Research Article |
Corresponding author: Simone Chinicz Cohen ( scohen@ioc.fiocruz.br ) Academic editor: Patrick Mathews Delgado
© 2023 Carine Almeida Miranda Bezerra, Simone Chinicz Cohen, Yuri Costa de Meneses, Helyab Gabriel Chaves Neres, Diego Carvalho Viana, Marcia Cristina Nascimento Justo.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bezerra CAM, Cohen SC, de Meneses YC, Neres HGC, Viana DC, Justo MCN (2023) Two new species of Curvianchoratus (Monogenoidea, Dactylogyridae) parasitizing Psectrogaster amazonica (Characiformes, Curimatidae) and a new record for Curvianchoratus singularis in the Tocantins River, Maranhão, Brazil. ZooKeys 1172: 101-116. https://doi.org/10.3897/zookeys.1172.105500
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Several studies have demonstrated parasitism by monogenoids in characiform fish in the Neotropics. During studies on the helminth fauna of curimatids from the Tocantins River, specimens of Psectrogaster amazonica Eigenmann & Eigenmann, 1889 were examined and species of Curvianchoratus Hanek, Molnar & Fernando, 1974 were found. Species of the genus are characterized mainly by the complex shape of haptoral anchors with a modified dorsal anchor, composed by two subunits, dorsal-median and dorsal. To date, two species of Curvianchoratus are known to parasitize curimatid fishes: the type species Curvianchoratus hexacleidus Hanek, Molnar & Fernando, 1974 and Curvianchoratus singularis (Suriano, 1980). During examination of specimens of P. amazonica collected in the Tocantins River, Embiral, Imperatriz, Maranhão State, Brazil, two new species of Curvianchoratus were found and are described herein. Curvianchoratus psectrogasteri sp. nov. and Curvianchoratus dominguesi sp. nov. are characterized by possessing the male copulatory organ formed by a long cirrus and a claw-shaped accessory piece, connected to the base of the male copulatory organ by a ligament. The new species differs from the two known congeneric species mainly by the morphology of the dorsal-median and dorsal subunits of the dorsal anchor. Curvianchoratus psectrogasteri sp. nov. also differs from other species of the genus by the absence of the ventral bar and Curvianchoratus dominguesi sp. nov. by the size and shape of the ventral bar. An amendment to the diagnosis of Curvianchoratus is provided to accommodate the new species. The present study increases the number of Curvianchoratus species to four and extends the occurrence of the genus to the Tocantins-Araguaia Basin.
Curvianchoratus dominguesi sp. nov., Curvianchoratus psectrogasteri sp. nov., ectoparasites, fish parasite, helminth fauna, Neotropical Region, taxonomy, Tocantins-Araguaia Basin
Characiformes is one of the main orders of Ostariophysi, which occur exclusively in freshwater, with the greatest diversity and species richness concentrated in the Neotropical Region. These fish represent the historical connection between Africa and South America, which can be proven through their distribution and the presence of fossil records (
Psectrogaster Eigenmann & Eigenmann, 1889 is a morphologically diverse lineage of Curimatidae, distributed in streams, rivers, and still waters throughout the drainage basins of the Orinoco River, Essequibo River, Amazon River, Paraguay-Parana River, and some of the rivers of northeastern Brazil (
Several studies have demonstrated parasitism by monogenoids in Curimatidae fish in the Neotropics (Table
Parasite | Host | Locality | References |
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Anacanthoroides mizellei Kritsky &Thatcher, 1976 | Steindachnerina insculpta | Brazil |
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Annulotrematoides amazonicus Kritsky & Boeger, 1995 | Psectrogaster rutiloides | Brazil |
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Annulotrematoides bonaerensis Rossim & Timi, 2016 | Cyphocharax voga | Argentina |
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Cacatuocotyle paranaensis Boeger, Domingues & Kritsky, 1997 | Cyphocharax nagelii | Brazil |
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Characithecium chascomusensis (Suriano, 1981) Rossin & Timi, 2014 | Cyphocharax gilbert | Argentina |
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C. voga |
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Curvianchoratus hexacleidus Hanek, Molnar & Fernando, 1974 | Cyphocharax nagelii | Brazil |
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Curvianchoratus singularis (Suriano, 1980) |
C. gilbert | Argentina |
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C. voga |
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Cyphocharax nagelii | Brazil |
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Cyphocharax modestus |
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Steindachnerina insculpta |
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Diaphorocleidus kabatai Mendoza-Franco, Reina & Torchin, 2009 | Stendachnerina insculpta | Brazil |
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Euryhaliotrema chaoi Kritsky & Boeger, 2002 | Steindachnerina insculpta | Brazil |
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Paranaella luquei Kohn, Baptista-Farias & Cohen, 2000 | Stendachnerina brevipinna | Brazil |
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Philocorydoras margolisi (Molnar, Hanek & Fernando, 1974) Yamada, Brandão, Yamada & Silva, 2015 | Steindachnerina insculpta | Brazil |
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Rhinoxenus guianensis Domingues & Boeger, 2005 | Curimata cyprinoides | French Guyana |
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Urocleidoides curimatae Molnár, Hanek & Fernando, 1974 | Steindachnerina argentea | Trinidad |
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Urocleidoides paratriangulus Freitas, Bezerra, Meneses, Justo, Viana & Cohen, 2021 | Psectrogaster amazonica | Brazil |
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Cyphocharax gouldingi | |||
Urocleidoides surianoae Rossim & Timi, 2016 | Cyphocharax voga | Argentina |
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Urocleidoides tocantinensis Freitas, Bezerra, Meneses, Justo, Viana & Cohen, 2021 | Psectrogaster amazonica | Brazil |
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Urocleidoides triangulus (Suriano, 1981) Rossim & Timi, 2016 | C. nagelii | Brazil |
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Cyphocharax modestus |
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C. gilbert |
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Argentina |
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Monogenoidea Bychowsky, 1937 are, in general, ectoparasites that mainly infect fish species (
Curvianchoratus was proposed by Hanek, Molnar and Fernando (1974) to accommodate Curvianchoratus hexacleidus Hanek, Molnar & Fernando, 1974, a parasite of the characiform Steindachnerina argentea (Gill, 1858) (syn. Curimatus argenteus Gill, 1858) from the Arouca River, Trinidad. The main characteristic of Curvianchoratus is the haptor with a modified dorsal anchor, composed of two subunits, which is a unique shape within Dactylogyridae.
To date, two species of Curvianchoratus are known, both parasites of curimatid fishes: the type species C. hexacleidus and Curvianchoratus singularis (Suriano, 1980), originally described as Notodiplocerus singularis by
During studies on the helminth fauna of curimatids from the Tocantins River, specimens of P. amazonica were examined and species of Curvianchoratus were found. The present paper presents an emended diagnosis of Curvianchoratus, with the proposal of two new species and a new geographical record for C. singularis.
From July 2018 to April 2022, 136 samples of P. amazonica (average 14 cm in standard length and average 62 g in weight) were collected in the Tocantins River, close to the urban perimeter of Imperatriz, in the village of Embiral, state of Maranhão, Brazil (5°27'50’’S, 47°33'48’’W) (Fig.
Scheme of measurements of the sclerotized structures of haptoral anchors of Curvianchoratus spp. A dorsal-median subunit and B dorsal subunit of Curvianchoratus psectrogasteri sp. nov. C dorsal-median subunit D dorsal subunit of Curvianchoratus dominguesi sp. nov. (sf) shaft, (pt) point, (dr) deep root, (sr) superficial root, (b) base, (tl) total length, (wd) width.
In the present study, a total of 87 monogenoid specimens were collected, being: 68 Curvianchoratus psectrogasteri sp. nov., eight Curvianchoratus dominguesi sp. nov. and 11 Curvianchoratus singularis.
Class Monogenoidea Bychowsky, 1937
Subclass Polyonchoinea Bychowsky, 1937
Order Dactylogyridea Bychowsky, 1937
Tegument smooth, thin. Body elongated; divisible into cephalic area, trunk, peduncle, and haptor. Terminal and lateral cephalic lobes developed or not; head organs and cephalic glands present. Eyespots present or absent. Mouth subterminal, midventral, prepharyngeal. Pharynx muscular; esophagus short. Intestinal caeca two, not presenting diverticula. Common genital pore midventral near the level of intestinal bifurcation. Gonads intercaecal, overlapping or not; testis dorsal to germarium. Seminal vesicle large, dilated portion of vas deferens; prostatic reservoir single. Copulatory complex comprising male copulatory organ (MCO) and accessory piece; MCO consisting of sclerotized coiled tube with counterclockwise rings, which make a short turn on itself near the base; cirrus and accessory piece articulated basally. Accessory piece with bifurcated distal portion, pincer-shaped. Ovary pretesticular. Vagina medial or sinistral. Vitellaria well developed, coextensive with intestinal ceca, absent from regions of other reproductive organs. Peduncle short, haptor subquadrate. Ventral bar present or absent. Dorsal bar absent. Ventral anchor of dactylogyrid type. Dorsal anchor modified, composed by two subunits, dorsal-median and dorsal, forming a full circle, the shaft of the dorsal subunit passes over the superficial root of the dorsal-median subunit anchor. Hooks 14; 5 pairs ventral, 2 pairs dorsal, with inflated base and slender shank. Parasites of curimatid fishes.
Curvianchoratus was proposed to accommodate Curvianchoratus hexacleidus Hanek, Molnár & Fernando, 1974, a parasite of the characiform S. argentea from the Arouca River, Trinidad (
Psectrogaster amazonica Eigenmann & Eigenmann, 1889 (Curimatidae).
Embiral, rural zone (5°27'50"S, 47°33'48"W), municipality of Imperatriz, Maranhão State.
22.06% prevalence; 68 total number of parasites; 2.27 ± 1.75 mean intensity; 1-15 range of intensity.
Holotype
:
The specific name of the species is derived from the generic name of the host.
Based on 43 specimens: 21 mounted in Gomori’s trichrome and 22 mounted in Hoyer’s medium: Body elongated, 425–883 (665; N = 30) long, 135–520 (308; N = 30) wide. Tegument smooth. Cephalic region with poorly-developed cephalic lobes; five pairs of head organs; cephalic glands lateral to pharynx. Eyes 4; anterior pair smaller than posterior. Pharynx round, muscular, 32–75 (50; N = 18) long, 32–87 (50; N = 18) wide; esophagus short. Peduncle inconspicuous, followed by a small haptor compared to body size, 125–292 (225; N = 21) wide. Ventral bar absent. Ventral anchor with inconspicuous deep root and elongated superficial root, long and slightly curved shaft; straight tip, not passing from the level of the tip of the superficial root, 21–30 (24; N = 43) long, base, 10–13 (12; N = 43) wide. Dorsal anchor complex heavily modified, composed by 2 subunits: dorsal-median and dorsal. Dorsal-median subunit strongly curved, 52–87 (64; N = 34) long and base, 41–63 (49; N = 48), with the robust shaft, 63–92 (78; N = 34) long, subdivided into two pieces, one anterior, with sclerotized ridges, and one posterior, lightly sclerotized, point sickle-shaped, articulated with the dorsal subunit, 4–7 (6; N = 36) long; deep and superficial roots well developed, crested-shaped, 12–27 (16; N = 46) long and 10–20 (14; N = 37) long, respectively. Dorsal subunit large, irregular, 40–65 (48; N = 15) long well-developed deep root 19–22 (20; N = 17), superficial root absent, and median region expands to form a rounded structure, 32–57 (40; N = 23) wide. Hooks similar in shape, pairs 1 and 5 smaller than others, 11–14 (12; N = 27) long, pairs 2–4,6,7 with erected thumb, curved shaft, short point, shank with dilated bulb at distal end, 13–18 (16; N = 95). Copulatory complex comprising male copulatory organ (MCO) and articulated accessory piece. Male copulatory organ composed by a tubular sclerotized cirrus that makes a short turn on itself near the base and spirals halfway towards the tip of the cirrus, with sclerotized base possessing delicate membrane, 47–60 (53; N = 5) in total length. Accessory piece, 25–30 (26; N = 5) long, claw-shaped, with dissimilar tip sizes, the smaller tip serves as guide to MCO, hinged by a ligament to the base of the cirrus. Testis oval, dorsal to germarium; seminal vesicle a distal enlargement of vas deferens; prostatic reservoir single, posterior to MCO. Germarium pretesticular, 62–122 (102; N = 7). Vaginal aperture midway between ovary and copulatory complex, sinistro-ventral, with vaginal canal slightly sclerotized, followed by rounded seminal receptacle, anterior to germarium. Oviduct, ootype, uterus not observed. Vitellaria dense, extends over the entire body, except in the region of the reproductive organs and haptor. Eggs operculated, 72–87 (82; N = 3) long by 60–70 (64; N = 3) wide.
Curvianchoratus psectrogasteri sp. nov. is allocated in the genus mainly by the morphology of the copulatory complex, composed by a tubular cirrus and a pincer-shaped accessory piece, connected to the base of the cirrus by a ligament and by the presence of the greatly modified dorsal anchor, composed by two subunits: dorsal-median and dorsal. The new species differs from the two known species by the absence of the ventral bar and by the morphology of the dorsal-median subunit (strongly curved, with the shank and tip visibly separated; a robust shank ornamented with a thorn at the base and crested-shaped deep and superficial roots in the new species vs. a stickle shaped end inserted in the cavity of the shaft in C. hexacleidus and C. singularis) and by the morphology of the dorsal subunit (elongated, with a broadly circular central region in the new species vs. elongated, with deep root in C. singularis and without in C. hexacleidus).
Curvianchoratus psectrogasteri sp. nov. from Psectrogaster amazonica from Tocantins River A whole specimen, ventral view B copulatory complex, ventral view C vagina D egg E ventral anchor F hook G dorsal-median subunit H dorsal subunit. Scale bars: 100 μm (A); 10 μm (B, C, E, F); 30 μm (D, G, H).
Psectrogaster amazonica Eigenmann & Eigenmann, 1889 (Curimatidae).
Embiral, rural zone (5°27'50"S, 47°33'48"W), municipality of Imperatriz, Maranhão State.
5.15% prevalence; 8 total number of parasites; 1.14 ± 0.26 mean intensity; 1–2 range of intensity.
Holotype
:
The specific name is in honor of Dr Marcus Vinicius Domingues for his contributions to the knowledge of neotropical monogenoidean fauna.
Based on 7 specimens: 1 mounted in Gomori’s trichrome and 6 mounted in Hoyer’s medium: Body short, broad, 460–750 (575; N = 6) long, 225–500 (362; N = 6) wide. Tegument smooth. Cephalic region with 3 pairs of lateral lobes (two lateral and one terminal); five pairs of head organs; cephalic glands lateral to pharynx. Eyespots absent. Pharynx muscular, 50–63 (55; N = 3) long, 48–69 (58; N = 3) wide, esophagus short. Haptor small, compared to body size length, 400 (N = 2) wide. Ventral bar short and robust, anvil-shaped, with slightly jagged edges, 50–58 (52; N = 4) long. Ventral anchor with inconspicuous roots, shaft with two subunits, 25–32 (30; N = 5) long, with a short base, 11–17 (14; N = 5). Dorsal anchor complex heavily modified composed by 2 subunits: dorsal-median and dorsal. Dorsal-median subunit robust curved and heavily sclerotized, 50–66 (58; N = 13) long, shaft, 41–47 (44; N = 14); point as a robust hooked thorn, 6–10 (8; N = 14); superficial root, 5–8 (7; N = 3) and deep root, 13–17 (15; N = 6), well developed with borders very close to each other; point, 6–10 (8; N = 14). Dorsal subunit elongated, 65–100 (77; N = 9) long and 18–23 (19; N = 9) wide, 30% larger than the dorsal-median subunit, posterior portion fan-shaped. Hooks similar in shape, with erected thumb, curved shaft, and dilated bulb in the end, pair 1 smaller than the others, 11–12 (11; N = 4) long; pairs 2–7, 14–17 (16; N = 37). Copulatory complex comprising male copulatory organ and articulated accessory piece. MCO tubular, sclerotized, makes a short coil on itself, near the cirrus base, 55–75 (69; N = 4) in total length. Accessory piece claw-shaped, bifurcated, with different tip sizes; the smaller serves as a guide for the MCO, 42–70 (56; N = 5) long. Testis oval dorsal to the germarium; seminal vesicle formed by a distal enlargement of the vas deferens; prostatic reservoir single, in form of half-moon. Germarium pretesticular; seminal receptacle anterior to germarium; vaginal opening sinistro-ventral; vaginal canal wall sclerotized; oviduct, ootype, uterus, and eggs not observed. Vitellaria dense extends over the entire body, except in the region of the reproductive organs and haptor.
Curvianchoratus dominguesi sp. nov. is similar to the other species of the genus mainly by the morphology of the dorsal anchor, the copulatory complex, which is composed by a long cirrus and a pincer-shaped accessory piece, connected to the base of the cirrus. The new species is similar to C. singularis and C. hexacleidus by the presence of the ventral bar. The new species differs from all congeneric species by the shape of the ventral anchor (formed by a shaft with two subunits in the new species vs. well-developed roots in C. hexacleidus and moderately developed deep root and well-developed superficial root in C. singularis and C. psectrogasteri sp. nov.), the morphology of the ventral bar (short and robust, anvil-shaped ventral bar in C. dominguesi sp. nov. vs. serpentine-shaped in C. hexacleidus, M-shaped in C. singularis and absent in C. psectrogasteri sp. nov.) and by the ratio of the subunits of the dorsal anchor (dorsal subunit is 30% larger than the dorsal-median subunit in C. dominguesi sp. nov. vs. the approximately same size of the subunits in the other three species of the genus).
Light photomicrographs of Curvianchoratus spp. A, B, E Curvianchoratus psectrogasteri sp. nov. A total, ventral view B copulatory complex, ventral view E haptor C, D, F Curvianchoratus dominguesi sp. nov. C copulatory complex, ventral view D total, ventral view F haptor. Scale bars: 100 μm (A); 20 μm (B); 30 μm (C, F); 100 μm (D); 40 μm (E).
Notodiplocerus singularis Suriano, 1980. Syn.
Psectrogaster amazonica Eigenmann & Eigenmann, 1889 (Curimatidae)
Gill.
Embiral, rural zone (5°27'50"S, 47°33'48"W), municipality of Imperatriz, Maranhão State.
29.37% prevalence; 104 total number of parasites; 2,81 (±6,3) mean intensity; 1–38 range of intensity.
Cyphocharax gilbert (syn. Pseudocurimata gilbert) from Chascomus Lagoon, Buenos Aires Province, Argentina (
Cyphocharax voga from Chascomus Lagoon, Buenos Aires Province, Argentina (
Voucher
Monogenoideans represent one of the main components of the helminth fauna present in freshwater fish in the Neotropics, most of which are dactylogyridean parasites of teleost fish (
Studies on the parasite diversity of freshwater fish from the Tocantins-Araguaia Basin have gradually increased in recent years [see
In this sense, the proposal of two new species of Curvianchoratus contributes to the knowledge of parasite fauna of the region and enlarges the morphological characters used to describe the unique species that ventral bar is absent (Curvianchoratus psectrogasteri sp. nov.), which is contrary to the known species of the genus. Although the presence of the bar is an important characteristic, we adopted a conservative approach when proposing a new species of this genus, because C. psectrogasteri exhibit the complex morphology of the dorsal anchor, characteristic of Curvianchoratus.
With the description of the two new species in the present study, Curvianchoratus now encompasses four species, all parasitizing curimatid fishes. Curvianchoratus singularis is herein reported in P. amazonica from the Tocantins River, expanding the occurrence of the species to the Tocantins-Araguaia Basin. The finding of three species of the genus in P. amazonica confirms the high specificity of the genus to neotropical curimatid hosts. On the other side, Psectrogaster amazonica harbors five monogenoidean species, two from a generalist monogenoidean genus, Urocleidoides (parasites from three different fish orders) (
No conflict of interest was declared.
Permission to collect the hosts was given by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio) through the Sistema de Autorização e Informação da Biodiversidade (SISBIO) under license number 79538-1.
Bezerra, CAM was supported by a doctoral scholarship Fundação de Amparo à Pesquisa e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA) #154086/2021.
Conceptualization: SCC, MCNJ, CAMB. Formal analysis: SCC, MCNJ. Methodology: CAMB, HGCN, YCM. Project administration: DCV. Writing – original draft: CAMB. Writing – review and editing: SCC, MCNJ.
Carine Almeida Miranda Bezerra: Collected the hosts, and processed the methodology of collect of parasites; substantial contribution in the concept; contribution to data analysis and interpretation; contribution to manuscript preparation; Simone Chinicz Cohen: Substantial contribution in the concept and design of the study; contribution to data analysis and interpretation; contribution to data collection; contribution to manuscript preparation; contribution to critical revision, adding intelectual content. Yuri Costa de Meneses: Processed the methodology to prepare of parasites; contribution to critical revision, adding intelectual content. Helyab Gabriel Chaves Neres Collected the hosts, and processed the methodology of collect of parasites. Diego Carvalho Viana: Project administration. Marcia Cristina Nascimento Justo: Substantial contribution in the concept and design of the study; contribution to data analysis and interpretation; contribution to manuscript preparation; contribution to critical revision; Writing original draft; prepared figures.
Carine Almeida Miranda Bezerra https://orcid.org/0000-0003-4842-1595
Simone Chinicz Cohen https://orcid.org/0000-0001-8204-336X
Yuri Costa de Meneses https://orcid.org/0000-0002-8737-1159
Helyab Gabriel Chaves Neres https://orcid.org/0000-0002-4454-0223
Diego Carvalho Viana https://orcid.org/0000-0002-3302-9892
Marcia Cristina Nascimento Justo https://orcid.org/0000-0002-0684-3389
All of the data that support the findings of this study are available in the main text.