Feeding ecology of two sympatric species of large-sized groupers (Perciformes: Epinephelidae) on Southwestern Atlantic coralline reefs

ABSTRACT

Red and black groupers are large-bodied opportunistic ambush predators commonly found in Southwestern Atlantic tropical reefs. We investigated the diet of both species in order to detail ontogenetic, spatial and temporal trends, and to assess the extent of overlap in resource use between these two sympatric predators on the Abrolhos Bank, Brazil. Decapods and fishes were the main food items of Epinephelus morio while fishes were the main prey of Mycteroperca bonaci. Both diets were significantly influenced by body size and habitat, but only smaller individuals of E. morio feed almost exclusively on crustaceans. While the two groupers rely on many of the same prey types, coexistence may be facilitated by E. morio feeding more heavily on crustaceans, particularly the blackpoint sculling crab Cronius ruber, while black grouper take comparatively few crustaceans but lots of fish prey. Predators like red and black groupers could trigger indirect effects in the community and influence a large range of ecological processes, such as linkages between top and intermediate predators, and intermediate predators and their resources.

Keywords:
Abrolhos Bank; Diet; Epinephelus morio; Feeding overlap; Mycteroperca bonaci

RESUMO

A garoupa e o badejo-verdadeiro são predadores oportunistas de grande porte, com estratégia de emboscada, comumente encontrados em recifes tropicais do Atlântico Sul. A dieta das duas espécies foi investigada, avaliando influências ontogenéticas, espaciais e temporais, assim como a sobreposição no uso de recursos entre estes dois predadores co-orrentes no Banco dos Abrolhos, Brasil. Decápodes e peixes foram os principais itens alimentares de Epinephelus morio, enquanto que os peixes foram as principais presas de Mycteroperca bonaci. Ambas as dietas foram significativamente influenciadas pelo tamanho corporal e habitat, mas apenas indivíduos menores de E. morio alimentaram-se quase que exclusivamente de crustáceos. Como as duas espécies utilizam muitas presas semelhantes, a coexistencia parece ser facilitada pelo fato de E. morio se alimentar principalmente de crustáceos, particularmente do caranguejo Cronius ruber, enquanto que o badejo-verdadeiro consome relativamente poucos crustáceos e grande quantidade de peixes. Predadores como as espécies estudadas podem causar efeitos indiretos na comunidade e influenciar uma grande variedade de processos ecológicos, como conexões entre predadores de topo e intermediários e predadores intermediários e seus recursos.

Palavras-chave:
Banco dos Abrolhos; Dieta; Epinephelus morio; Mycteroperca bonaci; Sobreposição alimentar

Introduction

Epinephelids are demersal predatory fishes found in shallow to mesophotic waters of all tropical and subtropical oceans, especially in hard bottom habitats (Heemstra, Randall, 1993; Craig et al., 2011). The 160 or so species in the family encompass a wide range of body sizes and food habits, ranging from small zooplanktivores to some of the largest predators in tropical and subtropical reef ecosystems (Claro et al., 2001).

The red grouper Epinephelus morio (Valenciennes, 1828) and black grouper Mycteroperca bonaci (Poey, 1860) are large (maximum sizes of 125 and 150 cm, respectively) carnivores that inhabit rocky and coralline reefs (Crabtree, Bullock, 1998). They are among the most common epinephelids in the Tropical Western Atlantic and support important fisheries throughout their range (Burgos et al., 2007; Crabtree, Bullock, 1998; Freitas et al., 2011b) from Massachusetts (EUA) to Southeastern Brazil (Heemstra, Randall, 1993). In the Abrolhos Bank, the largest and richest coralline reefs in the South Atlantic (Moura et al., 2013), groupers have been heavily targeted since at least the mid 16^th Century (Bueno, 1999).

Black and red groupers are important predators in hard-bottom communities of the tropical Western Atlantic (Brulé, Canché, 1993; Brulé et al., 1994; Brulé et al., 2005). In the Abrolhos Bank, they are the two most abundant epinephelids, representing more than three times the biomass of all other groupers combined, and 20% of large carnivore’s biomass, a category that also includes sphyraenids, lutjanids and carangids (Francini-Filho, Moura, 2008a). In the Northern Hemisphere, fishes, crustaceans, gastropods and cephalopods are important dietary components of both species (Moe, 1969; Bullock, Smith, 1991; Brulé, Canché, 1993; Brulé et al., 1994; Brulé et al., 2005), but there is no information on their food habits for the entire Southwestern Atlantic.

Groupers are predators thought to play important roles in ecosystem function through either direct or indirect interactions (Huntsman et al., 1999; Dulvy et al., 2004; Campbell, Perdede, 2006; Rizzari et al., 2014). Therefore investigations on the relationships among such large-bodied marine predators, their predator-prey interactions and the environment are important for an overall understanding of the mechanisms that structure populations and communities of reef fishes (Hixon, 1991; Hixon, Beets, 1993). Food partitioning among closely related co-occurring predators is crucial for their coexistence (Davies et al., 2007).

Several modes of space and food utilization enable reef fishes inhabiting structurally complex habits to generate differential patterns of resource partitioning (Jones, 1968; Smith, Tyler, 1972; Shpigel, Fishelson, 1989; Gibran, 2007). Resource partitioning includes food, habitat and/or temporal segregation (Pianka, 1973; Schoener, 1974), and has been extensively documented among reef and rocky fishes (e.g.Clarke, 1977; Hixon, 1980; Larson, 1980; Gladfelter, Johnson, 1983; Bouchon-Navaro, 1986; Sala, Ballesteros, 1997; Pratchett, 2005; Gibran, 2007). The degree of overlap in the use of available resource among grouper species is variable, and interactions are associated, for example, with seasonal and diel changes (Brulé et al., 1994), habitat use (Sierra et al., 2001; Craig et al., 2011) and ontogenetic shifts (Machado et al., 2008; Freitas et al., 2015). Food segregation seems to play a more important role than habitat or temporal separations within many fish assemblages (Ross, 1986).

In the present study we investigated food habits of the black and red groupers obtained from eight years of artisanal fisheries monitoring program in the Abrolhos Bank region in Brazil. This comprehensive dataset included stomach contents from groupers collected from a variety of habitats and seasons, and therefore presumably reflects the general feeding habits of species examined. Information provided here represents one of the most extensive databases assembled over a relatively large period of time, particularly for a coralline reef environment, and provides a uniquely large amount of information to investigate ecological interactions among large-bodied marine predators, and to understand the role of predation in the regulation of reef fish communities. Specifically, our objectives were to determine important prey groups in the diets of these groupers and estimate their relative importance, identify any spatial, temporal or ontogenetic shifts in their diets, and assess the extent of overlap in the diet between these two sympatric predators. Data provided here is the first information on the feeding ecology of the red and black groupers in the Southwestern Atlantic.

Material and Methods

Study area. The study was carried out in the Abrolhos Bank (16º40’- 19º40’ S; 39º10’- 37º 20’ W), a region with 42,000 km² and depths rarely exceeding 30 m, with a shelf edge at about 70 m depth. Abrolhos harbors an extensive mosaic of benthic megahabitats (Moura et al., 2013). Rhodolith beds comprise the largest megahabitat (~21,000 km²), followed by unconsolidated sediments (~20,000 km²) and reefs (~9,000 km²). The two groupers studied are predominantly found on reefs and less often on rhodolith beds, being absent from unconsolidated bottoms. Most reefs in this region assume the characteristic and highly peculiar form of mushroom-shaped pinnacles (chapeirões), which rise 5 to 25 m height above the bottom and extend from 20 to 300 m across their tops (Francini-Filho, Moura, 2008a,b).

There are four marine protected areas (MPAs) in the region, all of them poorly enforced. The Extractive Reserve of Cassurubá (ERC; 1,006 km²) includes large mangroves in which fishing is small-scale artisanal or for subsistence. The other three MPAs encompass reefs: the no-take National Marine Park of Abrolhos (NMPA; 913 km²), the multiple-use Marine Extractive Reserve of Corumbau (MERC; 895 km²), and the Environmental Protected Area Ponta da Baleia/Abrolhos (EPA; 3,460 km²).

Samples were obtained in two cross-shelf strata, Inner Shelf (IS) and Outer Shelf (OS) (Fig. 1). The IS includes a no-take zone of the NMPA (Timbebas Reefs) and other unprotected reefs such as the Parcel das Paredes (the largest continuous reef in the South Atlantic), Sebastião Gomes, Coroa Vermelha and Viçosa. Reefs in this IS arc consist of banks with flat and exposed tops, and mushroom-shaped pinnacles, with depths reaching up to 20 m. This area is subjected to the highest fishing pressure in the region, with ~200 boats operating regularly with hand lines, spears and various types of nets (Francini-Filho, Moura, 2008a). Siliciclastic (= terrigenous) contents in peri-reefal sediments are higher in the IS, while the carbonate fraction is higher in the OS. The OS includes the best-enforced area of the NMPA, including the Abrolhos islands and the Parcel dos Abrolhos. Besides this protected area with emerging pinnacles, the OS as also encompasses a large realm of mesophotic reefs, rhodoliths beds and seasonal fleshy algal pavements, from 25 to 90 m depths (Moura et al., 2013). The OS also harbors non-emergent pinnacles and coalesced reef structures (drowned reefs), paleo valleys and channels, as well as depressions (similar to sinkholes but formed differently) locally known as “buracas” (Bastos et al., 2013; Moura et al., 2013).

Sampling and analytical procedures. Specimens were obtained monthly through a fish landing monitoring program that target fleets on hook and line, longline and spear fishing in the Cities of Nova Viçosa, Caravelas, Alcobaça, and Prado (Fig. 1), between June 2005 and September 2012. After capture, fishes were immediately stored on ice on board, and transferred to the laboratory where they were kept until processing. Fishes were measured (Total Length - TL cm; Standard Deviation - SD), weighed, and their stomachs were immediately fixed in 10% formalin for 24 h, and subsequently transferred and stored in 70% alcohol. Voucher specimens were deposited in the ichthyological collection of Museu de História Natural Capão da Imbuia (MHNCI 12657 for E. morio and MHNCI 12658 for M. bonaci).

Fig. 1
Map of the Abrolhos Bank showing the municipalities where samples were collected and emerging coralline reefs are shown in dark grey. MER= Marine Extractive Reserve; ER= Extractive Reserve.

Stomach contents were examined in the laboratory using a stereomicroscope. The identification of food items was performed as refined as possible according to literature data (Melo, 1996; Amaral et al., 2006) and consultation with experts. All identifiable prey items were enumerated, weighed and identified to the lowest possible taxon (LPT). If gut contents were too digested for identification, the material was weighed and classified as “remains”. Frequency of occurrence (%FO) (i.e., percentage of stomachs in which a food item occurred), proportion by weight (%W) (i.e., percentage participation of each item in the total food weight), as well as the proportion in number (%N) (i.e., percent of each item within total food items) were determined (Hyslop, 1980; Bowen, 1996). These variables were used to calculate the Index of Relative Importance (IRI) (cf. Pinkas et al., 1971), which establishes the order of importance of food items in the diet. IRI values were standardized to percentages (Cortés, 1999) and were calculated according to the equation IRI = FO (%W + %N). Feeding strategy diagrams (Amundsen et al., 1996) were used to examine the dietary importance of a particular prey item. These diagrams allow for a visual assessment of niche width and the importance of different prey items, as well as the predators’ strategies (specialization vs. generalization), using occurrence and prey-specific weight.

Variations on diet were visualized with respect to cross-shelf strata (IS and OS), size classes (E. morio: juveniles 15-50.0 cm TL and adults 50.5-90 cm TL; M. bonaci: juveniles 26.1-62 cm TL and adults 68-147 cm TL; according to sex and reproductive development presented in Freitas, 2014) and seasons (cool and warm). Seasons were characterized from sea surface temperature (SST) historical data (November 1981- January 2008; http://nomad3.ncep.noaa.gov). The cool season has median SSTs < 26^oC and spans from June to November (min. SST 24.5^oC, August). The warm season has median SSTs >26^oC, spanning from December to May (max. SST 28^oC, February). The warm season is characterized by prevailing NE winds and higher water visibility, while the cold season is characterized by polar front intrusions causing strong sediment re-suspension (Segal et al., 2008).

A two-way crossed permutational multivariate analysis of variance (PERMANOVA) using a population-wide dissimilarity metric was employed to examine the effects of habitat, ontogeny and season (factors) on the standardized and transformed (Logx+1) weight contribution of each prey item (LPT). Significant factors were further analyzed using PERMANOVA pair-wise comparisons. The Bray-Curtis dissimilarity was used in all tests, with 999 permutations under a reduced model. Similarity of percent contribution (SIMPER) analysis was used to examine the prey categories that are most responsible for between-factors separation (Clarke, Gorley, 2001). All analyses were performed using the PRIMER/PERMANOVA 6.0 software (Plymouth Marine Laboratory, Plymouth, England).

Results

A total of 361 stomachs from Epinephelus morio (mean 51.2 cm; range: 15-96 cm TL; SD: ± 13.5) were obtained between May 2005 and September 2012, and only 180 (49.9%) stomachs contained prey items (mean 49.2 cm; range: 23.2-90 cm TL; SD: ± 9.7). Identifiable prey items included decapods, cephalopods, stomatopods and teleosts (Tab. 1). Crustaceans (59.9% IRI) and teleosts (38.1% IRI) were the most important items, while cephalopods, stomatopods and other invertebrates collectively represented 4.2% IRI.

Tab. 1
Diet composition of Epinephelus mori o and Mycteroperca bonac i showing number percentage (N), frequency of occurrence (FO), weight percentage (W) and percentage of Index of Relative Importance (IRI) of food items consumed in two different size classes (Juvenile=J and Adult=A) from the Abrolhos Bank, Brazil. T= Total.

Item	Epinephelus mori												Mycteroperca bonaci
	%N			%FO			%W			%IRI			%N			%FO			%W			%IRI
	J	A	T	J	A	T	J	A	T	J	A	T	J	A	T	J	A	T	J	A	T	J	A	T
TELEOSTEI	27.94	24.61	26.65	50.94	46.49	48.81	32.47	50.08	43.58	43.70	27.97	38.13	96.43	96.43	96.42	99.15	114.27	104.22	98.34	99.61	99.48	99.79	99.61	99.87
Acanthostracion polygonius Poey, 1876	0.53	-	0.30	0.96	-	0.55	0.58	-	0.23	0.04	-	0.01	-	3.57	1.79	-	4.76	2.12	-	0.05	0.05	-	0.36	0.06
Acanthurus bahianus Castelnau, 1855	-	0.75	0.30	-	1.41	0.55	-	2.11	1.23	-	0.13	0.03	-	-	-	-	-	-	-	-	-	-	-	-
Acanthurus coeruleus Bloch, Schneider, 1801	0.53	-	0.30	0.96	-	0.55	0.42	-	0.17	0.03	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Acanthurus spp.	0.53	1.49	0.91	0.96	2.82	1.67	0.16	7.40	4.39	0.02	0.85	0.33	-	-	-	-	-	-	-	-	-	-	-	-
Aluterus monoceros (Linnaeus, 1758)	-	-	-	-	-	-	-	-	-	-	-	-	-	3.57	1.79	-	4.76	2.12	-	23.59	21.16	-	2.70	0.75
Bleniidae	0.53	-	0.30	0.96	-	0.55	0.07	-	0.03	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Carangidae	-	-	-	-	-	-	-	-	-	-	-	-	3.85	3.57	3.57	3.57	4.76	4.25	6.98	5.57	5.72	0.42	0.91	0.61
Chilomycterus spinosus (Linnaeus, 1758)	0.53	0.75	0.60	0.96	1.41	1.11	1.70	1.86	1.75	0.08	0.12	0.10	-	-	-	-	-	-	-	-	-	-	-	-
Engraulidae	0.53	-	0.30	0.96	-	0.55	0.12	-	0.05	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Gobiidae	0.53	-	0.30	0.96	-	0.55	0.12	-	0.05	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Gymnothorax moringa (Cuvier, 1829)	0.53	-	0.30	0.96	-	0.55	2.39	-	0.94	0.10	-	0.02	-	-	-	-	-	-	-	-	-	-	-	-
Gymnothorax spp.	-	1.49	0.60	-	2.82	1.11	-	13.50	7.89	-	1.43	0.35	-	3.57	1.79	-	4.76	2.12	-	0.71	0.63	-	0.43	0.10
Haemulon aurolineatum Cuvier, 1830	-	-	-	-	-	-	-	-	-	-	-	-	-	17.86	8.93	-	14.29	6.38	-	13.40	12.02	-	9.32	2.06
Halichoeres brasiliensis (Bloch, 1791)	-	-	-	-	-	-	-	-	-	-	-	-	3.57	7.14	5.36	3.85	9.52	6.38	14.46	14.82	14.79	0.73	4.36	1.98
Halichoeres poeyi (Steindachner, 1867)	0.53	-	0.30	0.96	-	0.55	0.22	-	0.09	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Myripristis jacobus Cuvier, 1829	0.53	-	0.30	0.96	-	0.55	2.76	-	1.10	0.11	-	0.03	-	-	-	-	-	-	-	-	-	-	-	-
Ogcocephalus vespertilio (Linnaeus, 1758)	-	0.75	0.30	-	1.41	0.55	-	1.55	0.91	-	0.11	0.02	-	-	-	-	-	-	-	-	-	-	-	-
Ophichthydae	2.65	1.49	2.12	4.81	2.82	3.89	0.20	4.48	2.70	0.51	0.57	0.71	-	-	-	-	-	-	-	-	-	-	-	-
Paraclinus nigripinnis (Steindachner, 1867)	0.53	-	0.30	0.96	-	0.55	0.02	-	0.01	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Scarinae	1.59	2.99	2.12	2.88	5.63	3.89	0.55	4.73	2.98	0.23	1.47	0.75	3.57	3.57	3.57	3.85	4.76	4.25	6.64	0.72	1.32	0.41	0.43	0.32
Scarus spp.	0.53	-	0.30	0.96	-	0.55	0.31	-	0.12	0.03	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Scarus trispinosus Valenciennes, 1840	-	0.75	0.30	-	1.41	0.55	-	0.55	0.32	-	0.06	0.01	3.57	7.15	5.36	3.85	9.52	6.38	12.51	7.04	7.60	0.65	2.82	1.27
Sparidae remains	-	0.75	0.30	-	1.41	0.55	-	0.43	0.25	-	0.05	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Sparisoma spp.	-	-	-	-	-	-	-	-	-	-	-	-	-	3.57	1.79	-	4.76	2.12	-	5.81	5.21	-	0.93	0.23
Synodus spp.	0.53	-	0.30	0.96	-	0.55	2.88	-	1.13	0.12	-	0.30	-	-	-	-	-	-	-	-	-	-	-	-
Unidentified fish	16.81	13.40	15.80	30.77	25.35	28.89	19.97	13.47	17.24	42.33	23.18	35.39	81.87	42.86	62.47	84.03	52.38	68.10	57.75	27.90	30.98	97.58	77.35	92.49
ALGAE
Filamentous algae	-	1.49	0.60	-	2.82	1.11	-	0.10	0.06	-	0.15	0.03	-	-	-	-	-	-	-	-	-	-	-	-
MOLLUSCA
Octopus vulgaris Cuvier, 1797	3.17	1.49	2.42	5.77	2.82	4.45	9.66	0.46	4.07	2.75	0.18	1.09	-	-	-	-	-	-	-	-	-	-	-	-
BIVALVE	-	1.49	0.60	-	2.82	1.11	-	0.12	0.07	-	0.15	0.03	-	-	-	-	-	-	-	-	-	-	-	-
GASTROPODA	1.59	2.99	2.12	2.88	5.63	3.89	0.12	1.51	0.93	0.18	0.85	0.45	-	-	-	-	-	-	-	-	-	-	-	-
ECHINODERMATA
Echinoidea	-	1.49	0.60	-	2.82	1.11	-	2.62	1.53	-	0.39	0.10	-	-	-	-	-	-	-	-	-	-	-	-
CNIDARIA - CORAL	1.59	1.49	1.51	2.88	2.82	2.78	0.29	0.24	0.26	0.20	0.16	0.18	-	-	-	-	-	-	-	-	-	-	-	-
CRUSTACEA	65.71	64.95	65.5	119.23	122.57	118.79	57.46	44.87	49.50	53.17	70.15	59.98	3.57	3.57	3.58	3.85	4.76	4.24	1.66	0.39	0.52	0.21	0.39	0.13
Callinectes spp.	0.53	-	0.30	0.96	-	0.55	0.40	-	0.16	0.03	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Cronius ruber (Lamarck, 1818)	6.88	14.90	9.99	12.50	28.17	18.33	25.37	27.47	26.42	15.02	40.42	26.42	-	-	-	-	-	-	-	-	-	-	-	-
Cycloes bairdii var. atlantica Verrill, 1908	-	0.75	0.30	-	1.41	0.55	-	0.22	0.13	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Family Inachoidinae	0.53	0.75	0.60	0.96	1.41	1.11	0.03	0.22	0.14	0.02	0.04	0.03	-	-	-	-	-	-	-	-	-	-	-	-
Leptopisa setirostris (Stimpson, 1871)	-	0.75	0.30	-	1.41	0.55	-	0.06	0.04	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Lithadia sp.	-	0.75	0.30	-	1.41	0.55	-	0.02	0.01	-	0.03	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Macrocoeloma camptocerum (Stimpson, 1871)	0.53	-	0.30	0.96	-	0.55	0.23	-	0.10	0.02	-	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Majiidae	-	0.75	0.30	-	1.41	0.55	-	0.10	0.06	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Malacostraca - Shrimps remains	3.70	2.99	3.32	6.73	5.63	6.11	0.44	0.40	0.41	1.03	0.64	0.86	-	-	-	-	-	-	-	-	-	-	-	-
Microphrys antillensis Rathbun, 1901	5.82	2.99	4.53	10.58	5.63	8.34	1.71	0.50	0.97	2.96	0.66	1.74	-	-	-	-	-	-	-	-	-	-	-	-
Microphrys spp.	1.06	-	0.60	1.92	-	1.11	0.02	-	0.01	0.07	-	0.02	-	-	-	-	-	-	-	-	-	-	-	-
Mithraculus forceps Milne-Edwards, 1875	6.39	1.49	3.63	9.62	2.82	6.67	2.48	0.49	1.26	3.17	0.19	1.23	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax braziliensis Rathbun, 1892	3.70	0.75	2.42	6.73	1.41	4.45	2.87	0.54	1.44	1.64	0.06	0.65	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax forceps Milne-Edwards 1875	2.65	-	1.51	4.81	-	2.78	2.32	-	0.91	0.89	-	0.25	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax hemphilli Rathbun, 1892	1.06	-	0.60	1.92	-	1.11	0.90	-	0.36	0.14	-	0.04	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax hispidus (Herbst, 1790)	-	2.24	0.92	-	4.23	1.66	-	2.30	1.34	-	0.65	0.14	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax spp.	1.59	-	0.92	2.88	-	1.66	1.00	-	0.40	0.27	-	0.08	-	-	-	-	-	-	-	-	-	-	-	-
Mithrax tortugae Rathbun, 1920	2.12	0.75	1.51	3.85	1.41	2.77	1.79	1.59	1.64	0.56	0.11	0.33	-	-	-	-	-	-	-	-	-	-	-	-
Notolopas brasiliensis Miers, 1886	-	0.75	0.30	-	1.41	0.55	-	0.02	0.01	-	0.03	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Odontodactylus havanensis (Bigelow, 1893)	1.65	2.99	2.8	4.81	5.63	5.00	1.08	0.45	0.70	0.48	0.65	0.65	-	-	-	-	-	-	-	-	-	-	-	-
Panurilus argus Latreille, 1804	0.53	-	0.30	0.96	-	0.55	0.43	-	0.17	0.03	-	0.10	3.57	-	1.79	3.85	-	2.12	1.66	-	0.17	0.21	-	0.06
Parthenope serrata Schmidt, 1857	-	0.75	0.30	-	1.41	0.55	-	0.16	0.09	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Persephona sp.	1.06	-	0.60	1.92	-	1.11	0.59	-	0.23	0.11	-	0.03	-	-	-	-	-	-	-	-	-	-	-	-
Pilumnus dasypodus Kingsley, 1879	-	0.75	0.30	-	1.41	0.55	-	0.09	0.05	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Portunidae remains	1.06	2.24	1.51	1.92	4.23	2.77	3.24	0.42	1.52	0.30	0.38	0.32	-	-	-	-	-	-	-	-	-	-	-	-
Portunus ventralis (Milne-Edwards, 1879)	-	0.75	0.30	-	1.41	0.55	-	0.06	0.03	-	0.04	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Pseudosquilla ciliata (Fabricius, 1787)	2.12	-	1.21	3.85	-	2.22	1.16	-	0.46	0.47	-	0.14	-	-	-	-	-	-	-	-	-	-	-	-
Stenorhynchus seticornis (Herbst, 1788)	1.06	3.73	2.12	1.92	7.04	3.89	0.20	0.65	0.46	0.09	1.04	0.38	-	-	-	-	-	-	-	-	-	-	-	-
Stomatopoda	3.17	2.24	2.8	5.77	4.23	5.00	2.36	0.24	1.07	1.18	0.35	0.718	-	3.57	1.79	-	4.76	2.12	-	0.39	0.35	-	0.39	0.07
Superfamily Dromioidea	-	0.75	0.30	-	1.41	0.55	-	0.47	0.28	-	0.06	0.01	-	-	-	-	-	-	-	-	-	-	-	-
Unidentified Brachyura	15.85	16.41	16.98	28.85	30.99	30.00	6.62	6.33	6.49	24.15	23.87	25.00	-	-	-	-	-	-	-	-	-	-	-	-
Unidentified Decapoda	2.12	2.24	2.42	3.85	4.23	4.44	1.33	1.58	1.50	0.49	0.54	0.65	-	-	-	-	-	-	-	-	-	-	-	-
Xanthidae	0.53	1.49	0.91	0.96	2.82	1.66	0.89	0.49	0.64	0.05	0.19	0.10	-	-	-	-	-	-	-	-	-	-	-	-

Diet of juveniles (60.6% of the stomachs analyzed, mean 43.4 cm; range: 23.2-50 cm TL; SD: ±9.7) was dominated by fish (43.7% IRI) and brachyuran remains (24.1% IRI). Blackpoint sculling crab Cronius ruber (15.0% IRI) was the third most important item (Tab. 1). Diet included several teleosts (e.g. Blackbar soldier fish Myripristis jacobus, spotted moray Gymnothorax moringa and parrotfishes, Scarus spp.), common octopus Octopus vulgaris, shrimps, stomatopods, and a wide variety of decapods (13 species). The diet of adults (39.4% of the stomachs analyzed) was dominated by C. ruber (40.4% IRI), followed by brachyuran (23.8% IRI) and fish remains (23.2% IRI). Seven teleost species were registered as prey of adults, including greenback parrotfish Scarus trispinosus and Scarus spp., the ocean surgeon Acanthurus bahianus, the burrfish Chilomycterus spinosus and the seadevil Ogcocephalus vespertilio. Filamentous algae, bivalve remains, gastropods and echinoderms were also present in low quantities.

The diet of E. morio individuals from the IS was dominated by the portunid (swimming) crab C. ruber (30.5% IRI), followed by fish remains (29.2% IRI), while that of individuals from the OS was dominated by fish (64.9% IRI) and unspecified brachyuran remains (14.3% IRI). In the cold season, the E. morio diet was dominated by C. ruber (53.7% IRI), fish (15.5% IRI) and brachyuran remains (11.4% IRI), while in the warm season the most representative prey were brachyuran (40.3% IRI) and fish remains (31.4% IRI), followed by C. ruber (10.7% IRI).

A total of 162 stomachs from Mycteroperca bonaci (mean 70.9 cm; range: 26.1-147 cm TL; SD: ±24.4) were obtained between May 2005 and September 2012, and only 47 (29.1%) stomachs contained prey items (mean 68 cm; range: 36-117 cm TL; SD: ±20.5). Identifiable prey items included teleosts, stomatopods and Caribbean spiny lobster (Panurilus argus) (Tab. 1). Fish remains (92.4% IRI) were the most important prey category. Collectively, Tomtate grunt Haemulon aurolineatum (2% IRI), Brazilian wrasse Halichoeres brasiliensis (1.9% IRI) and S. trispinosus (1.2% IRI) were the most prevalent identifiable items.

Diet of juveniles (55.3% of the stomachs analyzed) was dominated by fish remains (98.0% IRI) and H. brasiliensis (0.79% IRI) (Tab. 1), besides several species of teleosts (e.g. parrotfish S. trispinosus, Scarinae and jacks represented collectively 1.48% IRI). The diet of adults (44.7% of the stomachs analyzed) was dominated by fish remains (77.3% IRI), followed by H. aurolineatum (9.3% IRI), H. brasiliensis (4.3% IRI), S. trispinosus (2.8% IRI) and unicorn leather jacket filefish Aluterus monoceros (2.7% IRI).

The diet of M. bonaci from the IS was composed by fish remains (97.3% IRI), and fish species more abundant were Acanthurus spp. (1.2% IRI), H. brasiliensis (0.4% IRI) and S. trispinosus (0.35% IRI), while the diet of individuals from the OS was dominated by fish remains (76.4% IRI), H. aurolineatum (9.5% IRI) and H. brasiliensis (4.5% IRI). During the cold season, diet was dominated by fish remains (84.1% IRI), A. monoceros (6.5% IRI) and H. aurolineatum (3.3% IRI), similarly to the warm season, when fish remains (91.5% IRI), H. brasiliensis (2.5% IRI) and H. aurolineatum (2.1% IRI) were the most representative items.

For E. morio several less abundant taxa clustered in the lower left quadrant of the feeding strategy diagram, representing items with low contribution to the diet in terms of prey-specific weight. For juveniles (Fig. 2a), the main prey items were C. ruber, fish remains, brachyuran remains, O. vulgaris, and several decapods (Leptopisa setirostris, Macrocoeloma camptocerum, Mithraculus forceps, Notolopas brasiliensis and Microphrys antillensis). Among adults (Fig. 2b) the dominant identifiable items included Gymnothorax spp., Acanthurus spp. and Scarinae. For M. bonaci juvenile samples the feeding strategy diagram showed a dominance of fish remains in the upper right portion (Fig. 2c), which suggested a more specialized feeding strategy than that of E. morio. This is also supported by the presence of other fish species (S. trispinosus and H. brasiliensis), and also of P. argus in the lower left quadrant. Adult samples of M. bonaci were similar, with presence of A. monocerus and H. aurolineatum (Fig. 2d).

Fig. 2
Feeding strategy diagram incorporating the preys taxa of red (a, b) and black (c, d) groupers and their feeding strategy classification in the Abrolhos Bank for juveniles (a, c) and adults (b, d). Images of select items are offset to the right of symbols for visual interpretation. Abbreviations: Cr= Cronius ruber; Fr= Fishes remains; Br= Brachyura remains; Gy= Gymnotorax spp.; Ac= Acanthurus spp.; Ov= Octopus vulgaris; St= Scarus trispinosus; Sr= Scaridae remains; Pa= Panurilus argus; Hb= Halichoeres brasiliensis; Ha= Haemulon aurolineatum; Am= Aluterus monocerus.

The diet of the red and black groupers was significantly influenced by body size and habitat (PERMANOVA P=0.001 and P=0.015, respectively; Tab. 2). We also found significant dietary differences in pairwise comparisons between cross shelf strata (PERMANOVA, P= 0.026) and species/stages of juvenile and adult E. morio (PERMANOVA, P= 0.011), juvenile E. morio and M. bonaci (PERMANOVA, P= 0.001), adult E. morio and juvenile M. bonaci (PERMANOVA, P= 0.001) and adult E. morio and M. bonaci (PERMANOVA, P= 0.016). Fish as prey were the main contributors to the dietary dissimilarities between species, with a greater importance for M. bonaci diet (Tab. 3). SIMPER analyses showed that fish remains (23.86%), C. ruber (12.18%) and brachyura remains (11.5%) (Tab. 4), where the main contributions to the dietary dissimilarities between IS and OS cross-shelf strata.

Tab. 2
Results from two-way crossed PERMANOVA of red and black grouper diet data. df = Degree of freedom, SS = sum of squares, MS = mean squares.

PERMANOVA
Source	df	SS	MS	Pseudo-F	P(perm)	Unique perms
Habitat	1	8086.2	8086.2	1.9322	0.015	998
Species/stages	3	51555	17185	4.1063	0.001	998
Season	1	5243.7	5243.7	1.253	0.211	999
Habitat X Species/stages	3	12000	4000	0.95578	0.511	997
Habitat X Season	1	3224.1	3224.1	0.77039	0.704	999
Species/stages X Season	3	10017	3338.9	0.79782	0.839	997
Habitat X Species/stages X Season	2	3294.8	1647.4	0.39364	0.997	999
Res	212	8.8723E5	4185
Total	226	9.8641E5

Tab. 3
Results from two-way crossed similarity of percent (SIMPER) analyses for significant species/stage effects. Species contributions that summed cumulatively to >75% are shown. Juv = Juvenile, Av.Abund = Average abundance, Av.Diss = Average dissimilarity, Diss/SD = Dissimilarity Standart Deviation.

Average dissimilarity= 89.16	E. morio Juv	M. bonaci Juv
Taxon	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contribution %	Cumulative %
Fish remains	0.45	0.87	27.27	1.23	30.58	30.58
Brachyura remains	0.25	0.00	8.40	0.51	9.42	40.01
Cronius ruber	0.32	0.00	8.01	0.36	8.99	49.00
Acanthurus spp.	0.01	0.23	5.95	0.32	6.67	55.67
Average dissimilarity= 92.01	E. morio Juv	E. morio Adult
Taxon	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contribution %	Cumulative %
Fish remains	0.32	0.64	17.90	0.69	19.45	19.45
Cronius ruber	0.45	0.49	13.93	0.64	15.15	34.60
Brachyura remains	0.25	0.37	10.91	0.71	11.86	46.45
M. antillensis	0.08	0.05	3.38	0.38	3.68	50.13
Average dissimilarity= 90.82	E. morio Adult	M. bonaci Adult
Taxon	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contribution %	Cumulative %
Fish remains	0.49	1.55	28.98	1.11	31.91	31.91
Brachyura remains	0.37	0.00	6.54	0.46	7.20	39.11
Cronius ruber	0.64	0.00	5.11	0.36	5.63	44.74
Haemulon aurolineatum	0.00	0.52	4.78	0.34	5.26	50.00
Average dissimilarity= 93.76	E. morio Adult	M. bonaci Juv
Taxon	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contribution %	Cumulative %
Fish remains	0.49	0.87	24.05	1.12	25.66	25.66
Cronius ruber	0.64	0.00	15.70	0.56	16.74	42.40
Brachyura remains	0.37	0.00	9.26	0.50	9.88	52.28

Tab. 4
Results from two-way crossed dissimilarity of percent (SIMPER) analyses for significant Habitat effects. Species contributions that summed cumulatively to >75% are shown. Av.Abund = Average abundance, Av.Diss = Average dissimilarity, Diss/SD = Dissimilarity Standart Deviation.

Average dissimilarity= 90.87	Inner-shelf	Outer-shelf
Taxon	Av.Abund	Av.Abund	Av.Diss	Diss/SD	Contribution %	Cumulative %
Fish remains	0.49	1.05	21.68	0.86	23.86	23.86
Cronius ruber	0.44	0.06	11.07	0.50	12.18	36.04
Brachyura remains	0.26	0.18	10.45	0.63	11.50	47.54
Cycloes bairdii var. atlantica	0.00	0.04	2.72	0.22	3.00	50.54

Discussion

Several stomachs of both species caught by hook and line, longline and spear fishing were empty. Despite the fact that some fish species regurgitated their prey(s) after capture, as already stated for some large-fish species (Randall, 1967), including groupers (Randall, Brock, 1960; Nakai et al., 2001; Dierking, Meyer, 2009), we suspect that epinephelids regularly experience long periods of empty stomachs (e.g.Condini et al., 2011; López, Orvay, 2005; Reñones et al., 2002), as a combined result of resource availability, digestion rates and energy balance (Arrington et al., 2002). Both species are opportunistic (Smith, 1971; Randall, 1967; Sierra et al., 2001), “sit and wait” ambush predators (Bullock, Smith, 1991; Brulé et al., 2005), and the regular occurrence of empty stomachs provides support to the idea that they are intermittent rather than continuous feeders.

Decapods and fishes were the main food items of E. morio, while fishes were the main prey of M. bonaci in the Abrolhos Bank. This pattern corroborates previous studies in the Northern Hemisphere (Gulf of Mexico and Caribbean), where red groupers also feed on brachyurans, stomatopods, molluscs, and small fishes (Randall, 1967; Moe, 1969; Brulé, Canché 1993; Brulé et al., 1994), while black groupers feed mainly on fishes, and secondarily on crustaceans (Brulé et al., 2005). Results were consistent with the notion that both species are important mesocarnivores on West Atlantic reefs (Randall, 1967; Parrish, 1987; Sierra et al., 2001).

The diet of red grouper changed significantly with size. Smaller individuals fed almost preferentially on crustaceans (especially Cronius ruber and brachyurans generally), and also on a wide range of rare items including teleosts, decapods, octopuses, shrimps, and stomatopods. Reef fragments and filamentous algae were recorded in small quantities and most probably represent accidental ingestion during predation (Linde et al., 2004; Brulé et al., 1994; Machado et al., 2008). Cronius ruber and brachyuran remains were also important components of the adult diet. Studies in the Northern Hemisphere (Brulé, Canché, 1993 - 12.1 to 40 cm TL; Brulé et al., 1994 - 13 to 36 cm FL) also recorded such a preference for crustaceans and mollusks in addition to small fishes by juveniles, even considering size-related differences among previous studies.

The increased consumption of fishes by larger individuals may represent a general trend in groupers (Smith, 1971; Brulé, Canché, 1993), and also for other large carnivorous reef fishes (Sierra et al., 2001; Linde et al., 2004), observations already noted for mutton snapper and goliath grouper on Abrolhos Bank (Freitas et al., 2011b, 2015). Such ontogenetic trend is clear for the more generalist red grouper, and is aligned with optimal foraging theory, i.e. maximum energetic return obtained when predator selects high quality prey (Gerking, 1994). Besides reducing the competition for food, or even meeting the higher energetic demand from migration and reproduction (Gerking, 1994; Sierra et al., 2001), ontogenetic shifts in diet are often accompanied by shifts in habitat (Sierra et al., 2001), possibly contributing to reduced niche overlap (Machado et al., 2008).

Red grouper juveniles (20-40 cm) are commonly found in crevices and under ledges in 5-25 m depths, in the inner and mid shelf. At 40-50 cm adults migrate to deeper water (50-300m), where they also occur over sandy or mud bottoms (Craig et al., 2011). The juvenile habitat for black grouper appears to vary geographically. Juvenile habitat in the Yucatán Peninsula mainly consists of sandy-rocky bottoms with some ridges and crevices (Renán et al., 2003) while in the north Atlantic and Gulf of Mexico it is largely seagrass beds in estuarine areas and on coral reefs (Bullock, Smith, 1991; Sluka et al., 1994; Ross, Moser, 1995). In our study, juveniles of E. morio and M. bonaci came from exclusively the IS while the adults mostly came from the OS. This pattern suggests that E. morio and M. bonaci exhibit size segregation according to depth, showed to dog snapper Lutjanus jocu (Bloch, Schneider, 1801), mutton snapper Lutjanus analis (Cuvier, 1828), goliath grouper Epinephelus itajara (Lichtenstein, 1822) and Cephalopholis fulva (Linnaeus, 1758), another carnivorous fish in Abrolhos Bank (Freitas et al., 2011a, 2015; Moura et al., 2011; Gathaz et al., 2013), and as noted by Moe (1969) for the Gulf of Mexico, and by González et al. (1974) and Valdés, Padrón (1980) at the Campeche Bank, Mexico. On the IS, juveniles of both species inhabited chapeirões, reef structures with a characteristic mushroom-shaped form, clustered at depths of 5 to 25m. This could explain the high occurrence of crustaceans in red grouper diet and reef fishes in black grouper diet in this particular reef habitat, because such structures increase the heterogeneity and complexity of habitat types (Dutra et al., 2005). In contrast, middle and outer shelf habitats comprise a much larger realm of mesophotic reefs, rhodolith beds, and fleshy algal pavement (Moura et al., 2013) in depths from 25-90 m. While the two groupers rely on many of the same prey types, coexistence may be facilitated by E. morio feeding more heavily on crustaceans, particularly C. ruber, while black grouper take comparatively few crustaceans but lots of fish prey. Furthermore, prey captured by young red grouper are generally slow-moving benthic species (principally decapods) while those consumed by black grouper are less bottom-dependent, and faster-moving organisms (reef-fishes) (Brulé et al., 2005), featuring a pattern similar to E. itajara, on Abrolhos (Freitas et al., 2015).

The annual rhythm of fish feeding intensity is strongly associated with environmental conditions and their effect on the food supply (John, 2001; Sierra et al., 2001). Feeding habits and diet composition of reef fishes are usually highly variable, in part because prey availability change seasonally (e.g. Roos, Moser, 1995; Monteiro et al., 2009; Pimentel, Joyeux, 2010). The lack of dietary temporal variation in this study (i.e. no significant seasonal variation in diet composition to E. morio and M. bonaci) is consistent with the results of Brulé et al. (1994, 2005) and others groupers (John, 2001) and we believe that the absence of major seasonal differences (e.g. mean and seasonal changes in SST) may explain our results. In fact, SST’s along the Abrolhos Bank are very homogeneous over the year, with fluctuations not exceeding 4ºC (see Freitas et al., 2011b).

Red and black groupers from Abrolhos Bank did not feed heavily on other species that are commercial harvested. Their diet is likely most influenced by variation in prey availability and diversity in different areas. In marine ecosystems, trophic cascades have been observed in hard bottom environments such as coral reefs (Pinnegar et al., 2000). Predators like E. morio and M. bonaci could trigger indirect effects in the community (e.g. Heithaus et al., 2008, 2010; Ferretti et al., 2010) and influence a large range of ecological processes (Babcock et al., 1999; Pinnegar et al., 2000; Willis, Anderson, 2003; Silveira et al., 2015), such as linkages between top and intermediate predators, and intermediate predators and their resources (Pace et al., 1999). For example, the high consumption of scarines, by both M. bonaci and E. morio, illustrate how these groupers could have a controlling role in the abundance of parrotfishes, which in turn play key roles as grazers and sand producers on coral reefs.

Acknowledgments

We thank Juliane Cebola, Guilherme Dutra, Danilo Araújo, Eduardo Camargo and Danieli Nobre (Conservation International) for help in the field and Gisleine Hoffman (GPIC/UFPR) for help in stomach analysis. We also acknowledge the fisher folks from the Extractive Reserves of Corumbau and Cassurubá for the continued support to our fieldwork, and the Colônias dos Pescadores (Fishing Guilds) from Prado, Alcobaça, Caravelas and Nova Viçosa. Financial support was provided by the Gordon and Betty Moore Foundation/Conservation International, Conservation Leadership Programme (Project ID: F024801), FUNBIO (Pró-Arribada), CNPq (SISBIOTA RedeAbrolhos, PELD Abrolhos - abrolhos.org), CAPES (grant 8938/11-3 to MOF) and FAPERJ (grant to RLM).

References

• Amaral ACZ, Rizzo AE, Arruda EP. Manual de identificação dos invertebrados marinhos da região Sudeste-Sul do Brasil. São Paulo: EDUSP; 2006.
• Amundsen PA, Gabler HM, Staldvik FJ. A new approach to graphical analysis of feeding strategy from stomach contents data - modification of the Costello (1990) method. J Fish Biol. 1996; 48(4):607-14.
• Arrington DA, Winemiller KO, Loftus WF, Akin S. How often do fishes “run on empty”? Ecology. 2002; 83(8):2145-51.
• Babcock RC, Kelly S, Shears NT, Walker JW, Willis TJ. Changes in community structure in temperate marine reserves. Mar Ecol Prog Ser. 1999; 189:125-34.
• Bastos AC, Moura RL, Amado-Filho GM, D’agostini DP, Secchin NA, Francini-Filho RB, Güth AZ, Sumida PYG, Mahiques MM, Thompson FL. Buracas: Novel and unusual sinkhole-like reef structures in the Abrolhos Bank. Cont Shelf Res. 2013; 70:118-25.
• Bouchon-Navaro Y. Partitioning of food and space resources by chaetodontid fishes on coral reefs. J Exp Mar Biol Ecol. 1986; 103(1-3):21-40.
• Bowen SH. Quantitative description of the diet. In: Murphy BR, Willis DW, editors. Fisheries techniques. Bethesda: American Fisheries Society; 1996. p.513-532.
• Brulé T, Avila DO, Crespo MS, Déniel C. Seasonal and diel changes in diet composition of juvenile red grouper (Epinephelus morio) from Campeche Bank. Bull Mar Sci. 1994; 55(1):255-62.
• Brulé T, Canché LGR. Food habits of juvenile red groupers, Epinephelus morio (Valenciennes, 1828), from Campeche Bank, Yucatan, Mexico. Bull Mar Sci . 1993, 52(2):772-79.
• Brulé T, Puerto-Novelo E, Pérez-Díaz E, Renán-Galindo X. Diet composition of juvenile black grouper (Mycteroperca bonaci) from coastal nursery areas of the Yucatán peninsula, Mexico. Bull Mar Sci . 2005; 77(3):441-52.
• Bueno E. Capitães do Brasil. Rio de Janeiro: Objetiva; 1999.
• Bullock LH, Smith GB. Seabasses (Pisces: Serranidae). St. Petersburg: Florida Department of Natural Resources; 1991. (Memoirs of the Hourglass Cruises, vol 8).
• Burgos JM, Sedberry GR, Wyanski DM, Harris PJ. Life history of red grouper (Epinephelus morio) off the coast of North Carolina and South Carolina. Bull Mar Sci . 2007; 80(1):45-65.
• Campbell SJ, Perdede ST. Reef fish structure and cascading effects in response to artisanal effects in response to artisanal fishing pressure. Fish Res. 2006; 79(1-2):75-83.
• Clarke KR, Gorley RN. PRIMER v. 5 - User manual/ tutorial. Plymouth: PRIMER-E; 2001.
• Clarke RD. Habitat distribution and species diversity of chaetodontid and pomacentrid fishes near Bimini, Bahamas. Mar Biol. 1977; 40(3):277-89.
• Claro R, Lindeman KC, Parenti LR. Ecology of the marine fishes of Cuba. Washington: Smithsonian Institution Press; 2001.
• Condini MV, Seyboth E, Vieira JP, Garcia AM. Diet and feeding strategy of the dusky grouper Mycteroperca marginata (Actinopterygii: Epinephelidae) in a man-made rocky habitat in southern Brazil. Neotrop Ichthyol. 2011; 9(1):161-68.
• Cortés E. Standardized diet compositions and trophic levels of sharks. ICES J Mar Sci. 1999; 56:707-17.
• Crabtree RE, Bullock LH. Age, growth, and reproduction of black grouper, Mycteroperca bonaci, in Florida waters. Fish Bull. 1998; 96(4):735-53.
• Craig MT, Mitcheson YJS, Heemstra PC. Groupers of the World: A Field and Market Guide. Grahamstown: CRC Press; 2011.
• Davies TJ, Meiri S, Barraclough TG, Gittleman JL. Species co-existence and character divergence across carnivores. Ecol Lett. 2007; 10(2):146-52.
• Dierking J, Meyer AL. Prey regurgitation in the grouper Cephalopholis argus J Appl Ichthyol. 2009; 25:600-02.
• Dulvy NK, Freckleton RP, Polunin NVC. Coral eef cascades and the indirect effects of predator removal by exploitation. Ecol Lett . 2004; 7(5):410-16.
• Dutra GF, Allen GR, Werner T, McKenna SA. A Rapid Marine Biodiversity Assessment of the Abrolhos Bank, Bahia, Brazil. Washington: Conservation International; 2005. (RAP Bulletin of Biological Assessment, 38).
• Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK. Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett . 2010; 13(8):1055-71.
• Francini-Filho RB, Moura RL. Evidence for spillover of reef fishes from a no-take marine reserve: An evaluation using the before-after control-impact (BACI) approach. Fish Res . 2008a; 93(3):346-56.
• Francini-Filho RB, Moura RL. Dynamics of fish assemblages on coral reefs subjected to different management regimes in the Abrolhos Bank, eastern Brazil. Aquatic Conservation: Mar Fresh Ecosyst. 2008b; 18(7):1166-79.
• Freitas MO. Auto-ecologia de Epinephelus morio e Mycteroperca bonaci: epinefelídeos comercialmente importantes e ameaçados no Banco dos Abrolhos. [PhD Thesis]. Curitiba, PR: Universidade Federal do Paraná; 2014.
• Freitas MO, Abilhoa V, Giglio VL, Hostim-Silva M, Moura RL, Francini-Filho RB, Minte-Vera CV. Diet and reproduction of the goliath grouper Epinephelus itajara in eastern Brazil. Acta Ichthyol Piscat. 2015; 45(1):1-11.
• Freitas MO, Abilhoa V, Silva GHC. Feeding ecology of Lutjanus analis (Teleostei: Lutjanidae) from Abrolhos Bank, Eastern Brazil. Neotrop Ichthyol . 2011a; 9(2):411-18.
• Freitas MO, Moura RL, Francini-Filho RB, Minte-Vera CV. Spawning patterns of commercially important reef fishes (Lutjanidae and Serranidae) in the tropical Western South Atlantic. Sci. Mar. 2011b; 75(1):135-46.
• Gathaz JR, Goitein R, Freitas MO, Bornatowski H, Moura RL. Diet of Cephalopholis fulva (Perciformes: Serranidae) in the Abrolhos Bank, Northeastern Brazil. Braz J Aquat. Sci Technol. 2013; 17(1):61-63.
• Gerking SD. Feeding ecology of fish. San Diego: Academic Press; 1994.
• Gibran FZ. Activity, habitat use, feeding behavior, and diet of four sympatric species of Serranidae (Actinopterygii: Perciformes) in southeastern Brazil. Neotrop Ichthyol . 2007; 5(3):387-98.
• Gladfelter WB, Johnson WS. Feeding niche separation in a guild of tropical reef fishes (Holocentridae). Ecology. 1983; 64(3):552-63.
• González PD, Zupanovic S, Ramis HE. Biologia pesquera de la Cherna americana del banco de Campeche. Rev Invest Mar. 1974; 1:107-11.
• Heemstra PC, Randall JE. Groupers of the world (Family Serranidae, Subfamily Epinephelinae) - An annotated and illustrated catalogue of the grouper, rockcod, hind, coral grouper and lyretail species known to date. Rome: FAO; 1993. (FAO species catalogue, vol 16).
• Heithaus MR, Frid A, Vaudo JJ, Worm B, Wirsing AJ. Unraveling the ecological importance of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR, editors. Biology of sharks and their relatives II. Boca Raton: CRC Press; 2010. p. 611-637.
• Heithaus MR, Frid A, Wirsing AJ, Worm B. Predicting ecological consequences of marine top predator declines. Trends Ecol Evol. 2008; 23(4):202-10.
• Hixon MA, Beets JP. Predation, prey refuges, and the structure of coral-reef fish assemblages. Ecol Monogr. 1993; 63(1):77-101.
• Hixon MA. Competitive Interactions between California reef fishes of the genus Embiotoca Ecology. 1980; 61(4):918-31.
• Hixon MA. Predation as a process structuring coral-reef fish communities. In: Sale PF, editor. The Ecology of Fishes on Coral Reefs. San Diego: Academic Press ; 1991. p. 475-508.
• Huntsman GR, Potts J, Mays RW, Vaughan D. Groupers (Serranidae, Epinephelinae): Endangered Apex Predators of Reef Communities. Amer Fish Soc Symp. 1999; 23:217-31.
• Hyslop EJ. Stomach contents analysis - a review of methods and their application. J Fish Biol . 1980; 17(4):411-29.
• John JS.Temporal variation in the diet of a coral reef piscivore (Pisces: Serranidae) was not seasonal. Coral Reefs. 2001; 20(2):163-70.
• Jones RS. Ecological relationships in Hawaiian and Johnston Island Acanthuridae (Surgeonfishes). Micronesica. 1968; 4(2):309-61.
• Larson RJ. Competition, habitat selection and the bathymetric segregation of two rockfish (Sebastes) species. Ecol Monogr . 1980; 50(2):221-39.
• Linde M, Grau AM, Riera F, Massutí-Pascual E. Analysis of trophic ontogeny in Epinephelus marginatus (Serranidae). Cybium. 2004; 28(1):27-35.
• López VG, Orvay FC. Food habits of groupers Epinephelus marginatus (Lowe, 1834) and Epinephelus costae (Steindachner, 1878) in the Mediterranean Coast of Spain. Hidrobiológica. 2005; 15(1):27-34.
• Machado LF, Daros FAML, Bertoncini AA, Hostim-Silva M, Barreiros JP. Feeding strategy and trophic ontogeny in Epinephelus marginatus (Serranidae) from Southern Brazil. Cybium . 2008; 32(1):33-41.
• Melo GAS. Manual de identificação dos Brachyura (Caranguejos e Siris) do litoral brasileiro. São Paulo: Plêiade/FAPESP; 1996.
• Moe MA. Biology of the red grouper, Epinephelus morio (Valenciennes) from the eastern Gulf of Mexico. San Petersburg: Florida Department of Natural Ressources, Marine Research Laboratory; 1969. (Professional Papers Series, vol 10).
• Monteiro DP, Giarrizzo T, Isaac V. Feeding ecology of juvenile dog snapper Lutjanus jocu (Bloch and Shneider, 1801) (Lutjanidae) in intertidal mangrove creeks in Curuçá Estuary (Northern Brazil). Braz Arch Biol Technol. 2009; 52(6):1421-30.
• Moura RL, Francini-Filho RB, Chaves EM, Minte-Vera CV, Lindeman KC. Use of riverine through reef habitat systems by dog snapper (Lutjanus jocu) in eastern Brazil. Estuar Coast Shelf Sci. 2011; 95(1): 274-78.
• Moura RL, Secchin NA, Amado-Filho GM, Francini-Filho RB, Freitas MO, Minte-Vera CV, Teixeira JB, Thompson FL, Dutra GF, Sumida PYG, Guth AZ, Lopes RM, Bastos AC. Spatial patterns of benthic megahabitats and conservation planning in the Abrolhos Bank. Cont Shelf Res . 2013; 70:109-17.
• Nakai T, Sano M, Kurokura H. Feeding habits of the darkfin hind Cephalopholis urodeta (Serranidae) at Iriomote Island, southern Japan. Fish Sci. 2001; 67(4):640-43.
• Pace ML, Cole JG, Carpenter SR, Kitchell JF. Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol . 1999; 14(12):483-88.
• Parrish JD. The trophic biology of snappers and groupers. In: Polovina JJ, Ralston S, editors. Tropical snappers and groupers: biology and fisheries management. Boulder: Westview Press; 1987. p. 405-463.
• Pianka ER. The structure of lizard communities. Annu Rev Ecol Syst. 1973; 4:53-74.
• Pimentel CR, Joyeux JC. Diet and food partitioning between juveniles of mutton Lutjanus analis, dog Lutjanus jocu and lane Lutjanus synagris snappers (Perciformes: Lutjanidae) in a mangrove-fringed estuarine environment. J Fish Biol . 2010; 76(10):2299-317.
• Pinkas L, Oliphant MS, Iverson ILK. Food habits of albacore, bluefin tuna, and bonito in California waters. Fish Bull , 1971; 152:1-105.
• Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazzo M, Zabala M, D’Anna G, Pipitone C. Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv. 2000; 27(2):179-200.
• Pratchett MS. Dietary overlap among coral-feeding butterfly fishes (Chaetodontidae) at Lizard Island, northern Great Barrier Reef. Mar Biol . 2005; 148(2):373-82.
• Randall JE. Food habits of reef fishes of the West Indies. Stud Trop Oceanogr. 1967; 5:665-847.
• Randall JE, Brock VE. Observations on the biology of epinepheline and lutjanid fishes of the Society Islands, with emphasis on food habits. Trans Am Fish Soc. 1960; 89(1):9-16.
• Renán X, Cervera-Cervera K, Brulé T. Probable nursery areas for juvenile groupers along the northern coast of the Yucatán Peninsula, Mexico. Gulf Caribbean Fish Inst. 2003; 54:496-505.
• Reñones O, Polunin NVC, Goni R. Size related dietary shifts of Epinephelus marginatus in a western Mediterranean littoral ecosystem: an isotope and stomach content analysis. J Fish Biol . 2002; 61(1):122-37.
• Rizzari JR, Frisch AJ, Hoey AS, McCormick MI. Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos. 2014; 123(7):829-36.
• Silveira CB, Silva-Lima AW, Francini-Filho RB, Marques JSM, Almeida MG, Thompson CC, Rezende CE, Paranhos R, Moura RL, Salomon PS, Thompson FL. Microbial and sponge loops modify fish production in phase-shifting coral reefs. Environ Microbiol. 2015; 17(10):3832-46.
• Ross SW, Moser ML. Life history of juvenile gag Mycteroperca microlepis, in North Carolina estuaries. Bull Mar Sci . 1995; 56(1):222-37.
• Ross ST. Resource Partitioning in Fish Assemblages: A Review of Field Studies. Copeia. 1986; 1986(2):352-88.
• Sala E, Ballesteros E. Partitioning of space and food resources by three fish of the genus Diplodus (Sparidae) in a Mediterranean rocky infralittoral ecosystem. Mar Ecol Progr Ser. 1997; 152:273-83.
• Schoener TW. Resource partitioning in ecological communities. Science. 1974; 185(4145):27-39.
• Segal B, Evangelista H, Kampel M, Gonçalves AC, Polito PS, Santos EA. Potential impacts of polar fronts on sedimentation processes at Abrolhos coral reef (South-West Atlantic Ocean/Brazil). Cont Shelf Res . 2008; 28(4-5):533-44.
• Shpigel M, Fishelson L. Habitat partitioning between species of the genus Cephalopholis (Pisces, Serranidae) across the fringing reef of the Gulf of Aqaba (Red Sea). Mar Ecol Progr Ser . 1989; 58:17-22.
• Sierra LM, Claro R, Popova OA. Trophic biology of the marine fishes of Cuba. In: Claro R, Lindeman KC, Parenti LR, editors. Ecology of the Marine Fishes of Cuba. Washington and London: Smithsonian Institution Press; 2001. p.115-148.
• Sluka R, Chiappone M, Sullivan KM. Comparison of juvenile grouper populations in southern Florida and the central Bahamas. Bull Mar Sci . 1994; 54(3):871-80.
• Smith CL, Tyler JC. Space resource sharing in a coral reef fish community. Bull Nat Hist Mus Los Angeles. 1972; 14:125-70.
• Smith CL. A revision of the American groupers: Epinephelus and allied genera. Bull Amer Mus Nat Hist. 1971; 146:69-241.
• Valdés E, Padrón G. Pesquerias de palangre. Rev Cub Invest Pesq. 1980; 5(2):38-52.
• Willis TJ, Anderson MJ. Structure of cryptic reef fish assemblages: relationships with habitat characteristics and predator density. Mar Ecol Progr Ser . 2003; 257:209-21.

Publication Dates

• Publication in this collection
  2017

History

• Received
  19 Apr 2016
• Accepted
  17 Apr 2017