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Colonization Processes and the Role of Coralline Algae in Rocky ShoreCommunity Dynamics

Valentina Asnaghi, Simon F. Thrush, Judi E. Hewitt, Luisa Mangialajo,Riccardo Cattaneo-Vietti, Mariachiara Chiantore

PII: S1385-1101(14)00135-XDOI: doi: 10.1016/j.seares.2014.07.012Reference: SEARES 1276

To appear in: Journal of Sea Research

Received date: 26 September 2013Revised date: 16 July 2014Accepted date: 18 July 2014

Please cite this article as: Asnaghi, Valentina, Thrush, Simon F., Hewitt, Judi E.,Mangialajo, Luisa, Cattaneo-Vietti, Riccardo, Chiantore, Mariachiara, Colonization Pro-cesses and the Role of Coralline Algae in Rocky Shore Community Dynamics, Journal ofSea Research (2014), doi: 10.1016/j.seares.2014.07.012

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Title: Colonization Processes and the Role of Coralline Algae in Rocky Shore

Community Dynamics

Authors: Valentina Asnaghi1*

, Simon F. Thrush2, Judi E. Hewitt

2, Luisa Mangialajo

3, Riccardo

Cattaneo-Vietti4, Mariachiara Chiantore

1

1DiSTAV, University of Genoa - Corso Europa, 26 - 16132 – Genoa, Italy

2 National Institute of Water and Atmospheric Research - PO Box 11-115 - Hillcrest, Hamilton

- New Zealand

3 Université de Nice-Sophia Antipolis, Laboratoire ECOMERS, Avenue de Valrose, BP71,

06108 NICE cedex 2, France

4 DiSVA - Marche Polytechnic University – P.zza Roma 22, 60121 - Ancona, Italy

* corresponding author: valentina.asnaghi@unige.it; phone: +39 010 3538384

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Abstract

Recovery from disturbance is an important attribute of community dynamics. Temperate

rocky shores will experience increases in both the type and intensity of impacts under future

expected global change. To gauge the community response to these potential changes in the

disturbance regime it is important to assess space occupancy and the temporal dynamics of

key species over the recovery process. We experimentally disturbed replicated 1m2 plots in

the lower intertidal at 5 sites along the Ligurian rocky coast (North-western Mediterranean)

and assessed early succession processes over 18 months. To identify colonization processes

and role of key species in affecting species richness on recovery trajectories, we monitored

species composition at the cm-scale along fixed transects within the plots. Our results

highlighted the role of a limited number of taxa in driving the recovery of species richness

across sites, despite site variation in community composition. Settlement of new propagules

and overgrowth were the principal pathway of space occupancy. We detected an important

role for coralline algae, particularly the articulated Corallina elongata, in promoting the

colonization of a diverse range of colonists. The present study highlights the important role

played by calcifying coralline macroalgae as substrate providers for later colonists, favouring

recovery of biodiversity after disturbance. This pivotal role may be compromised in a future

scenario of elevated cumulative disturbance, where ocean acidification will likely depress the

role of coralline algae in recovery, leading to a general loss in biodiversity and community

complexity.

Keywords

Recovery, disturbance, colonization processes, space occupancy, coralline algae

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1. Introduction

Recovery from disturbance is an important attribute of community dynamics and is controlled

by a combination of physical and biological features, operating at different spatial scales

(Dayton, 1971; Thrush et al., 2008). Coastal ecosystems, threatened by impacts from both

marine and terrestrial activities (Halpern et al., 2008), are affected by a wide range of

disturbances associated with urbanisation, increased sediment load, global warming and ocean

acidification, and, in many locations, physical disturbance associated with extreme climatic

events, whose magnitude and frequency are expected to increase in global change scenarios

(IPCC, 2007). Recovery dynamics following a physical disturbance event will be modified if

key species in the recovery process are affected by multiple stressors (Crain et al., 2008) and,

as a consequence of impaired recovery, biodiversity loss and changes in coastal ecosystem

functioning will potentially escalate (Airoldi and Beck, 2007).

The removal of plants and animals to expose bare rock in experimental plots is a useful

simulation of severe physical disturbance on rocky reefs (Airoldi, 1998; Airoldi, 2000b;

Benedetti-Cecchi and Cinelli, 1994; Keough, 1984; Paine and Levin, 1981; Underwood,

1980). Space occupancy processes that follow disturbance result from the interaction of

colonist supply (reproduction, dispersal, recruitment), interactions among species (growth,

competition, facilitation) and variation in local abiotic conditions (Dayton, 1975; Conway-

Cranos, 2012; Crowe et al., 2013; Foster et al., 2003).

Settlement and propagation patterns of the habitat forming macroalgal taxa and their positive

or negative interactions are at the basis of the successional process in rocky reef systems.

Encrusting algae are among the first colonisers of bare rocks in euphotic marine habitats

(Dethier, 1994; Kaehler and Williams, 1997; Littler, 1972), and coralline species (encrusting

and articulated) are usually both early colonists and important understory species that are

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overgrown by other conspicuous algal taxa in established assemblages on temperate reefs

(Airoldi, 2000a; Coleman, 2003; Maggi et al., 2011). Their life-history traits allow crusts to

occupy space by the settling of new propagules and lateral vegetative propagation (Airoldi

and Virgilio, 1998; Airoldi, 2000a). Encrusting coralline algae are known to facilitate

recruitment and settlement of later colonists, providing a substrate more suitable for algal

propagules and invertebrate larvae in comparison to bare rocks, because of increased surface

rugosity (Arenas et al., 2006; Bulleri et al., 2009). In the later stages of succession, encrusting

algae can coexist with epiphytic turf or as an understory to canopies (Bulleri, 2006;

Figueiredo et al., 1997; Miles and Meslow, 1990) without being damaged. Overgrowth by turf

can limit the biomass of crusts, but does not affect their cover or fertility and does not result in

increased mortality (Bulleri et al., 2006). Turf overgrowth may have possible direct or indirect

benefits, protecting underlying crusts from abrasion, desiccation, light and heat stress or

relieving crusts from competition for primary space by outcompeting erect and canopy algae

(Airoldi, 2000a).

Algal turf, made up of a complex matrix characterised by small Corallinales, Ceramiales and

other filamentous algae, is reported to secure space by encroachment of prostrate axes from

the periphery and regrowth of surviving prostrate axes (Airoldi, 1998; Airoldi, 2000a; Airoldi,

2000b), quickly regaining spatial dominance in experimentally cleared patches and persisting

over two years after disturbance (Dayton and Tegner, 1984; Kennelly, 1987). The settlement

of coralline turfs can be facilitated by ephemeral-filamentous algae (Coleman, 2003).

Coralline and non-coralline turf forming algae can inhibit the recruitment of canopy species in

clearings caused by storms or human activities (Ambrose and Nelson, 1982; Bellgrove et al.,

2010; Connell and Russell, 2010; Dayton, 1975; Kennelly, 1987) and may drive long-lasting

changes in community structure (Benedetti-Cecchi and Cinelli, 1992; Bulleri et al., 2002).

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Inhibition is mostly due to competition for space and light, but also by chemical interactions

(Kennelly 1987).

Canopy species are reported to occupy space mostly by colonisation of propagules released in

the surroundings and are consequently affected in their attachment by physical, chemical and

hydrodynamic conditions, and by timing and location of disturbance (Airoldi, 1998; Airoldi,

2000b; Bellgrove et al., 2010). Macroalgal canopies are often important ecosystem engineers:

they may regulate community structure in a number of ways, exerting positive (i.e. providing

refuges and shelter from wave action, solar radiation, extreme temperatures or desiccation,

(Bertness et al., 1999; Figueiredo et al., 2000; McCook and Chapman, 1991) or negative (i.e.

limiting light and space availability, e.g. Kennelly, 1989; Reed and Foster, 1984) effects on

other species.

In the present study, we performed a multi-site disturbance-recovery experiment along the

eastern Ligurian coast (North-Western Mediterranean) at five sites, encompassing over 80

kilometres of coastline. Macroalgal communities of the infralittoral shallow fringe along this

stretch of coast are mainly characterised by articulated and encrusting Corallinales and turf

forming species, with the dominance of individual species varying between sites. Species of

the genus Cystoseira, canopy forming assemblages in this microtidal system (Mangialajo et

al., 2012), are generally present in the studied area and dominant in two of our sites, while in

another two they are absent (see Asnaghi et al., 2009). Nevertheless, in the sites dominated by

canopies, articulated and encrusting Corallinales and turf forming species dominate the

understory. In the Mediterranean Sea, recovery dynamics after experimental clearings are

usually monitored for a period of 1-2 years (Airoldi, 2003a; Bulleri, 2005; Bulleri and

Benedetti-Cecchi, 2006; Perkol-Finkel and Airoldi, 2010) encompassing the time scale for the

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recovery of most of the taxa, even though it is known that communities dominated by canopy

species may take longer to recover (Perkol-Finkel and Airoldi, 2010). Our work assessed

early succession processes of temperate reef communities over 18 months after the

perturbation event. We experimentally cleared 1m2 plots, much larger than those commonly

used for disturbance-recovery experiment on intertidal rocky shores (e.g. Airoldi 1998;

Airoldi 2000a; Benedetti-Cecchi 2000), in order to discount edge effects associated with

lateral growth from the plot edge.

Considering communities as a dynamic mosaic of species whose patchiness results from

microsite differences and disturbances (Pickett and White, 1985), recovery processes were

followed at a very small scale (centimetre) along fixed transects to precisely document

species-specific space occupation patterns over time. This approach allowed us to take into

account different colonization pathways and test two different hypotheses regarding space

occupation dynamics during the initial 18 months of recovery: 1) occupancy at the centimetre

scale changes through replacement/overgrowth from free propagules; versus 2) changes occur

through lateral encroachment from patches of already settled species. This small-scale

measurement approach prevents spatial variation from confounding temporal patterns in

species replacement. It also allows us to assess the biodiversity enhancement effects of early

colonists that can occur when taxa are replaced/overgrown by a larger number of species. This

locally enhanced diversity can provide a wider range of species to support recovery and

response to changing environmental condition.

2. Materials & Methods

2.1 Study area

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Sampling sites were distributed along the eastern side of the Ligurian coast: one site near

Genoa city (Pontetto - PON), one in the C zone of Portofino Marine Protected Area (Punta

Chiappa - POR), one close to Framura (FRA) and two in the A zone of Cinque Terre MPA

(Monterosso - MES and Montenero – MON) (Figure 1). Tidal range in this region is small (30

cm) and the barometric tide may dominate water level. All sampling sites exhibited similar

wave exposure and wind-driven currents, which are the major hydrodynamic forces in this

area. Sampling sites were also similar in terms of slope (around 60-70°), but showed

differences in terms of the dominant macroalgal assemblage. In particular, the local

macroalgal community in Pontetto was dominated by canopy forming species of the genus

Cystoseira, followed by Corallina elongata (articulated Corallinales; the name of this species

is currently under review, and is regarded as a taxonomic synonym of Ellisolandia elongata,

see Hind & Saunders, 2013, although Walker et al., 2009 postulate that this species from the

Mediterranean Sea may have been misidentified and may belong to Corallina caespitosa, sp.

nov.); in Punta Chiappa the dominant taxa were articulated Corallinales and fleshy red

Laurencia spp.; in Framura the assemblage was dominated by Cystoseira compressa,

articulated and encrusting Corallinales and turf forming species (made up of a complex

intricate matrix of small Corallinales, Ceramiales and other filamentous algae); in Monterosso

and Montenero algal turf and articulated Corallinales were dominant.

2.2 Disturbance recovery experiment

In each site, we created 5 experimental plots (1m X 1m) in the lower intertidal, each separated

by about 10 meters. We mechanically removed the biotic component within each plot with a

combination of high pressure water and sand blasting (at 160 bar). Within each plot we

established a fixed transect (1 cm in width), parallel to the shoreline, at mid height of the plot.

We followed the recovery process over the 1 m transect, applying the line intercept method

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and taking note of the organism present every centimetre. We classified organisms at the

lowest taxonomic resolution possible and recorded a total of 32 taxa (Appendix I). We

grouped some species that were difficult to discriminate visually in the field under groups

according to their morphological and structural characteristics. All the encrusting Corallinales

were grouped in the group “Coralline Crustose Algae (CCA)”, non-calcareous crustose were

grouped as “Encrusting algae non-Corallinales”. Jania spp. and Haliptilon spp., and all

species with a J-type surface (according to Pueschel et al., 2002) where grouped as “Thin

Articulated Corallinales”, while Corallina elongata, which has a C-type thallus and a thicker

carbonate structure (Pueschel et al., 2002) was a separate group. Small articulated

Corallinales, Ceramiales and other filamentous, mainly red, algae that create an intricate

matrix, in which is difficult to discriminate among single individuals, were grouped in the

algal turf, as reported above in section 2.1.

The plots were cleared in May 2009 (time 0). Sampling in the following 18 months occurred

every 2-3 months, a time interval considered appropriate to quantify the rate of change in

assemblage structure during succession (Bulleri et al., 2009; Mangialajo et al., 2008): time 1

(July 2009), time 2 (September 2009), time 3 (December 2009), time 4 (April 2010), time 5

(July 2010) and time 6 (September 2010). In MES and MON locations, time 3 samples could

not be collected because of unfavourable weather conditions. Data were analysed in order to

highlight recovery patterns and interactions between species that typically characterise these

macroalgal communities.

While assessing the recovery trajectories, in order to draw a more detailed picture of the

studied area, the surrounding communities were investigated by recording macroalgal cover

over visual quadrats (20 x 20 cm): 5 replicate quadrats were assessed each time at each site, in

the undisturbed area close to the experimental plots.

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2.3 Overall community recovery trajectories

Multivariate analyses were performed on taxa percent cover along transects, applying the

Bray–Curtis similarity index on untransformed data (using the Primer 6 and PERMANOVA +

β3 software). We performed a Multi-Dimensional Scaling (MDS) ordination in order to

investigate recovery trajectories at the different sites. In order to highlight the taxa that played

the major role in determining differences in community composition between each sampling

occasion, we performed a SIMPER analysis on dissimilarities between consecutive times.

2.4 Colonization processes

In order to highlight space occupation in time along transects, we considered all the plots at

any given time, because we were specifically aiming at following the fate of each individual

centimetre along the temporal trajectory. Space occupancy at the centimetre level could

change in time according to two alternative processes: i) through lateral growth from patches

of already settled species or, ii) through settlement of new propagules on already established

patches. In the former case we predict that, over time, the length of the patches would be

negatively correlated to the patch number, that should, additionally, decrease in time (i.e.

patches would merge, increasing in length and reducing in number); in the latter no changes

over time should be observed in the relationship between patch length and number and a large

number of species changes should occur at the centimetre scale. In order to discriminate

between our two alternative hypotheses, we plotted the variability of patch size (measured as

the log of the variance of patch sizes) versus patch number at time 2 and time 6 (data from all

transects from all sites: 25 data points): early during the recovery, patches should be many and

homogeneously small (i.e. variance low), while, later in the recovery, successfully settled

patches should increase in size (i.e. decrease in number), resulting in a combination of large,

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increasing patches and small, reducing patches (and variance of patch size should be large).

Such a plot of variance of patch size vs number of patches early (time 2) and later (time 6) in

the recovery should have different slopes. In order to test differences in the slope of the linear

correlations we ran a t-test between slope estimates. Additionally, in order to assess if the

number of patches varied over time in the different sites, a two-way crossed PERMANOVA

(Factors: Site, random - 5 levels; Time, random - 6 levels) was performed on untransformed

data (using the Primer 6 and PERMANOVA + β3 software) and data were visually displayed

in an interaction plot.

2.5 Transition patterns

To evaluate the role of specific taxa in driving transitions among species, we selected 5 taxa

that the multivariate analyses (SIMPER, see section 2.3 Overall community recovery

trajectories) determined were important contributors to the temporal variability and that

natural history information suggested should be important by providing substrates for other

taxa. The 5 selected taxa were Coralline Crustose Algae (CCA), Thin Articulated Coralline

(TAC, e.g. Jania rubens), Corallina elongata, Laurencia complex and algal turf. We then

calculated transitional probabilities for each of these 5 taxa between subsequent sampling

times, starting from time 2. We excluded time 1 because at this time, very close to the clearing

of the plots, the community established was composed of more than 90% by ephemeral

filamentous species (FIL).

The transitional states used were: i) taxon is present in the same place on the next sampling

occasion, or ii) former taxon is replaced/overgrown by any other taxon. When replacement

occurred, we also calculated the number of different taxa that replaced the original one within

each centimetre. We standardised the number of taxa involved in the replacement by the

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number of replacements occurring along each transect for each of the 5 selected taxa, because

we expected to find increased number of taxa with increased number of replacements. These

transitional probabilities allowed us to quantify whether taxa persisted and grew during the

recovery or if the original colonist facilitated subsequent settlement of a few or a diverse array

of taxa. In order to assess consistency in the behaviour of the selected taxa during the

recovery process in the different sites, we performed a Friedman test on the transitional

probabilities calculated for each selected taxon in the 5 sampling sites, and on the number of

taxa replacing them.

3. Results

3.1 Overall community recovery trajectories

MDS based on percent cover of all taxa recorded along transects over the experiment showed

that recovery trajectories were consistent across sampling sites (Figure 2). From time 1 (2

months after the disturbance event) to time 6 (18 months after), the recovery process slowed,

with later times being more similar to each other than the samples collected early in the

experiment. An exception is time 4 (spring 2010; 11 months after disturbance), particularly

for Pontetto and Framura sites. Seasonal related effects on the structure of macroalgal

assemblages were detected also in the surrounding undisturbed area in the visual quadrats (20

x 20 cm). Composition in the undisturbed areas differed by site but remained similar across

sampling time, with the exception of time 4 (data not shown).

SIMPER (Table 1) highlighted which taxa and groupings were mainly affecting changes in

community composition between consecutive sampling occasions. The role of ephemeral

filamentous algae in driving the shift between the first and the following sampling times was

stressed. Moreover, the SIMPER procedure pointed out that a restricted number of taxa were

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involved in the recovery process: Crustose Coralline Algae, Thin Articulated Coralline and

Corallina elongata, algal turf (as defined in section 2.1, Appendix I) and algae belonging to

the Laurencia complex. Filamentous algae mainly contributed to community dissimilarity

between time 1 (2 months after disturbance) and time 2 (4 months after disturbance); they

decreased in relevance at time 3 (7 months after disturbance) and then disappeared in the

following sampling times. Coralline species, encrusting and articulated, significantly

contributed to dissimilarity at all sampling times, particularly starting from time 2: CCA with

a consistent percentage around 15%, Corallina around 5-6%, while TAC showed contribution

around 25%, growing in relevance over time.

3.2 Colonization processes

Plotting the number of individual patches per transect with the log of the variance of patch

size at times 2 and 6 (Figure 3) allowed us to test the two alternative hypotheses; changes at

the centimeter scale occur through lateral encroachment from patches of already settled

species or through settlement of new propagules on top of already settled patches. At both

times a significant linear correlation was found between number of patches and patch size

variance, showing that as patch number increases variability in patch size decreases (rather

obviously), but, more interestingly for testing our hypothesis, the two linear correlations

estimated for the two times (early in the recovery, time 2, and later in the recovery, time 6) are

not statistically different (two-tailed t-test for differences in slope = 0.696; p = 0.489). This

provided evidence to reject the hypothesis that growth of early settled patches is the major

mechanism of species interaction during the recovery. In fact, if this was true we would have

expected an increase in variability of patch sizes between times 2 and 6, as we should expect

more large and small patches at time 6 compared to time 2. Additionally we would have

expected different slopes of the two lines.

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The PERMANOVA performed on number of patches of each transect highlighted a significant

effect of the interaction between factors Site and Time (p<0.005, Table 2), while no

differences were detected among different sites. The interaction plot (Figure 4) shows that the

number of patches in the different sites was variable over time, but no clear detectable trend

was observed.

3.3 Transition patterns

Coralline species, encrusting and articulated (Corallina, TAC, CCA), algal turf and

Laurencia, were important in terms of abundance, persistence over time and their contribution

to dissimilarity among consecutive times. For this reason, we focused on these groups in our

investigation of centimetre-scale temporal transitions. Transitional probabilities were taxon-

dependent (as displayed in Figure 5), but interestingly for most of the selected taxa temporal

patterns were similar across site (see results of Friedman test in Table 3).

None of the selected taxa exhibited a probability of remaining at the same location along the

transects larger than 0.5, this implies a high level of colonisation and overgrowth during

recovery. Corallina demonstrated transitional probabilities of remaining in the same position

throughout the recovery process ranging between 0.0 – 0.3. CCA were more conservative,

exhibiting transitional probabilities of remaining the same ranging between 0.2 - 0.5. TAC

were absent from the transects on some sampling occasions, probably due to their epiphytic

nature and seasonality. The Freidman test on these last two taxa (TAC and CCA) detected

significant differences (p< 0.05) in transitional probabilities among sites. Seasonality also

affected Laurencia complex and turf, which both exhibited low (below 0.1) and variable

probabilities of remaining the same at all sites.

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Of the selected taxa, Corallina was consistently replaced by the highest number of taxa at all

sites, particularly between time 4 and 5. CCA generally followed the same trend, but

displayed lower substitution probabilities and a larger variance among sites: it was the only

taxon for which the Friedman test recorded a significant difference among sites for both

probabilities of remaining the same and number of taxa replacing (Table 3). TAC displayed

lower number of taxa replacing, generally decreasing through the recovery process. Laurencia

was replaced by a larger number of taxa in the first stages of the recovery but values

decreased along the process. Turf, in general, was replaced by fewer taxa compared to the

other taxa, over the study.

4. Discussion

Macroalgal assemblages, dominant along North-western Mediterranean rocky coasts, are

particularly sensitive to human-induced changes and are used for ecological status assessment

under the European Water Framework Directive 2000/60/EC (Asnaghi et al., 2009;

Ballesteros et al., 2007; Mangialajo et al., 2007). Shifts between macroalgal alternative stable

states in this system have been recorded (Sala et al. 1998; Airoldi 2003a), and a loss of

canopy forming species in favor of turf and coralline algae has been observed due to human

pressure as coastal urbanization, sediment load and overfishing and is expected to increase in

the future (Airoldi, 2003b; Airoldi and Beck, 2007; Bellgrove et al., 2010; Connell, 2005;

Mangialajo et al., 2008; Sala et al., 1998).

In future scenarios of increasing disturbance, recovery potential will play a crucial role in the

maintenance of community structure and function. Recovery after disturbance is a process

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controlled by a combination of physical and biological features, operating at different spatial

scales (Thrush et al., 2008); it is the culmination of interactions between species (dominance,

inhibition or facilitation) and extrinsic factors (e.g. colonist supply and environmental setting)

(Dayton et al., 1992). Disturbance/recovery experiments represent a useful tool to assess the

dynamics characterizing community recovery and provide insight into future scenarios.

Recording space occupancy processes and the role of key species in enhancing diversity, as in

the present study, when combined with information on species sensitivity to other stressors,

can inform forecasts of possible future shifts in dominant assemblages.

Recovery trajectories, as displayed by the MDS ordination (Figure 2), indicate that recovery

rates in our sampling sites were similar, irrespective of differences between sites in resident

community structure, and driven by seasonal patterns. Such similar trajectories may be a

consequence of response to similar environmental conditions: our sites exhibited comparable

conditions in terms of slope, local wave action, wind patterns and desiccation. Sampling sites

showed similar exposition to wind and main wave action: around 50% of the waves are

derived from 210 to 225°, with the other sectors (15°) accounting equally for the remaining

waves (data from “The Medatlas Group 2004”, details are provided in Thrush et al., 2011).

Also we did not observe signs of grazing by large mollusks at any of our sites, making

negligible the stress due to grazing pressure. Nevertheless, observed similar recovery

trajectories may be a consequence of biological interactions within the plots: in fact the taxa

driving the recovery were the same in all the sites, despite difference in dominance between

sites, and displayed similar interactions in time.

In the very early stage of recovery (time 1, 2 months after disturbance) only opportunistic

green filamentous algae completely colonized the bare substrates, without any sign of

encroachment from the margins of the plots. On the subsequent sampling times, coralline

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algae (CCA, Corallina elongata and TAC), along with the Laurencia complex (Ceramiales

order) and turf algae, started to occupy the plots and gained importance in driving the

recovery process, almost completely replacing the filamentous algae. Coralline species

became abundant (more than 30% cover) 4 months after the disturbance event, and then

became spatially dominant along the transects. Laurencia became abundant after time 3 (7

months after disturbance), probably in relation to its seasonal life cycle, while turf became

relevant in time 4 (11 months after disturbance, spring time), although showing less

consistency in relative abundance across sites. These taxa were strongly involved in the

successional process, being among the species that mostly contributed to dissimilarities

between consecutive sampling times, as displayed by SIMPER results (Table 1). SIMPER

results also highlighted a pulse in settlement and post-settlement variability and a period of

higher recruitment, e.g. for Cystoseira compressa, explaining the exception observed in the

MDS for time 4 (spring 2010) particularly for Pontetto and Framura sites.

Recovery of canopy forming species inside cleared plots is a slow process and is known to be

frequently inhibited by turf forming species, which are considered to be better competitors for

space and light, and probably also chemically inhibit colonists (Connell and Russell, 2010;

Kennelly, 1987). Along Ligurian shallow rocky shores, the two most conspicuous canopy

species are Cystoseira amentacea var. stricta and Cystoseira compressa. We observed that C.

compressa managed to settle during its reproductive period (early spring) in some sites

(Pontetto and Framura), but could not maintain space occupation, indicating that in

experimentally cleared plots some community dynamics inhibiting canopy development are

occurring, most possibly concurrently with physical displacement of isolated plants due to

wave action and/or desiccation (Jenkins et al., 1999; Schiel et al., 2006). C. amentacea is

absent in most of the sites in the very eastern portion of Liguria (including our study sites in

Monterosso and Montenero), probably due to river outflows and high sedimentation (Asnaghi

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et al., 2009). Yet, this species was not able to re-colonize our cleared plots, even in the sites

where it was largely present in the surrounding undisturbed area (e.g. Pontetto). Adding to the

very limited dispersal capacity of these canopy formers (Dìez et al. 1999; Mangialajo et al.

2012; Soltan et al. 2001), our experiment highlights that local factors affecting the post-

colonization viability of individual plants are also important in habitat dominance by

Cystoseira.

The rate and the direction of the successional process are defined by the probabilities of

replacement of one species by another (Hill et al., 2002). Several studies show that inhibition

is the prevalent mode of succession on rocky shores (Sousa, 1979; Underwood et al., 1983;

Van Tamelen, 1987), although facilitation has also been documented (Bertness et al., 1999;

Turner, 1983). Interference competition (sensu Miller, 1967) among space-limited sessile

marine organisms commonly occurs through overgrowth (Jackson, 1977; Jackson, 1979),

which does not necessarily imply the definitive displacement of competitively subordinate

organisms (Airoldi, 2000b; Miles and Meslow, 1990; Underwood, 2006). The intermingling

of patch growth and overgrowth by settlement of new propagules is a phenomenon that was

observed throughout our experiment. Yet, we did not observe a shift towards less numerous

and larger patches over time, as we found that number of patches per transect did not decrease

along the recovery time (Figure 4). We also observed a similar magnitude of variability of

patch size from early to later stages (Figure 3): both results diminish the importance of lateral

growth as major space occupation mechanism in favour of settlement of propagules.

CCA are known to be slow growing organisms, that occupy bare substrates and became

dominant by enlarging prostrate discs and fusion of encrusting thalli (Dethier & Steneck,

2001; Mariath et al, 2013). Nevertheless, CCA are reported to require a certain amount of

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disturbance to reduce competition with other algae and invertebrates (Mariath et al, 2013 and

citation therein) and to have plastic responses to being overgrown (Dethier & Steneck, 2001,

Figueiredo et al, 2000): many of them represent important understory species that are

overgrown by other conspicuous algal taxa (Airoldi, 2000a; Coleman, 2003; Maggi et al.,

2011).

In our study, a clear facilitative role in diversity maintenance was detected for coralline algae,

which after settling promoted a larger number of subsequent colonists, probably by providing

favourable substrate and micro-habitat for many other species. At the centimeter scale, the

degree of replacement/overgrowth by another species was higher for Corallina and CCA than

for turf and Laurencia. TAC, which are mainly epiphytic coralline species, behaved

differently from the other corallines and showed lower probabilities of being

replaced/overgrown. This epiphytic taxon is probably more likely to be the one that

substitutes for the others (growing on the top) in its season of major expansion. Given that our

study highlighted that replacement and overgrowth following the settlement of propagules is

the main way of re-colonization of disturbed plots, the role played by coralline species as

substrate providers is pivotal in enhancing biodiversity during the recovery process. Our data

also corroborate earlier studies that indicated that the establishment of turf limits the

subsequent development of more three-dimensionally complex assemblages (Benedetti-

Cecchi and Cinelli, 1992; Bulleri, et al. 2002; Kennelly, 1987), highlighting the role of

disturbance in modulating species interactions (Airoldi, 2000a; Benedetti-Cecchi, 1993).

Our results are particularly relevant in understanding the ecological consequences of climate

change scenarios, which imply both an increased frequency of disturbance and stress to

carbonate-utilizing species due to ocean acidification (Connell and Russell, 2010; Martin and

Gattuso, 2009; Nelson, 2009). Laboratory experiments and in situ observation in naturally

acidified areas (e.g. volcanic vents) have reported that coralline algae show decalcification

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and decrease in percent cover with pH decreases (Kuffner et al., 2007; Porzio et al. 2011).

This implies these important facilitators of local diversity may be less competitive for space in

high temperature and high pCO2 conditions, leading to a shift in recovery dynamics and a

shift from dominance by calcifying organisms to fleshy algae (Kroeker et al., 2012; Wootton

et al., 2008). Such interaction between intrinsic ecological dynamics and chronic, cumulative

or multiple stressor effects can lead to the loss of resilience and increased risk of critical shifts

to less diversified and less three-dimensionally complex ecosystems (Thrush et al., 2009).

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Acknowledgments

This research was performed in the framework of a Marie Curie International Incoming

Fellowship (FP7-PEOPLE-2007-4-2-IIF-ENV221065) to SFT. Authors thank the managers of

the Portofino and Cinque Terre Marine Protected Areas for permission to work in their

reserves, and the MPAs staffs for the boat support. We thank also Sommozzatori Italia, who

performed the clearings, Punta Mesco Diving Center and all the students who helped in the

sampling. The present work is a contribution to the project COCONET.

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Figure 1

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Figure 2

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Figure 3

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Figure 4

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Figure 5

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Table 1: The contribution of observed species to the dissimilarity in community composition between consecutive

sampling occasions, based on SIMPER procedure. The time where the taxon was more abundant, between the two

consecutive times, in shown in brackets.

Taxon Time 1-2 Time 2-3 Time 3-4 Time 4-5 Time 5-6

FIL 36.57 (+T1) 12.43 (+T2)

CCA 15.37 (+T2) 16.39 14.19 (+T3) 9.38 (+T5) 15.26

TAC 10.00 (+T2) 24.49 (+T3) 21.19 (+T3) 19.64 (+T5) 27.32 (+T6)

C. elongata 3.24 (+T1) 4.68 (+T3) 6.14 (+T4) 6.91(+T4) 8.77 (+T6)

Turf

4.53 (+T2) 13.25 (+T4) 14.87 (+T4) 16.82 (+T5)

Laurencia 13.46 (+T2) 16.54 (+T3) 12.84 (+T3) 11.89 (+T5) 10.50 (+T5)

C. compressa

13.22 (+T4) 14.00 (+T4)

Table 2: Two way crossed PERMANOVA (Factors: Site, random - 5 levels; Time, random - 6 levels) performed

on the number of patches along time.

Source df SS MS Pseudo-F P(perm) Unique

perms

Site 4 1491.2 372.8 1.4254 0.246 998

Time 5 6996.8 1399.4 5.3503 0.001 999

SitexTime 20 5231 261.55 2.3257 0.004 998

Res 90 10121

112.46

Total 119 23841

Table 3: The significance of differences among sites in terms of the number of taxa replacing each of the 5

selected taxon and transitional probabilities (t.p.) of that taxon remaining the same.

Taxon

Number of taxa replacing

Friedman p-value

t. p. of remaining the same

Friedman p-value

Corallina 8.32787 0.08028 8.16438 0.08574

CCA 11.03226 0.02620 * 11.50000 0.02148 *

TAC 8.39216 0.07822 10.58824 0.03160 * Laurencia 5.91549 0.20555 6.05714 0.19492

Turf 2.92857 0.56985 4.73333 0.31577

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Highlights: Temperate rocky shore communities respond to changes in the disturbance regime We investigated key species’ strategies for space occupancy during recovery process Overgrowth played a more important role than lateral encroachment in space occupancy dynamics A limited number of taxa drive the recovery of species richness

Coralline algae enhanced biodiversity by promoting settlement of a variety of later

colonists

In bold, _p-values showing significant differences among sites (*: p< 0.05)