Fisheries Research 242 (2021) 106037

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Fisheries Research
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Spawning aggregation sites of the cubera snapper, Lutjanus cyanopterus, on

the continental shelf of Bahia state, Northeastern Brazil
Priscilla Nogueira Malafaia *, Aline Rocha França, George Olavo
State University of Feira de Santana, Laboratory of Fisheries Biology, Postgraduate Program in Earth Sciences and Environment Modeling – PPGM/UEFS, Km 3, BR 116,
University Campus, s/n. Module I, UEFS, Novo Horizonte, 44031460 - Feira de Santana, BA, Brazil.

A R T I C L E I N F O A B S T R A C T

Handled by George A. Rose The cubera snapper (caranha), Lutjanus cyanopterus, is an important resource for reef fisheries in Northeastern
Brazil, currently classified as Vulnerable (VU) on the Red List of Threatened Species. This species forms large
Keywords: transient reproductive aggregations, concentrating their reproductive efforts in a short period of the year and in
Reef fisheries specific spawning sites, which have already been well documented in the Caribbean. These aggregations are
Reproductive aggregation
predictable in time and space, making them considerably vulnerable to overfishing and other sources of an­
Lutjanidae
thropic impacts. These tend to reduce the population’s renewal capacity and genetic diversity, thus contributing
Recovery plans
to the decline of fish stocks and to the process of local extinctions. Between 2009 and 2010 we identified two
L. cyanopterus aggregation sites, commonly known as “Caranheiros”, in two sub-areas located at the continental
shelf-break zone of Bahia state, Northeastern Brazil, in the East Brazil Shelf Large Marine Ecosystem (LME16),
between latitudes 12 ◦ S and 15 ◦ S. The present study aims to (1) describe patterns of spatial and temporal
distribution, and the biological characteristics of L. cyanopterus’ catches from line fisheries targeting the specific
aggregations in the two Caranheiros sites; and (2) validate the reproductive character of these aggregations
through macroscopic evaluation of sexual maturity phases of the fishes caught. We analyzed fisheries and bio­
logical sampling data from the catches of artisanal fleets monitored in the two sub-areas between 2005 and 2014.
The identified aggregations occur annually from December to May, with capture peaks concentrated in waning to
waxing moon phases, in January, February and March. The predominance of mature, pre-spawning and spent
(recent spawning) individuals, males and females, in these aggregations revealed the reproductive activity in
both sites. Identifying and validating these spawning sites may contribute to the development of recovery and
conservation plans for this threatened species. The continuous monitoring of fisheries on aggregations is a pri­
ority, aiming to trigger management responses and adaptative fisheries management. Considering these sites are
highly vulnerable and have high local socioeconomical importance, especially to traditional fishers, the exact
location of the analyzed “Caranheiros” is not revealed in this publication. However, it has been made available to
the government agencies responsible for fisheries control and surveillance, as well as for implementing man­
agement and conservation measures for the sustainable use of fisheries resources.

1. Introduction et al., 2012). However, its first occurrence on the Flores Island, Azores
Archipelago, Northeast Atlantic was published by (Ribeiro et al., 2017)).
The cubera snapper Lutjanus cyanopterus is the species reaching the Regionally known as “caranha”, L. cyanopterus is an important
largest sizes among species of the Lutjanid family, in the Western Atlantic. resource for artisanal reef fisheries in Northeastern Brazil, where the
It is a gonochoric species and presents little sexual dimorphism (Grimes, state of Bahia is responsible for around 90 % of the specific regional
1987; Thresher, 1984). It is distributed from Northern Florida (USA) to production. The most recent fisheries statistics published by the federal
the Santa Catarina state, Brazil (Allen, 1985; Osmar et al., 2008; Sanches agency IBAMA,1 available for the state of Bahia for the years of 1997

* Corresponding author at: Laboratory of Fisheries Biology, LABPESCA/DCBIO/UEFS - Km 3, BR 116, Av. Universitária, s/n. LABIO, Sala 26-27, UEFS, Novo
Horizonte, 44031460, Feira de Santana, BA, Brazil.
E-mail address: [email protected] (P.N. Malafaia).
1
Brazilian Institute of the Environment and Renewable Natural Resources from the Ministry of the Environment (Instituto Brasileiro de Meio Ambiente e dos Recursos
Naturais Renováveis do Ministério do Meio Ambiente – IBAMA/MMA).

https://doi.org/10.1016/j.fishres.2021.106037
Received 7 July 2020; Received in revised form 19 May 2021; Accepted 1 June 2021
Available online 22 June 2021
0165-7836/© 2021 Elsevier B.V. All rights reserved.
P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

and 2007, shows to the cubera snapper a 60 % reduction in total landed discovery was part of the Pró-Arribada Project (FUNBIO/IBAMA n◦
catches over one decade, going from 738 annual tons in 1997 to 310 02001.003030/2001-82), as reported in Ferreira et al. (2018).
tons reported in 2007 (Cepene, 1998; IBAMA (Instituto Brasileiro do The present study aims to (1) describe patterns of spatial and tem­
Meio Ambiente e dos Recursos Naturais Renováveis), 2009). Unfortu­ poral distribution, and the biological characteristics of L. cyanopterus’
nately, the institutional instability of the fisheries sector administration catches from line fisheries targeting the specific aggregations in the two
in Brazil resulted in the interruption of landing control systems since Caranheiros sites; and (2) validate the reproductive character of these
2008, as well as the collection and disclosure of national fisheries sta­ aggregations through macroscopic evaluation of sexual maturity phases
tistics. Recent data on reconstructed annual marine landings statistics of the fishes caught.
in Brazil (Freire et al., 2015) enable us to project annual average landed
catches around 125 tons, between 2010 and 2015 for the state of Bahia. 2. Materials and methods
It is worth considering that the taxonomic category “caranha” in the 2.1. Study area
national statistics may include a small proportion (<10 %) of other The study area is located in the South West Atlantic, in a region
lutjanids such as L. alexandrei and, occasionally, L. analis and L. jocu. On inserted in the East Continental Shelf Large Marine Ecisystem (LME16)
the other hand, L. cyanopterus may also represent a small fraction of (Ekau and Knoppers, 2003), off Bahia state, Northeastern Brazil. This
records of other multi-specific commercial categories of lutjanids (such region is characterized by a humid tropical climate with high temper­
as “vermelho”, “cioba” and “dentão”) (Freire, 2009; MMA (Ministério do atures and an irregular scanty precipitation regime, where northeast
Meio Ambiente), 2006; Martins et al., 2006; Olavo et al., 2018). trade winds predominate. Additionally, water masses are oligotrophic,
At the international level, the species is classified as Vulnerable influenced by the Atlantic Tropical Water (ATW), with thermohaline
(VU) on the world threatened species list (Lindeman et al., 2016). In characteristics of temperatures higher than 18 ◦ C (maximum 28.1 ◦ C)
Brazil, Lutjanus cyanopterus was included in the same category through and salinity above 36 (maximum 37.8), transported by the Brazil Cur­
the Ministry of the Environment’s Ordinance nº 445 of December 17, rent in the surface layer, up to 200 m deep. The South Atlantic Central
2014 (MMA (Ministério do Meio Ambiente), 2014). In Bahia state, Water (SACW) occurs below the 200 m depth, with distinct thermoha­
L. cyanopterus was also classified as a vulnerable species in the state’s line characteristics, temperatures between 13.6 and 14.3 ◦ C, and salinity
red list, published by the Bahia’s Secretariat of the Environment values ranging between 34.4 and 35.3 (Valentin et al., 2007; Rossi-­
Ordinance nº 37 of August 15, 2017 (Sema (Secretaria do Meio Ambi­ Wongtschowski et al., 2006).
ente do Estado da Bahia, 2017). The continental shelf in the area is shallow, with a shelf-break
Studies carried out over the last two decades showed that the cubera located between 45 and 60 m deep. Shelf width varies considerably,
snapper performs seasonal migrations, forming large reproductive ag­ narrowing to as little as 8 km north of Itapuã, in the Metropolitan Region
gregations (Boomhower et al., 2010; Heyman et al., 2005; Kadison et al., of Salvador city - RMS, and widening towards the south, reaching up to
2006). These aggregations are classified as transient (Domeier and 25 km to the east of Camamu Bay (Dominguez et al., 2013).
Colin, 1997), since they occur during short periods of the year and are The two reproductive aggregation sites studied, named “Car­
concentrated at specific locations, sometimes far from their home range. anheiros”, are in the shelf-edge zone (Olavo et al., 2011), between the
A reproductive aggregation is defined as a temporary phenomenon outer shelf and the beginning of the upper continental slope, one located
in which individuals of a given species concentrate in a certain area for at north limit of the RMS, and the other in Southern Bahia state, between
reproductive purposes (Domeier and Colin, 1997). This phenomenon latitudes 12 ◦ S and 15 ◦ S (Fig. 1).
is of biological importance for the replenishment of reef fish pop­ Considering these sites are highly vulnerable and have high local
ulations, as well as of socioeconomical importance, for subsistence, socioeconomical importance, especially to traditional fishers, the exact
commercial and recreational fisheries, and observation tourism ac­ location of the analyzed “Caranheiros” is not revealed in this publication.
tivities (Sadovy et al., 2012). However, it has been made available to the government agencies
The interaction between aggregations and both large- and small- responsible for fisheries control and surveillance, as well as for imple­
scale fisheries, or with other sources of anthropogenic impacts menting management and conservation measures for the sustainable use
(offshore industrial activities, marine pollution, port activity, aggres­ of fisheries resources.
sive tourism and recreational fisheries, for example), tend to reduce
the replenishment capacity and genetic diversity of aggregating spe­
cies populations (Chapman et al., 1999). Indeed, this contributes to 2.2. Data sources
the extirpation of reproductive aggregations (Colin et al., 2003; 2.2.1. Fishing landings data
Sadovy, 1994; Sadovy et al., 2012), to the decline of fish stocks, and The best available secondary data on the fisheries targeting L. cya­
the extinction of local populations (Hamilton et al., 2012; Sadovy nopterus aggregations came from the participatory monitoring of fishing
et al., 2012; Sala et al., 2001). landings project carried out by PETROBRAS in 12 fishing communities
The Science and Conservation of Fish Aggregations (SCRFA)’s at southern Bahia state, as a specific condition of environmental license
manual (Colin et al., 2003) recognizes three direct signs to verify the from government agencies, for oil and gas exploration in the Camamu-
occurrence of a reproductive aggregation: a) in situ spawning observa­ Almada sedimentary basin. In the present study, we analyzed data on
tions; b) females with hydrated eggs and c) presence of post-ovulatory handline fisheries performed at Caranheiro-1, with positive catch re­
follicles in the ovaries of aggregating females. If gonad materials can cords for L. cyanopterus in four of the main handline fleet ports in
be obtained then either macroscopic or microscopic techniques may be southern Bahia region (fishing communities of Valença, Camamu, Boi­
used as a tool to determine time of spawning (Colin et al., 2003). Indirect peba and Barra Grande). The data comprise landings between 2005 and
signs are also considered important indicators in the preliminary iden­ 2013, to a total of 102 fishing trips (Table 1).
tification of reproductive aggregations, for instance the analysis of In a complementary way, we collected primary data from handline
fisheries capture and effort data, the analysis of the gonadosomatic fisheries and sampled captured individuals for biological information,
index, and the observation of individuals with swollen abdomens. with the support of the Pro-Arribada project, a national interinstitu­
Between 2009 and 2010 we identified two L. cyanopterus aggrega­ tional research effort to investigate reef fish reproductive aggregations
tion sites, commonly known as “Caranheiros” by traditional fishers, in (Funbio/Ibama Process n◦ 02001.003030/2001-82). Sampling took
two sub-areas located at the shelf-break zone of Bahia state, North­ place between 2009 and 2014 in four of the main landing ports for the
eastern Brazil, in the East Brazil Shelf Large Marine Ecosystem (LME16) handline fleet in the study area. This was not limited to the Southern
(Ekau and Knoppers, 2003), between latitudes 12 ◦ S and 15 ◦ S. This Bahia region but also included the Metropolitan Region of Salvador
(RMS) further north, monitoring the artisanal handline fleet of Itapuã,

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P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

Fig. 1. Study area indicating the two sub-areas investigated (Metropolitan Region of Salvador – RMS and Southern Bahia) and the approximate location of ag­
gregation sites of Lutjanus cyanopterus, regionally known as “Caranheiros”, identified at the shelf-break of Bahia state by the Pro-Arribada Project.

an important regional fishing community. Another fishery targeting Table 1

aggregations of L. cyanopterus was identified there, in 2010, at the site Number of fishing landings with positive catch records for L. cyanopterus ob­
Caranheiro-2 (Fig. 1). tained from handline fisheries targeted to aggregations of the species at
Because of the intrinsic dynamics of handline fisheries in each sub- Caranheiro-1, monitored at the main landing ports of Southern Bahia state,
area, we adapted distinct monitoring and biological sampling strategies. between 2005 and 2013.
At Southern Bahia, data were collected by local field agents trained by the Landing Camamu Barra Boipeba Valença Total fishing trips
Pro-Arribada project, between 2009 and 2010. From 2011 to 2012, data ports Grande with catches of
L. cyanopterus (N)
were collected through an on-board participatory monitoring program
(Malafaia et al., 2014) implemented by the Federal Pact project2 in 2005 – 1 2 2 5
2006 6 2 1 7 16
2007 1 1 – 2 4
2008 2 3 – 2 7
2009 10 4 – 9 23
2
The Federal Pact Program was a partner of the Pro-Arribada Project through 2010 13 5 – 5 23
the articulation of the Ethnodevelopment Center of the Agriculture Develop­ 2011 3 4 – 5 12
ment Company of Bahia (EBDA) through the subproject Ethnodevelopment for 2012 2 – – 3 5
Indigenous Peoples and Communities, Quilombolas and Artisanal Fishers in Citi­ 2013 4 1 – 2 7
zenship Territories of Bahia State, developed under the project Sustainable Terri­ Total 41 21 3 37 102
torial Development and Multifunctionality of Family Agriculture in Citizenship
Territories of Bahia.

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P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

collaboration between the Pro-Arribada project and the Agriculture density, and was analyzed separately for each aggregation site. Individ­
Development Company of Bahia (EBDA). It involved fishing shipmasters ual CPUE were calculated according to the following equation:
and fishermen crew of two handline fishing boats from the ports of
CPUE = Ct,s / (Ft,s*Dd,s).
Valença and Camamu. For 2013 and 2014, the on-board participatory
monitoring was continued through the collaboration between researchers Where: Ct,s = total capture (kg) of Lutjanus cyanopterus on the fishing trip
from the Pro-Arribada project and volunteers fishers involved in this (t), at a fishing site (s); Ft,s = number of fishers on the trip (t), at the
research. For the RMS, the technical team of the Pro-Arribada project fishing site (s); Dd,s = time of trip duration in days of effective fishing (d),
sampled the landings of the handline fleet monitored in Itapuã, from at the fishing site (s).
February 2010 to May 2014 (Table 2). We performed an exploratory analysis to observe the monthly vari­
Primary and secondary data collected from fisheries were obtained at ation of the CPUE distribution per trip. We analyzed the mean CPUE for
fish landing sites via monitoring of the handline fleet using standard Caranheiros 1 and 2 to identify monthly or seasonal temporal patterns in
forms. Information included the dates of departure and arrival of each species occurrence. To test for differences between monthly CPUE me­
vessel sampled, fishing location, number of fishers on board, charac­ dians of the cubera snapper in each site, we used the non-parametric
teristics of the fishing equipment used (types of lines and hooks), and Kruskal-Wallis test, since not all samples were normally distributed.
supplies (gas, ice, baits). We collected these data through interviews Sex ratios were verified for the entire sample and by month, for each
with each vessel’s shipmaster upon their return from fishing trips. Each site. We performed a chi-squared test to evaluate statistical significance
fishing trip was considered as a sampling unit (Cadima, 2003). of data according to the proportionality between the observed and ex­
In addition to the monitoring and biological sampling of the land­ pected distributions with a 0.05 % confidence. To describe the repro­
ings, semi-structured interviews and questionnaires were conducted ductive period, we analyzed monthly frequencies of occurrence of the
with 27 traditional fishermen specialized in handline fishing. They were sexual maturity stages described by Vazzoler (1996) for each sex, which
approached in their home communities, in the RMS and in Southern was adapted to the classification of maturity phases proposed by
Bahia, to improve information about the characteristics of both fisheries Brown-Peterson et al. (2011) in order to facilitate comparison with other
and fishing areas, as well as about the aggregation processes and sites studies (Table 3). For that, we included all samples collected across all
known as Caranheiros. years (2009–2014), for each aggregation site analyzed.
Updated information for subsequent years (2015–2020) were ob­
tained through semi-structured interviews with the main ’Caranheiros’
3. Results
fishing masters identified and involved in the past research, during the
The description of the occurrence period and evidences of the repro­
landings data collection and the monitoring of the handline fleet, and
ductive activity of L. cyanopterus aggregations, in both sites investigated
who continued targeting on the cubera snapper fisheries at both ag­
in the study area, will be presented in the following subsections.
gregation sites.

2.2.2. Biological sampling 3.1. Distribution of monthly CPUE at both spawning sites
During each landing monitored by the Pro-Arribada project in which Between 2005 and 2013, 334 fishing trips of the handline fleet
the cubera snapper (L. cyanopterus) was caught, we collected informa­ monitored at Southern Bahia recorded catches of the cubera snapper.
tion on biometry, sex, and conducted a macroscopic inspection of go­ Among these, 30.5 % (n = 102) of landings came from Caranheiro-1.
nads to determine the phase of sexual maturity, according to the During the monitored period, total L. cyanopterus catch from this ag­
maturity stage description of Vazzoler (1996), adapted to the phase gregation site reached 29,033.5 kg, which representing 76.9 % of the
classification proposed by Brown-Peterson et al. (2011), in order to total removed biomass recorded for all the fishing trips monitored with
facilitate comparison with other studies. We obtained total length (TL, positive catches for the species (37,754.8 kg; n = 334 trips).
cm) by measuring specimens from the tip of the snout to the tip of the Cubera snapper catches at Caranheiro-1 were concentrated between
caudal fin. Taxonomic identification was performed based on Cervigón December and April (97 landings, representing 95.1 % of total landings
et al. (1992). Whenever possible, specimens and gonads at different with positive catch records for the species), with discrepant and sporadic
maturity phases were photographed for record. records in May of 2010 (n = 1 landing), June and October of 2006 (n = 1
for both months) and September of 2005 (n = 2). The highest mean
2.3. Data analyses CPUE were observed between January and March (Fig. 2).
The catch per unit effort (CPUE) was used as an indicator of aggre­ On the northern study area (RMS), 142 fishing trips of the handline
gation occurrence, assumed as a proxy of local relative abundance or fishery fleet monitored at Itapuã recorded catches of the cubera snapper
between 2010 and 2014. Among these, 61 % (n = 86) of landings came
Table 2
from captures at Caranheiro-2. The total sampled catch of L. cyanopterus
Number of fishing landings with positive catch records for L. cyanopterus ob­ during the monitored period for this aggregation site reached 4,505.7 kg,
tained from handline fisheries targeted to aggregations of the species at which represents 94.8 % of the total biomass captured in monitored trips
Caranheiro-1 e Caranheiro-2, monitored for biological by the Pro-Arribada with positive catch records for the species (4,749.9 kg; n = 142 trips).
Project, respectively in the Southern Bahia region and the Metropolitan Re­ Cubera snapper captures at Caranheiro-2 occurred between December
gion of Salvador (RMS). and May. The highest mean CPUE were observed in February, to the years
Region South Bahia (Caranheiro-1) RMS Total fishing of 2010 and 2011. In 2012, the highest mean CPUE was observed in
(Spawning (Caranheiro- trips with March, while in 2013 were observed in the months of February and April,
Site) 2) catches of and in 2014 it corresponded to the months of January and March (Fig. 3).
Landing Camamu Barra Valença Itapuã L. cyanopterus
For Caranheiro-1, the comparison of individual CPUE (per trip)
ports Grande (N)
obtained from the participatory monitoring data of PETROBRAS
2009 4 – 2 – 6 (2005–2013) shows significant differences between CPUE medians of
2010 10 3 4 11 28
2011 5 – 6 15 26
samples from December compared to those of January, February, and
2012 4 – 2 18 24 March. Furthermore, a similar pattern exists between median CPUE of
2013 – – – 14 14 April in relation to those of February (Table 4). Maximum CPUE values
2014 5 – 4 28 37 at Caranheiro-1 were observed for March/2008 (140 kg/fisher*day),
Total 28 3 18 86 135

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P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

Table 3 more frequent during the waning-to-new, new, and new-to-waxing

Macroscopic description of the five sexual maturity stages for females and males phases, especially in February, and March.
as established by Vazzoler (1996), used in the field work, adapted to maturity By looking at the distribution of monthly maximum CPUE by lunar
phases classification proposed by Brown-Peterson et al., 2011. phase at Caranheiro-2, we observed that they occurred more frequently
Sex Maturity phase Description during the new and waxing phases in January, February, March, and
Ovaries are filiform and translucent, with a April (Fig. 4).
considerably reduced size, and located close to the
A - Immature dorsal wall. They occupy less than 1/3 of the
3.2. Size distribution
coelomic cavity, with no signs of vascularization.
Oocytes not visible to the naked eye.
Ovaries occupy from 1/3 to 2/3 of the coelomic Total lengths (TL, cm) of the cubera snappers captured at Caranheiro-
B – Developing cavity; intense capillary network; small and medium 1 (n = 1135 individuals) varied between 40 and 150 cm in the period
opaque granules (oocytes) visible to the naked eye. between 2009 and 2012, and in 2014. No biometry was performed in
Ovaries occupy nearly the entire coelomic cavity;
oocytes are visible to the naked eye, turgid, and big,
2013. In the frequency distribution by size class, we observed higher
C – Spawning frequencies in the classes between 70 and 119 cm, with an average of 96
opaque and/or translucent; oviducts are filled with
Capable
Female oocytes. Translucent hydrated oocytes are present, cm and modes in classes 80–89 and 90− 99 cm (Fig. 5).
which indicate imminent spawning. Total lengths obtained for the cubera snappers captured at Caranheiro-
Ovaries present different stages of flaccidity, with a
2 (n = 287 individuals) varied between 58 cm and 131 cm, from 2010 to
distended membrane and bleeding aspect, once
D - Regressing again occupying 1/3 of the coelomic cavity; few 2014. The frequency distribution by size class showed that the highest
oocytes (under absorption) are observed, with the frequencies were recorded for individuals measuring between 80 and 109
aspect of whitish lumps. cm, with an average of 95 cm and mode in the class of 90− 99 cm (Fig. 5).
Ovaries are smaller and translucent, with weak Although Caranheiro-2 is located closer to the coastline (8 km), the
vascularization, occupying approximately 1/3 of the
E – Regenerating coelomic cavity, and are clearly bigger than
capture of L. cyanopterus at this site was limited to larger individuals
immature ones (A); no oocytes are visible to the when compared to the size range of individuals captured at Caranheiro-
naked eye. 1, located almost 25 km from the coast.
Testicles are reduced, filiform, translucent, and with
A - Immature
a similar position to that of ovaries.
Testicles are developed, with a lobulated shape; the 3.3. Sex ratio by month
B – Developing membrane ruptures easily under pressure, releasing
a milky and viscous sperm. Monthly sex ratio of the cubera snappers captured at Caranheiro-1,
Testicles are turgid and whitish, occupying a large
Male between 2009 and 2014, showed a predominance of females in
C - Spawning part of the coelomic cavity; the membrane ruptures
Capable easily under weak pressure, releasing a less viscous January, February, and April. However, no significant difference was
sperm than in the previous phase. found (χ2 < 3.840) between these months. As for specimens captured
D – Regressing
Testicles are flaccid, with a bleeding aspect; at Caranheiro-2, between 2010 and 2014, males predominated across
membrane does not rupture under pressure.
all sampled months, with significant differences being found in all of
E – Regenerating Testes are smaller, filiform, and translucent.
them (χ2 > 3.840).

3.4. Patterns of maturation phases

February/2009 (57.4 kg/fisher*day), March/2011 (48.39 kg/fisher*­
day), February/2012 (45.9 kg/fisher*day) and February/2013 (56.8 3.4.1. Distribution of maturation phases per month
kg/fisher*day). For Caranheiro-1, the highest numbers of specimens from both sexes
However, no significant difference between medians was found for (N = 104) with regressing gonads (D) were recorded in February and
Caranheiro-2 between samples from December and April (2010–2014) March. Immature (A) and/or regenerating (E) individuals of both sexes
(Table 5). At Caranheiro-2, maximum CPUE values were obtained for occurred in a lower frequency throughout all months analyzed. We
January (82,7 kg/fisher*day) and April (39.9 kg/fisher*day) of 2014; emphasize that due to difficulties in macroscopically distinguishing
February/2011 (40 kg/fisher*day) and March/2012 (54.3 kg/fisher*day). between phases A and E, we grouped them for analyses (Fig. 6).
When observing the distribution of monthly maximum CPUE by At Caranheiro-2, the highest number of specimens with developing
moon phase at Caranheiro-1, we noticed that maximum values were gonads (B) was recorded in February for females and April for males.

Fig. 2. Monthly distribution of the arithmetic mean and standard deviation CPUE of the cubera snapper (kg/fisher*day), from fishing trips (n = 102) of the handline
fishery targeting to aggregations at Caranheiro-1, in Southern Bahia, between 2005 and 2013.

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P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

Fig. 3. Monthly distribution of the arithmetic mean and standard deviation CPUE of the cubera snapper (kg/fisher*day), from fishing trips (n = 86) of the handline
fishery targeting to aggregations at Caranheiro-2, in RMS (Itapuã fleet), between 2010 and 2014.

Table 4
Comparison of p-values obtained through the non-parametric Kruskal-Wallis test, comparing monthly median CPUE of the cubera snapper L. cyanopterus (kg/fish­
er*day), from each fishing trip (n = 102) of Southern Bahia’s handline fleet at Caranheiro-1, between 2005 and 2013. Highlighted values in red and bold asterisks
represents significant differences.

Table 5
Comparison of p-values obtained through the non-parametric Kruskal-Wallis test, performed to compare monthly median CPUE of the cubera snapper L. cyanopterus
(kg/fisher*day) from each fishing trip (n = 86) of RMS’s handline fleet at Caranheiro-2, between 2010 and 2014.
January February March April December

January 0.8829 0.9733 0.7934 0.7728

February 0.8829 0.06507 0.1095 0.1535
March 0.9733 0.06507 0.9436 0.07385
April 0.7934 0.1095 0.9436 0.1136
December 0.7728 0.1535 0.07385 0.1136

Fig. 4. Distribution of the cubera snapper CPUE (kg/fisher*day) by moon phase and month, from 188 fishing trips of the handline fishery targeting to aggregations at
the two sites (Caranheiros) in the study area, between 2005 and 2014: (a) Caranheiro-1 (Southern Bahia), n = 102 fishing trips (2005-2013); (b) Caranheiro-2, RMS,
n = 86 fishing trips (2010-2014). F = full moon; FW = full/waning moon; W = waning moon; WN = waning/new moon; N = new moon; NC = new/waxing moon; C
= waxing moon.

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P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

March yielded the highest number of specimens of both sexes with

regressing gonads (D). Immature (A) and/or regenerating (E) females
occurred in a lower frequency in February and males were in April
(Fig. 6). It is important to highlight that these were grouped for analyses
due to the difficulties in macroscopically distinguishing between in­
dividuals of the A and E phases.
At Caranheiro-1, when looking at the distribution of maturity phases
of males and females by moon phase, we observed the capture of spec­
imens of both sexes with developing (B), spawning capable (C) and
regressing (D) gonads was more representative during the new moon,
especially of those in phase D. Immature (A) and/or regenerating (E)
individuals were captured in all moon phases, except for waxing moon
phase. And at Caranheiro-2, we observed a higher capture of specimens
of both sexes with developing (B), spawning capable (C) and regressing
(D) gonads during the new and waxing moon phases (Fig. 7).
It should be noted that a total of 128 gonads at Caranheiro-1, and
twenty-one gonads at Caranheiro-2, were excluded from maturity phase
analyses (monthly and lunar), since no specific information regarding
maturity phase was available, aside from the specimen’s gonads not
being at neither A/E phases.
Fig. 8 shows a gonad of a Lutjanus cyanopterus specimen at the (C)
spawning capable phase. This specimen was captured in February 21th,
2010, at Caranheiro-2 during waxing moon. The shipmaster and fishers
interviewed at the day of landing (Feb 22th, 2010) reported feeling a
strong fish smell while fishing, which he referred to as “fish air”.

3.5. Local ecological knowledge

The fishers interviewed in 2021, one from the RMS and the other
two from Southern Bahia, reported that the high catchability of the
cubera snapper continued between December and April at Caranheiro-
1, and between December and May at Caranheiro-2. As a side note, the
fishing master from the RMS stated that his last better cubera snapper
catch reached approximately 1 ton, during a fishery realized between
February 23rd and 25th, 2020, in the new moon phase (Fig. 9). All
fishers interviewed informed us that most specimens captured between
2015 and 2020 presented gonads in the B, C, and D phases, including
females and males.

Fig. 5. Total length (TL, cm) distribution of the sampled cubera snappers 4. Discussion
captured at the two aggregation sites (Caranheiros), between 2009 and 2014:
(a) Caranheiro-1 (Southern Bahia), n = 1135 fishes (2009-2012 and 2014). (b) 4.1. Seasonality and monthly catches
Caranheiro-2 (RMS), n = 287 fishes (2010-2014).
The monthly distribution of cubera snapper (L. cyanopterus) catches
from the handline fisheries taking place at the study area showed a well-

Fig. 6. Distribution of maturity phases of L. cyanopterus, by month, for males and females captured at the two aggregation sites (Caranheiros): (a) Caranheiro-1 (n =
222), males (80) and females (142), between 2009-2012 and 2014. (b)Caranheiro-2 (n = 121), males (78) and females (43), between 2010-2014. A = immature; B =
developing; C = spawning capable; D = regressing; E = regenerating.

7
P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

Fig. 8. Hydrated pre-ovulatory gonads of a female Lutjanus cyanopterus spec­

imen captured by the handline fishery targeting to aggregations at Caranheiro-
2, in February 2010, RMS – Bahia, Brazil. Biological data of the specimen: total
length = 105 cm, whole weight = 16,2 kg, gonad weight = 0,870 kg. Spawning
capable phase, and actively spawning subphase, as defined by Brown-Peterson
et al. (2011).

Fig. 7. Distribution of maturity phases of L. cyanopterus, by moon phase, for

males and females captured at the two aggregation sites (Caranheiros): (a)
Caranheiro-1 (n = 222), males (80) and females (142), between 2009-2012 and
2014. (b) Caranheiro-2 (n = 121), males (78) and females (43), between 2010-
2014. A = immature; B = developing; C = spawning capable; D = regressing; E
= regenerating.

defined annual seasonality at both aggregation sites (Caranheiros). In­ Fig. 9. L. cyanopterus captured at Caranheiro-2 between February 22nd and
dividuals were captured annually, during part of the dry season until the 25th, 2020 (new moon) by handline fishers of the Metropolitan Area of Sal­
beginning of the wet season, between December and May, in agreement vador (RMS).
with results of studies carried out in Central America (Biggs and Nemeth,
2016; Claro and Lindeman, 2003; Domeier and Colin, 1997; García-Ca­ reproductive aggregations of the species. Indeed, authors point to a
gide et al., 1994; Heyman et al., 2001, 2005; Heyman and Kjerfve, 2008; relationship between months of highest relative abundance and highest
Kadison et al., 2006; Naranjo, 1956; Sadovy and Colin, 2012). However, water temperatures, ranging between 26.2–30.0 ◦ C in Belize and
reproductive aggregations of L. cyanopterus in Central America occurred 26.9–28.2 ◦ C in the U.S. Virgin Islands. Results presented here also agree
between March and September, which corresponds to the spring-summer with this relationship, since the aggregations found in the Caranheiros of
in the Northern Hemisphere. In Brazil, aggregations were recorded solely Bahia state develop in months of highest accumulated surface seawater
between the Southern Hemisphere’s summer and fall seasons. temperature at the end of summer.
Studies on L. cyanopterus in Belize (Heyman et al., 2005) and the U.S. Months with highest CPUE varied between aggregation sites, which
Virgin Islands (Kadison et al., 2006) suggest that water temperature is could be the result of a latitudinal seasonality effect between both areas,
one of the most relevant environmental factors to the occurrence of separated by approximately one degree of latitude. Studies by Sadovy

8
P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

and Eklund (1999) in Central America also found a latitudinal season­ Heyman et al. (2005) and Kadison et al. (2006), who observed length
ality in reproduction sites of Epinephelus striatus. However, Claro and ranges between 40− 130 cm during L. cyanopterus aggregations in the
Lindeman (2003) found no latitudinal differences for spawning sites of Caribbean, with an average of 80 cm.
L. cyanopterus, even between sites separated by up to four degrees of Differences in sex ratios (male:female) were found between
latitude (19–22 ◦ N) in the Gulf of Mexico and the Caribbean Sea. Sadovy Caranheiro-1 (0.8:1) and Caranheiro-2 (2.3:1). The highest occurrence
and Colin (2012) suggest that the reason the spawning period of a of females in the former could be related to a sampling error during
species with broad latitudinal distribution varies with latitude, could be participatory monitoring, in which fishers directed data collection and
linked to changes in water temperature. gonad inspection towards females and males being initially dismissed
According to NOAA Coral Reef Watch (2020), monthly average from the research. For the Caranheiro-2 site, where this type of sam­
temperatures of the ocean surface at the Caranheiro-1’s location varied pling issue was not recorded, the occurrence of males was higher than
from 27.0 ◦ C to 28.5 ◦ C, between December and April, in the period that of females. Similar results (higher proportion of males) were re­
from 2005 to 2014. For the Caranheiro-2 sub-area, sea surface tem­ ported by Viana et al. (2015) for Lutjanus synagris (1.1:1) and by Cor­
peratures ranged from 26.5 ◦ C to 28.3 ◦ C, between the months of rea-Herrera and Jiménez-Segura (2013) for Lutjanus guttatus (1.5:1).
December and May, in the period from 2010 to 2014. Highest monthly Luckhurst et al. (2000) suggested that this difference is related to a
average temperatures for Caranheiro-1 were recorded between behavioral interaction with the fishing device, as larger males are more
February and April (2005–2013), and for Caranheiro-2 between March aggressive than females when competing for the bait, showing highest
and April (2010–2014). Therefore, these results confirms the transient recurrence in the fish landings sampled. Another point worth consid­
character of the aggregation formed by L. cyanopterus at the two sites ering is that female gonads tend to be more dilated during the repro­
investigated. According to Domeier and Colin (1997), transient ag­ ductive period (Brown-Peterson et al., 2011), when the abdominal
gregations occur seasonally within a particular temperature regime, cavity can be largely filled by gonads, thus compressing the digestive
generally in places with an annual variation of a few degrees. system and reducing both, the efficiency of bait attraction and handline
catchability.
4.2. Lunar periodicyty and hand-line fisheries targeting spawning
4.4. Validation of the reproductive nature of aggregations at both
aggregations
Caranheiros
Highest CPUE at Caranheiro-1 were concentrated between the
waning-to-waxing moon phases, including the new moon. As for
The predominance of spawning capable, pre-spawning and regressing
Caranheiro-2, catches were recorded only during the new and waxing
male and female individuals at Caranheiro-1 (56.7%) and Caranheiro-2
moon phases, agreeing with results by Kadison et al. (2006) at the
(58.7%) confirms the reproductive activity of Lutjanus cyanopterus in
Grammanik Bank (Virgin Islands), who identified larger L. cyanopterus
these two aggregation sites.. According to Colin et al. (2003), one of the
reproductive aggregations 10 days after the full moon and, to a lesser
essential criteria to identify a reproductive aggregation is spawning
extent, four days after the new moon. Nevertheless, studies by Biggs and
verification.
Nemeth (2016) and Heyman et al. (2005) identified the largest con­
Indeed, a higher frequency of individuals with phase D gonads
centrations of cubera snapper aggregations during waxing -to-waning
(regressing) was observed during the study period for both sites. More
moon phases, including the full moon. Additionally, Boomhower et al.
specifically, these patterns occurred in February and March at
(2010) and Paris et al. (2005) reported L. cyanopterus aggregations and
Caranheiro-1, and March at Caranheiro-2 throughout the years. One of
spawning during the full moon.
the ways to evaluate the reproductive period of a species is to verify the
One way to explain the observed lunar periodicity differences, is that
frequency of sampled individuals by maturity phase throughout the year
peak spawning does not necessarily coincide with peak of fish catch­
(Brown-Peterson et al., 2011). Besides, according to Domeier and Colin
ability. Kadison et al. (2006); Biggs and Nemeth (2016) and Heyman
(1997), one of the aspects which classifies an aggregation as transient is
et al. (2005) used fisheries independent data from visual observations or
the occurrence of a short reproductive season, at specific spawning sites.
telemetry to illustrate peak abundance and peak spawning. Our study
Therefore, the present study corroborates the available information on
was based on fisheries dependent data. For the data analyzed here, it is
the transient character of Lutjanus cyanopterus spawning aggregations, as
possible that the lack of catch records for the species during full moon is
described for both sites in the study area, which presented recurring
related to the strategy of handline fishery. Indeed, traditional fishers
aggregations during a few months throughout the years.
report that the hook and line are exposed to higher luminosity in the
water during the full moon, thus triggering a negative reaction (avoid­
4.5. Management and conservation
ance) by more reactive fishes, reducing the efficiency of this fishing
technique.
It is worth mentioning that the two cubera snapper spawning ag­
Another hypothesis is the possibility of reduced bait attraction effi­
gregation sites identified in this study are included in an Ecologicaly and
ciency due to the enlargement of mature and turgid (hydrated) gonads in
Biologicaly Significant Area (EBSA), classified by the Convention on
females in a pre-spawning condition (Brown-Peterson et al., 2011). This
Biological Diversity in 2014, named Northeastern Brazil Shelf-Edge
may compress their digestive systems by repletion of the body cavity,
Zone (Olavo et al., 2011), belonging to the Wider Caribbean and
thus reducing cubera snapper catches. This would explain the highest
Western Mid-Atlantic EBSA Region (Secretariat of the Convention on
frequency of occurrence and highest catch rates observed for females in
Biological Diversity, 2014).
the post-spawning maturity phase (D) with regressing gonads, which
There is an international concern regarding the protection of
were more frequent during waning, new, and waxing moon phases, as
reproductive aggregations for the maintenance of L. cyanopterus pop­
presented in the results section of this paper. Regressing gonads would
ulations (Colin et al., 2003). Characterizing the spatial-temporal dy­
enable a higher food ingestion and a more effective bait attraction and
namics and validating aggregations at the spawning sites identified in
higher catchability.
the study area may contribute to the development of recovery plans and
other management and conservation measures for this important fishery
4.3. Populational aspects resource, currently included on the IUCN red list of threatened species.
The cubera snapper population investigated at Caranheiro-1 Additionally, it may support the implementation of management mea­
showed a broader total length range (40− 150 cm) when compared to sures based on control of fishing effort and temporary or permanent
Caranheiro-2 (58− 131 cm). However, total length averages for both restriction of specific fishing gears, seasons, and areas. Finally, it can
sites were equal (95 cm). Similar patterns were found in studies by also subsidize regional and national efforts for marine space planning,

9
P.N. Malafaia et al. Fisheries Research 242 (2021) 106037

enable the ecological-economic zonation and the implementation of These evidences also confirm a transient spawning pattern, as
mitigating measures of socio-economic and environmental impacts observed for the cubera snapper in other areas of the Atlantic, such as in
resulting from offshore maritime developments. the Caribbean Sea. This information may contribute to the management of
Measures for fisheries resource recovery plans and protection of the fisheries in the ecosystem context of this study area, and to the develop­
species are recent and still not effective. These are related to the pub­ ment of local recovery plans for the species, subsidizing the revision and
lication of the national red list of threatened species by the Brazilian necessary adjustments foreseen for the national plan established by the
Ministry for the Environment’s Ordinance nº 445/2014 MMA, 2014, Interministerial Ordinance nº 59 - C, of November 9, 2018.
specific actions of the National Action Plan on Coraline Environments -
PAN Corais, under the coordination of the Chico Mendes Institute for Author’s contributions
Biodiversity Conservation - ICMBio (2016) and of the Interministerial
Ordinance nº 59 - C, of November 9, 2018 (MMA, 2018), which estab­ Priscilla Malafaia: Methodology, primary data collection, survey and
lished the Recovery Plan for Reef Fishes, including L. cyanopterus along systematization of secondary data; Adaptation of sampling strategies on-
with three grouper species (Mycteroperca bonaci, M. interstitialis, and board and at fishing landings; Data curation; Formal analysis; Writing -
Epinephelus morio). original draft, Writing - review & editing.
The continuous monitoring of fisheries targeted to spawning aggrega­ George Olavo: Conceptualization and project coordination;
tions, aiming to trigger management responses and an adaptive fisheries Methodology, survey and systematization of secondary data; Sam­
management must be a priority. This requires an active participation of pling design and adaptation of strategies on-board and at fishing
traditional fishers, especially artisanal handline fishers, who have a deep landings; Writing - review & editing; Project administration.
local knowledge on aggregation dynamics and the environmental char­ Aline Franca: Methodology, collaboration on primary data collec­
acteristics of aggregation sites, not only of the cubera snapper but of tion; Adaptation of sampling strategies on-board and at fishing landings;
several other reef fish species that form reproductive aggregations and are Data curation; Writing - review & editing.
of ecological and economical importance (Olavo et al., 2005; França and
Olavo, 2015; Ferreira et al., 2018; França et al., 2021; Bezerra et al., 2021). Declaration of Competing Interest
However, we noticed based on our fisheries monitoring and in­
terviews with fisher and fishing shipmasters that the targeting of hand­ The authors report no declarations of interest.
line fisheries towards cubera snapper spawning aggregation sites is
declining in both investigated Caranheiros. The explanation for this
Acknowledgments
decline is the reduction of number of fishers who know how to perform
this fishery and the low price in first commercialization of the cubera
The authors are thankful to the artisanal fishers and field agents for
snapper (R$6 to R$10 Brazilian reais per kilo). Additionally, many fishers
the invaluable understanding and collaboration during the research
end up directing their captures towards pelagic resources, especially the
process . To Dr. Beatrice Padovani Ferreira and Dr. Simone Marques for
mackerel (Scomberomorus spp.), which, according to them, are easier to
the enthusiasm and collaboration during the Pro-Arribada Project. To
catch and result in better economic return (R$14 to R$18 per kilo) when
PETROBRAS for the provision of secondary information and access to
compared to the cubera snapper (L. cyanopterus).
fisheries monitoring reports for Southern Bahia area. To the Agriculture
Since cubera snapper spawning aggregation sites are highly vulner­
Development Company of Bahia (EBDA) and the Foundation for Research
able and of socioeconomic relevance, especially to artisanal handline
Support in the State of Bahia (FAPESB) for the financial support. To the
fisheries, the exact location of the analyzed “Caranheiros” is not
Pro-Arribada Project (FUNBIO/IBAMA Process nº 02001.003030 / 2001-
revealed in this study. Nevertheless, it has been made available to the
82) for funding data collection. PNM thanks the Coordination for the
government agencies responsible for implementing management and
Improvement of Higher Education Personnel (CAPES) for granting a
conservation measures for the sustainable use of fisheries resources.
master’s degree scholarship. The authors also thank the two anonymous
These reproductive aggregations are actually threatened by the expan­
reviewers and the editor-in-chief for suggestions and criticisms that
sion of highly mobile fleets from other brazilian regions and states, that
brought important contributions to improve the original manuscript.
operate with high impacting gears and greater fishing power. Consid­
ering the current moment of institutional fragility and dismantling of the
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