crinitichelis Moreira , 1901 and Leodia sexiesperforata ( Leske , 1778 ) : first record of this symbiosis in Brazil

The crabs of the genus Dissodactylus are well known as ectosymbionts of irregular echinoids belonging to Clypeasteroida and Spatangoida. Dissodactylus crinitichelis is the only species of the genus reported in Brazil. The pea crab species has been already recorded associated with four species of echinoids in Brazilian waters. This paper reviews the known hosts for D. crinitichelis and registers for the first time the association between the pea crab and the sand dollar Leodia sexiesperforata increasing to five the number of known hosts for the crab.


Introduction
The diversity of the marine environment, specially the benthic substratum is commonly reflected by many interactions among organisms, even free living ones.Such event is quite common since many of these species act as substratum or environment for others.The existence of many organisms living in association and their close relation allows for the emergence of symbiotics relationships (Thiel et al., 2003;Rohde, 2005;Baeza, 2007).Symbiosis, sensu De Bary (1879), can be defined as "a phenomenon in which dissimilar organisms live together" (Vermeij, 1983;Paracer and Ahmadjian, 2000).These interactions are commonly observed among crustaceans.Therefore, these taxa have many species that have adapted to co-exist in symbiosis with other invertebrates (Barel and Kramers, 1977;Rohde, 2005).
The Pinnotheridae De Haan, 1833 Campos and Griffith, 1990).The distribution of Dissodactylus is restricted to the New World, ranging in the western Atlantic Ocean from Massachusetts (USA) to Argentina, with four species recorded, and in the eastern Pacific from Mexico to Peru, where five species are known (Rathbun, 1918;Schmitt et al., 1973;Werding and Sanchez, 1989;Martins and D'lncao, 1996;Fumis et al., 2006).However, so far, there are no common records between the Pacific and Atlantic regions (Griffith, 1987a;Campos and Griffith, 1990).

Material and Methods
Sampling was carried out on May 13 th , 2010 at the Porto da Barra beach, Salvador -BA, Brazil (13°00'24"S -38°31'48"W).Specimens of Leodia sexiesperforata were obtained by free diving in the subtidal zone.Only a single specimen of the sand dollar showed an associated pea crab.The host and the symbiont were photographed and immediately placed in a plastic bag containing sea water and then taken to the laboratory.Posteriorly they were photographed and fixed in 70% ethanol.The material was deposited in the Crustacean Collection of the Museu de Zoologia da Universidade Federal da Bahia (UFBA 430)
Leodia sexiesperforata (Leske, 1778) (Figs. 1 A-E) The sand dollar Leodia sexiesperforata (Leske, 1778) can be identified by the presence of six closed, narrow and elongated lunules (five ambulacrals and one interambulacral).The testis is compressed in the oral/aboral axis and shows five shorts and equal petaloids and four gonopores in the apical system.Color ranges from yellow to light brown (Goodbody, 1960;Serafy, 1979;Hendler et al., 1995;Manso et al., 2008).The specimen of L. sexiesperforata has 58.2 mm in diameter, while the known diameter ranges from 22 to 110 mm (Goodbody, 1960;Serafy, 1979;Hendler et al., 1995).A male specimen of D. crinitichelis, with 3.2 mm width and 2.6 mm length, was found clinging to the oral side, close to the anterior lunules (Fig. 1F).The position of the crab on the host may be explained as an evidence of its survival strategy due to its mode of living.
The family Pinnotheridae is usually considered as parasitic or at least semiparasitic.In this context, the dactyli bifid seem adequate, because they have no clear change in morphology to adapt themselves to a parasitic lifestyle (Telford, 1978).Dissodactylus crinitichelis is always characterized as irregular urchin's symbiont, however there are very few studies clarifying the correct association of the species and its sand dollar hosts.Pohle and Telford (1981) state that D. crinitichelis is an obligate parasite because it requires a nearby host to complete its larval development.However, the authors also say that sub-adults and adults stages seem to be facultative parasites.In a subsequent study, Telford (1982a), based on cheliped morphology, stomach contents of the pea crabs and spine allometry of sand dollars, defines the relationship as parasitism, showing that approximately 80% of the food obtained by the crab comes from the host.
However studies carried out by these authors (Pohle and Telford, 1981;Telford, 1982a) are exclusively based on data from L. sexiesperforata as a single host.Since D. crinitichelis is recorded as symbiont of four other species of irregular sea urchins (M. ventricosa, E. emarginata, E. michelini, C. subdepressus), it is important to investigate firstly if there is a preference of the pea crab for one of the sand dollars and secondly whether D. crinitichelis has the same behavior with other hosts.Gray et al. (1968) studied the relation of D. mellitae (Rathbun, 1900) with different echinoderm hosts and observed that the crab preferred E. michelini rather than Mellita quinquiesperforata (Leske, 1778).Subsequently Dexter (1977) noted the same pattern when studying D. nitidus Smith, 1870, which opted by Mellitella stokesii (L.Agassiz, 1841).Unfortunately there are not many studies with D. crinitichelis and its biology (Telford, 1978) and the very few ones deals with other hosts than L. sexiesperforata.In this panorama it is very difficult make further inferences on the preference of this pea crab.
The analysis of the association records with the sand dollars along the Brazilian coast reveals that D. crinitichelis is mainly associated with the Encope emarginata and Meoma ventricosa (Martins and D'lncao, 1996;Wirtz et al., 2009;Almeida et al., 2010).Additionally, Coelho and Ramos-Porto (1995) mentioned Encope sp. as a host in Tamandaré, Pernambuco State.However the genus Encope in Brazil is restricted to a single species, E. emarginata, which occurs from Pernambuco to Rio Grande do Sul State (Tommasi, 1999;Netto et al., 2005;Capítoli and Bemvenuti, 2006;Lima and Fernandes, 2009;Oliveira et al., 2010).Thus, it is possible to deduce that the record of Coelho and Ramos-Porto (1995) may also refer to E. emarginata.Martins and D'lncao (1996) also included the genera Mellita, Clypeaster and Luidia among potential hosts for D. crinitichelis but the specimens have not been identified further than the generic level.However as Luidia Forbes, 1839 belongs to Asteroidea its record as host for pea crabs is extremely unusual since Dissodactylus are characterized by their specific association with irregular echinoids (sand dollars and heart urchins) (Griffith, 1987a;Telford, 1982).
The genus Mellita is represented in Brazil by a single species, M. quinquiesperforata (Leske, 1778), which has a wide distributional range along the Brazilian coast, occuring from Pará to Rio Grande do Sul State (Matos et al., 2000;Barros et al., 2001;Netto et al., 2005).Consequently the record of Martins and D'lncao (1996) can be possibly attributed to this host species.
However, according to Tommasi (1999) eight species of Clypeaster have been recorded in Brazil.C. subdepressus (Gray, 1825) is the species with the widest distribution.Records along the Brazilian coast expand from Bahia to Southern Brazil (Krau, 1956;Alves and Cerqueira, 2000;Magalhães et al., 2005;Netto et al., 2005;Vellutini and Migoto, 2010;Xavier, 2010).Because of the range of this irregular echinoid it is possible to assume that C. subdepressus was the species observed by Martins and D'lncao (1996).
According to Tommasi (1999), six genera and fourteen species belonging to Clypeasteroidea Agassiz, 1872 have been registered along the Brazilian coast.Clypeaster is the largest genus with eight species whereas the others have only one species each.For Spatangoidea Claus, 1876 there are records of seven genera, each one with a single species.These two taxa (Clypeasteroidea and Spatangoidea) are the most important hosts for the species of Dissodactylus since the literature indicates the restriction of the association of these crabs to sand dollars and heart urchins (Rathbun, 1918;Telford, 1978;1982;Griffith, 1987a;Campos and Solís-Marín, 1998;Wirtz et al., 2009).