Habitat use and abundance of goliath grouper Epinephelus itajara in Brazil: a participative survey

Developing survey strategies for threatened species is often limited by access to sufficient individuals to acquire information needed to design appropriate conservation measures. The goliath grouper (Epinephelus itajara) is a large reef fish, globally classified as critically endangered. In Brazil, fishing has been prohibited since 2002. Herein we investigated habitat use and abundance of E. itajara in Brazil drawn from a participative survey, which engaged volunteer divers in data-collection. A total of 188 reports were recorded between 2005 to 2011 throughout 13 Brazilian states. Our results revealed that habitat type influenced the relationship between total length and depth of occurrence of E. itajara. We observed a significant difference between habitats, artificial presented a nonlinear and natural an asymptotic relationship. This study underscores the importance of developing conservation measures addressing specific habitats and locations to enhance population recovery. Artificial structures (shipwrecks and manmade reefs) are critical habitats that must be considered as highly sensitive areas to E. itajara strategic conservation policies. We suggest the creation and implementation of marine protected areas, as key strategies for E. itajara conservation, especially for artificial habitats and aggregation sites.


Introduction
Surveying rare and threatened species is often limited by access to sufficient individual records, challenging the build-up of comprehensive data sets needed to design appropriate conservation measures (Thompson, 2004;Wiley & Simpfendorfer, 2010). This is particularly the case for species that live in marine habitats where they can be difficult to locate and capture (Carlson et al., 2013). One approach to overcoming these challenges is the engagement of volunteers to collect data (Foster-Smith & Evans, 2003;Holt et al., 2013).
Participative ichthyologic research using volunteer diver databases has been widely applied over the past two decades (e.g., Darwal & Dulvy, 1996;Auster et al., 2005;Stallings, 2009;Ruttenberg et al., 2012). Recreational divers represent a potentially large community of skilled and often highly motivated volunteers (Hussey et al., 2013). This approach has proven to be valuable in structuring consistent largescale geographic databases encompassing marine system properties such as diversity and dynamics at multiple scales (Goffredo et al., 2010;Holt et al., 2013). However, the use of volunteers is often contested on the grounds that the information collected will be unreliable as a result of either insufficient training or lack of consistency derived from a large numbers of observers (Darwal & Dulvy, 1996). By engaging with and accepting the limitations of recreational divers' observational data -i.e., size over estimation, replicate counting of individuals and divers disturbance on mobile animals (Hussey et al., 2013) -this approach has provided a number of publications about marine fishes, demonstrating the value of data collected by volunteer divers. Examples include a variety of studies on reef fish population abundance and distribution in the Caribbean and Italy (Goffredo et al., 2004;Ward-Paige et al., 2010); seasonality of the manta ray Manta birostris in southeast Brazil (Luiz et al., 2009); evidences of recovery in goliath grouper Epinephelus itajara population in Florida U.S. (Koenig et al., 2011;Frias-Torres, 2012).
This paper undertakes a participative approach in the study of habitat use, depth of occurrence and abundance of E. itajara (Litchtenstein, 1822) (Perciformes: Epinephelidae) in Brazil. The species is the largest grouper in the Atlantic Ocean (>2 m total length -TL, >400 kg) (Bullock et al., 1992). They are sedentary and have a high degree of site fidelity (Eklund & Schull, 2001;Pina-Amargós & Gonzáles-Sansón, 2009). Adults inhabit both natural and artificial reefs, generally in depths less than 50 m (Bullock et al., 1992).
Historically, E. itajara was distributed throughout coastal and estuarine areas of the tropical and subtropical Atlantic (Heemstra & Randall, 1993). However, historical records of drastic reductions in abundance have been observed throughout its range (Sadovy & Eklund, 1999;Gerhadinger et al., 2006;McClenachan, 2009). Although there is reduced survey effort in the East Atlantic, it is suggested to have become extinct in Africa by Craig et al. (2009). Decreasing depth (15 -29 m), deep (≥ 30 m). For classification purposes, we considered herein an aggregation as the occurrence of more than five individuals at the same location. Goliath grouper TL between natural and artificial habitats was modeled as a function of the explanatory variable depth using generalized additive models (GAMs), performed with gam function from the mgcv package (Wood, 2006) in software R (R Core Development Team, 2013). GAMs are semi parametric models where the dependent variable is linked to an additive predictor through a nonlinear link function (Dalla Rosa et al., 2012). To evaluate changes in abundance between habitats, differences among depth categories were tested using non-parametric ANOVA (Kruskal-Wallis test). Tests were performed at a significance level of p < 0.05.

Results
Between 2005 and 2011, 188 reports from 84 volunteers were collected with a total of 306 individuals of E. itajara observed at 77 different sites along 13 Brazilian states. Reports were provided by recreational (n = 142), scientific (n = 31) and commercial divers (n = 15). Because reports with the presence of E. itajara are sporadic, it was not possible to obtain information about sampling efforts. The highest numbers of reports, 56%, came from the Northeast Brazil, followed by South, 23% and Southeast, 21%. Fernando de Noronha and Abrolhos, both National Marine Parks (NMPs) in Northeast, sheltered the majority of sites, with 17% and 14% respectively (Fig. 1). Sixty-five percent (n = 199) of sighted goliath groupers were associated to artificial habitats. 'Parque dos Meros' artificial reefs represented 13% (n = 26) of the total number of fish observed at artificial habitats, Recife shipwrecks and Victory 8B accounted for the largest number of reports at shipwrecks, with 9% (n = 18) and 7% (n = 14), respectively (Fig. 1). The most frequently reported structures were concrete reefs and shipwrecks, representing 27% and 28%, respectively. Oil-gas structures accounted to 9%.
Epinephelus itajara were sighted mostly during summer (n = 138; 59%), mainly in artificial habitats, with 61% of observations in comparison with natural habitats. Fig. 2 shows the frequency of season accumulated between the sighting period analyzed in natural and artificial habitats. The maximum depth of species occurence was 38 m. Overall, goliath grouper were sighted 63% (n = 222) in shallow water (0 -14 m). Individuals sighted in artificial habitats were at an average depth of 21.5 m (±5.1 s.d.), while in natural reefs, 16.3 m (±9.6 s.d.) (Fig. 3). There is a significant asymptotic relationship between TL and depth at natural habitats (F = 22.24, p < 0.0001; Fig. 4a). On the other hand, a clear nonlinear and non-significant relationship was observed at artificial habitats (F = 1.58; p = 0.18; Fig. 4b). Large adults were deeper, at average depth of 22.3 m (±6.7 s.d.), while juveniles and subadults were observed at an average depth of 18 m (±7.48 s.d.) (Fig. 4c) with no significant differences.
Observed E. itajara ranged from 10 to 200 cm TL and the most commonly reported sizes were subadults (60%) and adults (28%), with large adults (10%) and juveniles (2%) less represented. The highest number of individuals in an aggregation over artificial habitats was 10 and mean TL for all artificial habitat aggregations was 115.7 cm (±37.3 s.d.). For natural habitats, subadult and adult were the most frequent size classes observed (46% and 42%, respectively) (Fig. 4d). Subadults represents 65% of sightings at artificial habitat. The highest number of aggregated individuals at natural habitats was 11, at Gajiru rocky reefs, State of Sergipe. On natural habitats, average TL of aggregations was 110.6 cm (±39.8 s.d.), with 67% represented by subadult and 20% adult.
In general, sightings of a single individual were the most common situation (n = 146; 77%), followed by two to five specimens (n = 35; 18%) and seven aggregations accounted for six to eleven individuals, six of the ten smallest individuals (juveniles) were reported from estuaries.
At the monobuoy (a floating platform anchored offshore where tankers moor to unload oil) in south Brazil

Discussion
Our results revealed that habitat type influenced the relationship between TL and depth of occurrence of E. itajara. For artificial habitats there was a non-significant nonlinear relationship between TL and depth. The presence of artificial structures influences habitat choice, and the association of this species with artificial habitats is widely described in the literature (Carvalho-Filho, 1999;Eklund & Schull, 2001;Félix-Hackradt & Hackradt, 2008). Artificial reefs are usually high relief reefs (Collins & Barbieri, 2010;Koenig et al., 2011), and this vertical structure seems to exert an attraction to the species. The habitats reported in the present study (concrete reefs, shipwrecks and oil-gas structures) consisted of structures which can provide substantial shelter, especially for larger individuals, which demand habitats with abundant holes and caves sufficiently large to accommodate adultsized individuals (Koenig & Coleman, 2009). This is not necessarily available in shallow reefs. Abundances of E. itajara by sighting at artificial habitats were significantly higher than at natural ones, especially in mid depths. Such correlation between artificial habitat and the abundance of E. itajara was also observed in the central eastern Gulf of Mexico (Collins, 2008). In contrast, Koenig et al. (2011) observed that adults prefer high-relief habitats that provide shelter, but observed no preference between the high-relief artificial and high-relief natural reefs.
Although 'Parque dos Meros' and Fernando de Noronha accounted for the largest number of reports (25 and 24; see Fig. 1), it does not necessarily mean that the species is most abundant at these points. Such sites are frequently visited by recreational scuba divers, mainly during austral summer. Based in high site fidelity for E. itajara (Koenig et al., 2011) and the largest amount of reports on sites that diving tourism exists, it is possible that reports include several sightings of the same fish. Resightings of individual E. itajara at specific sites have been observed through the years, and images provide the photo-identification of individuals through scars (Giglio et al., 2014), showing high degrees (> 4 years) of residence.
Whilst size at first maturity has not been reported for the South Atlantic stock, Bullock et al. (1992) found that individuals around 115.5 cm were observed to be sexually mature in the Eastern Gulf of Mexico. During this study, the majority of observed fish were medium-sized (100 to 150 cm TL), suggesting that most fish documented were adults. Large adults were observed in all depth ranges (sightings were reported from 5 to 30 m). Juveniles are often found in estuarine areas (Eklund & Schull, 2001;Frias-Torres, 2006). However, ontogenetic offshore migration is not necessarily related to growth. For juveniles, previous studies observed individuals out of estuaries at wide range depths (Collins, 2008;Koenig et al., 2011), indicating that E. itajara may leave nursery habitats earlier than previously believed (100 cm TL; Koenig et al., 2007).
Goliath grouper aggregations were observed in three sites during austral summer, spring and winter. The species aggregates during spawning season, which is suspected to take place during the summer months within the study region. In South Brazil, at Santa Catarina State and 'Parque dos Meros' artificial reefs, aggregations were observed during austral summer and winter. However, our results have limitations once sampling effort is not available by seasons.
In Brazil, small aggregations have been reported by artisanal fishermen as reproductive events during austral summer (December -March;Reuss-Strenzel & Assunção, 2008;Gerhardinger et al., 2009). However, aggregations in Brazil have also been observed during autumn (Félix-Hackradt & Hackradt, 2008) and spring (J. Adelir-Alves, pers. comm.), demanding more specific investigations on the nature of these aggregations. These sites may shelter small resident aggregations throughout the year, possibly due to the availability of shelter and food resources, besides being close to estuaries.
Mapping spawning aggregation sites and seasons will be of importance when formulating conservation strategies to curb illegal fishing practices. Given that illegal fishing of aggregations are regularly observed in Brazil at sites still unknown to science (IBAMA, 2009;ICMBio, 2011;authors pers. obs.), data on species occurrence, seasonal distribution, and site preferences will provide the necessary information to better apply surveillance efforts and other E. itajara conservation initiatives.
Regarding quality and validity of the data collected by volunteers, a series of features in our study led us to conclude that the data presented here are reliable. Firstly, the distinctive morphological characteristics and behavior reduces the probability of E. itajara misidentifications. Secondly, the requested information such as dive site, depth, and habitat are details most divers habitually record in personal dive logs. Finally, we did not observe discrepancies regarding TL between the information of researchers and recreational divers. However, the main limitation of our study is that volunteer diver surveys are often concentrated in areas of prime habitat, are more frequent during certain seasons, and so being rarely distributed evenly through space and time.
This study provides the first broad spatial scale visualization of habitat use and abundance of E. itajara along the Brazilian coastline. Our results underscore the importance of developing conservation measures addressing specific habitats and locations to boost population recovery. Artificial structures might be strategic habitats for goliath grouper conservation policies, but should be properly protected from illegal fishing practices and habitat degradation as a fundamental strategy for the recovery of these populations, i.e., by spatially bounded and appropriately enforced governing regimes. Otherwise, artificial reefs will act as unintentional fishing enhancement devices. We believe this concern should be entirely and comprehensively thought as part of the stepzero process of environmental licensing for artificial reefs. As Gerhardinger et al. (2009) have suggested the 'Parque dos Meros' artificial reefs are of high conservation concern, as large goliath groupers attracted to these artificial reefs have become easy targets for spearfishermen. Nonetheless, the occurrence of this docile, large-sized and emblematic fish adds an important attraction to any diving sites. Therefore, only if they are properly governed, goliath grouper abundant seascapes could become an economic alternative allied with conservation outcomes.