Ectoparasitic crustaceans on mullet, Mugil curema (Osteichthyes: Mugilidae) in the coastal waters of Rio Grande do Norte State, Brazil

White mullet is a commercial fish species abundant in the coastal waters of Brazil. This study investigated the occurrence of crustacean ectoparasites on white mullet, Mugil curema captured from the littoral waters of Rio Grande do Norte State, Brazil. From 2006 to 2007, 31 individuals of M. curema were captured and encountered ectoparasites were observed, identified and counted. M. curema was parasitized by ectoparasitic crustaceans, caligid copepods, Caligus bonito and Caligus sp.; ergasilid copepods, Ergasilus versicolor and E. lizae; and isopod Cymothoa spinipalpa. Of the caligids detected, 66.66% were C. bonito and 33.33% Caligus sp. C. bonito occurred on males of M. curema during the drought season and Caligus sp. occurred on females during the rainy season. The prevalence of both caligid species was 3.23%. Of the ergasilids detected, E. versicolor (91.67%) occurred during the drought and rainy seasons, whereas E. lizae (8.33%) occurred during the rainy season. Prevalence of E. versicolor was 35.48% and E. lizae was 3.23%. C. spinipalpa was detected during the drought and rainy seasons with a prevalence of 16.13%. The preferred site of fixation by the parasites was the branchial chambers.


Introduction
The great diversity of species of the fish fauna is a striking feature of the Brazilian coast, though few are really abundant.Around 440 fish species were recorded in the coastal waters of Rio Grande do Norte State, Brazil (SOARES, 1988;CAVALCANTI et al., 2004).Studies on parasitic copepods of marine fishes are still scarce in Brazil because of the great diversity of ichthyofauna in its coastal waters.Many crustacean copepods and isopods are ectoparasites of fish and their infestation may affect the development, health and appearance of economically important fish species, thus rendering their marketing difficult (BOXSHALL; MONTÚ, 1997;FONSÊCA et al., 2000).
Acta Scientiarum.Biological Sciences Maringá, v. 33, n. 3, p. 357-362, 2011 There are about 35 known species of copepod parasites on marine teleost fishes along the Brazilian coast, and their hosts mostly belong to the families Belonidae, Scombridae, Mugilidae and Haemulidae (LUQUE; TAKEMOTO, 1996;TAKEMOTO;LUQUE, 2002;CAVALCANTI et al., 2004).The records of copepod parasites of marine fishes in Brazil were made by Schubert (1936), andRocha et al. (1982).Amado and Rocha (1995) reported on three new species of copepod parasites of the genus Ergasilus (Poecilostomatoidea, Ergasilidae) collected from gill filaments of mugilid fish species from Brazil.Boxshall and Montú (1997) published a manual with all the records of copepod parasites of marine fishes in Brazil.Cavalcanti et al. (2005Cavalcanti et al. ( , 2006aCavalcanti et al. ( , 2006b) ) reported on the occurrence of copepod parasites on marine fish from the coast of Natal, Rio Grande do Norte.Luque and Tavares (2007) established a record of copepods associated with fish from Brazil.
The parasitic isopod crustaceans inhabit the gill chamber, mouth and skin of the fish, which are easily identified with the naked eye (EIRAS et al., 2006;THATCHER, 2000;LIMA et al., 2005;THATCHER et al., 2007).Among the isopod crustaceans, species belonging to the family Cymothoidae are of special interest, because their hosts are fishes of commercial importance.Lima et al. (2005) observed the occurrence of isopod parasites in the fish serra, Scomberomorus brasiliensis (Collette, Russo & Zavala-Camin, 1978) in the coastal waters of Rio Grande do Norte State, Brazil.Thatcher et al. (2007) published the first record of Cymothoa spinipalpa (Isopoda: Cymothoidae) in the oral cavity of the marine fish, Oligoplites saurus in Rio Grande do Norte State.
Fish species of the family Mugilidae have wide geographic distribution and are represented by species found in tropical and subtropical waters around the world, especially in coastal waters and estuaries.Mullets are abundant in the Brazilian aquatic ecosystems and they belonging to a single genus Mugil.The commercially exploited species of this genus in the coastal waters of Brazil are M. liza and M. curema (MENEZES;FIGUEIREDO, 1985).Mullets have a greasy meat of good quality and are of commercial importance.They are sold fresh or salted and their eggs are much appreciated.This study investigated the occurrence of ectoparasitic crustaceans in mullet, M. curema (Osteichthyes: Mugilidae) from the coastal waters of Rio Grande do Norte State, Brazil.

Specimens of Mugil curema Valenciennes, 1836
were captured from the coastal waters located in the geographic coordinates 05° 47'42 "S and 35º 12'24" W of Rio Grande do Norte State.Fish samples were captured by local fishermen using beach-seines from the coastal waters of approximately 10 m depth, during the period from March 2006 to March 2007.The beach-seines were 110 m in length, 3 m in height, with a mesh size of 1 cm in the central part and 7 cm in the extremities.Fish collected from the beach-seine were numbered and samples of whole fish were used for morphometric and meristic analysis to confirm the taxonomical identification of the species (MENEZES, 1983;SOARES, 1988).The total length (cm) and body mass (g) of each fish was recorded.Rainfall data of the region was obtained from the Meteorological Department (EMPARN) of Natal, Brazil.
The body surface of each fish was checked for the presence of ectoparasites, and when detected they were carefully removed and observed under a stereoscope (Model TE TAIMIN 1L, coupled with a Kodo Digital video camera), processed and quantified using appropriate techniques (EIRAS et al., 2006;PAVANELLI et al., 2002).The taxonomic identification of parasites was performed in the Icthyoparasitological Laboratory of the State University of Maringá, UEM, Paraná State.
All fishes were dissected and their gonads were examined to identify the sexes.The sex ratio of the host fish was verified by analyzing the monthly relative frequency distribution of males and females during the study period.To check the difference in the proportion of males and females fishes and to verify whether the difference was statistically significant, the χ 2 test (chi-square) at 5% level of significance was performed, using the software Statistica 7.0.Parasitic ecological indices were calculated and expressed according to Bush et al. (1997).

Results
Rainfall: The period from March to August, with a mean monthly rainfall of 222.8 mm, was considered the rainy season.Conversely, the period from September to February with a mean monthly rainfall of 57.4 mm was considered as the drought period.
Size of hosts: A total of 31 specimens of M. curema were necropsied, with total length ranging from 10.1 to 37.3 cm (21.04 ± 5.64) and total weight varying from 11.5 to 696.6 g (127.97 ± 126.35).Among the specimens of M. curema captured, 22 were males and 9 were females, with significant difference in the sex ratio of males and females (χ 2 = 20.96;df = 1; p > 0.05).Of the 31 specimens of M. curema collected, 16 were parasitized, being 10 males and 6 females.Considering the sex ratio of males and females -71% and 29% respectively -there was no significant difference in the proportion of infected males and females (χ 2 = 0.45; df = 1; p < 0.05).

Parasitic ecological indices
The ergasilid species found on M. curema were Ergasilus versicolor (Wilson, 1911) and E. lizae (Kroyer, 1863).The species which showed the highest intensity was E. versicolor, with a representation of 406 individuals.During the rainy season an occurrence of 380 individuals was recorded and in the drought season 26 individuals were recorded.
Ergasilus versicolor was found during both seasons, being more frequent during the rainy season, while E. lizae was recorded only during the rainy season.E. versicolor showed high values of prevalence, mean abundance and mean intensity compared to E. lizae during the rainy season.However, during the drought season, E. versicolor showed low values of prevalence, mean abundance and mean intensity, and E. lizae was not registered during this season.The site of fixation preferred by the ergasilids was the gill chamber of the hosts (Table 1).
Caligus bonito was found only during the drought season, while Caligus sp. was found only during the rainy season.On the other hand, C. spinipalpa was more prevalent during the drought period (Table 1).During rainy season, all the parasites showed clear host specificity with respect to sex of the host M. curema, being more frequent in males (79.9%), specifically in immature males (47.93%) than in females (20.10%) (χ 2 = 35.76;df = 1; p > 0.05).During the drought season, the parasites occurred only in males (100%) and the number of parasites (n = 214) was higher in immature males of M. curema.
Ergasilus versicolor showed clear host specificity as to the sex of the host, being more frequent in males (66.66%) than in females (33.33%) of M. curema during the rainy season, and only occurred in males during the drought season.On the other hand, E. lizae occurred only in females during the rainy season.

Parasitism and pluviometry
Caligus bonito occurred only during the drought period, while E. lizae and Caligus sp.occurred only during the rainy season.E. versicolor and the isopod C. spinipalpa occurred during both rainy and drought seasons (Figure 2).Caligus bonito occurred on males of M. curema during the drought season and Caligus sp.occurred in females during the rainy season.E. versicolor occurred during both the rainy and drought seasons and E. lizae occurred only during the rainy season.C. spinipalpa occurred during both the rainy and drought seasons.The preferred site of fixation of the parasitic copepods and isopod was the gill chamber of hosts.Fonsêca et al. (2000) investigated the copepod parasites found on mugilid fishes cultivated in estuarine fish ponds in Itamaracá, Pernambuco State.They identified the following ectoparasites on mullet, M. liza: Ergasilus atafonensis.E. caraguatatubensis, E. lizae; Acanthocolax sp.; Caligus minimus and C. praetextus, parasitizing the gills and skin of the host fish.The intensity of infestation was 0 to 12 copepods per fish.

Discussion
Copepods E. versicolor and E. lizae were found in the gills of M. platanus (Günther), in the coastal waters of Rio de Janeiro (KNOFF et al., 1994), where prevalence values of 20.66% for E. versicolor and of 21.33% for E. lizae were verified.Comparing these data with the results obtained in this study, a low prevalence of E. lizae in M. curema was observed.This is possibly due to the high stocking density of cultivated fishes in ponds, which facilitates parasitic infestations.
The gills of the hosts were the preferred site of attachment by C. bonito.A similar occurrence was observed in the gills of M. platanus in the coast of Rio de Janeiro State, with a prevalence of 13.33% (KNOFF et al., 1994).This paper reports a low prevalence of caligids in M. curema in relation to the results obtained by Knoff et al. (1994) for M. platanus.Caligus bonito was found in carangid fish of the genus Oligoplites Gill (TAKEMOTO et al., 1993). Takemoto et al. (1996), conducted studies on comparative analysis of metazoan parasitic communities of Oligoplites palometa, O. saurus and O. saliens in Sepetiba Bay, Rio de Janeiro State, and they found C. bonito with a prevalence of 3.6%.The present study also reports a low prevalence of C. bonito on M. curema.Lima et al. (2005) observed the occurrence of parasitic isopods in the fish serra, Scomberomorus brasiliensis (Collette, Russo & Cavala-Camin, 1978) in coastal waters of Rio Grande do Norte State, Brazil.Of the total fish captured, 31% was parasitized, where 86% was Livoneca redmani (Leach, 1818) (Cymothoidea) and 14% was Rocinela signata (Schioedt & Meinert, 1879).
Ergasilus versicolor and the isopod C. spinipalpa occurred during both seasons; as such, their presence was not influenced by the rainy and drought seasons.However, rain and drought influenced the occurrence of the parasites, C. bonito, E. lizae and Caligus sp.Rainfall is one of the environmental factors that may influence the parasitic infestation and the degree of temporal or permanent aggregation of host communities, which facilitates the contact with the larval stages of parasites (ROHDE et al., 1995;LUQUE;TAKEMOTO, 1996).

Conclusion
Present work confirms that M. curema was parasitized by ectoparasitic crustaceans, caligid copepods, Caligus bonito and Caligus sp.; ergasilid copepods, Ergasilus versicolor and E. lizae; and isopod Cymothoa spinipalpa.C. bonito occurred on males of M. curema during the drought season and Caligus sp.occurred on females during the rainy season.E. versicolor occurred during the drought and rainy seasons, whereas E. lizae occurred during the rainy season.The preferred site of fixation by the parasites was the branchial chambers.

Figure 2 .
Figure 2. Values of Prevalence and Mean Abundance of crustacean ectoparasites on mullet, M. curema from the coastal waters of RN during periods of drought and rain.

Table 1 .
Parasitic ecological indices and standard deviation of M. curema (when n > 1) examined during the rainy and drought seasons during March 2006 to March 2007.