Factors affecting habitat occupancy of fish assemblage in the Gulf of Trieste (Northern Adriatic Sea)

Marine Ecology. ISSN 0173-9565 ORIGINAL ARTICLE Factors affecting habitat occupancy of fish assemblage in the Gulf of Trieste (Northern Adriatic Sea) Martina Orlando Bonaca & Lovrenc Lipej Marine Biology Station, National Institute of Biology, Piran, Slovenia Keywords Adriatic Sea; fish assemblage; Gulf of Trieste; habitat occupancy; shallow waters; visual census. Correspondence Lovrenc Lipej, Marine Biology Station, National Institute of Biology, Fornače 41, SI 6330 Piran, Slovenia. E-mail: lipej@mbss.org Accepted: 23 December 2004 doi:10.1111/j.1439-0485.2005.00037.x Abstract Species composition, richness and abundance of the fish assemblage were studied over six different inshore macrohabitats in the southern part of the Gulf of Trieste (Northern Adriatic Sea) using the visual counts technique. Fifteen environmental variables were taken into consideration in order to determine microhabitat preferences of fish species, using canonical correspondence analysis and electivity indices. The results suggest that the structure of the fish assemblage in shallow habitats is affected by a large number of interplaying factors. Depth, type of bottom and vegetation cover incorporating both abiotic and biotic variables are some of the factors responsible for coastal fish distribution. Microhabitat preferences for 29 fish species are presented in the depth range from 0.5 to 3 m. Problem A highly diverse fish-assemblage exists in the mediolittoral and infralittoral zones of some parts of the Mediterranean Sea, comprising species of the families Blenniidae, Gobiidae, Sparidae, and Labridae. The members of this assemblage are closely associated with the seabed and are often the dominant fish in these nearshore habitats (Gibson 1969, 1982; Dulčić et al. 1997). A number of studies have been performed on such species in the Mediterranean Sea (Harmelin 1987; Koppel 1988; Kotrschal 1988; Illich & Kotrschal 1990; Harmelin-Vivien & Francour 1992; Wilkins & Myers 1992; Francour 1994; Kovačić 1995, 1999, 2002a, b; Castellarin et al. 2001; Letourneur et al. 2003), yet the factors responsible for species density and distribution remain poorly understood. In the past, fish populations were usually estimated using specific fishing gear, mainly small trawl nets (Sogard et al. 1987), using baited traps (Beja 1995), or by poisoning with narcotics (Diamant et al. 1986; Bouchereau & Lam Hoaï 1997). Nowadays, potential deleterious impacts on the investigated ecosystems make these approaches unacceptable for intensive studies of fish assemblages; they have therefore been substituted by visual counts carried out using SCUBA diving (Harmelin 1987; Francour 1991, 1994; Harmelin-Vivien & Francour 1992; Patzner & Serrao Santos 1993; Harmelin-Vivien et al. 1995; Ciriaco et al. 1998; Mouillot et al. 1999; Castellarin et al. 2001). In the southern part of the Gulf of Trieste there is almost a complete lack of data on the coastal ichthyofauna, with a few available works (Lipej & Richter 1999; Lipej et al. 2003). Therefore, the present study aimed at testing the null hypotheses that there were no differences in species composition, species richness and abundance of fish assemblages occurring over six different shallow inshore macrohabitats, namely (i) Posidonia oceanica (L.) Delile meadow, (ii) Cymodocea nodosa (Ucria) Ascherson meadow, (iii) association with Cystoseira spp., (iv) Halopithys incurvus (Hudson) Batters and Corallina granifera Ellis & Solander settlements, (v) Wrangelia penicillata (C. Agardh) C. Agardh and Padina pavonica (L.) Thivy settlements, and (vi) boulders covered with algal turf. The microhabitat preferences among common inshore fish species are presented as well. Material and Methods 1. Study area The southern part of the Gulf of Trieste covers only a small portion of the Adriatic Sea (Fig. 1). The Slovenian 42 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage Fig. 1. Map of the study area with sampling locations (A H). coastline is approximately 46 km long. It is a shallow, semi-enclosed gulf with a maximum depth of ca. 33 m in waters off Piran. The present study was conducted in shallow waters (from 0.5 to 3 m) because benthic communities in shallow waters are generally high primary production areas with relevant secondary production, and they maintain the richest ichthyofauna (García-Rubies & Zabala 1990; Bouchereau & Lam Hoaï 1997; Methven et al. 2001). For the present research, different investigation sites were selected, described using the broad-scale for habitat types suggested by Syms (1995), and defined by a combination of depth and biogenic structure. Vegetation was defined as the major biogenic feature, and therefore the six macrohabitats selected in eight locations (Fig. 1) were: Posidonia oceanica meadow (association Posidonietum oceanicae Molinier 1958), Cymodocea nodosa meadow (association Cymodoceetum nodosae Giaccone & Pignatti 1967), association with Cystoseira spp. (ass. Cystoseiretum crinitae fac. Cystoseira barbata Molinier 1958), Halopithys incurvus and Corallina granifera settlements (ass. Cystoseiretum crinitae subass. Halopitetosum incurvae Boudouresque 1971), Wrangelia penicillata and Padina pavonica settlements, and boulders covered with algal turf. 2. Fieldwork The fieldwork was carried out using SCUBA diving and snorkeling from May to October of 2001 and 2002, during the reproductive period of most coastal fish species. Data were collected in situ using the transect technique (Harmelin 1987), a non-destructive diving visual census methodology. Horizontal transects (Macpherson 1994; Marconato et al. 1996b; Bussotti & Guidetti 1999) from 60 to 90 m in length were laid out at different depths, depending on the vegetation type on the bottom. In each range, two fixed transects were established on the bottom with meter-marks. The fish were counted mostly within 2m 2,1m 2 to the left and 1 m 2 to the right of the line. Visual transects were conducted by a pair of SCUBA divers who swam down one tape and back along the adjacent tape. In our surveys, a constant swimming speed was maintained. A sample generally took 25 min, but depended on the number of fish individuals present at each site. Species names were prelisted on a slate - the system follows the nomenclature after Whitehead et al. (1986) and Jardas (1996) - so the abundance was marked during diving. In total, 84 transects were performed in the southern part of the Gulf of Trieste, distributed over eight locations (Fig. 1). Once the visual counts had been done, a number of environmental variables were measured. A wide range of variables can be considered, although one must decide a priori the scale of habitat one wishes to examine (Copp & Garner 1995). For this study the following microhabitat variables were examined, adapted from Larsonneur (1977; in UNEP 1998): bottom substrate composition [boulders (>2 m; 2 1 m; 1 0.50 m), rocks (50 10 cm), pebbles (10 2 cm), gravel (2 0.2 cm), sand (2 0.05 mm) and mud (<0.05 mm)], water depth, and the abundance of physical structures such as macrophytes (Posidonia oceanica, Cymodocea nodosa, Cystoseira spp., Halopithys incurvus and Corallina granifera, Wrangelia penicillata and Padina pavonica, and algal turf). Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 43

Factors affecting coastal fish assemblage Orlando Bonaca & Lipej 3. Data analysis The average density of fish individuals per 100 m 2 for each species and for the whole fish assemblage was calculated at all studied sites. The total number of species (S), the average richness of species per transect, and Pielou s evenness index values were also calculated for each site. In order to test for interspecific differences in microhabitat use, the data were subjected to canonical correspondence analysis (CCA) (ter Braak 1986), using the package CANOCO version 4.5. The CCA method operates on abundances (e.g. counts of individuals) of species and data on environmental variables at sites, and extracts from the environmental variables synthetic gradients (ordination axes) that maximize the niche separation among species (ter Braak & Verdonschot 1995). In preparation for direct gradient analysis of microhabitat use, data were arranged in two matrices: samples by species (84 37), containing densities per 100 m 2, and samples by environmental variables (84 15). From the original samples by species matrix, rarer species (<3% of occurrence) were eliminated (Fig. 2) to produce the final reduced matrix (84 29). Subsequently, three abiotic environmental variables (mud, sand, rocks) were eliminated because the correlations with some biotic variables were too high (more than 0.56 with Posidonia oceanica, Cymodocea nodosa and Cystoseira spp. covers). Prior to the CCA, the statistical significance of the effect of each variable was tested by a Monte Carlo permutation test (ter Braak & Verdonschot 1995). Consequently, the Wrangelia penicillata Padina pavonica cover was excluded from the analysis as well. Finally, the two reduced matrices were subsequently subjected to CCA. By measuring the environmental variables at all sampling sites, information on the available habitat resources was obtained; this can be compared (e.g. chi-square analysis, electivity indices) with fish frequencies of occurrence to build up profiles of habitat use/preference (Copp & Garner 1995). Owing to insufficiently high frequencies of occurrence, chi-square analysis could not be used. Therefore, the electivity index (EI) was preferred. It was calculated as the difference between the frequency of a species in the group of samples having a given variable and the frequency of that species in all samples (Copp & Jurajda 1999). Positive EI values (up to 1.00) indicate preference and negative values, avoidance (down to )1.00). Results 1. Species inventory, density and diversity With the visual counts technique 37 fish species, distributed over 12 families, were identified during the entire survey (Table 1). The number of species was highest in Blenniidae (8), Sparidae (8), Labridae (6) and Gobiidae (5), while other families were represented by only a few species. Regardless of the habitat type and the sampling location, labrids dominated the fish assemblage, with four species (Symphodus cinereus, S. roissali, S. tinca and S. ocellatus) showing more than 75% of frequency of occurrence (Fig. 2) in 84 samples. Such a value was also reached by Serranus scriba (Fig. 2). The highest number of fish species, 31, was recorded (Table 1) in the association with Cystoseira spp. On boulders covered only with a low stratum of algal turf, 25 species were recorded. Twenty-five species were counted also in both the Wrangelia penicillata and Padina pavonica settlements and in the Cymodocea nodosa meadows. In areas with a Halopithys incurvus and Corallina granifera settlement, 24 species were counted. The number of species found in the Posidonia oceanica meadow was much lower than in other habitat types (Table 1). Clear differences were observed between the systems in the total average fish density per 100 m 2 (Table 1). The H. incurvus and C. granifera settlements had the highest average density of individuals, followed by the W. penicillata and P. pavonica settlements. The boulders covered with algal turf had the third highest value, while the Cystoseiretum with the highest number of species was merely fourth in terms of average density. This sequence remains unchanged even if we subtract the numerical contribution of the gregarious species Atherina hepsetus, whereas different values are obtained for the P. oceanica meadow, where A. hepsetus was very abundant (Table 1) and produced the so-called noisy effect. Without the values for A. hepsetus, the P. oceanica meadow shows the lowest average density of individuals (8.09 ± 7.98). Excluding the values for gregarious species such as A. hepsetus, the members of the family Labridae also dominated the assemblage in terms of average density of individuals in each habitat type (Table 1). The Pielou s evenness index also showed the lowest values for the fish assemblage at the P. oceanica bed. The Cystoseira spp. association had the highest diversity (Table 1), the W. penicillata and P. pavonica cover had the second highest diversity, while the boulders covered with algal turf, the H. incurvus and C. granifera settlements, and the C. nodosa meadow had approximately the same diversity of the fish community (Table 1). 2. Microhabitat use Canonical correspondence analysis yielded a diagram that shows the main pattern of variation in the fish assemblage composition as accounted for by the environmental 44 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage Fig. 2. Frequency of occurrence of fish species in all studied samples (n ¼ 84) collected with the visual counts technique. variables; it also approximately represents the distribution of the species along each environmental variable. Figure 3 shows the CCA ordination diagram for 29 species. Only axes 1 and 2 are presented, as they cumulatively account for 61.6% of the total variance. The species environment correlations of each axis were 0.831 (axis 1) and 0.716 (axis 2). Axis 1 is strongly related to P. oceanica and C. nodosa cover, which results in the separation of A. hepsetus from the other species. Axis 2 is principally correlated with turf cover and boulders measuring 1 0.5 m. This type of microhabitat is preferred by Parablennius sanguinolentus (Fig. 3). This species presents a negative correlation with depth (Fig. 3). Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 45

Factors affecting coastal fish assemblage Orlando Bonaca & Lipej Table 1. Checklist of all species recorded during the study with visual counts, number of species in six different habitat types, average density [(100 m 2 ) )1 ] and SD (in parentheses) of the recorded species and values of Pielou s evenness index. Posidonia oceanica Cymodocea nodosa Cystoseira spp. Halopithys Corallina Wrangelia Padina boulders + turf Aidablennius sphynx 0.02 (0.13) 0.08 (0.19) 0.06 (0.12) Atherina hepsetus 21.00 (14.00) 6.86 (11.63) 1.79 (6.57) 5.60 (11.81) 8.12 (14.37) 1.40 (4.43) Chromis chromis 1.97 (3.51) 0.77 (0.66) 2.00 (4.29) Dicentrarchus labrax 0.01 (0.05) Diplodus annularis 0.28 (0.32) 2.32 (1.79) 1.40 (1.75) 0.82 (0.68) 1.72 (1.61) 0.35 (0.56) Diplodus puntazzo 0.03 (0.09) 0.10 (0.21) Diplodus sargus 0.17 (0.38) 0.03 (0.09) 0.14 (0.27) Diplodus vulgaris 1.05 (0.27) 1.07 (0.67) 1.18 (1.20) 3.12 (1.44) 1.71 (1.20) 0.07 (0.15) Gobius cobitis 0.04 (0.13) 0.40 (0.63) 0.22 (0.31) 0.07 (0.15) 0.18 (0.28) Gobius cruentatus 0.07 (0.14) 1.32 (1.61) 0.72 (0.86) 0.77 (0.70) 0.86 (1.27) 0.93 (1.82) Gobius fallax 0.68 (0.78) 0.92 (2.02) 3.18 (2.61) 0.58 (0.79) 0.46 (0.77) Gobius paganellus 0.06 (0.12) Hippocampus guttulatus 0.03 (0.09) Labrus merula 0.04 (0.13) 0.20 (0.30) 0.36 (0.34) 0.14 (0.23) 0.11 (0.18) Lipophrys dalmatinus 0.53 (0.76) 0.71 (0.86) 0.47 (0.56) 1.12 (1.90) 2.52 (3.27) Mugilidae 0.08 (0.26) Mullus surmuletus 0.03 (0.09) 0.04 (0.15) 0.20 (0.30) Oblada melanura 0.03 (0.09) 0.86 (3.17) 7.37 (10.56) 0.47 (1.00) Pagellus erythrinus 0.06 (0.18) Parablennius gattorugine 0.04 (0.13) 0.25 (0.53) 0.20 (0.22) 0.27 (0.28) 0.06 (0.12) Parablennius incognitus 0.10 (0.22) 0.06 (0.12) 0.06 (0.12) 0.22 (0.43) Parablennius rouxi 0.21 (0.55) 0.04 (0.13) Parablennius sanguinolentus 0.11 (0.27) 0.28 (0.52) 0.42 (0.59) 0.92 (1.01) 2.91 (3.73) Parablennius tentacularis 0.15 (0.21) 0.01 (0.04) 0.03 (0.09) Pomatoschistus bathi 0.46 (0.52) 0.97 (1.46) 0.66 (1.05) 3.66 (6.30) 0.42 (0.57) Salaria pavo 0.03 (0.09) Sarpa salpa 0.25 (0.50) 0.48 (0.81) 1.82 (3.91) 1.75 (2.51) 2.20 (4.19) 0.54 (1.44) Sciaena umbra 0.01 (0.05) Serranus hepatus 0.10 (0.26) 0.03 (0.09) Serranus scriba 0.49 (0.35) 0.91 (0.76) 1.64 (1.06) 2.70 (1.99) 1.47 (1.45) 1.59 (1.20) Sparus auratus 0.03 (0.09) Symphodus cinereus 1.33 (1.26) 5.31 (2.47) 3.39 (2.19) 3.47 (2.34) 4.16 (2.97) 4.99 (2.37) Symphodus ocellatus 0.07 (0.14) 3.34 (3.20) 2.97 (3.58) 9.31 (6.94) 4.71 (5.50) 3.08 (6.09) Symphodus roissali 4.55 (5.00) 2.14 (2.20) 7.68 (4.51) 19.83 (11.49) 6.51 (2.79) 10.19 (6.44) Symphodus rostratus 0.03 (0.10) 0.14 (0.19) 0.08 (0.26) Symphodus tinca 0.51 (0.41) 3.17 (3.28) 2.97 (2.96) 1.96 (1.71) 1.07 (1.50) Tripterygion tripteronotus 0.15 (0.17) 0.30 (0.50) 0.85 (1.13) 1.16 (1.29) 0.59 (0.72) total number of species 9 25 31 24 25 25 average richness/transect (SD) 6.0 (0.82) 11.50 (2.55) 12.21 (3.21) 14.40 (3.06) 12.40 (2.91) 10.70 (2.26) total density: average (SD) 29.09 (21.98) 26.72 (29.47) 33.35 (44.43) 65.16 (61.49) 42.29 (51.11) 34.02 (41.05) tot. density without A. hepsetus 8.09 (7.98) 19.86 (17.84) 31.55 (37.86) 59.56 (49.68) 34.17 (36.74) 32.62 (36.62) Pielou s evenness index 0.44 0.71 0.78 0.74 0.79 0.74 Also Tripterygion tripteronotus, Parablennius gattorugine and P. incognitus can be found in this type of microhabitat (Fig. 4), but they are less specific in their preference. Parablennius rouxi exhibits a positive correlation with increasing depth. Pomatoschistus bathi and Gobius fallax strongly prefer gravel, but G. fallax was also recorded in other microhabitat types, preferring H. incurvus C. granifera settlements (Figs 3 and 4). Among wrasses, Symphodus tinca avoids the P. oceanica bed (Fig. 4). Labrus merula is less specific in its preference for the abiotic substratum type (Fig. 3), but inhabits microhabitats such as moderate Cystoseira spp. and H. incurvus C. granifera covers (Figs 3 and 4). Oblada melanura exhibits a high preference for H. incurvus C. granifera settlements (Figs 3 and 4), while D. sargus is positively correlated with rocks with a Cystoseira spp. cover and W. penicillata P. pavonica settlements 46 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage Fig. 3. Canonical correspondence analysis ordination diagram for 29 species: 1 Aidablennius sphynx; 2 Atherina hepsetus; 3 Chromis chromis; 4 Diplodus annularis; 5 Diplodus puntazzo; 6 Diplodus sargus sargus; 7 Diplodus vulgaris; 8 Gobius cobitis; 9 Gobius cruentatus; 10 Gobius fallax; 11 Labrus merula; 12 Lipophrys dalmatinus; 13 Mullus surmuletus; 14 Oblada melanura; 15 Parablennius gattorugine; 16 Parablennius incognitus; 17 Parablennius rouxi; 18 Parablennius sanguinolentus, 19 Parablennius tentacularis; 20 Pomatoschistus bathi; 21 Sarpa salpa; 22 Serranus hepatus; 23 Serranus scriba; 24 Symphodus cinereus; 25 Symphodus ocellatus; 26 Symphodus roissali; 27 Symphodus rostratus; 28 Symphodus tinca; 29 Tripterygion tripteronotus. (Fig. 4). Diplodus puntazzo also shows a clear preference for deeper waters (Fig. 3). Diplodus vulgaris exhibits a positive relation with many microhabitat types, as well as with seagrass meadows (Figs 3 and 4). Diplodus annularis is more selective in its choice of seagrass, inhabiting only the C. nodosa meadow. The nektonic species A. hepsetus was found mainly in seagrass meadows and W. penicillata P. pavonica settlements (Figs 3 and 4). Chromis chromis avoids seagrass meadows and W. penicillata P. pavonica settlements (Figs 3 and 4). Discussion Despite the limited depth range considered in our study, a high number of species were recorded with the visual counts technique (Table 1). The Northern Adriatic ichthyofauna has a lower species richness than other Adriatic areas. According to Marčeta (1999), 259 fish species belonging to 88 families were recorded in the Gulf of Trieste, and at least 184 species (68 families) in Slovenian waters, while Lipej & Dulčić (2004) reported 429 species belonging to 118 families for the whole Adriatic Sea. Only a few researchers using the visual counts technique recorded higher species richness in the Adriatic Sea than that reported in the present research (Marconato et al. 1996a; Kovačić 2002a); only one work reported such a high number of blennioid and gobiid species as recorded during this study (Kovačić 2002a). The accuracy and precision of density estimates when using the transect technique may be influenced by large numbers of organisms, especially when these are difficult to identify (Bortone et al. 1986). Color, life habits, shoal distribution (Atherina hepsetus, Chromis chromis, Sarpa salpa) or low fish density may also reduce the accuracy of visual counts (Francour 1997). Moreover, fish detectability may drop in a more structured habitat (Guidetti & Bussotti 2000b). Successive diver passages along the same transects, even with a short time interval, apparently do not represent a bias, as pointed out by De Girolamo & Mazzoldi (2001). When epibenthic species encounter a diver they usually move a few meters and then return just after the diver s passage, whereas benthic and cryptobenthic species remain motionless or hide in holes (De Girolamo & Mazzoldi 2001; authors, personal observation). Particularly, Costello (1992) reported that many gobies appeared to be attracted to sediment that was disturbed by divers. Extensive training is needed to accurately detect Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 47

Factors affecting coastal fish assemblage Orlando Bonaca & Lipej Fig. 4. Electivity indices for 18 fish species (abbreviations: Po, Posidonia oceanica; Cn, Cymodocea nodosa; Cy, Cystoseira spp.; HC, Halopithys)Corallina; WP, Wrangelia)Padina; tu, turf; bo, boulders; pe, pebbles; gr, gravel). benthic species. Harmelin-Vivien & Francour (1992) collected such species in a Posidonia oceanica meadow only by trawling, whereas species recorded mainly by visual counts were good swimmers (Sparidae and certain Labridae). Fifteen environmental variables were taken into consideration in order to determine the microhabitat preferences of fish species, using CCA and electivity indices. The results of the present research suggest that the structure of the fish assemblage in shallow habitats is affected by a large number of interplaying factors. Depth, the bottom composition and vegetation type incorporating both abiotic and biotic variables are among the factors responsible for the distribution of coastal fish. Microhabitat preferences for 29 fish species are presented here, mostly in the depth range from 0.5 to 3 m. Many species coexisted in the same microhabitat type. The results also indicate that depth is largely responsible for structuring the fish assemblage, as has also been established by other studies. Bell (1983), who pointed out the depth effect, found that Chromis chromis, which is a diurnal planktivore (Bell & Harmelin-Vivien 1983), is far more abundant at deeper sites. This is presumably because there is a greater volume of water in which to 48 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage Fig. 4. Continued. feed (Bell & Harmelin-Vivien 1983). The electivity indices presented in this work for some species mostly inhabiting deeper waters, like C. chromis and Serranus hepatus, would probably be different if the depth range considered had been greater. According to Macpherson (1994), higher species number and density levels in areas where rocks and boulders are abundant are associated with higher substratum complexity (as opposed to areas in which sand, gravel or P. oceanica beds predominated), thus affording more Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 49

Factors affecting coastal fish assemblage Orlando Bonaca & Lipej shelter as well as more nesting sites for spawning. The structure of algal communities is also an important element of substratum complexity and can influence habitat selection in fish assemblages. Algal cover also strongly influences the quantity and quality of epifaunal communities. Consequently, algal communities and fish assemblages seem to be linked at two levels: spatial (habitat selection) and trophic (access to prey) (Ruitton et al. 2000). On the other hand, homogeneous habitat, like P. oceanica meadows, have a very low habitat complexity and low fish species richness (Biagi et al. 1997). In area B (Fig. 1), only one quite homogeneous patch of P. oceanica was visually censused, yielding nine fish species. This location contains the only remaining living meadow in the Gulf of Trieste (Vukovič & Turk 1995). It is approximately 1 km long, starts close to the coastline (depth 0.5 m) and extends 50 m offshore (depth 4 m) (Turk & Vukovič 1998). It is formed of patches of different sizes and shapes and does not fit into normal meadow types. Turk et al. (2002), whose census also included the areas among the patches of this P. oceanica meadow (thus a higher habitat complexity), recorded 33 fish species. This value can be compared with the results of Bussotti & Guidetti (1999). During their work in the Tyrrhenian Sea they counted 27 species in a mixed meadow of Cymodocea nodosa and Zostera noltii, and just 23 species in a P. oceanica meadow. They did not find any blennies in the mixed meadow of C. nodosa and Z. noltii, and just one (Parablennius gattorugine) in the P. oceanica bed. The absence of blennioid species in the P. oceanica meadow was previously pointed out by Macpherson (1994). The present study also dealt with other vegetation types. From this point of view, the comparison with other papers was very difficult because many authors still devote exclusive attention to seagrass meadows. Some papers divided the algal cover into just two groups (e.g. fleshy and calcareous algae; in Letourneur et al. 2003), while others recorded only the total abundance of macroalgae. Ruitton et al. (2000) considered four strata of algal cover (encrusting, turfy, shrubby and arborescent). They recorded a total of 46 fish species on the French Mediterranean coast, in a depth range from 1 to 8 m. Guidetti (2000) reported that the rocky-algal reef bottom at Otranto was represented by a heterogeneous hard substrate, characterized by a dense algal cover of erect macroalgae (mainly articulated Corallinaceae and Cystoseira spp.). In this habitat type he recorded 21 fish species, while in our study 31 species were found in the Cystoseiretum (Table 1). We found an almost constant occurrence of blennioid species at all of the investigated sites, with the exception of the P. oceanica bed (Table 1). These results are supported by the apparent stability of the blennioid assemblages throughout the Adriatic (Illich & Kotrschal 1990) and in the Ligurian and Tyrrhenian Seas (Nieder et al. 2000). Most of the Mediterranean blennies share the same shallow shore habitat and show similar feeding behavior. Several of the species investigated may overlap in habitat demand, making inter- and intraspecific competition for holes possible (Zander 1980). According to Nieder et al. (2000), the abundance of small benthic fish is correlated to the production of epifauna, which does not develop on rock surfaces with scarce algal cover. With the aid of SCUBA diving, Lipej & Richter (1999) recorded eighteen blennioid species; this compares with only six blennioids mentioned in the first report for this area, when samples were mostly collected with trawling nets (Matjašič et al. 1975). The present study recorded just nine blennioid species, failing to detect species inhabiting deeper waters, species inhabiting only the upper mediolittoral zone and certain cryptobenthic species. The preference of wrasses for shallow rocky substrates colonized by macroalgae, as observed in this study (Figs 3 and 4), is well known for the whole Mediterranean Sea (Bell 1983; García-Rubies & Zabala 1990; Mouillot et al. 1999; Ruitton et al. 2000) and was also reported for the Adriatic Sea (Guidetti & Bussotti 2000a). Ruitton et al. (2000) found that Symphodus species were always more abundant in erect algal cover sites, which allow them access to abundant prey and provide shelter and nesting sites. In the same work they noted that a low algal stratum is significantly linked to the density of Diplodus spp. and S. salpa, a result supported by this study (Fig. 4), probably because of the trophic behavior of these species. The present study provides a basis for further improving our understanding of the mechanisms regulating the distribution of the fish assemblage in shallow coastal areas of the Northern Adriatic Sea. Summary The present study analyses species richness and abundance of fish assemblages at six different shallow inshore macrohabitats in the southern part of the Gulf of Trieste (Northern Adriatic Sea), namely Posidonia oceanica meadow; Cymodocea nodosa meadow; association with Cystoseira spp.; Halopithys incurvus and Corallina granifera settlements; Wrangelia penicillata and Padina pavonica settlements; and boulders covered with algal turf. Altogether 37 fish species, distributed over 12 families, were identified using the visual census technique. The highest species diversity was recorded in the association with Cystoseira spp., whereas the highest fish density was found in the H. incurvus and C. granifera settlements. Fifteen environmental variables were examined in order to determine the microhabitat preferences of fish species, using canonical correspondence analysis and electivity indices. The 50 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage results suggest that the structure of the fish assemblage in shallow habitats is affected by numerous interplaying factors. The results indicate that depth, type of bottom and vegetation cover incorporating both abiotic and biotic variables are largely responsible for structuring the fish assemblage. Microhabitat preferences for 29 fish species were presented in the depth range from 0.5 to 3 m. Acknowledgements The authors would like to express their gratitude to two anonymous referees for the critical reading of the manuscript. Special thanks to Miljan Šiško for his help in the statistical evaluation of the data, to Tihomir Makovec for his invaluable assistance during the fieldwork, and to Dr. Aleksander Vukovič for his help in algal identification, as well. Suitable scientific literature was provided by Dr. Gordon H. Copp. This work was financially supported by the Ministry of Education, Science and Sport of the Republic of Slovenia. References Beja P.R. (1995) Structure and seasonal fluctuations of rocky littoral fish assemblages in south-western Portugal: implications for otter prey availability. Journal of the Marine Biological Association of the UK, 75, 833 847. Bell J.D. (1983) Effects of depth and marine reserve fishing restrictions on the structure of a rocky reef fish assemblage in the north-western Mediterranean sea. Journal of Applied Ecology, 20, 357 369. Bell J.D., Harmelin-Vivien M.L. (1983) Fish fauna of French Mediterranean Posidonia oceanica seagrass meadows. 2. Feeding habits. Tethys, 11, 1 14. Biagi F., Gambaccini S., Zazzetta M. (1997) Popolamento ittico di un area protetta all Isola d Elba. Biologia Marina Mediterranea, 4, 466 468. Bortone S.A., Hastings R.W., Oglesby J.L. (1986) Quantification of reef fish assemblages: a comparison of several in situ methods. Northeastern Gulf Science, 8, 1 22. Bouchereau J.L., Lam Hoaï T. (1997) The ichthyofauna of the Lavezzi Island (Corsica, France) at depths between 0 and 1 m: inventory, quantitative evaluation and recolonisation after experimental destruction. Oceanological Studies, 2 3, 191 207. Braak C.J.F. ter (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology, 67, 1176 1179. Braak C.J.F. ter, Verdonschot P.F.M. (1995) Canonical correspondence analysis and related multivariate methods in aquatic ecology. Aquatic Sciences, 57, 255 289. Bussotti S., Guidetti P. (1999) Fish communities associated with different seagrass systems in the Mediterranean Sea. Il Naturalista Siciliano, 23 (Suppl.), 245 259. Castellarin C., Visintin G., Odorico R. (2001) L ittiofauna della Riserva Naturale Marina di Miramare (Golfo di Trieste, Alto Adriatico). Annals for Istrian and Mediterranean Studies, 11, 207 216. Ciriaco S., Costantini M., Italiano C., Odorico R., Picciulin M., Verginella L., Spoto M. (1998) Monitoring the Miramare Marine Reserve: assessment of protection efficiency. The Italian Journal of Zoology, 65 (Suppl.), 383 386. Copp G.H., Garner P. (1995) Evaluating the microhabitat use of freshwater fish larvae and juveniles with point abundance sampling by electrofishing. Folia Zoologica, 44, 145 158. Copp G.H., Jurajda P. (1999) Size-structured diel use of river banks by fish. Aquatic Sciences, 61, 75 91. Costello M.J. (1992) Abundance and spatial overlap of gobies (Gobiidae) in Lough Hyne, Ireland. Environmental Biology of Fishes, 33, 239 248. De Girolamo M., Mazzoldi C. (2001) The application of visual census on Mediterranean rocky habitats. Marine Environmental Research, 51, 1 16. Diamant A., Ben Tuvia A., Baranes A., Golani D. (1986) An analysis of rocky coastal eastern Mediterranean fish assemblages and a comparison with an adjacent small artificial reef. Journal of Experimental Marine Biology and Ecology, 97, 269 285. Dulčić J., Kraljević M., Grbec B., Pallaoro A. (1997) Composition and temporal fluctuations of inshore juvenile fish populations in the Kornati Archipelago, Eastern Middle Adriatic. Marine Biology, 129, 267 277. Francour P. (1991) The effect of protection level on a coastal fish community at Scandola, Corsica. Revue d Ecologie (la Terre et la Vie), 46, 65 81. Francour P. (1994) Pluriannual analysis of the reserve effect on ichthyofauna in the Scandola natural reserve (Corsica, Northwestern Mediterranean). Oceanologica Acta, 17, 309 317. Francour P. (1997) Fish assemblages of Posidonia oceanica beds at Port-Cros (France, NW Mediterranean): assessment of composition and long-term fluctuations by visual census. P.S.Z.N.: Marine Ecology, 18, 157 173. García-Rubies A., Zabala M. (1990) Effects of total fishing prohibition on the rocky fish assemblages of Medes Islands marine reserve (NW Mediterranean). Scientia Marina, 54, 317 328. Gibson R.N. (1969) The biology and behaviour of littoral fish. Oceanography and Marine Biology, an Annual Review, 7, 367 410. Gibson R.N. (1982) Recent studies on the biology of intertidal fishes. Oceanography and Marine Biology, an Annual Review, 20, 363 414. Guidetti P. (2000) Differences among fish assemblages associated with nearshore Posidonia oceanica seagrass beds, rockyalgal reefs and unvegetated sand habitats in the Adriatic Sea. Estuarine, Coastal and Shelf Science, 50, 515 529. Guidetti P., Bussotti S. (2000a) Nearshore fish assemblages associated with shallow rocky habitats along the southern Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 51

Factors affecting coastal fish assemblage Orlando Bonaca & Lipej Croatian coast (Eastern Adriatic Sea). Vie Milieu, 50, 171 176. Guidetti P., Bussotti S. (2000b) Fish fauna of a mixed meadow composed by the seagrasses Cymodocea nodosa and Zostera noltii in the Western Mediterranean. Oceanologica Acta, 23, 759 770. Harmelin J.G. (1987) Structure et variabilité de l ichtyofaune d une zone rocheuse protégéeenméditeranée (Parc national de Port-Cros, France). P.S.Z.N. I: Marine Ecology, 8, 263 284. Harmelin-Vivien M.L., Francour P. (1992) Trawling or visual censuses? Methodological bias in the assessment of fish populations in seagrass beds. P.S.Z.N. I: Marine Ecology, 13, 41 51. Harmelin-Vivien M.L., Harmelin J.G., Leboulleux V. (1995) Microhabitat requirements for settlement of juvenile sparid fishes on Mediterranean rocky shores. Hydrobiologia, 300/ 301, 309 320. Illich I.P., Kotrschal K. (1990) Depth distribution and abundance of Northern Adriatic littoral rocky reef Blennioid fishes (Blenniidae and Tripterygion). P.S.Z.N. I: Marine Ecology, 11, 277 289. Jardas I. (1996) Jadranska ihtiofavna, 1st edn. Školska knjiga, Zagreb, 536 pp. Koppel V.H. (1988) Habitat selection and space partitioning among two Mediterranean blenniid species. P.S.Z.N. I: Marine Ecology, 9, 329 346. Kotrschal K. (1988) Blennies and endolithic bivalves: differential utilization of shelter in Adriatic Blenniidae (Pisces: Teleostei). P.S.Z.N. I: Marine Ecology, 9, 253 269. Kovačić M. (1995) Gobius roulei De Buen, 1928 (Pisces, Teleostei, Gobiidae), a fish new to the Adriatic fauna. Natura Croatica, 4, 173 184. Kovačić M. (1999) Gammogobius steinitzi Bath, 1971, a fish new to the Adriatic Sea. Natura Croatica, 8, 1 7. Kovačić M. (2002a) A visual census of the littoral fish assemblage at Kostrena (the Kvarner area, Croatia). Annals for Istrian and Mediterranean Studies, 12, 1 8. Kovačić M. (2002b) A northern Adriatic population of Buenia affinis (Gobiidae). Cybium, 26, 1 5. Letourneur Y., Ruitton S., Sartoretto S. (2003) Environmental and benthic habitat factors structuring the spatial distribution of a summer infralittoral fish assemblage in the northwestern Mediterranean Sea. Journal of the Marine Biological Association of the UK, 83, 193 204. Lipej L., Dulčić J. (2004) The current status of Adriatic fish diversity. In: H.L. Griffiths, Kryštufek B., Reed J.M. (Eds.), Balkan Biodiversity. Pattern and Process in Europe s Biodiversity Hotspot. Kluwer Academic Publishers, Dordrecht, 291 306. Lipej L., Orlando Bonaca M., Šiško M. (2003) Coastal fish diversity in three marine protected areas and one unprotected area in the Gulf of Trieste (Northern Adriatic). P.S.Z.N.: Marine Ecology, 24, 259 273. Lipej L., Richter M. (1999) Blennioids (Blennioidea) of the Slovenian coastal waters. Annals for Istrian and Mediterranean Studies, 9, 15 24. Macpherson E. (1994) Substrate utilization in a Mediterranean littoral fish community. Marine Ecology Progress Series, 114, 211 218. Marčeta B. (1999) Ichthyofaunal research and the taxonomic survey of fishes of the Gulf of Trieste. In: J. Forte, L. Lipej (Eds), Biodiversity and Conservation of the Slovenian Coastal Sea at the Threshold of the 21st Century. National Institute of Biology Ljubljana, Marine Biology Station Piran, 53 63 (in Slovenian). Marconato A., Mazzoldi C., De Girolamo M., Stefanni S. (1996a) Analisi del popolamento ittico della zona infralitorale dell osasi di Torre Guaceto (Br) con l uso del visual census. Biologia Marina Mediterranea, 3, 152 154. Marconato A., Mazzoldi C., De Girolamo M., Stefanni S., Maio G. (1996b) L uso del visual census nello studio della fauna ittica costiera. Biologia Marina Mediterranea, 3, 512 513. Matjašič J., Štirn J., Avčin A., Kubik L., Valentinčič T., Velkovrh F., Vukovič A. (1975) Flora and fauna of the northern Adriatic. Contribution 1. Slovenian Academy of Science and Arts, Ljubljana, 54 pp. (in Slovenian). Methven D.A., Haedrich R.L., Rose G.A. (2001) The fish assemblage of a New Foundland estuary: diel, monthly and annual variation. Estuarine, Coastal and Shelf Science, 52, 669 687. Mouillot D., Culioli J.M., Lepretre A., Tomasini J.A. (1999) Dispersion statistics and sample size estimates for three fish species (Symphodus ocellatus, Serranus scriba and Diplodus annularis) in the Lavezzi Islands Marine Reserve (South Corsica, Mediterranean Sea). P.S.Z.N.: Marine Ecology, 20, 19 34. Nieder J., La Mesa G., Vacchi M. (2000) Blenniidae along the Italian coasts of the Ligurian and the Tyrrhenian sea: community structure and new records of Scartella cristata for northern Italy. Cybium, 24, 359 369. Patzner R.A., Serrao Santos R. (1993) Ecology of rocky littoral fishes of the Azores. Courier Forschungsinstitut Senckenberg, 159, 423 427. Ruitton S., Francour P., Boudouresque C.F. (2000) Relationships between Algae, Benthic Herbivorous Invertebrates and Fishes in Rocky Sublittoral Communities of a Temperate Sea (Mediterranean). Estuarine, Coastal and Shelf Science, 50, 217 230. Sogard S.M., Powell G.V.N., Holmquist J.G. (1987) Epibenthic fish communities on Florida Bay banks: relations with physical parameters and seagrass cover. Marine Ecology Progress Series, 40, 25 39. Syms C. (1995) Multi-scale analysis of habitat association in a guild of blennioid fishes. Marine Ecology Progress Series, 125, 31 43. Turk R., Orlando Bonaca M., Makovec T., Vukovič A., Lipej L. (2002) A topographical survey of habitat types in the area characterized by seagrass meadow of Posidonia oceanica in the southern part of the Gulf of Trieste (Northern Adriatic). Annals for Istrian and Mediterranean Studies, 12, 191 202. 52 Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd

Orlando Bonaca & Lipej Factors affecting coastal fish assemblage Turk R., Vukovič A. (1998) Phenology of Posidonia oceanica (L.) Delile in the Gulf of Koper (Gulf of Trieste), North Adriatic. Rapport du Congrès de la Commission Internationale pour l Exploration Scientifique de la Mer Méditerranée, 35, 592 593. UNEP (1998) Draft classification of marine habitat types for the Mediterranean region. Mediterranean Action Plan. Meeting of experts on marine habitat types in the Mediterranean region. SPA/RAC, 149/3: Annex I and II. Vukovič A., Turk R. (1995) The distribution of the seagrass Posidonia oceanica (L.) Del. in the Gulf of Koper. Preliminary report. Rapport du Congrès de la Commission Internationale pour l Exploration Scientifique de la Mer Méditerranée, 34: 49. Whitehead P.J.P., Bauchot M.L., Hureau J.C, Nielsen J., Tortonese E. (Eds) (1986) Fishes of the North-Eastern Atlantic and Mediterranean. UNESCO, Paris, Volumes 1 3, 1473 pp. Wilkins H.K.A., Myers A.A. (1992) Microhabitat utilisation by an assemblage of temperate Gobiidae (Pisces. Teleostei). Marine Ecology Progress Series, 90, 103 112. Zander C.D. (1980) Morphological and ecological investigations on sympatric Lipophrys species (Blenniidae, Pisces). Helgoländer Meeresuntersuchungen, 34, 91 110. Marine Ecology 26 (2005) 42 53 ª 2005 Blackwell Publishing Ltd 53