NEW RECORDS OF THE ISOPOD Leidya distorta INFESTING THE MANGROVE CRAB Ucides cordatus FROM SOUTH AMERICA*

Nota Científica: Recebido em 24/08/2016; Aprovado em 14/02/2017 1UNESP – Universidade Estadual Paulista, Departamento de Parasitologia, Instituto de Biociências de Botucatu (IBB) Distrito de Rubião Jr., s/n – 18618-970 – Botucatu (SP) – Brasil. E-mail: awunderlich@gmail.com (corresponding author) 2Centro de Ecologia, Instituto Venezolano de Investigaciones Cientificas, apartado 21827, 1020A, Caracas – Venezuela; 3UNESP – Universidade Estadual Paulista, Instituto de Biociências (IB), Campus do Litoral Paulista (CLP), Grupo de Pesquisa em Biologia de Crustáceos (CRUSTA) – Praça Infante Dom Henrique, s/n. – Parque Bitaru – 11330-900 – São Vicente (SP) – Brasil; *Fundação de Amparo e Pesquisa do Estado de São Paulo (FAPESP); Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq); Instituto Venezolano de Investigaciones Científicas (IVIC). NOVOS REGISTROS DE Leidya distorta INFESTANDO O CARANGUEJO-UCÁ Ucides cordatus NA AMÉRICA DO SUL


INTRODUCTION
Isopods associated with crustacean hosts show a broad distribution around the world (SMIT et al., 2014). According to WILSON (2008), isopods are a diverse group of crustaceans, with more than 10,300 species found in several environments, with 7.7% represented by parasitic isopod epicarideans. Specifically, Bopyridae is represented by 369 genres and 638 species described (WILLIAMS and BOYKO, 2012), being approximately 586 species of this family associated with decapods (BOYKO and WILLIAMS, 2009).
Bopyrid isopods are macroparasites with an indirect life cycle that involves two hosts, both crustaceans (LESTER, 2005). Most of them are found in the branchial chambers of shrimps, for instance, Probopyrus spp., (MASUNARI et al., 2000 andGOPALAKRISHNAN et al., 2017) or attached to the pleon of hermit and brachyuran crabs, for example, Athelginae (AN, 2009;WILLIAMS and BOYKO, 2012). According to LESTER (2005), the cryptoniscus that is a free-swimming larvae that seek out a definitive host settles between the gill lamellae and after moulting a few times, migrates to the roof of the branchial chamber and later mature into a female in a decapod host.
Specifically, the mangrove crab Ucides cordatus (Linnaeus, 1763) has been found infested with Leidya distorta (Leidy, 1855) for the first time in the Northeast Brazil (LEMOS DE CASTRO, 1973). Leidya distorta, an isopod species of the family Bopyridae BOYKO et al., 2016) has also been found in crabs of the genus Uca spp., from New Jersey, USA (LEIDY, 1855;ROCCATAGLIATA and JORDÁ 2002) to the Rio de La Plata estuary, Argentina JORDÁ and ROCCATAGLIATA, 2002) in Table 1.
However, there is little information about this bopyrid infesting U. cordatus in the east coast of South America.
In this study, we recorded three new localities of L. distorta infestation in the mangrove crab U. cordatus, in two latitudinal separated regions on the Atlantic coast of South America (North-Eastern Venezuela and Southern Brazil), and also reviewed the hosts for this bopyrid species.

METHODS
Mangrove crabs were collected from two localities in Southern Brazil (São Vicente and Cananéia) and one in Venezuela (Cumaná, Sucre State) (Figure 1).
In Cumaná, the crabs were collected between February and August 2011 at the spillway of the sea close to the Manzanares river, Sucre State, Venezuela (10°27'43.11"N, 64°6'07.99"W). This site had a predominant vegetation of Avicennia germinans (L.) with a scarce presence of R. mangle at the border of the spillway. With local fishermen help, fishing net pieces were placed over the burrow entrances. Crabs trying to exit the burrows got entangled in the net and could be easily captured. Afterwards, they were put in an icebox and transported to the laboratory.
In the laboratory, the specimens of U. cordatus were sexed by inspection of the abdomen shape and number of pleopods (PINHEIRO and FISCARELLI, 2001), and the carapace width (CW) measured with a precision vernier caliper (0.05 mm). Later, the specimens were sacrificed and searched for bopyrids in their branchial chambers. The collected isopods were identified as L. distorta based on the descriptions given by RICHARDSON (1908), BOURDON and BOWMAN (1970), and ROCCATAGLIATA and JORDÁ (2002).
The bopyrids were fixed in 70% ethanol, photographed, and the prevalence was calculated as the number of hosts infested divided by the number of hosts examined expressed as a percentage (BUSH et al., 1997).

RESULTS
A total of 281 crabs were collected from the three localities (Cananéia,N = 40;São Vicente,N = 45;and Cumaná,N = 196). From this total, three specimens (one of each locality) were infested with different developmental stages of the bopyrid L. distorta (Figures 2, 3, and 4). The prevalence of L. distorta in U. cordatus was very low throughout the study from the three localities, with a mean value of 1.1%. The prevalence was slightly higher for Cananéia (2.6%) and São Vicente (2.2%) when compared to Cumaná (0.5%) ( Table 2). One juvenile of L. distorta was found in each locality. A total of six male bopyrids and an adult female of L. distorta were found only in Cananéia (Table 2), parasitizing a mature adult male of U. cordatus (73 mm CW).
The adult female of this species is characterised by possessing a large bilobed head, with a strong dorsal anterior carina (HE, head; Figure 2A). Older mature female possesses a fully expanded and spherical marsupium and well-developed dorsal bosses (Figure 2 A, B). First two pereomere (1-2) are shorter. The three following segments are the largest (3-5) and are sub equal in length, about twice as long as the first. The 6-7 th pereomeres are a little shorter than the fifth, and the seventh is half as long as the sixth. The seven pairs of pereopods are small and feeble, with the propodus and dactyls forming a prehensile hand. The terminal segment is furnished with a single pair of elongated pinnate appendages, the uropod (Figure 2 C). The pleopods are biramous (Figure 2 C, D), and the antennae are little developed. The maxillipeds with palp are present, articulated or not. There are also five pairs of incubatory plates, which overlap each other on the ventral side, completely inclosing the marsupial cavity. The pereonites with prominent mid-dorsal projections (i.e., dorsal bosses on the pereon) is an important diagnosis which is characteristic for this species in adult females (Figure  2 A). The juvenile females (Figure 3) differs from the adult in its narrower and elongated form, the thorax not much distended, and more symmetrical segments of the pereon (Figure 3 A), which do not have the mid-dorsal projections as in the adult. They also have the segments of the pereon more distinctly separated and the lateral appendages more elongated (Figure 3 A, B). Also, the oostegites in the juvenile females are much smaller than the ones in the adult females, and the marsupial pouch greatly reduced in size (Figure 3).
The marsupial pouch is never filled with eggs at this stage. The male of this species possessed a body narrow and elongated (Figure 4). Head than long; frontal margins straight, with anterolateral angles rounded (Figure 4 C). The posterior portion is somewhat wider than the anterior (Figure 4 D). Vestiges of ocular pigment visible from posterior part of the head. The first pair of antennae (Figure 4 B) composed of three joints, the second pair composed of seven, the last two being minute and tipped with setae. The seven thoracic segments are separated from each other by lateral incisions (Figure 4 A, B) so that the lateral margins are not continuous. There are seven pairs of prehensile legs. The six abdominal segments are perfectly distinct, separated from each other by lateral incisions, and decrease gradually in width, from the first to the sixth, which carries a pair of elongated, tapering appendages, the uropod (Figure 4 D). The pleopods are rudimentary. Table 2. Infestation levels of Leidya distorta (Isopoda, Bopyridae) registered in three localities from South America in the present study.

DISCUSSION
In this study, we recorded for the first time the infestation of the mangrove crab U. cordatus by L. distorta in Venezuela, and it also represents the second report in Brazil. LEMOS DE CASTRO (1973) reported the first record of this isopod infestation previously in U. cordatus in two different localities of Northeast Brazil (Natal, Rio Grande do Norte State; and Caucaia, Ceará State). Thus, in the present study, we expanded the distribution of this bopyrid by adding three new localities, two in the Southeast region (Cananéia and São Vicente, São Paulo state, Brazil) and another one in the Northwest of South America (Cumaná, Sucre state, Venezuela). This bopyrid has also been found in species of the genus Uca in several regions of the American continent coast (Table 1), since New Jersey, USA (LEIDY, 1855;ROCCATAGLIATA and JORDÁ, 2002) until Rio de La Plata estuary, Argentina JORDÁ and ROCCATAGLIATA, 2002). From all the known species of the genus Uca in Brazil, this bopyrid only infests the fiddler crab U. pugnax (Smith) (LEMOS DE CASTRO, 1973). Moreover, according to an important revision about the diversity of parasitic isopods associated with crustacean hosts, the poor knowledge about Neotropical bopyrids could be due to a lack of sufficient sampling in many of these regions (e.g. east coast of South America), rather than reflecting real biogeographic patterns for bopyrids (WILLIAMS and BOYKO, 2012).
According to LESTER (2005), adult males are much smaller than the females ( Figure 4) and are usually found attached to their pleopods. JORDÁ and ROCCATAGLIATA (2002), found a very low prevalence in both sexes of Uca uruguayensis Nobili, 1901 (males, 12%; and females, 5%). The data given by these authors are similar, with the lowest prevalence found in the populations of U. cordatus in São Vicente (Brazil), Cananéia (Brazil), and Cumaná (Venezuela). LEMOS DE CASTRO (1973), also found a very low prevalence in U. cordatus from Rio Grande do Norte and Ceará states, and in U. pugnax from Rio de Janeiro, all considered Brazilian sites. Moreover, LAFFERTY and KURIS (2009) point out that the infestation pattern of L. distorta is often aggregated, which could explain the lowest prevalence in mangrove crabs. In addition, single infestations in adult female bopyrid isopods are generally accompanied by a single dwarf male consort LAFFERTY and KURIS, 2009). Rarely two parasites can occur together in the branchial chamber or under the abdomen of the decapod hosts, and never three or more (LAFFERTY and KURIS, 2009), but this fact was not verified in the present study. Therefore, the low prevalence of bopyrid species in brachyuran crabs and the reported numbers of undescribed species in recent studies suggest a large yet undescribed fauna of marine isopoda, especially in the tropical Atlantic waters (POORE and BRUCE, 2012). Our results revealed a lower prevalence of L. distorta infesting the mangrove crab U. cordatus from South America.