Read Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical­subtropical estuary text version

Journal of Fish Biology (2008) 73, 1314­1336 doi:10.1111/j.1095-8649.2008.02005.x, available online at http://www.blackwell-synergy.com

Factors affecting seasonal variations in demersal fish assemblages at an ecocline in a tropical­subtropical estuary

^ M. B ARLETTA *, C. S. A MARAL *, M. F. M. C ORRE A §, F. G UEBERT §, D. V. D ANTAS *, L. L ORENZI k AND U. S AINT -P AUL {

´rio *Laborato de Ecologia e Gerenciamento de Ecossistemas Costeiros e Estuarinos, ´ Dept Oceanografia, Universidade Federal de Pernambuco, Cidade Universitaria, 50740-550, Recife, Pernambuco, Brazil, Instituto de Ecologia e Gerenciamento de ´ Ecossistemas Aquaticos (IEGEA). P. O. Box: 8132, Recife, 51020-970, Pernambuco, ´rio de Ictiologia, Centro de Estudos do Mar, Universidade Federal do Brazil, §Laborato ´ ´ ´ Parana. Av. Beira Mar, Pontal do Sul, 83000-000 Pontal do Parana, Parana, ´gicas, Unidade de Sao Francisco do Sul, ~ Brazil, kDepartamento de Ci^ncias Biolo e ~ ~ Universidade da Regiao de Joinville, Caixa Postal 1005, 89240-000, Sao Francisco do Sul, Santa Catarina, Brazil and {Zentrum fur Marine Tropeno ¨ ¨cologie, Fahrenheitstr., 06, Bremen, Germany (Received 17 August 2007, Accepted 25 June 2008)

Seasonal changes of fish species composition in terms of biomass, density and number of species ´ in three areas of the main channel of the Paranagua Estuary (axis east­west) are described in relation to seasonal fluctuations in salinity, water temperature and dissolved oxygen in the main channel. Two hundred and thirty-four samples were collected monthly, between July 2000 and June 2001, in the main channel. Seventy-nine species of 29 families were captured with a total estimated mean density and biomass of 1513 individuals haÀ1 and 34 kg haÀ1, respectively. The number of species and total mean density differed significantly among areas and seasons, but the total mean biomass differed only significantly throughout the ecocline (areas) of the ´ Paranagua Estuary. For the most abundant species, the mean densities of Stellifer rastrifer, Aspistor luniscutis, Menticirrhus americanus, Sphoeroides testudineus, Cynoscion leiarchus and Symphurus tesselatus (with the exception of Cathorops spixii and Genidens genidens) differed significantly among seasons. The mean biomass of these species, with the exception of G. genidens, S. rastrifer, A. luniscutis and S. testudineus, also differed significantly for the factor seasons. Area was a significant factor for the eight most abundant species (density and biomass), except S. testudineus (density), G. genidens, C. leiarchus and S. tesselatus (biomass). The season v. area interaction term was significant for C. leiarchus (density). Most of these differences occurred during the rainy season when fishes concentrated principally in the middle of the estuary, where the salinity remained stable. It is suggested that the salinity stability in the middle of the estuary is the main reason why the most estuarine resident fish species move downstream and remain there, regardless of the increased freshwater runoff. Moreover, canonical correspondent analysis output detected that during the late rainy season, the variable dissolved oxygen (P < 0Á01) was the most important environmental variable, responsible for structuring ´ patterns of fishes assemblages in the west­east axis of Paranagua Estuary. During the end of the

Author to whom correspondence should be addressed. Tel. and fax: þ55 8121268225; email: [email protected] ufpe.br

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dry season, both salinity (P < 0Á01) and dissolved oxygen (P < 0Á05) were responsible for this ecological feature in the estuary. Finally, it was possible to detect that juveniles and adults of some important species respond differently to seasonal fluctuations of the ecoclinedetermining environmental factors. This behaviour is suggested as a strategy to avoid compe´ tition and predation during the rainy season in the middle estuary. The Paranagua Estuary did not fit with the pre-existing models described in the tropical and subtropical estuarine fish literature since its main channel fish assemblages remained within its bounds even during the # 2008 The Authors rainy season.

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´ Key words: Brazil; fish ecology; mangrove estuary; Paranagua Estuary; south-western Atlantic; spatial and temporal variability.

INTRODUCTION The seasonal variation in abundance of freshwater, estuarine and marine fish species in estuarine habitats is a result of both the seasonal variation of environmental factors (rainfall and salinity) and a suite of biological variables (including reproduction and recruitment). Some species occur in specific habitats such as tidal marshes (Mathieson et al., 2000; Akin et al., 2003), seagrass beds (Dorenbosch et al., 2006), mangrove forest (Barletta et al., 2000; Hindell & Jenkins, 2004), mangrove tidal creeks (Barletta et al., 2003; Krumme et al., 2005) and the main channel of the estuary (Blaber et al., 1989; Marshall & Elliott, 1998; Barletta et al., 2005). Others species use these habitats and areas of the estuary (upper, middle and lower) according to their life stages and when environmental conditions allow (Thayer et al., 1987; Barletta et al., 2005; Ramos et al., 2006; Barletta & Blaber, 2007). In tropical estuaries, seasonal fluctuations of salinity are a major factor determining larval abundance (Morais & Morais, 1994; Barletta-Bergan et al., 2002a, b) and juvenile and adult biomass and density of fishes (Blaber & Blaber, 1980; Blaber et al., 1989; Barletta et al., 2003), mainly due to the effects of large fluctuations of freshwater inputs during the year. In a tropical estuary in the eastern Amazon (northern Brazil), the estuarine dependent species are ordered along a large-scale spatial gradient, when relatively stable hydrological conditions create a well-defined salinity gradient in the estuary, during the late dry season (Barletta et al., 2005). Moreover, during the late rainy season, the freshwater runoff increases, the salinity drops and the estuary become suitable for Neotropical freshwater species. Salinity and distance from the estuary mouth are the most important environmental variables structuring the fish assemblages in this estuary (Barletta et al., 2005). In the temperate R ´io de la Plata Estuary (Uruguay­Argentina), salinity has a stronger influence on the spatial structure of the fish assemblages than temperature, and the pattern of seasonal fish species distribution in the R ´io de la Plata Estuary reflects the seasonal discharge of this river (Jaureguizar et al., 2004). ´ Paranagua Estuary is the largest estuary located in the tropical­subtropical transition zone (south Brazil). In this estuary, studies of the fish assemblages have been conducted principally on tidal flats (Vendel et al., 2003) and the tidal

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channel of the lower estuary (Spach et al., 2003). The fish assemblage composition in terms of seasonal variation in species numbers, density and biomass, as well as fish migration and movements along the whole extension of the main ´ channel (main estuarine ecocline) of the Paranagua Estuary, however, are still poorly understood. The objective of the present study was to determine the fish assemblage ´ (number of species, density and biomass) of the Paranagua Estuary and its variation in relation to seasonal fluctuations of the environmental variables (salinity, water temperature and dissolved oxygen) in the main channel.

MATERIALS AND METHODS

STUDY AREA

´ The main channel of the east­west axis of the Paranagua Estuary (25°159­25°359 S; 48°209­48°459 W) was divided into three areas (upper, middle and lower estuary) according to the salinity gradient and geomorphology (Fig. 1). The upper estuary is located between the mouth of the River Cachoeira and Ilha do Teixeira where the

´ FIG. 1. Paranagua Estuary, showing the upper estuary (1), middle estuary (2) and lower estuary (3). Samples were taken in the main channel of the east­west axis with an otter trawl.

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width of the main channel varies from 0Á5 to 5 km. The upper estuary has mesohaline and oligohaline characteristics without vertical stratification during the dry season, with partial or strong stratification during the rainy season. Further upstream, the salinity is <1 even in the dry season. The middle estuary is located between Ilha do Teixeira and Ilha das Cobras where the width of the main channel varies from 0Á5 to 7 km. This area has intermediate salinities, and during the rainy season is influenced by mesohaline and oligohaline waters. During the dry season, sea water influences this area. The lower estuary, located between Ilha das Cobras and Ilha da Galheta, is dominated by marine waters throughout the year.

SAMPLING METHODS

Water temperature (° C), salinity and dissolved oxygen (mg lÀ1) were recorded at the bottom before fish samples were taken. In all three areas, fish samples were collected with an otter trawl. The net, the methodology utilized to take the samples and the calculations of the swept area are described in Barletta et al. (2005). The net was 7Á72 m long and consisted of 35 and 22 mm (between knots) mesh-size in the body and cod-end, respectively. In order to obtain a representative sample for the entire size range of the fish species, a cover with a smaller mesh-size (6Á0 mm) was used over the cod-end. The length of the ground rope was 8Á5 m and the head rope was 7Á1 m. The position of the boat before and after each trawl was recorded by means of a GPS (Garmin GPS 12 Navigation, Olathe, KS, U.S.A.) and was used for the calculation of the swept area. For each sample, the swept area (A) was estimated from: A ¼ DhX2, where D is the length of the path, h is the length of the head rope and X2 is that fraction of the head rope (hX2) which is equal to the width of the path swept by the trawl, the wing spread (Sparre et al., 1989). According to Barletta et al. (2005) the ideal towing speed, at which the otter trawl has the optimal width, was recorded between 3Á7 km hÀ1(2Á0 knots) (h ¼ 3Á4 m; X2 ¼ 0Á4787) and 6Á5 km hÀ1 (3Á5 knots) (h ¼ 3Á8 m; X2 ¼ 0Á5352). In this study, the samples were taken at speeds between 4 and 5Á5 km hÀ1, and it was assumed that the fraction of the head-rope which was close to the width of the swept area was X2 ¼ 0Á5. The catch per unit area (CPUA) was used for the estimation of density (D) and biomass (B). It was calculated by dividing the catch by the swept area (ha): D ¼ CNAÀ1 (individuals mÀ2) and B ¼ CMAÀ1 (g mÀ2), where CN is the catch in number and CM is the catch in mass of fishes. The total mean density ðDT Þ and biomass ðBT Þ was estimated from: DT ¼ DaX1 and BT ¼ BaX1 , where D and B are the mean catch, in number and in mass, respectively, per unit area of all hauls, a is the total sampled area and X1 is the catchability coefficient [in this study as in Barletta et al. (2005) the catchability coefficient was considered to be 1Á0]. Six monthly replicate samples were collected during the first quarter moon between July 2000 and June 2001 in the upper, middle and lower estuary. In order to investigate ´ variations in the fish species composition within season for each area of Paranagua Estuary, each season (dry and rainy) was subdivided, according to the local rainfall pattern, and environmental variables into early (July, August and September) and late (October, November and December) dry, and early (January, February and March) and late (April, May and June) rainy seasons.

SPECIES CLASSIFICATION

The fish species were classified in seven estuarine-use functional groups proposed by Elliott et al. (2007): (1) marine stragglers, species that spawn at sea and typically enter estuaries only in low numbers most frequently in the lower reaches and occur where salinities are c. 35; (2) marine migrants, species that spawn at sea and often enter estuaries in large numbers, particularly as juveniles. Some of these species are highly euryhaline and move throughout the full length of the estuary; (3) estuarine residents, estuarine species capable of completing their entire life cycle within the estuary environment; (4) estuarine migrants, estuarine species that have larval stages of their life cycles

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completed outside the estuary or are also represented by discrete marine or freshwater populations; (5) semi-catadromous, species whose spawning run extends only to estuarine areas rather than the marine environment; (6) freshwater migrants, freshwater species found regularly and in moderate numbers in estuaries and whose distribution can extend beyond the oligohaline sections of these systems; (7) freshwater stragglers, freshwater species found in low numbers in estuaries and whose distribution is usually limited to the low salinity, upper reaches of estuaries. The scientific nomenclature followed Nelson (1994), Eschmeyer (2006), Froese & Pauly (2006) and Marceniuk & Menezes (2007).

STATISTICAL ANALYSIS

ANOVA was used to determine whether significant differences in fish density, biomass and number of species (community variables) occurred in space and time. Twoway ANOVA was used to test differences in fish community variables (density, biomass and number of species) among areas (upper estuary, middle estuary and lower estuary) and seasons (early dry season, late dry season, early rainy season and late rainy season). Data were log10(x þ 1) transformed to increase the normality of distribution. Cochran's test was used to check the homogeneity of variances. Since Cochran's test showed that the variance was often heterogeneous, conclusions from the results of ANOVA have concentrated on those cases where significance levels were <0Á01 (Underwood, 1997). Tukey's honestly significant difference (HSD) test was used whenever significant differences were detected (Day & Quinn, 1989). When the assumptions of parametric statistics could not be met, a non-parametric Kruskal­Wallis test with a 5% level of significance was used (Quinn & Keough, 2002). A Euclidean distance was computed for Q analysis (coefficient similarity matrix among samples) (Romesburg, 1984), where the abiotic factors (salinity, water temperature and dissolved oxygen) were considered attributes (Clarke & Warwick, 1994). These data were used to compare samples and identify groupings graphically using cluster analysis. The environmental data were log transformed [(log10(x þ 1)] to avoid the high value units. In the R analysis (coefficient similarity matrix among species), the species matrix (biomass) was computed using log10(x þ 1)-transformed data. Preceding the analysis, the original data matrix was reduced to remove any undue effects of rare species on analysis (Gauch, 1982). Species occurring in <3% of the samples within a habitat (main channel) were excluded. A similarity matrix using the Bray­Curtis index was computed using PRIMER 6 following Clark & Warwick (1994). Canonical correspondence analysis (CCA) of biomass data for the most important species (frequency >3% in all catches) was conducted after log10(x þ 1) transformation (Legendre & Legendre, 1998) to investigate the structure of the fish assemblage and particularly its seasonal variation in different areas of the estuary in terms of the environmental variables measured at sampling (i.e. direct gradient analysis; ter Braak, 1986). In this analysis, the environmental variables (rainfall, salinity, water temperature and dissolved oxygen) were introduced to the main matrix as descriptors (Legendre & Legendre, 1998). With this procedure, statistical associations among fish assemblage patterns, environmental variables and season were quantified. This method constrains the ordination of the species matrix by linear multiple regression on the environmental variables matrix, so that each successive canonical axis accounts for a smaller proportion of the total variance. The CCA was run with 100 iterations with randomized site locations to facilitate Monte-Carlo tests between the eigenvalues and species­environment correlations for that each axis that resulted from CCA and those expected by chance. The CCA produces a biplot where environmental variables are represented as arrows (vectors) radiating from the origin of the ordination. The length of an environmental vector is related to strength of the relationship between the environmental variable that the vector represents and the species assemblages for each season, which were analysed.

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RESULTS

ENVIRONMENTAL VARIABLES

Salinities showed a seasonal trend, especially in the upper estuary. The lowest salinity values (0­12) were observed between January and March (early rainy season) (Fig. 2). After this time, rainfall decreased and salinities increased. Independent of season, the upper estuary always had the lowest

600

(a)

Rainfall (mm)

400

200

0 35

Water temperature (° C)

(b)

30 25 20 15 10 12

(c)

O2 (mg l­1)

9

6

3 40 30

(d)

Salinity

20 10 0 Jul Aug Sep Oct Nov Dec Jan Feb Mar Apr May Jun

2000

2001

FIG. 2. (a) Total rainfall and mean Æ S.D. values of (b) water temperature, (c) dissolved oxygen and (d) ´ salinity in the Paranagua Estuary [upper ( ), middle ( ) and lower estuary ( )].

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salinity (0­16) and the lower estuary the highest (>25). In relation to salinity, the middle estuary showed characteristics closer to the lower estuary, independent of season. In relation to dissolved oxygen, however, the middle estuary showed characteristics closer to the upper estuary during the early rainy season (January to March). During the early dry season (July to September), the highest concentrations of dissolved oxygen (>7 mg lÀ1) were observed along the entire estuary. Water temperature values showed the same seasonal trends throughout the estuary. The highest temperatures (>28° C) were observed during the early rainy season (January to March) and the lowest temperatures (>15° C) were observed during the early dry season (July to September) (Fig. 2). The R-mode cluster analysis of the environmental variables (salinity, water temperature and dissolved oxygen; Fig. 3) distinguished three main groups. Group I consisted of samples taken in the upper estuary, principally during the early dry (July to September) and late dry (October to December) seasons. In addition, this group contained samples from the end of rainy season (April and May) also from the upper estuary. Group II was represented by samples from the upper estuary during the beginning of rainy season (January to March). The third group comprised all samples from the middle and lower estuary and was divided in two sub-groups: sub-group `a' consisted of samples taken principally at the lower estuary independent of season; sub-group `b' was formed by samples taken during the beginning of dry season in the middle and lower estuary (July to September). Therefore, December to January and June to July were considered transition periods between seasons.

I

II

a

III

b

1·0 0·8 0·6 0·4 0·2 0

Jun 1 Nov 1 May 1 Apr 1 Oct 1 Dec 1 Sep 1 Aug 1 Jul 1 Feb 1 Jan 1 Mar 1 Apr 3 Apr 2 Jun 3 Oct 3 May 3 Jun 2 May 2 Oct 2 Nov 3 Nov 2 Feb 3 Jan 2 Jan 3 Feb 2 Mar 2 Dec 2 Mar 3 Dec 3 Sep 3 Aug 2 Sep 2 Aug 3 Jul 2 Jul 3

Euclidean distance

FIG. 3. Cluster dendrogram of abiotic data (water temperature, dissolved oxygen and salinity). Bottom ´ samples from Paranagua Estuary (1, upper; 2, middle and 3, lower estuary) between July 2000 and June 2001.

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COMPOSITION OF THE FISH FAUNA

Two hundred and thirty-four samples were collected representing a total sampled area of 541 375 m2 (54Á1 ha). Seventy-nine species of 29 families were ´ collected from the east­west axis of Paranagua Estuary with absolute mean density and biomass values of 1513 individuals haÀ1 and 33 837 g haÀ1, respectively. The upper estuary had the highest mean density (2147 individuals haÀ1) and the middle estuary the highest mean biomass (495 003 g haÀ1) (Appendix). The estuarine species Cathorops spixii (Agassiz), Stellifer rastrifer (Jordan), Anchoa parva (Meek & Hildebrand), Achirus lineatus (L.) and Genidens genidens (Cuvier) comprised 76% of the total density and 77% of the total biomass (Appendix). The data in the Appendix show that the importance of the more abundant (in density and biomass) species varies considerably in each of the three main regions of the estuary. Stellifer rastrifer occurred in all three areas, but the highest densities and biomasses were observed in the upper and middle estuary. Species such as C. spixii were captured in highest numbers and greatest biomass mainly in the middle and upper estuary, but, A. parva, Lycengraulis grossidens (Agassiz), Prionotus punctatus (Bloch), Menticirrhus americanus (L.), Eucinostomus gula (Quoy & Gaimard), Diplectrum radiale (Quoy & Gaimard) and Rhinobatus horkeli Muller & Henle, were most abundant in the lower ¨ estuary.

SEASONAL VARIATIONS

The mean number of species and total density differed significantly among seasons and areas, but the biomass varied significantly only by area (Fig. 4 and Table I). Since the ANOVA showed that the number of species, total density and biomass were influenced by both or one of these main effects (season and area), the most abundant fish species [C. spixii, G. genidens, S. rastrifer,

Density (individuals m­2) 0·8 0·6 0·4 0·2 0 25 20 15 10 5 0 20 15 10 5 0 Early Late Dry Early Late Rainy Early Dry Late Early Late Rainy

0·8 0·6 0·4 0·2 0 25 20 15 10 5 0 20 15 10 5 0

(a)

0·8 0·6 0·4 0·2 0 25 20 15 10 5 0 20 15 10 5 0

(b)

(c)

Number of species

Biomass (g m­2)

Early Dry

Late

Early Late Rainy

Season

´ FIG. 4. Mean þ S.D. range in total density, biomass and number of Paranagua Estuary fish species as a function of area (a) upper, (b) middle and (c) lower and season (dry and rainy).

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TABLE I. Summary of the (a) ANOVA and (b) Kruskal­Wallis test results for number of ´ Paranagua Estuary fish species and total (and component) density and biomass. Analysis performed on log10(x þ 1)-transformed data. Differences among areas and season were determined by Tukey's HSD test post hoc comparisons (--) Source of variance Variables Number of species (a) Density (individuals mÀ2) Total (a) C. spixii (a) G. genidens (a) S. rastrifer (b) A. luniscutis (b) M. americanus (b) S. testudineus (a) C. leiarchus (a) S. tesselatus (b) Biomass (g mÀ2) Total (a) C. spixii (a) G. genidens (b) S. rastrifer (a) A.. luniscutis (a) M. americanus (b) S. testudineus (a) C. leiarchus (a) S. tesselatus (a) Season (1) ** EDS; LDS ERS; LRS ** LDS; EDS ERS; LRS NS NS ** * ** * EDS; LDS; ERS; LRS ** EDS; LDS ERS; LRS * NS ** LDS EDS; ERS; LRS NS NS NS ** NS ** ERS; LDS EDS; LRS ** LDS; ERS EDS; LRS Area (2) ** (UE­ME) > LE ** (ME­UE) > LE * (UE­ME) > LE * UE > (ME­LE) ** ** ** NS ** (UE­ME) > LE ** ** (ME­UE) > LE ** (ME­UE) > LE NS ** (ME­LE) > UE ** UE > (ME­LE) ** * (UE­ME) > LE NS NS Interactions NS

NS NS NS -- -- -- NS 1 Â 2** -- NS NS NS NS NS NS NS NS NS

EDS, early dry season (2000); ERS, early rainy season; LDS, late dry season; LE, lower estuary; LRS, late rainy season; ME, middle estuary; NS, non-significant (P > 0Á05); UE, upper estuary. *P < 0Á05; **P < 0Á01.

Aspistor luniscutis (Valenciennes), M. americanus and Syphurus tesselatus (Quoy ´ & Gaimard)] in the Paranagua Estuary were investigated separately for each area over the entire sampling period.

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Mean densities of the 10 most numerous species, except C. spixii and G. genidens, differed significantly between seasons (Fig. 5 and Table I). Furthermore, the mean biomass of these species, with the exception of G. genidens, S. rastrifer, A. luniscutis and Sphoeroides testudineus (L.), also differed significantly between seasons (Fig. 6 and Table I). Area was a significant factor for the 10 most abundant species (density and biomass), except S. testudineus (density), G. genidens, Cynoscion leiarchus (Cuvier) and S. tesselatus (biomass) (Figs 5 and 6 and Table I). The season v. area interaction term was significant (P < 0Á01) for C. leiarchus (density).

P A T T E R N S I N T H E F I S H F A U N A S T R U C TU R E A N D I T S RELATIONSHIPS WITH ENVIRONMENTAL FACTORS

The Q-mode cluster analysis distinguished three main groups among the 26 most frequent species (Fig. 7). Group I consisted of two sub-groups. The first sub-group was represented by species that were common in the upper estuary and is represented by estuarine resident species [Ctenogobius stigmaticus (Poey) and Bairdiella rhonchus (Cuvier)]. These species were more common in the upper (dry season) and lower estuary (rainy season). Sub-group `b' was represented by estuarine resident and migrant species [Micropogonias furnieri (Desmarest), Citharichthys spilopterus Gunther, A. lineatus, C. leiarchus, Genyatremus luteus ¨ (Bloch), S. rastrifer, S. tesselatus, C. spixii, A. luniscutis, Citharichthys arenaceus Evermann & Marsh and G. Genidens]. During the rainy season, these species were found mainly in the middle estuary. Group II consisted of species that were more common in the lower estuary, and this group was also divided into two sub-groups. The first sub-group (II ­ a) comprised estuarine resident and migrant species [M. americanus, Etropus crossotus Jordan & Gilbert, S. testudineus, C. spilopterus, D. radiale, P. punctatus, Synodus foetens (L.), Stephanolepis hispidus (L.), R. horkeli and Hyppocampus reidi Ginsburg] that were more frequent in the lower estuary during the late dry season. The second sub-group (II ­ b) was represented by marine migrants [Caranx hippos (L.), Selene vomer (L.) and Chloroscombrus chrysurus (L.)], which occurred only as juveniles in the lower and middle estuary during the end of the dry season and early rainy season. The third group consisted principally of juveniles of marine migrant species that were common in the estuary during the end dry and early rainy seasons. The CCA ordination biplot diagrams of species scores (Fig. 8), as well as regression statistics (Table II), permitted an interpretation of the distribution of the fish species groups per season, in relation to the seasonal fluctuation of environmental variables. The CCA output detected that, for all seasons, axis I was represented principally by the salinity gradient. Moreover, during the end of the dry season, salinity and dissolved oxygen (P < 0Á01 and P < 0Á05, respectively) were the most important environmental variables. These variables were responsible for structuring patterns of the fish assemblages and the formation of axis I and II. On the other hand, during the end of rainy season, dissolved oxygen (P < 0Á01) was the only significant environmental variable responsible for the formation of axe I. The second factorial axis best represents the seasonality of the water temperature and rainfall.

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DISCUSSION

M A I N C H A N N E L F I S H A SS E M B L A G E

´ In spite of the high number of species, the fish assemblage of the Paranagua Estuary was dominated by a few species, nine (C. spixii, S. rastrifer, A. parva, A. lineatus, G. genidens, L. grossidens, C. chrysurus, A. luniscutis and C. leiarchus) out of 79 represented 85% of the total density and 83% of total biomass. This is similar to the situation in the Caet Estuary (Barletta et al., 2005). In both e estuaries, Ariidae species are responsible for >60% of total biomass and density. Other studies in the American region also emphasize the importance of

0·6 0·4 0·2 0 0·03 0·02 0·01 0 0·3 0·2 0·1 0 0·04 0·03 0·02 0·01 0 0·04 0·03 0·02 0·01 0 0·003 0·002 0·001 0 0·02 0·015 0·01 0·005 0 0·006 0·004 0·002 0

(a)

0·6 0·4 0·2 0 0·03 0·02 0·01 0 0·3 0·2 0·1 0 0·04 0·03 0·02 0·01 0 0·04 0·03 0·02 0·01 0 0·003 0·002 0·001 0 0·02 0·015 0·01 0·005 0 0·006 0·004 0·002 0

(b)

0·06 0·04 0·02 0 0·03 0·02 0·01 0 0·3 0·2 0·1 0 0·04 0·03 0·02 0·01 0 0·04 0·03 0·02 0·01 0 0·003 0·002 0·001 0 0·02 0·015 0·01 0·005 0 0·006 0·004 0·002 0

(c)

Cathorops spixii

Genidens genidens

Stellifer rastrifer

Density (individuals m­2)

Aspistor luniscutis

Menticirrhus americanus

Sphoeroides testudineus

Cynoscion leiarchus

Symphurus tesselatus

Early Late Dry

Early Late Rainy

Early Dry

Late

Early Late Rainy

Early

Late Dry

Early Late Rainy

Season

FIG. 5. Mean þ S.D. range in density of the eight numerically dominant species in each reaches of ´ Paranagua Estuary (a) upper, (b) middle and (c) lower during each season.

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this family, e.g. Trminos Lagoon, Mexico (Lara-Dom ´inguez et al., 1981), the e mangrove tidal channel of Caet Estuary, north Brazil (Barletta et al., 2003), e the Tibiri Estuary, north-east Brazil (Batista & R^go, 1996) and Sepetiba e Bay, south-east Brazil (Azevedo et al., 2002), Lagoa dos Patos estuary, south Brazil (Chao et al., 1985) and R ´io de la Plata Estuary, Uruguay­Argentina (Jaureguizar et al., 2004). These studies suggest that the different ontogenetic phases of ariids are well adapted (e.g. parental care and Weberian apparatus) to live in different reaches of the estuaries of the neotropics and other zoogeographic realms of the tropical (Barletta & Blaber, 2007) and subtropical world. ´ Moreover, Cervigon (1985) suggested that the eurythermal capacity of this

20 15 10 5 0 6 4 2 0 0·8 0·6 0·4 0·2 0 0·6 0·4

(a)

20 15 10 5 0 6 4 2 0 0·8 0·6 0·4 0·2 0 0·6 0·4 0·2 0 0·6 0·4 0·2 0 0·4 0·3 0·2 0·1 0 0·3 0·2 0·1 0 0·1 0·08 0·06 0·04 0·02 0

(b)

0·2 0·15 0·1 0·05 0 6 4 2 0 0·8 0·6 0·4 0·2 0 0·6 0·4 0·2 0 0·6 0·4 0·2 0 0·4 0·3 0·2 0·1 0 0·3 0·2 0·1 0 0·1 0·08 0·06 0·04 0·02 0

(c)

Cathorops spixii

Genidens genidens

Stellifer rastrifer

Aspistor luniscutis

Biomass (g m­2)

0·2 0 0·6 0·4 0·2 0 0·4 0·3 0·2 0·1 0 0·3 0·2 0·1 0 0·1 0·08 0·06 0·04 0·02 0 Early Dry Late Early Late Rainy

Menticirrhus americanus

Sphoeroides testudineus

Cynoscion leiarchus

Symphurus tesselatus

Early Dry

Late

Early Late Rainy

Early Dry

Late

Early Late Rainy

Season

FIG. 6. Mean þ S.D. range in biomass of the eight numerically dominant species in each reaches of ´ Paranagua Estuary (a) upper, (b) middle and (c) lower during each season.

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family is most important for determining their success in the estuarine ecosystem. The evidence listed above, when considered all together, explain why ariids are the dominant family in estuarine resident fish assemblage at their latitudinal distribution range worldwide. ´ In the Paranagua Estuary, the number of species and their total mean density differed significantly among areas and seasons. The total mean biomass, however, differed significantly only between areas. For the most abundant species, A. luniscutis, M. americanus, S. testudineus, C. leiarchus, S. tesselatus and C. chrysurus (with the exception of C. spixii, G. genidens and S. rastrifer), the mean density differed significantly among seasons. The mean biomass of these species, with the exception of G. genidens, S. rastrifer, A. luniscutis and S. testudineus, also differed significantly among seasons. Most of these differences occurred during the late rainy season, when fishes concentrated in the middle of the estuary (principally juveniles and adults of C. spixii, C. leiarchus and M. americanus), where the salinity was stable even during the rainy period. During the same period, however, juveniles (high density) of G. genidens, S. rastrifer and A. luniscutis remain and in the upper estuary avoiding the high fish concentration on the middle estuary. Probably for this reason, quite independent of season, the estuarine resident fish species could remain in the estuary. Plots of species cluster and CCA highlighted distinct seasonal patterns in ´ the structure of the fish assemblage in the main channel of the Paranagua Estuary. For example, projection of these centroids onto environmental

250

Bray­Curtis similarity (ranked)

200

I

II

III

150

a

b

100

a

b

50

G. genidens

C. arenaceus

S. foetens

C. spixii

C. leiarchus

S. tesselatus

M. americanus

S. testudineus

C. stigmaticus

C. spilopterus

A. luniscutis

E. crossotus

P. punctatus

B. rhonchus

C. crysurus

S. hispidus

M. furnieri

A. lineatus

G. luteus

H. reidii

S. rastrifer

D. radiale

R. horkeli

C. hippos

A. parva

FIG. 7. Cluster dendrogram of the most abundant species (see Appendix) to otter-trawl samples from the ´ main channel of the Paranagua Estuary. Samples clustered by group average of ranked Bray­Curtis similarity index based on log10 (x þ 1)-transformed biomass in 234 samples.

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S. vomer

0

SEASONAL CHANGES IN ASSEMBLAGES

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vectors reflected large-scale changes in assemblage structure that coincided with abiotic environmental gradients. They were more evident during the end of dry (salinity and dissolved oxygen) and rainy (dissolved oxygen) seasons when the environmental variables were responsible for the fish assemblage distribution in the estuary. The estuarine fish assemblage in the ´ Paranagua Estuary underwent large seasonal and spatial fluctuations in biomass and density. The estuarine-dependent species were ordered along a large-scale spatial gradient during the late dry season, when relatively stable

1·5

(a)

ED12

Sfoet Mamer

2

Stess

ED13

(b)

Rainfall LD22 LD23 Ggen Alineat DO2 Salinity

DO2 ED22 Cleiar Cspix Cspilop ED21 Ggen ED31 Rainfall ED23

Salinity Ecross

ED11 ED33

ED32 Stest

Ppunc T° C Dradi Srastr

Alunis

LD11 LD31 Cspix LD21 T° C Alunis Cleiar Caren Srastr

Aparva Dradi Stess LD13 Mamer LD32 Sfoet LD12 Stest Ppunc Ecross Cspilop LD33 Gstig Alineat

­1·5

Caren

­1·5 2·5

2·0

­2 ­2

3

(c)

Cleiar

2·0

Rainfall ER32 Caren ER31 Srastr Cspix ER22 ER11 Ggen ER21 Alunis Stess Aparva ER33 Salinity DO2

(d)

Ggen

Aparva LR31 Stest Sfoet Stess LR21 Alunis Srastr T° C Cspix Cspilop Rainfall Caren LR33 Ecross Alineat Cleiar LR12 LR22 LR32 Mamer Salinity Gstig LR13 DO2 Sfoet LR23 Stest Ppunc Dradi

T° C Ppunc ER12 Mamer ER13 Alineat Dradi ER23 Gstig

Ecross Cspilop

LR11

­3·0

­1·5

­2·0

3·0

­1·5

2·5

FIG. 8. Canonical correspondent analysis ordination biplot showing species (see Appendix) centroids in relation to environmental variables (T° C, water temperature; DO2, dissolved oxygen; salinity; rainfall) during each season (a) early dry, (b) late dry, (c) early rainy and (d) late rainy. D, species: Cspix, C. spixii; Cleiar, C. leiarchus; Cspilop, C. spilopterus; Alunis, A. luniscutis; Caren, C. arenaceus; Ggen, G. genidens; Dradi, D. radiale; Ecross, E. crossotus; Mamer, M. americanus; Alineat, A. lineatus; Ppunc, P. punctatus; Stess; S. tesselatus; Srastr, S. rastrifer; Sfoet, S. foetens; Aparva, A. parva; Cspilop, C. spilopterus; Gstig, G. stigmaticus; Stest, S. testudineus. s, season month area: ED11, early dry month 1, area 1; LD11, late dry month 1, area 1; ER11, early rainy month 1, area 1; LR11, late rainy month 1, area 1.

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TABLE II. Results of canonical correspondence analysis Axis 1. Early dry Total inertia Eigenvalues Cumulative percentage variance Of species data Of species­environment relation Species­environmental correlations Pearson 1 0Á26 48Á4 72Á1 0Á842 2 0Á659 0Á06 57Á5 88Á6 0Á869 Canonical axis Environmental variables Water temperature Dissolved oxygen Salinity Rainfall 1 0Á5753 0Á0822 0Á7945 À0Á1091 Axis 2. Late dry Total inertia Eigenvalues Cumulative percentage variance Of species data Of species­environment relation Species­environmental correlations Pearson 1 0Á72 48Á1 51Á5 0Á995 2 1Á893 0Á39 57Á8 78Á7 0Á955 Canonical axis Environmental variables Water temperature Dissolved oxygen Salinity Rainfall 1 À0Á2763 0Á8684* 1Á6974** À0Á3158 Axis 3. Early rainy Total inertia Eigenvalues Cumulative percentage variance Of species data Of species­environment relation Species­environmental correlations Pearson 1 0Á43 37Á8 69Á2 0Á650 2 0Á875 0Á06 50Á3 85Á3 0Á723 2 À0Á6275 1Á3330* 1Á2549** 1Á2549 2 À0Á6000 0Á6818 0Á6270 À0Á5182

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TABLE II. Continued Canonical axis Environmental variables Water temperature Dissolved oxygen Salinity Rainfall 1 1Á0909 1Á4805 1Á2857 0Á0779 Axis 4. Late rainy Total inertia Eigenvalues Cumulative percentage variance Of species data Of species­environment relation Species­environmental correlations Pearson 1 0Á23 40Á6 58Á4 0Á899 2 0Á742 0Á10 61Á6 82Á1 0Á847 2 0Á0769 0Á1923 0Á3077 0Á8846

Canonical axis Environmental variables Water temperature Dissolved oxygen Salinity Rainfall

*P < 0Á05; **P < 0Á01.

1 À0Á8025 1Á5432** 1Á2346* À0Á1235

2 À0Á3438 0Á4375 À0Á5313 À0Á5313

hydrological conditions created a well-defined salinity gradient in the estuary. On the other hand, during the late rainy season, the freshwater runoff increased and salinity in the upper estuary dropped. This environmental instability induced the fish movement towards more stable areas in the middle and lower estuary. Such movement, however, increases the competition for space and predation among many estuarine fish species, therefore juveniles (G. genidens, S. rastrifer and A. luniscutis) and adults (A. luniscutis) of some species benefit and by remaining in the upper estuary. Studies differ in their estimation of the importance of salinity gradients for the distribution of fish assemblages in the estuary. Barletta et al. (2005) suggested that these disagreements can be attributed to seasonal alterations in large-scale salinity gradients, and the integration of sequential recruitment of species throughout the year. For example, in the present study, there is no doubt that the stability of the salinity gradient in the middle estuary and lower estuary, even during the rainy season, was an important factor determining the distribution of the estuarine fish species. Other environmental (dissolved oxygen) and biological (competition for space and predation) variables also influence this distribution of fish assemblages particularly during the end of the dry and rainy seasons.

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S E A S O N A L M O V E M E N T S O F F I S H SP E C I E S I N T H E ESTUARY

´ Fish movements between areas of the Paranagua Estuary were detected through seasonal variations of density and biomass. These variables indicated spatio-temporal changes for both adults (high biomass and low density) and juveniles (high densities and low biomass) of the estuarine fish assemblages, ´ especially the most important species. These movements in the Paranagua Estuary were inferred from changes in biomass catch rates. Apparent migration from the upper to middle estuary was influenced by seasonal fluctuations in salinity and dissolved oxygen, principally during the end of the rainy season. ´ Rainfall in the Paranagua Estuary (tropical and subtropical transition zone) is concentrated mainly from January to June and this is reflected by higher river discharge into the estuary. During the rainy season, the upper area of ´ the Paranagua Estuary is a flushed system, and at this time the fish assemblage (mainly adults) moves downstream to concentrate in the middle estuary and nearshore areas, as evidenced by a large reduction of total density and biomass detected in the upper estuary during this time. Studies in estuaries located in tropical humid areas such as north Brazil (Barletta et al., 2005), Orinoco Delta ´ (Cervigon, 1985), Cayenne Estuary (Morais & Morais, 1994) and costal areas of Guyana (Lowe-McConnell, 1962), however, suggest that throughout estuaries in northern South America the estuarine fish species move out of the system to adjacent coastal areas in search of stable salinity conditions. This is the main ´ difference between Paranagua Estuary (tropical and subtropical transition zone) and the estuaries located in northern South America. The most abundant species captured in the main channel (C. spixii) in terms of density and biomass showed seasonality which was negatively correlated with the peak of the rainy season, principally in the upper estuary. Juveniles (high densities) from some other estuarine species (G. genidens, S. rastrifer, A. luniscutis and S. tesselatus), however, remained in the upper estuary during the same period. Meanwhile, the adults of these species (high biomass) moved to the middle estuary (S. rastrifer, A. luniscutis and S. tesselatus) as C. spixii. A second situation can be illustrated by G. genidens, whose adults (high biomass), moved to the lower estuary from the mangrove forest, while juveniles remained in the upper estuary throughout the year. The concentration of adults in the deeper waters of the main channel of the estuary occurred during the dry season when the lowest temperatures were recorded in the shallow waters of the mangrove creeks. The estuarine fish assemblages concentrated in the upper (density) middle (density and biomass) estuary at the end of the rainy season. This does not conform to findings in Albatross Bay, northern Australia (Blaber et al., ´ ´ 1989, 1990; Robertson & Duke, 1990), Teacapan­Agua Brava lagoon­estuarine system in the Mexican Pacific (Flores-Verdugo et al., 1990), Caet Estuary northe ern Brazil (Barletta et al., 2003, 2005), Lagoa dos Patos a lagoon­estuarine system in South Brazil (Chao et al., 1985) and the Rio de la Plata Estuary (Uruguay and Argentina) (Jaureguizar et al., 2004). Seasonal changes in the catch rates of tropical, subtropical and temperate fish communities have also been reported in France (Marchand, 1980), Spain (Iglesias, 1981), Kuwait (Wright, 1988), Madagascar (Laroche et al., 1997),

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North Carolina, U.S.A. (Ross & Epperly, 1985), southern Florida, U.S.A. (Thayer et al., 1987), Guyana (Lowe-McConnell, 1987), north Brazil (Batista & R^go, 1996), and are ascribed mainly to reproduction patterns and increased e recruitment. Blaber et al. (1990) suggest that this phenomenon of fishes concentrating around estuaries, together with the probability that during the rainy season non-estuarine species move to the lower estuary may explain the correlation between fish abundance and rainfall. Data from Barletta et al. (2005) support these findings and indicate that the seasonal changes of estuarine fish assemblages may be determined by a combination of temporal fluctuations of abundance induced by rainfall, reproduction and recruitment of estuarine spe´ cies and recruitment of marine and freshwater species. Paranagua Estuary, however, seems to be an exception to this model since the middle of the estuary has stable salinities even during the rainy season, and the most abundant estuarine fish species move to this area during this period. Moreover, juveniles of some species (e.g. G. genidens, S. rastrifer and S. luniscutis) avoid this area, remaining in the upper estuary even during the rainy season, probably to avoid the adults that concentrate mainly in the middle and also in the lower estuary.

This work resulted from a co-operation between the Zentrum fur Marine Tropeno¨ ¨ cology (ZMT), Bremen, Germany, and the Centro de Estudos do Mar (CEM-UFPR), ´ Pontal do Parana ­ PR, Brazil under the Governmental Agreement on Co-operation in the Field of Scientific Research and Technological Development between Germany and Brazil. It was financed by the German Ministry for Education, Science, Research and Technology (BMBf) [Project number: 03F0154A, Mangrove Management and Dynamics ­ MADAM] and the Conselho Nacional de Desenvolvimento Cient ´ifico e Tec´ nologico (CNPq No.30041900-7). The authors thank S. Blaber and two anonymous reviewers for helpful comments on earlier versions of this manuscript.

References

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´ APPENDIX. Density, biomass and mean and range of standard length (LS) of the fish species from the Paranagua Estuary (upper, middle and lower estuary) collected by otter trawl

Mean biomass % 61Á28 9Á81 0Á31 0Á11 9Á28 0Á35 <0Á1 10Á18 1Á05 <0Á1 0Á37 0Á84 <0Á1 0Á97 <0Á1 0Á94 <0Á1 0Á27 0Á65 1Á36 <0Á1 0Á21 <0Á1 0Á74 <0Á1 1Á00 <0Á1 <0Á1 <0Á1 49 29 23 34 28 25 19 42 34 25 42 29 9 10 16 10 46 12 23 32 22 7 27 22 6 29 10 16 5 g ha

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À1

Total density (%) Upper Middle Lower

Total biomass (%) Frequency of Mean Upper Middle Lower occurrence (%) LS (mm) LS (mm)

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#

M. BARLETTA ET AL.

Cathorops spixii Stellifer rastrifer Anchoa parva Achirus lineatus Genidens genidens Lycengraulis grossidens Chloroscombrus chrysurus Aspistor luniscutis Cynoscion leiarchus Prionotus punctatus Pomadasys corvinaeformis Menticirrhus americanus Symphurus tesselatus Ctenogobius stigmaticus Micropogonias furnieri Eucinostomus gula Diplectrum radiale Harengula clupeola Etropus crossotus Sphoeroides testudineus Chaetodipterus faber Eucinostomus argenteus Citharichthys spilopterus Diapterus rhombeus Geniatremus luteus Anchoviella brevirostris Isopisthus parvipinnis Anchoviella lepidentostole Cynoscion microlepidotus

686Á39 289Á08 85Á81 50Á86 45Á44 35Á09 34Á80 33Á64 21Á80 21Á69 21Á51 14Á95 14Á47 13Á96 12Á64 12Á19 11Á29 8Á85 8Á68 6Á36 6Á05 4Á97 4Á77 4Á35 4Á34 4Á18 4Á16 3Á96 3Á95

45Á37 20145Á58 59Á54 29Á74 19Á11 1665Á34 4Á93 32Á35 5Á67 55Á01 0Á16 7Á30 3Á36 65Á06 0Á19 6Á82 3Á00 4219Á49 12Á47 4Á96 2Á32 75Á27 0Á22 2Á52 2Á30 27Á62 <0Á1 3Á65 2Á22 1405Á03 4Á15 4Á19 1Á44 322Á04 0Á95 1Á13 1Á43 164Á38 0Á49 <0Á1 1Á42 196Á17 0Á58 0Á99 617Á36 1Á82 0Á41 0Á96 243Á61 0Á72 1Á00 0Á92 3Á23 <0Á1 0Á25 0Á84 208Á23 0Á62 0Á97 0Á81 61Á14 0Á18 <0Á1 0Á76 382Á84 1Á13 0Á23 0Á59 8Á41 <0Á1 0Á20 0Á57 136Á34 0Á40 0Á23 0Á42 604Á16 1Á79 0Á16 0Á40 216Á05 0Á64 0Á52 0Á33 16Á72 <0Á1 <0Á1 0Á32 71Á79 0Á21 0Á30 0Á29 17Á22 0Á05 <0Á1 0Á29 110Á58 0Á33 0Á51 0Á28 0Á39 <0Á1 0Á28 30Á54 <0Á1 <0Á1 0Á26 1Á45 <0Á1 0Á44 0Á26 26Á65 <0Á1 0Á33

72Á62 8Á52 0Á59 0Á15 0Á88 0Á63 1Á07 0Á43 1Á76 1Á78 0Á75 1Á00 0Á83 1Á44 0Á83 0Á33 0Á40 0Á73 0Á48 0Á29 0Á23 <0Á1 0Á24 0Á11 0Á10 0Á64 0Á58 0Á13 0Á25

1Á03 2Á46 20Á05 0Á92 2Á95 8Á68 1Á24 0Á71 1Á52 6Á30 11Á07 3Á63 1Á30 1Á87 0Á24 6Á58 4Á69 1Á80 2Á63 2Á20 0Á55 3Á14 0Á68 2Á00 <0Á1

82Á89 3Á03 <0Á1 0Á10 1Á36 0Á21 <0Á1 1Á66 0Á97 0Á60 0Á31 1Á59 0Á72 <0Á1 0Á60 0Á11 0Á37 <0Á1 0Á24 0Á96 0Á21 <0Á1 0Á18 <0Á1 0Á12 <0Á1 0Á14 <0Á1 0Á13

0Á60 1Á96 0Á29 0Á78 23Á63 <0Á1 0Á17 0Á27 1Á04 1Á21 2Á23 6Á82 0Á73 <0Á1 <0Á1 0Á87 4Á22 <0Á1 1Á34 8Á14 0Á44 0Á27 0Á45 0Á30 0Á20

97Á4 45Á1 28Á8 34Á5 94Á6 25Á5 21Á5 108Á2 76Á9 61Á4 59Á2 82Á9 114Á9 15Á0 63Á3 55Á0 27Á1 18Á5 100Á1 102Á5 69Á6 57Á8 82Á6 46Á4 69Á7 14Á0 70Á6 27Á2 45Á9

5­240 5­140 10­80 5­110 40­310 5­160 10­110 20­400 10­190 10­160 20­100 10­230 20­180 5­50 10­160 20­100 10­150 10­140 10­290 10­210 5­120 30­90 20­140 20­70 5­160 10­30 10­130 10­70 10­160

# 2008 The Authors 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 73, 1314­1336

APPENDIX. Continued

Mean biomass % <0Á1 0Á32 <0Á1 <0Á1 <0Á1 0Á33 <0Á1 <0Á1 0Á15 <0Á1 0Á23 0Á10 <0Á1 <0Á1 <0Á1 0Á53 0Á55 <0Á1 <0Á1 0Á59 <0Á1 0Á84 0Á52 <0Á1 0Á31 0Á44 <0Á1 0Á12 <0Á1 0Á16 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á14 <0Á1 <0Á1 0Á98 <0Á1 <0Á1 <0Á1 <0Á1 0Á24 0Á11 <0Á1 <0Á1 0Á86 <0Á1 0Á18 1Á38 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á14 <0Á1 <0Á1 0Á10 0Á18 0Á10 0Á10 <0Á1 0Á22 <0Á1 1Á35 0Á28 1Á53 1Á53 0Á83 1Á56 <0Á1 0Á20 <0Á1 <0Á1 <0Á1 0Á12 0Á16 <0Á1 <0Á1 0Á46 <0Á1 1Á05 37Á80 0Á15 <0Á1 g ha

À1

Mean density

À1

Total density (%) Upper Middle Lower

Total biomass (%) Frequency of Mean Upper Middle Lower occurrence (%) LS (mm) LS (mm)

Species

Individuals ha

%

SEASONAL CHANGES IN ASSEMBLAGES

# 2008 The Authors Journal compilation # 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 73, 1314­1336

Eucinostomus melanopterus Citharichthys arenaceus Sphoeroides greeleyi Rhinobatus horkeli Diapterus argenteus Chirocentrodon bleekerianus Anchoa hepsetus Selene vomer Cynoscion acoupa Bairdiela ronchus Eugerres brasilianus Caranx hippos Cetengraulis edentulus Synodus foetens Oligoplites saurus Mullus auratus Stephanolepis hispidus Genidens barbus Pellona harroweri Anchoa lyolepis Lagocephalus laevigatus Hyppocampus reiidi Menticirrhus littoralis Cyclichthys spinosus Anchoa spinifer Bathygobios soporator Cynoscion sp. Ctenogobius schuifeldti Gobioides broussonnetii Carangoides bartholomaei <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á26 0Á25 <0Á1 0Á12 <0Á1 0Á10 <0Á1 0Á15 <0Á1 <0Á1 0Á12 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á21 <0Á1 0Á13 <0Á1 <0Á1 0Á15 <0Á1 <0Á1 <0Á1 0Á13 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1

3Á40 3Á36 2Á97 2Á74 2Á72 2Á63 2Á35 2Á16 1Á90 1Á88 1Á80 1Á76 1Á47 1Á39 1Á38 1Á36 1Á34 0Á95 0Á92 0Á77 0Á76 0Á55 0Á49 0Á34 0Á32 0Á14 0Á11 0Á11 0Á07 0Á05 3 3 3 2 2 1 1 8 13 8 14 2 1 4 4 5 3 8 3 8 2 17 1 1 1 14 3 1 4 1

0Á22 0Á22 0Á20 0Á18 0Á18 0Á17 0Á16 0Á14 0Á13 0Á12 0Á12 0Á12 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1

33Á75 30Á53 69Á02 1821Á83 16Á92 2Á75 0Á22 17Á13 39Á41 27Á15 30Á01 6Á59 18Á02 64Á67 18Á91 8Á79 67Á14 43Á06 0Á86 0Á50 20Á30 3Á22 14Á35 61Á89 3Á71 1Á05 0Á01 0Á04 2Á93 0Á31

0Á10 <0Á1 0Á20 5Á38 <0Á1 <0Á1 <0Á1 <0Á1 0Á12 <0Á1 <0Á1 <0Á1 <0Á1 0Á19 <0Á1 <0Á1 0Á20 0Á13 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á18 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1

63Á0 59Á2 49Á6 410Á8 55Á4 48Á8 13Á6 46Á5 76Á8 76Á9 65Á5 38Á5 71Á8 141Á2 89Á0 130Á1 43Á5 135Á2 35Á4 29Á3 71Á9 73Á3 60Á0 104Á3 34Á0 57Á5 10Á0 22Á5 350Á0 60Á0

10­90 10­170 10­140 140­670 30­90 50­70 10­20 20­80 10­170 40­11 40­100 10­110 20­140 20­230 50­150 90­150 5­190 50­250 20­140 20­40 40­140 60­90 60 40­220 20­60 50­60 10 20­30 280­420 60

1335

APPENDIX. Continued

Mean biomass % <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á10 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 1Á78 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 g haÀ1 % Upper Middle Lower Total density (%) Total biomass (%) Frequency of Mean Upper Middle Lower occurrence (%) LS (mm) LS (mm)

1336

Mean density

Journal compilation

Species

Individuals haÀ1

#

M. BARLETTA ET AL.

Stellifer brasiliensis Selene setapinnis Gobionellus ocellatus Urophisis brasiliensis Oligoplites palometa Macrodon ancylodon Dasyatis guttata Dormitator maculatus Trachinotus falcatus Arius parkeri Batrachoides sp. Anchoa tricolor Centropomus parallelus Epinephelus itajara Pleuronectes sp. Sphyraena barracuda Rypticus randalli Paralichthys orbignyanus Narcine brasiliensis Trichiurus lepturus Total Total mean catch Number of species Number of samples Sampled area (m2) <0Á1 <0Á1 2147 1981 451 32 774 49 504 14 007 38 556 34 519 8453 588 674 862 421 262 697 63 66 60 78 78 78 179 614 174 214 187 547

0Á05 0Á05 0Á04 0Á04 0Á03 0Á03 0Á03 0Á03 0Á03 0Á03 0Á02 0Á02 0Á02 0Á02 0Á02 0Á02 0Á02 0Á02 0Á02 0Á01 1513 81 910 79 234 541 375 1 8 1 3 3 6 1 1 1 1 1 1 1 3 8 3 1 1 1 1

<0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1

0Á60 0Á24 4Á10 0Á22 2Á08 0Á07 286Á69 0Á04 6Á52 1Á32 0Á08 0Á21 1Á63 0Á09 2Á10 0Á06 0Á30 1Á42 4Á88 1Á27 33 837 1 831 851

<0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 0Á85 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1 <0Á1

65Á0 46Á0 270Á0 70Á0 90Á0 40Á0 640Á0 60Á7 170Á0 120Á0 70Á0 90Á0 160Á0 60Á0 120Á0 270Á0 80Á0 88Á2 330Á8 498Á8

30­100 30­50 270 70 90 40 640 60,7 170 120 70 90 160 60 120 270 80 88,2 330,8 498,8

# 2008 The Authors 2008 The Fisheries Society of the British Isles, Journal of Fish Biology 2008, 73, 1314­1336

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