New morphological data on Colobomatus belizensis Cressey and Schotte, 1983 (Copepoda: Philichthyidae), parasitic in the mandibular canals of the white grunt, Haemulon plumierii (Lacepède, 1801) (Actinopterygii: Haemulidae) off Rio de Janeiro, southeastern Brazil

ABSTRACT

New morphological and morphometric data on females of Colobomatus belizensis Cressey and Schotte, 1983 is provided based on specimens collected from the mandibular canals of Haemulon plumierii (Lacepède) in Sepetiba Bay, state of Rio de Janeiro, southeastern Brazil. Specimens were identified as C. belizensis by the presence of a smooth, not bifid, anterior cephalic process, two pairs of dorsolateral thoracic processes with rounded tips, and third abdominal somite with one pair of lateral process with rounded tips. The original description of the female of C. belizensis was superficial, lacking details on some structures with taxonomic value that are fully described here, such as the processes ornamented with six sensilla, caudal rami armed with 11 elements, as well as the armature of the legs and ornamentation of the buccal cone. These new data add robustness to the diagnosis and confirm the validity of C. belizensis, contributing to the taxonomy of the genus Colobomatus as a whole.

Keywords:
coast of Rio de Janeiro; Cyclopoida; haemulid fish; parasitic copepods; philichthyid

INTRODUCTION

The family Philichthyidae Vogt, 1877 comprises copepods with highly modified bodies, commonly found in subcutaneous spaces that are associated with the sensory canals of the lateral line and skull bones of marine actinopterygians and, rarely, elasmobranchs (Boxshall and Halsey, 2004; Paschoal et al., 2022). Currently, this family contains 97 species distributed in nine genera, of which ColobomatusHesse, 1873 is the richest genus with 76 valid species, followed by SarcotacesOlsson, 1872 with nine species; ProcolobomatusCastro-Romero, 1994 with three species; LernaeascusClaus, 1886, LeposphilusHesse, 1866, and SphaeriferRichiardi, 1876 with two species; and ColobomatoidesEssafi and Raibaut, 1980, IchthyotacesShiino, 1932, and PhilichthysSteenstrup, 1862 with one species each (Paschoal et al., 2022; Walter and Boxshall, 2024).

According to some authors, current knowledge about the distribution and diversity of philichthyids can be inaccurate, since their sites of infestation are difficult to access and normally overlooked during fish dissections. Moreover, their uneven global distribution may be explained by the concentration of research effort in certain regions of the planet, which becomes more evident when compared with other groups of parasitic copepods (Kabata, 1979; Madinabeitia et al., 2013; Paschoal et al., 2016a; Couto and Paschoal, 2021). Along the Brazilian coast, ten species of philichthyids have been recorded parasitizing fish; nine of which belong to Colobomatus and one to Leposphilus (see Paschoal et al., 2022).

Colobomatus belizensisCressey and Schotte, 1983 was originally described by Cressey and Schotte (1983) based on females and males collected from a wide spectrum of haemulid fish, totaling 11 host species (see Paschoal et al., 2016a). Subsequently, this species was revisited by Luque and Takemoto (1996), in a study on parasitic copepods of Haemulon atlanticus Carvalho, Marceniuk, Oliveira and Wosiacki (reported as H. steindachneri) off Brazil, who provided new morphological data on the thoracic somites. Despite the remarkable sampling effort and the relevance of the previous studies that analyzed C. belizensis, the morphology of the species remains poorly detailed, lacking accurate description of some taxonomically important structures, which can hinder its correct diagnosis by other parasitologists.

During a survey of philichthyid copepods of Brazil, six specimens of C. belizensis were retrieved from the mandibular canals of Haemulon plumierii (Lacepède) (Haemulidae). To improve our knowledge of philichthyid copepods and to provide new morphological data on C. belizensis, a detailed redescription of the species based on females is given here.

MATERIALS AND METHODS

Eighteen specimens of H. plumierii (body length 13.7-31.7 cm; mean ± standard deviation 24.2 ± 4.7 cm) were caught by artisanal fishermen, between January and April 2022 in Sepetiba Bay (22°57′18″S 43°54′44″W), state of Rio de Janeiro, Brazil. Fish were kept in thermal boxes filled with ice and transported to the laboratory for analysis. Copepods were collected using the procedures described by Madinabeitia and Nagasawa (2012), fixed and preserved in 80% ethanol. For microscopical observation, specimens were cleared in 85% lactic acid and the appendages were dissected and examined using the wooden slide procedure described by Humes and Gooding (1964). Drawings were made with the aid of a Zeiss Standard 20 microscope (Carl Zeiss Foundation, Germany) attached to a drawing tube. Measurements were made using an ocular micrometer and are given as range followed by mean and standard deviation in parentheses, all in micrometers unless otherwise stated. The material of C. belizensis deposited in the carcinological collection of the Museu Nacional do Rio de Janeiro Brazil (catalogue numbers MNRJ 4428; 4429; 4430), studied by Luque and Takemoto (1996), was also examined for confirmation of morphological data. The descriptive terminology and classification follow Boxshall and Halsey (2004). Prevalence and intensity are according to Bush et al. (1997). Host identification was based on the key by Figueiredo and Menezes (1980); nomenclature and classification were updated according to Eschmeyer’s Catalog of Fishes (Van der Laan et al., 2024). Voucher specimens were deposited in the collection of the Museu de Zoologia da Universidade de São Paulo (MZUSP), Brazil.

SYSTEMATICS

Order Cyclopoida Burmeister, 1834

Family Philichthyidae Vogt, 1877

Genus Colobomatus Hesse, 1873

Colobomatus belizensis Cressey and Schotte, 1983

(Fig. 1)

Figure 1.
Colobomatus belizensis (adult female). A, Habitus, ventral, an = antennule, p1 = leg 1, p2 = leg 2, p3 = leg 3, p4 = leg 4, p6 = leg 6; B, habitus, lateral, p1 = leg 1, p2 = leg 2, p3 = leg 3, p4 = leg 4, p6 = leg 6; C, detail of thoracic process, ventral, se = sensillium; D, detail of caudal rami, lateral, se = sensillium, black arrow = seta, white arrow = seta stylet-like; E, antennule, ventral, black arrows = aesthetascs; F, buccal area, ventral, a = antenna, me = maxillule, ma = maxilla and la = labium, ventral; G, leg 1, ventral; H, leg 2, ventral; I, leg 3, ventral; J, leg 4, ventral; K, leg 6, ventral. Scale bars: A, B = 2000 µm; C = 30 µm; D-F = 20 µm; G = 25 µm; H, I = 10 µm; J, K = 5 µm

Type-host and type-locality. The blue-striped grunt Haemulon sciurus (Shaw) (Haemulidae); Caribbean Sea, Belize, Carrie Bow Cay (geographic coordinates not available) (Cressey and Schotte, 1983).

Host and locality of presently reported material. The white grunt, Haemulon plumierii (Lacepède); Sepetiba Bay, (22°57′18″S 43°54′44″W), state of Rio de Janeiro, Brazil.

Site in host. Mandibular canals.

Prevalence and mean intensity: 22% (four infected fish out of 18 examined); mean of 1.5 copepods per infected fish [range 1-2].

Voucher specimens: Four females (MZUSP-46885); two specimens were dissected and kept in the personal collection of the corresponding author.

Redescription of adult female [based on six specimens]. Body elongate and transformed (Fig. 1 A , B), 4.55-13.23 mm (8.44 ± 3.54 mm); thoracic and abdominal processes (Fig. 1 C ) with rounded tips, bearing six sensilla: four apical, one on inner margin and one on outer margin. Cephalosome (Fig. 1 A , B) ovoid, longer than wide, 436-866 (615 ± 169) × 355-502 (415 ± 66), bearing dorsal hood shaped process (Fig. 1 A , B), 484-833 (656 ± 147) long. First to fourth pedigerous somites fused, forming ovoid thoracic region, 1620-4420 (3000 ± 1300) × 950-1830 (1420 ± 380), representing about 28-34% (31 ± 3) of total body length. Thoracic region with 2 pairs of tapering processes emerging from dorsolateral surface: anterior processes equal in size, 1380-3000 (2220 ± 700); posterior processes unequal, left process 1850-5300 (3400 ± 1250) long, right process 1200-3800 (2510 ± 900) long. First to fourth pairs of legs located on ventral surface of fused somites. Fifth pedigerous somite squared and separated from preceding fused somites by slight constriction, 389-963 (657 ± 216) × 436-1211 (771 ± 319). Genital somite wider than long, 443-702 (572 ± 115) × 573-1192 (952 ± 267), with weak lateral protrusions. Abdomen 4-segmented, first somite longer than wide, 396-998 (628 ± 258) × 359-816 (600 ± 199), second and third somites wider than long, 372-834 (598 ± 215) × 354-900 (619 ± 243) and 267-655 (424 ± 170) × 283-762 (535 ± 205), respectively. Third abdominal somite with pair of lateral processes, 1218-3847 (2682 ± 1013) long. Last abdominal somite shorter, fused to caudal rami. Caudal rami (Fig. 1 D ) armed with 1 seta on inner margin, plus 2 apical setae stylet-like and 8 sensilla: 2 on inner margin, 4 on outer margin and 2 on apical margin.

Antennule (Fig. 1 E ) indistinctly 4-segmented, with armature formula 5, 1 + aesthetasc, 1 + aesthetasc, 6; all setae naked. Antenna modified, forming buccal capsule enclosing mouthparts, and bordered posteriorly by simple and undivided labium (Fig. 1 F ). Labrum not observed. Maxillule (Fig. 1 F ) minute and located at anterior part of buccal capsule, 1-segmented, bearing 2 apical setae of unequal sizes. Maxilla (Fig. 1 F ) robust and located in middle part of buccal capsule, apparently 2-segmented, both segments with 1 thick distal element ornamented with row of spinules. Maxilliped absent. Posterior rim of buccal capsule divided.

Legs 1 and 2 inserted in rugose area. Leg 1 (Fig. 1 G ) biramous, located immediately posterior to junction of cephalosome and first pedigerous somite. Protopod with 1 outer seta; exopod 1-segmented, armed with 1 distal seta and 1 outer seta of unequal sizes, all setae naked; endopod vestigial, unsegmented and unarmed. Leg 2 (Fig. 1 H ) biramous, posterior to leg 1, in second part of fused somites; protopod armed with outer seta; exopod 1-segmented, armed with 1 distal seta and one inner lateral seta of similar sizes; endopod vestigial, unsegmented, and armed with 2 distal setae of unequal sizes, all setae naked. Leg 3 (Fig. 1 I ), located in third part of fused somites and reduced to small lobe bearing 2 naked setae of unequal sizes. Leg 4 (Fig. 1 J ), located in last part of fused somites (fourth pedigerous somite), and represented by lobe bearing one naked seta. Leg 5 absent. Leg 6 (Fig. 1 K ) located near genital apertures, represented by 2 naked setae of unequal sizes.

DISCUSSION

Females of the genus Colobomatus have highly modified bodies, usually elongated (comprising cephalosome, fused thoracic somites, abdomen, and caudal rami), with at least two pairs of divergent lateral processes in the thoracic region that are arranged in an X-shaped pattern, and leg 4 reduced to a single seta or completely absent (West, 1992; Boxshall and Halsey, 2004; Pereira et al., 2012; Uyeno and Nagasawa, 2021). So far, 76 species of Colobomatus have been described (Paschoal et al., 2022), but only six congeners have been reported parasitizing haemulid fish worldwide, namely, C. belizensis, Colobomatus caribbeiCressey and Schotte, 1983; Colobomatus hispidusWest, 1992; Colobomatus mackayiWest, 1992; Colobomatus miniprocessusCastro Romero and Muñoz, 2011; and Colobomatus quadrifariusCressey and Schotte, 1983 (West, 1992; Paschoal et al., 2016b). Nevertheless, the presently reported specimens were identified as C. belizensis based on the presence of a smooth, not bifid, anterior cephalic process, two pairs of dorsolateral, not globose, thoracic processes distally rounded, with the left posterior thoracic process longer than the others, and third abdominal somite with a pair of distally rounded lateral processes (Cressey and Schotte, 1983; Luque and Takemoto, 1996). The newly collected females sampled in Sepetiba Bay have a body length (4.55-13.23 mm) overlapping that of the type specimens collected by Cressey and Schotte (1983), which are originally from the Caribbean Sea (body length 4.13-9.38 mm), and the specimens collected by Luque and Takemoto (1996) (7.20-9.15 mm) from Rio de Janeiro, Brazil.

The morphology of the body of females is the most important diagnostic tool for Colobomatus spp. (Paschoal et al., 2022). Furthermore, detailed descriptions of the size, proportion, number and ornamentation of appendages, permit researchers to differentiate the congeners, and reinforce the value of morphological data (West, 1992; Kim and Moon, 2013; Paschoal et al., 2016a). Existing descriptions of females of C. belizensis have been superficial, lacking morphometric data and details on some taxonomically important structures, such as the proportion and ornamentation of body processes and of small appendages. The thoracic processes and caudal rami were originally described as “simple and with rounded tips” (see Cressey and Schotte, 1983), but according to the present observations, the thoracic processes were clearly ornamented with six elements and the caudal rami were armed with 11 elements. Our results also revealed for the first time the armature of legs and ornamentation of buccal cone, which have been suggested as relevant features for supplementing the specific diagnosis of Colobomatus spp. (see Paschoal et al., 2022). These results highlight the real complexity associated with the morphology of C. belizensis females and, consequently, the importance of revisiting and redescribing those species that remain poorly described. These facts are particularly relevant in relation to Colobomatus, since several species were described in the late 19^th to the mid-20^th centuries and are in critical need of adequate redescription (Paschoal et al., 2022).

The host specificity in Colobomatus has been debated based on two main hypotheses: (1) these parasites are highly specific, commonly restricted to a single host species or rarely two; (2) these parasites can have a broader host range, being specific at the genus, or even at the family, level regarding host taxa (Grabda, 1991; Hayward, 1996). In this sense, C. belizensis better fits the second case, since this copepod has been recorded in 11 species of haemulid fish (Cressey and Schotte, 1983). However, Grabda’s (1991) proposal currently appears to be more accurate for explaining the host specificity of most Colobomatus spp., since 63% of the congeners (48 out of 76 species) have been reported from a single host species (Paschoal et al., 2016 b ; Uyeno and Nagasawa, 2021; Paschoal et al., 2022).

It should be mentioned that the real host-parasite associations regarding species of Colobomatus may be well underestimated, due to the low sampling effort directed to philichthyids as well as to their site of infection that is frequently overlooked during fish dissections (Madinabeitia et al., 2013; Paschoal et al., 2022). Therefore, further investigations are necessary to improve our knowledge of the diversity and distribution of Colobomatus, as well as to clarify the host specificity patterns of these parasites.

ACKNOWLEDGMENTS

We thank the anonymous reviewers for their suggestions.

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ADDITIONAL INFORMATION AND DECLARATIONS

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  All authors declare that they have reviewed the content of the manuscript and gave their consent to submit the document.
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  JVC was supported by a student fellowship from the Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior (CAPES), Brazil. FP was supported by the Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA, Process no. 84516/2022), Brazil.
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Edited by

• Associate Editor:
  Jessica Colavite

Edited by

• Editor-in-chief:
  Christopher Tudge

Publication Dates

• Publication in this collection
  10 Jan 2025
• Date of issue
  2025

History

• Received
  23 Apr 2024
• Accepted
  04 Sept 2024
• Corrected
  28 Jan 2025