Effect of Environmental Factors on the Spatial Distribution of the Epifauna of the Alga Halopteris Scoparia in Algeciras Bay, Southern Spain

Effect of environmental factors on the spatial distribution of the epifauna of the alga Halopteris scoparia in Algeciras Bay, Southern Spain

J.E. Sanchez-Moyano,´ E.M. Garc´ıa-Adiego, F.J. Estacio and J.C. Garc´ıa-Gomez´ Laboratorio de Biolog´ıa Marina, Dpto. Fisiolog´ıa y Biolog´ıa Animal, Facultad de Biolog´ıa, Universidad de Sevilla, Apdo. 1095, 41080 Sevilla, Spain (E-mail: [email protected].)

Accepted 17 January 2001

Key words: algal epifauna, Halopteris scoparia, southern Spain

Abstract The physical characteristics and environmental versatility of the alga Halopteris scoparia (Phaeophyta, Sphacelari- ales) make it a suitable substrate for development of epiphytic communities. Spatial variation of the epifauna on this alga in Algeciras Bay (southern Spain) in response to different environmental conditions is investigated. There is a clear difference in community composition between external and internal areas of the bay, with an important group of species present in only one of the areas (e.g., in outer areas crustaceans such as Tanais dulongii or Amphilochus neapolitanus or the polychaete Nicolea venustula; and species from inner areas such as the crustacean Jassa marmorata and the mollusc Alvania montagui or Rissoa similis). The external zone shows high hydrodynamics and low sedimentation rates, whereas in the internal one, there is a high sedimentation rate (as a result of two main rivers, a less strong current regime, and the presence of urban and industrial wastes). The conditions prevailing in the internal zone of the bay are unfavourable for most of the epifaunal species in the external bay areas.

Introduction of waters from the Atlantic and Mediterranean seas, reduce the possible negative effects. Algeciras Bay (southern Spain) located in the Strait Such has been demonstrated previously by our re- of Gibraltar, provides a non-uniform medium with di- search team in the distribution of particular zoological verse environmental conditions that should give rise to groups such as sponges and ascidians; certain condi- differing composition of the benthic communities. It is tions (e.g., lesser regimen of currents, urban and indus- a submarine canyon of pronounced bathymetry (with trial effluents, river mouth, ...) were found to be more depths of more than 500 m) and includes a narrow restricting for growth of the organisms towards the in- platform limited by the 30-m contour, with a width terior of the bay (Carballo et al., 1994, 1996; Naranjo not exceeding 2 km. Its coast (30 km in perimeter et al., 1996). However, in these cases, quantification and 8 km wide at the mouth) houses an important in- is complicated, above all for colonial organisms. This, dustrial complex, including petrochemical companies, together with the problems derived from a great spatial two power stations, iron and steel works, paper mills, non-uniformity, makes comparisons between rocky ar- etc., together with a busy port whose seawalls, piers eas difficult. Other studies carried out by us on the and fills cause alterations in the natural currents, with, communities of the sediment and the epiphytes of the in some cases, a low water renovation rate. This is Bryozoan Bugula neritina have enabled us to evalu- worsened by the lack of urban sewage treatment and ate the environmental state of some of the bottoms a considerable load of nutrients and sediments from (Conradi et al., 1997; Estacio et al., 1997). The study the rivers – due to increasing agricultural activity and of the structure of animal communities associated to the effect of erosion. Nevertheless, its great water macroalgae of wide spatial distribution, relatively easy mass and intense hydrologic regimen, with circulation to collect and quantify, could reveal the effect of the 356 different environmental characteristics throughout the The samples were sieved through a 0.5-mm mesh. bay. The different species were separated, classified, and In order to discover the effect of environmental quantified. The vagile epifauna was selected, although factors on the epifauna of macroalgae, the variations solitary sessile organisms such as polychaetes and caused by the algal configuration must be elimi- bivalves were also included. The remaining sessile an- nated. Thus, we selected a single algal species of imals were discarded, in particular the colonial ones, high environmental versatility, and assumed that the because they were impossible to quantify, at least at a intraspecific variations produced in the alga by the level different to that of the vagile organisms. different environmental conditions will be less than The data of abundance were expressed as number between different substrates. The macroalga selected of individuals per 100 g (dry weight) of alga. was Halopteris scoparia (L.) Sauvageau (Phaeophyta, A series of parameters was calculated for each al- Sphacelariales). This species is erect and flexible, gal specimen: maximum height, diameter, volume, perennial, and can be found from the midlittoral, in and dry and fresh weight. Volume was estimated by intertidal pools, to the infralittoral, especially on rocks displacement of water in test-tube. The theoretical vol- of sandy bottoms. It is common in the whole area of ume (‘canopy volume’) was calculated assuming that, Algeciras Bay, and is one of the most abundant algal in the environment, H. scoparia adopts a geometric species throughout the year. Its physical characteris- form akin to a parabola. Deducting the real volume tics (dense ramification, large number of interstices, from the theoretical one gives the interstitial volume, ...) make it a suitable alga for supporting an interesting which represents the space useful for organisms. Fur- epiphyte community (Sánchez-Moyano, 1996). thermore, the ratio between the theoretical and real volumes gives an idea of the level of compactness of the alga (compactness index) (Sánchez-Moyano, Materials and methods 1996; Sánchez-Moyano & García-Gómez, 1998). This compactness can be considered a measurement of Thirteen stations were selected, grouped in five areas habitat complexity. along the coast of Algeciras Bay in order to encom- Species richness and Shannon–Wiener diversity pass the greatest range of environmental conditions (loge) were calculated from the data of species abun- (Figure 1). The Isla de las Palomas (IP), located at the dance. western lip of the bay, is a photophil rock zone. Punta The following environmental variables were con- de San García (SG) has similar characteristics to the sidered: maximum and minimum temperature, hydro- former, although with a sciophilous environment at dynamics, sedimentation rate, % of organic matter lesser depth. In both areas, stations were established of the sediment, and solids and % of organic mat- along a transect (200 m long) and at 5, 8, and 10 m ter in suspension. Sampling was carried out monthly in depth. The Cucareo inlet (CU), close to the port from November 1992 to November 1993 from con- of Algeciras, is a wide platform between 3 and 5 m crete structures sunk throughout the bay between 5 and in depth; its three stations were located on a transect 10 m in depth (Figure 1: sites S1 to S9). 200 m long. Los Rocadillos (Guadarranque) (GU) is Water movement was estimated using the ‘plas- in the internal zone of the bay, close to the mouth ter dissolution’ method modified by Gambi et al. of the River Guadarranque on a strip of natural rock (1989) with six replicates and an exposure time of running along the coast between 3 and 5 m in depth. 48 hours. Hydrodynamics is expressed as ‘equiva- Two stations were set up at different distances from lent water speed’ (V). The sedimentation rate was the mouth: GU1 (the further) and GU2. Crinavis (CR), measured using sediment traps (six 1-l bottles) which also located in the internal zone, is a disused shipyard. were removed monthly. The data are expressed as The two stations were situated at 5 m in depth. kg/m2/month. Part of the sediment was used to calcu- Four samples were taken at each station in five late the percentage of organic matter by combustion samplings during the year (September 92, Decem- at 500 ◦C. Solids and organic matter in suspension ber 92, March 93, June 93, and September 93). Each were determined by the method of Strickland & Par- sample consisted of one algal specimen, which was son (1969). The median was employed for statisti- bagged in situ and extracted from the substrate by cal analysis and to show the annual trend for each SCUBA diving. variable. 357

Figure 1. Location of the sampling stations in Algeciras Bay. IP: Las Palomas Island; SG: San Garc´ıa Point; CU: Cucareo inlet; GU: Guadarranque; CR: Crinavis; S1 to S9: physical data sites.

The space and time differences in diversity, species in grouping of the different stations. This analysis, richness, total abundance, and environmental variables based on the matrix of similarity in species abundance were analyzed by one-way ANOVA, after verifying obtained from the Bray–Curtis index, calculates the normality (Kolmogorov–Smirnov test) and uniformity contribution of each species to either the dissimilarity of variances (Barlett test). Homogenous groups were between groups of stations (discriminatory species) or separatedbyaTukeytest. the similarity within a group (typifying species). Affinities between stations were established using an MDS (non-metric multidimensional scaling) analysis with the annual average species abundance Results (transformed by the fourth root). Canonical correspondence analysis (CCA) was ap- Environmental variables plied to determine whether the environmental variables affected community composition, and to estab- Most of the physical data of the sites were selected lish affinities between stations. This technique is one to show the general variability of these parameters of direct gradient, where the resulting ranking is di- throughout the bay, although, on the other hand, some rectly related with the values of the environmental were selected as representative areas of the sites where factors (Ter Braak, 1986). The statistical significance biological data were collected (Figure 1). of the analysis was verified applying the Monte Carlo Spatial variations were tested using one-way test for the first axis. ANOVA and Figure 2 shows the trends of the differ- Percentage of similarity analysis (SIMPER) (Clarke, ent environmental variables through the bay. It can 1993) was used to determine the species involved be observed that hydrodynamics is high in the more 358

Table 1. Contribution of the main taxonomic groups in the sampling stations according to the average annual abundance (No. indiv/100 g dry weight of alga)

IP1 IP2 IP3 SG1 SG2 SG3 CU1 CU2 CU3 GU1 GU2 CR1 CR3

Miscellaneous 332.4 453.6 608.7 582.1 645.3 567.3 421.8 276.4 257.8 367.4 213.1 358.8 446.0 Mollusca Bivalvia 168.7 163.8 313.6 252.8 337.6 437.2 187.1 150.3 289.1 2159.8 1667.4 547.6 213.0 Prosobranchia 3735.4 3949.6 4400.7 1503.3 2282.9 2344.0 3657.8 3640.2 2869.5 9599.4 4581.0 2883.3 5001.3 Opistobranchia 288.8 475.6 558.3 607.5 843.1 631.6 329.4 342.2 338.3 798.8 483.1 562.1 458.2 Annelida Polychaeta 8747.6 9099.4 12200.0 8143.0 11573.3 8073.9 12512.9 12572.9 11889.7 11257.7 7031.9 13952.0 9346.5 Hirudinea 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 5.2 Oligochaeta 48.1 6.1 6.8 0.0 0.0 0.0 19.1 6.6 3.9 1.6 7.0 0.0 0.0 Arthropoda Pantopoda 166.3 151.9 321.2 458.4 510.7 714.6 226.0 305.9 238.0 712.3 471.5 497.9 286.1 Amphipoda 6687.1 6144.3 8185.7 8875.9 8662.9 12972.8 9501.2 19086.4 9641.4 16649.8 21531.0 17008.9 19438.6 Cumacea 205.4 279.0 313.7 196.6 429.8 312.3 172.1 101.8 137.0 1364.4 659.7 269.7 287.6 Decapoda 46.0 82.2 29.7 169.9 161.2 139.5 166.0 50.5 47.8 77.5 60.9 130.0 404.0 Isopoda 435.2 342.2 504.4 590.8 550.6 494.6 664.4 804.6 524.4 499.2 73.2 588.2 694.0 Leptostraca 0.0 0.0 0.0 0.0 0.0 10.4 0.0 0.0 0.0 0.0 0.0 0.0 0.0 Mysidacea 19.7 5.3 6.9 2.6 23.6 0.0 1.6 5.4 1.7 0.0 0.0 7.1 0.0 Tanaidacea 1245.9 847.4 1462.0 3042.8 3003.9 3236.1 1843.0 2181.1 2392.7 2075.8 1994.7 1381.7 797.7 Insecta 36.2 27.9 30.8 41.1 24.7 18.5 1.8 2.0 3.6 8.8 0.0 2.0 3.4 Echinodermata 199.1 272.6 605.8 157.5 539.6 350.3 173.7 58.0 125.0 34.9 84.4 156.2 48.6

external zones, diminishes towards the interior, and The solids in suspension also tend to increase to- rises to a new peak in the Crinavis area (points 9 and wards the interior, affected by the presence of the two 10). The main cause lies in the tidal current regime of rivers and the proximity to urban effluents. This case the bay. These currents originated by the circulation of is not statistically significant. masses of Atlantic and Mediterranean waters through The structural characteristics of the algae (Fig- the Strait of Gibraltar, are eastward or westward with ure 3) show greater interstitial volume and com- the flood- or ebb-tide (Camiñas, 1987). During flood- pactness in the more external zones, with a grad- tide, a branch of the general current of the Strait flows ual decrease towards the interior, particularly marked in behind during the Isla de las Palomas, bathes the in the Guadarranque area. The interstitial volume whole coastline of the bay, and exits via Gibraltar; increases during winter and decreases during the during ebb-tide, two parallel branches are set up, one warmest months. flowing along each side of the bay, and converging in the Crinavis area. Hydrodinamism shows significant Faunistic analysis differences (F = 29.6, P<0.001, degrees of freedom = 9). The 13 studied stations provided a total of 309 taxa of The behaviour of the sedimentation rate (F = 171,9; which 99 were molluscs, 82 polychaetes, 100 crus- P<0.001, degrees of freedom = 9) is slightly inverse: taceans, 6 pantopods, 1 insect, 6 echinoderms, and the rate is higher in the internal zones, especially 15 belonging to other groups. Table 1 summarizes those located in the areas of influence of the Rivers the contribution of the main taxonomic groups in the Palmones (point 6) and Guadarranque (point 7). At different zones according to annual mean abundance. Cucareo (point 4), there is a great resuspension of the Figure 4 shows the spatial changes for the substrate, together with sedimentation due to the shal- Shannon–Wiener diversity index, species richness, low depth and the effect of waves lifted by the strong and total number of individuals of the epifaunal east winds prevailing throughout the zone. species. In general, there is a slight behavioural trend of these parameters from the stations of the more ex- 359

Hydrodynamism (v) Sedimentation rate (kg/m2/month)

Sedimentation rate (kg/m2/month): S6 excluded % 0rganic matter of sedimentation

Solids in suspension (mg/l) Organic matter in suspension (mg/l)

Figure 2. Variation of the environmental parameters in the stations. The thick line corresponds to the median; the rectangles contain 50% of the values, between 1st and 3rd quartile; the thin lines connect the extreme values, unless located at a distance superior to 3 times the height of the rectangle than they are indicated by an asterisk. ternal zones (Isla de las Palomas, San García and zone. Species richness is high at all the stations, and Cucareo) to the more internal ones (Guadarranque and does not show dependence of the spatial gradient in the Crinavis). bay. The number of species is maximum (189) at CR1 Thus, diversity tends to decrease slightly from I1 and minimum (157) at SG3. The total number of in- to CR3, although the index values are generally high dividuals (abundance) increases progressively towards in the whole bay (with a maximum and minimum the interior. of 3.81 and 3.29, respectively). The Cucareo area, The spatial and seasonal variations for these para- despite being located geographically in the external meters were tested using one-way ANOVA (degrees zone, presents values closer to those of the internal of freedom 12 and 4, respectively). Diversity shows 360

140 Compactness index Richness, as observed in Figure 4, shows no spatial

120 differences (F = 1.60; P<0.001), although seasonally, the winter months are separated from the rest, 100 as in the case of diversity (F = 31.58; P<0.001). Fi- 80 nally, the number of individuals presents differences = 60 at both levels (sites: F 6.32, P<0.001; period: F = 2.69, P<0.001). Spatially, the external stations (I1, 40 I2, I3, S1, S2, S3, C1 and C3) and internal ones (G1, 20 G2, CR1 and CR3) are separated as uniform groups.

0 However, station C2 (Cucareo) resembles the internal IP1 IP2 IP3 SG1 SG2 SG3 CU1 CU2 CU3 GU1 GU2 CR1 CR3 stations. The seasonal differences are based on the samples of different years (1992 and 1993). Interstitial volume (ml) 1000 Multivariate analysis

800 With the MDS analysis (Figure 5) we obtain a clear

600 separation between the stations located at the external zones of the bay (Isla de las Palomas, San García, and 400 Cucareo) and those situated close to the internal zone (Guadarranque and Crinavis), although in this zone the 200 separation between both areas is more noticeable. Figure 6 shows the station ranking obtained by 0 IP1 IP2 IP3 SG1 SG2 SG3 CU1 CU2 CU3 GU1 GU2 CR1 CR3 CCA for the first two axes (only carried out with Figure 3. Spatial variations of the interstitial volume and com- stations where environmental data were collected), re- pactness index of Halopteris scoparia specimens during the study vealing the existence of two groups of stations: those period. situated in the more external zones (areas of Isla de Table 2. Results of the canonical correspondence las Palomas, San García, and Cucareo) and those in analysis the more internal ones (Guadarranque and Crinavis). As detailed in Table 2, the first axis is related with the Intraset values compactness index and the organic matter of the sedi- Axis 1 Axix 2 ment, while the second axis is correlated preferentially with hydrodynamics and solids in suspension. The SEM 0.524 0.163 location of the stations with respect to each arrow rep- − SUS 0.219 0.900 resents the prevailing environmental characteristics. SUM 0.154 −0.038 Thus, Figure 6 displays a gradient from the external HYD 0.145 0.671 stations (IP, SG and CU) to the internal ones (GU and CI 0.967 0.061 Species-environment correl 0.991 0.989 CR) marked by the first axis. One of the factors appar- Cumulative % variance 35.9 49.7 ently most important in discriminating the two zones of species data is the morphological characteristics of the plants, rep- resented by the compactness index. Hydrodynamics discriminates the rest of the stations of CR3, zone of convergence and entrance of tidal currents in the Strait of Gibraltar. The Monte Carlo test was significant for significant differences both spatially and seasonally (F < = the first axis (P 0.03). 7.32 and 7.66, respectively, P<0.001). Because of The percentage of similarity analysis (SIMPER) the high values recorded throughout the zone, no uni- applied for the group of external stations shows that form spatial groups are clearly distinguishable. Sea- the species typifying this area are the polychaetes sonally, the winter months (December 92 and March Amphiglena mediterranea and Syllis prolifera,the 93) are well differentiated, with a fall in the values amphipod crustaceans Stenothoe monoculoides and for the summer-autumn months (September 92 and 93 Amphilochus neapolitanus, and the isopod crustacean and June 93), when the populations tend to recover. Paranthura nigropunctata (Table 3). For the internal 361

Table 3. Average abundance (Av. Abund.) of the most relevant species of the stations located in the external areas (Las Palomas Island, San Garc´ıa and Cucareo). Species are listed in decreasing order according to its contribution to the average of the similarity (Av. Sim.) between the stations until 40% of the accumulated total similarity. The total 0 mean similarity between the stations is 65 62%. Group keys: A, amphipods; I, isopods; M, molluscs; P, polychaetes; T, tanaids

Species Group Av. abund. Av.sim. Ratio Sim.%

Nicolea venustula P 2598.34 2.0 5.31 3.02 Amphiglena mediterranea P 2202.34 1.9 7.48 2.87 Syllis prolifera P 1023.14 1.7 7.16 2.57 Rissoella opalina M 2064.12 1.6 3.16 2.45 Stenothoe monoculoides A 902.20 1.5 6.24 2.32 Sphaerosyllis histrix P 827.94 1.5 5.54 2.31 Platynereis dumerilii P 1146.48 1.5 4.97 2.23 Leptochelia dubia T 1221.61 1.5 2.94 2.21 Pseudobrania clavata P 656.58 1.4 5.41 2.20 Corophium acutum A 1635.17 1.4 2.24 2.14 Oriopsis armandi P 748.89 1.4 4.84 2.10 Gammaropsis palmata A 1290.10 1.4 2.79 2.08 Paranthura nigropunctata I 377.85 1.3 8.28 2.03 Aoridae sp A 1045.27 1.3 4.01 1.93 Apherusa bispinosa A 491.88 1.3 5.70 1.92 Tanais dulongii T 832.42 1.2 3.02 1.87 Amphilochus neapolitanus A 286.53 1.2 6.76 1.81 Ampithoe ramondi A 599.71 1.2 3.50 1.78 Microprotopus sp A 267.70 1.1 5.16 1.73

stations, only the polychaetes Platynereis dumerilii take into account the identity of the species involved and Sphaerosyllis pirifera are of note (Table 4). When (Warwick & Clarke, 1991). the analysis was applied to detect the species con- The existence of two types of stations (external tributing most to the dissimilarity between the two and internal) based on the composition and abundance groups of stations, the outstanding organisms were the of their species, and the maintenance without sig- polychaetes Nicolea venustula and Micromaldane or- niﬁcant differences of parameters such as diversity nitochaeta, the amphipod crustaceans Hyale schmidti, and species richness (the former falls slightly, but Microprotopus sp and Amphilochus neapolitanus,the values are generally high), indicate a predominance tanaid crustacean Tanais dulongii, and the gastropod of the phenomenon of species substitution. That is, mollusc Rissoa similis (Table 5). rather than a gradient of spatial impoverishment of the medium, there appear to be different communities adapted to given environmental conditions. Discussion The two great areas show differing behaviour in several of the environmental factors measured. In the The general impression is that there is a marked external zone, prevailing conditions are high hydrody- difference between the composition of the epifaunal namics, low sedimentation rate, and high percentage communities of the areas deﬁned as external and in- of organic matter in the sediment (although lower in ternal. Diversity tends to decrease towards the interior, absolute values than for the internal zone). The inter- while the total number of individuals increases. How- nal zone presents high sedimentation rate and higher ever, these differences between areas are not shown so values for organic matter. However, hydrodynamics is clearly by the univariate analysis as by the multivariate low in Guadarranque and high in Crinavis – the two ones, among other reasons because the former do not branches of tidal currents in the Strait converge in the 362

Table 4. Average abundance (Av. Abund.) of the most relevant species of the stations located in the internal areas (Guadarranque and Crinavis). Species are listed in decreasing order according to its contribution to the average of the similarity (Av. Sim.) between the stations until 40% of the accumulated total similarity.The total mean sim- 0 ilarity between the stations is 60 56%. Group keys: A, amphipods; M, molluscs; P, polychaetes; PT, pantopods; T, tanaids

Species Group Av. abund. Av.sim. Ratio Sim.%

Platynereis dumerilii P 2169.26 2.0 6.62 3.23 Corophium acutum A 4399.16 1.9 2.57 3.19 Sphaerosyllis histrix P 2376.81 1.9 4.26 3.14 Amphiglena mediterranea P 2787.90 1.7 3.26 2.74 Aoridae sp A 1832.83 1.6 2.62 2.65 Stenothoe monoculoides A 1539.70 1.4 3.12 2.37 Leptochelia dubia T 850.84 1.4 3.93 2.32 Bittium reticulatum M 1286.45 1.4 3.02 2.29 Gammaropsis maculata A 960.40 1.3 2.31 2.20 Oriopsis armandi P 873.69 1.3 2.48 2.14 Pseudobrania clavata P 329.49 1.2 4.93 2.05 Sphaerosyllis pirifera P 330.26 1.2 6.05 2.01 Jassa marmorata A 3130.60 1.2 1.46 2.01 Achelia sp PT 362.15 1.2 4.27 1.98 Phtisica marina A 1499.46 1.2 1.64 1.98 Ceratonereis costae P 431.55 1.2 4.37 1.96 Musculus costulatus M 395.51 1.1 3.73 1.90

latter (Camiñas, 1987). This is demonstrated by the garding its possible effect on the fauna is its quality CCA grouping, in which the external stations appear – that is, granulometric composition and percentage closer one to another than the internal ones due es- of organic matter. Coarse sediment tends to increase pecially to the different hydrodynamic characteristics the density and diversity of the epifauna by increas- resulting from tidal currents. Even between the two ing habitat diversity and stimulating colonization by stations of Crinavis, despite their closeness (approx- psammolittoral species (Hicks, 1980). In contrast, a imately 200 m), differences are clear. Station CR3 fine sediment reduces diversity and abundance by col- receives the tidal current more directly, whereas at lapsing interfrond spaces and by interfering in the CR1, hydrodynamics is practically only the exposure alimentary structures of the fauna (Dahl, 1948; Hicks, to wave action. 1980). An increase in the amount of detritus (organic Of all the physical parameters studied, those con- matter) usually promotes diversity, or at least density sidered best in determining faunal composition are of individuals, possibly by increasing the number of hydrodynamics (Dommasnes, 1968; Moore, 1972; detritivores (Southgate, 1982). Fretter & Manly, 1977; Grahame & Hanna, 1989; In any case, hydrodynamics determines the amount Dodds, 1991) and sedimentation rate (Dahl, 1948; and physical characteristics (above all granulometry) Hagerman, 1966; Hicks, 1980; Gibbons, 1988). Their of sediment accumulating. With strong currents or joint action is decisive in the establishment of partic- heavy wave action, fine material cannot be deposited ular species. However, in our case, sedimentation rate on the algae, and only coarse material accumulates, has not been detected as having a conclusive effect. whereas with weak currents or in areas sheltered from Another important factor is the percentage of or- wave action, the finest particles (organic matter and ganic matter in the sediment. This parameter, and silt-clays) adhere to the algae and may cover the epi- secondarily the solids in suspension, can be consid- fauna (Gibbons, 1988). In zones such as Isla de las ered a consequence of sedimentation rate. In fact, one Palomas, with high hydrodynamics prevailing, the al- of the most important aspects of sedimentation re- gae have practically no fine material on them except 363

Table 5. Average abundance of the most relevant species of the stations located in the internal (B) and external areas (A).Species are listed in decreasing order according to its contribution to the average of the dissimilarity (Av. Dis.) between the two groups until 30% of the accumulated total dissimilarity. The 0 total average dissimilarity between the stations is 50 20%. Group keys: A, amphipods; M, molluscs; P, polychaetes; T, tanaids

Species Group B A Av.dis. Ratio Av.dis.%

Nicolea venustula P 0.00 2598.34 1.13 4.55 2.24 Jassa marmorata A 3130.60 3.93 0.89 1.62 1.78 Tanais dulongii T 4.95 832.42 0.71 2.40 1.42 Hyale schmidti A 1.01 467.63 0.67 2.90 1.34 Apherusa sp A 3.05 1099.27 0.66 1.42 1.32 Amphilochus neapolitanus A 0.00 286.53 0.66 5.81 1.31 Eatonina fulgida M 1.42 609.79 0.60 1.79 1.19 Ampithoe ramondi A 34.82 599.71 0.59 1.85 1.17 Microprotopus sp A 2.16 267.70 0.58 3.18 1.16 Gammaropsis palmata A 2237.79 1290.10 0.58 1.44 1.15 Bittium reticulatum M 1286.45 94.30 0.53 1.56 1.06 Rissoella opalina M 1088.28 2064.12 0.52 1.42 1.04 Rissoa similis M 264.17 0.00 0.51 2.00 1.02 Corophium acutum A 4399.16 1635.17 0.50 1.51 0.99 Caprella acanthifera A 54.87 426.28 0.49 1.64 0.97 Apherusa bispinosa A 44.68 491.88 0.48 1.70 0.96 Ericthonius brasiliensis A 928.97 1.96 0.46 0.97 0.92 Alvania montagui M 334.11 0.00 0.44 1.22 0.87 Rissoa guerini M 391.69 20.08 0.42 1.74 0.84 Phtisica marina A 1499.46 527.53 0.42 1.44 0.83 Gammaropsis maculata A 960.40 390.49 0.41 1.43 0.82 Modiolula phaseolina M 294.40 3.60 0.41 1.28 0.81 Zeuxo normani T 168.97 0.00 0.39 1.31 0.78 Aora spinicornis A 665.76 186.58 0.39 1.29 0.78 Jujubinus ruscurianus M 337.97 26.25 0.39 1.20 0.77 Guernea coalita A 0.00 133.67 0.38 1.33 0.77 Cingula pulcherrima M 308.48 18.85 0.38 1.36 0.76 Micromaldane ornitochaeta P 0.74 58.92 0.38 2.22 0.75 Aoridae sp A 1832.83 1045.27 0.37 1.46 0.74

immediately after storms (very frequent in the zone), Some authors indicate that an increased turbulence when they present a certain amount of coarse sand. In in the medium implies an epifauna less diverse and contrast, in zones such as Guadarranque, with little less abundant (Hagerman, 1966). Tararam and Wak- hydrodynamics (even wave action is low at this point, abara (1981), in a study of the epifauna associated to which is sheltered from the prevailing east wind) and Sargassum in Brazil, found no relationship between a high sedimentation rate (due to the closeness of the the different levels of exposure and the diversity, al- river mouth), the algae are totally covered with ﬁne though density increased in sheltered zones. Our data material. In areas such as Cucareo and Crinavis, the show that in zones of greater hydrodynamics (Isla de algae grow on a wide sandy platform, and normally las Palomas or San García, for example), however, appear with a great amount of coarse sand, enabling the diversity index is higher and the abundance of the arrival of species such as the gammarid Ampelisca organisms lower. In the internal zones (particularly unidentata from adjacent sandy bottoms. Guadarranque), the density of individuals is notably higher and diversity lower. 364

3.5 DIVERSITY SPECIES RICHNESS 8

3.3 7

3.1 6

2.9 5

2.7 4

2.5 3 I1 I2 I3S1 S2 S3 C1 C2 C3 G1 G2 CR1 CR3 I1 I2 I3S1 S2 S3 C1 C2 C3 G1 G2 CR1 CR3

60 ABUNDANCE (X 1000)

0 I1 I2 I3S1 S2 S3 C1 C2 C3 G1 G2 CR1CR3 Figure 4. Spatial variations of the diversity, species richness and total abundance. Vertical bars show standard deviation.

Without doubt, the possible effects of all these fac- drodynamics alters algal size (Boaden et al., 1975; tors on the community composition are determined Dommasnes, 1968); seasonal cycles of H. scoparia ultimately by the physical structure of the substrate. mean the partial loss of fronds during the winter The structural complexity of a habitat affects the abun- months; more light leads to a greater growth of epi- dance, diversity, and distribution of its associated phyte algae – a food source contribution to greater fauna (Edgar, 1983; Stoner & Lewis, 1985; Dean & structural complexity of the environment (Hall & Bell, Connell, 1987; Russo, 1989, etc.). An increase in habi- 1988; Schneider & Mann, 1991; Martin-Smith, 1993), tat complexity means an increase in food resources, a etc. higher number of microhabitats, an increased capac- H. scoparia is a much-ramiﬁed alga. Its intersti- ity of shelter from predators and from the mechanical tial volume is moderate with very small spaces. This effect of hydrodynamics, among other aspects. means, according to Hacker and Steneck (1990), that The choice of a single substrate, such as Halopteris the abundance of individuals is high, because of the scoparia, for spatio-temporal comparisons of the com- large availability of microhabitats, and it is a good munity minimizes structural variability. However, the trap for sediment and epiphytes, but that the size of same environmental parameters affect the structure the organisms is restricted. and distribution of the algal population: strong hy- 365

rect measurement of the vital space, considering both the surface of the fronds and the space between them; while compactness can give an approximate idea of the size of these interfrond spaces, which are smaller the closer the index is to unity (a hypothetical value that would mean that the alga occupies the whole space). SG3 CR3 In the external zone, the possible effect of the SG2 physical component of the alga is demonstrated by an CR1 IP3 SG1 increase in diversity, but not in the density of individ- IP2 uals (perhaps density is controlled more by a factor IP1 CU2 CU3 GU1 such as hydrodynamics). In the internal zone, there is CU1 a higher number of individuals. Here, the high sedi- GU2 mentation rate should favour this increase, especially of trophic groups such as the detritivores (Southgate, 1982). In fact, the most abundant species are detritivores, such as the crustaceans Jassa marmorata, Ischyrocerus inexpectatus and Corophium acutum,the molluscs Alvania montagui and various species of Figure 5. MDS ordination of the stations according to the annual the genus Rissoa, and the polychaete Sphaerosyllis average of abundance (Stress: 0.03). pirifera. One of the most noteworthy fact is the existence CR3 of a considerable group of species present in one area of the bay but absent from, or with an in- significant presence in the other zone. These species are, apriori, those determining the differences of HYD the various communities. It seems obvious that there is an exclusive character preventing many external species penetrating the bay, although most ‘internal’ SEM CR1 SG species can also be found outside. Various exam- CI ples have been reported, especially with crustaceans SUM IP3 such as Tanais dulongii or Amphilochus neapolitanus SG3 CU IP (Sánchez-Moyano & García-Gómez, 1998) and mol- GU1 luscs such as Eatonina fulgida or Cingula amabilis (Sánchez-Moyano et al., 2000), all of them in outer GU2 areas. Nevertheless, most of the polychaete species are SUS spread uniformly throughout the stations, except for Figure 6. Graph representation of the stations and species with re- some species such as the terebellid Nicolea venustula spect to the first two axes of the canonical correspondence analysis (it is very abundant in the external area and not found (CCA). HYD: hydrodynamics; SUS: solid in suspension; SUM: organic matter in suspension; SEM: organic matter of the sedimen- in the interior). tation; CI: compactness. Conradi et al. (1997) indicates that the external stations are more non-uniform and more subject to changes in environmental conditions, in particu- Canonical correspondence analysis (CCA) con- lar those referring to the wind. This greater non- firms that the morphological characteristics of the uniformity may be the cause of the higher diversity plants are one of the factors most affecting epifaunal in this zone, although there must be environmental composition. The structural and spatial component of conditioning agents preventing access to the internal each alga is expressed by the interstitial volume and zone. the ratio between the theoretical volume occupied by In conclusion, the prevailing conditions in the the plant in the medium and the frond volume (com- internal zone of the bay are, in principle, more un- pactness index). These parameters are highly related favourable for most of the external species, hindering = (r 0.75; P<0.001). The interstitial volume is a di- their establishment and determining the differences 366 in the final composition of the epiphyte community. Fretter V and Manly R (1977) Algal associations of Tricolia pullus, These conditions are imposed, above all, by the effect Lacuna vincta and Cerithiopsis tubercularis (Gastropoda) with of the two main rivers flowing into the bay (Palmones special reference to the settlement of their larvae. J Mar Biol Ass UK 57: 999–1017 and Guadarranque), the closeness of effluents – both Gambi MC, Buia MC, Casola E and Scardi M (1989) Estimates of urban and industrial – that are discharged in the area, water movement in Posidonia oceanica beds: a first approach. and, in some measure, a less strong regime of currents. Int Workshop Posidonia Beds 2: 101–112 Gibbons MJ (1988) The impact of sediment accumulations, relative habitat complexity and elevation on rocky shore meiofauna. J Exp Mar Biol Ecol 122: 225–241 Acknowledgements Grahame J and Hanna FS (1989) Factors affecting the distribution of the epiphytic fauna of Corallina officinalis (L.) on an exposed Appreciation to CEPSA (Compañía Española de rocky shore. Ophelia 30 (2): 113–129 Hacker SD and Steneck RS (1990) Habitat architecture and the Petróleos, S.A.), Sevillana de Electricidad, Excmo. abundance and body-size-dependent habitat selection of a phytal Ayuntamiento de los Barrios, Mancomunidad de Mu- amphipod. Ecology 71 (6): 2269–2285 nicipios del Campo de Gibraltar for financial support Hagerman L (1966) The macro- and microfauna associated with of this work. Fucus serratus L. with some ecological remarks. Ophelia 3: 1–43 Hall MO and Bell SS (1988) Response of small motile epifauna to complexity of epiphytic algae on seagrass blades. J Mar Res 46: 613–630 References Hicks GR (1980) Structure of phytal harpacticoid copepod assem- blages and the influence of habitat complexity and turbidity. J Boaden PJS, O’Connor RJ and Seed R (1975) The composition and Exp Mar Biol Ecol 44: 157–192 zonation of a Fucus serratus community in Strangford Lough, Martin-Smith KM (1993) Abundance of mobile epifauna: the role Co. Down. J Exp Mar Biol Ecol 17: 111–136 of habitat complexity and predation by fishes. J Exp Mar Biol Camiñas JA (1987) La Bahía de Algeciras: Características Ecol 174: 243–260 oceanográficas y biológicas. Contaminación y áreas de protec- Moore PG (1972) Particulate matter in the sublittoral zone of an ex- ción. Delegación de Ecología y Medio Ambiente, Ayuntamiento posed coast and its ecological significance with special reference Algeciras, 34 pp to the fauna inhabiting kelp holdfasts. J Exp Mar Biol Ecol 10: Carballo JL, Sánchez-Moyano JE and García-Gómez JC (1994) 59–80 Taxonomic and ecological remarks on boring sponges (Clion- Naranjo SA, Carballo JL and García-Gómez JC (1996) Effects of idae) from the Straits of Gibraltar (southern Spain): tentative environmental stress on ascidian populations in Algeciras Bay bioindicators? Zool J Linnean Soc 112: 407–424 (southern Spain). Possible marine bioindicators? Mar Ecol Prog Carballo JL, Naranjo SA and García-Gómez JC (1996) Use of Ser 144: 119–131 marine sponges as stress indicators in marine ecosystems at Al- Russo AR (1989) Fluctuations of epiphytal gammaridean am- geciras Bay (southern Iberian Peninsula). Mar Ecol Prog Ser 135: phipods and their seaweed hosts on an hawaiian algal reef. 109–122 Crustaceana 57 (1): 25–37 Clarke KR (1993) Non-parametric multivariate analyses of changes Sánchez-Moyano JE (1996) Variación espacio-temporal en la com- in community structure. Aust J Ecol 18: 117–143 posición de las comunidades animales asociadas a macroalgas Conradi M, López-González PJ and García-Gómez JC (1997) The como respuestas a cambios en el medio. Implicaciones en la amphipod community as a bioindicator in Algeciras Bay (South- caracterización ambiental de las áreas costeras. Doctoral Thesis, ern Iberian Peninsula) based on a spatio-temporal distribution. Univ. Sevilla, 407 pp P.S.Z.N.I.: Mar Ecol 18 (2): 97–111 Sánchez-Moyano JE and García-Gómez JC (1998) The arthropod Dahl E (1948) On the smaller Arthropoda of marine algae, espe- community, especially Crustacea, as a bioindicator in Algeciras cially in the polyhaline waters off the Swedish west coast. Diss Bay (Southern Spain) based on a spatial distribution. J Coast Res Lund (Undersökn över Öresund 35), 193 pp 14 (3): 1119–1133 Dean RL and Connell JH (1987) Marine invertebrates in an al- Sánchez-Moyano JE, Estacio FJ, García-Adiego EM and García- gal succession. III. Mechanisms linking habitat complexity and Gómez JC (2000) The molluscan epifauna of the alga Halopteris diversity. J Exp Mar Biol Ecol 109: 249–273 scoparia in Southern Spain as a bioindicator of coastal environ- Dodds WK (1991) Community interactions between the filamen- mental conditions. J Mollus Stud 66: 431–448 tous alga Cladophora glomerata (L.) Kuetzing, its epiphytes, and Schneider FI and Mann KH (1991) Species specific relationships epiphyte grazers. Oecologia 85: 572–580 of invertebrates to vegetation in a seagrass bed. II. Experiments Dommasnes A (1968) Variations in the meiofauna of Corallina on the importance of macrophyte shape, epiphyte cover and officinalis L. with wave exposure. Sarsia 34: 117–124 predation. J Exp Mar Biol Ecol 145: 119–139 Edgar GJ (1983) The ecology of south-east Tasmanian phytal Southgate T (1982) The biology of Barleeia unifasciata (Gas- animal communities. IV. Factors affecting the distribution of tropoda: Prosobranchia) in red algal turfs in S.W. Ireland. J Mar amphitoid amphipods among algae. J Exp Mar Biol Ecol 70: Biol Ass UK 62: 461–468 205–225 Stoner AW and Lewis FG (1985) The influence of quantitative Estacio FJ, García-Adiego EM, Fa DA, García-Gómez JC, Daza JL, and qualitative aspects of habitat complexity in tropical seagrass Hortas F and Gómez-Ariza JL (1997) Ecological analysis in a meadows. J Exp Mar Biol Ecol 94: 19–40 polluted area of Algeciras Bay (Southern Spain): external ‘ver- Strickland JDH and Parson TR (1969) A practical handbook of sea sus’ internal outfalls and environmental implications. Mar Poll water analysis. Fish Res Board. Canad Bull 167 Bull 34 (10): 780–793 367

Tararam AS and Wakabara Y (1981) The mobile fauna- especially Warwick RM and Clarke KR (1991) A comparison of some methods gammaridea- of Sargassum cymosum. Mar Ecol Prog Ser 5: 157– for analysing changes in benthic community structure. J Mar Biol 163 Ass UK 71: 225–244 Ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67 (5): 1167–1179