Continental Shelf Research 70 (2013) 126–134 Contents lists available at ScienceDirect Continental Shelf Research journal homepage: www.elsevier.com/locate/csr Research papers Sinkhole-like structures as bioproductivity hotspots in the Abrolhos Bank Giselle S. Cavalcanti a, Gustavo B. Gregoracci a, Leila de L. Longo b, Alex C. Bastos c, Camilo M. Ferreira d, Ronaldo B. Francini-Filho d, Rodolfo Paranhos a, Renato D. Ghisolfi c, Ricardo Krüger e, Arthur Z. Güth f, Paulo Y.G. Sumida f, Thiago Bruce a, Oswaldo Maia-Neto a, Eidy de O. Santos a, Tetsuya Iida g, Rodrigo L. Moura a, Gilberto M. Amado-Filho b, Fabiano L. Thompson a,n a Departamento de Biologia Marinha, Instituto de Biologia, Centro de Ciências da Saúde, Universidade Federal do Rio de Janeiro. Ilha do Fundão, CP 68011, Rio de Janeiro, RJ 21944-970, Brazil b Instituto de Pesquisas Jardim Botânico do Rio de Janeiro. Rua Pacheco Leão 915, Rio de Janeiro, RJ 22460-030, Brazil c Departamento de Oceanografia, Universidade Federal do Espírito Santo. Avenida Fernando Ferrari 514 Vitória, ES 29090-600, Brazil d Departamento de Engenharia e Meio Ambiente, Centro de Ciências Aplicadas e Educação, Universidade Federal da Paraíba, Rua da Mangueira S/N, Rio Tinto, PB 58109-753, Brazil e Laboratório de Enzimologia, Departamento de Biologia Celular, Universidade de Brasília, Brasília, DF 70910-900, Brazil f Departamento de Oceanografia Biológica, Instituto Oceanográfico, Universidade de São Paulo, São Paulo, SP 05508-120, Brazil g Laboratory of Genomic Research on Pathogenic Bacteria, International Research Center for Infectious Diseases, Research Institute for Microbial Diseases, Osaka University, Suita, Osaka 565-0871, Japan article info abstract Available online 7 June 2013 We performed a biological survey in the novel system of sinkhole-like structures (“buracas”) of the Keywords: Abrolhos Bank, Brazil. We found dissimilar benthic assemblages and higher nutrient concentration, fi Microbial productivity microbial abundance (and activity) and sh abundance inside the buracas than in the surrounding Nutrients rhodolith beds. Our results support the view that these cup-shaped structures trap and accumulate Reefs organic matter, functioning as productivity hotspots in the mid and outer shelf of the central portion of Marine ecology the Abrolhos Bank shelf, where they aggregate biomass of commercially important fishes. This distinctive system is being increasingly pressured by commercial fisheries and needs urgent management measures such as fishing effort control and representation in the network of Marine Protected Areas (MPAS). & 2013 Elsevier Ltd. All rights reserved. 1. Introduction and functioning because of logistic constraints (Hinderstein et al., 2010). Technological advances are now providing easier access to The Abrolhos Bank contains the largest and richest coralline reefs rebreathers and mixed-gas diving, remotely operated vehicles of the South Atlantic. This coastal system is well known for its coral (ROVs) and high-resolution sidescan imagery, making it possible assemblages dominated by Brazilian-endemic species (Leão and to investigate these environments in more detail. Ginsburg, 1997) with distinctive mushroom-shaped reef pinnacles While hosting some depth-restricted species, mesophotic reefs (Hartt, 1870; Verrill, 1868; Laborel, 1969), dwelling under high contain many shallow-water species (Thresher and Colin, 1986; siliciclastic sedimentation. Current knowledge on local reef morpho- Macintyre et al., 1991), often representing refugia for commercially- genesis and ecology is derived mainly from studies on inner-shelf important species that are already threatened in shallower reefs Holocene structures. Recent assessments have shown a high geodi- (Glynn, 1996; Armstrong et al., 2006). Within the large mesophotic versity in the mid- and outer shelf (Moura et al., 2013), including reef realm of the Abrolhos Bank, the unusual sinkhole-like sinkhole-like structures described by Bastos et al., 2013) and herein. depressions, locally named “buracas” (“buraca” meaning “hole” in Mesophotic coralline ecosystems occur in many locations Portuguese) are outstanding features with potentially important throughout the tropics, from about 30-m depth to the bottom of ecological roles in the mid- and outer shelf. Although diverse the photic zone (Lesser et al., 2009; Kahng et al., 2010). However, submerged sinkholes have been described worldwide, typically until recently only scarse information existed on their biodiversity found on shallow carbonate platforms, exemplified by the Bahama Banks (Whitaker and Smart, 1998; Reed et al., 2005), as well as on and around the Yucatán Peninsula (Schmitter-Soto et al., 2002), n such as at the Great Blue Hole at Lighthouse Reef Atoll, Belize Corresponding author. Tel./fax: +55 21 256 265 67. E-mail address: [email protected] (F.L. Thompson). (Gischler et al., 2008), the majority of studies of the underwater 0278-4343/$ - see front matter & 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.csr.2013.05.011 G.S. Cavalcanti et al. / Continental Shelf Research 70 (2013) 126–134 127 sinkholes focus on various aspects of their geology (Betzler et al., part at 93 m depth and a diameter of approximately 55 m; the 2011; van Hengstum et al., 2012; Martin et al., 2012). Few studies second site (Buraca 2—B2) is located 115 km offshore (at 26 m focus on the ecology or biology of either the microbial, benthic or depth), with its deepest part at 43 m depth and a diameter of fish communities (Reed et al., 2005; Baumberger et al., 2010; Nold approximately 40 m (Fig. 1). Site B1 comprises a single isolated et al., 2010). structure, while site B2 comprises two adjacent structures. Water The numerous novel sinkhole-like structures located off eastern sampling was carried out between 27 and 85 m depth, inside (IN) Brazil were initially discovered by local fishermen, as they were B1 (1 m from the bottom) and in the largest structure at site B2 anecdotally reported as major fishing grounds. The underlying (8 m from the bottom), as well as in two control areas outside reasons for such increased fisheries yields were initially unclear, as (OUT) the structures, 200—500 m away from the edge. Other fishermen also reported different water color and odor, a character- biological sampling (fish counts and benthic assessments) was istic “mangrove-like” smell in these very specific spots. Although the carried out inside the three structures and in two outside control “buracas” aggregate fishes (both reef and pelagic) and lobsters, which sites. Field work was conducted in two consecutive summers are important targets for commercial fisheries, those structures are (2009–2010). not comprised in the existing network of Marine Protected Areas. We assessed the main biological and chemical features of these 2.2. Chemical analysis and bacterial abundance cup-shaped structures in order to evaluate their potential role as productivity hotspots. The specific aims of our study were: (1) to Environmental parameters were analyzed by standard oceano- assess the physicochemical characteristics of the “buracas” system, graphic methods (Grasshoff et al., 1999). Chlorophyll-a quantifica- including inorganic and organic nutrient content; (2) to quantify tion was performed after vacuum filtration (o25 cm of Hg; microbes and to describe their diversity through metagenomic cellulose membrane Millipore HAWP 0.45 mm) of 1-L seawater analyses and metabolic profiles; (3) to survey the main benthic samples. Membranes were frozen in liquid nitrogen until labora- taxa and fish communities associated with such structures. The tory analysis, when pigments were extracted overnight in 90% mesophotic reefs in the mid- and outer shelf of Abrolhos add acetone at 4 1C and analyzed with a UV–vis Perkin Elmer Lambda complexity to the models explaining the evolution of this unique 20 spectrophotometer (Perkin Elmer, USA). Water samples were tropical continental shelf (Laborel, 1969; Leão et al., 2003), and frozen in the field for inorganic nutrients analyses, which were also challenge the understanding of biological processes and cross- carried out by the following methods: (1) ammonium by indo- shelf connectivity patterns (e.g. Moura et al., 2011), with important phenol, (2) nitrite by diazotization, (3) nitrate by reduction in implications for natural resources management. Cd–Cu column followed by diazotization, (4) total nitrogen by digestion with potassium persulfate following nitrate determina- tion, (5) orthophosphate by reaction with ascorbic acid, (6) total 2. Materials and methods phosphorous by acid digestion to phosphate, and (7) silicate by reaction with molibdate. 2.1. Study sites and sampling design Total bacterial abundance was determined from 2 mL water subsamples (three replicates) immediately fixed in the field with The distribution, location and geomorphological characteristics sterile 2% paraformaldehyde for 15 min and further preserved in of the sinkhole-like structures are described elsewhere (Bastos liquid nitrogen (Gasol and Del Giorgio, 2000). Microbial cells with et al., this issue). Briefly, a total of 35 circular depressions (17–55 m high (HNA) and low (LNA) nucleic acids content were distinctly in diameter, 8—44 m height) occurring between 77 and 198 km off quantified through measurement of fluorescence intensity by flow the coast were recently identified within the Abrolhos region, cytometry with Syto-13 (Life Technologies, Carlsbad, CA), with eastern Brazil. Sampling was carried out