Marine Biology (2005) 147: 653–661 DOI 10.1007/s00227-005-1587-8
R ES E AR C H A RT I C L E
J. J. Bell
Influence of occupant microhabitat on the composition of encrusting communities on gastropod shells
Received: 1 July 2004 / Accepted: 11 November 2004 / Published online: 28 April 2005 Springer-Verlag 2005
Abstract The exploitation of microhabitats is widely considered to increase biodiversity in marine ecosystems. Although intertidal hermit crabs and gastropods may inhabit the same shell type and shore level, their microhabitat may differ depending on the state of the tide. On the south coast of Wales the hermit crab Pagurus bernhardus mainly inhabits the shells of Nucella lapillus (84%). Hermit crab shells had a significantly different encrusting community compared with live N. lapillus shells. At low tide the live gastropods were found on exposed rock surfaces whereas hermit crabs were restricted to tidal pools. Communities encrusting live gastropod shells were characterised by lower species richness and abundance compared with shells inhabited by hermit crabs (12 species found in total). A greater abundance and richness of epibionts was recorded from both shell types during the summer compared with winter. Differences in community composition between shell occupant types were attributed to microhabitats used by gastropods and hermit crabs and the associated desiccation pressures, rather than competitive interactions or shell characteristics. This contradicts earlier studies of subtidal shells where biological processes were considered more important than physical factors in controlling species abundance and richness patterns. The use of rockpool microhabitats by hermit crabs increases the biodiversity of rocky shores, as some species commonly found on hermit-crab-inhabited shells were rare in other local habitats.
Communicated by J.P. Thorpe, Port Erin J. J. Bell School of Animal and Microbial Sciences, University of Reading, Whiteknights, PO Box 228, Reading, Berkshire, RG6 6AJ, UK E-mail:
[email protected] Present address: J. J. Bell Institute of Biological Sciences, University of Wales, Aberystwyth, Edward Llwyd Building, Aberystwyth, Ceredigion, SY233DA, UK
Introduction For many years hermit crabs have been used to investigate inter- and intra-specific competition, resource selection, and habitat partitioning because the gastropod shells used for protection are often in limited supply (Markham 1968; Childress 1972; Fotheringham 1976; Kellogg 1977; Bertness 1980, 1981; Busato et al. 1998; Barnes and De Grave 2000; Barnes 1999, 2001; Absher et al. 2001). In addition to providing shelter for hermit crabs, gastropod shells may also be used by other freeliving or encrusting organisms including algae, anemones, bryozoans, molluscs, hydroids, barnacles, polychaetes, and sponges (e.g. Jensen and Bender 1973; Karlson and Shenk 1983; McDermott 2001). The nature of these associations has received considerable attention with a number of costs and benefits to hermit crabs and epibionts described (e.g. Partridge 1980; Brooks and Gwaltney 1993). Different suites of species have been reported for the same type of unoccupied, live gastropod- and hermitcrab-inhabited shells in local subtidal habitats. These differences have been attributed to competition, negative associations, and hermit crab interactions (Karlson and Shenk 1983; Van Winkle et al. 2000). Yet, intertidal gastropod shells may be influenced by different environmental pressures from those in subtidal environments irrespective of whether they contain the live gastropod, are unoccupied, or are inhabited by a hermit crab. Tidal emersion is probably a primary factor controlling epibionts on shells as they will be periodically exposed at low tide and may experience desiccation. This may be prevented if the shell inhabitant can show tidal migration or movement to suitable microhabitats on the ebbing tide (e.g. rockpools). Habitat differences between live gastropods and hermit crabs may play an important role in controlling shell epibiont communities. Microhabitat exploitation is increasingly recognised as contributing significantly to biodiversity (Voight and
654
Walker 1995). Pagurus bernhardus (L.) is commonly found in intertidal rockpools at low tide and in a range of subtidal habitats (Jensen and Bender 1973). The migration of hermit crabs to rockpools as the tide retreats may reduce or mitigate the effects of desiccation for shell epibionts. Large adult P. bernhardus are often found inhabiting the shells of the Buccinium undatum (L.), whereas smaller individuals inhabit a number of shell types usually reflecting those available locally. Intertidal P. bernhardus are usually found inhabiting the shells of Nucella lapillus on the south coast of Wales in close proximity to the live gastropods (scale of centimetres). N. lapillus is common on open, exposed rock surfaces and although hermit crabs are found on there when covered by the tide, they shelter in rockpools as the tide retreats. Descriptions of the fauna associated with sublittoral populations of P. bernhardus have been described from a number of locations over the species range (Balss 1924; Chevreux 1908; Samuelsen 1970; Jensen and Bender 1973) but comparisons with live gastropod shells or intertidal populations have not been made. Shells of gastropods, irrespective of occupant, represent an additional settlement surface in intertidal habitats where space is limited. Shell age may influence surface characteristics, as older shells are likely to be smoother than younger shells because of greater scouring over time and wave. Shell age may also be important in determining community composition due to succession (Dayton 1971). Live gastropod shells (for any given size class) will inevitably be younger than hermit-crabinhabited shells, although the actual age of hermit-crabinhabited shells is virtually impossible to estimate. This study will consider the following questions: (1) do communities inhabiting gastropod- and hermit-crabinhabited shells differ due to occupant microhabitat differences, competitive interactions, or shell quality? (2) Is there temporal (seasonal) and spatial (site) variability in encrusting communities inhabiting shells occupied by live gastropods and hermit crabs?
Materials and methods Encrusting communities on Nucella lapillus shells inhabited by the hermit crab Pagurus bernhardus and the live gastropod were investigated at three sites on the south coast of Wales (Southerndown: 5126¢743N, 00336¢227W; Ogmore-by-Sea: 5127¢400N, 003W; and Porthcawl: 5128¢661N, 00342¢672W). Habitats at the three sites were characterised by large areas of flat bedrock separated by coarse sand. Much of the rocky substrate (>85%) is colonised by dense, well-developed Sabellaria reefs. Bedrock and tubeworm reefs create a rocky shoreline marked with many shallow rockpools (sizes up to 30 m across). Hermit crabs (mainly P. bernhardus) are very abundant on the lower shore within these rockpools. Over a 12-h tidal cycle the area of the intertidal zone where shells were collected is uncovered for approximately 2 h during spring tides.
Fifty N. lapillus shells (with lengths of 25–35 mm) inhabited by hermit crabs and gastropods (since these were the most dominant shells) were randomly collected from the lower shore at each site during summer (August) and winter (January). A total of 600 shells were collected. Only this size class of shell was used to reduce the problem of area effects that may influence community structure and faunal abundance. The encrusting epibiont communities inhabiting the external surface of these hermit crab and live gastropod shells were recorded as numbers present and area occupied by each species. Area occupied was calculated using the method described by Conover (1979). Transects were used on the lower shore to determine the microhabitats of live gastropods and hermit crabs. Three 100-m transects were placed parallel to the shore at each of the sites. Random 1-m2 quadrats were placed (the distance along the quadrat was determined using random number tables) along the transect and the number of hermit crabs and live N. lapillus in rockpools and on open rocks was recorded. Contact matrices were constructed for all interactions between shell epibionts, with each cell in the matrix consisting of pair-wise species summed interactions (as for Turner and Todd 1994; Barnes et al. 1996). Overall community transitivity was measured by subjecting the data to the most recently accepted and widely used indices of transitivity, suggested by Tanaka and Nandakumar (1994). Results from these indices generate an output from 0 to 1, irrespective of sample size or competitor number, and are comparable across studies. Therefore the extent to which the encrusting community is hierarchical (transitive) can be estimated. Although Tanaka and Nandakumar (1994) calculated three indices, the win index (WI) and standoff index (SI) were calculated in the present study to determine the degree of community intransitivity: vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi vffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi uP uP n n un P un P Pij½W 2 Pij½S2 u u ui¼1 j¼1 ui¼1 j¼1 WI ¼ t SI ¼ t nðn1Þ nðn1Þ 2
2
Pij [W] and Pij [S] represent the probability of species i winning an encounter with species j for the win index and standoff indices, respectively. The number of species in the community is denoted by n. This index assumes all (or nearly all) competitors meet, therefore species involved in few interactions were not included in the calculation of the index. A series of settlement arrays were used to investigate the influence of immersion on the recruitment of invertebrates to shells (at Porthcawl only). Arrays consisted of two rows of 10 gastropods shells, all approximately the same size (30–35 mm), attached to wooden boards by cementing bolts to the apertures of the shells and attaching these bolts to the boards. Six arrays were constructed with a total of 20 gastropods on each. Ten of these shells were previously inhabited by gastropods
655
and the other 10 were inhabited by hermit crabs prior to the experiment. All shells were collected during the winter (because the epibiont cover was lower than in the summer) and boiled to remove the epibionts and live gastropods. Three of the arrays were placed in rockpools (experimental areas) on the lower shore that were permanently filled with water (the pools were approximately 50 m apart). The arrays were secured using large boulders from the site. Next to each rockpool a second array was placed on the open rock surface (orientated in the same direction) in a tidally submerged environment (non-rockpool). Therefore each of the three experimental areas contained two arrays: one in a rockpool, the other on an open rock surface within 2 m. The arrays were deployed in March 2003 and recovered in October 2003. The number of recruits found on each shell was recorded after this time. A balanced, orthogonal (fully crossed) three-way analysis of variance (ANOVA) was used to compare species richness and abundance between sites, shell occupant, and season. There are three fully orthogonal factors giving a 3·2·2 factorial design. As a factor in the analysis, site indicated the location where sampling took place and was considered as a fixed factor (three levels). Shell occupant (fixed factor) indicated whether shells were inhabited by a hermit crab or live gastropod (two levels). Season (fixed factor) referred to whether sampling took place in the winter or summer (two levels). The same analysis of variance was used to compare the number of recruits found on different prior shell occupant types (fixed factor—two levels), microhabitats (either rockpool or open rock: fixed factor—two levels), and in different experimental areas (fixed factor—three levels). Three-way G-tests were used to compare the number of shells encrusted by the different species (Absence vs Presence·Season·Shell occupant). A goodness-of-fit test was used to compare the number of shells encrusted by different species for species not found on both types of shell (Absence vs Presence·Season). Overall community data (for each shell inhabitant, site, and season) were subjected to Bray–Curtis similarity analysis using hierarchical agglomerative group average clustering. This was performed using the unweighted pair group method using arithmetic averages (UPGMA) with the PRIMER program (Plymouth Marine Laboratory). 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 the dissimilarity matrix created from the Bray–Curtis similarity analysis. The above analysis was completed separately for species numbers and percentage cover data. The RELATE function in PRIMER was then used to compare the Bray–Curtis similarity/dissimilarity matrices produced for species number and percentage cover data. SIMPER analysis (in PRIMER) was used to determine the contribution of each species to the average Bray–Curtis dissimilarity between microhabitats, sites,
and shell occupant. This analysis determines which species are responsible for any differences that might occur. Data were transformed as for the Bray–Curtis analysis.
Results Observations were made of the intertidal microhabitat of 496 and 234 live gastropods and hermit crabs, respectively, along transects at low water. Eighty-four percent (n=417) of the live gastropods observed were found on open rock surfaces out of rockpools, compared with only 2% (n=5) of hermit crabs, which were mainly found in rockpools. Species found encrusting the shells inhabited by gastropods and hermit crabs included Elminius modestus Darwin (Crustacea), Conopeum reticulum (Bryozoa) (L.), Spirorbis spirorbis (L.) (Annelida), Pomatoceros triqueter (L.) (Annelida), Sabellaria alveolata (L.) (Annelida), Crepidula fornicata (L.) (Mollusca), Flustra foliacea (Bryozoa) (L.), Alcyonidium gelatinosum (Bryozoa), Lithothamnia (Algae), Electra pilosa (L.) (Bryozoa), Mytilus edulis L.(Mollusca), and an unidentified encrusting green algae. Only Elminius modestus, Conopeum reticulum, Spirorbis spirorbis, and Pomatoceros triqueter were found on the shells inhabited by live gastropods, whereas all the species found were also reported on hermit crab shells. Significant differences were found between the number of shells encrusted by the different species (Table 1). This was attributable to the different shell occupants and seasons. The number of shells inhabited by E. modestus varied significantly (G=36.41, df=1, P33.24, df=1, P0.01, df=1, P>0.50) was seen in the number of shells occupied by S. spirorbis for different shell occupants or seasons (10% of shells). P. triqueter occupied a significantly lower (G=14.17, df=1, P3.84, df=1, P
