Use of otolith elemental signatures to unravel lifetime movement patterns of Atlantic spadefish, Chaetodipterus faber, in the Southwest Atlantic Ocean

Journal Pre-proof Use of otolith elemental signatures to unravel lifetime movement patterns of Atlantic spadefish, Chaetodipterus faber, in the Southwest Atlantic Ocean

Marcelo Soeth, Henry Louis Spach, Felippe Alexandre Daros, Jorge Pisonero Castro, Alberto Teodorico Correia PII:

S1385-1101(19)30283-7

DOI:

https://doi.org/10.1016/j.seares.2020.101873

Reference:

SEARES 101873

To appear in:

Journal of Sea Research

Received date:

4 October 2019

Revised date:

19 January 2020

Accepted date:

23 February 2020

Please cite this article as: M. Soeth, H.L. Spach, F.A. Daros, et al., Use of otolith elemental signatures to unravel lifetime movement patterns of Atlantic spadefish, Chaetodipterus faber, in the Southwest Atlantic Ocean, Journal of Sea Research (2020), https://doi.org/ 10.1016/j.seares.2020.101873

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© 2020 Published by Elsevier.

Journal Pre-proof

Use of otolith elemental signatures to unravel lifetime movement patterns of Atlantic spadefish, Chaetodipterus faber, in the Southwest Atlantic Ocean Marcelo Soetha,b,c , Henry Louis Spachc , Felippe Alexandre Darosd, Jorge Pisonero Castroe, Alberto Teodorico Correiab,f,* a

Programa de Pós-Graduação em Sistemas Costeiros e Oceânicos, Universidade

b

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Federal do Paraná, P.O 61, 83255-976, Pontal do Paraná, PR, Brazil. Centro Interdisciplinar de Investigação Marinha e Ambiental, Terminal de

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Cruzeiros do Porto de Leixões, Avenida General Norton de Matos S/N, 4450-208,

Laboratório de Ecologia de Peixes, Centro de Estudos do Mar, Universidade

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c

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Matosinhos, Portugal.

d

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Federal do Paraná, P.O 61, 83255-976, Pontal do Paraná, PR, Brazil. Universidade Estadual Paulista Julio de Mesquita Filho, Campus Experimental de

Department of Physics, Faculty of Science, University of Oviedo, Federico Garcia

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e

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Registro, 11900-000, Registro, SP, Brazil.

Lorca nº18, 33007, Oviedo,Spain. f

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Faculdade de Ciências da Saúde da Universidade Fernando Pessoa, Rua Carlos

Maia 296, 4200-150, Porto, Portugal. *

Corresponding author at: Centro Interdisciplinar de Investigação Marinha e

Ambiental (CIIMAR/CIMAR), Terminal de Cruzeiros do Porto de Leixões, Avenida General Norton de Matos S/N, 4450-208 Matosinhos, Portugal. E-mail address: [email protected] (A.T. Correia). ABSTRACT

Journal Pre-proof Otolith fingerprinting was used to test the hypotheses that estuarine systems are effective juvenile habitats for Chaetodipterus faber in the Southwest Atlantic Ocean, and that this species displays seasonal migrations between estuarine and marine environments. Adult C. faber were collected in euhaline environments from five Brazilian states (Espírito Santo, Rio de Janeiro, São Paulo, Paraná, and Santa Catarina) and otolith elemental ratios (Sr/Ca, Ba/Ca and Mn/Ca) were recorded

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from the core to otolith edge. The otolith Sr/Ca pattern demonstrated that most fish

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(95%) spend the first year of life within estuaries, but then move toward seawater;

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migrations between estuarine and marine environments appear not to occur after

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estuarine egress. Evidence of marine residence throughout life was found in only 5% of individuals. Moreover, the general otolith Sr/Ca pattern indicated that

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spawning occurs mainly in coastal waters adjacent to estuaries. Additionally, otolith

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element/Ca ratios suggest that adult C. faber display seasonal migrations between inshore and offshore waters, which corroborate with monthly fishery C. faber

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landings. This finding implies that artisanal and industrial fisheries require a shared

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quota. The inferential scope of seasonal movements was sometimes limited by the lack of water chemistry data and unknown relative effects of environmental and physiological factors. Thus additional research is required to evaluate the connectivity

between

environments,

a

pre-requisite

for

effective

fisheries

conservation and management of C. faber. Keywords: Ephippidae; SW Atlantic, otolith microchemistry; laser ablation; salinity migratory behavior. 1.

Introduction

Journal Pre-proof A robust description of reef-associated fish movements in the wild has always been a challenge in seascape ecology. It has proved difficult because reefassociated species commonly reside in high-diversity systems and complex seascapes, where population dynamics are inherently linked to connectivity occurring over spatial and temporal scales (Elliott et al., 2007; Mumby and Hastings, 2008; Rooker et al., 2018). A broad spectrum of reef-associated fishes

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uses estuarine habitats during the juvenile stage and then migrate seaward to reef

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habitats as young adults (Hamer et al., 2006; Elliott et al., 2007; Aschenbrenner et

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al., 2016). Not all fishes are dependent on specific nursery grounds; instead they

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are able to utilize a wide variety of estuarine and marine environments (Whitfield and Pattrick, 2015). Effective juvenile habitat (EJH) for a particular species results

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in a greater proportion of individuals to the replenishing of the adult population

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compared to the mean level contributed by all habitats used by juveniles (Dahlgren et al., 2006). A variety of methods has been used to determine EJH, including

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distribution, abundance and size structure, artificial tags, stable isotopes and otolith

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elemental signatures (Gillanders et al., 2003). Among these methods, otolith elemental signatures offer a direct measure of EJH (Dahlgren et al., 2006), providing high resolution of temporal and spatial fish movements (Albuquerque et al., 2012; Correia et al., 2014; Avigliano et al., 2017). Otoliths are considered to be metabolically inert structures that grow continuously in fish throughout life, accreting trace elements from the aquatic environment (Campana and Thorrold, 2001). Some elements, such as strontium (Sr) and barium (Ba), display high correlations between environmental and otolith concentration (Bath et al., 2000; Tabouret et al., 2010; Webb et al., 2012).

Journal Pre-proof Manganese (Mn) has been included in studies as an environmental indicator, particularly of estuarine habitats (Hanson et al., 2004; Laugier et al., 2015; Aschenbrenner et al., 2016). While Mn water concentrations tend to decrease with distance from coastlines, Sr shows an inverse pattern increasing with the transition from freshwater to marine waters (Thomas and Bendell-Young, 1999; Hanson et al., 2004; Elsdon et al., 2008; Laugier et al., 2015). However, in addition to properties

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the

surrounding

aquatic

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physical-chemical

environment,

the

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incorporation of different elements into otoliths is influenced by multiple factors

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(i.e., genetic, physiological, and diet) and the effect of salinity on otolith chemistry

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requires careful consideration (Webb et al., 2012; Sturrock et al., 2015; Izzo et al., 2018).

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The Atlantic spadefish Chaetodipterus faber (Broussonet 1782) is a reef-

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associated fish, distributed along the tropical and subtropical western Atlantic Ocean, encompassing the Caribbean Sea and Gulf Mexico (Burgess, 2002;

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Machado et al., 2017; Soeth et al., 2019b). Adult C. faber are benthopelagic and

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frequently observed in reef environments down to depths of 30-40 meters (Hayse, 1990; Burgess, 2002; Soeth et al., 2019a). The presence of large-size C. faber within or nearby estuaries in the warm season appears to be related to reproduction (Soeth et al., 2019a). Early life stages of C. faber have been collected mainly inside or at the entrance to bays and estuarine systems (Ditty et al., 1994; De Castro et al., 2005; Burghart et al., 2014), and early juveniles are notably abundant in these regions (Hayse, 1990; Possatto et al., 2016; Soeth et al., 2019a). However, the contribution of estuary habitats as nurseries remains unknown for this species.

Journal Pre-proof Chaetodipterus faber is particularly important to artisanal fisheries operating in estuarine and coastal inshore areas of Brazil (PMAP-BS, 2017a, b), but in the past decade landings for offshore industrial C. faber fisheries increased by 6 times (PMAP-SC, 2018). With a poorly understood migratory behavior (Machado et al., 2017; Soeth et al., 2019b), the understanding of C. faber population dynamics relies on fishing and abundance data. However, a clear understanding of C. faber

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movement patterns is critical to management of inshore and offshore fisheries.

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Therefore, otolith elemental fingerprints were hereby used as natural tags to test

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the hypothesis that estuarine systems are effective juvenile habitats for the C.

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faber across Southwest Atlantic Ocean, and that this species displays seasonal

Material and Methods

2.1

Biological sampling

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migrations between estuarine and marine environments.

Fish sampling was conducted in euhaline coastal environments of Southeast

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and South Brazil, including Espírito Santo (ES), Rio de Janeiro (RJ), São Paulo

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(SP), Paraná (PR), and Santa Catarina (SC) states (Fig. 1). Further details about the study area was reported by Soeth et al. (2019b). In brief, a total of 75 individuals (15 per site) were collected between December 2015 and March 2016 by spearfishing or from artisanal fishermen. Upon collection or immediately after landing, fish were preserved on ice and processed in the laboratory. The individuals were measured for total length (TL, 1 mm), and sagittal otoliths were removed and stored using established protocols (Soeth et al., 2019b).

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Figure 1. Map of South America (top left) and the Brazilian coast (A) showing

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(circles) where samples were collected. Rectangles (dashed lines) indicate Chaetodipterus faber sampling collection sites; Espírito Santo (B), Rio de Janeiro (C), São Paulo (D), Paraná (E), and Santa Catarina (F). 2.2.

Age determination and microchemical analysis Left otoliths were embedded in transparent epoxy resin (Buehler, Epothin),

and thereafter a transverse cross section (0.5 mm) was take out preserving the core region using a precision diamond saw (Buehler, Isomet Low-speed Saw). Slices were ground with abrasive grinding papers of 800, 1200 and 2400 grit (Buehler, Ø 200 mm SiC Paper) to expose the primordium, and further polished

Journal Pre-proof with 6, 3, and 1 μm diamond pastes (Buehler, Metadi II,) (Correia et al., 2012). Age estimation of transverse otolith sections was made using an established protocol for C. faber (Davies et al., 2015). The annual growth pattern increment deposition was recently validated by Soeth et al. (2019a). Otolith microchemistry was used in order to examine movement behaviors of the C. faber. The transverse otolith sections were attached on a glass slide with

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epoxy resin (Buehler, Epothin), cleaned in an ultrasonic bath with ultrapure water

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(Milli-Q-Water) for 5 min, and dried in a laminar flow cabinet (Correia et al., 2012,

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2014). Elemental concentrations in transverse otolith sections were measured

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using a 193-nm ArF* Excimer Laser Ablation System (Photon Machines Analyte G2) coupled to an ICP-MS Agilent 7700 (Agilent Technologies) at University of

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Oviedo, Spain. Concentrations of isotopes

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Ca,

55

Mn,

88

Sr and

138

Ba were

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transect (Fig. 2).

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determined from the core to ventral-proximal otolith edge using a continuous

Fig. 2 Transverse section from the left sagittal otolith of a five-year-old C. faber (TL = 341 mm) collected in Santa Catarina region showing the laser ablation sampling transect. The opaque zones were numbered from the otolith core (white arrow) to its proximal-ventral edge (dark arrow).

Journal Pre-proof Laser ablation settings were: spot diameter 50 µm, nominal fluence 12 J cm-2, repetition rate 10 Hz, and scan speed 10 µm s-1.

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Ca was used as internal

standard to compensates any variation in ablation yield along the laser transect improving

the

reliability of the measurements (Campana, 1999). External

calibration was performed using SRM NIST612 silicate glass (www.nist.gov) that was analyzed at the beginning and after every six otoliths (Webb et al., 2012; Sirot

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et al., 2017). Moreover, the operating conditions of the LA-ICP-MS system were

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optimized to minimize fractionation effects that might induce quantification

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uncertainties: the ratio U/Th in NIST 612 was kept below 120% in raster mode and

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the formation of oxides was controlled to be less than 0.5%. Furthermore, all the operating conditions (e.g., spot size, laser frequency, laser energy/pulse, and gas

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flow) were kept constant in both the reference material and otoliths. In order to

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avoid any surface contamination, a pre-ablation using a spot diameter of 85 µm (nominal fluence at 12 J cm-2, repetition rate 10 Hz, and scan speed 30 µm s-1)

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was run prior to the main 50 µm transects. Before each ablation, 30 seconds of

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background chemical signals were measured for each isotope in the ICP-MS with the laser switched off. The background average value of each isotope was used as a blank correction (Sirot et al., 2017). The average relative standard deviation for 20 NIST612 transects of two millimeters each was less than 5% regardless of the element.

All

isotope

data

are

given as

concentration relative

to

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Ca

(element/Calcium). Elemental ratios were converted to mmol mol–1 for Sr/Ca and to µmol

mol–1

for

Ba/Ca

and

Mn/Ca. Ablated

otolith cross-sections

were

photographed using a microscope with transmitted light coupled to a 5 megapixels Opticam (OPT5000 Power) at 40x magnification. Laser transects were measured

Journal Pre-proof using the software ImageJ (1.46r version) and ablation time was converted to distance from core to edge of otoliths (Fig. 3). 2.3

Data analyses In order to identify salinity environments and unravel lifetime movement

patterns of C. faber, the Sr/Ca ratio on the edges (the mean of the three last laser spots) of otoliths was assumed to represent the capture environment (Tabouret et

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al., 2010; Albuquerque et al., 2012; Avigliano et al., 2017). The assumption of

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positive correlation between otolith Sr/Ca and habitat salinities (Secor and Rooker,

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2000) was used to discriminate between water masses of different salinities.

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Marine waters worldwide are a large reservoir of Sr, and therefore a robust value to use as a marine end member (Banner, 2004; Seeley and Walther, 2017). The

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threshold that represents the transition between seawater (i.e., euhaline waters -

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capture environment) and estuarine water (i.e., polyhaline waters) was calculated as the mean of the otolith edge Sr/Ca ratios minus the standard deviation

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multiplied by 2 [mean – (2 * SD)], a similar approach used by Tabouret et al.

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(2010), Lin et al. (2015) and Avigliano et al. (2017).

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Figure 3. Representative laser ablation transects along the growth axis of two

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Chaetodipterus faber with chronological marks (annuli formation, vertical gray bars)

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superimposed on data. The grey dots indicate each otolith Sr/Ca ratio point value, while the solid black line with black circles and gray shading indicate the fitted

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Generalized Additive Model and 95 % Bayesian confidence intervals, respectively.

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Otolith Mn/Ca (green line) and otolith Ba/Ca (red line) profiles were square root scaled to allow resolution of variation with otolith Sr/Ca data. Horizontal blue line indicates estuarine-marine thresholds for otolith Sr/Ca ratios. Note that sample codes start with the abbreviation of each sampling region. To evaluate whether annuli formation occurs among regions at similar distances

from

core,

a

permutational

multivariate

analysis

of

variance

(PERMANOVA) was performed using PRIMER 7 v.7.0.13. Differences in element/Ca ratios averaged by age and among sampling regions were also analyzed by PERMANOVA. In those cases where poor legibility of cross-sectioned

Journal Pre-proof annuli did not allow the estimation of the fish age, the mean distance of annuli from the core was used as a proxy for the age. PERMANOVA dissimilarity matrices were based on Euclidean distance, and p-values were generated using 9999 permutations. The correlations between otolith elements/Ca ratios across sampling regions were assessed by Spearman correlation coefficient (Fowler et al., 2016; Avigliano et al., 2017).

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Sr/Ca ratio variations from the core to otolith edge of C. faber were analyzed

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by Generalized Additive Models (GAMs) implemented with the MGCV package in

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R programming language (R Development Core Team, 2017). Models were fitted

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using a Gaussian distribution (identity link) and thin-plate regression spline smoothing functions. The basis dimension (k) for the smooth [i.e., the maximum

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number of possible effective degrees of freedom (edf) allowable for a smooth term

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in the model] was defined by the empirical formula k =10N2/9 , where N is the number of data records in each profile (Kim and Gu, 2004; Brennan et al., 2015).

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Confidence intervals (95%, C.I.) to GAM and p-values were obtained by a

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Bayesian approach (Marra and Wood, 2012) and were used to determinate where and when significant shifts in the Sr/Ca ratio occurred (Brennan et al., 2015). The elemental patterns and confidence intervals (95%, C.I.) across entire C. faber otoliths were used to classify the individuals as Marine Resident (MR), Marine Migrant (MM) and Estuarine Visitor (EV). Individuals were characterized as MR when otolith Sr/Ca ratios remained at marine levels, and as MM when otolith Sr/Ca ratios remained at estuarine levels at the age-0 group and changed to otoliths Sr/Ca ratios seawater levels toward the otolith edges. Individuals for which

Journal Pre-proof the otolith Sr/Ca ratios oscillated more than once between the estuarine and marine threshold were classified as EV (Franco et al., 2019). To estimate the time at which 50% (T50) of individuals egress from estuarine to marine environments (Albuquerque et al., 2012), otolith Sr/Ca ratios were converted to binary environment determinations (0 = estuarine, 1 = marine). A bias-reduction generalized linear model with binomial responses (brglm) and logit-

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link (Kosmidis, 2014) implemented with the brglm package in R programming

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language (R Development Core Team, 2017) was used to estimate the time of

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estuarine egress. The distance from the otolith core was used as a predictor

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variable (i.e., a proxy of age). Graphics results are shown with the mean age estimated in the upper axis for better ecological interpretation. Results

3.1

Age estimates and annuli measures

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Fish TL and age estimates ranged from 272 to 475 mm and 2 to 7 years,

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respectively (Table 1). Otolith cross-sections from SC, PR, and SP were largely

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readable (100%). Poor legibility of annuli was found in RJ and ES otolith crosssections, and only 47% and 27% of otoliths respectively, were aged successfully (Table 1). Along the laser ablation transects, the first and subsequent annuli showed similar distances from the core among regions (PERMANOVA, pseudo-F = 1.56; df = 4; p > 0.05). Therefore, the distances of annuli formation from the core (mean ± S.D) for pooled regions were 0.85 ± 0.13 mm (1 st annuli), 1.30 ± 0.16 mm (2nd annuli), 1.61 ± 0.17 mm (3 rd annuli), 1.81 ± 0.20 mm (4 th annuli), 1.95 ± 0.25 mm (5th annuli), 2.07 ± 0.13 (6 th annuli), 2.11 ± 0.05 mm (7 th annuli) and 2.18 ± 0.03 mm (8th annuli).

Journal Pre-proof 3.2

Otolith elemental composition For all individuals and along the entire laser ablation transects, the Sr/Ca

ratios ranged from 2.97 mmol mol-1 to 15.54 mmol mol-1 (mean ± SD: 5.89 ± 1.65 mmol mol-1), while otolith Ba/Ca and Mn/Ca ratios ranged broader, from 3.15 µmol mol-1 to 1,420 µmol mol-1 (mean ± SD: 11.39 ± 33.30 µmol mol-1) and from 0.35 µmol mol-1 to 1,684 µmol mol-1 (mean ± SD: 11.39 ± 33.30 µmol mol-1),

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respectively (Fig. 4). Differences among regions and age were significant

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(PERMANOVA, p < 0.01) for all three otolith trace elements analyzed (Table 2).

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Estimates of components of variation showed that otolith Sr/Ca and Mn/Ca ratios

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variation were mainly explained by fish age (>45%), while sampling region explained less than 14% of the variation accounted by the PERMANOVA model.

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For otolith Ba/Ca ratios only 36% of the variation was explained by the model

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terms indicating that otolith Ba/Ca ratios could be difficult to interpret in a manner related to ontogeny. Otolith Sr/Ca ratios were negatively correlated (Spearman

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correlation, p < 0.05) with the otolith Mn/Ca ratios in all sampling regions (Table 3).

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In contrast, positive and negative correlations were found between otolith Sr/Ca and Ba/Ca ratios across sampling regions (Table 3). Table 1. Sample size (n), total length (TL), and age of Chaetodipterus faber by sampling region [Mean (±SD, standard deviation) and range (minimum and maximum)]. Region labels as in Figure 1. TL (mm) Region

ES

Age (years)

n

15

Mean±SD

Range

Mean±SD

Range

354 ± 36

320 - 475

5.0 ± 1.6

3-7

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334 ± 17

310 - 373

3.7 ± 0.5

3-7

SP

15

320 ± 24

281 - 360

3.0 ± 0.5

2-4

PR

15

397 ± 24

354 - 448

4.3 ± 0.9

3-7

SC

15

316 ± 22

272 - 345

3.8 ± 0.7

3-5

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RJ

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Figure 4. Regional and age comparisons (mean ± SE) of otolith Sr/Ca ratios (a), Ba/Ca ratios (b), and Mn/Ca ratios (c) from Chaetodipterus faber caught in five euhaline coastal areas of Southeast and South Brazil. Region labels as in Figure 1.

Journal Pre-proof Table 2. Regional and age comparisons of element/Ca ratios profiles (averaged by age) by permutational univariate analysis of variance from Chaetodipterus faber caught in coastal areas of Southeast and South Brazil. * = p < 0.01; ** = p < 0.001.

df

MS

Pseudo-F

ECV (%)

Sr/Ca

Region

4

0.28

22.84**

13.63

Age

7

1.11

91.85**

55.32

Region x Age

23

0.05

3.92**

6.98

Residual

331

0.01

4

3.2

9.19**

13.76

7

1.43

4.11*

5.1

3.54**

16.34

Region

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Age

3.3

24.07

23

1.23

Residual

331

0.35

Region

4

6.71

17.37 **

14.51

Age

7

21.45

55.53**

47.16

Region x Age

23

0.86

2.22*

4.15

Residual

331

0.39

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Region x Age

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Mn/Ca

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Ba/Ca

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Variable Source

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ECV = Estimates of components of variation.

64.81

34.19

Otolith elemental profiles The mean Sr/Ca ratio (mean ± SD) measured on the edges of otoliths from

fish captured in euhaline waters was 8.20 ± 1.50 mmol mol−1. Therefore, any otolith

Journal Pre-proof Sr/Ca ratio below 5.20 mmol mol-1 [i.e., 8.20 – (2*1.50)] was used to identify movement into estuarine environments (i.e, polyhaline waters). Table

3.

Spearman

correlations

between

otolith

element/Ca

ratios

of

Chaetodipterus faber by sampling region (labels as in Figure 1). Significant (p <

ES

RJ

SP

PR

SC

Sr/Ca vs Ba/Ca

0.411*

-0.429*

0.165*

0.541*

-0.015

Sr/Ca vs Mn/Ca

-0.441*

-0.609*

-0.483*

-0.319*

-0.595*

Mn/Ca vs Ba/Ca

0.039

0.634*

0.072*

0.268*

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Variable

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0.05) correlations are indicated by asterisk (*).

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0.163*

For all C. faber otoliths, the distance from the core was a significant

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predictor of otolith Sr/Ca ratio variation (GAM p < 0.001; Supplementary data, table

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S1). Over 25% of the profiles showed an otolith Sr/Ca ratio estuarine signature at the beginning of the profile. A smaller fraction of samples (16%) showed an otolith

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Sr/Ca ratio at the beginning of the profile indicating seawater signature, which then

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declined quickly to estuarine levels until 0.15-0.4 mm from the core. In most cases (59%), the confidence interval of otolith Sr/Ca ratios at the beginning of the profile overlapped the threshold between estuarine and marine environments (Fig. 3 and Fig. 5; Supplementary Data, Fig. S1-S5). Changes in otolith Sr/Ca ratios for fish less than 1 year-old were often between the thresholds expected for fish residing in estuarine habitats (Fig. 5). Superimposing chronological marks of otolith and fitted GAMs, the C. faber tended to exhibit the greatest changes in Sr/Ca ratios (at 95% Bayesian confidence intervals) in median and outer regions of the otoliths (>0.85 mm or >1 year-old) that were often with a regular time interval of one year (Fig. 3

Journal Pre-proof and Fig. 5). A fast increase of otolith Sr/Ca ratios was generally accompanied by a sharp decrease of otolith Mn/Ca ratios, namely in RJ and SC samples (Fig. 3 and Fig. 5). A coincident abrupt increase in otolith Sr/Ca and Ba/Ca ratios were common in outer portions of the otoliths from ES. In contrast, no expressive change was found to Mn/Ca ratios at these otolith portions. The otolith Sr/Ca ratio profiles allowed identifying two migratory patterns.

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Marine migrants (MM) were the typical life history of the C. faber from all regions,

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including 100% of the individuals from SP, PR, and SC, 93% from ES, and 80%

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from RJ. Otolith Sr/Ca ratios from MM varied significantly (at 95% C.I.) but rarely

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returned to otolith age-0 mean levels (~5 mmol mol-1) after reaching marine otolith Sr/Ca ratio levels (Fig. 5). Therefore, the estuarine visitor (EV) pattern was not

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assigned to sampled individuals. For all C. faber caught, only four individuals were

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classified as Marine resident (Fig 3 – Sample RJ10), which represented 20% and

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7% from RJ and ES samples, respectively.

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Figure 5. Otolith microchemical profiles of six Chaetodipterus faber individuals classified as Marine Migrants. Graphical legend as in Figure 3. The bias-reduction generalized linear model estimated a mean estuarine egress (T50) relative to otolith size (i.e., distance from the core) of (mean ±

Journal Pre-proof standard error) 0.71 ± 0.01 mm for pooled data, representing mean estuary

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residence of less than one year (Fig. 6).

Figure 6. Bias-reduction generalized linear model with binomial responses for the

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estimated proportion of the mean estuarine egress of Chaetodipterus faber relative to otolith size (i.e., distance from the core). Horizontal gray bar represents the otolith size when 50% of the individuals (T50) emigrate from estuarine to marine environments, which were (T50 ± standard error): 0.70 ± 0.02 mm (ES), 0.41 ± 0.02 mm (RJ), 0.89 ± 0.02 mm (SP), 0.80 ± 0.02 mm (PR), 0.74 ± 0.02 mm (SC), and 0.71 ± 0.01 mm for pooled data (Av), which represents an age close to 1 year-old. Vertical gray bars represent the mean age of the C. faber regarding the distance from the core in Southwest Atlantic Ocean.

Journal Pre-proof 4.

Discussion This study inferred migration patterns through different salinity environments

during the lifetime of Chaetodipterus faber using microchemical analyses of otoliths by LA-ICP-MS techniques. While there is no experimental validation of the relationship between salinity and otolith element/Ca ratios for C. faber or even Ephippidae fishes, the mean Sr/Ca ratio in the seawater zone of otoliths were

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comparable to values already reported for otoliths in other teleosts residing in

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marine environments in the Southwestern Atlantic Ocean (e.g., about 6 to 10 mmol

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mol-1), including Epinephelus marginatus (Condini et al., 2016), Genidens barbus

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(Avigliano et al., 2017a), Mugil liza (Callicó-Fortunato et al., 2017), Micropogonias furnieri (Franco et al., 2019) and Abudefduf saxatilis (Adelir-Alves et al., 2019).

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Interpreting the data under the hypotheses of a positive relationship between

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otolith Sr/Ca ratio and water salinity (as a proxy for water Sr/Ca ratio), the otolith Sr/Ca ratio variation within the individuals examined should represent C. faber

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inhabiting estuarine and marine environments throughout the life history (Fowler et

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al., 2016; Avigliano et al., 2017; Franco et al., 2019). In the present study, the otolith Sr/Ca ratio threshold between estuarine and marine habitats (5.20 mmol mol-1)

was

empirically

established

following

previously

published

similar

approaches used to delimitate salinities environments (Tabouret et al., 2010; Lin et al., 2015; Avigliano et al., 2017). This threshold value was slightly lower comparatively to other euryhaline species, such as 6.40 mmol mol-1 for Mugil cephalus (Fowler et al., 2016), 5.98 mmol mol-1 for G. barbus (Avigliano et al., 2017), and 6.00 mmol mol-1 for M. furnieri (Franco et al., 2019).

Journal Pre-proof Based on the resultant otolith Sr/Ca ratio signatures and bayesian confidence intervals, 95% of the individual C. faber were classified as Marine Migrant. In past decades the Fish Ecology Laboratory (FEL) from the Center of Studies of the Sea (CEM/UFPR) has investigated the fish assemblages over a complete salinity gradient (0–36) in the main coastal estuarine systems from PR and SC regions (e.g., Vilar et al., 2011; Soeth et al., 2014; Possatto et al., 2016).

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Spatial analyses of size structure and abundance of the FEL data in relation to

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water salinity indicate ontogenetic movements of C. faber, as individuals caught in

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estuarine zones were mostly demersal juveniles (mean ± SD, 56 ± 27 mm TL) and

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their presence was limited to salinities ranging from 15 to 36 (mean ± SD, 27 ± 5.2). This salinity range agrees well with aquaculture experiments that showed C.

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faber juveniles grow and survive in salinities from 15 to 35 (Senett et al., 2011).

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This spatial size structure and salinity range corroborate with elemental/Ca profiles recorded in the present study, where consistent lower otolith Sr/Ca ratios in otolith

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portions representing the early life stages of C. faber were found. In addition, the

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otolith Mn/Ca ratios showed an inverse pattern to otolith Sr/Ca ratios and supported an evidence of estuarine use encompassing the first stages of life (Hanson et al., 2004; Laugier et al., 2015; Aschenbrenner et al., 2016). Otolith Mn/Ca ratios are positively correlated with water Mn/Ca ratios (Dorval et al., 2007; Sturrock et al., 2015), being particularly high in fish otolith inhabiting estuarine environments (Hanson et al., 2004; Laugier et al., 2015; Aschenbrenner et al., 2016). Mn is rapidly precipitated in the marine environment (Thomas and BendellYoung, 1999), but trophic transfer and habitat constituents may be considered potential Mn sources to fish otoliths (Sanchez-Jerez et al., 2002). Moreover,

Journal Pre-proof maternal effects may increase the levels of near-core Mn/Ca ratios (<100 µm diameter), but outside of this otolith zone reflects ambient Mn concentrations and diet (Sanchez-Jerez et al., 2002; Brophy et al., 2004; Sturrock et al., 2015). Alternatively, Mn is available as a redox product and as such may be indicative of low-oxygen conditions (Limburg et al., 2015). Disentangling the relative effect of these factors is impossible at this point, but both Mn sources are expected to be

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incremented in regions of estuarine influence (Thomas and Bendell-Young, 1999;

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Sanchez-Jerez et al., 2002; Aschenbrenner et al., 2016).

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In the present study, otolith Ba/Ca ratios demonstrated heterogenic patterns

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and most variation was not explained by the age and region factors. Water Ba levels are associated with different sources (Elsdon el at., 2008). For instance,

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estuarine Ba water concentration can increase with terrestrial runoff (Hamer et al.,

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2006), and typically under this influence the values of water Ba/Ca and Sr/Ca ratios vary in opposite directions in relation to salinity; more notably, at estuarine regions

ur

with salinities lower than 20 (Hamer et al., 2006; Tabouret et al., 2010;

Jo

Albuquerque et al., 2012). In coastal and ocean open systems dissolved Ba and Sr variability may be attributed to upwelling of cold deep waters (Lea et al., 1989; Elsdon et al., 2008; Woodson et al., 2013). High otolith Sr/Ca and Ba/Ca ratios in oceanodromus and non-dispersing reef fish have been associated with upwelling phenomena (Kingsford et al., 2009; Wang et al., 2009; Macdonald et al., 2013). In fact, a positive relationship between otolith Sr/Ca and Ba/Ca ratios were predominant among the samples, and simultaneous increases of these element/Ca ratios were recorded in outer otolith portions. Following above arguments, this may indicate that C. faber individuals had migrated to upwelling or deep areas of the

Journal Pre-proof continental shelf; the bottom South Atlantic Central Water (SACW) intrusions in the inner- and middle-shelf during summer and spring is an event well documented in the study area (Cerda and Castro, 2014; Palóczy et al., 2016). During these seasons sea surface temperatures can be greater than 27°C but near-bottom (15– 30 m) temperatures are often lower than 20°C (Castro, 2014; Cerda and Castro, 2014). Moreover, the benthopelagic and feeding behavior of this species (Hayse,

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1990; Burgess, 2002) and its capture by trawl fisheries (mean TL around 250 mm,

ro

M. M. Rotundo, personal communication) within these latitudes and depths

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(Rotundo et al., 2019) support a hypothesis of SACW intrusions through vertical

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(deep) or horizontal (upwelling) excursions. As temperature may drive complex endogenous and exogenous interactions on Sr and Ba uptake into otoliths (Walther

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et al., 2010; Izzo et al., 2018), application of high-resolution δ18O otolith

na

measurements as a proxy for temperature (Sturrock et al., 2015) may promote a better understanding of C. faber residence within the SACW in additional studies.

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Although seascape movements can be difficult to distinguish from changing

Jo

conditions around a resident fish (Walther and Limburg, 2012; Baker et al., 2019), monthly fishery landings (PMAP-BS, 2017a,b), reproductive biology (Soeth et al., 2019a), and the hereby otolith Sr/Ca ratios suggest that C. faber display seasonal migrations. The otolith Sr/Ca ratio variation observed within a year period (Fig. 2) supports the interpretation that the fish moved between inshore (less saline) and offshore (high saline) waters, a displacement that may be associated to spawning aggregation purposes (Soeth et al., 2019a). For fisheries management, the seasonal movements recorded indicate that inshore (artisanal) and offshore (industrial) fisheries likely require a shared quota (UNIVALI/CTTMar, 2010, 2013a,

Journal Pre-proof b; PMAP-SC, 2018). This is especially important given that the landings for industrial C. faber fisheries have increased in the past decade (UNIVALI/CTTMar, 2010, 2013a, b; PMAP-SC, 2018). At present, there is no specific legislation to properly address equity in resource access and to ensure the long-term sustainability of C. faber small-scale fishing. The low levels of otolith Sr/Ca ratios at the beginning of most profiles

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suggested that fish were spawned in coastal waters adjacent to estuaries. Early life

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stages of C. faber (eggs, larvae, and newly settled) have been collected mainly

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inside or at the entrance to bays and estuarine systems (Barletta-Bergan et al.,

re

2002; De Castro et al., 2005; Burghart et al., 2014), reinforcing the hypothesis that the presence of large-sized C. faber within or nearby estuaries is related to their

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reproduction (Soeth et al., 2019a). A smaller fraction of samples showed otolith

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Sr/Ca ratio at the beginning of the profiles indicating seawater signatures, but declining quickly to estuarine levels suggesting a coastal spawning and a quick

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larval/juvenile ingress into estuaries, a common pattern in life cycles of estuarine

Jo

associated species (Secor and Rooker, 2005). Although extensive literature documenting the positive relationship between otolith Sr/Ca ratios and water Sr/Ca ratio exist (Izzo et al., 2018), some otolith Sr/Ca ratio variation could have been influenced by physiological processes (e.g., growth and gonad development) and other exogenous factors (e.g., temperature and diet) (Webb et al., 2012; Sturrock et al., 2015; Izzo et al., 2018). For example, differentiated Sr incorporation rates may occur between juveniles and adults and between winter and summer as less strontium is likely to be incorporated into otoliths during periods with higher otolith accretion rates (Sadovy and Severin,

Journal Pre-proof 1994; De Pontual et al., 2003; Stanley et al., 2015). This assumption may partially explain the close correspondence between the formation of opaque zones, mainly deposited in the spring (Soeth et al., 2019a), and observed patterns of Sr/Ca ratio drop in some individuals C. faber. In addition, the otolith Sr/Ca ratio variation could also be caused by differences in Sr availability relative to Ca availability in the adult body (i.e., blood plasma) caused by the remotion of Ca into gametes (Clarke and

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Friedland, 2004; Sturrock et al., 2015). In subtropical latitudes Brazil, the C. faber

ro

reaches sexual maturity between 100 and 150 mm TL (1 to 2 years old) and

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reproduction occurs mainly from spring through summer (Soeth et al., 2019a).

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Therefore, during the warm reproductive season, while higher otolith accretion rates are likely to drop otolith Sr/Ca ratios, gonad development could potentially

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increase its content (Kalish, 1991; Sturrock et al., 2015).

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The otolith microchemical approach used in this study provided evidence to suggest that estuarine environments are effective juvenile habitats for the C. faber

ur

in a widely latitudinal range. Coastal and highly urbanized estuaries have

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experienced high rates of mangrove loss and habitat degradation (Osland et al., 2018), which may have potential ecological consequences for this species showing a limited life cycle strategy in the first stages of life. These results also suggested that C. faber stock-recruitment projections may be largely derived from estuarine nursery areas. However, the contribution that each local population receives from distant recruitment sources is unknown and demands further studies (Soeth et al., 2019b). Otolith elemental signatures also suggest that this species performs inshore-offshore seasonal migrations. This result is an alert to C. faber fisheries management as the increasing offshore fisheries of C. faber may impact artisanal

Journal Pre-proof small-scale fisheries by reducing recruitment and stock biomass of C. faber in inshore areas. Inferential scope of seasonal movements was sometimes limited by lack of water chemistry data and unknown relative effects of environmental and physiological factors (Sturrock et al., 2015; Izzo et al., 2018). Further studies should be conducted to indicate whether environmental factors may outweigh physiological influences on otolith of the C. faber. Additionally, the application of

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high-resolution stable isotopic analysis will promote a better understanding of C.

ro

faber lifetime movements patterns.

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Acknowledgments

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We thank the Center of Studies of the Sea and the Coastal and Oceanic Systems Post-graduate Program for sampling support. A special thanks to Ana Mendez for

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LA-ICP-MS technical support at SCTs (Unidad de Ensayos Medio ambientales –

na

University of Oviedo). Financial support was provided by Araucária Foundation (Cov. 020/2015). This study was partially supported by the Strategic Funding through

ur

UID/Multi/04423/2019

national

funds

provided

by

the

Portuguese

Jo

Foundation for Science and Technology and European Regional Development Fund (PT2020). The first author was funded from a doctoral Fellowship (CAPES). Jorge

Pisonero

acknowledges

financial support from

the

Government of

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Highlights  Estuaries are effective juvenile habitats for Chaetodipterus faber  Most C. faber spend the first year of life within estuaries  Two distinct movement patterns were found for C. faber throughout lifetime  Spawning appears to occur mainly in coastal waters adjacent to estuaries  Lifetime movements evidenced that inshore-offshore fisheries require a shared quota