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Zoologia (Curitiba)

Print version ISSN 1984-4670On-line version ISSN 1984-4689

Zoologia (Curitiba) vol.33 no.4 Curitiba  2016  Epub Sep 05, 2016

http://dx.doi.org/10.1590/S1984-4689zool-20160022 

TAXONOMY AND NOMENCLATURE

A new species of Diaphorocleidus (Monogenea: Ancyrocephalinae) from the gills of Argonectes robertsi (Characiformes) and new records of dactylogyrids parasitic on fishes from the Xingu River, Amazon Basin, Brazil

Juliana Moreira1 

Tomáš Scholz2 

José Luis Luque3  * 

1Programa de Pós-Graduação em Biologia Animal, Universidade Federal Rural do Rio de Janeiro. 23890-900 Seropédica, RJ, Brazil.

2Institute of Parasitology, Biology Centre of the Czech Academy of Sciences. Branišovská 31, 370 05 České Budĕjovice, Czech Republic.

3Departamento de Parasitologia Animal, Universidade Federal Rural do Rio de Janeiro. Caixa postal 74540, 23851-970 Seropédica, RJ, Brazil.

ABSTRACT

Diaphorocleidus altamirensis sp. nov., parasitic on the gills of Argonectes robertsi Langeani, 1999 from the Xingu River, northern Brazil, is described. The new species differs from its six congeners by the morphology of the male copulatory organ (which comprises a coil of six rings), by the midventral vagina, and by the presence of only one pair of eyespots. It is the first species of Diaphorocleidus Jogunoori, Kritsky & Venkatanarasaiah, 2004 described from hemiodontid fishes. In addition, new host and geographical records of seven species of dactylogyrids found on fish from the Xingu River are reported.

KEY WORDS: Dactylogyridae; Hemiodontidae; Monogenea; Neotropics; Xingu River

Monogeneans represent one of the main components of the parasite fauna of freshwater fishes in the Neotropical Region, and as many as 629 species have been reported by Cohen et al. (2013) from South America, most of which belonging to the Dactylogyridae and parasitizing on the gills of teleost fishes. However, the number of species of these ectoparasites has increased steadily, with descriptions of dozens new species in recent decades, especially from characiform fishes (Cohen et al. 2012, Moreira et al. 2015).

One of 39 genera of dactylogyrids parasitic on characiform fishes from South America, Diaphorocleidus (Monogenea: Dactylogyridae) was proposed by Jogunoori et al. (2004), with D. armillatus Jogunoori, Kritsky & Venkatanarasaiah, 2004 from the Neotropical Gymnocorymbus ternetzi (Boulenger, 1895) (Characidae) as the type species, introduced to India via the aquarium trade. They also proposed three new combinations, D. affinis (Mizelle, Kritsky & Crane, 1968) (syn. Urocleidoides affinis Mizelle, Kritsky & Crane, 1968), D. kabatai (Molnar, Hanek & Fernando, 1974) (syn. U. kabatai Molnar, Hanek & Fernando, 1974) and D. microstomus (Mizelle, Kritsky & Crane, 1968) (syn. U. microstomus Mizelle, Kritsky & Crane, 1968). At present, Diaphorocleidus includes six species, i.e., D. affinis (Mizelle, Kritsky & Crane, 1968) Jogunoori, Kritsky & Venkatanarasaiah, 2004 from Bryconops affinis (Günther, 1864) (= Creatochanes affinis ) (Iguanodectidae) in Brazil, D. armillatus , D. kabatai (Molnar, Hanek & Fernando, 1974) Jogunoori, Kritsky & Venkatanarasaiah, 2004 from Astyanax bimaculatus (Linnaeus, 1758) (Characidae) in Trinidad, D. microstomus (Mizelle, Kritsky & Crane, 1968) Jogunoori, Kritsky & Venkatanarasaiah, 2004 from Hemigrammus microstomus Durbin, 1918 (Characidae) in Brazil, D. orthodusus Mendoza-Franco, Reina & Torchin, 2009 from Astyanax orthodus Eigenmann, 1907 (Characidae) in Panama and D. petrosusi Mendoza-Franco, Aguirre-Macedo & Vidal-Martínez, 2007 from Brycon petrosus Meek & Hildebrand, 1913 (Bryconidae) also in Panama (Jogunoori et al. 2004, Mendoza-Franco et al. 2007, 2009). Diaphorocleidus kabatai was also recorded from Steindachnerina insculpta (Fernandez-Yépez, 1948) (Curimatidae) and from Astyanax altiparanae Garutti & Britski, 2000, both in Brazil (Almeida & Cohen 2011, Acosta et al. 2013). In addition, Camargo et al. (2015) reported Diaphorocleidus sp. from Ancestrorhynchus lacustris (Lütken, 1875) (Ancestrorhynchidae) also in Brazil.

Examination of fishes from the lower reach of the Xingu River near Altamira, a tributary of the Amazon River in Brazil (State of Pará), has revealed dactylogyrid monogeneans on the gills of several fishes, including Argonectes robertsi Langeani, 1999 (Characiformes: Hemiodontidae). This fish occurs in the Tapajós, Xingu, Tocantins and Capim River basins (Froese & Pauly 2015). To date, only two monogeneans have been recorded parasitizing hemiodontids in South America, i.e, Cleidodiscus microcirrus Price & Schlueter, 1967 and Monocleithrium lavergneae Price & McMahon, 1966, both reported from Hemiodus semitaeniatus Kner, 1858 in Brazil. In contrast, no data exist on the parasites of A. robertsi (see Cohen et al. 2013).

Herein, we describe a new species of Diaphorocleidus collected from A. robertsi from the Xingu River in Brazil. In addition, several new host and geographical records of dactylogyrids parasitizing fishes from the Xingu River are provided.

MATERIAL AND METHODS

Fish were collected by local fishermen with nets and hooks in April 2013 from the Xingu River, a tributary of the Amazon River, around Altamira (3°12'S, 52°12'W), state of Pará, Brazil. Gills excised from fish were placed in Petri dishes with tap water and examined for monogeneans using dissecting microscope. Some monogeneans found were fixed in a mixture of glycerin-ammonium picrate (GAP) to study sclerotized structures. After morphological evaluation, the specimens were remounted, dehydrated and mounted in Canada balsam following the procedure of Ergens (1969). Other specimens were fixed in 4% hot formalin, stained with Gomori's trichrome and mounted in Canada balsam to study internal organs; some worms were mounted in Gray and Wess medium (Humason 1979) to study sclerotized structures. Drawings were made with the aid of an Olympus BX53 microscope (Olympus Corporation, Tokyo, Japan) equipped with a drawing tube. Measurements, all in micrometers, represent straight-line distances between extreme points and are expressed as the range followed by the mean and number (n) of structures measured in parentheses; body length includes that of the haptor. Numbering (distribution) of hook pairs follows Mizelle (1936) and Mizelle & Price (1963). Type and voucher specimens were deposited in the Helminthological Collection of Institute Oswaldo Cruz (CHIOC), Rio de Janeiro, Brazil.

TAXONOMY

Dactylogyridae Bychowsky, 1933

Ancyrocephalinae Bychowsky, 1937

Diaphorocleidus altamirensis sp. nov.

Figs. 1-8

urn:lsid:zoobank.org:act: 4E69D9B9-3DE2-44AF-91E3-1D93BC1B61CC

Description (based on 6 specimens): Body fusiform 345-414 (367, n = 6) long; greatest width 53-68 (62, n = 6) usually at level of gonads. Cephalic lobes poorly developed; 3 bilateral pairs of head organs; cephalic glands indistinct. Eyespots 2; accessory granules present in cephalic region. Pharynx spherical 13-24 (17, n = 6) in diameter; esophagus moderately long. Peduncle broad; haptor hexagonal, 56-71 (64, n = 6) wide. Ventral anchor 45-50 (47, n = 6) long, with well-developed and elongate superficial root, shorter deep root, curved shaft and point; base 21-26 (23, n = 6) wide. Dorsal anchor 33-36 (34, n = 6) long, with well-developed superficial root, short deep root, straight shaft and curved point; base 14-20 (17, n = 6) wide. Ventral bar 40-57 (44, n = 6) long, with medial suture and expanded ends; dorsal bar 24-36 (30, n = 6), slender, widely U-shaped, with slightly expanded ends. Hooks similar each with protruding thumb, curved shaft and point, dilated shank; pairs 1 and 5 reduced in size; filamentous hooklet (FH) loop ⅓-1/2 shank length; hook pairs 1, 5 - 9-13 (11, n = 6) long; hook pair 2 - 16-20 (18, n = 6) long; hook pair 3 - 16-26 (20, n = 6); hook pairs 4, 6, 7 - 11-24 (19, n = 6) long. MCO comprising a delicate coil of 6 counterclockwise rings, base with lateral flange, diameter of first ring 8-12 (10, n = 5). Accessory piece 14-30 (22, n = 5) long, comprising two articulated subunits, distal subunit bifurcate, proximal subunit curved and elongate, serving as guide for MCO. Vaginal aperture midventral, a coiled tube leading into a medial seminal receptacle anterior to germarium. Gonads overlapping; germarium 40-54 (45, n = 3) long. Testis dorsal, slightly visible at end of germarium; seminal vesicle a distal expansion of vas deferens; prostatic reservoir single. Oviduct, ootype and uterus not observed. Vitellarium scattered throughout trunk, except in regions of reproductive organs.

Figures 1-8 Diaphorocleidus altamirensis sp. nov.: (1) whole mount (composite, ventral view); (2) ventral anchor; (3) dorsal anchor; (4) ventral bar; (5) dorsal bar; (6) hook (pair 2); (7) hook, pair 5; (8) copulatory complex (dorsal). Scale bars: 1 = 100 µm, 2-5 = 25 µm, 6-7 = 10 µm, 8 = 20 µm. 

Type host: Argonectes robertsi Langeani, 1999 (Characiformes, Hemiodontidae).

Site of infection: Gills.

Type locality: Xingu River around Altamira (3°12'S, 52°12'W), state of Pará, Brazil.

Type specimens: Holotype and five paratypes deposited as CHIOC 38406a-f.

Etymology: This species is named for the type locality from which it was collected.

Remarks. Diaphorocleidus includes species with overlapping gonads, submarginal sinistral vaginal pore, a coiled male copulatory organ with counterclockwise rings, unarticulated to accessory piece and hook shank with two subunits. The midventral vaginal aperture of D. altamirensis sp. nov. is the only major difference of this species from congeners, but this unusual vaginal morphology does not seem us to justify proposal of a new genus. In addition to the position of the vagina, D. altamirensis differs from all congeners by having a male copulatory organ with 6 counterclockwise rings (2-3 in D. affinis , 2 in D. armillatus , 1-11/2 in D. kabatai and in D. petrosusi , 11/2-21/2 in D. microstomus and 1 in D. orthodusus ), by the accessory piece comprising two subunits (distal bifurcate and proximal curved and elongate) and by the presence of just one pair of eyespots. Diaphorocleidus petrosusi also possesses an accessory piece subdivided in two parts, plate-shaped, but D. altamirensis sp. nov. can be easily distinguished by the haptoral structures and by the coiled vaginal tube (a nondilated sclerotized in D. petrosusi ), which is also an unique feature of this new species. None of the two dactylogyrids recorded from H. semitaeniatus in Brazil, i.e., C. microcirrus and M. lavergneae , shows similarity with D. altamirensis .

New host and geographical records. In addition to the new species described above, another seven species of gill monogeneans of the family Dactylogyridae were found on four species of fishes during parasitological surveys carried out in the Xingu River. All fishes represent new hosts of these monogeneans and except for Jainus amazonensis Kritsky, Thatcher & Kayton, 1980, all parasites are reported from the Xingu River, Amazon basin, for the first time (Table 1).

Table 1 New host and geographical records of dactylogyrids parasitizing fish from the Xingu River, Amazon basin, Brazil. 

Species Host Host family River basin/Country References
Characiformes
Apedunculata discoidea Cugliana, Cordeiro & Luque, 2009 (CHIOC 38405) Prochilodus lineatus, P. argenteus , P. nigricans* Characidae Paraná, São Francisco and Amazon (Brazil)** Cuglianna et al. (2009), Monteiro & Brasil-Sato (2014)
Jainus amazonensis Kritsky, Thatcher & Kayton, 1980 (CHIOC 38407) Brycon melanopterus, B. cephalus , Anostomoides passionis* Characidae and Anostomidae Amazon (Brazil and Peru) Kritsky et al. (1980), Andrade et al. (2001), Delgado et al. (2014)
Jainus leporini Abdallah, Azevedo & Luque, 2012 (CHIOC 38408) Leporinus copelandii, Anostomoides passionis* Anostomidae Southeast Atlantic, Amazon (Brazil)** Abdallah et al. (2012)
Jainus piava Karling, Bellay, Takemoto & Pavanelli, 2011 (CHIOC 38409) Schizodon borelli, Anostomoides passionis* (Anostomidae) Anostomidae Paraná, Amazon (Brazil)** Karling et al. (2011)
Tereancistrum toksonum Lizama, Takemoto & Pavanelli, 2004 (CHIOC 38411) Prochilodus lineatus, P. nigricans* Characidae Paraná (Argentina and Brazil), Amazon (Brazil)** Lizama et al. (2004), Chemes & Gervasoni (2013)
Perciformes
Sciadicleithrum kritskyi Bellay, Takemoto, Yamada & Pavanelli, 2009 (CHIOC 38410) Geophagus proximus, G. argyrostictus* Cichlidae Paraná, Amazon (Brazil)** Bellay et al. (2009)
Siluriformes
Amphocleithrium paraguayensis Price & Romero, 1969 (CHIOC 38404a-c) Pseudoplatystoma corruscans, P. fasciatum* , Pseudoplatystoma sp. Pimelodidae Paraguay-Paraná (Paraguay), Paraná (Argentina and Brazil), Amazon (Brazil)** Price & Romero (1969), Suriano & Incorvaia (1995), Takemoto et al. (2009)

*New host record, **New geographical record.

DISCUSSION

The present study provides the first data on the monogeneans parasites of A. robertsi . Currently the family Hemiodontidae comprises five genera and 31 species of fishes distributed in South America (Froese & Pauly 2015). They are poorly studied fishes and only very few species were examined for parasites (Azevedo et al. 2009, Cohen et al. 2013, Silva Júnior 2014), indicating that many new taxa of parasites can be discovered.

Species of Diaphorocleidus have been recorded from characiform fishes, mainly characids, in a large area which spans from Trinidad through Panama to Brazil, i.e., the Caribbean Region, Central America and South America. Most dactylogyrid monogeneans, including those of Ancyrocephalinae, are considered highly host-specific (Boeger & Vianna 2006). Therefore, such large distribution area is uncommon in species-poor Neotropical genera. However no information exists on interrelations of species of Diaphorocleidus to reconstruct possible evolutionary history of this monogenean group in the Neotropical region.

Diaphorocleidus altamirensis sp. nov. is the third species of the genus described in Brazil, but is the first species found on a hemiodontid, which also belongs to the order Characiformes. Diaphorocleidus can be easily distinguished from the other genera of dactylogyrids associated with hemiodontids, i.e., Cleidodiscus Mueller, 1934 and Monocleithrium Price &McMahon, 1966. Monocleithrium is a monospecific genus, with M. lavergneae as its type and only species, which is characterized by having two pairs of eyespots, tandem gonads, coiled MCO with accessory piece directly articulated, and dorsal bar absent. In contrast, Diaphorocleidus exhibits overlapping gonads, a MCO unarticulated to accessory piece and a pair of bars (one ventral and one dorsal). Cleidodiscus is a poorly known genus of ancyrocephaline monogeneans and its taxonomic status remains unclear, especially because inadequate descriptions of its species. Many of the species originally described as members of Cleidodiscus have been then transferred to other genera (e.g., Calpidothecium , Pithanothecium , Urocleidoides ; see Boeger & Vianna 2006, Cohen et al. 2013). Diagnostic features of Cleidodiscus are two pairs of eyespots, accessory piece generally articulated to MCO basally and the vagina usually present and opening at the left margin of the body near the middle length of the trunk, thus showing no similarity to Diaphorocleidus .

Except for J. amazonensis , all dactylogyrids collected from the Xingu River, represent new geographical records from the Amazon River basin; all of them also expand host ranges of respective species. The records of J. amazonensis , J. leporiniAbdallah, Azevedo & Luque, 2012, and J. piava Karling, Bellay, Takemoto & Pavanelli, 201 on Anostomoides passionis Santos & Zuanon, 2006 are noteworthy because they represent the first data on the parasites of this fish host, which has been described just recently.

Based on the study and other recent accounts on the monogenean parasites of fishes from the Xingu River (Moreira et al. 2015, Paschoal et al. 2016), we assume that the actual diversity of monogeneans in the Amazon River basin and South America in general is still poorly known and discovering many new taxa, especially on poorly studied fish hosts, can be anticipated.

ACKNOWLEDGEMENTS

We wish to thank Aldenice Pereira, Fabiano Paschoal and Philippe V. Alves for help with collecting and their parasitological examination and Emil J.H. Ruz, Universidade Federal do Pará - Altamira, for providing the facilities during the field trip. This study was supported by the 'Ciência sem Fronteiras' Brazilian program - visitant researcher modality (135/2012; stay of T. Scholz at the Universidade Federal Rural de Rio de Janeiro) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) grants to J.L. Luque (474077/2011-0, 304254/2011-8, 402665/2012-0). Tomáš Scholz was also supported by Institute of Parasitology of the Academy of Sciences of the Czech Republic (RVO60077344) and the Czech Science Foundation (project P505/12/G112). Juliana Moreira was supported by a student fellowship from CAPES (Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior, Brazil).

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Received: February 05, 2016; Revised: April 21, 2016; Accepted: June 14, 2016

*Corresponding author. E-mail: luqueufrrj@gmail.com

Author Contributions:

TS and JLL have collected the specimens; JM and JLL analyzed the specimens; JM, TS and JLL wrote the paper.

Competing Interests:

The authors have declared that no competing interests exist.

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