Response of estuarine fish assemblages to an atypical climatic event in northeastern Brazil

Journal Pre-proof Response of estuarine fish assemblages to an atypical climatic event in northeastern Brazil Caroline Stefani da Silva Lima, Maria Luísa de Araújo Souto Badú, André Luiz Machado Pessanha

PII: DOI: Reference:

S2352-4855(19)30386-X https://doi.org/10.1016/j.rsma.2020.101121 RSMA 101121

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Regional Studies in Marine Science

Received date : 19 March 2019 Revised date : 5 November 2019 Accepted date : 29 January 2020 Please cite this article as: C.S. da Silva Lima, M.L. de Araújo Souto Badú and A.L.M. Pessanha, Response of estuarine fish assemblages to an atypical climatic event in northeastern Brazil. Regional Studies in Marine Science (2020), doi: https://doi.org/10.1016/j.rsma.2020.101121. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Response of estuarine fish assemblages to an atypical climatic event in northeastern Brazil

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Caroline Stefani da Silva Lima, Maria Luísa de Araújo Souto Badú & André

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Luiz Machado Pessanha

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Universidade Estadual da Paraíba, Laboratório de Ecologia de Peixes, Avenida das Baraúnas, 351, Bairro Universitário, 58429-500, Campina Grande, PB, Brazil. Corresponding author: Andre Luiz Machado Pessanha Email: [email protected]

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Running head: Response of estuarine fish assemblages to atypical climatic event

16 Abstract

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Knowledge of the effects of environmental variables on estuaries with intermittent

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upstream rivers is scarce. Thus, understanding how environmental filters affect fish

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assemblages in these estuaries is important when an atypical drought occurs. Three

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zones in the Mamanguape River estuary designated according to the salinity gradient

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were sampled during an atypical climatic event in 2015. A total of 18,084 fishes of 125

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species were recorded. Density and richness showed significant differences between

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seasons, while density, biomass, diversity and evenness showed significant differences

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in spatial pattern. By ecological guild, marine estuarine-dependent, solely estuarine,

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marine estuarine-opportunist and estuarine and marine were the most representative

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groups in the estuary during the sampling period. Chlorophyll a and salinity were major

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filters that explained only the spatial distribution of fish assemblages, relating mainly to

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richness increasing from the upper to the lower parts of the estuary. Our study supports

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the need to understand the filters for species richness and spatial distribution patterns.

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Changes in those filters may shift fish assemblages, hence altering ecosystem function.

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Keywords: Young-of-the-year; Recruitment; Environmental gradient; Semi-arid;

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Tropical estuary; Climate changes.

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1. Introduction

36 Estuaries are dynamic systems characterized by spatiotemporal fluctuations in

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physico-chemical characteristics that significantly influence their ecological process

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(Potter et al., 2010; Blaber, 2013). This high environmental variability exerts a strong

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effect on fish assemblages, setting limits on species distribution in estuarine habitats

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(Rozas et al., 2013). These variables restrict which species can settle in the estuary,

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controlling those who can pass through the environmental filters and removing

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unsuitable species (Cornwell et al., 2006; Carvalho & Tejerina-Garro, 2014; Kraft et al.,

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2015). Therefore, species that occur in the same habitat are able to tolerate and share

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similar environmental conditions (Kraft et al., 2015). In addition, biotic interactions

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such as competition have been considered a controlling factor on abundance due to

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interactions among species with similar niches (Webb et al., 2002). Thus, habitat

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characteristics and biological interactions are also mechanisms that significantly

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influence community structure in estuarine ecosystems (Attrill & Power, 2000; Tsou &

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Matheson Jr., 2002; Wetz &Yoskowitz, 2013).

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Climate change affects individuals, populations and communities through

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individual physiological and behavioral responses to environmental change (Booth et

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al., 2011). For instance, changes in the intensity and frequency of precipitation events

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during extreme droughts may contribute to lower amounts of freshwater input, which

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have profound effects on habitat fragmentation, altering salinity regimes and reducing

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productivity and water quality in estuaries (Wetz & Yoskowitz, 2013). Salinity is the

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main environmental factor linked to freshwater input that plays a decisive role in

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defining the structural and functional characteristics of aquatic biota in estuaries (Telesh

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& Khlebovich, 2010). Changes in salinity affect fish metabolism through

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osmoregulation and oxygen demands, since extreme and sudden shifts induce stress for

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many fish species (Gillanders et al., 2011). Furthermore, increasing seawater incursion

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generates ecological changes in the guild composition of estuaries (Martinho et al.,

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2007; Feyrer et al., 2015). One example comes from the Mondego estuary (Portugal),

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where during a severe drought (2004/2005), an extended intrusion of seawater inside the

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estuary was observed, resulting in the depletion of freshwater species and an increase in

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marine species (Martinho et al. 2007). Most detailed studies on climate change in

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estuaries suggest that variability in salinity impacts fecundity, spawning success and

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recruitment of fish species (Gillanders et al., 2011; Feyrer et al., 2015; Wedderburn et

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al., 2016). Since 2010, the semiarid part of the Northeast Region of Brazil has been

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experiencing one of the longest and most intense droughts in decades (Marengo et al.,

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2013; Pereira et al., 2014; Erfanian et al., 2017). Climatic drought in the Northeast

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Region has been attributed to shifts in the anomalously warm tropical North Atlantic

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and the presence of El Niño conditions (Marengo et al., 2018). Two-thirds of the

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Mamanguape River basin is under the influence of a semiarid climate, which causes an

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intermittent flow regime in most of the basin; the river is perennial near the coast, where

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the basin is influenced by tributaries from wetter areas (Oliveira-Silva et al., 2018).

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Therefore, the functioning of this tropical estuary is strongly influenced by the

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magnitude and timing of freshwater runoff reaching the estuary, and the freshwater

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runoff largely determines the salinity distribution in this ecosystem. For instance,

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sampling of estuarine conditions in 1997 and 2000 (during the dry period) (Leonel et

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al., 2000, Leonel et al., 2006) indicated that salinity means in the Mamanguape River

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estuary were lower than those observed in surveys conducted in 2011 and 2014 (during

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the extended drought) (Oliveira & Pessanha, 2014; Silva et al., 2018). Perhaps for this

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reason, many fish species move across estuarine systems in response to salinity

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changes, linked to a decrease in both precipitation intensity and frequency. Therefore,

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combined with other environmental variables, salinity could be an important predictor

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for habitat selection by fish assemblages.

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Estuarine biodiversity has been and will continue to be severely affected by

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global change (Dudgeon et al., 2006; Baptista et al., 2015; Sloterdijk et al., 2017).

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Unfortunately, information about the effect of decreased riverine discharge on estuarine

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fish assemblages in intermittent upstream river estuaries remains scarce. Indeed, the

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degree to which the biodiversity of naturally intermittent rivers is affected may differ

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from of the degree of the effect on perennial rivers (Williams et al., 2017). Therefore, if

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fish assemblages are recurrently affected by seawater intrusion during prolonged

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drought, modifications linked to estuarine environmental changes will affect the

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abundance of juveniles, through what Pasquaud et al. (2012) call the hypothesis of

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“marinization”. Therefore, the hypothesis underlying this work is that increasing

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salinity during the drought period drives changes in the fish community throughout this

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tropical estuary. Understanding how seawater intrusion affects the composition and abundance of

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fish assemblages in estuaries with features such as those found in a Brazilian semiarid

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region became important in the face of an atypical drought experienced in this region.

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The findings of the current study will address key knowledge gaps and improve our

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understanding of the influence of decreased freshwater discharge on fish community

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structures and species richness in a tropical estuary.

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2. Material and Methods

109 2.1. Study Area

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The Mamanguape River estuary is located on the north coast of Paraíba State,

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Brazil. The estuarine area is 25 km in length, including the Environmental Protection

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Area of the Mamanguape River (EPA Decree 924/1993), with an area of 146.4 km2

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(Mourão & Nordi, 2003). The estuarine channels are covered by mangrove forests that

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include the species Rhizophora mangle, Avicennia germinans, Avicennia schaueriana,

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Laguncularia racemosa and Conocarpus erectus (Nascimento et al., 2011). In the

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estuary entrance, a long reef barrier exists perpendicular to the shoreline, creating a

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semiclosed bay with calm waters and a mix of fresh water and seawater (Fig. 1).

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The aim of the EPA creation was to protect marine manatees, which use the

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estuary as the main breeding site in the Northeast Region of Brazil (Silva et al., 2011),

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as well as to create a natural resource conservation area (Cruz & Costa, 2014).

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However, this estuary shows anthropogenic impacts caused by sugarcane cultivation

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(Alves & Nishida, 2003), shrimp farming (Silvestre et al., 2011) and mangrove

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deforestation (Alves & Nishida, 2003; Alves et al., 2005). Recently, microplastics were

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reported in the stomach contents of several fish species in this estuary (Vendel et al.,

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2017).

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The regional climate is classified as tropical As and is divided into two periods:

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the winter rainfall season (March until August) and the summer dry season (September

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until February) (Alvares et al., 2013). According to Marengo et al. (2017), between

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1990 and 2016, the Northeast Region of Brazil suffered a sequence of drought years due

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to El Niño events. The rainfall data from 2010 to 2016 were obtained from the Paraíba

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State Water Management Executive Agency and plotted to demonstrate the effects of

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negative rainfall anomalies since 2010 (Supporting File-S1).

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2.2.

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Sampling We sampled the fish community during the daytime in the rainy season (May,

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June and July 2015) and in the dry season (October and November 2015 and January

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2016). We conducted all samples during the low tide. The estuary was divided

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according to the salinity gradient and geomorphology, forming three zones located in

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the upper, middle and lower Mamanguape estuary main channel. Zones 1 and 2 were

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located in the upper estuary. These zones contain relatively shallow waters surrounded

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by a mangrove forest and have a greater freshwater influence. Zone 3, located in the

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lower part of the estuary, includes extensive seagrass beds, unvegetated mud areas and

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sandbanks nearest to the estuary mouth, with a stronger seawater influence.

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The fish were collected with a beach seine net (10 m long, 1.5 m high and with

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0.8 cm mesh) and the hauls were taken parallel to the coastline at a depth of

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approximately 1.5 m. We performed nine samples in each of the three zones. The

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sample design contained a total of 162 samples (3 zones x 3 sites x 3 replicates x 6

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months). The area covered by the beach seine net was calculated following the

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procedure proposed by Sparre & Venema (1998) and Ramos et al. (2016), which was

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used for calculating the fish densities, following equation below:

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AB =D*W

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, where D is length swept by the hauls and W is length of beach seine net. The collected

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fish were identified, counted, measured (total length in mm) and weighed (g) (reported

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to 2 decimal places).

We measured salinity and water temperature (°C) in situ using a multiparameter

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sensor, while transparency (cm) and depth (cm) were measured using a Secchi disc and

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a meter, respectively. Grain size analysis was carried out by mechanical separation

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through a column of sieves with different mesh sizes, following Brown & McLachlan

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(1990) classification which was classified in Very Coarse Sand (VCS: > 2.0 mm),

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Coarse Sand (CS: 0.5 to 2.0 mm), Medium Sand (MS: 0.25 to 0.5 mm), Fine Sand (FS:

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<0.125 mm). Types of grains percentages were obtained through the total and each type

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Journal Pre-proof 6 of grains weights. Organic matter content was quantified through difference between the

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weight before and after burning of 3 g sediment samples by 500° C during 8 h in a

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moufle. Primary production was also quantified by analyzing chlorophyll a content in

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the water, following the methodology proposed by Wetzel & Likens (1991) using a

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spectrophotometer to reading chlorophyll a through two wave lengths (665 and 750

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nm).

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2.3.

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Data analysis

To examine the spatiotemporal variations of the environmental parameters, two

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fixed factors were used for the analyses: spatial (3 levels: zone 1, 2 and 3) and seasonal

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(2 levels: rainy and dry). Environmental variables were log(x+1) transformed prior to

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analysis, except for the granulometric data, which was arcsine transformed into. A

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Euclidean distance matrix was used on the transformed data to test the differences

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among factors, with 9,999 permutations for the probability tests (PERMANOVA;

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Anderson, 2001; Anderson & Ter Braak, 2003). The full set of 10 available

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environmental variables was tested for collinearity (Draftsman plot and Spearman

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correlation matrix), and redundant variables with correlations (r) > 0.7 were omitted

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from the model. Environmental variables were normalized and examined using

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principal component analysis (PCA), which used environmental and granulometric data

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to summarize and describe relationships among variables and to detect patterns along

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the estuary.

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We obtained the density (individuals/m2), biomass (g/m2) and richness

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(species/m2) through catch per unit area (CPUA; Sparre & Venema, 1998).

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Correspondence Analysis (CA; Thiolouse et al., 1997) was performed to view species

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abundance (density and biomass) in sampled zones and between seasons (R

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Development Core Team, 2017). The analysis was performed using the functions of the

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“Ade4” package in R statistical software. Diversity indices (J’= Pielou’s species

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evenness and H’= Shannon-Wiener diversity) were computed for zones and seasons.

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Fish assemblage structure expressed as density or biomass of individuals was

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fourth-root transformed to perform comparisons among the zones and seasons, with

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9,999 permutations for the probability tests (PERMANOVA). Transformed sample data

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were then used to create a Bray-Curtis similarity matrix calculated for two fixed factors

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(spatial and seasonal). The SIMPER routine was performed to obtain species

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contributions within zones from each sample season. Diversity indices and multivariate

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analyses were performed with the PRIMER software package, version 6.0 (Clarke &

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Gorley, 2006; Anderson et al., 2008).

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2.4.

Ecological guilds Each captured species was assigned to an ecological guild, as described by

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Elliott et al. (2007) and Potter et al. (2013): Marine Straggler (MS), Marine Estuarine-

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Opportunist (MEO), Marine Estuarine-Dependent (MED), Solely Estuarine (SE),

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Estuarine and Marine (EM), Freshwater Straggler (FS), and Freshwater Estuarine-

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Opportunist (FEO). Fish life cycle features and Fishbase® (www.fishbase.org) were

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taken into account in guild classification (Wyanski & Targett, 2000; Miranda-Marure et

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al., 2004; Fávaro et al., 2007; Oliveira & Fávaro, 2010).

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Environmental variables’ influence on fish assemblages We used Canonical Correspondence Analysis (CCA) to examine the

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interactions between the fish density, biomass values (response variable) and

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environmental effects (explanatory variables) among the zones and seasons. Direct

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analysis of gradients across the CCA allowed the clarification of the roles that

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environmental factors played in structuring the fish community (ter Braak &

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Verdonschot, 1995). The CCA was performed on transformed data to detect joint

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species distribution and environmental patterns (ter Braak, 1986). The forward selection

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option, together with the Monte Carlo permutation test, was used prior to CCAs, using

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499 sample permutations (p < 0.01). To reduce the effects of rare species, only species

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with a Frequency of Occurrence ≥ 7% were included in the CCA. Multivariate analysis

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was performed with CANOCO.

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3.

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3.1. Environmental variables

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Results

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Spatially, temperature, salinity, transparency, depth, very coarse sand, fine sand

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and organic matter showed the highest values in zone 3 (Figure 2). Coarse sand

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displayed the highest values in zone 1, while medium sand showed the highest values in

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zone 2 (Table 1). Spatial variations were significant only for salinity (Pseudo-F2.161 =

Journal Pre-proof 8 125.32; p = 0.0001), transparency (Pseudo-F2.161 = 7.9432; p = 0.0001), depth (Pseudo-

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F2.161 = 8.187; p = 0.0007), very coarse sand (Pseudo-F2.161 = 14.577; p = 0.0001),

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coarse sand (Pseudo-F2.161 = 10.166; p = 0.0001), medium coarse (Pseudo-F2.161 =

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5.1164; p = 0.0068), fine sand (Pseudo-F2.161 = 0.0068) and organic matter (Pseudo-

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F2.161 = 22,757; p = 0.0001). We recorded the highest values of salinity, transparency

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and chlorophyll a in the dry season, while depth showed the highest values in the rainy

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season. Temperature did not show great variation between seasons (Table 1). However,

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according to PERMANOVA, only temperature (Pseudo-F1.161 = 38.42; p = 0.0001),

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salinity (Pseudo-F1.161 = 50,711; 0.0001), transparency (Pseudo-F1.161 = 44.11; p =

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0.0001) and chlorophyll a (Pseudo-F1.161 = 22.543; p = 0.0001) showed significant

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differences between seasons.

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PCA ordination using zone and season levels as environmental variables showed

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a variation pattern. Seasonally, the rainy season showed the highest correlations with

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medium sand, fine sand and organic matter, whereas the dry season showed the highest

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correlations with temperature, chlorophyll a, very coarse sand, transparency, salinity

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and depth (Table 2; Fig. 3-a). Spatially, samples from zones 1 and 2 are clustered in the

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upper quadrant in the diagram, correlating with coarse sand, medium sand and

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temperature, whereas chlorophyll a, very coarse sand, transparency, salinity, depth,

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organic matter and fine sand are correlated with zone 3 in the lower quadrant of the

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diagram (Table 2; Fig. 3-b).

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3.2.

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Species Composition

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During the study, 18,084 fishes were recorded from 125 species in the estuary,

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including larval stages. Engraulidae, Atherinopsidae, Gerreidae and Lutjanidae had the

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highest densities, while Atherinopsidae and Tetraodontidae had the highest biomass (see

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Table S1 in supplementary material).

Species composition and density differed between seasons and zones. The most

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abundant species during the rainy season were Sciades herzbergii, Atherinella

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brasiliensis, Eucinostomus melanopterus, Engraulidae and Gerreidae larvae in zone 1,

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Engraulidae larvae and Atherinella brasiliensis in zone 2 and Gerreidae larvae,

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Atherinella brasiliensis and Caranx latus in zone 3. In the dry season, Atherinella

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brasiliensis showed a higher density in zones 1 and 2, while Atherinella brasiliensis,

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Rhinosardinia bahiensis, Anchoa januaria, Harengula clupeola, Caranx latus, Anchoa

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hepsetus, Lycengraulis grossidens and Ulaema lefroyi were most abundant in zone 3. The species with the highest biomass during the rainy season were S. herzbergii

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and A. brasiliensis in zone 1, whereas zones 2 and 3 had the highest biomass of A.

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brasiliensis and Sphoeroides testudineus, respectively. During the dry season, A.

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brasiliensis, Hyporhamphus unifasciatus and E. argenteus had the highest biomass in

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zone 1; A. brasiliensis and S. testudineus had the highest biomass in zone 2; and in zone

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3, A. brasiliensis, S. testudineus, C. latus and R. bahiensis had the highest biomass (Fig.

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4).

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3.3.

Spatiotemporal variation in fish assemblages

PERMANOVA demonstrated that community descriptors differed significantly

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among estuarine zones, but only density and richness differed between seasons. During

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the rainy seasons, we registered the highest values for density (Pseudo-F 1.156 = 13.215,

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p <0.001) and richness (Pseudo-F1.156 = 19.156, p < 0.001; Zone x Season: Pseudo-F2.156

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= 8.9479, p < 0.001), mainly due to the Engraulidae species. Spatial patterns of changes

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in community descriptors were significantly higher in zones 2 and 3, mainly for density

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(Pseudo-F2.156 = 13.811, p = 0.0001), biomass (Pseudo-F2.156 = 29.38, p = 0.0013) and

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diversity (Pseudo-F2.156 = 4.475, p = 0.0001). However, evenness was higher in zone 1

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during rainy season, but it was higher during dry season than in the other zones

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(Pseudo-F = 4.0701; p = 0.0003; Fig. 5).

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According to the SIMPER analysis and density data, the composition of the fish

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fauna differed mainly by zone and season. SIMPER indicated that A. brasiliensis, E.

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melanopterus, M. brevirostris, A. lineatus and were S. testudineus the primary

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contributors to the observed similarity during rainy season. The similarity during dry

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season indicated that A. brasiliensis, E. melanopterus, S. testudineus, A. lineatus and E.

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argenteus were the most influencers for the community structure. Spatially, the most

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contributions were A. brasiliensis, E. melanopterus, C. boleosoma, A. lineatus and H.

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unifasciatus in zone 1, S. testudineus, A. brasiliensis, A. lineatus, E. melanopterus and

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E. argenteus in zone 2, and A. brasiliensis, C. latus, E. melanopterus, S. testudineus and

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H. unifasciatus in zone 3.

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Journal Pre-proof 10 Using biomass data, SIMPER showed E. melanopterus, A. brasiliensis, S.

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testudineus, C. latus and C. boleosoma were the highest contributions to similarity

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during rainy season. Meanwhile, A. brasiliensis, A. lineatus, S. testudineus, E.

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melanopterus and H. unifasciatus showed the most contribution to similarity during dry

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season. Lastly, spatial contributions of fish species to similarity showed A. brasiliensis,

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E. melanopterus, C. boleosoma, C. latus and S. testudineus the most contributors to

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zone 1, A. brasiliensis, S. testudineus, E. melanopterus, E. argenteus and A. lineatus to

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zone 2, and C. latus, S. testudineus, E. melanopterus,

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unifasciatus to zone 3 (Table 3).

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3.4.

Ecological Guilds

Gerreidae larva and H.

In terms of the number of species in each guild, 65 (52%) of the 125 fish species

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caught in the estuary were marine estuarine-dependent (MED) types, followed by 21

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(16.8%) solely estuarine (SE), 12 (9.6%) marine estuarine-opportunist (MEO) and 11

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(8.8%) estuarine & marine (EM). The guilds with the least number of species

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corresponded to 5 (4%) marine straggler (MS), 4 (3.2%) freshwater straggler (FS) and 1

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(0.8%) freshwater estuarine opportunist (FEO). In terms of density (abundance) and

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biomass of ecological guilds, we registered differences between seasons (Density:

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Pseudo-F2.156 = 5.10, p = 0.0033; Biomass: Pseudo-F2.156 = 3.54, p = 0.0185) and among

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estuarine zones (Density: Pseudo-F1.156 = 8.12, p = 0.0001; Biomass: Pseudo-F1.156 =

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11.33, p = 0.0001). During rainy seasons, the highest abundance and biomass for the

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solely estuarine (SE) species was reported; in contrast, the highest dominance for

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marine estuarine dependent species (MED) and estuarine & marine (EM) species

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occurred during the dry season. In the estuarine gradient, solely estuarine (SE) species

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were more abundant and showed high biomass in zones 1 and 2, while marine estuarine-

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dependent (MED) species dominated in abundance and biomass in zone 3. Freshwater

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estuarine opportunist (FEO) species were only found in zone 1 while marine straggler

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(MS) species were only found in zone 3. The least abundant freshwater straggler species

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were found in zone 1 and 2 (Table 4).

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3.5.

Effects of environmental variables on fish assemblages

Journal Pre-proof 11 Among the 125 species identified, 37 were used in the CCA analysis because

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they are more abundant than other species (numerical percentage > 7%). All

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environmental variables were significant (p < 0.05, Monte Carlo test), with the

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exception of sediment grain size, which was excluded from the analysis. The first two

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axes of the CCA explained 66.5% of the variation in the species-environment

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relationship for density data and 70.6% of the variation for biomass data. Chlorophyll a

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and salinity were the major factors affecting fish assemblages in density and biomass

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distribution (Table 5), wherein samples from zone 1 were most associated with

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chlorophyll a, but samples from zone 3 were most associated with salinity.

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For density, the CCA plot projected the samples for zone 3 in the left-lower side

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of the diagram due to the high abundance of S. greeleyi, Gerreidae larva, C. latus,

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Anchoa januaria and A. spinifer, which were from selected areas with the highest

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salinity and transparency. Conversely, a part of the samples from zones 1 and 2 was

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projected in the upper side of the diagram and were related to the high abundance of P.

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vivipara, S. herzbergii, H. unifasciatus and E. melanopterus that were from selected

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areas with the lowest salinity and highest temperature and sediment organic matter

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content. While the part was projected in the middle-right side and was related to

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abundance of A. fasciatus, A. bimaculatus, Bryconamericus sp., C. rendalli and

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Engraulidae larva with habitats high productivity (Chlorophyll a). Similar to density,

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biomass revealed spatial shifts in fish assemblage structures. Species loadings on CCA

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axes indicated that A. januaria, A. lepidentostole, L. grossidens, U. lefroyi and Albula

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vulpes (leptocephalus larvae) showed higher biomass in zone 3, related mainly to the

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higher salinity and organic matter. The biomass of A. fasciatus, A. bimaculatus,

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Bryconamericus sp., C. boleosoma and T. paulistanus was strongly associated with high

344

productivity, low salinity and organic matter and abundance of E. argenteus, D,

345

auratus, H. unifasciatus was related to low transparency in zone 1 (Fig. 6).

lP

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329

348 349

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3474. 4. Discussion

The spatial pattern of the fish assemblages in the Mamanguape River estuary

350

was more noticeable than the temporal pattern. This is probably related to changes in

351

environmental variables associated with the continuum theory (Dame et al., 1992),

352

which states that changes in composition and abundance correspond to estuarine

Journal Pre-proof 12 gradient salinity and chlorophyll a concentration. These main variables operated as

354

environmental filters of fish assemblages whose abundance and composition increased

355

from upper to lower zones, and in which a greater marine influence occurred. The

356

interaction of freshwater and the salt wedge allowed the formation of an environmental

357

gradient, meaning that the lowest salinity values occurred in zones of greater freshwater

358

influence and that the highest salinity values were nearest to the ocean. Among

359

environmental variables, the salinity selected for species that differed in osmoregulatory

360

ability (Whitfield, 2015), allowing them to be part of the different fish assemblages that

361

were established under different salinity ranges in the estuary (Never et al., 2011).

362

Meanwhile, chlorophyll a was indicative of areas that are more productive where there

363

are great food availabilities for fishes (Claudino et al., 2015).

pro of

353

We considered only 45 species as residents in this estuary. However, only

365

juveniles and adults of Atherinella brasiliensis, Hyporhamphus unifasciatus

366

Eucinostomus argenteus, Eucinostomus melanopterus, Sphoeroides testudineus and

367

Sphoeroides greeleyi were found to be abundant throughout the zones as a result of the

368

sampling method used in estuarine shallow areas. These organisms were classified as

369

core species (Magurran et al., 2003) because they maintained an elevated abundance

370

across the spatiotemporal variation in the estuary compared to other species, according

371

to our observations in this study. Core species have the ability to tolerate environmental

372

condition variations (Hanki, 1982; Gibson et al., 2005; Magurran et al., 2011), since

373

they do not experience the effects of environmental filters in their spatial distribution

374

(Poff, 1997).

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364

Two distinct fish assemblages were prominent in this tropical estuary. Both

376

zones 1 and 2 showed low diversity and abundance that decreased when approaching

377

zone 3. This gradient may be a result of the more complex habitats present in zone 3

378

(e.g., seagrass beds, rock reef and mudflats; Xavier et al., 2012), which could explain

379

the greater species number and biomass in zone 3 than in zone 1. Our results support the

380

complexity theory (Diehl,1992; Humphries et al., 2011), which states that habitats with

381

high complexity may be able to support a greater number of species by reducing

382

predation and preventing prey depletion (Nargelkerken et al., 2010; Hylkema et al.,

383

2014; Claudino et al., 2015). The highest larval abundance of several species in the

384

lower estuary may have been promoted by the influence of habitat complexity offering

385

shelter or food abundance, suggesting that the development of the early life stages of

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375

Journal Pre-proof 13 these species was influenced by more diverse habitats. Furthermore, studies have shown

387

that distinct habitats benefit from the colonization of different species in tropical

388

estuaries, such as pipe fishes (Cosmocampus elucens and Syngnathus pelagicus) in

389

seagrass (Silva et al., 2018), R. bahiensis and C. latus in mudflats (Clark & Pessanha,

390

2015; Garcia & Pessanha, 2018) and S. testudineus in mangroves (Araújo et al., 2016).

391

The highest contribution to diversity in the lower part of the estuary was associated with

392

the presence of some stenohaline species that tolerate less salinity variation (Barletta et

393

al., 2005; Whitfield et al., 2012, 2015). Thus, the spatial distribution of fish species in

394

estuaries, represented more extensively by juveniles, has been linked to the

395

osmoregulatory ability that allows for spreading into different ranges of the salinity

396

gradient (Araújo & Azevedo, 2001).

pro of

386

The species composition in zones 1 and 2 displayed a lower percentage of

398

freshwater fishes than marine ones. Freshwater fishes, such as A. bimaculatus, A.

399

fasciatus and Bryconamericus sp., were rarely found in those zones, mainly because of

400

the lower freshwater inflow and pronounced seawater intrusion. Whitfield (2015)

401

suggested that freshwater fish species in most estuaries are not as species-rich as the

402

marine assemblage in the same systems. We recorded some juvenile marine species at

403

the highest density and biomass in the upper estuary, e.g., Diapterus auratus, Mugil

404

brevirostris, M. curema and H. unifasciatus which may tolerate low salinity levels in

405

these zones. It is possible that these species are using these areas as nursery areas

406

because of the low abundance of predators or larger fishes, as suggested by Whitfield

407

(2015), or the availability of food, such as zooplankton and benthic invertebrates

408

(Figueiredo & Pessanha, 2015). The same pattern was observed to juveniles of D.

409

auratus in Pueblo Viejo lagoon which was found in areas with low salinities and

410

protected by vegetation (Castillo-Rivera et al., 2005).

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397

The strong presence of the Marine Estuarine-Dependent and Estuarine and

412

Marine species throughout the estuary may lie in the associated saline intrusion, which

413

is mainly related to the influence of the tides and could have promoted the transport of

414

eggs and larvae in seawater upward into the estuary (zones 1 and 2). Species guild

415

dominance in this area is associated with the decreased river flow, particularly during

416

the dry season, which is typical in semiarid climates (Barbosa et al., 2012). In 2015,

417

rainfall was insufficient (Erfanian et al., 2017); however, during this study, larval fish

418

transportation occurred. These findings also show that Elops saurus (leptocephalus

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411

Journal Pre-proof 14 larvae), Engraulidae larvae and R. bahiensis used the upper reaches of the estuary only

420

during their early life stages, which suggests changes in species distribution ranges for

421

larvae habitats. In temperate estuaries, previous research also found a relationship

422

between decreasing freshwater and increasing marine fish species due to an extended

423

intrusion of seawater inside the estuary and a significant reduction in abundance during

424

the driest period (Garcia et al., 2001; Martinho et al., 2007; Acuña-Plavan et al., 2010);

425

this pattern was also observed in this estuary. Studies published by Pasquaud et al.

426

(2012) in a Gironde estuary (France) suggested that these effects, called “marinization,”

427

may favor the nursery function for marine juvenile fishes in estuarine areas. A similar

428

pattern was exhibited by fishes in Australian estuaries in response to climate change

429

(Booth et al., 2011; Rolls et al., 2012; Williams et al., 2017).

pro of

419

However, typical estuarine species were exceedingly abundant and were

431

recorded in all three zones, indicating that they may reside in and endure a wider range

432

of salinity concentrations, e.g., in the Mamanguape estuary, species such A. brasiliensis

433

and S. testudineus were the dominant species indicated by SIMPER. There is good

434

evidence to support the case of A. brasiliensis, and its high abundance is attributed to

435

the fact that this species showed salinity tolerance (Souza-Bastos & Freire, 2011), was

436

fast growing and had a short life cycle (Contente et al., 2011). The physiological

437

capacity (Hostim-Silva et al., 1995; Neves et al., 2006) and reproductive strategy

438

(Favaro et al., 2003) of A. brasiliensis might also influence and drive their success in

439

estuarine areas. The distribution of S. testudineus within the estuary may be closely

440

linked to its consumption of abundant prey, in particular Gastropoda, Bivalvia and

441

Decapoda, as well as other food sources available in this habitat (Araújo et al., 2016).

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430

The relative biomass abundance of several species changed in the estuary based

443

on seasonal periods that are mainly influenced by environmental variables, which

444

probably led to assemblage displacement along the estuary. Such results coincide with

445

recruitment peaks for most fish species. Several authors have noted that temporal

446

variations resulted in young fish migration in estuaries and, hence, were linked to the

447

nursery-ground function. In our results, higher density values for Engraulidae and

448

Gerreidae larvae correspond to their larval stages during the rainy seasons (Dantas et al.,

449

2012; Amorim et al., 2016; Ramos et al., 2016). This follows density patterns suggested

450

by Araújo et al. (2016) for Gerreidae and Oliveira & Pessanha (2014) for Engraulidae,

451

who hypothesized that during the peak of the rainfall period, those species avoid more

Jo

442

Journal Pre-proof 15 452

saline water, hence minimizing the energetic cost of osmoregulation (Rhody et al.,

453

2010) Changes in assemblage structure during the rainy season may also occur in

455

response to estuarine zone expansion; the expanded zone displays unstable

456

environmental conditions that lead fishes to specific trend distributions during the rainy

457

season. Bate et al. (2002) classified this zone as the river-estuary-interface (REI) region

458

and demonstrated changes in the relative abundances of euryhaline marine and estuarine

459

fish species; these results were influenced by the quality and quantity of freshwater

460

entering the estuary. Environmental variables during this study in the rainy season, such

461

as transparency and salinity, decreased towards the upper estuary (zones 1 and 2).

462

Hence, the large numbers of juveniles, the density of which decreased from 37.45

463

individuals/m2 in zones 1 and 2 to 20.24 individuals/m2 in zone 3, had a particular

464

significance. The species richness also decreased from 2.94 species/m2 in the upper

465

estuary to 1.37 species/m2 in the lower estuary. We noted that these results may be due

466

to the growing recruitment into the estuary from the marine environment and the

467

dominance of estuarine resident species (e.g., A. brasiliensis). Thus, this species’

468

activity results in a significant change in fish assemblages within the upper reaches

469

because there was an increase in available niches there.

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pro of

454

This seasonal cycle also regulates predator species and recruitment success,

471

which produces temporal shifts in fish assemblages in estuaries (Faye et al., 2011). Our

472

results also revealed that during the rainy seasons, there were differences in the densities

473

of juveniles of piscivore species. During this period, S. timicu, C. latus, Lutjanus sp. and

474

O. saurus were registered less frequently in shallow waters in the estuary. Figueiredo &

475

Pessanha (2015) showed higher abundance patterns of piscivorous species during the

476

dry seasons compared to rainy seasons in tidal creeks in this tropical estuary. Changes

477

in transparency (< 30 cm registered in zones 1 and 2) should affect the encounter and

478

predation rates of piscivores by altering their search efficiency. Low water transparency

479

during the recruitment season decreases predation rates (Rhody et al., 2010) by

480

decreasing predator visibility and providing a protection strategy that prevents fish at

481

the early life stages from being caught (Blaber & Blaber, 1980; Araújo et al., 2008).

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482

urn a

470

In the dry season, the density of marine estuarine species increased mainly

483

because the estuary was under an increasing influence of the tides and a decreasing

484

influence of the river. Therefore, the increase in marine guilds in zone 1 was due to

485

seawater influence at this site and the loss of freshwater habitats, which was reflected in

Journal Pre-proof 16 the decreasing estuarine guilds. In addition, there is a conspicuous salinity gradient

487

among the estuarine zones that plays a fundamental role in the different guild

488

distributions. Salinity fluctuations influence fish assemblage distribution in tropical

489

estuaries. Such approaches were also suggested by Barletta et al. (2005) and Whitfield

490

et al. (2012), who described the abundance of stenohaline species in lower areas of

491

estuaries, corresponding with our observations of the distribution of the Lutjanidae and

492

Haemulidae species Nicholsina usta usta, Atherinella blackburni and Chaetodipterus

493

faber. Studies on the effects of a salinity gradient on fish movement patterns have

494

shown that when relatively stable hydrological conditions create a well-defined gradient

495

in a tropical estuary, it promotes the large-scale spatial distribution of estuarine species

496

(Dantas et al., 2010; Clark & Pessanha, 2015; Ramos et al., 2016).

pro of

486

Another aspect associated with the dry season was the fish species size pattern;

498

the largest individuals were found during the dry season (e.g., D. auratus, A. januaria,

499

Lycengraulis grossidens and Rhinosardinia bahiensis). This evidence reflects the

500

ontogenetic habitat shifts hypothesis (Medeiros et al., 2018), in which small individuals,

501

such as larvae and juveniles, obtain an environmental refuge during the rainy season and

502

appear to migrate to adjacent areas as they grow throughout the dry season. This

503

migration is particularly beneficial because they can rapidly grow and develop,

504

becoming less vulnerable to predation. The earliest evidence of this theory was provided

505

by Clark & Pessanha (2015), who found large schools of R. bahiensis juveniles

506

selecting sheltered sites in tidal creek habitats, while adults were found in intertidal

507

mudflats. Araújo et al. (2016) also documented a greater proportion of juvenile mojarras

508

in shallow waters than in deeper waters, which was interpreted as a size-dependent

509

refuge response to increasing predation pressure.

urn a

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497

According to the CCA, during this atypical year, chlorophyll a and salinity were

511

the variables most related to fish density and biomass. These environmental variables

512

contributed to the spatial gradient that separated zone 1, which had estuarine

513

characteristics, from zone 3, which was closely correlated with the marine environment.

514

Distribution of freshwater fishes (A. bimaculatus, A. fasciatus, Bryconamericus sp. and

515

C. rendalli), Engraulidae larvae, A. brevirostris, Citarichthys macrops and Diapterus

516

rhombeus was correlated with rising primary productivity, whereas species such as

517

Mugil brevirostris, Citharichthys spilopterus, Bathygobius soporator, Lycengraulis

518

grossidens, Ulaema lefroyi and Rhinosardinia bahiensis occurred in areas with the

Jo

510

Journal Pre-proof 17 highest salinity concentrations. Furthermore, salinity induced a spatial pattern that

520

limited freshwater species to the upper reaches and marine species to the lower reaches,

521

mainly because of the physiological tolerance associated with osmoregulation (Barletta

522

& Blaber, 2007; Sánchez-Botero et al., 2009; Vilar et al., 2011, Whitifield et al., 2015).

523

Therefore, a well-defined salinity gradient could be a physiological limit of spatial

524

distribution for some marine fish species (Araújo et al., 2002).

pro of

519

The richness of species exhibited an inverse relationship with primary

526

productivity. This pattern does not follow the species-energy theory (Wright, 1983),

527

which proposes that species richness in a certain area is limited by the quantity of

528

energy available. However, Witmam et al. (2008) found that richness decreased despite

529

high productivity, which they attributed to covarying environmental (low salinity) stress

530

or to high consumer pressure at high productivity sites. Spatial changes in trophic

531

organization have been extensively documented in the Mamanguape estuary (Claudino

532

et al., 2015; Dolbeth et al., 2016; Figueiredo & Pessanha, 2015). In this study, the

533

authors verified that low prey availability increased the predation pressure at higher

534

reaches, wherein most community members were omnivorous and detritivorous fishes

535

such as Mugil curema and Ctenogobius boleosoma. Future changes in precipitation in

536

Brazilian coastal regions due to low freshwater input events may play a critical role in

537

trophic interactions in estuaries. Mallin et al. (1993) proposed a hypothesis that suggests

538

that if precipitation decreases, coastal primary production may also decline, leading to

539

possible trophic implications, including reductions in fishery productivity.

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525

In conclusion, our results corroborated the hypothesis that salinity acts as a

541

spatial filter for fish assemblages due to the apparent longitudinal gradient in the

542

Mamanguape River estuary and temporal changes in the freshwater discharge structure,

543

composition and recruitment process. In addition, primary productivity levels were

544

important in determining species richness in fish assemblages based on food resource

545

availability from the upper to the lower reaches. In general, more attention is required

546

concerning the effects of drought on tropical estuaries. For instance, studies on the

547

influences of low freshwater inputs on recruitment processes and the distribution of fish

548

populations will provide fundamental information about dynamic of fish assemblages in

549

estuaries. Understanding these mechanisms during droughts will explain how fish

550

assemblages are established and coexist through variation in the main environmental

551

filters in tropical estuaries.

Jo

540

Journal Pre-proof 18 552 553

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AESA – Agência Executiva de Gestão das Águas do Estado da Paraíba (2016) Climatologia da precipitação anual acumulada (mm) – ano 2016. Available in: http://site2.aesa.pb.gov.br/aesa/jsp/monitoramento/chuvas/climatologias Graficos.jsp. Access 01 jun 2016.

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Alves, R.R.N., Nishida, A.K., 2003. Aspectos socioeconômicos e percepção ambiental dos catadores de caranguejo-uçá Ucides cardatus cordatus (L. 1763) (Decapoda, Brachyura) do estuário do rio Mamanguape, Nordeste do Brasil. Interciência 28, 36-43.

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Alves, R.R.N., Nishida, A.K., Hernandez, M.I.M. 2005. Environmental perception of gatherers of the crab caranguejo-uçá (Ucides cordatus, Decapoda, Brachyura) affecting their collection attitudes. Journal of Ethnobiology and Ethnomedicine 1, 1-8. doi: 10.1186/1746-4269-1-10

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Alvares, C.A., Stape, J.L., Sentelhas, P.C., Gonçalves, J.L.M., Sparovek, G., 2013. Köppen’s climate classification map of Brazil. Meteorologische Zeitschrif 22, 711-728. doi: 10.1127/0941-2948/2013/0507

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Araújo, F.G., Azevedo, M.C.C., Silva, M.A., Pessanha, A.L.M., Gomes, I.D., CruzFilho, A.G., 2002. Environmental influences on the demersal fish assemblages in the Sepetiba Bay, Brazil. Estuaries 25, 441-450. doi: 10.1007/BF02695986

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Araújo, P.R.V., Costa, S.Y.L., Duarte, M.R.N., Pessanha, A.L.M., 2016. Feeding and spatial distribution of two estuarine puffer fish in a tropical estuary, north-eastern Brazil. Journal of the Marine Biological Association of the United Kingdom 89, 581-588. doi: 10.1017/S0025315416001454

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Attrill, M.J., Power, M., 2000. Modelling the effect of drought on estuarine water quality. Water Research 34, 1584-1594. doi: 10.1016/S0043-1354(99)00305-X

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Barbosa, J.E.L., Medeiros, E.S.F., Brasil, J., Cordeiro, R.S., Crispim, M.C.B., Silva, G. H.G., 2012. Aquatic systems in semi-arid Brazil: limnology and management. Acta Limnologica Brasiliensia 24, 103-118. doi: 10.1590/S2179975X2012005000030

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Barletta, M., Blaber, S.J.M., 2007. Comparison of fish assemblage and guilds in tropical habitats of the embley (indo-west pacific) and Caeté (western atlantic) estuaries. Bulletin of Marine Science 80, 647-680.

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Bate, G.C., Whitfield, A.K., Adams, J.B., Huizinga, P., Wooldridge, T.H., 2002. The importance of the river-estuary interface (REI) zone in estuaries. Water SA 28, 271-280. doi: 10.4314/wsa.v28i3.4894

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Elliott, M., Whitfield, A.K., Potter, I.C., Blaber, S.J.M., Cyrus, D.P., Nordlie, F.G., Harrison, T.D., 2007. The guild approach to categorizing estuarine fish assemblages: a global review. Fish and Fisheries 8, 241-268. doi: 10.1111/j.14672679.2007.00253.x

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Figure Captions

912

Fig. 1 Study area. Mamanguape River estuary with sampling areas indicated: Circle =

914

Zone 1; Triangle = Zone 2 and Square = Zone 3.

re-

913

915

923 924 925 926 927 928 929 930 931

lP

urn a

922

Fig. 2 Box-plot of spatiotemporal variation of environmental variables measured in three zones sampled in the Mamanguape River estuary for the rainy and dry seasons: Temperature (A), Salinity (B), Transparency (C), Depth (D), Chlorophyll a (E), Organic matter (F) Very coarse sand (G), Coarse sand (H), Medium sand (I) and Fine sand (J). Zone 1 (■), Zone 2 (■), Zone 3 (■). Box-plot: median, interquartile range, maximum and minimum values.

Fig. 3 Principal component analysis (PCA) of environmental variables in the Mamanguape River estuary. Codes: (A) temporal variation: Rainy (▲), Dry (○); (B) spatial variation: Zone 1(▲), Zone 2 (■), Zone 3 (○). OM = Organic matter; VCS = Very coarse sand; CS = Coarse sand; MS = Medium sand; FS = Fine sand.

Fig. 4 Fish taxa density and biomass in zones 1, 2 and 3 during the 2015 rainy and dry seasons in the Mamanguape estuary. Density: (a) and (b), Biomass: (c) and (d); Seasons: Rainy (■), Dry (■).

Jo

916 917 918 919 920 921

932

Fig. 5 Box-plot of spatiotemporal variation in density (A), biomass (B), richness (C),

933

diversity (D) and evenness of fish assemblage. Zone 1 (■), Zone 2 (■), Zone 3 (■). Box-

934

plot: median, inter-quartile width, minimum and maximum values.

Journal Pre-proof 28 935

pro of

Fig. 6 Ordination triplot of canonical correspondence analysis (CCA) based on density (A) and biomass (B) data on fish assemblages in the Mamanguape River estuary correlated to environmental variables represented by vectors. Rainy: Zone 1 (▲), Zone 2 (■), Zone 3 (●). Dry: Zone 1 (Δ), Zone 2 (□), Zone 3 (○). Species are coded by the first two letters of genus and species or epithets (ATBR = Atherinella brasiliensis, ACLI = Achirus lineatus, ANSP = Anchoa sp., ANJA = Anchoa januaria, ANCSP = Anchoviella sp., ANBR = Anchoviella brevirostris, ANLE = Anchoviella lepidentostole, ASBI = Astyanax bimaculatus, ASFA = Astyanax fasciatus, BASO = Bathygobius soporator, BRSP = Bryconamericus sp., CALA = Caranx latus, CIMA = Citharichthys macrops, CISP = Citharichthys spilopterus, CTBO = Ctenogobius boleosoma, DIAU = Diapterus auratus, DIRH = Diapterus rhombeus, EUAR = Eucinostomus argenteus, EUME = Eucinostomus melanopterus, HYUN = Hyporhamphus unifasciatus, AVLL = Albula vulpes leptocephalus larva, ENLA = Engraulidae larva, GELA = Gerreidae larva, LYGR = Lycengraulis grossidens, MUBR = Mugil brevirostris, MUCU = Mugil curema, OLPA = Oligoplites palometa, OLSA = Oligoplites saurus, POVI = Poecilia vivipara, RHBA = Rhinosardinia bahiensis, SCHE = Sciades herzbergii, SPGR = Sphoeroides greeleyi, SPTE = Sphoeroides testudineus, STTI = Strongylura timucu, CORE = Coptodon rendalli, TRPA = Trinectes paulistanus, ULLE = Ulaema lefroyi).

re-

936 937 938 939 940 941 942 943 944 945 946 947 948 949 950 951 952 953 954

956

lP

955

957

Supporting file

958

Fig. S1 Means Rainfall on the Mamanguape river estuary, Northeast of Brazil.

961 962 963 964 965

Jo

960

urn a

959

2 

1 

27.41 (±0.36)

3.18 (±0.83)

27.22 (±3.92)

58.51 (±4.85) 3.88 (±0.42) 15.20 (±2.84) 5.47 (±0.62) 34.17 (±3.02) 33.71 (±2.10) 46.32 (±4.77)

Salinity (ppt)

Transparency (cm)

Depth (cm)

Chlorophyll a (µg/L)

Organic matter (%)

Very coarse sand

Coarse sand

Medium sand

Fine sand

Zone 1

urn a

Temperature (°C)

Variables

Jo

31.28 (±3.19)

44.50 (±2.14)

31.35 (±3.28)

4.94 (±0.84)

4.94 (±3.27)

7.79 (±1.52)

52.85 (±4.80)

21.74 (±2.51)

27.53 (±1.38)

lP

27.53 (±0.30)

Zone 2

Rainy

45.61 (±4.37)

32.61 (±3.26)

23.09 (±2.24)

13.31 (±3.25)

13.31 (±4.15)

4.11 (±1.01)

69.25 (5.53)

re-

40.74 (±3.80)

27.42 (±1.39)

28.15 (±0.42)

Zone 3

29.44 (±9.39)

57.40 (±4.81)

46.66 (±2.91)

17.52 (±1.45)

28.74 (±0.25)

Zone 2

13.67 (±1.78)

28.51 (±2.22)

57.51 (±3.06)

5.71 (±0.61)

3.23 (±0.32)

15.58 (±2.56)

35.68 (±3.12)

46.46 (±3.61)

8.89 (±2.82)

7.33 (±1.43)

pro of

26.73 (±9.00)

46.11 (±4.16)

42.77 (±3.55)

5.19 (±0.67)

30.28 (±0.30)

Zone 1

Dry

38.75 (±5.57)

27.94 (±2.97)

33.03 (±3.95)

17.16 (±2.16)

20.81 (±2.43)

28.41 (±9.44)

73.70 (±5.08)

55.18 (±4.67)

38.19 (±1.18)

29.29 (±0.42)

Zone 3

Table 1 Means and standard deviation of environmental variables in zones for 2015/2016 rainy and dry seasons in Mamanguape estuary.

Journal Pre-proof

0.197

-0.190 0.273

0.396 -0.288 -0.409 2.47 24.7

OM VCS CS MS FS Eigenvalues %Variation

22.1

2.21

-0.394

-0.080

0.374

-0.207

-0.445

-0.099

pro of

-0.432

-0.269

-0.434

0.012

PC2

re-

0.105

0.384

0.325

0.423

PC1

Chlorophyll a

Depth

Transparency

Salinity

Temperature

lP

Components/variables

urn a Eigenvector coefficient

matter; VCS = Very coarse sand; CS = Coarse sand; MS = Medium sand; FS = Fine sand.

Jo

Table 2 Eigenvalues coefficients of principal components (PC1 and PC2) and environmental variables in Mamanguape estuary. OM = Organic

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urn a

(29.91)

27.81

13.74

11.62

10.73

Similarity average

A. brasiliensis

E. melanopterus

C. boleosoma

M. brevirostris

Z1

and dry seasons from SIMPER.

7.72

12.71

8.55

(40.68)

Z2

Rainy

3.22

9.45

10.40

(46.19)

Z3

8.59

11.70

20.21

(44.96)

Z1

7.44

16.83 5.94

11.67

(39.73)

Z3

Rainy

Z3

Z1

Biomass

11.65

18.47

23.07

(29.91)

4.86

13.64

10.69

(40.68)

Z2

3.02

9.64

(46.19)

8.48

7.81

8.17

19.73

(44.96)

pro of Z1

re-

(47.48)

Z2

Dry

lP

Density

8.05

18.04

(47.48)

Z2

Dry

5.83

9.40

(39.73)

Z3

Table 3 Contribution (%) 70% cut level of species for density and biomass data in three zones in Mamanguape estuary during 2015/2016 rainy

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5.85 5.21 4.27 4.11 3.72

Gerreidae – larva

Engraulidae – larva

Achirus lineatus

M. curema

C. spilopterus

A. vulpes –

7.18

C. latus

(40.68)

8.92

6.96

(29.91)

Z2

S. testudineus

C. macrops

H. unifasciatus

Similarity average

Z1

Z3

7.62

9.88

9.34

6.09

5.84

(46.19)

urn a

Jo Rainy

Z1

15.01

7.75

16.80

16.60

7.97

6.57

(39.73)

Z3

5.87

(29.91)

Z1

9.06

8.96

10.69

(40.68)

Z2

Rainy

11.12

8.09

5.33

(46.19)

Z3

16.52

8.85

7.86

(44.96)

Z1

Biomass

7.60

6.86

8.03

10.01

pro of 5.61

7.49

re-

(47.48)

Z2

Dry

lP

(44.96)

Density

16.64

15.47

6.07

(47.48)

Z2

Dry

2.19

8.04

8.56

4.63

(39.73)

Z3

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Z3

3.09 3.06 2.92

Anchoa sp.

A. hepsetus

H. corvinaeformis

U. lefroyi

4.06

3.93

B. soporator

12.66

3.84

4.30

7.40

4.16

(39.73)

Z3

6.29

(40.68)

Z2

Rainy

5.27

(46.19)

Z3 (44.96)

Z1

Biomass

pro of

(29.91)

Z1

re-

(47.48)

Z2

lP

(44.96)

Z1

Dry

O. saurus

E. argenteus

4.13

(46.19)

L. grossidens

(40.68)

6.63

(29.91)

Z2

S. greeleyi

Leptocephalus larva

Similarity average

Z1

urn a

Jo Rainy

Density

11.52

(47.48)

Z2

Dry

2.56

2.94

3.28

4.34

3.10

4.66

4.84

3.30

(39.73)

Z3

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(29.91)

(40.68)

Z2

Z3

(46.19)

(39.73)

Z3 (40.68)

Z2

Rainy

(46.19)

Z3 (44.96)

Z1

pro of

(29.91)

Z1

re-

(47.48)

Z2

lP

(44.96)

Z1

Dry

Biomass

(47.48)

Z2

Dry

2.53

(39.73)

Z3

4,56

0,39

FEO

FS

Z1

0,08

-

Z2

Rainy

-

-

Z3

Abundance (%)

0,12

-

Z1

-

-

Z2

Dry

-

-

Z3

0,11

0,63

Z1

-

-

Z2

Rainy

-

-

Z3

0,22

-

Z1

Biomass (%)

Estuarine Dependent (MED), Estuarine & Marine (EM), Freshwater Straggler (FS), Freshwater Estuarine Opportunist (FEO).

-

-

Z2

Dry

-

-

Z3

during 2015 rainy and dry seasons. Guilds: Solely Estuarine (SE), Marine Straggler (MS), Marine estuarine opportunist (MEO), Marine

Table 4 Spatio-temporal frequency of contribution in density and biomass for different ecological guilds recorded in Mamanguape estuary

A. januaria

Similarity average

Z1

urn a

Jo Rainy

Density

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-

-

32,32

MEO

MS

SE

76,03

21,09 58,07

35,83

18,60

-

0,17

2,66

0,04

0,18

5,98

-

-

urn a

39,25

41,91

41,88

-

-

15,61

41,77

re-

2,17

0,30

1,35

79,09

17,10

lP

3,91

-

0,01

68,45

27,62

39,86

-

0,05

18,89

41,20

40,29

0,02

0,11

32,97

26,61

8,96

-

-

26,37

64,44

20,32

-

0,03

18,30

61,35

22,42

0,05

2,79

49,66

25,08

pro of -0.443

-0.735 -0.312

Temperature (°C) Salinity (ppt)

0.243

Axis 1 Axis 2

Components/variables

Density

0.047

-

-0.563

-

Axis 1 Axis 2

Biomass

Eigenvectors coefficient

Density: F-ratio = 11.81, p-value = 0.0020; Biomass: F-ratio= 4.06, p-value 0.0020.

Table 5 Values of mains results of canonical correspondence analysis of environmental variables and density and biomass data relations.

31,36

MED

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31,37

EM

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-0.247

OM (%)

Total inertia

lP

70.6

0.11

-0.340

0.302

-0.191

6.178

44.4

0.20

0.146

-0.498

0.335

pro of

66.5

6.634

45.9

0.22

0.202

-0.025

0.041

re-

Species-environmental relation (%)

Eigenvalues

0.50

0.834

Chlorophyll a (µg/L)

urn a

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-0.642

Transparency (cm)

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