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BULLETIN OF MARINE SCIENCE, 80(3): 647–680, 2007

Comparison of fish assemblages and guilds in tropical habitats of the Embley (Indo-West Pacific) and Caeté (Western Atlantic) estuaries Mário Barletta and Stephen J. M. Blaber ABSTRACT

Fish assemblages of two tropical estuaries are compared with regard to taxonomic structure and functional guilds using biomass data from different habitats of the Embley Estuary (north Australia) and the Caeté Estuary (north Brazil). First, the similarity of the habitats of the two estuaries was compared using taxonomic classification of their respective ichthyofauna. Important taxonomic differences between the two estuaries emerged: the Neotropical fish species of the upper Caeté Estuary have no equivalents in the Embley Estuary, and the diverse chondrichthyan fauna of the Embley have no equivalents in the Caeté Estuary. On the other hand, the more ubiquitous families Engraulidae, Sciaenidae, Ariidae, Carangidae, Haemulidae, and Clupeidae, which were characteristic of the main channel and mangrove tidal creeks of the Caeté Estuary, showed 70% similarity with the main channel of the Embley Estuary. Second, the similarity of the fish assemblages was compared in terms of ecological guilds (estuarine use and feeding mode). For the Embley Estuary, marine immigrants (mainly piscivorous and benthophagous) were the dominant functional guild, whereas in the Caeté Estuary, the estuarine functional guild (mainly benthophagous) contributed to more than 50% of the biomass in each habitat. Factorial analysis of species functional guilds shows that the first factorial axis was formed positively by the dominant fish species which spend part of their life cycle in Embley Estuary habitats, principally in the main channel, tidal channel (anadromous/piscivorous, marine immigrants/piscivorous, benthophagous, detritivorous, and marine stragglers/piscivorous), and negatively by dominant estuarine (planktivorous and benthophagous) fish species which spend their life in the seagrass beds and in the mangrove intertidal creeks. The second factorial axis best represented the distribution of fish species in the estuary (upper, middle, and lower), which was evident in the Caeté than in the Embley Estuary, where the freshwater and marine straggler guilds were most important in determining this second factorial axis.

Organisms, organic matter, and nutrients are transferred between freshwater and the ocean via estuaries and nearshore coastal waters (Lee, 1995; Wolanski, 1995; Barletta-Bergan et al., 2002a,b; Barletta et al., 2003, 2005). Fish landings around the world are composed of species that spend part of their lives in estuarine waters (Barthem, 1985; Pauly and Yáñes-Arancibia, 1994; Barthem and Goulding, 1997; Barletta et al., 1998; Blaber, 2000; Islam and Haque, 2004). Like estuaries in temperate regions (Thiel et al., 1995), tropical (Blaber and Blaber, 1980; Barletta-Bergan et al., 2002a,b; Barletta et al., 2003, 2005; Dorenbosch et al., 2005) and sub-tropical estuaries (Jaureguizar et al., 2004) act as nursery areas for many invertebrate and fish species. The species composition of estuarine fish assemblages is dictated by a combination of biotic and abiotic variables, particularly competition for space and food, tolerance of diel and seasonal changes in salinity, turbidity, and temperature (Cyrus and Blaber, 1987a,b; Blaber et al., 1989, 1990; Cyrus and Blaber, 1992; Barletta et al., 2003, 2005; Krumme et al., 2005). An understanding of the roles and relative importance to fish of different habitats within estuaries is necessary for both management and conserBulletin of Marine Science

© 2007 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

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vation (Elliott and Hemingway, 2002). Although there have been many comparative studies of the fish assemblages of estuaries and their relationships with habitat types and physical conditions, they have generally been restricted to one zoogeographic region. Such studies have demonstrated that factors such as geology, geomorphology, and more immediate environmental factors such as salinity and temperature, are associated with fish distributions, species richness, and fisheries catch (Vieira and Musik, 1993, 1994; Mahon et al., 1998; Mathieson et al., 2000; Araújo and Azevedo, 2001; Roy et al., 2001; Thiel et al., 2003). In addition, broad-scale comparisons of tropical estuaries across zoogeographic regions have indicated possible significant differences in the ways in which their fish assemblages use the various estuarine habitats, as well as differences in their patterns of species composition (Blaber, 2000). For example, it has been suggested that the relative proportions of freshwater and marine species using estuaries may be different (Blaber, 2000; Barletta et al., 2003, 2005). To explore possible fundamental similarities and differences in tropical estuarine fishes from different zoogeographic realms, it is necessary to compare their fish assemblages, not only taxonomically, but also in terms of their ecological structure and resource use in different habitats of the estuary. In this paper, the fish assemblages of two tropical estuaries, one in the Indo-West Pacific and one in the Tropical West Atlantic, are compared with regard to taxonomic structure, estuarine functional groupings, and habitat use. Material and Methods Source of Data and Study Sites Previously unpublished and published data sets of the authors were used for this study. Analyses based on biomass percentage for different habitats of each estuary were used. The source of each data set is described below. Data were available for a total of 10 individual estuarine habitats of Embley Estuary (North Australia) and Caeté Estuary (North Brazil). Location characteristics and sampling methods are described below. Embley Estuary.—The Embley Estuary (12˚37´S; 141˚50´E) is approximately 59 km long, almost entirely fringed by a well developed intertidal zone of mangrove forest (2962 ha), and with a freshwater catchment of 2076 km2. It has a maximum tidal range of 2.6 m. The mangrove forest is drained by tidal channels and mangrove tidal creeks. Seagrass beds occur on the south side of the lower reaches. Samples were taken in the main channel (upper–MCUe, middle–MCMe, and lower–MCLe; monofilament gill nets–66 m of 50, 75, 100, 125, and 150 mm stretch mesh), tidal channel (middle–TCMe and upper–TCUe; multifilament block net– 50 mm stretch mesh), mangrove tidal creeks (middle–MTCe) (rotenone), intertidal sandy mud beaches (lower–BLe; seine net–60 m × 2 m of 25 mm stretch mesh fitted with a 25 mm cod-end), seagrass beds (lower–SLe; beam trawl–2 m × 1 m with 28 mm stretch mesh fitted with a 12 mm mesh cod-end was towed at 5 km hr–1 and rotenone–20 m2 sampled area) and intertidal mud flats (lower–IMLe; stake net–240 m × 2 m × 50 mm stretch mesh). Sampling methods and study area details are available in Blaber et al. (1989), Blaber et al. (1990), Blaber (2000), and Cyrus and Blaber (1992). Caeté Estuary.—Caeté River and its estuary (1˚07´S; 46˚40´E) has a length of approximately 100 km, a freshwater catchment of 3000 km2, and a inundation area (mangrove forest and wetland) of approximately 100 km2. Salinity is higher during the dry season. During the rainy season, freshwater run-off contributes to the salinity decrease throughout the estuary, and even in adjacent coastal waters. The coastal plain is a macro tidal (4–5 m) depositional system and is characterized by sand-mud and mud sediments. The mangrove forest is drained by tidal channels, mangrove tidal creeks, and mangrove intertidal creeks. In this region the mangrove forest is flooded twice daily at high tide. During low tide the mangrove is exposed.

BARLETTA AND BLABER: FISH ASSEMBLAGES AND ESTUARINE GUILDS COMPARISON

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Fish samples were collected in the main channel (upper–MCUc, middle–MCMc, and lower–MCLc; otter trawl net–7.72 m long and consisted of 35, 22, and 7.2 mm stretch mesh in the body, cod-end and cover, respectively), in the mangrove tidal creeks (lower–MTCc; block net–30 m × 5 m and stretch mesh 10 mm) and in the mangrove intertidal creeks during low tide (upper–MICUc, middle–MICMc, and lower–MICLc; ichthyocide–cunabí–250 g 10 m 2). The tidal channel (lower–TCLc) was sampled using a seine net (15 m × 2 m and stretch mesh 10 mm) during low tide. Sampling methods and the study area details are available in Barletta (1999) and Barletta et al. (2000), (2003), and (2005). Data Classification and Analysis The fish species were classified taxonomically and by the estuarine use and feeding mode functional groups guilds described by Elliott et al. (in press) who proposed eight estuarine use functional groups: marine stragglers, marine immigrants, estuarine species, anadromous, catadromous, aphidromous, freshwater stragglers, freshwater immigrants; and seven feeding mode functional groups: planktivorous, detritivorous, herbivorous, piscivorous, benthophagous, hyperbenthophagous, opportunistic (see Appendix). Fish nomenclature followed Nelson (1994), Eschemeyer (2006), Marceniuk and Menezes (2007), and Froese and Pauly (2006). Data were available as species biomass per unit area or catch per unit effort (CPUE), depending on the sampling methods employed. Species biomass or CPUE (in grams) for each individual habitat were summed for the entire time series and the percentage was calculated for each species per habitat. A similarity matrix (presence/absence) using Bray-Curtis index was computed for the R analysis; where the fish species (for each estuary separated) and families (both estuaries together) were considered as attributes (Clarke and Warwick, 1994). Preceding the analyses, the original data matrix for species was reduced to remove any undue effects of rare species on the analysis (Gauch, 1982). The similarity matrix using the Bray-Curtis index was computed using Primer 5 (Plymouth routines in multivariate ecological analysis: Clarke and Warwick, 1994). Multidimensional scaling analysis (MDS) was performed on a Bray-Curtis (presence/ absence) similarity index matrix where each habitat from each estuary (species level) and for both estuaries (family level) (described above) were considered as attributes. Factorial analysis of biomass data (percentage) for each estuarine functional group and for feeding mode groups for each habitat of both estuaries was conducted after log10 (x+1)-transformation (Legendre and Legendre, 1998). Statistical associations of the estuarine functional groups and feeding mode patterns were thereby quantified and compared between estuaries.

Results Taxonomic Comparisons Patterns in the Fish Species Structure and Species-environment Associations.— Embley Estuary.—The cluster analysis distinguished two main groups among the 65 dominant species in six habitats of this estuary (Fig. 1A). Group I consisted of two sub-groups: The first sub-group was represented by species which occurred in shallow (< 2 m) intertidal beach areas of the lower estuary (sand/mud) (Leiognathus equulus, Ambassis nalua, Gerres filamentosus, Leiognathus decorus, Arrhamphus sclerolepis, Anodontostoma chacunda, Acanthopagrus berda, Pseudorhombus elevatus, Sillago analis, and Trixiphichthys weberi) and species which were common in beach (sand/mud-lower estuary), seagrass (lower estuary), and mangrove intertidal creeks (middle estuary) (Terapon jarbua, Pseudomugil gertrudae, Zenarchopterus buffonis, Sardinella albella, Tetraodon erythrotaenia, and Omobranchus rotundiceps). Sub-group 2 was represented by species characteristic of the seagrass habitat (Arothron immaculatus, Monacanthus chinensis, Acreichthys tomentosus, Siganus

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Figure 1. For the Embley Estuary, (A) Cluster dendrogram based on similarities of the most important species distribution in different habitats, and (B) MDS plot of the habitats [MICM, mangrove intertidal creeks middle-; SBL, beach (sand/mud) lower-; SGL, seagrass lower-; MTCU, mangrove tidal creek upper-; MTCM, mangrove tidal creek middle-; MCU, main channel upper-; MCM, main channel middle-; MCL, main channel lower- and IML, intertidal mud flat lower estuary], in which these species occur. Samples were clustered by group average of Bray-Curtis similarity index (presence/absence). Species codes are listed in the appendix.


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canaliculatus, Lethrinus lentjan, Gerres longirostris, Lutjanus russellii, Secutor ruconius, Apogon rueppellii, Pelates quadrilineatus, Amniataba caudavittata, Centrogenys vaigiensis, Epinephelus coioides, Ambassis dussumieri, and Chelonodon patoca). Group II contained three sub-groups: The first sub-group was represented by species which occur principally in the middle and upper tidal channel and mangrove intertidal creeks (Toxotes chatareus, Stolephorus carpentariae, Tylosurus punctulatus, and Sphyraena putnamae), and by species, except Carcharhinus leucas, which occur principally in the middle and upper main channel and tidal channel (Pomadasys argenteus, Gnathanodon speciosus, Epinephelus malabaricus, Megalops cyprinoides, Arius sp. 2, Nematalosa erebi, Arius proximus, Arius macrocephalus, Valamugil buchanani, Scomberoides commersonnianus, Liza subviridis, Pomadasys kaakan, Lates calcarifer, Rhynchobatus australiae, Negaprion acutidens, Drepane punctata, and Polydactylus macrochir). Sub-group 2 included species that occur mainly in the intertidal mudflats (lower estuary) (Gerres erythrourus, Tylosurus crocodilus, Himantura uarnak, Pastinachus sephen, and Taeniura lymna). The third sub-group contained species which were more frequent in the main channel (lower estuary) (Lactarius lactarius, Sciades mastersi, Rhizoprionodon acutus, Carcharhinus dussumieri, Carcharhinus cautus, Carcharhinus amblyrhynchoides, and Eleutheronema tetradactylum). The resulting MDS plot, based on the importance of each estuarine habitat for the dominant species shows that, in the Embley Estuary, the habitats divided in two groups (Fig. 1B). The first group (I) was the shallow water habitats located in the lower and middle estuary [seagrass beds, beach (sand/mud)] and mangrove intertidal creeks). All of these habitats are adjacent to the tidal channels of the middle and lower estuary. The second group (II) contained the deeper water habitats of the main channels of the upper, middle and lower reaches, the tidal channels of the upper and middle reaches and the intertidal mud flats of the lower reaches. Caeté Estuary.—Two main groups were also identified from this estuary (Fig. 2A). Group I can be divided in two sub-groups: Sub-group 1 contained species which stay in the mangrove creeks at low tide, mainly in crab burrows (Myrophis punctatus and Guavina guavina), or buried or attached to the Rhizophora mangle roots (Gobionellus oceanicus, Evortodus lyricus, Ctenogobius stigmaticus, and Ctenogobius smaragdus). Poecilia sp. and Gambusia sp. stay in open water during low tide. Sub-group 2-A, consisted of species, both adults and juveniles, which occur in the mangrove creeks throughout the year (Sciades herzbergii, Cathorops agassizii, Anchovia clupeoides, Pterengraulis atherinoides, Anableps anableps, Stellifer naso, Genyatremus luteus, Cynoscion acoupa, Colomesus psitacus, Aspistor parkeri, and Sciades proops). Sub-group 2-B contained species which are more common in the mangrove tidal creeks during high tide (lower estuary) (Caranx latus, Selene vomer, Epinephelus itajara, Strongylura timucu, Batrachoides surinamensis, Cetengraulis edentulus, Rhinosardinia amazonica, Megalops atlanticus, Scomberomorus maculatus, Trichiurus lepturus, Lutjanus jocu, and Caranx crysus). Group II consisted of species characteristic of the main channels of the upper estuary (II-1-A) (Hypostomus plecostomus, Plagioscion squamosissimus, Eigenmania virescens, Distocyclus conirostris, and Gymnotus carapo), and upper and middle estuary (II-1-B) (Aspredo aspredo, Stellifer microps, Pseudauchenipterus nodosus, Brachyplatystoma vaillanti, and Aspredinichthys filamentosus), and middle and lower estuary (II-2) (Stellifer rastrifer, Cathorops spixii, and Conodon nobilis).

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Figure 2. For the Caeté Estuary, (A) Cluster dendrogram based on similarities of the most important species distribution in the different habitats, and (B) MDS plot of the habitats (MICU, mangrove intertidal creek upper-; MICM, mangrove intertidal creek middle-; MICL, mangrove intertidal creek lower-; MTCL, mangrove tidal creek lower-; TC, tidal channel lower-; MCU, main channel upper-; MCM, main channel middle; MCL, main channel lower estuary). Samples were clustered by group average of Bray-Curtis similarity index (presence/absence). Species codes are listed in the appendix.


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Results of MDS analysis of habitat groups based on the distribution of dominant species in the Caeté Estuary indicate that as in the Embley Estuary, the habitats in the Caeté Estuary could be divided in two groups (Fig. 2B). The first group included the habitats of the main channel of the upper, middle, and lower estuary. Group two consisted of the intertidal mangrove creeks (upper, middle, and lower estuary), and the mangrove intertidal channel and tidal channel habitats of the lower estuary. All of these habitats are located in shallow waters adjacent to the main channels. Analysis of Taxonomic Similarity Many families were common to both estuaries. Embley Estuary had the highest diversity in both numbers of species (203) and families (65). For this estuary, the families Carcharhinidae (12 spp.—main channel, tidal channel, and intertidal mudflats), Carangidae (10 spp.—main channel, tidal channel, beaches, intertidal mudflat, and mangrove intertidal creeks), and Gobiidae (16 spp.—beaches, seagrass, and mangrove intertidal creeks) had the highest number of species (Table 1). In Caeté Estuary, the families Ariidae (10 spp.—main channel, mangroves tidal creeks, and tidal channels), Carangidae (12 spp.—main channel and mangroves tidal creeks), Sciaenidae (15 spp.—main channel am mangrove tidal creeks), and Gobiidae (10 spp.—main channel, mangrove intertidal, and tidal creeks) were the families with the highest number of species (Table 2). Species diversity was highest in the main channel, beaches, seagrass, and mangrove intertidal creeks in the Embley Estuary and in the main channel and mangrove tidal creeks of the Caeté Estuary. Assessment of the similarity of estuarine habitats of two estuaries based on taxonomic classification was undertaken using presence/absence of common families. This analysis showed, at 60% similarity, a clear major division into three separate groups of habitats for each estuary (Fig. 3), but overall, these two estuaries were clearly separated at only a relatively low level of similarity (40%). Based on this information, further cluster analyses were undertaken at the family level, based on the habitats clustered in each estuary. Comparisons were conducted between each cluster from one estuary and each from the other estuary. Family composition comparisons among mangrove intertidal creeks (MICc–Caeté Estuary) and the groups of habitats from Embley Estuary showed very low similarity (< 30%) (Fig. 4B 1 and 2). Even when compared with others habitats of Caeté Estuary, this habitat showed low similarity (40%) (Fig. 4A). The main channel of Caeté Estuary (MCc) and the main channel (MCe), tidal channel (TCe), and intertidal mudflats (IMe) from the Embley Estuary showed also low similarity (< 20%) (Fig. 4D 1). This group consisted of families which are characteristic of the upper reaches of Caeté Estuary. They include Auchnipteridae, Pimelodidae, Loricaridae, Auchnipteridae, Characidae, Sternopygidae, and Gymnotidae, families that are characteristic of the neotropical region. On the other hand, the more ubiquitous families Engraulidae, Sciaenidae, Ariidae, Carangidae, Haemulidae, and Clupeidae which are characteristic of the main channel (lower and middle reaches) of Caeté Estuary showed 70% similarity with the main channel of the Embley Estuary (Fig. 4D 3-b-2). Comparisons between the main channel (MCc–Caeté Estuary) and seagrass bed habitats (SLe– Embley Estuary) revealed two main groups (Fig. 4E). Group I consisted of the families characteristic of seagrass habitats, and group II (at the level of 70% of similarity) was divided in two sub-groups: Sub-group “a” consisted of the common families of

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Taxonomic groups Carcharhinidae Sphyrnidae Pristidae Rhinobatidae Dasyatidae Myliobatidae Rhinopteridae Elopidae Megalopidae Ophicthidae Clupeidae Pristigasteridae Engraulidae Chirocentridae Chanidae Synodontidae Ariidae Plotosidae Batrachoididae Hemirhamphidae Belonidae Atherinidae Pseudomugilidae Syngnathidae Platycephalidae 1

1

3

3

1

1

1

1

1

3

1 1

2

1

1

Main channel Middle Lower 4 8 2 1 1 1 1

1

Upper 7 1 1 1

2 1 4

1

1

1

2 1

1

1

1

Tidal channel Upper Middle 2 2

Table 1. Number of fish species per family in each habitat of Embley Estuary.

2 3 2 1 2 2

3

4

1

1 2

Beaches Lower

2 2

1

1

1

1

Seagrass Lower

Intertidal mudflats Mangroves intertidal creeks Lower Middle Total 1 12 2 2 1 2 6 7 1 1 1 1 1 1 1 5 7 1 1 2 5 1 1 1 1 1 9 1 1 1 3 6 2 2 6 1 2 1 1 1 4 2 3

654 BULLETIN OF MARINE SCIENCE, VOL. 80, NO. 3, 2007

26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50

Taxonomic groups Centropomidae Ambassidae Serranidae Centrogeniidae Terapontidae Apogonidae Sillaginidae Lactariidae Rachycentridae Echeneidae Carangidae Stromateidae Leiognathidae Lutjanidae Gerreidae Haemulidae Lethrinidae Sparidae Sciaenidae Mullidae Monodactylidae Toxotidae Drepaneidae Ephippidae Scatophagidae

Table 1. Continued.

1 2

1

2

1

1

2 1

2

1

1

1

2

1

3

1

Main channel Middle Lower 1 1

1

Upper 2

1 1

1

1 1 1

1

2

1 1 1 1

2

2

Tidal channel Upper Middle 1 1 1 1

1 1 1 2

1 1 1

5

7

2

3

2

Beaches Lower 1 1

1

6 1 4

Seagrass Lower 2 3 1 1 3 3 1

Intertidal mudflats Mangroves intertidal creeks Lower Middle Total 1 2 3 3 3 1 2 5 1 4 4 6 1 1 1 1 1 1 2 10 1 2 4 9 2 2 4 1 2 5 2 1 3 1 1 1 1 2 1 1 1 1 1 1 1 2 1 1 2


655

51 52 53 54 55 56 57 58 59 60 61 62 63 64 65

Taxonomic groups Chaetodontidae Mugilidae Sphyraenidae Polynemidae Blenniidae Callionymidae Gobiidae Eleotridae Signatidae Scombridae Paralichthyidae Soleidae Triacanthidae Monacanthidae Tetraodontidae No. of species No. of families

Table 1. Continued.

1

35 19

34 21

2

2

1

26 16

2

1

1

3

Main channel Middle Lower

3

Upper

25 18

1

2 1 2

28 21

1

3 1 1

Tidal channel Upper Middle

2 1 2 1 3 71 34

1 2

5 2

Beaches Lower

3 3 51 24

1

3 1 4

Seagrass Lower 2

Intertidal mudflats Mangroves intertidal creeks Lower Middle Total 2 4 5 5 1 1 3 1 2 1 1 1 11 16 1 4 4 1 1 2 2 2 3 1 4 5 37 66 203 24 29


1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25

Taxonomic groups Gymnuridae Megalopidae Ophicthidae Clupeidae Pristigasteridae Engraulidae Ariidae Batrachoididae Belonidae Centropomidae Serranidae Gerreidae Carangidae Haemulidae Sciaenidae Ephippidae Mugilidae Polynemidae Gobiidae Eleotridae Trichiuridae Scombridae Paralichthyidae Achiridae Cynoglossidae 1 2 1

1

1

1 2 1

3

2

5

1 2 1

5 2 9 1 1

6 1 11 1 1

3 1 9 1 1

2 1 4 8 1

2 1 5 7 1

1 1 4 9 1

Main channel Upper Middle Lower 1 1 1 1

1

4 2

1

1

6 1

1

3

1

Mangroves Intertidal creeks Upper Middle Lower

Table 2. Number of fish species per family in each habitat of Caeté Estuary.

1 1 1 1

5 3 1 1 1 1 1 8 1 9 1 1 1 1

1

1

Mangroves Tidal creeks Lower

1

1

1 2

4

2

Tidal channels

Total 1 1 1 3 1 6 10 1 1 1 1 1 12 2 15 1 1 1 10 3 1 1 1 2 1


657

26 27 28 29 30 31 32 33 34 35 36 37

Taxonomic groups Tetraodontidae Diodontidae Ogcocephalidae Aspredinidae Pimelodidae Auchnopteridae Loricariidae Gymnotidae Sternopygidae Characiidae Poecilidae Anablepidae No. of species No. of families

Table 2. Continued.

55 22

5 3 1 2 1 2 2 50 20

1

1 5 2 1

46 19

1

5

Main channel Upper Middle Lower 1 2 1

11 7

1

1

11 4

2 4 2

Mangroves Intertidal creeks Upper Middle Lower

1 37 23

1

Mangroves Tidal creeks Lower 1 1

1 13 8

Tidal channels 1

Total 3 1 1 5 3 1 2 1 2 2 2 1 103



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Figure 3. Cluster dendrogram based on similarities in the distribution of fish families in the habitats of the Caeté Estuary (CE) (MICc, mangrove intertidal creeks; MCc, main channel; MTCc, mangrove tidal creeks; TCc, tidal channel) and the Embley Estuary (EE) (MCe, main channel; TCe, tidal channel; IMe, intertidal mudflats; SGe, seagrass beds; SBe, sand/mud beaches; MICe, mangrove intertidal creeks). Samples were clustered by group average of Bray-Curtis similarity index (presence/absence).

both habitats, and sub-group “b”, the families characteristic of the upper, middle, and lower reaches of the Caeté Estuary. Comparisons of the main channel of the Caeté Estuary (MCc) with the beach, sand/ mud, (Be), and mangrove intertidal creeks (MICe) of the Embley Estuary revealed four groups at the level of about 60% similarity (Fig. 4F). The first group comprised families characteristic of the upper reaches of the main channel of Caeté Estuary. The second group was represented by the families common to the main channel of Caeté Estuary (MCc) and to the sand/mud beach habitats. Group 3 contained families characteristic of the beach (sand/mud) habitat of the Embley Estuary, sub-group 4-a, those common to the mangrove intertidal creeks and beach (sand mud) (subgroup 3-a), and sub-group 4-b, those characteristic of the mangrove intertidal creeks of the Embley Estuary (Fig. 4F 4-b). Mangrove tidal creeks and tidal channels (MTCc and TCc–Caeté Estuary), and main channel, tidal channel, and intertidal mudflats (MCe, TCe, and IMe–Embley Estuary) comparisons (Fig. 4G) revealed four groups at the level of 60% similarity. The first group consisted of families characteristic of the mangrove tidal creeks and tidal channel of the Caeté Estuary. Groups 2 and 3 were formed by families characteristic of tidal channels and intertidal mudflats, respectively, of the Embley Estuary. Group 4, at 80% of similarity, consisted of sub-group 4a, which contained the families common in the main channel and tidal channel of the Embley Estuary, and sub-group 4b were families common to these habitats in both estuaries. The comparison of mangrove tidal creeks (MTCc) and tidal channels (TCc) of the Caeté Estuary with the seagrass beds (SLe) of the Embley Estuary revealed that the

660


Figure 4. Cluster dendrogram based on similarities in the distribution of fish families in the different habitats of both estuaries: (A) mangrove intertidal creeks (MICc–Caeté Estuary) and main channel (MCe-), tidal channel (TCe-), and intertidal mudflats (IMe–Embley Estuary); (B) mangrove intertidal creeks (MICc–Caeté Estuary) and seagrass beds (SGe–Embley Estuary); (C) MICc and sand/mud beaches (SBe), mangrove intertidal creeks (MICe–Embley Estuary); (D) (see page 661) main channel (MCc–Caeté Estuary) and MCe, TCe, and IMe; (E) MCc and SGe; (F) MCc and SBe, and MICe; (G) (see page 662) mangrove tidal creeks (MTCc), and tidal channel (TCc–Caeté Estuary) and MCe, TCe, and IMe; (H) MTCc, and TCc and SGe; (I) MTCc, and TCc and SBe, and MICe. Samples were clustered by group average of Bray-Curtis similarity index (presence/absence). The common families (CF) among habitats are indicated.


Figure 4. Continued.

661

662

Figure 4. Continued.



663

estuaries had only two families in common (Group 2-a-1)—the ubiquitous Engraulidae and Tetraodontidae. The comparison between the mangrove tidal creeks (MTCc) and tidal channels (TCc) of the Caeté Estuary, and the beach (sand/mud) (BLe), and mangrove intertidal creeks (MICe) of the Embley Estuary revealed four groups at a 60% level of similarity (Fig. 4I). The first group comprised the families characteristic of mangrove tidal creeks and tidal channels of the Caeté Estuary. The common families for all habitats from both estuaries were represented in group 2. Groups 3 and 4 were represented by families’ characteristic of the beach and mangrove intertidal creeks of the Embley Estuary, respectively. Ecological Comparisons Analysis by Estuarine Use and Feeding Mode Functional Groups (Guilds).—The proportions of each guild in terms of biomass varied among habitats within and between estuaries (Table 3). For the Embley Estuary, marine immigrants (66%), marine stragglers (17%), estuarine (12%), and anadromous (10%) guilds were dominant. Marine immigrants (piscivorous–main channel and tidal channel; benthophagous–main channel upper, beach (sand/mud), and intertidal mudflats) were the dominant functional guild in the Embley Estuary, but marine stragglers (piscivorous) were also important in the main channel and tidal channels. Mangrove intertidal creeks (MICMe–38.4%) and seagrass (Sle–20.1%) habitats were important habitats for the estuarine guild (Table 3). In contrast, in the Caeté Estuary the estuarine guild (82%), principally benthophagous fish (81%), was dominant and contributed to > 50% of biomass in each habitat (Table 3). Marine immigrants (planktivorous and hyperbenthophagous) were only important in the habitats of the lower reaches of this estuary. Cluster analysis of the percentage of biomass composition of functional guilds (Fig. 5) indicated a major division at low similarity levels among all habitats of both estuaries. However, at around 60%– 70% similarity, it was possible to separate the habitats of each estuary into two main groups. In the Embley Estuary group 1 was characterized by the sand/mud beaches (Ble) located in the lower estuary. In this habitat the marine immigrant—benthophagous (41%) was the most important functional guild (Table 3). Group 2 consisted of intertidal mudflat habitats also located in the lower estuary. This habitat was used principally by marine immigrant-benthophagous fish species (54%). The third group was formed by the main channel (upper, middle, and lower estuary), tidal channel (upper and middle estuary) where the predominant functional groups were the marine straggler-piscivorous, marine immigrant-piscivorous, and anadromous-piscivorous (Table 3). Seagrass bed habitat (Fig. 5-A, group 4; Table 3) was characterized principally by the presence of marine immigrant-planktivorous (33%) and hyperbenthophagous groups (35%), and the estuarine-planktivorous functional group (11%). The fifth group, mangrove intertidal creeks, was characterized principally by the functional groups marine immigrant-detritivorous (26%) and estuarine-herbivorous (23%). In the Caeté Estuary, the first group consisted of the mangrove intertidal habitats (upper, middle, and lower), where most of the species were estuarine (Table 3; Fig. 5B). Group 2 was formed principally by freshwater immigrants and stragglers, characteristic of the main channel of the upper estuary (MCUc; Fig. 5B), while group 3 contained estuarine and marine immigrant guilds characteristic of the upper (during the end of dry season) middle and lower main channel of Caeté Estuary (Fig. 5-3a). The sub-group 3b contained the mangrove tidal creeks and the tidal channel habitats. In those habitats, the most im-

Functional guilds 1. Marine straggler 1. Planktivorous 2. Piscivorous 3. Benthophagous 4. Hyperbenthophagous Total 2. Marine immigrant 1. Planktivorous 2. Detritivorous 3. Herbivorous 4. Piscivorous 5. Benthophagous 6. Hyperbenthophagous 7. Lepidophagous Total 3. Estuarine 1. Planktivorous 2. Herbivorous 3. Benthophagous 4. Omnivorous Total

(A) Embley Estuary MCMe 15.10 0.26 15.36 5.01 39.68 12.15 4.53 61.38

MCUe

19.38 1.72

21.10

32.08

9.86 24.27 6.92

73.14

46.85

32.74 4.95 6.90

2.24

41.83

41.80 0.03

MCLe

55.36

0.04 0.04

0.88 0.88

30.63 14.59 2.78

0.01 7.33

28.39

22.01 6.37

Habitats TCMe

60.50

9.06 0.34 31.36 14.35 5.37

27.36

27.36

TCUe

0.05 0.01 0.07

0.85 12.68 10.60 10.04 41.11 1.42 0.01 76.74

20.11

11.36 3.67 5.07

78.70

0.83 5.90 3.71 35.28

32.98

0.48 0.04 0.17 0.34 1.04

0.11 0.57 0.45 1.14

Sle

Ble

86.72

0.01 8.96 0.08 4.20 54.25 19.19

9.50

0.79 8.71

IMLe

23.51 0.03 38.45

14.90

14.56 25.56 2.60 3.53 12.27 1.16 0.74 60.45

0.01 0.01 0.05

0.02

MICMe

13.13 3.67 9.55 0.24 26.59

9.68 12.87 2.89 18.67 20.19 9.29 0.38 73.97

0.21 18.07 2.23 0.27 20.78

Average

Table 3. Biomass (%) of each functional guild for each habitat of (A) Embley Estuary—(BLe, sand/mud beach; IMLe, intertidal mudflats lower estuary; MCUe, main channel upper estuary; MCMe, main channel middle estuary; MCLe, main channel lower estuary; TCUe, tidal channel upper estuary; TCMe, tidal channel middle estuary; SGe, seagrass bed lower estuary; MICMe, Mangrove intertidal creeks), and (B) Caeté Estuary—(MICUc, mangrove intertidal creeks upper estuary; MICMc, mangrove intertidal creeks middle estuary; MICLc, mangrove intertidal creeks lower estuary; MCUc, main channel upper estuary; MCMc, main channel middle estuary; MCLc, main channel lower estuary; MTCLc, mangrove tidal creeks lower estuary; TCLc, tidal channel lower).


Functional guilds 4. Anadromous 1. Piscivorous Total 5. Fresh water immigrant 1. Planktivorous 2. Benthophagous Total (B) Caeté Estuary 1. Marine straggler 1. Planktivorous 2. Herbivorous 3. Piscivorous 4. Benthophagous Total 2. Marine immigrant 1. Planktivorous 2. Piscivorous 3. Benthophagous 4. Hyperbenthophagous Total 3. Estuarine 1. Piscivorous 2. Benthophagous 3. Hyperbhenthophagous Total

Table 3. Continued.

1.59 0.09 0.29 8.24 10.23 0.29 68.07 20.80 89.18

1.62 1.62 0.09 0.09 0.09 0.30 5.22 0.09 0.09 6.40 11.81 0.19 51.59 35.41 87.20

0.26 0.26

0.01 0.01

0.02

0.09 0.09 0.09 0.86 1.15

74.67 13.44 88.12

0.09 0.09 0.09 0.09 0.40

11.31 11.31

21.63 21.63

5.48 5.48

MCLe

MCMe

MCUe

3.54 74.98 4.10 82.63

12.57 0.25 0.47 1.62 14.92

0.52

0.34 0.16

11.25 11.26

TCUe

1.25 90.09 1.25 92.59

0.56 7.40

6.83

16.20 16.20

Habitats TCMe

97.36 97.36

98.49 98.49

100

100

1.04

MICMe

0.01

3.77 3.77

IMLe

1.03

0.13 0.13

Sle

0.01

22.00 22.00

Ble

1.32 81.91 15.01 98.24

5.26 0.14 0.24 3.54 9.18

0.07 0.14 0.12 0.10 0.43

0.53 0.94 1.47

11.47 11.47

Average BARLETTA AND BLABER: FISH ASSEMBLAGES AND ESTUARINE GUILDS COMPARISON

665

Functional guilds 4. Anadromous 1. Detritivous 2. Piscivorous Total 5. Fresh water straggler 1. Herbivorous 2. Benthophagous 3. Hyperbenthophagous 4. Lepidophagous Total 6. Fresh water immigrant 1. Planktivorous 2. Detritivorous 3. Hyperbenthophagous Total

Table 3. Continued.

0.19 0.29 0.09 0.39

1.07 3.70 4.77

0.10

0.10 0.19

0.09

0.09

0.97 4.67 0.09 0.09 5.84

MCMe

MCUe

0.94 0.95

0.10

0.94 0.03 0.98

TCUe

0.09

0.10

0.09

MCLe

Habitats TCMe

0.31 0.06 0.37

Average

0.76

0.36

2.63

1.69 0.60 1.90 4.19

MICMe

0.76

IMLe

0.66 2.44 0.10 0.10 3.30 2.63

Sle

0.36

0.29 0.08 0.37

Ble



667

Figure 5. Cluster dendrogram of habitats from (A) Embley Estuary (BLe, sand/mud beach; IMLe, intertidal mudflats lower estuary; MCUe, main channel upper estuary; MCMe, main channel middle estuary; MCLe, main channel lower estuary; TCUe, tidal channel upper estuary; TCMe, tidal channel middle estuary; SGe, seagrass bed lower estuary; MICMe, Mangrove intertidal creeks) and (B) Caeté Estuary (MICUc, mangrove intertidal creeks upper estuary; MICMc, mangrove intertidal creeks middle estuary; MICLc, mangrove intertidal creeks lower estuary; MCUc, main channel upper estuary; MCMc, main channel middle estuary; MCLc, main channel lower estuary; MTCLc, mangrove tidal creeks lower estuary; TCLc, tidal channel lower). Habitats were clustered by group average of Bray-Curtis Similarity index based on (log x+1) transformed biomass (%) of ecological guilds.

portant functional guild was the estuarine-benthophagous, which was responsible for 75% and 90% of total biomass, respectively (Table 3). Factorial analysis ordination biplot diagrams of species functional guild scores (Fig. 6), as well as regression statistics (Table 4) and cluster analysis (Fig. 5) permitted an interpretation of the distribution of the estuarine functional guilds in different habitats of both estuaries. The first factorial axis explained 40% of the total variability in the Embley Estuary and in the Caeté Estuary. This axis was formed positively by the dominant fish species which spend part

668


Figure 6. Factorial analysis ordination biplot showing the ecological guilds (see Table 4 for codes) centroids in relation to the different habitats in (A) Embley Estuary and (B) Caeté Estuary.

of their life cycle in Embley Estuary habitats, principally in the main channel and tidal channels (Anadromous/piscivorous, marine immigrants/piscivorous, benthophagous and detritivorous, and marine stragglers/piscivorous), and negatively by dominant estuarine (planktivorous and benthophagous) fish species which spend their life in the seagrass beds and in the mangrove intertidal creeks (Fig. 6A). The second factorial axis explained only around 20%–30% and best represented the distribution of fish species along the estuary (upper, middle, and lower). This was more evident in the Caeté than in the Embley Estuary (Fig. 6A,B). The freshwater and marine stragglers were most important in determining this second factorial axis in the Caeté Estuary (Fig. 6B). The freshwater Neotropical species were the most important in negatively determining the second factorial axis, and defined the main gradient structuring the fish species into ecological groups in the upper and lower Caeté Estuary.


669

Table 4. Results of factorial analysis for fuctional guilds from (A) Embley Estuary and (B) Caeté Estuary. (A) Embley Estuary Code Variables 11 Marine straggler/Planktivorous 12 Marine straggler/Piscivorous 13 Marine straggler/Benthophagous 14 Marine straggler/Hyperbenthophagous 21 Marine immigrant/Planktivorous 22 Marine immigrant/Detritivorous 23 Marine immigrant/Herbivorous 24 Marine immigrant/Piscivorous 25 Marine immigrant/Benthophagous 26 Marine immigrant/Hyperbenthophagous 27 Marine immigrant/Lepidophagous 31 Estuarine/Planktivorous 32 Estuarine/Herbivorous 33 Estuarine/Benthophagous 34 Estuarine/Omnivorous 41 Anadromous/Piscivorous 51 Fresh water immigrant/Planktivorous 52 Fresh water immigrant/Benthophagous (B) Caeté Estuary Code Variables 11 Marine straggler/Planktivorous 12 Marine straggler/Piscivorous 13 Marine straggler/Benthophagous 14 Marine straggler/Hyperbenthophagous 21 Marine immigrant/Planktivorous 22 Marine immigrant/Detritivorous 23 Marine immigrant/Herbivorous 24 Marine immigrant/Piscivorous 31 Estuarine/Planktivorous 32 Estuarine/Herbivorous 33 Estuarine/Benthophagous 41 Anadromous/Detritivorous 42 Anadromous/Piscivorous 51 Fresh water stragler/Herbivorous 52 Fresh water stragler/Benthophagous 53 Fresh water stragler/Hyperbenthophagous 54 Fresh water stragler/Lepidophagous 61 Fresh water immigrant/Planktivorous 62 Fresh water immigrant/Detritivorous 63 Fresh water immigrant/Hyperbenthophagous * P < 0.05; **P < 0.01

Axis 1 −0.73** 0.79** 0.34 * −0.50* −0.98** 0.25 −0.47* 0.73** 0.35* −0.17 −0.60* −0.96** −0.68* −0.90** 0.23 0.87** −0.60* 0.34*

Axis 2 −0.62** −0.16 0.05 −0.32* −0.10 0.88** 0.35* −0.27 0.50* −0.77** 0.73** 0.06 −0.72** 0.30* 0.03 −0.05 0.73** −0.07

Axis 1 0.53* 0.89** 0.96** 0.35* 0.78** 0.91** 0.91** 0.79** 0.67* −0.76** 0.72** 0.64* −0.12 −0.25 -0.05 -0.09 -0.09 −0.56* 0.573* −0.07

Axis 2 0.01 0.15 0.19 0.1 0.27 −0.21 −0.01 −0.05 0.27 0.26 −0.45* 0.09 0.21 −0.89** −1** −0.99** −0.99** 0.27 −0.69** −0.99**

670


Discussion The present study focused on comparisons of the taxonomy, ecological structure, and resource use of fish assemblages in distinct habitats of two tropical estuaries located in different zoogeographic realms. Both estuaries were subdivided according to their geomorphology and salinity gradients into upper, middle, and lower reaches. These divisions were reflected in the distribution of fish assemblages and their use of the estuaries. The main channel, the flood plain tidal channels, and mangrove tidal and intertidal creek habitats each had characteristic fish assemblages. Another important habitat was the seagrass beds, characteristic of the lower reaches of the Embley Estuary. Zoogeographical Analysis of the Taxonomic Composition in Both Estuaries.—No single species occurred in the data sets of both estuaries, although C. leucas, Aetobatus narinari, T. lepturus, and Chilomycterus spinosus are known to inhabit both regions (Blaber et al., 1989; Cyrus and Blaber, 1992; Barletta et al., 1998, 2003). The numbers of species and families are greater in the Embley Estuary (IndoWest Pacific) than in the Caeté Estuary. Similarly, other Indo-West Pacific estuaries, such as those of the Solomon Islands (Blaber and Milton, 1990) and Moreton Bay, Australia (Morton, 1990) have higher species diversity than the Caeté Estuary, Brazil (Barletta et al., 2000, 2003, 2005). This difference in species numbers between the Indo-West Pacific and Tropical West Atlantic owes its origins to evolutionary history and tectonics. In the Indo-West Pacific region there is a concentration of species in the triangle bordered by the Philippines, Malay Peninsula, and New Guinea (Briggs, 1995; Blaber, 1997, 2000). This area was considered by Briggs (1995) as the East Indies center of evolutionary radiation (Indo-Polynesian Province) of the Indo-West Pacific region. This center of high diversity originated in the Tethys Sea of the Cretaceous to early Miocene Ocean, which was situated between the northern and southern continents (Briggs, 1995). The Indo-West Pacific Region (and within it, the East Indies Triangle) represents an evolutionary and distributional center for much of the world’s tropical fauna and flora and there is a notable decrease in species diversity correlated with distance from this center of high diversity (East Indies Triangle). This is true for almost every tropical fish family for which the systematics are well known (Gobiesocidae, Lutjanidae, Singnathidae, Chaetodontidae, Ariidae, Clupeidae, Engraulidae, and Sciaenidae) (Allen, 1975; Burgess, 1978, 1989; Allen and Talbot, 1985; McDowall, 1988; Blum, 1989; Blaber, 2000; Marceniuk and Menezes, 2007). It is important to note, however, that many taxa reached the Atlantic region from the Indo-West Pacific. For example, Ricklefs and Latham (1993) and Briggs (1995) suggested, that the mangrove genus Rhizophora, a very important component of tropical estuarine ecosystems, probably originated in the East Indies, spread west to East Africa and thence east to the New World, reaching the Atlantic through the Central American archipelago. This genus probably reached the Eastern Atlantic from the western Atlantic, since the three West African mangrove species are identical to those of the Western Atlantic (Ricklefs and Latham, 1993). The Western Atlantic Region, which includes three main provinces (Caribbean, West Indian, and Brazilian), constitutes a secondary center of evolutionary radiation (Briggs, 1995). Many species that evolved in this area migrated eastwards to colonize the Tropical Eastern Atlantic.


671

A significant difference between the Indo-West Pacific and Tropical Western Atlantic estuarine fish faunas is the much higher diversity of freshwater species in tropical South America. Caeté Estuary, located in the Brazilian Province, is strongly influenced, especially in its upper reaches, by freshwater species (Characiforms, Siluriforms, Gymnotiforms, and Perciforms) characteristic of the Neotropic Zoogeographic Region. According to Nelson (1994) and Fink and Fink (1997), the Ostariophysan fish (Characiforms, Siluriforms, and Gymnotiforms) are a monophyletic primary freshwater group, which arose in the Upper Jurassic. The most primitive orders of this group are the Characiforms and Siluriforms. Representatives of these two orders were able to colonize Asian, African and South American waters before these continents were separated. Aside from two catfish families (Ariidae and Plotosidae) that became secondarily adapted to salt water, Ostariophysan fish have not been able to reach Madagascar, the West Indies, New Zealand, and Australia. This suggests that those land masses have not been connected to any of the larger continents since the upper Jurassic (Briggs, 1995). This also explains why, despite seemingly suitable habitats and hydrological conditions, there are no freshwater Ostariophysan fish species in the Embley Estuary. Ecological Functional Groups.—Certain functional guilds have a clear and demonstrated value for describing the use of different estuarine habitats by fish and for comparing the different estuarine use and feeding mode functional groups in the estuary. In particular, the ecological guilds proved useful for highlighting the predominance of estuarine species and marine juveniles, and the strong effects of salinity on assemblages in the different reaches of the two systems, particularly in the Caeté Estuary (Barletta-Bergan et al., 2002a,b; Barletta et al., 2003, 2005). Based on studies of the Orinoco Delta, Venezuela (Cervigón, 1985), in the Cayenne River Estuary, French Guiana (Morais and Morais, 1994) and in the coastal areas of Guyana (Lowe-McConnell, 1962) and Caeté Estuary, north Brazil (Barletta et al., 2003, 2005) it may be concluded that the fish species distribution and movement patterns induced by salinity gradients and seasonal fluctuations could be generalized for northern South America. Also the similarity of the fish assemblages and habitats among these estuaries suggests that estuarine use and feeding mode functional groups could be generalized for all estuaries in northern South America. Similarly, the Embley Estuary fish assemblages and ecological information (Blaber et al., 1989; Blaber, 1990, 1997, 2000; Cyrus and Blaber, 1992) indicate that the ecological characteristics of these guilds may be common to many estuaries of the Indo-West Pacific, and particularly for those of northern Australia. In estuaries such as the Embley, where salinities are relatively uniform in all reaches throughout the year, marine immigrants (piscivorous—main and tidal channel; benthophagous—main tidal channels, beaches, and intertidal mud flats; hyperbenthophagous—seagrass beds) and marine stragglers (piscivorous—main and tidal channels) were the dominant guilds. The semi-catadromous (piscivorous) functional group (L.. calcarifer) was also an important component of all habitats, except the seagrass beds of the lower reaches of Embley Estuary. Plots of functional groups of cluster and factorial analysis centroids for both estuaries show distinct patterns in the structure of the guilds in both estuaries. In the Caeté Estuary, the distribution of guilds reflected the salinity gradient in the estuary, principally for freshwater groups (straggler and immigrant guilds) and marine stragglers, whereas, in the Embley Estuary, the stability of the salinity even in the

672


upper reaches (Cyrus and Blaber, 1992) allowed the marine immigrant and marine straggler guilds to use most of the habitats. In this case, the dominant fish species which spend part of their life cycle in Embley habitats (principally the main channel and tidal channels)–anadromous/piscivorous, marine immigrant/piscivorous, benthophagous, and detritivorous, and marine straggler/piscivorous–and the dominant estuarine (planktivorous and benthophagous) fish species which spend their life in the seagrass beds and mangrove intertidal creeks explain the patterns of fish distribution in Embley Estuary. Main Conclusions and Recommendations The Neotropical fish species of the upper Caeté Estuary and the chondrichthyan fauna of the Embley underlie the most important taxonomic differences between these estuaries. On the other hand, the families Engraulidae, Sciaenidae, Ariidae, Carangidae, Haemulidae, and Clupeidae, which are characteristic of the main channel and mangrove tidal creeks of Caeté Estuary showed 70% similarity with the main channel of the Embley Estuary. Moreover, for the Embley Estuary, marine immigrants (mainly piscivorous and benthophagous) were the dominant functional guilds, whereas in Caeté Estuary the estuarine functional guilds (benthophagous) contributed to > 50% of the biomass in each habitat. The fish communities inhabiting estuaries have been studied worldwide and there have been several attempts to indicate common features of those communities. In addition to supporting their own resident fish community, estuaries are nursery grounds, migration corridors, and refuge areas for a variety of fish species at different life stages. Given the increase in available data, it is possible to begin determining similarities and differences among biogeographical areas and thus to examine the features of fish community structure of estuaries on a global basis. Acknowledgments The authors would like to thank CSIRO Marine Laboratories, Cleveland, Australia for the 2-mo stay during which this manuscript was prepared. The data from Caeté Estuary was undertaken within the framework of the “Mangrove Dynamics and Management (MADAM)”, supported by the Ministry for Education, Science, Research and Technology (BMBf) (Project number: 03F0154A)–Germany, and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq–Brazil).

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676


Appendix 1. List of families and species with their codes, ecological guilds (EG; 1, marine straggler; 2, marine immigrants; 3, estuarine species; 4, anadromous; 5, catadromous; 6, amphidromous; 7, freshwater stragglers; 8, freshwater immigrants), trophic guilds (TG; 1, planktivorous; 2, detritivorous; 3, herbivorous; 4, piscivorous; 5, benthophagous; 6, hyperbenthophagous; 7, opportunistic), and life stage (A, adult; J, juvenile) found in each estuary (E, Embley; C, Caeté) considered in this study. No. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41

Code CARCH CAMBL CCAUT CDUSS CLEUC NACUT RACUT SPHYR SLEWI SMOKA PRIST PPECT PPRIS RHINO RDJID DASYA PSEPH HUARN TLYMN RHINOP RADSP ELOPI EMACH MEGAL MCYPR MATLA OPHIC MPUNC ENGRA SANDH SCARP PATHE CEDEN ACLUP CLUPE ACHAC NEREB SALBE RAMAZ CHANI CCHAN

Taxonomic groups Carcharhinidae Carcharhinus amblyrhynchoides (Whitley, 1934) Carcharhinus cautus (Whitley, 1945) Carcharhinus dussumieri (Müller and Henle, 1839) Carcharhinus leucas (Müller and Henle, 1839) Negaprion acutidens (Rüppell,1837) Rhizoprionodon acutus (Rüppell, 1837) Sphyrnidae Sphyrna lewini (Griffith and Smith, 1834) Sphyrna mokarran (Rüppell, 1837) Pristidae Pristis pectinata Lathan, 1794 Pristis pristis (Linnaeus, 1758) Rhinobatidae Rhynchobatus australiae Whitley, 1939 Dasyatidae Pastinachus sephen (Forsskål, 1775) Himantura uarnak (Forsskål, 1775) Taeniura lymma (Forsskål, 1775) Rhinopteridae Rhinoptera cf. adspersa Müller and Henle, 1841 Elopidae Elops machnata (Forsskål, 1775) Megalopidae Megalops cyprinoides (Broussonet, 1782) Megalops atlanticus Valenciennes, 1847 Ophicthidae Myrophis punctatus Lütken, 1852 Engraulidae Stolephorus andhraensis Babu Rao, 1966 Stolephorus carpentariae (De Vis, 1882) Pterengraulis atherinoides (Linnaeus, 1766) Cetengraulis edentulus (Cuvier, 1829) Anchovia clupeoides (Swainson, 1839) Clupeidae Anodontostoma chacunda (Hamilton, 1822) Nematalosa erebi (Günter, 1868) Sardinella albella (Valenciennes, 1847) Rhinosardinia amazonica (Steindachner, 1879) Chanidae Chanos chanos (Forskäl, 1775)

EG

TG

Life Stage E A J

1 2 1 2 2 1

4 4 4 4 4 4

1 1 1 1 1 1

1 1 1 1 1 1

E E E E E E

1 1

4 4

0 0

1 1

E E

2 2

4 4

1 1

1 1

E E

1

5

0

1

E

2 2 2

5 5 5

1 1 1

1 1 1

E E E

1

5

1

0

E

2

4

1

1

E

2 2

4 4

1 0

1 1

E C

3

5

1

1

C

1 2 3 2 2

1 1 4 1 1

1 1 1 0 1

1 1 1 1 1

E E C C C

2 8 2 2

2 2 1 1

1 1 1 1

1 1 1 1

E E E C

2

2

1

1

E

677


Appendix 1. Continued. No. 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87

Code ASPRE AASPR AFILA PIMEL BVAIL AUCH PNODO ARIID AMAST APROX AMACR CSPIX CAGAS HPARK SHERT HPROO PLOTO ENUDI LORICA HPLEC STERN DCONI EVIRE GYMNO GCARA SYNOD SAUSP BATR BSURI MUGIL LSUBV VBUCH PSEUDM PGERT ATHER ADUOD ANDRA BELON TCROC TPUNC STIMO HEMI ASCLE ZBUFF ANABL AANAB

Taxonomic groups Aspredinidae Aspredo aspredo (Linnaeus, 1758) Aspredinichthys filamentosus (Valenciennes, 1840) Pimelodidae Brachyplatystoma vaillanti (Valenciennes, 1840) Auchnopteridae Pseudauchenipterus nodosus (Bloch, 1794) Ariidae Sciades mastersi Ogilby, 1898* Arius proximus (Ogilby, 1898) Arius macrocephalus (Bleeker, 1846) Cathorops spixii (Agassiz, 1829) Cathorops agassizii (Eigenmann and Eigenmann, 1888) Aspistor parkeri (Traill, 1832)** Sciades hertzbergii (Bloch, 1794) Sciades proops (Valenciennes, 1840)*** Plotosidae Euristhmus nudiceps (Günther, 1880) Loricariidae Hypostomus plecostomus (Linnaeus, 1758) Sternopygidae Distocyclus conirostris (Eigenmann and Allen, 1942) Eigenmania virescens (Valenciennes, 1836) Gymnotidae Gymnotus carapo Linnaeus, 1758 Synodontidae Saurida sp. 2 Batrachoididae Batrachoides surinamensis (Bloch and Schneider, 1801) Mugilidae Liza subviridis (Valenciennes, 1836) Valamugil buchanani (Bleeker, 1854) Pseudomugilidae Pseudomugil gertrudae Weber, 1911 Atherinidae Atherinomorus duodecimalis (Valenciennes, 1835) Atherinomorus endrachtensis (Quoy and Gaimard, 1825) Belonidae Tylosurus crocodilus (Péron and Lesueur, 1821) Tylosurus punctulatus (Günther, 1872) Strongylura timucu (Walbaum, 1792) Hemiramphidae Arrhamphus sclerolepis Günther, 1866 Zenarchopterus buffonis (Valenciennes, 1847) Anablepidae Anableps anableps (Linnaeus, 1758)

EG

TG

Life Stage E A J

3 3

5 5

1 1

1 1

C C

8

6

1

1

C

8

2

1

1

C

2 2 2 3 3 1 3 2

5 5 5 5 5 5 5 5

1 1 1 1 1 0 1 0

1 0 1 1 1 1 1 1

E E E C C C C C

2

5

1

1

E

7

3

0

1

C

7 7

5 5

1 1

0 1

C C

7

5

1

1

C

1

4

1

0

E

3

6

1

1

C

2 2

2 2

1 1

1 1

E E

8

1

1

1

E

2 2

1 1

1 1

1 1

E E

2 2 2

4 4 4

1 1 1

1 1 1

E E C

2 3

3 1

1 1

1 1

E E

3

5

1

1

C

678


Appendix 1. Continued. No. 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131

Code POECI POECSP GAMSP SYNGN HHEPT HKUDA HWHIT HSP PLATY CNEMA PENDR PINDI CENTR LCALC AMBAS ADUSS ANALU SERRA EMALA ECOIO EITAJ CENTRG CVAIG APOGO AHYAL ARUPP ASANG SROSE SILLA SANAL SINGE SMACUL SSIHA SLUTE LACT LLACT RACHI RCANA CARAN SCOMM CCRYS SVOME CLATU GSPEC

Taxonomic groups Poeciliidae Poecilia sp. Gambusia sp. Syngnathidae Hippichthys heptagonus Bleeker, 1849 Hippocampus kuda Bleeker, 1852 Hippocampus borboniensis Duméril, 1870 Hippocampus sp. Platycephalidae Cymbacephalus nematophthalmus (Günther, 1860) Platycephalus endrachtensis Quoy and Gaimard, 1825 Platycephalus indicus (Linaeus, 1758) Centropomidae Lates calcarifer (Bloch, 1790) Ambassidae Ambassis dussumieri (Cuvier, 1828) Ambassis nalua (Hamilton, 1822) Serranidae Epinephelus malabaricus (Bloch and Schneider, 1801) Epinephelus coioides (Hamilton, 1822) Epinephelus itajara (Lichtenstein, 1822) Centrogeniidae Centrogenys vaigiensis (Quoy and Gaimard, 1824) Apogonidae Apogon hyalosoma Bleeker, 1852 Apogon rueppellii Günther, 1859 Apogon sangiensis Bleeker, 1857 Siphamia roseigaster (Ramsay and Ogilby, 1887) Sillaginidae Sillago analis Whitley, 1943 Sillago ingenuua McKay, 1985 Sillago maculata Quoy and Gaimard, 1824 Sillago sihama (Forsskål, 1775) Sillago lutea McKay, 1985 Lactariidae Lactarius lactarius (Bloch and Scheneider, 1801) Rachicentridae Rachycentron canadum (Linnaeus, 1766) Carangidae Scomberoides commersonnianus (Lacépède, 1801) Caranx crysos (Mitchill, 1815) Selene vomer (Linnaeus, 1758) Caranx latus Agassiz, 1831 Gnathanodon speciosus (Forsskål, 1775)

EG

TG

Life Stage E A J

8 8

1 1

1 1

1 1

C C

2 2 2 2

1 1 1 1

1 1 1 1

1 1 1 1

E E E E

2 2 2

4 4 4

1 1 1

0 1 1

E E E

4

4

1

1

E

2 2

1 1

1 1

1 1

E E

2 2 2

4 4 5

1 1 0

0 1 1

E E C

2

5

1

1

E

3 2 2 3

1 1 1 1

1 1 1 1

1 0 0 1

E E E E

2 2 2 2 2

5 5 5 5 5

1 1 0 0 0

1 1 1 1 1

E E E E E

2

4

1

0

E

1

4

1

0

E

2 2 2 2 2

4 6 6 6 6

1 0 0 0 0

1 1 1 1 1

E C C C E

679


Appendix 1. Continued. No. 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168 169 170 171 172 173 174 175 176 177 178 179

Code LEIOG LDECO LEQUU SRUCO LUTJA LRUSS LJOCU GERRE GEURY GFILA GLONG HAEMU PARGE PKAAN GLUTE CNOBI SPARI ABERD LETHR LLENT POLYN ETETRA PMACR PVIRG SCIAE SRAST SMICR CACOU PSQUA SNASO MULLI UTRAG MONOD MARGE TOXOT TCHAT DREPA DPUNC CHAET CMUELL PECEL TERAP ACAUD PQUAD TJARB TPUTA BLENN OROTU

Taxonomic groups Leiognathidae Leiognathus decorus (De Vis, 1884) Leiognathus equulus (Forsskål, 1775) Secutor ruconius (Hamiltton, 1822) Lutjanidae Lutjanus russellii (Bleeker, 1849) Lutjanus jocu (Bloch and Schneider, 1801) Gerreidae Gerres erythrourus (Bloch, 1791) Gerres filamentosus Cuvier, 1829 Gerres longirostris (Lacépède, 1801) Haemulidae Pomadasys argenteus (Forsskål, 1775) Pomadasys kaakan (Cuvier, 1830) Genyatremus luteus (Bloch, 1790) Conodon nobilis (Linnaeus, 1758) Sparidae Acanthopagrus berda (Forsskål, 1775) Lethrinidae Lethrinus lentjan (Lacépède, 1802) Polynemidae Eleutheronema tetradactylum (Shaw, 1804) Polydactylus macrochir (Günther, 1867) Polydactylus virginicus (Linnaeus, 1758) Sciaenidae Stellifer rastrifer (Jordan, 1889) Stellifer microps (Steindachner, 1864) Cynoscion acoupa (Lacépède, 1801) Plagioscion squamosissimus (Heckel, 1840) Stellifer naso (Jordan, 1889) Mullidae Upeneus tragula Richardson, 1846 Monodactylidae Monodactylus argenteus (Linnaus, 1758) Toxotidae Toxotes chatareus (Hamilton, 1822) Drepaneidae Drepane punctata (Linnaeus, 1758) Chaetodontidae Chelmon muelleri Klunzinger, 1879 Parachaetodon ocellatus (Cuvier, 1831) Teraponidae Amniataba caudavittata (Richardson, 1845) Pelates quadrilineatus (Bloch, 1790) Terapon jarbua (Forsskål, 1775) Terapon puta Cuvier, 1829 Blenniidae Omobranchus rotundiceps (Macleay, 1881)

EG

TG

Life Stage E A J

2 2 1

1 1 1

0 0 0

1 1 1

E E E

2 2

6 6

0 0

1 1

E C

2 2 2

5 5 5

0 0 0

1 1 1

E E E

2 2 3 2

5 5 5 5

0 0 1 1

1 1 1 1

E E C C

2

5

1

1

E

2

6

0

1

E

2 2 2

4 6 6

1 1 1

1 1 0

E E C

2 3 2 7 3

6 6 6 6 6

1 1 0 1 1

1 1 1 1 1

C C C C C

2

5

0

1

E

3

1

1

1

E

3

7

1

1

E

2

6

0

1

E

1 1

6 6

0 0

1 1

E E

2 2 2 1

6 6 8 6

1 0 0 0

1 1 1 1

E E E E

2

5

1

0

E

680


Appendix 1. Continued. No. 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218

Code CALLI CSP ELEO GGUAV GOBII ELYRI GOCEA CSMAR CSTIG EPHIP ZNOVE CFABE SCATO SARGUS SMULT SIGN SCANA SPHYR SPUTN TRICH TLEPT SCOMB SMACU PARAL PELEV ACHIR ADUME ALINEA TRIAC TWEBER MONAC ATOMEN MCHINE PJAPO TETRA AIMMA CPATO TERYTH CPSIT

Taxonomic groups Callionymidae Callionymus sp. Eleotridae Guavina guavina (Valenciennes, 1837) Gobiidae Evorthodus lyricus (Girard, 1858) Gobionellus oceanicus (Pallas,1770) Ctenogobius smaragdus (Valenciennes, 1837) Ctenogobius stigmaticus (Poey, 1860) Ephippidae Zabidius novemaculeatus (McCulloch, 1916) Chaetodipterus faber (Broussonet, 1782) Scatophagidae Scatophagus argus (Linaeus, 1766) Selenotoca multifasciata (Richardson, 1846) Siganidae Siganus canaliculatus (Park, 1797) Sphyraenidae Sphyraena putnamae Jordan and Seale, 1905 Trichiuridae Trichiurus lepturus Linnaeus, 1758 Scombridae Scomberomorus maculatus (Mitchill, 1815) Paralichthyidae Pseudorhombus elevatus Ogilby, 1912 Achiridae Apionichthys dumerili Kaup, 1858 Achirus lineatus (Linnaeus, 1758) Triacanthidae Trixiphichthys weberi (Chaudhuri, 1910) Monacanthidae Acreichthys tomentosus (Linnaeus, 1758) Monacanthus chinensis (Osbeck, 1765) Paramonacanthus japonicus (Tilesius, 1809) Tetraodontidae Arothron immaculatus (Bloch and Schneider, 1801) Chelonodon patoca (Hamilton, 1822) Tetraodon erythrotaenia Bleeker, 1853 Colomesus psittacus (Bloch and Schneider, 1801)

* Originally cited in Appendix as Arius mastersi (non-valid). ** Originally cited in Appendix as Hexanematichthys parkeri (non-valid). *** Originally cited in Appendix as Hexanematichthys proops (non-valid).

EG

TG

Life Stage E A J

1

5

0

1

E

3

5

1

1

C

3 3 3 3

5 6 5 5

1 1 1 1

1 1 1 1

C C C C

1 1

3 3

1 0

0 1

E C

2 2

3 3

1 1

1 1

E E

2

3

0

1

E

2

4

0

1

E

1

4

0

1

C

1

4

0

1

C

2

5

0

1

E

3 3

5 5

1 1

1 1

C C

2

6

0

1

E

2 2 1

6 3 6

0 0 0

1 1 1

E E E

2 2 3 3

5 5 5 5

1 0 1 1

1 1 1 1

E E E C