ACTA ICHTHYOLOGICA ET PISCATORIA (2015) 45 (1): 1–11 DOI: 10.3750/AIP2015.45.1.

01

DIET AND REPRODUCTION OF THE GOLIATH GROUPER, EPINEPHELUS ITAJARA

(ACTINOPTERYGII: PERCIFORMES: SERRANIDAE), IN EASTERN BRAZIL

Matheus O. FREITAS 1, 2, 3*, Vinícius ABILHOA 2, 3, Vinicius J. GIGLIO 4,

Maurício HOSTIM-SILVA 1, 5, Rodrigo L. de MOURA 6, Ronaldo B. FRANCINI-FILHO 7,
and Carolina V. MINTE-VERA 8, 9

Instituto Meros do Brasil, Brazil

1

2 Grupo de Pesquisa em Ictiofauna – GPIC, Museu de História Natural Capão da Imbuia, Curitiba, PR, Brazil
3 Programa de Pós-Graduação em Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil

4 Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

5 Universidade Federal do Espírito Santo – UFES-DCAB – CEUNES, São Mateus, ES, Brazil

6 Instituto de Biologia, Depto de Biologia Marinha, Universidade Federal do Rio de Janeiro.

Rio de Janeiro, RJ, Brazil

7 Universidade Federal da Paraíba, Centro de Ciências Aplicadas e Educação, Campus IV – Litoral Norte,
Rio Tinto, PB, Brazil
8 Núcleo de Pesquisas em Limnologia Ictiologia e Aquicultura, Universidade Estadual de Maringá,

Maringá, PR, Brazil

9 Inter-American Tropical Tuna Commission, La Jolla, CA, USA (present address)

Freitas M.O., Abilhoa V., Giglio V.J., Hostim-Silva M., Moura R.L., Francini-Filho R.B., Minte-Vera C.V.
2015. Diet and reproduction of the goliath grouper, Epinephelus itajara (Actinopterygii: Perciformes:
Serranidae), in eastern Brazil. Acta Ichthyol. Piscat. 45 (1): 1–11.
Background. The goliath grouper, Epinephelus itajara (Lichtenstein, 1822), is the largest Atlantic grouper. It
has been the first marine fish subjected to a fishing moratorium in Brazil (since 2002). The aim of this study was
to investigate basic biological aspects, particularly the diet and reproduction of this endangered species. We
believe that our results, together with information already available in the literature, may be a foundation for new
management and conservation strategies for this grouper in Brazil.
Materials and methods. Specimens were obtained from an artisanal fish landings collaborative monitoring pro-
gram in the cities of Caravelas and Alcobaça, Abrolhos Bank, eastern Brazil. Because of the fishing moratorium,
we relied on sporadic incidental captures from fishermen or donation from the law enforcement agencies. Diet
and reproduction of the goliath grouper was evaluated based on 34 specimens obtained between May 2005 and
September 2010.
Results. Body size of 32 females ranged from 27.4 to 150.0 cm total length (TL) (mean 87.4 ± SD 34.8), while
size of 2 males were 97.0 and 115.0 cm TL. Of these, 16 specimens (47%) were juveniles. Sex ratio was estimat-
ed as 1 : 16 (males to females). Two developing females were recorded, one obtained in February 2006 and
another in January 2007. The length of first maturation (L50) for females was estimated at 105.64 cm and the
length where 100% of individuals are mature (L100) at 126.0 cm TL. A total of 34 stomachs were analyzed, six
of them were empty. Teleosts and decapods dominated the diet. The major food items of mangrove-associated
fish were decapods Callinectes sp., while the coral reef-associated fish ingested mainly the boxfish
Acanthostracion sp. The most important item for juveniles was Callinectes sp., while Acanthostracion sp. was
the most important item for adults.
Conclusion. We suggest that the goliath grouper moratorium in Brazil should be maintained for a relatively long
time frame—more than four decades.
Keywords: fish conservation; Abrolhos Bank; threatened fishes, fisheries management, ontogenetic variations,
Epinephelinae
*Correspondence: Dr. Matheus Oliveira Freitas, GPIC, Museu de História Natural Capão da Imbuia, Rua Prof. Benedito Conceição, N. 407. CEP: 82810-080, Curitiba,
PR, Brazil, phone: +55 41 3267-0819, e-mail: (MOF) [email protected], (VA) [email protected], (VJG) [email protected], (MHS) [email protected],
(RLM) [email protected], (RBFF) [email protected], (CVMV) [email protected].
2 Freitas et al.

INTRODUCTION uration, maximum size, and reproductive patterns, for

The goliath grouper, Epinephelus itajara example, are essential for fishery management of larger
(Lichtenstein, 1822), is the largest Atlantic grouper, groupers and snappers (Freitas et al. 2011b, 2014), as well
exceeding 2 meters of total length (TL), and >400 kg of as the information on predator/prey abundance and con-
weight (Bullock et al. 1992). It inhabits tropical and sub- sumption rates of predators, which may be used to assess
tropical coastal and estuarine areas on both sides of the the magnitude of trophic fluxes (Heithaus et al. 2010).
Atlantic (Heemstra and Randall 1993) from Florida to Herein we investigate the diet and reproduction, of
southern Brazil, including the Gulf of Mexico, as well as Epinephelus itajara specimens obtained from an artisanal
along the west coast of Africa (Bullock et al. 1992, fish landings collaborative monitoring program in the
Heemstra and Randall 1993). The goliath grouper is Abrolhos Bank, eastern Brazil. The region features the
a mangrove-dependent reef fish with the post-larval and richest coralline complex in the South Atlantic known for
juvenile phases thought to recruit to estuaries (Frias- its biodiversity and also for serious threats to its integrity
Torres 2006, Frias-Torres and Luo 2009). In southern and existence (Moura et al. 2013). The emphasis was
Brazil, however, juveniles (<100 cm) were recorded in placed on the assessment of ontogenetic and habitat shifts
open waters (Félix-Hackradt and Hackradt 2008). In the in diet, as such information may be relevant for future
Northern Hemisphere, juveniles generally show high site attempts to model trophic pathways and assess the possi-
fidelity, moving little within their home range and rapid- ble ecosystem implications of E. itajara removal (Pauly et al.
ly returning to their original habitat after handling 1998, Farmer and Wilson 2011). We believe that our results,
(Eklund and Schull 2001, Frias-Torres et al. 2007). together with information already available in the litera-
Goliath grouper is an opportunistic ambush predator and ture, may be a foundation for new management and con-
feeds at a relatively low trophic level (Koenig and servation strategies for the goliath grouper in Brazil.
Coleman 2009). The diet includes slow-moving fishes,
invertebrates (particularly lobsters and crabs), and even MATERIAL AND METHODS
sea turtles (Randall 1967, Bullock and Smith 1991). Study area. This study was carried out in the Abrolhos
The goliath grouper is extremely vulnerable to over- Bank, Bahia State, eastern Brazil, which encompasses
fishing (principally spearfishing and long-lines), mainly a wide portion (42 000 km2) of the continental shelf, with
due to critical life history traits such as slow growth, late depth rarely exceeding 30 m and a shelf edge at about
gonadal maturity, long life span, strong site fidelity, and 70 m depth (16º40′–19º40′S, 39º10′–37º20′W). The
formation of seasonal spawning aggregations (Bullock et region comprises the largest and richest coral reefs in the
al. 1992, Sadovy and Eklund 1999, Morris et al. 2000, South Atlantic, as well as an extensive mosaic of algal
Eklund and Schull 2001). The International Union for bottoms, mangrove forests, beaches, and vegetated sand-
Conservation of Nature (IUCN) lists it as a critically banks (Leão and Kikuchi 2005, Moura et al. 2013). Four
endangered species (Craig 2011). In Brazil, it has been marine protected areas (MPA) occur in the region, one of
fully protected by the federal law since September 2002 them with large mangroves— the Cassurubá Extractive
(Hostim-Silva et al. 2005) and the main demand to sup- Reserve (CER; multiple use; 1006 km2), in which the
port new management measures would be to obtain infor- fishing activities are either recreational or for subsistence
mation on the population status and species recovery. (Moura et al. 2011). The other three MPAs encompass
This moratorium was renewed twice in 2007 and 2012 for important reef formations: the Abrolhos Marine National
another three years*. In the South Atlantic there has Park (no fishing allowed; 913 km2), the Corumbau Marine
almost been no studies on the basic life history traits of Extractive Reserve (multiple use; 895 km2), and the
this fish. In Brazil, available information is fragmented Environmental Protected Area Ponta da Baleia/Abrolhos
and insufficient for a comprehensive evaluation of the (3460 km2), which in fact is a reserve only theoretically
population status. Available data comes from studies on due to the lack of regulations (Francini-Filho and Moura
the local ecological knowledge, from artisanal fishermen, 2008a, Francini-Filho et al. 2013). About 290 species of
spatio-temporal characteristics of aggregations (Ferreira fishes are recorded in the region (Dutra et al. 2005,
and Maida 1995, Gerhardinger et al. 2006, 2009, Reuss- Previero et al. 2013). Most reef structures display
Strenzel and Assunção 2008), monitoring of population a characteristic form of mushroom-shaped pinnacles,
size (Félix-Hackradt and Hackradt 2008), genetic charac- which attain 5 to 25 m in height and 20 to 300 m across
terization of populations, and cryptic genetic divergence their tops (Francini-Filho and Moura 2008b). Brazilian
(Silva-Oliveira et al. 2008, 2013, Craig et al. 2009). No reefs are a conservation priority in the Atlantic Ocean due
data, however, is available on its growth, maturity, fecun- to high endemism levels (about 25% in fish and 30% in
dity, and diet. scleractinian corals) that are concentrated in only 5% of
Combined with commercial and recreational fisheries West Atlantic reefs (Francini-Filho et al. 2013). The rich
data, the biological information collected from fisheries biodiversity of the Abrolhos Bank is threatened by over-
can contribute to regular assessments of the status of fish fishing, pollution, dredging, sedimentation from coastal
stocks, helping the evaluation of fisheries management deforestation, and large-scale oil-gas exploration projects
strategies (Pilling et al. 2008). Length and age at first mat- (Leão and Kikuchi 2005, Moura et al. 2013).
* In December 2014, the Brazilian government published a new endangered species list according IUCN criteria. Goliath grouper was categorized as critically endan-

gered, because has not shown signs of population recovery.

 Biological information on Epinephelus itajara in Brazil 3

Sampling and analytical procedures. Specimens of Abrolhos NMP

Epinephelus itajara were obtained from an artisanal fish

Corumbau MER

landing monitoring program of commercially important

Cassurubá ER
Reefs

reef fishes (see Freitas et al. 2011b) that focused on fish

N
caught using hook and line, longline, spearfishing, and
17°S
Bahia State
gillnets in the main fish markets in the cities of Caravelas
and Alcobaça (Fig. 1). All the mangrove individuals were
Prado

collected in the CER. Sampling was performed in collab-

Alcobaça

oration with local fishermen opportunistically between

Caravelas

June 2005 and September 2010. Because of the moratori-

Nova
18°S

um on fishing of the species, biological studies rely on

Viçosa

donation by fishermen after sporadic incidental captures

and/or donation by the law enforcement agencies after
confiscations, (permits # 038/2004 DIFAP-IBAMA, Fig. 1. Map of the Abrolhos Bank, eastern Brazil
39°W 38°W

042/2006 DIFAP-IBAMA and SISBIO 15080-5).

In the laboratory, the total length (TL) of individuals were created by using the Spearman’s correlation on the
was measured to the nearest 1 mm and the total weight proportionate contributions of food items. The final solu-
(TW) was determined to the nearest 10 g. Stomach and tion represents the set of relations between samples and
gonads were removed and immediately fixed in 10% for- food items in a two-dimensional, with determination of the
malin solution for 24 h and subsequently transferred and stress level of the representation (Clarke and Gorley 2001).
stored in 70% ethanol. Stomach contents were examined All analyses were performed using the PRIMER-E 6.0 soft-
in laboratory using a stereomicroscope. Prey individuals ware (Plymouth Marine Laboratory, Plymouth, England).
were identified to the highest possible taxonomic level Gonad weight (GW) was determined to the nearest
according to specialized literature (Matsuura 2001) and con- 0.01 g. Sex and maturity were macroscopically determined
sultation with experts. Parameters such as percentage from gonad size, consistency, colour, vascularization,
Frequency of occurrence (F) (i.e., percentage of stomachs presence of lateral sperm sinuses, ovarian cavity, ovarian
where the food item was present), gravimetric abundance lamellae, and identifiable oocytes (Colin et al. 2003). After
a food item (WA) (i.e., percentage of the weight of a food item macroscopic classification, gonads were dehydrated with
in relation to the weight of total food), as well as the increasing alcohol concentration series, cleared in xylene,
numerical abundance of a food item (N) (i.e., percentage of and then embedded in histological paraffin. Histological
the number of food item i in relation to the total number of all sections of 4–6 µm were stained in Harris haematoxylin
food items) were determined (Hyslop 1980, Bowen 1996). and eosin. Five developmental phases were considered fol-
These variables were used to calculate the Index of lowing Brown-Peterson et al. (2011): immature (IM),
Relative Importance (IRI) (see Pinkas et al. 1971), accord- developing (DV), spawning capable (SC), regressing
ing to the equation (RG), and regenerating (RT). The IM phase corresponds to
IRI = (N + WA) × F a fish that has never spawned, characterized histologically
The IRI establishes the order of importance of food in females by the presence of oogonia and primary growth
items in the diet. IRI values were standardized to percent- oocytes through the perinuclear stage, as well as little
ages following Cortés (1999). space among oocytes in the lamellae and ovarian wall gen-
Variations on diet according to the factors habitat erally thin (Brown-Peterson et al. 2011). In DV females,
(coral reefs or mangroves) and ontogeny (juveniles: the ovary is beginning to develop, but not ready to spawn.
<100 cm TL, or adults: >100 cm TL) were examined The SC fish are developmentally and physiologically able
using multivariate analyses considering all individuals to spawn; the RG represents the cessation of spawning and
with no empty stomachs (n = 28). Size classes were estab- the RT phase corresponds to a sexually mature, but repro-
lished according to our results on L50 for Epinephelus ita- ductively inactive individual.
jara in Abrolhos Bank (see results). A two-way permuta- Sex ratio was estimated using Bayesian method using
tional multivariate analysis of variance (PERMANOVA) the total numbers of females (f) and the number of
examined the effects of the factors habitat (fixed, two lev- females plus males (n). We used the conjugate beta-bino-
els) and ontogeny (fixed, two levels) on the standardized mial model to estimate the proportion of females with
and transformed (Log x + 1) weight contribution of items. uninformative beta (1,1) as a prior distribution and beta
The Bray–Curtis dissimilarity was used in all tests, using (f + 1, n – f + 1) as posterior distribution (Gelman et al.
unrestricted permutation of raw data with 999 random per- 2004). The minimum size at maturity (Lmin) was recorded
mutations. Similarity of percent contribution (SIMPER) for females. The TL at which 50% of females were mature
analysis was employed to examine the prey categories most (L50) (King 2007) was estimated using Bayesian methods
responsible for the between-factors separation (Clarke and (Kinas and Andrade 2010). The following logistic regres-
Gorley 2001). Non-metric multidimensional scaling sion model was used:
(NMDS) was employed to visually assess dispersion of PMF = 1 × (1 + exp (a + β × L)) –1
individuals. Vectors superimposed to the NMDS diagram where PMF is the proportion of mature females in length
4 Freitas et al.

class L, a is a parameter, and L50 = – a × β–1. For the L50 Brachyura (IRI = 5.91%). The analysis performed for dif-
analysis, developing, spawning capable, actively spawn- ferent size classes showed that Callinectes sp. (IRI =
ing, regressing, and regenerating individuals were consid- 66.51%) and fish remains (IRI = 27.40%) were the most
ered as sexually mature (adults). The model was imple- important items for juveniles. Most important items for
mented using the Automatic Differentiation Model adults were Acanthostracion sp. (IRI = 70.79%), followed
Builder (ADMB) software (Fournier et al. 2012) and by yellowtail snapper, Ocyurus chysurus (Bloch, 1791)
uninformative priors. Samples from the posterior distribu- (IRI = 8.57%) and Haemulon spp. (IRI = 6.58%).
tions of the parameters were obtained using the Markov The PERMANOVA analysis revealed differences in
Chain Monte Carlo algorithm (Gelman et al. 2004) with diet between juveniles and adults (Pseudo-F = 2.44 and
a 10 million chain and samples saved once every 10 000 P = 0.009) and also considering the interaction between the
interactions. factors size and habitat (Pseudo-F = 2.03 and P = 0.034)
(Table 2). However, the diet between habitat categories was
RESULTS marginally significant (Pseudo-F = 1.85 and P = 0.052).
General biological parameters and reproduction. Pairwise tests found that the diet of juveniles vary signif-
A total of 34 specimens (32 females and 2 males) of icantly between habitats (Table 3). In spite of the dietary
Epinephelus itajara were analyzed (Fig. 2), and from
these 16 (47%) specimens were juveniles. Body size of 6
females (94.1% of sampled animals) ranged from 27.4 to
Male n=2
Female n = 32
150 cm TL (mean 87.4 ± SD 34.8), while the size values 5
of males (5.9%) were 97.0 and 115.0 cm TL. The
length–weight relation was estimated at TW =
No. of individuals
4
0.0004TL 3.8127 (r = 0.7004, n = 34). Sex ratio was 1 : 16
2

males to females, with the median of the posterior distri- 3

bution of the proportion of females equal to 0.924 (90%
credibility interval = 0.831–0.976) (Fig. 3). 2

Analyses of gonadal histological sections confirmed

the predominance of immature females. Only two devel- 1

oping females were recorded (Fig. 4), one obtained on 2

February 2006 and another on 28 January 2007. The
beginning of the reproductive period is indicated by the
20–29.9

50–59.9

100–109.9

130–139.9

140–149.9
30–39.9

40–49.9

60–69.9

70–79.9

80–89.9

90–99.9

120–129.9
110–119.9
presence of the early developing sub-phase, in which only
the primary growth and cortical alveolar are present.
Total length [cm]

Thus, the spawning season of Epinephelus itajara in the Fig. 2. Size and sex composition of Epinephelus itajara
Abrolhos Bank may occur during austral summer individuals in individual size groups, sampled
(January to March). Nine RT females were registered between May 2005 and September 2010 in the
between April and October. The two males were classi- Abrolhos Bank, eastern Brazil
fied as RT and caught in January and April 2007. We did
not record any histological evidence of hermaphrodite 10
individuals. The L50 for females was estimated at
Bullock et al. (1992)

105.5 cm (mean of the posterior distribution, 90% credi-

This study

bility interval = 992.57–1116.72, Figs. 5 and 6) and L100

8

at 126.0 cm TL.
Diet. A total of 34 stomachs were analyzed, six of them
Probability

6
were empty (17.4%). Among the 12 items consumed by
Epinephelus itajara, the most important were fishes (IRI
= 46.31%), fish remains (IRI = 28.14%), the boxfish,
4

Acanthostracion sp., (IRI = 12.32%), and decapods (IRI =

52.77%), with Callinectes sp. corresponding to IRI = 2

42.59%. Teleosts and decapods dominated the diet based

on all dietary metrics. Among identifiable prey items, the
blue crab, Callinectes ornatus (F = 25.0%; n = 1), and the
0 0.2 0.4 0.6 0.8 1

blackpoint sculling crab, Cronius ruber (F = 7.14%; n = 5),

Proportion of females

were the most important prey based on number and fre- Fig. 3. Posterior distribution of the proportion of females
quency of occurrence (Table 1). The major food items of of Epinephelus itajara from the Abrolhos Bank, east-
mangrove-associated fish were Callinectes sp. (IRI = ern Brazil (south-western Atlantic population) esti-
87.97%) and fish remains (IRI = 10.93%), while coral reef- mated through the beta-binomial model; For compari-
associated fish ingested mainly Acanthostracion sp. son, the estimates of Bullock et al. (1992) obtained in
(IRI = 37.92%), fish remains (IRI = 29.10%), and the eastern Gulf of Mexico are shown
 Biological information on Epinephelus itajara in Brazil 5

overlap among individuals of Epinephelus itajara, NMDS 120–135 cm TL). This suggests that the population of the
analysis allowed the visualization of slightly distinct Abrolhos is not recovering yet from the great fishing pres-
groups considering the factors studied (Fig. 7). sure that motivated the establishment of the fishing mora-
The SIMPER analysis performed considering juve- torium in 2002. According to Bullock et al. (1992) and
niles and adults showed that fish remains and McClenachan (2009) Epinephelus itajara is highly vul-
Acanthostracion sp. were the most important items con- nerable to overfishing due mainly to its large size and late
tributing to the between-groups dissimilarities. The per- maturity. The size reduction at first maturity due to over-
centage contribution of Callinectes sp. (76.33%) and fish fishing was reported for several other commercially
remains (22.54%) were the most important items for juve- important marine species (Carlson and Baremore 2003,
niles, while Acanthostracion sp. (100%) was the most Hutchings 2005, McBride et al. 2013). Alternative expla-
important items for adults. Considering habitats, SIMPER nations for the differences between the present results and
analysis showed that most of the dissimilarity between- that from Bullock et al. (1992) are the relatively low sam-
groups was explained by the percentage contribution of ple size in the presently reported study, as well as differ-
fish remains, Callinectes sp. and Cronius ruber in the ence between years of data collection (1980s vs. 2000s),
diet. In mangrove samples, Callinectes sp. contributed natural variability in temperature, food availability, and
with 83.36% and fish remains with 16.34%, while in coral predation rates. Clearly, more studies focusing on the
reef grouper, Acanthostracion sp. represented 51.01% of reproduction of goliath grouper from different geographi-
food, followed by fish remains (42.41%). cal locations are necessary to adequately address these
questions.
DISCUSSION In the Northern Hemisphere Epinephelus itajara
This is the first study providing basic biological infor- spawns between July and September (Colin 1994,
mation about the largest Epinephelinae species in the Bullock et al. 1992, Sadovy and Eklund 1999, Koenig and
Atlantic Ocean. The size at first maturation of the goliath Coleman 2009, Mann et al. 2009). Results from this study
grouper in Abrolhos Bank estimated here (105.5 cm TL) (based solely on females) suggest that in the Abrolhos
was lower than that estimated by Bullock et al. (1992) in Bank the spawning season of E. itajara occurs in austral
the Gulf of Mexico (males: 110 to 115 cm and females: summer (January to March). Similar conclusions were

Fig. 4. Photomicrograph of ovaries of Epinephelus itajara sampled on 28 January 2007 in the Abrolhos Bank, east-
ern Brazil, illustrating Primary Growth (PG) and Cortical Alveolar (CA) stages; Scale bar: 10 µm
 6 Freitas et al.

obtained to the South Atlantic in previous studies based female : male proportion is around 4 : 1 (Claro et al. 1990,
on local ecological knowledge (Gerhardinger et al. 2006, Brulé et al. 2003). The presently determined sex ratio is
Reuss-Strenzel and Assunção 2008) and indirect evi- highly skewed towards females, suggesting that large
dences (see Colin et al. 2003) such as colour patterns males are overfished in the Abrolhos Bank. A caution is
(Félix-Hackradt and Hackradt 2008). Although Smith necessary, however, when comparing sex ratio estimates
(1971) assumed protogynous hermaphroditism for the from different studies, because of the possible influence
goliath grouper, no conclusive evidences for this repro- of gear selectivity, differences between sexes in time
ductive strategy were obtained here (see similar results in spent at aggregations sites, and/or migrations patterns
Bullock et al. 1992). Besides the data determined by us, (Sadovy and Eklund 1999).
the only information on sex ratios available for E. itajara As expected, this study supports the idea that
was provided by Bullock et al. (1992), who estimated the Epinephelus itajara is a carnivorous fish (Bullock and
sex ratio as 1.75 : 1 (females to males) in the Gulf of Smith 1991, Koenig and Coleman 2009). Decapod crus-
Mexico. For other Epinephelinae species in general the taceans and fish were the most important food items
observed. Similar results were obtained in previous stud-
ies. A broad array of preys is known to be consumed by
10

E. itajara, including: Atlantic spadefish, Chaetodipterus

9

faber (Broussonet, 1782); scrawled cowfish,

Proportion of mature females

8
7 Acanthostracion quadricornis (Linnaeus, 1758); striped
burrfish, Chilomycterus schoepfi (Walbaum, 1792); gas-
tropods; or decapod crustaceans (e.g., lobsters, Panulirus
6

argus and Scyllarides sp., as well as the crabs Calappa

5

flammea and Callinectes sp.) (see Bullock and Smith

4

1991, Koenig and Coleman 2009). In Brazil,

3
2 Gerhardinger et al. (2006) also confirmed this pattern
1 through surveys of fishermen ecological knowledge,
which indicate that most commonly food items of the
0 50 100 150 200 250 goliath grouper are lobsters, spadefish Chaetodipterus
faber, octopuses, and catfish (Family Ariidae).
Proportion of females

Fig. 5. Estimated logistic regression of proportion of Altogether, information on the diet of E. itajara available
mature females of Epinephelus itajara (maximum of
the posterior distribution) in relation to total length,
A
Habitat
from the Abrolhos Bank, eastern Brazil (May 2005 to
M

September 2007); Grey lines indicate length at which

CR

50% (L50) of individuals were mature (mean of the L50 Callinectes spp.
posterior distribution), and dashed lines indicate the
90% of credibility interval
A
10 JJJ
A
Bullock et al. (1992) J
J
A
L 50 (this study) J
JJJAJJJ
8
Fish remains A
Probability

6
A

Acanthostracion sp.
4

A A
A 2D Stress: 0.01
A
2

Fig. 7. Ordination plot based in the non-metric multidi-

mensional scaling analysis (nMDS) for diets of adults
(A) and juveniles (J) of Epinephelus itajara from the
80 100 120 140

Abrolhos Bank, eastern Brazil using the index of rela-

Total length [cm]

Fig. 6. Posterior distribution of the length when 50% of tive importance (IRI) of food categories [Log(x + 1)].
the females of Epinephelus itajara from the Abrolhos Symbols represent the factor habitat: mangrove (▼)
Bank, eastern Brazil (south-western Atlantic popula- and coral reefs (●); Vectors superimposed on the
tion) are mature (a = 18.43, β = – 0.017 and L50 = nMDS diagram were created by using the Spearman’s
105.5); For comparison, the range of possible values correlation on the proportionate contributions of the
for L50 from Bullock et al. (1992) are also shown food categories that most influenced the ordination
 Biological information on Epinephelus itajara in Brazil 7

to date indicates predominance of large sized and slow associated with mangroves and fishes predominated in
moving preys (Bullock and Smith 1991). A relevant num- diet of adults associated with coral reefs. This variation
ber of cowfish Acanthostracion sp. were recorded here, may be due to crustaceans (the primary food item), are
all from coral reef habitats. Because only dermal plates low in abundance in coral reef habitat and/or inaccessible
were detected, it is suggested that these structures take to adults because of the extreme rugosity of coral reefs
longer periods to be digested and are thus more frequent (Koenig and Coleman 2009, Koenig et al. 2011).
inside E. itajara stomachs. Despite of the fact that high trophic level species like
Ontogenetic shifts in diet of epinephelins and lutjanids adult Epinephelus itajara may cause indirect effects in the
may occur when juvenile and adult fish occupy different community (Heithaus et al. 2008, 2010, Ferretti et al. 2010)
habitats. For example, this pattern was recorded for dusky and influence a large range of ecological processes (Babcock
grouper, Epinephelus marginatus (Lowe, 1834) (see et al. 1999, Pinnegar et al. 2000, Willis and Anderson 2003),
Machado et al. 2008); mutton snapper, Lutjanus analis the goliath grouper in the Abrolhos Bank feed primarily on
(Cuvier, 1828) (see Freitas et al. 2011a); and grey snap- prey from relatively low trophic levels (detritivorous and
per, Lutjanus griseus (Linnaeus, 1758) (see Randall herbivorous), many of them with no direct economic value.
1967). The goliath grouper is considered a mangrove- In Florida (USA), population recovery of the goliath grouper
dependent species (Frias-Torres 2006), with clear ontoge- did not affect the abundance of commercially important
netic shifts in habitat use. In general, juveniles are found snappers and lobsters (Frias-Torres 2012). Conversely,
in fringing mangrove shorelines, while adults occur in Graham et al. (2003) observed that the reduction in groupers
coral reefs, isolated patch reefs, reef/rock ledges, and arti- abundance by fishing pressure in Australia caused an
ficial structures (Bohnsack and Ault 1996, Sadovy and increase on their small fish preys.
Eklund 1999, Félix -Hackradt and Hackradt 2008). In our Alterations in large groupers populations, such as
study, crustaceans predominated in the diet of juveniles Epinephelus itajara, can have significant commercial and

Table 1
Diet composition of 28 individuals of Epinephelus itajara, captured between May 2005
and September 2010 from Abrolhos Bank
Total Mangrove Coral reef Juvenile Adult
Prey item
n F IRI n F IRI n F IRI n F IRI n F IRI
TOTAL FISH 23 64.29 46.31 5 30.77 10.93 19 87.50 84.99 10 41.18 28.44 15 90.91 95.88
Fish remains 10 32.14 28.14 5 30.77 10.93 5 31.25 29.10 9 35.29 27.40 1 9.09 1.38
Acantrostracion sp. 6 14.29 12.32 0 0.00 0.00 6 25.00 37.92 0 0.00 0.00 6 45.45 70.79
Synodus sp. 1 3.57 0.60 0 0.00 0.00 1 6.25 1.83 1 5.88 1.03 0 0.00 0.00
Diodon sp. 2 3.57 0.60 0 0.00 0.00 2 6.25 1.86 0 0.00 0.00 2 9.09 2.93
Gymnothorax spp. 1 3.57 1.30 0 0.00 0.00 1 6.25 3.95 0 0.00 0.00 1 9.09 5.64
Haemulon spp. 4 3.57 1.37 0 0.00 0.00 4 6.25 4.25 0 0.00 0.00 4 9.09 6.58
Ocyurus chrysurus 1 3.57 2.00 0 0.00 0.00 1 6.25 6.08 0 0.00 0.00 1 9.09 8.57
TOTAL DECAPODS 24 71.43 52.77 14 61.54 89.07 10 37.50 12.12 18 66.52 71.20 6 45.45 11.56
Panulirus argus 1 3.57 0.43 0 0.00 0.00 1 6.25 1.33 0 0.00 0.00 1 9.09 2.02
Cronius ruber 5 7.14 3.51 2 0.00 0.00 3 6.25 3.25 3 5.88 1.71 2 9.09 3.38
Callinectes spp. 13 25.00 42.59 11 53.85 87.97 2 6.25 1.63 11 41.18 66.51 0 0.00 0.00
C. ornatus 1 25.00 3.41 1 7.69 1.10 0 6.25 0.00 0 0.00 0.00 1 9.09 1.26
Brachyura 4 10.71 2.82 0 0.00 0.00 4 12.50 5.91 4 11.76 2.98 2 18.18 4.90
CORAL FRAGMENTS 2 7.14 0.92 0 0.00 0.00 2 12.50 2.89 1 5.88 0.36 1 9.09 1.13
TOTAL 51 142.8 100 19 92.3 100 32 137.5 100 29 113.57 100 22 145.45 100

n = number, F = frequency of occurrence of the food items consumed [%], IRI = index of relative importance of individual
food items [%].

Table 2
F

Results of two-way crossed PERMANOVA analysis on the use of food resources

by Epinephelus itajara from Abrolhos Bank considering the factors of size and habitat

Factor df SS MS Pseudo-F P(perm) UP

Size 1 8842.2 8842.2 2.44 0.009 S
999
Habitat 1 6695.5 6695.5 1.85 0.052 999
Size × habitat 1 7341.9 7341.9 2.03 0.034S 999
Residuals 24 86788 3616.2
Total 27 1.159E5
S= significant results, df = degrees of freedom, SS = sum of squares, MS = mean squares, P(perm) = permutation P-value,
Pseudo-F =PERMANOVA’s statistics, UP = unique values obtained under permutation.

G
8 Freitas et al.

Table 3 ACKNOWLEDGEMENTS
Pair-wise tests based on PERMANOVA We thank Juliane Cebola, Guilherme Dutra, Danilo
analysis considering significant factors Araújo (CI), Beatrice Ferreira, and Sergio Rezende
on the use of food resources by Epinephelus itajara (UFPE), NGO Ecomar for their help in the field, advice
from Abrolhos Bank and criticism. We thank Dr. Rosimeire Brogin for identi-
fication of several prey items and Áthila Bertoncini for
Size × habitat helping in figures formatting. We are grateful to the
GRF Juvenile (17) Adult (11) Conservation International’s Marine Management Areas
M (11) vs. C (6) M (2) vs. C (9) Science Program that provided lab and logistic support.
t 1.853 1.104 This project benefited from grants from Conservation
Leadership Programme (CLP) and SISBIOTA/Rede
Abrolhos (CNPq/CAPES/FAPES), as well as from
P(perm) 0.033S 0.426

a FAPESB grant to MOF and CNPq grants to RLM,

UP 964 17
GRF = grouping factor, M = mangrove, C = coral reef, t = two-
sample t-test, P(perm) = permutation P-value, UP = unique CVMV and MOF (Process: 151102/2014-7). This is
values obtained under permutation; Number in brackets shows a contribution of the Meros do Brasil project, with finan-
the number of samples, S indicates significant results. cial support of the Programa Petrobras Ambiental –
Petrobras.
ecological consequences (Brulé et al. 2005). Goliath
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