ࡱ> 7 .bjbjUU {7|7|;pLlBBBBBBBT$LpLxxȎގ^<<<$ BEBB<<:EEEB<B<EEEæhBBK< Ӊ.+Kt,0Hx;. :.KEBBBBInfralittoral fish assemblages in a temperate estuary, Adriatic Sea SANJA MATI-SKOKO, MELITA PEHARDA, ARMIN PALLAORO and BRANIMIR BA}DARI Institute of Oceanography and Fisheries, `etaliate Ivana Meatrovia 63, P.O. Box. 500, 21000 Split, Croatia Corresponding author:  HYPERLINK "mailto:sanja@izor.hr" sanja@izor.hr Short title: Fish assemblages in a temperate estuary SUMMARY: The infralittoral fish assemblage was investigated inside a temperate Zrmanja river estuary, Adriatic Sea. The specimens were caught using a beach seine at three stations and four times over the year. Total of 47 species, belonging to 17 families were represented in the catch, out of these Atherina boyeri (60.3%), Symphodus ocellatus (14.4%) and Pomatoschistus marmoratus (7.5%) were most abundant, comprising 82.2% of the total catch. Marine and estuarine species represented 89.6 and 10.4 %, respectively, while freshwater species were not observed in samples. Differences in fish assemblages were observed with respect to sampling dates and station mostly due different temporal and spatial distribution of juvenile fish settlers. Juveniles of open sea spawners (L. mormyrus, P. erythrinus) were found with increased distance from the river mouth. As they progressively grow, they disperse throughout the estuary. Juveniles of resident species (Pomatoshistus sp.) stayed closer to the river mouth. Permanent estuary residents comprised 11 species, 33 species were opportunists and the remaining 3 were transients. The data thus show that in even small temperate estuaries characteristics of river inflow have the potential to alter spatio-temporal patterns in infralittoral fish assemblage. Keywords: infrallitoral fish assemblages, juveniles, distribution, temperate estuary RESUMEN: Palabras clave: INTRODUCTION Estuaries are important nursery habitats for marine juvenile fish and are characterized by high fish species richness and abundance of juveniles (Claridge et al., 1986; Lenanton and Potter, 1987; Reina-Harvas and Serrano, 1987; Robertson and Duke, 1990; Tzeng and Wang, 1992; Thiel et al., 1995). Moreover, estuaries, by their high productivity provide juvenile fish with food resources (Forrester, 1990). The value of tropical estuaries as habitats for marine animals is relatively well studied (Reina-Harvas and Serrano, 1987; Tzeng and Wang, 1992). However, little is known about the biodiversity, community structure, temporal variations and life history of fishes in temperate latitude estuaries, particularly along the Mediterranean coast. Previous studies conducted in the Adriatic analyzed fish infralittoral assemblages on rocky shores (Dul i et al., 1997; Guidetti and Bussotti, 2000) and on sandy bottom beaches (Dul i et al., 2004; Dul i et al., 2005). Unfortunately, there is no data about fish community structure in an Adriatic estuary although there are four bigger Croatian rivers that belong to the Adriatic Sea basin and all are placed in interesting fishing areas. Understanding juvenile fish distribution patterns is important for estimating the relative value of different estuarine habitats, as well as for assessing habitat restoration or rehabilitation needs (Hannan and Williams, 1998). The main objective of this study was to test the hypothesis that there is no difference in fish assemblages within the small temperate estuaries. Results obtained in this study could be useful for giving a better understanding of fish community structure in a temperate Mediterranean estuary. MATERIALS AND METHODS The karstic Zrmanja River (69 km) belongs to the Adriatic Sea basin. Its bottom is graveled and has steady flow with few cascades and rapids, with a karst stream running partly underground. The estuary of the Zrmanja River ( 44 11' N,  15 34' E) empties into the Novigrad Sea (mean depth 28 m, length 11km, width 5 km) that is connected to the Adriatic and the adjacent Karin Sea (length 3.8 km, width 2.4 km) by narrow channels (Fig.1). The estuary (cca 500 m around river mouth) is highly stratified with salt wedge and a sharp halocline. The fresh water Zrmanja river inflow determines the depth of the halocline. In summer salinity was high due to low river inflow. The highest inflow (mean 65 m3 s-1) and lowest salinity occur in the period December  April (Buri et al., 2004). Annual temperature varies from 6.7  26.6 C (mean 16.4 C), while the salinity ranged from 0  38 (mean 19.0). Nutrient concentrations are low and transparency high, characteristics of an oligotrophic system (Buljan, 1969). Three sampling stations were selected in different parts of the estuary (1-2 km apart). The depths of the sampling stations ranged from 0.5 to 2.5 m and the substrate was heterogeneous rocky, sandy and muddy. Zostera noltii meadows were present at Station 1 and in clumps on Station 3, while this species was not observed on Station 2. The fish fauna was sampled on 4 occasions: (A) August 25th 2003, (B) November 8th 2003, (C) February 20th 2004 and (D) May 20th 2004. Fish samples were collected using a 50m long beach seine. Net depth at the beginning of wings was 30 cm, while at the central part it was 250 cm including the sac. The wings had an 8 mm mesh size, while the mesh size of central sac was 4 mm. The net was always hauled from the deeper part of a sampling station perpendicularly toward the shore. At each sampling station four replicate net deployments (100 - 200 m apart) were made. The maximum working depth was up to 1.5 m. The collected organisms were sorted and preserved in 4% formalin (pH 8.5-9.0). Fish species were identified according to Jardas (1996). Total length (to the neareast 0.1 cm) and weight (to the nearest 0.01 g) were measured for each individual. Species were places in three categories on the bases of habitat use: permanent residents (R) which spend their entire life within estuary and are highly adapted for estuary conditions by possessing specialised physiological adaptations; opportunists or secondary residents (O) that spend only a part of their life history in the estuary, usually as juveniles, and generally have few physiological adaptations for estuary life and transients (T), often stenoterm and stenohalin species that only occasionally enter estuary, usually when estuary conditions are very similar to those of open sea. Physical-chemical parameters were measured three times before each net deployment; temperature was measured with a mercury thermometer and salinity with a laboratory inductive salinometer (accurate to 0.1) 20-30 cm beneath the surface. Fish assemblage structure was analyzed using the PRIMER software package (Clarke and Warwick, 2001). Species richness (S) as simply count of species and abundance (N) values were recorded. Data were log transformed and the Bray-Curtis similarity matrix was used to generate 2-dimensional ordination plots with the non-metric multidimensional scaling (nMDS) technique (Clarke, 1993). ANOSIM test for a replicated two-way crossed experimental layout was used for testing differences in species assemblage between seasons and sites (Clarke and Warwick, 2001). The  level for rejecting the null hypothesis was set at 0.05. All species that constituted less than 3% of total sample were omitted from the analysis. Differences between sampling dates and stations with respect to temperature, salinity, biomass, species richness, total abundance, Pielous evenness (J) and Shannon Wiener diversity (H) were tested with ANOVA using the Minitab software package. Prior to the analysis, homogeneity of variance was tested using Levenes test. RESULTS Salinity and temperature significantly differed between sampling dates and stations (Tab. 1). Station 2 was characterized by lowest salinity values at all sampling dates (Tab. 2). Although temperature differences were significant between sampling times and stations, they were less pronounced with respect to stations. A total of 10,035 fishes, belonging to 17 families and 47 species were caught at three stations in the Zrmanja estuary. The majority of caught specimens were juveniles (with already formed scales and fins, but still not reach first maturity), with the exception of about 10% of the Atherina boyeri and Pomatoschistus marmoratus adult individuals in total sample. Sixteen species were found at all three stations (Tab. 3). Eight species were present throughout the year and comprised almost 90% of the total catch, while three of them Atherina boyeri (60.3%), Symphodus ocellatus (14.4%) and Pomatoschistus marmoratus (7.5%) made up majority of that percentage. High total abundance was driven by A. boyeri (6,055 individuals ranging from 2.4 to 7.6 cm). Juveniles of marine euryhaline species appear to be the most common in our samples. We observed only four (Lipophrys pavo, Platichthys flesus, Pomatoschistus bathi, P. minutus) real estuarine species (their entire life-cycle occurs in the estuary), while true freshwater species were never recorded. Juveniles of some marine species (B. boops, B. luteum, H. ramulosus, L. mormyrus) were found only in August, while others like S. cinereus or P. erythrinus were found at Station 3 only in November. Estuarine species, including A. laterna (Lt = 9.1 cm; Wt = 5.58g) and Knipowitchia caucasica (Lt = 2.6 cm; Wt = 0.14g), occurred in February. Biomass of fish sample in Zrmanja estuary varied temporally and spatially (Tabs 4,5). Species richness varied between sampling dates, but did not show variations between sampling stations. Number of individuals varied only between stations, the highest abundance was recorded on Station 1. Pielous evenness index varied only between stations. Shannon-Wiener diversity index showed both temporal and spatial variations. The nMDS plots of fish assemblages in the Zrmanja estuary show differences in fish abundance (N) with respect to sampling date and station (Fig. 2). Station 2 differed in fish community composition from Stations 1 and 3 (Fig 2a). With respect to dates, assemblages sampled in colder months were similar to each other, while there appears to be difference in community structure between those sampled in warmer part of the year (Fig 2b). According to the results of 2-way crossed ANOSIM test, fish assemblage abundances differed among stations (av=0.49, P=0.001) and sampling dates (av=0.51, P=0.001). The most pronounced difference was observed between Stations 1 and 2, but all pair-wise comparisons showed that stations differed in their fish community composition (Tab. 6a). With respect to pair-wise comparison of temporal differences, the most pronounced difference was observed between February and May, while there was no difference in assemblage structure between November and February samples (Tab. 6b). In terms of relative contribution of species and individuals to each residential category, permanent estuary residents comprised 12 species (Gobiidae, Blenniidae, Pleuronectidae) that were represented by 1,752 individuals (17.46% of the catch). A total of 33 species represented by 8,237 fish (82.08% of the total) were considered to be opportunists. The remaining 3 species (Clupeidae, Engraulidae) represented by 46 individuals (0.46% of the catch) were considered to be transients. Juveniles of open sea spawners (Sparidae, Centracanthidae, Serranidae) were found on Station 1 or 3. For example, a total of 40 juveniles of L. mormyrus, ranging from 1.8 to 4.4 cm Lt, were recorded in August on Station 1. Furthermore, 70% of 1447 juveniles of S. occelatus were found also on Station 1 in August (ranging from 2.3 to 4.9 cm Lt), but larger individuals (ranging from 3.8 to 13.4 cm Lt) were recorded in all sampling dates and on all stations. Juveniles of D. annularis ranging from 1,5 to 2.4 cm were found on Station 1 and 3, while larger ones ranging from 2.2 to 10.3 cm were recorded throughout the estuary. On the other side, juveniles of estuary spawners, mainly resident species (Gobiidae, Blennidae) were recorded on Station 2. DISCUSSION The fluctuating nature of the estuarine environment determines its fish community structure. Results of the present study indicate that in a temperate Zrmanja estuary, fish assemblage, salinity and temperature exhibit both spatial and temporal variations. Due to lack of temporal replicates we cannot make conclusions about seasonal differences in fish assemblages. However, fish assemblage sampled in February (winter) in Zrmanja estuary was low in diversity and composed of only the most physiologically tolerant species such as A. boyeri (Bardin and Pont, 2002). Temperature also influences other biological processes and thus indirectly determines composition of fish community. Jardas (1996) indicated that early spring and late summer (period of increasing temperature) were main spawning periods for the most common Adriatic fish species. Our results suggest that in May (spring) and November (fall) samples, temperate estuaries received recruits of many species that spawn in the open sea, due to the timing of their settlement and recruitment. For example, more than 70% of juvenile S. ocellatus were observed in the August and November, following early summer spawning, while A. boyeri entered Zrmanja estuary in the May. Bardin and Pont (2002) previously reported spring immigration of A. boyeri and Pomatoschistus spp. into a Mediterranean lagoon. Furthermore, C. niger, C. labrosus and S. kleini, all winter spawners, were found only in February samples. Ecological separation of the dominant species by settlement timing resulted in the fact that species did not compete for the same niche (Tzeng and Wang, 1992). Only few species dominate total abundances, for example the atherinid made up more than 60% of the total abundance in this study. In mangrove forests, gobiid (Clynick and Chapman, 2002) and mugilid species (Kuo et al., 1999) dominated the samples. Those dominant taxa, like A. boyeri and S. ocellatus in this area, are important in the trophic support of fishery populations (Vega-Cendejas et al., 1994) due their belonging to the productive and low trophic level species with high ecological efficiency (Dul i et al., 1997). On the other side, we found that 82.08% of the caught species were opportunists. Five species, namely A. laterna, C. labrosus, L. aurata, S. kleini and Z. zebrus, were found only once and only at ST2 which is strongly influenced by Zrmanja River. Therefore, we characterized them as rare species with narrower spatial distribution. But, also many other species (38.3%) were present only at one of three stations or only once. Although, the remaining species (48.9%) had wider temporal and spatial distribution, most of them were more abundant only at one station or only on one date. L. mormyrus juveniles were most abundant in August after their settlement from ichthyoplankton. Similarly, P. bathi and P. marmoratus were most abundant at Station 2 in May, while P. minutus was the most numerous at ST2 in November. It seems that in temperate estuary majority of species only occasionally occupy some parts of estuary following certain life-cycle phases such as settlement, recruitment, or spawning. Recruitment of such small juvenile fishes is limited by the supply of larvae that settle in the first seagrass they encounter (Bell et al., 1988). Hannan and Williams (1998) concluded that settling fish do not discriminate between seagrass beds of different structure; in fact, they settle in any available shelter. In our study, some marine species, such as B. boops or S. tinca, were found only on Station 1 that is nearest to the real marine environment, and has meadows of Zostera noltii. The preference by small labrids for substrates colonized by macroalgae, as observed on that station, was known not only for the Mediterranean (Garcia-Rubies and Macpherson, 1995), but it is also a common feature in other temperate waters (Choat and Ayling, 1987). Large sized juveniles of some open sea spawners were distributed throughout the entire Zrmanja estuary because most of these were presumably old enough to move widely. Also, those large juveniles may easily leave seagrass shallows for alternative habitats in case of some accidental situation (Hannan and Williams, 1998). Juveniles of resident species always stayed around low salinity stations. Therefore they quantitatively dominated on such stations and differed them from others. However, in spring when the strongest northern winds occur in the Zrmanja canyon (Buljan, 1969) juveniles of resident species are carried straightforward to marine areas by the created currents. Further on, Hannan and Williams (1998) stated that ocean-spawned juveniles, after settlement, tend to stay closer to the entrance of the estuary, while juveniles of lagoon spawners are widely distributed within the lagoon. Although majority of species found in this study could be classified by spawning area, very little is known about their specific spawning habitats or larval transportation routes. In relation to our investigated habitat, we found that fewer species of open sea spawners (L. mormyrus, P. erythrinus, S. flexuosa) are found with increased distance from the river mouth. As they progressively grow, they disperse throughout the estuary, and such juveniles recruit at later times and at larger sizes far from the river mouth. As opposite, juveniles of estuary spawners, mainly resident species (Pomatoshistus sp.), stayed closer to the river mouth or near the shoreline with main influence of river outflow. Results of this study contribute to the knowledge of temperate estuarine biodiversity and indicate spatial and temporal variations in infralittoral fish assemblages inside a small temperate estuary. Observed variations can be attributed to temporal shifts in faunal composition, immigration and emigration in terms of settlement and recruitment of both marine and estuarine fishes and their trophic interactions. However, due to insufficient replicates, it is necessary to proceed with investigation on a wider temporal and spatial scale including manipulation experiments, in order to determine effects of biological interaction and environmental factors in structuring fish assemblage in these environments. ACKNOWLEDGEMENTS Many thanks are expressed to Ba~dari family for their help with fieldwork. Also, we would like to thank Paulo Guidetti and Robert Hamersley for providing helpful comments on the manuscript. REFERENCES Bardin, O. and D. Pont. - 2002. Environmental factors controlling the spring immigration of two estuarine fishes A. boyeri and Pomatoschistus spp. into a Mediterranean lagoon. J. Fish Biol., 61: 560-578. Bell, J.D., A.S. Steffe and M. Westoby. - 1988. Location of seagrass beds in estuaries: Effects on associated fish and decapods. J. Exp. Mar. Biol. Ecol., 122: 127-146. Buljan, M. - 1969. Some hydrographic properties of the estuarial areas of the Krka and Zrmanja rivers. Kr Jugoslavije, 6: 303-331. Buri, Z., Caput, K., Cetini, I., Vili i, D. and M. Cari. - 2004. Cyclotella striata (Ktzing) Grun. in the eastern coastal Adriatic Sea. In: Proceedings of the 14th Hungarian algological meeting, Gd, 2-4 April 2004. pp. 12-12. Gd: Hungarian Algological Society. Choat, J.H. and A.M. Ayling. - 1987. 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Environmental factors as forces structuring the fish community of the Elbe Estuary. J. Fish Biol., 46: 47-69. Tzeng, W.N. and Y.T. Wang. - 1992. Structure, composition and seasonal dynamics of the larval and juvenile fish community in the mangrove estuary of Tanshui River, Taiwan. Mar. Biol., 113: 481- 490. Vega-Cendejas, M.E., Hernndez de S.M. and F. Arreguin-Sanchez. - 1994. Trophic interrlations in a beach seine fishery from the northwestern coast of the Yucatn Peninsula, Mexico. J. Fish Biol., 44: 647-659. TABLES Table 1. - Results of ANOVAs comparing salinity and temperature at three station and four dates (*p < 0.05; **p < 0.01; ns: not significant, p >0.05). Table 2. - Mean values of salinity and temperature at three station and four occasions together with total number of individuals and total number of species sampled in Zrmanja estuary. Table 3. - List of all sampled fish species (+ present; - absent) with their total abundances at stations (1, 2 and 3) and dates: August (A), November (B), February (C), May (D) with habitat utilization: residents (R), opportunists (O) and transients (T). Table 4. - Total values of biomass, species richness (S) and total abundance (N), and mean values of Pielous evenness (J) and Shannon Wiener diversity (H) of fishes collected by four replicate hauls at three station and four dates. Table 5. - Results of ANOVAs comparing biomass, species richness (S), total abundance (N), Pielous evenness (J) and Shannon Wiener diversity (H) of fishes at three station and four dates (*p < 0.05; **p < 0.01; ns: not significant: p >0.05). Table VI. - a) Two-way crossed ANOSIM test for differences in fish assemblage abundance among stations (Global r = 0.506; p < 0.001); and b) among dates: August (A), November (B), February (C), May (D) (Global r = 0.490; p < 0.001). Table 1. SalinityTemperatureSourcedfMSFMSFDate (T)31175.19401.1**316.66020.8**Station (ST)2106.0847.6**0.917.2**TxST610.180.9**0.23.7**Residual300.10.1Levenensns Table 2. OccasionsSalinityTemperatureTotal no. individualsTotal no. speciesST1ST2ST3ST1ST2ST3August34.032.035.025.125.225.3180420November16.08.016.011.411.211.6266927February8.06.09.012.211.912.8245618May27.020.027.018.117.218.1310635 Table 3. SpeciesHabitat util.TotalStation 1Station 2Station 3ABCDABCDABCDClupeidaeSardina pilchardusT17+Sprattus sprattusT27++EngraulidaeEngraulis encrasicolusT2++SyngnathidaeSygnathus abasterO13++++Syngnathus acusO2+Syngnathus tenuirostrisO58+++++++++Syngnathus typhleO14++++++++Nerophis maculatusO3++Nerophis ophidionO14++++Hippocampus ramulosusO1+SerranidaeSerranus hepatusO1+Serranus scribaO10+++MullidaeMullus barbatusO27++++++Mullus surmuletusO16+++SparidaeBoops boopsO1+Diplodus annularisO101+++++++++Diplodus vulgarisO2++Lithognathus mormyrusO40++Pagellus erythrinusO10+++CentracanthidaeSpicara flexuosaO38+++Spicara smarisO59+++LabridaeSymphodus cinereusO37+++++++Symphodus ocellatusO1447++++++++++++Symphodus roissaliO98++++++++Symphodus tincaO2+GobiidaeGobius nigerR185+++++++++++Gobius cobitusR2++Knipowitchia caucasicaR7+Pomatoschistus bathiR286+++++++++Pomatoschistus marmoratusR748+++++++++Pomatoschistus minutusR257+++++Zebrus zebrusO1+Zosterissessor ophiocephalusR211+++++++++++CallionymidaeCallinonymus fasciatusO28+++Callionymus rissoO151+++++BlenniidaeLipophrys dalmatinusO2++Lipophrys pavoR14+++Parablennius sanguinolentusR7++++Parablennius tentacularisR11+++++++++CentrolophidaeCentrolophus nigerO1+MugilidaeChelon labrosusO1+Liza aurataO1+AtherinidaeAtherina boyeriO6055++++++++++++BothidaeArnoglosus laternaO1+PleuronectidaePlatichthys flesusR24+SoleidaeSolea kleiniO1+Buglossidium luteumO1+Total species47131210231316142614181221Total individuals1003511921047173513151719293501072441693371719 Table 4. OccasionsBiomassSNJHST1ST2ST3ST1ST2ST3ST1ST2ST3ST1ST2ST3ST1ST2ST3August1448.0640.6661.713131411921714410.350.750.520.811.801.19November807.7442.8594.912161810479296930.310.490.310.540.830.63February1654.9507.9551.110141217353503710.300.540.670.581.091.22May2641.31428.51320.4232621131510727190.480.660.491.191.611.21 Table 5. BiomassSNJ'HSourcedfMSFMSFMSFMSFMSFDate (T)32464426.0**74.49.8**149940.6ns0.11.9ns1.06.0**Station (ST)23048117.4**0.20.03ns2409309.4**0.25.5**1.05.7**TxST6220630.5ns1.30.2ns413151.6*0.041.1ns0.10.8nsResidual30409747.6255360.040.2Levenensnsnsnsns Table 6a. StationsR-value p1 vs.20.646< 0.011 vs.30.446< 0.012 vs.30.476< 0.01 Table 6b. DatesR-value pA vs. B0.679< 0.05A vs. C0.762< 0.01A vs. D0.655< 0.05B vs. C0.156nsB vs. D0.438< 0.01C vs. D0.618< 0.01 FIGURES Figure 1. - Study area of the Zrmanja river estuary with three stations (1, 2 and 3) where spatial and temporal changes in fish assemblages were studied. Figure 2. - A) nMDS ordination plot (stress = 0.21) of three stations in the Zrmanja river estuary: (% Station 1, %Station 2, % Station 3); B) nMDS ordination plot (stress = 0.21) of sampling dates (% A - August, % B - November, % C - February, % D - May). Figure 3. - Spatial and temporal distribution of three the most abundant fish species in Zrmanja river estuary fish assemblage.  Figure 1.  Figure 2.  Figure 3. PAGE  PAGE 18 PAGE  PAGE 19 PAGE  PAGE 25 456CD=q = J r  0 5 .84fgp0136!! 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