Trophic ecology of dusky grouper Epinephelus marginatus (Actinopterygii, Epinephelidae) in littoral and neritic habitats of southern Brazil as elucidated by stomach contents and stable isotope analyses Mario V. Condini, David J. Hoeinghaus & Alexandre M. Garcia Hydrobiologia The International Journal of Aquatic Sciences ISSN 0018-8158 Hydrobiologia DOI 10.1007/s10750-014-2016-0 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. This e- offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Hydrobiologia DOI 10.1007/s10750-014-2016-0 PRIMARY RESEARCH PAPER Trophic ecology of dusky grouper Epinephelus marginatus (Actinopterygii, Epinephelidae) in littoral and neritic habitats of southern Brazil as elucidated by stomach contents and stable isotope analyses Mario V. Condini • David J. Hoeinghaus • Alexandre M. Garcia Received: 11 March 2014 / Revised: 11 August 2014 / Accepted: 14 August 2014 Ó Springer International Publishing Switzerland 2014 Abstract Groupers are large-bodied fishes with SIA distinguished ingested versus assimilated dietary broad global distribution and commercial and ecolog- components, improved dietary resolution, and pro- ical importance. Many grouper species are endan- vided a more comprehensive assessment of grouper in gered, but information on trophic ecology of groupers the food webs. Dusky grouper integrate benthic and outside the Mediterranean Sea is limited. We inte- pelagic trophic pathways, as well as estuarine and grated stomach contents analyses (SCA) and stable marine food webs via consumption of migratory prey. isotope analyses (SIA) to test the hypotheses that diets Our findings have applications to other threatened of dusky grouper Epinephelus marginatus differ grouper populations, for example, in managing frag- between littoral and neritic zones in the southwestern mented populations or for reserve designs considering Atlantic, but exhibit similar ontogenetic shifts in prey inclusion of artificial substrates as grouper habitat, and size and consumption of fishes. SCA were dominated more broadly for approaches examining trophic ecol- by fishes, crabs, and shrimp and differed significantly ogy of generalist predators. between habitats, but prey size and consumption of fishes increased with grouper body size at both sites. Keywords Food web Á IUCN red list Á Man-made Grouper stable isotope ratios were similar between habitats Á Migration Á Ontogenetic shifts Á Subsidies sites and among size classes, but integrating SCA and Handling editor: I. A. Nagelkerken Introduction Electronic supplementary material The online version of Groupers are large-bodied fishes of the families this article (doi:10.1007/s10750-014-2016-0) contains supple- mentary material, which is available to authorized users. Serranidae and Epinephelidae with a broad global distribution and large commercial and ecological M. V. Condini (&) Á A. M. Garcia importance (Sadovy de Mitcheson et al., 2013). Laboratory of Ichthyology, Institute of Oceanography, Groupers are targeted by artisanal, industrial, and Federal University of Rio Grande, Av. Ita´lia Km 8, Carreiros, Rio Grande, RS 96.201-900, Brazil sport fishing throughout their ranges (Heemstra & e-mail: [email protected] Randall, 1993; Craig et al., 2011) and often have strong influences on food webs and ecosystems through their D. J. Hoeinghaus roles as top predators (Heemstra & Randall, 1993; Department of Biological Sciences and the Institute of Applied Sciences, University of North Texas, 1155 Union Sluka et al., 2001). Alterations to grouper populations Circle #310559, Denton, TX 76203-5017, USA can thus have significant commercial and ecological 123 Author's personal copy Hydrobiologia consequences (Parrish, 1987; Brule´ et al., 2005). Most protected areas (e.g., Ren˜ones et al., 2002). That being grouper species exemplify a periodic life-history said, there is very limited information on the trophic strategy (Winemiller, 2005) with slow growth rates, ecology of dusky grouper outside of the Mediterranean late maturation and a complex mode of seasonal Sea (e.g. Machado et al., 2008; Begossi & Silvano, reproduction including spawning aggregations and 2008; Condini et al., 2011). This is especially true for the sexual reversal (Manooch & Mason, 1987), that southern Atlantic coast of Brazil, even though the dusky combined with high fishing pressure leads to vulner- grouper is an important high-value species harvested by ability and/or over-exploitation of many grouper small-scale fisheries (Condini et al., 2007)andis populations (Huntsman et al., 1999; Coleman et al., broadly recognized for its cultural and conservation 2000). One such example is the dusky grouper importance (e.g., gracing the Brazilian R$100 banknote; Epinephelus marginatus (Lowe, 1834), that like many Fig. S1). For groupers in general, most trophic ecology other species of the family Epinephelidae, is included studies are restricted to stomach contents analyses in the International Union for the Conservation of (Grover, 1993;Brule´ et al., 2005; Condini et al., 2011) Nature (IUCN) red list as ‘‘endangered’’ (EN a2d), and few studies utilize stable isotope analyses (Ren˜ones probably due to its complex life-history strategy and et al., 2002;Nelsonetal.,2012). increasing fishing pressure (Cornish & Harmelin- In this study, we integrate stomach contents and Vivien, 2004). stable isotope analyses to describe the trophic ecology of The dusky grouper occurs along the southwestern dusky grouper at two locations along the southern Atlantic coastline with Argentina, Uruguay, and south- Brazilian coast. Our objectives were to indentify key eastern Brazil (Figueiredo & Menezes, 1980; Irigoyen prey species, test for ontogenetic shifts in diet and et al., 2005), throughout the British Isles and the between males and females, and finally to compare Mediterranean Sea (Heemstra & Randall, 1993)and trophic ecology of dusky grouper populations between along the African coast to Mozambique in the extreme natural and man-made habitats. We expect grouper diets southeastern Atlantic (Fennessy, 2006). Dusky grouper to differ between sites, specifically with greater impor- typically inhabit rocky substrates up to 250 m depth but tance of estuarine-dependent prey for littoral grouper with a preference for shallower waters up to 50 m depth and marine-dependent prey for neritic grouper, but (Brusle´, 1985; Heemstra & Randall, 1993; Harmelin & exhibit similar ontogenetic diet shifts of increasing prey Harmelin-Vivien, 1999). Similar to other grouper species size and greater dependence on fishes with increasing (Beckley, 2000), dusky grouper juveniles are commonly grouper body size at both sites. Carbon and nitrogen found in the coastal zone, including tidal pools (Azevedo stable isotope values should complement the stomach et al., 1995) and small bays in estuarine regions (MVC contents data, specifically, we expect carbon stable unpublished data). Rocky substrates are utilized as cover isotope values of grouper to differ between sites due to by this ambush predator and individuals may use different differences in carbon sources supporting littoral and habitat structures and body positioning depending on neritic food webs and grouper nitrogen stable isotope grouper body size and what prey item is being sought values to increase with increasing body size as larger (e.g., fishes vs. octopii; Barreiros & Santos, 1998). The individuals feed higher in the food web (i.e., consume dusky grouper is a monandric protogynous hermaphro- greater biomass of fishes). This study contributes to the ditic species (Marino et al., 2001) and sexual transition limited knowledge currently available for this endan- can occur in individuals between 52 and 77 cm TL gered species in the southern Atlantic and has direct (Ren˜ones et al., 2010). In extreme southern Brazil, application to management and conservation activities individuals larger than 75 cm TL have usually undergone for this region and elsewhere. sexual transition (Condini et al., 2013, 2014). Studies on the trophic ecology of dusky grouper are relevant for basic understanding of the ecology of the Materials and methods species, as well as insights into the trophic organization of the ecosystem and mechanisms affecting interactions Study area and field collections among species (Herra´n, 1988). Furthermore, such information is relevant for applications such as fisheries This research was conducted at two locations on the management and selection and monitoring of marine southern Brazilian coast. The first location is in the 123 Author's personal copy Hydrobiologia Fig. 1 Patos Lagoon (10,360 km2) and its estuarine zone in the mouth of the lagoon (B), and Carpinteiro Bank in the adjacent state of Rio Grande do Sul, southern Brazil (A), showing the marine area (C). The lines along the coast (A) denote 10, 15, and locations of the two sampling