Mollusc assemblages and their biogeographical affinities
The mollusc fauna associated with the Zostera marina bed from Cantarriján bay, with 80 species, is the most diverse from the studied Z. marina beds, in the Atlantic (Jacobs & Huisman 1982; Jacobs et al. 1983; Currás et al. 1993; Boström & Bonsdorff 1997; Frost et al. 1999; Hily & Bouteille 1999; Blanchet et al. 2005; Quintas 2005), and in the Mediterranean (Ledoyer 1962, 1964; Çinar et al. 1998; Sfriso et al. 2001).
Several circumstances could be related with this high species richness:
(1) Sampling procedures, such as: (i) the relatively high number of replicates; (ii) the extended period of sampling allowing to collect also occasional species (some of them probably ephemeral species, and others that use the bed only for feeding or breeding); (iii) the relatively large sampling area considered (several replicates of 222 m2) (i.e. in a study on mollusc epifauna of Posidonia oceanica, Russo & Terlizzi (1998) sampled with a hand-towed net an area of about 20 m2; (iv) the efficiency of the type of trawls (small Agassiz) for epifauna.
(2) The deeper situation of the studied bed (between 14 and 16 m depth), which implies a certain stability in time moderating environmental variability, such as wave action, storms, desiccation, etc.Hemminga & Duarte (2000) discussed the role of the depth in the stability of the seagrasses formations. Jacobs & Huisman (1982) found an increment of diversity with depth in Z. marina and Zostera noltii meadows that they consider correlated with environmental stability.
(3) The patchy distribution of the Z. marina bed from Cantarriján bay, with a sandy bottom surrounding the fragmented bed. Actually most Z. marina beds are somehow patchy at different scales (i.e. square meters, or tens of square meters), and the influence of such fragmentation in seagrass beds for the macrofauna has been largely discussed (Robbins & Bell 1994; Bologna & Heck 1999; Frost et al. 1999; Sánchez-Jerez et al. 1999; Bell et al. 2001; Bologna 2006). According to Bologna (2006), the edges in a fragmented Z. marina bed, have a significantly greater density of benthic organisms than the interior and the unvegetated zones. Consequently, the edges of Z. marina formations may actively and passively accumulate food resources and organisms, which would lead to increased secondary production and potentially elevate trophic transfer to the higher level consumers (Bologna & Heck 1999; Bologna 2006). Moreover, the edges of a seagrass bed would be the first available refuge for organisms moving between habitat patches or an active refuge for organisms living in nearby unvegetated bottoms. However, Frost et al. (1999) did not find significant differences between the species of the macrofauna from fragmented and continuous Z. marina beds in Salcombe Estuary, Devon (UK), the differences found were related with differences in density of some species.
The transition from the unvegetated to vegetated bottom in Z. marina beds is less abrupt than in patchy P. oceanica beds. The bottom inside the bed is sandy and similar to the nearby soft bottom and in fact many species typical of soft bottoms have been collected inside the bed by SCUBA diving and digging (J.L. Rueda and C. Salas, unpublished data). Nevertheless, only eight species (with only 21 individuals) can be considered typical of the unvegetated sandy bottom, and were not collected in other Z. marina beds from Southern Spain. The influence of the nearby soft bottom on the composition of the mollusc assemblage from the studied Z. marina bed can thus be considered quite limited. The similarity of the infauna in the Zostera bed and in unvegetated surrounding sediments was likewise explicitly stated by Mars (1966, p. 53) in the French Mediterranean lagoons.
Some of these soft-bottom species are gastropods and may use the bed as a feeding ground, such as the carnivorous Orania fusulus (2 ind.) and Crassopleura maravignae (3 ind.) or the scavengers Nassarius heynemanni (1 ind.) and Gibberula miliaria (3 ind.). The other four species are filter feeders, such as the gastropod Turritella communis (1 ind.), and the three bivalves, Digitaria digitaria (2 ind.), Acanthocardia aculetata (1 ind.) and Clausinella fasciata (4 ind.). These bivalves are typically associated with bioclastic bottoms that occur at the deeper edge of the bed.
(4) The latitudinal location, in the Alborán Sea, near the Strait of Gibraltar and in front of the African coast. This marine zone has probably the highest species richness from the littoral of Europe (Gofas 1999). From a biogeographical point of view, most of the molluscs (65%) found in the Z. marina bed from Cantarriján have a Lusitanian–Mediterranean distribution (sensuEkman 1953). About 22% show a Mediterranean distribution, although some of them can be found up to the South of Portugal and a few of them have been collected around the Canary Islands, such as Smaragdia viridis or Bolma rugosa. The proximity to Africa is shown by the presence of four species with a mainly West African distribution, which have a Northern limit in the Western Mediterranean, such as Cancellaria cancellata, Tectonatica filosa, O. fusulus and N. heynemanni (Table 1). Only Rissoa membranacea has a typical Atlantic distribution associated with Z. marina or Caulerpa prolifera meadows (Rueda & Salas 2003). This relationship is reflected by its high abundance (9.8% of total molluscs), and frequency (95% of the samples) (Table 1). Taking into account the dominance and the frequency, only a few species can be considered frequent and typically associated with the Zostera bed (Table 2): Jujubinus striatus, R. membranacea, Nassarius pygmaeus, Mitrella minor, S. viridis, Rissoa monodonta, Bittium reticulatum, Calliostoma cf. planatum, among the gastropods; and Anomia ephippium, Musculus subpictus, among the bivalves. Most of these species were also collected in a C. prolifera bed from the Bay of Cádiz, in which were not found S. viridis strictly associated with Z. marina and Cymodocea nodosa nor R. monodonta, a typical Mediterranean species (Rueda & Salas 2003). This pattern of dominance by a few species was also found in other studies on macrofauna associated with Z. marina: Thayer et al. 1975 in Newport River estuary (North Carolina, USA), Turner & Kendall 1999 in the River Yealm (UK).
In P. oceanica meadows from five western Mediterranean sites Russo & Terlizzi (1998) found a wide variability in the composition of the molluscan assemblages. Each seagrass meadow was well characterized by the high dominance of a few particular species; among them J. striatus, B. reticulatum and Nassarius incrassatus are also dominant in the mollusc assemblage of Z. marina from Cantarriján bay. Templado (1984), nevertheless, found similar molluscan assemblages in different P. oceanica beds from Cabo de Palos (Eastern Spain), with a few characteristic (dominant) species, which were different from those found in the Cantarriján Z. marina bed. Scipione et al. (1996) also found a few dominant species in P. oceanica and C. nodosa, from which only B. reticulatum is shared by C. nodosa (from Ischia) and Z. marina (from Cantarriján). Actually the Posidonia meadow differs so much from Zostera because its rhizome stratum is edificating an equivalent to a hard substrate, whereas the rhizomes of Zostera remain within the sediment.
The mollusc assemblage of our study differs from those found in the lagoon of Venice (Sfriso et al. 2001) and in the Turkish coast (Çinar et al. 1998). In these areas the Zostera spp. studied were shallow, between 0.5 and 2 m, and influenced by fresh water inputs. Most of the fauna collected in these studies was infauna, due mainly to the use of sampling methods such as corers or small quadrates. Moreover, in these areas and shallow depths, the winter water temperatures are similar to those registered in Northern Europe.
The most similar mollusc assemblage from a Zostera bed has been found by Quintas (2005) in Galicia (NW Spain), in the mixed meadows of Z. marina and Z. noltii, with 68 species of molluscs identified, among which J. striatus, R. membranacea, B. reticulatum and Nassarius reticulatus were the most common species.
From a trophic point of view, most of the dominant mollusc species (gastropods) from Z. marina bed are grazers, such as rissoids or trochids. These feed on diatoms and other periphyton, as it has been indicated in other seagrasses (Peduzzi 1987; Lepoint et al. 2000; Fredriksen et al. 2004; Hily et al. 2004). Nassarius pygmaeus is a scavenger, feeding among others on dead animals. The presence of M. minor is very interesting from a trophic point of view; because this species is a specialized predator feeding on eggs of various species, generally other molluscs, but probably also other taxa such as fishes (García Raso et al. 2004). Its frequency (82.5%) and abundance (1799 individuals collected and an average density of about 20 ind. per 100 m2) point out the role as a spawning site and a nursery of Z. marina (Hemminga & Duarte 2000). Thayer et al. (1975) found also Mitrella lunata as the third most abundant species in a Western Atlantic Z. marina bed, where 45 species of macrofauna were identified, among which 33 were fishes.
The two most frequent and abundant bivalves are suspension-feeders (A. ephippium, M. subpictus), that seem to find a sufficient source of particles, considering their abundance values.
Temporal changes in the mollusc assemblages
Seagrasses in temperate areas generally show large temporal variations in shoot density, canopy morphological features and epiphyte biomass, although mainly observed in the temperate northern seagrass meadows, most of them distributed in the intertidal zone (Hemminga & Duarte 2000). Consequently, there is a temporal variation in densities of seagrass-associated animals that often coincides with that of the macrophyte biomass (Z. marina: Thayer et al. 1975; Toyohara et al. 1999; Sfriso et al. 2001; C. nodosa: Scipione et al. 1996; Sfriso et al. 2001).
The structure of the mollusc taxocoenosis here studied changed over time (Figs 2–5), although with a relatively high variability especially in the autumn and winter months. This pattern is probably related to the different degree of patchiness in mollusc populations, and variability also of the Z. marina bed features, which seem stronger during the autumn–winter months due also to more variable and unstable environmental conditions.
High abundance and species richness values were found in the spring and summer in coincidence with the increment of seagrass canopy height and shoot density. Similar temporal patterns in relation with biomass or shoot/frond density of seagrass and seaweed beds were found in studies of mollusc assemblages from other vegetated bottoms off Southern Spain (Rueda et al. 2001; Sánchez-Moyano et al. 2001; Rueda & Salas 2003) and also in other locations within the Mediterranean Sea (Terlizzi & Russo 1998; Sfriso et al. 2001). In C. nodosa beds from Ischia (Scipione et al. 1996) and from the Canary Islands (Brito et al. 2005), maximum abundance is found in September for molluscs and polychaetes, respectively.
As most of the species of molluscs associated with seagrasses are grazers that feed on the periphyton living on the leaves, the increments in abundance during the warm period could be related with the increment of leaf surface and likely of epiphyte colonizaton. In contrast during the autumn and winter, when the leaves fall and shoot density is reduced, the abundance also decreases. Another factor related with changes in the abundance of the species is recruitment (Rueda et al. 2001; Rueda & Salas 2003), which in the studied Zostera bed is responsible for the density increments for some of the dominant species, such as B. reticulatum, N. pygmaeus or J. striatus. The latter is responsible for the increase in abundance observed in February, and in the various spring and summer months (Table 1). The peak of September is related with recruitment events [during the summer months there is an increment of juveniles (1–3 mm) of some dominant species, such as Rissoa spp., Nassarius spp., J. striatus, M. minor].
The temporal trend of species richness values (Fig. 3) was mainly related with the presence in the bed of occasional species during the warm period (Table 1). Some of these occasional species use the bed for feeding (Sepia officinalis) or for breeding (opistobranchs); they may have a short life cycle but no detailed information is available. It is interesting to note the increment of carnivorous gastropods and cephalopods in the bed, probably attracted by the increment in animal densities during the summer. Diversity and evenness values show also a temporal trend (Fig. 4). The relatively low values of these indices in various months were related with the high abundance of J. striatus (Table 1, Fig. 2). These values are similar to those found in Newport River (North Carolina) (Thayer et al. 1975). These authors suggested that these low values reflect a young and evolving eelgrass-bed community. In fact the studied patchy bed from Cantarriján bay can be considered somehow unstable, because of the small size of the patches, which make it very sensitive to environmental (i.e. sea storms or torrential rains) or antropogenic influences (i.e. frequent fishery activity). In fact, after completing this study, there were torrential rains, which smothered the bed under sediments; and ever more illegal trawling in the protected area is damaging these beds.