Rocinela signata ( Isopoda : Aegidae ) parasitizing the gills of the spotted goatfish Pseudupeneus maculatus ( Actinopterygii : Mullidae ) in Northeastern Brazil

Parasitic isopods of fishes usually show wide distribution and low host specificity. This study investigated the occurrence of gill parasites in 120 specimens of spotted goatfish Pseudupeneus maculatus, marine fish of great economic importance for fishery community. The fish were captured monthly in the Coast of Pernambuco State, Northeast Brazil, between October 2012 and September 2013. Eleven isopods were found and identified as Rocinela signata. We observed lower infections in the gills of P. maculatus (prevalence 8.3%, mean intensity 1.6±0.3 and mean abundance 0.1±0.3) when compared to other studies of different host fishes from geographically close locations. This parasite has been reported from a wide variety of fish species, not only in Brazil, but also in the eastern Atlantic and the Pacific oceans. This is the first report of R. signata in spotted goatfish.


INTRODUCTION
Isopods are crustaceans that present a great variety of shapes and sizes, occurring in different habitats, from the bottom of the ocean to mountain regions (Wilson 2008); their marine representatives are important constituents of the invertebrate fauna of this ecosystem, especially considering their different roles in the marine foodchain (Riseman and Brusca 2002).Among the isopods, members of the family Aegidae Dana, 1853 are known for its association to the body surface of fish and sponges (Porifera); comprising isopods with different modes of life, from free living organisms to obligatory parasites (Brusca 1983).Their species are widely distributed throughout the oceans, from tropical to polar waters, from shallow regions to great depths (Bruce 2001(Bruce , 2009)).
The family Aegidae comprises five genera and approximately 107 described species; the genus
Rocinela Leach, 1818 in this family is cosmopolitan and includes described 40 species (Brusca 1983).
Rocinela signata (Schiodte and Meinert 1879) can be found either in the free-living form in the bottom of the ocean, or as a fish parasite.The species has a wide distribution on the West Atlantic Ocean, from Florida to Southern Brazil, and most of the records are from coastal regions (Brusca and France 1992).This species differs from its congeners by presenting the image of a pigmented and inverted "W" on its pleotelson, an important characteristic considered for its identification (Moreira 1977).
When parasitizing fish, R. signata is mostly found in the oral cavity, gills and tegument of several species, including some economically important hosts (Garzón-Ferreira 1990, Bunkley-Williams et al. 2006).Its attachment apparatus and feeding activity causes injuries to the fish and predisposes the hosts to secondary infections, and reducing its growth rate (Moreira 1977, Cavalcanti et al. 2012).
In addition to the damages to the host fitness and health, the parasite affects the appearance of the fish and consequently their commercial value (Ravichandran et al. 2010).
Spotted goatfish known as "saramunete" in Northeastern Brazil Pseudupeneus maculatus (Bloch, 1793) (Mullidae) forages on the bottom, and is commonly found in coral reefs on the West Atlantic from the Bermudas through New Jersey, USA to Santa Catarina, South Brazil (Hostim-Silva et al. 2006).They are versatile predators that use their camouflage to capture small fishes and crustaceans on the substrates mixed by sand, gravel and stones (Krajewski et al. 2006, Sazima et al. 2006).Pseudopeneus maculatus is not considered to be threatened at present, being classified in the IUCN Category of Least Concern (Dooley et al. 2015).In Brazil, they are abundant in the Northeastern coast, mainly in the State of Pernambuco where they are commercially valued and have their exploitation destined to the internal and external market (United States and Europe) (Santana et al. 2006, Lima et al. 2008).
Pseudupeneus maculatus is generally captured in the continental platforms in shallow waters, part of a coastal tropical system from which dozens of people depend (Campos andOliveira 2001, Rocha et al. 1998).The stocks of P. maculatus have been impacted by the capture of immature specimens in hatchery areas, compromising the biological and fishery recruitment of the species (Lessa et al.

2004).
The aim of this study was to report for the first time the occurrence of R. signata on the gills of the spotted goatfish P. maculatus captured by artisanal fishermen in the Brazilian Northeast.The global and Brazilian distributions of the parasite are also discussed.
Fish were individually identified and kept on ice in thermal boxes for biometry and posterior necropsy.The gonads were exposed and observed to determination of sex and the gills were collected and fixed in alcohol 70%, identified and shaked for parasite detachment according to Eiras et al. (2006) and Jerônimo et al. (2011).
The isopods found were analyzed under stereomicroscope and identified according Rocinela signata PARASITE OF Pseudupeneus maculatus IN BRAZIL 2077 to Brusca and France (1992).Parasitological descriptors followed the recommendations of Bush et al. (1997).

RESULTS AND DISCUSSION
Among the 120 (64 males, 50 females and 6 indeterminate sex) specimens of P. maculatus that were examined (Figure 1), the gills of 10 were parasitized (6 on males, 4 on females and 1 on indeterminate sex) by at least one of the eleven individuals of R. signata (Figure 2), with prevalence 8.3%, mean intensity of infestation of 1.1.±0.Regarding the levels of infestation, the present study found similar prevalence and intensities to those reported previously.The prevalence of the parasite found in this study was slightly higher than that reported by Luque et al. (2002) I).Although the parasite can be found parasitizing several fish species, its preference for some species must not to be dismissed.Isopods of the family Aegidae are temporary or facultative parasites with low host specificity (Brusca 1983).They feed on blood and are generally found associated with the gill chamber of marine fish of economic importance (Hermida et al. 2014, Bunkley-Williams et al. 2006).In aquaculture, for example, fish parasitized by these isopods exihibit respiratory problems, low growth rate and are more susceptible to secondary infections due to opened wounds (Bunkley-Williams and Williams Jr 1998).However, the effects of these isopods on the host health and survival (e.g., increased predation) in the nature remains unknown, and it might be strongly associated to their modes of attachment and injury caused to the host tissue.

Figure 1 -
Figure 1 -The host Pseudupeneus maculatus, from the Coast of Pernambuco State, Northeast Brazil.Scale bar: 3 cm.

Figure 2 -
Figure 2 -Rocinela signata from the gills of Pseudupeneus maculatus, Northeastern Brazil.a -dorsal view; b -lateral view; cventral view.The arrow indicates the pigmented inverted W on the pleotelson.Scale bar: 1 mm.

TABLE I Hosts, Locality, Prevalence (P), mean intensity (MI), and references of the records of Rocinela signata parasitizing fish in Brazil. Host Locality (State) P(%) MI Reference
Lima et al. (2005)reported higher prevalence (44.44%) of R. signata in S. brasiliensis from the Rio Grande do Norte, region close to Pernambuco, the same region where the present study was performed.Similarly to Lima et al. (2005), 37.5% prevalence was found by Cavalcanti et al. (2012) in S. frondosum from Rio Grande do Norte with mean intensity 2.58 and abundance 0.97 in male and female fish in both rainy and dry seasons.Apart from the highest prevalence of R. signata observed in H. steindachneri (20%), Bunkley-Williams et al. (2006) have reported the lowest ones in H. aurolineatum (0.45%), O. ruber (0.49%) and in H. cruentatus (0.22%).