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Diversity, distribution and ecology of the family Syllidae (Annelida) in the Portuguese coast (Western Iberian Peninsula)

Abstract

The diversity, distribution and ecology of the family Syllidae along the Western Iberian coast was studied, based on 145 sediment samples covering the whole Portuguese coastal shelf and 30 Saccorhiza polyschides holdfasts sampled in the north of Portugal. A total of 55 species were identified in 2,306 specimens. A total of 33 species were recorded in the holdfasts and 36 in the shelf samples spanning a wide range of sediments, bathymetry and latitude. A total of 14 species were shared between both substrates. A total of 26 species were here firstly recorded, increasing to 80 the number of species known in Portugal, and new insights were added to the ecology and geographic distribution of several species. A multivariate analysis identified three assemblages, characterized by the species (a) Sphaerosyllis bulbosa and Syllis pontxioi in the western shelf coarse sediments, (b) Parapionosyllis brevicirra and Syllis mercedesae in the southern shelf muddy sands and (c) Brania pusilla and Myrianida brachycephala in the kelp holdfasts. The type of substrate (kelp holdfast vs. soft-bottom sediments) and the sediment grain size (coarser vs. finer) were the descriptors best related to the Syllid assemblages.

Introduction

The family Syllidae Grube, 1850 (Annelida, Polychaeta, Phyllodocida) is one of the most complex, diverse, abundant and widespread among the annelid polychaetes. The number of valid species is estimated between 700 (Aguado et al. 2012) and 900 (Faulwetter et al. 2011), belonging to 74 genera (Aguado et al. 2012; Glasby et al. 2012; Lucas et al. 2012; Nygren et al. 2010). Syllids are very abundant and diverse among sponges, seaweed, seagrass, coral or hydrozoans and in soft bottoms, due to a generalist feeding strategy and active mode of life, moving in the interstitial space or crevices (Giangrande et al. 2000; San Martín 2003). The attention devoted to this family is shown by the several recent papers on their diversity and/or description of new species and genera (e.g., Abd-Elnaby and San Martín 2010; del Pilar-Ruso and San Martín 2012; Granados-Barba et al. 2003; Lattig et al. 2007; Lucas et al. 2012; San Martín and Hutchings 2006; San Martín and López 2003, among many others). New insights were recently given regarding the soft-bottom Portuguese continental shelf polychaete fauna (Martins et al. 2013) and macrobenthic communities (Martins et al. in press). The Syllid fauna was, however, still poorly known, with only close to 50 reported species and very few specialized papers (Ravara et al. 2004).

Along the Portuguese coast, north Atlantic colder waters mix with northern Africa and Mediterranean warmer waters. The western Portuguese continental shelf presents a complex current system and high energetic waves and tides regime, particularly in the northwestern sector, in contrast with the sheltered southern shelf, characterized by lower hydrodynamic energy and warmer waters (Fiúza 1983). According to the hydrodynamic regime, the intertidal coastal area has been classified into mesotidal exposed, from the northern border to Cape Carvoeiro on the west coast, mesotidal moderately exposed, from Cape Carvoeiro to Ponta da Piedade on the south coast, and mesotidal sheltered, from Ponta da Piedade to Vila Real de Santo António, southern coast (Bettencourt et al. 2004 and Fig. 1). The sedimentary coastal shelf seascape partially reflects this regime, mostly coarse sediments in the northwestern sector, predominance of sands at greater depths and in the southwestern sector and muds in the southern sector and off the major Portuguese rivers (Martins et al. 2012a). The Portuguese shelf is also dissected by several canyons, namely Porto, Aveiro, Nazaré, Cascais/Lisboa, Setúbal, S.Vicente and Portimão which represent important morphological, sedimentary and hydrological boundaries (Oliveira et al. 2007).

Fig. 1
figure1

Study area: the Portuguese coast (Western Iberia), indicating the positioning of the shelf sediment samples (black circles) and the Saccorhiza polyschides holdfasts samples (gray circle, Viana do Castelo). The hydrodynamic regime coastal subdivisions according to Bettencourt et al. (2004) are also shown

This study focus on the diversity of Syllids from the Portuguese coast (Western Iberia Peninsula) and is based on sediment samples collected on the western and southern shelf and in holdfast samples of Saccorhiza polyschides (Lightfoot) Batters 1902, from a northwestern rocky shore. This seaweed presents a long stipe and a large holdfast with internal channeling system, securing the algae to the rock, which can support a high biodiversity (McKenzie and Moore 1981). Few studies were developed about the faunal communities inhabiting the holdfasts of this species (McKenzie and Moore 1981; Tuya et al. 2011), when compared to other kelp species (Christie et al. 2003; Jørgensen and Christie 2003; Norderhaug et al. 2012; Tuya et al. 2011). Sacchoriza polyschides can be found from Norway to Portugal and is abundant on subtidal rocky shores in northern Portugal (Ardré 1970; Tuya et al. 2011).

This work is integrated in a holistic study on the diversity and distribution of the Portuguese continental shelf benthic macrofauna (Martins et al. 2012b, c, 2013, in press), and the macrofauna inhabiting S. polyschides holdfasts. Given the high abundance and diversity of Syllids in samples from both substrates and the lack of knowledge in this coastal European region, the aims of the present work were (a) to identify and characterize the diversity and distribution of the Syllidae fauna of the Portuguese coast; (b) to give new insights about the ecology of this fauna; and (c) to identify and discuss biological–environmental relationships.

Materials and methods

Study area

A total of 145 sites were sampled, covering the entire Portuguese continental shelf, from Caminha (41°51.8′N, 9°15.6′W) to Vila Real Santo António (36°56.1′N, 7°24.7′W) (Fig. 1), and a wide bathymetric range (13–195 m depth). Two sediment samples per site were collected during 2007 and 2008, with a 0.1 m2 Smith-McIntyre grab, one for macrofauna and the other for sediment grain size and total organic matter content. Sediment samples were sieved on board over 1-mm mesh screen, and the residue fixed in neutralized formalin (4 %) stained with rose Bengal. The study area sedimentary seascape is given in Martins et al. (2012a). The northwestern inner and mid-shelf and areas south of the Nazaré and Setúbal submarine canyons are dominated by coarse sediments with low fines content. The deep northwestern shelf and the southwestern shelf are characterized by sands with moderate fines content. The southern shelf is heterogeneous with a predominance of muds, sandy muds and muddy sands. Mud patches were also recognized off the Tagus and Douro rivers and north of the Nazaré canyon. The total organic matter was correlated with fines content (Spearman ρ = 0.71) and ranged from 0.3 to 9.18 % of the total sediment (Martins et al. 2012a).

A total of 30 Saccorhiza polyschides holdfasts were collected in the infralittoral zone of a rocky shore located in Viana do Castelo, northern coast of Portugal (41°42′N,8°51′W), in September 2011. Only submerged holdfasts were selected. They were carefully separated from the stipe and frond and kept in a plastic bag. Magnesium chloride (2 g per 5 L of seawater) was added to the bags, to anesthetize the organisms, during 5 min. The samples were sieved in the field over 0.5-mm mesh size and the residue fixed in neutralized formalin (4 %).

Laboratory analysis

In the laboratory, the samples were carefully washed to remove excess fixative. The holdfast maximum and minimum diameter was measured and used to calculate the area, according to 2(π × radius2). The holdfast volume was also obtained by measuring water displacement in a volumetric balloon. After hand sorting and taxonomic identification, the specimens were transferred for long-term storage in 70 % ethanol. Syllids were identified to species level, whenever possible, following San Martín (2003) and recent species descriptions references (e.g., Lucas et al. 2012).

Abundance and species richness were determined per sample. The Bray–Curtis similarity among sites was calculated after presence/absence of data transformation. Affinity groups among samples were obtained following the Unweighted Pair Group Method with Arithmetic Mean clustering (UPGMA) and visualized in Principal Coordinates Ordination analysis (PCO). These groups were characterized using total and mean species richness, mean abundance, characteristic species and quantity of exclusive species, as well as the environmental baseline data (depth, grain size and total organic matter) for the soft-bottom samples and the biometric data (diameter, area and volume) for the holdfast samples. The characteristic species per affinity group were selected from the set of species that showed the highest constancy and fidelity, according to the scaling proposed by Dajoz (1971) for constancy (constant (C > 50.0 %); common (50.0 ≥ C > 25.0 %); occasional (25.0 ≥ C > 12.5 %); rare (C ≤ 12.5 %)) and by Retière (1979) for fidelity (elective (F > 90.0 %); preferential (90 ≥ F > 66.6 %); indifferent (66.6 ≥ F > 33.3 %); accessory (33.3 ≥ F > 10.0 %); and accidental (F ≤ 10.0 %).

An environmental data matrix for all samples was prepared including latitude, longitude, depth, hydrodynamic regime (1—sheltered sites; 2—moderately exposed sites; 3—exposed sites, following Bettencourt et al. 2004) and substrate type (0—kelp holdfasts; 1—shelf sediments). For the soft-bottom shelf samples, a dedicated environmental data matrix also included the sediment median grain size and the sediment content in gravel (>2 mm), sand (0.063–2 mm), fines (>0.063 mm), biogenic fraction and total organic matter. The environmental data matrices were related to the biological data using the BIOENV procedure (BEST routine) in PRIMER v.6 (Clarke and Gorley 2006). Abundance and species richness per site and the abundance of key species in the biological affinity groups were plotted using ArcGis 10.

Results

Syllidae fauna abundance and diversity

A total of 55 species in 27 genera were identified in 2,306 Syllids. These annelids were present in all 30 holdfasts and in 68 of the 145 soft-bottom samples.

In the shelf sediments and in the holdfasts, a total of 36 and 33 species were collected, respectively, 14 of which were common to both substrates (cf. Table 1). The genera Syllis and Sphaerosyllis contributed with the highest number of species (13 and 5, respectively).

Table 1 List of species occurring in the soft-bottom sediments and/or in the S. polyschides holdfasts collected in the Portuguese coast

In the shelf sediments 1,459 syllids were collected. The most abundant were Sphaerosyllis bulbosa Southern, 1914, Syllis garciai (Campoy, 1982), Trypanosyllis coeliaca Claparède, 1868, Syllis pontxioi San Martín and López, 2000 and Eurysyllis tuberculata Ehlers, 1864 (Table 1). The following species were recorded in more than 20 sites: Syllis garciai, Sphaerosyllis bulbosa, Eurysyllis tuberculata and Syllis mercedesae Lucas et al. 2012. The spatial distribution of Syllids abundance (Fig. 2a) and species richness (Fig. 2b) showed the highest values in coarse sediments off Peniche, Aveiro and Setúbal, mostly in shallower areas (below 60 m), in opposite to muddy or sandy mud sites from the outer shelf and the southern shelf sector. In the soft-bottom samples, the mean species richness and mean abundance reached 4.5 species and 21.5 individuals per unit sampling area (0.1 m2).

Fig. 2
figure2

Spatial distribution of the abundance (a) and species richness (b) of syllids per site (shelf sediments). Legend: N number of specimens, S number of taxa

A total of 847 Syllids were sampled in the 30 holdfasts. Brania pusilla (Dujardin, 1851), Sphaerosyllis hystrix Claparéde, 1863, Myrianida brachycephala (Marenzeller, 1874) and Synmerosyllis lamelligera (Saint Joseph, 1887) were the most abundant (total abundance >50 specimens, Table 1) and the most frequent (total frequency >50 %). The mean species richness and mean abundance were 8.2 species and 28.2 individuals. The correlation between total abundance and total species richness with the holdfast biometric data was low (area: ρ = 0.19 and 0.22, respectively; volume: ρ = 0.21 and 0.08, respectively).

Species spatial distribution

Total abundance, maximum abundance per site or holdfast, substrate type, bathymetric range and sedimentary data for each species are shown in Table 1. Among the 22 Syllid species recorded exclusively in the shelf sediments, 15 were found in the coarser sediments of the northwestern shelf, off Peniche and near the head of Setúbal head canyon (Table 1), such as Odontosyllis gibba Claparède, 1863, Palposyllis prosostoma Hartmann-Schröder, 1977 (Fig. 3c), Plakosyllis brevipes Hartmann-Schröder, 1956, Streptodonta pterochaeta (Southern, 1914) (Fig. 3d) and Syllis licheri Ravara, San Martín and Moreira, 2004. Other species were only found in the coarse sediments (Table 1) of both western and southern shelf sectors, such as Dioplosyllis cirrosa Gidholm, 1962, Eurysyllis tuberculata (Fig. 3a), Opisthodonta serratisetosa (López, San Marin and Jiménez, 1997) and Syllis pontxioi. The species Syllis mercedesae was recorded along the entire shelf (Fig. 3b), in a large range of sediment types, mostly in fine sands and coarse sediments (Table 1) and sometimes in symbiosis with bivalves (Montacuta phascolionis Dautzenberg and Fischer H., 1925) and sipunculids (Phascolion (Phascolion) strombus strombus (Montagu, 1804). Two species were recorded exclusively in the southern shelf, Exogone (Exogone) verugera (Claparède, 1868) and Parexogone gambiae Lanera, Sordino and San Martín, 1994. Syllis gerlachi (Hartmann-Schröder, 1960) was recorded in fine sand off Aveiro (Table 1).

Fig. 3
figure3

Abundance distribution on the shelf sediments of Eurysyllis tuberculata (a), Syllis mercedesae (b), Palposyllis prosostoma (c), Streptodonta pterochaeta (d), Sphaerosyllis bulbosa (e), Synmerosyllis lamelligera (f), Syllis garciai (g) and Parapionosyllis brevicirra (h)

Concerning the species recorded both in the shelf sediments and in the alga holdfasts, some presented a wide spatial distribution (e.g., Myrianida brachycephala), while others were mostly recorded in the western coarse sediments, such as Haplosyllis spongicola (Grube, 1855), Paraehlersia ferrugina (Langerhans, 1881), Sphaerosyllis bulbosa (Fig. 3e), Synmerosyllis lamelligera (Fig. 3f) and Trypanosyllis coeliaca (Table 1). Sphaerosyllis hystrix higher abundance was recorded in the holdfasts but was also found in coarser sediments (Table 1). Syllis armillaris (O.F. Müller, 1776) and S. garciai (Fig. 3g) were found in a wide range of sediments and in the holdfasts (Table 1). Other species were found in the southern shelf and in the holdfasts, such as Exogone (Exogone) naidina Örsted, 1845, Parapionosyllis brevicirra Day, 1954 (Fig. 3h), Sphaerosyllis sp., Syllides edentatus Westheide, 1974 and Syllis gracilis Grube, 1840 (Table 1).

Finally, 19 species were recorded exclusively in the kelp holdfasts of which Brania pusilla in all the samples. Syllis krohni Ehlers, 1864, S. variegata Grube, 1860, Odontosyllis ctenostoma Claparède, 1868, S. alternata Moore, 1908 and S. corallicola Verrill, 1900 were recorded in 63, 57, 37, 33 and 30 % of the samples, respectively.

Multivariate analysis

The multivariate analysis results are shown in Fig. 4 and the spatial representation of the affinity groups in Fig. 5. Three major affinity groups were identified, A1, A2 and B (Figs. 4 and 5). Their overall characterization is shown in Table 2 and the species succession in Table 3. Thirteen samples with a single specimen were excluded from the analysis.

Fig. 4
figure4

Classification (a) and ordination diagrams (b) based on the presence/absence of Syllids. The clusters (A1, A2, B) are overlaid on the ordination diagram, which also represent the substrate type for each sample. Spearman’s correlation vectors of environmental data are provided as supplementary variables. The species with the highest Spearman’s correlation (ρ > 0.4) are represented as vectors in a separate ordination

Fig. 5
figure5

Spatial distribution of the Syllids assemblages along the Portuguese coast

Table 2 Characterization of the syllids assemblages identified on the Portuguese coast (Western Iberia)
Table 3 Mean species abundance per affinity group A1, A2 (ind. 0.1 m−2) and B (holdfast)

The PCO axis 1 (cf. Fig. 4b) gathered 30.3 % of the total variation and opposed A1 and A2 to B. Group B included all the holdfast samples, and so PCO axis 1 made the partition between Syllids from the shelf sediments and from the coastal kelp holdfasts. This was also shown by the superimposed vectors representing the environmental variables. Axis 2 accounted for 16.5 % of the total variation and separated A1 from A2. Fig. 4b also illustrates the sediment type of each sample showing that PCO axis 2 separated the sites located on coarser sediments in the northern exposed shelf (A1) from the sites on finer sediments in the southern sheltered shelf (A2). The vectors of the most correlated species (Fig. 4) showed two large sets of species, one in the top left side, associated with A1 (e.g., Plakosyllis brevipes), and the other in the right side, exclusively found in group B (e.g., Brania pusilla). Other species, represented in the top right, were shared by two or three groups (e.g., Sphaerosyllis hystrix), and in the bottom left, the species Syllis mercedesae were more related with group A2.

Group A1 comprised 31 sites mostly located on the mid-western shelf (Fig. 5), characterized by coarse sediments with the highest gravel content and by low fines and total organic matter content (Table 2). This group presented the highest mean abundance and high mean species richness (Table 2). A1 was characterized and dominated by Sphaerosyllis bulbosa, Syllis pontxioi and Trypanosyllis coeliaca (all constant and elective) (Tables 2, 3). Sixteen species were exclusively found in this group (Table 2).

Group A2 comprised 24 sites located in finer sediments, mostly on the southern shelf (Fig. 5). Sand, fines and total organic matter content were high (Table 2). Abundance and species richness were the lowest among all groups (Table 2). Group A2 was characterized by Parapionosyllis brevicirra, Syllis mercedesae and S. garciai (cf. Tables 2, 3). Parexogone gambiae and P. hebes (Webster and Benedict, 1884) were exclusively found here (cf. Tables 2, 3).

Group B corresponded to the Syllids collected in the kelp holdfasts. The S. polyschides holdfasts were collected at the end of the growing season and reached mean values of 21.7 cm for maximum diameter, 188.9 cm2 for area and 198.7 cm3 for the volume (cf. Table 2). Total and mean species richness values were the highest (Table 2). The group was characterized by Brania pusilla, Myrianida brachycephala, Syllis krohni and S. variegata (cf. Tables 2, 3). A total of 19 species occurred exclusively in this group.

The BIOENV procedure identified latitude, depth and substrate type as the best related variables with the Syllids spatial distribution along the Portuguese coast (ρ = 0.592). Considering the soft-bottom samples alone, the best related variables were latitude, depth, median grain size, fines and organic matter content (ρ = 0.475). If only the sedimentary variables were used, the correlation slightly decreased (ρ = 0.438), and fines content was the best related variable.

Discussion

Diversity, distribution and ecology of syllids in the Portuguese coast

Before this study, a total of 54 Syllid species were known in the Portuguese coast (e.g., Amoureux 1974; Amoureux and Calvário 1981; Campoy 1982; Carvalho et al. 2001; Fauvel 1914; Freitas et al. 2011; Hartmann-Schröder 1977; Gil and Sardá 1999; Marques 1987; Rodrigues et al. 2006, 2011; Saldanha 1995; San Martín 2003, and unpublished data). From the 55 species reported here, 26 are new records for the Portuguese fauna, namely Odontosyllis fulgurans (Audouin and Milne-Edward, 1833), Opisthodonta serratisetosa, Parexogone gambiae, Plakosyllis brevipes, Streptodonta pterochaeta, Streptosyllis bidentata Southern, 1914, Syllides convolutus (Webster and Benedict, 1884), Syllis mercedesae, Syllis parapari San Martín and López, 2000 and Syllis pontxioi (species exclusively found in the soft-bottom samples); Amblyosyllis formosa (Claparède, 1863), Miscellania dentata Martin, Alós and Sardá, 1990, Nudisyllis pulligera (Krohn, 1852), Salvatoria clavata (Claparède, 1863), Salvatoria limbata (Claparède, 1868), Syllides fulvus (Marion and Bobretzky, 1875), Syllis alternata, Syllis corallicola, Syllis schulzi (Hartmann-Schröder, 1960) and Virchowia clavata Langerhans, 1879 (species only found in the holdfasts); Myrianida brachycephala, Parapionosyllis brevicirra, Sphaerosyllis bulbosa, Sphaerosyllis sp. (accordingly to San Martín 2003), Syllides edentatus and Synmerosyllis lamelligera (species found in both substrates). This study increased the number of valid Syllid species known in Portugal from 56 to 80. Recent appropriate taxonomic developments and the heterogeneity and taxonomic complexity of these polychaetes (e.g., San Martín 2003) could explain such increase. This is key knowledge for future studies. Syllids are good faunal and ecological indicators of the physical environment, and therefore, they could be used in studies of long-term changes in marine areas and to validate the taxonomic sufficiency effectiveness (e.g., Musco et al. 2009). These 80 species represent half of the reported species for the Iberian Peninsula mainland and Spanish Islands (Lattig et al. 2007; Lucas et al. 2012; San Martín 2003), one of the best studied areas for Syllids worldwide. Other well-studied areas include Australia (160 species, San Martín and Hutchings 2006; San Martín 2005; San Martín et al. 2008a, b, 2010), the Mediterranean Sea (approximately 190 species; Musco and Giangrande 2005), the Great Caribbean Region (167 species; Salazar-Vallejo 1996), México (more than 60 species in the Pacific Mexican coast and more than 70 in the Atlantic Mexican coast; Granados-Barba et al. 2003) and Brazil where 139 species are known (Fukuda 2010; Nogueira and San Martín 2002; Nogueira and Yuanda-Guarin 2008; Nogueira et al. 2001, 2004). Other areas with a longer coastline than Portugal have fewer reported species, such as the US Gulf of México (44 species, Uebelacker and Johnson 1984), Egypt (nearly 60 species, Abd-Elnaby and San Martín 2010) or Venezuela (40 species in Thalassia testudinum (Bank and Köning, 1805) meadows, San Martín and Bone 2001; 26 species in different substrates, Liñero-Arana and Díaz 2011).

This study gives new insights about the ecology and geographic distribution of several species. The meridional distribution limit of the Lusitanean species Syllis mercedesae, recently described for the continental slope off Ártabro Gulf (Galicia, NW Spain; Lucas et al. 2012), is now set in the southern Portuguese shelf. The distribution limit of Syllis licheri, firstly described off Aveiro (northwestern Portuguese coast; Ravara et al. 2004), is now established between the Chausey Islands (English Channel; Olivier et al. 2012) and the Setúbal canyon (southwestern Portuguese continental shelf; this study). Other species considered so far endemic to the Mediterranean Sea, Parexogone gambiae and Sphaerosyllis sp. (Musco and Giangrande 2005; San Martín 2003), are recorded here for the first time in the Atlantic Ocean, in the southern Portuguese continental shelf and off Peniche, respectively. The temperate species Miscellania dentata and Virchowia clavata, known for the Mediterranean Sea and the Macaronesia biogeographic provinces (San Martín 2003), are here firstly reported for the Lusitanean biogeographic province. This study also sets the first record of the 33 species found in S. polyschides holdfasts, previously only known from other substrate types, namely hard bottoms, Posidonia oceanica rhizomes (or other seagrass meadows), photophilic algae, coralline bottoms, sponges, maërl or below infralittoral stones (San Martín 2003). Sphaerosyllis bulbosa, previously known from coarse sediments, sand and maërl, between 30 and 70 m (San Martín 2003), was reported in this study for kelp holdfasts and wider sedimentary (mud to gravel) and bathymetric (up to 127 m) range. The habitat preferences of Haplosyllis spongicola, Opisthodonta serratisetosa, Parexogone gambiae, Syllis gerlachi, S. armillaris, S. gracilis and S. mercedesae now also include soft bottom, as they were previously associated with different hard-bottom types only, such as sponges, Posidonia oceanica rhizomes, photophilic or sciaphilic algae (Lucas et al. 2012; San Martín 2003).

The present study also sets wider bathymetric range for several species. Some species were recorded for deeper waters compared to San Martín (2003) namely Dioplosyllis cirrosa (127 m), Parexogone gambiae (43 m), Plakosyllis brevipes (69 m), Streptodonta pterochaeta (50 m), Syllis gerlachi (100 m), S. pontxioi (127 m), Exogone (Exogone) naidina (99 m), Haplosyllis spongicola (179 m), Myrianida brachycephala (129 m), Paraehlersia ferrugina (127 m), Parapionosyllis brevicirra (102 m), Sphaerosyllis hystrix (195 m), Syllides edentates (29 m), Syllis armillaris, S. garciai (133 m) and Synmerosyllis lamelligera (99 m).Other species were recorded at lower depth, as Syllis mercedesae, 29–1,132 m (Lucas et al. 2012), and Palposyllis prosostoma, between 25 and 200 m (San Martín 2003) and for Syllis licheri new minimum and maximum depth were set (25 and 99 m).

Syllis mercedesae was in this study sometimes found in gastropod shells, in symbiosis with a bivalve (Montacuta phascolionis) and a sipunculid (Phascolion (Phascolion) strombus strombus). A symbiotic mode of life is known for nearly 20 Syllid species, mostly with decapods, cnidarians and sponges (López et al. 2001; Martin and Britayev 1998; Martin et al. 2002). Symbiotic species have developed morphological adaptations, such as the simplification of chaetae, camouflage coloring or particular behavior (e.g., short-distance host recognition; Martin et al. 2002). Among the genus Syllis, only S. armillaris, S. cornuta Rathke, 1843, S. gracilis, S. onkylochaeta Hartmann-Schröder, 1991 and S. sclerolaema Ehlers, 1901 show commensal habits. The symbiotic associations and the morphological features of those species are very different from Syllis mercedesae, suggesting that this can correspond to a distinct symbiotic association. In fact, Cutler (1994) refers that only Syllis cornuta is usually found with one of the following sipunculans: Phascolion (Phascolion) strombus strombus, Aspidosiphon (Aspidosiphon) muelleri muelleri Diesing, 1851 (in shells) or Phascolosoma (Phascolosoma) meteori (Hérubel, 1904) (in mud tubes). On the other hand, Phascolion (Phascolion) strombus strombus was already found with the bivalve Montacuta phascolionis [or Epilepton clarkiae (Clark W., 1852)] and the gastropod Ondina diaphana (Jeffreys, 1848), but never before with Syllids.

The present study also revealed that the total number of species in the soft-bottom shelf sediments was only slightly higher than in the kelp holdfasts (36 and 33, respectively), despite the range of sediment types, depth and latitude covered by the soft-bottom samples. The complexity of the internal channeling system of the S. polyschides holdfast may offer larger and more protective areas for this fauna (McKenzie and Moore 1981) than the sediment interstitial spaces. Several studies also suggest that hard substrates are more important for Syllids than soft substrates (e.g., Antoniadou et al. 2004; Liñero-Arana and Díaz 2011; San Martín 2003; Serrano et al. 2006). Faulwetter et al. (2011) recorded only 23 species in soft-bottom samples (in Israel) when compared to the 62 species found in several hard substrates (e.g., filamentous Phaeophyceae and Chlorophyceae, Jania sp., Cystoseira sp.), in Crete, in the Mediterranean Sea. Granados-Barba et al. (2003) also described a lower Syllid diversity and abundance in the soft bottom of the eastern coast of Mexico when compared to coralline hard bottoms. Authors attributed this to the complexity of the coral habitat, with crevices and fissures furnishing shelter. From the 45 species they reported, 38 were found in hard bottom (corals), 31 in soft bottoms (mostly in coarse carbonate sands) and 21 were shared by the two substrates.

Syllids assemblages and relationships with environmental factors

The present study found three major assemblages, one associated with coarser sediments, another with finer sediments and another with S. polyschides holdfasts. Syllids have been reported from several habitats showing differential affinity for hard or soft bottom (San Martín 2003). The coarse sand Syllid assemblage here described with Sphaerosyllis bulbosa, Syllis pontxioi and Trypanosyllis coeliaca is part of the coarse sediment macrobenthic community reported by Martins et al. (in press), for the Portuguese continental shelf. This is a similar community to the gravels dominated by Astarte sulcataVenus casina (Glémarec 1973) or the Venus community (Thorson 1957), identified in several European coasts, in Portugal with a high number of warm water species (e.g., Opisthodonta serratisetosa, Palposyllis prosostoma or Syllis licheri) co-occurring with boreal, Atlantic–Mediterranean, amphi-Atlantic or cosmopolitan species (e.g., Odontosyllis gibba, Plakosyllis brevipes or Sphaerosyllis bulbosa; Musco and Giangrande 2005; San Martín 2003). The fine sand Syllids assemblage dominated by the warm water species Parapionosyllis brevicirra, Syllis mercedesae and S. garciai is part of the Lusitanean macrofauna assemblage found in muddy sands of the southern Portuguese shelf (Martins et al. in press). Granados-Barba et al. (2003) found a decreasing abundance and diversity of Syllids from carbonate (coarse sands with coral and shell fragments) to terrigenous sediments (mud and sandy mud). This agrees with our results, in which the assemblage installed in coarser sediments was more diverse and abundant than that from finer sediments. It is recognized that polychaete communities exhibit a close relationship with sediments, depth, hydrodynamics and other abiotic parameters (e.g., Labrune et al. 2007; Simboura et al. 2000). The coarse sediments from the northwestern Portuguese continental shelf provide interstitial space to the small-sized and highly motile syllids and pisionids (Martins et al. 2012c), but also lumbrinerids (Martins et al. 2012b). The space between the gravel and sand particles, the internal channeling system of S. polyschides holdfasts or the cracks and crevices in the coralline hard bottoms create adequate shelter and therefore support a high abundance and diversity of small-sized polychaetes, such as the Syllids. They use those spaces to move through, to feed, to hide from predators and to reproduce, which explain why Syllids are considered one of the most successful polychaete groups in both soft and hard bottoms (e.g., Faulwetter et al. 2011; Granados-Barba et al. 2003; San Martín 2003).

The group associated with kelp holdfasts was characterized by Brania pusilla, Myrianida brachycephala, Syllis krohni and S. variegata, species showing primary affinity for hard bottom, including seagrass and/or kelp rhizomes, photophilic algae, corals and sponges. Among the holdfasts inhabitants, the majority have been regarded cosmopolitan or to have an Atlantic–Mediterranean distribution and only few species showed Mediterranean and/or Macaronesian distribution (Miscellania dentata, Sphaerosyllis sp., Virchowia clavata) (San Martín 2003). Several works have studied the faunal communities associated with kelp species, mostly Laminaria (e.g., Christie et al. 2003; Jørgensen and Christie 2003; Norderhaug et al. 2012; Tuya et al. 2011) and with seagrass meadows (rhizomes and leaves), namely Posidonia oceanica (e.g., San Martín 2003; San Martín et al. 1990; Somaschini et al. 1994) or Thalassia testudinum (San Martín and Bone 2001; Stoner and Lewis 1985). In such habitats, a high number of Syllid species and specimens have been found (e.g., San Martín 2003). Christie et al. (2003) and Jørgensen and Christie (2003) revealed important differences on the fauna abundance and diversity associated with the holdfast, the stipe and the frond of the kelp Laminaria. Polychaetes of the genera Anaitides, Eulalia, Harmothoe, Hediste, Kefersteinia, Lagisca and Lepidonotus were recorded in the holdfasts, while the syllids Amblyosyllis, Brania, Pionosyllis and Trypanosyllis were found mostly in the stipe (Christie et al. 2003; Jørgensen and Christie 2003). In our case, the later genera were all found in the holdfasts of S. polyschides. No specific studies were found in the literature focusing on Syllids associated with holdfasts of S. polyschides and only very few dedicated to the overall fauna. A study undertaken by McKenzie and Moore (1981) highlighted that in the space between the base of the holdfast and the hard substrate (to which it is attached), several amphipods, ophiuroids and polychaetes were found, while many polychaetes, amphipods, decapods and fish were recorded inside the holdfasts. McKenzie and Moore (1981) recorded a total of 77 species, while in our study, considering Syllids alone, we reported a total of 33 species. Gestoso et al. (2012) comparing the epifaunal assemblages in native and invasive seaweed species found mostly gastropods (45 % of the total taxa), polychaetes and ophiuroids in S. polyschides.

Conclusions

A total of 2,306 syllids belonging to 55 species were identified with only 14 species shared by the shelf sediments and Saccorhiza polyschides holdfasts. A total of 26 species were firstly recorded in this study, increasing to 80 the number of Syllid species known to Portugal. This study sets 20 new bathymetric ranges and gives new insights about the geographic distribution of six species and the ecology of several others (7 species first record in soft bottom; first record of several Syllids in the holdfasts). The type of substrate (holdfast vs. soft bottom) and the sediment grain size (coarser vs. finer) were the descriptors best related to the Syllids assemblages.

References

  1. Abd-Elnaby FA, San Martín G (2010) Eusyllinae, Anoplosyllinae, and Exogoninae (Polychaeta: Syllidae) for the Mediterranean Coasts of Egypt, together the description of one new species. Life Sci J 7(4):132–139

    Google Scholar 

  2. Aguado MT, San Martín G, Siddall M (2012) Systematics and evolution of syllids (Annelida, Syllidae). Cladistics 28:234–250

    Article  Google Scholar 

  3. Amoureux L (1974) Annélides Polychetes recueillies sur les pentes du talus continental au Nord-Ouest de I’Espagne et du Portugal (Campagne 1972 de la «Thalassa»). Cuad C Biol 3:121–154

    Google Scholar 

  4. Amoureux L, Calvário J (1981) Annélides Polychétes du Portugal Données nouvelles et indroduction. Arq Mus Bocage B 1(12):147–155

    Google Scholar 

  5. Antoniadou C, Nicolaidou A, Chintiroglou C (2004) Polychaetes associated with the sciaphilic alga community in the northern Aegean Sea: spatial and temporal variability. Helgol Mar Res 58:168–182

    Article  Google Scholar 

  6. Ardré F (1970) Contribution à l’étude des algues marines du Portugal I. La Flore. Port Acta Biol B 10:1–423

    Google Scholar 

  7. Bettencourt AM, Bricker SB, Ferreira JG, Franco A, Marques JC, Melo JJ, Nobre A, Ramos L, Reis CS, Salas F, Silva MC, Simas T, Wolff W (2004) Typology and reference conditions for Portuguese transitional and Coastal waters, Development of guidelines for the application of the European Union Water Framework Directive. INAG/IMAR, Lisboa

    Google Scholar 

  8. Campoy A (1982) Fauna de España. Fauna de anélidos poliquetos de la Península Ibérica. EUNSA, Publicaciones de Biología de la Universidad de Navarra, Serie Zoológica, Pamplona

    Google Scholar 

  9. Carvalho S, Ravara A, Quintino V, Rodrigues AM (2001) Macrobenthic community characterisation of an estuary from the western coast of Portugal (Sado estuary) prior to dredging operations. Bol Inst Esp Oceanogr 17(1–2):179–190

    Google Scholar 

  10. Christie H, Jorgensen NM, Norderhaug KM, Waage-Nielsen E (2003) Species distribution and habitat exploitation of fauna associated with kelp (Laminaria hyperborea) along the Norwegian coast. J Mar Biol Assoc UK 83:687–699

    Article  Google Scholar 

  11. Clarke KR, Gorley RN (2006) PRIMER v.6: user Manual/Tutorial PRIMER-E. Plymouth, UK

  12. Cutler EB (1994) The Sipuncula: their systematics, biology, and evolution. Cornell University Press, New York

    Google Scholar 

  13. Dajoz R (1971) Précis d’Ecologie. Ed. Dunod, Paris

    Google Scholar 

  14. del Pilar-Ruso Y, San Martín G (2012) Description of a new species of Sphaerosyllis Claparède, 1863 (Polychaeta: Syllidae: Exogoninae) from the Alicante coast (W Mediterranean) and first reports of two other species of Syllidae for the Mediterranean Sea and the Iberian Peninsula. Mediterr Mar Sci 13:187–197

    Google Scholar 

  15. Faulwetter S, Chatzigeorgiou G, Galil BS, Arvanitidis C (2011) An account of the taxonomy and distribution of Syllidae (Annelida: Polychaetes) in the eastern Mediterranean, with notes on the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean. ZooKeys 150:281–326

    PubMed  Article  Google Scholar 

  16. Fauvel P (1914) Annélides polychètes pélagiques provenant des campagnes des yachts Hirondelle et Princesse-Alice, 1885–1910. Imprimerie de Monaco, Monaco

    Google Scholar 

  17. Fiúza AFG (1983) Upwelling patterns off Portugal. In: Suess E, Thiede J (eds) Coastal upwelling: its sediment record. Plenum Publishing Corporation, New York, pp 85–98

    Chapter  Google Scholar 

  18. Freitas R, Ricardo F, Pereira F, Sampaio L, Carvalho S, Gaspar M, Quintino V, Rodrigues AM (2011) Benthic habitat mapping: concerns using a combined approach (acoustic, sediment and biological data). Estuar Coast Shelf Sci 92:598–606

    Article  Google Scholar 

  19. Fukuda MV (2010) Contribution to the taxonomic knowledge of the syllids (Polychaeta: Syllidae) from the southeastern-southern Brazil. PhD thesis, Universidade de São Paulo, Brazil

  20. Gestoso I, Olabarria C, Troncoso JS (2012) Effects of macroalgal identity on epifaunal assemblages: native species versus the invasive species Sargassum muticum. Helgol Mar Res 66:159–166

    Article  Google Scholar 

  21. Giangrande A, Licciano M, Pagliara P (2000) The diversity of diets in Syllidae (Annelida: Polychaeta). Cah Biol Mar 41:55–65

    Google Scholar 

  22. Gil J, Sardá R (1999) New records of Annelida Polychaeta for the Portuguese Fauna (with comments on some already known species). Arq Mus Bocage 3(10):287–336

    Google Scholar 

  23. Glasby C, Schroeder P, Aguado MT (2012) Branching out: a remarkable new branching syllid (Annelida) living in a Petrosia sponge (Porifera: Demospongiae). Zool J Linn Soc 164:481–497

    Article  Google Scholar 

  24. Glémarec M (1973) The benthic communities of the European North Atlantic continental shelf. Oceanogr Mar Biol Ann Rev 11:263–289

    Google Scholar 

  25. Granados-Barba A, Solís-Weiss V, Tovar-Hernández MA, Ochoa-Rivera V (2003) Distribution and diversity of the Syllidae (Annelida: Polychaeta) from the Mexican Gulf of Mexico and Caribbean. Hydrobiologia 496:337–345

    Article  Google Scholar 

  26. Hartmann-Schröder G (1977) Polychaeten aus dem Sublitoral und Bathyal vor der portugiesischen und marokkanischen Küste. Auswertung der Fahrt 8 (1967) von F.S. ‘Meteor’. METEOR Forsch-Ergebnisse Ser D 26:65–99

    Google Scholar 

  27. Jørgensen NM, Christie H (2003) Diurnal, horizontal and vertical dispersal of kelp-associated fauna. Hydrobiologia 503:69–76

    Article  Google Scholar 

  28. Labrune C, Grémare A, Amouroux J-M, Sardá R, Gil J, Taboada S (2007) Assessment of soft-bottom polychaete assemblages in the Gulf of Lions (NW Mediterranean) based on a mesoscale survey. Estuar Coast Shelf Sci 71:133–147

    Article  Google Scholar 

  29. Lattig P, San Martín G, Martin D (2007) Taxonomic and morphometric analyses of the Haplosyllis spongicola complex (Polychaeta: Syllidae: Syllinae) from Spanish seas, with re-description of the type species and descriptions of two new species. Sci Mar 71(3):551–570

    Article  Google Scholar 

  30. Liñero-Arana I, Díaz O (2011) Syllidae (Annelida, Polychaeta) from the Caribbean coast of Venezuela. ZooKeys 117:1–28

    PubMed  Article  Google Scholar 

  31. López E, Britayev T, Martin D, San Martín G (2001) New symbiotic associations involving Syllidae (Annelida: Polychaeta) with taxonomic and biological remarks on Pionosyllis magnifica and Syllis cf. armillaris. J Mar Biol Assoc UK 81:399–409

    Article  Google Scholar 

  32. Lucas Y, San Martín G, Parapar J (2012) Two new species of Syllidae (Annelida: Polychaeta) from DIVA-Artabria I project (cruise 2002) to deep areas off NW Spain. Zootaxa 3589:77–88

    Google Scholar 

  33. Marques V (1987) A plataforma continental do Algarve: definição qualitativa das biocenoses de substrato móvel. Instituto Hidrográfico, Lisboa

    Google Scholar 

  34. Martin D, Britayev TA (1998) Symbiotic polychaetes: review of known species. Oceanogr Mar Biol Ann Rev 36:217–340

    Google Scholar 

  35. Martin D, Núñez J, Riera R, Gil J (2002) On the associations between Haplosyllis (Polychaeta, Syllidae) and gorgonians (Cnidaria, Octocorallaria), with the description of a new species. Biol J Linn Soc 77:455–477

    Article  Google Scholar 

  36. Martins R, Quintino V, Rodrigues AM Diversity and spatial distribution patterns of the soft-bottom macrofauna communities on the Portuguese continental shelf. J Sea Res. doi:10.1016/j.seares.2013.03.001 (in press).

  37. Martins R, Azevedo MR, Mamede R, Sousa B, Freitas R, Rocha F, Quintino V, Rodrigues AM (2012a) Sedimentary and geochemical characterization and provenance of the Portuguese continental shelf soft-bottom sediments. J Mar Syst 91:41–52

    Article  Google Scholar 

  38. Martins R, Carrera-Parra LF, Quintino V, Rodrigues AM (2012b) Lumbrineridae (Polychaeta) from the Portuguese continental shelf (NE Atlantic) with the description of four new species. Zootaxa 3416:1–21

    Google Scholar 

  39. Martins R, San Martín G, Rodrigues AM, Quintino V (2012c) On the diversity of the genus Pisione (Polychaeta, Pisionidae) along the Portuguese continental shelf, with a key to European species. Zootaxa 3450:12–22

    Google Scholar 

  40. Martins R, Sampaio L, Rodrigues AM, Quintino V (2013) Soft-bottom Portuguese continental shelf polychaetes: diversity and distribution. J Mar Syst 123–124:41–54

    Article  Google Scholar 

  41. McKenzie JD, Moore PG (1981) The micro-distribution of animals associated with the bulbous holdfasts of Saccorhiza polyschides (Phaeophyta). Ophelia 20:201–213

    Google Scholar 

  42. Musco L, Giangrande A (2005) Mediterrnean Syllidae (Annelida, Polychaeta) revisited: biogeography, diversity and species fidelity to environmental features. Mar Ecol Prog Ser 304:143–153

    Article  Google Scholar 

  43. Musco L, Terlizzi A, Licciano M, Giangrande A (2009) Taxonomic structure and the effectiveness of surrogates in environmental monitoring: a lesson from polychaetes. Mar Ecol Prog Ser 383:199–210

    Article  Google Scholar 

  44. Nogueira JMM, San Martín G (2002) Species of Syllis Lamarck, 1818 (Polychaeta: Syllidae) living in corals in the state of Sao Paulo, southeastern Brazil. Beaufortia 52(7):57–93

    Google Scholar 

  45. Nogueira JMM, Yuanda-Guarin G (2008) A new species of Syllis (Polychaeta: Syllidae: Syllinae) from off Fortaleza, north-eastern Brazil. J Mar Biol Assoc UK 88(7):1391–1399

    Article  Google Scholar 

  46. Nogueira JMM, San Martín G, Amaral ACZ (2001) Description of five new species of Exogoninae Rioja, 1925 (Polychaeta: Syllidae) associated with the stony coral Mussismilia hispida (Verril, 2868) in São Paulo State, Brazil. J Nat Hist 35(12):1773–1794

    Article  Google Scholar 

  47. Nogueira JMM, San Martín G, Fukuda MV (2004) On some exogonines (Polychaeta, Syllidae, Exogoninae) from the northern coast of the state of São Paulo, southeastern Brazil. Results of BIOTA/FAPESP/Bentos Marinho Project. Meiofauna Mar 13:45–77

    Google Scholar 

  48. Norderhaug KM, Christie H, Andersen G, Bekkby T (2012) Does the diversity of kelp forest macrofauna increase with wave exposure? J Sea Res 69:36–42

    Article  Google Scholar 

  49. Nygren A, Sundkkvist T, Mikac B, Pleijel F (2010) Two new and two poorly known autolytines (Polychaeta: Syllidae) from Madeira and the Mediterranean Sea. Zootaxa 2640:35–52

    Google Scholar 

  50. Oliveira A, Santos AI, Rodrigues A, Vitorino J (2007) Sedimentary particle distribution and dynamics on the Nazaré canyon system and adjacent shelf (Portugal). Mar Geol 246:105–122

    Article  Google Scholar 

  51. Olivier F, Grant C, San Martín G, Archambault P, McKindsey CW (2012) Syllidae (Annelida: Polychaeta: Phyllodocida) from the Chausey Archipelago (English Channel, France), with a description of two new species of the Exogoninae Prosphaerosyllis. Mar Biodivers 42(1):55–63

    Article  Google Scholar 

  52. Ravara A, San Martín G, Moreira MH (2004) Syllidae (Annelida, Polychaeta) from the continental shelf off Aveiro (NW Portugal) with the description of a new species, Syllis licheri. Senckenb Biol 84:1–11

    Google Scholar 

  53. Retière C (1979) Contribution à la connaissance des peuplements benthiques du golfe Normano-Breton. Thèse d’Etat, Université Rennes I, France

  54. Rodrigues AM, Meireles S, Pereira T, Gama A, Quintino V (2006) Spatial patterns of benthic macroinvertebrates in intertidal areas of a southern European estuary: The Tagus, Portugal. Hydrobiologia 555:99–113

    Article  Google Scholar 

  55. Rodrigues AM, Quintino V, Sampaio L, Freitas R, Neves R (2011) Benthic biodiversity patterns in Ria de Aveiro, Western Portugal: environmental-biological relationships. Estuar Coast Shelf Sci 95:338–348

    Article  CAS  Google Scholar 

  56. Salazar-Vallejo SI (1996) Lista de especies y bibliografía de poliquetos (Polychaeta) del Gran Caribe. An Inst Biol Univ Nac Aut Mex 67(1):11–50

    Google Scholar 

  57. Saldanha L (1995) Fauna Marinha Atlântica. Publicações Europa-America, Mem-Martins

    Google Scholar 

  58. San Martín G (2003) Annelida, Polychaeta II: Syllidae. In: Ramos MA, Alba J, Bellés X, Gosálbez J, Guerra A, Macpherson E, Martín F, Serrano J, Templado J (eds) Fauna Ibérica, vol 21. Museo Nacional de Ciencias Naturales, CSIC, Madrid, pp 1–554

    Google Scholar 

  59. San Martín G (2005) Exogoninae (Polychaeta: Syllidae) from Australia with the description of a new genus and twenty-two new species. Rec Aust Mus 57:39–152

    Article  Google Scholar 

  60. San Martín G, Bone D (2001) Syllidae (Polychaeta) de praderas de Thalassia testudinum en el Parque Nacional Morrocoy (Venezuela). Rev Biol Trop 49(2):609–620

    PubMed  Google Scholar 

  61. San Martín G, Hutchings P (2006) Eusyllinae (Polychaeta: Syllidae) from Australia with the description of a new genus and fifteen new species. Rec Aust Mus 58:257–370

    Article  Google Scholar 

  62. San Martín G, López E (2003) A new genus of Syllidae (Polychaeta) from Western Australia. Hydrobiologia 496:191–197

    Article  Google Scholar 

  63. San Martín G, Estapé S, García-Ocejo A, Gómez C, Jiménez P (1990) Estudio de la taxocenosis de anélidos poliquetos de rizomas de Posidonia oceanica en las costas de Almería. Bol Inst Esp Oceanogr 6:41–58

    Google Scholar 

  64. San Martín G, Hutchings P, Aguado MT (2008a) Syllinae (Polychaeta: Syllidae) from Australia. Part 1. Genera Branchiosyllis, Eurysyllis, Karroonsyllis, Parasphaerosyllis, Plakosyllis, Rhopalosyllis, Tetrapalpia n.gen, and Xenosyllis. Rec Aust Mus 60:119–160

    Article  Google Scholar 

  65. San Martín G, Hutchings P, Aguado MT (2008b) Syllinae (Polychaeta: Syllidae) from Australia. Part 2. Genera Inermosyllis, Megasyllis n. gen., Opisthosyllis and Trypanosyllis. Zootaxa 1840:1–53

    Google Scholar 

  66. San Martín G, Hutchings P, Aguado MT (2010) Syllinae (Polychaeta: Syllidae) from Australia. Part 3. Genera Alcyonosyllis, Genus A, Parahaplosyllis, and Trypanosyllis (Trypanobia). Zootaxa 2493:35–48

    Google Scholar 

  67. Serrano A, San Martín G, López E (2006) Ecology of Syllidae (Annelida: Polychaeta) from shallow rocky environments in the Cantabrian Sea (South Bay of Biscay). Sci Mar 70(3):225–235

    Google Scholar 

  68. Simboura N, Nicolaidou A, Thessalou-Legaki M (2000) Polychaete communities of Greece: an ecological overview. Mar Ecol 21:129–144

    Article  Google Scholar 

  69. Somaschini A, Gravina MF, Ardizzone GD (1994) Polychaete depth distribution in a Posidonia oceanica bed (Rhizome and Matte Strata) and neighbouring soft and hard bottoms. Mar Ecol 15:133–151

    Article  Google Scholar 

  70. Stoner AW, Lewis FG (1985) The influence of quantitative and qualitative aspects of habitat complexity in tropical seagrass meadows. J Exp Mar Biol Ecol 94:19–40

    Article  Google Scholar 

  71. Thorson G (1957) Bottom communities (sublittoral or shallow shelf). In: Hedgpeth JW (ed) Treatise on marine ecology and paleoecology. Geological Society of America, USA, pp 461–534

    Google Scholar 

  72. Tuya F, Larsen K, Platt V (2011) Patterns of abundance and assemblage structure of epifauna inhabiting two morphologically different kelp holdfasts. Hydrobiologia 658:373–382

    Article  Google Scholar 

  73. Uebelacker JM, Johnson PG (1984) Taxonomic guide to the Polychaetes of the Northern Gulf of México. Minerals Management Service, Gulf of Mexico Regional Office, Louisiana

    Google Scholar 

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Acknowledgments

The first author benefited from a PhD Grant (SFRH/BD/44231/2008) awarded by the Portuguese Foundation for Science and Technology (FCT—Fundação para a Ciência e Tecnologia) and co-financed by FSE (Fundo Social Europeu). This investigation was supported by the FCT-funded project “ACOSHELF” (POCI/MAR/56441/2004—PPCDT/MAR/56441/2004) and by “MeshAtlantic,” funded by European Union ERDF-Atlantic Area Program 2009-1/110. We are grateful to our colleagues which helped during the sampling campaigns.

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Martins, R., Magalhães, L., Peter, A. et al. Diversity, distribution and ecology of the family Syllidae (Annelida) in the Portuguese coast (Western Iberian Peninsula). Helgol Mar Res 67, 775–788 (2013). https://doi.org/10.1007/s10152-013-0362-3

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Keywords

  • Portuguese continental shelf
  • Polychaetes
  • Latitude
  • Sediments
  • Kelp holdfast
  • Saccorhiza polyschides