Increased diversity of sessile epibenthos at subtidal hydrothermal vents: seven hypotheses based on observations at Milos Island, Aegean Sea

Advances in Oceanography and LimnologyVol. 2, No. 1, June 2011, 1–31

Increased diversity of sessile epibenthos at subtidal hydrothermal vents:

seven hypotheses based on observations at Milos Island, Aegean Sea

Carlo Nike Bianchia*, Paul R. Dandob and Carla Morria

aDipTeRis (Department for the study of the Territory and its Resources), University of Genoa,Genova, Italy; bThe Marine Biological Association of the UK, Plymouth PL1 2PB, UK

(Received 18 November 2010; final version received 21 February 2011)

Research on subtidal hydrothermal vent ecosystems at Milos, Hellenic VolcanicArc (Aegean Sea), suggested that vent activity increased the species richnessof sessile epibenthic assemblages. Based on 303 species found in 6 sites (3 close tovents, 3 farther away), the present paper uses correspondence analysis andspecies/samples curves to examine the species composition and richness of theseassemblages. Differences due to vent proximity were more important than thosedue to bottom depth and distance from the shore. Diversity was confirmed to behigher near the vents, although none of the 266 species found at the vent sites canbe considered as obligate vent-associated species. Seven different, although notmutually exclusive, hypotheses are discussed to explain the pattern of increasedepibenthic species diversity at the vent sites, namely: (i) vents represent anintermediate disturbance, inducing mortality by the emission of toxic fluids;(ii) higher winter temperature allows for the occurrence of warm-water species,which add to the regional background; (iii) venting disrupts the homogeneity ofthe water bottom layer, increasing bottom roughness and hence habitatheterogeneity; (iv) deposition of minerals and enhanced bioconstruction byCa enrichment increment habitat provision; (v) fluid emission induces advectivemechanisms that favour recruitment; (vi) vents emit CO2, nutrients and traceelements that enhance primary productivity; and (vii) bacterial chemosynthesisadd to photosynthesis to provide a diversity of food sources for the fauna.

Keywords: sessile epibenthos; unitary organisms; clonal organisms; biodiversity;shallow hydrothermal vents; Milos Island; Mediterranean Sea

Introduction

Studies on the biota surrounding shallow-water sites of hydrothermal activity on theseafloor dates back to the beginning of the 20th century [1]. However, it was only after themore recent discovery of the peculiar biota living at deep-sea hydrothermal vents [2] thatthe systematic study of vent ecosystems has been undertaken: subsequent extensive reviewsillustrate the pace of growing information with time [3–8]. After three decades of intensiveresearch, a large body of published literature is available on the biotic communities livingat deep-sea vents, which allowed for faunal syntheses [9], biogeographic comparisons[10,11], and recommendations for conservation [12].

Despite the longer knowledge of, and easier access to, their shallow counterparts,less has been published on these [13]. A major difference between shallow and deep

*Corresponding author. Email: [email protected]

ISSN 1947–5721 print/ISSN 1947–573X online

� 2011 Taylor & Francis

DOI: 10.1080/19475721.2011.565804

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hydrothermal vent communities is the usual occurrence of obligate taxa of a high rank(genus and family) in deep vents, although exceptions are known [14,15]. In shallow-waterareas, i.e. those located at less than 200m depth [16], vent-obligate taxa are absent or theirtaxonomic rank does not exceed a species [17]. Shallow vents, in general, are colonised bycommunities that consist of a subset of the background biota, especially those speciesthat are less sensitive to hydrogen sulphide toxicity [13]. The proportion of organicmatter derived from chemosynthesis and photosynthesis is also an important distinctionbetween deep and shallow vent ecosystems: while deep-sea hydrothermal vents representdistinct ecosystems where most of the organic matter is derived from chemoynthesis,those at shallow depths are mostly fuelled by photosynthesis, and chemosynthesisonly plays an additional role. Consistently, deep vent ecosystems have only a smallinput from phytoplankton and lack macroalgae and diatom mats, which are commonat shallow vents. However, there is increasing evidence that a nutritional input fromphytoplankton is important for some deep-sea vent species, especially at the shallowerdeep-sea vents [18–20].

Deep-sea areas near vents are known to support a high biomass of macro- andmegafaunal species but a low diversity compared to the deep sea [21,22]; meiofaunaldiversity is also reduced at deep-sea vents [23]. There are contrasting views about thecorresponding patterns in shallow vent communities. In many cases, a reduction ofdiversity in phytobenthos [24,25], meiofauna [26], and macrofauna [27] has been observed.In the well-studied Kraternaya Bight, Kurile Islands, reduced species diversity wasaccompanied by a high population density and biomass for individual species [28].In shallow hydrothermal vents of the western Pacific, at various latitudes, themacrozoobenthos had low species diversity [29]. Studies on epifaunal communitiesaround shallow vents in the Aeolian Islands, southern Italy, showed a lowering of diversityfor bryozoans [30] but little or no effect on sponges [31]. In contrast, studies carried out atthe Island of Milos, Aegean Sea [32], revealed high diversity of both sessile epifauna [33,34]and macroalgae [35] at vent sites.

The aim of the present paper, which also takes into account the results of furtherstudies of the sessile organisms of shallow-water hydrothermal vents at Milos [36–43], is toexplore synoptically the structure of the sessile assemblages of Milos and to comparespecies richness at vent and non-vent sites. The results will be discussed in the frame ofseven hypotheses about the effects of vent emissions on the epibenthic communities.

Study area

Milos Island is part of the Cyclades Archipelago in the Aegean Sea. Venting affects an areaof about 35 km2 of seabed [44] extending from the intertidal down to 240m water depthoff Milos. The sampling area for the present study was in the subtidal, off the �1.4 kmwide Palaeochori Bay on the SE coast of Milos. The basement rock off Palaeochori is anassociation of phyllites and metabasalts with marble and quartz veins. This is overlainby marine and volcanoclastic sediments of varying thickness, consisting predominantly ofsand with variable amounts of silt, clay and gravel, and with rocks outcropping in places[45]. Sediment permeability varies locally, partly dependent on the degree of sedimentcementation. Hydrothermal activity appears to be more intense in the north-west andin the centre of the bay, where extensive ‘white patches’ of mineral-microbial mats andwarm brine pools occur on the seabed [46,47]. Near these brine seeps the temperature

2 C.N. Bianchi et al.


can reach up to 120�C at 10m depth. The seagrasses Posidonia oceanica and Cymodoceanodosa, which largely cover the seabed of the bay, are absent where the sedimenttemperature is 2�C higher than ambient [48].

The vent chemistry varies across Palaeochori Bay and with increasing distance fromthe shore [32]. Different authors described a mixture of hydrothermal brine seepingthrough the sediment together with flows of both low and high salinity water [49,50].Most of the gas released is carbon dioxide but some vents have significant concentrationsof hydrogen, methane or hydrogen sulphide [44]. The pH of the venting fluids at 10moffshore ranges between 5.5 and 6.9, and the fluids may be enriched in sodium chloride orbe of reduced salinity, due to dilution with water vapour or meteoric water, by about 20%with respect to seawater (the mean chloride concentration of the venting water is 475mM).At a distance of more than 50m offshore the venting water is less diluted and only enrichedin metals by up to 3-fold compared to the local seawater [32,43].

The precipitates vary in composition from vent to vent with deposits high in silica(up to 6mM in venting fluids) being found around the more acidic vents, below pH 6,while iron and manganese hydroxides are preferentially deposited at higher pH. Dissolvedsulphide concentrations up to 3mM were reported in hydrothermal fluids, some of whichis believed to have resulted from sulphate reduction within the upper sediment layers [49].Elemental sulphur is heavily deposited at some sites forming fluffy mats up to 6 cm thick.Over hot sediments yellow deposits of arsenic sulphides are evident [51]. However, at mostsites the water issuing from the vents consists mainly of shallow re-circulated seawater witha small component of hydrothermal fluids. The interstitial circulation, driven by the risingvent fluids, controls the distribution of diatoms, bacteria, archaea and infauna around thevents [32,46,49,52,53].

Materials and methods

Apart from some nomenclatural and taxonomic update following the World Registerof Marine Species (www.marinespecies.org), the data used are those previously published[33–37,39–41] on the sessile organisms collected by scraping the substratum in six subtidalrocky reefs (2 to 45m deep), named SR, E, ST, CR, VS, and S (Figure 1). Although allsites were located in a hydrothermal area, only the rocky reefs at sites SR, CR and VSharboured active vents and continuous emission of fluid was observed there during fieldwork (Figure 2). These three sites will be thereafter called ‘vent sites’, the remaining three‘non-vent sites’. In vent sites, the sessile organisms were scraped from the substratumin proximity (55m) of fluid emissions.

Species were divided into unitary and clonal, the two life strategies having contrastingadaptive significance on marine hard substrata [54]. Solitary metazoans were considered asunitary, whereas macroalgae, sponges and colonial animals were considered as clonalorganisms [55], and so was the scissiparous serpulid polychaete Salmacina dysteri, whichformed colony-like aggregates [37].

The species composition of assemblages at the six sites was compared throughcorrespondence analysis [56] applied to a presence–absence matrix of 303 species� 6 sites.The significance of the axes extracted was evaluated using Lebart’s tables [57]. Thetendency of individual species to colonise vent areas was calculated through frequentialanalysis [58], assigning a value of 100% to species found exclusively at vent sites, anda value of 0% to species found exclusively at non-vent sites; a species equally frequent at

Advances in Oceanography and Limnology 3


both vent and non-vent sites scored 50%. Similarly, the individual species affinity withdepth and distance from shore was calculated by direct gradient analysis [59], based onthe observed distribution of species at the 6 sites and using m and km, respectively, as theunits of measure.

Species richness at the different sites was compared by plotting the cumulative numberof species against the number of samples taken at each site (direct plots). The number ofsamples varied from a minimum of 12 (site VS) to a maximum of 20 (site CR). Curves werefitted to these plots according to the equation S¼ c �Nz, where S is the number of species,N is the number of samples, c is a constant giving the number of species that may beexpected with one sample, and z is the slope of the regression line relating S and N [60].Since z is independent from the value and the unit of measure of the parameter on theabscissa, it can be used as a non-dimensional measure of species richness as well as beingcompared with the corresponding figures derived from species/area curves [61]. Plottingthe reciprocals of the cumulative number of species against the reciprocals of the numberof samples was also tried. This allowed an extrapolation to show the number of speciesfound with an ‘infinite’ number of samples, i.e. the theoretical maximum number of speciesin each site.

Results

Correspondence analysis gave two significant axes (P5 0.05), together explaining 68%of the total variance. In the plane formed by the first two axes, the points correspondingto the three vent sites lay well separated from those of the three non-vent sites, whilespecies-points spread more or less regularly over most of the plane (Figure 3a). Since many

Figure 1. Study area and location of the six sites (SR, E, ST, CR, VS, and S) where sessileepibenthos was collected. Sites SR, CR, and VS were close to hydrothermal vent systems on thesea floor.



of the 303 species showed coincident distribution among sites, only 43 differentdistribution patterns resulted. These patterns ranged from species found exclusively in asingle site (codes 1–6 in Table 1) to species that occurred at all sites (code 43 in Table 1),whose points therefore occupied a central position in the graph (Figure 3a).

Plotting the isopleths of percent tendency toward vent areas (computed throughfrequential analysis) on the plane formed by the first two axes from correspondenceanalysis, a clear gradient along the first axis was observed from vent to non-ventsites (Figure 3b). The first axis scores correlated with percent vent tendency

Figure 2. (a) Pictorial view of a representative rocky reef in a vent site. (b) Fluid emission withgas bubbling at a rocky reef in a vent site. Scale: each mark on the frame is 1 cm.



(Spearman r¼�0.914, P5 0.001). Similarly, the isopleths of depth (Figure 3c) anddistance from the shore (Figure 3d) trended mostly along the second axis, the resultsshowing correlation with both parameters (depth: r¼ –0.710, P5 0.001; distance fromshore: r¼ –0.913, P5 0.001).

The equation S¼ c �Nz fitted well all the six species/samples curves (Table 2). Curves ofspecies from vent sites always lay above curves of non-vent sites (Figure 4), due to highervalues of both c and z. Similarly, the plots of the reciprocals of species against samplenumbers were well fitted by regression lines of the form 1/S¼ a � 1/Nþ b (Figure 5): thereciprocal of the intercept b represents the number of species S1 to be found after infinite(i.e. 1/0) samples and can be taken as the maximum number of species expected at the site.The values of S1 clearly confirmed higher species richness at vent sites, independentlyfrom the slight differences in sampling effort (Table 2). Species richness, expressed as zvalues, increased with both bottom depth and distance from shore. Vent sites, however,

(a) (b)

(c) (d)

Figure 3. Plot on the plane formed by the first two axes extracted by correspondence analysis.The cross indicates the origin of the axes. The proportion of the total variance explained by eachaxis is given in parenthesis. (a) Site-points (bold characters) and species-points (numbers accordingto the codes in Table 1). (b) Isopleths of percent tendency toward vent areas (computed throughfrequential analysis). (c) Isopleths of depth (m). (d) Isopleths of distance from shore (km). See textfor explanations.



Table 1. List of the sessile epibenthic species, ordered by distribution code number and thenalphabetically, collected at vent and non-vent sites off Palaeochori Bay, Milos.

Vent sites Non-vent sites

Code Species, Phylum – unitary or clonal SR CR VS E ST S

1 Acetabularia acetabulum, Chlorophyta – clonal þ . . . . .1 Aglaophenia octodonta, Cnidaria – clonal þ . . . . .1 Aglaophenia picardi, Cnidaria – clonal þ . . . . .1 Amphiroa rigida, Rhodophyta – clonal þ . . . . .1 Amphiroa verruculosa, Rhodophyta – clonal þ . . . . .1 Beania hirtissima cylindrica, Bryozoa – clonal þ . . . . .1 Botryocladia boergesenii, Rhodophyta – clonal þ . . . . .1 Corallina elongata, Rhodophyta – clonal þ . . . . .1 Cornularia cornucopiae, Cnidaria – clonal þ . . . . .1 Cystoseira compressa, Heterokontophyta –

clonalþ . . . . .

1 Cystoseira crinita, Heterokontophyta – clonal þ . . . . .1 Cystoseira spinosa, Heterokontophyta – clonal þ . . . . .1 Dictyota fasciola, Heterokontophyta – clonal þ . . . . .1 Escharina dutertrei, Bryozoa – clonal þ . . . . .1 Eudendrium racemosum, Cnidaria – clonal þ . . . . .1 Eudendrium sp., Cnidaria – clonal þ . . . . .1 Filogranula gracilis, Annelida – unitary þ . . . . .1 Halopithys incurva, Rhodophyta – clonal þ . . . . .1 Laurencia microcladia, Rhodophyta – clonal þ . . . . .1 Laurencia obtusa, Rhodophyta – clonal þ . . . . .1 Laurencia sp., Rhodophyta – clonal þ . . . . .1 Liagora viscida, Rhodophyta – clonal þ . . . . .1 Lithophyllum frondosum, Rhodophyta – clonal þ . . . . .1 Microcosmus vulgaris, Chordata – unitary þ . . . . .1 Modiolarca subpicta, Mollusca – unitary þ . . . . .1 Mycale (Aegogropila) retifera, Porifera – clonal þ . . . . .1 Odontoporella lata, Bryozoa – clonal þ . . . . .1 Polysiphonia scopulorum, Rhodophyta – clonal þ . . . . .1 Rhynchozoon pseudodigitatum, Bryozoa – clonal þ . . . . .1 Spondylus gaederopus, Mollusca – unitary þ . . . . .1 Turbicellepora camera, Bryozoa – clonal þ . . . . .1 Valonia utricularis, Chlorophyta – clonal þ . . . . .1 Vermiliopsis striaticeps, Annelida – unitary þ . . . . .2 Antennella secundaria, Cnidaria – clonal . . . þ . .2 Bowerbankia gracilis, Bryozoa – clonal . . . þ . .2 Codium bursa, Chlorophyta – clonal . . . þ . .2 Corallophila cinnabarina, Rhodophyta – clonal . . . þ . .2 Cystoseira sp. 1, Heterokontophyta – clonal . . . þ . .2 Dictyota dichotoma v. intricata,

Heterokontophyta – clonal. . . þ . .

2 Gulsonia nodulosa, Rhodophyta – clonal . . . þ . .2 Halopteris catharina, Cnidaria – clonal . . . þ . .2 Hippopodina feegeensis, Bryozoa – clonal . . . þ . .2 Nolella gigantea, Bryozoa – clonal . . . þ . .2 Retevirgula akdenizae, Bryozoa – clonal . . . þ . .2 Schizomavella mamillata, Bryozoa – clonal . . . þ . .2 Schizoporella unicornis, Bryozoa – clonal . . . þ . .

(continued )



Table 1. Continued.



2 Tricleocarpa fragilis, Rhodophyta – clonal . . . þ . .3 Schizomavella rudis, Bryozoa – clonal . . . . þ .3 Stypocaulon scoparium, Heterokontophyta –

clonal. . . . þ .

4 Aetea sica, Bryozoa – clonal . þ . . . .4 Amathia lendigera, Bryozoa – clonal . þ . . . .4 Aplidium sp., Chordata – clonal . þ . . . .4 Cellepora pumicosa, Bryozoa – clonal . þ . . . .4 Chaetomorpha ligustica, Chlorophyta – clonal . þ . . . .4 Chlidonia pyriformis, Bryozoa – clonal . þ . . . .4 Clytia noliformis, Cnidaria – clonal . þ . . . .4 Contarinia peyssonneliaeformis, Rhodophyta –

clonal. þ . . . .

4 Cruoria cruoriaeformis, Rhodophyta – clonal . þ . . . .4 Dictyopteris polypodioides, Heterokontophyta –

clonal. þ . . . .

4 Drachiella minuta, Rhodophyta – clonal . þ . . . .4 Halydictyon mirabile, Rhodophyta – clonal . þ . . . .4 Hippaliosina depressa, Bryozoa – clonal . þ . . . .4 Hoplangia durotrix, Cnidaria – clonal . þ . . . .4 Hydrolithon farinosum v. chalicodityum,

Rhodophyta – clonal. þ . . . .

4 Lithophaga lithophaga, Mollusca – unitary . þ . . . .4 Metroperiella lepralioides, Bryozoa – clonal . þ . . . .4 Microcosmus sabatieri, Chordata – unitary . þ . . . .4 Mollia multijuncta, Bryozoa – clonal . þ . . . .4 Plumularia obliqua, Cnidaria – clonal . þ . . . .4 Polyclinum aurantium, Chordata – clonal . þ . . . .4 Pseudochlorodesmis furcellata, Chlorophyta –

clonal. þ . . . .

4 Ptilothamnion pluma, Rhodophyta – clonal . þ . . . .4 Puellina gattyae, Bryozoa – clonal . þ . . . .4 Scrupocellaria sp., Bryozoa – clonal . þ . . . .4 Semivermilia pomatostegoides, Annelida –

unitary. þ . . . .

4 Titanoderma cystoseirae, Rhodophyta – clonal . þ . . . .5 Ascidiella aspersa, Chordata – unitary . . . . . þ

5 Asperococcus bullosus, Heterokontophyta –clonal

. . . . . þ

5 Axinella damicornis, Porifera – clonal . . . . . þ

5 Cladosiphon cylindricus, Heterokontophyta –clonal

. . . . . þ

5 Cutleria cfr chilosa, Heterokontophyta – clonal . . . . . þ

5 Dasya rigidula, Rhodophyta – clonal . . . . . þ

5 Diplosolen obelia, Bryozoa – clonal . . . . . þ

5 Escharina sp., Bryozoa – clonal . . . . . þ

5 Hydrolithon farinosum v. farinosum,Rhodophyta – clonal

. . . . . þ

5 Jania rubens, Rhodophyta – clonal . . . . . þ

(continued )



Table 1. Continued.



5 Molgula complanata, Chordata – unitary . . . . . þ

5 Onychocella marioni, Bryozoa – clonal . . . . . þ

5 Palmophyllum crassum, Chlorophyta – clonal . . . . . þ

5 Sargassum (Sargassum) vulgare,Heterokontophyta – clonal

. . . . . þ

5 Sertularella mediterranea, Cnidaria – clonal . . . . . þ

5 Spatoglossum solieri, Heterokontophyta –clonal

. . . . . þ

5 Sphacelaria sp., Heterokontophyta – clonal . . . . . þ

5 Stilophora tenella, Heterokontophyta – clonal . . . . . þ

5 Zonaria tournefortii, Heterokontophyta – clonal . . . . . þ

6 Aglaophenia elongata, Cnidaria – clonal . . þ . . .6 Amathia pruvoti, Bryozoa – clonal . . þ . . .6 Anarthropora monodon, Bryozoa – clonal . . þ . . .6 Anomia ephippium, Mollusca – unitary . . þ . . .6 Apomatus similis, Annelida – unitary . . þ . . .6 Ascidia virginea, Chordata – unitary . . þ . . .6 Axinella cannabina, Porifera – clonal . . þ . . .6 Bougainvillia muscus, Cnidaria – clonal . . þ . . .6 Bugula fulva, Bryozoa – clonal . . þ . . .6 Caberea boryi, Bryozoa – clonal . . þ . . .6 Caryophyllia (Caryophyllia) smithii, Cnidaria –

unitary. . þ . . .

6 Celleporina caliciformis, Bryozoa – clonal . . þ . . .6 Chorizopora brongniartii, Bryozoa – clonal . . þ . . .6 Codium effusum, Chlorophyta – clonal . . þ . . .6 Corticium candelabrum, Porifera – clonal . . þ . . .6 Cystoseira corniculata, Heterokontophyta –

clonal. . þ . . .

6 Didemnum maculosum, Chordata – clonal . . þ . . .6 Diplosoma listerianum, Chordata – clonal . . þ . . .6 Erylus euastrum, Porifera – clonal . . þ . . .6 Escharina hyndmanni, Bryozoa – clonal . . þ . . .6 Eudendrium glomeratum, Cnidaria – clonal . . þ . . .6 Eudendrium ramosum, Cnidaria – clonal . . þ . . .6 Halecium mediterraneum, Cnidaria – clonal . . þ . . .6 Hemicyclopora multispina, Bryozoa – clonal . . þ . . .6 Hincksina flustroides, Bryozoa – clonal . . þ . . .6 Hippoporidra picardi, Bryozoa – clonal . . þ . . .6 Hydroides norvegicus, Annelida – unitary . . þ . . .6 Idmidronea sp., Bryozoa – clonal . . þ . . .6 Kirchenpaueria pinnata, Cnidaria – clonal . . þ . . .6 Lissoclinum perforatum, Chordata – clonal . . þ . . .6 Microcosmus savignyi, Chordata – unitary . . þ . . .6 Microporella umbracula, Bryozoa – clonal . . þ . . .6 Novocrania anomala, Brachiopoda – unitary . . þ . . .6 Obelia bidentata, Cnidaria – clonal . . þ . . .6 Osmundaria volubilis, Rhodophyta – clonal . . þ . . .6 Peyssonnelia polymorpha, Rhodophyta – clonal . . þ . . .

(continued )



Table 1. Continued.



6 Phallusia mammillata, Chordata – unitary . . þ . . .6 Pileolaria heteropoma, Annelida – unitary . . þ . . .6 Pileolaria militaris, Annelida – unitary . . þ . . .6 Plagioecia sp., Bryozoa – clonal . . þ . . .6 Platonea stoechas, Bryozoa – clonal . . þ . . .6 Plumularia setacea, Cnidaria – clonal . . þ . . .6 Polycarpa sp., Chordata – unitary . . þ . . .6 Pomatoceros triqueter, Annelida – unitary . . þ . . .6 Puellina orientalis, Bryozoa – clonal . . þ . . .6 Puellina sp., Bryozoa – clonal . . þ . . .6 Pyura microcosmus, Chordata – unitary . . þ . . .6 Rhodophyllis divaricata, Rhodophyta – clonal . . þ . . .6 Rhynchozoon sp., Bryozoa – clonal . . þ . . .6 Schizomavella hastata, Bryozoa – clonal . . þ . . .6 Scrupocellaria scrupea, Bryozoa – clonal . . þ . . .6 Segonzactis platypus, Cnidaria – unitary . . þ . . .6 Semivermilia agglutinata, Annelida – unitary . . þ . . .6 Semivermilia torulosa, Annelida – unitary . . þ . . .6 Serpula lobiancoi, Annelida – unitary . . þ . . .6 Serpula sp., Annelida – unitary . . þ . . .6 Sertularia distans, Cnidaria – clonal . . þ . . .6 Smittoidea reticulata, Bryozoa – clonal . . þ . . .6 Sphaerococcus coronopifolius, Rhodophyta –

clonal. . þ . . .

6 Styela canopus, Chordata – unitary . . þ . . .6 Tubulipora plumosa, Bryozoa – clonal . . þ . . .6 Tubuliporidae gen. sp., Bryozoa – clonal . . þ . . .7 Scrupocellaria scruposa, Bryozoa – clonal þ þ þ þ . .7 Tubulipora sp., Bryozoa – clonal þ þ þ þ . .8 Anadyomene stellata, Chlorophyta – clonal þ þ . . . .8 Clavularia crassa, Cnidaria – clonal þ þ . . . .8 Cliona rhodensis, Porifera – clonal þ þ . . . .8 Dictyota linearis, Heterokontophyta – clonal þ þ . . . .8 Gelidium pusillum, Rhodophyta – clonal þ þ . . . .8 Halimeda tuna, Chlorophyta – clonal þ þ . . . .8 Mecynoecia sp., Bryozoa – clonal þ þ . . . .8 Pherusella tubulosa, Bryozoa – clonal þ þ . . . .8 Protolaeospira striata, Annelida – unitary þ þ . . . .9 Filogranula calyculata, Annelida – unitary þ þ þ . þ .9 Reteporella grimaldii, Bryozoa – clonal þ þ þ . þ .10 Bantariella verticillata, Bryozoa – clonal þ þ þ . . .10 Geodia cydonium, Porifera – clonal þ þ þ . . .10 Neodexiospira pseudocorrugata, Annelida –

unitaryþ þ þ . . .

10 Pyura squamulosa, Chordata – unitary þ þ þ . . .10 Rhynchozoon neapolitanum, Bryozoa – clonal þ þ þ . . .10 Vinearia koehleri, Annelida – unitary þ þ þ . . .11 Celleporina lucida, Bryozoa – clonal þ . þ . . .11 Clytia hemisphaerica, Cnidaria – clonal þ . þ . . .

(continued )



Table 1. Continued.



11 Janua (Dexiospira) pagenstecheri gnomonica,Annelida – unitary

þ . þ . . .

11 Leucetta solida, Porifera – clonal þ . þ . . .11 Mimosella gracilis, Bryozoa – clonal þ . þ . . .11 Mitrocoma annae, Cnidaria – clonal þ . þ . . .11 Molgula occulta, Chordata – unitary þ . þ . . .11 Mollia patellaria, Bryozoa – clonal þ . þ . . .11 Obelia dichotoma, Cnidaria – clonal þ . þ . . .11 Schizomavella discoidea, Bryozoa – clonal þ . þ . . .11 Scrupocellaria reptans, Bryozoa – clonal þ . þ . . .11 Vermiliopsis infundibulum, Annelida – unitary þ . þ . . .11 Vermiliopsis monodiscus, Annelida – unitary þ . þ . . .12 Acinetospora crinita, Heterokontophyta – clonal . þ þ . . .12 Adeonella polystomella, Bryozoa – clonal . þ þ . . .12 Aetea lepadiformis, Bryozoa – clonal . þ þ . . .12 Aplidium elegans, Chordata – unitary . þ þ . . .12 Barbatia barbata, Mollusca – unitary . þ þ . . .12 Cladophora sp., Chlorophyta – clonal . þ þ . . .12 Crassimarginatella maderensis, Bryozoa – clonal . þ þ . . .12 Cystoseira schiffneri f. latiramosa,

Heterokontophyta – clonal. þ þ . . .

12 Flabellia petiolata, Chlorophyta – clonal . þ þ . . .12 Janita fimbriata, Annelida – unitary . þ þ . . .12 Megathiris detruncata, Brachiopoda – unitary . þ þ . . .12 Metavermilia multicristata, Annelida – unitary . þ þ . . .12 Mycale (Mycale) lingua, Porifera – clonal . þ þ . . .12 Parasmittina tropica, Bryozoa – clonal . þ þ . . .12 Polycarpa gracilis, Chordata – unitary . þ þ . . .12 Pyura dura, Chordata – unitary . þ þ . . .12 Savignyella lafontii, Bryozoa – clonal . þ þ . . .12 Scrupocellaria delilii, Bryozoa – clonal . þ þ . . .12 Serpula vermicularis echinata, Annelida –

unitary. þ þ . . .

12 Serpulorbis arenarius, Mollusca – unitary . þ þ . . .12 Umbonula ovicellata, Bryozoa – clonal . þ þ . . .13 Annectocyma major, Bryozoa – clonal þ þ þ . . þ

13 Didemnum granulosum, Chordata – clonal þ þ þ . . þ

13 Mesophyllum lichenoides, Rhodophyta – clonal þ þ þ . . þ

13 Microdictyon tenuius, Chlorophyta – clonal þ þ þ . . þ

13 Salmacina dysteri, Annelida – clonal þ þ þ . . þ

13 Semivermilia crenata, Annelida – unitary þ þ þ . . þ

13 Sertularella ellisii, Cnidaria – clonal þ þ þ . . þ

14 Amphiroa cryptarthrodia, Rhodophyta – clonal þ . . þ . .14 Balanophyllia (Balanophyllia) europaea,

Cnidaria – unitaryþ . . þ . .

14 Cladostephus spongiosus f. verticillatus,Heterokontophyta – clonal

þ . . þ . .

14 Cystoseira sp. 2, Heterokontophyta – clonal þ . . þ . .14 Gelidium spinosum, Rhodophyta – clonal þ . . þ . .

(continued )



Table 1. Continued.



14 Haliptilon virgatum, Rhodophyta – clonal þ . . þ . .14 Sarcotragus foetidus, Porifera – clonal þ . . þ . .14 Taonia atomaria, Heterokontophyta – clonal þ . . þ . .15 Cystoseira barbata, Heterokontophyta – clonal þ . . . . þ

16 Chondrosia reniformis, Porifera – clonal þ . . þ þ .17 Schizobrachiella sanguinea, Bryozoa – clonal þ þ . þ . .17 Sphacelaria cirrosa, Heterokontophyta – clonal þ þ . þ . .18 Hydroides pseudouncinatus pseudouncinatus,

Annelida – unitaryþ þ . . þ .

18 Microcosmus polymorphus, Chordata – unitary þ þ . . þ .18 Synoicum sp., Chordata – clonal þ þ . . þ .19 Beania hirtissima hirtissima, Bryozoa – clonal þ . þ þ . .20 Reptadeonella violacea, Bryozoa – clonal þ . . þ þ þ

21 Spongia (Spongia) officinalis, Porifera – clonal þ . . . þ þ

22 Fenestrulina malusii, Bryozoa – clonal þ þ . . . þ

22 Polysiphonia subulifera, Rhodophyta – clonal þ þ . . . þ

22 Serpula concharum, Annelida – unitary þ þ . . . þ

22 Zanardinia typus, Heterokontophyta – clonal þ þ . . . þ

23 Ircinia variabilis, Porifera – clonal þ þ . . þ þ

23 Phorbas tenacior, Porifera – clonal þ þ . . þ þ

24 Calpensia nobilis, Bryozoa – clonal þ . þ . . þ

24 Hiatella arctica, Mollusca – unitary þ . þ . . þ

24 Janua (Dexiospira) pagenstecheri, Annelida –unitary

þ . þ . . þ

24 Serpula vermicularis, Annelida – unitary þ . þ . . þ

25 Caryophyllia (Caryophyllia) inornata, Cnidaria– unitary

. þ . þ þ þ

25 Crambe crambe, Porifera – clonal . þ . þ þ þ

25 Hymeniacidon perlevis, Porifera – clonal . þ . þ þ þ

25 Ircinia oros, Porifera – clonal . þ . þ þ þ

25 Petrosia (Petrosia) ficiformis, Porifera – clonal . þ . þ þ þ

26 Axinella verrucosa, Porifera – clonal . . þ þ þ .27 Puellina hincksi, Bryozoa – clonal . þ þ þ . .27 Womersleyella setacea, Rhodophyta – clonal . þ þ þ . .28 Cliona copiosa, Porifera – clonal . þ . . þ .28 Phyllangia mouchezi, Cnidaria – clonal . þ . . þ .29 Aaptos aaptos, Porifera – clonal . þ þ . þ .29 Dysidea avara, Porifera – clonal . þ þ . þ .29 Smittina cervicornis, Bryozoa – clonal . þ þ . þ .30 Beckerella mediterranea, Rhodophyta – clonal . þ . . . þ

30 Celleporina tubulosa, Bryozoa – clonal . þ . . . þ

30 Cliona viridis, Porifera – clonal . þ . . . þ

30 Haplopoma impressum, Bryozoa – clonal . þ . . . þ

30 Sphacelaria plumula, Heterokontophyta – clonal . þ . . . þ

30 Stypopodium schimperi, Heterokontophyta –clonal

. þ . . . þ

30 Tribonema marinum, Heterokontophyta – clonal . þ . . . þ

30 Vermetus granulatus, Mollusca – unitary . þ . . . þ

31 Ascidia mentula, Chordata – unitary . þ þ . . þ

(continued )



always exhibited greater values than non-vent sites at similar depths or distances fromthe shore (Figure 6).

A total of 171 species (coded 1, 4, 6, 8, 10, 11, and 12 in Table 1) were collectedexclusively at vent sites in Palaeochori Bay, compared to only 37 species (coded 2, 3, 5, and33 in Table 1) found exclusively at non-vent sites. There were higher numbers of speciesat vent sites for each of the 10 phyla to which the 303 species belonged, namelyRhodophyta, Heterokontophyta, Chlorophyta, Porifera, Cnidaria, Mollusca, Annelida,

Table 1. Continued.



31 Celleporina mangnevillana, Bryozoa – clonal . þ þ . . þ

31 Cystoseira brachycarpa, Heterokontophyta –clonal

. þ þ . . þ

31 Escharina vulgaris, Bryozoa – clonal . þ þ . . þ

31 Escharoides coccinea, Bryozoa – clonal . þ þ . . þ

32 Leptopsammia pruvoti, Cnidaria – unitary . þ . . þ þ

33 Polycyathus muellerae, Cnidaria – clonal . . . . þ þ

33 Sargassum sp., Heterokontophyta – clonal . . . . þ þ

34 Protula tubularia, Annelida – unitary . þ þ . þ þ

35 Argyrotheca cuneata, Brachiopoda – unitary . . þ . . þ

35 Disporella hispida, Bryozoa – clonal . . þ . . þ

35 Halopteris filicina, Heterokontophyta – clonal . . þ . . þ

35 Joania cordata, Brachiopoda – unitary . . þ . . þ

35 Monoporella nodulifera, Bryozoa – clonal . . þ . . þ

35 Nidificaria clavus, Annelida – unitary . . þ . . þ

35 Puellina radiata, Bryozoa – clonal . . þ . . þ

35 Puellina setosa, Bryozoa – clonal . . þ . . þ

35 Sargassum acinarium, Heterokontophyta –clonal

. . þ . . þ

35 Walkeria tuberosa, Bryozoa – clonal . . þ . . þ

36 Agelas oroides, Porifera – clonal þ þ . þ þ þ

36 Rhynchozoon sp. 1, Bryozoa – clonal þ þ . þ þ þ

37 Crisia sp., Bryozoa – clonal þ þ þ þ . þ

37 Halocynthia papillosa, Chordata – unitary þ þ þ þ . þ

37 Lichenopora radiata, Bryozoa – clonal þ þ þ þ . þ

37 Schizomavella auriculata, Bryozoa – clonal þ þ þ þ . þ

37 Sycon raphanus, Porifera – clonal þ þ þ þ . þ

38 Josephella marenzelleri, Annelida – unitary þ þ þ . þ þ

38 Madracis pharensis, Cnidaria – clonal þ þ þ . þ þ

38 Myriapora truncata, Bryozoa – clonal þ þ þ . þ þ

38 Spirobranchus polytrema, Annelida – unitary þ þ þ . þ þ

38 Vermiliopsis labiata, Annelida – unitary þ þ þ . þ þ

39 Eudendrium armatum, Cnidaria – clonal . þ . . þ þ

40 Padina pavonica, Heterokontophyta – clonal þ þ . þ . þ

41 Dasycladus vermicularis, Chlorophyta – clonal þ . þ . þ þ

42 Jania adhaerens, Rhodophyta – clonal . . þ þ . .43 Aetea truncata, Bryozoa – clonal þ þ þ þ þ þ

43 Schizoporella dunkeri, Bryozoa – clonal þ þ þ þ þ þ

Species sharing the same code number exhibit the same distribution among sites.



Bryozoa, Brachiopoda, and Chordata (Figure 7). This difference was significant (two-tailsign test, P¼ 0.002). However, for individual phyla the difference in species numbersbetween vent and non-vent sites was significant only for Chlorophyta (Student’s t-test,P¼ 0.016), Cnidaria (P¼ 0.018), Mollusca (P¼ 0.016), Annelida (P¼ 0.028), andChordata (P¼ 0.045). Due to the high number of macroalgae and bryozoans, in all sitesclonal organisms were more represented than unitary organisms (236 vs. 67), but the latterwere proportionately species richer at vent sites than at non-vent sites (Figure 8).

Table 2. Summary of the main parameters and coefficients of the species/samples regressions.

N S1 SN c z rdir S1 rrec

Vent sitesSR 14 40 116 42.1 0.371 0.968 113 0.997CR 20 29 128 33.7 0.442 0.956 127 0.998VS 12 36 154 36.7 0.575 0.992 162 0.997

Non-vent sitesE 18 21 48 21.8 0.266 0.990 49 0.998ST 15 16 38 16.1 0.308 0.999 39 0.998S 15 22 88 23.9 0.441 0.978 91 0.999

N, number of samples collected in the different sites; S1, maximum number of species found in onesample (compare with c); SN, cumulative number of species in N samples; c, z, coefficients calculatedfrom the relation S¼ c.Nz; rdir, correlation coefficient of the curve resulting from the direct plot ofcumulative number of species against number of samples (see Figure 4); S1, theoretical maximumnumber of species in each site, by extrapolation; rrec, correlation coefficient between the reciprocalsof both the cumulative number of species and the number of samples (see Figure 5).

Figure 4. Species/samples curves for the sessile epibenthos collected at different sites at Milos.All curves conform to the equation S¼ c.Nz (see Table 2).



Discussion

This study confirmed that the sessile epibenthos collected near vent sites at Milos wassignificantly richer in species than that collected at non-vent sites, especially within thephyla Chlorophyta, Cnidaria, Mollusca, Annelida, and Chordata. Molluscs and annelidsare known to preponderate also at deep-sea hydrothermal vents, when compared withnon-vent areas [6]. The available information on the phyletic composition at shallow ventsis too scarce to allow for comparison, but in Papua New Guinea chordates were foundonly at vent sites, whereas cnidarians were present at both vent and control sites [62].

By analogy with a classification proposed for cold seeps [63], biota inhabiting ventareas would include ‘obligate’ species, restricted to sites in direct proximity to the fluids,and ‘regional’ species, which occupy both vent and neighbouring non-vent sites. The terms‘endemic’, for the species totally restricted to vents, and ‘colonist’, for the opportunisticspecies that were more abundant around vents than in the surrounding environment, have

Figure 5. Plot of the reciprocals of cumulative species numbers (1/S) against the reciprocals ofsample numbers (1/N) at different sites at Milos. The equations of the corresponding regression linesare indicated (see Table 2 for the correlation coefficients).



also been introduced [64]. However, this use of the term ‘endemic’ has been criticised, as intraditional biogeography it indicates a taxon restricted to a geographical region, not to ahabitat [17]. Despite the high number of species (171, i.e. 56% of the total) found onlyin sites closest to the actual vents at Milos, all of them were regional, being already knownfrom ‘normal’ sites in the Mediterranean Sea. Thus, no vent-obligate species could berecognised among the sessile epibenthos at Milos. However, six species (coded 10 inTable 1) were found at all the three vent-sites off Palaeochori and at none of the threenon-vent sites. Among these, the sponge Geodia cydonium is noteworthy since the samespecies has been shown to grow better in areas influenced by hydrothermal waters [65,66]and two species of Geodia are known that may be cold-seep obligate [67].

The lack of vent obligate species in the sessile epibenthos at Milos agrees with findingson infauna [68], although a sibling species of Capitella capitata may be a vent obligate [69].The same situation is also found for most other shallow-water vents all around the word,with few exceptions [17]. These exceptions occur mostly at sites adjacent to oceanic waters[13], which is not the case for the Mediterranean Sea. The increase of epibenthic species

Figure 6. Trends of z coefficient with respect to bottom depth and distance from shore at ventand non-vent sites. Values of z coefficient, calculated from the species/samples curves (see Figure 4and Table 2), are taken as a non-dimensional measure of species richness.



diversity around the vents at Milos is in marked contrast to the decline in diversity amongthe infauna [68]. The latter is probably due to the increasingly lethal physical and chemicalconditions with increasing sediment depth [49], such that infaunal organisms are unableto burrow deeper in order to escape unfavourable conditions such as storms. A similarsituation was seen at a shallow water cold-seep site where sediment cementation preventeddeep burrowing [69].

Figure 7. Mean (�SE) number of species belonging to the different phyla of sessile organisms(in taxonomic order) at vent and non-vent sites.

Figure 8. Mean (�SE) ratio in the number of unitary to clonal species of sessile organisms at ventand non-vent sites.



Results of correspondence analysis indicated that proximity to the vents was the majorfactor in determining the species composition of the sessile epibenthic assemblages atMilos, playing a greater role than depth (within the range 2–45m) and distance fromthe shore (0.2–5 km). What are the possible mechanisms for the influence of vent activityon sessile epibenthos? Based on our own observations and data, together with a shortreview of the literature, we offer seven hypotheses.

Hypothesis 1: intermediate disturbance

Temporal and spatial instabilities of active venting are known to exert a key rolein structuring vent communities [70]. Early underwater observations at shallow vents inthe Aegean [71] suggested a high species variability in space and time due to thedisturbance caused by suspended colloidal sulphur. Episodic changes in ventingtemperature and water chemistry have been described at Milos [72,73]. The hydrothermalbrine seeps [49] result in the deposition of a layer, up to 3 cm thick, of sulphur and silicaon the seabed, before being periodically dispersed by wave action during high winds;in some years, but not in others, the coating, with sulphur and/or silica deposits, of sessileorganisms on reefs was observed [68].

Disturbance can be expected to favour unitary organisms as compared to clonalorganisms [54], which is consistent with the proportionally higher number of unitaryspecies observed at the Milos vent sites. Molluscs and annelids, which were found to besignificantly species-richer at vent sites, exhibit a greater adaptation, than many othergroups, to varying supplies of oxygen [3,75]. High mortality rates have been observedat deep-sea hydrothermal vents [76]. Events of explosive volcanic submarine activityhave been recorded at shallow hydrothermal vents in the Aeolian Islands, Italy [77,78]. AtMilos, evidence of high mortality at vent-sites was found in serpuloidean polychaetes [37],bryozoans (unpublished observations) and the seagrass Cymodocea nodosa [68]. Highor frequent mortality would indicate that vent activity acts as an intermediate disturbanceto epibenthic communities, allowing for coexistence of a larger number of species.

Hypothesis 2: higher winter temperature favours the occurrence of warm-water species

Temperature time series taken at Milos on the sea floor at vent sites showed that wintertemperature was about 1�C higher on average than in a corresponding non-vent site; theminima (in February) were up to 3.4�C higher [72]. These conditions favoured thesettlement and persistence of warm-water species, especially among macroalgae [78]but also among hydroids and bryozoans [34]. This is consistent with the notion that aminimum temperature above 15�C is needed for the survival of species with tropicalaffinity (either native or alien) within the Mediterranean [79].

The alien tropical species found near vents include Red Sea immigrants, represented bythe seaweed Stypopodium schimperi [80], the hydroid Clytia linearis [36], the bryozoanHippopodina feegeensis [34], and the opisthobranch Melibe fimbriata [81] at Milos ventsites, by 14 foraminiferal species at a vent site off Kus� adasi, Turkey [82], and by theseagrass Halophyla stipulacea at vent sites in the Tyrrhenian Sea, western Mediterranean[83]. The addition of alien species to the regional pool may imply increased species richness,although the risk of competitive exclusion of native species has been envisaged [84].



Hypothesis 3: venting generates bottom roughness thus increasing habitat heterogeneity

The positive relation between physical heterogeneity of the habitat and species richness hasbeen widely demonstrated [85,86], and has been long known in the case of marine benthos[87–90]. Bottom currents at the Milos vent sites were weak [91,92] and the outflow fromhydrothermal springs thus has an important influence on water movement. This would beespecially marked at reefs, where rocky walls and overhangs create confined environmentsthat can retain water cells with different physical and chemical characteristics [67].Previous research has shown that in areas with reduced water motion, such as depressionsand hollows, venting activity exerts a major influence [27].

Rising gas bubbles [93–95] and hydrothermal water plumes [96] entrain bottom water,producing complex patterns in stratified water; under stratified conditions, horizontallayers of water form, with different concentrations of chemicals and particulates [97]. Thishas been observed on echosounder records [13] and will cause sessile organisms occupyingslightly different depths on a rock face to be exposed to different conditions. Depressionsformed by gas release remove lighter sediments from the bottom, often down to hardsubstrata. Upwelling occurs over shallow depressions in the seabed so that a proportionof the upward flow is not simply due to fluid release at the vent [98].

As venting disrupts the homogeneity of the water bottom layer [99], it is conceivablethat the emission of fluids from the vents has the effect of increasing the hydraulicroughness [100], and hence the physical heterogeneity of the sea floor. Increasedheterogeneity of the environment is said to diminish the competitive superiority of clonalover unitary organisms [54], which might offer a further explanation for the proportionallyhigher number of unitary species observed at the Milos vent-sites. Environmentalheterogeneity alone may be sufficient to explain species richness, especially when thespecies–area curve parameter z equals 0.5 [61]: at Milos, z values from species–samplescurves at the vent sites were much closer to 0.5 than those at the non-vent sites (Table 2).

Hypothesis 4: habitat provision by deposition of minerals and bioconstruction

Species biodiversity generally increases with the physical complexity of the habitat in boththe marine and terrestrial environments [101–103]. The presence of bioconstructions alsoincreases biodiversity [104].

The formation of chimneys and mounds of polymetallic sulphide, anhydrite andbarite at deep-sea vents is well known to form a key habitat, if a somewhat unstable one,for vent epifauna [105]. At shallow-water vents, a variety of minerals have been shownto precipitate [16], forming mounds, chimneys and reef-like structures. This mineraldeposition is sometimes aided or caused by microbial activity, especially with respect toiron oxides/hydroxides, silica, sulphur and carbonates [106–111]. Arcobacter is probablyone of the microbes responsible for the formation of the silica-sulphur mats at Milos [112].Filamentous sulphur excreted by Arcobacter sp. is believed to aid the settlement ofalvinellid polychaetes at deep-sea vents [113].

The chemical conditions around several of the Milos vents are such that thehydrothermal brine is supersaturated with respect to calcite and calcite cementedsediments have been found [49]. The flux of methane from vents may also supportmicrobial sulphate reduction, leading to authigenic carbonate formation, both calcite anddolomite [13,110,114]. The chemical conditions near the Milos vents appear to favour thegrowth of calcifying macrobiota. Conspicuous mounds of the coralline alga Mesophyllum



lichenoides were observed near vents at Milos [38] and the scleractinian coral Madracispharensis exhibited higher cover and skeletal accretion at vent sites than at non-vent sites[39]. Habitat provision by both calcite deposition and bioconstructional organisms wouldin turn increase species richness [115], creating secondary substratum for the settlement ofencrusting organisms and numerous interstices and microcavities for the cryptic species.Many of the sessile species we found at Milos belong to one of these two categories.

These results contrast with those obtained at cold CO2 vents at Ischia, Italy, where seawater acidification has been shown to hamper the calcification of many organisms [116].The composition of hydrothermal fluids at Milos is more complex than that of the fluidsat Ischia, which are low temperature and almost exclusively enriched in CO2, with littleCH4 and H2S and no Ca. The escaping gas from the Milos vents is mainly CO2 [116] andthe escaping hydrothermal fluids are enriched in Ca to 62mM [49]. Experiments in aquariaindicated that in some species net calcification increases under high levels of pCO2

[117,118]. The coralline red alga Neogoniolithon, closely related to Mesophyllum, increasednet calcification under pCO2 levels that were 1.5–2 times higher than the ambient value,although the scleractinian coral Oculina arbuscula exhibited no response [118]. A highpCO2 in seawater may enhance the organism’s rate of photosynthesis, potentiallyincreasing the amount of energy available for converting HCO�3 to CO¼3 via pH regulationat the site of calcification. Thus, the chemical environment due to the venting can bothstimulate chemical deposition of minerals forming raised areas on the seabed and theactivity of bioconstructional organisms.

Hypothesis 5: higher recruitment

Recruitment, i.e. the addition of new organisms to the resident community, has beendemonstrated to be a diversity-maintaining mechanism in subtidal epibenthic assemblages[119]. Larvae and propagules of most epibenthic taxa have little dispersal capacity[120,121] and may be easily retained in circulation cells [122]. Fluid emission at vents givesrise to advective mechanisms [123] that may concentrate larval stages in the vicinity. Highlevels of recruitment have been observed near hydrothermal vents on the East Pacific Riseand Galapagos spreading centre [124].

At Milos, the occurrence of many small-sized individuals of some serpuloidean speciesat vent sites might suggest a similarly higher level of recruitment [37]. Oceanographicinstruments moored near to vent sites were fouled by species of hydroids, serpuloideans,bryozoans, and ascidians in great number with respect to the short deployment period [34],which also might suggest high levels of recruitment. As unitary organisms recruit moreheavily than clonal organisms [54], the observed higher number of unitary species at ventsites may also be due to this explanation.

Depressions in which seepage has stopped, due, for example, to cementation ofsubsurface fluid channels, show a reduced bottom current flow [125]. The reduction inbottom currents below a critical minimum means that depressions can be larval traps andareas of increased settlement [126].

Hypothesis 6: enhanced primary productivity

Shallow hydrothermal vents have been demonstrated to enrich the surrounding waterswith nutrients and trace elements, beside CO2 [71,127]. Enhanced primary productionhas been reported at several sites in the Pacific [62,128].



Species richness is known to be dependent on productivity [85,129] and the structureof sessile communities, in particular, has been shown to be linked to primary productivity[130]. Too high a level of productivity, however, can be a source of stress, creatinglow diversity, so that the relation between productivity and species richness should followa humped pattern [86]. The Aegean Sea is one of the most oligotrophic regions of theworld [131] and therefore a local increase in primary productivity in the vicinity of thevents might induce a higher diversity of species.

Although no increase in gross plankton production could be detected in the watercolumn near venting sites at Milos, there was a conspicuous increase in benthic diatomsand cyanobacteria around vent outlets and a high rate of photosynthesis by benthic algae[132,133]. Seagrass were abundant in Palaeochori Bay [48,53], and macroalgal covershowed higher at vent sites than at non-vent sites [43].

Hypothesis 7: diversity of food sources for the fauna

Bacterial chemosynthesis at shallow vents provides suspension-feeders with a sourceof organic matter additional to that provided by photosynthetic production [128]. TheMilos vents support giant sulphur bacteria, colourless sulphur bacteria and numerousspecies of thermophilic and hyperthermophilic bacteria and archaea [134].

Chemoautotrophic bacteria production has been shown to increase species numbersin isolated cave ecosystems [135,136]. At Palinuro, Italy, a submarine cave with ahydrothermal vent inside had an unusually rich benthic community [66,137], with speciesderiving part of their nutrition from chemosynthetically produced organic matter [138]:bacterial chemosynthesis produced 31% of the suspended material available to cavesuspension feeders [139]. In addition, the wide diversity of primary producers provides anincreased number of feeding niches for consumers, again increasing species richness.Sudden increases in vent outflow as well as storm activity will suspend benthic algae andprokaryotes, making them available to filter feeders [140].

All the sessile invertebrates we collected at Milos are suspension feeders, but thedifferent taxa exploit particles of different size using different mechanisms [141]. Spongesand cnidarians exhibited significantly higher cover at vent sites than at non-vents sites [43].Species of the same two phyla were more abundant and larger in size than usually in thehydrothermally influenced submarine cave of Palinuro [65,66]. Similarly, a considerableeffect of hydrothermalism was observed on filter-feeding epifaunal communities ofNew Guinea dominated by sponges and cnidarians [62]. Both groups grew well inhydrothermally influenced water off Ambitle Island, Papua New Guinea [142] and spongesgrew close to vent outlets at Kolbeinsey, Iceland [143]. High particulate organic matterfluxes, not related to phytoplankton biomass, were found in sediment traps at Milos [91].Fluid release draws into the vent environment bottom water enriched in benthic diatoms,bacteria, and archaea. The subsurface circulation stimulate by gas rising through thesediment will also enrich the near-vent environment with microbes from the subsurface.The addition of bacterial production to that derived from photosynthesis enlarges the size-range of particles in the water column and the quantity and variety of organic matteravailable to filter feeders in the vent environment, and therefore may well accommodatea greater number of species [29]. Aggregations of sessile suspension-feeders also occurand are typical around deep-sea vents, and are usually explained by the increasedconcentration of suspended organic matter in the near-bottom layer [144–146].



Although our study concentrated on sessile epibenthos, increased diversity of food

sources is likely to favour also the mobile fauna. Toxic substances released from vents into

the water column will, under periods of low water flow, cause the death of less tolerant

plankton species, resulting in a rain of dead organisms to the seabed [147], which may

support detritivores and scavenger. Dead fish and salps have been observed over the brine

seeps at Milos [148]. Additionally, there is evidence that fish numbers are higher close

to strong gas plumes, positioning alongside the bubble stream and using it as a feeding

station, awaiting food [149]. A similar explanation may be the cause of crabs, Carcinus

maenas, positioning themselves over methane gas bubble outlets in shallow water [69].

Final remarks

The seven different hypotheses offered are not mutually exclusive; rather, they are

complementary. The importance of multiple factors controlling biodiversity was similarly

derived from a study of benthic fauna in deep-sea canyons [150]. At Milos, the synergy

of these factors may explain why the vent sites showed an approximately 3-fold increase

in species numbers compared to the equivalent non-vent sites, at three different depths and

distances from the shore. In other venting areas, all these conditions might not be met

and diversity would be lower. For example, a higher winter temperature and enhanced

carbonate deposition may be of little relevance in the tropics, especially in areas where

venting occurs in a coral reef [142]. Disturbance may be too frequent to allow resettlement,

for example at vents with frequent eruptions of sulphur [147] and in areas with excess

fluid toxicity. In already eutrophic areas, additional production by chemosynthesis may be

a source of stress. Few studies, however, have adopted a comparative approach similar

to that used at Milos, thus the alleged low diversity at some shallow-water vent sites should

be reconsidered in comparison with equivalent control sites.Other shallow-water vent sites with varied topography, multifarious food supplies,

enhanced fluid circulation and regular habitat disturbance also exhibit, like Milos,

a greater number of species than the nearby areas, to the point to that they can be

considered as hotspots of species diversity [13]. Mediterranean shallow-water vents have

been included among the ‘priority habitats’ listed in the protocol for Specially Protected

Areas and Biological Diversity in the Mediterranean of the Barcelona Convention [151],

and similar initiatives have been taken in other seas of the world [13].Epibenthic organisms act as foundation species [152], shaping submarine landscape

and generating habitats for the associate mobile fauna. Several studies in the

Mediterranean Sea indicate that the ‘biological conditioning’ of the substratum by the

epibiota may greatly influence the associated fauna [153–157]. High diversity at vents

is therefore likely to reverberate through the whole reef community [158,159], but no

indication of such a cascade process is available at the present stage of knowledge.Increased epibenthic species richness at vents is in marked contrast to studies on the

infauna, which both at Milos [68] and elsewhere [13] showed less diversity at vents.

The sessile epibenthos interacts primarily with the water column, the infauna with the

sediment – two media with very different conditions. Meiofauna and prokaryotes, on and

within the sediment, typically exhibit a reduced number of taxa at the vent centres,

probably due to the high temperatures, and reached a maximum in numbers and diversity

on the edge of the vent influence [26,112,160,161]. The influence of shallow-water



hydrothermalism on biodiversity, therefore, depends on the ecosystem compartmentunder study.

The complex influence that venting exerts on the biota makes shallow-waterhydrothermal vents model ecosystems for testing hypotheses about the effect of globalchange on marine biodiversity and ecosystem functioning [84]. Shallow-water hydrother-mal vents emit warm water, carbon dioxide, toxic chemicals, nutrients and reducedcompounds that altogether mimic climate and human impacts [29]. They are widespreadin tectonically active areas worldwide and may provide unique opportunities for fieldobservations about biotic change and ecosystem response. Laboratory or mesocosmexperiments can deliver information about specific mechanisms but will hardly help ourunderstanding of what may happen in complex systems. Of course, vent systems maynot be taken as perfect predictors, owing to the spatial proximity of ecosystems unaffectedby their emissions; previous research at Milos [38], however, has shown that they exerttheir influence on sufficiently large spatial and temporal scales to integrate most significantcommunity processes.

Acknowledgements

We thank Roberto Danovaro, Editor in Chief of Advances in Oceanography and Limonology,for inviting us to publish this paper in his journal, and Carles Canet (Coyoacan, Mexico) and ananonymous reviewer for comments that have improved the manuscript. Colleagues from the MarineEnvironment Research Centre (La Spezia, Italy) helped with fieldwork, which has beenaccomplished in the frame of the project ‘Hydrothermal fluxes and biological production in theAegean’ and was funded by the EC under contract MAS3-CT95-0021. The University of Patrasprovided support and the Greek Ministry of Culture permission to dive at Milos. We also thankStefano Aliani (La Spezia, Italy), Chariton Charles Chintiroglou (Thessaloniki, Greece), Maria DiSanto (Genoa, Italy), Mario Mori (Ancona, Italy), Ilaria Niccolai (La Spezia, Italy), Ivor Rees(Bangor, UK) and Carol Robinson (East Anglia, UK) for information and/or advice. For CNB andCM, research on Mediterranean Sea biodiversity is partly supported by the project ‘The impacts ofbiological invasions and climate change on the biodiversity of the Mediterranean Sea’ (Italy–Israelco-operation) funded by the Italian Ministry of the Environment.

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Increased diversity of sessile epibenthos at subtidal hydrothermal vents: seven hypotheses based on observations at Milos Island, Aegean Sea