Habitat residency and movement patterns of Centropomus parallelus juveniles in a subtropical... by Meros do Brasil

Journal of Fish Biology (2016) doi:10.1111/jfb.12944, available online at wileyonlinelibrary.com

Habitat residency and movement patterns of Centropomus parallelus juveniles in a subtropical estuarine complex F. A. Daros*†, H. L. Spach† and A. T. Correia*†‡§ *Centro Interdisciplinar de Investigação Marinha e Ambiental (CIIMAR/CIMAR), Rua dos Bragas 289, 4050-123, Porto, Portugal, †Universidade Federal do Paraná (UFPR), Campus Politécnico, Caixa Postal 19031, 81531-900 Curitiba, Brasil and ‡Faculdade de Ciências da Saúde da Universidade Fernando Pessoa (FCS/UFP), Rua Carlos Maia 296, 4200-150, Porto, Portugal (Received 2 August 2015, Accepted 8 February 2016) Sixty Centropomus parallelus juveniles were collected in March 2013 in two locations (Tromomó and Guaraguaçu) inside the Paranaguá estuarine complex, southern Brazil. The habitat residency and movement patterns of the individuals were inferred from Sr:Ca ratios and age recorded in the otoliths. Data suggest that the species spawns preferentially in brackish areas mainly from October to January, and that growth rate during the early juvenile stage could be influenced by environmental salinity. Furthermore, the data also show that C. parallelus can occupy diverse salinity habitats and migrate among marine, brackish and freshwater areas within the Paranaguá estuarine complex, showing a high environmental plasticity and adaptation. © 2016 The Fisheries Society of the British Isles

Key words: Centropomidae; life cycle; microchemistry; microstructure; sagitta.

INTRODUCTION The fat snook Centropomus parallelus Poey 1860 is an important euryhaline species in recreational and commercial fisheries (Mendonça & Katsuragawa, 2001), and its high retail value (Alvarez-Lajonchère & Tsuzuki, 2008) means that it has a large aquaculture potential (Corrêa & Cerqueira, 2009). It inhabits inshore waters, estuaries and coastal lagoons of the tropical and subtropical western Atlantic, occurring from Florida to the southern coast of Brazil (Rivas, 1986). In the Paranaguá estuarine complex (PEC), C. parallelus is found in several environments, ranging from marine coastal areas to freshwater streams (Spach et al., 2004; Felix et al., 2007; Contente et al., 2011; Vitule et al., 2013). Centropomus parallelus is now considered as amphidromous, i.e. it migrates between fresh water and salt water during a portion of its life cycle (Riede, 2004; Silvano et al., 2006; Fortes et al., 2014). It has a feeding regime mainly based on fishes, insects and crustaceans, although early juveniles are also zooplanktivorous (Corrêa & Uieda, 2007; Alvarez-Lajonchère & Tsuzuki, 2008; Feltrin-Contente et al., 2009). It is a protandric §Author to whom correspondence email: atcorreia.ciimar@gmail.com

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hermaphrodite, which means that individuals become sexually mature first as males and later undergo sex inversion to females as they grow (Alvarez-Lajonchère & Tsuzuki, 2008). It spawns asynchronously near river mouths, inlets, bays, estuaries, islands or in coastal inshore waters (Silvano et al., 2006; Alvarez-Lajonchère & Tsuzuki, 2008). The pelagic eggs and larvae drift into brackish water swamps or mangroves where they develop (Alvarez-Lajonchère & Tsuzuki, 2008). Embryonic development lasts c. 20 h after fertilization (Cerqueira & Tsuzuki, 2009) and post-larval settlement occurs c. 2⋅5 weeks after hatching (Itagaki, 2005). The complete transformation to the juvenile stage occurs at 40 days, with early juveniles having a total length (LT ) of 10 mm (Alvarez-Lajonchère et al., 2002). For the Brazilian coast, C. parallelus does not show evidence of genetic spatial differentiation, suggesting the existence of high gene flow (Prodocimo et al., 2008). At present C. parallelus populations are considered threatened by overfishing, water pollution and habitat loss (Rocha et al., 2007; Feltrin-Contente et al., 2009). Fisheries regulations (resolution number 016/2009) are currently imposed in Paraná State, such as minimum and maximum landing LT (40 and 50 cm, respectively), and closure of the fishing season from November to December (SEMA, 2009). Estuaries, besides providing habitats for many fishes, frequently act as nursery areas for growth of larvae and early juveniles before they recruit to adult populations (Able, 2005). Estuaries are also characterized by temporal and spatial fluctuations of abiotic factors, namely temperature and salinity, mainly due to freshwater runoff, inflow and tidal cycles, creating a very dynamic physicochemical environment (Heupel & Simpendorfer, 2008; Tyler et al., 2009). The relationship between the spatial distribution of estuarine fishes and abiotic factors is well known (Marshall & Elliott, 1998). Salinity is one of primary factors influencing the habitat use and movement of fishes within an estuary (Harrison & Whitfield, 2006; Selleslagh & Amara, 2008; Passos et al., 2013). Furthermore, fish populations are highly dependent upon the characteristics of their habitat, which supports all their biological functions. Fishes may require a diversity of habitats for the main phases of their life cycle, such as reproduction, growth and sexual maturation. Habitat loss, discharge modifications, changes in water quality and temperature, increased predation pressure and dam construction are important environmental issues to take into account in successful fish conservation measures (McDowall, 1992). Fish movements have been studied using a variety of tools, such as mark and recapture, telemetry and otolith chemistry (Campana et al., 1999; Trotter et al., 2012; Liu et al., 2014). Otoliths are metabolically inert structures as new mineral material is neither resorbed nor reworked after deposition, and the uptake of elements into the growing structures usually reflects the physical and chemical aquatic environment (Campana et al., 2000). The Sr:Ca ratios of otoliths can be used as natural tags to describe fish movements between freshwater, brackish and seawater habitats (Secor & Rooker, 2000; Suzuki et al., 2011; Mai et al., 2014). Furthermore, for a wide range of salinities and fish species a well-known positive relationship exists between Sr:Ca ratios in the otoliths and the water where fishes live (Kraus & Secor, 2004). Using Sr:Ca ratios linked to the chronological proprieties of otoliths, the individual movement of a fish can be retrospectively tagged in a given population (Elsdon & Gillanders, 2006). The objective of this study was to examine the habitat residency and movement pattern of juvenile C. parallelus, an estuarine-dependent species in PEC, obtained from Sr:Ca ratios and microstructural analyses of otoliths.

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MATERIALS AND METHODS S T U DY A R E A The PEC (Fig. 1) has an area of 612 km2 and is characterized by a diversity of habitats, including tidal flats, channels, mangroves, tidal creeks, estuarine beaches, rivers and rocky shores (Lana et al., 2001). It is a partially mixed estuary with semidiurnal tides and diurnal inequality, which is connected to the Atlantic Ocean in the east, by the Sueste and Galheta Channels (Knoppers et al., 1987). The PEC is divided into five sectors with 12 sub-estuaries based on their morphological and hydrological characteristics The Guaraguaçu River is characterized by a large mesohaline coastal plain drainage area of c. 397 km2 , with runoff to the Cotinga sub-estuary. The Tromomó site, a polyhaline area, is located in the mouth of Serra Negra River that discharges to the Benito sub-estuary, Laranjeiras sector, being the largest drainage area of the PEC (Noernberg et al., 2006). BIOLOGICAL SAMPLING Sixty C. parallelus early juveniles were sampled in March 2013. Fish collection took place at two different sites (Tromomó and Guaraguaçu, polyhaline and mesohaline sites, respectively) using a seine (15 m long with a stretched mesh size of 5 mm) operated from the margin by two people. In laboratory, the fish were measured (standard length, LS , mm) and weighed (M, g). Sagittal otoliths were extracted from the otic cavity, rinsed with fresh water, air dried and stored in Eppendorf vials until further analysis. WAT E R A N A LY S I S Post hoc water samples were collected from the two sampling points during the low and high tide periods at different water column depths (surface, middle and bottom) and were preserved by addition of nitric acid and kept at 4∘ C until further analysis. Water Sr concentration was determined using ICP-OE. Salinity and temperature were also recorded in situ using a YSI CTD CastAway (www.ysi.com). O T O L I T H P R E PA R AT I O N The left sagittal otoliths were cleaned of organic tissues using distilled water, air dried and mounted in epoxy resin (Struers, Epofix; www.struers.co.uk) with the sulcus acusticus facing down. The blocks were sectioned near the otolith margins by cutting away the excess resin with a low speed diamond saw (IsoMet, Buehler; www.buehler.co.uk) at 6000 rpm. Otoliths were ground in the transverse plane to expose the core with 800, 1200 and 2400 silicon carbide papers (Hermes; www.hermes-abrasives.com) by making regular optical inspections under a metallographic microscope (Meiji, ML7100; www.metallographic-equipment.com), and further polished with 6, 3, 1 and 0⋅25 μm diamond pastes (Metadi II, Buehler). Finally, otoliths were cleaned in an ultrasonic bath with ultrapure water (Milli-Q water) and given a carbon coating by high vacuum evaporation. Sr and Ca concentrations (% dry mass) were measured along the ventral ridge of the sulcus from the core to the edge using an X-Ray Electron Probe Micro-Analyser (EPMA, JEOL JXA-8500F; www.jeol.co.jp). Apatite [Ca5 (PO4 )3 ] and celestite (SrSO4 ) were used as standards. Accelerating voltage and beam current were 15 kV and 20 nA, respectively. The electron beam was focused on a point c. 10 μm in diameter, spacing measurements at 20 μm intervals. The acquisition time was 180 s (30 s per element, 30 s for the measurement of the counts in the corresponding peak and 30 s for measuring background contribution) per point. The limit of detection was 100 mg l−1 . The microprobe measurement points, which were seen as burn depressions on the otolith surface, were assigned later to otolith growth increments. Each electron microprobe spot represented about five primary growth increments. Because the EPMA transect was not continuous along the otolith radius, the two adjacent spots (pre and post) to each growth incremental section without measurements were averaged to represent the mean Sr and Ca concentration. For the core and edge analysis, a single ablation point was used. The

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Fig. 2. Transverse section from the sagittal otolith of a 72 day Centropomus parallelus individual (standard length, LS = 24 mm) collected in Guaraguaçu showing the primary increments ( ) and the location of the burn depressions (

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results are presented as the amount of Sr divided by the amount of Ca, ×1000. Although a data review in the literature indicates that the mean Sr:Ca ratios of teleosts are highly variable, it is noteworthy that the mean ± s.d. values of Sr:Ca × 1000 for Perciformes are significantly different between certain concentric zones in otoliths, reflecting the freshwater (2⋅8 ± 1⋅3), brackish water (6⋅2 ± 1⋅0) and seawater (8⋅4 ± 2⋅9) habitats (Yang et al., 2011). Furthermore, Sr:Ca ratios recorded in the otolith edge of Guaraguaçu (mesohaline environment) and Tromomó (polyhaline environment) individuals were from 4⋅8 to 9⋅3 and 8⋅0 to 11⋅4, respectively. According to this information and assuming similar approaches (Tabouret et al., 2010), the reconstruction of the history of C. parallelus habitat use was made considering all individuals, irrespective of sampling location, that Sr:Ca ratios (×103 ) between 2–5, 5–8 and 8–11 were considered as fresh, brackish and seawater residency, respectively. A standard qualitative approach for classifying fish otolith Sr:Ca sequences into environmental histories was used since the produced classifications were not significantly different from those determined using algorithms in quantitative approaches (Hedger et al., 2008). Furthermore, it was also assumed that otoliths in the present study do not present vateritic inclusions since no dark areas were observed under reflected light after EDTA etching (Tzeng et al., 2007). Following microprobe analysis, the otolith surface was re-polished with diamond pastes (0⋅25 μm), etched for 2 min with 5% EDTA, cleaned in an ultrasonic bath with ultrapure water (Milli-Q water) and vacuum coated with Au/Pd for scanning electron microscope observation (Quanta 400 FEG ESEM/EDAX genesis X4M; www.fei.com) at 15 kV and ×700 magnification. The primary increment measurements were performed using ImageJ in combination with the ObjectJ plug-in (http://imagej.nih.gov/ij/). The averages of every five successive primary increments widths from the core to the otolith edge were used for otolith growth analysis. Primary increments were assumed to be deposited daily for this species (Itagaki, 2005) (Fig. 2).

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Frequency (%)

Autumn

Spring Winter Spawning season

Summer

Fig. 3. Backcalculated frequency of spawning dates of Centropomus parallelus individuals.

S TAT I S T I C A L A N A LY S I S The data were checked for normality and homoscedasticity prior to statistical analysis. Differences between sampling sites for LS , age and Sr:Ca ratios in otolith core and edge were evaluated using t-tests. The statistical level of significance (đ?&#x203A;ź) was 0â&#x2039;&#x2026;05. Data are presented as mean values Âą s.d. The statistical analysis was performed using R (version 2.15.3; www.r-project.org).

RESULTS The juveniles of C. parallelus had an LS ranging from 21 to 55 mm. The post-hatching ages were between 61 and 157 days. LS and age showed no significant differences between the locations (t = â&#x2C6;&#x2019;0â&#x2039;&#x2026;348, d.f. = 56â&#x2039;&#x2026;32, P > 0â&#x2039;&#x2026;05 and t = 1â&#x2039;&#x2026;367, d.f. = 35â&#x2039;&#x2026;99, P > 0â&#x2039;&#x2026;05, respectively). Reproduction dates backcalculated from estimated otolith daily ages, indicated that the C. parallelus has multiple spawnings per year, with a peak between October and January (Fig. 3). Water Sr concentrations ranged from 1â&#x2039;&#x2026;3 Âą 0â&#x2039;&#x2026;3 to 2â&#x2039;&#x2026;5 Âą 0â&#x2039;&#x2026;9 mg lâ&#x2C6;&#x2019;1 , for GuaraguaĂ§u and TromomĂł, respectively. Salinity and temperature varied from 6â&#x2039;&#x2026;4 Âą 2â&#x2039;&#x2026;8 to 11â&#x2039;&#x2026;9 Âą 6â&#x2039;&#x2026;5â&#x2C6;&#x2DC; C and from 28â&#x2039;&#x2026;1 Âą 0â&#x2039;&#x2026;1 to 26â&#x2039;&#x2026;3 Âą 0â&#x2039;&#x2026;2â&#x2C6;&#x2DC; C, for GuaraguaĂ§u and TromomĂł, respectively. Otolith Sr:Ca ratios (Ă&#x2014;103 ) ranged from 2â&#x2039;&#x2026;3 to 10â&#x2039;&#x2026;4 and from 5â&#x2039;&#x2026;8 in to 11â&#x2039;&#x2026;6 in GuaraguaĂ§u and TromomĂł, respectively. The C. parallelus caught in both locations showed no significant differences in their otolith cores for the Sr:Ca ratio concentrations (t = 0â&#x2039;&#x2026;116, d.f. = 57â&#x2039;&#x2026;77, P > 0â&#x2039;&#x2026;05) showing an overall value of 7â&#x2039;&#x2026;8 Âą 1â&#x2039;&#x2026;5. For the otolith edge, Sr:Ca ratios were statistically different (t = â&#x2C6;&#x2019;13â&#x2039;&#x2026;114, d.f. = 55â&#x2039;&#x2026;96, P <0â&#x2039;&#x2026;001) between GuaraguaĂ§u (6â&#x2039;&#x2026;3 Âą 1â&#x2039;&#x2026;0) and TromomĂł (9â&#x2039;&#x2026;5 Âą 0â&#x2039;&#x2026;9) (Table I). ÂŠ 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.12944

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Table I. Collection site, geographic co-ordinates, date, sample size (n), standard length (LS ), age and Sr:Ca ratios of Centropomus parallelus

Sites

Location

Date

30 March 25∘ 36⋅151′ S; Guaraguaçu 48∘ 29⋅465′ W 2013 Tromomó

21 March 25∘ 15⋅845′ S; 48∘ 24⋅641′ W 2013

Age (posthatching days)

LS (mm)

30 Maximum = 55 Minimum = 23 Mean ± s.d. = 37 ± 10 30 Maximum = 53 Minimum = 21 Mean ± s.d. = 37 ± 9

Maximum = 149 Minimum = 70 Mean ± s.d. = 109 ± 27 Maximum = 157 Minimum = 61 Mean ± s.d. = 116 ± 25

Sr:Ca (×103 ) (mass %) mean ± s.d. Core: 7⋅8 ± 1⋅5 Edge: 6⋅3 ± 1⋅0 Core: 7⋅8 ± 1⋅6 Edge: 9⋅5 ± 0⋅9

High resolution life-history scans of Sr:Ca ratios in the otoliths from core to edge allowed several types of residency patterns to be distinguished. Four patterns of fish movement were recorded in the C. parallelus individuals caught in PEC (Fig. 4). The observed number of patterns depends, however, on how fine a detail is put on them, but observed Sr:Ca ratios profiles were grouped to minimize the existing number of profile patterns without losing relevant information. Some patterns may, however, exist in the same catchment site. Twenty individuals caught in PEC showed consistently medium values of Sr:Ca ratios in the core increasing until 30–40 days post-hatching (brackish water), followed by high and constant Sr:Ca ratios throughout their remaining life history (salt water) (marine migrant juveniles), sometimes with rare and quick incursions into mesohaline waters (Fig. 4; type 1). The other 10 individuals showed consistently high Sr:Ca ratios (salt water) through the otolith ratio from core to edge (marine resident juveniles), some with quick incursions into mesohaline water (marine resident juveniles with occasional brackish water entry) (Fig. 4; type 2). These two kinds of Sr:Ca profiles were only recorded in individuals caught in Tromomó (66 and 33% for types 1 and 2, respectively). Eighteen of the individuals caught at Guaraguaçu remained in mesohaline waters through their life (brackish resident juveniles), although some fish had a transitory entry in oligohaline waters around 30–50 days post-hatching (brackish resident juveniles with occasional freshwater entry) (Fig. 4; type 3). The other remaining 12 individuals had high Sr:Ca ratios in the otoliths core, after which they had medium and constant Sr:Ca ratios values throughout their remaining life history (brackish migrant juveniles). Some of these fish, however, had a brief incursion into oligohaline waters (downstream migrant juveniles) (Fig. 4; type 4). These last two Sr:Ca profiles were only recorded in individuals caught in Guaraguaçu (60 and 40% for types 3 and 4, respectively). The primary increment width pattern through the otolith radius showed a similar general pattern for all individuals. There was an abrupt increase of primary increment widths from the larval hatching until 20 days of age, remaining relatively constant (c. 1⋅8 μm) until 60 days, after which the increment width starts to decrease. Tromomó individuals showed, however, a slightly higher otolith growth rate from 60 days (Fig. 5).

2 0

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Fig. 4. Otolith transects of types of residency patterns of Centropomus parallelus from the core to the edge. (a)Tromomó type 1, (b) Tromomó type 2, (c) Guaraguaçu type 3 and (d) Guaraguaçu type 4. , the mean values from the individual profiles ( ).

Age (days)

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Otolith primary increments width ( m)

1·80 1·60 1·40 1·20 1·00 0·80 0·60 0·40 0·20 0·00 5 10 15 20 25 30 35 40 45 50 55 60 65 70 75 80 85 90 95 100 105 110 115 120 125 130 135 140 145 150 155

Age (days post-hatching)

Fig. 5. Profile of mean otolith increment widths for the Centropomus parallelus individuals collected in Tromomó ( ) and Guaraguaçu ( ).

DISCUSSION Recent studies of habitat use by C. parallelus juveniles in estuarine environments suggest a meso-oligohaline habitat preference for the species (Aliaume et al., 1997; Itagaki, 2005; Chaves & Nogueira, 2013) and the Sr:Ca ratios in juvenile C. parallelus from PEC are within the range of values reported for other estuarine fish species (Chang et al., 2004; Diouf et al.; 2006; Yang et al., 2011). This study showed that, based on the Sr:Ca ratios in the otoliths, that juvenile C. parallelus have a high environmental plasticity in terms of habitat, salinity, residence and movement. This behaviour was expected, based on the frequent records of C. parallelus individuals in areas of different salinities within the PEC (Felix et al., 2007; Contente et al., 2011; Vitule et al., 2013). Furthermore, laboratory experiments showed that growth and survival of individuals were not significantly affected by salinity shifts (Tsuzuki et al., 2007; Sterzelecki et al., 2013). Similar conclusions were reached for Centropomus nigrescens Günther 1864 (Nonell, 1995) Backcalculation estimates from daily increments recorded in the otoliths indicate that C. parallelus has a protracted spawning season from May to January, with a peak between October and January (spring and summer). Two spawning seasons have been already observed in the Cananéia (Itagaki, 2005) and Guaratuba Bays (Chaves & Nogueira, 2013) in spring and autumn, and late summer and early autumn respectively. It seems that even over short distances (c. 100 km), i.e. between nearby estuaries, the C. parallelus reproductive period could differ. Similar behaviour was observed for common snook Centropomus undecimalis (Bloch 1792), which showed a long reproductive season (April to December or January) including multiple spawnings

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(Peters et al., 1998). A protracted spawning period from September to November has also been recorded for blackfin snook Centropomus medius Günther 1864 (Maldonado-García et al., 2005). This reproductive plasticity within the genus could be related to environmental conditions, such as tidal cycles, rain regimes and drainage areas (Gilmore et al., 1983; Tucker & Campbell, 1988; Tilmant et al., 1989). This could favour the larval dispersion of eggs, larvae and early juveniles from the nearby nurseries areas (Itagaki, 2005), allowing low levels of competition, a reduction of the risk of predation and increased food availability. The Sr:Ca ratios in the otolith cores of C. parallelus, which represent the natal origin of the fish, suggest that spawning occurs preferentially in a mesohaline environment, although spawning in salt water was also observed. Due to the large area of the PEC, with the existence of several mesohaline environments, (Noernberg et al., 2006), it is difficult to pinpoint precise spawning grounds, but some studies indicate that spawning occurs near the mouths of the rivers, probably within estuarine systems (Seaman & Collins, 1983; Della-Patrona, 1984; Itagaki, 2005). The spatial proximity between the spawning and the nurseries areas in C. parallelus could be advantageous by decreasing the larval dispersion time and the settlement period, which in turn may reduce predation risk (Itagaki, 2005). Several experiments for aquaculture purposes showed that C. parallelus juveniles can grow and survive in salinities from 0 to 35 (Tsuzuki et al., 2007; Sterzelecki et al., 2013). Although a higher food uptake efficiency was observed at low salinities (5) (Rocha et al., 2005), a more successful larval hatching rate and fish development was recorded at higher salinities (30–35) (Araujo & Cerqueira, 2005). The somatic growth rate inferred from the daily otolith increment width profiles suggest a high fish growth rate until 20 days of age (first phase), followed by a constant growth rate until 60 days (second phase) and thereafter a decreasing growth rate until the moment of fish capture (third phase). Moreover, it can be assumed that the first, second and third stages of the otolith increment widths profile could be related to known early life-history traits, such as larval developmental phase (including the larval hatching and the first exogenous feeding), metamorphosis and settlement, and the beginning of the juvenile stage, respectively (Itagaki, 2005). The fact that Guaraguaçu and Tromomó individuals have a higher growth rate in the second and third stages, respectively, may be related to salinity. A better food uptake (important after the absorption of the yolk sac) and fish development (onset of the juvenile stage) occur at low and high salinities, respectively (Araujo & Cerqueira, 2005; Rocha et al., 2005). Beside the effect of salinity, other exogenous factors, such as temperature and food availability, cannot be excluded. Unfortunately, there are no historical data on salinity, temperature and Sr concentration in PEC, but the two sites where fish were collected revealed different local water mass characteristics. Salinity values were within the accepted range for oligohaline (Guaraguaçu) and mesohaline (Tromomó) environments (Bald et al., 2005). Water Sr content was also higher for the mesohaline site (Tromomó). This means that the observed variation in the Sr:Ca ratios in otoliths of C. parallelus juveniles should represent different patterns of use of the estuarine gradient, movements among locations and different spawning grounds. Furthermore, it is accepted that although early juveniles of the Centropomidae have some kind of site fidelity after the post-larval settlement, they perform short migrations (Itagaki, 2005; Barbour & Adams, 2012).

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The fact that fish from Guaraguaçu have more individual Sr:Ca ratios profiles than Tromomó individuals can probably be associated with different hydrological conditions at the collection sites. It is well known that the variation of salinity in the lower estuary (Guaraguaçu) is higher due to rain and tidal regimes (Contente et al., 2011). On the other hand, Tromomó is located in the mouth of the Serra Negra River, on the border of the Benitido sub-estuary, where the salinity is more related to tidal cycles, and less to freshwater outflow (Noernberg, 2001). Tromomó is a more stable and homogeneous water environment in terms of salinity, but the salinity changes experienced by the individuals of type 1, from meso- to polyhaline waters, and from poly- to mesohaline in type 4, are coincidental with the age of larval settlement (18 days according to Itagaki, 2005). Individuals of types 3 and 4 also show a punctual incursion into oligohaline waters. These occasional freshwater incursions are coincidental with the transition from larval to juvenile stage (40–56 days in the laboratory and wild environments, respectively, according to Alvarez-Lajonchère et al., 2002 and Itagaki, 2005), but could also result from a local rainfall episode. Other individuals, however, belonging to types 2 and 3, appear to have passed their entire life cycle, from birth until capture, in seawater and brackish waters. The high plasticity of C. parallelus could allow higher survival rates since the swimming systems of the larvae and post-larvae are not fully developed and they passively drift on water currents during their early life history. Also, the possibility that the fish migration patterns observed here may also reflect residency in a variable environment, cannot at present be excluded, and needs further investigation. Amphidromous fishes, such as C. parallelus, are highly susceptible to loss of migratory corridors, habitat degradation and exotic species introductions. The present results show that C. parallelus could occupy and migrate between different salinity habitats within the Paranaguá estuarine complex. Although showing a high environmental plasticity and adaptation, for a species that ranges widely among freshwater, estuarine and marine environments, the maintenance of connectivity could be particularly important. The present data suggest that this species is quite flexible in its life history and quite resilient to such effects, at least during the juvenile stage. Loss of connectivity (e.g. dam construction), however, can disrupt contributions to the larval pool and post-larval recruitment, while also reducing stream habitat required for reproduction (Walter et al., 2012). More studies, particularly of adult fishes, using environmental data and otolith microchemistry, are needed to measure migratory patterns and habitat utilization in this species. This research was supported by the CNPq (National Council of Technological and Scientific Development – 473181/2012-6 and 401190/2014-5) and by the Strategic Funding UID/Multi/04423/2013 through national funds provided by FCT – Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the programme PT2020. F.A.D. benefited from a Brazilian PhD Grant (CAPES – BEX 1906/13-5). A special thanks to the two anonymous referees for their suggestions and comments, which allowed us to improve an earlier draft of this manuscript.

References Able, K. W. (2005). A re-examination of fish estuarine dependence: evidence for connectivity between estuarine and ocean habitats. Estuarine, Coastal and Shelf Science 64, 5–17. Aliaume, C., Zerbi, A. & Miller, J. M. (1997). Nursery habitat and diet of juvenile Centropomus species in Puerto Rico estuaries. Gulf of Mexico Science 15, 77–87.

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Alvarez-Lajonchère, L. & Tsuzuki, M. Y. (2008). A review of methods for Centropomus spp. (Snooks) aquaculture and recommendations for the establishment of their culture in Latin America. Aquaculture Research 39, 684–700. Alvarez-Lajonchère, L., Cerqueira, V. R. & Reis, M. (2002). Desarrollo embrionario y primeros estadios larvales del robalo chucumite, Centropomus parallelus Poey (Pisces, Centropomidae) con interés para su cultivo. Hidrobiológica 12, 89–100. Araujo, J. & Cerqueira, V. R. (2005). Influência da salinidade na incubação de ovos do robalo-peva (Centropomus parallelus Poey, 1860). Acta Scientiarum Biological Sciences 27, 85–89. Bald, J., Borja, A., Muxika, I., Franco, J. & Valencia, V. (2005). Assessing reference conditions and physico-chemical status according to the European Water Framework Directive: a case-study from the Basque Country (Northern Spain). Marine Pollution Bulletin 50, 1508–1522. Barbour, A. B. & Adams, A. J. (2012). Biologging to examine multiple life stages of an estuarine-dependent fish. Marine Ecology Progress Series 457, 241–250. Campana, S. E., Chouinard, G. A., Hanson, J. M. & Frechet, A. (1999). Mixing and migration of overwintering Atlantic cod (Gadus morhua) stocks near the mouth of Gulf of St. Lawrence. Canadian Journal of Fisheries and Aquatic Sciences 56, 1873–1881. Campana, S. E., Chouinard, G. A., Hanson, J. M., Frechet, A. & Brattey, J. (2000). Otolith elemental fingerprints as biological tracers of fish stocks. Fisheries Research 46, 343–357. Cerqueira, V. R. & Tsuzuki, M. Y. (2009). A review of spawning induction, larviculture, and juvenile rearing of the fat snook, Centropomus parallelus. Fish Physiology and Biochemistry 35, 17–28. Chang, C. W., Iizuka, Y. & Tzeng, W. N. (2004). Migratory environmental history of the grey mullet Mugil cephalus a revealed by otoliths Sr:Ca ratios. Marine Ecology Progress Series 268, 277–288. Chaves, P. T. & Nogueira, A. B. (2013). Influência da salinidade no crescimento e relação peso-comprimento do robalo-peva. Boletim do Instituto da Pesca 39, 423–432. Contente, R. F., Stefanoni, M. F. & Spach, H. L. (2011). Fish assemblage structure in an estuary of the Atlantic Forest biodiversity hotspot (southern Brazil). Ichthyological Research 58, 38–50. Corrêa, C. F. & Cerqueira, V. R. (2009). Densidade de estocagem para juvenis de robalo-peva após a larvicultura. Boletim do Instituto da Pesca 34, 571–576. Corrêa, M. & Uieda, V. (2007). Diet of the ichthyofauna associated with marginal vegetation of a mangrove forest in southeastern Brazil. Iheringia Série Zoologia 97, 486–497. Della-Patrona, L. (1984). Contribution à la biologie du robalo Centropomus parallelus (Pisces Centropomidae) du sud-est du Brésil: possibilities aquacoles. PhD Thesis, Institut National Polythecnique de Tolouse, Tolouse, France. Diouf, K., Panfili, J., Labonne, M., Aliaume, C., Tomás, J. & Chi, T. D. (2006). Effects of salinity on strontium:calcium ratios in the otoliths of the West African black-chinned tilapia Sarothrodon melanotheron in a hypersaline estuary. Environmental Biology of Fishes 77, 9–20. Elsdon, T. S. & Gillanders, B. M. (2006). Identifying migratory contingents of fish by combining otolith Sr:Ca with temporal collections of ambient Sr:Ca concentrations. Journal of Fish Biology 69, 643–657. Felix, F. C., Spach, H. L., Moro, P. S., Schwarz-Jr, R., Santos, C., Hackradt, C. W. & Hostim-Silva, M. (2007). Utilization patterns of surf zone inhabiting fish from beaches in Southern Brazil. Pan-American Journal of Aquatic Sciences 2, 27–39. Feltrin-Contente, R., Freitas-Stefanoni, M. & Gadig, O. (2009). Size-related shifts in dietary composition of Centropomus parallelus (Perciformes: Centropomidae) in an estuarine ecosystem of the southeastern coast of Brazil. Journal of Applied Ichthyology 25, 335–342. Fortes, W. L. S., Pedro, H., Almeida-Silva, P. H., Prestrelo, L. & Monteiro-Neto, C. (2014). Patterns of fish and crustacean community structure in a coastal lagoon system, Rio de Janeiro, Brazil. Marine Biology Research 2, 111–122.

R E S I D E N C Y A N D M O V E M E N T S O F C E N T R O P O M U S PA R A L L E L U S

Gilmore, R. G., Donahoe, C. J. & Cooke, D. W. (1983). Observations on the distribution and biology of the common snook, Centropomus undecimalis (Bloch). Florida Scientist 46, 313–336. Harrison, T. D. & Whitfield, A. K. (2006). Temperature and salinity as primary determinants influencing the biogeography of fishes in South African estuaries. Estuarine, Coastal and Shelf Science 66, 335–345. Hedger, R. D., Atkinson, P. M., Thibault, I. & Dodson, J. J. (2008). A quantitative approach for classifying fish otolith strontium: calcium sequences into environmental histories. Ecological Informatics 3, 207–217. Heupel, M. R. & Simpendorfer, C. A. (2008). Movement and distribution of young bull sharks Carcharhinus leucas in a variable estuarine environment. Aquatic Biology 1, 277–289. Itagaki, M. K. (2005). Potencial de recrutamento das larvas e juvenis de robalo-peva, Centropomus parallelus (Teleostei: Centropomidae), no Sistema Cananéia-Iguape, São Paulo, Brasil. PhD Thesis, Universida de São Paulo, São Paulo, Brazil. Knoppers, B. A., Brandini, F. P. & Thamm, C. A. (1987). Ecological studies in the Bay of Paranaguá. II. Some physical and chemical characteristics. Nerítica 2, 1–36. Kraus, R. T. & Secor, D. H. (2004). Incorporation of strontium into otoliths of an estuarine fish. Journal of Experimental Marine Biology and Ecology 302, 85–106. Lana, P. C., Marone, E., Lopes, R. M. & Machado, E. C. (2001). The subtropical estuarine complex of Paranaguá Bay, Brazil. In Coastal Marine Ecosystems of Latin America (Seeliger, U. & Kjerfve, B., eds). Berlin: Springer-Verlag. Liu, H., Jiang, T., Huang, H., Shen, X., Zhu, J. & Yang, J. (2014). Estuarine dependency in Collichthys lucidus of the Yangtze River Estuary as revealed by the environmental signature of otolith strontium and calcium. Environmental Biology of Fishes 98, 165–172. doi: 10.1007/s10641-014-0246-7 Mai, A. C. G., Condini, M. V., Albuquerque, C. Q., Loebmann, D., Saint’Pierre, T. D., Miekeley, N. & Vieira, J. P. (2014). High plasticity in habitat use of Lycengraulis grossidens (Clupeiformes, Engraulidae). Estuarine, Coastal and Shelf Science 141, 17–25. Maldonado-García, M., Gracia-López, V., Carrillo, M., Hernández-Herrera, A. & RodríguezJaramillo, C. (2005). Stages of gonad development during the reproductive cycle of the blackfin snook, Centropomus medius Günther. Aquaculture Research 36, 554–563. Marshall, S. & Elliott, M. (1998). Environmental influences on the fish assemblage of the Humber Estuary, UK. Estuarine, Coastal and Shelf Science 46, 175–184. McDowall, R. M. (1992). Particular problems for the conservation of diadromous fish. Aquatic Conservation: Marine and Freshwater Ecosystems 2, 351–355. Mendonça, J. T. & Katsuragawa, M. (2001). Caracterização da pesca artesanal no complexo estuarino-lagunar de Cananéia- Iguape, SP, Brasil (1995–1996). Acta Scientiarum Maringá 23, 535–547. Noernberg, M. A. (2001). Processos morfodinâmicos no complexo estuarino de Paranaguá, Paraná, Brasil: um estudo a partir de dados in situ e LANDSAT-TM. PhD Thesis, Universidade Federal do Paraná, Curitiba, Brazil. Noernberg, M. A., Lautert, L. F. C., Araújo, A. D., Marone, E., Angelotti, R., Netto Junior, J. P. B. & Krug, L. A. (2006). Remote sensing and GIS integration for modelling the Paranaguá Estuarine Complex - Brazil. Journal of Coastal Research 39, 1627–1631. Nonell, J. G. (1995). Growth of Pacific snook (Centropomus nigrescens) juveniles at different salinities. Uniciência 12, 35–38. Passos, A. C., Contente, R. F., Abbatepaulo, F. V., Spach, H. L., Vilar, C., Joyeux, J. C., Cartagena, B. F. C. & Fávaro, L. F. (2013). Analysis of fish assemblages in sectors along a salinity gradient based on species, families and functional groups. Brazilian Journal of Oceanography 61, 251–264. Peters, K. M., Matheson, R. E. & Taylor, R. G. (1998). Reproduction and early life history of common snook, Centropomus undecimalis (Bloch), in Florida. Bulletin of Marine Science 62, 509–529. Prodocimo, V., Tscha, M. K., Pie, M. R., Oliveira-Neto, I. F., Ostrensky, A. & Boeger, W. A. (2008). Lack of genetic differentiation in the fat snook Centropomus parallelus

F. A . D A R O S E T A L.

(Teleostei: Centropomidae) along the Brazilian coast. Journal of Fish Biology 73, 2075–2082. Riede, K. (2004). Global Register of Migratory Species - From Global to Regional Scales. Bonn: Federal Agency for Nature Conservation. Rivas, L. R. (1986). Systematic review of the perciform fishes of the genus Centropomus. Copeia 1986, 579–611. Rocha, A. J. S., Gomes, V. G., Ngan, P. V., Passos, M. J. A. C. R. & Furia, R. R. (2005). Metabolic demand and growth of juveniles of Centropomus parallelus as function of salinity. Journal of Experimental Marine Biology and Ecology 316, 157–165. Rocha, A., Gomes, V., Ngan, P., Passos, M. & Furia, R. (2007). Effects of anionic surfactant and salinity on the bioenergetics of juveniles of Centropomus parallelus (Poey). Ecotoxicology and Environmental Safety 68, 397–404. Secor, D. H. & Rooker, J. R. (2000). Is otoliths strontium a useful scalar of lifecycles in estuarine fishes. Fisheries Research 46, 359–371. Selleslagh, J. & Amara, R. (2008). Environmental factors structuring fish composition and assemblages in a small macrotidal estuary (eastern English Channel). Estuarine, Coastal and Shelf Science 79, 507–517. SEMA (2009). Resolução no. 016/2009. Secretaria de Meio Ambiente do Estado do Paraná. Curitiba: Estado do Paraná. Silvano, R., MacCord, P., Lima, R. & Begossi, A. (2006). When does this fish spawn? Fishermen’s local knowledge of migration and reproduction of Brazilian coastal fishes. Environmental Biology of Fishes 76, 371–386. Spach, H. L., Godefroid, R. S., Santos, C., Schwarz-Jr, R. & Queiroz, G. M. L. N. (2004). Temporal variation in fish assemblage composition on a tidal flat. Brazilian Journal of Oceanography 52, 47–58. Sterzelecki, F. C., Rodrigues, E., Fanta, E. & Ribeiro, C. A. O. (2013). The effect of salinity on osmoregulation and development of the juvenile fat snook, Centropomus parallelus (Poey). Brazilian Journal of Biology 13, 609–615. Suzuki, K., Yoshitomi, T., Kawaguchi, Y., Ichimura, M., Edo, K. & Otake, T. (2011). Migration history of Sakhalin taimen Hucho perryi captured in the Sea of Okhotsk, northern Japan, using otoliths Sr:Ca ratios. Fisheries Science 77, 313–320. Tabouret, H., Bareille, G., Claverie, F., Pecheyran, C., Prouzet, P. & Donard, O. F. X. (2010). Simultaneous use of strontium:calcium and barium:calcium ratios in otoliths as markers of habitat: application to the European eel (Anguilla anguilla) in the Adour basin, South West France. Marine Environmental Research 70, 35–45. Tilmant, J. T., Rutherford, E. S. & Thue, E. B. (1989). Fishery harvest and population dynamics of the common snook (Centropomus undecimalis) from Florida bay and adjacent waters. Bulletin of Marine Science 44, 523–524. Trotter, A. A., Blewett, D. A., Taylor, R. G. & Stevens, P. W. (2012). Migrations of common snook from a tidal river with implications for skipped spawning. Transactions of the American Fisheries Society 141, 1016–1025. Tsuzuki, M. Y., Cerqueira, V. R., Teles, A. & Doneda, S. (2007). Salinity tolerance of laboratory reared juveniles of the fat snook Centropomus parallelus. Brazilian Journal of Oceanography 55, 1–5. Tucker, J. W. Jr. & Campbell, S. W. (1988). Spawning season of common snook along the east central Florida coast. Florida Scientist 51, 1–6. Tyler, R. M., Brady, D. C. & Targett, T. E. (2009). Temporal and spatial dynamics of diel-cycling hypoxia in estuarine tributaries. Estuaries and Coasts 32, 123–145. Tzeng, W. N., Chang, C. W., Wang, C. H., Shiao, J. C., Iizuka, Y., Yang, Y. J., You, C. F. & Lozyz, L. (2007). Misidentification of the migratory history of anguillid eels by Sr/Ca ratios of vaterite otoliths. Marine Ecology Progress Series 348, 285–295. Vitule, J. R. S., Silva, F. F. G. S., Bornatowski, H. & Abilhoa, V. (2013). Feeding ecology of fish in a coastal river of the Atlantic Rain Forest. Environmental Biology of Fishes 96, 1029–1044. Walter, R. P., Hogan, J. D., Blum, M. J., Gagne, R. B., Hain, E. F., Gilliam, J. F. & McIntyre, P. B. (2012). Climate change and conservation of endemic amphidromous fishes in Hawaiian streams. Endangered Species Research 16, 261–272.

R E S I D E N C Y A N D M O V E M E N T S O F C E N T R O P O M U S PA R A L L E L U S

Yang, J., Jiang, T. & Liu, H. (2011). Are there habitat salinity markers of the Sr:Ca ratio in the otoliths of wild diadromous fishes? A literature survey. Ichthyological Research 58, 291–294.

Electronic Reference Seaman, W. Jr. & Collins, M. (1983). Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (South Florida) – snook. U.S. Fish & Wildlife Service FWS/OBS-82/11.16. U.S. Army Corps of Engineer, TR EL-82-4, 1–16. Available at www.nwrc.usgs.gov/publications/specnumber.htm