A Review of The Biology, Ecology, Behavior and Conservation Status of The Dusky Grouper, Epinephelus Marginatus (Lowe 1834)

Rev Fish Biol Fisheries
DOI 10.1007/s11160-017-9502-1
REVIEWS
A review of the biology, ecology, behavior and conservation

status of the dusky grouper, Epinephelus marginatus (Lowe
1834)
Mario Vinicius Condini . José Antonio Garcı́a-Charton . Alexandre Miranda Garcia
Received: 3 October 2016 / Accepted: 12 October 2017

Ó Springer International Publishing AG 2017
Abstract The dusky grouper is a large-bodied high commercial value for professional fishers and is
marine species usually associated with rocky sub- also highly prized by recreational spearfishers. These
strates and reefs currently experiencing increasing biological features, associated with increasing fishing
anthropogenic pressures. Here, we critically evaluate pressures throughout most of its geographical distri-
studies conducted during the last few decades on this bution, have led to Epinephelus marginatus being
endangered species, focusing on its biology, ecology, included since 2004 in the IUCN Red List of Threat-
behavior, stock structure and fisheries, and identify ened Species as Endangered. Despite a large amount of
future research directions to fill current knowledge research being conducted on this species over the last
gaps. This species plays an important functional role in five decades or so, using a number of different tools and
the rocky bottom habitats in which it lives, usually techniques, key questions regarding its biology still
occupying the highest trophic levels and with the remain unanswered. In terms of conservation and
potential role as a keystone species in some ecosys- management plans designed to safeguard this endan-
tems. It has a complex life cycle characterized by a high gered species, we identified the crucial need to improve
longevity, a slow growth rate and a monandric fisheries landing statistics for the species and to
protogynous hermaphroditic mode of reproduction. increase the number of marine protected areas within
The species also exhibits spawning aggregation behav- its distribution beyond the Mediterranean Sea.
ior, which makes it more vulnerable to fishing activity.
Aside from its ecological importance, this species has Keywords Endangered Epinephelidae Fisheries
Protogynous hermaphrodite Top predator
M. V. Condini (&) A. M. Garcia

Laboratory of Ichthyology, Institute of Oceanography, Introduction
Federal University of Rio Grande, Av. Itália Km 8,
Carreiros, Rio Grande, RS 96.201-900, Brazil
e-mail: [email protected]
Groupers1 are a group of generally large-bodied fishes
with a broad global distribution and high commercial
M. V. Condini
Laboratory of Ichthyology, Biology Department, State
1
University of Feira de Santana, Feira de Santana, Based on evidence provided by more recent molecular and
BA 44.036-900, Brazil previous morphological studies, Smith and Craig (2007) recom-
mended taxonomic changes to the family Serranidae (sensu Nelson
J. A. Garcı́a-Charton 2006) because it was a polyphyletic group. They proposed that the
Departamento de Ecologı́a e Hidrologı́a, Universidad de groupers (Subfamily: Epinephelinae) should be separated from the
Murcia, Campus de Espinardo, 30100 Murcia, Spain Anthiinae and Serraninae Subfamilies. These two latter
123
and ecological importance (Sadovy de Mitcheson et al. Linnaeus) Jordan and Evermann 1896, and currently
2013). They are targeted by artisanal, industrial, and as Epinephelus marginatus (Lowe 1834) (Heemstra
sport fishing throughout their ranges (Heemstra and 1991). However, in the phylogenetic study of Craig
Randall 1993; Craig et al. 2011), and often have strong and Hastings (2007), they indicate that this species
influences on food webs and ecosystems through their probably belongs to the genus Mycteroperca, but due
role as top predators (Heemstra and Randall 1993; to the lack of additional studies this proposal has not
Sluka et al. 2001). Alterations to grouper populations been accepted by most researchers.
can thus have significant commercial and ecological The dusky grouper E. marginatus (Fig. 1) has a
consequences (Parrish 1987). Several groupers have large body size, growing to at least 150 cm (total
slow growth rates, late maturation and a complex length, TL) (Louisy 2015) and reaching up to 60 kg
mode of seasonal reproduction, including spawning (Figueiredo and Menezes 1980). It has an important
aggregations and sex change (Manooch and Mason functional role in the rocky bottom substrates that it
1987; Craig et al. 2011), which, combined with high inhabits, especially as a main predator occupying the
fishing pressure, leads to vulnerability to overex- highest trophic levels (Parrish 1987; Reñones et al.
ploitation in many grouper populations (Huntsman 2002; Condini et al. 2015) and potentially playing a
et al. 1999; Coleman et al. 2000; Sadovy de Mitcheson central role as a keystone species (Valls et al. 2012;
et al. 2013). The groupers of the family Epinephelidae Prato et al. 2016). For instance, Valls et al. (2012)
include numerous species that are important to world modeled trophic interactions to assess the effects of a
fisheries (Sadovy de Mitcheson et al. 2013), but little is marine protected area in the Port-Cros National Park,
known about many of them. northwestern Mediterranean Sea. The Ecopath model
According to the International Union for the Con- results highlighted the central role played by both the
servation of Nature (IUCN), almost a third of grouper large dusky grouper and amberjack and suggest these
species (50 out of * 163 species) are currently two abundant top predators play a central role in the
classified as Data Deficient (i.e., there is not enough ecosystem in terms of keystone species and trophic
information available to classify them as being either cascades. The dusky grouper has a complex life cycle
threatened or not threatened) (IUCN 2017). Another 71 characterized by high longevity (it may reach
species are classified as Least Concern (i.e., they were * 60 years of age) (Reñones et al. 2007), a slow
not considered to be threatened) and 22 species as Near growth rate (Reñones et al. 2007; Condini et al. 2014a)
Threatened. The remaining 20 species are classified and a monandric protogynous hermaphroditic mode of
into one or other of the three threatened categories; 12 reproduction (Bruslé and Bruslé 1975; Marino et al.
species as Vulnerable, five as Endangered and three as 2001). Due to its reproductive strategy, all specimens
Critically Endangered (Luiz et al. 2016). The dusky initially mature as females, and the sexual transition
grouper Epinephelus marginatus is one of the can occur in individuals from 9 to 16 years old, which
Epinephelidae currently included as Endangered in become functional males (Chauvet 1988), although
the IUCN’s Red List of Threatened Species (Pollard
et al. unpublished data).
Epinephelus marginatus was originally described
in the eighteenth century as Perca gigas Brünnich
1768, and since then has been attributed several
scientific names: Serranus gigas Valenciennes 1828,
Serranus marginatus Lowe 1834, Epinephelus gigas
Jordan and Swain 1885, Epinephelus guaza (non
Footnote 1 continued
subfamilies were considered as a new Serranidae Family, as they
comprised a monophyletic group, whereas the previous Sub-
family Epinephelinae was elevated to full family status as the
Epinephelidae. These two reset families (Epinephelidae and Fig. 1 Underwater photograph of the dusky grouper Epine-
Serranidae) include approximately 160? and 245 species, phelus marginatus in its natural habitat (Image by Áthila
respectively. Bertoncini Andrade)
123
some individuals can undergo sexual transition earlier communities (Oliver 1986; Balci et al. 2006; Marzouk
(from * 7 years of age) (Reñones et al. 2010). et al. 2010; Roumbedakis et al. 2014), genetic
Another significant feature of this species is its structure (Maggio et al. 2005; Innocentiis et al.
spawning aggregation behavior (Zabala et al. 2008; Schunter et al. 2011), fishing (Condini et al.
1997a, b; Hereu et al. 2006), which makes it more 2007; Kouassi et al. 2010; Cardoso and Haimovici
vulnerable to fishing activity. 2011; Begossi et al. 2012) and its genetic identification
Epinephelus marginatus has great economic impor- in fish markets (Trotta et al. 2005; Asensio et al. 2008;
tance and high commercial value, especially for Mottola et al. 2014). Studies on dusky grouper
artisanal fishing (Heemstra and Randall 1993; Condini aquaculture, with the aim of replenishing wild fish
et al. 2007; Begossi and Silvano 2008; Lloret and stocks (Marino et al. 2003; Sarter et al. 2006; Cunha
Riera 2008; Begossi et al. 2012). Additionally, this et al. 2009) or for commercial production purposes,
species is widely caught by underwater sport fishers have also increased in the last 10 years or so (Sanches
using spearguns throughout most of its distribution et al. 2006; Pierre et al. 2008). Such biological and
(Heemstra and Randall 1993; Machado et al. 2003; ecological studies are crucial sources of information to
Coll et al. 2004; Lloret et al. 2008; Diogo and Pereira guide the conservation and sustainable fishery man-
2014). Declining populations due to increasing fishing agement of this endangered species (Tzanatos et al.
pressure in most areas of its geographical distribution, 2008; Damalas et al. 2010). This review critically
potentially augmented by a vulnerability associated evaluates the available literature on E. marginatus,
with their above-mentioned biological characteristics, focusing on its biology, ecology, behavior, stock
has resulted in the inclusion of E. marginatus since structure and fisheries, and suggests future research
2004 in the IUCN’s Red List of Threatened Species as directions to fill current knowledge gaps.
Endangered (ENA2d) (Cornish and Harmelin-Vivien
2004). According to the latest assessment of the IUCN
in 2016 (Pollard et al. unpublished data), the decline in Geographical distribution
total catches of dusky grouper has been increasing.
Global catches of this species have also declined by The dusky grouper E. marginatus (Lowe, 1834) has a
approximately 87% over the past 20 years up to 2014. discontinuous distribution occurring int at least three
This updated assessment providing evidence of an main groups in: (1) northeastern Atlantic Ocean and
ongoing and continuing population decline, indicates Mediterranean Sea, and north and northwestern
that this species should probably now be regarded as Africa; (2) southeastern Atlantic Ocean and south-
Critically Endangered (CR, A2d) in southern Europe western Indian Ocean; and (3) southwestern Atlantic
and the Mediterranean Sea. However, the latest IUCN Ocean (Fig. 2). According to Schunter et al. (2011),
assessment adopted a conservative approach and did the first and second groups represent separate popu-
not classify the species as Critically Endangered due to lations with minimal gene flow between them, prob-
the lack of accurate data of dusky grouper catches in ably due to the large distance involved. There are no
South Africa and South America (Pollard et al. current studies comparing these two groups with the
unpublished data). one found in the southwestern Atlantic Ocean.
Several studies have been conducted during the last In Europe, the dusky grouper has been observed
few decades on the biology and ecology of this throughout the Mediterranean Sea (Oliver 1986;
endangered species. The main topics that have been Heemstra and Randall 1993; Kara and Derbal
addressed in these studies cover several subjects, such 1995a, 1995b; Zabala et al. 1997a, b; Bouchereau
as behavior (Azevedo et al. 1995; Zabala et al. et al. 1999; Bilecenoglu et al. 2002; La Mesa et al.
1997a, b; Lembo et al. 2002; Machado et al. 2003; 2002; Lembo et al. 2002; Reñones et al.
Gallego et al. 2013), reproduction and growth (Marino 2002, 2007, 2010; Bertucci et al. 2015), including
et al. 2001; Fennessy 2006; Reñones et al. 2007, 2010; the Aegean Sea (Bilecenoglu et al. 2002). Only one
Condini et al. 2014a, b), trophic ecology (Barreiros individual was recorded at the beginning of the
1988; Derbal and Kara 1996; Reñones et al. 2002; twentieth century in the Marmara Sea (Devedjian
Linde et al. 2004; López and Orvay 2005; Machado 1915 APUD Bilecenoglu et al. 2002), but never in the
et al. 2008; Condini et al. 2011, 2015), parasite adjacent Black Sea (Keskin 2010). It has also been
123
Fig. 2 Map showing (dark lines) the geographic distribution of Atlantic Ocean and southwestern Indian Ocean and (3)
the dusky grouper Epinephelus marginatus that includes three southwestern Atlantic Ocean. The asterisks denote the occur-
main areas: (1) northeastern Atlantic Ocean and Mediterranean rence of only one individual so far at Réunion Island
Sea, and north and northwestern Africa, (2) southeastern
recorded in the northeastern Atlantic, in the English southeastern coast of the Arabian Peninsula, in
Channel (French territory) and in the Macaronesian southern Oman (Randall 1995). Considering this was
Islands off the coast of southern Europe and north- a single record and new occurrences have not been
western Africa (Azevedo et al. 1995; Barreiros and observed since then, it may have been a case of
Santos 1998; Cunha et al. 2009; Mahé et al. 2012). misidentification (Pollard et al. unpublished data).
In the African continent, dusky groupers have been Finally, in the south Atlantic coast, the dusky
observed along the entire Atlantic coast, and around grouper has been recently (2017) recorded south of
the southern tip of Africa towards southern Mozam- Bahia in northeastern Brazil (M. Condini, pers. ob-
bique (Smale 1986; Fennessy 2006; Kouassi et al. serv.), which represents the northermost recording of
2010; Maggs et al. 2013a, b). In 2012, the dusky this species on the Atlantic coast. Towards its south-
grouper was recorded for the first time in La Réunion ernmost distribution limit, the species have been
Island in the Indian Ocean (Reid et al. 2016). recorded in southeastern and southern Brazil (Figueir-
According to these authors, the dispersal of the species edo and Menezes 1980; Bertoncini et al. 2003;
may have occurred from South Africa, with Mada- Machado et al. 2003; Gibran 2007; Seyboth et al.
gascar probably being an important area facilitating 2011; Condini et al. 2011, 2013, 2014a, b, 2015; Ander-
the connection between the South Africa coast and la son et al. 2014), in Uruguay (Condini et al. 2016a) and
Réunion Island. The dusky grouper was once reported Argentina from Plata River to Patagonian Gulf Nuevo
in a local fish market at Fort Dauphin, Madagascar (S. (Rico and Acha 2003; Irigoyen et al. 2005).
Fennessy, pers. obs., by Pollard et al. unpublished Despite several aforementioned studies having
data). The dusky grouper was also reported on the provided a detailed view of the distribution of the
123
dusky grouper around the globe and a few attempts to Koeck et al. (2014) studied a dusky grouper population
explain regional distribution patterns (e.g., Schunter in a marine reserve at Cerbère-Banyuls (France) using
et al. 2011), the reasons for its discontinuous distri- telemetry, and showed diurnal movement patterns
bution have been intriguing researchers for many throughout the year, with an active phase during the
decades. Recently, Ma et al. (2016) proposed biogeo- day (high detection frequencies) and a resting phase at
graphic hypotheses to explain the evolutionary history night (low detection frequencies). A similar pattern
of Epinephelidae. Based on an extensive time-cali- was described on an acoustic-telemetry study by
brated molecular phylogeny, they proposed that the Hackradt (2012) in a marine reserve at Cabo de
clade, from which E. marginatus evolved, emerged Palos—Islas Hormigas (Spain), although with marked
approximately in the mid-Miocene (* 16 million interindividual variability (15 out of 27 tagged indi-
years ago). This clade appeared first in the western viduals displayed a clearly diurnal pattern of activity,
Indo-Pacific and then shifted westward during the another 10 specimens did not differ in their activity
mid-Miocene and occurred in the eastern Pacific later between day and night, and only one fish showed a
on during the Pliocene (5–2 mya). Nearly half of the greater probability of detection at night than by day).
divergences in this clade originated within regions, Through telemetry studies, Afonso et al. (2016) in
while the other half were attributed in equal amounts Faial Island (Azores) determined that the dusky
to vicariant splits and isolation events. In particular, grouper showed a strong movement patterns where
the most recent ancestor of the dusky grouper would the majority of individuals leave its site of residency
have occurred in the eastern Atlantic in the late- for a short period, usually a maximum 2 days and
Miocene (Ma et al. 2016). seldom for longer than a week. Individuals showed a
very small area of home range ranging between 0.070
and 0.268 km2 with core activity areas ranging
Habitats and habitat use between 0.018 and 0.034 km2. There was also
evidence that some individuals undertook daily
This species usually inhabits rocky bottoms, such as migrations to the same point in all consecutive
reefs, offshore banks and rocky shores. Overall, adults summers over the 5 years of study, very likely related
are generally more abundant at depths down to 50 m, to preferred mating sites. Based on visual observations
but they can be found occasionally at depths down to made during scuba diving on rocky bottom habitats in
250 m (Bruslé 1985; Heemstra and Randall 1993; southern Brazil, Gibran (2007) reported that most
Harmelin and Harmelin-Vivien 1999). In contrast, dusky groupers were active during daytime, whereas
small juveniles are usually found in coastal tide pools few individuals showed activity during the night. He
(Azevedo et al. 1995; Machado et al. 2003), shallow also noticed that E. marginatus appeared to become
rocky reefs with highly structurally complex habitats ‘‘excited’’ during the twilight hours, and could be
(La Mesa et al. 2002; Bussotti and Guidetti 2009), and found outside their hiding places foraging for prey
in rocky habitats of bays and estuaries (Condini et al. during this period.
2016b). Several authors have claimed a relationship
A better knowledge of habitat use patterns among between dusky grouper body size and depth range.
marine fish populations is extremely important to During the early juvenile stages, the species preferen-
determine population dynamics and to guide appro- tially inhabits shallow rocky habitats rich in shelter
priate measures for their conservation and fisheries (Derbal and Kara 1995; Harmelin and Harmelin-
management (Andrello et al. 2014; Davoren et al. Vivien 1999; La Mesa et al. 2002), the entrances of
2015). Hence, many studies on dusky groupers have shallow caves (Bussotti and Guidetti 2009), and
been conducted to evaluate their habitat use, home intertidal pools (Azevedo et al. 1995; Machado et al.
range and site fidelity. 2003; Cottalorda et al. 2009), shifting to deeper water
Epinephelus marginatus is generally a sedentary as they grow older (Chauvet 1991; Kara and Derbal
species, displaying strong site fidelity and usually 1995a; Francour and Ganteaume 1999; La Mesa et al.
small home ranges (Chauvet and Francour 1990; 2002; Ruitton et al. 2010; Hackradt 2012; Bodilis et al.
Lembo et al. 1999, 2002; Spedicato et al. 2005, Pastor 2013; Condini et al. 2014a, b).
et al. 2009; Koeck et al. 2014; Afonso et al. 2016).
123
Other relationships with body size are related to are related to changes in their foraging strategies,
their behavior. Smaller individuals may form groups transitioning from an active predator searching for
of up to three individuals and actively swim in open smaller prey (e.g., crabs) to an ambush predator
waters over soft bottoms. In contrast, larger individ- targeting larger prey (e.g., fishes and cephalopods).
uals have more solitary habits, are less active, and are Overall, these feeding habit studies indicate that the
usually found near their shelters among rocks or inside dusky grouper is a carnivorous fish, feeding essentially
hiding places, from where they rarely come out (Kara on larger macrocrustaceans, fish and molluscs (mainly
and Derbal 1995a; Gibran 2007). cephalopods). However, as expected, there are differ-
A strong seasonal variation in dusky grouper ences in the taxonomic composition of the diet among
density has also been reported, with higher abun- feeding studies, probably due to differences in envi-
dances observed during summer probably being ronmental conditions and prey availability occurring
associated with spawning aggregations (see below). across distant geographic areas (Reñones et al. 2002;
After peaking in activity during summer, they Linde et al. 2004; Machado et al. 2008) or even
decrease their activity thereafter, becoming more between adjacent sites (e.g., shallow,\ 5 m vs. deeper
sedentary for most of the winter (Zabala et al. 1997b). areas, 20–30 m deep; Condini et al. 2011, 2015). It is
worth noting the importance of cephalopods in the
diets of dusky grouper populations from the Mediter-
Feeding and trophic ecology ranean Sea (Derbal and Kara 1996; Reñones et al.
2002; Linde et al. 2004; López and Orvay 2005), the
Studies on the trophic ecology of dusky groupers have southwestern Indian Ocean (Smale 1986) and the
basically been restricted to stomach content analyses eastern coast of the Atlantic Ocean (Azevedo et al.
(Smale 1986; Azevedo et al. 1995; Derbal and Kara 1995; Barreiros and Santos 1998), in contrast with
1996; Barreiros and Santos 1998; Linde et al. 2004; their low representation or absence in the diets of
López and Orvay 2005; Begossi and Silvano 2008; populations from the southwestern coast of the
Machado et al. 2008; Condini et al. 2011), with only Atlantic Ocean (Begossi and Silvano 2008; Machado
two studies using more advanced approaches such as et al. 2008; Condini et al. 2011, 2015). Other food
stable isotope analysis (Reñones et al. 2002; Condini items reported in very low abundance in dusky
et al. 2015) (Table 1). groupers’ stomach contents are plant fragments,
The frequency of empty stomachs is usually found polychaetes, and small bivalves and gastropods
to be higher in carnivorous fishes when compared to (Azevedo et al. 1995; Derbal and Kara 1996; Linde
detritivorous and omnivorous fishes (Arrington et al. et al. 2004; Machado et al. 2008). It is still unclear
2002), and this pattern is consistently reported in all whether these items, especially plant fragments, are
feeding studies of the dusky grouper throughout its ingested accidentally when they are preying upon their
geographical distribution (Table 1). Most studies preferential animal prey, or ingested intentionally.
showed ontogenetic diet shifts, transitioning from In the last decades, the combination of stomach
consumption of crustaceans at smaller sizes to fishes contents and stable isotope tools has become one of the
and cephalopods by larger individuals. The only most powerful approaches to investigate feeding
exception to this general trend was reported by ecology in fishes (Layman et al. 2012). To date, only
Machado et al. (2003) in Santa Catarina, Brazil. These two studies have employed these complementary
authors did not find ontogenetic dietary changes in the approaches to study the trophic ecology of dusky
proportions of dominant prey groups, with brachyuran groupers. Reñones et al. (2002) observed intermediate
crabs remaining the most representative food category d15N values (between 8.8 and 13.1%) and a positive
throughout the species’ lifespan. correlation with body size in dusky groupers, poten-
These studies on ontogenetic dietary shifts also tially indicative of ontogenetic changes in trophic
revealed a tendency to consume prey with greater size position in dusky groupers in the Mediterranean Sea.
or biomass as dusky groupers increased in body size In contrast, Condini et al. (2015) found no significant
(Reñones et al. 2002; Linde et al. 2004; Machado et al. relationship between d15N and body size in popula-
2008; Condini et al. 2015). Linde et al. (2004) tions in the southwestern Atlantic Ocean. They
suggested that ontogenetic dietary shifts in groupers observed higher d15N values compared to other fish
123
Table 1 Bibliographical review of the known diet of wild mm), class sizes (ontogeny), number of the individuals
dusky grouper Epinephelus marginatus; study site, frequency analyzed of the stomach contents, and stable isotope analysis
of empty stomachs (Vacuity %), range of total lengths (TLs,
References Study site Vacuity TL (mm) Ontogeny (TL, mm) n Stomach n
(%) Contents Stable Isotopes
Analyzed Analyzed
Smale (1986) Southern Western 71.8 250–875 300–400; 401–500; 319 No

Indian—South 501–700
Africa
Azevedo et al. Atlantic Ocean— 33.8 – 40–70; 130–250; [ 360 71 No
(1995) Azores (Portugal)
Derbal and Mediterranean Sea— 48.5 160–980 No 68 No
Kara (1996) Algeria
Barreiros and Atlantic Ocean— 38.6 600–1380 \ 900; [ 900 57 No
Santos Azores (Portugal)
(1998)
Reñones et al. Western 56.1 144–1035 \ 300; 300–450; 450–600; 123 53
(2002) Mediterranean— [ 600
Spain
Linde et al. Western 32.5 134–1056 \ 400; 401–500; 501–600; 203 No
(2004) Mediterranean— [ 600
Spain
López and Western 16.6 0.325–20.88a \ 3; 3–6; 6–9; 9–12; 139 no
Orvay Mediterranean— 12–15; 15–18; 18–21;
(2005) Spain [ 21a
Begossi and Southeastern 34.4 – \ 401; [ 400 61 No
Silvano Western Atlantic—
(2008) Brazil
Machado et al. Southern Western 37.7 197–920 \ 400; 401–500; 501–600; 257 No
(2008) Atlantic—Brazil [ 600
Condini et al. Southern Western 48.3 150–1160 \ 351; 351–500; 501–650; 348 262
(2015) Atlantic—Brazil [ 650
a
Total size was described by weight (kg), such as to ontogeny classes
predators in rocky bottoms located in the shallow (less greater proportion in the dusky grouper’s muscle
than 5 m) and deeper (between 20 and 30 m) waters, tissues than crabs, despite this latter being the
suggesting that dusky groupers occupy the uppermost dominant food item found in their stomach contents
trophic levels in habitats located at distinct depths in in most areas. This difference is likely due to a
the southwestern Atlantic. Carbon isotope ratios relatively greater amount of refractory material in
(d13C) of dusky groupers in the Mediterranean Sea crabs (e.g., their carapaces) versus fishes (e.g., their
provided evidence of strong linkages to the benthic bones and scales). Thus, crabs may be more frequently
food web, whereas in the southwestern Atlantic it was encountered in stomach contents due to their slower
suggested that this top marine predator integrates both digestion rates, but may contribute less energetically
pelagic and benthic food web pathways (Reñones et al. (per unit of ingested biomass) to the dusky grouper.
2002; Condini et al. 2015). Condini et al. (2015) suggested that stomach contents
It is also worth noting that stable isotopes may and stable isotope analyses are highly complementary
reveal that prey are not assimilated into a consumer’s for elucidating the trophic ecology of dusky groupers,
tissues (e.g., muscle) in the same proportion that they and call attention to the possibility that relying solely
appear in the stomach contents (Layman et al. 2012). on one technique (e.g., stomach contents) may render
Stable isotope mixing models carried out by Condini inaccurate or misleading results.
et al. (2015) indicated that fishes are assimilated in
123
Feeding behavior this information because the reported higher sex ratio
can be due the fishing selectivity or sampling effects.
The dusky grouper is an opportunistic predator On other hand, Seyboth et al. (2011) did not collect
operating mainly during twilight hours (diurnal and any males, probably because their study was con-
crepuscular) (Gibran 2007; Condini et al. 2011) and ducted in a shallow area (less than 5 m) where larger,
using different feeding strategies to capture prey, such mature individuals are absent and, therefore, it was not
as ‘‘drift feeding,’’ ‘‘ambush hunting’’ and ‘‘roving or possible to calculate the sex ratio.
patrolling’’ (Gibran 2007). Its opportunistic learning The reproductive cycle of dusky groupers has been
behavior can lead to successful feeding tactics, such as established based on the histological analysis of
following the snake eel Myrichthys ocellatus (Ger- gonads, temporal analysis of the gonadosomatic index
hardinger et al. 2006), octopus Octopus vulgaris (GSI), and/or the frequency of the gonadal develop-
(Machado and Barreiros 2008), and other teleost ment stages. Histological analyses of gonads indicated
fishes like the Brazilian damselfish Stegastes fuscus that the species spawns between late spring and late
(Bessa 2011), and even the common dentex Dentex summer (Bruslé and Bruslé 1975; Marino et al. 2001;
dentex in the Mediterranean Sea (Garcı́a-Charton J.A., Bertoncini et al. 2003; Reñones et al. 2010; Condini
pers. observ.). et al. 2014b). Dusky groupers from the southern
hemisphere showed spawning peaks from November
to January (Bertoncini et al. 2003; Fennessy 2006;
Reproductive biology Gerhardinger et al. 2006; Condini et al. 2014b),
whereas in the northern hemisphere the peaks
As a monandric protogynous hermaphroditic species occurred between July and September (Bruslé and
(Bruslé and Bruslé 1975; Bouain and Siau 1983; Bruslé 1975; Kara and Derbal 1999; Marino et al.
Marino et al. 2001), it is usually difficult to observe 2001; Reñones et al. 2010; Özen and Balcı 2011)
dusky grouper individuals undergoing sexual transi- (Table 2). The body length at first maturation (L50)
tion due to the low number of specimens engaged in reported for female E. marginatus ranged from
this phase of their life cycle at any one time (Condini 391 mm TL in Turkey to 622 mm TL in South Africa
et al. 2014b). Additionally, this sex change phase is (Table 2). There are only two records for males, both
probably significantly faster and briefer compared in the Mediterranean Sea, with L50 ranging from
with other life cycle phases like initial sexual devel- 813 mm TL in Italy (Marino et al. 2001) to 835 mm
opment and maturation to adulthood (Sadovy and TL in Turkey (Özen and Balcı 2011). This parameter
Shapiro 1987). Dusky grouper individuals undergoing is crucial for conservation and management purposes
sexual transition have been found in many reproduc- and can change among populations from different
tive studies carried out in the Mediterranean Sea and geographic areas, and under different environmental
the western Indian Ocean, whereas only one individual conditions and levels of fishing pressure (Gulland
was collected in this transition phase in all reproduc- 1983).
tive studies conducted in the entire Atlantic Ocean Another important reproductive parameter is fecun-
(Table 2). As a protogynous hermaphrodite species, it dity, but only one study, by Reñones et al. (2010),
is expected that a higher proportion of females provided information on this aspect. These authors
compared to the number of males will be found in estimated the fecundity in a total of 39 females with
the population, and all studies reporting sex (adults sizes ranging from 386 to 915 mm TL and ages
male:female) ratios corroborate this pattern (Bruslé between 6 and 42 years, and demonstrated that they
and Bruslé 1975; Zabala et al. 1997a; Marino et al. are spawners with asynchronous oocyte development.
2001; Fennessy 2006; Gerhardinger et al. 2006; The potential fecundity ranged from 65 thousand to 8
Reñones et al. 2010; Özen and Balcı 2011; Condini million oocytes in females of different sizes, with a
et al. 2014b; Tsikliras and Stergiou 2014). However, mean relative fecundity of 334 9 103 oocytes kg-1.
the study of Gerhardinger et al. (2006) in south Brazil Females could spawn up to 10 batches of eggs during
stands out because they showed higher sex ratios in the spawning season, with an average batch fecundity
dusky groupers (adults male:female 1:46) (Table 2). of 75 9 103 oocytes 9 kg-1.
These authors suggested caution when considering
123
Table 2 Bibliographical review of the known reproductive biology of wild dusky grouper Epinephelus marginatus; study site, range
of total lengths (TLs), number of specimens sampled (n)
Reference Study site LT range n Females Transitionals Males Sex ratio Spawning L50
(mm) (n) (n) (n) (M:F) season (mm)
Bruslé and Mediterranean Sea— – 419 279 19 121 1:2.1 July–August –

Bruslé Tunisia
(1975)
Kara and Mediterranean Sea— XX–795 – – – – – July–August 570
Derbal Algeria
(1999)
Marino et al. Southern 245–1050a 405 321 25 59 1:3.5 July–August 438a
(2001) Mediterranean—Italy
Bertoncini Southern Western 197–1002 109 107 0 5 1:15.6 December 470
et al. (2003) Atlantic—Brazil
Fennessy Southern Western 95–1100 395 352 1 42 1:5.5 December– 622
(2006) Indian—South Africa January
Gerhardinger Southern Western 300–1000 193 190 0 3 1:46 November– 460
et al. (2006) Atlantic—Brazil December
Reñones et al. Western 66–1056 399 346 10 43 1:7.4 July–August 491
(2010) Mediterranean—
Spain
Özen and Balcı Eastern 240–1110 104 77 8 19 1:3.5 July– 391
(2011) Mediterranean— September
Turkey
Seyboth et al. Southern Western 260–800 130 130 0 0 – – 451
(2011) Atlantic—Brazil
Condini et al. Southern Western 278–1160 201 184 1 16 1:6.6 November– 496
(2014a, b) Atlantic—Brazil January
Number of females, sexual transition and males collected, relative proportions of adults male and female (M:F), spawning season
peaks and average female length at first maturity (L50)
a
Marino et al. (2001) used standard length (SL) in their study
Reproductive behavior withdrawals of males by the fishery, thus inducing

sexual transition to occur earlier. However, this effect
The dusky grouper has a complex life-history strategy has not been corroborated in some studies showing
characterized by a monandric protogynous hermaph- evidences of a decrease in the size of males in recent
roditic mode, where all individuals initially mature as studies. For instance, earlier studies showed that
females, with the potential to change their sex to males sexual transition occurred in individuals with body
sometime during their life span (Bruslé and Bruslé sizes from 68.0 cm TL in Tunisia (Chauvet 1988),
1975; Heemstra and Randall 1993; Marino et al. 2001; from 68.5 cm TL in Italy (Marino et al. 2001) and
Reñones et al. 2010). Sadovy and Shapiro (1987) 67.0 cm TL in South Africa (Fennessy 2006). In
reported that several monandric species have bimodal contrast, recent studies suggest that sexual transition
frequency distributions for body size and age, with occurs in smaller individuals, such as from 52.1 cm
females being both smaller and younger than males. TL in Spain (Reñones et al. 2010) and from 51.5 cm
Such bimodal frequency distributions can cause a TL in Brazil (Condini et al. 2014a).
considerable population sex imbalance, because larger One of the most relevant, although least under-
individuals are often the main target of fishermen and stood, aspects of the complex life-history of the dusky
the first ones to be taken out of the fished stocks grouper is its aggregation behavior during spawning
(Gulland 1983). Consequently, there are higher (Zabala et al. 1997a, b). Spawning aggregations of
123
dusky groupers have been rarely observed and the always exhibited patterns CP1 or CP2, whereas
current knowledge about this behavior in this species patterns CP4 to CP8 were observed only during the
is limited to observations within marine protected reproductive season. CP4 is characterized by light
areas (MPAs) located in the Mediterranean Sea, such colour and was mainly observed in small females
as the Medes Islands Marine Reserve (Zabala et al. (40–60 cm TL). CP5 is distinguished by a dark
1997a, b; Hereu et al. 2006) and the Cerbère-Banyuls streaked pattern and occurred in dusky groupers with
Marine Reserve (Mathieu-Tissot 1999) in the western body sizes (TL) between 40 and 95 cm, larger females
Mediterranean. Other authors have reported only ([ 60 cm TL) and younger males (\ 80 cm TL), the
indirect evidence (e.g., an increase in the abundance fish being differentiated for sex determination by
of dusky groupers being caught in a single limited characteristics such as swollen abdomens (egg-swol-
location in the space of a few days) of the occurrence len bellies). The dominant larger males ([ 95 cm TL)
of spawning aggregation sites in the Mediterranean usually exhibited the patterns CP6 (silver-streaked),
Sea (Marino et al. 2001), in southeastern Africa CP7 (basic male) and CP8 (light male) (see Fig. 2–3 in
(Fennessy 2006) and in the southwestern Atlantic Zabala et al. 1997b).
Ocean (Bertoncini et al. 2003, 2012; Gerhardinger Once in the reproductive area, there is a marked
et al. 2006; Condini et al. 2014b), which still needs to segregation between females and males. Males estab-
be corroborated by direct observations. lish a territory in deeper water (from 15 and 35 m
Spawning of dusky groupers is reported to occur deep), generally below the thermocline, at tempera-
between late spring and late summer. The observed tures of 17–20 °C. In contrast, females tend to remain
population density usually achieves the greatest peaks in less deep waters (over or between 5 and 20 m most
during spawning aggregations, when it can increase by often) above the thermocline (Louisy and Culioli
five to 12 times compared to densities observed during 1999). During a spawning event, a dominant male
winter (Zabala et al. 1997b; Louisy and Culioli 1999). performs courtship activities within a small area of its
Another feature is the appearance of large individuals territory, showing agonistic behavior against males
([ 80 cm TL) during such aggregations. Some of the entering into his territory. The spawning event occurs
larger individuals remain throughout the year in these between a single male and female pair and has
reproductive areas, but most appear during late spring different phases: (1) approach, where males exhibit
and remain only until late summer. Usually, large lateral displays on the sea bottom, below the thermo-
males are the first ones to arrive. During these cline; (2) ascent and false rise, where males join
reproductive aggregations, large males ([ 80 cm females and they rise together vertically through the
TL) comprised only 10–17% of the aggregation, water column in parallel, side by side, and less than
smaller females (40–60 cm TL) constituted 45–60%, 20 cm apart. Just after reaching the upper level of the
and large females ([ 60 cm TL) represented 10–25%. thermocline they abort the rise and come back to the
There were no juvenile dusky groupers (\ 40 cm TL) bottom. The false rise can be repeated two or three
found in areas where adults are concentrated for times over a few minutes before the actual spawning
reproduction, at least in summer (Louisy and Culioli act takes place; (3) actual spawning, where males and
1999). After spawning, the dominant males progres- females approach again and they move up through the
sively abandoned their territorial behavior in the water column above the thermocline. Then, the rising
spawning area until the next reproductive event during process is followed by a short, but frenetic swimming
the following summer (Zabala et al. 1997b). acceleration that ends up with the emission of gametes
In order to facilitate the identification of female and and the immediate separation of the pair. After the
male individuals during underwater surveys, Zabala gametes have been liberated, each mate goes back to
et al. (1997b) proposed gender identification during the bottom (see Zabala et al. 1997a; Fig. 4). A single
the reproductive period based on their color patterns male is able to repeat a successful spawning several
(CPs). They identified eight CPs, where the first three times in a few minutes, and with different females.
are probably shared by all size classes and sexes Courtship activities have been observed at both
throughout the year. The differences between the first sunrise and sunset (Pelaprat 1999).
three CPs occur according to the different behaviors The first observation of dusky groupers spawning at
(CP1, CP2 and CP3). The immature individuals the Medes Islands (Zabala et al. 1997a, b) suggested a
123
close relationship with the lunar cycle, specifically the Early life history
new moon phase. However, information obtained
from observations of spawning aggregations in other There is a widely recognized knowledge gap regarding
regions did not confirm these earlier reports (Louisy the planktonic life history stage for the Epinephelidae
and Culioli 1999). Monitoring of spawning aggrega- in general. Not surprisingly, almost nothing is known
tions of dusky groupers at the Medes Islands for three about the occurrence of the planktonic eggs and larvae
consecutive years revealed that the dates of gamete of E. marginatus throughout its entire geographic
release in relation to the lunar cycle changed every distribution. The first reports of specimens less than
year (Louisy and Culioli 1999). In the same MPA, 10 cm TL were observed in 1989 in the south of
Hereu et al. (2006) showed that spawning occurred Corsica and in the Cerbère-Banyuls MPA, with further
during all moon phases, although it was more frequent collections of such small individuals being made in
during the new moon and the first quarter. They subsequent years in different sites along the French
attributed this lack of synchronicity to the relatively Mediterranean coast (Bodilis et al. 2003). Marinaro
long reproduction period of E. marginatus et al. (2005) employed a bongo net and sampled dusky
(2–4 weeks) compared to more tropical grouper grouper eggs at the marine reserve of Cerbère-
species (e.g., 7 days for E. striatus; Sala et al. 2001). Banyuls, and were thus able to monitor their devel-
Although it has been observed in other grouper species opment until hatching. These eggs were perfectly
(Johannes 1978; Colin 1992; Shapiro et al. 1993; spherical, had a diameter between 0.79 and 0.90 mm
Sadovy et al. 1994; Samoilys and Squire 1994), the (average of 0.855 mm) and a single oil drop. This oil
synchronization between lunar cycles and gamete drop measured 0.16–0.18 mm in diameter and was
release in dusky grouper populations still needs further usually colorless, but in some cases exhibited a
validation. yellowish color. Crec’hriou et al. (2010), using both
Regarding other environmental factors triggering towed bongo nets and fixed plankton nets around the
spawning aggregations in this species, like tempera- Cabrera National Park (Balearic Islands, Western
ture, daylight hours, tidal amplitude, wave height and Mediterranean Sea) during July 2004, documented
others, the seasonal variation in temperature undoubt- that the eggs of Epinephelus spp. (mostly E. margina-
edly plays a major role (Louisy and Culioli 1999; tus) appeared to be continuously abundant there
Pelaprat 1999; Hereu et al. 2006). According to Hereu through this time, thus indicating spawning during
et al. (2006), extreme events, such as very strong the entire 12 day sampling period. Muntoni et al.
currents or low temperatures, could inhibit the repro- (2011) caught two post-larvae of E. marginatus
ductive activity of males. Several of the above- measuring 2.2 and 2.5 cm TL with light traps in
mentioned authors demonstrated that dusky grouper September and October 2010 in the southern Gulf of
reproduction occurs between late spring and late Cagliari (Italy). Félix-Hackradt et al. (2013) also
summer. Louisy and Culioli (1999) corroborated this employed light traps and collected a few specimens
pattern when they observed dusky grouper spawning smaller than 6 cm TL on shallow reefs surrounding
in the warmest period across different sites and years, Cabo de Palos–Islas Hormigas Marine Reserve
with temperatures ranging between 21 and 24 °C and (Spain).
always above the thermocline. Hereu et al. (2006)
analyzing dusky groupers from the Medes Islands
determined that spawning occurred during the highest Age and growth
surface temperatures (mean 24–25 °C) and the highest
frequency of spawning occurred when the thermocline Tetracycline marking has revealed annual depositions
was shallowest. A clear circadian pattern was also in otoliths and clearly demonstrated that a single
observed, with all spawning occurring at dusk within annulus was deposited each year for dusky groupers in
less than 1.5 h before sunset. southeastern Africa (Fennessy 2006). Studies carried
out elsewhere had not employed direct tetracycline
markings as age validation, but rather had relied on
patterns of alternating translucent and opaque bands
and marginal increment analyses (Reñones et al. 2007;
123
Condini et al. 2014a). Although marginal increment obtained from scales (785–1850 mm and
analysis through patterns of alternating translucent 0.028–0.160, respectively) (Table 3). These differ-
and opaque bands is not considered the most trust- ences of the growth parameters between studies using
worthy technique for validation of growth in otoliths otoliths versus scales may be due to otolith analysis
(Campana 2001), studies using marginal increments tending to be more precise than using scales (Campana
also suggested annual depositions as demonstrated by 2001). This is the case mainly in larger fishes, as
the experimental approach with tetracycline con- precision decreases with increasing fish length (Welch
ducted by Fennessy (2006). The annual deposition of et al. 1993; Secor and Trice 1995), because discerning
growth increments in otoliths has been found in other annuli on scales in larger fishes is more difficult due to
grouper species as well, such as E. flavolimbatus crowding near the margins (Welch et al. 1993). Thus,
(Manickchand-Heileman and Phillip 2000), Myc- age determination studies that used scales may have
teroperca interstitialis (Manickchand-Heileman and underestimated age, altering the values of growth
Phillip 2000), M. rosacea (Dı́az-Uribe et al. 2001), E. parameters (L? and K). Alternatively, this may be
coioides (Grandcourt et al. 2005), and M. fusca simply because some of these studies (e.g., that of
(Bustos et al. 2009), suggesting that it is a common Kara and Derbal 1999) failed to sample large-sized
feature in large epinephelids. individuals, which strongly underestimates the value
Data currently available on size, age, length–weight of L?. The growth rate of E. marginatus increases
relationships and growth parameters of E. marginatus rapidly during the first 5 years of life, when it reaches
are compiled in Table 3. These studies have relied an average of approximately 45% of the theoretical
both on the counting of annuli on scales collected maximum length. After this age, the growth rate tends
beneath the pectoral fins (Rafail et al. 1969; Bouain to decline rapidly and, after reaching * 30 years of
1986; Chauvet 1988; Azevedo et al. 1995; Kara and age the growth is slower (Chauvet 1988; Kara and
Derbal 1995b; Bouchereau et al. 1999; Ximenes- Derbal 1995b; Bouchereau et al. 1999; Fennessy 2006;
Carvalho et al. 2012) and readings of growth rings in Reñones et al. 2007; Condini et al. 2014a).
sectioned sagittae otoliths (Fennessy 2006; Reñones According to available studies on length–weight
et al. 2007; Seyboth et al. 2011; Condini et al. 2014a). relationships, there are low variations among these
In a few cases, age estimates were also based on parameters, with individuals of the same body size
analysis of whole sagittae otoliths (Chauvet 1988). generally showing similar weight (Table 3). Excep-
The absence of older ages in some regions may be a tions are the studies from Kara and Derbal (1995b) and
consequence of (1) fishing, which can selectively Ximenes-Carvalho et al. (2012), which showed values
remove older individuals (Ricker 1975), (2) insuffi- below and above average, respectively, probably due
cient sampling of the entire population (e.g., in Algeria to the lack of larger individuals in their data sets.
in the Mediterranean Sea, Kara and Derbal 1995b), or However, as the length–weight relationship may vary
(3) simply because that region contains mostly throughout the life cycle, and according to the
immature individuals (e.g., in the littoral zone, Sey- environmental conditions, seasonality, and individual
both et al. 2011). physiological state, this parameter is not recom-
The parameters of the von Bertalanffy growth mended for comparing different populations (Froese
equation (L?, K, and t0) have been widely used to 2006).
describe growth rates in many species, including E.
marginatus (Table 3). A comparison of these studies
revealed considerable differences among individuals Parasitology and disease
from different sites, mainly in terms of the theoretical
maximum length (L?) and growth coefficient (K). Occurrence of parasites has been used in a variety of
Such differences could be partially explained by fish species as biological tags or indicators to provide
inherent differences between the readings of different information for stock identification, movement pat-
hard structures (e.g. otoliths vs. scales). Otoliths terns and population connectivity of fished stocks
showed lower variation for both parameters (L? (Williams et al. 1992; MacKenzie and Abaunza 1998;
and K between 900 and 1249 mm and 0.069 and 0.129, Vignon et al. 2008). However, there are few investi-
respectively), when compared with age readings gations concerning the parasite faunas of dusky
123
Table 3 Bibliographical review of the known age and growth of specimens sampled (n), and von Bertalanffy growth
of wild dusky grouper Epinephelus marginatus; study site, parameters of E. marginatus examined in this study and in
aging structure, range of total lengths (TLs), age range, number previous investigations
Reference Study site Ageing LT range Age n L? k to Length–weight
structure (mm) range (mm) (years-1) (years) relationship (W = a.
(years) LTb)
Rafail et al. Mediterranean Sc 166–475 1–7 251 800 0.112 -1.08 W = 0.0069LT3.222
(1969) Sea—Egypt
Bouain (1986) Mediterranean Sc 150–890 0–16 97 1850 0.028 -1.53 –
Sea—Tunisia
Chauvet Mediterranean Sc and 53–1180 0–36 270 1144 0.093 -0.75 *W = 0.01256LT3.073
(1988) Sea—Tunisia Wo
Chalabi et al. Mediterranean Ra 250–900 1–8 60 1774 0.073 -1.24 W = 0.0000243LT2.971
(1992) Sea—Algeria
Azevedo et al. North Atlantic Sc 40–360 0–4 74 – – – W = 0.0139LT3.065
(1995) Ocean—Azores
(Portugal)
Kara and Mediterranean Sc 197–567 1–7 41 785 0.160 -0.73 W = 0.0081LT3.140
Derbal Sea—Algeria
(1995)
Bouchereau Mediterranean Sc 200–1200 1–14 22 1359 0.080 -0.80 W = 0.123LT2.60
et al. (1999) Sea—France
Fennessy Southern Western So 95–1020 1–16 215 1249 0.090 -1.43 –
(2006) Indian—South
Africa
Reñones et al. Western So 66—1056 0–61 358 955 0.087 -1.12 W = 0.0098LT3.14
(2007) Mediterranean—
Spain
Seyboth et al. Southern Western So 260–800 2–12 108 1249 0.069 -1.49 –
(2011) Atlantic—Brazil
Ximenes- Southeastern Sc 115–705 1–14 135 1010 0.075 -2.20 W = 0.00008LT3.221
Carvalho Western
et al. (2012) Atlantic—Brazil
Condini et al. Southern Western So 150–1160 1–40 190 900 0.129 -1.45 W = 0.0125LT3.094
(2014a, b) Atlantic—Brazil
Length–weight relationship, W = total weigth; *W = gutted weigth. Ageing structures used were scales (Sc), sectioned otoliths
(So), whole otoliths (Wo) and ray (Ra). Von Bertalanffy growth parameters included L?, the mean theoretical maximum TL; t0, the
theoretical age at zero length; and K, the growth coefficient or the rate at which the curve approaches the asymptote
grouper throughout its area of occurrence (Oliver Other studies on parasites of dusky grouper have
1984; Scholz et al. 1993; Santos et al. 2000; Bartoli called attention to symbiotic relationships with other
et al. 2003; Merella et al. 2005; Genc 2007; Marzouk fishes. For instance, dusky groupers may have a
et al. 2010; Roumbedakis et al. 2013) (Table 4), and symbiotic relationship with a clingfish (Lepadogaster
no studies using parasites as biological tags to candolii), which removes parasites from the grouper’s
determine stock identification, movement patterns mouth (Weitzmann and Mercader 2012). In aquacul-
and population connectivity in this species. Future ture settings, the symbiotic barber goby Elacatinus
studies could explore the potential of this approach to figaro, remove the parasite Neobenedenia melleni
advance our current knowledge on population struc- from dusky grouper individuals (Souza et al. 2014).
ture and connectivity of E. marginatus. Groupers are subject to a number of diseases in
aquaculture facilities (Harikrishnan et al. 2010), with
123
Table 4 Bibliographical review of the known parasites of wild dusky grouper Epinephelus marginatus; geographical location,
identification of class and species of the parasite and position of the parasites in the body
References Study site Class Famı́ly Parasite Species Position
Oliver (1984) Western Monogenea Diplectanidae Cycloplectanum riouxi Gills

Mediterranean
Sea—France
Oliver (1984) Northeastern Monogenea Diplectanidae Cycloplectanum riouxi Gills
Atlantic
Ocean—Ireland
Scholz et al. Southern Cestoda Lacistorhynchidae Grillotia epinepheli Body cavity and peritoneum
(1993) Mediterranean
Sea—Italy
Santos et al. Southeastern Monogenea Diplectanidae Pseudorhabdosynochus Gills
(2000) Western beverleyburtonae
Atlantic—Brazil
Bartoli et al. Western Trematoda Opecoelidae Podocotyle temensis Cephalic glands, testes,
(2003) Mediterranean ovaries, digestive and
Sea—France excretory systems
Merella et al. Western Chromadorea Philometridae Philometra jordanoi Gonads
Sea—Spain
Genc (2007) Northeast Malacostraca Gnathiidae Gnathia sp. Buccal cavity
Mediterranean
Sea Turkey
Marzouk et al. Southeast Microsporea Gluguidea Glugea anomala Gills
Sea—Egypt
Roumbedakis Southeastern Monogenea Diplectanidae Pseudorhabdosynochus Gills
et al. (2013) Western beverleyburtonae
Atlantic—Brazil
Roumbedakis Southeastern Monogenea Capsalidae Neobenedenia melleni Body surface
et al. (2013) Western
Atlantic—Brazil
Roumbedakis Southeastern Trematoda Opecoelidae Helicometrina nimia Stomach and intestines
Atlantic—Brazil
Roumbedakis Southeastern Chromadorea Anisakidae Contracaecum sp. Mesentery
Atlantic—Brazil
Roumbedakis Southeastern Monogenea Ancyrocephalidae Pseudempleurosoma sp. Stomach
Atlantic—Brazil
the most commonly reported being infection by phenomenon has been observed in Sicily (Marino
vibrios, Pseudomonas spp. and Aeromonas spp. (La and Azzurro 2001) and other Italian sites, in Greece
Mesa et al. 2008). Frequent observations of mortalities (Panzarin et al. 2012), the northern Ionian Sea
of wild fish worldwide (including of dusky groupers in (Vendramin et al. 2013), Tunisia (Haddad-Boubaker
the Mediterranean Sea) have been associated with et al. 2014), the Balearic Islands, and Algeria (Kara
viral encephalopathy and retinopathy, a disease caused et al. 2014), Corsica, Libya, Malta and Crete (GEM
by infectious agents of the Betanodavirus genus 2015). This disease seems to have originated from
(Munday et al. 2002; Doan et al. 2016). This aquaculture facilities, thus showing the risk of viral
123
exchange between wild and farmed fish populations important target species in many artisanal fisheries
(Vendramin et al. 2013; Haddad-Boubaker et al. within its broad distribution range. The main fishing
2014). Rizgalla et al. (2016) also recently reported a gear employed to catch dusky grouper is the bottom
so-called ‘‘dusky grouper dermatitis’’ in Libyan longline (Galili et al. 2004; Gomez et al. 2006;
coastal waters, the causes of which have yet to be Cardoso and Haimovici 2011; Martı́n et al. 2012;
established. There is concern that seawater warming Lloret and Font 2013), both in artisanal and industrial
due to climate change may increase the occurrence of fishing. The species may also be caught by traditional
infectious diseases in the near future, which could pose hook-and-line fishing methods (Galili et al. 2004;
another risk to the endangered dusky grouper (Ven- Condini et al. 2007), or by gillnet (Galili et al. 2004;
dramin et al. 2013). Martı́n et al. 2012). In the case of sport fishing, dusky
groupers are usually captured by speargun (Coll et al.
2004; Lloret et al. 2008; Lloret and Font 2013), and
Fisheries and human consumption also occasionally by hook and line (Condini et al.
2007).
Groupers have been caught by man for more than ten A crucial prerequisite for efficient fishery manage-
thousand years, as indicated by well-preserved archae- ment is knowledge of the health of the fish stocks.
ological deposits on the Mediterranean coast. For Therefore, not only is information about the biology of
instance, records of E. marginatus were found in the target species important, but also adequate
deposits from the Neolithic in Cyprus (Desse and fisheries’ catch statistics data. Data on fisheries’
Desse-Berset 1999), and in Neolithic sites in the Nerja landings and fishing effort have been used since the
Cave (Málaga, Spain) (Morales and Roselló 2004). nineteenth century, when English scientists realized
The occurrence of dusky grouper remains on the that they could not investigate fishing effects on fish
Mediterranean Island of Favignana (Italy) were also stocks due to a lack of adequate fishing statistics
recorded between the late Mesolithic and the early (Williams 1977). Information on both the catch and
Neolithic (Mannino et al. 2012). Groupers have also the fishing effort are also fundamental to determine
been recorded in other archaeological sites around the public policies and management measures to guaran-
world, such as in the northeastern Atlantic (Roselló tee the maintenance of fish stocks and the conservation
and Morales 1990), the Bahamas (Blick 2007), and the of the ecosystems involved. The relative lack of data
Pacific islands (Dalzell 1998). on both fisheries’ landings and the fishing effort
Groupers have high economic value, and many currently employed to catch dusky grouper worldwide
species are consumed in many different parts of the is a major obstacle to sustainable management of this
world (Heemstra and Randall 1993). According to the endangered species.
Food and Agricultural Organization of the United There are some dusky grouper catch statistics data
Nations (FAO), there was an increase in the global available in some areas of its geographical distribu-
captures of groupers from 1950, when approximately tion, mainly in the southwestern Atlantic and southern
16,000 tons per year were landed, up until 2009, when tip of Africa, but these are still quite poor. In fact, the
captures reached approximately 275,000 tons per statistical data are more concentrated in the Mediter-
year. Of the total grouper production in 2008, more ranean region. According to FAO’s catch landings
than 80% was reported from Asia. This increasing statistics (FAO 2015), there are landings data for
trend is, however, probably substantially underesti- dusky grouper since 1950. In this year, there was a
mated because of the unreported catches from many record of 200 metric tons (mt) of dusky grouper caught
small-scale, multispecies fisheries (Sadovy de Mitch- in Spain. Between 1950 and 1963 there were only
eson et al. 2013). catches registered to Spain, but from 1964 records of
The dusky grouper is targeted by artisanal, indus- dusky grouper catches were started for other countries,
trial and sport fishing throughout its geographical beginning with Italy and followed by Turkey and
range (Heemstra and Randall 1993; Craig et al. 2011). others (Fig. 3). From 1950 until the beginning of the
The dusky grouper is usually not a target species in 1980s, the total annual catches of dusky groupers
industrial fisheries, but an accessory species with high gradually increased (from 200 to * 2000 mt, respec-
economic value. In contrast, dusky groupers are an tively), with a peak during 1972 and 1973 (3238 and
123
Fig. 3 Temporal variation (1950–2014) in gross catch (tonnes) of dusky grouper Epinephelus marginatus from European and North
and Northwest African countries (compiled from FAO 2015 database)
5832 mt, respectively) (Fig. 4). Most of these catches rapidly until the last evaluation in 2015 (Fig. 4), when
occurred in Italian waters (Fig. 3). From the mid only 1111 mt of the dusky grouper was recorded.
1980s onwards, there was a substantial increase in Given that the generation length of the dusky grouper
dusky grouper harvesting, which continued through is on average 20 years (Pollard et al. unpublished
the mid 1990s (ranging from * 5000 to * 8000 mt, data), when we compare the two last generation
respectively). Besides Italy, Libya also had substantial lengths of the dusky grouper harvesting, * 4650 mt
reported catches of dusky groupers during this period (1976–1995) and * 2350 mt (1996–2015), we
(Fig. 3). After that, the global catches began declining
Fig. 4 Temporal variation (1950–2014) in global gross catch (tonnes) of dusky grouper Epinephelus marginatus (compiled from FAO
2015 database)
123
observed a decline of * 50% in the global dusky recovery since then. When we analyzed the last two
grouper catch. periods from 1976 to 1995 and from 1996 to 2015
The analysis of landing data by region (Europe vs. (* 3600 and * 300 mt, respectively) it was possible
Africa) reveals two different scenarios (FAO 2015). In to observe a decline of more than 90% in dusky
Europe, the pattern is similar to that of the global grouper catches in Europe. Among the European
catches, that is, there is a gradual increase between countries reporting dusky grouper catches, Italy stands
1950 and the beginning of the 1980s (Fig. 5a), with a out as having the largest fish landings, followed by
peak in 1972-–1973. From 1984 there began a period Spain and Portugal. The largest catch of the species
of greater harvests of dusky grouper until 1994 (3920 ever in a single year (5332 mt) was recorded in Italy in
and 3947 mt, respectively), with a mean catch of 1973. Since then, Italy has stayed as the county
approximately 4000 mt during this period. After this reporting the highest catches until 1995, when an
time, there began an abrupt decrease, reaching values abrupt decline occurred. Since 2000, the average catch
of below 500 mt in 1998 (465 mt) and with no signs of per year in Italy has been approximately 65 mt, which
Fig. 5 Temporal variation (1950–2014) in gross catch (tonnes) of dusky grouper Epinephelus marginatus from (A) Europe and
(B) Africa (compiled from FAO 2015 database)
123
corresponds to a decline of 98% in a period of less than considering that this species is highly valued for
30 years. Spain ranked at second place as the Euro- human consumption throughout its geographical dis-
pean country reporting the largest dusky grouper tribution. Since the dusky grouper is a large-bodied
catches until 1980, showing average year catches of and long-lived fish species, there is a great risk of
approximately 500 mt. After that there was a collapse heavy metal contamination (e.g., by mercury) via
and the average catches since then have stayed at bioaccumulation (Evers et al. 2009; Tremain and
approximately 130 mt per year, which represents a Adams 2012). Mercury is a nonbiologically essential
decline of most of 70% compared with the initial and toxic element commonly found in aquatic ecosys-
phase. In 1980, Portugal started showing considerable tems. It is released through a variety of natural and
high catches of dusky groupers with the peak averag- anthropogenic processes including geological weath-
ing 646 mt between 1981 and 1985, but after this ering, gold mining, and the burning of coal (Pacyna
period there was also an abrupt decline, as observed et al. 2010). In aquatic systems, mercury can be
for the other countries. transformed by microbial activity into organic
The analysis of the reported landings of dusky methylmercury, which biomagnifies in the food web
grouper in Africa (Fig. 5b), only started in 1983 in and results in high concentrations of methylmercury
Lybia, with very low values (FAO 2015). It was only (MeHg) in both fishes and other fish-eating species
in the early 1980s that an increase in grouper catches (including humans) (Chen et al. 2008).
was observed in Libya, with a peak in 1994 (3752 mt). Despite the potential risk of mercury contamination
Since then, reports of dusky grouper catches in Africa in dusky groupers, there are few studies addressing
are declining progressively (Fig. 5b) (FAO 2015). this topic throughout the geographical distribution of
There is no long-term fishery landing statistics of the species. The first study on mercury contamination
dusky grouper populations in South America. The in the dusky grouper was in the Mediterranean Sea, in
main fishery landing data available for this species for Israel, by Levitan et al. (1974). These authors analyzed
the whole continent is in Santa Catarina, a southern total mercury and methylmercury in 18 individuals,
state in Brazil (Pollard et al. unpublished data). The and 13 showed concentrations above the safety levels
scarce data available show that catches of dusky (World Health Organization—WHO) for human con-
grouper in South America are much more modest sumption, which is \ 0.3 wet weight (mg/kg). They
when compared to European and African harvests. also found higher contamination levels in older
The reports of dusky grouper catches in Santa Catarina specimens. The mercury source in this study was
started in 1988 with approximately 25 mt, showing a probably wastewater from nearby industrial plants
gradual increase until 1998 with a peak of around discharging into inflowing streams or directly into the
75 mt, followed by a steady decline towards only study site.
approximately 1 mt in 2012. Two more recent studies have also revealed mer-
Another aspect to highlight when assessing dusky cury contamination in dusky grouper populations.
grouper catches and their subsequent marketing is the Banana et al. (2016) reported that the dusky grouper
occurrence of fraudulent reports when other less showed the second highest Hg concentration above the
valuable species are commercialized and sold as safety levels (WHO) for human consumption among
dusky groupers. For example, Asensio et al. (2009), different fishes, oysters and cuttlefish species evalu-
using Polymerase Chain Reaction (PCR)-based ated in the Mediterranean Sea (in west Zawya, Libya).
methodology, detected fraudulent labeling of 58 out These authors found no relationships between mercury
of 70 grouper fillet samples in different fish markets in concentration and the dusky grouper’s biological
Madrid, which were in fact originally from other parameters such as its length, weight or age, despite
species, such as Nile perch Lates niloticus and wreck high Hg concentrations in sediment samples. Condini
fish Polyprion americanus. Cutarelli et al. (2014) also et al. (2017) analyzed a suite of parameters (i.e., body
detected, by DNA barcoding, the substitution of filets size, age, diet and trophic position) to investigate
of dusky grouper by the pleuronectid Reinhardtius mercury concentrations in 224 dusky groupers in
hippoglossoides in Italian markets. southern Brazil. They revealed that larger ([ 650 mm
Dusky grouper contamination by heavy metals and TL) and older ([ 8 years old) individuals showed
other pollutants is also a cause of concern, especially mercury contamination levels that are potentially
123
harmful if consumed by humans. When considering successfully rear this species under different condi-
similar body sizes, individuals inhabiting littoral tions (Boglione et al. 2009).
habitats had higher concentrations of mercury than
those in neritic habitats, probably due to their prox-
imity to pollution sources associated with human Conservation and management
activities.
Fishing overexploitation is the main threat to the
dusky grouper (Pollard et al. unpublished data).
Aquaculture Considering its slow growth rate and complex repro-
duction along with its inability to withstand high
In order to supply the worldwide demand that has not fishing pressure, it is crucial and urgent to create
been fulfilled because of decreasing fishing landings, management strategies to protect this endangered
grouper mariculture has started to develop in several species. As highlighted in this current review, there are
regions (Harikrishnan et al. 2010). This trend is key aspects of the biology, ecology and fisheries of the
especially observed in Asia where these species dusky grouper that remain poorly understood, such as
achieve high commercial value in the fishing markets accurate location of spawning aggregations, and
of Hong Kong, Singapore and Taiwan (Pierre et al. spatial and temporal trends in fisheries landing data,
2008). Ottolenghi et al. (2004) reported an increase in which constitute fundamental information for the
annual aquaculture production of groupers from 1991 planning and implementation of efficient management
to 2000 (approximately from 2000 to 9300 tons, actions. Despite these crucial gaps in many areas of its
respectively). Most groupers are cultured in floating geographical distribution, there are fisheries manage-
net cages either in the open sea or at the seaward end of ment actions in place for several Epinephelidae
estuaries (Pierre et al. 2008). However, since mari- species showing promising results (IUCN 2004): (1)
culture depends heavily on wild-caught seed for its A minimum size limit for capture has been imple-
farming, this activity seems unsustainable at current mented for E. albomarginatus in South Africa, where
levels and could also aggravate ongoing overfishing of it is prohibited to catch individuals \ 400 mm TL
this species (Pierre et al. 2008; Sadovy de Mitcheson (Fennessy 2004); (2) a limitation in the number of
et al. 2013). fishing vessels has been used in the Arabian Sea to
Despite the potential usefulness of mariculture for control fishing effort on E. gabriellae (Macllwain et al.
restocking purposes, and its high economic potential, 2008); (3) a total ban has been imposed on the fishing
few aquaculture studies have been undertaken using of E. itajara in Brazil, Puerto Rico and the US Virgin
the dusky grouper, and rearing it is still only on an Islands (Craig 2011), of E. striatus in the US federal
experimental scale (Glamuzina et al. 1999). The first waters and Puerto Rico (Cornish and Eklund 2003),
attempts at artificial reproduction of the E. marginatus and of E. marginatus in France (Pollard et al. unpub-
were made in 1995 by research groups in Italy and lished data); (4) a system of catch quotas has been
Croatia (Glamuzina et al. 1998; Marino et al. 1998). implemented to control fishing of E. albomarginatus
Studies on larval rearing of the dusky grouper were in South Africa (Fennessy 2004), E. striatus in Cuba
also undertaken (Glamuzina et al. 1998; Spedicato (Cornish and Eklund 2003) and Hyporthodus niveatus
et al. 1998; Russo et al. 2009; Kerber et al. 2012; in the USA (Thierry et al. 2008); (5) a fishing ban
Cunha et al. 2013), but successful larval rearing is still during specific periods like spawning seasons and
remains a difficulty in the mariculture of this species spawning aggregations has been implemented for E.
(Pierre et al. 2008; Cunha et al. 2009). During dusky striatus in the Dominican Republic, Mexico, the
grouper cultivation, mortality is mainly linked to low Bahamas and Belize (Cornish and Eklund 2003); (6)
feeding rates and starvation, particularly before or the creation of marine protected areas (MPAs) has
during the onset of exogenous feeding (Glamuzina been broadly used as a conservation tool to protect
et al. 1998; Toledo et al. 2002; López and Orvay 2003; several endangered Epinephelidae species (Claudet
Russo et al. 2009; Kerber et al. 2012). Dusky grouper et al. 2008; Garcı́a-Charton et al. 2008; Wood et al.
reproduction in captivity still poses many problems 2008; Lester et al. 2009; Guidetti et al. 2014; Costello
(Pierre et al. 2008), despite some efforts to and Ballantine 2015; Di Franco et al. 2016).
123
Unfortunately, there is insufficient evidence to Vivien et al. 2008; Hackradt et al. 2014; Di Lorenzo
evaluate the efficiency of some of these management et al. 2016).
approaches. For example, the determination of a The creation of MPAs in the Mediterranean Sea has
minimum size limit to capture protoginic species like been extremely beneficial for dusky groupers, since
the dusky grouper could cause deleterious effects this region constitutes one of the most important parts
because they tended to protect only the younger of the geographical distribution of the species.
individuals, but not stop the removal of larger/older Biological attributes of dusky groupers, such as
females and males (Hixon et al. 2014). In theory, a sedentarism and territorial behavior in adults (Chauvet
greater removal of males, for instance, would decrease and Francour 1990; Lembo et al. 1999, 2002; Spedi-
the male:female sex ratio and could affect the species’ cato et al. 2005; Pastor et al. 2009; Koeck et al. 2014)
reproduction due to the potential diminishing capabil- and a planktonic phase during its larvae development,
ity of male fertilization during spawning aggregations. where individuals can be passively dispersed by sea
Similarly, the removal of larger and older females currents (Andrello et al. 2013), make this species a
could reduce oocyte production because they are more good candidate to respond positively to the protection
efficient in producing greater numbers of higher- provided by MPAs. In fact, a number of studies in both
quality offspring (Berkeley et al. 2004; Hixon et al. Mediterranean and Atlantic MPAs have emphasized
2014). that dusky groupers are benefited by protected areas
On the other hand, the management action of (e.g., Harmelin et al. 1995; Reñones et al. 1999;
fishing prohibition during spawning aggregations is, Lenfant et al. 2003; Garcı́a-Charton et al. 2004, 2008;
probably, an effective way to protect this endangered Tuya et al. 2006; Afonso et al. 2011; Coll et al.
species. Species that periodically and predictably 2012, 2013; Garcı́a-Rubies et al. 2013; Harmelin
congregate can be extremely vulnerable to overex- 2013; Cheminée et al. 2017). The same is true for other
ploitation (Sadovy de Mitcheson and Liu 2008), Epinephelidae in MPAs worldwide (e.g., Chiappone
because once an aggregation is discovered, uncon- et al. 2000; Russ and Alcala 2003, 2010; Anderson
trolled exploitation can have devastating effects on the et al. 2014; Arai 2015).
targeted population. Many coral reef fishes form In a recent study undertaken in several MPAs in the
spawning aggregations that are increasingly the target Mediterranean Sea, Hackradt et al. (2014) showed that
of fishing (Sadovy de Mitcheson and Liu 2008). the average abundances, biomasses and individual
Overfishing has been implicated in the disappearance weights of dusky groupers were higher within the
of grouper aggregations worldwide, including the US protected areas than immediately outside them. Hack-
(Gilmore and Jones 1992), Australia (Domeier and radt et al. (2014) also reported grouper biomass
Colin 1997), Belize (Carter 1989), Mexico (Aguilar- gradients across MPA limits in most studied cases,
Perera and Aguilar-Davila 1996), the Caribbean thus indicating that spillover is likely to occur,
(Olsen and LaPlace 1978; Colin 1992), the western although its spatial scale is probably small (hundreds
Atlantic (Sadovy 1993) and the Indo-Pacific (Johannes of meters). Other studies conducted in the Mediter-
et al. 1999). ranean Sea have also shown a greater abundance of the
Among the aforementioned management actions, dusky grouper inside the MPA, where fishing is totally
the establishment of MPAs has been considered by prohibited, than in other open areas in the same region
several authors as one of the most effective conser- (La Mesa and Vacchi 1999; Lenfant et al. 2003;
vation tools for rebuilding fish stocks (Claudet et al. Garcı́a-Rubies et al. 2013; Harmelin 2013; Guidetti
2008; Garcı́a-Charton et al. 2008; Wood et al. 2008; et al. 2014). Regarding the early life history stages,
Lester et al. 2009; Fenberg et al. 2012; Guidetti et al. Crec’hriou et al. (2010) documented a gradient in egg
2014; Costello and Ballantine 2015; Lubchenco and abundance of Epinephelus spp. across the limits of the
Grorud-Colvert 2015; Di Franco et al. 2016). On the Cabrera National Park as a clue to indicate that this
other hand, spillover—i.e., the export of fish biomass MPA acts as a source of grouper propagules to
from MPAs to adjacent habitats (both in ecological neighboring unprotected areas.
and fisheries terms) is considered a common phe- Andrello et al. (2013) used biophysical modeling to
nomenon, although its spatial extent is usually limited evaluate self-recruitment, larval supply and connec-
to a few hundred meters (Goñi et al. 2008; Harmelin- tivity for Mediterranean MPAs. However, they could
123
not determine MPA productivity because crucial structure throughout its geographical distribution. In
knowledge regarding larval biology is still lacking. contrast, studies on habitat use and behavior were
Hence, precise evaluations of recruitment levels in generally restricted to the Mediterranean Sea, with
Mediterranean MPAs and recruitment supply beyond fewer studies in the Atlantic and Indian Oceans.
MPA borders remain a challenge. On the other hand, Important questions still remain unanswered regarding
Andrello et al. (2013) showed a potential high level of its life cycle, such as: (1) The specific sites and
self-recruitment, but low connectivity, among conditions where reproductive aggregations occur; (2)
Mediterranean MPAs. These modeling results corrob- dispersion patterns of eggs and larvae in the sea on
orate the empirical data of De Innocentis et al. (2001) multiple scales, and subsequent connectivity patterns
on the genetic structure of E. marginatus in the west- with adult stocks and their colonization of rocky
central Mediterranean. These results impose further bottoms, using a multidisciplinary approach; (3)
challenges to the conservation plan of the Convention habitat requirements throughout the life cycle of the
on Biological Diversity (COP10) to create new MPAs, species (based on habitat and niche models on spatial
with connectivity within and among them, to supply scales); (4) the current fishing effort employed world-
larvae all over the Mediterranean continental shelf. wide to catch this endangered species; and (5) the
This conservation action may be even more crucial in management options necessary to maintain viable
the near future, considering that climate change is populations.
likely to affect the connectivity patterns of dusky A suite of tools and techniques have been used to
grouper in the whole Mediterranean region (Andrello investigate the biology and ecology of dusky groupers
et al. 2014). Nevertheless, connectivity studies based worldwide, such as stable isotope analysis (Reñones
on field data at local and regional scales, and on et al. 2002; Condini et al. 2015), otolith microchem-
multidisciplinary approaches, are still needed to istry (Condini et al. 2016b), parasite taxonomy
confirm the outcomes of these large-scale modeling (Marzouk et al. 2010; Roumbedakis et al. 2014) and
studies and to assist in the design of MPA networks genetics (Ramirez et al. 2006; Schunter et al. 2011).
(Calò et al. 2013). Future studies on E. marginatus should strive to
Another form of conservation is from the noncon- further integrate these tools to better understand dusky
sumptive use of the species, where the local commu- grouper population connectivity and habitat use across
nity exploits this emblematic species through scuba its geographical distribution. In order to have more
divers and underwater photography via sustainable efficient public policies and management strategies to
tourism. This practice is common in the national park safeguard this species worldwide, it is crucial to
of Port-Cros, where Briquet-Laugier et al. (2007) increase the collection and availability of fisheries’
estimated that 74% of the scuba divers visiting the catch landing statistics, both in terms of geographic
Port-Cros came to watch groupers, mainly E. margina- representation and data quality. Concomitantly, estab-
tus. In this scenario of rentable tourism (Sala et al. lishing MPAs in other areas beyond the Mediterranean
2013), the dusky grouper is more economically Sea (while further advancing the MPA networks
valuable alive than dead. within this regional sea) and other management
actions (e.g., fishing prohibition during spawning
aggregations, nonconsumptive use of the species via
Conclusions and future research perspectives sustainable tourism) would be highly beneficial to help
the conservation of this species throughout its geo-
The dusky grouper E. marginatus is a large-body graphical distribution.
species playing important ecological roles (e.g., as top
predator and keystone species) in rocky bottom Acknowledgements We are thankful to João P. Vieira,
Eduardo Secchi and Felipe Dumont for comments on an early
ecosystems throughout its wide geographical distri-
draft of the manuscript, Débora Troca for the map and Áthila
bution. Dusky grouper populations across their range Bertoncini for the dusky grouper image. The KAOSA ONG for
are declining due to overfishing and the species is support. This study received financial support from the CAPES-
currently classified as endangered by the IUCN. Our Brasil (PVE N8A101/2013), Fundação O Boticário de Proteção a
Natureza (0962_20122) and PADI Foundation Grant Application
review identified extensive scientific studies on its
(21667), Spanish Ministry for Economy and Competitiveness
feeding ecology, reproductive biology and age
123
(CGL2013-49039-R) and Fundación Séneca (19516/PI/14). MVC Barreiros JP, Santos RS (1998) Notes on the food habitats and
and AMG acknowledge fellowship support from Conselho predatory behaviour of the dusky grouper Epinephelus
Nacional de Desenvolvimento Cientı́fico e Tecnológico (CNPq: marginatus (Lowe, 1834) (Pisces: Serranidae) in the
140570/2013-6 and 305888/2012-9, respectively). Azores, Arquipélago. Life Mar Sci 16A:29–36
Bartoli P, Bray RA, Gibson DI (2003) Opecoelidae (Digenea)
from western Mediterranean fishes: three rare species. Syst
Parasitol 55:81–95
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A Review of The Biology, Ecology, Behavior and Conservation Status of The Dusky Grouper, Epinephelus Marginatus (Lowe 1834)

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Rev Fish Biol Fisheries

A review of the biology, ecology, behavior and conservation

Received: 3 October 2016 / Accepted: 12 October 2017

M. V. Condini (&) A. M. Garcia

Smale (1986) Southern Western 71.8 250–875 300–400; 401–500; 319 No

Bruslé and Mediterranean Sea— – 419 279 19 121 1:2.1 July–August –

Reproductive behavior withdrawals of males by the fishery, thus inducing

Oliver (1984) Western Monogenea Diplectanidae Cycloplectanum riouxi Gills

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