Zonation patterns of benthic communities in an upwelling area from the western Mediterranean ( La Herradura , Alboran Sea ) *

Species composition and distribution of marine benthic communities from La Herradura (Alboran Sea, western Mediterranean) are described to characterise its rocky and sedimentary bottoms bionomically. Rocky bottoms were studied by means of several underwater transects and soft bottoms with fixed stations along a bathymetric gradient. The study of the floristic and faunistic composition of the rocky benthic communities highlights depth as the main axis of variation. Factorial Correspondence Analysis segregates deep-water communities below 25 m depth (circalittoral communities) from shallower communities (axis I), and communities thriving between 5 and 25 m depth (lower infralittoral communities) from communities thriving close to the surface (shallow infralittoral communities) (axis II). The study of the sedimentary bottoms also suggests that depth, together with physical sedimentary properties, is the main axis of variation in species distribution. Floristic and faunistic records show the particular composition of La Herradura benthic communities, compared to Mediterranean and Atlantic ones. Mixing of Mediterranean and Atlantic waters, together with deep water upwelling episodes typical of this area, probably determine the peculiar composition of the benthic communities.


INTRODUCTION
The Alboran Sea is located at the westernmost part of the Mediterranean and has its own physical and biological traits (Gil, 1988).Surface Atlantic waters enter the Mediterranean through the Strait of Gibraltar and reach the Alboran Sea poorly mixed with Mediterranean waters (Cano, 1978).Furthermore, Atlantic waters usually describe an anticyclonic gyre that generates an upwelling of deep waters along the coasts of Málaga and Granada (southern Spain; Lanoix, 1974;Parrilla and Kinder, 1987;Minas et al., 1991;Tintoré et al., 1991).Deep water upwellings are enhanced by the strong western winds that usually blow in this area (Rodríguez, 1990).The combination of all these hydrological features together with the pronounced biogeographical differences between the Atlantic Ocean and the Mediterranean Sea (Conde, 1989;Pérès, 1985;González and Conde, 1993;Maldonado and Uriz, 1995;Cebrian et al. 2000) should affect benthic communities and their zonation patterns.
Although submerged vegetation patterns have been studied in several localities of the Alboran Sea (Giaccone, 1972;González, 1994), species composition of some circalittoral communities has been described (Templado et al., 1986;Templado et al., 1993;Maldonado, 1992Maldonado, , 1993)), and the knowledge of the main invertebrates thriving in its waters is compiled in Ocaña et al. (2000), there are no available data on macroalgae and macrofauna species composition and distribution of communities along depth gradients in shallow (0-50 m) waters, with the exception of two transects described in Cebrian et al. (2000).
In the present study we describe the species composition and the zonation patterns of benthic communities thriving in the rocky and sedimentary bottoms of the village of La Herradura, whose coastal waters are regularly affected by deep water upwellings (Lanoix, 1974;Rodríguez, 1990;Templado et al., 1993), and we compare the structure of the studied communities and their spatial distribution with similar studies performed in other western Mediterranean localities.

MATERIALS AND METHODS
La Herradura (36°44'N, 3°45'W) (Fig. 1), was selected amongst other localities of the southern coast of Spain due to its geographical position in front of an upwelling area, its rather steep sea bottom slopes which are responsible for a high landscape diversity, the presence of deep rocky bottoms close to the coast, and its diving facilities.Sampling was performed with SCUBA diving techniques (Zabala et al., 1982) between 18 June and 6 July 1997.
Sampling stations were selected covering different substrates, ranges of wave exposure and orientation.Identification of communities was performed following a transect perpendicular to the shore at every sampling station.
Transects on rocky bottoms were performed by two divers.In the first stage (descent) the topographic and bathymetric characteristics of the transect were noted, from the surface to the deeper zone (Table 1).Different communities were distinguished along the transect according to the dominant species.In the second stage (ascent) each community was carefully checked for ten minutes and its species composition and abundances were recorded according to a semi-quantitative index (Braun Blanquet, 1979).Qualitative samples of each predefined community were collected for identification of the organisms in the laboratory.
On sedimentary bottoms the sampling was performed at 5 different stations located along a transect situated in the middle of the bay.Dives were performed at depths of 10, 20, 30, 40 and 50 metres and species composition and abundance were recorded for ten minutes, with collection of samples for identification of the organims.Sediment samples were collected using two cores and two dredges (van Veen) at each sampling station.Dredges were obtained by ordinary methods below 50 m depth and characterised qualitatively by their species composition.Cores were of 12.5 cm diameter and 30 cm length.Small superficial sediment subsamples were collected from the core for granulometrical analysis.They were analysed using an LS particle size analyser at the Department of Geology of the University of Barcelona.The grain size distribution of the sediment was performed following Wentworth (1972) classification.
Data obtained from the transects were used to describe them and to draw precise sketches of benthic communities.
A factorial correspondence analysis (Legendre and Legendre, 1979;Ter Braak, 1987) was performed with the samples collected on rocky bottoms to show affinities and differences between samples.Mean percent abundance values obtained from the six rocky transects were used as data entries in a species-station raw matrix.Species present in only one or two samples were not considered in the analysis.Sample 3HO collected in a crevice was also omitted from the analysis due to its very peculiar species composition.The final analysed matrix included 30 points and 84 taxa.Rocky bottoms (Figs. 2, 3) Ordination of samples along the two first axes discriminated by the factorial correspondence analysis shows the presence of three clusters (Fig. 6).The first axis discriminates between samples collected below 25 meters depth and those collected above, whilst the second axis segregates the samples collected above 5 m depth from all the rest.Samples collected between 5 and 25 m depth are in the same big cluster near the origin, but within this group the deepest communities are situated at positive values of axis I, whilst the shallowest samples are situated at negative values of axis I.The cumulative percentage of variance explained by the species data for the first two axes was only 28.2% (15.7% axis I and 12.5% axis II), as it corresponds to a highly variable data set.

Species composition and abundances for each sample are indicated in
Shallow water samples are characterised by two geniculate coralline algae which are very common above 5 m depth (Amphiroa beauvoisii and Corallina elongata), and also by the corallimorph Corynactis viridis (Fig. 7).The encrusting coralline algae, Mesophyllum alternans and Lithophyllum incrustans, although not restricted to these depths, are the most abundant species for all transects, whilst Peyssonnelia rosa marina is especially found in sheltered conditions.Red algal turfs are regularly present.Asparagopsis armata is the most abundant soft erect alga.Suspension feeders are also present and even abundant in very shallow waters; besides the scleractinian Astroides calycularis, other common species include the sponge Clathrina cerebrum, the sea anemone Actinothoe sphyrodeta, and the bryozoan Schizobrachiella sanguinea.Sea urchins Paracentrotus lividus and Arbacia lixula are sometimes abundant but they are absent in the surf zone (Figs. 2,3).
Samples thriving at intermediate depths (5 to 25 m) are characterised by most of the recorded algae and sea urchins (Fig. 7).There are species that are more abundant in shallow waters (algae: Asparagopsis armata, both in the gametophytic and the tetrasporophytic phase of Falkenbergia rufolanosa, Lithophyllum incrustans, Codium bursa, Aglaozonia sp.; sponges: Cliona celata, Clathrina cerebrum; cnidarians: Actinia sp., Actinothoe sphyrodeta, Astroides calycularis; sea urchins: Arbacia lixula, Paracentrotus lividus, Sphaerechinus granularis) that are situated at negative values of the axis I (Fig. 7), and species that prefer deeper waters (algae: Rhodymenia ardissonei, Halopteris filicina, Peyssonnelia spp.; sponges: Dysidea avara, Ircinia fasciculata, Axinella damicornis, Chondrosia reniformis; cnidarians: Parazoanthus axinellae, Aglaophenia spp.; bryozoans: Myriapora truncata and Pentapora fascialis; sea cucumbers: Holothuria tubulosa) that are mostly situated at positive values of the axis I (Fig. 7).Other species are common everywhere, like the sponges Crambe crambe and Cliona viridis, and the bryozoan Schizobrachiella sanguinea.Relative abundances of suspension feeders increase with depth and they are more abundant in crevices, boulder zones, and north-facing slopes (e.g.Punta de la Mona-North transect) (Fig. 3).The group of samples collected in deep waters is characterised by large suspension feeders that are more or less restricted to these areas (Fig. 7): the cnidarians Dendrophyllia ramea, Leptogorgia sarmentosa, Parazoanthus axinellae, Cerianthus membranaceus and Alcyonium acaule; the sponges Axinella damicornis and Hemimycale columella; the tunicates Didemnum maculosum and Clavelina dellavallei; the bryozoan Pentapora fascialis; and the colonial worm Salmacina dysteri.Other more ubiquituous species also very common at these depths include the sponge Cliona viridis, hydroids of the genus Aglaophenia, and bryozoans such as Rynchozoon sp. and Savygniella lafontii.The detritic muddy bottoms of these deepest sites are colonised by the same suspension feeders but with a highly scattered distribution and growing on the detritic cobbles.Communities dominated by these organisms are restricted to transects of Punta de la Mona East and West (see Fig. 3).
Sedimentary bottoms (Fig. 5) The medium grain size decreases all along the transect, with a discontinuity between 20 and 30 m depth, where fine sand is replaced by very fine sand and mud.(Fig. 8) The bivalve Acanthocardia tuberculata, the gastropod Cerithium vulgatum and the hermit crab Clibanarius erythropus are abundant at 10 m depth.At 20 m, the worm Phyllochaetopterus socialis is abundant inside the sediment and Acanthocardia tuberculata is also common.The bryozoans Amathia semiconvoluta and Bugula neritina colonise dead mollusc shells and small detritic stones (Fig. 5).
Between 30 and 40 m depth, Phyllochaetopterus socialis and Acanthocardia aculeata are the main infaunal species.Epibenthic macrofauna include the hermit crab Dardanus arrossor and the gastropod Aporrhais pespelecani.Dead mollusc shells provide a substratum for the hydroids Nemertesia antennina and Synthecium evansii and the bryozoan Amathia semiconvoluta.The soft coral Alcyonium palmatum is particularly abundant at 40 m depth (Fig. 5).
There is an impoverishment of the macrofauna at 50 m depth, where only Phyllochaetopterus socialis and Alcyonium palmatum are abundant.Below 50 m depth, samples collected by dredging at 60, 70, 80, 90 and 100 m depth show an assemblage dominated by the sea-pen Pennatula phosphorea.

DISCUSSION
Most of the species found in this study have a wide distribution and are common for temperate Mediterranean and Atlantic waters.According to the literature (Conde, 1989;González, 1994) most of the algal species of tropical affinities inhabiting the Mediterranean have their westernmost distribution limit at about 3°W longitude, and this is also the case for several Mediterranean endemisms (although other typical Mediterranean species such as Posidonia oceanica have western limits that may include La Herradura inside their distribution area; Fig. 9).Conversely, no or very few genuine Atlantic species of macrophytes are found east of about 4°30'W longitude in southern Spain (Fig. 9), so its absence in La Herradura was not unexpected.Therefore, La Herradura is situated east from the expected distribution of Atlantic species and west from most of the Mediterranean species with tropical affinities, but not from other Mediterranean species.Nevertheless, none of these last species have been found (e.g.Posidonia oceanica, Cystoseira spinosa), with the exception of Rissoella verruculosa, a mediolittoral species that does not appear in our sublittoral samples, but which is present in La Herradura (Flores-Moya et al., 1998).
Deep (20-50 m depth) Mediterranean rocky bottom communities are characterised by the dominance of algae specially adapted to dim light conditions such as the encrusting corallines Mesophyllum alternans and Lithophyllum stictaeforme, and Peyssonnelia spp., with erect algae Cystoseira zosteroides, Halopteris filicina, Flabellia petiolata and Halimeda tuna, amongst others (Feldmann, 1937;Boudouresque, 1973;Boudouresque et al., 1986;Ballesteros, 1990Ballesteros, , 1991;;Ballesteros et al., 1993).The growth, death and accretion of encrusting corallines builds-up a biogenic structure called coralligenous that is typical of Mediterranean circalittoral rocky bottoms (Ros et al., 1985).Many species of suspension feeders grow over the coralligenous banks (Ballesteros et al., 1993) and their abundance is related to depth, currents and available particulate organic matter (Zabala and Ballesteros, 1989).On the other hand, the coralligenous structure is absent in Atlantic waters near the straits of Gibraltar, and kelp beds dominated by Laminaria ochroleuca and Cystoseira usneoides develop at the 20-50 m bathymetric range (Werner, 1962).Coralligenous or kelp beds are absent in La Herradura deep waters and the floristic component is very poor and scarcely developed.The dominance corresponds to big suspension feeders such as Cerianthus membranaceus, Salmacina dysteri, Pentapora fascialis and Dendrophyllia ramea, species that are also common in both the southwestern Mediterranean and Atlantic deep waters.
Most species of fauna and flora dwelling in La Herradura sea bottoms have an Atlantic-Mediterranean distribution, and are common in both.Benthic communities are neither typically Atlantic nor typically Mediterranean, since most genus and species defining Atlantic or Mediterranean communities are lacking.We suggest that deep water upwellings peculiar to this area (Lanoix, 1974;Cano, 1978;Rodríguez, 1990) prevent the development of the typical Mediterranean species and communities thriving in shallow waters.However, since the deep waters are of Mediterranean origin, pure Atlantic species and communities are also absent.This situation described for La Herradura can probably be extrapolated to the coasts of southern Spain affected by the upwelling, that is between 3°and 4°30'W.This reasoning could also explain the biogeographical asymmetry found between southern Spain and northern Morocco.Much research is needed in this geographical area to support this assessment.
The zonation patterns of La Herradura are well defined, as can be easily observed in Figures 3 and  4 and has been demonstrated in the ordination analysis for the rocky bottoms.Both axes I and II are related to depth, a situation that is predictable when sampling has been performed along a strong environmental gradient (Legendre and Legendre, 1979;Ballesteros and Romero, 1988).The ordination of samples defined by the first and second axes highlights two discontinuities.The first, situated at around 25 m depth, can be interpreted as the change from algal to animal dominance and can be interpreted as the boundary between the infralittoral and the circalittoral zone.The second one is situated above 5 m depth and may be related to the change from highly reophilic species that withstand heavy surf and hydrodynamism (upper infralittoral zone) to species not adapted to surf or to strong water movement (lower infralittoral zone).
FIG. 8. -Bathymetric distribution of the different sort of sediment along the sedimentary transect.

Table 2 (
rocky transects) and in Table 3 (sedimentary transect) and are diagrammatically shown in Figures 2 to 5.
BENTHIC COMMUNITIES IN UPWELLING AREA 71

TABLE 1 .
-Code, depth, orientation and kind of substrate for each sample.
Sample representation in the two first axes derived from a factorial correspondence analysis.Sample codes correspond to those appearing in Table1.
18FIG.7.-Species representation in the two first axes derived from a factorial correspondence analysis.Numbers correspond to species as indicated in Table2.