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Seasonal variation of a molluscan assemblage living in a

Caulerpa

prolifera

meadow within the inner Bay of Ca´diz (SW Spain)

Jose L. Rueda*, Carmen Salas

Departamento de Biologı´a Animal, Facultad de Ciencias, Universidad de Ma´laga, Campus de Teatinos, s/n, 29071-Malaga, Spain

Received 15 August 2002; accepted 6 December 2002

Abstract

The molluscan macrofauna living in shallow muddy bottoms with the green algae Caulerpa proliferawas studied monthly between February 1994 and January 1996 in the inner Bay of Ca´diz (SW Spain). The molluscan assemblage followed a similar pattern over the 2 years, displaying seasonal trends in species richness, abundance and structure. During the autumn and winter months, a decrease in abundance, species richness and diversity and an increase in evenness occurred. During the spring and summer months, the molluscan assemblage was characterised by an increase in species richness, abundance and diversity. These seasonal trends were supported statistically by the presence of significantly different groupings of seasonal samples in multivariate analyses. Despite human impacts in the bay (e.g. aquaculture activities, sewage), the presence of repetitive seasonal trends, based on the qualitative and quantitative data, indicates the stability of the molluscan assemblage over 2 years. Benthic characteristics from the inner Bay of Ca´diz, such as shallow soft bottoms with the presence of macrophytes and current dynamics, seem to be key factors influencing the composition and seasonality of this molluscan assemblage.

Keywords:mollusc; species richness; diversity; temporal variation; seaweed; coastal lagoon

1. Introduction

The meeting of diﬀerent biogeographical regions, as documented in previous faunistic lists, points to the importance of southern Spain for the European marine diversity of molluscs (Rueda, Salas, & Gofas, 2000; Salas, 1996; Van Aartsen, Menkhorst, & Gittenberger, 1984). Molluscan assemblages have been studied from Mediterranean coastal waters of southeastern Spain, in soft bottoms (Luque, 1986; Rueda, Ferna´ndez-Casado,

Salas, & Gofas, 2001; Salas, personal communication;

Salas, 1996; Van Aartsen et al., 1984), bioclastic bot-toms (Rueda et al., 2000), seagrass beds (Hergueta, personal communication; Templado, 1984), intertidal and subtidal rocky shores (Garcı´a-Go´mez, 1983; Salas & Luque, 1986; Sa´nchez-Moyano, Estacio,

Garcıá-Adiego, & Garcıá-Go´mez, 2000), calcareous algal formations (Hergueta & Salas, 1987; Salas & Hergueta, 1986) and red coral bottoms (Salas & Sierra, 1986; Templado et al., 1986). By contrast, information on molluscan assemblages of the Atlantic coasts of south-ern Spain is scarce (Rueda et al., 2001), though there have been general studies of benthic communities (Arias, 1976; Del Vals, Conradi, Garcıá-Adiego, Forja, & Go´mez-Parra, 1998; Rodrı´guez & Vieitez, 1992; Templado et al., 1993). In most of these previous studies there has been no temporal investigation of the mol-luscan assemblages, therefore changes in composition and structure over time remain poorly documented.

In southern Spain, certain habitats of the Mediterra-nean coasts, such as calcareous algal formations (Salas & Hergueta, 1986) or seagrass beds (Hergueta, personal communication) are known for seasonal changes of molluscan assemblages. In those habitats, seasonal changes in faunistic composition and structure of the assemblage were related to seasonal variations of the * Corresponding author.

E-mail addresses:[email protected](J.L. Rueda),casanova@ uma.es(C. Salas).

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vegetated component of the seabed. The available data on temporal and/or seasonal studies of molluscan as-semblages from the Atlantic coasts of southern Spain re-main very poor, particularly in shallow waters (Arias & Drake, 1994). This type of study is therefore necessary to understand the dynamics of the benthic communities and their relationships with seasonal environmental changes or the eﬀects on time of anthropogenic dis-turbances.

The Bay of Ca´diz (SW Spain) is an interesting area for the study of spatial and temporal dynamics of benthic communities, as it is located in the Atlantic Ocean, close to the Mediterranean Sea and to northern Africa, which implies the confluence of fauna from different biogeographical regions (Rueda et al., 2001). A second interesting feature of this bay is the presence of different habitats such as seagrass beds, soft and rocky bottoms and salt marshes where aquaculture activities occur. Arias (1976)studied the benthic communities of this bay and included some general information about the species of molluscs. Seasonality of the macro-benthos, including molluscs, and their productivity have been recently studied in some shallow lagoons (depth between 0.4 and 2 m) related to aquaculture activities (Arias & Drake, 1994; Drake & Arias, 1997). The distribution and growth of the Hydrobia species from these shallow lagoons have been studied temporally, displaying seasonal trends (Drake & Arias, 1995). Information about temporal variation of benthic com-munities of deeper subtidal habitats of the bay is needed for a better management of the Bay of Ca´diz, which is a protected natural park.

Rueda et al. (2001)described the seasonal changes of

a molluscan assemblage living in shallow sandy bottoms with macrophytes in the outer part of the bay (depth between 3 and 6 m). The assemblage displayed seasonal trends in species composition, however, its structure was more inﬂuenced by recruitment events of bivalves, favoured by oceanic currents, rather than seasons.

The aim of the present study is to characterise the composition and structure of a mollusc assemblage living in shallow muddy bottoms with the presence of the algae Caulerpa prolifera, within the inner Bay of Ca´diz. This shallower part of the bay is less influenced by oceanic currents than the outer part, however, it is contiguous to several aquaculture lagoonal areas, where seasonal trends of their benthic assemblages have been observed (Arias & Drake, 1994). The inner part of the Bay of Ca´diz receives a large quantity of fine sediments from the aquaculture lagoonal area, accumulated at an average of 0.52 cm per year (Munõz-Pe´rez & Sańchez-Lamadrid, 1994). This high sedimentation has favoured the presence of muddy bottoms in the inner bay where dense C. prolifera meadows are well established. The shallow depth of the sampling area (between 1 and 3 m) and the presence of macrophytes may indicate that clear

seasonal trends in species composition, as well as in the structure of the assemblage, will occur, despite the in-ﬂuence of human activities in the area.

2. Material and methods

2.1. Area of study

The Bay of Ca´diz (SW Spain; 36239–36379N and 6099–6219W) is a shallow ecosystem, which is largely used for aquaculture activities in the intertidal salt marshes and lagoonal areas (Fig. 1). The bay is subdivided into two basins, a shallower basin (inner bay), with a maximum depth of 11 m, and a deeper basin (outer bay) with a maximum depth of 17 m. The water temperature from the bay shows a seasonal trend with high values in August (24–26_{C) and low values in} December (12_{C). The mean salinity values (practical} salinity units) in the inner bay range from 32 in some autumn and winter months (wet season) to ca. 42 in summer (dry season). A progressive increase of the concentration of organic matter in the sediments of the bay has been recorded over time (Blasco, Go´mez-Parra, Frutos, & Establier, 1987), as a result of aquaculture activities and the polluted eﬄuents of a population of approximately 400,000 inhabitants. A progressive en-hancement in chlorophyllaconcentration in the bay has also been detected in the water column (Establier, Blasco, Lubian, & Go´mez-Parra, 1990).

2.2. Collection of samples

Samples were collected every month from a subtidal bottom, (36299N; 6159W) with a water depth between 1 and 3.3 m (tidal variation), containing a dense bed of the green algae Caulerpa prolifera. This macrophyte shows a seasonal pattern of growth with a peak in the summer months (Sańchez-Moyano, Estacio, Garcıá-Adiego, & Garcıá-Go´mez, 2001). The sediment of the sampling site was composed mainly of fine sand (38.8%) and mud (20%). In the inner bay, the organic carbon content of the sediment is generally higher than in the outer bay, with values oscillating between 1.97 and 5.18%, and normally higher than 3%.

One monthly sample was collected from February 1994 to January 1996, except in December 1995 due to unfavourable weather. Samples were obtained from a ﬁshing boat by towing a semicircular dredge (width 1 m), with a 1 cm mesh inner bag, for 10 min at a constant speed of 1 knot. The dredged area for each monthly sample was approximately 300 m2. This sampling area represents more than three times the minimum area for a correct estimation of the species richness of molluscs living in this particular habitat (Salas, personal communication). The sampled area was of this size in order to collect other 910 J.L. Rueda, C. Salas / Estuarine, Coastal and Shelf Science 57 (2003) 909–918

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groups of mobile organisms (e.g. crustaceans) for current studies. No replication of the samples was con-sidered. Samples were sieved on different mesh sizes (10, 5, and 3 mm) and both epifauna and infauna were col-lected. The smaller fractions were sorted using a stereo-microscope. Molluscs were separated from the other macrobenthos, fixed in formaldehyde 10% and finally preserved in neutralised alcohol 70%. All fractions were sorted quantitatively over the 2 years and all mollusc individuals were identified and measured.

2.3. Data analysis

Dominance (D) (relative abundance of a particular species within the sample expressed as percentage) and frequency (F) (calculated as the percentage of monthly

samples in which a particular species is present over the 2 years) were calculated for each monthly sample and for the total collected over the 2 years. The following basic and derived parameters were also calculated on each sample: total abundance (individuals per sample), number of species, percentage of juveniles (number of juveniles of a particular species within the monthly sample expressed as percentage), diversity of Shannon– Wiener (H9) (Krebs, 1989) and evenness index (J) (Pielou, 1969).

Seasonal and annual similarities/dissimilarities of the composition and structure of the assemblage were analysed by multivariate methods, using group-average sorting classiﬁcation and non-metric multidimensional scaling (MDS) ordination with the Bray–Curtis similarity measure (Clarke, 1993). Both sorting classiﬁcations and Fig. 1. Sampling site of the present study in the inner bay (1) and its location in the Bay of Ca´diz (SW Spain). Sampling site of a previous study in the outer bay (Rueda et al., 2001) is also displayed in the map (2). The salt marshes area contains several lagoons and ponds used for aquaculture activities.

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MDS ordinations were calculated: (1) qualitatively based on the presence or absence of species, and (2) quantita-tively using fourth root transformed abundance data. Molluscan assemblages from the diﬀerent monthly samples were compared statistically using an analysis of similarities (ANOSIM). Multivariate analyses were performed using the PRIMER package from Plymouth Marine Laboratory, UK.

3. Results

3.1. Composition of the molluscan assemblage

A total of 6003 individuals, belonging to 26 species, were collected and identiﬁed over the 2 years (Table 1). The assemblage was dominated in terms of number of species (65%) by gastropods, with 14 species of pro-sobranchs and three opistobranchs. The family Nassar-idae (four species) and the family RissoNassar-idae (three species) were the most abundant in terms of number of species. Gastropods also showed higher abundance and dominance values in comparison with the other classes of molluscs, with 70.9% of the total number of individuals collected. Bivalves were represented by only nine species, and showed lower abundance compared with gastro-pods. The Cephalopoda group was not abundant in the samples (Table 1).

Only seven species showed Dominance values (D) higher than 1% and, of these, the trochid Jujubinus striatuscorresponded to the 30.1% of the total (Table 1). Other dominant species were the gastropods Tricolia tenuis,Pusillina marginata,Calliostoma sp.,Rissoa mem-branacea and the bivalves Corbula gibba and Parvi-cardium exiguum. In general, the values ofDwere higher for gastropods than for bivalves.

The species occurring most frequently in time

ðF>75%) were mainly gastropods, such asCalliostoma

sp.,Jujubinus striatus,Tricolia pullus, Rissoa membrana-cea,Pusillina radiataandNassarius incrassatus(Table 1). A total of nine species, including Nassarius vaucheri,

Abra alba,Venerupis aureaorPandora inaequivalvis, had

Fvalues lower than 10%.

3.2. Seasonal variation of the molluscan assemblage

The abundance of molluscs was higher in the summer months of the ﬁrst year (maximum 1840 individuals in July 1994) than in the second year (up to 758 individuals per monthly sample in September 1995) (Fig. 2, Table 1). This was inﬂuenced by high juvenile densities of the bivalveCorbula gibba, during July and August of 1994. This bivalve, however, displayed a lowFvalue (30.4%) (Table 1) indicating its lower presence in this assemblage. In both years, similar abundance trends were observed for the remainder of the species from the assemblage

(withoutC. gibba), with higher values in the spring and summer months (Mean¼408 ind. sample1) than in the autumn and winter months (Mean¼108 ind. sample1) (Fig. 2).

Most species increased in abundance in the spring and summer months (Table 1), due to recruitment. In both years, the abundance of juveniles represented between 20 and 40% of the total abundance of molluscs in those months (Fig. 3). The recruitment of diﬀerent species, such as the trochids Calliostomasp. (from June to August) andJujubinus striatus(from April to August) or the rissoids Rissoa membranacea (from April to September) and Pusillina marginata (from March to September), was similar in both years. A similar trend was also found in both years for the epifaunal bivalve

Parvicardium exiguum(from April to July). Other species, such as Corbula gibba or Ostrea sp. were generally represented in this assemblage by juvenile stages (<5 mm) in the summer months. The peaks of abun-dance were thus related to an increase in juveniles due to similar recruitment in both years.

Species richness followed a similar trend in both years (Fig. 4), with high values in the spring and summer months (11 spp.2; MeanSD) and low values in the autumn and winter periods (6 spp.2). The presence of the opistobranchsBulla striataorHaminoeasp., as well as juveniles of some bivalves, such as Ostrea stentina,

Venerupis aureaorAbra alba only occurred in the sum-mer months (Table 1).

Diversity values of Shannon–Wiener index (H9) displayed similar trends in both years (Fig. 4). The highest values of H9 were registered in the spring and summer months in both years (2.30.5) and the lowest values were registered in the autumn and winter months (1.70.4). The evenness (J) (Fig. 5) followed a simi-lar trend in both years with low values in the spring and summer months (0.670.15), and high values in the autumn and winter months (0.750.16), with a decrease during the autumn of 1995 (values between 0.4 and 0.6). This decrease in evenness was a consequence of the increase in abundance of trochids such as Callios-toma sp. and Jujubinus striatus during the autumn of 1995 (Table 1). The temporal trend in evenness was generally opposite to that observed for the diversity and species richness.

3.3. Seasonal and inter-annual variability of the assemblage

Seasonal groupings of samples were obtained in both the sorting classiﬁcation and the MDS based on qualitative data (presence/absence). The summer and spring samples (warm season) from both years were dissimilar to the autumn and winter samples (cold season) in the MDS ordination plot (Fig. 6A). The spring samples from both years were grouped together 912 J.L. Rueda, C. Salas / Estuarine, Coastal and Shelf Science 57 (2003) 909–918

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Monthly abundance of the species collected from February 1994 to January 1996

1994 1995 1996

F M A M J J A S O N D J F M A M J J A S O N J N D F

Gastropods

Calliostomasp. 6 2 12 2 46 21 98 20 84 52 4 27 7 11 4 5 16 22 83 62 131 49 3 767 12.78 100

Jujubinus striatus 16 28 8 56 88 44 107 80 55 25 8 22 27 24 7 47 34 66 166 582 143 120 57 1810 30.15 100

Tricolia tenuis 1 9 3 2 7 419 106 76 7 3 3 15 19 1 1 31 35 17 60 33 14 3 865 14.41 95.6

Rissoa membranacea 7 5 5 34 59 12 14 6 5 14 11 3 18 118 49 12 6 16 24 15 8 441 7.35 91.3

Rissoa similis 2 7 3 10 14 1 37 0.62 26.1

Pusillina marginata 5 6 18 3 52 400 56 44 1 66 29 23 13 6 43 3 2 770 12.83 73.9

Bittium reticulatum 1 1 2 0.03 8.7

Cerithiopsis minima 1 1 0.02 4.3

Nassarius incrassatus 11 1 7 4 5 4 1 4 1 4 1 43 0.72 47.8

Nassarius pygmaeus 2 1 2 6 1 2 1 1 16 0.27 34.8

Nassarius reticulatus 1 1 1 2 1 6 0.10 21.7

Nassarius vaucheri 1 1 0.02 4.3

Odostomia unidentata 1 4 1 1 8 15 0.25 21.7

Chrysallida terebellum 1 1 1 1 1 5 0.08 21.7

Bulla striata 4 1 1 1 7 0.12 17.4

Haminoeasp. 1 5 2 8 0.13 13.0

Dendrodorissp. 1 1 2 4 0.07 13.0

Bivalves

Musculus costulatus 1 1 2 0.03 8.7

Ostreola stentina 1 4 1 1 7 0.12 17.4

Loripes lacteus 1 1 0.02 4.3

Parvicardium exiguum 5 4 6 63 68 39 34 1 1 3 42 33 12 11 3 1 326 5.43 69.6

Abra alba 1 1 0.02 4.3

Venerupis aurea 1 1 2 0.03 8.7

Corbula gibba 1 1 812 32 1 11 2 860 14.33 30.4

Pandora inaequivalvis 1 1 0.02 4.3

Cephalopods

Sepiasp. 5 5 0.08 4.3

Total abundance 29 59 63 77 303 1840 474 273 147 88 23 78 67 40 115 308 196 149 340 758 317 187 72 6003

N, total abundance (number for 2 years);D, dominance (%);F, frequency (%). Winter samples from January (J) to March (M); spring samples from April (A) to June (J); summer samples from July (J) to September (S) and autumn samples from October (O) to December (D).

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with the summer samples from both years. Samples from both winter periods were located between autumn samples. No significant qualitative differences were found between the assemblages for the 2 years (one-way ANOSIM: Factor year,p¼0:26), the two autumn– winter periods (one-way ANOSIM: Factor cold season 1 vs cold season 2, p¼0:169), or the two spring–sum-mer periods (one-way ANOSIM: Qualitative, Factor warm season 1 vs warm season 2, p¼0:331). Assemblages from the spring and summer months from both years were significantly different to those from the autumn

and winter months of the same year (one-way ANOSIM: Factor warm season 1 vs cold season 1, p<0:005; Factor warm season 2 vs cold season 2, p<0:005) or contiguous years (one-way ANOSIM: Qualitative, Factor warm season 1 vs cold season 2, p<0:005; Factor warm season 2 vs cold season 1,p<0:005).

In the quantitative MDS ordination plot (Fig. 6B), the monthly samples were also grouped according to season. The autumn and winter samples were also located at different sides of the MDS ordination plot to the spring and summer months. No significant quanti-tative differences were found between the assemblages for the 2 years (one-way ANOSIM: Factor year, Fig. 4. Monthly values of species richness (line and squares) and diversity (H9) (dotted line and open circles) of the molluscan assemblage throughout the study period. The line represents the average values between monthly samples. Monthly sample area is 300 m2.

Fig. 3. Monthly percentages of juveniles collected between February 1994 and January 1996. Shell length of juveniles:Corbula gibba, 3–5 mm;

Parvicardium exiguum, 3–4 mm;Tricolia tenuis, 3–4 mm; trochids, 3–4 mm; rissoids, 3 mm. The group trochids includesCalliostomasp. andJujubinus striatus. The group rissoids includesRissoa membranacea,Rissoa similisandPusillina marginata.

Fig. 2. Monthly values for abundance (number of individuals per monthly sample) of molluscs between February 1994 and January 1996. Circles represent the entire assemblage. The solid line represents the average values between months for the entire assemblage. Squares are data without the bivalveCorbula gibba. Dotted line represents the average values between months without the data forC. gibba. Monthly sample area is 300 m2.

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p¼0:568), the two autumn–winter periods (one-way ANOSIM: Factor cold season 1 vs cold season 2,

p¼0:504), or the two spring–summer periods (one-way ANOSIM: Factor warm season 1 vs warm season 2,

p¼0:348). Assemblages from the spring and summer months from both years were, however, signiﬁcantly diﬀerent to those from the autumn and winter months of the same year (one-way ANOSIM: Factor warm season 1 vs cold season 1,p<0:005; Factor warm season 2 vs cold season 2,p<0:005) or contiguous years (one-way ANOSIM: Factor warm season 1 vs cold season 2,

p<0:005; Factor warm season 2 vs cold season 1,

p<0:005). Both the presence/absence of species and their abundance thus displayed a very clear seasonal trend that was similar over the 2 years.

4. Discussion

4.1. Faunistic composition

The bulk of the molluscan species listed in this study are representative of the broader Lusitanian region and are similar to a previous study in the outer part of this bay (Rueda et al., 2001). Some of the molluscan species, inhabiting these muddy bottoms with the presence of the green algaeCaulerpa prolifera, are also associated with seagrass species such as Zostera marina, Zostera noltii

andCymodocea nodosa. The presence of seagrass mead-ows (e.g.Z. noltiiin the outer bay and few small beds of

C. nodosa in the lagoonal system of the inner bay) inﬂuences the faunistic composition of the assemblages living in C. prolifera. Of the recorded species, Tricolia tenuis and Rissoa membranaceaare generally found on the seagrassesZ. marina or C. nodosa(Gofas, personal communication), whereas Jujubinus striatus, with a strong preference for these seagrasses, is also frequent and abundant in bottoms withC. prolifera(Rueda et al., 2001; Sa´nchez-Moyano et al., 2001). In general, this molluscan assemblage is similar to that observed in

other closed and shallow bays of the Mediterranean coasts, containing seagrass and seaweed beds (Dantart, Frechilla, & Ballesteros, 1990; Murillo & Talavera, 1983). On the Atlantic littoral of France, the molluscan fauna of similar lagoonal areas is characterised by fewer species than in the Mediterranean Sea, with dominance of a few species displaying certain heterogeneity of abundances and biomass (Labourg & Desprez, 1997).

The fauna from tropical and temperate waters of Western Africa is represented in the soft bottoms of the outer Bay of Ca´diz byNassarius elatusand some bivalves such asMacoma meloandEastonia rugosa(Rueda et al., 2001). Populations of other subtropical species from the Atlantic coasts of Africa have been described re-cently in diﬀerent coastal habitats of the southern Iberian Peninsula (Rueda & Gofas, 1999; Rueda & Salas, 1998; Rueda et al., 2000). No species from tropical or Fig. 6. MDS ordination plots of the monthly samples based on the presence/absence (A) and on the fourth root transformed quantitative data (B) of the molluscan assemblage. Winter samples from January (J) to March (M); spring samples from April (Ap) to June (Jn); summer samples from July (Jl) to September (S) and autumn samples from October (O) to December (D). Encircled points represent sample groups with an average dissimilarity (Bray–Curtis measure) between clusters of 68.4 and 70.3% for qualitative and quantitative data, respectively.

Fig. 5. Monthly values of the evenness (J) between February 1994 and January 1996.

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temperate Western Africa has been found in the studied assemblage of the inner bay. The absence of this faunal component could be explained by a lower level of oceanic inﬂuence in this part of the bay (Alvarez et al., 1999), which could aﬀect the larval settlement of species from similar habitats around the area. Moreover, the inner bay of Ca´diz stands rather isolated from other similar la-goonal ecosystems. To the west, it is separated from the shallow lagoons of the Algarve coast by the mouth of the Guadalquivir river area. To the east, the Mediterranean lagoons (e.g. Nador in Northern Morocco, Mar Menor in SE Spain) are remote and separated by a long stretch of rocky coast.

In this assemblage, gastropods were the dominant group both in terms of number of species and in-dividuals. The dominance of gastropod species, com-pared with bivalves, could be favoured by their direct development, the hydrodynamics of this shallower part of the bay of Ca´diz (e.g. less oceanic inﬂuence) (Alvarez et al., 1999), sediment characteristics (e.g. organic carbon content in the sediment), and the dense vegetated cover ofCaulerpa prolifera. The presence of benthic vegetation (e.g. seagrasses, seaweeds) may beneﬁt the presence of high species richness with large and stable populations of dominant species (e.g. trochids, rissoids) within this zone of a lagoonal habitat, despite the presence of unvegetated muddy bottoms which usually support lower species richness (Salas, personal communication).

The dominance of gastropods in the inner Bay of Ca´diz is particularly notable when comparing this assemblage with that of the outer bay (Rueda et al., 2001). The recruitment events of some bivalves, such as

Corbula gibba,Venerupis aureaorPandora inaequivalvis, did not develop populations in the inner bay, while juveniles of the same species developed large populations in the outer bay (Rueda et al., 2001) during the same studied period. In benthic habitats, sediments with high organic load generally result in increase of abundance, biomass, and production of fauna, except under anae-robic conditions (Buchanan and Moore, 1986). The large sediment-retention capacity of the stolons of Caulerpa prolifera results in an organic enrichment of the sedi-ments (Sańchez-Moyano et al., 2001). The dense algal cover ofC. proliferacan have an indirect negative effect on the infauna, especially bivalves, because of the pro-motion of anoxic conditions in the sediments (Sańchez-Moyano et al., 2001; Sundba¨ck, Jo¨nsson, Nilson, &

Lindstro¨m, 1990). In soft bottoms withC. prolifera, the

epifauna (e.g. gastropods) seem to be favoured over the infaunal bivalves due to changes in the vegetated surfaces (e.g. fronds growth, increment of fronds density) and the organic enrichment of the sediments.

The abundant and frequent gastropodCalliostomasp. could not be identiﬁed to species, as the species of this genus are problematic in the area of transition between the Mediterranean Sea and the Atlantic Ocean. The

Atlantic forms usually have a heavier sculpture of spiral cords than Mediterranean ones, and this variation of sculptures obscures the delimitation of the species. This species is close to the Mediterranean speciesCalliostoma conulus, but it possesses heavier ribs. A similar species has been found living in bioclastic bottoms (18–30 m depth) in the Straits of Gibraltar and was named as

Calliostoma sp. 1 (Rueda et al., 2000). A taxonomic re-vision of the species of the genus Calliostoma is needed in the Straits of Gibraltar area. In the present study, the species is named Calliostoma sp. for concordance with other studies on mollusc assemblages of the area.

4.2. Seasonal changes in the assemblage over 2 years

The molluscan composition and structure followed a seasonal trend, similar to that observed in molluscan assemblages from other vegetated habitats in southern Spain, such as shallow soft bottoms with macroalgae (Dantart et al., 1990; Rueda et al., 2001), calcareous algae formations (Salas & Hergueta, 1986) or seagrass beds (Hergueta, personal communication). The presence of vegetation on soft bottoms causes better stabilisation of the sediments and greater accumulation of organic mat-ter compared with unvegetated seabeds. This results in signiﬁcantly higher animal richness, abundance and biomass in vegetated habitats in temperate and cold areas (Bostro¨m & Bonsdorﬀ, 1997; Edgar, Shaw, Watson, & Hammond, 1994). Generally, juveniles or adults are sheltered in vegetated bottoms, diminishing the risk of being re-suspended and transported away (O´lafsson, Peterson, & Ambrose, 1994) or predated (Irlandi, 1994). The presence of the dense algal layer of

Caulerpa prolifera may reduce the inter-annual varia-bility of the assemblage because of the survival of most juveniles, especially of the dominant gastropod species. Moreover, the increase of food available (e.g. organic matter due to sediment-retention) for juveniles could represent a key factor in the population dynamics of some gastropod species and of the entire assemblage (Sa´nchez-Moyano et al., 2001).

High abundance and species richness values occurred in the spring and summer months, when the algae

Caulerpa prolifera displays maximum frond densities and biomass in southern Spain, as found in the Bay of Algeciras (Sańchez-Moyano et al., 2001). Similar trends of high abundance of molluscs associated with the biomass or shoot/frond density of seagrass and seaweed beds have been found in studies of molluscan assemb-lages of vegetated bottoms off Southern Spain (Hergueta, personal communication; Rueda et al., 2001; Salas & Hergueta, 1986; Sańchez-Moyano et al., 2001). In spring and summer months, an increase in abundance or in number of species has been generally related to the recruitment events. The increase of the availability of microhabitats (e.g. higher fronds density, epiphytes) 916 J.L. Rueda, C. Salas / Estuarine, Coastal and Shelf Science 57 (2003) 909–918

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may also support the presence of higher numbers of species and abundances as found in benthic assemblages of heterogeneous sediment types (Dewarumez, Davoult, Sanvicente Anorve, & Frontier, 1992; Frontier & Pichod-Viale, 1991).

A repetitive seasonality in species composition and abundance was found in both years. Abundance and recruitment events, as well as diversity and evenness were very similar in the same months of consecutive years. In general, no year to year differences occurred in the recruitment of gastropods with direct development, the most dominant and frequent molluscan class of this habitat. Conversely, in the outer Bay of Ca´diz, inter-annual similarities of the molluscan assemblage from vegetated soft bottoms were based only on the species presence/absence but not on their abundance (Rueda et al., 2001). In that assemblage, recruitment of bivalves played a significant role during 1995, influenced by the presence of high densities of the filter feeder bivalve

Corbula gibba. The presence of large populations of bivalves may result in adult–larval interactions, causing reductions in larval recruitment of up to 40% (Andre & Rosenberg, 1991). In the inner part of the bay, dense populations of bivalves such asC. gibbadid not develop successfully, despite the high abundance of juveniles in the summer recruitment of 1994. The unsuccessful development of bivalve populations in this part of the bay could be related to the higher organic loads of the sediment and the dense algae cover, which can promote anoxic conditions of the sediments and aﬀect adversely some infaunal species such as bivalves (Sa´nchez-Moyano et al., 2001).

For the same period of study, a seasonal trend in both years was observed for the community of decapod crustaceans in the outer bay (Lo´pez de la Rosa, Garcı´a-Raso, & Rodriguez, 2002), whereas the decapod assem-blage remained stable in the inner and shallower part of the bay (Lo´pez de la Rosa, personal communication).

5. Conclusions

The molluscan assemblage ofCaulerpa proliferabeds within this area of southern Spain shows a relatively higher species richness than similar habitats of other semiclosed and muddy lagoonal areas from European coasts. The seasonal trends observed in the molluscan assemblage seem to follow the vegetative cycle of the algaeC. prolifera. The absence of year to year variability in this study may indicate a general stability of the molluscan assemblage.

The intense aquaculture activities in the saltmarsh zone of the bay, together with the aﬄuence of the town of Ca´diz, give rise to deposition of ﬁne sediments in the inner bay (ca. 0.52 cm yr1) and, consequently, to eutrophica-tion of this basin. In the absence of rich and structured

seagrass meadows in the inner bay, the dense beds ofC. proliferamay stabilise the year to year variations of the molluscan assemblages by retaining the sediment with high organic matter content and developing heteroge-neous microhabitats for the epifauna (e.g. gastropods).

Acknowledgements

This study is within the project PB 92-0415 supported by the Spanish government M.E.C., DGICYT funds. We are grateful to Dr Inmaculada Lo´pez de la Rosa for her assistance with the sampling programme, Manuel Ferna´ndez-Casado for his help in the laboratory and to Dr Serge Gofas (University of Ma´laga, Spain) for his valuable comments and taxonomical support. The authors would also like to thank two anonymous ref-erees for their valuable comments.

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