4) were used to distinguish between sponge assemblages within different habitats and sites. The Bray-Curtis analysis identified five major assemblage groups that showed increasing similarity, as follows: rocks (all sites and sizes), panels (all sites), Whirlpool Cliff, Bullock Island, and Labhra Cliff/West Cliff. However, each major assemblage group had a very low similarity (<25%) with the others. MDS distinguished two additional, smaller assemblages, which were not obvious from the Bray-Curtis analysis. The first of these assemblages was at 30 m at Labhra Cliff; it showed the greatest affinity with the other cluster at Labhra Cliff and West Cliff (cliff habitat). The second assemblage was composed of 0-m sponges at Labhra Cliff and West Cliff (cliff habitat). These assemblages were most similar to those at Whirlpool Cliff. The subtidal (6 and 12 m) panels had high levels of correspondence ([approximately equal to] 65%) between sites, but differed considerably from those in the intertidal zone (0 m) ([approximately equal to] 30% similarity). To account for morphological differences created by the nature of the different habitats, the same MDS and Bray-Curtis analysis was repeated using only species that exhibited encrusting or massive morphologies. However, no differences were observed between the original dendrogram and the 2-D scaling plot produced (output not shown).
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SIMPER analysis was used to determine which species were most responsible for the differences seen between sites and habitats with the Bray-Curtis analysis. Only the top five of these indicator, or "discriminating" species (those with the least similarity between different habitats) are illustrated (Table 5). The discriminating species between rock habitats (irrespective of site) and all other habitats were very similar. Plakortis simplex, Clathrina coriacea, Aplysilla rosacea, H. brondstedi, and L. complicata can all be considered indicative of rock habitats. When the rock assemblages from West Cliff and Whirlpool Cliff were compared, the discriminating species were, however, not those found at only one of the sites. The most important discriminating species from the cliffs at Bullock Island was Hemimycale columella. In most cases, Whirlpool Cliff could be characterized by the presence of Esperiopsis fucorum and Scypha ciliatum. For panel habitats, it was not possible to identify true discriminating species because only seven species were reported from panels. Therefore, the technique of using individual species as discriminating, or indicator, species was not applicable in these very young (panel) sponge assemblages.
Development of assemblages on panels
The contribution of sponges to early community development (panels) varied considerably between Whirlpool Cliff and Labhra Cliff (Fig. 5). The percentage cover of sponges on subtidal panels at Whirlpool Cliff and Labhra Cliff increased significantly (from about 0% to between 4% and 10% cover) over the 12-month period (Kruskal-Wallis, H < 11.12, P < 0.01, df = 4). In contrast, sponges did not constitute any part of the community on intertidal panels at either site (irrespective of time interval). At Labhra Cliff, the panels did not have a significantly higher percentage cover of sponges than at Whirlpool Cliff after 1, 2, or 6 months (at either 6 or 12 m). However, a significantly higher percentage cover (twice as high) of sponges was found on panels at Labhra Cliff than at Whirlpool Cliff after 12-month deployments at both 6 and 12 m (Mann-Whitney, W = 144, P < 0.01, df = 5).
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Assemblages on rocks
Bray-Curtis analysis and MDS showed that sponge assemblages on rock had a very high level of similarity (65%) between sites and different rock sizes (Fig. 4). But, when the cluster composed of assemblages from various sized rocks was considered alone, assemblages inhabiting medium, large, and very large rocks had a greater similarity between different sites than the assemblages on small rocks bad with other rock sizes within the same site. At both sites, assemblages on medium, large, and very large boulders gave rise to clusters that then formed a larger cluster with the small rock assemblages. Rock size had important influences on sponge assemblages (Table 2). A higher number of species was reported from larger rather than smaller rocks at both sites (as expected given the area effect). Yet few differences were observed between the sponge assemblages on the small and medium-sized rocks at West Cliff and Labhra Cliff.
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There was a logarithmic relationship between substratum area and sponge species diversity on rocks from both West Cliff and Whirlpool Cliff. Data were Log10 transformed, resulting in linear relationships (Fig. 6). The relationship between the number of sponges (per rock) and the area of rock surface at both sites was linear (Fig. 7). General linear model (GLM) ANOVA was used to compare the linear relationships between substratum area, number of sponges, and diversity. In the relationships between species diversity and area, no significant difference was observed in slope or intercept between West Cliff and Whirlpool Cliff (GLM ANOVA; F ratio = 0.07, P = 0.78, denominator df = 1, numerator df = 278). This was also true for the transformed relationships between species richness and rock surface area at West Cliff and Whirlpool Cliff (graph not shown) (GLM ANOVA; F-ratio = 1.1, P = 0.25, denominator df = 1, numerator df = 278). However, when GLM ANOVA was used to compare the linear relationship between sponge numbers and rock surface area, a significant difference was found between the slopes of the relationships at West Cliff and Whirlpool Cliff (GLM ANOVA; F ratio = 16.16, P < 0.001, denominator df = 1, numerator df = 278). Any unit increase in surface area resulted in a greater increase in sponge density at West Cliff than at Whirlpool Cliff. Also, any given rock size harbored a greater number of sponges at West Cliff than at Whirlpool Cliff.
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Animal communities are known to vary between large geographic areas (scale of kilometers), but the variability between localized habitats (1 to 100 m) under similar environmental conditions is far less well known. This is true for sponge assemblages: broad distributions have been described by habitat at Lough Hyne (Picton, 1991; van Soest and Weinberg, 1980; van Soest et al., 1981), and recently more detailed studies have added environmental variables to such distributions (Bell and Barnes, 2000b, c). As with most, if not all organisms, environmental factors are critical to the distribution of sponge species. To date, little quantitative information has been provided on localized (where confounding factors are minimized) habitat-associated differences between sponge assemblages in temperate localities.
Morphological variability with habitat stability and environmental characteristics
The studied sponge assemblages (within Lough Hyne) varied considerably between habitats of differing stability (i.e., cliff and boulders) and environmental conditions (i.e., high and low flow), even when habitats were separated by only several meters or less. Sponges inhabiting hard substratum have been shown to exhibit considerable morphological adaptation in response to a variety of factors, including flow regime, sedimentation, and substratum type, at both assemblage (Bell and Barnes, 2000d) and individual levels (Manconi and Pronzato, 1991; Bell et al., 2002). It seems, therefore, that morphology alone may account for some of these differences in assemblage composition between sites and habitats. The two-dimensional nature of rock (under-surface) habitats undoubtedly accounts for the high proportion of entrusting forms because the overt three-dimensional nature of many other sponge species common to cliff habitats is inhibited (e.g., arboresccnt forms). High-energy cliff sites were dominated by encrusting and massive forms and showed greater levels of similarity (in assemblage composition) to rock habitat assemblages than to those of low-energy cliffs. However, high proportions of entrusting and massive morphologies were round in both cliff and rock habitats, although the species compositions were very different. Morphology alone cannot account for all the differences found. Organisms living on the undersides of rocks have a number of advantages, including reduced competition from fast-growing algae found on upper rock surfaces, since many sponges are considered slow-growing (Ayling, 1983), and protection against potentially harmful UV radiation. Underside rock communities also experience reduced sediment settlement in areas of low current flow, reduced effects of desiccation (in the inter-tidal), and reduced predation from fish and other large invertebrates (Dunlap and Pawlik, 1996; Wulff, 2000). A combination of these factors may account for the presence or absence of any single species on the undersides of loose rocks. Therefore, the distribution and habitat of each species should be considered individually.
Morphology alone has already proved valuable in separating sponge assemblages inhabiting sublittoral cliffs (Bell and Barnes, 2000a). Increased numbers of delicate morphologies, exhibited by a number of species exclusive to low-energy sites, have been associated with decreasing flow rate and as a mechanism to reduce sediment settlement (Bell, 2001). However, the rate of water flow had little effect on the sponge assemblages found on rocks and apparently was not a regulatory factor of such assemblages (in the present study). One aspect of morphology that was not considered within this study is the potential importance of the surface texture of encrusting sponges in response to habitat disturbance or stability. For example, sponges with smooth surfaces may be suited to areas of high current flow since they experience reduced drag. Also, the actual flow (in terms of speed and direction) experienced by sponges may be significantly influenced by seabed characteristics (Hiscock, 1983), such that their morphology and species distribution may be influenced by microscale environmental characteristics, which are themselves difficult to characterize. For example, the overlying nature of loose rocks may lead to localized areas of negligible current flow, even in high-current areas.
Assemblage composition variability with flow rate and rock size
Negligible (between-site) differences in sponge diversity or species richness attributable to flow rate were found on the under-surfaces of rocks. This suggests that in rock habitats unlike cliff habitats (Bell and Barnes, 2000a), water flow rate is not directly important in determining the composition of sponge assemblages. Sponge diversity and richness did, as with most organisms, increase with area (rock size), which is usually termed an area effect. The density of sponges for any given rock size was greater at West Cliff than at Whirlpool Cliff, most likely due to reduced competition in low energy environments from superior spatial competitors such as colonial ascidians and anthozoans (Maughan and Barnes, 2000b; Bell, 2001a; Bell and Barnes, 2003). Increased sedimentation, to which sponges may show morphological and physiological adaptation, has been credited for the shift in competitive ability (Bell, 2001a). However, since the organisms inhabiting the undersides of rocks experience little direct sedimentation, other factors must be responsible for the lack of superior competitors, such as increased sediment loading (rather than direct settlement) in the water, a condition that sponges appear to tolerate (Lilly et al., 1953). Also important is the difference between upper and lower rock surfaces. The domination of sponges on lower surfaces relates to the absence of macroalgae, which has been considered to control both large-and small-scale sponge distributions (Witman and Scbens, 1990). Sponge proliferation on upper surfaces may also be prevented by interference competition from the sweeping action of algal fronds, as suggested for other invertebrates (Jenkins et al., 1999). The linear increase in the number of sponges with increasing surface area of rock may appear unusual. One might expect that the dominant sponge species would occupy most of the primary substratum (Russ, 1982; Maughan and Barnes, 2000b). However, competitive encounters and interactions between sponges may be nonhierarchical and resemble a network (Buss and Jackson, 1979; Bell and Barnes, 2003), thereby preventing monospecies dominance. Even if certain sponge species inhabiting rocks are dominant over others, these species may show seasonal growth and retraction of tissue that prevents them from monopolizing rock surfaces (Sara, 1970; Stone, 1970; Elvin, 1976; Barthel, 1989). The distribution of sponges may also be limited by other biological factors, in particular predation (e.g., Wulff, 1995); but in the observations of sponge assemblages at Lough Hyne, predation of sponges was rarely observed. Fish feeding on algae sometimes broke branches from arborescent species on cliffs, but extensive predation was not seen. Sponge population heterogeneity is also affected by competitive processes (Becerro et al., 1994), because interactions between spatial competitors influence the direction of growth (in encrusting species) and lead to the patchiness observed within habitats.
Disturbance has been considered an important factor structuring marine epifaunal communities, and rock size has been considered a surrogate of such disturbance (Dayton, 1971; Osman, 1977). This theory is based upon the principle that smaller rocks are more likely to be moved than larger rocks. However, all but the smallest rocks at Lough Hyne showed very similar sponge assemblages across sites experiencing differential flow rates. Sponge assemblages do vary between some surrogate measures of disturbance (flow rate), but not between actual extremes of habitat stability. This suggests that treatment of rock surface area as a surrogate measure of disturbance is unsatisfactory and shows no correlation between extremes of surrogate (i.e., small and large rocks) and true (i.e., high- and low-energy sites) measures of disturbance. At Lough Hyne, small rocks are often held in place by overlying larger rocks, as a result, the probability of motion can be lower (rather than higher) for small rocks than for larger rocks, because the movement of smaller rocks is dependent on the movement of larger rocks a priori. Thus, lack of space rather than level of community development (and age) can explain why impoverished sponge assemblages are seen more frequently on small rocks. For organisms (including sponges) that inhabit disturbed habitats (such as loose rocks), succession will be important in structuring the community. Occasional disturbance will prevent the development of a climax community and permit colonization by weaker competitors that might have been excluded from a habitat that had reached a state of climax.
Sponge assemblages on panels had little similarity with other habitats examined and, in contrast to findings with other taxa (Maughan and Barnes, 2000a; Barnes and Maughan, 2001), showed negligible inter-site differences. However, the space occupation (percentage cover) of sponges during the development of the (pioneer succession) panel assemblage varied significantly over the 12-month deployment period (continuous immersion for 12 months). The greater area occupied by sponges on the undersides of panels at Labhra Cliff than Whirlpool Cliff is consistent with the results of other studies of sponge assemblage differences between cliff environments at these two sites (Bell and Barnes, 2000a, d). Sponges are more abundant on panels, rocks, and cliffs at low-energy sites in Lough Hyne than at high-energy sites. Again, this is most likely due to reduced competition in low-energy environments from superior spatial competitors, such as colonial ascidians and anthozoans (Maughan and Barnes, 2000b; Bell, 2001; Bell and Barnes, 2003). All species found on panels submerged for 2-month periods were also found on rocks and cliffs. These early colonizers were important to both mature and immature communities, even though sponges are widely regarded as late colonizers (Dayton, 1971; Maughan, 2000). Since all species found on panels, which simulated early development of rock communities, were also found in cliff and rock habitats, we suggest that habitat is not as critical in determining species composition at this early stage in development as it is in more mature communities. However, sponge assemblages (rather than species) found on panels did show greater affinities with rock assemblages than with cliffs, which is to be expected given that the panels were used as a surrogate for young rock habitats. Even though a number of sponges were reported from the panels, it is also true that most of the species found in this study did not settle on the panels and thus can still be considered late colonizers of benthic communities. For a complete evaluation of the contribution of sponges to communities of different ages (since panels represent a pioneer succession stage, while cliff communities may be many years old), monitoring must extend over many more time intervals than in the present study. Small rock assemblages had a much greater affinity with the species found to inhabit panels, with two species (Leucosolenia complicata and Scypha ciliatum) being of particular interest. The presence of these two calcareous species is consistent with other studies of panels (Maughan and Barnes, 2000b) and of the early development of hard-substratum communites (Osman, 1977). These were two of only three calcareous sponges reported during the study, and they appear to be r-strategic, or opportunistic, in the use of newly available space. It is unclear if the calcareous nature of these sponges provides them with some adaptive advantage over siliceous sponges.
Are there discriminating species for (local) habitats of differing stability and experiencing different flow rates?
Most habitats and sites could be characterized by several abundant sponge species. Different cliff sites were easily distinguishable from each other and from other habitats on the basis of many species. In rock habitats seven species differed between the high- and low-energy sites, though they were too rare to be between-site discriminating species (as determined by SIMPER analysis). Given the similarities in assemblage composition, it is not surprising that the five most important discriminating species between rock and other habitats did not differ between sites. The low number and ubiquitous nature of species on artificial substrata made the identification of true inter-site discriminating species in this habitat irrelevant.
Are there consistent similarities or differences in assemblage composition from extremes of flow rate and habitat stability?
Although certain environmental characteristics have been found to influence sponge communities, patterns of sponge assemblages on rocks are not consistent with those described from other hard-substratum environments (Storr, 1976; Alvarez et al., 1990; Witman and Sebens, 1990; Bell and Barnes, 2000a). From our results, the abundance of sponges on rocks, but not the composition of the assemblage, seemed to be manifestly affected by rate of water flow.
Despite the late-colonizer "tag" applied to sponges in marine communities (Dayton, 1971; Maughan 2000), the present study found a number of species contributing to lithophyllic communities on panels that had been deployed for only a few months. Rock habitats did not display a consistent trend of decreasing similarity in assemblage composition from extremes of environmental stability, and rock size was judged to be more important than current flow rate in determining sponge assemblage composition. Disturbance seemed to be more important in determining sponge assemblage composition on cliffs than in loose rock habitats. This study has shown that habitat stability is an important factor to be taken into account along with other measures of disturbance such as flow rate, when considering the distribution of sponge species.
Table 1 Sponge species found within Lough Hyne on sublittoral cliff and rocks and on the adjacent Atlantic coast B W L W U H A C Antho involvens(A) (EN) * * Antho inconstans #(A) (EN) Aplysdlu rosea(A) (EN) * * Aplysilla sulfurea(A) (EN) * * * * Axinella damicornis (FL) * * Axinella dissimilis (AR) * * * Biemnia variantia (MA) * * Clathrina coriacea(A)(B) (CL) * * * Cliona celara(A) (MA) * * * * Dercitus bucklandi (A)# (MA) Dysidea fragilis(A)(B) (MA) * * * * Dysidea pallescens(A) (MA) * * Esperiopsis fucorum(A)(B) (RE) * * Eurypon sp. 1 (EN) * * Eurypon sp. 2 (EN) * * Eurypon sp. 3 (EN) * * Eurypon sp. 4 (EN) * * Eurypon sp. 5 (EN) * * Eurypon sp. 6 (EN) * * Eurypon sp. 7 (EN) * * Eurypon sp. 8 (EN) * * Halichondria bowerbanki(A) (RE) * * * Halichondria panicea(B) (EN) * * Haliclona cinerea (MA) * Haliclona fistulosa (RE) * * * * Haliclona simulans (RE) * Haliclona sp. 1 (MA) * * * Haliclona sp. 2 (MA) * * * Haliclona sp. 3 (RE) * Haliclona sp. 4 (MA) * * * Haliclona sp. 5(A) (MA) * * Haliclona sp. 6 #(A) (MA) Haliclona sp. 7 #(A) (RE) Haliclona sp. 8 #(A) (RE) Haliclona sp. 9 #(A) (RE) Haliclona sp. 10 #(A) (MA) Haliclona sp. 11 #(A) (MA) Haliclona sp. 12 #(A) (RE) Haliclona urceolus (TU) * * Haliclona viscosa (MA) * Halicnemia patera (EN) * * Halisarca sp. (MA) * Hemimycale columella (EN) * * Hymedesmia brondstedi #(A) (EN) Hymedesmia jecusculum #(A) (EN) Hymedesmia pansa #(A) (EN) Hymedesmia paupertus(A) (EN) * * Hymeniacidon perlevis(A) (MA) * * * * Hymeraphia stellifera (EN) * * * * Iophon hyndmani (EN) * Lophon ingalli(A) (EN) * * Iophonopsis nigricans (EN) * Laxosuberites incrutans (EN) * Leucasolenia complicata(A)(B) (RE) * * Leuconia nivea (EN) * * Microciona fallax(A) # (EN) Microciona strepsitoxa(A) # (EN) Mycale contarenii(A) (MA) * * * Mycale macilenta(A) (MA) * Mycale rotalis(A) (MA) * * Myxilla rosacea(A) (MA) * * Myxilla incrustans(A) (EN) Myxilla fimbriata (MA) * Pachymatistma johnstonia(A) (MA) * * Paratimea constellata (EN) * * * * Phakellia sp. (PA) * * Phorbas fictitius(A) (EN) * * Plakortis simplex(A) (EN) * * Plocamilla coriacea #(A) (EN) Polymastia sp. 1 (PA) * * Polymastia sp. 2 (PA) * * Polymastia sp. 3 (PA) * * Polymastia sp. 4 (PA) * * * Polymastia sp. 5 (PA) * * * Polymastia sp. 6 (PA) * * Polymastia sp. 7 (PA) * * * Polymastia sp. 8 (PA) * * * Pseudosuberites sulphureus (EN) * * Rhaphidostyla kitchingi (AR) * * Raspailia hispida (AR) * * * Raspailia ramosa (AR) * * * Scypha cilatum(A)(B) (TU) * * * * Spanioplon armaturum #(A) (EN) Stelligera rigida (FL) * * * Stelligera stuposa (AR) * * * * Stylostichon dives(A) (EN) * Stylostichon plumosum #(A) (MA) Suberites carnosus (FI) * * Suberites ficus (FI) * * Suberites sp. 1(A) (EN) * * Suberites sp. 2 (EN) * * * Suberites sp. 3 (EN) * * Suberites sp. 4 (EN) * Terpias fugax #(A) (EN) Tethya auranaum (MG) * * * * Unidentified sponges(B) An asterisk indicates species found at a particular site (BU, Bullock Island; WH, Whirlpool Cliff; LA, Labhra Cliff; WC, West Cliff). Underlining denotes species found on rocks, and the symbol # indicates that the species was exclusive to rocks; boldface type denotes species found on panels (none were exclusive). Uppercase letters in parentheses after the species name are macro-morphological descriptions: AR, arborescent; CL, clathrate; EN, encrusting: FI, ficiform; FL, flabellate; MA, massive; MG, massive globulose; PA, papillate; RE, repent; TU, tubular. Notes: (A) denotes species found on rocks. (B) type denotes species found an panels (none were exclusive). Table 2 Sponge species that were reported from the under (*) and upper (+) sides of rocks found at two sites at Lough Hyne West Cliff ([dagger]) Species (Morphology) (#) S M L VL Antho inconstans (EN) * * Antho involvens (EN) * * Aplysilla silfurea (EN) * * * * Aplysilla rosea (EN) * * * * Clathrina coriacea (CL) * * * * Cliona celata (MA) * * Dercitus bucklandi (MA) * * * Dysidea fragilis (MA) * * * * Dysidea pallenscens (MA) * * Esperiopsis fucorum (RE) * * * Haliclona sp. 1 (MA) * * * * Haliclona sp. 2 (RE) * * * * Haliclona sp. 3 (RE) * * * Haliclona sp. 4 (RE) * * * * Haliclona sp. 5 (MA) * * * * Haliclona sp. 6 (MA) * * * * Haliclona sp. 7 (MA) * * * Haliclona sp. 8 (MA) * * * * Halichondria bowerbanki (RE) (+) * + * + Hymedesmia brondstedi (EN) * * * * Hymedesmia jecusculum? (EN) * Hymedesmia pansa (EN) * Hymedesmia puupertus (EN) * * * Hymeniacidon perlevis (MA) (+) * + * + * + * + Iophon ingalli (EN) * Lenconia nivea (EN) * * * Leucosolenia complicata (RE) * * * * Microciona fallax (EN) * * * Microciona strepsitoxa (EN) * Mycale contarenii (MA) * * Mycale macilenta (MA) * * Mycale rotalis (MA) Myxilla rosacea (MA) * * * * Myxilla incrustans (EN) * Pachymatisma johnstonia (MA) * * * Phorbas fictitius (EN) * * Plakortis simplex (EN) * * * * Plocamilla coriacea? (EN) * Scypha ciliatium (TU) * * * Spanioplon armaturum (EN) * * Stylostichon dives (EN) * * * * Stylostichon plumosum (MA) * * * * Suberites sp. (EN) * * * * Terpios fugax (EN) * * Total number of species 18 27 37 43 Whirlpool Cliff ([dagger]) Species (Morphology) (#) S M L VL Antho inconstans (EN) * * * * Antho involvens (EN) * * Aplysilla silfurea (EN) * * * * Aplysilla rosea (EN) * * * * Clathrina coriacea (CL) * * * * Cliona celata (MA) * * Dercitus bucklandi (MA) * * * Dysidea fragilis (MA) * * * * Dysidea pallenscens (MA) * * Esperiopsis fucorum (RE) * * * Haliclona sp. 1 (MA) * * Haliclona sp. 2 (RE) * * * * Haliclona sp. 3 (RE) * * * * Haliclona sp. 4 (RE) * * * * Haliclona sp. 5 (MA) * * * * Haliclona sp. 6 (MA) * * * * Haliclona sp. 7 (MA) * * * Haliclona sp. 8 (MA) * * * Halichondria bowerbanki (RE) (+) * + * + Hymedesmia brondstedi (EN) * * * * Hymedesmia jecusculum? (EN) * * Hymedesmia pansa (EN) * * * Hymedesmia perlavis (EN) * * * Hymeniacidon puupertus (MA) (+) * + * + * + * + Iophon ingalli (EN) * Lenconia nivea (EN) Leucosolenia complicata (RE) * * * * Microciona fallax (EN) Microciona strepsitoxa (EN) * * Mycale contarenii (MA) Mycale macilenta (MA) Mycale rotalis (MA) * * Myxilla rosacea (MA) * * * Myxilla incrustans (EN) Pachymatisma johnstonia (MA) * * * * Phorbas fictitius (EN) Plakortis simplex (EN) * * * * Plocamilla coriacea? (EN) * Scypha ciliatium (TU) * * Spanioplon armaturum (EN) * * * Stylostichon dives (EN) * * * * Stylostichon plumosum (MA) * * * * Suberites sp. (EN) * * * Terpios fugax (EN) * * * Total number of species 17 25 30 30 # The morphological group of each species is given in parentheses: CL. clathrate: EN. encrusting; MA. massive; RE, repent: TU, tubular. ([dagger]) Four sizes of rock were distinguished: S, small; M. medium L. large: VL. very large. Table 3 The number of sponge species shared between sites WC (B) WH (B) BI (C) WH (C) (43.1) (38) (31) (40) [down [down [down [down Site arrow] arrow] arrow] arrow] WH (B) (38) 37 (84%) BI (C) (31) 14 (23%) 13 (23%) WH (C) (40) 16 (23%) 17 (28%) 22 (45%) LC (C) (52) 13 (16%) 13 (17%) 15 (22%) 22 (31%) WC (C) (52) 15 (19%) 16 (22%) 16 (24%) 20 (28%) WH (P) (7) 6 (14%) 6 (15%) 5 (15%) 6 (15%) WC (P) (7) 6 (14%) 6 (15%) 5 (15%) 6 (15%) LC (C) WC (C) WH (P) (52) (52) (7) [down [down [down Site arrow] arrow] arrow] WH (B) (38) BI (C) (31) WH (C) (40) LC (C) (52) WC (C) (52) 48 (86%) WH (P) (7) 3 (5%) 3 (5%) WC (P) (7) 3 (5%) 3 (5%) 7 (100%) Numbers in parentheses indicate total number of species at each site and habitat. C, cliff; B, rock, P, panel; WC, West Cliff; WH, Whirlpool Cliff; BI, Bullock Island; LC, Labhra Cliff. % indicates the proportion of all species shared for each pair of habitats: % = numher of shared species / (number of species at habitat A x number of species at habitat B)--number of shared species. Table 4 The number of sponge species showing different morphological types at different sites and habitats at Lough Hyne and the percentage of each morphology as a proportion of the total number of species Morphological Group [dagger] Site * EN MA RE PA FL Bullock Island (C) 14 8 4 2 0 45% 26% 13% 6% 0% Whirlpool Cliff (C) 16 10 5 2 0 40% 25% 13% 5% 0% Labhra Cliff (C) 17 12 2 9 2 33% 23% 4% 17% 4% West Cliff (C) 16 13 2 9 2 31% 25% 4% 17% 4% Whirlpool Cliff (B) 16 14 6 0 0 42% 37% 16% 0% 0% West Cliff (B) 20 15 6 0 0 47% 35% 14% 0 0 Whirlpool Cliff (P) 1 1 1 0 0 17% 17% 17% 0% 0% Labhra Cliff (P) 1 1 2 0 0 17% 17% 33% 0% 0% Morphological Group [dagger] Site * CL AR TU FI MG Bullock Island (C) 0 1 1 0 1 0% 3% 3% 0% 3% Whirlpool Cliff (C) 1 4 1 0 1 3% 10% 3% 0% 3% Labhra Cliff (C) 1 5 2 1 1 2% 10% 4% 2% 2% West Cliff (C) 1 5 2 1 1 2% 10% 4% 2% 2% Whirlpool Cliff (B) 1 0 1 0 0 3% 0% 3% 0% 0% West Cliff (B) 1 0 1 0 0 2% 0 2% 0 0 Whirlpool Cliff (P) 1 0 1 0 0 17% 0% 17% 0% 0% Labhra Cliff (P) 1 0 1 0 0 17% 0% 17% 0% 0% * C, cliff; B, rocks; P, panels. [dagger] EN, encrusting; MA, massive; RE, repent; PA, papillate; FL, flabellate; CL, clathrate: AR, arborescent; TU, tubular; FI ficiform; MG, massive globulose. Table 5 Simper analysis (Printer) to determine the five most dissimilar species in terms of percentage abundance for each pair of habitats/sites West Cliff (Cliff) Whirlpool Cliff Site [down arrow] (rocks) [down arrow] Whirlpool Cliff (rocks) Plakortis simplex * Clathrina coriacea * Aplysilla rosacea * H. brondstedi * L complicata * West Cliff (rocks) Plakortis simplex * Haliclona sp. 6 A. rosacea * Hymedesmia pansa Clathrina coriacea * Hymeniacidon perlevis * Haliclona sp. 7 * Scypha ciliatum * H. brondstedi * Leuconia nivea * Whirlpool Cliff (cliff) Esperiopsis fucorum * Plakortis simplex Scypha ciliatum * Clathrina coriacea Suberites carnosus Aplysilla rosacea Eurypon orange H. brondstedi Stelligera rigida L. complicata Bullock Island (cliff) Halichondria panacea * Plakortis simplex Suberites carnosus Clathrina coriacea Stelligera rigida H. brondstedi Raspailia ramosa L. complicata Hemimycale columella * S. plumosum Labhra Cliff (panels) Scypha ciliatum * Plakortis simplex Stelligera rigida Clathrina coriacea Suberites carnosus Aplysilla rosacea Raspailia ramosa H. brondstedi Eurypon orange L. complicata Labhra Cliff (cliff) Suberites carnosus * Plakortis simplex Haliclona sp. 4 * Clathrina coriacea Eurypon orange Aplysilla rosacea Raspailia ramosa * H. brondstedi Paratimea constellata * L. complicata Whirlpool Cliff (panels) Halichondria panacea * Plakortis simplex Scypha ciliatum * Clathrina coriacea Esperiopsis fucorum * Aplysilla rosacea Stelligera rigida H. brondstedi Suberites carnosus L. complicata West Cliff Whirlpool Cliff Site (rocks) [down arrow] (cliff) [down arrow] Whirlpool Cliff (rocks) West Cliff (rocks) Whirlpool Cliff (cliff) Plakortis simplex Aplysilla rosacea Haliclona sp. 7 H. brondstedi Clathrina coriacea Bullock Island (cliff) Plakortis simplex Halichondria panacea * Aplysilla rosacea Suberites carnosus Clathrina coriacea Stelligera rigida Haliclona sp. 7 Raspalia ramosa Hemimycale H. brondstedi columella * Labhra Cliff (panels) Plakortis simplex Esperiopsis fucorum A. rosacea Scypha ciliatum Haliclona sp. 7 Tethya aurantium H. brondstedi Dysidea fragilis Clathrina coriacea Haliclona sp. 4 Labhra Cliff (cliff) Plakortis simplex Esperiopsis fucorum A. rosacea Scypha ciliatum Clathrina coriacea Haliclona sp. 4 Halicloma sp. 7 Eurypon major * H. brondstedi Stelligera rigida * Whirlpool Cliff (panels) Plakortis simplex Halichondria panacea * A. rosacea Scypha ciliatum Clathrina coriacea Esperiopsis fucorum Haliclona sp. 7 Tethya aurantium H. brondstedi Dysidea fragilis Bullock Island (cliff) Labhra Cliff Site [down arrow] (panels) [down arrow] Whirlpool Cliff (rocks) West Cliff (rocks) Whirlpool Cliff (cliff) Bullock Island (cliff) Labhra Cliff (panels) Scypha ciliatum * Halichondria panacea * Dysidea fragilis * Hemimycale columella Cliona celata Labhra Cliff (cliff) Halichondria panacea Scypha ciliatum Stelligera rigida * Dysidea fragilis * Hemimycale columella Stelligera rigida * Haliclona sp. 4 * Haliclona sp. 4 * Cliona celata * Eurypon major * Whirlpool Cliff (panels) Halichondria panacea * Scypha ciliatum Scypha ciliatum Halichondria panacea Dysidea fragilis Esperiopsis fucorum Hemimycale columella Dysidea fragilis Esperiopsis fucorum L. complicata Labhra Cliff (cliff) Site [down arrow] Whirlpool Cliff (rocks) West Cliff (rocks) Whirlpool Cliff (cliff) Bullock Island (cliff) Labhra Cliff (panels) Labhra Cliff (cliff) Whirlpool Cliff (panels) Halichondria panacea * Scypha ciliatum * Dysidea fragilis Stelligera rigida Haliclona sp. 4 An asterisk indicates that the species is characteristic of the site or habitat to its left; an unasterisked species is characteristic of the site or habitat at the top of the column.
The authors thank Claire Shaw for assisting in data collection and manuscript revision, Declan O'Donnell (Irish Wildlife Service) for granting permits for research at Lough Hyne, and Chris Todd for provision of artificial substrata. We also thank Enterprise Ireland for financial assistance. Thanks also to the anonymous referees for significantly improving this manuscript.
Alcolado, P. M. 1990. Genera] features of Cuban sponge communities. Pp. 351 357 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
Alvarez, B., M. C. Diaz, and R. A. Laughlin. 1990. The sponge fauna on a fringing coral reef in Venezuela, I. Composition, distribution, and abundance. Pp. 358-366 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
Ayling, A. L. 1983. Growth and regeneration rates in thinly encrusting demospongiae from temperate waters. Biol. Bull. 165: 343-352.
Barnes, D. K. A., and B. C. Maughan. 2001. Seasonality and inter-annual variability in recruitment patterns of temperate encrusting bryozoans. Pp. 19-27 in Bryozoan Studies 2001, P. Wyse Jackson, C. Buttler and M. Spencer Jones, eds., Balkema, Rotterdam.
Barnes, D. K. A., P. Rothery, and A. Clarke. 1996. Colonisation and development in encrusting communities from the Antarctic intertidal and sublittoral. J. Exp. Mar. Biol. Ecol. 196:248-265.
Barthel, D. 1989. Growth of the sponge Halichondria panicea in the North Sea habitat. Pp. 23-30 in Proceedings of the 21st European Marine Biology Symposium, R. Z. Klekowski, E. Styczynska-Jurewicz, and L. Falkowski, eds. Gdansk, 14-19 September 1986.
Barthel, D., and O. S. Tendal. 1993. The sponge association of the abyssal Norwegian Greenland Sea: species composition, substrate relationships and distributions. Sarsia 78: 83-96.
Bassindale, R., E. Davenport, F. J. Ebling, J. A. Kitching, M. A. Sleigh, and J. F. Sloane. 1957. The ecology of Lough Hyne Rapids with special reference to water currents. VI. Effects of the rapids on the hydrography of the South Basin. Ecology 45: 879-900.
Becerro, M. A., M. J. Riuz, and X. Turon. 1994. Trends in space occupation by the encrusting sponge Crambe crambe: variation in shape as a function of size and environment. Mar. Biol. 121: 301-307.
Bell, J. J. 2001. The ecology of sponges at Lough Hyne Marine Nature Reserve, Co. Cork, Ireland. Ph.D. thesis, University College Cork.
Bell, J. J., and D. K. A Barnes. 2000a. A sponge diversity centre within a marine island. Hydrobiologia 440: 55-64.
Bell, J. J., and D. K. A Barnes. 2000b. The distribution and prevalence of sponges in relation to environmental gradients within a temperate sea lough: vertical cliff surfaces. Divers. Distrib. 6: 283-303.
Bell, J. J, and D. K. A. Barnes. 2000c. The distribution and prevalence of sponges in relation to environmental gradient within a temperate sea lough: inclined cliff surfaces. Divers. Distrib. 6: 305-323.
Bell, J. J., and D. K. A. Barnes. 2000d. The influence of bathymetry and flow regime on the morphology of sublittoral sponge populations at Lough Hyne MNR. J. Mar. Biol. Assoc. UK 80: 707-718.
Bell J. J., and D. K. A Barnes. 2003. The importance of competitor identity, morphology and ranking methodology to outcomes in interference competition: an example of sponges. Mar. Biol. (In Press).
Bell, J. J., D. K. A. Barnes, and J. R. Turner. 2002. The importance of micro and macro morphological variation in adaptation of a sublittoral demosponge to current extremes. Mar. Biol. 140: 75-81.
Boury-Esnault, N., and K. Rutzler, eds. 1997. Thesaurus of Sponge Morphology. Smithson. Contrib. Zool. 596. Smithsonian Institution Press, Washington DC.
Buss, L. W., and J. B. C. Jackson. 1979. Competitive networks: nontransitive competitive relationships in cryptic coral reef environments. Am. Nat. 113: 223-234.
Cheshire, A. C., and C. R. Wilkinson. 1991. Modelling the photosynthetic by sponges on Davies Reef, Great Barrier Reef. Mar. Biol. 109: 13-18.
Dayton, P. K. 1971. Competition, disturbance and community organisation: the provision and subsequent utilization of space in a rocky intertidal community. Ecol. Monogr. 41: 351-389.
Dayton, P. K. 1978. Observations of growth, dispersal and population dynamics of some sponges in McMurdo Sound, Antarctica, Pp. 271-282 in Sponge Biology, C. Levi, and N. Boury-Esnault, eds. Colloques internationaux du C.N.R.S 291.
Diaz, M. C., B. Alvarez, and R. A. Laughlin. 1990. General features of Cuban sponge communities. Pp. 367-375 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press. Washington, DC.
Dunlap, M., and J. R. Pawlik. 1996. Video-monitored predation by Caribbean reef fishes on an array of mangrove and reef sponges. Mar. Biol. 126: 117-123.
Elvin, D. W. 1976. Seasonal growth and reproduction of an intertidal sponge. Haliclona permollis (Bowerbank). Biol. Bull. 151: 108-125.
Hiscock, K. 1983. Water movement. Pp. 58-96 in The Ecology of the Shallow Sublittorol Benthos, R. Earll, and D. G. Erwin, eds. Clarendon Press, Oxford.
Hiscock, K., S. Stone, and D. George. 1983. The marine fauna of Lundy. Porifera (sponges): A preliminary study. Rep. Lundy Field Soc. 34: 16-35.
Hooper, J. N. A., J. A. Kennedy, and R. J. Quinn. 2002. Biodiversity 'hotspots,' patterns of richness and endemism, and taxonomic affinities of tropical Australian sponges (Porifera). Biodivers. Conserv. 11: 851-885.
Jenkins, S. R., T. A. Norton, and S. J. Hawkins. 1999. Settlement and post-settlement interactions between Semibalanus balanoides (L.) (Crustacea: Cirripedia) and three species of fucoid canopy algae. J. Exp. Mar. Biol. Ecol. 236: 49-67.
Kitching, J. A. 1987. Ecological studies at Lough Hyne. Adv. Ecol. Res. 17: 115-186.
Konnecker, G. 1973. Littoral and benthic investigations on the West Coast of Ireland. I. The sponge fauna of Kilkieran Bay and adjacent areas. Section A: Faunistic and Ecological Studies. Proc. R. Ir. Acad. 73B (26): 450-472.
Krebs, C. J. 1989. Ecological Methodology. Harper Collins, London.
Lilly, S. J., J. F. Sloane, R. Bassindale, F. J. Ebling, and J. A. Kitching. 1953. The ecology of the Laugh Hyne rapids with special reference to water currents. IV. The sedentary fauna of sublittoral rocks. J. Anim. Ecol. 22: 87-122.
Maldonado, M., and M. J. Uriz. 1995. Biotic affinities in a transitional zone between the Atlantic and the Mediterranean: a biogeographical approach based on sponges. J. Biogeogr. 22: 89-110.
Manconi, R., and R. Pronzato. 1991. Life cycle of Spongilla lacustris (Porifera. Spongillidae): a cue for environment-dependent phenotype. Hydrobiologia 220: 155-160.
Maughan, B. C. 2000. The ecology of encrusting epifauna in Lough Hyne Marine Nature Reserve. Ph.D. thesis. University College Cork.
Maughan, B. C., and D. K. A. Barnes. 2000a. Epilithic boulder communities of Lough Hyne: the influences of water movement and sediment. J. Mar. Biol. Assoc. UK 80: 767-776.
Maughan, B. C., and D. K. A. Barnes. 2000b. A 'minimum stress inflexion' in relation to environmental and biotic influences on the dynamics of subtidal encrusting communities. Hydrobiologia 440: 101-109.
McCook, L. J., and A. R. O. Chapman. 1997. Patterns and variations in natural succession following massive ice-scour of a rocky intertidal seashore. J. Exp. Mar. Biol. Ecol. 214: 121-147.
Osman, R. W. 1977. The establishment and development of a marine epifaunal community. Ecol. Monogr. 47: 37-63.
Paine, R. T. 1974. Intertidal community structure: experimental studies on the relationship between a dominant competitor and its principal predator. Oecologia 15: 93-120.
Picton, B. E. 1991. The sessile fauna of sublittoral cliffs. Pp. 139-142 in The Ecology of Lough Hyne: Proceedings of a Conference 4-5 Sept. 1990, A. A. Myers, C. Little, M. J. Costello, and J. C. Partridge, eds. Royal Irish Academy, Dublin.
Russ, G. R. 1982, Overgrowth in a marine epifaunal community: competitive hierarchies and competitive networks. Oecologia 53: 12-19.
Rutzler, K., M. C. Diaz, R. W. M. Van Soest, S. Zea, K. P. Smith, B. Alvarez, and J. Wulff. 2000. Diversity of sponge fauna in mangrove ponds, Pelican Cays, Belize. Pp. 232-248 in Natural History of the Pelican Cars, Belize, Atoll Research Bulletin, National Museum of Natural History, Smithsonian Institution Press, Washington DC.
Sara, M. 1970. Competition and cooperation in sponge population. Syrup. Zool. Soc. Loud. 25: 273-284.
Sara, M., M. Pansini, and R. Pronzato. 1978, Zonation of photophilous sponges related to water movement in reef biotopes of Obhor Creek (Red Sea). Pp. 283-295 in Sponge Biology. C. Levi, N. Boury-Esnault, eds. Colloques internationaux du C.N.R.S 291.
Schmahl, G. P. 1990. General features of Cuban sponge communities. Pp. 376-383 in New Perspectives in Sponge Biology, K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
Sousa, W. P. 1979. Disturbance in marine intertidal boulder fields: the non-equilibrium maintenance of species diversity. Ecology 60: 1225-1239.
Stone, A. R. 1970. Growth and reproduction of Hymeniacidon perleve (Montagu) (Porifera) in Langstone Harbour. Hampshire. J. Zool. Lond. 161: 443-459.
Storr, J. F. 1976. Ecological factors controlling sponge distributions in the Gulf of Mexico and the resulting zonation. Pp. 261-276 in Aspects of Sponge Biology. F.W. Harrison, and R.R. Cowden. eds. New York Academic Press, New York.
Turner, S. J., and C. D. Todd. 1994. Competition for space in encrusting bryozoan assemblages: the influence of encounter angle, site and year on outcome variability. J. Mat'. Biol. Assoc. UK 74: 603-622.
van Soest, R. W. M., and S. Weinberg. 1980. A note on the sponges and octocorals from Sherkin Island and Lough the. Co. Cork. Ir. Nat. J. 20: 1-15.
van Soest, R. W. M., J. D. Guiterman, and M. S. Sayer. 1981. Sponges from Roaring water Bay and Lough Hyne. J. Sherkin Island 12: 35-49.
Wilkinson, C. R., and A. C. Cheshire. 1989. Patterns in the distribution of sponge populations across the central Great Barrier Reef. Coral Reefs 8: 127-143.
Witman, J. D., and K. P. Sebens. 1990. Distribution and ecology of sponges at a subtidal rock ledge in the central Gulf of Maine. Pp. 391-396 in New Perspectives in Sponge Biology. K. Rutzler, ed. Smithsonian Institution Press, Washington, DC.
Wulff, J. L. 1995. Sponge-feeding by the Caribbean starfish Oreaster reticulatus. Mar. Biol. 123: 313-325.
Wulff, J. 2000. Sponge predators may determine differences in sponge fauna between two sets of mangrove cays, Belize barrier reef. Pp. 249-263 in Natural History of the Pelican Cays, Belize, Atoll Research Bulletin. National Museum of Natural History. Smithsonian Institution Press, Washington DC.
Received 27 August 2001; accepted 23 May 2003.
J. J. BELL (1), * AND D. K. A. BARNES (2)
(1) Department of Zoology and Animal Ecology, University College Cork, Lee Maltings, Co. Cork, Ireland; and (2) British Antarctic Survey, N.E.R.C., High Cross, Madingley Road, Cambridge CB3 0ET, United Kingdom
* To whom correspondence should be addressed. Current address: Institute of Biological Sciences, Edward Llwyd Building, The University of Wales, Aberystwyth, Ceredigion SY23 3DA.
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|Author:||Bell, J.J.; Barnes, D.K.A.|
|Publication:||The Biological Bulletin|
|Date:||Oct 1, 2003|
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