benthic colonization and succession on temperate sublittoral rocky cliffs
TRANSCRIPT
Journal of Experimental Marine Biology and Ecology 382 (2010) 145–153
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Journal of Experimental Marine Biology and Ecology
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Benthic colonization and succession on temperate sublittoral rocky cliffs
Chryssanthi Antoniadou ⁎, Eleni Voultsiadou, Chariton ChintiroglouSchool of Biology, Department of Zoology, Aristotle University of Thessaloniki, Gr-54124, Greece
⁎ Corresponding author.E-mail address: [email protected] (C. Antoniadou
0022-0981/$ – see front matter © 2009 Elsevier B.V. Aldoi:10.1016/j.jembe.2009.11.004
a b s t r a c t
a r t i c l e i n f oArticle history:Received 26 June 2009Received in revised form 29 October 2009Accepted 5 November 2009
Keywords:Aegean SeaColonizationEcological successionHard substratumMediterraneanSublittoral
Patterns of benthic colonization and succession were investigated on a temperate rocky cliff (Aegean Sea,Eastern Mediterranean). Cement and ceramic panels deployed on the rocky substratum at 25–30 m depthwere sampled every 3 months over a 2-year period yielding 28 floral and 156 animal species. Diversity, coverand abundance had low values at short immersion periods and increased at the long ones. The vagile faunaresponded to the increasing habitat complexity offered by the development of algal turfs and sessile species,and the community structure remained highly dynamic. Unlike the duration of immersion, the type ofsubstratum didn't affect species colonization except for decapods that showed a preference for cementpanels. Three to four stages of succession were recorded over immersion periods, according to vagile andsessile biota, respectively, during which species richness and abundance increased. The structure of thedeveloped communities on both artificial materials differed from the natural algal-dominated benthiccommunity of the same area, suggesting that the recovery of rocky shore communities on temperate cliffs istime consuming.
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1. Introduction
Ecological succession is a fundamental process in marine ecosys-tems, involving significant modifications in community structure andfunction. These modifications can be summarized as a floristic andfaunistic substitution, an increase of biodiversity, abundance andbiomass, and a shift from r- to K-life strategy (Odum, 1993). The entireprocess is slow, continuous and perceptible over a long time scale,commonly interrupted by local natural disturbances of varyingmagnitude. Accordingly, benthic communities can be viewed as amosaic of patches of different successional stages (Menge, 1975;Olabarria, 2002; Bulleri and Benedetti-Cecchi, 2006).
The first attempts to describe ecological succession in marineecosystems appeared in the middle of the previous century (Weiss,1948; Huve, 1960). Afterwards, much effort has been devoted inunderstanding the processes of succession in the shallow sublittoralzone (Dean and Hurd, 1980; Vance, 1988; Maughan and Barnes, 2000;Watson and Barnes, 2004; Bulleri, 2005; Bowden et al., 2006; Fieldet al., 2007), as well as in restoring hard substratum communities(Duval et al., 1982; Fitzhardinge and Bailey-Brock, 1989; Svane andPetersen, 2001; Manoudis et al., 2005). A number of studies coveredthe intertidal zone attributing the observed succession patterns to theeffects of animal predation, grazing or competition for space (Deanand Connell, 1987a,b,c; Anderson and Underwood, 1994; Benedetti-
Cecchi and Cinelli, 1996; Jacobi and Langevin, 1996; Brown andSwearingen, 1998; Olabarria, 2002; Foster et al., 2003).
In spite of all the above efforts, the mechanisms of succession inthe marine environment are not yet fully understood, since i) moststudies examine the colonization of artificial substrata by sessile biotaonly (Olabarria, 2002), ignoring the vagile fauna, ii) intertidalhabitats, where a large number of studies have been conducted,are peculiar environments in which a limited number of species isadapted to live (Jackson, 1977), iii) the subtidal zone has been onlypartly surveyed focussing on its shallower part (but see Hunt et al.,2004 who studied colonization at deep-see hydrothermal vents), andiv) different types of artificial substrate, a factor influencing theoutcome of the process (Field et al., 2007), have been used in differentstudies without comparing results. Consequently, additional infor-mation from deeper sublittoral communities is required (Fraschetti etal., 2003) examining both sessile and vagile organisms settling ondifferent artificial substrates, in order to comprehend the generaltrends and underlying principles of succession in the marineenvironment.
Considering all the above, the main goal of the present study wasto provide comprehensive data on the structure of macrobenthiccommunities following initial colonization on a temperate rocky cliff,at depths of 25–30 m, by monitoring both sessile and vagile biota fortwo annual cycles, using settlement panels of different material. Theabove task was accomplished by taking the following assumptions asworking hypotheses: (1) succession process follows different ratethrough time, which predicts that the structure of the developingcommunity will be relatively stable over time (low rate) with periodsof rapid changes (fast rate) and thus different stages of succession
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could be identified according to the structure of the developingcommunity — this hypothesis was motivated by similar resultsreported from the intertidal and shallow sublittoral zones (Hirata,1987; Rapp de Eston and Bussab, 1990); (2) colonization andsuccession processes are expected to differ with respect to the typeof substratum (Anderson and Underwood, 1994; Field et al., 2007);and (3) the structure of the advanced community stages on theexamined artificial materials is similar to the structure of the algal-dominated community naturally present over the study area — thiswas tested in order to assess the recovery rate of rocky shore benthiccommunities (Foster et al., 2003).
2. Materials and methods
2.1. Study site
The study was conducted in Porto Koufo Bay (N 39° 57.44' E 23°55.09') located in the North Aegean Sea, EasternMediterranean (Fig. 1).The sea bottom consists of an almost vertical (80–90° inclination)limestone rocky cliff down to a depth of 60 m. Salinities average 36.1–37.4 psu and temperature varies from lows of about 12 °C inwinter to ashigh as 22 °C in late summer (Antoniadou et al., 2004).
At the study area a photophilic algae community occurs down toabout 10 m depth; deeper it is replaced by a typical sciaphilouscommunity which is algal-dominated down to 35 m and animal-dominated below 40 m (Antoniadou and Chintiroglou, 2005, 2007). Atthe algal-dominated sciaphilous community, the red algaWomersleyellasetacea prevails forming a dense carpet, sparsely interrupted bythe presence of large sessile animals, such as sponges (Agelas oroides,Axinella cannabina, A. verrucosa, Chondrosia reniformis, Ircinia variabilis,Petrosia ficiformis, Sarcotragus foetidus, Spongia officinalis), polychaetes(Sabella spallanzanii, Serpula sp.), molluscs (Spondylus gaederopus),bryozoans (Myriapora truncata, Reteporella grimaldii), echino-derms (Antedon mediterraneum) and ascidians (Halocynthia papillosa,Microcosmus sabatieri). At the animal-dominated community, thealgal cover decreases consisting only of calcareous red algae (e.g.Mesophyllum expansum, Peyssonnelia sp., Lithophyllum sp,Lithothamnion sp.) and, besides the increased abundance of all theabove animal species, the presence of various anthozoans (Eunicellacavolinii, E. verrucosa, Leptopsammia pruvoti, Parazoanthus axinellae)is enhanced.
2.2. Experimental artificial panels
Square panels, 30×30×2 cm, constructed either of rough cementor ceramic, covering a 1 cm layer of soft foamed plastic, were
Fig. 1. Map of the study area ind
randomly deployed on the rocky cliff at 25 to 30 m depth, by SCUBAdiving. Each panel was fixed on the substratum with four nails,squeezing the plastic layer to ensure its homogenous attachment tothe rock. Cement and ceramic panels were arranged in pairs on therocks keeping a distance of 0.5 m from each other, at a relativelyhomogenous area covered by the red alga W. setacea, avoiding thepresence of large animal species and at a distance of at least 5 m fromother pairs of panels.
2.3. Field sampling and processing
Twenty four cement and equal number of ceramic panels weredeployed in April 1998, and surveyed for a two-year period at 3-monthintervals; thus, the panels were immersed for eight succession timelags. At each sampling time (i.e. July 1998 — 3 months of immersion,October 1998 — 6 months of immersion, January 1999 — 9 monthsof immersion, April 1999 — 12 months of immersion, July 1999 —
15 months of immersion, October 1999 — 18 months of immersion,January 2000 — 21 months of immersion, April 2000 — 24 months ofimmersion) three replicate pairs of panels, i.e. of each substratum type,were randomly collected. Panels were carefully detached from therocks by removing the nails, and were put separately in net bags of0.25 mm mesh size. Forty eight samples were totally obtained. Inthe laboratory, the upper surface of each panel was photographed inorder to estimate cover of sessile organisms, as percentage of the panelarea, and then examined under a magnifying lamp to collect sessilebiota (e.g. algae, sponges, bryozoans, ascidians). Then, the panel wascarefully scraped using a scalpel blade and the collected material wassieved (mesh opening 0.5 mm) and preserved in 8% formaldehyde–seawater solution. After sorted, all living organisms were identified tothe species level and counted.
2.4. Data analysis
2.4.1. Taxonomic diversity, cover and abundanceAnalysis of variance (two-way balanced ANOVA) was used to test
the effect of substratum type (two-level fixed factor), time lag ofimmersion (eight-level fixed factor), and their interaction on theaverage abundance of vagile fauna and each dominant taxonomicgroup separately, through a general linear model (Underwood, 1997).Prior to the analyses, the homogeneity of variances was testedwith Cohran's test and, when necessary, data were transformed tolog(x+1). The Fisher LSD test was used for post hoc comparisonswhen appropriate. ANOVAs were performed using the SPSS softwarepackage.
icating sampling field (dot).
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Diversity, expressed in terms of species number (S), and diversityindices estimated for the vagile biota, i.e. Margalef's richness,Shannon–Wiener and Pielou's evenness (based on log2) were alsotested using the samemodel of ANOVA. Τhe relationships of the vagileand of sessile species number with the cover of the latter wereassessed using a linear regression analysis.
2.4.2. Temporal changes in communities — succession patternsIn order to examine changes in species composition during
colonization and ecological succession process, the species found ateach time lag of immersion were grouped into three categories:(1) new, the novel settlers at each time lag, (2) old, which alsoappeared at the previous time lag of immersion, and (3) extinct,which appeared at the previous time lag of immersion and eventuallyvanished. The relation of the abundance of these three categories withtime lag of immersion was assessed using non parametric Spearmanrank correlation (SR).
Multivariate analyses were used to compare the similarity ofbenthic communities developed on the panels with respect to thetime lag of immersion (i.e. among samplings). Sessile and vagilespecies were treated separately on the basis of cover and numericalabundance data, respectively. Non-metric multidimensional scaling(nMDS) via Bray-Curtis distances on log transformed data was used tovisualise changes in species composition across time lags ofimmersion. Analysis of similarity (ANOSIM) was used to test fordifferences in composition of the community between the twotypes of artificial substrata (2-level) and across periods of immersion(8-level). SIMPER was used to identify the species responsible for anydifferences between the biotic patterns observed on the two types ofartificial substrata through immersion times. Multivariate analyseswere performed using the PRIMER software package (Clarke andWarwick, 2001).
Table 1Number of species collected from the deployed panels at the study site and the surroundin
Taxonomic group Species number
Ceramic panels Cement panel
Time lag of immersion Total Time lag of im
3 6 9 12 15 18 21 24 3 6 9
Chlorophyta 2 1 1 3 1Phaeophyta 2 1 1 1 2 2 1 2 3 2 2 1Rhodophyta 4 6 7 4 6 6 4 7 15 5 8 9Porifera 1 1 1 1 1 1 1 1 1CnidariaNematoda + + + + +Polychaeta 2 9 6 7 6 14 14 20 26 4 9 9Sipuncula 1 1 2 2 2 2 1Polyplacophora 1 1 1 2 3Bivalvia 3 4 4 10 6 6 9 8 14 3 7 3Gastropoda 6 7 10 11 11 16 26 19 37 10 8 11Brachiopoda 1 1 1 2 2 2 1 1Cirripedia 1 1 1Ostracoda 1 1Copepoda + + + + + +Amphipoda 3 2 3 10 5 9 7 8 14 5 4 8Tanaidacea 1 1 1 1 1 1 1 1 1 1Isopoda 1 1 1 3 1Cumacea 1 1 3 2 1 3 1Mysida 1 1 1Decapoda 1 4 2 2 2 7 4 5 10 2 7 6PycnogonidaStenolaemata Bryozoa 3 4 3 3 3 3 3 3 4 2 3 3Gymnolaemata Bryozoa 2 3 7 5 2 5 4 5 8 2 2 4OphiuoroideaEchinoidea 1 1 1 2 2 3 1 1 1Ascidiacea 1 1 1 1 1
+Taxa not identified to species level.
2.4.3. Comparisons with the natural communityPresence or absence data of both sessile and vagile species
collected from the panels at the end of the two-year immersionperiod were compared with data on the biota found on thesurrounding rocky substrata at the study site using also nMDS andANOSIM analyses; full taxa lists for these analyses were derived fromAntoniadou and Chintiroglou (2005, 2007), who collected seasonalsamples of both sessile andmotile species from the natural reef, in thesame site and depth, using a 400-cm2 quadrate sampler by totallyscraping off the substrate.
3. Results
3.1. Taxonomic diversity, cover and abundance
Twenty-eight algae and 156 animal species were collected fromboth types of panels (Table 1). The filamentous red alga Polysiphoniastricta was the dominant species in cover over the two years of thesurvey, together with the bryozoan Lichenopora radiata and thebrown alga Dictyota fasciola var. repens at the early time lags ofimmersion, and with Sphacelaria cirrosa after 12 months of immer-sion. Total cover of panels was low (15–20%) during the first trimesterof succession. Afterwards, it reached 40% (6 to 15 months ofimmersion), whereas at the later sampling stages (18–24 months ofimmersion) ranged from 60 to 90%.
Molluscs was the most speciose (63 species, 39.7%) and abundantgroup (3802 individuals, 46.8%), followed by crustaceans (37 species,23.7%; 1463 individuals, 18.01%) and polychaetes (27 species, 17.3%;1117 individuals, 13.75%). Sixteen species, namely the polychaetesHydroides norvegicus, Nereis zonata, Pomatoceros triqueter, thesipunculan Phascolosoma granulatum, the molluscs Alvania cimex,Bittium latreillii, Caecum trachea, Hiatella arctica, Modiolus adriaticus,
g algal-dominated benthic community.
s Both artificialsubstrata
Algal-dominatednatural substrata
Both artificialand naturalsubstrata
mersion Total
12 15 18 21 24
1 1 3 3 22 2 3 2 1 3 4 5 26 7 4 5 6 17 21 16 91 1 2 2 15 2
10+ + + + + + + +12 9 14 14 16 22 27 42 212 2 2 2 2 2 2 2 2
1 2 3 3 2 211 5 4 9 5 15 15 16 1217 19 19 20 13 39 45 73 40
1 2 2 2 2 21 1 11 1 1
+ + + + + + + + +7 5 6 7 7 14 14 21 121 1 1 1 1 1 1 2 1
1 1 2 2 3 4 31 2 2 1 2 3 3 3
1 1 1 1 15 1 7 4 5 11 13 7 7
23 3 4 4 3 4 4 4 44 5 6 4 4 9 10 13 9
2 1 1 3 3 2 21 2 2 3 3 31 2 1 3 3 5 3
Table2
Two-way
ANOVAresu
ltsof
theeffectsof
thekind
ofartificial
subs
tratum
andthetimelagof
immersion
ontheav
erag
eab
unda
ncean
ddive
rsityof
theva
gile
faun
aan
dof
thedo
minan
ttaxo
nomic
grou
ps(S
=nu
mbe
rof
species,d=
Marga
lef's
rich
ness,H
=Sh
anno
n–W
iene
r,J=
Pielou
'sev
enne
ss).
Source
ofva
riation
dfMS
Fp
MS
Fp
MS
Fp
MS
Fp
MS
Fp
Taxo
nomic
grou
pPo
lych
aeta
Biva
lvia
Gastrop
oda
Peracarida
Decap
oda
Timelagof
immersion
711
97.6
5.57
0.00
113
130
2.76
0.02
312
001
2.60
0.03
014
60.5
12.47
0.00
155
3.19
9.38
0.00
1Kindof
subs
trata
11.7
0.01
0.93
385
0.08
0.77
854
00.12
0.73
412
3.5
1.05
0.31
252
6.69
8.93
0.00
4Timelag×Kindof
subs
trata
733
5.8
1.56
0.18
337
760.79
0.59
936
650.79
0.59
810
5.9
0.90
0.51
693
.64
1.59
0.17
5
Totalfau
naTF
Sd
HJ
Timelagof
immersion
746
801
5.99
0.00
199
5.7
22.75
0.00
119
.02
22.63
0.00
10.89
84.50
0.00
10.03
094.28
0.00
2Artificial
material
166
80.09
0.77
212
.00.27
0.60
40.32
20.38
0.54
0.00
10.00
10.99
70.00
390.55
0.46
2Timelag×Artificial
material
771
200.91
0.51
155
.91.28
0.29
30.94
91.13
0.37
0.17
30.87
0.54
10.00
971.35
0.26
1
Sign
ificant
differen
ces,i.e
.pN0.05
,inbo
ld.
148 C. Antoniadou et al. / Journal of Experimental Marine Biology and Ecology 382 (2010) 145–153
Vermetus triquetrus, and the crustaceans Caprella rapax, Cestopagurustimidus, Leptochelia savignyi, Lysianassa costae, Microdeutopus anom-alus, Pagurus anachoretus, showed increasing population density andwere frequently collected from the panels. Among these species, onlythe polychaete P. triqueter and the gastropod B. latreillii occurred at alltime lags of immersion. The diversity and the abundance of the vagilefauna and of each main taxonomic group separately varied signifi-cantly with time lag of immersion (ANOVA results, Table 2). Incontrast, the type of artificial panel used as substratum didn't affectspecies colonization, with one exception: decapods abundance washigher on the cement panels. Fisher LSD post-hoc tests showed thatfaunal abundance was very low at the first 3-months of immersion; itincreased at the next time lag of immersion (i.e. 6-months) andremained almost even up to the 15-months (Fig. 2). Finally, asignificant increment was recorded at the last three time lags ofimmersion (i.e. 18, 21 and 24-months). The same general pattern wasobserved when the abundance of the dominant taxa was separatelytested, with the following exceptions: (1) the abundance of bivalvespeaked at 12-months immersion and subsequent decreased tothe previously recorded levels at the next two samplings (i.e. 15and 18-months of immersion), and (2) the abundance of decapodspeaked at 6- and 18-months of immersion (Fig. 2). The diversity of thebiota, expressed in terms of species number, and the diversity of thevagile fauna, expressed through Margalef's richness, increased withtime lag of immersion, the higher values recorded at the last threetime lags of immersion (i.e. 18, 21 and 24-months). Shannon–Wienervalues (H) ranged from 3.29 to 4.56 and evenness (J) from 0.67 to0.89; the former showed low values at 9 and 15-months of immersionand a peak over the 24 months of immersion, while the latter peakedat the first 3-months of immersion (Fig. 2).
A very strong relationship was assessed between the number ofvagile species and the cover of panels (determination coefficientR2=92% and R2=80.6% for ceramic and cement panels, respectively),while the relationship of sessile species with panel cover was low(R2b1%).
3.2. Temporal changes in communities — succession patterns
Community structure changed over time due to the replacement ofsome species or the addition of new ones. The cumulative amount of‘new’, ‘old’ and ‘extinct’ species per time lag showed a similar patternfor both artificial substratum types used. A strong correlation wasobserved between time lag and number of ‘old’ species (SR=0.97pb0.05 for cement panels; SR=0.98 pb0.05 for ceramic panels),while the relationship with ‘new’ and ‘extinct’ species was weak.
Multidimensional analyses of the sessile community structureover time lags of immersion discriminated four stages in thecolonization and succession process: the first including samplesfrom 3-months immersion, the second including samples from6-months immersion, the third including samples from 9, 12, 15and 18-months immersions and the fourth including samples from 21and 24-months immersions (Fig. 3). The same analysis consideringthe vagile biota discriminated three stages: the initial stage, includingthe samples from 3-months immersion, the intermediate stageincluding samples from 6, 9, 12 and 15-months immersions, and theadvanced stage including samples from 18, 21 and 24-monthsimmersions (Fig. 3). Two-way ANOSIM showed that the type ofsubstratum and the time lag of immersion significantly affectedcommunity structure of sessile biota (R=0.56 pb0.01 and R=0.95pb0.01, respectively). A pairwise test revealed increased similaritybetween 15 and 18-months and between 21 and 24-monthsimmersions. The same analysis applied on vagile biota showed thatonly time lag of immersion had a significant effect (R=0.68 pb0.01).A pairwise test revealed increased similarity between 6 and 9-months,12 and 15-months and between 18, 21 and 24-months immersions.SIMPER analysis on sessile biota showed that 2 species contributed
Fig. 2. Variability of diversity (S = number of species, d = Margalef's richness, H = Shannon–Wiener, J = Pielou's evenness) and abundance (number of individuals m−2) of thevagile fauna in total, and of each dominant taxonomic group, over time lag of immersion (bars represent standard error).
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60% of the average similarity of each stage of succession, while 2–3species contributed 60% of the average dissimilarity among the fourstages of succession (Table 3). Similarly, considering the vagile biota,2–4 species contributed 60% of the average similarity of each stage ofsuccession, while 6–11 species contributed 60% of the averagedissimilarity among the three stages of succession (Table 3).
3.3. Comparison with the natural community
About half (54.82%) of themacrobenthic species reported from thealgal-dominated community at the surrounding natural substratawere collected on the artificial panels deployed at the same site anddepth (Table 1). Eighteen algal and 38 animal species were found
Fig. 3. Non-metric multidimensional scaling ordination of community structure over time lags of immersion, based on Bray-Curtis similarity index calculated from cover and log-transformed numerical abundance data, for sessile (left) and vagile species (right), respectively (3–24=months of immersion).
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exclusively on the artificial panels; nevertheless, most of these specieshave been also reported from the area at shallower depths. Juvenilesof the bivalve Spondylus gaederopus and the sea urchin Sphaerechinusgranularis, whosemature individuals occurred over the study area andrecreationally exploited, were collected from the panels.
Multidimensional analyses of the community structure showed aclear, statistically significant (ANOSIM results, R=0. 78 pb0.1),discrimination of artificial versus natural substrata samples (Fig. 4).
4. Discussion
4.1. Diversity, cover and abundance
The filamentous Polysiphonia stricta was the first algal species tosettle on artificial panels and dominated at all time-lags of immersion,over the 2-year survey. Filamentous algal forms are generally resistantto various environmental pressures, which, in combination with theirability to reproduce vegetatively, allow fast expansion and longpersistence of their populations over large spatial scales (Connell and
Table 3Species contribution to 60% similarity within groups and/or among groups dissimilarity (I=immersion) analysing sessile and vagile biota.
Species/Taxa Sessile biota
I II III IV
88.1% 86.6% 78.6 88.1%
Polysiphonia stricta 38.46 24.69 43.28 49.16Lichenopora radiata 30.77 40.74 30.77Sphacelaria cirrosa 23.78Dictyota fasciola var. repensCeramium comptum
Vagile biota
I II
50.8% 59.0%
Bittium latreillii 28.29 50.58Caprella rapaxCestopagurus timidus 7.27CopepodaForaminiferaHydroides norvegicusLeptochelia savignyiLichenopora radiata 35.56Phascolosoma granulatumPomatoceros triqueter 7.78Spirobranchus polytrema
Slatyer, 1977; Rindi and Cinelli, 2000); hence, this morphology seemsto prevail on artificial substrata (Falace and Bressan, 2002). Thediversity and abundance of benthic organisms generally followedcover of panels; few species were collected from panels at the initialtime lags of immersion, while benthic biota was much more specioseand abound at the advanced samplings, since more and more speciesand individuals were settling during the progress of succession. Theabove pattern was produced by the vagile component of the biota,since the number of sessile species was not related to the cover ofpanels. This suggests that benthic fauna responded to increasinghabitat complexity (i.e. cover by algae and sessile fauna) offeringliving space, refuge, and food (Dean and Connell, 1987b,c; Hata andNishihira, 2002; Antoniadou and Chintiroglou, 2005).
Data from temperate areas indicate a rapid increase in speciescover that reaches 75–100% in one year, in contrast with data fromhigher latitudes, where the process is much slower (Bowden et al.,2006). Most studies report a clear dominance of a few sessile animalspecies, either solitary or colonial (Greene et al., 1983; Harms andAnger, 1983; Hirata, 1987; Watson and Barnes, 2004). However, the
samples 3-months immersion, II=6–15-months immersion, III=18, 21, 24-months
I–II I–III I–IV II–III II–IV II–IV
31.5% 46.8% 66.6% 44.3% 62.1% 40.6%
26.96 39.52 23.85 37.54 35.9136.43 10.82 19.73
29.56 33.59 26.13 31.91 26.4120.836.25
III I–II I–III II–III
59.5% 71.5% 83.5% 53.2%
41.70 36.50 34.47 26.412.01
7.63 4.16 3.682.14
10.23 5.19 7.97 6.945.73 2.64
6.20 5.74 6.173.67 2.60 3.33
3.06 3.054.58 4.46 3.36 2.04
1.98
Fig. 4. Non-metric multidimensional scaling ordination of community structure onnatural versus artificial substrata, based on Bray-Curtis similarity index calculated frompresence/absence data (S = summer, A = autumn, W = winter and Sp = springsamples of the natural substrata).
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majority of these results come from suspended panels and it has beenshown that the deployment method severely affects the outcome ofsuccession processes (Glasby, 2001; Field et al., 2007). In our case, thesubstratum reached a cover of about 70% after a 18-monthsimmersion period and it was occupied mostly by filamentous algae,on which both solitary (mostly serpulids) and colonial (mostlybryozoans) animal species coexisted. None of the large-sized sessileanimals, which are abundant in the surrounding rocky cliff, such asthe sponges Agelas oroides, Axinella verrucosa, Ircinia variabilis,were recorded during the 2-year survey. The only exception wasChondrosia reniformis, a sponge capable of extending its choanosomeover small-scale distances, which was settled partially on the rocksand partially on the edge of the panels.
With respect to the vagile fauna, very few data exist since mostsuccession studies deal exclusively with sessile species (Olabarria,2002). Molluscs appeared to be the most diverse group, followed bycrustaceans and polychaetes, as shown for the intertidal zone (Deanand Connell, 1987a). Molluscs weremainly represented by gastropodsand bivalves; the former showed a peak in abundance at 18-months ofimmersion, while the later largely fluctuated with time. Interestingly,equitability of the vagile fauna is very high at the beginning ofexperimental deployment, since none of the recorded speciesdominated at the first 3 months of immersion. Thereafter, equitabilitydropped (Pielou's evenness varied around 0.7) due to the increase inabundance of the gastropod Bittium latreillii, a fact also observed inthe surrounding benthic community (Antoniadou and Chintiroglou,2005). The variability in abundance across time lags of immersionscan be attributed to various competitive interactions among dominantspecies. For example, at the end of the experiment a decline ingastropod abundance was observed coinciding with an increment inpolychaete and peracarid abundances. The species responsible forgastropod decline is B. latreilli, which is a grazer, deposit-feeder(Gambi et al., 1992). Nereis zonatawhich is the species responsible forthe increment in polychaete abundance is omnivorous (Fauchald andJumars, 1979), whereas the relevant species for peracarids, i.e.Caprella rapax, Microdeutopus anomalus and Leptochelia savignyi, arepredators, grazers or deposit-feeders (Bellan-Santini, 1998). Accord-ingly, these species may compete for food at the developed algal-dominated community, and might have taken advantage when thedensity of B. latreilli decreased probably as a result of its life cyclelasting about 18 months and characterized by lowmortality rate up tothe adult stage and increased mortality later on (Russo et al., 2002).
4.2. Temporal changes in communities — succession patterns
During our survey, community structure was continuouslymodified by the addition of new species and disappearance of others.
The first colonizers, such as the alga Polysiphonia stricta, thepolychaete Pomatoceros triqueter, the bivalve Anomia ephippium, andthe bryozoan Lichenopora radiata have been reported among pioneerspecies in benthic colonization (Manoudis et al., 2005; Nicoletti et al.,2007). Thereafter other species, characteristic of the natural commu-nity, started to settle and the first colonizers diminished, as previouslyreported (Vance, 1988). However, almost half of the recorded speciesper sampling stage were constantly present throughout succession;their cumulative sum was highly correlated with time lag ofimmersion. In contrast, the cumulative number of ‘new’ and ‘extinct’species was independent of immersion period; the appearance of anovel species or the loss of a previously existing one seemed to bestochastic events. Such data indicate that the community developedon the studied artificial substrata is characterised by a very dynamicstructure, since immigration and extinction occurred at variousimmersion periods; similar evidence has been also provided byrelevant works (Anderson and Underwood, 1994).
Several authors have suggested that during the process ofsuccession in the marine environment, sequential stages may bediscriminated with respect to the structure of the developingcommunities (Dean and Connell, 1987b,c; Hirata, 1987; Rapp deEston and Bussab, 1990; Manoudis et al., 2005). According to thesimilarity of the benthic community structure over time lags ofimmersion, three or four stages of succession were identified,considering the vagile or the sessile component of the biota,respectively. The initial stages showed the highest dissimilaritybetween cement and ceramic plates, while the structure of developingcommunities was very similar on both materials during moreadvanced stages. Similarly, the early stages of succession have provedto be more random, whereas the later more self-organized (Menge,1975; Dean and Connell, 1987a; Anderson and Underwood, 1994).Another reason for the largely deterministic nature of the later stagesis probably the absence of further disturbances (Bowden et al., 2006).The effect of competitive interactions was probably of minorimportance at the studied temperate cliff, at least during earlysuccession. This is because, in contrast to most previous studies(Holmes et al., 1997; Manoudis et al., 2005; Bowden et al., 2006),there was always free space available and the developed communitieswere algal dominated, with a large number of vagile species living onand among algal thalli, just as in the surrounding benthic community(Antoniadou and Chintiroglou, 2005, 2007). Thus, the associatedinvertebrate fauna was probably structured in accordance with thesummation of individual responses to the changing physical structureof the sessile biota (mainly algae in our case) during succession,responding to the increasing habitat complexity (Dean and Connell,1987c).
4.3. Substratum effect
The nature of substratum can affect benthic colonization by severalspecies (Dean and Hurd, 1980; Anderson and Underwood, 1994;Bulleri, 2005; Field et al., 2007), as well as the structure of the sessilecommunity in temperate rocky cliffs (Guidetti et al., 2004). Besideschemical composition of the substratum, which can be toxic forcertain species (Leewis et al., 1989), roughness is among basicqualities (Jacobi and Langevin, 1996; Wieczorek and Todd, 1997),because it can accelerate the succession rate by successfullymimicking the complexity of natural substratum (Duval et al.,1982). Cement and ceramic are suitable materials for restorationpurposes in coastal management (Duval et al., 1982; Fitzhardinge andBailey-Brock, 1989; Leewis et al., 1989) and the panels used in thepresent study had similar rough surfaces, so their geometriccomplexity should be considered equivalent. Species richness andabundance showed insignificant differences between the cement andceramic panels and both artificial substrata tested were successfullycolonized by roughly the same species. Thus, in contrast to the
152 C. Antoniadou et al. / Journal of Experimental Marine Biology and Ecology 382 (2010) 145–153
duration of immersion, the effect of substratum type had a minoreffect on the composition of the developed communities and theoutcome of succession process. Decapods were the only taxon withsignificantly increased abundance on cement plates. Similar resultshave been reported from cement artificial reefs (Pickering et al.,1998), indicating a potential behavioural pattern of this taxon. Thetype of substratum affected mostly the initial stage of succession,since the structure of the developed communities was diversified onlyduring the first 3 months of immersion; thereafter, it was much morehomogenous. It seems that the first colonizers, mostly the sessile ones,interact and modify the substratum properties through the process ofbiological conditioning (Jacobi and Langevin, 1996; Hata andNishihira, 2002). The algal or animal cover gain importance assuccession proceeds by inhibiting or facilitating further colonization(Connell and Slatyer, 1977; Dean and Hurd, 1980; Hirata, 1987;Wieczorek and Todd, 1997; Foster et al., 2003). Accordingly, the effectof substratum can be considered as ephemeral, being important onlyat the early stages of succession (Bourget et al., 1994; Anderson andUnderwood, 1994; Jacobi and Langevin, 1996).
4.4. Comparison with the surrounding community
Almost half of the species growing naturally on the algal-dominatedcommunity at the rocky cliff were collected during succession survey,while 46more species were found exclusively on the deployed artificialpanels. Some of these species were early colonizers (e.g. Hydroidesnorvegicus, Spirobranchus polytrema, Vermetus triquetrus) but themajority colonized the substratum after the first year (e.g. Flexopectenhyalinus, Bela nebula, Securiflustra securifrons) or around the end ofthe second year of succession (e.g. Chiton corallinus, Pollia dorbignyi,Metaphoxus gruneri, Ebalia deshayesi, Liocarcinus maculatus, Paguristeseremita, Ophioderma longicauda). The basic pool of potential colonizersoccurs at the surrounding rocky environment. Which species willsuccessfully settle on the deployed panels seems to depend on variousbiotic interactions, such as predation (Brown and Swearingen, 1998;Foster et al., 2003), competition (Jackson, 1977; Hirata, 1987; Vance,1988; Benedetti-Cecchi and Cinelli, 1996; Maughan and Barnes, 2000),reproductive output and mortality (Anderson and Underwood, 1994;Brown and Swearingen, 1998; Watson and Barnes, 2004).
The succession patterns on artificial panels during the 2-yearssurvey may be used as a surrogate of the ecological succession orrecovery rate after disturbances (Foster et al., 2003). By comparing thestructure of the surrounding algal-dominated rocky-bottom commu-nity with the ones that developed on the panels, we demonstrated thelow rate of ecological succession, as their Bray-Curtis similarity reachedonly 55%. Accordingly, the recovery of algal-dominated benthiccommunities developing on temperate sublittoral rocky cliffs seem tobe time-consuming, a fact indicative of their low resilience oradjustment stability (Menge, 1975). However, the studied communityshowed low variability at both spatial and temporal scales (Antoniadouet al., 2004; Antoniadou and Chintiroglou, 2005, 2007); thus itspersistence stability can be considered high (Menge, 1975). Theseintrinsic properties of the studied community could be due to itsincreased biodiversity and structural complexity (Bellan-Santini et al.,1994; Antoniadou and Chintiroglou, 2005).
5. Conclusion
Summarizing, the following conclusion can be drown: (1) benthiccolonization and succession at the temperate rocky cliff studiedfollowed a different rate through time. This rate was probablyinfluenced by the previous colonizers, especially the sessile onesthat provided physical structure and acted as ecosystem engineershaving the potential to facilitate or inhibit further colonization.(2) The type of the available substratum seemed to be of minorimportance, at least after the early stages of succession. (3) Most of
the species settled on panels were distributed at the algal-dominatedbenthic community naturally present over the studied rocky cliff,which probably acted as a pool of potential colonizers. However, thestructure of the developed communities at the end of the experi-mental deployment remained quite different from the natural one,implying that the recovery of rocky shore communities on temperatecliffs is time consuming. (4) All the above considerations haveimportant implications for the management and restoration of rockyshore communities, and similar studies for much longer periodsseems necessary for the understanding of the mechanisms ofsuccession in the marine environment.
Acknowledgments
Wewould like to thank anonymous reviewers andDr. D. Bowden fortheir useful comments and suggestions upgrading the manuscript. [ST]
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