First record of Hamaticolax scutigerulus (Copepoda: Bomolochidae) in Brazil, ectoparasite of the spotted goatfish Pseudupeneus maculatus (Actinopterygii: Mullidae)

Primeiro registro de Hamaticolax scutigerulus (Copepoda: Bomolochidae), parasito de saramunete Pseudupeneus maculatus (Actinopterygii: Mullidae), no Brasil

Copepods comprise the second most frequent parasites of marine fishes in the Neotropical region (Luque & Poulin, 2007). The family Bomolochidae Claus, 1875 has at least 20 genera and the species are characterized by specialized structures on the body for attachment and feeding on their hosts, generally on the gills, branchial cavity and noses (Kim & Moon, 2013, Maran, Moon, Adday, Khamees, & Myoung, 2014, Walter & Boxshall, 2015).

The genus Hamaticolax Ho and Lin (2006) was proposed together with Cresseyus Ho and Lin (2006), to accommodate some orphan species previously allocated to the genus Holobomolochus Vervoort (1969). Hamaticolax differs from the genera Cresseyus and Holobomolochus in having a pair of rostral hooks (Ho & Lin, 2006). To make a taxonomic identification of Hamaticolax, several characteristics need to be taken into consideration. However, the leg armor (Le), i.e. leg composition in terms of setae and spines, are the feature that has been most characterized in previous descriptions (Kabata, 1971).

The spotted goatfish Pseudupeneus maculatus (Bloch, 1793) is a demersal marine fish that is frequently found in shallow coral reef waters, along the entire western Atlantic seaboard from New Jersey, USA, to Santa Catarina, Brazil (Lessa & Nóbrega, 2000, Hostim-Silva et al., 2006). This species is caught mainly by means of trap fishing on the coast of the state of Pernambuco, Brazil, and its meat has been appreciated in both the national and the export market. Hence, this fish is economically valuable (Lessa & Nóbrega, 2000).

The aims of this study were to provide the first report of occurrences of the parasite Hamaticolax scutigerulus (Wilson, 1935) in Pseudupeneus maculatus caught in the state of Pernambuco, northeastern Brazil, and to present information on the leg armor of this parasite, in comparison with 10 described species.

A total of 120 fish were obtained for parasite evaluation between October 2012 and September 2013. They were caught by an artisanal fisherman at a mean depth of 20 m, in an area comprising the following coordinates: site 1 (7° 37' 28.43" S; 34° 1' 10.24" W), offshore from the municipality of Goiana; site 2 (7° 37' 50.34" S; 34° 43' 41.73" W), in the metropolitan region of Recife; and site 3 (8° 54' 41.79" S; 33° 57' 23.45" W), offshore from the municipality of São José da Corôa Grande (Figure 1).

Figure 1.
Location of the three sites (1, 2 and 3) of capture of 120 specimens of Pseudupeneus maculatus used in this study.

The fish were stored in thermal boxes with ice and were transported to the Marine Fish Farm Laboratory of the Fisheries and Aquaculture Department of the Universidade Federal Rural de Pernambuco (UFRPE) for necropsy. The gills were collected and fixed in 70% alcohol, and were slightly agitated to detach the parasites (Eiras, Takemoto, & Pavanelli, 2006, Jerônimo, Martins, Ishikawa, Ventura, & Tavares-Dias, 2011) for subsequent analysis.

The copepods were clarified in lactic acid (Humes & Gooding, 1964), and then dissected and observed on compressed slides under a DIC Iamger.A2 microscope equipped with Axio Cam MRc camera. The adult specimens were identified as described by Vervoort (1969), Ho and Lin (2006) and Morales-Serna and Gómez (2010). The composition of the setae and spines of the leg armor was compared with previous studies on 10 described species in the genus Hamaticolax. Prevalence, mean intensity of infestation and mean abundance were calculated as described by Bush, Lafferty, Lotz, and Shostak (1997).

A total of 80 copepods were collected, comprising 77 females and three males in hosts of both sexes. Nine gravid females and three males were measured (Table 1) and identified as Hamaticolax scutigerulus (Wilson, 1935) (Figure 2).

The total length was 1480±70 µm for females and 549±32 µm for males, and the greatest width was about 993±67 µm for females and 290±20 µm for males.

The measurements and characteristics of the setae and spines on the legs of the present material were compared with those of another species (Table 2). The prevalence of Hamaticolax scutigerulus in the fish examined here was 35%; its mean intensity was 1.9±1.3 and its mean abundance was 0.7±1.2.

The present specimens were similar to the specimens of H. scutigerulus that were observed parasitizing P. maculatus in Piscadera Bay, Curaçao, by Vervoot (1969). On the other hand, our specimens and those reported by Vervoot (1969) showed larger measurements (total length, greatest width, length and width of somites and furcal rami, and length of longest furcal seta) than those found by Cressey (1983).

However, some differences in comparison with other species of the genus Hamaticolax need to be emphasized (Table 1). Females of H. scutigerulus showed shorter total body length than those of H. attenuatus and H. paralabracis, longer total body length than those of H. embiotocae and similar total body length to those of H. galeichthyos, H. occultus, H. spinulus, H. unisagittatus and H. prolixus.

The body width of the specimens collected in Pernambuco was similar to the width in H. attenuatus, H. paralabracis and H. spinulus and greater than in H. galeichthyos, H. unisagittatus and H. prolixus. The long seta length was shorter than in H. attenuatus, H. galeichthyos, H. occultus and H. spinulus and longer than in H. paralabracis and H. unisagittatus. The male specimens in the present study had shorter body length than in H. galeichthyos and H. prolixus, but their length resembled the body length of H. embiotocae. However, the body width was shorter than that found in H. galeichthyos.

The legs of copepods in the genus Hamaticolax have distinct composition in terms of the number of segments (proximal, medial and distal articulations) that form the endopodite and exopodite rami. The number of setae and spines of these rami differ among Hamaticolax species and the findings from the present study are in agreement with those from previous studies (Table 2). Vervoort (1969) argued that the exopodite of the first legs (Le1) in females of H. scutigerulus possess one segment with six setae and five spines, thus differing from the other species. Moreover, male specimens present distal segments of the Le1 exopodite (three setae and three spines) that differ from those of other species.

Figure 2.
Hamaticolax scutigerulus, ventral view: (A) female and its (B) anterior portion, (C) egg sacs and (D) uropods; (E) male.

Table 1.
Comparative values (mean values ± standard deviation, in µm) of measurements of Hamaticolax species, especially Hamaticolax scutigerulus from the gills of Pseudupeneus maculatus captured in the Coast of Pernambuco State, Brazil, and other regions. Length (L), Width (W), and minimum and maximum values between parentheses.

In contrast to that related by Vervoort (1969), the textual information and drawings from Cressey (1983) showed an Le4 endopodite with one seta and no spines, both in proximal and medial segments, and three setae and no spines in the distal segment. Also, Le5 had four setae and no spines in the distal segment was reported in H. scutigerulus females.

In the present study, it was found that the medial segment of the Le4 endopodite of the H. scutigerulus females had one element, which was probably a spine and not a seta as proposed by Cressey (1983), and the distal segment of Le5 had four setae, as also observed by Cressey (1983). In addition, for the males, the distal segment of the Le4 endopodite had one seta and one spine, according to Cressey (1983). In the present study, it was not possible to discern whether there were two or three elements in the distal segment of the Le4 endopodite for the males.

Table 2.
Setation of legs (Le) of the Hamaticolax species (setae in arabic, spines in roman numerals).

*According to Cressey (1969), three terminal spines or setae. **Textual information of Hanan (1976) is different from his schematic drawings. ***According to schematic drawnings of Oldewage (1994). ****According to schematic drawnings of Cressey (1969), setae or spines.

The parasitological indices of H. scutigerulus in P. maculatus examined in Brazil were lower than those found for Bomolochus soleae Claus, 1864, in Soleasolea in Portugal (Durieux, Marques, Sasal, Bégout, & Cabral, 2007). Similarly, Tavares and Luque (2003) described Hamaticolaxunisagittatus (Tavares & Luque, 2003) (= Acantholochus unisagittatus sp. nov.) in Centropomus undecimalis in Rio de Janeiro, with high prevalence and mean abundance. Pseudupeneus maculatus has also been found to be parasitized by two other species of Bomolochidae: Orbitacolax analogus Vervoort (1969) and Orbitacolax hapalogenyos (Yamaguti & Yamasu, 1959 – Maran et al., 2014) on the gills of fish in Belize (Cressey & Cressey, 1989). On the other hand, all of the present material examined was H. scutigerulus.

The ventral body structures and hooks of the antennae in the family Bomolochidae are adapted so as to allow the parasite to become attached to the host on the gills, internal wall of the operculum, fins and integument, and around the eyes (Radhakrishnan & Nair, 1983, Boxshall, 2005).

In conclusion, some morphometric differences in the composition of the setae and spines of the leg armor can be found in the genus Hamaticolax. Nonetheless, these constitute the most valid characteristic for specific identification.

The authors thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for research grant to M. L. Martins (305869/ 2014-0).