Accepted Manuscript

Environmental control on larval stages of fish subject to specific

salinity range in tropical estuaries

Régis Vinı́cius Souza Santos, Sandra Ramos, Ana Cristina Teixeira

Bonecker

PII: S2352-4855(16)30297-3
DOI: http://dx.doi.org/10.1016/j.rsma.2017.03.010
Reference: RSMA 238

To appear in: Regional Studies in Marine Science

Received date: 23 January 2017

Revised date: 29 March 2017
Accepted date: 30 March 2017

Please cite this article as: Santos, R.V.S., Ramos, S., Bonecker, A.C.T., Environmental control
on larval stages of fish subject to specific salinity range in tropical estuaries. Regional Studies
in Marine Science (2017), http://dx.doi.org/10.1016/j.rsma.2017.03.010

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 Environmental control on larval stages of fish subject to specific salinity range in tropical
estuaries

Régis Vinícius Souza Santosa*, Sandra Ramosb,c, Ana Cristina Teixeira Boneckera
a
Universidade Federal do Rio de Janeiro, Instituto de Biologia, Departamento de Zoologia, Laboratório Integrado de
Zooplâncton e Ictioplâncton, Av. Carlos Chagas Filho, 373, 21.941-902, Rio de Janeiro, RJ, Brazil.
b
CIIMAR - Interdisciplinary Centre of Marine and Environmental Research, ECOBIOTEC, Avenida General Norton
de Matos, S/N, 4450-208 Matosinhos, Portugal
c
Institute of Estuarine and Coastal Studies, University of Hull, Hull HU6 7RX, UK

* corresponding author: regisvinicius@gmail.com

Abstract

In this study, we used a comparative cross-system analysis and a standardized methodological

approach to understand which abiotic parameters, in addition to salinity, can play an important role
in determining larval fish assemblages in tropical estuaries. Surveys were performed by using
surface trawls in the same water mass (salinity ranging from 15 to 25) in four Brazilian estuaries
(Macaé, São João, Bracuí and Perequê-Açu) from May 2013 to March 2015. Water temperature,
oxygen saturation, pH, chlorophyll-a, nitrate, nitrite, ammonia, phosphate and total particulate
matter were obtained at each sampling area. Comparative analysis of structural attributes of larval
fish assemblages, showed inter-estuarine differences in terms of total abundance and diversity.
Perequê-Açu Estuary registered the highest abundance levels and was highly dominated by a typical
anadromous species Anchoviella lepidentostole. Macaé Estuary presented the most diverse larval
fish assemblage, which was comprised by several marine species. Temperature and precipitation, in
addition to salinity, were the main environmental variables regulating the larval fish assemblages.
Temperature has played an important role in determining anadromous species abundance, since the
greatest abundances were associated with high water temperatures recorded mainly in Perequê-Açu
Estuary. Precipitation was responsible for episodic events of runoff in Bracuí, São João and
Perequê-Açu estuaries, where the high precipitation collaborated to carry anadromous larvae from
the spawning habitat to the estuarine zone. Conversely, the low precipitation in Macaé Estuary
favored the immigration of marine species due to the decrease of the river flow. Oxygen saturation
and nutrient load could have operated in an indirect way, through their effect on food supply, but
further studies are necessary to investigate this question. Our study highlighted that fish larvae are
highly sensitive to environmental variations and emphasized that conservation of estuarine habitats
is essential to ensure success in the fish recruitment.

1
Keywords: fish larvae; environmental forcing; cross-system analysis; estuaries; Brazil.

1 Introduction

Estuaries are among the most productive ecosystems of the world, supporting fundamental
ecological links between the sea and rivers (McLusky and Elliott, 2004; Able, 2005). As transition
areas, estuaries are naturally sheltered zones with favourable characteristics to many species, such
as shallow water refugia, rich food resources and a diversity of habitats (Beck et al., 2001;
Whitfield and Elliott, 2002). Fish are an important component of the estuarine fauna as they may
utilize these habitats for the entire life cycle (estuarine species), for a particular period of their life
cycle (marine migrants, anadromous and catadromous fishes) or only use them occasionally (marine
stragglers, freshwater and amphidromous) (Elliott et al., 2007).

The composition and distribution patterns of fish larvae within estuarine ecosystems has been
studied for temperate (e.g. Neira et al., 1992; Witting et al., 1999; Ramos et al., 2006a; Costa et al.,
2014; Munk et al., 2014; Ribeiro et al., 2015; Costa and Muelbert, 2017) and tropical habitats (e.g.
Morais and Morais, 1994; Harris et al., 2001; Barlleta-Bergan et al., 2002; Bonecker et al., 2009;
Ooi and Chong, 2011; McKinnon et al., 2015; Rezagholinejad et al., 2016; Correa-Herrera et al.,
2017). However, estuarine research on fish larvae comparing two or more estuaries subject to the
same sampling methods, effort and climatic regions, is still limited internationally (e.g. Whitfield,
1994; Harris and Cyrus, 2000; Montoya-Maya and Strydom, 2009; Ramos et al., 2012, 2015;
Pattrick and Strydom, 2014; Strydom, 2015). A cross-system comparative analysis involves using
similar data from many different systems to develop a model, which explains the observed patterns
across a range of time and space scales (Kemp and Boynton, 2012). At estuarine ecosystem levels,
these studies provide essential information about early-stage fish dynamics and estuarine use
pattern, contributing to assess the suitability of the estuaries in relation to an ecological function
(i.e. nursery function).

Estuarine larval fish assemblages change frequently in time and space, according to reproductive
periods of the species and due to the environmental variability (Whitfield, 1994; Harris and Cyrus,
1995; Barletta-Bergan et al., 2002; Ramos et al., 2006a; Bonecker et al., 2007). Many
environmental variables are assumed to be responsible for the distribution of larval fish populations
(e.g. Tzeng and Wang, 1993; Ramos et al., 2006b; Gonçalves et al., 2015). However, salinity and

2
water temperature have shown to be the most important parameters affecting the distribution and
abundance of fish larvae (e.g. Strydom et al., 2003; Ramos et al., 2006b; Bonecker et al., 2007;
Amorim et al., 2016; Spies and Steele, 2016). Due to the relative stability in temperature patterns in
tropical estuaries throughout the year (Araújo et al., 1998; Araújo et al., 2002), salinity plays the
major role in modeling larval fish assemblage structure in this region (e.g. Barletta-Bergan et al.,
2002; Bonecker et al., 2009; Ooi and Chong, 2011).

Although with less impact, other parameters may also influence larval fish dynamics in tropical
estuaries. However, their effects can be masked by major drivers like salinity. In some temperate
estuarine ecosystems, peaks in larval fish abundance appears to be correlated with low precipitation,
which increase the river flow and can flush fish larvae out of the estuarine habitat (Ramos et al.,
2006b; Gonçalves et al., 2015). Water turbidity may increase the mortality by interacting with other
biological processes that can affect the rates at which larval fish capture their prey, and by
increasing the visibility of predators (Fortier et al., 1996; Gallego et al., 1996; Dower et al., 1997;
Utne-Palm and Stiansen, 2002). Furthermore, it has been shown that nutrient load also have an
important influence on the dynamics of larval fish assemblages (Ramos et al., 2012), including the
consequent increase of food availability through productivity primary and secondary (Martin et al.,
1992; Garcia et al., 2003; Meynecke et al., 2006; Hsieh et al., 2010).

Given the demonstrated effects that the environmental variables may have upon ichthyoplankton,
understanding the relationships between distribution patterns of these life stages and physico-
chemical features of the estuary is extremely relevant for estuarine conservation (Costa et al., 2015).
In this sense, the present study provides new foci for future studies on processes affecting the fish
larvae in tropical estuaries. Here, we use a sampling standardization of salinity range in order to
understand which abiotic parameters, in addition to salinity, can play important roles in determining
larval fish assemblages in tropical estuaries. For this, we performed a comparative cross-system
analysis of estuarine fish larvae based on structural and functional attributes in four Brazilian
estuaries. The purpose of this study is to provide valuable information about early-stage fish
dynamics and estuarine use pattern, contributing to the study of population dynamics, management
of fish stocks, definition of nursery habitats and the design of protected areas.

2 Material and Methods

2.1 Study area
The study focused on four permanently open estuaries along the coast of the Rio de Janeiro State
(South-eastern Brazil): Macaé (22° 22’ S and 41° 46’ W), São João (22° 35’ S and 41° 59’ W),
3
Bracuí (22° 57’ S and 44° 23’ W) and Perequê-Açu (23° 13’ S and 44° 42’ W) (Fig. 1). Macaé and
São João are large estuarine systems with 130 km and 120 km long and total area of 1,765 km² and
2,160 km², respectively. Bracuí and Perequê-Açu are smaller systems (32 km covering a total area
of 190 km² and 22 km with an area of 110 km², respectively). The four estuaries are shallow (mean
depth ranging from 2 to 4 meters), microtidal and partially mixed, with semidiurnal tidal regime.
Climate is classified as tropical semi-humid, where rainfall dominates summer months (December-
March). The average annual temperature is 18° C to 30° C and rainfall ranges between 1,000 mm to
1,500 mm annually (INMET, 2015).

2.2 Sampling and sample processing

Sampling surveys were conducted every two months between May 2013 and March 2015. All
samples were taken from the same water mass (salinity ranging from 15 to 25) during nightly ebb
tides. Triplicates of surface trawls were performed in each estuary using a Bongo net (60-cm
diameter, 500 µm mesh size, 1-2 knot ship speed). A flowmeter (General Oceanics®) was attached
to the net in order to determine the volume of the water filtered. At each sampling site, subsurface
(0.5 to 1m depth) water temperature (°C) and pH were measured using a multiparameter probe
(Hach HQ40d) and water samples were collected for further analyses (chlorophyll-a, inorganic
nutrients, total particulate matter and oxygen saturation).

2.3 Analytical procedures

Chlorophyll-a and inorganic nutrients (ammonia, nitrite, nitrate and phosphate) were determined
following previously described methods (Grasshoff et al., 1999). Chlorophyll-a samples were
collected using positive pressure filtration of 2 L of water. When chlorophyll (or other particle)
concentration in the water sample was high, the filtration volume was reduced to prevent filter
clogging. The filters (cellulose HAWP, Millipore, Darmstadt, Germany) were extracted overnight
in a solution of 90% acetone at 4°C, and analyzed by spectrophotometry or fluorimetry. For the
inorganic nutrient analyses, 500 mL of water was frozen and analyzed in laboratory using the
following methods: ammonia by indophenol; nitrite by diazotization; nitrate by reduction in a Cd—
Cu column followed by diazotization; and phosphate by reaction with ascorbic acid. Oxygen
saturation was calculated as the percentage of dissolved oxygen concentration relative to the
temperature and salinity of the water, and the dissolved oxygen concentration was determined by
the Winkler method (Grasshoff et al., 1999). Total particulate matter (TPM) was determined
following APHA (2005) method. Monthly precipitation data was obtained from the National
Agency of Water (ANA, 2016). Fish larvae were sorted from 144 ichthyoplankton samples and

4
identified to the highest possible taxonomic separation (e.g. Richards, 2005; Fahay, 2007).
Abundance data were standardized into number of larvae per 100 m³ of filtered water.

2.4 Data analysis

Months were aggregated into two season groups: dry comprising May, July, September and
November; and rainy comprising January and March. Species were assigned to an ecological guild
derived from their estuarine use patterns, according to Elliott et al. (2007): amphidromous species
(AM), anadromous species (AN), catadromous species (C), estuarine species (ES), freshwater
species (F), marine migrants (MM; spawn at sea and regularly enter estuaries in large numbers,
including marine species using estuaries as nursery grounds) and marine stragglers (MS; spawn at
sea and enter estuaries accidentally in low numbers). The most representative species (abundance >
10 larvae 100 m-³ and frequency of occurrence > 10%) were selected as the top taxa for detailed
spatiotemporal analysis.

According to the taxonomic sufficiency approach for ichthyoplankton data (Herdandez Jr et al.,
2013), genus- and species-level data may be informative as a first order assessment of
ichthyoplankton assemblage structure related to seasonality or other environmental parameters.
Considering this, we used the genus-level (at minimum) to examine ichthyoplankton assemblages in
multivariate analysis. Diversity of the larval fish assemblage was expressed using the Shannon-
Wiener index (H’) (Shannon and Weaver, 1963) and equitability was measured by Pielou’s
evenness index (J’) (Pielou, 1966). Two-way analysis of similarity (ANOSIM) (Clarke and
Warwick, 1994) was used to test the difference of inter-estuarine and seasonal trends in the
assemblages, at a significance level of P < 0.05 and R statistic > 0.5. The tests were based on a
Bray-Curtis rank similarity matrix, calculated using square root transformed data. Similarity
percentages (SIMPER) (Clarke, 1993) were used to identify the percentage contribution of each
taxon to the average dissimilarity between samples of the various pair combinations. Multivariate
analyses were performed with the software package PRIMER (Plymouth Routines Multivariate
Ecological Research) (Clarke and Warwick, 1994).

Analysis of variance (ANOVA) type II was used to test for differences in water parameters
(temperature, pH, oxygen saturation, TPM, chlorophyll-a, ammonia, nitrite, nitrate and phosphate)
between season and estuaries (Sokal and Rohlf, 1995; Zar, 1996). We also used ANOVA type II in
order to ascertain the differences in the larval fish assemblages descriptors (abundance, diversity
and the Pielou’s evenness), abundances of each ecological guild and top four species between
seasons and estuaries (Sokal and Rohlf, 1995; Zar, 1996).
5
Water parameters (except pH) were log transformed [ln(x)], as were the raw abundance, diversity
and Pielou’s evenness data [log 10(x+1)] to achieve normality requirements of residuals and
homogeneity of variance, fulfilling one of the ANOVA assumptions. Homogeneity of variance was
tested with a Cochran test, and whenever variance was still heterogeneous, conclusions from
ANOVA results were only accepted for those cases where significance levels were less than 0.01.
Furthermore, in the event of significance, an a post-hoc Tukey HSD was used to determine which
means were significantly different at a 0.05 level of significance.

To evaluate the influence of environmental variables on the larval fish assemblages, we conducted a
canonical correspondence analysis (CCA) (Ter Braak, 1986) using CANOCO software (version 4.5,
Microcomputer Power, Ithaca, NY). The monthly precipitation, water temperature, oxygen
saturation, pH, TPM, chlorophyll-a, nitrate, nitrite, ammonia and phosphate were standardized and
used as explanatory environmental variables. Only the most representative species were considered
in this analysis to minimize the influence of rare species on results. Larval abundances were square
root transformed to normalize the data. The statistical significance of the correlations between
explanatory and species variables extracted from the CCA was determined by the Monte–Carlo test,
based on 499 permutations. Environmental variables were considered to be biologically important
when inter-set correlation coefficients were |≥0.4| (Rakocinski et al., 1996).

3 Results
3.1 Environmental characteristics
The minimum mean precipitation was observed in Macaé and São João estuaries (107.4 mm and
138.6 mm, respectively), while the highest precipitation values were recorded in Bracuí and
Perequê-Açu (mean of 153.2 mm and 149.1 mm, respectively) (Fig. 2a). The water temperature
reached significantly higher values in Perequê-Açu Estuary (F= 6.30, P < 0.001), and the warmest
period was the rainy (F = 114.7, P < 0.001) (Fig. 2b). Oxygen saturation was found in lower
percentages in Macaé Estuary (F = 8.62, P < 0.001) during dry surveys (F = 9.64, P < 0.01) (Fig.
2c). The pH values did not differ among estuaries (F = 0.80, P > 0.05), but during the rainy season
were observed the lowest values (F = 17.0, P < 0.001) (Fig. 2d). Chlorophyll-a was found in higher
concentrations in Macaé Estuary (F = 10.20, P < 0.001) during the rainy season (F = 5.90, P < 0.01)
(Fig. 2e). TPM, nitrite and ammonia also were recorded in higher concentrations in Macaé Estuary
(F = 25.24, P < 0.001; F = 26.72, P < 0.001; F = 44.68, P < 0.001, respectively), but their values did
not differ between seasons (F = 1.91, P > 0.05; F < 0.01, P > 0.05; F = 1.08, P > 0.05, respectively)
(Figs. 2f, 3a and 3b). Nitrate and phosphate concentrations were significantly higher (F = 26.84, P <
6
0.001; F = 56.17, P < 0.001, respectively) in Macaé and Perequê-Açu estuaries than in São João and
Bracuí estuaries (Figs. 3c and 3d), but while nitrate did not vary between seasons (F = 1.55, P >
0.05), phosphate was higher during the dry season (F = 9.12, P < 0.01).

3.2 Species composition

From the 56 taxa of teleost identified, 23 were considered as marine migrant species, 15 as marine
stragglers, 10 as estuarine species, 4 as anadromous, 2 as freshwater species, 1 as amphidromous
and 1 as catadromous (Table 1). The total number of ecological guilds ranged between 4 in São
João and Perequê-Açu and 6 in Macaé (Table 2). Anadromous, estuarine and marine migrant
species were the most abundant guilds and comprised more than 90 % of the total fish larvae caught
in each estuary (Fig. 4). Anadromous species were the most abundant species in Perequê-Açu
(94.6%), Bracuí (68.2%) and São João (56.9%) estuaries, and only represented 34.1% of the total
catch in Macaé. Marine migrants were the most abundant in Macaé reaching 48.8% of the total
catch, but did not overreached 15% in the others estuaries (1.9% Perequê-Açu, 12% São João,
13.5% Bracuí). Estuarine species contributed 28.1% to the total catch in São João, 12.5% in Macaé,
15.4% in Bracuí and 3.4% in Perequê-Açu estuaries.

Engraulidae was the most abundant family in São João, Bracuí and Perequê-Açu, corresponding to
56.5%, 68.2% and 94.5% of the total catch in each estuary, respectively (Table 1). In contrast,
Sciaenidae was the most abundant family in Macaé contributing 40% to the catch. At the species
level, Anchoviella lepidentostole was the top species (94.5%) in Perequê-Açu and Micropogonias
furnieri (30.4%) in Macaé Estuary. Bracuí and São João estuaries were characterized by
Anchoviella spp. as the most abundant taxon (53.1% and 47.6%, respectively).

3.3 Inter-estuarine and seasonal trends

During the study period, mean abundance reached 1,125 larvae 100 m-3 in Perequê-Açu, 89 larvae
100 m-3 in Macaé, 65 larvae 100 m-3 in São João and 58 larvae 100 m-3 in Bracuí (Table 2). The
larval fish abundance varied significantly among estuaries and seasons (F = 4.43, P < 0.01). The
highest abundance values were found in Perequê-Açu Estuary during the rainy season (Fig. 4).

The Shannon-Wiener diversity index and Pielou’s evenness also differed significantly among
estuaries (F = 40.65, P < 0.001; F = 24.01, P < 0.001; respectively), but not between dry and rainy
seasons (P > 0.01) (Fig. 4). In average, Macaé larval fish assemblages were more diverse (H’ = 1.65
± 0.30), in contrast with Perequê-Açu where the lower values of diversity were registered (H’ =

7
0.67± 0.40). The Pielou’s evenness were lower in Perequê-Açu (mean of 0.39 ± 0.27), where the
larval fish assemblage was highly dominated by a single species (A. lepidentostole, Table 1).

According to ANOSIM results, the larval fish assemblages were barely distinguishable seasonally
(R = 0.18, P = 0.001), but varied among estuaries (R = 0.54, P = 0.001). The Perequê-Açu
assemblage significantly differed from the other estuarine assemblages (0.55 ≤ R ≤ 0.87, P = 0.001).
According to SIMPER results, this was due to abundance differences of A. lepidentostole (Table 3).
Bracuí and Macaé estuarine assemblages also differed significantly (R = 0.62, P < 0.001), and
Anchoviella spp. and M. furnieri were identified as responsible for 22.7% of dissimilarities (Table
3).

Regarding the ecological guilds, anadromous species were significantly more abundant in Perequê-
Açu than in other estuaries (F = 21.61, P < 0.001). A significant seasonal difference was observed
(F = 11.14, P < 0.01), with anadromous reaching maximum abundances during the rainy season.
Estuarine species also differed significantly among estuaries (F = 4.80, P < 0.01), but not between
seasons (F = 0.48, P ≥ 0.49), with highest abundances found in Perequê-Açu in comparison with
Macaé and Bracuí estuaries. Marine migrants were significantly more abundant in Macaé (F =
12.28, P < 0.001) and no seasonal trend was observed (F = 0.69, P ≥ 0.41). No significant
differences were observed in amphidromous (F = 0.98, P ≥ 0.40), freshwater (F = 1.00, P ≥ 0.39),
catadromous (F = 0.97, P ≥ 0.41) and marine straggler species (F = 1.57, P ≥ 0.20).

3.4 Inter-estuarine and seasonal trends in the abundances of the top taxa
Anchoviella lepidentostole, Anchoviella spp., Microgobius meeki and M. furnieri were the top four
taxa and their inter-estuarine and seasonal trends were investigated further. Anchoviella
lepidentostole was significantly more abundant (F = 84.14, P < 0.001) in Perequê-Açu than in other
estuaries, with the highest abundance values occurring during the rainy season (F = 10.52, P < 0.01)
(Fig. 5). Anchoviella spp. showed significant inter-estuarine differences (F = 23.65, P < 0.001) since
no specimen was collected in Perequê-Açu during this study (Fig. 5) and abundance was
significantly lower during the dry season (F = 5.90, P < 0.05), mainly in São João Estuary.
Microgobius meeki was significantly more abundant in Perequê-Açu (F = 16.33, P < 0.001), with a
peak of abundance observed during the dry months, despite the lack of significant differences
between seasons (F = 1.07, P ≥ 0.30) (Fig. 5). Significantly greater abundances of M. furnieri were
observed in Macaé during the dry season (F = 7.42, P < 0.001) (Fig. 5).

8
3.5 Relationship between the top taxa and environmental variables

During the dry season (Fig. 6a), the first CCA axis (CCA1) was negatively correlated with
temperature and chlorophyll-a (Table 4). The second CCA axis (CCA2) was negatively correlated
with TPM and nitrate (Table 4). Perequê-Açu samples were isolated on the left side of CCA1
associated with high water temperature and chlorophyll-a (Fig. 6a). Bracuí, São João and Macaé
samples were negatively correlated with temperature and chlorophyll-a (clustering on the right side
of CCA1) and were mainly discriminated by CCA2, with Macaé samples positively correlated with
TPM and nitrate such as Perequê-Açu samples (Fig. 6a).

CCA analysis of the rainy season (Fig. 6b) showed that the first CCA axis (CCA1) was negatively
correlated with temperature, oxygen saturation and nitrate, while the second CCA axis (CCA2) was
positively correlated with ammonia and phosphate (Table 4). Perequê-Açu samples were isolated on
the left side of CCA1 associated with high water temperature, oxygen saturation and nitrate (Fig.
6b). Bracuí, São João and Macaé samples were negatively correlated with temperature, oxygen
saturation and nitrate (clustering on the right side of CCA1) and were mainly discriminated by
CCA2, with Macaé samples positively correlated with ammonia and phosphate (Fig. 6b).

Overall, species such as A. lepidentostole was associated with warmer water and high nitrate
concentration, observed in Perequê-Açu Estuary (Fig. 6). Micropogonias furnieri was negatively
correlated with water temperature and showed preference for habitats with high nutrient load and
TPM, such as Macaé Estuary (Fig. 6). Anchoviella spp. and M. meeki was negatively correlated
with nitrate and TPM, which were the water conditions observed in São João and Bracuí estuaries
(Fig. 6). However, while M. meeki was associated with warmer water during dry season,
Anchoviella spp. was negatively correlated with water temperature during both seasons (Fig. 6).

4 Discussion
Distinct variation in larval fish assemblage was evident across the different estuaries sampled,
however, a select suite of species dominated catches. These were mainly larvae derived from
estuarine residents or migrant species, especially A. lepidentostole, Anchoviella spp., M. meeki and
M. furnieri. Composition variability was driven by different combinations of the environmental
variables, giving rise to intra- and inter-estuary differences. In Perequê-Açu Estuary, the water
temperature, precipitation, chlorophyll-a, oxygen saturation and nitrate levels were the main
environmental variables that regulated its distinct community composition. In this estuary, the larval
fish assemblage was highly dominated by a single species A. lepidentostole. It is an anadromous

9
species with wider distribution (Western Central and South Atlantic) that migrates to the interior of
the rivers for spawning (Whitehead et al., 1988). Previous studies verified that its entrance in the
river for reproduction depends on climatic factors, especially temperature (Giamas et al., 1983;
Paiva-Filho et al., 1986; Souza et al., 1988; Ribeiro et al., 2014). In fact, the temperature is a
determinant factor at several stages of a fish life cycle, including gonadal development and
spawning (Pawson et al., 2000; Fincham et al., 2013; Amorim et al., 2016) and survival and growth
of early life stages prior to nursery recruitment (Meekan et al., 2003; Vinagre et al., 2009). During
our study, water temperature reached the highest values in Perequê-Açu Estuary. We hypothesize
that this warmer water could have been a result of the Tropical Water mass (TW) intrusion. The TW
flows southwards near the shelf break in the upper 200 m depth layer with temperature higher than
20°C (Castro Filho and Miranda, 1998), and is apparently predominant in this coastal region of the
Rio de Janeiro State (Lopes et al., 2006). Considering this, our results suggest that the warmer water
in Perequê-Açu Estuary is thought to be one of the determinants of high A. lepidentostole
abundance, by affecting the spawning stock and the reproductive success. As a limiting factor for
reproductive success, the water temperature becomes a particularly important feature at the
geographic limit of the A. lepidentostole distribution, with regard to climate change.

Besides the water temperature, the food supply is believed to be one of the primary environmental
determinants of fish larvae recruitment variability (Houde and Zastrow, 1993; Bergenius et al.,
2002; Durant et al., 2007). Thus, the food availability, within optimal temperature conditions, could
have favored the larval growth and survival of A. lepidentostole in Perequê-Açu Estuary. The
relationship between water temperature, chlorophyll-a, oxygen saturation and nitrate levels and the
abundance of A. lepidentostole in this estuary highlights the ‘match–mismatch’ phenomenon
(Cushing, 1990). However, despite of peaks in larval fish abundance to be correlated with peaks in
primary and secondary productivity (Cushing, 1990; Martin et al., 1992; Garcia et al., 2003;
Meynecke et al., 2006; Ramos, et al., 2006b; Hsieh et al., 2010), in the present study it was not
clear, because was not observed algal blooms (>20 µg L-1) (Bricker et al., 2003). Therefore, more
studies are necessary to infer that the water temperature, oxygen saturation and nitrate levels could
have favored the growth and survival of A. lepidentostole by increasing the productivity.

Eggs and larvae of many anadromous species are passively transported downstream by the water
flow to estuaries with better rearing conditions (water quality and prey supply) for the young, e.g.
striped bass (Morone saxatilis) and white perch (Morone americana) (North and Houde, 2003). In
this sense, freshwater discharge events during the rainy season may have favored the downstream
transport of A. lepidentostole in Perequê-Açu Estuary, explaining the high capture in the water mass
10
surveyed. A similar positive relationship between downstream and rainfall events also was observed
in other estuarine ecosystems (e.g. Jonsson, 1991; North and Houde 2001; 2003; Martino and
Houde, 2010) and in Bracuí and São João estuaries during this study. The latter, were dominated by
anadromous species Anchoviella spp., that as well as A. lepidentostole also showed a peak of
abundance during the rainy period. On the other hand, Macaé Estuary showed the lower
precipitation rates during our study, and interestingly it was less dominated by this anadromous
species. Thus, the consistent peaks in Anchoviella larval abundances in our study suggest that
transport of eggs down-estuary and passive retention of fish larvae in the middle estuary zone can
be an important component of the Anchoviella life-history strategy. Freshwater flow is also
important for other anadromous migratory species, such as the sea lamprey (Petromyzon marinus)
(Almeida et al., 2002). Additionally, the presence of olfactory cues used by both anadromous and
catadromous species to locate inland freshwater habitats (e.g. Grange et al., 2000; Bolliet et al.,
2007; Moore et al., 2007; Bett and Hinch, 2016) can be affected by reduced flows (Baptista et al.,
2010). Consequently, our results imply that long-term changes in freshwater flow related to global
climate change and anthropogenic modifications of the estuary (e.g. dams, weirs) could have
significant implications for Anchoviella spawning, survival and recruitments.

Nonetheless, the relationships between larval fish abundance and freshwater flow may be quite
different according to species (e.g. Kimmerer, 2002; Ramos et al., 2006b; Gonçalves et al., 2015).
In Macaé Estuary, the lower precipitation favored the immigration of several marine species.
Typically, many marine fish species recruit to estuaries as late-stage larvae or juveniles (e.g.
Boehlert and Mundy, 1988; Neira et al., 1992; Whitfield, 1994; Strydom et al., 2003), and
consequently increase the diversity of fishes in these habitats (Strydom, 2015). Thus, the high
presence of the marine species in Macaé Estuary may have been the reason for this estuary to be
clearly more diverse, despite of the eutrophic conditions (high nutrient load, TPM and lower oxygen
saturation). Marine species were mainly represented by a marine migrant species M. furnieri. This
species occurs in the Western Atlantic from Greater Antilles to Argentina (Froese and Pauly, 2016)
and its high larval abundances seemed to be associated with low salinity or high temperature (Neira
et al., 1992; Morais and Morais, 1994; Bruno and Muelbert, 2009; Costa et al., 2014). In Macaé
Estuary, the peak of M. furnieri did not coincide with this environmental condition, since M.
furnieri was more abundant during the dry and not during the rainy season (warm months). This
result can be associated with the transport and retention of eggs and larvae into the estuaries, since
M. furnieri reproduce in coastal areas near the entrance of the estuaries (Isaac, 1988). Thus, greater
precipitation during the rainy period could highly favor the exportation of eggs and larvae to coastal
areas. Bruno and Muelbert (2009) recorded the precipitation effect on the variability of M. furnieri
11
larvae in Patos Lagoon Estuary, Brazil. According to these authors, the high flow rate can cause a
low abundance of eggs and probably unfavorable conditions for growth and food. In fact, estuarine
processes that affect hatching or fish larvae transport (Witting et al., 1999), or episodic events of
runoff and intensity of the winds on a seasonal scale, can determine the survival of fish larvae and
eggs transport/retention (North and Houde, 2001). Similar river flow effects on fish larvae were also
found in temperate and other tropical estuaries (e.g. Barletta-Bergan et al., 2002; Ramos et al.,
2006b). Thus, a combination of factors such as spawning timing and freshwater flow seemed to
explain the seasonal pattern of the marine species M. furnieri in Macaé Estuary during this study.

During the rainy months, the abundance of the estuarine resident species such as the goby M. meeki
were also lower. Considering the general tendency for estuarine fish larvae to show a peak in
abundance during the rainy seasons (Harris et al., 1999; Young and Potter, 2003; Joyeux et al.,
2004), we hypothesized three different causes for this abundance reduction that could have worked
either separately or in synergy. The first possible cause was the increase in river flow during the
rainy period, which could have flushed fish larvae out of the estuarine habitat. Although estuarine
resident species have developed several traits adapted to estuarine environmental conditions, such
as benthic eggs that are deposited in the substrate (Dando, 1984; Neira et al., 1992; Pampoulie,
2001), an intense flow may transport eggs and larvae towards offshore areas, which should have
marked impact on survival (Ramos et al., 2006b). In fact, the highest M. meeki abundances were
recorded in September and November, when precipitation was low. The second possible cause of
low abundances was a downward vertical migration of fish larvae, keeping them from being flushed
out of the estuarine habitat (Weinstein et al., 1980; Rowe and Epifanio, 1994; Schultz et al., 2000;
Ramos et al., 2006b). Because collections were always performed at 0.5- to 1-m depth, such a
migration also could explain the abundance reduction of M. meeki from the rainy samples. The third
cause could have been that whenever the anadromous species spawn inside the river and get flushed
down the rivers during rain events, they reach such high abundances that might overreach the
carrying capacity of the estuary, and ultimately limiting the abundance of other species, especially
estuarine resident species. In fact, in estuaries where Anchoviella were less abundant, such as
Macaé Estuary, the abundance of estuarine species followed the general trend to peaked in rainy
periods. In this case, estuarine species were mainly represented by the goby Gobiosoma parri
(Table 1), whose spawning tends to occur mainly during rainy months (Acha, 1994; Gomes and
Bonecker, 2014). Thus, in Perequê-Açu Estuary, where M. meeki was more abundant, the
impressive abundances of A. lepidentostole during the rainy season may have limited the occurrence
of this estuarine species. However, estuarine species seem well-evolved to cope with having
planktonic stages competing for planktonic prey resources (Strydom, 2015). Often, sympatric
12
species such as many of the Gobiidae, appear to have staggered spawning periods (Strydom and
Neira, 2006) or respond opportunistically to unpredictable environmental condition (Strydom and
Whitfield, 2000). Consequently, the dominance of plankton catches by estuarine resident species is
typical in temperate and tropical estuaries (e.g. Barletta-Bergan et al., 2002; Ramos et al., 2006b;
Wasserman and Strydom, 2011). Considering this, the timing of occurrence of M. meeki may be the
result of flexibility in the timing of spawning. Thus, we hypothesized that if A. lepidentostole
overreached the carrying capacity of the Perequê-Açu Estuary during the rainy period, M. meeki
may have responded opportunistically, making it ideally suited to use this estuary during the dry
season in order to optimize refuge and feeding opportunities and therefore survival and recruitment.
Nevertheless, more studies focusing a long-term assessment of temporal variability in spatial
patterns of A. lepidentostole and M. meeki larvae will be necessary to confirm this hypothesis.

5 Conclusions
The results suggest that mainly temperature and precipitation, in addition to salinity, regulated the
larval fish assemblages in the studied tropical estuaries. Temperature has played an important role
in determining anadromous species abundance, and precipitation was responsible for episodic
events of runoff and immigration of fish larvae. Alternatively, parameters such as oxygen saturation
and nutrient load could have operated in an indirect way, through their effect on food supply, but
further studies are necessary to investigate this question. This study showed that fish larvae are
highly sensitive to environmental variations, highlighting their potential role in assessing the effects
of climate change and anthropogenic pressures on the estuarine fish assemblages in future
researches. Finally, our results highlight the importance of the conservation of estuarine habitats,
emphasizing that the protection of the habitat used by fishes is essential for ensuring success in the
reproduction and recruitment process and, consequently, to sustain the adult population.

Acknowledgments
This work was supported by the Coordination for the Improvement of Higher Education Personnel
(CAPES), through a PhD grant awarded to Régis Santos and also by the Brazilian National Council
for Scientific and Technological Development (CNPq) (Split Fellowship Program, ref.
204767/2014-8). Sandra Ramos was funded by a FCT Post-doc fellowship
(SFRH/BPD/102721/2014). The authors thank all who participated in field surveys and laboratory
processing; special thanks to Adriana Araújo, Mariana Julio, Marta Quintas, Pedro Carvalho and
Sérgio Bonecker. We also thank to Rodolfo Paranhos and his team from Hydrobiology Laboratory,
Department of Marine Biology of the Federal University of Rio de Janeiro, for their support in
water analysis.
13
14
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22
FIGURE CAPTIONS

Fig. 1 Location of the four estuaries of the study. (1) Macaé, (2) São João, (3) Bracuí and (4)
Perequê-Açu, in the Rio de Janeiro State, South-eastern Brazil.

Fig. 2 Monthly average values and standard deviation (error bars) for precipitation (a), water
temperature (b), oxygen saturation (c), pH (d), chlorophyll-a (e) and total particulate matter (f) in
Macaé (MA), São João (SJ), Bracuí (BR) and Perequê-Açu (PA) estuaries.

Fig. 3 Monthly average values and standard deviation (error bars) for inorganic nutrients: nitrite (a),
ammonia (b), nitrato (c) and phosphate (d) in Macaé (MA), São João (SJ), Bracuí (BR) and
Perequê-Açu (PA) estuaries.

Fig. 4 Seasonal and inter-estuarine patterns of mean abundance (larvae 100m-3), Pielou’s evenness
(J’) and Shannon-Wiener diversity index (H’) of the Macaé (MA), São João (SJ), Bracuí (BR) and
Perequê-Açu (PA) larval fish assemblages. The stacked plots represent sequences of values of the
ecological guilds: C: catadromous, AM: amphidromous, F: freshwater species, MS: marine
stragglers, ES: estuarine species, MM: marine migrants and AN: anadromous.

Fig. 5 Seasonal and inter-estuarine patterns of mean abundance (larvae 100m-3) of the top taxa
(Anchoviella lepidentostole, Anchoviella spp., Micropogonias furnieri and Microgobius meeki).
MA: Macaé; SJ: São João; BR: Bracuí; PA: Perequê-Açu.

Fig. 6 Ordination of sampling estuaries along the first two axes of the canonical correspondence
analysis (CCA) relating top taxa (Alepi: Anchoviella lepidentostole; Anch: Anchoviella spp.; Mmee:
Microgobius meeki; Mfur: Micropogonias furnieri) with environmental variables (arrows) during
the dry (a) and rainy (b) season. Pp: precipitation; T: water temperature; O%: oxygen saturation;
TPM: total particulate matter; Chla: chlorophyll-a; NO3: nitrate; NO2: nitrite; NH3: ammonia;
PO4: phosphate.

23
Fig. 1

24
 350 36
MA SJ BR PA MA SJ BR PA
A 34 B
300
32
Precipitation (mm)

250

Temperature (°C)
30

28
200
26
150
24

100 22

20
50
18

0 16
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Month-Year
Rainy Dry Rainy Dry Month-Year
Rainy Dry Rainy

120 9.0

C MA SJ BR PA D MA SJ BR PA
8.8
110
Oxygen saturation (%)

8.6
100
8.4

90 8.2
pH

80 8.0

7.8
70
7.6
60
7.4

50 7.2
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Month-Year
Rainy Dry Rainy Dry Month-Year
Rainy Dry Rainy

20 60
MA SJ BR PA MA SJ BR PA
E F
Total particulate matter (mg.L-1)

18
50
16
Chlorophyll-a (µg.L-1)

14
40
12

10 30

8
20
6

4
10
2

0 0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Month-Year
Rainy Dry Rainy Dry Month-Year
Rainy Dry Rainy

Fig. 2

25
 1.2 50
MA SJ BR PA MA SJ BR PA
A B
1.0
40

Ammonia (µM)
0.8
Nitrite (µM)

30

0.6

20
0.4

10
0.2

0.0 0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Month-Year
Rainy Dry Rainy Dry Month-Year
Rainy Dry Rainy

14 2.4
MA SJ BR PA MA SJ BR PA
C 2.2 D
12
2.0
1.8
10
Phosphate (µM) 1.6
Nitrate (µM)

8 1.4
1.2
6 1.0
0.8
4
0.6
0.4
2
0.2
0 0.0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Month-Year
Rainy Dry Rainy Dry Month-Year
Rainy Dry Rainy

Fig. 3

26
 400 2.6 400 2.6
Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

MA AM F MS ES MM AN SJ MS ES MM AN
2.4 2.4
350 350
J' H' 2.2 J' H' 2.2

300 2.0 300 2.0

1.8 1.8
250 1.6 250 1.6

J' and H'

J' and H'

1.4 1.4
200 200
1.2 1.2
150 1.0 150 1.0
0.8 0.8
100 0.6 100 0.6
0.4 0.4
50 50
0.2 0.2
0 0.0 0 0.0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Rainy Dry Rainy Dry Rainy Dry Rainy
m m

400 2.6 6.0

9000
Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

C MS ES MM AN PA MS ES MM AN
BR 2.4 5.8
350
J' H' 2.2 J' H'
8500
2.0 2500
300 1.6
1.8
1.4
250 1.6 2000
J' and H'

J' and H'

1.2
1.4
200
1.2 1500 1.0

150 1.0 0.8

0.8 1000
0.6
100 0.6
0.4
0.4 500
50
0.2 0.2

0 0.0 0 0.0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Rainy Dry Rainy Dry Rainy Dry Rainy
m m

Fig. 4

27
 140 180

Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

A. lepidentostole MA SJ BR PA 9000 Anchoviella spp. MA SJ BR PA
160

120 8000 140

in Perequê-Açu
120
7000
100
100
6000 80

60
2000

20 40
1000
20

0 0 0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Rainy Dry Rainy Dry Rainy Dry Rainy
m m

10 240 180
Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

Mean Abundance (larvae 100m-3)

M. furnieri MA SJ BR PA 220 M. meeki MA SJ BR PA
9 160
200
8 140
180
7
160 120
in Macaé

6 140
100
5 120
80
4 100
80 60
3
60
2 40
40
1 20
20
0 0 0
May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15 May-13 Sep-13 Jan-14 May-14 Sep-14 Jan-15
Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15 Jul-13 Nov-13 Mar-14 Jul-14 Nov-14 Mar-15
Dry Rainy Dry Rainy Dry Rainy Dry Rainy
m m

Fig. 5

28
 1.0
A

O%
Pp

T Anch
Mmee pH
Chl a NO2
Alep
Mfur
NH3

PO4
NO3
TPM
-1.0

-1.0 1.0
1.0

Mfur
B
PO4
NH3

NO3 NO2
TPM
Chl a
pH
Anch
Alep Mmee
O%

T Pp
-1.0

-1.0 1.0

SPECIES

ENV. VARIABLES

SAMPLES

Macaé São João Bracuí Perequê-Açu

Fig. 6
29
TABLES

Table 1. Mean abundances (larvae per 100 m-³) and frequency of occurrence (%FO) of larval fish
species recorded in four estuaries (Macaé, São João, Bracuí and Perequê-Açu) between May 2013
and March 2015. - indicates species not caught in that region. EG: ecological guild; MS: marine
stragglers; MM: marine migrants; ES: estuarine species; AN: anadromous; C: catadromous; AM:
amphidromous; F: freshwater species.
Macaé São João Bracuí Perequê-Açu
Family Taxa EG
Abundance %FO Abundance %FO Abundance %FO Abundance %FO
Achiridae Achirus lineatus ES <1 3 <1 2 2 12 1 7
Atherinopsidae Atherinella brasiliensis ES <1 1 <1 1 <1 1 <1 1
Blenniidae Hypleurochilus fissicornis MM 2 19 <1 4 1 9 5 19
Carangidae Caranx spp. MM - - - - <1 1 - -
Carangidae Chloroscombrus chrysurus MS - - <1 1 1 7 <1 5
Carangidae Oligoplites spp. MM - - <1 1 <1 6 <1 2
Carangidae Seriola spp. MS - - 0 1 <1 2 <1 6
Centropomidae Centropomus spp. C - - - - <1 1 - -
Cichlidae Australoheros sp. F <1 1 - - - - - -
Cichlidae Oreochromis niloticus F <1 1 - - - - - -
Clupeidae Harengula jaguana MM 5 13 2 10 1 7 1 6
Clupeidae Opisthonema oglinum MS - - <1 3 <1 1 - -
Cynoglossidae Symphurus plagusia MM <1 1 - - - - - -
Dactyloscopidae Dactyloscopus sp. MS - - <1 1 - - - -
Eleotridae Eleotris pisonis AM <1 1 - - - - - -
Elopidae Elops smithi MM <1 4 1 10 <1 1 <1 3
Engraulidae Anchoviella brevirostris AN 5 17 1 8 1 8 - -
Engraulidae Anchoviella lepidentostole AN 7 22 1 13 11 15 1,062 25
Engraulidae Anchoviella spp. AN 16 23 34 15 28 23 - -
Ephippidae Chaetodipterus faber MS - - <1 1 <1 1 - -
Gerreidae Diapterus rhombeus MM <1 1 <1 1 - - - -
Gerreidae Eucinostomus spp. MM <1 5 <1 5 4 11 2 9
Gerreidae Gerres cinereus MM <1 1 <1 4 <1 3 9 9
Gobiesocidae Gobiesox strumosus MS <1 3 <1 3 <1 2 - -
Gobiidae Bathygobius soporator ES <1 1 - - <1 4 <1 1
Gobiidae Ctenogobius boleosoma ES 4 15 2 13 <1 3 <1 2
Gobiidae Gobionellus oceanicus ES 1 10 <1 4 <1 1 <1 1
Gobiidae Gobionellus stomatus ES <1 4 <1 3 - - <1 1
Gobiidae Gobiosoma nudum MM 1 13 2 5 <1 1 - -
Gobiidae Gobiosoma parri ES 5 19 1 3 - - - -
Gobiidae Microgobius meeki ES 1 11 15 16 6 15 34 25
Haemulidae Haemulidae sp. 1 <1 3 <1 2 - - - -
Haemulidae Haemulidae sp. 2 - - <1 1 - - - -
Haemulidae Haemulon flavolineatum MS <1 1 <1 1 <1 2 - -
Haemulidae Haemulon plumierii MS <1 6 <1 6 <1 3 - -
Microdesmidae Cerdale floridana ES <1 3 <1 3 - - - -
Monacanthidae Stephanolepis hispidus MS - - - - <1 1 - -
Mugilidae Mugil curema MM - - - - <1 1 - -
Muraenidae Gymnothorax spp. MS <1 2 - - - - <1 1
Not identified not identified <1 1 <1 3 <1 1 - -
Paralichthyidae Citharichthys macrops MS <1 1 - - - - - -
Paralichthyidae Citharichthys sp. MS <1 1 - - <1 1 - -
Paralichthyidae Etropus longimanus MM <1 1 - - - - - -
Paralichthyidae Paralichthys brasiliensis MM <1 1 - - - - - -
Paralichthyidae Paralichthys sp. MM - - - - <1 1 - -
Pristigasteridae Odontognathus mucronatus MM <1 1 - - - - - -
Pristigasteridae Pellona harroweri MS 3 13 0 1 - - - -
Sciaenidae Bairdiella ronchus ES <1 1 <1 1 <1 6 3 13
Sciaenidae Isopisthus parvipinnis MM <1 1 - - - - - -
Sciaenidae Macrodon ancylodon MM <1 3 - - - - - -
Sciaenidae Menticirrhus americanus MM <1 2 <1 3 - - <1 2
Sciaenidae Micropogonias furnieri MM 27 19 <1 3 <1 3 <1 3
Sciaenidae Stellifer spp. MM 8 20 1 13 <1 1 4 15
Sparidae Archosargus probatocephalus MS <1 1 - - - - - -
Sparidae Archosargus rhomboidalis MM <1 1 <1 1 1 4 <1 3
Sphyraenidae Sphyraena guachancho MM - - 0 1 - - - -
Syngnathidae Microphis lineatus AN 2 18 <1 7 <1 1 2 10
Tetraodontidae Sphoeroides spp. MM <1 3 0 2 <1 1 - -
Triglidae Prionotus punctatus MS <1 3 - - - - - -

Total no. of larvae 5,399 2,529 2,012 26,162

30
Table 2. Comparative board in relation to the number of species and guilds, density (larvae 100 m-
3
), diversity (H’) and Pielou’s evenness (J’) of the Macaé, São João, Bracuí and Perequê-Açu larval
fish assemblages.
Descriptors Macaé São João Bracuí Perequê-Açu
Number of species 46 39 36 23
Number of functional guilds 6 4 5 4
Density (mean ± SD) 89 ± 85 65 ± 93 58 ± 91 1125 ± 2504
Diversity (H') (mean ± SD) 1.65 ± 0.30 1.22 ± 0.47 1.26 ± 0.37 0.67 ± 0.40
Pielou’s evenness (J') (mean ± SD) 0.70 ± 0.14 0.67 ± 0.19 0.7 4 ± 0.15 0.39 ± 0.27

Table 3. Results of 2-way ANOSIM (R values and significance levels) and SIMPER analysis on the
abundance of all species from four estuaries

Groups ANOSIM SIMPER

R P Average dissimilarity Discriminating species Contribution (%)
Macaé vs São João 0.392 0,001* 76.93 Anchoviella spp. 13.34
Micropogonias furnieri 9.39
Microgobius meeki 8.85
Macaé vs Perequê-Açu 0.868 0,001* 80.98 Anchoviella lepidentostole 32.08
Microgobius meeki 9.58
Anchoviella spp. 7.85
Macaé vs Bracuí 0.616 0,001* 77.10 Anchoviella spp. 11.31
Micropogonias furnieri 9.55
Stellifer spp. 7.96
São João vs Perequê-Açu 0.552 0,001* 84.68 Anchoviella lepidentostole 39.76
Microgobius meeki 11.26
Anchoviella spp. 8.77
São João vs Bracuí 0.210 0,001* 77.59 Anchoviella spp. 19.27
Microgobius meeki 12.93
Anchoviella lepidentostole 7.48
Perequê-Açu vs Bracuí 0.625 0,001* 81.16 Anchoviella lepidentostole 40.42
Anchoviella spp. 12.24
Microgobius meeki 11.02
* Significant differences.

31
Table 4. Results of canonical correspondence analysis (CCA) performed on larval fish
abundance, relating top taxa with environmental variables of Macaé, São João, Bracuí and Perequê-
Açu estuaries during dry and rainy seasons. Underscores values are the highest correlation values
for each variable.

Dry Rainy
Axes Axes
1 2 3 4 1 2 3 4
Eigenvalues 0.37 0.18 0.06 0.25 0.51 0.36 0.18 0.14
Species-environment correlations 0.84 0.69 0.52 0.00 0.96 0.97 0.92 0.89
Cumulative percentage variance
of species data 32.9 49.0 54.1 76.2 17.8 30.3 36.7 41.6
of species-environment relation 60.8 90.6 100.0 0.0 33.9 57.5 69.7 78.9

Sum of all unconstrained eigenvalues (total inertia) 1.12 2.84

Sum of all canonical eigenvalues 0.60 1.49

Summary of Monte Carlo test

Test of significance of all canonical axis

Trace 0.603 1.49
F-ratio 9.65 3.24
P-value 0.002 0.002

Temperature -0.62 0.09 0.10 0.00 -0.49 -0.27-0.37 0.00

Oxygen saturation -0.31 0.29 -0.19 0.00 -0.57 -0.14-0.34 0.00
pH 0.00 0.06 -0.07 0.00 -0.15 0.02-0.31 0.00
Chlorophyll-a -0.44 -0.01 -0.08 0.00 -0.12 0.08-0.11 0.00
Total particulate matter 0.31 -0.46 -0.12 0.00 -0.25 0.19-0.21 0.00
Precipitation -0.26 0.26 -0.13 0.00 -0.18 -0.25 0.37 0.00
Nitrate -0.18 -0.40 0.18 0.00 -0.51 0.25 0.30 0.00
Nitrite 0.18 -0.02 0.38 0.00 0.00 0.24 0.03 0.00
Ammonia 0.29 -0.18 0.19 0.00 -0.06 0.44 0.21 0.00
Phosphate 0.01 -0.31 0.36 0.00 0.01 0.54 0.21 0.00

32