SciELO - Scientific Electronic Library Online

 
vol.7 issue3The more stirring the better: cichlid fishes associate with foraging potamotrygonid raysPutative extinction of two sawfish species in Mexico and the United States author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

Share


Neotropical Ichthyology

Print version ISSN 1679-6225On-line version ISSN 1982-0224

Neotrop. ichthyol. vol.7 no.3 Porto Alegre Sept. 2009

http://dx.doi.org/10.1590/S1679-62252009000300019 

SCIENTIFIC NOTE

 

Feeding behavior and follower fishes of Myrichthys ocellatus (Anguilliformes: Ophichthidae) in the western Atlantic

 

 

Maria E. AraújoI; Pedro H. C. PereiraI; João L. L. FeitosaI; Guilherme GondoloII; Daniel PimentaI; Mara C. NottinghamIII

IDepartamento de Oceanografia, CTG, Universidade Federal de Pernambuco (UFPE) and Grupo de Ictiologia Marinha Tropical. Av. Arquitetura, s/n, Cidade Universitária, 50670-901 Recife, PE, Brazil. elisabeth.araujo@ufpe.br (MEA); pedrohcp2@yahoo.com.br (PHCP)
IILaboratório de Genômica Evolutiva e Ambiental, Departamento de Zoologia, CCB, Universidade Federal de Pernambuco (UFPE). Av. Prof. Moraes Rego, s/n, Cidade Universitária, 50670-420 Recife, PE, Brazil
IIISecretaria Especial de Aqüicultura e Pesca. Esplanada dos Ministérios, Bloco D, sala 232, 70043-900 Brasília, DF, Brazil

 

 


ABSTRACT

This paper described aspects of feeding behavior of Myrichthys ocellatus in the Western Atlantic, using diving observations and additional data from literature. The feeding behavior of M. ocellatus was characterized by scanning the sand surface and searching for buried preys, using its head and tail as a searching tool. Twelve species of reef fish were detected as followers of M. ocellatus, including three new records of follower species. The food overlap index between M. ocellatus and most follower species was low.

Key words: Interspecific associations, Goldspotted eel, Food overlap.


RESUMO

O presente estudo descreveu aspectos do comportamento alimentar de Myrichthys ocellatus no Atlântico ocidental, através de observações subaquáticas, complementadas com dados compilados da literatura. Myrichthys ocellatus caracteriza-se por buscar presas entocadas ou enterradas no substrato não consolidados e por usar a cauda e a cabeça como ferramentas de busca. Doze espécies de peixes recifais foram observadas como seguidoras de M. ocellatus, incluindo três novas ocorrências. O índice de sobreposição alimentar entre M. ocellatus e a maioria das espécies seguidoras foi baixo.


 

 

Snake eels of the Ophichthidae family typically have a long and cylindrical body and a pointed and finless tail (McCosker, 1977). They differ from most other eels because their posterior nostrils are located within the mouth or along the upper lip (McCosker, 1977; Nelson, 2006). Ophichthidae fishes use their rigid, pointed tail for burrowing (Nelson, 2006). The Goldspotted eel Myrichthys ocellatus (Lesueur, 1825) is distributed throughout the Atlantic Ocean from Bermuda to southern Brazil (McCosker et al., 1989). This is a very common species in northeastern Brazil, occurring in depths of up to 30 m (Carvalho-Filho, 1999). Myrichthys ocellatus reaches a total length of about 1 m (McCosker et al., 1989). Its body is pale brown, with a yellow or green cast, yellow polka dots and a dark outline (McCosker & Rosenblatt, 1993), and its ventral region varies from yellowish to white (Cervigón, 1996; Randall, 1996).

Myrichthys ocellatus inhabits coastal reefs and forages on sand banks, in clumps of algae or between reef crevices, feeding mostly on crabs from the families Portunidae, Xanthidae and Majidae (Randall, 1967; Robins & Ray, 1986; Randall, 1996; Lieske & Myers, 1999). The vigorous and agitated manner in which M. ocellatus searches for prey, and its capacity to penetrate and explore small holes in the substrate makes it a typical nuclear species for opportunistic follower fishes, presumably to increase their foraging success. Many studies describe a nuclear-follower foraging association between Anguilliformes and other reef fishes (e. g. Karplus, 1978; Dubin, 1982; Diamant & Shpigel, 1985; Strand, 1988; DeLoach, 1999; Gerhardinger et al., 2006; Sazima et al., 2007; Maia-Nogueira et al., 2008).

The objectives of the present study were to describe the feeding behavior of M. ocellatus, specially using the tail as a hunting tool, and to characterize qualitatively feeding associations between these nuclear species and its follower reef fishes.

Underwater observations were made off the northeastern coast and oceanic islands of Brazil: Pecém and Iparana (Ceará State), Rocas Atoll and Maracajaú (Rio Grande do Norte State), Fernando de Noronha, Porto de Galinhas, Serrambi and Tamandaré (Pernambuco State), Barra Grande and Maragogi (Alagoas State). Results were complemented with the compiled information from previous studies: Puerto Rico (Randall, 1967), and Brazil: Cairu - Bahia State (Maia-Nogueira et al., 2008), São Sebastião - São Paulo State (Gibran, 2007) and Arvoredo - Santa Catarina State (Gerhardinger et al., 2006). The total area studied encompass the latitudes 18º11'N 27º16'S and the longitudes 32°25'W 67°10'W.

The dives were conducted from July 2005 to January 2008, through 135 hours of snorkeling or scuba diving at low tide, with 54 diurnal observation sessions (150 min each). Observed specimens (n = 63) of M. ocellatus ranged from around 20 to 100 cm TL (average of 45 cm) that were visually estimated on field. The acquisition of ethological data obeyed the ad libitum and animal focal methods (Altmann, 1974). A voucher specimen from Carneiros Beach (Pernambuco State, Brazil) was deposited at Ichthyological Collection of the Universidade Federal de Pernambuco (CI-DOCEAN/UFPE # 1507).

Comparative analysis between food items of M. ocellatus and its followers was performed using compiled data from Randall (1967). To obtain the diet similarity between each pair of species was employed the food overlap index of Morisita (1959) modified by Horn (1966). This index ranges from 0 to 1, values equal to or greater than 0.6 are considered as high food overlap (Zaret & Rand, 1971).

Myrichthys ocellatus was often found alone, seeking prey through side movements of the head and nostrils, which were expanded. The feeding behavior was characterized by initially scanning the sand surface and searching clumps of algae and reef rock crevices, using its head and anterior region of the body as a searching tool. A variety of capture modes procedures were observed in M. ocellatus once prey was sighted. The most common form of capture was to cut a path to the prey by removing sand with jets of water in order to insert its head and catch the prey.

The rigid tail usually helped in searching for prey, depending on the effort required for success. It sometimes used the tip of the tail, once buried in the sand, to support vigorous movements performed, flipping the rear and/or anterior regions, and destroying the hideout where the prey was located, by widening the holes. To reach prey, M. ocellatus stops its head over the spot where the prey is buried and brings the tail to the head level with the substrate, forming an arc with its body and the tail takes over the head position over the prey. From this position, the animal moves vertically like a whip, both quickly and vigorously, enabling it to scatter the substrate and make enough room for the head to go deeper and catch the prey (Figs. 1-2). Besides the bury behavior on sand, M. ocellatus' tail can create holes in calcareous reefs. This sequence of capture tactics was first described here and named "head and tail feeding behavior".

 

 

 

 

When foraging in rocky substrates, the digging mode is not effective, so M. ocellatus seeks its prey on crevices using just its head. At the Rocas Atoll and Iparana, for instance, individuals of M. ocellatus were found foraging in shallower depths with barely enough water to cover them. In these cases, the horizontal wave-like movements of these animals constantly exposed their bodies to the air.

The senses of smell and touch are highly involved when M. ocellatus is hunting for prey, since the fish extends its tube-shaped nostrils (McCosker & Rosenblatt, 1993), and moves them excitedly, directly touching the substrate. Myrichthys ocellatus moves by undulations of muscle contractions stemming mainly from its trunk. Greater amplitudes towards the tail create a counter-stream that pushes the Anguilliformes fishes forward (Wilson & Wilson, 1992; Moyle & Cech-Jr, 2004).

Individuals of this species commonly move under the sand as both a foraging procedure and for defensive purposes (Lieske & Myers, 1999). This behavior was recorded along study area; in Iparana calcareous reefs the Goldspotted eel's specimens were recorded using their tails to made holes on this substratum. The use of the tail as a traction tool in Anguilliformes was recorded by DeLoach (1999) in an agonistic behavior observed between Gymnothorax moringa (Cuvier 1829) and Echidna catenata (Bloch 1795).

The results of the present study, added to the bibliographic information for the western Atlantic, recorded 12 species belonging to five families as followers of M. ocellatus (Table 1). Among these, Eucinostomus lefroyi (Goode, 1874), Halichoeres brasiliensis (Bloch, 1791) and juveniles of Lutjanus alexandrei Moura & Lindeman, 2007 are recorded for the first time as followers of M. ocellatus during the dives made at Porto de Galinhas and Serrambi. Epinephelidae had the highest number of species acting as nuclear-followers of M. ocellatus, totaling five species. Despite the relatively high frequency of following behavior records, it is uncommon to sight the prey been captured by the follower species. In the present study, only in one observation, it was possible to see when M. ocellatus captured a crab and some pereopods detached from its body, and remained floating in the water, until being bitten by Epinephelus adscensionis (Osbeck, 1765) (Fig. 3).

 

 

 

 

The diurnal associative feeding behavior known as 'nuclear hunting' (Fricke, 1975; Sazima et al., 2007) is characterized by a nuclear individual that forages actively in the substrate, exposing organisms that may serve as prey for opportunistic follower species (Strand, 1988). The followers recorded here swam near the head of M. ocellatus, but E. adscencionis and L. alexandrei dared to draw closer.

Cephalopholis fulva (Linnaeus, 1758) is the species with the greatest number of interaction records with M. ocellatus (Sazima et al., 2007; Maia-Nogueira et al., 2008) as confirmed in the present study. This may be due to the high cognitive capacity and opportunist behavior of groupers (Gerhardinger et al., 2006); this group of fishes have among the greatest number of species in association with M. ocellatus. Groupers are also known followers of other species, such as octopus (Strand, 1988; Sazima et al., 2007; Machado & Barreiros, 2008), moray eels (Karplus, 1978; Dubin, 1882; Diamant & Shpigel, 1985; Strand, 1988; Bshary et al., 2006; Sazima et al., 2007), sea stars (Gibran, 2002, 2007), other Actinopterygii fishes (Barreiros & Santos, 1998; Sazima et al., 2007), and also Elasmobranchii (Sazima et al., 2007).

The majority of the follower fishes have low food overlap with M. ocellatus (Table 1). This pattern was also found by Dubin (1982), who compared the diet of Myrichthys breviceps (Richardson, 1848) with that of Cephalopholis fulva (food overlap of 0.29) and Hypoplectrus puella (Cuvier 1828) (0.34). Although some followers have a low degree of similarity to the diet of the nuclear species, certain prey that remain hidden and buried are only accessible to followers through this kind of association, making it easier for the follower to catch the disturbed or mutilated prey. On the other hand, E. adscencionis, in the present study, showed a high value of food overlap (0.92), as their diet is composed mainly of crabs (66.70%), which is also the most common item for M. ocellatus, corresponding to 61.20% of its diet according to Randall (1967). The genus Mycteroperca was considered by this author to feed only on fish, and it was the one with the lowest food overlap value among all the species analyzed. This may be due to the fact that Randall (1967) only studied adult individuals, while interaction records involved juveniles (Gerhardinger et al., 2006; Maia-Nogueira et al., 2008; Luiz-Jr. et al., 2008).

 

Acknowledgements

We thank Dr. Jonh McCosker (California Academy of Sciences), Dr. Peter Wirtz (Universidade da Madeira) and Dr. Robson T. Ramos (Universidade Federal da Paraíba) for reading the manuscript and providing suggestions; Simone Marques for the photographs and suggestions regarding the manuscript; Vanessa Marques for the photographs; Dr. Richard R. Boike and Lais Chaves for English review; CNPq, CAPES and FACEPE for financial support.

 

Literature Cited

Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49: 227-265.         [ Links ]

Barreiros, J. P. & R. S. Santos. 1998. Notes on the food habits and predatory behaviour of the dusky grouper, Epinephelus marginatus (Lowe, 1834) (Pisces: Serranidae) in the Azores. Arquipélago Life and Marine Sciences, 16(A): 29-35.         [ Links ]

Bshary, R., A. Hohner, K. Ait-el-Djoudi & H. Fricke. 2006. Interspecific communicative and coordinated hunting between groupers and giant moray eels in the Red Sea. Plos Biology 4(12): e431. doi:10.1371/journal.pbio.0040431.         [ Links ]

Carvalho-Filho, A. 1999. Peixes da costa brasileira. São Paulo, Ed. Melro, 320p.         [ Links ]

Cervigón, F. 1996. Los peces marinos de Venezuela. Caracas, Fundación Científica Los Rocques, IV, 254p.         [ Links ]

DeLoach, N. 1999. Reef fish behavior: Florida, Caribbean, Bahamas. Florida, New World Publications, 359p.         [ Links ]

Diamant, A. & M. Shpigel. 1985. Interspecific feeding associations of groupers (Teleostei: Serranidae) with octopuses and moray eels in the Gulf of Eilat (Aqaba). Environmental Biology of Fishes, 13(2): 153-159.         [ Links ]

Dubin, R. E. 1982. Behavioral interactions between Caribbean reef fish and eels (Muraenidae and Ophichthidae). Copeia, 1982(1): 229-232.         [ Links ]

Fricke, H. W. 1975. The role of behaviour in marine symbiotic animals. Pp. 581-594. In: Jennings D. H. & D. L. Lee (Eds.). Symbiosis, Symposia of the Society for Experimental Biology 29.Cambridge, Cambridge University Press, 633p.         [ Links ]

Gerhardinger, L. C., M. Hostim-Silva, R. Samagaia & J. P. Barreiros. 2006. A following association between juvenile Epinephelus marginatus (Serranidae) and Myrichthys ocellatus (Ophichthidae). Cybium, 30(1): 82-84.         [ Links ]

Gibran, F. Z. 2002. The sea basses Diplectrum formosum and D. radiale (serranidae) as followers of the sea star Luidia senegalensis (asteroidea) in Southeastern Brazil. Brazilian Journal of Biology, 62(4A): 591-594.         [ Links ]

Gibran, F. Z. 2007. Activity, habitat use, feeding behavior, and diet of four sympatric species of Serranidae (Actinopterygii: Perciformes) in southeastern Brazil. Neotropical Ichthyology, 5(3): 387-398.         [ Links ]

Horn, H. S. 1966. Measurement of "overlap" in comparative ecological studies. American Naturalist, 100: 419-424.         [ Links ]

Karplus, I. 1978. A feeding association between the grouper Epinephelus fasciatus and the moray eel Gymnothorax griseus. Copeia, 1978: 164.         [ Links ]

Lieske, E. & R. Myers. 1999. Collins Pocket Guide. Coral reef fishes. Indo Pacific & Caribbean including the Red Sea. Haper Collins Publishers, 400p.         [ Links ]

Luiz-Jr, O. J., A. Carvalho-Filho, C. E. L. Ferreira, S. R. Floeter, J. L. Gasparini. & I. Sazima. 2008. The reef fish assemblage of the Laje de Santos Marine State Park, Southwestern Atlantic: annotated checklist with comments on abundance, distribution, trophic structure, symbiotic associations, and conservation. Zootaxa, 1807: 1-25.         [ Links ]

Machado, L. F. & J. P. Barreiros. 2008. A previously undescribed following association between juvenile dusky grouper, Epinephelus marginatus (Serranidae) and Octopus vulgaris. Cybium, 32(2): 187-188.         [ Links ]

Maia-Nogueira, R., J. A. C. C. Nunes, E. O. C. Coni, C. M. Ferreira & C. L. S Sampaio. 2008. The twinspot bass Serranus flaviventris (Serranidae) as follower of the goldspotted eel Myrichthys ocellatus (Ophichthidae) in north-eastern Brazil, with notes on others serranidis. Journal of the Marine Biological Association - JMBA2 - Biodiversity Records, 6001. doi:10.1017/S1755267209000591        [ Links ]

McCosker, J. E. & R. H. Rosenblatt. 1993. A revision of the snake eel genus Myrichthys (Anguilliformes: Ophichthidae) with the description of a new eastern Pacific species. Proceedings of the California Academy of Sciences, 48(8): 153-169.         [ Links ]

McCosker, J. E. 1977. The osteology, classification, and relationships of the eel family Ophichthidae. Proceedings of the California Academy of Sciences, 41(1): 1-123.         [ Links ]

McCosker, J. E., E. B. Böhlke & J. E. Böhlke. 1989. Family Ophichthidae. Pp. 254-412. In: Böhlke, E. B. (Ed.). Fishes of the Western North Atlantic. New Haven, Sears Foundation for Marine Research (Memoir No. I, Part 9, vol. 1), 599p.         [ Links ]

Morisita, M. 1959. Measuring interspecific association and similarity between communities. Memoria Faculty of Science Kyushu University Serie E (Biology), 3: 65-80.         [ Links ]

Moyle, P. B. & J. J. Cech-Jr. 2004. Fishes. An introduction to ichthyology. New Jersey, Prentice Hall, 726p.         [ Links ]

Nelson, J. S. 2006. Fishes of the world. New York, John Wiley & Sons, 601p.         [ Links ]

Randall, J. E. 1967. Food habits of reef fishes of the West Indies. Studies in Tropical Oceanography, 5: 665-847.         [ Links ]

Randall, J. E. 1996. Caribbean reef fishes. New Jersey, TFH Publications, 368p.         [ Links ]

Robins, C. R. & G. C. Ray. 1986. A field guide to Atlantic coast fishes of North America. Boston, Houghton Mifflin Company, 354p.         [ Links ]

Sazima, C., J. P. Krajewski, R. M. Bonaldo & I. Sazima. 2007. Nuclear-follower foraging associations of reef fishes and other animals at an oceanic archipelago. Environmental Biology of Fishes, 80: 351-361.         [ Links ]

Strand, S. 1988. Following behavior: interespecific foraging associations among Gulf of California reef fishes. Copeia, 1988(2): 351-357.         [ Links ]

Wilson, R. & J. Q. Wilson. 1992. Swimming. Pp. 34-42. In: Pisces guide to watching fishes: understanding coral reef fish behavior. Hong Kong, Pisces Books, 275p.         [ Links ]

Zaret, T. M. & A. S. Rand. 1971. Competition in tropical stream fishes: support for the competitive exclusion principle. Ecology, 52: 336-342.         [ Links ]

 

 

Accepted July 17, 2009
Published September 30, 2009

Creative Commons License All the contents of this journal, except where otherwise noted, is licensed under a Creative Commons Attribution License