INTRODUCTION
The gastropods of the family Eulimidae Philippi, 1853 comprise about 850 species that are almost exclusively parasitic, living in association with echinoderms. Some species are free-living and change their host, while others are permanently associated with the host. Most eulimids are ectoparasites, living attached to their host's body by their snout or proboscis. The proboscis allows them to penetrate and feed on the host's tissues or body fluids (Warén, Reference Warén1984; Jangoux, Reference Jangoux1987; Warén & Crossland, Reference Warén and Crossland1991).
Within the family Eulimidae, the genus Annulobalcis Habe, 1965, is characterized by a wide shell aperture with an outer lip strongly projected, a high shell and a brightly coloured body (Warén, Reference Warén1984). All the species of Annulobalcis are ectoparasites restricted to comatulids (Warén, Reference Warén1984), including Annulobalcis aurisflamma, which is a parasite of the crinoid Tropiometra carinata (Lamarck, 1816).
The genus comprises ten species (Dgebuadze et al., Reference Dgebuadze, Fedosov and Kantor2012), with only two of them recorded from the Atlantic Ocean: Annulobalcis procera Simone, Reference Simone2002 (from deep water off Espírito Santo, Brazil), whose host is unknown; and Annulobalcis aurisflamma Simone & Martins, Reference Simone and Martins1995 (originally described from São Paulo coast, south-eastern Brazil and recently recorded from Bahia coast, north-eastern Brazil by Queiroz et al., Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011).
Based on specimens collected on recent expeditions, in the present paper we report a northward range extension for Annulobalcis aurisflamma into the western Atlantic.
MATERIALS AND METHODS
Study area
The study was carried out at the Francês sandstone reef (ca. 09°45′58.35″S, 35°50′10.62″W) off the central coast of Alagoas State, north-eastern Brazil (Correia & Sovierzoski, Reference Correia and Sovierzoski2009), which comprises a reef ecosystem formed by three successive parallel lines of sandstone reefs (Figure 1).
Map of Alagoas state (north-eastern Brazil) with the collection site (red spot) on the Francês sandstone reef.
Methodology
Large populations of the crinoid Tropiometra carinata were observed when snorkelling during four field trips conducted in the dry season of 2012 (on 27 January, 8 February, 20 and 21 April). The crinoids were carefully removed from the rocks to avoid the snails' release. After the removal, we examined the crinoids for the presence or absence of snails and recorded the body parts of the crinoid where the snails were found, including the crinoid's colour pattern.
Parasitic snails living on T. carinata were collected and transported alive to the Setor de Comunidades Bentônicas, Universidade Federal de Alagoas, for identification. In the laboratory, the snails were observed and photographed alive through a stereomicroscope, subsequently fixed in 70% ethanol and then deposited in the Mollusca collection of the Universidade Federal de Alagoas. The geographic distribution of Annulobalcis aurisflamma was mapped using the Marine Ecoregions of the World (Spalding et al., Reference Spalding, Fox, Allen, Davidson, Ferdaña, Finlayson, Halpern, Jorge, Lombana, Lourie, Martin, McManus, Molnar, Recchia and Robertson2007) in order to identify distinct ecoregions where the species are known to occur.
SYSTEMATICS
Family EULIMIDAE Philippi, 1853
Genus Annulobalcis Habe, 1965
Annulobalcis aurisflamma Simone & Martins, 2005
(Figures 2 & 3)
Annulobalcis sp. Migotto et al., Reference Migotto, Tiago and Magalhães1993.
Anulobalcis auriflama Rios, Reference Rios2009: 474.
Morphological variation in Annulobalcis aurisflamma from Alagoas (specimens deposited under UFAL-MOL 0042). Ventral view of the shell (A, C, E, G, I). Lateral view of the shell (B, D, F, H, J). Scale bar = 2 mm.
Annulobalcis aurisflamma alive. Dorsal view (A). Ventral view (B). Specimens in situ living in the aboral region of Tropiometra carinata arms (C, D). A, B: scale bar = 0.2 cm; C, D: scale bar = 1 cm.
MATERIAL EXAMINED
UFAL-MOL 0041; Francês sandstone reefs; coordinates: ca. 09°45′58.35″S 35°50′10.62″W; Marechal Deodoro (Alagoas, Brazil), seven specimens, water depth: ca. 1–2 m; coll. by A. Bispo, A.L.S. Miranda, E.A. Albuquerque, R.L. Nascimento & M.D. Correia, 27 January 2012. UFAL-MOL 0042; Francês sandstone reefs; coordinates: ca. 09°45′58.35″S 35°50′10.62″W; Marechal Deodoro (Alagoas, Brazil), nine specimens; water depth: ca. 1–2 m; coll. by A. Bispo, A.L.S. Miranda, E.A. Albuquerque, R.L. Nascimento & M.D. Correia, 8 February 2012.
DESCRIPTION
Shell transparent, slender, elongated-conical, 3.0–7.4 mm, with many axial striae (Figure 2). Shell of up to nine whorls. Protoconch with three convex (less convex than teleoconch) whorls. Teleoconch of up to seven convex whorls; sutures are prominent. Aperture oval. Inner lip sigmoid in ventral view. Outer lip convex in lateral view, slightly retracted at suture, with the lip mostly protruded in the middle part (Figure 2B, D, F, H, J).
Mantle brown-coloured, with up to eight yellowish axial stripes in the body whorl (Figure 3A, B). Usually, there is also a spiral stripe of the same colour. Tentacles are predominantly yellow, but brownish in the inner face near the base (Figure 3A, B). Eyes well developed, black, situated at the base of tentacles (Figure 3A). Foot with a longitudinal lilac furrow and a yellow band at the margin (Figure 3B).
BIOECOLOGY
We observed a higher number of crinoids being parasitized in January and February 2012 than in April 2012. During the first two field trips (January and February 2012), each of the parasitized crinoids were hosting six or seven parasites and juvenile snails were largely observed, sometimes exceeding the number of adults on the same crinoid. In April 2012, each parasitized crinoid was hosting one or two snails. All of the snails associated with Tropiometra carinata were observed and collected in the intertidal region at depths of 1–2 m.
The snails were normally located on the proximal aboral region of the crinoid arms (Figure 3C, D), making it almost impossible to see them without removing the crinoid from the substrate; observation was further complicated by the fact that the snails leave the crinoid almost immediately if disturbed. Despite the high variation of colour pattern in T. carinata, the snails were observed in most of them.
REMARKS
There is no uncertainty in the co-specificity of our specimens with those of the type series of Annulobalcis aurisflamma. They all share the diagnostic characteristics of the species that allowed us to identify them with confidence: the same host (Tropiometra carinata), the same morphology of the shell and the same colouration of the mantle, tentacles and feet. Although our specimens only reached sizes of up to 7.4 mm, as opposed to those found in the type series that reach sizes of up to 11 mm, their size was still within the expected intraspecific variation (see Simone & Martins, Reference Simone and Martins1995; Queiroz et al., Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011). For comparison with other congeners, see Simone & Martins (Reference Simone and Martins1995).
TYPE LOCALITY
Brazil: Ubatuba, São Paulo.
GEOGRAPHIC DISTRIBUTION
São Paulo, Brazil: Ubatuba, Praia Grande (Simone & Martins, Reference Simone and Martins1995) and São Sebastião (Migotto et al., Reference Migotto, Tiago and Magalhães1993) [entire South-eastern Brazil Ecoregion]; Bahia: Salvador (Queiroz et al., Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011) [Eastern Brazil Ecoregion]; Alagoas: Marechal Deodoro (present study) [North-eastern Brazil Ecoregion] (Figure 4).
Distribution of Annulobalcis aurisflamma in the western Atlantic.
DISCUSSION
Here we present the northernmost known limit for Annulobalcis aurisflamma and extend its distribution up to 400 km north into the western Atlantic. The only three previous records of A. aurisflamma were made by Simone & Martins (Reference Simone and Martins1995), Migotto et al. (Reference Migotto, Tiago and Magalhães1993) and Queiroz et al. (Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011) from the South-eastern and Eastern Brazil Ecoregions, respectively. The present record of this species in the North-eastern Brazil Ecoregion suggests that the species is widespread along the Brazilian coast.
The new records presented in this study and in Queiroz et al. (Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011) have filled a gap in the distribution of A. aurisflamma, which might had been previously overlooked due to its cryptic habits and the absence of sampling in these sectors of the Brazilian coast.
Our findings confirm the conclusions made by Simone & Martins (Reference Simone and Martins1995) and Queiroz et al. (Reference Queiroz, Sales, Sampaio, Neves and Johnsson2011) that A. aurisflamma parasitizes all morphotypes of Tropiometra carinata despite their colour variation and are normally found in the crinoid's aboral region.
The observations also suggest the presence of a temporal pattern in the population of A. aurisflamma as demonstrated by another Eulimidae species, Hypermastus placentae, in Australia (Crossland et al., Reference Crossland, Alfolad and Collins1991, Reference Crossland, Alfolad and Collins1993).
ACKNOWLEDGEMENTS
The authors are grateful to Prof Dr Luiz Ricardo Lopes de Simone (Museu de Zoologia da Universidade de São Paulo) for confirming the identification of Annulobalcis aurisflamma and to two anonymous reviewers that helped us improve this manuscript. We are also grateful to Dr Anders Warén (The Swedish Museum of Natural History), Dr Michael Crossland (The University of Sydney) and Dr Polina Dgebuadze (Severtsov Institute of Ecology and Evolution) for providing useful literature on the eulimids.
