RAFFLES BULLETIN OF ZOOLOGY 2015 Conservation & Ecology RAFFLES BULLETIN OF ZOOLOGY 63: 401–417 Date of publication: 2 October 2015 http://zoobank.org/urn:lsid:zoobank.org:pub:9648B3CD-ADE3-4F0B-8190-4F3A1CFB822A Tropical polychaete community and reef dynamics: insights from a Malayan Sabellaria (Annelida: Sabellariidae) reef Gianluca Polgar*1, Eijiroh Nishi2, Izwandy Idris3, 4 and Christopher J. Glasby5 Abstract. The ecology of tropical sabellariid reefs is scarcely known, and only few records of such systems were reported from Southeast Asia. The present investigation describes the only documented polychaete reef of western Peninsular Malaysia, which has been previously reported on in two other studies. More recent surveys documented dramatic temporal changes of the reef’s extension and polychaete community composition. This reef appears to experience different phases of growth and destruction, associated with sediment dynamics, possibly determined by monsoons. In the present study, the extent, temporal dynamics and polychaete species composition of the reef are documented from December 2010 to April 2013. Semi-quantitative sampling of the polychaete community in selected portions of the reef along the intertidal zone revealed drastic changes in the composition and geomorphic structure of the reef. The reef reached its largest extension in December 2010, when Sabellaria sp. 1 was the primary builder. The tubiculous Polydora cavitensis and Loimia verrucosa dominated the reef at different stages of reef development. A total of 26 polychaete species from 12 families were recorded, including errant and associated species. Eight un-described species were found, plus five new records for an area including the South China Sea, the Malacca Straits and the Andaman Sea, and five new records for the Malay Peninsula only. Hypotheses of the reef cycle, the synecological dynamics, and the abiotic factors triggering the ecological succession are also discussed. Keywords. Sabellariidae, Polychaeta, biogenic reef, ecological succession, intertidal ecology, tidal flat INTRODUCTION considered ecosystem engineers. Polychaete reefs also host more diversified communities than adjacent sand-flats, and Polychaete reefs are biogenic structures globally distributed associated species include fishes and shrimps of commercial in intertidal and subtidal marine benthic ecosystems (Kirtley, importance (Vorberg, 2000). 1994). The reef framework is typically built by a single tube-building species, the primary frame-builder, forming All polychaete primary frame-builders belong to the families aggregations with areal extensions from a few square metres Sabellariidae and Serpulidae (Canalipalpata: Sabellida), up to several hectares (Dubois et al., 2002). This framework which build their tubes by cementing sand grains and shell is also encrusted and strengthened by several secondary fragments, or by secreting calcium carbonate, respectively frame-builder polychaete species (Scoffin & Garrett, (Bosence, 1979; Naylor & Viles, 2000). Recently, the 1974). A polychaete reef affects bottom hydrodynamics, terebellid Lanice conchilega (Pallas, 1766) has also been alters sedimentation processes, and has a stabilising effect discussed as a potential reef-building species, although its on sediments (e.g., Van Hoey et al., 2008). Such three- aggregations cannot fit the current definition of reef (Van dimensional structure offers a variety of habitats and trophic Hoey et al., 2008; Callaway et al., 2010). niches to diverse animal associations, including crustaceans, molluscs, echinoderms and other polychaetes (Cusson & Sabellariids are filter-feeders usually occurring in the Bourget, 1997). For these reasons, primary frame-builders are intertidal or shallow subtidal zone, although some species have been found at greater depths, in the mesopelagic (e.g., the genus Bathysabellaria Lechapt & Gruet, 1993; see Lechapt & Kirtley, 1996), bathyal and abyssal zones 1Environmental and Life Sciences Programme, Faculty of Science, Universiti Brunei [e.g., Phalacrostemma elegans, sensu Kirtley, 1994 = Darussalam, Jalan Tungku Link, BE 1410, Gadong, Negara Brunei Darussalam; Email: Gesaia elegans (Fauvel, 1911)]. Several studies indicated [email protected] (*corresponding author) that sabellariids have diverse life histories and ecological 2College of Education and Human Sciences, Yokohama National University, niches, and often are stenotopic, stenobathic and endemic Tokiawadai, Hodogaya, Yokohama 240-8501, Japan (Pohler, 2004). However, although this family includes > 130 3Laboratory of Aquatic Biology and Ecology, Department of Aquaculture, Faculty of Agriculture, Universiti Putra Malaysia, 43400 Serdang, Malaysia valid species (Barrios et al., 2009), ecological studies have 4Marine Biology Programme, School of Marine and Environmental Sciences, Universiti been conducted on few representatives, such as Sabellaria Malaysia Terengganu, 21030 Kuala Nerus, Terengganu, Malaysia alveolata (Linnaeus, 1767), S. spinulosa (Leuckart, 1849), 5Museum and Art Gallery Northern Territory, GPO Box 4646, Darwin NT, Australia Phragmatopoma californica (Fewkes, 1889), and Idanthyrsus cretus Chamberlin, 1919 (e.g., Pawlik et al., 1991; Holt et al., © National University of Singapore ISSN 2345-7600 (electronic) | ISSN 0217-2445 (print) 1998; Barrios et al., 2009). In the western Pacific and Indian 401 Polgar et al.: Polychaetes from a Sabellaria reef oceans, some Sabellaria, Neosabellaria and Idanthyrsus clumps. Hypotheses on the reef’s sedimentological and species have been known to form miniature reefs or intertidal ecological processes are also discussed. to subtidal belts (Badve, 1996; Pandolfi et al., 1998; Nishi & Kirtley, 1999; Bailey-Brock et al., 2007; Huang et al., 2008; MATERIAL AND METHODS Chen & Dai, 2009; Reuter et al., 2009; Nishi et al., 2010). In particular, ecological knowledge of tropical sabellariid Field and laboratory work. The Jeram beach [= Pantai polychaete reefs is considerably fragmentary (e.g., Pohler, Jeram], Selangor; 3°13’27”N, 101°18’13”E) is a tidal flat 2004; McCarthy et al., 2008). on the west coast of the Malay Peninsula (Fig. 1), 3.8 km north of the mouth of Sungai [= river] Sembilang and 3.3 Dramatic changes in the areal extension of sabellariid reefs km south of the mouth of Sungai Buluh. During spring have been reported in several studies conducted in temperate low tides, the exposed tidal flat extends from sea to land regions (e.g., Holt et al., 1998; Frost et al., 2004; Vorberg, for approximately 800 m (Fig. 1). The tidal flat is fringed 2005). Gruet (1986) subdivided the typical ecological by a mangrove stand of stunted Avicennia alba Blume and succession of a reef of Sabellaria alveolata into four different scattered trees of Sonneratia sp., and it is crossed by Sungai phases: absence or pre-settlement, settlement or growth, Jeram [= Jeram creek]. stagnation, and destruction. Each phase is characterised by specific geomorphic structures and ecological dynamics. Five surveys were made on 7 December 2010, 19 January Described factors driving such changes include temperature 2011, 7 August 2012, 30 November 2012 and 26 April 2013. fluctuations, changes of sedimentological regimes, and Six sites were georeferenced during spring low tides when anthropogenic impacts, such as bottom trawling and the Sabellaria reef was in place (December 2010); along alterations of the hydrological regime (Hendrick & Foster- the exposed intertidal zone, and along the northern margin Smith, 2006). of a large barrier south of Jeram creek (Fig. 1). Two sites (A, B) were positioned in the first and the last patch of the Seilacher (1984) described a periodic fluctuation of a inner reef, one site (C) in the back reef, one (D) on the reef sabellariid intertidal reef on the Jeram shore, along the flat, one (E) along the northern exposed margin of the reef, west coast of the Malay Peninsula. A preliminary study of and one (F) along its western exposed margin. this reef provided a qualitative description of the associated macrofauna (Ribero & Polgar, 2012). Seilacher (1984) One qualitative sample of substrate or reef tubes (~ 1 L) observed rapid and sharp changes in the grain size of was collected at each site during each survey. Large errant superficial sediments throughout the intertidal zone, occurring species were collected by digging and sorting ~ 75 L of over a four-year period (1979–1983). In particular, the tidal substrate inside a quadrat (50×50 cm) dug to a depth of flat was either covered by a layer of mud overlapping a shell 30 cm (n = 1 per site). Measurements of the clumps’ height bed, or by a shelly substrate, on top of which he recorded the relative to ground level were also conducted in August and presence of rapidly growing “Sabellaria reeflets” (Seilacher, November 2012. 1984). According to his ‘Jeram model’, the Jeram shore is normally under positive sedimentary regime, dominated by mud sediments. The mudflat is colonised by infaunal communities, and the sessile epibenthos (e.g., barnacles) is restricted to other organisms or their remains (brachyuran crabs, gastropods and bivalves). Interviews with local fishermen suggested that in the 1920s, a catastrophic storm event established an extensive intertidal lag deposit of infaunal shell material (Seilacher, 1984). After the storm, a different and dominant epibenthos (sabellariid polychaetes, bryozoans, oysters, solitary corals, large barnacles) developed on top of the shell bed. As the mud gradually buried the shell bed and its encrusting community, the former dominant infaunal community was re-established. Since then, the mud layer has been repeatedly winnowed by storm events, and its infaunal shell content projected onto the previous shell lags, including the reference level of the 1920s. This model predicts that both epifaunal and infaunal communities are repeatedly mixed up in an increasingly thick shell lag by frequent and intense storm events, with no alternating layers Fig. 1. Jeram Beach and sampling sites. Diagram of the polychaete of mud and shell beds. reef as in December 2010. Sites: A, B (inner reef patches); C (back reef); D (reef flat); E (northern exposed margin); and F (western In this study, the species composition of the Jeram polychaete exposed margin). Hatched line = water’s edge during spring low community is presented, and observations of its spatial extent tide; crosses = trees of Avicennia alba and Sonneratia sp.; stippled area = sand berm; shaded areas with black contours = polychaete and temporal dynamics are provided, including measurements reefs. Map redrawn from a satellite image (Google Earth Plus, v. of the height, tube density, and tube diameter of the sabellariid 7.0, 2012). Inset: black arrow = Jeram. 402 RAFFLES BULLETIN OF ZOOLOGY 2015 Table 1. Polychaete species and morphospecies collected in the Jeram Reef. First records: SA = new record for the South China Sea, Malacca Straits (including the Malay Peninsula) and Andaman Sea (Hylleberg et al., 1986; Tan & Chou, 1993; Paxton & Chou, 2000; Aungtonya et al., 2002; Chan, 2009; Rajasekaran & Fernando, 2012; Idris & Arshad, 2013); MP = new record only for the Malay Peninsula (Tan & Chou, 1993; Chan, 2009; Idris & Arshad, 2013). Family, species First records Chrysopetalidae Paleaequor breve (Gallardo, 1968) MP Eunicidae Lysidice sp. 1 Lysidice sp. 2 Marphysa sp. 1 Glyceridae Glycera nicobarica Grube, 1868 MP Lumbrineridae Lumbrineris sp. 1 Nereididae Ceratonereis (Composetia) burmensis (Monro, 1937) Laevispinereis sp. 1 Leonnates crinitus Hutchings & Reid, 1991 SA Neanthes willeyi (Day, 1934) MP Nectoneanthes oxypoda (Marenzeller, 1879) Nicon sp. 1 Perinereis maindroni Fauvel, 1943 SA Perinereis singaporiensis (Grube, 1878) Onuphidae Diopatra claparedii Grube, 1878 Pilargidae Cabira sp. 1 Sigambra sp. 1 MP Polynoidae Lepidonotus sp. 1 Lepidonotus sp. 2 Lepidonotus sp. 3 Lepidonotus cf. sublevis Verrill, 1873 SA Parahalosydnopsis tubicola (Day, 1973) SA Phyllodocidae Eulalia sp. 1 Sabellariidae Sabellaria sp. 1 Spionidae Polydora cavitensis Pillai, 1965 MP Terebellidae Loimia verrucosa Caullery, 1944 SA 403 Polgar et al.: Polychaetes from a Sabellaria reef Samples were haphazardly selected within each site, When the reef was dominated by aggregations of sabellariids transported to the lab, sorted, and specimens were euthanised (December 2010), the density (tubes m-2) and the diameter by chilling at 2–4°C or freezing at -25°C, then fixed in 10% (mm) of tube openings were also measured. Tube density was formalin or 70% ethanol, and preserved in 70% ethanol. In measured counting all the tubes contained in digital photos the absence of phylogenies for most of the taxa considered containing 2–4 quadrats of 5×5 cm each (n = 30 quadrats, in this study, the definition of species adopted here is the i.e. 1–2 photos per site, or 4-8 quadrats per site; Photoshop morphospecies concept as defined by Cronquist (1978), CS2 v. 9.0 ©Adobe). Tube diameters were measured in each i.e., species are the smallest groups that are consistently collected sample (1 L), on haphazardly selected clusters of and persistently distinct, and distinguishable by ordinary 30 adjacent tubes (n = 180 tubes, i.e. one cluster of 30 tubes means. Where these taxonomic groups matched existing per site). Measurements were taken with a digital calliper described species we have applied the appropriate Linnean to the nearest 0.1 mm. binomial, otherwise we have used morphospecies units (sp. 1, sp. 2, etc.). Our proposed species are therefore hypotheses Statistical analyses. To explore the degree of association which are falsifiable when independent data, for example between polychaete species and morphospecies relative to morphological synapomorphies and DNA sequences, become space (sampling sites) and time (surveys), we performed available. Genus group determinations were made using hierarchical cluster analyses, utilising the Jaccard similarity Wilson et al. (2003) and species identifications were made index and the strong linkage aggregation method (Johnson using regional checklists and revisionary studies, including & Wichern, 1992). Groups of taxa were considered, which Hylleberg et al. (1986), Tan & Chou (1993), Paxton & Chou corresponded to an arbitrary similarity cut-off value of (2000), Aungtonya et al. (2002), Chan (2009), Rajasekaran 0.65. Distances from missing values were calculated by & Fernando (2012) and Idris & Arshad (2013). pairwise deletion (Hammer & Harper, 2005). All analyses Fig. 2. Some of the species found in this study. a = Lumbrineris sp. 1 (scale bar = 1 mm); b = Perinereis maindroni (scale bar = 1 mm); c = Parahalosydnopsis tubicola (scale bar = 5 mm); d = Eulalia sp. 1 (scale bar = 3 mm); e = Polydora cavitensis (scale bar = 1 mm); f = Loimia verrucosa (scale bar = 5 mm). 404 RAFFLES BULLETIN OF ZOOLOGY 2015 Fig. 3. Diagram illustrating the observed conditions of the polychaete communities. December 2010/January 2011: a = reef barriers; b = detail of a clump of Sabellaria sp. 1 (scale bar = 5 cm). August 2012: c = exposed shell bed, with erosive ridges perpendicular to the shore line with small (longest dimension: 5–20 cm) and scattered clumps of Sabellaria sp. 1; d = detail of a polychaete clump, on top of the shell lag (scale object’s diameter = 5 cm). November 2012: e = polychaete reef, with larger and more tightly packed clumps than in c; f = detail of a clump mainly formed by tubes of spionids (scale bar = 3 cm). April 2013: g = the shore covered by a mud layer; h = detail of a patch of coarse sediments, heavily colonised by terebellid worms (scale bar = 10 cm); hatched lines: water’s edge during spring low tide 405 Polgar et al.: Polychaetes from a Sabellaria reef ) 2 -m s e b u t . n ( y t i s n e d e b u T Fig. 4. Bar charts of Sabellaria sp. 1 tubes’ density (a) and tubes’ diameter (b) measured in December 2010. Bars indicate mean values, and whiskers indicate one-sigma intervals based on standard deviations. were conducted using PAST v.2.09 (Hammer et al., 2001; (Table 2). Lysidice sp. 1, Lysidice sp. 2, Neanthes willeyi Hammer & Harper, 2005). and Lepidonotus cf. sublevis were collected in the inner and back reef (sites A, B, and C, respectively; Table 2). RESULTS In January 2011, the shore was covered by mud and the Community composition. Overall, 26 species and condition of the sabellariid reef was essentially the same morphospecies from 12 families were found (Fig. 2, Table of December 2010. No samples were collected during this 1, Online Resource 1). Five species are new records for a survey. geographic area including the South China Sea, the Malacca Straits and the Andaman Sea (Hylleberg et al., 1986; Paxton & In August 2012, only scattered, visibly eroded clumps of Chou, 2000; Aungtonya et al., 2002; Chan, 2009; Rajasekaran Sabellaria sp. 1 were observed, whose mean height per & Fernando, 2012; Idris & Arshad, 2013); four species plus site increased in a seaward direction (overall mean = 10.0 the morphospecies Sigambra sp. 1 are new records for the cm ± 5.0 cm, n = 13; Online Resource 4a; Fig. 3c, d). A Malay Peninsula only (Tan & Chou, 1993; Chan, 2009; shell lag was exposed in sites A, B and C (Figs. 1; 3c), Idris & Arshad, 2013). and the superficial substrate was richer in mud towards the sea. The shell lag was crossed by numerous parallel ridges, Field surveys and measurements. In December 2010, perpendicular to the shore and partially filled with mud (Fig. the reef was made of several elongated barriers or patches 3c). Along the western exposed margin, the clumps were along coast (Fig. 3a), formed by clustered and fused clumps more eroded. Excavations showed that these clumps grew of polychaete tubes (Fig. 3b). The barriers were several on top of the shell bed, at a depth of 10–15 cm. No buried hundred metres long and 50–200 m wide. The primary polychaete clumps were found below the mud. Only six builder species was Sabellaria sp. 1, occurring at all sites in species were collected during this survey (Table 2). The this survey (Table 2). During spring low tide, the surveyed only tubiculous polychaetes in the scattered and eroded reef barrier spanned through the lower and middle intertidal reef clumps were Sabellaria sp. 1 and Loimia verrucosa. zones, from a point at ~200 m from the supratidal sand This survey was characterised by the presence of the errant berm, down to the sea water’s edge (Fig. 1). Clusters of polychaetes Nectoneanthes oxypoda and Lepidonotus sp. 1, smaller clumps and ball-shaped structures of 50–100 cm found in the lower intertidal zone (sites E, F; Fig. 1; Table in diameter hemmed the reef’s margins (sites A, B, F; Fig. 2). Marphysa sp. 1 and the tubiculous Diopatra claparedii 1). The superficial substrate was muddy, and excavations were also collected in this survey. indicated that the clumps grew on top of a shell lag. The clumps’ height was 20–50 cm above ground level (Ribero & In November 2012, the polychaete clumps were both larger Polgar, 2012). The mean (± standard deviation) tube density and more tightly packed than three months earlier (Figs. of the primary builders per site was 89,467 ± 27,485 tubes 3e, f). The shell bed was found below 15–20 cm of mud m-2, n = 30 (26,000–131,600 tubes m-2; Online Resource throughout the intertidal zone, except at sites A and B, where 2). The average tube diameter was 2.3 ± 0.8 mm, n = 180 it was exposed. The mean height per site of the polychaete (0.5–4.5 mm; Online Resource 3). clumps was 11–19 cm (overall mean 14.5 cm ± 5.1 cm, n = 58; Online Resource 4b), and were mainly composed of tubes Ten polychaete taxa were collected during this survey. In of Polydora cavitensis (Fig. 3f), with few scattered tubes particular, the secondary tube builder Polydora cavitensis and of Sabellaria sp. 1. The polychaete assemblage included 17 the errant species Perinereis maindroni occurred at all sites species. The high species richness observed in this survey 406 RAFFLES BULLETIN OF ZOOLOGY 2015 e survey of August 2012. Shaded a sp. 1; Glyceridae: nic = Glycera mai = Perinereis maindroni, nicon = Eulalia sp. 1; Pilargidae: cab = ub = Parahalosydnopsis tubicola; 7 Aug 2012 (Destruction) BCDEF ?????×??×××××??×???????×???×?????× ? 11125 Table 2. Spatial and temporal species distributions. Upper case letters indicate sites (Fig. 1). ? = Absence/presence data for sites A and C are not available for thareas = dominant builders. Species abbreviations: Chrysopetalidae: bre = Paleaequor breve; Eunicidae: lys1 = Lysidice sp. 1, lys 2 = Lysidice sp. 2, mar = Marphysnicobarica; Lumbrineridae: lum = Lumbrineris sp. 1; Nereididae: bur = Ceratonereis (Composetia) burmensis, cri = Leonnates crinitus, lae = Laevispinereis sp. 1, = Nicon sp. 1, oxy = Nectoneanthes oxypoda, sin = Perinereis singaporiensis, wil = Neanthes willeyi; Onuphidae: cla = Diopatra claparedii; Phyllodocidae: eul Cabira sp. 1; sig = Sigambra sp. 1; Polynoidae: lep1 = Lepidonotus sp. 1, lep2 = Lepidonotus sp. 2, lep3 = Lepidonotus sp. 3, sub = Lepidonotus cf. sublevis, tSabellariidae: sab = Sabellaria sp. 1; Spionidae: cav = Polydora cavitensis; Terebellidae: ver = Loimia verrucosa (see also Tab. 1). Species26 Apr 2013 (Absence)30 Nov 2012 (Growth)7 Dec 2010 (Stagnation) ABCDEFABCDEFABCDEFA bre×?bur×?cab××?cav×××××××××××××?cla?cri××?eul×?sab×××××××××××××lae×?lep1?lep2×?lep3××××××?lum××?lys1×?lys2×?mai××××××××××?mar×××××?nic××?nicon×?oxy?sig×?sin×?sub×?tub××××?ver××××××? wil××? Totals:0000013123105264463631 407 Polgar et al.: Polychaetes from a Sabellaria reef (Fig. 5a) was mainly due to seven nereidid species (Table Four groups of species (S1–S4) are associated with different 2). Except Perinereis maindroni, which was also found at sites (Figs. 1, 6b). Group S2 includes species that were found site F, all these nereidids were found in the inner reef (site in the back reef and the seaward exposed margin (sites C and A), where the shell lag was exposed, and in the back reef F, respectively), plus at least two different sites. In particular, (site C; Fig. 5b; Table 2). the tube builders Sabellaria sp. 1 and P. cavitensis, and the errant Perinereis maindroni were found at all sites. The In April 2013, the reef completely disappeared, and the tubiculous L. verrucosa was found at all sites, except the whole tidal flat was covered by a superficial layer of mud seaward portion of the inner reef (site B; Table 2). Groups (Fig. 3g). Excavations demonstrated the presence of a shell S3 and S4 include species that were all collected in one lag at a depth of 15–30 cm. No buried clumps of polychaete site. In particular, S4 includes four nereidids, Eulalia sp. 1 tubes were found. An isolated ~100 m wide patch of sand and Lysidice sp. 2, which were only found in the landward and shell debris was observed at site F, heavily colonised portion of the inner reef (site A). In group S1, all the species by Loimia verrucosa (Fig. 3h). Thirteen polychaete species were found in the seaward exposed margin (site F). Glycera were found here (Table 2). A few, small sabellariid clumps nicobarica was also found at site A, and Lumbrineris sp. 1 (height ~5–10 cm, longest dimension ~5–20 cm) were was also found in the back reef (site C; Table 2). scattered inside this patch, but no live sabellariid polychaetes were found inside. These empty tubes were colonised by L. DISCUSSION verrucosa and Marphysa sp. 1. Parahalosydnopsis tubicola was often observed to co-occur in the same tubes of L. Insights on the reef’s dynamics. The ecosystem’s states verrucosa. The tubiculous Polydora cavitensis was also observed during the different surveys are consistent with present in this patch, together with the predatory Lumbrineris the four phases of a classical cycle of a sabellariid reef sp. 1. No polychaetes were found in the other sites, but we (Gruet, 1986). In this view, our surveys can be defined as: observed pairs of openings (spaced at ~60 cm) in all other (i) absence or pre-settlement (April 2013); (ii) settlement or sites, possibly corresponding to large U-shaped burrows dug growth (November 2012); (iii) stagnation (December 2010, by polychaete worms. January 2011); (iv) destruction (August 2012). In particular, these phases are associated with a conspicuous turnover of Species richness: temporal and spatial patterns. Polychaete the polychaete community’s composition. species richness varied both in time and space (Fig. 5). The highest richness was recorded in November 2012 (17 species) During the absence phase (April 2013), the tubiculous Loimia and the lowest in August 2012, when single representatives verrucosa was a dominant component of the community, of six families were recorded (Fig. 5a). Except the seaward forming dense aggregations. In all other surveys, L. verrucosa exposed margin (F), where species richness increased over was found at lower densities in almost all the sites (Fig. 6; time (Fig. 5b), values were higher in December 2010 and Table 2). This indicates that this species, being capable of November 2012 than in August 2012 and April 2013. Overall, colonising mud deposits, becomes dominant when no hard the number of species was higher in marginal and more substrate is available in the system. The co-occurrence of exposed sites (A, F) than in internal sites (D, E), except Parahalosydnopsis tubicola in its tubes suggests a species- the seaward portion of the inner reef (site B), which was specific association, since P. tubicola has been already found less rich than the back reef (site C; Figs. 1, 5c). A similar in mutualistic association with the congeneric Loimia medusa pattern was observed in November 2012; species richness (Savigny in Lamarck, 1818) in other parts of the Indo-Pacific increased in a seaward direction both in August 2012 and (Martin & Britayev, 1998). It can be reasonably hypothesised April 2013. In December 2010, a comparable number of that this isolated patch of coarser sediments was determined species was recorded at all sites (Fig. 5d). by the feeding and tube building activity of L. verrucosa. This species appears to establish and maintain patches of Polychaetes’ temporal and spatial distribution. The coarser sediments when the superficial substrate is dominated temporal and spatial species distributions (Table 2) are by mud deposits, possibly facilitating the establishment of summarised by the dendrograms of cluster analyses (Fig. 6). sabellariid colonies in the Jeram system. Loimia verrucosa is a surface deposit feeder, like its congener, L. medusa Six groups of species (T1–T6) were associated with different (see Llanso & Diaz, 1994). Due to its feeding strategy, this surveys (Fig. 6a). Groups T2 and T3 include species that latter species can effectively destabilise mud substrates, were found in November 2012 and at least one more survey, by decreasing the sedimentation rate of finer particles including the three tube builders: Sabellaria sp. 1, Polydora (Luckenbach, 1986). High densities of the terebellid Lanice cavitensis and Loimia verrucosa. In particular, the latter conchilega (Pallas, 1766) can increase the coarse sand fraction species (group T2) was collected in all surveys. Marphysa and heterogeneity of the sediment (Rabaut et al., 2007), thus sp. 1 (group T2) was also collected in August 2012 (Table 2). facilitating the establishment of sabellariid colonies on mud Each of the other groups (T1, T4, T5, T6) includes species substrates (Larsonneur et al., 1994). In general, this phase that were all collected in a single survey. In particular, T4 was characterised by the presence of opportunistic species includes five nereidids, Eulalia sp. 1 and Cabira sp. 1, all that both occurred in at least two different phases (group collected in November 2012. Leonnates crinitus and Cabira T2; Fig. 6a), and in at least two different zones (group S2; sp. 1 were also collected in April 2013 (Table 2). Fig. 6b), and by the absence of Sabellaria sp. 1, which occurred in all other phases. Paleaequor breve, Sigambra 408 RAFFLES BULLETIN OF ZOOLOGY 2015 Fig. 5. Species richness (grouped by family): per survey, at all sites (a); per survey, at each site (b); per site, in all surveys (c); per site, in each survey (d); chr = Chrysopetalidae, eun = Eunicidae, gly = Glyceridae, lum = Lumbrineridae, ner = Nereididae, onu = Onuphidae, phy = Phyllodocidae, pil = Pilargidae, pol = Polynoidae, sab = Sabellariidae, spi = Spionidae, ter = Terebellidae. sp. 1 and Lepidonotus sp. 2 were exclusively found in this Pearson & Rosenberg, 1978; Gallagher et al., 1983; Zajac, phase (Table 2). 1991). The nereidids, four ones exclusively collected in this phase (Table 2), include species found in soft substrates, The settlement or growth phase (November 2012) corresponded and species opportunistically colonising both soft and hard to the richest polychaete assemblage, and the dominant tube substrates, such as Ceratonereis (Composetia) burmensis builder was the spionid Polydora cavitensis. This species and Perinereis singaporiensis, respectively (Paterson et al., was collected in all the sites and in almost all surveys (Table 2004; Metcalfe & Glasby, 2008). This reasonably indicates 2). Spionids are typical pioneer species, which can rapidly that the unusually high number of nereidid species during colonise disturbed habitats during post-disturbance and early- this phase in Jeram (e.g., Frith et al., 1976; Nakao et al., successional phases (e.g., Polydora ligni Webster, 1879 = 1989; Sarkar et al., 2005) is related to the higher habitat Polydora cornuta Bosc, 1802; see Grassle & Grassle, 1974; complexity offered by the highly heterogeneous substrate 409 Polgar et al.: Polychaetes from a Sabellaria reef Fig. 6. Hierarchical cluster analyses of species relative to time (a) and space (b). In (a), six groups of species (T1–T6) are associated with different surveys; in parentheses: surveys in which all the group’s components were found (De = 7 December 2010; No = 30 November 2012; Au = 7 August 2012; Ap = 26 April 2013; Fig 2). In (b), four groups of species (S1–S4) are associated with different sites; in parentheses: sites where all the group’s components were found (A–F; Fig. 1); ‘wil’ (found at sites B and C) and ‘cla’ (found at site E) were not included in any group. Vertical dashed lines: 0.65 similarity cut-off value. Species’ abbreviations as in Table 2. conditions. Several other polychaetes were also found in facilitate sediment-stabilising tube-builders, promoting a shift the previous phase, such as Marphysa sp. 1, Lumbrineris from a community dominated by infaunal organisms to a sp. 1 and Glycera nicobarica (group T2; Fig. 6a), when they community dominated by epibenthic organisms (Reise, 2002), all occurred in a more seaward direction (Table 2). Other thus preparing the conditions for the pre-settlement phase, species were also found in the next stagnation phase, such and completing the cycle. The three species (Lepidonotus as the tubiculous Sabellaria sp. 1 and L. verrucosa, and P. sp. 1, Nectoneanthes oxypoda and Diopatra claparedii) tubicola (groups T2, T3; Fig. 6a). which characterise this phase (group T6; Fig. 6a) occurred in the lower intertidal zone (sites E, F). The other species During the stagnation phase (December 2010), three species were opportunists, which occurred in at least three different (Lysidice sp. 1, Lysidice sp. 2 and Lepidonotus cf. sublaevis) phases and five different sites (Table 2). were exclusively found in this phase, in the higher intertidal zone (group T1; Fig. 6a). The presence of the eunicids Species richness: spatial and temporal patterns. The Lysidice sp. 1 and Lysidice sp. 2 only when the sabellariid observed temporal patterns of species richness are largely reef was best developed may reflect a preference for reefal consistent with Gruet’s model (1986), with lower levels at habitats for some members of this group. Three species all sites except F during the absence phase (April 2013), only occurred in this and in the previous phase (group T3; highest levels during the settlement or growing phase Fig. 6a; Table 2). (November 2012), intermediate levels during the stagnation phase (December 2010), and again lower levels during the During the destruction phase (August 2012), the superficial destruction phase (August 2012). Similar temporal patterns substrate was dominated by shell deposits. The thick shell of species richness were observed in other benthic intertidal bed typically inhibits sediment-destabilising infaunal borers communities of polychaetes and other organisms, such (taphonomic inhibition, sensu Kidwell & Jablonski, 1983), as as aggregations of Lanice conchilega, reefs of Sabellaria also noted by Seilacher (1984) in Jeram. Given the mutually alvelolata, and seagrass communities (Cunningham et al., exclusive occurrence of sediment-stabilising and destabilising 1984; Kirkman, 1985; Van Hoey et al., 2008). Such patterns species in soft-bottom ecosystems (Posey, 1987; Volkenborn are consistent with the general properties of ecological et al., 2009), the inhibition of bioturbators would further successions (Connell, 1978; Pearson & Rosenberg, 1978). 410