Age, Growth and Maturity of Red Porgy Pagrus Pagrus (Sparidae) from Southeastern Brazil P

ISSN 0032-9452, Journal of Ichthyology, 2021, Vol. 61, No. 2, pp. 230–242. © Pleiades Publishing, Ltd., 2021.

Age, Growth and Maturity of Red Porgy Pagrus pagrus (Sparidae) from Southeastern Brazil P. A . S . C o s t a a, *, A. C. Bragaa, J. M. S. Vieirab, C. E. L. Ferreirab, M. C. Barbosab, and R. R. B. São-Clementea a Universidade Federal do Estado do Rio de Janeiro (UNIRIO), Rio de Janeiro, Brazil b Universidade Federal Fluminense (UFF), Niterói, Brazil *е-mail: [email protected] Received May 22, 2020; revised May 26, 2020; accepted May 26, 2020

Abstract—Age, growth and length-at-maturity of the red porgy Pagrus pagrus were studied off the southeastern coast of Brazil. A total of 798 otoliths from specimens sampled from the hook-and-line commercial landings between January and December 2017 were used. Age and growth were estimated by counting and mea- suring increments in sectioned sagitta otoliths, and length-at-maturity was estimated based on macroscopic gonadal analysis. The annual periodicity of opaque zones was validated by marginal increment analysis. Growth curves were estimated by fitting von Bertalanffy growth model to the observed length-at-age data. Asingle annulus was laid down in summer, from November to February, associated with coastal upwelling of the subtropical South Atlantic Central Water (14.9–18.0°C) and with the onset of reproductive activity. The maximum age observed was 11 years in females and 12 years in males. The parameters of the von Bertalanffy −1 model were: males (L∞ = 419.9 mm, k = 0.347 year , t0 = – 0.199), females (L∞ = 503.8 mm, k = −1 −1 0.253 year , t0 = – 0.154) and sexes combined (L∞ = 461.0 mm, k = 0.290 year , t0 = – 0.260). The mean length and age at first maturity was estimated at 258 mm (2.5 years) for males and 274 mm (3.0 years) for females. For both sexes, maturity precedes size and age at which specimens are fully recruited to hook-and- line fisheries at age 4 (327 mm).

Keywords: age, growth, length-at-maturity, southeastern Brazil, Pagrus pagrus, red porgy DOI: 10.1134/S003294522102003X

INTRODUCTION increased ~20% annually on average (www.argen- The red porgy Pagrus pagrus (Linnaeus 1758) is a tina.gob.ar). Last landings reported for the species in protogynous sparid with an Amphi-Atlantic distribu- Brazil (2000 t) are probably underestimated tion, but also occurring in the Mediterranean Sea (https://www.icmbio.gov.br/cepsul/images/stories/ (Manooch and Hassler, 1978). It is a generalist, ben- biblioteca/download/estatistica/est_2011_bol__bra.pdf). thivorous, species usually associated with a variety of Pagrus pagrus is catch with traps and trawling in reef and sand habitats in subtropical and temperate Argentina (Lagos, 2010) and bottom trawl, hook-and- oceans (Manooch and Hassler, 1978; Labropoulou line, bottom longlines and traps in Brazil (Ávila-da- et al., 1999). The species is an important component Silva and Haimovici, 2006). of commercial and recreational fisheries in many parts In southeastern Brazilian waters (20°–23° S), of its distribution (Russell et al., 2014), while top pro- higher densities of P. pagrus in bottom-trawl samples ducers countries include Argentina (34.1%), Brazil occurred between 16.2–19.7°C (Costa et al., 2015), (22.0%), Greece (11.7%) and Turkey (10.8%) associated to seasonal upwelling of the nutrient-rich (www.tridge.com). South Atlantic Central Water (SACW) in the Cabo There are four main fishing areas of P. pagrus in the Frio region. SACW moves from offshore depths of southwestern Atlantic (SWA), including the south- 300 m to the shelf, reaching the photic zone and estab- eastern Brazil from 19° to 23° S (Costa et al., 1997), lishing a stable thermocline at depths of 10–15 m (Val- the southern Brazil between 30° and 34° S (Hai- entin, 2001). In areas of concentration of the species in movici, 1998), the Argentine–Uruguayan Common Argentina bottom temperatures range between 8.2– Fishing Zone from 34° to 39° S, and along the Argen- 17.7°C (García and Molinari, 2015). tine Economic Exclusive Zone from 39° to 42° S Contributions related to P. pagrus growth in the (García and Molinari, 2015). Pagrus pagrus landings in western Atlantic using otoliths have been presented by Argentina between 2016 (2488 t) and 2019 (4269 t) Harris and McGovern (1997), Hood and Johnson

230 AGE, GROWTH AND MATURITY OF RED PORGY PAGRUS PAGRUS 231

(2000), Potts and Manooch (2002), DeVries (2006), ratory on ice and examined shortly while still fresh. García et al. (2018) and Kikuchi (2019). Red porgy Each fish was measured from the snout to the tip of the attains a maximum age of at least 18 years (Potts and upper limb of the tail to the nearest mm for total length Manooch, 2002), although very few exceed 12 years (TL), weighed to the nearest 0.1 g for total mass (TW), (DeVries, 2006). A few 30-year-old specimens were sexed and eviscerated, recording the gonad mass (GW) recently recorded in southern Brazil (Kikuchi, 2019) to the nearest 0.001 g. and Argentina (García et al., 2018). On average, female red porgy mature at comparatively smaller sizes Gonads were examined through simple macro- in the northeastern Gulf of Mexico (210–215 mm) scopic analysis, as this is a powerful tool for distin- P. pagrus (DeVries, 2006). Although red porgy are hermaphro- guishing sex and developmental phases in ditic, hermaphroditism is never simultaneous and at (Klibansky and Scharf, 2015). Reproductive terminol- the sexual maturity, the majority of individuals are ogy used in this work follows Brown-Peterson et al. males or females. (2011) and include “immature”, “developing”, “spawning capable”, “regressing” or “regenerating”. Different P. pagrus stocks in the SWA have been The latter four stages were considered sexually mature suggested based on aspects of its population dynamics (adults). Reproductive cycles of sexually mature and fisheries (Cotrina and Raimondo, 1997), DNA females were assessed by recording monthly changes markers and body landmarks techniques (Porrini in the gonadosomatic index (GSI), calculated as GSI = et al., 2015), comparison of long-lived endoparasite (GW/(TW–GW))×100. Gonadal development and guilds (Soares et al., 2018) and otolith shape analysis GSI were analyzed by exploratory analysis of variance (Kikuchi, 2019). According to these studies, fisheries (ANOVA). Normality and homoscedasticity of GSI 1 along Argentina, southern Brazil and southeastern data were verified with Shapiro-Wilk and Bartlett Brazil occur over distinct populational units. These tests. When normality and homoscedasticity were not 1 data support that stocks can be managed inde- met, a non-parametric analysis of variance Kruskal- pendently and, in case of overfishing or recovery, they Wallis (H) was applied followed by Mann-Whitney’s have no immediate influence on each other, reinforc- (U) post hoc test. Sex ratios were compared with two- ing the importance to obtain parameters regionally. tailed Chi-square (χ2) tests (Zar, 2010). A Kolmog- Pagrus pagrus populations along the southeastern orov–Smirnov (KS) test was used to compare length- coast of the US have declined sharply due to overfish- frequency distributions between sexes. The F-ratio test ing (Vaughan and Prager, 2002) as in the southern (F) was used to test if regression itself was statistically Brazil (Haimovici, 1998; Haimovici and Cardoso, significant, associated with n – 1 degrees of freedom 2016). Management measures for P. pagrus were intro- (df). Length at which 50% of examined individuals duced in the US and Argentina, but in Brazil no regu- were mature (L50) was estimated by fitting the logistic lation is in place to ensure P. pagrus sustainability. –r regression model P = 1/(1 + exp (L – L50)), where Currently, Pagrus pagrus is listed globally as “Least P —proportion of mature individuals in the length Concern”, but population trends require to be re-eval- class L, r—slope of the curve, L—lower limit of the uated given the economic importance of the species length class, L —mean length-at-maturity. and its complex biological and ecological require- 50 ments (Russell et al., 2014). The left-side sagitta otolith was removed from 793 In this study we provide updated information on individuals (209–502 mm TL), washed and dried, age, growth and maturity of P. pagrus in the Cabo Frio weighted to the nearest 0.0001 g and embedded in region, a coastal upwelling system in the subtropical polyester resin. Sectioning (0.5–0.6 mm) was per- SWA where P. pagrus has been heavily exploited in the formed with a Buehler-Isomet metallographic saw in last decades. We also provide suggestions for future 620 otoliths. Cuts were performed transversely monitoring of the stock based on its age and size struc- through the core and were subsequently mounted on ture, key elements for the preservation of fishery sus- glass slides. Sections were photographed with a digital tainability. stereoscopic microscope (Zeiss STEMI 508®), with reflected light at ×10 objective power, using a 5megapixel resolution camera. All images and mea- MATERIALS AND METHODS surements were processed following Campana (2001). The otolith radius (Ro) and the distances from the oto- Sampling and Processing lith nucleus to the end of each opaque band (Ri) were Specimens were randomly obtained from hook- measured to the nearest 0.001mm along the otolith’s and-line commercial landings in the port of Cabo Frio ventral axis. Increments (annuli), defined as one (Fig. 1), in the southeastern Brazilian coast, between translucent and one opaque bands combined, were January and December 2017. Interviews with skippers counted. Two independent readings without prior revealed that fishing grounds extended from Macaé to access to information on size, sex or sampling date, Arraial do Cabo between 50–100 m, but it was impos- were made twice in successive times. When counts dis- sible to associate fish to a particular location due to agreed, the otolith was read again and the counts were mixing during fishing. Fish were brought to the labo- compared. If counts still disagreed, the otolith was

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Macaé

22.6° Brazil

Study area

Búzios 22.8°

Cabo Frio

Arraial do Cabo

50 m 23.0°

100 m

23.2° 42.3° 42.1° 41.9° 41.7°

Fig. 1. Fishing area of red porgy Pagrus pagrus from Cabo Frio region, southeastern Brazil ( ) and the position of temperature measurements ( ). excluded from further analysis. The accuracy of the where L is the totallength at the time of capture, Li is readings was assessed by the average coefficient of per- the length at the formation of the ith ring and Ri are cent variation (Chang, 1982). To validate the periodic- distances between the focus and each age ring, R is the ity of the increment formation, marginal increment total length of otolith, and a is the intercept of otolith analysis and percentage of edge pattern analysis were radius on fish length regression. performed (Panfili and Morales-Nin, 2002). Marginal The von Bertalanffy growth model was used to increment (MI) was calculated as: MI = (Ro–Rn)/(Rn – −−kt() t0 Rn – 1), where Rn is the distance from the nucleus to describe growth: L = L∞(1e− ), where L is the the outer increment and Rn – 1 is the distance from length of fish at age t; L∞ is the asymptotic length, k is the nucleus to the penultimate opaque increment the growth rate constant i.e. the rate of approaching (Mio, 1961). Differences in MI between two subse- L∞ and t0 is the age when fish length is theoretically quent seasons were assessed with a t-test (Campana, zero. The model was fitted to the observed length-at- 2001). Back-calculated lengths-at-age were computed age data by non-linear regression. Parameters were by using the scale proportional hypothesis (Francis, estimated for all pooled samples and for males and 1990) with the Fraser−Lee formula: females separately. Curves were compared using the Kimura’s likelihood ratio test—LRT (Kimura, 1980; Li=(()(/), L− a Ri R) + a Haddon, 2011).

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Table 1. Monthly variation in sex proportion of Pagrus pagrus sampled in 2017 from southeastern Brazil Number Total Month Sex-ratio χ2 p unknown hermaphrodites females (F) males (M) (F + M) January 0 1 43 32 75 1 : 1.3 2.13 0.144 February 0 1 28 44 72 1 : 0.6 4.92 0.026 March 6 3 24 9 33 1 : 2.7 20.61 <0.010 April 0 10 20 14 34 1 : 1.4 3.09 0.078 May 0 36 28 50 78 1 : 0.6 7.95 0.004 June 0 7 28 47 75 1 : 0.6 6.450.011 July 1 11 36 12 48 1 : 3.0 25.00<0.010 August 0 10 36 28 64 1 : 1.3 1.56 0.211 September 0 1 22 13 35 1 : 1.7 6.65 0.009 October 0 1 17 34 51 1 : 0.5 11.15 <0.010 November 3 2 45 19 64 1 : 2.4 16.48<0.010 December 1 0 39 36 75 1 : 1.1 0.16 0.689 Total 11 83 366 338 704 1 : 1.1 0.16 0.691 χ2—chi-square test, p—significance level.

The minimum age at which females mature (Amin) (Table 1). Size distribution between sex was not sig- was recorded, and the age at which 50% of females nificantly different (KS = 0.167, p = 0.93). Females were mature (A50) was estimated by fitting the logistic 209–500 mm (mean ± SD 341.3 ± 57 mm) and males – r 219–416 mm TL (334.6 ± 55 mm) were mostly repre- regression model P = 100/(1 + exp (A – A50)). Three simple fisheries indicators (Froese, 2004) were used to sented (69% of all fish) between 280–360 mm TL assess the state of P. pagrus stock, based on the catch (Fig. 2a). This range also included most of sex-chang- composition and proportions in relation to a optimum ing hermaphrodites, found between 200–458 mm TL (331.8 ± 53 mm). Length classes < 200 mm TL were length (Lopt) that indicates the length range where maximum yield could be obtained : (i) percentage of underrepresented in the samples. The number of her- mature fish (>L ) in the catch; (ii) percent of fish maphrodites in our samples was limited and it was 50 only briefly described. caught at ± 10% of the optimum length (L ), (iii) opt The body weight of the females and males was 75– percentage of large fish (>1.1 Lopt) in the catch. The size composition of red porgy from hook-and-line 3.325 (620 ± 342) and 75–3.625 (583 ± 383) g, respec- commercial landings sampled during this study was tively (Fig. 2b). The frequency distribution of the body compared to the size composition of bottom-trawl weight of the females and males did not differ from (Costa et al., 2015) and bottom longline catches from normal distributions (KS = 0.183, p = 0.93). The dif- the same area (Olavo et al., 2011). Parameters L , L ference between the body weight of the females and 50 opt males was not significant (U-test: p = 0.25). The max- L and max were analysed comparatively, in order to imum age of the males and females was 12 and facilitate an effective assessment of status and trends of 11 years, respectively (Fig. 2c). P. pagrus fisheries in southeastern Brazil. During the sampling period, sea surface temperature (SST) was continuously recorded by a Data logger Sexual Maturation (HOBO Tidbit UTBI-001) fixed at 1-m water depth at The L50 and L100 were 274 to 406 mm TL for a rocky shore (Fig. 1). The data were used to analyze females and 258 to 386 mm TL for males, respectively seasonal trends in reproductive indicators and the (Fig. 3). Spawning capable males and females were periodicity in the formation of growth rings in the oto- present year-round, but variation in GSI indicates that liths. maximum reproductive activity occurs from Novem- ber to February (Fig. 4). Changes in GSI were signifi- RESULTS cant for females (H = 218, p < 0.01) and males (H = 182, p < 0.01). Cold waters, between 14.9–18°C Sex Ratio, Size and Age Structure recorded at surface (SST) characterize upwelling of The overall female to male proportion (368 : 338) SACW from the deep continental shelf, up to the shal- was not significantly different from 1 : 1 (χ2 = 0.16, p = lower coastal areas. Increases in GSI were observed as 0.6914), despite some monthly significant differences mean water temperatures decreased from 21.8°C in

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(a) (a) 20 1.0

15 0.8

10 0.6

5 0.4

0 0.2 160 200 240 280 320 360 400 440 480 TL, mm 0 30 (b) (b) 1.0 25 20

Propotion Propotion of adults 0.8 15 0.6 10 Propotion, % 5 0.4 0 0.1 0.4 0.7 1.0 1.3 1.6 1.9 2.2 2.9 3.2 0.2 TW, kg 0 35 (c) 150 200 250 300 350 400 450 30 TL, mm 25 20 Fig. 3. Proportion of mature specimens according to total length (TL) of red porgy Pagrus pagrus landed in Cabo 15 Frio-Rio de Janeiro, Brazil, between January and Decem- 10 ber 2017: (a) females, (b) males. (×)—L50, (*)—L100. 5 0 0.01) and males (TL = –76.398 + 123.07 × Rt, r = 123456799101112 0.79, F = 312, p < 0.01), as analysis of covariance indi- Age, years cated that otolith growth was significantly different between sexes (ANCOVA: F = 4.08, df = 213, p = Fig. 2. Body size and age of the females ( ) and males 0.04). Although there was no significant differences (---) of red porgy Pagrus pagrus in the samples from Cabo (H = 16.2, p = 0.132) in monthly MI of the pooled Frio region, southeastern Brazil: (a) total length (TL), samples from age 3, 4 and 5 (Fig. 7), MI estimated (b) body weight (TW), (c) age. from upwelled SACW (0.48 ± 0.16 mm) were significantly lower (H = 6.75, df = 9; p = 0.002) from those recorded in CW (0.95 ± 0.19 mm) (Fig. 5). April to 14.9oC in September, the lowest mean temperature recorded. Maximum GSI values occurred in November, at mean water temperatures of 17.8°C. Age and Growth Mean GSI in females were significantly higher during upwelling of the SACW (H = 4.3, p = 0.02), but not in Ages were determined for 440 of 620 (71%) sec- males (H = 3.5, p = 0.06) (Fig. 5). tioned sagitta otoliths, 29% (n = 180) were either bro- ken or unreadable and 215 were used in back-calculation. The mean percent error (CV) among successive Relationship between the Otolith readings by the same author was 5.8%. Females pre- Length and Body Length dominated in most ages except 4, 7 and 9. Observed and back-calculated lengths-at-age for females, males Left otoliths were preferentially used, although and sexes combined are presented in Table 2. Growth there were no significant differences in length (p = parameters were estimated by fitting the von Berta- 0.24) or width (p = 0.42) between left and right oto- lanffy growth model to observed length-at-age data liths. The regressions between otolith radius (Rt) and (Fig. 8). Nonlinear comparison through LRT showed total length (Fig. 6) were fitted separetely for females that P. pagrus individual growth parameters signifi- (TL = –162.15 + 151.94 × Rt, r = 0.88, F = 499.8, p < cantly differed between sexes (Table 3). Significant

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2.5 (a) 24 2.0

2.0 22 1.5

1.5 20 1.0

1.0 18 GSI, MI 0.5 0.5 16 0 SACW CW 0 14 SST GSI (b) 2.0 24 Fig. 5. Mean gonadosomatic index (GSI) of females (u) and males ( ) and mean marginal increment (MI) for sexes combined (j) of red porgy Pagrus pagrus from Cabo 1.6 22 Frio region, southeastern Brazil. SACW—South Atlantic Central Water, CW—Coastal Water. 1.2 20 DISCUSSION 0.8 18 The onset of P. pagrus spawning in the spring in the Cabo Frio region was associated with a 7°C decrease 0.4 16 in mean SST from 21.8°C to 14.9°C (April–Septem- ber). This is in accordance with minimum tempera- 0 14 ture of 15.2°C reported by Aristizabal (2007) to the JFMAMJJASOND onset of spawning in Argentina, though lower than 17°C reported by Ciechomski and Weiss (1973) in the Fig. 4. Monthly mean GSI ( ( ) ) and mean sea surface same region. Values reported elsewhere range between temperature SST,°C (---) of females (a) and males (b) of 16.0–16.4°C in the southeastern US (Manooch, 1976; red porgy Pagrus pagrus from Cabo Frio region, southeast- Sedberry et al., 2006; Farmer et al., 2017), ~17°C in ern Brazil. Refer to Table 1 for the sample size in each month. Here and in Fig. 5, 7: (I)—95% confidence inter- the northeastern Gulf of Mexico (DeVries, 2006) and val. 18°C in the Canary Islands (Pajuelo and Lorenzo, 1996). Highest GSI in November and December agree differences were observed for asymptotic length L∞ 2 2 with peak spawning of the species in Mar del Plata- (χ = 26.2, p < 0.001), growth rate k (χ = 9.9, p = Argentina (Aristizabal, 2007). Peak spawning at each 2 0.0016) and t0 (χ = 13.6, p = 0.0002). The growth latitude (~23°S vs. ~38°S) occurred from 14.9–17.8°C parameters are presented separately for males (L∞ = and 15.2–17.6°C, respectively, but following a decline −1 419.9 mm, k = 0.347 year , t0 = – 0.199), females (L∞ = in temperature in the Cabo Frio region and after a rise −1 in temperature in Mar del Plata. Spawning of the New 503.8 mm, k = 0.253 year , t0 = – 0.154) and for sexes −1 Zealand snapper Pagrus auratus extends from 5 to combined (L∞ = 461.0 mm, k = 0.290 year , t0 = 6months, and is also triggered by the lowest SST tem- ‒1.26). For pooled samples (males and females), A50 peratures of 15–16°C and concluded within 19–21°C and A100 were estimated as 3.2 and 7 years respectively (Scott and Pankhurst, 1992). Another sparid (Diplodus (Fig. 9). Juvenile, adult (mature), Lopt and large fish argenteus), with clear subtropical/warm temperate (± 1.1 Lopt) specimens corresponded to 11.7, 88.3, 39.0 affinity (Summerer et al., 2001), was reported to syn- and 6.4% of fish sampled from commercial hook-and- chronize spawning in temperatures below 21°C in the line landings (n = 784), respectively (Fig. 10). This Cabo Frio region (David et al., 2005). indicated that P. pagrus in the Lopt range (300–400 mm Globally, length at first maturity (L50) for P. pagrus TL) were aged between 4 and 7 years and weighted has more often been estimated for females or sexes 0.4–1.0 kg. With respect to other fishing gears used in combined. Our estimates for separated sexes (males- southeastern Brazil, P. pagrus juveniles (98.9%) were females: 258–274 mm TL) are comparable to those the bulk of bottom-trawl catches (n = 505). Con- previously reported for the species in the Cabo Frio versely, adults and large fish (mega spawners) were region based on samples collected during 1993–1995 mostly represented in bottom longline (n = 212) (235–225 mm) (Costa et al., 1997). It is also compa- catches (1.8, 98.2, 22.8 and 67.7%). Large fish (mega rable to the Argentine Sea (231–236 mm) from sam- spawners) were absent from bottom-trawl samples. ples collected during 1976–1982 (Cotrina and Chris-

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(a) DeVries, 2006) and South Atlantic Bight between 600 175–255 mm (Harris and McGovern, 1997; Klibansky 500 and Scharf, 2013). L50 < 275 mm would indicate populations intensely exploited and L50 > 276 mm lightly 400 or newly exploited ones (Hood and Johnson, 2000). 300 This is the first attempt using otoliths to age P. pagrus in Brazilian waters, as previous studies have 200 used either scales or the urohial bone (Haimovici, 1991; Ávila-da-Silva, 1996; Costa et al., 1997). The 100 mean percent error (CV) among successive readings in

, mm 600 (b) this study (5.8%) is comparable to the 5% acceptable

TL criterion of Campana (2001). 500 The oldest male and female found herein were, respectively, 12 and 11 years old. Maximum ages 400 obtained in this study are close to the range (13–14 years) 300 reported for the species in the Azores (Serafim and Krug, 1995), the Canary Islands (Pajuelo and 200 Lorenzo, 1996) and the South Atlantic Bight (Harris and McGovern, 1997). Fish as old as 16–18 years were 100 reported in southeastern United States (Potts and 2.3 2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9 4.1 Manooch, 2002), northeastern Gulf of Mexico (Hood Rt, mm and Johnson, 2000; DeVries, 2006), southern Brazil (Kikuchi, 2019) and Argentina (García and Despós, 2015). Fig. 6. Relationship between the otolith radius (Rt) and total length (TL) of females (a) and males (b) of red porgy Increment formation is an independent physiolog- Pagrus pagrus from Cabo Frio region, southeastern Brazil. ical process, more directly responsive to environmen- tal variations (Wright et al., 2002). In tropical environ- ments, even slight temperature changes could be tiansen, 1994) and in the Canary Islands (267– related to increment deposition in the otoliths 226 mm) (Pajuelo and Lorenzo, 1996). Recent L50 (Morales-Nin and Panfili, 2005). Our results evi- estimates in the Argentine Sea for sexes combined denced that P. pagrus laid down a single annulus in (~245 mm) matched our results (Militelli et al., 2017). summer, from November to February, associated with upwelling of the subtropical SACW and with the onset Aside from Manooch (1976), L50 estimates for females of reproductive activity. Previous studies for this spe- are within a relatively narrow range: Gulf of Mexico cies also have validated the annual formation of one between 210–250 mm (Hood and Johnson, 2000; ring in scales (Cotrina, 1977; Manooch and Hunsts-

1.6 24

22 1.2

20 18 37 0.8 47 SST 21 MI, mm 42 51 43 18

0.4 51 23 16 25 0 14 JFMAMJJASOND

Fig. 7. Mean monthly marginal increment (MI) of red porgy Pagrus pagrus of ages 3, 4 and 5 ( ) and mean sea surface temperature (SST) (---) recorded from Cabo Frio region, southeastern Brazil; numbers bellow bars represent the sample size (n).

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Table 2. Observed mean-length (ML) and back-calculated mean lengths-at-age (LAA) by sex of Pagrus pagrus fished in southeastern Brazil Females Males Sexes combined Age n ML LAA n ML LAA n ML LAA 1− −141− −134− −138 2322021522002355226222 3272892802328727950288282 4273253183531230462320327 5253573482133833246348361 6123703631237035924368386 78419418937436317386405 8343044014083964433419 9145945424244063438430 10 −−465 1 421 409 1 421 437 11 1 480 474 1 431 416 2 458 443 12 1 488 481 −−−1 488 448 n— the sample size, (–)—no data.

Table 3. Kimura test by sex of Pagrus pagrus from southeastern Brazil Tests Hypothesis χ2 df p

H0 vs H1 L∞1 = L∞2 26.2 10.002 H0 vs H2 k1 = k29.910.001

H0 vs H3 t01 = t02 13.6 10.006

H0 vs H4 L∞1 = L∞2, k1 = k2, t01 = t02 19.7 30.001 Lines describe the alternative hypothesis (H1–H4) of differential growth among sexes. χ2—сhi-square tests, df—degrees of freedom, p— significance level, L∞—asymtoptic length, k—growth rate constant, t0—age when fish length is theoretically zero. man, 1977; Ávila-da-Silva, 1996; Costa et al., 1997) Growth performance in this study (ϕ' = 4.78) is the and one increment in the otoliths (Pajuelo and highest ever recorded for red porgy, despite the narrow Lorenzo, 1996; Harris and McGovern, 1997; Potts range elsewhere (4.36–4.75). Negative t0 values (as and Manooch, 2002; Kikuchi, 2019). herein) agree with other studies and indicate very fast

500 450 400 350

, mm 300

TL 250 200 150 100 0 1 2 3 4 5 6 7 8 9 10 11 12 13 Age, years

Fig. 8. Growth curves used to estimate growth parameters of red porgy Pagrus pagrus from Cabo Frio region, southeastern Brazil: sexes combined ( ), females (··s··), males (--n--), back-calculated (e).

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1.0 mentation of a 14-inch minimum size limit, recreational and commercial quotas, closed season and 0.8 even a one-year moratorium were among the actions implemented to promote recovery of the species by the 0.6 South Atlantic Fishery Management Council (SAFMC Amendment 4 : 10 years, beginning in 1991; SAFMC Amendment 12, 18 years, beginning in 1999) 0.4 (September 1999 through August 2000). Nevertheless, Propotion, % observed recruitment values for 2013–2017 were lower 0.2 than the average expected from stock-recruit curve, while the stock is yet to be rebuilt (SEDAR, 2020). 0 1 2 3 4 5 6 7 8 9 10 11 12 The management of red porgy in Argentina Age, years includes a yearly catch limit (the Total Allowable Catch or CMP in spanish) set by the commission Fig. 9. Proportion of mature individuals at each age of red (Comisión Técnica Mixta del Frente Marítimo, porgy Pagrus pagrus from Cabo Frio region, southeastern CTMFM) that administers the northern area Brazil. (×)—A50, (*)—A100. (ZCPAU: 34°–39° S), where most of its fishing occurs. After a progressive decrease in the past few years (2013–6000 t, 2014–2016 – ~4600 t, 2017–3600 t), growth in the first years of life, slowing down consider- since 2018 CMP was established in 3900 t. Projections ably afterwards. Our growth parameters (L∞ = 461 mm, based on surplus production model using CMP 2016 k = 0.29 year−1) are closest to those reported by Kikuchi (CTMFM Resolution 2/2016) indicated that risk that −1 (2019) in southern Brazil (L∞ = 431mm, k = 0.29 year ) biomass falls below 50% of the virgin biomass in 5, 10 and 15 years is low (<10%) (Ficha técnica BESUGO and off the southeastern United States (L∞ = 422.6 mm, k = 0.30 year−1), including 42434 samples (SEDAR, (Pagrus pagrus): http://www.ctmfm.org/fichas-tecni- 2020), possibly because individuals > 450 mm were cas/34/ficha-tecnica-besugo/. Version 04/2020). scarce in the samples (Fig. 11). In Argentina, lower L∞ In Brazil, no regulation is in place to ensure −1 P pagrus and higher k (L∞ =402 mm, k = 0.33 year ) occurred . sustainability. Although the species was in the common fishing zone (ZCPAU), where fishing included in the 2004 national list of overfished or pressure is high (García et al., 2018). threatened overfished species, it is not currently endan- gered (Normative Instruction MMA/163/2015). In the Red porgy populations along the southeastern past (1970s) the bottom-trawling fishery in southern coast of the US have declined precipitously due to waters severely depleted an important outer-shelf overfishing, with spawning stock biomass falling from stock (Haimovici, 1998; Haimovici and Cardoso, 3530 tonnes in 1979 to 397 tonnes in 1997 (Vaughan 2016), suggesting that this destructive and non-selec- and Prager, 2002). Gear limitations and the imple- tive method should be discouraged. In the present

12 L50 Lopt L∞ Lmax

Frequency, % Frequency, 4 Juvenilles Large ﬁsh 2 Mature

0 50 100 150 200 250 300 350 400 450 500 TL, mm

Fig. 10. Length-frequency of red porgy P. pagrus from bottom-trawl (---), hook-and-line ( ) and bottom longline (− − ) survey from southeastern Brazil. L50—length-at-maturity, Lopt—length range where maximum yield could be obtained, L∞— asymptotic length, Lmax—maximum size (n = 1498).

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500

450 1 2 3 400 4 350

300 , mm 250 TL 200

150

100

50 0 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Age, years

Fig. 11. Comparative growth curves using parameters estimated by otolith analysis in Pagrus pagrus populations from different regions. 1—present study, 2—Kikuchi, 2019; 3—SEDAR, 2020; 4—García et al., 2018. study P. pagrus became sexually mature at 2.5– adult populations establish (Afonso et al., 2008). 3.0 years, (258–274 mm) far in advance it was fully Aggregations of larger individuals on hard bottoms recruited to hook-and-line fisheries at age 4 (327 mm) that are not trawable were suggested to explain the and this probably contributes to its resilience to this absence of mature specimens in trawl nets in a three- fishery. year survey along the Cretan continental shelf (Labropoulou et al., 1999). Although hook-and-line is size selective (Welch et al., 2010), P. pagrus male and female fish appear to Pagrus pagrus was the most abundant species in one be captured proportionally, suggesting that they are of the assemblages (southern, 19°–22° S) distributed equally vulnerable to this gear (DeVries, 2007). There- over shelf-edge reefs considered as priority areas for fore, we assume that the size structure of samples in conservation in the tropical SWA (Оlavo et al., 2011). this study accurately reflect the true size distribution at In the Azores islands, red porgy in reserves seem to the site at the time of collection. The negligible devia- have a good potential for the spillover effect, which tion from the expected 1 : 1 global sex ratio observed could also benefit adjacent fisheries (Afonso et al., herein might indicate absence of sexual segregation, 2009). Conservation programs should therefore enabling transition to occur year-round (Koenig et al., account for habitat that P. pagrus use over its entire life 1996). This would be advantageous, as the impact of cycle, and in particular the younger life stages (Grol overfishing on a protogynous species is reduced if the et al., 2014). This involves a better understanding of numerical sex ratio is maintained (Huntsman and their habitat preferences for recruitment and nursery, Schaaf, 1994). in order to keep ecological processes that maintain connectivity among mosaics of habitats required by Conversely, we believe that a strong size-related the species (Nagelkerken et al., 2015). Fishing for this segregation occurs herein, as reported for red porgy in species is still increasing for industrial and recreational the Azores (Afonso et al., 2008). This is based on purposes in Brazil, and despite its large distribution between gear differences in size composition of the from subtropical to tropical water, the available data catch (Fig. 10), as previously noticed in southern Bra- on population biology for this species is still scarce for zil (Ávila-da-Silva and Haimovici, 2006). The over management aims. The suggestion to keep the popula- dominance of juveniles in bottom-trawl catches tion status in Brazil as Data Deficient is yet precau- (98.9%) and adults in hook-and-line and bottom- tionary. longlines catches (88.3–98.2%) presumably indicate that habitat of juvenile red porgy in southeastern Bra- zilian waters is well separated from that of adult speci- ACKNOWLEDGMENTS mens, as these fisheries develop at increasing depths. We thank Mr. Vincenzo Scuotto from Brasfish – Young-of-the-year red porgy are known to recruit to Indústria e Comércio Ltda. and Mr. Edivaldo dos Santos shallow, sandy habitats, and migrate toward deeper Ribeiro (Perrota) for providing support during sampling at and progressively rockier bottoms, where sedentary Cabo Frio fish market. We would like to thank the referees

JOURNAL OF ICHTHYOLOGY Vol. 61 No. 2 2021 240 COSTA et al. for their critical reviews and suggested changes to the man- Mar Argentino (Pisces, Sparidae), Physis (Buenos Aires), uscript. 1973, vol. 32, no. 85, pp. 481–487. Costa, P.A.S., Fagundes-Netto, E.B., Gaelzer, L.R., Lac- erda, P.S., and Monteiro-Ribas, W.M., Crescimento e ciclo FUNDING reprodutivo do pargo-rosa (Pagrus pagrus Linnaeus, 1758) This work was supported by the Fundo Brasileiro para a na região do Cabo Frio, Rio de Janeiro, Nerítica, 1997, Biodiversidade (FUNBIO) under Grant Marine Research vol. 11, pp. 139–154. 104/2016. Costa, P.A.S., Mincarone, M.M., Braga, A.C., Martins, A.S., Lavrado, H.P., Haimovici, M., and Falcão, A.P.C., Mega- faunal communities along a depth gradient on the tropical COMPLIANCE WITH ETHICAL STANDARDS Brazilian continental margin, Mar. Biol. Res., 2015, vol. 11, pp. 1053–1064. The authors declare that they have no conflict of inter- https://doi.org/10.1080/17451000.2015.1062521 est. 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SPELL: 1. homoscedasticity

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