Spatial diversity of rocky midlittoral macro

ARTICLE IN PRESS Estuarine, Coastal and Shelf Science xxx (2010) 1–9

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Spatial diversity of rocky midlittoral macro-invertebrates associated with the endangered species Patella ferruginea (Mollusca: Gastropoda) of Tunisian coastline Sabiha Tlig-Zouari*, Lotfi Rabaoui, Hosni Fguiri, Moctar Diawara, Oum Kalthoum Ben Hassine Unite´ de recherche de Biologie, Ecologie et Parasitologie des Organismes Aquatiques, Campus Universitaire, Universite´ Tunis El Manar, Faculte´ des Sciences de Tunis, De´partement de Biologie, 2092 Tunis, Tunisia

a r t i c l e i n f o

a b s t r a c t

Article history: Received 26 September 2009 Accepted 8 December 2009 Available online xxx

The present study focuses on horizontal spatial variability of benthic macrofauna associated with Patella ferruginea. Thirty-six samples collected at 12 transects belonging to 4 midlittoral sites along the rocky Tunisian coastline, were examined. A total of 44 species belonging to 5 taxa were found. Multivariate analysis applied on gathered data did not show a horizontal spatial variability at small scale (between transects), but at large scale, between sites as well as sectors. Thus, three groups of communities were identified (GI: Korbous and El Haouaria; GIIa: Zembra Island and GIIb: Kelibia). The distribution of species abundance within these groups revealed that crustaceans were the most abundant taxon, due to the overwhelming dominance of Chthamalus stellatus. This substratum appeared to create favourable micro-habitats for the installation of molluscs including gastropods. Regarding the low diversity index (H’) and evenness (J), they seemed to reflect a disturbance and a demographic unbalance within these communities. The heterogeneity of substrate surface, created by C. stellatus specimens appeared to be caused by various complex interactions established between the key components of these communities in particular suspension feeders, predators, herbivorous molluscs and macroalgae. Thus, the dynamic status of each of these communities is the result of these complex interactions. Ó 2009 Elsevier Ltd. All rights reserved.

Keywords: rocky midlittoral Patella ferruginea horizontal variability Chthamalus stellatus habitat heterogeneity predators herbivorous molluscs

1. Introduction Geomorphologic heterogeneity of midlittoral rocky shores provide various types of habitats (cracks, crevices, ravines, ponds, etc.) hosting different and various life forms (Raffaelli and Hawkins, 1999; Terlizzi et al., 2002). These habitats are usually subjected to a great variability of environmental variables (e.g. wetting degree, intensity of wave action, temperature, salinity and irradiation.etc) leading to important spatial and temporal differences in macrobenthic communities characterizing these ecosystems (Terlizzi et al., 2002). In fact, these environmental fluctuations usually affect some biological processes such as recruitment, predation, magnitude of spatial distribution and trophic competition (Terlizzi et al., 2002). Abiotic and biotic factors combine together to play an important role in the functioning of this ecosystem (Dethier, 1984). They modulate the demographic parameters of communities (species richness, abundance, distribution) depending on the availability of trophic resources and habitats, and through competition and recruitment

* Corresponding author. E-mail address: [email protected] (S. Tlig-Zouari).

processes. Despite the low tide amplitudes, midlittoral of Mediterranean rocky coasts hosts several species of algae grazers and invertebrates (Benedetti-Cecchi et al., 2001). Limpets are among the most dominant grazers of this community. They have some mobility enabling them to move to search for a more abundant feeding resource (Frank, 1965). Patella ferruginea is an endemic species to the Western Mediterranean (Laborel-Deguen and Laborel, 1990) where it was once widespread. Actually, its distribution area was reduced (Cretella et al., 1994; Templado, 1997). As a consequence, P. ferruginea was considered to be in danger of extinction in this area (Cretella et al., 1994; Espinosa et al., 2007). Despite the species is subject to exploitation for food in other Mediterranean areas, it is not appreciated by Tunisians. This species is encountered in the lower midlittoral horizon exposed to wave action (Pe´re`s and Picard, 1964), just below the barnacles (Chthamalus) and slightly above the calcareous algae Lithophyllum lichenoides within a very wide horizontal band (Laborel-Deguen and Laborel, 1991). It feeds on cyanobacteria and multicellular algae, mainly encrusting algae such as Phaeophyceae, Corallinaceae and Bangiophyceae (Boudouresque et al., 1986). Patella ferruginea is usually encountered lonely and do not form dense populations (Laborel-Deguen and Laborel, 1990; Espinosa et al., 2005).

0272-7714/$ – see front matter Ó 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.ecss.2009.12.007

Please cite this article in press as: Tlig-Zouari, S., et al., Spatial diversity of rocky midlittoral macro-invertebrates associated with the endangered..., Estuar. Coast. Shelf Sci. (2010), doi:10.1016/j.ecss.2009.12.007

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S. Tlig-Zouari et al. / Estuarine, Coastal and Shelf Science xxx (2010) 1–9

In Tunisia, P. ferruginea is mainly encountered within two sectors: Gulf of Tunis and Eastern tip of Bon Cape (Kelibia) at the gulf of Hammamet (Boudouresque et al., 1986; Tlig-Zouari et al., unpublished data). The present study aims to characterize the benthic communities living in the rocky midlittoral, and associated with P. ferruginea along the Tunisian coastline, to know their spatial variability, their diversity and trophic structure in relation to environmental factors with the aim to conserve the biodiversity and in particular the endangered limpet P. ferruginea. 2. Material and methods 2.1. Sampling Taking into account the current distribution of P. ferruginea, along the Tunisian coastline, which is limited to the Gulf of Tunis (6 stations) and the peninsula of Bon Cape in Hammamet Gulf (1 station) (Tlig-Zouari et al., unpublished data), 36 samples of associated macro-invertebrates were collected, from four sites with highest P. ferruginea densities e.g. Korbous, El Haouaria, Zembra Island (Gulf of Tunis) and Kelibia (Gulf of Hammamet) (Fig. 1). At each site, three horizontal (parallel to the shoreline) transects of 10 m2 of surface (10 m length and 1 m width) were regularly carried out. They were 10 m equidistant (Laborel-Deguen and Laborel, 1990; Espinosa et al., 2005). Within each transect, sampling of macrobenthos (fauna and flora) associated with P. ferruginea was done using a plot of (50 50) cm2 of surface (Benedetti-Cecchi et al., 2001). At each transect, three quadrats were randomly sampled on rocky midlittoral. At each sample, the position of different limpet species with respect to midlittoral height was noted. Rocky substrata were carefully scratched, except for P. ferruginea specimens which were directly counted. Because of their high abundances, densities of C. stellatus were also estimated in the field, with the use of 6 quadrats of 5 5 cm2 surface, randomly carried out within each quadrat of 50 50 cm2 of surface (150 replicates) (Power et al., 2001). Samples of each replicate (50 50 cm2) were preserved in 5% formalin solution. In the laboratory, algae were separated and identified up to the species level. Faunistic samples were washed and gently sieved through a 1 mm mesh. They were thereafter identified under a binocular microscope (Olympus) and counted. Average values of species abundances were estimated from replicate made for each transect and expressed in m2. 2.2. Statistical analysis

Fig. 1. Location of the sampling localities along the Northern Tunisian coastline (Ko: Korbous, Ze: Zembra, Ha: El Haouaria, Ke: Kelibia).

Different methods, commonly used in population ecology (Tlig-Zouari and Maamouri-Mokhtar, 2008; Rabaoui et al., 2009) were used to test nul hypotheses relative to the absence of spatial variability between the different macro-benthic communities associated with P. ferruginea. The homogeneity or heterogeneity of transects was illustrated by a Bray–Curtis clustering and a non parametric multidimensional scaling (nmMDS), carried out based on the similarity index of Bray–Curtis and using the arithmetic mean ‘‘UPGMA’’ (Sneath and Sokal, 1973). One-way Analysis of similarity (ANOSIM) between transects (taken in pairs) was conducted to test the differences between the structure of the macro-benthic communities, on a larger scale, taking into account separately the following factors: ‘‘Sector’’ (1- Gulf of Tunis, 2- Gulf of Hammamet), ‘‘Site’’ (1- Korbous, 2- El Haouaria, 3- Zembra, 4- Kelibia), ‘‘Wave Action’’ (1- extremely exposed, 2- very exposed, 3- exposed), ‘‘Slope’’ (1- very high, 2- high, 3- medium), ‘‘Density of P. ferruginea’’, ‘‘Density of limpet species’’ (1- low, 2- average, 3- high), ‘‘Percentage of herbivores’’, (1- low, 2- average, 3- high), ‘‘Percentage of carnivores’’ (1- low, 2- high), ‘‘Presence/Absence of macrophytes’’ (1- present, 2- absent)

and ‘‘Environmental conditions’’ (1- protected area, 2- non protected area) (Table 1). Regarding ‘‘Wave Action’’ factor, the categories considered were estimated based on bibliographic data (Oueslati, 2004) in which the method adopted by Ballantine (1961) was used. The level of dissimilarity and the contribution of each species to the total dissimilarity among groups separated by Bray–Curtis clustering were determined using SIMPER analysis. Inter and Intra-group differences were checked by a Canonical Discriminant Analysis (CDA) taking into account the identified groups as classification variables. Descriptive ecological parameters evaluated in transect groups (discriminated by nm MDS and Bray–Curtis clustering) as well as in sites were the following: species richness (S), abundance (A), dominance, Shannon–Wiener’s diversity (H’) (Shannon and Weaver, 1963) and Pielou’s evenness (J’) (Pielou, 1966). Collected species were classified into trophic groups according to the classification available in the literature (Word, 1990; Mucha and Costa, 1999; Grall et al., 2006). Thus, the trophic groups considered in the present work are the following: Herbivores (H), Carnivores (C), Detritus feeders (Dt), Deposit feeders (Ds) and


ARTICLE IN PRESS S. Tlig-Zouari et al. / Estuarine, Coastal and Shelf Science xxx (2010) 1–9

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Table 1 Ecological characteristics of study localities hosting the limpet P. ferruginea. Site (Sector)

Density (ind m2)

Geographic position

Exposure to wave action

Slope

% of Carnivores

% of Herbivores

Environmental conditions

Density of limpets

Korbous (Gulf of Tunis) El Haouaria (Gulf of Tunis) Zembra (Gulf of Tunis) Kelibia (Gulf of Hammamet)

4.5

36 500 48.9000 N 10 340 10.4500 E

High

Non protected

High

37 30 36.3900 N 10 590 40.1300 E

Very high High

Low

3.4

Extremely exposed Very exposed

Low

Low

Non protected

Average

2.5

37 070 00.7100 N 10 480 13.4700 E

Extremely exposed Exposed

Very high High

High

High

Protected

Low

Average

High

Non protected

Average

0.83

0

00

0

00

36 50 4.66 N 11 7 6.24 E

Suspension feeders (S). The impact of algal composition on the structure of macro-invertebrate communities was conducted using Canonical Correspondence Analysis (CCA) (Ter Braak, 1986) coupling contingency matrices (macro-invertebrates species/ stations; algae species/stations) then elaborating a cross-matrix (macro-invertebrate species/macroalgae species). Multivariate analyses were performed using the PRIMER E-5 package (Clarke and Warwick, 1994) based on log (x þ 1) transformed values of abundance per m2. 3. Results 3.1. Macrophytobenthos and its spatial distribution Nine algae species were collected in different stations. The analysis of algae samples revealed a significant spatial variability with a maximum of 8 species in Zembra Island and a minimum of 4 species in Kelibia. Transects belonging to the same site presented the same algal cover. Bray–Curtis clustering, based on algae composition in different transects separated two groups (clusters) at the level 58. The first group is represented by Kelibia samples (Ke1, Ke2 and Ke3); while the second, split into two sub-groups separated El Haouaria samples (H1, H2 and H3) from those of Korbous (K1, K2 and K3) and Zembra (Z1, Z2 and Z3) (Fig. 2) which showed the highest similarity. 3.2. Macrozoobenthos and its spatial distribution Within the whole macro-invertebrate samples (9784 individuals), a total of 44 species belonging to 5 taxa were identified. Molluscs were the most dominant (45.5%), followed by crustaceans (36.4%) and annelids (9.1%). Cnidarians and echinoderms were very poorly represented (4.5%). The percentage abundance of identified taxa in different transects showed the dominance of molluscs in all samples and absence of cnidarians from the three transects of El

Fig. 2. Bray–Curtis clustering of samples based on the presence/absence of macroalgae.

Haouaria (H1, H2 and H3) and echinoderms from the transect H1 on El Haouaria (Fig. 3). Bray–Curtis clustering, on the basis of species abundances, grouped together transects of each site and separated three groups at a similarity distance of 93. The first group (GI) was presented by Kelibia and Zembra and subgrouped into GIa (samples of Kelibia: Ke1, Ke2 and Ke3) and GIb (samples of Zembra: Z1, Z2 and Z3). The second group (GII) consisted of El Haouaria samples (H1, H2, and H3) and those of Korbous (K1, K2, and K3) (Fig. 4). Non metric multidimensional scaling (nmMDS) showed a strong similarity between transect of El Haouaria and Korbous (GI) as well between those of Kelibia and Zembra (GII). It also showed an intraseparation between Kelibia samples (GIIa) and those of Zembra (GIIb) (Fig. 5). SIMPER analysis, based on the benthic species abundance, showed that average dissimilarity between different study sites ranged from a minimum of 16.10% (between Korbous and El Haouaria) and a maximum of 26.47% (between Korbous and Kelibia). It is worth noting that the species C. stellatus was the most contributing to dissimilarity as well between sectors as between sites (Appendices I and II). ANOSIM analysis revealed that ‘‘Sector’, ‘‘Site’’ and ‘‘Percentage of carnivores’’ were the most discriminating (R ¼ 1 and 0.985, respectively; p ¼ 0.10%). The other factors were not found to affect the community structure (Table 2). The factorial plan D1/D2 of the Canonical Discriminant Analysis (CDA) (Fig. 6) explained 99.99% of the total inter-group variability (99.97% for axis D1 and only 0.02% for axis D2). The variance between groups (3.8%) indicated, on the one hand, many similarities between the groups of crustaceans, molluscs, echinoderms and cnidarians (pvalue ¼ 0.195) and a dissimilarity between these taxa and annelids, especially within transects K1, K3 and H1. Intra-group variability (96.2%) reflected the existence of much dissimilarity in the spatial distribution of each group populations. This important intra-group dissimilarity may be attributed to the spatial variability of annelid

Fig. 3. Frequency distribution of encountered taxa in the different transects (Cnd: Cnidarians, Ann: Annelids, Crus: Crustaceans, Mol: Molluscs; Ech, Echinoderms).


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Fig. 4. Bray–Curtis clustering of samples based on abundances of species associated with P. ferruginea.

and crustacean abundances. The analysis of average species richness showed a spatial variability with a maximum of 35.33 in the group GI (Korbous and El Haouaria) and a minimum of 33.33 at GIIa (Kelibia) (Table 3). The examination of species composition showed that certain species were present in all groups (GI, GIIa and GIIb) e.g. the molluscs Chiton olivaceus, Thais haemastoma, Monodonta turbinata, Pisania striata, Columbella rustica, Lunatia Poliana, Littorina neritoides, Gibbula cineraria, Gibbula umbilicaris and other limpet species occupying different midlittoral levels: Patella rustica, Patella ulyssiponensis and Patella caerulea. For the pulmonate gastropod Siphonaria pectinata, this species was omnipresent in all groups, except Zembra Island (GIIb). This is also the case of several crustaceans such as Chthamalus stellatus, Clibanarius erythropus, Clibanarius misanthropus, Orchestia gammarella, Hyale perieri, Limnoria quadripunctata, Sphaeroma serratum, Carcinus mediterraneus, and some polychaeta such as Nereis falsa and Perinereis cultrifera. In addition, other species were encountered in only one group e.g. the crustacean Eriphia verrucosa (GI), the echinoderm Phyllophorus urna (GIIa) and the gastropod Fissurella nubecula (GIIa) (Appendix III). The distribution of species abundances within groups showed a different pattern than that of species richness. In fact, crustaceans were found to be the most dominant taxon in all groups. Thus, the most diversified group (molluscs) was not always the most

abundant one (crustaceans). Moreover, C. stellatus was found to be the most dominant species in all groups. It represented over 80% of total species collected. The dominance of one species in rocky midlittoral communities is the cause of low values of diversity indices. Shannon–Wiener diversity (H’) recorded within different groups ranged from 0.83 bits/individual in GI and 1.12 in GIIb. As for Pielou’s evenness, it ranged from a minimum of 0.23 bits/individual at GII and a maximum of 0.317 bits at GIa (Table 3). Concerning the trophic structure, it was represented by 13 carnivorous species (29.5%), 13 herbivorous (29.5%), 9 detritus feeders (20.4%), 6 deposit feeders (13.6%) and 3 suspension feeders (6.81%). In terms of species richness, carnivores and herbivores are more dominant within GI and GIIa groups. As for trophic structure of GIIb, it was dominated by herbivores. Suspension feeders were the less represented (Fig. 7). With respect to cumulative abundance of individuals, macro-benthic communities were clearly dominated by suspension feeders (Fig. 7). The factorial plan C1/C2 of Canonical Correspondence Analysis (CCA) (Fig. 8) showed that the algae Neogoniolithon notarisii was negatively the most strongly correlated with the canonical component C1 while macrophytes Cladophora laetivirens and Bryopsis muscosa were positively the most strongly correlated with the same axis. C1 explained 78.6% of the initial variability. The species Eriphia verrucosa, Carcinus mediterraneus, Ligia italica, Chiton olivaceus, Middendorfia caprearum, Littorina neritoides, Gibbula umbilicaris, Diodora italica, Fissurella nubecula and Phyllophorus urna most contributed negatively to the formation of the canonical axis C1; while the species Clibanarius misanthropus, Hyale Perieri, Limnoria quadripunctata, Columbella rustica, Monodonta turbinate, Mytilus galloprovincialis most contribute positively

Table 2 Impact of environmental factors on the structure of macro-invertebrate communities associated with P. ferruginea (ANOSIM).

Fig. 5. Non-metrical multidimensional scaling of transects based on abundances of species associated with P. ferruginea.

Factors

Global R

p-level

Algal Species Richness Site Sector P. ferruginea density Slope Degree of wave exposure Locality status Density of limpet species Percentage of Carnivores Percentage of Herbivores

0.488 0.985 0.552 0.552 0.098 0.488 0.077 0.31 1 0.009

0.7% 0.10% 0.90% 0.90% 18.6% 0.6% 25.9% 3.7% 0.1% 44.7%



5

negatively-correlated with the axis C2, while Orchestia gamarella, Gammarus marinus, Clibanarius erythropus most contributed positively to the canonical axis C2. 4. Discussion Macro-benthic communities were usually used as excellent indicators of direct or indirect effects of natural (climate)/anthropogenic factors on marine biodiversity (Southward et al., 2005; Hawkins et al., 2008). Our obtained results showed that P. ferruginea occupies the mid-horizon of rocky midlittoral exposed to wave action. It was encountered in association with the algae Ralfsia verrucosa and Nemalion helminthoides which appeared to be its major food source within the whole study area. These results are in agreement with the observations of Boudouresque et al. (1986). During the present study, P. ferruginea was found to share the rocky midlittoral exposed to wave action with other limpet species, similarly to the observations reported by Laborel-Deguen and Laborel (1990) in Corsica and Espinosa et al. (2006) in Ceuta. However, densities and ecological features were different compared with limpet species (Laborel-Deguen and Laborel, 1990). Limpet species showed a clear vertical stratification as follows: P. rustica occupied the supralittoral and upper layer of midlittoral with an average density of 1.9 ind m2. This species was encountered above all other limpets and seemed to be more tolerant to the duration of the exudation and desiccation. P. caerulea colonized all midlittoral horizons (higher density at the mid-horizon) sharing it with P. ferruginea. The density of its population was found to reach 8 ind m2 (Korbous) while its average density was about 4.7 ind m2. In addition to P. caerulea, midlittoral mid-horizon is also occupied by P. ferruginea (average density 2.8 ind m2) and the pulmonate gastropod Siphonaria pectinata (2 ind m2) which disappears at Zembra Island. As for P. ulyssiponensis it was found settled at the inferior midlittoral and it appeared frequently

Fig. 6. Canonical Discriminant Analysis (CDA) based on taxa identified during the present study.

to the canonical axis C1. The algae Callithamnion granulatum was negatively the most correlated with the canonical component C2; while Corallina elongata and Laurencia undulata were positively correlated with the same component. C2 explained 16.65% of the initial variability. The species Anemonia sulcata, Actinia equina, Lysidice ninetta and Sphaeroma serratum were found to be the most

Table 3 Comparison between the three groups considered: GI, GIIa and GIIb. Groups

GI

Sites

Kourbous

Transects

K1

Species Richness (S) Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups Abundance (N) Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups Shannon–Wiener index (H’) Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups Pielou’s index (J’) Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups % of Carnivores Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups % of Herbivores Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups % of Suspension feeders Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups % of Deposit feeders Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups % of Detritivores Average SD (Max–Min) - Sites Average SD (Max–Min) - Groups

37 37 37.33 0.57 35.33 2.33 1331 1264 1320.66 52.27 1178.66 159.76 0.965 1.015 0.94 0.077 0.832 0.143 0.267 0.281 0.262 0.022 0.23 0.037 24.3 24.3 24.96 1.15 26 1.46 29.7 29.7 29.43 0.46 28.2 2.42 16.2 16.2 16.06 0.23 15.56 0.69 24.3 24.3 24.1 0.34 23.53 0.88 5.4 5.4 5.36 0.057 5.52 0.29

El Haouaria K2

GIIa

GIIb

Zembra

Kelibia

K3

H1

H2

H3

Z1

38

32 34 33.33 1.15

34

1367

1018 1064 1036.66 24.19

1028

0.864

0.774 0.639 0.71 0.069

0.734

0.237

0.223 0.181 0.204 0.0212

0.208

26.3

28.1 26.5 27.03 0.92

26.5

28.9

28.1 23.4 26.96 3.15

29.4

15.8

15.8 14.7 15.06 0.63

14.7

23.7

21.9 23.5 22.96 0.92

23.5

5.3

5.25 5.9 5.68 0.37

5.9

33 33 34.66 0.57 34.66 0.57 592 587 785.66 18.87 785.66 18.87 1.104 1.072 1.125 0.053 1.125 0.053 0.316 0.306 0.317 0.016 0.317 0.016 29.4 28.6 28.86 0.46 28.86 0.46 26.5 28.6 27.9 1.21 27.9 1.21 17.6 17.1 17.22 0.28 17.22 0.28 20.6 20 20.2 0.34 20.2 0.34 5.9 5.7 5.76 0.11 5.76 0.11

Z2

Z3

Ke1

34

34 35 33.33 0.57 33.33 0.57 802 790 563 45.96 563 45.96 1.177 1.129 1.10 0.040 1.10 0.040 0.333 0.317 0.316 0.010 0.316 0.010 18.2 20 19.6 1.24 19.6 1.24 36.4 33.3 34 2.13 34 2.13 15.1 15.1 14.96 0.23 14.96 0.23 20 20 20.2 0.34 20.2 0.34 9.1 9.1 9 0.17 9 0.17

510

1.151

0.326

28.6

28.6

17.1

20

5.7

Ke2

Ke3 35

765

1.069

0.300

20.6

32.3

14.7

20.6

8.8


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Fig. 7. Percentage distribution of trophic levels in the three groups considered GI, GIIa and GIIb, based on species abundances (A) and species number (B) (C: Carnivores, H: Herbivores, S: Suspension feeders, Dt: Detritus feeders, Ds: Deposit feeders).

covered with epiphytic algae with an average density of about 3.5 ind m2. Both multivariate analysis (nmMDS and Bray–Curtis clustering) revealed a homogeneous structure of macro-invertebrate community among all transects within the same site as well as between the sites of Korbous and El Haouaria (group GI). They also showed discrimination between these latter sites and that of Zembra Island (group GIIb). Thus, these analyses applied to both macrofauna and macrophytes data allowed to separate Zembra (GIIa) and Kelibia (GIIb) in comparison with other sites. This could be attributed to its geographical position at the eastern edge of Bon Cape (ANOSIM, significant difference) and probably due to the quality and purity of water in these localities, their algal cover which is richer and more diversified. Otherwise, low inter-group variation obtained with CDA showed that encountered invertebrate taxa studied express relatively similar responses (p-value ¼ 0.195). However, the high intra-group variance seemed to indicate much dissimilarity in the distribution of annelids and crustaceans. The overall results seem to indicate a horizontal spatial variability not at small scale (between transects) but at large scale (between sites). These results are contradictory to the findings of Benedetti-Ceccchi

Fig. 8. Canonical Correspondence Analysis (CCA) based on the matrix presence/ absence of macroalgae – abundances of species associated with P. ferruginea.

et al. (2001) who found, in North-West Mediterranean, horizontal variability only at small scale. In addition, the numerical analysis of these communities showed that crustaceans are the most abundant class with respect to number of individuals. Indeed, the species C. stellatus covers almost the total surface of midlittoral rocky substratum with very high densities exceeding sometimes a thousand individuals (GI: Korbous and El Haouaria) per square meter and can even cover mussel and limpet shells. The latter seems to benefit from this epibiontic fauna (barnacle, epizoa) to camouflage and escape from predators. These results corroborate with those of Menconi et al. (1999) and Benedetti-Cecchi et al. (2001) who reported that the species C. stellatus is also the most abundant sessile invertebrate in rocky midlittoral communities in NorthWestern Mediterranean. Thus, substrata with C. stellatus, encountered in the midlittoral along Tunisian coasts, seem to create microhabitats favourable for the settlement of molluscs in particular gastropods which were more abundant (Apolinario, 1999). Furthermore, differences noted in the species composition and abundance between the three considered groups (GI, GIIa and GIIb) could be attributed to habitat complexity (Underwood, 2004). Diversity of micro-habitats is of considerable influence on the number and survival of species, particularly herbivore molluscs (Moreira, 2006). Therefore, the presence of anfractuosities pits and tide ponds on rocky shores could improve the recruitment and consequently the density of certain species (Underwood, 2004). Lapointe and Bourget (1999) reported that the heterogeneity of substrate surface could reduce the environmental stress exerted on midlittoral communities at low tide enabling the development of a greater diversity of communities (Thompson et al., 1996). This could explain the highest species richness and abundance recorded at Korbous and El Haouaria (GI) (high density of C. stellatus). In addition, differences in P. ferruginea densities, recorded between the different study sites could be matched with the availability of anfractuosities and other structures (micro-habitats) which can be used as refuge by limpets (Underwood, 1976; Chapman and Bulleri, 2003). The low values of Shannon–Wiener diversity (H’) and Pielou’s evenness (J), estimated within all groups, seem to reflect a disturbance and a demographic disequilibrium within these communities probably caused by the overwhelming numerical dominance of C. stellatus. It is worth noting that this imbalance status, due to abundances differences of certain species, in particular barnacles, is a frequent phenomenon in midlittoral populations (Hawkins and Hartnoll, 1982; Dye, 1998). Given that all sites are not significantly different with respect to ‘‘hydrodynamics’’ factor (ANOSIM: not significant difference), the dominance of C. stellatus may be attributed to other factors that may affect recruitment and survival of planktonic larvae of this species. Benedetti-Cecchi et al. (2001) reported that C. stellatus recruitment, in the Mediterranean, is under the influence of space



availability and interaction with macroalgae. Within this context, experimental studies showed that barnacle colonization may have indirect consequences on community structure of rocky coasts, with the presence of limpets. In fact, these grazers appear to facilitate the settlement of barnacles preventing monopolization of substratum by filamentous algae (Benedetti-Cecchi et al., 2001). According to Arrontes et al. (2004), the development of algae can have a direct effect on barnacles by preventing them from settling and an indirect effect by increasing the density of whelks and other predators. The latter organisms use algae as a refuge feed on limpets. The present study would suggest a complex situation: a substratum colonized by C. stellatus, a diversified but with limited cover, and a number of herbivores often greater than that of carnivores (Fig. 2). However, the latter seem to be more influential in the organization of these communities (ANOSIM: significant difference), what reflects a spatial variability of predation pressure. It is worth noting that the lowest values of diversity (H’ and J), recorded at the group GI (Korbous and El Haouaria) could be explained by the high densities of C. stellatus. As for the highest values of H’ and J, these were reported within Zembra Island (GIIb). This could be related to the diversity and abundance of algal cover. Indeed, diversity and importance of algal cover on the rocky midlittoral of this locality (Boudouresque et al., 1986) seem to indicate a certain availability of trophic resources and presence of relatively less stressed organisms. This could be related to the preservation status of this island. Considering the trophic structure, the coexistence of five trophic groups, across all populations analyzed (GI, GIIa and GIIb), would be matched with the presence of a wide range of resources available for the species inhabiting these biotopes. The latter finding seems to reflect the existence of a wide variety of ecological niches available to species (Bonsdorff and Pearson, 1999). Because of high densities of C. stellatus, considered communities (GI, GIIa and GIIb) were numerically dominated by suspension feeders. The abundance of species appeared to be regulated by food resources originating from benthic algae and nutritive particles in the water column. Within this context, suspension feeders’ dominance could be explained by the rocky nature of substratum and presence of many organic particles carried by currents which are perpetually suspended in the water column due to the hydrodynamic activity (Rosenberg, 1995). The proliferation of the suspension feeder C. stellatus could be attributed to the absence of spatial competitor (less developed algal cover) and trophic competition. In fact, the other two suspension feeders encountered in the three considered groups (GI, GIIa, and GIIb), were poorly represented e.g. the bivalve Mytilus galloprovincialis whose maximum density did not exceed 9 ind m2 and the echinoderm Phyllophorus urna which was found only at Kelibia (GIIa) with a very low density (1 ind m2). Similar to these results, previous studies showed a positive correlation between suspension feeders and predators, i.e. strong dominance of suspension feeders and significant frequency of carnivores (Menge et al., 1999; Schiel, 2004). This observation can be matched with the importance of predation intensity which is a key component in the organization of midlittoral communities (Connolly and Roughgarden, 1999; Menge et al., 1999). In fact, it regulates the interactions between benthic and pelagic species in areas with high hydrodynamics (Menge et al., 1999). Within areas where the recruitment of suspension feeders’ larvae is important, production increases and strengthens the pressure of predation (Menge et al., 1999). Predation plays also a role in the interaction between macroalgae and suspension feeders for space occupation by creating new spaces where other species can settle and live (Schiel, 2004). Fauna associated with P. ferruginea is characterized by a diversity of typical predators of limpet species (including P. ferruginea) in particular the gastropods Lunatia poliana and Thais haemastoma (the latter species is abundant in all study localities), the crabs

7

Pachygrapsus marmoratus (in Kelibia and Zembra), Carcinus mediterraneus (in all localities) and Eriphia verrucosa (in Korbous) and birds particularly gulls, which are common along these shores. Thus, natural predation seems to contribute to the depletion of this endangered species. Furthermore, the lowest frequency of herbivores was recorded at the group GI (Korbous and El Haouaria) characterized by the highest frequency of suspension feeders. According to Underwood et al. (1983), biological components of rocky substrata such as barnacles differently affect the abundance and distribution of herbivores. They modulate these parameters either by spatial competition (Underwood et al., 1983) or by the heterogeneity of substratum surface they determine (Jernakoff, 1985). Recruitment and survival of young grazers could be strengthened by crusts of barnacles (Sebastian et al., 2002). These juvenile specimens use barnacles’ tests as a shelter and take advantage of present microalgae for food (Apolinario, 1999). However, dense cover of barnacles could be a barrier for adult herbivores and larger species such as P. ferruginea, preventing them from moving to feed and/or look for a micro-habitat to use as a shelter (Steffani and Branch, 2003; Moreira, 2006). Experimental studies conducted on the migration of herbivorous molluscs showed that the migration of these animals increases mortality and decreases the shell and body mass growth with these molluscs (Underwood et al., 1983). This could explain the differences in P. ferruginea density between the study sites. In fact, the highest densities were noted at Korbous (4.5 ind m2) and El Haouaria (3.5 ind m2) where small-sized specimens were encountered (average sizes are 39.7 mm and 31.86 mm respectively). In contrast, the lowest density of P. ferruginea was recorded in Zembra Island (0.83 ind m2) where the population was dominated by large-sized specimens (average size ¼ 58.1 mm) (Tlig-Zouari et al., unpublished data). Intensive occupation of the habitat by C. stellatus would contribute to the mortality of P. ferruginea specimens preventing them to move to search for food resources. The results of numerical dominance of limpet species (Table 1) associated with P. ferruginea showed that P. caerulea is the most dominant limpet. Similar results were reported by Espinosa et al. (2006) in Ceuta. These authors reported asymmetric interspecific interactions for trophic resources between P. ferruginea and P. caerulea, and showed that the latter species is the major trophic competitor of P. ferruginea. Interspecific competition for food resources and space is a known ecological aspect in limpets (Underwood, 2004). In case of food lack, the presence of a species can have significant effects on the other (Ortega, 1985; Iwasaki, 1993). Such phenomenon could contribute to the scarcity of P. ferruginea. Thus, herbivores especially molluscs seem also to play an important role in the structure of macrofaunal assemblages associated with P. ferruginea, in rocky midlittoral along the Tunisian coasts (Hartnoll and Hawkins, 1982; Underwood et al., 1983). At the level of spatial distribution of benthic macrofauna with respect to macroalgae, CCA showed that certain macro-invertebrate species seem to have more affinity to the presence of one or two macroalgae species. These organisms seem to use these macroalgae either as a refuge to escape the stress, or as a spawning ground to reproduce, or as trophic source. Therefore, the species Ligia italica, Chiton olivaceus, Middendorfia caprearum, Littorina neritoides, Gibbula umbilicaris, Diodorus italica, Fissurella nubecula, Phyllophorus urna, Anemonia sulcata, Actinia equina, Lysidice ninetta and Sphaeroma serratum seems to develop better in Kelibia especially in the presence of the algae Neogoniolithon notarisii; while the species Clibanarius misanthropus, Hyale perrieri, Limnoria quadripunctata, Columbella rustica, Monodonta turbinata and Mytilus galloprovincialis seem to proliferate in Zembra Island in association with the alga Callithamnion granulatum and Bryopsis muscosa. Note that the


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abundance of the species Orchestia gamarella, Gammarus marinus and Clibanarius erythropus in El Haouaria seem to be in relation with the presence of the algae Laurencia undulata and Neogoniolithon notarisii. Summarizing, multivariate analysis showed a horizontal spatial variability only on a large scale, as well between sites as between sectors. Thus, habitat heterogeneity obtained at smaller scale (between transects) did not appear as a distinctive character in structuring the communities of rocky midlittoral along the Tunisian coastline. Three communities groups were identified from the analyses conducted during the present study: GI, GIIa, and GIIb. The discrimination of Kelibia and Zembra (GII) from the group Haouaria–Kourbous (GI) because they are both the most un-impacted sites, the one protected (Zembra Isalnd: GIIa) and the other in an exposed area (Kelibia: GIIb). In addition, associated macrofauna of P. ferruginea, in rocky midlittoral of Tunisian coasts, is developed on a biological substratum consisting of C. stellatus. This barnacle substrate seems to offer many micro-habitats favourable to the installation of molluscs including gastropods. Therefore, changes in density of barnacles can have both direct and indirect consequences on communities’ structure. The heterogeneity of substrate surface, created by barnacles, appears to be caused by various complex interspecific interactions established between the key components of the identified communities e.g. predators, herbivorous molluscs and macroalgae. These biological interactions are involved in the abundance regulation, diversity and structure of communities’ assemblages (Leonard, 1999; Benedetti-Cecchi et al., 2001; Araujo et al., 2005). Thus, the dynamic status of each of these communities is the result of these complex interactions (Hawkins et al., 2008). AppendixSupplementary material Supplementary material can be found, in the online version, at doi: 10.1016/j.ecss.2009.12.007 References Apolinario, M., 1999. Temporal, variations in community structure in and around intertidal, barnacle (Chthamalus challengeri Hoek) patches on a Plebby shore in Japan. Revista Brasileira de Biologia 59, 43–53. Araujo, R., Barbara, I., Sousa-Pinto, I., Quintino, V., 2005. Spatial variability of intertidal rocky shore assemblages in the northwest coast of Portugal. Estuarine Coastal and Shelf Science 64, 658–670. Arrontes, J., Arenas, F., Fernańdez, C., Rico1, J.M., Oliveros1, J., Martıńez, B., Viejo, R.M., Alvarez1, D., 2004. Effect of grazing by limpets on mid-shore species assemblages in northern Spain. Marine Ecology Progress Series 277, 117–133. Ballantine, W.J., 1961. A biologically-defined exposure scale for the comparative description of rocky shores. Field Studies 1, 1–19. Benedetti-Cecchi, L., Bulleri, F., Cinelli, F., 2001. The interplay of physical and biological factors in maintaining mid-shore and lowshore assemblages on rocky coasts in the north-west Mediterranean. Oecologia 123, 406–417. Boudouresque, C.F., Harmelin, J.G., Jeudy de Grissac, A., 1986. Le benthos marin de l’ile de Zembre (Parc National, Tunisie). GIS Posidonie Publishers, Marseille. Bonsdorff, E., Pearson, T.H., 1999. Variation in the sublittoral macrozoobenthos of the Baltic Sea along environmental gradients: a functional-group approach. Australian Journal of Ecology 24, 312–326. Chapman, M.G., Bulleri, F., 2003. Intertidal seawalls – new features of landscape in intertidal environments. Landscape and Urban Planning 62, 159–172. Clarke, K.R., Warwick, R.M., 1994. Change in Marine Communities: an Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory, Plymouth, 141 pp. Connolly, S.R., Roughgarden, J., 1999. Theory of marine communities: competition, predation, and recruitmentdependent interaction strength. Ecological Monographs 69 (3), 277–296. Cretella, M., Scillitani, G., Toscano, F., Turella, P., Picariello, O., Cataudo, A., 1994. Relationships between Patella ferruginea Gmelin, 1791 and the other Tyrrhenian species of Patella (Gastropoda: Patellidae). Journal of Molluscan Studies 60, 9–17. Dye, A.H., 1998. Community-level analyses of long-term changes in rocky littoral fauna from South Africa. Marine Ecology Progress Series 164, 47–57. Dethier, M.N., 1984. Disturbance and recovery in intertidal pools: maintenance of mosaic patterns. Ecological Monographs 54, 99–118.

Espinosa, F., Fa, D.A., Ocana, T.M.J., 2005. Status of the endangered limpet Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae) in the Algeciras bay and Gibraltar. Iberus 23 (2), 39–46. Espinosa, F., Guerra-Garcia, J.M., Fa, D., Garcia-Gomez, J.C., 2006. Effects of competition on an endangered limpet Patella ferruginea (Gastropoda: Patellidae): implications for conservation. Journal of Experimental Marine Biology and Ecology 330, 482–492. Espinosa, F., Garcıá, I.D., Garcia-Gomez, J.C., 2007. Chromosome and Cytological analysis of the endangered limpet Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae): taxonomical and monitoring implications. Journal of Conchology 39 (3), 345–354. Frank, P.W., 1965. The biodemography of an intertidal snail population. Ecology 46, 831–844. Grall, J., Le Loch, F., Guyonnet, B., Riera, P., 2006. Community structure and food web based on stable isotopes (d15N and d13C) analysis of a North Eastern Atlantic maerl bed. Journal of Experimental Marine Biology and Ecology 338, 1–15. Hawkins, S.J., Hartnoll, R.G., 1982. Settlement patterns of Semibalanus balanoides (L.) in the Isle of Man (1977–1981). Journal of Experimental Marine Biology and Ecology 62, 271–283. Hawkins, S.J., Moore, P.J., Burrows, M.T., Poloczanska, E., Mieszkowska, N., Herbert, R.J.H., Jenkins, S.R., Thompson, R.C., Genner, M.J., Southward, A.J., 2008. Complex interactions in a rapidly changing world: responses of rocky shore communities to recent climate change. Climate Research 37, 123–133. Iwasaki, K., 1993. The role of individual variability in limpet resting site fidelity and competitive ability in the organization of a local rocky intertidal community. Physiology and Ecology Japan 30, 31–70. Jernakoff, P., 1985. An experimental evaluation of the influence of barnacles, crevices and seasonal patterns of grazings on the algal diversity and cover in an intertidal barnacle zone. Journal of Experimental Marine Biology and Ecology 88, 287–302. Laborel-Deguen, F., Laborel, J., 1990. Nouvelles donneés sur la patelle geánte Patella ferruginea Gmelin en me´diterraneé. I. Statut, re´partition et e´tude des populations. II. Ecologie, biologie, reproduction. Haliotis 10, 41–62. Laborel-Deguen, F., Laborel, J., 1991. Statut de Patella ferruginea Gmelin en Me´diterraneé. In: Boudouresque, C.F., Avon, M., Gravez, V. (Eds.), Les espe`ces marines a` prote´ger en Me´diterraneé. GIS Posidonie Publishers, Marseille, pp. 119–128. Lapointe, L., Bourget, E., 1999. Influence of substratum heterogeneity scales and complexity on a temperate epeibenthic marine community. Marine Ecology Progress Series 189, 159–170. Leonard, G.H., 1999. Positive and negative effects of intertidal algal canopies on recruitment and survival of barnacles. Marine Ecology Progress Series 178, 241–249. Menconi, M., Benedetti-Cecchi, L., Cinelli, F., 1999. Spatial and temporal variability in the distribution of algae and invertebrates on rocky shores in the northwest Mediterranean. Journal of Experimental Marine Biology and Ecology 233, 1–23. Menge, B.A., Daley, B.A., Lubchenco, J., Sanford, E., Dahlhoff, E., Halpin, P.M., Hudson, G., Burnaford, J.L., 1999. Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecology Monographs 69 (3), 297–330. Moreira, J., 2006. Patterns of occurrence of grazing molluscs on sandstone and concrete seawalls in Sydney Harbour (Australia). Molluscan Research 26 (1), 51–60. Mucha, A.P., Costa, M.H., 1999. Macrozoobenthic community structure in two Portuguese estuaries: relationship with organic enrichment and nutrient gradients. Acta Oecologia 20, 363–373. Ortega, S., 1985. Competitive interactions among tropical intertidal limpets. Journal of Experimental Marine Biology and Ecology 90, 11–25. Oueslati, A., 2004. Littoral et ameńagement en Tunisie. Des enseignements de l’expe´rience du vingtie`me sie`cle et de l’approche geóarcheólogique a` l’enqueˆte prospective. Orbis, Tunis, ISBN 9973-51-570-6. 530 pages. Pe´re`s, J.M., Picard, J., 1964. Nouveau manuel de bionomie benthique de la Mer Me´diterraneé. Recueil Travaux de la Station Marine d’Endoume 31, 5–137. Pielou, E.C., 1966. The measurement of diversity in different types of biological collections. Journal of Theorical Biology 13, 131–144. Power, A.M., Myers, A.A., O’Riordan, R.M., McGrath, D., Delany, J., 2001. An investigation into rock surface wetness as a parameter contributing to the distribution of the intertidal barnacles Chthamalus stellatus and Chthamalus montagui. Estuarine Coastal and Shelf Science 52, 349–356. Rabaoui, L., Tlig-Zouari, S., Cosentino, A., Ben Hassine, O.K., 2009. Associated fauna of the fan shell Pinna nobilis (Mollusca: Bivalvia) in the northern and eastern Tunisian coasts. Scientia Marina 73 (1), 129–141. Raffaelli, D., Hawkins, S.J., 1999. Intertidal Ecology. Kluwer Academic Publishers, Dordrecht. Rosenberg, R., 1995. Benthic marine fauna structured by hydrodynamic processes and food availability. Netherland Journal of Sea Research 34 (4), 303–317. Schiel, D.R., 2004. The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons. Journal of Experimental Marine Biology and Ecology 300, 309–342. Sebastian, C.R., Steffani, C.N., Branch, G.M., 2002. Homing and movement patterns of a South African limpet Scutellastra argenvillei in an area invaded by an alien mussel Mytilus galloprovincialis. Marine Ecology Progress Series 243, 111–122. Shannon, C.E., Weaver, W., 1963. The Mathematical Theory of Communication. University of Illinois Press, Urbana. Sneath, P.H.A., Sokal, R.R., 1973. Numerical Taxonomy. The Principles and Practice of Numerical Classification. WWH Freeman and Company, San Francisco. Southward, A.J., Langmead, O., Hardman-Mountford, N.J., Aiken, J., 2005. Long-term oceanographic and ecological research in the Western english channel. Advances of Marine Biology 47, 1–105.


ARTICLE IN PRESS S. Tlig-Zouari et al. / Estuarine, Coastal and Shelf Science xxx (2010) 1–9 Steffani, C.N., Branch, G.M., 2003. Spatial comparisons of populations of an indigenous limpet Scutellastra argenvillei and an alien mussel Mytilus galloprovincialis along a gradient of wave energy. South African Journal of Marine Science 25, 195–212. Templado, J., 1997. La lapa ferruginea. Biologica 6, 80–81. Ter Braak, C.J.F., 1986. Canonical correspondence analysis: a new eigen vector technique for multivariate direct gradient analysis. Ecology 69, 69–77. Terlizzi, A., Fraschetti, S., Guidetti, P., Boero, F., 2002. The effect of sewege discharge on shallow hard substrate sessile assemblages. Marine Pollution Bulletin 44, 544–550. Thompson, R.C., Wilson, B.J., Tobin, M.L., Hill, A.S., Hawkins, S.J., 1996. Biologically generated habitat provision and diversity of rocky shore organisms at a hierarchy of spatial scales. Journal of Experimental Marine Biology and Ecology 202, 73–84.

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Tlig-Zouari, S., Maamouri-Mokhtar, F., 2008. Macrozoobenthic species composition and distribution in the Northern lagoon of Tunis. Transitional Water Bulletin 2, 1–15. Underwood, A.J., Denley, E.J., Moran, M.J., 1983. Experimental analysis of the structure and dynamics of mid-shore rocky intertidal communities in New South Wales. Oecologia 56, 202–219. Underwood, A.J., 1976. Analysis of patterns of dispersion of intertidal prosobranch gastropods in relation to macroalgae and rock-pools. Oecologia 25, 145–154. Underwood, A.J., 2004. Landing on one’s foot: small-scale topographic features of habitat and the dispersion of juvenile gastropods. Marine Ecology Progress Series 268, 173–182. Word, J.Q., 1990. The Infaunal Trophic Index. A Functional Approach to Benthic Community Analyses. University of Washington, Seattle, 297 pp.
