evidence for spawning aggregations of the endangered atlantic goliath grouper in brazil

Journal of Fish Biology (2016)

doi:10.1111/jfb.13028, available online at wileyonlinelibrary.com

Evidence for spawning aggregations of the endangeredAtlantic goliath grouper Epinephelus itajara in southern

Brazil

L. S. Bueno*†‡§, A. A. Bertoncini‡‖, C. C. Koenig¶, F. C. Coleman¶,M. O. Freitas‡**, J. R. Leite‡**, T. F. De Souza† and

M. Hostim-Silva‡††

*Programa de Pós-Graduação em Oceanografia Ambiental, Universidade Federal do Espírito,Santo – Base Oceanográfica – UFES, 565 Rodovia ES 010, km 16, Aracruz, ES 29199-970,

Brazil, †Instituto COMAR – Conservação Marinha do Brasil, 104 Helena Degelmann St,Joinville, SC 89218-580, Brazil, ‡Instituto Meros do Brasil, 67 Benjamin Constant St,

Curitiba, PR 80060-020, Brazil, ‖Laboratório de Ictiologia Teórica e Aplicada (LICTA),Universidade Federal do Estado do Rio de Janeiro – UNIRIO, 296 Pasteur Av., Urca, RJ

22290-240, Brazil, ¶The Florida State University Coastal and Marine Laboratory, 3618Coastal Highway, St Teresa, FL 32358, U.S.A., **Rede Abrolhos, Jardim Botânico St, 920,

Rio de Janeiro, RJ 22.460-000, Brazil and ††Centro Universitário Norte do Espírito,Santo/Universidade Federal do Espírito Santo, Rodovia BR 101 Norte, Km. 60, São Mateus,

ES 29932-540, Brazil

In this study, seasonal numerical abundance of the critically endangered Atlantic goliathgrouper Epinephelus itajara was estimated by conducting scuba dive surveys and calculatingsightings-per-unit-effort (SPUE) at three sites in southern Brazil. Seasonal differences in size andreproductive condition of captured or confiscated specimens were compared. The SPUE differedsignificantly with season, increasing in late spring and peaking during the austral summer months. Asignificant effect was observed in the number of fish relative to the lunar cycle. All females sampledduring the summer were spawning capable, while all those sampled during other seasons were eitherregressing or regenerating. What these data strongly infer is that the E. itajara spawning aggregationsites have been located in the southern state of Paraná and the northern state of Santa Catarina andsummer is the most likely spawning season. Size frequency distributions, abundance and reproductivestate were estimated and correlated with environmental variables.

© 2016 The Fisheries Society of the British Isles

Key words: artificial reefs; endangered species; Epinephelidae; reef fish; South Atlantic.

INTRODUCTION

Atlantic goliath grouper Epinephelus itajara (Lichtenstein 1822), the largest reef fishin the western Atlantic Ocean, is considered critically endangered throughout its range(IUCN, 2013). In the western Atlantic Ocean, it ranges from North Carolina to southernBrazil, including the Gulf of Mexico and the Caribbean Sea. In the eastern AtlanticOcean, its distribution extends from Senegal to Congo, although it is rare in the CanaryIslands (Ferreira et al., 2012) and is believed to be extinct in the eastern Atlantic Ocean

§Author to whom correspondence should be addressed. Tel.: +55 47 96346873; email: [email protected]

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© 2016 The Fisheries Society of the British Isles

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from Senegal to Congo (Craig et al., 2009). Epinephelus itajara can reach over 2 min total length (LT) and weigh up to 400 kg with late maturation at around 6–8 years(males between 110 and 115 cm LT, and females between 120 and 135 cm LT) withlongevity of at least 37 years (Bullock et al., 1992; Sadovy & Eklund, 1999).

Epinephelus itajara form reproductive aggregations in shallow water (<50 m) (Fer-reira et al., 2012; C. C. Koenig & F. C. Coleman, unpubl. data), with a preference forhigh-relief rocky and artificial reefs (C. C. Koenig & F. C. Coleman, unpubl. data).Their spawning aggregations may consist of >100 individuals (Bullock et al., 1992;Sadovy & Eklund, 1999; Koenig et al., 2007, 2011; C. C. Koenig & F. C. Coleman,unpubl. data). Domeier (2012) defined reproductive aggregations as single species thatgather at specific times at specific locations at densities or numbers that are signifi-cantly higher than those found at the same site during non-reproductive times. Theseaggregations generally occur at the same time and same site annually (Johannes, 1978;Carter & Perrine, 1994; Sadovy et al., 1994; Domeier & Colin, 1997).

Gerhardinger et al. (2009) using fishermen’s local ecological knowledge andFreitas et al. (2015), based on biological evidences suggested that the E. itajara spawnduring the summer (January to March) in south Atlantic, similar to summer spawning(July to September) in the northern hemisphere (Bullock et al., 1992). Knowledgeand protection of these spawning aggregations are key factors for the species’ persis-tence (Sadovy de Mitcheson & Colin, 2012). Fishers threaten species persistence bytargeting spawning aggregations to increase catch per effort.

In Brazil, E. itajara are protected by a fishing moratorium set in place in 2002 for5 years (2002–2007), renewed in 2007 for another 5 years (2008–2012) and again in2012 for additional 3 years (2012–2015). Illegal catches, however, continue (Giglioet al., 2014) which stifles stock recovery and reduces any ability to understand theirecology. During the processing of this manuscript the moratorium was renewed inOctober of 2015, protecting goliath grouper for more 8 years in Brazil (2015–2023).

This study was initiated to provide critical data relevant to the effective managementand conservation of E. itajara in Brazil. The main objective was to locate and verifyE. itajara spawning aggregations in southern Brazil and to describe the physical andbiological characteristics of spawning sites as well as seasonal timing of spawning.

MATERIALS AND METHODS

S T U DY A R E A

The study area was located in southern Brazil, between 25∘ and 27∘ south latitude in thewestern Atlantic Ocean (Fig. 1). The region has distinct seasonality with summer (late Decemberthrough to late March) being the warmest months. During this time, moderate east and north-eastwinds predominate, bringing warm (up to 27∘ C) clear waters from the east. The weather is morevariable in autumn (late March through to late June), and spring (late September through to lateDecember) with an increase in large eastern and south-eastern swells and a coincident decreasein underwater visibility. The winter (late June through to late September) is dominated by coldfronts that bring very large swells from the south and south-east, decreasing water temperature(18∘ C) and increasing turbidity in coastal waters. The surface currents 3·6 m deep in this regionin summer and spring, direct currents towards the coast and parallel to the coast in the autumnand winter (E. A. M. Stein & M. A. Noernberg, unpubl. data).

Three artificial reefs were chosen as sampling sites: two in the state of Paraná–BalsaNorte (BN) and Marine Artificial Reefs (RAM), and one offshore in the state of Santa

© 2016 The Fisheries Society of the British Isles, Journal of Fish Biology 2016, doi:10.1111/jfb.13028

R E P RO D U C T I O N O F E P I N E P H E L U S I TA JA R A 3

25° 30' S

25° 45' S

26° 0' S

26° 15' S

26° 30' S

48° 30' W 48° 15' W

SäoFrancisco

do Sul

Monobóia

RAMBalsa Norte

Paranagua

Guaratuba

N

Fig. 1. Map of Brazil indicating the study area on the left and an expanded view of the study sites on the rightincluding Balsa Norte (BN), Marine Artificial Reefs (RAM) and Monobóia (MB).

Catarina–Monobóia (MB). These three sites were selected after 7 years of dive samples at eightdifferent reef areas. The selection criteria were frequency and abundance of E. itajara.

The shipwreck Balsa Norte was intentionally sunk in January 2001 to form an artificial reefand is located 38 km offshore at a depth of 27 m. The ship is 76·3 m long× 11·4 m wide× 5 mhigh with large features and dark crevices (Fig. 2). The RAM site is composed of two reef areas,separated by 1 km, each composed of 30 concrete structures, block forms and reef balls, sunk inJune 2000. The structures are 1·5 m high, spread on the sand in an area of 30 m× 30 m (Fig. 2).These structures occur 12 km offshore at a depth of 18 m over sand bottom. Since both areascompose one single site, they were sampled on the same day.

The Monobóia is an artificial reef, formed by pipelines, manifolds and some concrete andmetallic structures, installed in the 1970s. This reef is attached to a single point mooringbuoy located 8 km offshore, where tankers moor to unload oil. The main artificial reef area is50 m× 50 m and is composed of diverse materials spread on the sand at 25 m deep. A protectivestructure, located on top of the manifold, is 9 m long, 8 m wide and 2 m high. Flexible pipelinesextend from the manifold to the surface buoy, and six heavy chains, arranged in a radial pattern,support the entire structure which extends from the bottom to the surface (Fig. 2).

DATA C O L L E C T I O N

Data were collected from: (1) underwater visual census (UVC) using scuba, (2) photographsof E. itajara taken during scuba dives, (3) live specimens obtained by hook-and-line and (4)dead specimens donated by law enforcement officers. All activities were authorized by licenses:SISBIO 15080-2 and SISBIO 31719-1.

U V C S U RV E Y S

Between 2007 and 2014, UVC surveys were conducted for E. itajara at all three study sitesduring each season, with greater emphasis during summer. The roving diver technique (RDT)


4 L . S . B U E N O E T A L.

RAM Monobóia Balsa norte

Fig. 2. Sketches and photographs of artificial reefs study sites: RAM, Monobóia and Balsa Norte. Drawings fromR. Schlögel and photographs from L. S. Bueno.

(Jones & Thompson, 1978) was used, with the surveys conducted only when visibility exceeded3 m. During UVC, each site was thoroughly surveyed including all crevices and the surroundingperimeter. Temperature, visibility and number of E. itajara encountered were recorded.

Epinephelus itajara were photographed to determine size, with size estimations conductedusing two parallel laser beams, 25 cm apart, when fish were perpendicular to the beams. In thephotograph, laser dots appearing on the fish are used to determine the fish’s LT in cm size classes(Koenig et al., 2011).

C AT C H S U RV E Y S

In addition to the diving surveys, E. itajara were captured with hook-and-line. After the fishwas hooked, it was slowly brought to the surface, gently pulled onto a stretcher on the deck ofthe boat and strapped down. The fish was then vented using a trocar and cannula, eyes werecovered with a wet towel (to avoid eye damage from the sun) and gills were irrigated with seawater from a pump. The fish were measured (cm LT) and tagged using conventional dart tagsfor the purpose of identifying individuals during subsequent UVC or recapture. Gonad biopsieswere obtained by inserting one end of a plastic tube (0·7 cm ID) through the gonoduct into thegonad; the other end was attached to a manually operated vacuum pump. The pump was used tosuck gonad tissue into an in-line vial (135 ml). The contents were immediately preserved in 10%formalin for 24 h, and then transferred to 70% ethyl alcohol. After sampling, fish were releasedat the same site. Gonad samples were also obtained from dead fish donated by law enforcementofficials. These samples were processed in the same manner as those from captured fish.

Gonad tissue samples were embedded in paraffin, sectioned to 4–6 um, stained inhaematoxylin-eosin and then examined under a compound microscope to determine sexand reproductive condition. For gonad analysis, five developmental phases were used followingBrown-Peterson et al. (2011): immature (IM), developing (DV), spawning capable (SC),regressing (RG) and regenerating (RT). The IM phase corresponds to fish that have neverspawned, characterized histologically in females by the presence of oogonia and primarygrowth oocytes through the perinuclear stage (Grier et al., 2009), as well as little space amongoocytes in the lamellae and ovarian wall generally thin. In DV females, the ovary is beginningto develop, but not ready to spawn. The SC fish are developmentally and physiologically able



to spawn; RG represents the cessation of spawning, and the RT phase corresponds to a sexuallymature, but reproductively inactive individual.

DATA A NA LY S I S

Sightings data obtained during diving surveys were transformed into sightings-per-unit-effortSPUE (equation 1), thus taking into account the different dive sampling times (in min) for eachsurvey. For the purpose of this index, 30 min was the standard effort time because this was theaverage time of surveys.

y = nTt−1 (1)

where y is SPUE, n the number of fish observed, T the duration in min of each survey and t isthe 30 min to standardization efforts.

A three-factor PERMANOVA (season× site× lunar phase) design was used to evaluate dif-ferences in SPUE by season. A one-way PERMANOVA was applied to evaluate differencesin sightings per unit effort by months. Linear regression was used to evaluate the relation-ship between water temperature and SPUE, as well as the relationship between underwatervisibility and SPUE. Approximately, a four-fold increase in spawning season abundance overaverage monthly abundance was considered as strong evidence for spawning aggregation forma-tion (Domeier, 2012). The seasons were defined by the Gregorian calendar. Lunar phases weredefined as new moon, first quarter, full moon and third quarter. Each phase consisted of thepeak± 3 days (=7 days total). The LT classes were created using the Sturges’s formula (Vieira,2003).

RESULTS

D I V I N G S U RV E Y

Between 2007 and 2014, 107 RDT surveys were distributed over the three study sitestotalling 3040 min (50·7 h sampling effort; Table I). Epinephelus itajara were sightedmore frequently during surveys at Balsa Norte (at least one present at 100% of thesamples) followed by Monobóia (96·2%) and RAM (74%). Monobóia was also the sitewhere the highest number of E. itajara was observed during a single survey (n= 54)(32 for RAM and 30 for Balsa Norte).

SPUE of E. itajara was higher during summer at Monobóia, RAM and Balsa Norte.High values were also observed during spring at Monobóia and RAM. Comparisonof seasonal mean abundance for spring and summer showed mean values (15 and 12)more than four times higher than autumn and winter (1·5 and 2·9) (Table II).

Table I. Characteristics of three primary study sites off southern Brazil

Characteristics Balsa Norte RAM Monobóia

Site area (m2) 870 900 2500Height of site (m) 5 1·5 25Number of surveys 25 30 52Total time (min) 635 761 1644Mean± s.d. effort time 29·2± 5·8 26·5± 8·7 28·8± 8·4


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Table II. Seasonal differences in sightings-per-unit-effort (SPUE; unit effort= 30 min survey)for Epinephelus itajara on artificial habitats in southern Brazil, showing number of dive surveys(n samples), and maximum abundance (max), minimum abundance (min) and mean± s.d. SPUE

Season Samples (n) Max Min Mean± s.d.

Spring 23 22 8 15·2± 3·1Summer 47 54 0 12·6± 12·8Autumn 27 4 0 1·5± 1·4Winter 10 5 1 2·9± 1·5

PERMANOVAs of E. itajara SPUE showed significant differences among seasons(F3,107 = 33·53, P< 0·05). Pair-wise comparisons showed differences among all sea-sons, except for winter and autumn (Table III). Furthermore, summer had many extremevalues with high abundances exceeding other seasons. Spring showed high abundancesin mid-December, a few days before the summer.

Months that show greatest maximum values in abundance were February (n= 54)followed by January (n= 42), December (n= 34) and November (n= 20). Comparingsightings among months, January had the highest mean SPUE followed by February,December and November (Fig. 3). A sudden drop in abundances occurred in March,reaching a low value in July. The PERMANOVA one-way test of SPUE by monthsshowed that November, December, January and February, each showed significant dif-ferences from the other months (P< 0·05).

Size-class distributions measured by lasers (n= 126) and catches (n= 10) by season(Fig. 4) were examined. LT ranged from 50 to 230 cm. The most abundant LT classesin summer were 98–121, 146–169 and 170–193 cm, summer being the only seasonwith specimens >194 cm.

While the mean size of fish appeared to differ little among seasons (Table IV), thegreatest range in LT and the largest fish were recorded during summer (Fig. 4) whilethe smallest (50 cm) was observed during autumn.

G O NA D S A M P L E S

Gonad samples were obtained from 17 E. itajara (15 females and two males): 10collected from the study sites, one that was found dead and six obtained from law

Table III. Pair-wise a posteriori comparison of seasonal differences in Epinephelus itajarasightings-per-unit-effort (SPUE) (t-statistic on pseudo-F values)

Season t P

Summer×winter 4·42 <0·05Summer× autumn 3·19 <0·05Summer× spring 2·53 <0·05Winter× autumn 7·79 >0·05Winter× spring 20·75 <0·05Autumn× spring 14·65 <0·05



JanuaryFebruary

MarchApril

MayJune

JulyAugust

SeptemberOctober

NovemberDecember

60

50

40

30

20

10

0

SPU

E

Fig. 3. Monthly average SPUE (sightings-per-unit-effort) of Epinephelus itajara determined by roving diver sur-veys conducted from 2007–2014 at Monobóia, RAM and Balsa Norte artificial reefs in southern Brazil.Error bars represent the maximum values observed and black dots represent means.

enforcement officers. Confiscated specimens (n= 6) obtained during winter (16 July2011) from areas close to the study sites were also sampled. Four of these werefemales (132, 144, 148 and 180 cm LT) and two were males (136 and 147 cm). Allfemales were in the RT stage [Fig. 5(a)], indicating that they were not reproduc-tively active. Among the E. itajara collected, seven females (100–195 cm) obtainedfrom RAM during December and January of 2013 and January and February of

30

25

20

15

10

5

0

50–7

3·9

74–9

7·9

98–1

21·9

122–

145·9

146–

169·9

170–

193·9

194–

217·9

218–

241

Num

ber

of fi

sh

LT classes (cm)

Fig. 4. Total length (LT) class distributions of Epinephelus itajara from south Brazil relative to seasons ( ,autumn; , spring; , summer; , winter), measured in situ using laser metrics, hook-and-line samples andconfiscated specimens from 2007 to 2014. The dashed vertical line marks size at 50% maturity, accordingto Bullock et al. (1992) and Freitas et al. (2015).


8 L . S . B U E N O E T A L.

Table IV. Seasonal differences in the mean± s.e. total length (LT) of all Epinephelus itajarameasured with lasers and caught from study sites off southern Brazil (pooled Balsa Norte, RAM

and Monobóia)

Season n LT (cm)

Autumn 7 121·4± 12·0Spring 18 125·0± 5·7Summer 87 137·2± 4·6Winter 14 126·4± 6·4Total 126 133·4

n, sample size.

2014 were at SC phase [Fig. 5(b)]. A partially decayed E. itajara found on 27December 2012 was sampled revealing a female (230 cm LT), also at SC phase. Afemale (159 cm LT) captured on 4 February 2014 at RAM was in SC phase, at theactively spawning sub-phase with hydrated oocytes [Fig. 5(c)]. Another two femalescaptured at the same site on 14 February 2013 (119 cm LT) and 10 January 2014(205 cm LT) were in post-spawning condition with post-ovulatory follicles (POFs)[Fig. 5(d)].

C O R R E L AT I O N W I T H E N V I RO N M E N TA L VA R I A B L E SA N D M O O N P H A S E S

Assuming that November to February is the spawning season, the factors that mayinfluence aggregating behaviour in this period were analysed. SPUE of E. itajarashowed no correlation with either water temperature (r2 = 0·02, P> 0·05) or visibility(r 2 = 0·003, P> 0·05).

Comparing the abundance among lunar phases, the full and new moons had higherSPUE mean and maximum values (Fig. 6; peak of error bar) when compared to otherphases. The maximum value of SPUE was associated with the new moon phase (Fig. 6;peak of error bar). The PERMANOVA for SPUE showed that moon phase has a sig-nificant effect on E. itajara aggregation (P< 0·05). The pair-wise test showed that newmoon is significantly more important (P< 0·05) than the full moon and second quarter.

DISCUSSION

According to Sadovy de Mitcheson et al. (2008), spawning aggregations of manyspecies have been severely disrupted by overexploitation and loss of habitat to thepoint of disappearing from traditional sites. This is a global phenomenon that bringsa sense of urgency to the need to better understand how aggregations function wher-ever they occur (Nemeth, 2009). In southern Brazil in the 1950s, for instance, E. ita-jara aggregations were quite large and also heavily fished (Souza, 2000; Gerhardingeret al., 2006). Nowadays, most of the aggregations known from anecdotal referenceshave disappeared without being even documented. Historically, little is known aboutthe dynamics of reproductive aggregations of reef fish or the locations and timing ofspawning in the South Atlantic Ocean. This study is the first to describe E. itajara



Fig. 5. Photomicrographs of histological sections of ovarian biopsies of Epinephelus itajara sampled in southBrazil (×10 magnification): (a) female, 144 cm total length (LT), sampled in July 2011, in regenerating (RT)phase (MB, muscle bundle; PG, primary growth oocyte), (b) female, 230 cm LT, sampled on 27 Decem-ber 2012, showing spawning-capable reproductive phase (CA, cortical alveolar; PG, primary growth; Vtg,primary vitellogenesis oocyte; Vtg3, tertiary vitellogenic oocyte; GVM, germinal vesicle migration), (c)female, 159 cm LT showing capable of spawning (SC) phase in active spawning condition (H, hydratedoocytes) and (d) female 205 cm LT, sampled on 10 January 2014, in the post-spawning reproductive phase(POF, post-ovulatory follicle complex).

spawning aggregations in south Brazil, based on histological data and seasonal abun-dance recorded from diver surveys.

Based on the definition of Domeier (2012), the abundance data indicate that spawningaggregations of E. itajara are formed near artificial reefs. Moreover, data also suggeststhat there is a seasonal component for the aggregation, with highest abundance valuesin summer months. Therefore, the extreme values and significant differences observedbetween the seasons are also strong evidences for the occurrence of spawning aggre-gations. According to Colin et al. (2003), to identify a spawning aggregation site, thearea must meet two main criteria: (1) a sudden increase in the number of individualsin a certain location and certain time and (2) that the physical characteristics of thefish suggest imminent reproduction including changes in colour patterns, distendedabdomens or the presence of hydrated eggs, post-ovulatory follicles or viewing therelease of gametes in the water column. These two criteria were satisfied in this study:the number of E. itajara increased significantly during the summer, November toFebruary, and fish were reproductively active (spawning capable, SC and RG phases,with hydration and POFs oocytes) during this time. Thus, with both of these criteria


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60

50

40

30

20

10

0

SPU

E

Newmoon

Fullmoon

Firstquarter

Secondquarter

Fig. 6. Mean values of SPUE (sightings-per-unit-effort) of Epinephelus itajara among lunar phases, for pooledmonths (November, December, January and February) from 2007–2014 in south Brazil. Peak of error barsindicate maximum number observed.

satisfied, it is likely that the spawning sites and seasons for E. itajara have beencorrectly identified. Summer spawning has also been confirmed in the south-easternU.S.A. (Colin, 1990; Bullock et al., 1992; Eklund & Schull, 2001; Koenig et al.,2011).

Spawning of E. itajara occurs at night according to Mann et al. (2009). Spawningwas not observed in this study because the surveys were conducted during the day, butthe observation of night-time spawning is difficult even in the best of conditions (C.C. Koenig & F. C. Coleman, unpubl. data). Nevertheless, behaviours were seen thatare believed to be related to courtship and spawning such as ‘stacking behaviour’ andcolouration changes were observed, both of which were reported by Colin (1990) inhis description of E. itajara on spawning sites in south-western Florida.

The three study sites are located near large estuarine areas (Paranaguá, Guaratubaand Babitonga Bay). This proximity may be a factor for E. itajara choosing these asspawning areas, since juveniles are mangrove-dependent during their first 5–6 years(Koenig et al., 2007). This hypothesis is reinforced by the fact that a surface currentflows towards the coast in this region during spring and summer (E. A. M. Stein & M.A. Noernberg, unpubl. data) possibly transporting eggs and larvae to suitable mangrovehabitats.

Among the sites, Monobóia had the highest abundances of E. itajara during aggre-gation time and throughout the year, this may be related to two characteristics: (1) thesite has the most complex structure, including many artificial reefs, anchors, chains,pipelines and concrete and (2) there may be an advantage to the fish in having thestructure extend from the bottom to the surface. Epinephelus itajara avoid very coldwater [temperatures below 15∘ C may be lethal (Sadovy & Eklund, 1999)], so thenear-surface structure may provide refuge from cold water brought onto the shelf byupwelling events, known to occur in the area. Supporting this hypothesis, E. itajarawere observed occupying the higher vertical structures during the presence of strongthermoclines.



Fifty-five per cent of individuals observed during the dives were >130 cm LT.According to Bullock et al. (1992) and Koenig et al. (2011), this size is probablyadult, but the size range of smaller individuals extended from 98 to 121 cm LT,suggesting either that all the individuals at the purported spawning sites did notactively participate in spawning or that size at maturity is lower in southern Brazilthan it is in Florida (Bullock et al., 1992) and in Abrolhos Bank Brazil (Freitas et al.2015), that all of the individuals present participated in spawning. The latter is likelybecause histological samples of ovaries from two females, 100 and 119 cm LT, weremature (spawning capable and post-spawning phases). Smaller sizes at maturity maybe related to overfishing (Dayton et al., 2003) which occurred in this area. Thesefindings, combined with the estimates of size structure, provide data required for stockassessment models, while replication of the visual surveys across sites and over timecould provide an index of abundance within the study area (Porch & Eklund, 2004;Porch et al., 2006).

Several studies (Gerhardinger et al., 2006, 2009; Mann et al., 2009; C. C. Koenig& F. C. Coleman, unpubl. data) have shown a lunar pattern to spawning of E. itajara.Similar lunar patterns of aggregation activity have been observed with the fish here, butacoustic recordings, such as those used by Mann et al. (2009) are needed to confirmthat night-time sounds in Brazil are similar to those observed in the Gulf of Mexico.

New technologies such acoustic telemetry and passive acoustic monitoring areneeded to improve the knowledge of the location and nature of E. itajara spawningaggregations in Brazil. Protection of these aggregation locations should be a highpriority, but the condition of mangroves, the primary juvenile habitat, should also beimproved once the most productive habitats are found. Continued research will providethe necessary impetus for the conservation and production of this species. Based onthe present experience and findings, long-term and intensive short-term monitoringstrategies are recommended to fully characterize trends in seasonal abundance andhabitat use for E. itajara. On the other hand, during this study, diving surveys atthe Monobóia, the most important spawning site after the summer of 2012, wereprohibited. This restriction, imposed by the organization maintaining the structure,seriously compromised ongoing studies of E. itajara spawning in south Brazil.

N E E D S F O R M A NAG E M E N T A N D E N F O R C E M E N T

Illegal fishing of E. itajara in Brazil (Giglio et al., 2014), and more specifically inthe study area, is very common. Unfortunately, apprehensions and punishment, such asthe one carried out by Federal Maritime Police Special Core-NEPOM/SDF during thepresent research, are rare. As enforcement operations are uncommon, illegal fishing isnot being controlled in the region. Two actions that could prove to be effective are theestablishment of marine protected areas (MPA) around the presumed spawning areasand increased enforcement during the spawning season. An MPA called the NationalMarine Park of Currais Islands was established on 20 June 2013, this was an importantfirst step because it protects one of the studied sites (RAM). Such protection shouldbe expanded to include other spawning sites as well as increases in surveillance andenforcement.

Enforcement is an important deterrent to illegal fishing, but raising awareness of thepublic about the value of E. itajara aggregations for dive tourism may be equally effec-tive. Monetary benefits of ecotourism dives on Nassau grouper Epinephelus striatus


12 L . S . B U E N O E T A L.

(Bloch 1792) aggregations were described by Sala et al. (2003), and are also beingused by dive boat operators in south-eastern Florida since multiple dive boats are fer-rying divers out to see E. itajara aggregations nearly every day and the business isexpanding (C. C. Koenig, pers. obs.). When government agencies realize that healthypopulations and aggregations of E. itajara can increase revenues through ecotourism,there will be increased incentive for protection.

In addition to illegal fishing, pollution and mangrove habitat destruction threaten thesurvival of E. itajara populations in Brazil. Koenig et al. (2007) have clearly demon-strated the importance of mangrove habitat to juvenile E. itajara in the south-easternU.S.A. High water quality standards in mangrove and coastal habitats must be main-tained or the consequences could be dire, not only for E. itajara, but also for manyother estuary-dependent species as well.

This study shows evidence for the formation of spawning aggregations of E. itajarain southern Brazil, and provides a starting point for additional research into the ecol-ogy and behaviour of this endangered species over a broader area. It is intended toraise awareness of the importance of the areas described here as highly significant tothe recovery of E. itajara populations throughout southern Brazil. Through this aware-ness, management agencies must continue to take effective conservation measures thatwill lead to population recovery and therefore benefit both a limited fishery and anecotourism dive industry.

We are grateful to J. A. Alves, T. F. Souza, F. Darros, R. L. Velo and L. F. Machado for theiractive participation in this research. We also thank all Meros of Brazil Project team, which issponsored by Petrobras, and all the team of Fish Ecology Lab (FSUCML). L.S.B. has receiveda scholarship from FAPES (Fundação de Amparo a Pesquisa do Espírito Santo) and Sandwichscholarship by CAPES Foundation, Ministry of Education of Brazil from PDSE programme.Thanks to P. C. Pinheiro, A. Cattani, V. Abilhoa and D. A. Moreira. We would like to acknowl-edge the support from COMAR Institute, Lancha Furacão and Submarine Serviços for providingimportant technical help for dive operations.

References

Brown-Peterson, N. J., Wyanski, D. M., Saborido-Rey, F., Macewicz, B. J. & Lowerre-Barbieri,S. K. (2011). A standardized terminology for describing reproductive development infishes. Marine and Coastal Fisheries: Dynamics, Management, and Ecosystem Science3, 52–70.

Bullock, L. H., Murphy, M. D., Godcharles, M. F. & Mitchell, M. E. (1992). Age, growth, andreproduction of jewfish, Epinephelus itajara, in eastern Gulf of México. Fishery Bulletin90, 243–249.

Carter, J. & Perrine, D. (1994). A spawning aggregation of dog snapper, Lutjanus jocu(Pisces: Lutjanidae) in Belize, Central America. Bulletin of Marine Science 55,228–234.

Colin P. L. (1990). Preliminary investigations of reproductive activity of the Jewfish,Epinephelus itajara (Pisces: Serranidae). In Proceedings of the 43rd Gulf and CaribbeanFisheries Institute (Goodwin, M. H. & Waugh G. T., eds). Miami, FL: Gulf andCaribbean Fisheries Institute.

Colin, P. L., Sadovy, Y. J. & Domeier, M. L. (2003). Manual for the study and conservation ofreef fish spawning aggregations. Society for the Conservation of Reef Fish AggregationsSpecial Publication 1, 98.

Craig, M. T., Graham, R. T., Torres, R. A., Hyde, J. R., Freitas, M. O., Ferreira, B. P.,Hostim-Silva, M., Gerhardinger, L. C., Bertoncini, A. A. & Robertson, D. R. (2009).How many species of goliath grouper are there? Cryptic genetic divergence in a threat-ened marine fish and the resurrection of a geopolitical species. Endangered SpeciesResearch 7, 167–174.



Dayton, P. K., Thrush, S. & Coleman, F. C. (2003). Ecological Effects of Fishing in MarineEcosystems of the United States. Arlington, VA: Pew Oceans Commission.

Domeier, M. L. (2012). Revisiting spawning aggregations: definitions and challenges. In ReefFish Spawning Aggregations: Biology, Research and Management (Sadovy de Mitche-son, Y. & Colin, P. L., eds), pp. 1–20. Dordrecht: Springer. doi: 10.1007/978-94-007-1980-4_12

Domeier, M. L. & Colin, P. L. (1997). Tropical reef fish spawning aggregations: defined andre-viewed. Bulletin of Marine Science 60, 698–726.

Eklund, A. & Schull, J. (2001). A stepwise approach to investigating the movement patterns andhabitat utilization of goliath grouper, Epinephelus itajara, using conventional tagging,acoustic telemetry and satellite tracking. In Electronic Tagging and Tracking in MarineFisheries (Sibert, J. R. & Nielsen, J. L., eds), pp. 189–216. Dordrecht: Kluwer AcademicPublishers.

Ferreira, B. P., Hostim-Silva, M., Bertoncini, A. A., Coleman, F. C. & Koenig, C. C. (2012).Atlantic goliath grouper – Epinephelus itajara. In Reef Fish Spawning Aggregations:Biology, Research and Management (Sadovy de Mitcheson, Y. & Colin, P. L., eds), pp.417–422. Dordrecht: Springer. doi: 10.1007/978-94-007-1980-4_12

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, Epinephelusitajara (Actinopterygii: Perciformes: Serranidae), in eastern Brazil. Acta Ichthyologicaet Piscatoria 45, 1–11.

Gerhardinger, L. C., Medeiros, R., Marenzi, R. C., Bertoncini, A. A. & Hostim-Silva, M. (2006).Local ecological knowledge on the goliath grouper Epinephelus itajara. NeotropicalIchthyology 4, 441–450.

Gerhardinger, L. C., Hostim-Silva, M., Medeiros, R. P., Matarezi, J., Bertoncini, A. A.,Freitas, M. O. & Ferreira, B. P. (2009). Fishers’ resource mapping and goliath grouperEpinephelus itajara (Serranidae) conservation in Brazil. Neotropical Ichthyology 7,93–102.

Giglio, V. J., Bertoncini, A. A., Ferreira, B. P., Hostim-Silva, M. & Freitas, M. O. (2014). Land-ings of goliath grouper, Epinephelus itajara, in Brazil: despite prohibited over ten years,fishing continues. Natureza & Conservação 12, 118–123.

Grier, H. J., Uribe-Aranzábal, U. C. & Patiño, R. (2009). The ovary, folliculogenesis, and ooge-nesis in teleosts. In Reproductive Biology and Phylogeny of Fishes (Jamieson, B. G. M.,ed), pp. 25–84. Enfield, NH: Science Publishers.

Johannes, R. E. (1978). Reproductive strategies of coastal marine fishes in the tropics. Environ-mental Biology of Fishes 3, 65–84.

Jones, R. S. & Thompson, M. J. (1978). Comparison of Florida reef fish assemblages using arapid visual technique. Bulletin of Marine Science 28, 159–172.

Koenig, C. C., Coleman, F. C., Eklund, A. M., Schull, J. & Ueland, J. (2007). Mangroves asessential nursery habitat for goliath grouper (Epinephelus itajara). Bulletin of MarineScience 80, 567–586.

Koenig, C. C., Coleman, F. C. & Kingon, K. (2011). Pattern of recovery of the goliath grouperEpinephelus itajara population in the southeastern US. Bulletin of Marine Science 87,1–20. doi: 10.5343/bms.2010.1056

Mann, D. A., Locascio, J. V., Coleman, F. C. & Koenig, C. C. (2009). Goliath grouper(Epinephelus itajara) sound production and movement patterns on aggregation sites.Endangered Species Research 7, 229–236.

Nemeth, R. S. (2009). Dynamics of reef fish and decapod crustacean spawning aggregations:underlying mechanisms, habitat linkages, and trophic interactions. In Ecological Con-nectivity among Tropical Coastal Ecosystems (Nagelkerken, I., ed), pp. 73–134. NewYork, NY: Springer.

Porch, C. E. & Eklund, A. M. (2004). Standardized visual counts of goliath grouper off southFlorida and their possible use as indices of abundance. Gulf of Mexico Science 2,155–163.

Porch, C. E., Eklund, A. M. & Scott, G. P. (2006). A catch-free stock assessment model withapplication to goliath grouper (Epinephelus itajara) off southern Florida. Fishery Bulletin104, 89–101.


14 L . S . B U E N O E T A L.

Sadovy de Mitcheson, Y. & Colin, P. L. (Eds) (2012). Reef Fish Spawning Aggregations:Biology, Research and Management. Dordrecht: Springer. doi: 10.1007/978-94-007-1980-4_12

Sadovy, Y. & Eklund, A.M. (1999). Synopsis of biological data on the Nassau grouper,Epinephelus striatus (Bloch, 1792), and the jewfish, E. itajara (Lichtenstein, 1822).NOAA Technical Report NMFS 146.

Sadovy, Y., Colin, P. L. & Domeier, M. L. (1994). Aggregation and spawning in the tigergrouper, Mycteroperca tigris (Pisces: Serranidae). Copeia 1994, 511–516.

Sadovy de Mitcheson, Y., Cornish, A., Domeier, M. L., Colin, P., Russell, M. & Lindeman, K.(2008). A global baseline for spawning aggregations of reef fishes. Conservation Biology22, 1233–1244.

Sala, E., Arbuto-Oropeza, P. G. & Thompson, G. (2003). Spawning aggregations and repro-ductive behavior of reef fishes in the Gulf of California. Bulletin of Marine Science 72,103–201.

Souza, H. S. (2000). O homem da ilha e os pioneiros da caça submarina, 2nd edn. Florianópolis:Editora Dehon.

Vieira, S. (2003). Bioestatística: tópicos avançados. Rio de Janeiro: Elsevier.

Electronic Reference

IUCN (International Union for the Conservation of Nature) (2013). IUCN Red List of ThreatenedSpecies. Available at www.iucnredlist.org (last accessed 25 August 2013).


evidence for spawning aggregations of the endangered atlantic goliath grouper in brazil

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