311 Abstract—We examined the age Age and growth of dusky grouper (Epinephelus and growth of dusky grouper (Epinephelus marginatus) at off- marginatus) (Perciformes: Epinephelidae) shore Carpinteiro Bank (32°16′S; in the southwestern Atlantic, with a size 52°47′W) in the southwestern Atlantic through the analysis of comparison of offshore and littoral habitats growth increments in otoliths. We also examined the hypoth- Mario V. Condini (contact author)1 esis that this offshore habitat Cristiano Q. Albuquerque2 represents a superior site for Alexandre M. Garcia1 fish growth compared with in- shore habitats. Samples con- Email address for contact author: [email protected] sisted of 211 groupers captured by small-scale fisheries between 1 Instituto de Oceanografia 2008 and 2011 and with total Universidade Federal do Rio Grande lengths ranging from 150 to Avenida Itália km 8, Carreiros 1160 mm. Otolith growth incre- 96201-900, Rio Grande ments were deposited once per Rio Grande do Sul, Brazil year, and opaque bands formed 2 Departamento de Oceanografia e Ecologia mostly during the summer, as Universidade Federal do Espírito Santo determined through marginal 29075-900, Vitória increment analysis. Ages ranged Espírito Santo, Brazil from 1 to 40 years, and most fish were aged to be between 2 and 8 years (global mean: 7.4 years, standard deviation 6.9). Von Bertalanffy growth parameters for pooled sexes were L∞=900.9 The dusky grouper (Epinephelus Harmelin-Vivien, 2004), with a de- mm, K=0.129 and t0=−1.45. Fish marginatus) (Epinephelidae) inhab- creasing global population trend. from the offshore habitat were its shelter-rich, hard substrata on the The dusky grouper is the only generally older and their mean continental shelf along the eastern large epinephelid that is usually sizes were significantly larger coast of South America from Brazil to found along the extreme southern at ages 3, 4, 5, and 6 than those Argentina (Figueiredo and Menezes, part of the Brazilian coast, where it of fish from the inshore habi- 1980; Irigoyen et al., 2005), through- is fished over inshore rocky bottoms tat. Our findings highlight the out the Mediterranean Sea, and from (depths <5 m) and offshore banks importance of Carpinteiro Bank the British Isles around the southern (depths >10 m) by small-scale fish- as an important growth habitat tip of Africa (Heemstra and Randall, eries (Condini et al., 2007). Offshore for dusky groupers in the south- 1993) to southern Mozambique (Fen- populations of dusky grouper occa- western Atlantic and indicate nessy, 2006). Adults inhabit rocky sionally are targeted opportunistical- that fishery management mea- bottoms, generally at depths up to 50 ly by large-scale commercial fisheries sures should be implemented to that use hand lines, but the species m, and they can be found occasion- ensure the maintenance of this is otherwise not a commercially tar- ally at depths up to 250 m (Bruslé, endangered species in this off- geted species. The most frequently 1985; Heemstra and Randall, 1993), shore bank in the future. visited site in the southwestern At- whereas juveniles are usually found lantic for commercial offshore fishing in coastal tide pools (Azevedo et al., of this species is Carpinteiro Bank. 1995). Like other epinephelids, the The role of dusky groupers in the dusky grouper is a slow-growing pro- coastal ecosystems of South America togynous hermaphrodite species with is not completely understood. Given late sexual maturation and low nat- the likely importance of this spe- Manuscript submitted 18 June 2013. ural mortality rates (Manooch and cies as a predator (Reñones et al., Manuscript accepted 22 August 2014. Mason, 1987), and it is also a highly 2002), it is imperative to understand Fish. Bull. 112:311–321 (2014). valuable commercial fish (Heemstra the implications of any sort of com- doi:10.7755/FB.112.4.7 and Randall, 1993). These combined mercial exploitation that may be characteristics make the dusky grou- involved. To prevent stock collapse, The views and opinions expressed or per highly vulnerable to overfishing. implied in this article are those of the reef fishes should be fished carefully author (or authors) and do not necessarily This species is classified as endan- because slow-growing, late-maturing reflect the position of the National gered by the International Union for fish species are found frequently in Marine Fisheries Service, NOAA. Conservation of Nature (Cornish and coastal ecosystems and are vulner- 312 Fishery Bulletin 112(4) SOUTH AMERICA B 32°08 S A Rio Grande 52°04 W Figure 1 Map showing (A) Patos Lagoon and its estuarine zone (10.36 km2) in Rio Grande, the southern- most state in Brazil; (B) the location of the pair of rocky jetties at the mouth of the lagoon (arrow) and, in the adjacent marine area, Carpinteiro Bank in the southwestern Atlantic. The lines along the coast denote the 10-, 15- and 20-m isobaths. The specimens of the dusky grouper (Epinephelus marginatus) sampled in this study were caught at the Carpinteiro Bank by small-scale fisheries from 2008 to 2011. able particularly to overfishing (Coleman et al., 2000; better habitats for growth and reproduction of dusky Sadovy et al., 2013). Quantifying the age and growth groupers than inshore habitats (depths <5 m). of dusky groupers is required, therefore, to support ad- equate conservation and management of this species at its southernmost region of occurrence. Material and methods Previous investigations have provided initial infor- mation on the age structure of the dusky grouper in Sampling, fish processing, and study area South America and also revealed the absence of repro- duction in a coastal population associated with littoral Dusky grouper samples examined in this study (n=211) rocky jetties from extreme southern Brazil (Seyboth et were identified according to Heemstra and Randall al., 2011). Those authors adopted the classification de- (1993). They were collected twice a month from land- veloped by Craig and Hastings (2007) that placed the ings in small-scale fisheries in Rio Grande, a port city dusky grouper in Mycteroperca. For our study, we fol- in southern Brazil (Fig. 1), from 2008 to 2011. Fish lowed the most recent classification (Craig et al., 2011), were caught with hand lines, and their origin was eval- in which the species was retained in Epinephelus, given uated through interviews with owners of fishing boats. the absence of conclusive studies to change the genus. Only fish caught specifically at the Carpinteiro Bank Another study conducted in this region revealed that were considered. In the laboratory, the total length the dusky grouper reproduces at offshore Carpinteiro (TL) in millimeters and weight (WT) in grams of each Bank (Condini et al., 2014). In this study, we validated the timing of increment specimen were measured, and sex was identified by a deposition in otoliths and examined the aging struc- macroscopic examination of the gonads following Ma- ture and growth parameters of dusky grouper in an rino et al. (2001). Male and female gonadal differences offshore habitat (Carpinteiro Bank, at depths of 15– are quite clear in macroscopic examination for this 25 m). Because we had access to the original data of hermaphroditic grouper (Marino et al., 2001; Condini Seyboth et al. (2011), we also aimed to test the hypoth- et al., 2014). The Carpinteiro Bank (32°16′S; 51°47′W) esis, previously reported by Seyboth et al. (2011), that (Fig. 1) is a submersed reef, with depths ranging from offshore habitats (depths of 15–25 m) may constitute 15 to 25 m, formed by beach rocks and is superficially Condini et al.: Age and growth of Epinephelus marginatus in the southwestern Atlantic 313 colonized by bryozoans, sponges, crustaceans, poly- Growth increment measurements were conducted with chaetes, and coralline algae (Buchmann et al., 2001). otolith images by using the free software ImageTool Located approximately 30 km offshore from the city of (University of Texas Health Science Center, San An- Rio Grande (32° S), this bank is likely the most aus- tonio), which was calibrated with a micrometric scale tral region where the dusky grouper is commercially glass. For MIA, 188 otoliths (from fish of sizes from 277 exploited. to 1160 mm TL) were used. During summer, autumn, winter, and spring, 91, 48, 10, and 39 otoliths, respec- Otolith processing tively, were obtained,. Marginal increment values were averaged over the summer (January–March), autumn The sagittal otoliths were dissected from all samples (April–June), winter (July–September) and spring (Oc- and stored dry. The otoliths were then embedded in ep- tober–December). These averages were compared by oxy resin and sectioned through the core with an Isom- using the nonparametric Kruskal-Wallis and Mann- et1 low speed saw (Buehler, Lake Bluff, IL) coupled to a Whitney tests (Zar, 1999) because the data were not diamond wafering blade to obtain sections 0.4–0.6 mm normally distributed. thick. These sections were glued to histological glass To estimate average growth, the number of otolith slides, polished with fine sandpaper (grits of 2000– increments was modeled against TL by fitting a von 8000), embedded in Entellan mounting medium (Merck Bertalanffy (Eq. 3) curve and by using a nonlinear KGaA, Darmstadt, Germany), covered with thin glass least squares method (Ricker, 1975). slides, and, finally, examined under a stereomicroscope –K(t–t ) coupled to a computerized imaging system. All sections TL = L∞ (1 – e 0 ), (3) were photographed under transmitted light so that where TL = the TL corresponding to age I; translucent and opaque bands in the otoliths could be L∞ = the mean theoretical maximum TL; appear as white and dark bands in the digital photo- t0 = the theoretical age at zero length; and graphs, respectively. Each otolith was read 3 times at K = the growth coefficient, the rate at which the intervals of one month by an experienced reader with curve approaches the asymptote.