ACTIVITY, HABITAT UTILIZATION, FEEDING BEHAVIOUR, AND DIET OF THE SAND MORAY Gymnothorax ocellatus (ANGUILLIFORMES, MURAENIDAE) IN THE SOUTH WESTERN ATLANTIC Flávia Borges Santos* and Ricardo M. C. Castro** Biota Neotropica v3 (n1) – http://www.biotaneotropica.org.br/v3n1/pt/abstract?article+BN00103012003 Date Received 10/18/2002 Revised 01/13/2003 Accepted 03/07/2003 Departamento de Zoologia, Instituto de Biociências - Universidade de São Paulo, CP 11461, 05422-970 São Paulo, São Paulo, Brazil. (http://www.ib.usp.br) *Author to whom correspondence should be addressed. Tel:+55-11-3091-7511; fax:+55-19-3232-1745; e-mail: [email protected] **Laboratório de Ictiologia de Ribeirão Preto (LIRP), Departamento de Biologia, FFCLRP-Universidade de São Paulo, Av. Bandeirantes 3900, 14040-901 Ribeirão Preto, São Paulo, Brazil, e-mail: [email protected] Abstract Activity, habitat utilization, feeding behaviour, and diet of the sand moray Gymnothorax ocellatus (Anguilliformes, Muraenidae) in the South western Atlantic. The sand moray Gymnothorax ocellatus is a nocturnal predator from the western South Atlantic that actively forages on the bottom, preying mostly on crustaceans (mainly shrimps and crabs) and ray-finned fishes, which are located primarily by the sense of smell. The individuals stay stationary during the day, almost always being hidden in individual tunnels dug by animals other than the morays in the muddy sand bottom. Key words: Muraenidae; Gymnothorax ocellatus; habitat use; feeding behaviour; diet. Resumo Atividade, utilização do habitat, comportamento alimentar, e dieta da moréia-de-areia Gymnothorax ocellatus (Anguilliformes, Muraenidae) no Atlântico sudoeste. A moréia-de-areia Gymnothorax ocellatus é um predador noturno do Atlântico ocidental que forrageia ativamente o fundo, predando principalmente crustáceos (em especial camarões e siris) e peixes actinopterígios, os quais são localizados principalmente pelo olfato. Os indivíduos permanecem inativos durante o dia, quase sempre escondidos em túneis individuais escavados por outros animais, que não moréias, em substrato areno-lodoso. Palavras-chave: Muraenidae; Gymnothorax ocellatus; utilização do habitat; comportamento alimentar; dieta. http://www.biotaneotropica.org.br Santos, F. B. & Castro, R. M. C. - Biota Neotropica, v3, n1 - BN00103012003 2 1. INTRODUCTION edge may be due to the flat, turbid water sites occupied by Moray-eels of the family Muraenidae are specialized the sand moray, which are unappealing to divers. This ar- secretive and largely nocturnal reef-dwelling predators, ticle provides the first published information on the activity which typically hunt fish and crustaceans deep in rock crev- period, spatial distribution, habitat use, feeding behavior ices (Lowe-McConnell 1987, Böhlke & Chaplin 1993, Randall and diet of G. ocellatus on a coastal stretch of the State of 1996). The prey is located primarily by smell, and some mo- São Paulo, southeastern Brazil. ray species are known to use a knotting behavior to break up large prey items (Miller, 1987, 1989). The muraenid genus 2. MATERIAL AND METHODS Gymnothorax has a worldwide distribution and is repre- sented by five species off the southeastern coast of Brazil: G. funebris Ranzani, 1839, G. moringa (Cuvier 1829), G. 2.1. STUDY SITE vicinus (Castelnau 1855), G. conspersus Poey, 1867, and G. The field observation were carried out monthly from ocellatus Agassiz, 1831 (Figueiredo & Menezes 1978, May 1996 to May 1998, in a 12.5 km stretch of the continen- Böhlke et al. 1989). The first three Gymnothorax species are tal margin of the São Sebastião Channel, south-eastern Bra- associated with coral or rock reefs, whereas the sand moray zil (Fig. 1). Underwater activities were conducted within an G. ocellatus is associated with gravel, sand, or mud sub- approximately pentagonal open bottom area 0.5-5 m deep in strates of open sedimentary bottoms (Figueiredo & Menezes front of the 50 m long Cabelo Gordo beach (23º49’30" S, 1978, Carvalho-Filho 1999), and G. conspersus is a poorly 45º25’18" W). The study area was limited by the surf line, known species living below 200 m (Böhlke & Böhlke 1980). the two bordering rocky shores and three tethered floating The biology of the central and south west Atlantic markers. This site is characterized by a muddy sand sub- morays dwelling in clear water reefs is relatively well known strate (71.7-90.4% sand, 4.3-19.4% silt and 5.3-8.9% clay) (e. g., Bardach et al. 1959, Bardach & Loewenthal 1961, Dubin and the occurrence of green seagrass Halodule wrightii. 1982, Abrams & Schein 1986). However very little is known During the study period, water temperature at the surface about the biology of G. ocellatus, an abundant species over varied 17.4-24.2º C (average 21.5º C) and horizontal trans- mud/sand bottoms (Carvalho-Filho 1999). This lack of knowl- parency of water, measured with a Secchi disk, varied 0.85- 1.9 m (average 1.4 m). Fig. 1. Position of the study site in the Brazilian coast. http://www.biotaneotropica.org.br Santos, F. B. & Castro, R. M. C. - Biota Neotropica, v3, n1 - BN00103012003 3 2.2. PROCEDURE 3. RESULTS The 66 examined specimens were collected on muddy sand bottoms shallower than 13 m using hook-and-line baited 3.1. ACTIVITY PERIOD with sardines (n=64, 97%), a nylon beach seine (n=1, 1.5%) and a hand net during scuba dives (n=1, 1.5%). The speci- Thirty eight (48.7%) sightings of G. ocellatus oc- mens were fixed in 10% formalin on capture and latter trans- curred during daytime, when the individuals were hiding ferred to ethanol 70%. Voucher specimens (LIRP 2281-2303) within shelters (n=36, 94.7%) (Fig. 1), swimming (n=1, 2.6%) were deposited in the fish collection of the Laboratório de or eating offered baits (n=1, 2.6%). Thirty seven (47.4%) Ictiologia de Ribeirão Preto (LIRP), at the FFCLRP- sightings occurred at night, when individuals were hiding Universidade de São Paulo, São Paulo, Brazil. within shelters (n=13, 35.1%), swimming (n=6, 16.2%), search- ing for prey (n=2, 5.4%), eating offered baits (n=12, 32.4%), A total of 91 hours of underwater observations were or feeding or trying to feed on live crustaceans and fish made during scuba (85 h) and skin diving (6 h) over bottoms (n=4, 10.8%). During the three (3.8%) sightings recorded at 5 meters deep or shallower. Data on activity period, habitat twilight, the individuals were swimming between the sunset use, and feeding behavior were obtained during 51 diurnal, time and 1 h after it (n=1, 33.3%), and entering shelters be- 27 nocturnal and 13 crepuscular observation hours, distrib- tween sunrise time and 1 h after it (n=2, 66.6%). uted throughout the 24-h cycle (daytime is defined here as the period between the end of sunrise and beginning of sunset and night as the period between the end of sunset 3.2. SPATIAL DISTRIBUTION AND HABITAT and the beginning of sunrise). During the observational USE sessions ad libitum and focal animal sampling were used All 78 sightings of G. ocellatus were between depths (Altmann 1974, Lehner 1996). During each dive the number of 1.5-3.5 m on muddy sand open bottom with seagrass, of observed G. ocellatus individuals was recorded together Halodule wrightii, an isolated group of three boulders and with the type of substrate on which they were found and a variable number of small patches of debris discarded from also the type of shelter used during inactivity periods. Ac- recreational and fishing boats. On no occasion G. ocellatus tivity was assessed based on food searching behavior, and was seen associated with adjacent rocky habitats. mobility was categorized as follows: stationary while total or partially hidden, laterally undulating immediately over Sand morays were recorded hidden total or partially the bottom, with the body vertical axis perpendicular to the within shelters during the day (94.7%, n=36) and at night bottom or with the specimen swimming on its side with (35.1%, n=13). We recorded three shelter types: 1) individual strong lateral undulations about 0.15 m over the bottom; holes dug in the muddy bottom (n=23, 46.9%) (Fig. 2a); 2) and searching for prey or taking offered baits. During night small patches of debris (plastic and ceramic tubes, plank and crepuscular dives, an underwater torchlight with a red fragments, bottle fragments and pieces of ironwork) dis- filter was used to diminish the disturbance caused to white- light sensitive sand morays (cf. Helfman 1992). To locate the shelters of G. ocellatus within the study site, we used four circular 1-10 m radius concentric transects - derived from the common “search-in-circles” scuba proce- dure (Shreeves et al. 1991) - centered in four 1.3 m high upright PVC cylinders permanently fixed to the bottom. Once located, the shelters were marked with tethered floating markers (Helfman 1992). Three PVC tubes (one straight; one C-shaped; and one U-shaped) 60 cm long and 7 cm wide, were experimentally positioned on the substrate of the study site for about four months to verify the opportunistic shel- ter use by G. ocellatus. Contents of the whole digestive tracts of 62 speci- mens (43 individuals collected during the day, 14 during the night and five during twilight) of G. ocellatus were ana- lyzed. Collecting was carried out evenly through the year. The ratio of digestive tube length/standard length was cal- culated (LDT: LS index - intestinal ratio - see Knöppel 1970), as well as the frequency of occurrence (Bowen 1992) and Fig. 2a. Gymnothorax ocellatus within shelter almost totally hidden in a hole in the muddy sand bottom during the day the per cent composition (Hynes 1950) for each broad cat- (photograph by H.