SCRS/2008/080
Collect. Vol. Sci. Pap. ICCAT, 64(6): 1927-1940 (2009) PRELIMINARY ANALYSIS OF GONAD DEVELOPMENT, SPAWNING PERIOD,
SEX RATIO AND LENGTH AT FIRST SEXUAL MATURITY OF SAILFISH,
ISTIOPHORUS PLATYPTERUS, IN BRAZILIAN COAST
Bruno L. Mourato 1, Patrícia Pinheiro 2, Fábio H.V. Hazin2, Vanessa Basante2,
Alberto F. Amorim3, Eduardo Pimenta 4, Charles Guimarães4
SUMMARY
From May 2006 to February 2008, gonads of 215 sailfish caught in the western South Atlantic
were examined. In Area 1 (7°N to 24°S/15.5° to 40°W) 153 specimens were examined, of which
95 were females ranging in LJFL from 114-210 cm, whereas the 58 males ranged from 104-185
cm. In Area 2 (22° to 27°S/39° to 47°W) 62 specimens were examined, of which 32 were
females ranging in LJFL from 130–197 cm. The 30 males ranged from 133-176 cm LJFL. The
sex ratio analysis indicated the predominance of females in almost all months in both areas.
However, in September in Area 1 a significant difference was always noted on the expected
proportion 1:1. In area 1, females with maturing stage ovaries were the majority and occurred
in all sampled months. Immature females were more frequent in January and February.
Females with ripe ovaries were practically absent, with only one specimen caught in November.
In contrast, in Area 2 females with ripe or spent ovaries were frequently found from December
to February. The gonad index analysis showed higher mean values (>2) in Area 2 from
December and January. In comparison, Area 1 presented smaller mean values of gonad index
(< 1.5) throughout the year. In this study, the size at first sexual maturity (L50) of females based
on ovarian macroscopic examination was equal a 154.93 cm LJFL. The results of the present
study confirm the hypothesis that sailfish spawn in the southeast Brazilian coast (Area 1 of the
present study) during the 1st and 4th quarters. However, the results are preliminary since the
visual assessment of ovaries to determine the maturity stage is felt to be an imprecise indicator
of reproductive condition. New studies based on histological analysis of gonads are needed, as
well as additional research (including tagging experiments) is necessary to better understand
the migration route after spawning.
RÉSUMÉ
Du mois de mai 2006 à février 2008, des gonades de 215 voiliers capturés dans l’Atlantique
Sud-Ouest ont été examinées. Dans la zone 1 (7°N à 24°S/15,5° à 40°W), 153 spécimens ont été
étudiés : 95 femelles, dont la taille allait de 114 à 210 cm LJFL, et 58 mâles dont la taille allait
de 104 à 185 cm. Dans la zone 2 (22° à 27°S/39° à 47°W), 62 spécimens ont été étudiés : 32
femelles, dont la taille oscillait entre 130 et 197 cm LJFL, et 30 mâles dont la taille variait de
133 à 176 cm LJFL. L’analyse de sex-ratio indiquait la prédominance des femelles pendant
presque tous les mois de l’année dans les deux zones. Cependant, en septembre, dans la zone 1,
une différence significative a toujours été notée dans la proportion attendue 1:1. Dans la zone
1, les femelles avec des ovaires en phase de maturation représentaient la majorité et étaient
présentes dans tous les mois échantillonnés. Les femelles immatures étaient les plus fréquentes
en janvier et février. Les femelles avec des ovaires matures étaient pratiquement absentes, avec
un seul spécimen capturé en novembre. En revanche, dans la zone 2 les femelles avec des
ovaires matures ou vides étaient fréquentes de décembre à février. L’analyse de l’indice
gonadique présentait des valeurs moyennes élevées (>2) dans la zone 2 de décembre à janvier.
Par comparaison, la zone 1 présentait des valeurs moyennes plus faibles de l’indice gonadique
(< 1,5) tout au long de l’année. Dans la présente étude, la taille à la première maturité sexuelle
(L50) des femelles, basée sur un examen macroscopique des ovaires, s’élevait à 154,93 cm
LJFL. Les résultats de cette étude confirment l’hypothèse selon laquelle le voilier fraye sur la
1
PhD. Student – Universidade Federal de Pernambuco/Departamento de Oceanografia, Recife-PE, Brasil ([email protected]).
Universidade Federal Rural de Pernambuco/Departamento de Pesca e Aqüicultura, Recife- PE, Brasil.
3
Instituto de Pesca/APTA/SAA, Santos-SP, Brasil.
4
Universidade Estácio de Sá - Curso de Tecnologia Pesqueira/Escola Superior de Pesca.
2
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côte brésilienne du Sud-Est (zone 1 de la présente étude) au cours des 1er et 4ème trimestres. Ces
résultats sont toutefois provisoires, étant donné que l’évaluation visuelle des ovaires visant à
déterminer la phase de maturité est considérée comme un indicateur imprécis des conditions de
reproduction. De nouvelles études basées sur l’analyse histologique des gonades sont
nécessaires ainsi que des recherches additionnelles (y compris des expériences de marquage)
afin de mieux comprendre les trajets migratoires post-ponte.
RESUMEN
De mayo de 2006 a febrero de 2008, se examinaron las gónadas de 215 ejemplares de pez vela
capturados en el Atlántico suroccidental. En la zona 1 (7°N a 24°S/15.5° a 40°W) se
examinaron 153 ejemplares, de los cuales 95 eran hembras con una LJFL que oscilaba entre
114 y 210 cm, mientras que las tallas de 58 machos oscilaron entre 104 y 185 cm. En la zona 2
(22º a 27°S/39° a 47°W), se examinaron 62 ejemplares, de los cuales 32 fueron hembras con
una LJFL que osciló entre 130-197 cm. Los 30 machos presentaban una LJFL que oscilaba
entre 122 y 176 cm. En el análisis de ratio de sexos se observó un predominio de las hembras
en casi todos los meses en ambas zonas. Sin embargo, en septiembre y en la zona 1, se constató
siempre una diferencia notable en la proporción prevista 1:1. En la zona 1, las hembras con
ovarios en fase de madurez fueron mayoritarias y estuvieron presentes en todos los meses
muestreados. Las hembras inmaduras fueron más frecuentes en enero y febrero. Las hembras
con ovarios en plena madurez estaban casi ausentes, con sólo un ejemplar capturado en
noviembre. Por el contrario, en la zona 2 y desde diciembre a febrero, se encontraron
frecuentemente hembras con ovarios plenamente maduros o usados. Los análisis de índice
gonadal mostraban valores medios más elevados (>2) en la zona 2, de diciembre a enero. En
comparación, la zona 1 presentaba valores medios inferiores en el índice gonadal (<1,5)
durante todo el año. En este estudio se situó en 154,93 cm la talla de primera madurez (L50) de
las hembras, basándose en el examen macroscópico de los ovarios. Los resultados de este
estudio confirman la hipótesis de que el pez vela desova en la costa suroriental brasileña (zona
1 en este estudio) durante el primer y cuarto trimestre. Sin embargo, los resultados son
preliminares, ya que se considera que determinar la fase de madurez mediante la evaluación
visual de los ovarios es un indicador poco preciso de la condición reproductiva. Es necesario
realizar más estudios basados en el análisis histológico de las gónadas, así como
investigaciones adicionales (lo que incluye experimentos de marcado) para entender mejor la
ruta de migración tras el desove.
KEYWORDS
Sailfish, western South Atlantic, gonad development, sex ratio, spawning period
1. Introduction
In the Atlantic Ocean, sailfish is widely distributed in subtropical and tropical waters, and occasionally in
Atlantic temperate waters, being also present in the Mediterranean Sea. Geographical limits based on
commercial catches is approximately 40°N in the western North Atlantic, 50°N in the eastern North Atlantic,
40°S in the western South Atlantic, and 32°S in the eastern South Atlantic (Beardsley et al. 1974; Nakamura,
1985).
The impact of fishing on billfish stocks in the south Atlantic is currently the focus of considerable international
concern. Major recreational fisheries for billfishes (Istiophoridae) exist throughout the world’s tropical oceans,
thus placing them among the most sought-after big gamefish (IGFA, 2001). Besides, although billfishes are not a
target species, they are caught in great numbers by commercial fisheries, including both industrial, such as the
tuna longline fishery, as artisanal.
The largest concentration of sailfish in Brazilian waters is located along the southeast coast of Brazil, between
latitudes of 20o-27oS, and longitudes of 39o-48oW, where they aggregate, mainly during the first and fourth
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quarters of the year. Sailfish usually appear in this area from October to March, but occasionally in September
(Arfelli and Amorim, 1981). The monthly catches from November to January were (in weight) about 14%, 27%
and 10% of the total catches, respectively of Santos longliners in the 1971 to 91 period (Hazin et al., 1994). In
the northeast Brazilian coast, the sailfish is caught along the whole year, but CPUEs are much lower than those
obtained from the southeast Brazilian coast, during the fishing season (Hazin et al., 1994).
In spite of the great importance of the species, for both recreational and commercial fisheries, including artisanal
and industrial, little information on sailfish biology off Brazilian Coast has been published so far (Arfelli and
Amorim, 1981; Souza et al., 1994; Pimenta et al., 2005). The aim of the present paper is thus to contribute
information on the reproductive biology of sailfish in Brazilian waters.
2. Material and methods
The data and samples examined in the present study were collected by observers, of the National Observer
Program, on board of chartered tuna longliners based in the Ports of Natal (RN) and Cabedelo (PB), located in
northeast Brazil. Additionally, gonad samples were also obtained from small longliners, based in the Port of
Cabo Frio (RJ), located in southeast coast of Brazil, and from tuna longliners based in São Paulo State (SantosSP). All specimens were measured for lower jaw-fork length (LJFL), being then dissected for the collection of
gonads, which were then frozen and stored in freezers, up to the time of landing. In the laboratory, they were
thawed, weighted and examined for macroscopic characteristics. The sexual stages were estimated, according to
the following scale, adapted from Jolley (1977):
• IMMATURE- gonad small with no evidence of having spawned, tissue pink;
• RESTING- mature resting ovaries remain compact but weigh > 85g. Muscular ovarian tunic well developed
and thick. Color of tissue pinkish-orange and dark red;
• MATURING- ovaries enlarging because of vitellogenesis. Weight ≥ 200g, color changes from dark red to
yellowish-orange.
• RIPE- ovaries turgid, attaining maximum size of 2-4 kg and occupying most of the body cavity.
• SPENT- ovaries become flaccid and greatly reduced in weight from active and ripe phases. Color varies
progressively from reddish-orange to dark red.
The data were analyzed separately for the samples obtained from tuna longliners based in Natal and Cabedelo
(Area 1) and for those collected from the boats based in São Paulo and Rio de Janeiro (Area 2)(Table 1, Figure
1).
The sex ratio was analyzed by month, with the statistical significance of the differences being tested by the chisquare test (χ2), with the significance level of 5 percent. The monthly mean GI for females, excluding juveniles,
was calculated in order to evaluate the seasonal variation of reproductive activity. The gonad index (GI) was
calculated based on Cayré and Laloé, (1986), as follows:
⎛ GW ⎞ 4
GI = ⎜
⋅10
3 ⎟
⎝ LJFL ⎠
where GW is gonad weight (g) and LJFL is the lower jaw fork length (cm).
The length at which 50% of all individuals were sexually mature (L50) was estimated from a logistic model
(King, 1995), using the nonlinear least square procedure, described as:
P=
1
1 + exp[ − r ⋅ ( LJFL − L50)]
where P is the proportion of mature individuals within length class LJFL (5 cm length interval); r is the slope of
the curve describing the rate of changes in P from 0 to 1; and L50 is the LJFL at 50% sexual maturity.
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3. Results
3.1. Size composition and sex ratio
Area 1- A total of 153 specimens were examined from Area 1, 95 of which were females, ranging in LJFL from
114 to 210 cm (Figure 2), and 58 were males, ranging from 104 to 185 cm (Figure 3). Most of the females
were from 160 to 190 cm LJFL, with a mode in 170 cm, while most of the males showed a LJFL between 150
and170 cm, with a mode at 160cm, about 10 cm shorter than females. The overall sex ratio was 1.63 female to 1
male, which differed significantly (χ2 =8.947; p < 0.002) from the expected proportion of 1:1. Females
predominated in almost all months, except for May, August and December, but only in September the difference
was statistically significant (Table 2). The sex ratio analysis by size showed a predominance of males among
specimens with smaller size (except to 130 cm LJFL class), while females predominated in LJFL larger than160
cm (Table 3).
Area 2- Sixty two (62) specimens were examined from area 2, 32 of which were females, ranging in LJFL from
130 to 197 cm (Figure 2), and 30 were males, ranging from 133 to 176 cm LJFL (Figure 3). The LJFL
frequency distribution of females showed a higher frequency of specimens between 150 and 180 cm, with a
mode in 170 cm. For males, the LJFL frequency distribution showed a mode in 160 cm, with most specimens
ranging from 150 to 160. The estimated sex ratio for all samples was 1.06 females to 1 male, which not differed
significantly from the expected proportion 1:1 (Table 2). The proportion of females was higher than the
proportion of males in December and January, while males predominated in January, but the differences were
not significantly different from the expected ratio of 1:1 (p>0.05). The sex ratio analysis by size showed a
predominance of males in almost all size classes, except for 170 cm LJFL, where all specimens were females
(Table 3).
The relationship between the sex ratio and LJFL for both areas combined and for the specimens within the range
from 130 to 180cm, by 10 cm class interval, was calculated, as follows (Figure 4):
Sex ratio = 2x10-6*LJFL 7.172 (R 2=0.922)
3.2. Gonad development and spawning season
Female gonads (n=126) were found in five different maturity stages: immature, mature, resting, ripe and spent.
The ripe ova were surely the heaviest ones, reaching close to 3 kg, ranging from 1,263 to 2,740g (Figure 5). The
LJFL of ripe females ranged between 145 and 197 cm. Imature females, in turn, had a LJFL between 114 and
173 cm and GW from 37 to 180g. Maturing females ranged in size from 137 to 200 cm, with a GW from 127 to
1,166g. Resting females, with a LJFL between 171 and 210 cm, had a GW from 93.74 to 1226.44g. Finally, the
spent females presented a LJFL between 146 and 185 cm with a GW ranging from 310 to 1655g (Figure 5).
In Area 1 the spent phase was absent and only one specimen was ripe (1.1%). The great majority of the
specimens analyzed were in maturing stage (69.5%). Immature and resting stages accounted, respectively, for
(23.2%) (6.3%) (Figure 6). In contrast, in area 2 most of the specimens were either spent (recently spawned) or
ripe, representing, respectively, 46.9% and 37.5% of the sample (Figure 7).
In Area 1, females with maturing ovaries occurred in all sampled months, while immature females were more
frequent in January and February. The only ripe female was caught in November (Figure 8). In area 2, females
with ripe or spent ovaries were more frequent from December to February (Figure 9). The monthly gonad index
showed higher mean values in Area 2, in December and January, but was always higher than 2 (Figure 10). In
contrast, the monthly mean gonad index in Area 1 presented much smaller values, being always less than 1.5.
The largest values in Area 1 were observed in March and May (no data available from April) (Figure 10).
3.3. Length at first sexual maturity
The size at first sexual maturity (L50) was estimated at 154.9 cm LJFL (Figure 11), with a standard error (S.E.)
of 1.1. The proportion of mature females for each LJFL class was fitted to the following logistic regression:
P=
1
1 + exp[ −0.119( LJFL − 154.935)]
(pseudo-R2 = 0.975; n = 18; 5cm classes).
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4. Discussion
According to the results shown in the present work, the western equatorial Atlantic Ocean, off Brazilian coast, is
not a spawning ground for sailfish, since most of the specimens were either maturing or resting, with only one
ripe female being found in the sample. This is also supported by the low values of gonad index, when compared
to the fish caught off southern Brazil. Similar results were also reported by Souza et al. (1994). In contrast, the
southeast Brazilian coast seems to be an important spawning area for the species, with the spawning season
happening mainly from December to February. The vast majority of females caught in this area, during this
period of the year, were either ripe or spent, with high values of gonad indices. Important concentrations of
mature specimens in this area were previously reported by several authors (Arfelli and Amorim, 1981; Pimenta
et al., 2005).
The large proportion of females in early maturation in area 1, with sizes that are similar to those found in the
spawning ground off southeastern Brazil (Area 2), where most of females have ripe and spent ovaries, from
December to February, seems to support the hypothesis of a southward reproductive migration. The spatial
analysis of CPUE also seems to support it, since the highest value of CPUE in area 1 happened from July to
September, immediately prior to October, when the CPUE begins to increase in area 2, peaking in December
(Figure 12). As it has been shown to occur with white and blue marlin, this southward migratory movement is
probably related to the seasonal change of sea surface temperature, particularly to the displacement of surface
isotherms (Hazin, 1993). Several authors believe that the sailfish migration pattern is restricted to the 28°C
surface isotherm in several parts of the world (Ovchinnikov, 1970; Ueyanagi et al., 1970; Voss, 1972; Nakamura
1985), a sea surface temperature that in the area 2 of the present study always occur during the 1st and 4th
quarters of the year (Matsuura, 1986).
Evidence presented by Hazin et al. (2008), based on spatial catch prediction maps and size distribution
composition for the western South Atlantic, suggests that the larger sailfishes depart to more oceanic areas after
the spawning season. Probably the sailfish after spawning activity in southeast Brazilian coast, are driven
eastward, following the south Atlantic Gyre, in order to return to the tropical western tropical Atlantic area
(Peterson and Stramma, 1991). Beardsley (1980) also founded the largest sailfish in the eastern south Atlantic
off African coast. It is possible, therefore, that the sailfish, after the spawning season off southeast Brazil, move
as far as the eastern side of the South Atlantic.
Other important feature related to the reproductive cycle is the spatio-temporal changes in the sex ratio. In the
present study there was a general predominance of females in each season, mainly in the northern area. Similar
results were also observed by Hernández and Ramírez (1998) for the sailfish in the Pacific Coast of Mexico, but
differs from the finds obtained by Chiang et al. (2006) in the eastern Taiwan, where the sailfish females
proportion was lower than 0.5. Due to the small number of specimens analyzed, it was not possible to draw any
definitive conclusion on the seasonal variation of sex ratio, although it was close to 1:1, in the 1st quarter in area
2, which also helps to confirm the spawning season in the southern area. In general, the proportion of females
increased with size (Figure 4), a pattern that was also observed by Chiang et al. (2006). The relationship
between sex ratio and body size in the studied region can thus be used to reconstruct the sex composition from
catch data.
In general, there is a lack of exhaustive studies on sailfish sexual maturity. A first attempt to estimate the L50 of
sailfish in Brazilian waters was tried in the present paper, obtaining a LJFL of the 154.9 cm. Jolley (1977)
reports that female sailfish attains sexual maturity between 147-160 cm LJFL (13 to 18 kg). Recently, Arocha
and Marcano (2008) estimated that 50% of the females are mature at 180.2 cm LJFL based on macroscopic
assessment of gonad samples caught between 5°N and 25°N in western North Atlantic. In the Mexican Pacific
coast, Hernández and Ramírez (1998) estimated that 50% of the females mature at 175 cm EOFL (eye-orbit fork
length) (198.5 cm LJFL) based on histological analysis of gonads. The size at first sexual maturity found in the
present work was inside the interval proposed by Jolley (1977), but different from all other works cited above.
The reason for these differences might be a result of geographical isolation, stock structuring, different
environmental conditions, or sampling errors resulting from sample size and timing. The different fisheries
strategies are also a likely source of variation, due the non-selective nature of fishing gears.
The results of the present study seem to confirm the hypothesis that the sailfish spawns in the southeast Brazilian
coast during the1st and 4th quarter. New studies based on histological analysis of gonads are, however, needed, as
well as additional research, including tagging experiments, in order to better understand the migration route after
spawning. As the sample collection continues and more data on the reproductive biology of sailfish along the
1931
Brazilian coast are generated, a clearer comprehension of the spatial-temporal variation of the spawning ground
of sailfish, a crucial information for the management of this species, will hopefully be made possible.
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Acknowledgements
The first author wishes to thank to the CNPq for the PhD scholarship. The present work was made possible also
by funding from the Secretaria Especial de Aqüicultura e Pesca da Presidência da Republica do Brasil (SEAP).
Table 1. Number of sailfish sampled by year in each sub-area of equatorial and southwestern Atlantic Ocean.
Year
Month
2006
2007
2008
Area 1
Area 2
Area 1
Area 2
Area 1
Area 2
1
2
-
-
1
-
-
5
10
23
28
3
4
5
6
7
8
9
10
11
12
1
3
5
7
16
7
6
-
2
2
7
32
12
18
11
11
8
-
-
Total
45
-
85
11
23
51
Table 2. Monthly sex ratio of sailfish caught in equatorial and southwestern Atlantic Ocean.
Months
F
M
AREA 1
Sex Ratio
1
2
3
4
5
6
7
8
9
10
11
12
4
8
5
1
6
2
30
17
15
7
2
2
3
2
2
4
3
9
11
10
10
2:1
4:1
1.66:1
0.5:1
1.5:1
0.33:1
3.33:1
1.54:1
1.5:1
0.7:1
Total
95
58
1.63:1
χ
2
AREA 2
Sex Ratio
χ2
Pr(chi)
F
M
0.6667
3.600
0.500
0.333
0.400
0.200
11.308
1.286
1.000
0.529
0.4142
0.05778
0.4795
0.5637
0.5271
0.6547
0.0008*
0.2568
0.3173
0.4669
13
12
7
10
16
4
1.3:1
0.75:1
1.75:1
0.391
0.571
0.818
0.5316
0.4497
0.3657
8.9477
0.0028*
32
30
1.06:1
0.065
0.7995
*Values statiscally significatives with 95% confidence.
1933
Pr(chi)
Table 3. Sex ratio by LJFL size class of sailfish caught in equatorial and southwestern Atlantic Ocean.
LJFL class
F
AREA 1
M
Sex ratio
100|-110
110|-120
120|-130
130|-140
140|-150
150|-160
160|-170
170|-180
180|-190
190|-200
200|-210
210|-220
1
1
1
5
12
37
21
14
2
1
2
1
5
11
12
20
7
-
1:1
0.20:1
0.45:1
1.00:1
1.85:1
3.00:1
-
χ
2
0.0000
2.6667
2.2500
0.0000
5.0702
7.0000
-
Pr(chi)
F
M
1.0000
0.1025
0.1336
1.0000
0.0243*
0.0082*
-
1
3
7
6
12
2
1
-
5
4
8
11
2
-
AREA 2
Sex ratio
0.2:1
0.8:1
0.9:1
0.5:1
6.0:1
-
χ2
Pr(chi)
2.6667
0.1429
0.0667
1.4706
7.1429
-
0.1025
0.7055
0.7963
0.2253
0.0075*
-
*Values statiscally significatives with 95% confidence.
Figure 1. Geographical distribution of the sailfish sampled, by sex, in the two different sub-areas (Area 1:
sampled by observers on board longliners based in Natal- RN and Cabedelo- PB; Area 2: sampled by longliners
based in Cabo Frio- RJ and Santos- SP).
1934
Figure 2. Lower- Jaw Fork- Length (LJFL) frequency distribution of female sailfish cautght in the equatorial
and southwestern Atlantic.
Figure 3. Lower Jaw Fork Length (LJFL) frequency distribution of male sailfish cautght in the equatorial and
southwestern Atlantic.
s
1935
Figure 4. Relationship between the proportion of females and LJFL (10 cm interval class) for the sailfish caught
in the equatorial and southwestern Atlantic.
2500
immature
maturing
resting
ripe
spent
Gonad weight (g)
2000
1500
1000
500
0
100
120
140
160
180
200
LJFL (cm)
Figure 5. Relationship between LJFL and gonad weight by maturity stages.
1936
Figure 6. Relative participation of each maturity stage in Area 1.
Figure 7. Relative participation of each maturity stage in Area 2.
1937
Figure 8. Monthly relative participation of each maturity stage in Area 1.
Figure 9. Monthly relative participation of each maturity stage in Area 2.
1938
Area 2
1.5
Area 1
6
n=4
n=1
x
1.0
n=13
n=6
n=12
n=14
x
n=10
4
Gonadal Index
x
x
x
x
0.5
n=4
n=2
x
n=2
n=7
x
x
x
x
x
0.0
x
n=25
2
Gonadal Index
n=2
1
2
3
5
7
8
9
10
11
1
12
2
12
Months
Months
Figure 10. Box plot of gonad index of adult females of sailfish caught in the western south Atlantic. x point
represents the mean value.
Figure 11. Size at first sexual maturity (L50) of female sailfish estimated by the logistic curve.
1939
Figure 12. Monthly mean values of nominal CPUE of sailfish caught in in the equatorial and southwestern
Atlantic.
1940