Journal of the Marine Biological Association of the United Kingdom, 2012, 92(3), 633 641.

doi:10.1017/S0025315411000142

# Marine Biological Association of the United Kingdom, 2011

Age and growth of the snowy grouper,

Epinephelus niveatus, off the Brazilian coast
paulo a.s. costa1, adriana c. braga1, juan p. rubinich1, anto^nio olinto avila-da-silva2
and cassiano m. neto3
1
Universidade Federal do Estado do Rio de Janeiro, Laboratorio de Dinamica de Populacoes Marinhas, Departamento de Ecologia e
Recursos Marinhos, Avenida Pasteur, 458, Urca, Rio de Janeiro, RJ, 22290-240, Brazil, 2Centro APTA Pescado Marinho, Instituto de
Pesca, Av. Bartolomeu de Gusmao, 192, Ponta da Praia, Santos, SP, 11030-906, Brazil, 3Universidade Federal Fluminense,
Departamento de Biologia Marinha, Caixa-Postal 100644, Niteroi, RJ, 24001-970, Brazil

The age and growth of the snowy grouper, Epinephelus niveatus, from central and south-eastern Brazil were studied by
otolith analysis from a sample of 341 specimens, ranging from 325 to 1216 mm in total length (TL) caught with bottom
longlines between 1996 and 1998. Otolith length grew proportionally with the increasing TL of the sh. Marginal increment
analysis indicated that a single opaque band forms each year during autumn winter. The maximum estimated age was
54 years, which signicantly extends the previously estimated life-span of 21 29 years for this species. The von Bertalanffy
growth parameters for both sexes were estimated as L1 1098.4 mm TL, K 0.062 year 21 and t0 2.68. The study
revealed differences in mean length-at-age and size at recruitment, as well as in growth parameters between the central
and the south-eastern Brazilian coast, which can be attributed mainly to different shing pressures. The snowy grouper
was found at depths of 82 492 m, and showed a positive relationship between age and depth, suggesting differential
movements of older sh to deeper waters.
Keywords: growth, otoliths, Epinephelus niveatus, south-western Atlantic
Submitted 11 October 2010; accepted 6 January 2011; rst published online 4 March 2011

INTRODUCTION

The snowy grouper Epinephelus niveatus (Valenciennes,

1828) (Serranidae: Epinephelinae) is widely distributed in
the western Atlantic from Massachusetts (USA) to the Gulf
of Mexico, Bermuda, the Caribbean, and southern Brazil
(Heemstra et al., 2002). More than one-third of the Atlantic
latitudinal distribution of the snowy grouper lies in tropical
and subtropical Brazilian waters, with records extending
from the Amazon estuary to the southernmost limit at the
Uruguayan border (Heemstra & Randall, 1993). Recruits
and juveniles inhabit the shelter-rich, hard substrata along
the shore, whereas sub-adults and older sh tend to be
found on the shelf-edge, reaching maximum densities
beyond 150 m depth (Martins et al., 2005).
Because of its large size, wide bathymetric distribution and
high value, snowy grouper is one of the main targets of the
bottom line sheries operating off south-eastern and southern
Brazil. Although grouper landings in Brazil are not reported
separately by species, E. niveatus and Polyprion americanus
comprise most of bottom longline commercial landings.
These species have been traditionally shed with hand-line
and in the mid-1990s a new shing method with a steel
vila-da-Silva
cable and hydraulic winch was introduced (A
et al., 2001). From the 1980s to the mid-1990s the annual

Corresponding author:
P.A.S. Costa
Email: paulocosta.unirio@gmail.com

landings varied around 700 tonnes per year. After a fast

increase from 1995 to 1998 (up to 1500 tonnes were recorded
in 1996), due to the new shing method, annual landings of
groupers progressively decreased, reaching 307 tonnes in
2004 (Valentini & Pezzuto, 2006). After 2000, commercial
trawlers also started to land snowy grouper, tilesh
(Lopholatilus villarii) and sandperch (Pseudopercis numida),
as they expanded their activities to deeper shing grounds
vila-da-Silva, 2008).
(Okubo-da-Silva & A
The snowy grouper is also exploited by unregulated spearshing, artisanal and hook-and-line sheries on the tropical
(central) Brazilian coast, together with 11 other commercial
species of Epinephelinae (Costa et al., 2005; Martins et al.,
2005). The conservation status of grouper populations in
Brazilian waters is poorly known, but according to the
IUCN (2009) they can be classied as critically endangered
(E. nigritus and E. itajara), endangered (E. marginatus), nearthreatened (E. morio and Mycteroperca bonaci), vulnerable
(E. avolimbatus, E. niveatus and M. interstitialis), and
least concern species (E. mystacinus, E. adscensionis,
Cephalopholis fulva and M. microlepis).
Snowy grouper is a highly prized shery resource throughout its range (Wyanski et al., 2000), and plays an important
ecological role as an active top-predator at shelf-edge depths
(Dodrill & Manooch, 1993; Epperly & Dodrill, 1995).
Previous age and growth studies for the snowy grouper were
conducted within its northern distribution area, such as in
the South Atlantic Bight (Matheson & Huntsman, 1984;
Waltz, 1986; Wyanski et al., 2000) and in the Florida Keys
(Moore & Labisky, 1984). In Brazil, the only attempt to
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paulo a.s. costa et al.

estimate growth parameters for this species was carried out by

Ximenes-Carvalho et al. (1999), using scales from specimens
sampled from commercial (longline) landings.
In this study, we describe and compare age and growth of
the snowy grouper from off central and south-eastern Brazil,
based on age readings from sectioned otoliths. We also briey
discuss the implications of the snowy grouper life-history
characteristics, as they relate to the species management.

MATERIALS AND METHODS

Most sh used in this study were collected between 1996 and

1998 during two bottom longline surveys in central Brazil
from 158S to 228S (Martins et al., 2005) and in south-eastern
Brazil from 228S to 278S (Haimoivici et al., 2004) in the
depth-range of 82 to 492 m (Figure 1). Both surveys were
undertaken in the context of the large scale Brazilian research
programme REVIZEE (MMA, 2006) and were conducted
on-board commercial longline vessels leased from the industrial eet, following a pre-established sampling design.
Additional samples of small specimens were collected by
SCUBA divers in Cabo Frio (428W 238S) region (Figure 1).
For each sh caught, total weight (WT, kg) and total length
(TL, mm) were recorded, and, when possible, the sex was
determined.
Left otoliths (sagittae) were removed from 340 snowy
groupers and stored dry prior to processing for age analysis.
Each otolith was measured to its length antero-posterior

axis between the rostrum and post-rostrum and width

dorsal-ventral axis, mm.
Size and otolith relationships between the two areas were
compared using analysis of covariance (ANCOVA) to test
the hypothesis of parallelism between regression slopes and
equality of the intersections (Sokal & Rohlf, 1994). Prior to
the comparisons, the data were tested for normality and
homoscedasticity after logarithmic transformation. To test
for normality, we used the graph (q q plot) method and
the distribution of residuals. The Bartlett test was used to
test the homoscedasticity of variances within each group. In
all tests we used the same signicance level (a 0.05).
Transverse sections in the dorso-ventral plane, approximately 0.3 mm thick, were cut from each sagitta with a
Buehler Isomet low-speed saw. Sections were mounted on
glass slides with Canada balsam, and when necessary were
ground and polished with low-impact sandpaper. Age marks
were examined in a stereoscopic microscope (20 50),
under transmitted light. The opaque zones were counted
and considered for age determination. For growth analysis,
nine small specimens (157 165 mm TL) collected by
SCUBA-diving were included, to increase the number of
small sh in the tting of the growth curve.
The distance between the focus and the last age mark (Ri) and
between the otolith edge (R) were recorded from digitalized
images of each sagitta, using the UTHSCSA Image Tool free software. Monthly mean marginal increment (MI R Ri) ratios
were calculated for the most frequent age-classes in the sample
and used to determine the periodicity of mark formation.

Fig. 1. Fishing stations for snowy grouper caught with bottom longlines () and the location (D) where small specimens were collected by SCUBA divers (dive).

age and growth of epinephelus niveatus off brazil

Non-linear regression was used to estimate von Bertalanffy

growth equation parameters: Lt L1 (1 e2K(t2t0)), where
Lt is the TL in the age t (years), L1 (mm) is asymptotic
maximum length, K (year21) is the growth constant, and t0
(year) is the theoretical age at zero length. Likelihood ratio
methods (Kimura, 1980) were used to compare von
Bertalanffy growth parameters between the central and southeastern regions using the maximum-likelihood quotient, contrasted against a Chi-square table (gl, a 0.05), according to
Cerrato (1990) and Aubone & Wholer (2000). The growth
performance index was calculated according to the equation
of Pauly & Munro (1984): f Log(K ) + 2Log(L1) and
was used to compare growth rates obtained in previous
studies.
Age distribution along the bathymetric range in both areas
was also described and compared using linear regression and
ANCOVA (Sokal & Rohlf, 1994). Deviations in the sex-ratio
were compared using the Chi-square test (a 0.05).

RESULTS

Size and age composition

The TL of snowy grouper obtained from longline shing
ranged between 345 and 1216 mm. Both the smallest and
the largest sh were recorded in the central area. In the southeastern area, sizes ranged from 420 to 1130 mm TL.
Length frequency distributions for each shing region
(central and south-eastern) were grouped into 50-mm class
intervals. A polymodal shape was observed in histograms
for both areas. In the central area, 19.5% of sh were
between 725 and 750 mm TL and 71% between 600 and
675 mm TL (Figure 2). In the south-eastern area, 16% of the
sh were between 625 and 675 mm TL and 71% between
625 and 925 mm TL. Snowy groupers were found at depths
of 82 492 m. The majority of the sh (91%) were recorded
between 120 and 300 m. Depths between 180 and 240 m
accounted for 63% and 31% of all sh caught, respectively,
in the south-eastern and central regions (Figure 3).
A low, but signicant relationship (R2 0.04, P 0.024)
between age and depth was observed in the central region
(Figure 4). Conversely, in the south-eastern region
(Figure 5), older sh tended to be more clearly associated
with greater depths (R2 0.28, P , 0.001).

Fig. 3. Distribution for snowy grouper according to depth of capture in the

central (black bars) and south-eastern (white bars) regions. Numbers on
x-axis represent the lower limit of depth-classes.

This analysis considered exclusively age groups between 7

and 28 years, which represented 84.8% of all data. Fish older
than 28 years with a low frequency in the samples, were
excluded due to loss of normality. Analysis of covariance
showed that the regressions between the two regions were signicantly different regarding their slopes (P , 0.001) and
intercept coefcients (P 0.024).
Parameters of the length weight relationship were not signicantly different between the two regions when comparing
their slopes (P 0.855) and intercept coefcient (P 0.167).
The transformed (logarithmic) data were homoscedastic, and
the residuals were normally distributed. ANCOVA indicated
that both slope and regressions between the two regions
were similar (P 0.058). The general model showing the
relationship between TL and WT for snowy groupers
from both regions is: WT 0.0000410.TL2.846 (R2 0.995;
N 298).

Otolith growth
The initial dorso-ventral growth is replaced by a left right
growth, and new increments are formed perpendicularly to
the otoliths width (Figure 6). This also leads to allometric
growth of otolith length in relation to its width.

Sex and age distribution

There was a highly signicant (P , 0.001) deviation from
unity in the sex-ratio, with males poorly represented in the

Fig. 2. Length frequency distribution for snowy grouper collected in the

central (black bars) and south-eastern (white bars) regions. Numbers on
x-axis represent the lower limit of length-classes.

Fig. 4. Relationship between snowy grouper age and depth of capture in the
central region.

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paulo a.s. costa et al.

Fig. 5. Relationship between snowy grouper age and depth of capture in the
south-eastern region.

samples. A signicant difference in sex-ratio was also observed

between the two regions (P 0.006). The youngest sh was 5
years old, and only one specimen of this age was recorded in
each region. The oldest sh (54 years) was found in the central
region. There was a higher frequency of younger sh (,10
years) in the south-eastern region (18 %) than in the central
region (6%).
Fish smaller than 475 mm TL were all males. In all other
length-classes except the largest, females tended to predominate in the samples (Figure 7). Younger sh (,10 years)
were associated with shallower depths, mainly down to
180 m, and were absent from depths greater than 240 m.
Older sh (11 54 years) occurred in all depths. Both young
and old sh were observed in higher numbers in the same
depth-range, between 180 and 210 m (Figure 8).

Validation
To analyse the periodicity of growth marks, we used the marginal increment analysis from 305 otoliths of the mostpopulated age-classes (14, 16, 17 and 20 years). The decrease
in the mean marginal increment values indicates that growth
opaque marks are probably formed between May and June.
The lack of samples during the following months precludes
a more-detailed interpretation of the deposition period, but
it probably extends up to October, when low values can still
be observed (Figure 9). The non-parametric Kruskal Wallis
test applied to the data indicated that the medians were
statistically different (P 0.0005).

Fig. 6. Images from otolith sections of snowy grouper at different ages,

showing the ontogenetic changes (from left to right) in the growth of
otoliths. Left to right: 14, and 30 years.

Fig. 7. Length2frequency distribution for males and females of the snowy

grouper. Numbers on x-axis represent the lower limit of length-classes.

Age and growth

Growth parameters for the von Bertalanffy model were calculated for both regions and using all data, as a global model
(Table 1).
Length-at-age data for each region are presented together
with their respective tted curve (Figure 10). The von
Bertalanffy model tted well to the data, showing small condence intervals. The curves overlapped along the age-classes,
suggesting that only one model could adequately describe
the observed data. Juveniles caught by SCUBA-diving (N
9) improved the estimates of t0 values for the two data sets,
and are also shown. The narrow range of the condence intervals observed in the estimates of growth parameters suggests a
relatively precise estimation of each component of the von
Bertalanffy growth model.
Condence intervals and comparisons for snowy grouper
growth parameters between regions were deduced from
maximum-likelihood scenarios (Figure 11). This methodology
is necessary because of the asymmetry in the probability distribution, which arises as a product from the combination
(interaction) of growth parameters. These asymmetries were
more evident in the probabilities of L1 and t0. The gure
also evidences the similarities of K between the two areas.
As shown in Table 2, the hypothesis of a global (unique)
model, with equality of the growth parameters L1, K and
t0 was rejected (P 0.013). The models for the two populations showed that the pairs L1 and t0 (P 0.104) and K

Fig. 8. Distribution of younger (,10 years) and older (11258 years) snowy
grouper catches in relation to depth of shing. Numbers on x-axis represent
the lower limit of depth-classes.

age and growth of epinephelus niveatus off brazil

Fig. 9. Mean marginal increment (mm) for snowy grouper. Vertical lines
indicate the standard error (SE), and numbers indicate the sample size.

and t0 (P 0.136) were not statistically different, but the combination of L1 and K showed a signicant change (P 0.011).
In contrast, when each parameter was tested separately, the
differences were not signicant (P . 0.05). This indicates
that differences between the models result from the parameter
interaction.
Fig. 10. Snowy grouper length-at-age data for the sexes combined. Fitted von
Bertalanffy growth curve for both regions, as a global model (A). Growth
curves for snowy grouper, tted with parameters available in the literature (B).

DISCUSSION

In the south-eastern region, the snowy grouper was completely recruited to the longline at smaller sizes when compared
to the central region. This difference could not be attributed to
gear-selectivity, since the same gear was used in both regions.
Similarly, the sh were sampled within the same seasons
(spring and autumn) and with similar shing effort. The
central region shows a higher degree of environmental complexity, which provides more shelter for juveniles and subadults. Nevertheless, in the longline shery, sh are attracted
by the bait, and thus, their accessibility could not be solely
affected by shelter availability (Haimovici et al., 2004;
Martins et al., 2005). With the initial hypothesis discarded,
we may assume that differences in size-at-recruitment resulted
from a differential recruitment of sh to the shing gear, with
the snowy grouper recruiting at smaller sizes to the shing
gear in south-eastern Brazil.
Despite the increase of landings of snowy grouper between
1994 and 2000 as the introduction of industrial longline was
observed, shing areas and eet dynamics did not change in
subsequent years. The cycle of industrial longline shery
was relatively short (Haimovici et al., 2006; Valentini &
Pezzuto, 2006) when compared with the estimated longevity
for the species. For these reasons it is believed that the
growth parameters calculated in this study may still be
applied to snowy grouper stocks off the Brazilian coast.
Table 1. Von Bertalanffy growth parameters calculated for snowy
grouper from off the Brazilian coast, using all data.
Models

L1 + CI

K + CI

to + CI

Central

1132.3
(1061/1228)
1078.2
(1023/1146)
1098.4

0.061
(0.049/0.074)
0.060
(0.050/0.071)
0.062

2.37
(1.24/3.82)
3.22
(2.05/4.64)
2.68

165

South-eastern
Global

N, number; CI, condence interval (in parentheses).

176
341

The age composition of samples included a higher proportion of juveniles in the south-eastern region. This may
be related either to the recruitment of younger sh to the
shing grounds, or increased overshing, as most of the
target stocks on the south-eastern Brazilian coast have been
reported as over-exploited (Haimovici et al., 2003). The differences observed in the sex-ratio are a common feature of the
life-cycle in hermaphroditic protogynous serranids (Shapiro,
1987; Jennings et al., 2001), and have been specically
recorded for snowy grouper populations. In some cases,
these variations were associated with differential shing mortality (Moore & Labisky, 1984; Wyanski et al., 2000). As males
are normally larger than females, they become more vulnerable to shing. This selective effect, reducing the number of
males from their social assemblages, can also affect the reproductive success (Shapiro, 1987; Coleman et al., 1999, 2000).
Sagittal otoliths of E. niveatus grow proportionally through
the life of the sh, and display a regular and interpretable
pattern of growth marks, which can be used to assess the
age of an individual. Although E. niveatus otoliths grow continuously with TL, growth becomes asymmetrical over time,
as a result of ontogenetic changes. The initial growth rate
along the dorso-ventral axis declines after a few years and is
replaced by an increased rate of growth on the proximal
distal edge, when new increments are formed perpendicularly
to the otoliths width, thickening the structure. This also leads
to allometric growth of otolith length in relation to its width.
Only the relationship between otolith length and weight
was isometric. Similar asymmetries in otolith growth have
been described in E. niveatus by Wyanski et al. (2000),
Epinephelus marginatus (Renones et al., 2007) and several
other species (Beamish & McFarlane, 1987; Casselman, 1990).
Marginal increment analysis, based on incomplete seasonal
samples, indicated that peak annulus formation probably
occurred from May to June, in agreement with Matheson &

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paulo a.s. costa et al.

Fig. 11. Distribution of probabilities of growth parameters (L1, K and t0) for snowy grouper, by the maximum-likelihood method in the central (dotted line) and
south-eastern (solid line) regions.

Huntsman (1984) and Moore & Labisky (1984), who found

that increment formation appeared to begin in April and
peaked in June. Waltz (1986) found a wide period of increment formation and was not able to conclude that deposition
was annual, due to a lack of samples from the entire year.
These results are also in agreement with those found by
Wyanski et al. (2000), who assumed an annual period of deposition, with only one increment formed in April May, corresponding to the beginning of the spawning season. As noted
by Renones et al. (2007), the marks develop at the same
time in juveniles and adults, which suggests that the mechanism that regulates band formation cannot be related solely to
somatic growth or to reproductive activity. The most probable
hypothesis is that band formation is an independent physiological process, more directly responsive to environmental
variations (Wright et al., 2002). Although marginal increment
analysis is not recommended for long-lived sh, it is one of the
most commonly used methods to assess annulus formation,
mainly due to its modest sampling requirements and low
cost (Campana, 2001). All previous growth and age studies
of snowy grouper populations also used marginal increment
analysis as a validation method. Considerable evidence indicates that almost all tropical serranids, lutjanids and sparids
so far studied do indeed deposit increments annually (Choat
et al., 2009), including several species in which annual periodicity of increment formation has been conrmed independently by bomb radiocarbon analysis.
The snowy grouper can be considered a long-lived species,
with a slow growth rate and a life-span estimated from 22
(Wyanski et al., 2000) to 54 years (present study). The
maximum age of 54 years found in this study considerably

extends previous estimates. This may possibly be explained

by the extremely low growth coefcient (K , 0.061) estimated
for populations in Brazilian waters (Table 3), which was
notably less than those estimated by Wyanski et al. (2000)
for this species off North Carolina and South Carolina
(0.103 , K , 0.119). Epinephelus niveatus exhibits high individual variation of TL at age. This makes TL a poor predictor
of age for this species. This discrepancy and the greater longevity reported here, result in slower increase in TL with age,
and as a consequence a greater discrepancy between this
and previous growth curves.
The comparison of growth parameters for snowy grouper,
using data from the literature, indicates that the Brazilian
coastal population shows the lowest growth rates estimated
for snowy grouper populations in the Atlantic. It is worth
noting that all sh from these studies were aged using the
same method.
Growth parameters estimated for the North Atlantic populations were, in general, higher than those estimated in the
present study, and some fall within the condence intervals
calculated for Brazilian waters. According to Wyanski et al.
(2000), the higher L1 values observed in the rst two
studies (Matheson & Huntsman, 1984; Moore & Labisky,
1984) resulted from the non-existence of an asymptotic
shape in the growth curves, mainly due to the low number
of large-sized sh (.900 mm TL).
A study on growth and mortality of the snowy grouper is
available for southern Brazil (Ximenes-Carvalho et al.,
1999). Unfortunately, in this study, the authors used scales
to assess age. Because scales normally present several problems such as regeneration, reabsorption, and low legibility

Table 2. Results of the hypothesis testing for the equality of growth parameters between the populations of snowy grouper off the central and southeastern Brazilian coast. Probabilities in bold type indicate statistically signicant values.
Parameters
Parameters

L1

to

L1, K, to

L1, K

L1, to

K, to

L1 (central)
L1 (south-eastern)
k (central)
k (south-eastern)
to (central)
to (south-eastern)

1132
1078
0.0608
0.0603
22.37
23.22

1106
1106
0.0646
0.0561
22.16
23.58

1134
1077
0.0606
0.0606
22.39
23.19

1146
1065
0.0581
0.0635
22.78
22.78

1105
1105
0.0608
0.0608
22.75
22.75

1099
1099
0.0614
0.0614
23.01
22.55

1101
1101
0.0630
0.0593
22.81
22.81

1132
1078
0.0602
0.0602
22.89
22.89

2229740

2237110
1
3.84
0.280

2229765
1
3.84
0.950

2235133
1
3.84
0.358

2299068
3
7.81
0.013

2288337
2
5.99
0.011

2259367
2
5.99
0.104

2255865
2
5.99
0.136

Statistics
SQ
gl.
x2 (0.05; gl)
Probability

age and growth of epinephelus niveatus off brazil

Table 3. Growth parameters for snowy grouper, taken from the literature. N, sample size; Lmax, maximum recorded length; L1, asymptotic length; K,
growth constant; to, age at zero length; f , growth performance index from Pauly & Munro (1984). The parameters that fall within the condence interval
calculated for the present study are in bold type.
Period

Country

Region

Lmax

L1

to

1972 2 1979a
1978 2 1981b
1979 2 1985c
1982 2 1985d
1993 2 1994d
1993 2 1994d
1996 2 1997e
1996 2 1998e

USA
USA
USA
USA
USA
USA
Brazil
Brazil

North and South Carolina

Florida Keys
South Carolina
South Carolina
North Carolina
South Carolina
Central Brazil
South-eastern Brazil

536
178
326
163
311
1218
165
176

1130
1180
1090
1034
1110
1137
1216
1130

1255
1320
970
948
1201
1117
1132
1078

0.074
0.087
0.109
0.122
0.103
0.119
0.061
0.060

2 1.92
21.01
22.12
20.67
2 1.14
2 1.41
2 2.89
2 2.89

7.06
7.32
6.93
7.00
7.30
7.30
6.66
6.56

Matheson & Huntsman, 1984, bMoore & Labisky, 1984, cWaltz, 1986, dWyanski et al., 2000, ePresent study.

of rings in older sh, there is a dangerous tendency to underestimate ages by this method (Beamish & McFarlane, 1995;
Masuda et al., 2000).
According to Fowler (2009), many tropical species have
been found to be remarkably long-lived, contrary to the previous belief that tropical sh species are short-lived. Such
unexpected longevity is true not only for those species that
attain a large maximum size, for which it might be expected
that older individuals attain some protection from predation
because of their size, but also applies to the small reefassociated species. Several pomacentrid species from the
Galapagos Islands even reached .30 years of age, despite
barely attaining 100 mm TL (Meekan et al., 2001). Several
species of acantaurids had some of the highest estimates of
maximum age, with Acanthurus lineatus living up to 42
years, although it attains only 183 mm TL (Choat & Axe,
1996; Choat & Robertson, 2002).
Similarly, the small serranid Cephalopholis cyanostigma,
which grows to 350 mm TL, reaches up to 46 years of age
(Mosse et al., 2002), whilst the tropical snapper Lutjanus
bohar attains a maximum age of 54 years (Marriott, 2002).
The greater longevity reported here for E. niveatus (54
years-old) indicates that this species, along with Epinephelus
caninus (55 years-old; Morales-Nn et al., 2005), Epinephelus
nigritus (41 years-old; Manooch & Manson, 1987) and
Epinephelus marginatus (61 years-old; Renones et al., 2007)
attain the greatest ages of the Epinephelus species aged to date.
In the south-western Atlantic, other examples of extreme
longevity in commercial species include the wrecksh
Polyprion americanus attaining 120 cm TL and living up to
76 years (Peres & Haimovici, 2003) and Helicolenus lahillei,
living up to 44 years and attaining around 50 cm TL
(Bernardes et al., 2005).
The von Bertalanffy growth model was statistically different when considering the entire set of parameters (L1, K
and t0) from the south-eastern and central Brazilian waters.
Maximum-likelihood scenarios indicated that these differences arise only by the interaction of L1 and K factors.
When factors are analysed individually, the parameters
showed no signicant differences (P . 0.05). This suggests
that although the populations exhibit similar growth rates,
they reach smaller mean lengths by age-classes, leading to a
small maximum length in the south-eastern region. Possibly
these discrepancies can be explained by higher levels of
shing mortality caused by the industrial longline eet,
which historically concentrated its shing effort in the
southern Brazilian shing grounds (MMA, 2006). Because

of its large size and abundance, E. niveatus was considered

one of the most prized species of the demersal Brazilian sheries. Nevertheless, the species has never been subjected to
specic regulations for its conservation.
The positive relationship between age and depth suggests
the existence of a migratory behaviour as sh increase in
size. The same pattern was found by Dodrill & Manooch
(1993) and Moore & Labisky (1984), who explained the movement of sh to deeper waters as a result of sexual maturation.
Heemstra & Randall (1993) stated that this behaviour is a
common strategy in species of Epinephelus. However, the
highest densities of snowy grouper were recorded at the shelfbreak and upper slope, between 150 and 280 m. These ndings are in accordance with the distribution of higher shing
yields between 100 and 300 m, as recorded by Haimovici
et al. (2004) and Martins et al. (2005).
The snowy grouper, similarly to the majority of other largesized Epinephelinae, is a top-predator and a slow-growing
species. The long and late maturation process, together with
the complexity of the protogynous sex-reversal phenomenon,
makes it seriously vulnerable to over-exploitation (Heemstra
& Randall, 1993; Coleman et al., 2000; Morris et al., 2000).
According to the rst classication of the IUCN, the snowy
grouper was considered a vulnerable species, mainly
because of its restricted geographical distribution and fragmented populations, with low densities of mature individuals
(Morris et al., 2000). Of the 85 species of Epinephelinae
studied by the IUCN, Epinephelus niveatus was considered
one of the 20 threatened species with a greater need for conservation. In the Brazilian shery scenario, this classication is
supported by the rapid decrease of snowy grouper landings in
the past 10 years (Haimovici et al., 2003), the predominance of
immature small-sized individuals in the commercial landings,
and changes in the population parameters such as those documented in this study.

ACKNOWLEDGEMENTS

We are grateful to Jean L. Valentin (UFRJ), who was very generous with his time and support during the coordination of
the REVIZEE Program. We thank the captains and crews of
the longline vessels Cricare, Margus I and Margus II for
helping us to carry out the shing surveys. We are also grateful
to all research collaborators, especially Eduardo B.F. Netto and
Luiz Ricardo Gaelzer (IEAPM) for assistance during the
cruises and biological sampling. The authors would like to

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paulo a.s. costa et al.

thank two anonymous referees for critically reading the

manuscript. This study was partially funded through grants
from CNPq (Brazilian Science Council) to P.A.S. Costa
(304131/2007-5).

REFERENCES
Aubone A. and Wohler O.C. (2000) Aplicacion del metodo de maxima
verosimilitud a la estimacion y comparacion de curvas de crecimiento
de von Bertalanffy. INIDEP Informe Tecnico 37, 1 21.
vila-da-Silva A.O., Bastos G.C. and Tutui S.L. (2001) A atividade pesA
queira do Estado de Sao Paulo: analise das capturas do bienio 1998
1999 com espinhel-de-fundo. Boletim do Instituto de Pesca, Sao
Paulo 27, 3338.
Beamish R.J. and McFarlane G.A. (1987) Current trends in age determination methodology. In Summerfelt R.C. and Hall G.E. (eds) Age and
growth of sh. Ames, IA: Iowa State University Press, pp. 1542.
Beamish R.J. and McFarlane G.A. (1995) A discussion of the importance
of aging errors, and an application to walleye pollock: the worlds
largest shery. In Secor D.H., Dean J.M. and Campana S.E. (eds)
Recent developments in sh otolith research. Columbia, SC:
University of South Carolina Press, pp. 545 565.
Bernardes R.A., Mello G.P.M.B. and Cergole M.C. (2005). Helicolenus
vila-da-Silva A.O.,
lahilei (Norman, 1937). In Cergole M.C., A
Rossi-Wongtschowski C.L.D.B. (eds) Analise das principais pescarias
comerciais da regiao sudeste-sul do Brasil: Dinamica populacional
das especies em explotacao, pp. 5761.
Campana S.E. (2001) Accuracy, precision and quality control in age
determination, including a review of the use and abuse of age validation methods. Journal of Fish Biology 59, 197242.
Casselman J.N. (1990) Growth and relative size of calcied structures of
sh. Transactions of the American Fisheries Society 119, 673 688.
Cerrato R.M. (1990) Interpretable statistical tests for growth comparisons
using parameters in the von Bertalanffy equation. Canadian Journal of
Fisheries and Aquatic Sciences 47, 14161426.
Choat J.H. and Axe L.M. (1996) Growth and longevity in acanthurid
shes: an analysis of otolith increments. Marine Ecology Progress
Series 134, 1526.
Choat J.H. and Robertson D.R. (2002) Age-based studies. In Sale P.F.
(ed.) Coral reef shesdynamics and diversity in a complex ecosystem.
San Diego, CA: Academic Press, pp. 5788.
Choat J.H., Kritzer J.P. and Ackerman J.L. (2009) Ageing in coral reef
shes: do we need to validate the periodicity of increment formation
for every species of sh for which we collect age-based demographic
data? In Green B.S., Mapstone D.B., Carlos G. and Begg G.A. (eds)
Tropical sh otoliths: information for assessment, management and
ecology. Reviews: methods and technologies in sh biology and sheries
11. Berlin: Springer Science + Business Media B.V., pp. 2354.
Coleman F.C., Koenig C.C., Eklund A.M. and Grimes C.B. (1999)
Management and conservation of temperate reef shes in the
groupersnapper complex of the southeastern United States. In
Musick J.A. (ed.) Life in the slow lane: ecology and conservation of longlived marine animals. Proceedings of the Symposium Conservation of
Long-Lived Marine Animals, Monterey, California, USA 24 August
1997. American Fisheries Society Symposium 23, pp. 233 242.
Coleman F.C., Koenig C.C., Huntsman G.R., Musick J.A., Eklund
A.M., McGovern J.C., Chapman R.W., Sedberry G.R. and Grimes
C.B. (2000) Long-lived reef shes: the groupersnapper complex.
Fisheries 25, 1420.
reas de pesca e rendiCosta P.A.S., Olavo G. and Martins A.S. (2005) A
mentos da frota de linheiros na regiao central da costa brasileira entre

SalvadorBA e Cabo de Sao TomeRJ. In Costa P.A.S., Martins A.S.

and Olavo G. (eds) Pesca e potenciais de exploracao de recursos vivos na
regiao central da Zona Economica Exclusiva brasileira. Rio de Janeiro:
Museu Nacional (Serie Livros, n.13), pp. 5770.
Dodrill J.W. and Manooch A.B. (1993) Food and feeding-behavior of
adult snowy grouper, Epinephelus niveatus (Valenciennes) (Pisces,
Serranidae), collected off the central North-Carolina coast with ecological notes on major food groups. Brimleyana, 101135.
Epperly S.P. and Dodrill J.W. (1995) Catch rates of snowy grouper,
Epinephelus niveatus, on the deep reefs of Onslow Bay, Southeastern
USA. Bulletin of Marine Science 56, 450461.
Fowler A.J. (2009) Age in years from otoliths of adult tropical sh. In
Green B.S., Mapstone D.B., Carlos G. and Begg G.A. (eds) Tropical
sh otoliths: information for assessment, management and ecology.
Reviews: methods and technologies in sh biology and Fisheries 11.
Berlin: Springer Science + Business Media B.V., pp. 5592.
vila-da-Silva A.O., Lucato S.H.B., Velasco G. and
Haimovici M., A
Arantes L.H. (2003) A pesca de linha-de-fundo na plataforma
externa e talude superior da regiao sudeste-sul do Brasil em 1997 e
1998. In Cergole M.C. and Rossi-Wongtschowski C.L.D.B. (eds)
Analises das principais pescarias comerciais do sudestesul do Brasil:
Dinamica das Frotas. Sao Paulo: Programa REVIZEE/MMA/
SECIRM. Evoluir, pp. 347 363.
vila-da-Silva A.O., Tutui S.L.S., Bastos G.C.C., Santos
Haimovici M., A
R.A. and Rossi-Wongtschowski C.L.D.B. (2004) Prospeccao pesqueira de especies demersais com espinhel-de-fundo na regiao
vila-da-Silva A.O. and
sudeste-sul do Brasil. In Haimovici M., A
Rossi-Wongtschowski C.L.D.B. (eds) Prospeccao pesqueira de especies
demersais com espinhel-de-fundo na zona economica exclusiva da
regiao sudeste-sul do Brasil. Sao Paulo: Instituto Oceanograco,
Universidade de Sao Paulo, pp. 1 112.
Haimovici M., Rossi-Wongtschowski C.L.D.B., Cergole M.C.,
vila-da-Silva A.O. (2006)
Madureira L.S., Bernardes R.A. and A
Recursos Pesqueiros da Regiao Sudeste-Sul. Avaliacao do potencial sustentavel de recursos vivos na Zona Economica Exclusiva do Brasil
(MMA). Braslia: MMA, pp. 207242.
Heemstra P.C. and Randall J.E. (1993) Groupers of the world (family
Serranidae, subfamily Epinephelinae). An annotated and illustrated
catalogue of the grouper, rockcod, hind, coral grouper and lyretail
species known to date. FAO species catalogue. Volume 16. Rome:
FAO, 382 pp.
Heemstra P.C., Anderson W.D. and Lobel P.S. (2002) Serranidae.
Groupers (seabasses, creolesh, coney, hinds, hamlets, anthiines, and
soapshes). In Carpenter K.E. (ed.) FAO species identication guide
for shery purposes. The living marine resources of the Western
Central Atlantic. Volume 2: Bony shes part 1 (Acipenseridae to
Grammatidae). Rome: FAO, pp. 13081369.
IUCN (2009) IUCN Red List of Threatened Species. Version 2009.2.
,www.iucnredlist.org. (accessed 26 February 2010).
Jennings S., Kaiser M.J. and Reynolds J.D. (2001) Marine sheries
ecology. Oxford: Blackwell, 417 pp.
Kimura D. (1980) Likelihood methods for the von Bertalanffy growth
curve. Fishery Bulletin 77, 765766.
Manooch C.S. and Manson D.L. (1987) Age and growth of the Warsaw
grouper, and black grouper from the southeast region of the United
States. Northeast Gulf Science 9, 6575.
Marriott R. (2002) Age, growth and sex structure of red sea bass populations on the Great Barrier Reef. In Williams A.J., Welch D.J.,
Muldoon G., Marriott R., Kritzer J.P. and Adams S. (eds) Bridging
the gap: a workshop linking student research with sheries stakeholders.
CRC Reef Research Centre Technical Report No. 48. Townsville, QL:
CRC Reef Research Centre, pp 8593.

age and growth of epinephelus niveatus off brazil

Martins A.S., Olavo G. and Costa P.A.S. (2005) Recursos demersais capturados com espinhel-de-fundo no talude superior da regiao entre
Salvador (BA) e o Cabo de Sao Tome (RJ). In Costa P.A.S., Martins
A.S. and Olavo G. (eds) Pesca e potenciais de exploracao de recursos
vivos na regiao central da Zona Economica Exclusiva brasileira. Rio
de Janeiro: Museu Nacional (Serie Livros, n.13), pp. 109 228.
Masuda Y., Ozawa T., Onoue O. and Hamada T. (2000) Age and growth
of the athead, Platycephalus indicus, from the coastal waters of west
Kyushu, Japan. Fisheries Research 46, 113121.
Matheson R.H. and Huntsman G.R. (1984) Growth, mortality, and
yield-per-recruit models for speckled hind and snowy grouper from
the United States South Atlantic Bight. Transactions of the American
Fisheries Society 113, 607616.

Peres M.B. and Haimovici M. (2003) Age and growth of southwestern

Atlantic wrecksh Polyprion americanus. Fisheries Research 66,
157169.
Renones O., Pineiro C. and Goni R. (2007) Age and growth of the dusky
grouper Epinephelus niveatus (Lowe, 1834) in an exploited population
of the western Mediterranean Sea. Journal of Fish Biology 71, 346362.
Shapiro D.Y. (1987). Reproduction in groupers. In Polovina J.J. and
Ralston S. (eds) Tropical snappers and groupers: biology and sheries
management. Boulder, CO: Westview Press, pp. 295 327.
Sokal R.R. and Rohlf F.J. (1994) Biometry. 3rd edition. New York: W.H.
Freeman and Co., 880 pp.

Meekan M.G., Ackerman J.L. and Wellington G.M. (2001) Demography

and age structures of coral reef damselshes in the tropical eastern
Pacic Ocean. Marine Ecology Progress Series 212, 223 232.

Valentini H. and Pezzuto P.R. (2006) Analise das principais pescarias

comerciais da Regiao Sudeste-Sul do Brasil com base na producao controlada no perodo 1986 2004. Serie Documentos Revizee: Score Sul,
Instituto Oceanograco Universidade de Sao Paulo, Sao Paulo, 56 pp.

MMA (Ministerio do Meio Ambiente) (2006) Programa REVIZEE:

Avaliacao do Potencial Sustentavel de Recursos Vivos na Zona
Economica Exclusiva. Braslia: Relatorio Executivo Ministerio do
Meio Ambiente, 279 pp.

Waltz W. (1986) The size and age of snowy grouper (Epinephelus niveatus) in the South Atlantic Bight. Charleston, SC: South Carolina
Department of Natural Resources, 30 pp.

Moore C.M. and Labisky R.F. (1984) Population parameters of a relatively unexploited stock of snowy grouper in the Lower Florida
Keys. Transactions of the American Fisheries Society 113, 322329.
Morales-Nn B., Bauza D. and Grau A.M. (2005) Otolith characteristics
and age estimation of an exceptionally old dogtooth grouper
(Epinephelus caninus) captured off Majorca Island (western
Mediterranean). Cybium 29, 100102.
Morris A.V., Roberts C.M. and Hawkins J.P. (2000) The threatened
status of groupers (Epinephelinae). Biodiversity and Conservation 9,
919942.
Mosse J.W., Adams S. and Welch D.J. (2002) Bommie cod
(Cephalopholis cyanostigma): a big surprise from a little sh. In
Williams A.J., Welch D.J., Muldoon G., Marriott R., Kritzer J.P. and
Adams S. (eds) Bridging the gap: a workshop linking student research
with sheries stakeholders. CRC Reef Research Centre Technical
Report No. 48. Townsville, QL: CRC Reef Research Centre, pp. 94
107.
vila-da-Silva A.O. (2008) Estrutura das associaOkubo-da-Silva S. and A
coes de peixes demersais da Bacia de Santos: Resultados da pesca
comercial de arrasto. In Elisabete de Santis Braga (Org.)
Oceanograa e Mudancas Globais. Volume 1. Sao Paulo:
Universidade de Sao Paulo, pp. 185197.
Pauly D. and Munro J.L. (1984) Once more on the comparison of growth
in sh and invertebrates. Fishbyte 2, 21.

Wright P.J., Panli J., Morales-Ln B. and Greffen A.J. (2002) Types of
calcied structures otoliths. In Panli J., Pontual H., Troadec H. and
Wright P.J. (eds) Manual of sh sclerochronology. Brest: Ifremer
IRD co-edition, pp. 3157.
Wyanski D.M., White D.B. and Barans C.A. (2000) Growth, population
age structure, and aspects of the reproductive biology of snowy
grouper, Epinephelus niveatus, off North Carolina and South
Carolina. Fishery Bulletin 98, 199218.
and
Ximenes-Carvalho M.O., Fonteles-Filho A.A., Almeida-Tubino R.,
Andrade-Tubino M.F and Pinto-Paiva M. (1999) Parametros de
crescimento e mortalidade do cherne, Epinephelus niveatus
(Valenciennes) (Osteichthyes: Serranidae), no sudeste do Brasil.
Arquivos de Ciencias do Mar 32, 111 117.

Correspondence should be addressed to:

P.A.S. Costa
Universidade Federal do Estado do Rio de Janeiro
Laboratorio de Dinamica de Populacoes Marinhas
Departamento de Ecologia e Recursos Marinhos
Avenida Pasteur, 458, Urca, Rio de Janeiro, RJ, 22290-240,
Brazil
email: paulocosta.unirio@gmail.com

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