Research Article |
Corresponding author: Cassiano Monteiro-Neto ( cmneto@id.uff.br ) Academic editor: Paulo Lana
© 2021 Geysa Marinho de Souza, Cassiano Monteiro-Neto, Marcus Rodrigues da Costa, Ana Luiza Bastos, Raquel Rennó Mascarenhas Martins, Francyne Carolina dos Santos Vieira, Magda Fernandes de Andrade-Tubino, Rafael de Almeida Tubino.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
de Souza GM, Monteiro-Neto C, da Costa MR, Bastos AL, Martins RRM, Vieira FCS, de Andrade-Tubino MF, Tubino RA (2021) Reproductive biology and recruitment of bluefish Pomatomus saltatrix (Perciformes: Pomatomidae) in the southwestern Atlantic. Zoologia 38: 1-14. https://doi.org/10.3897/zoologia.38.e53756
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The bluefish, Pomatomus saltatrix (Linneus 1766) is captured by industrial, artisanal, and recreational fisheries throughout its distribution range. The reproductive biology of P. saltatrix in the southwestern Atlantic was studied using 1,102 specimens captured by the Brazilian commercial fleet between March 2014 and December 2015. The recruitment period was identified from records of juveniles in experimental beach seine hauls carried out on sandy beaches in the external sector of Guanabara Bay for four years (2012–2015). Based on the reproductive indices and on the macro- and microscopic analyses of the gonads, spawning peaks were identified in autumn and spring. The size at first maturity was estimated at 35.5, 38.3, and 37.4 cm for females, males, and general, respectively. Ovary analyses and measurements of the oocyte diameters indicated that bluefish are multiple spawners with asynchronous oocyte development. The batch fecundity estimate was 202,752.5 eggs and ranged from 9,800.9 to 426,787.0 eggs. The species reproduces throughout the entire study area, but it is more active in the south of Arraial do Cabo. The young-of-the-year were recorded on shallow water in all seasons, with modal peaks in the summer months. The parameters estimated in this study expand and update information on this species, providing important data for the evaluation and fisheries management of the stock of P. saltatrix in the southwestern Atlantic.
Fecundity, histology, oocyte development, reproductive dynamics, spawning seasons, young-of-the-year
The bluefish, Pomatomus saltatrix (Linneus 1766), is a migratory pelagic species with a wide geographic distribution. It occurs preferentially in continental shelf waters in temperate and tropical regions (
The fishery production data series have indicated a decline in catches in the southwestern Atlantic, with a reduction of 14,000 tons per year between the 1960s and 1970s, to around 4,000 tons per year between the 1980s and 1990s, reaching an average production of 3,600 tons per year in the 2000s (
Despite its recognized importance as a fishery resource, management policies for the species have not been established throughout its distribution range. The current legislation governing bluefish fisheries in Brazil covers only part of its distribution along the southern coast (Rio Grande do Sul, Santa Catarina, and Paraná) (
The natural renewal of the population is a complex process, resulting from a series of events during the species’ life cycle such as maturity, egg laying, metamorphosis, growth, survival in nursery areas, and migration to feeding areas (
Studies on the reproductive biology of the species are important in fisheries science because these are used to determine the resilience of populations to fishing pressure (
Between March 2014 and December 2015, 49 commercial landings of the fleet operating on the southeast coast of Brazil, between latitudes of 20°30’ and 24°00’S (Fig.
The fishing area (Fig.
We also collected data on the occurrence, abundance, and sizes of young-of-the-year (YOY) fishes on the shallow waters of the sandy beaches based on the monthly experimental beach seining conducted between January 2012 and December 2015 (SISBIO/IBAMA/ICMBio collection license #15787-1). Beach seining was conducted in the shallow surf zones of the three beaches located in the marine boundary and lower sector of Guanabara Bay. On each occasion, three hauls were carried out for a distance of 20 m in a direction parallel to the coastline at a maximum depth of 1.5 m. The beach seine used was 9.0 m long and 2.6 m wide, made of a 210/06 silk thread with a 13 mm bar mesh on the sides and a 5 mm bar mesh in the bag. Records of P. saltatrix juveniles were used to identify the recruitment periods in the beach shallow waters and to evaluate the size of the YOY. All individuals were measured for total length (TL, cm) and total weight (TW, g). Individuals from commercial fisheries had their sex identified through a macroscopic examination of gonad characteristics (
The relative growth of the juveniles and adults (females and males) was evaluated using the length-weight relationship (LWR) according to the equation: TW = aTLb (
The sex ratio was determined for the different length classes (intervals of 5 cm TL), and the austral seasons were defined as summer (January-March), autumn (April–June), winter (July–September), and spring (October-December). Deviations from the null hypothesis of a 1:1 ratio were statistically tested using the chi-squared test (χ2) with a 5% significance level. Reproductive activity was assessed by observing the macroscopic characteristics of the gonads, microscopic examination of the ovarian histological slides, frequency distribution of the oocyte diameter, and the reproductive indices. All individuals had their gonads macroscopically classified according to the following stages: immature, developing, spawning capable, spent, and regenerating (
Description of gonadal maturity stages of Pomatomus saltatrix, adapted from
Maturity stage | Macroscopic and histological features in females |
Immature | Ovaries are very small, occupy about 1/3 of the body length, and are thin and translucent. Only oogonia and primary growth oocytes (PG) are seen. There is little space between the oocytes. The ovarian wall (OW) is slightly thick. |
Developing | Ovaries range from small to medium and occupy between 1/3 to 2/3 of the celomatic cavity. Ovaries are yellow in color, and blood vessels may be apparent. Only PG are seen, with cortical alveolar (CA) and are in vitellogenesis (Vtg1 and Vtg2). |
Spawning capable | Ovaries are large, occupying more than 2/3 of the body length, are pale yellow in color, and have evident blood vessels. Hydrated oocytes are macroscopically visible. Primary growth oocytes are prevalent, with CA and vitellogenesis (Vtg1, Vtg2, and Vtg3). Oocytes are seen with germinal vesicle migration (GVM) and late germinal vesicle migration (LATE GVM). Hydrated oocytes (HYD) or post-ovulatory follicles (POF) are seen. There is the possibility of atresias (A). |
Spent | Ovaries are small, occupying between 1/3 to 2/3 of the body length, are flaccid, and have prominent blood vessels. Atresic oocytes (A), post-ovulatory follicles (POF), and CA and vitellogenic oocytes (Vtg1 and Vtg2) may be present. |
Regenerating | Ovaries are very small, occupying up to 1/3 of the body length, and with reduced blood vessels. Brown in color. Ovarian wall (OW) is thick. Only oogonia and PG are present. There are evident spaces between oocytes. Atresic oocytes and degenerating POF may be present. |
Maturity stage | Macroscopic features in males |
Immature | Testes are very small, filiform, and are clear or translucent, occupying 1/3 of the celomatic cavity. |
Developing | Testes are small but easily identifiable, occupying up to 2/3 of the celomatic cavity. Light and homogeneous in color. |
Spawning capable | Testes are large and firm with opaque white color, occupying more than 2/3 of the body length. They break easily when applied with pressure. |
Spent | Testes are small and flaccid, may be brown in color, occupying about 1/3 of the celomatic cavity. |
The gonadosomatic index (GSI), as a proxy of the degree of gonadal development, was calculated for each sex and grouped sexes based on the eviscerated weight to avoid possible variations from differences in the stomach content using the equation: GSI = (GW/EW) x 100, where GW is the gonad weight (g), and EW is the weight of the fish eviscerated. The condition factor under the influence of the gonad weight (K) and without the gonad weight (K’) were calculated according to the methods of
Finally, the size at 50% maturity (L50) was estimated to define sexual maturity as a function of body length, according to the following equation (
Batch fecundity (F) was estimated by direct counts of the hydrated oocytes (
Out of the 1,102 individuals sampled from the commercial landings, 671 were females ranging in size from 30.0 to 82.0 cm TL (mean ± SD; 48.9 ± 6.7 cm), and 431 were males, ranging from 29.2 to 61.6 cm TL (mean ± SD; 47.8 ± 5.6 cm) (Fig.
The length-weight relationship determined for the juveniles was TW = 0.004 TL3.281, which indicated a positive allometric growth (b > 3) (p < 0.05) (t(1127) =18.45, p < 0.05). The relationships for females and males were expressed by the following equations: TW = 0.028 TL 2.693 and TW = 0.036 TL 2.628, respectively, indicating a negative allometric growth (b < 3) (p < 0.05) (female t(575) = -14.97, p < 0.05, and male t(389) = -15.19, p < 0.05) for the commercial landings population stratum. There were no significant differences between the sexes (ANCOVA: F1,965 = 0.20, p > 0.05). Thus, we assumed that the b value obtained for the grouped sexes would be representative of the study population (Table
The total sex ratio (0.61; female:male = 1.6:1) was significantly different from the expected value of 0.5 (χ2calc = 4.74, df = 1, p > 0.05). There were no significant differences (χ2calc = 0.33 and 0.52, df = 1, p > 0.05) in the intermediate size classes (between 40.0 and 49.9 cm). In the other size classes, females predominated, especially above 65.0 cm (χ2calc = 51.02, df = 1, p < 0.05). Females were more abundant during almost the entire study period. Males were more abundant only in the summer of 2014 (χ2calc = 36.00, df = 1, p > 0.05).
Parameters of the length-weight relationship of juveniles (beach seine) and individual juveniles and adults (males, females, and grouped sexes in commercial fisheries) of Pomatomus saltatrix. n = number of individuals, a and b = coefficients of the exponential equation TW = aTLb, SD = standard deviations of a and b respectively, R2 = coefficient of determination.
Sex | n | Total Weight (TW, g) |
Total length (TL, cm) |
a | SD a | b | SD b | R² |
Juveniles | 1,127 | 0.043–31.712 | 1.2–15.5 | 0.0042 | 0.0104 | 3.281 | 0.0153 | 0.973 |
Females | 577 | 233.0–4036.0 | 30.0–82.0 | 0.0281 | 0.0345 | 2.693 | 0.0205 | 0.967 |
Males | 391 | 234.0–2218.0 | 29.2–61.1 | 0.0367 | 0.0411 | 2.628 | 0.0245 | 0.967 |
Grouped | 968* | 233.0–4036.0 | 29.2–82.0 | 0.0310 | 0.0265 | 2.668 | 0.0158 | 0.967 |
Histological analyses of the ovaries revealed that the oocyte development showed a consistent pattern in batch spawning. In spawning capable ovaries, oocytes at all stages of development were recorded (Figs
The presence of hydrated oocytes and oocytes at advanced stages of development (Vtg2 and Vtg3) in the same ovary indicates the possibility of more than one spawning event in the same season (Fig.
The frequency distributions of the oocyte diameter by maturity stage revealed a similar unimodal pattern for immature oocytes and regeneration. Other stages showed multimodal distributions, especially the ovaries classified as spawning capable (Fig.
Steps and stages of oocyte development of Pomatomus saltatrix. Primary growth (PG), Secondary growth is cortical alveolar (CA), early vitellogenesis (Vtg1), intermediate vitellogenesis (Vtg2), late vitellogenesis (Vtg3). The interval between CA and germinal vesicle migration (GVM), late germinal vesicle migration (late GVM), and hydration (HYD) corresponds to oocyte maturation (OM), followed by post-ovulatory follicle (POF).
Histological sections of the ovaries of Pomatomus saltatrix. Spawning capable: (4) presence of oocytes at the different stages of development; (5, 6) oocytes in advanced secondary growth (GVM and late GVM); (7) Hydrated oocytes (HYD); Spent: (8) oocytes in β atresia; (9) oocytes in Vtg3 and POF. Oocyte primary growth (PG); cortical alveolar (CA); early vitellogenesis (Vtg1); intermediate vitellogenesis (Vtg2); late vitellogenesis (Vtg3); ovarian wall (OW); post-ovulatory follicle (POF); hydrated oocytes (HYD); germinal vesicle migration (GVM); late germinal vesicle migration (late GVM).
Frequency distribution of the oocyte diameters. Frequencies through the stages of gonadal development of Pomatomus saltatrix caught on the southeastern coast of Brazil. The vertical dashed line indicates the diameter at the beginning of vitellogenesis (Ø = 127 μm). Number of oocytes measured per maturity stage: immature (n fish = 4, n oocytes = 388), developing (n fish = 3, n oocytes = 673), spawning capable (n fish = 25, n = 2,330), spent (n fish = 3, n = 172), and regenerating (n fish = 4, n = 412).
The size at 50% maturity (L50) was estimated at 35.5 cm LT for females, 38.3 cm for males, and 37.4 cm for both sexes (Fig.
To identify seasonal spawning patterns, we calculated the reproductive indices (GSI, KΔ, and HI) separately for females and males, considering only adult and spawning individuals. The mean values of GSI and KΔ varied similarly over time for both sexes. Despite the interannual variation in GSI values, the seasonal pattern was repeated in both cycles, revealing two annual reproductive peaks.
The highest GSI values for females were observed during autumn (May 2014 and April 2015) and spring (December 2014 and October 2015). The lowest GSI values were recorded during the summer months in both annual cycles (Fig.
(12) Gonadosomatic index (GSI); (13) gonadal condition factor (KΔ); (14) hepatosomatic index (HI). Mean monthly values ± SE for females and males of Pomatomus saltatrix caught off the southeastern coast of Brazil, between March 2014 and December 2015 (n = 646 and 404, females and males, respectively).
Individual fecundity estimated from fresh ovarian samples of seven fishes (41.8–52.8 cm; 0.786–1.280 kg) was 9,800.9–426,787.0 eggs, with a mean ± SD of 202,752.5 ± 160,900.9. The estimates of individual relative fecundity ranged between and 81–548 oocytes g-1, with a mean ± SD of 273.5 ± 152.3 oocytes g-1.
The relationship between fecundity (F), total length (TL), and total weight body (TW) was fitted using the following equations: F = 5E-08 TL.476 (R² = 0.734) and F = 5E-10 TW 3.866 (R² = 0.985).
The sampling program carried out in the shallow surf zone of the sandy beaches recorded the occurrence of 1,136 individuals with TL varying between 1.0 and 15.5 cm (mean = 4.7 ± 2.6 SD), essentially during late winter and summer. No individual was caught in the autumn or early winter months.
The YOY was recorded between the end of winter and early spring, with an average size of 3.1 cm (± 1.9 SD) remaining in this environment for a period of three to five months, when they reached a TL of approximately 11.2 cm (± 1.9 SD) (Fig.
Monthly distribution of mean values (vertical bars ± SE) of the total length of juvenile fish caught by experimental trawls on the surf zone of three sandy beaches of Niterói (RJ), between January 2012 and December 2015 (n = 1,127). Variation of the mean monthly gonadosomatic index (GSI) (black triangle ± SE) of individuals of Pomatomus saltatrix caught on the southeastern coast of Brazil between March 2014 and December 2015 (n = 1,050). The annual cycles from 2012 to 2015 were organized by month.
The sex ratio of a population is an important population attribute because it varies throughout their life cycle, which depends on several ecological and evolutionary events that affect the individuals of each sex (
The parameters derived from the length-mass relationship, i.e., condition factor and “b” observed, revealed different energy investments between the juveniles (b > 3) and adults (b < 3). This is in agreement with the classic pattern of fish development, in which juveniles allocate energy for somatic growth only, while adults allocate energy for growth and reproduction (
The estimated L50 for grouped sexes was 37.4 cm, greater than the estimates from previous studies on the south coast (
Histological analyses of the ovaries confirmed the macroscopic stages observed and indicated that the bluefish have a batch spawning pattern, with asynchronous oocyte development and continuous reproduction. This is supported by the seasonal patterns of oocyte development widely documented in the literature (
The results of this study also showed the presence of individuals capable of spawning in almost all months, with clear seasonality in the reproductive period, having one spawning peak in spring and the other in autumn. The presence of HYT, which occurs a few hours before spawning (
Bluefish exhibit a characteristic migratory behavior, that is, migrating to higher latitudes in the spring and returning to lower latitudes in the fall and winter, which is linked to the displacement of warmer water bodies (14 to 30 °C) (
Fecundity is generally proportional to the size, weight, and condition of the fish, which are key parameters for assessing fecundity at the population level (
The recruitment pattern observed corroborates the reproductive period of the species in the southeastern Brazilian region. Inflows of YOY in the spring and summer months confirmed the occurrence of two recruitment pulses (winter and summer) linked with the two reproductive peaks observed. For instance, shallow coastal habitats such as nearshore waters of sandy beaches play an important role as a breeding site or nursery for the growth of P. saltatrix. Several studies have reported that the recruitment pattern of bluefish is similar between populations. Eggs and larvae are usually found along the coast in breeding habitats (
The integrated analysis of the reproductive dynamics and recruitment patterns in the present study suggests that reproduction occurs within the studied area. This result is further supported by the presence of POF and hydrated females concentrated in spring and summer months in the northernmost range of southeastern Brazil. Additionally, the size of the first maturity reported here is higher than the minimum landing size established in the legislation. In light of this evidence and the fact that the legislation was established based on information gathered three decades ago, fisheries regulations for P. saltatrix should be reviewed, including the updated results. Furthermore, future studies on the migratory movements and spawning dynamics of P. saltatrix in the southwestern Atlantic off the coast of Brazil must be elucidated to aid in the conservation and protection of spawning stock biomass from various fishery interactions.
This study was financially supported by the Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ # E-26/112.613/2012) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq # 406249/2012-1). The project was presented to and approved by the Departamento de Biologia Marinha, Instituto de Biologia, Universidade Federal Fluminense. Research was conducted according to approved ethical standards. G.M. de Souza held a Master’s degree scholarship from Capes and R.A. Tubino a post-doctoral fellowship PNPD-CAPES, during the course of the study. C. Monteiro-Neto is a Research Productivity Fellow from CNPq (# 305292/2016-1). We thank the staff and trainees from ECOPESCA-UFF, LEPHEC-UFF and FIPERJ. Editing and review of the English language was performed by Editage – Cactus Communications Services Pte. Ltd.