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New records of Monogenoidea (Platyhelminthes) from three marine fish species from the coast of Angra dos Reis, Rio de Janeiro, Brazil

ABSTRACT

During a survey of helminth parasites, five monogenoid species were reported from marine fishes from the coast of Angra dos Reis, littoral of Rio de Janeiro State, Atlantic Ocean. A total of 810 monogenoids were collected: Pseudotagia pomadasys Hernández-Vale, Bunkley-Williams & Williams Jr, 2016, Pseudoeurysorchis travassosi Caballero & Bravo-Hollis, 1962 in Haemulopsis corvinaeformis (Steindachner, 1868) (=Pomadasys corvinaeformis), Neodiplectanum mexicanum (Mendoza-Franco, Roche & Torchin, 2008) Domingues, Diamanka & Pariselle, 2011 and Aristocleidus hastatus Mueller, 1936 in Diapterus rhombeus (Cuvier, 1829) and Acanthocercodes bullardi Kritsky & Diggles, 2015 in Polydactylus virginicus (Linnaeus, 1758). The presence of P. pomadasys, P. travassosi and A. hastatus in the Southwest Atlantic Ocean represents a new geographical distribution for these species. Haemulopsis corvinaeformis represents a new host record for P. travassosi and A. bullardi is reported in the present paper for the first time parasitizing the gills of a polynemid in South Atlantic Ocean. The findings show that they belong to species previously recorded from the same or congeneric hosts from Central America and Mexico, representing new data on hosts and geographical records.

KEY WORDS:
Acanthocercodes ; Aristocleidus ; fish parasites; monogenoideans; Neodiplectanum ; Pseudoeurysorchis ; Pseudotagia

INTRODUCTION

Diapterus rhombeus (Cuvier, 1829) (Eupercaria: Gerreidae) is a marine and estuarine fish that may enter freshwater, distribu ted from Florida to Brazil (Gilmore et al. 2002Gilmore RG Jr, Beach V, Greenfeld DW (2002) Gerreidae. Mojarras. In: Carpenter KE (Ed.) The living marine resources of the Western Central Atlantic . FAO, American Society of Ichthyologists and Herpetologists, Rome, Special Publication #5, vol. 3, 1506-1521.). This species is one of the most abundant demersal fishes in Central and South America and its populations are usually found aggregated in small groups (Reis-Filho and Leduc 2018Reis-Filho JA, Leduc AOHC (2018) Mysterious and elaborated: the reproductive behavior of the rhomboid mojarra, Diapterus rhombeus (Cuvier, 1829), in Brazilian mangrove habitats. Helgoland Marine Research 72(7): 1-6. https://doi.org/10.1186/s10152-018-0511-9
https://doi.org/10.1186/s10152-018-0511-...
). They feed mainly on plants and microbenthic crustaceans, pelecypods, and polychaete worms (Gilmore et al. 2002Gilmore RG Jr, Beach V, Greenfeld DW (2002) Gerreidae. Mojarras. In: Carpenter KE (Ed.) The living marine resources of the Western Central Atlantic . FAO, American Society of Ichthyologists and Herpetologists, Rome, Special Publication #5, vol. 3, 1506-1521.). The species is common in mangrove-lined lagoons; also found over shallow mud and sand grounds in marine areas (Froese and Pauly 2022Froese R, Pauly D (2022) FishBase. Version 06/2021, Version 06/2021, http://www.fishbase.org [Acessed: 11/10/2022]
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). Diapterus rhombeus is a species widely studied for parasites and all groups of helminths have been reported in this host: Homalometron longulumTravassos, Freitas & Buhrnheim, 1965Travassos L, Freitas JFT, Bührnheim PF (1965) Trematódeos de peixes do litoral capixaba: Homalometron longulum sp. n., parasito de caratinga. Atas da Sociedade de Biologia do Rio de Janeiro 9: 95-97. (Trematoda); Neodiplectanum mexicanum (Mendoza-Franco, Roche & Torchin, 2008Mendoza-Franco EF, Roche DG, Torchin ME (2008) New species of Diplectanum (Monogenoidea: Diplectanidae), and proposal of a new genus of the Dactylogyridae from the gills of gerreid fishes (Teleostei) from Mexico and Panama. Folia Parasitologica 55: 171-179.) Domingues, Diamanka & Pariselle, 2011Domingues MV, Diamanka A, Pariselle A (2011) Monogenoids (Diplectanidae, Polyonchoinea) from the gills of mojarras (Perciformes, Gerreidae) with the resurrection of Neodiplectanum Mizelle & Blatz, 1941 and the proposal of Darwinoplectanum n. gen. Zootaxa 3010: 1-19., Aristocleidus lamotheiKritsky & Mendoza-Franco, 2008Kritsky DC, Mendoza-Franco EF (2008) Revision of Aristocleidus (Monogenoidea: Dactylogyridae), rediscovery of Aristocleidus hastatus, and description of Aristocleidus lamothei n. sp. from the Peruvian mojarra Diapterus peruvianus (Teleostei: Gerreidae) in Mexico. Revista Mexicana de Biodiversidad 79: 75-82. and Aristocleidus hastatusMueller, 1936Mueller JF (1936) New gyrodactyloid trematodes from North American fishes. Transactions of the American Microscopic Society 55: 457-464 (Monogenoidea); Contracaecum sp. and Raphidascaris sp. (Nematoda); Nybelinia sp. (Cestoda) and Corynosoma australe Johnston, 1937 and Caballerorhynchus lamothei Salgado-Maldonado, 1977 (Acanthocephala) (Travassos et al. 1965Travassos L, Freitas JFT, Bührnheim PF (1965) Trematódeos de peixes do litoral capixaba: Homalometron longulum sp. n., parasito de caratinga. Atas da Sociedade de Biologia do Rio de Janeiro 9: 95-97., 1967Travassos L, Freitas JFT, Bührnheim PF (1967) Relatório da excursão do Instituto Oswaldo Cruz ao estado do Espirito Santo em novembro de 1964. Boletím do Museu de Biologia Prof. Mello Leitão, Zoologia 31: 1-5., Vicente and Santos 1973Vicente JJ, Santos E (1973) Alguns helmintos de peixes do litoral norte fluminense 1. Memórias do Instituto Oswaldo Cruz 71(1-2): 95-113., Escobar-Briones et al. 1999Escobar-Briones E, Álvarez F, Salgado-Maldonado G (1999) Discapseudes holthuisi (Crustacea: Tanaidacea) as an intermediate host of Caballerorhynchus lamothei (Acanthocephala: Cavisomidae). The Journal of Parasitology 85(1): 134-137., Luque and Poulin 2004Luque JL, Poulin R (2004) Use of fish as intermediate hosts by helminth parasites: a comparative analysis. Acta Parasitologica 49 (4): 353-361., Mendoza-Franco et al. 2008Mendoza-Franco EF, Roche DG, Torchin ME (2008) New species of Diplectanum (Monogenoidea: Diplectanidae), and proposal of a new genus of the Dactylogyridae from the gills of gerreid fishes (Teleostei) from Mexico and Panama. Folia Parasitologica 55: 171-179., 2009Mendoza-Franco EF, Violante-González J, Roche DG (2009) Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research 105(3): 703-408. https://doi.org/10.1007/s00436-009-1442-9
https://doi.org/10.1007/s00436-009-1442-...
, Domingues et al. 2011Domingues MV, Diamanka A, Pariselle A (2011) Monogenoids (Diplectanidae, Polyonchoinea) from the gills of mojarras (Perciformes, Gerreidae) with the resurrection of Neodiplectanum Mizelle & Blatz, 1941 and the proposal of Darwinoplectanum n. gen. Zootaxa 3010: 1-19.).

The Roughneck grunt Haemulopsis corvinaeformis (Steindachner, 1868) (=Pomadasys corvinaeformis) (Eupercaria: Haemulidae) is distributed from Mexico to the Caribbean coasts, both continental and insular to the Antilles, and Brazil (Smith 1997Smith CL (1997) Field guide to tropical marine fishes of the Caribbean, the Gulf of Mexico, Florida, the Bahamas, and Bermuda. National Audubon Society, New York, 718 pp., Froese and Pauly 2022Froese R, Pauly D (2022) FishBase. Version 06/2021, Version 06/2021, http://www.fishbase.org [Acessed: 11/10/2022]
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) and is a common species on the Brazilian coast (Menezes and Figueiredo 1980Menezes NA, Figueiredo JL (1980) Manual de Peixes Marinhos do Sudeste do Brasil. v. IV. Teleostei. Museu de Zoologia da Universidade de São Paulo, São Paulo, 90 pp.). Individuals are small, reaching a maximum size of 25 cm and usually form small aggregates, being a migratory species and estuarine dependent. It feeds mainly on crustaceans and small fish and has commercial value (Menezes and Figueiredo 1980Menezes NA, Figueiredo JL (1980) Manual de Peixes Marinhos do Sudeste do Brasil. v. IV. Teleostei. Museu de Zoologia da Universidade de São Paulo, São Paulo, 90 pp.). Until now, only two helminth species have been reported in this host: an unidentified species of trematode, Stephanostomum sp. in Puerto Rico and the monogenoid Pseudotagia pomadasysHernández-Vale, Bunkley-Williams &Williams Jr, 2016Hernández-Vale O, Bunkley-Williams L, Williams H Jr (2016) New records of species of Macrovalvitrematidae Yamaguti, 1963 (Monogenea) from Puerto Rio including one new genus and two new species. The Journal of Parasitology 102(1): 114-130. https://doi.org/10.1645/14-520
https://doi.org/10.1645/14-520...
, described from Mexico (Bunkley-Williams et al. 1996Bunkley-Williams L, Dyer WG, Williams EH (1996) Some aspidogastrid and digenean trematodes of Puerto Rican marine fishes. Journal of Aquatic Animal Health 8(1): 87-92. https://doi.org/10.1577/1548-8667(1996)0082.3.co;2
https://doi.org/10.1577/1548-8667(1996)0...
, Hernández-Vale et al. 2016Hernández-Vale O, Bunkley-Williams L, Williams H Jr (2016) New records of species of Macrovalvitrematidae Yamaguti, 1963 (Monogenea) from Puerto Rio including one new genus and two new species. The Journal of Parasitology 102(1): 114-130. https://doi.org/10.1645/14-520
https://doi.org/10.1645/14-520...
).

Polydactylus virginicus (Linnaeus, 1758) (Carangaria: Polynemidae) is found on sandy and muddy bottoms of coastal waters, mangroves and commonly enters estuaries. Small specimens are caught in large numbers at the mouths of rivers (Feltes 2002Feltes RM (2002) Polynemidae. In: Carpenter KE (Ed.) The living marine resources of the Western Central Atlantic. FAO, American Society of Ichthyologists and Herpetologists, Rome, Special Publication #5, vol. 3, 1578-1582.). This fish is a nocturnal feeder, taking crustaceans, chaetognaths, plant material, and polychaetes, and may have a prolonged spawning season. They have been reported in the Western Atlantic ranging from New Jersey to Uruguay (Feltes 2002Feltes RM (2002) Polynemidae. In: Carpenter KE (Ed.) The living marine resources of the Western Central Atlantic. FAO, American Society of Ichthyologists and Herpetologists, Rome, Special Publication #5, vol. 3, 1578-1582., Motomura 2004Motomura H (2004) Threadfins of the world (Family Polynemidae). An annotated and illustrated catalogue of polynemid species known to date. FAO, Rome, vol. 3, 117 pp., Froese and Pauly 2022Froese R, Pauly D (2022) FishBase. Version 06/2021, Version 06/2021, http://www.fishbase.org [Acessed: 11/10/2022]
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). The only helminth species described in this host is Procamallanus (Spirocamallanus) cruziGuimarães, Cristofaro & Rodrigues, 1976Guimarães JF, Cristofaro R, Rodrigues HO (1976) Alguns nematódeos de peixes de Salvador, Bahia. Atas da Sociedade de Biologia do Rio de Janeiro 18: 21-25. (Nematoda) from Pituba, Salvador, state of Bahia, Brazil (Guimarães et al. 1976Guimarães JF, Cristofaro R, Rodrigues HO (1976) Alguns nematódeos de peixes de Salvador, Bahia. Atas da Sociedade de Biologia do Rio de Janeiro 18: 21-25.), considered ‘species inquirenda’ by Sardella et al. (2017Sardella CJ, Pereira FB, Luque JL (2017) Redescription and first genetic characterisation of Procamallanus (Spirocamallanus) macaensis Vicente & Santos, 1972 (Nematoda: Camallanidae), including reevaluation of the species of Procamallanus (Spirocamallanus) from marine fishes off Brazil. Systematic Parasitology 94(6): 657-668. https://doi.org/10.1007/s11230-017-9728-2
https://doi.org/10.1007/s11230-017-9728-...
). Lopes et al. (2009Lopes PRD, de Oliveira-Silva JT, Fernandes IP (2009) Notas sobre a alimentação de Polydactylus virginicus (Linnaeus, 1758) (Actinopterygii: Polynemidae) na praia do Malhado, Ilhéus (Bahia). Revista Mosaicum (9): 126-131.), in a survey on feeding of this species, observed the presence of Acanthocephala and Nematoda in the digestive system of P. virginicus collected from Ilhéus, state of Bahia, with no specific identification.

During a survey on marine fishes from the littoral of Angra dos Reis, state of Rio de Janeiro, specimens of Monogenoidea were recovered from D. rhombeus, P. virginicus, and H. corvinaeformis. The findings show that they belong to species previously recorded from the same or congeneric hosts from Central America and Mexico, representing new data on hosts and geographical records.

MATERIAL AND METHODS

Fifty-two specimens of H. corvinaeformis, 32 specimens of P. virginicus, and 201 of D. rhombeus were collected in “Saco Piraraquara de Dentro”, coast of Angra dos Reis, state of Rio de Janeiro, Brazil (23°00’24”S, 44°19’05”W) (Fig. 1), and examined between August 2007 and February 2013. The fishes were captured by fishermen with the aid of gill nets and examined in the laboratory. The gill arches were separated and the monogenoids collected were fixed in 5% formaldehyde. Mazocraeidae and Diclidophoridae specimens were stained with Langeron’s alcoholic acid carmine, dehydrated by means of an ethyl alcohol series, cleared using beechwood creosote and mounted in Canada balsam as permanent slides (Eiras et al. 2006Eiras JC, Takemoto RM, Pavanelli GC (2006) Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Eduem, Maringá, 2nd ed., 199 pp.) and Dactylogyridae and Diplectanidae specimens were mounted in Hoyer’s medium (Humason 1979Humason GL (1979) Animal Tissue Techniques. W.H. Freeman, San Francisco, 4th ed., 468 pp.). The specimens were observed using a Zeiss Axioskop 2 Plus microscope and digital images were captured with a SONY MPEG Movie EX DSC-S75 digital camera. The measurements are given in micrometers unless otherwise stated, and the range is presented followed by the mean and the numbers of structures measured in parentheses. The parasitological index was calculated as proposed by Bush et al. (1997Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4): 575-583.), followed by the standard deviation. Representative specimens were deposited in the Helminthological Collection of the Oswaldo Cruz Institute (CHIOC), Rio de Janeiro, Brazil.

Figure 1
Map of the area of new geographical records.

TAXONOMY

In the present study, a total of 810 monogenoids were collected, comprising seven specimens of P. pomadasys, eight of Pseudoeurysorchis travassosiCaballero & Bravo-Hollis, 1962Caballero E, Bravo-Hollis M (1962) Trematodos de peces de aguas mexicanas Del Pacifico. XXI. Sobre un nuevo genero de la familia Diclidophoridae Fuhrmann, 1928. Revista Brasileira de Biologia 22(1): 107-114. parasitizing H. corvinaeformis (6-23 cm in total body length and 10-205 g in weight); 546 specimens of N. mexicanum and 186 of A. hastatus parasitizing D. rhombeus (7-26 cm in total body length and 10-200 g) and 63 Acanthocercodes bullardiKritsky & Diggles, 2015Kritsky DC, Diggles BK (2015) Acanthocercodes n.g. (Monogenoidea: Diplectanidae) for species parasitising threadfins (Perciformes: Polynemidae), with description of Acanthocercodes bullardi n. sp. from the Atlantic threadfin Polydactylus octonemus (Girard) and reassignment of three species of Diplectanum Monticelli, 1903 from the Indo-Pacific Ocean. Systematic Parasitology 91(3): 191-201. https://doi.org/10.1007/s11230-015-9574-z
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from P. virginicus (20-26 cm in total body length and 75-250 g in weight). Parasitological indices are presented in Table 1.

Table 1
Prevalence (P), mean intensity (MI), mean abundance (MA) and range of infection (R) of monogenoideans from D. rhombeus, P. virginicus, and H. corvinaeformis from “Saco Piraraquara de Dentro”, coast of Angra dos Reis, littoral of Rio de Janeiro State, Brazil. Data presented as Mean (±) Standard deviation.

Mazocraeidae

Pseudotagia pomadasys Hernández-Vale, Bunkley-Williams & Williams Jr, 2016

Fig. 2A-D

Host: Haemulopsis corvinaeformis (Steindachner, 1868) (Haemulidae).

New record. Brazil, Atlantic Ocean - Rio de Janeiro State • coast of Angra dos Reis, “Saco Piraraquara de Dentro”; 23°00’24”S, 44°19’05”W; CHIOC 39729.

Type-host: Haemulopsis corvinaeformis [=Pomadasys corvinaeformis (Steindachner, 1868)]

Type-locality: Guanajibo and Boquilla, Mayaguez, Puerto Rico (Caribbean) and Loíza, Puerto Rico (Atlantic Ocean).

Figure 2
Pseudotagia pomadasys: (A) whole mount; (B) anterior region with buccal suckers; (C) genital atrium; (D) clamp. Scale bars: A = 500 μm, B = 100 μm, C, D = 50 μm.

Description (based on six specimens). Body 2,750-3,550 (3,079; n = 6) long by 480-550 (513; n = 6) wide. Anterior end with a pair of oval buccal suckers, 80-105 (93; n = 12) long by 75-110 (95; n = 12) wide. Pharynx 62-87 (79; n = 5) long by 70-77 (74; n = 5) wide. Oesophagus short. Intestinal caeca bifurcate at level of genital atrium and extend to posterior region of body proper, joining in one and reaching the haptor. Genital atrium 42-55 (47; n=5) long by 47-50 (47; n=5) wide, with eight to nine spines. Haptor composed of four pairs of pedunculated clamps. Each clamp is formed by two plate-like valves and sclerites: central sclerite with bifurcated base and lateral sclerites. Clamps: pair 1, 80-92 (84; n = 12), pair 2, 85-97 (90; n = 11), pair 3, 80-97 (90; n = 12), pair 4, 77-100 (85; n = 11). Testes 12 in number, post ovarian. Ovary large, inverted J shaped, located immediately anterior to testes. Genito-intestinal canal observed at mid level of testes. Eggs not observed.

Diclidophoridae

Pseudoeurysorchis travassosi Caballero & Bravo-Hollis, 1962

Fig. 3A-C

Host: Haemulopsis corvinaeformis (Steindachner, 1868)

New record. Brazil, Atlantic Ocean - Rio de Janeiro State • coast of Angra dos Reis, “Saco Piraraquara de Dentro”; 23°00’24”S, 44°19’05”W; CHIOC 39730.

Type-host: Microlepidotus inornatus Gill, 1862 (Haemulidae).

Type-locality: California Gulf, San Carlos Bay, Guaymas, Sonora, Mexico.

Figure 3
Pseudoeurysorchis travassosi: (A) whole mount; (B) genital atrium; (C) clamp. Scale bars: A = 1 mm, B = 30 μm, C = 250 μm.

Other hosts: Microlepidotus brevipinnis (Steindachner, 1869) (Haemulidae), and Isacia conceptionis (Cuvier, 1830) (Haemulidae).

Other localities: Mexico and Puerto del Callao, Peru.

Description (based on six specimens). Large monogenoids, easily distinguished on the gills. Body, not including haptor 3,325-3,750 (3,483; n = 3) long by 1,625-1,925 (1,817; n = 3) wide. Buccal suckers 67-105 (90; n = 10) long by 80-100 (89; n = 10) wide, muscular, septate. Pharynx 82-150 (130; n = 5) long by 75-107 (91; n = 5) wide. Genital atrium 45-57 (51; n = 6) long by 40-55 (50; n = 6) wide with 10 to 11 spines, which bears long point curved towards the center of the crown and bifurcated extremity toward the margin. Testes numerous, posterior to ovary, reaching the haptor. Ovary located immediately anterior to haptor, irregular shaped. Vitelline glands distributed throughout the body, including the haptor. Haptor 3,250-4,375 (3,687; n = 4) long by 2,125 -2,575 (2,350; n = 4) wide, robust, occupying most part of the body of the parasite, composed of four pairs of sessile clamps. Clamps similar in size and shape, 480-810 (675; n = 24) long by 540-800 (644; n = 24) wide, constituted by two reinforced valves, ventral and dorsal, heavily sclerotized and articulated, supported by a median and marginal sclerites in the borders.

Diplectanidae

Acanthocercodes bullardi Kritsky & Diggles, 2015

Fig. 4A-C

Host: Polydactylus virginicus (Linnaeus, 1758) (Polynemidae).

New record. Brazil, Atlantic Ocean - Rio de Janeiro State • coast of Angra dos Reis, “Saco Piraraquara de Dentro”; 23°00’24”S, 44°19’05”W; CHIOC 39724.

Type-host: Polydactylus octonemus (Girard, 1858) (Polyne midae).

Type-locality: Gulf of Mexico, approximately 2 miles south of Cameron (Davis Road), south-west corner of Cameron Parish, Louisiana.

Figure 4
Acanthocercodes bullardi: (A) whole mount; (B) copulatory complex; (C) haptor. Scale bars: A = 150 μm, B = 20 μm, C = 50 μm.

Description (based on 15 specimens). Body with cephalic region, trunk and elongate peduncle, 356-530 (425; n = 10) long by 80-170 (113; n = 10) wide. Four eye-spots. Tegument with scales extending from the eyespots region to the peduncle. Pharynx subspherical, 18-27 (22; n = 10) long by 20-27 (23; n = 10) wide. Intestinal caeca extending posteriorly to level of peduncle. Peduncle tapered and elongate with spines, peduncular spines 16-25 (20; n = 12) long by 16-25 (23; n = 12) wide. Dorsal and ventral squamodiscs with 10 rows of rodlets. Diplectanid haptor composed of ventral bar, paired dorsal bars and marginal hooks, ventral anchor with perpendicular superficial root, long deep root, elongate shaft, and short recurved point, 59-68 (63; n = 22) by 19-25 (22; n = 22) at base; dorsal anchor with short superficial root and inconspicuous deep root, straight shaft and recurved point, 54-62 (58; n = 23) by 17-25 (21; n = 23) at base. Ventral bar broadly U-shaped 75-103 (89; n = 13) long. Paired dorsal bar with tapered ends, 35-51(44; n = 25) long. Hooks 9-13 (11; n = 36). Male copulatory organ a short and broad tube, 34-52 (44; n = 10) long. Testes 60-90 (75; n = 10) long by 50-82 (66; n = 10) wide.

Diplectanidae

Neodiplectanum mexicanum (Mendoza-Franco, Roche & Torchin, 2008) Domingues, Diamanka & Pariselle, 2011

Fig. 5A-C

Host: Diapterus rhombeus (Cuvier, 1829) (Gerreidae)

Locality: Brazil, Atlantic Ocean - Rio de Janeiro State • coast of Angra dos Reis, “Saco Piraraquara de Dentro”; 23°00’24”S, 44°19’05”W; CHIOC 39726a,b, 39727, 39728.

Type-host: Diapterus rhombeus (Cuvier, 1829)

Type-locality: Coast of Campeche State, Mexico (18°48’45”N, 92°03’45”W) in the Gulf of Mexico, Mexico

Other locality: Guaratuba Bay, Municipality of Guaratuba, Paraná, Brazil (25°52’19”S, 48°39’02”W).

Figure 5
Neodiplectanum mexicanum: (A) whole mount; (B) detail of the anterior region, showing copulatory complex and vagina; (C) haptor, showing the anchor bars complex and squamodisc. Scale bars: A = 100 μm; B, C = 50 μm.

Description (based on 38 specimens). Body 300-670 (406; n = 20) long by 80-140 (107; n = 20) wide, fusiform. Four eye spots. Pharynx muscular, glandular. Intestinal caeca 2, non-confluent posteriorly, lacking diverticula. Genital pore opening midventral, posterior to copulatory complex. Male copulatory organ 50-66 (58; n = 21) long, sclerotized, tubular, enlarging distally; accessory piece sclerotized, non-articulated with male copulatory organ, distally hooked. One testis, postgermarian. Vaginal opening sinistral, vaginal atrium 30-35 (32; n = 15) long by 18-37 (28; n = 15), heavily sclerotized. Seminal receptacle spherical. Haptor 112-167 (139; n = 22) wide. Two squamodiscs 50-125 (87; n = 13) long by 62-125 (95; n = 13), one ventral and one dorsal, with 15 to 20 rows of sclerites. Anterior rows concentric. Ventral bar 75-107 (88; n = 21) with longitudinal groove; paired dorsal bars 40-53 (46; n = 29) long, medially expanded. Ventral anchor with well-developed superficial root and deep root, twice as long as superficial root; outer 35-39 (37; n = 11), inner 20-27 (22; n = 11), base 7-11 (9; n = 11). Dorsal anchor with conspicuous superficial and deep roots; outer 35-39 (36; n = 7), inner 21-25 (23; n = 7), base 7-10 (8; n = 7). Hooks similar 12-15 (13; n = 40) long, with depressed thumb, straight shaft, short point, uniform shank; filamentous hooklet (FH) loop nearly shank length.

Dactylogyridae

Aristocleidus hastatus Mueller, 1936

Fig. 6A-C

Host: Diapterus rhombeus (Cuvier, 1829) (Gerreidae)

New record. Brazil, Atlantic Ocean - Rio de Janeiro State • coast of Angra dos Reis, “Saco Piraraquara de Dentro”; 23°00’24”S, 44°19’05”W; CHIOC 39723, 39725.

Type-host: Morone saxatilis (Walbaum, 1792) [as Roccus lineatus (Bloch, 1792)], Moronidae

Type-locality: Peace River near Fort Ogden, Florida.

Figure 6
Aristocleidus hastatus: (A) whole mount; (B) copulatory complex; (C) haptor, with anchor bars complex. Scale bars: A, C = 50 μm, B = 20 μm.

Other hosts: Diapterus auratus Ranzani, 1842, Diapterus peruvianus (Cuvier, 1830), D. rhombeus, Eugerres plumieri (Cuvier, 1830), Eugerres brasilianus (Cuvier, 1830), Gerres cireneus (Walbaum, 1792) (Gerreidae).

Other localities: Lagartos and Celestun estuaries, Yucatán Peninsula, Las Barrancas and Maquinas River in the state of Veracruz, Lake Gatun, near Barro Colorado Island in Panama and the Chautengo and Tres Palos Lagoon, Pacific Coast of Guerrero State, Mexico.

Description (based on 20 specimens). Body 220-325 (271; n = 12) long by 50-92 (71; n = 12) wide. Four eye-spots. Pharynx wide, spherical. Male copulatory organ 27-40 (32; n = 10) long, comprising proximal funnel-shape base, with well-developed flange, coiled thin tube with about one complete ring; accessory piece rod shaped. Vaginal pore sclerotized, dextral; vaginal tube delicate, extending to seminal receptacle. Haptor 55-82 (69; n = 12) wide. Ventral anchor 28-33 (30; n = 28) and point 12-17 (15; n = 28) with deeply incised base forming deep and superficial roots, straight shaft and point forming an angle of 90o. Dorsal anchor 38-43 (40; n = 15) long, 20-24 (22; n = 15) base, elongated superficial root, short to nonexistent deep root, tapered shaft, elongated recurved point. Ventral bar 19-25 (22; n = 13) long, with elongated distally bifurcated anteromedian projection and bifurcated edges; dorsal bar 35-41 (38; n = 15) long, with slightly expanded ends, delicate anteromedian flange. Hooks similar in shape and size, 10-14 (12; n = 46) long, each with upright thumb, shank comprising a single subunit, filamentous hook (FH) loop about 80% shank.

DISCUSSION

The specimens reported herein are conspecific with P. pomadasys by the absence of serration of lateral sclerites and the relative size of the clamps, with the two larger pairs positioned centrally in the haptor and the two smaller pairs in the outer positions. The present material differs from Pseudotagia cupida (Hargis, 1956) Yamaguti, 1963Yamaguti S (1963) Systema Helminthum. IV. Monogenea and Aspidocotylea. Interscience Publishers, New York, vol. 4, 699 pp., previously reported in Brazil from Haemulon sciurus (Shaw, 1803) by Kohn et al. (1984Kohn A, Abramson B, Macedo B (1984) Studies on some monogeneans parasites of Haemulon sciurus (Shaw, 1803) (Pomadasyidae). The Journal of Helminthology 58: 213-218.) by the relative size of the three first pairs of clamps that are larger than the fourth and by the serration of the two valves of the clamps and by the number of spines in the genital atrium (8 to 9 in P. pomadasys and 6 in P. cupida). The measurements of the present material agree with the original description (Hernández-Vale et al. 2016Hernández-Vale O, Bunkley-Williams L, Williams H Jr (2016) New records of species of Macrovalvitrematidae Yamaguti, 1963 (Monogenea) from Puerto Rio including one new genus and two new species. The Journal of Parasitology 102(1): 114-130. https://doi.org/10.1645/14-520
https://doi.org/10.1645/14-520...
).

Pseudotagia pomadasys was described from H. corvinaeformis (=Pomadasys corvinaeformis) from Guanajibo and Boquilla, Mayaguez, Puerto Rico (Caribbean) and Loíza, Puerto Rico (Atlantic Ocean) by Hernández-Vale et al. (2016Hernández-Vale O, Bunkley-Williams L, Williams H Jr (2016) New records of species of Macrovalvitrematidae Yamaguti, 1963 (Monogenea) from Puerto Rio including one new genus and two new species. The Journal of Parasitology 102(1): 114-130. https://doi.org/10.1645/14-520
https://doi.org/10.1645/14-520...
). Suriano (1975Suriano DM (1975) Tetrasepta dischizosepta gen et sp nov (Monogenea Monopisthocotylea) parasita branquial de Acanthistius brasilianus (Cuvier y Valenciennes, 1928) (Pisces, Serranidae) del Oceano Atlantico sudoccidental. Physis Buenos Aires Sect A 34: 283-290.) argued that species of PseudotagiaYamaguti, 1963Yamaguti S (1963) Systema Helminthum. IV. Monogenea and Aspidocotylea. Interscience Publishers, New York, vol. 4, 699 pp. were the only macrovalvitrematids that do not parasitize the gills of a sciaenid fish, since they have been found parasitizing the families Haemulidae and Serranidae, with great abundance in the former. In Brazil, two other species of the genus were recorded: P. cupida from H. sciurus and in Diplectrum sp. (Serranidae) and Pseudotagia rubriLuque, Amato & Takemoto, 1993Luque JL, Amato JFR, Takemoto RM (1993) A new species of Pseudotagia Yamaguti, 1963 (Monogenea: Macrovalvitrematidae) parasitic ob Orthopristis ruber (Cuvier) (Osteichthyes: Haemulidae) from Brazilian coast. Revista Brasileira de Parasitologia Veterinária 2(2): 111-114. from Orthopristis ruber (Cuvier, 1830), both in the littoral of the state of Rio de Janeiro (Kohn et al. 1984Kohn A, Abramson B, Macedo B (1984) Studies on some monogeneans parasites of Haemulon sciurus (Shaw, 1803) (Pomadasyidae). The Journal of Helminthology 58: 213-218., 1992Kohn A, Santos CP, Baptista-Farias MF (1992) New host records and localities of some Monogenea from Brazilian marine fishes with scanning electron microscopy of Bicotylophora trachinoti (MacCallum, 1921). Memórias do Instituto Oswaldo Cruz 87(Suppl. 1): 109-114., Luque et al. 1993Luque JL, Amato JFR, Takemoto RM (1993) A new species of Pseudotagia Yamaguti, 1963 (Monogenea: Macrovalvitrematidae) parasitic ob Orthopristis ruber (Cuvier) (Osteichthyes: Haemulidae) from Brazilian coast. Revista Brasileira de Parasitologia Veterinária 2(2): 111-114., Cohen et al. 2013Cohen SC, Justo MCN, Kohn A (2013) South American Monogenoidea parasites of fishes, amphibians and reptiles. Oficina de Livros, Rio de Janeiro, 659 pp.). The presence of P. pomadasys in the Southwest Atlantic Ocean represents a new geographical distribution for this species.

The monotypic P. travassosi is a remarkable diclidophorid due to the robustness of the body provided by the size of the haptor and its compounds. Pseudoeurysorchis travassosi was described by Caballero and Bravo-Hollis (1962Caballero E, Bravo-Hollis M (1962) Trematodos de peces de aguas mexicanas Del Pacifico. XXI. Sobre un nuevo genero de la familia Diclidophoridae Fuhrmann, 1928. Revista Brasileira de Biologia 22(1): 107-114.) from the gills of M. inornatus from Sonora, Gulf of California, Mexico. Posteriorly, this species was reported from the gills of I. conceptionis in Peru, and M. brevipinnis from Mexico (Tantaleán et al. 1985Tantalean MV, Martinez RR, Escalante AH (1985) Monogeneos de las costas del Peru II. Cambio de nombre por homonimia y nuevos registros. Revista Faculdade Ciencias Veterinárias 32: 91-95., Pérez-Ponce de León et al. 1999Pérez-Ponce De León G, Mendoza LGB, León-Règagnon V, Pulido G, Aranda C, García F (1999) Listados Faunísticos de México IX. Biodiversidad de Helmintos Parástos de Peces Marinos y Estuarinos de la Bahía de Chamela, Jalisco, México. Universidade Autónoma de Mexico, México, Serie Listados Faunísticos del Instituto de Biologia, 48 pp., respectively). Our specimens are similar to P. travassosi based on its morphology and morphometry and the measurements of the present material agree with the type material collected in Mexico (Caballero and Bravo-Hollis 1962). Haemulopsis corvinaeformis represents a new host record for P. travassosi.

Acanthocercodes bullardi is reported in the present paper for the first time parasitizing the gills of a polynemid in South American waters. Acanthocercodes was proposed by Kritsky and Diggles (2015Kritsky DC, Diggles BK (2015) Acanthocercodes n.g. (Monogenoidea: Diplectanidae) for species parasitising threadfins (Perciformes: Polynemidae), with description of Acanthocercodes bullardi n. sp. from the Atlantic threadfin Polydactylus octonemus (Girard) and reassignment of three species of Diplectanum Monticelli, 1903 from the Indo-Pacific Ocean. Systematic Parasitology 91(3): 191-201. https://doi.org/10.1007/s11230-015-9574-z
https://doi.org/10.1007/s11230-015-9574-...
) for this species from Atlantic threadfin P. octonemus and is distinguished by the larger peduncular spines with a plate-like base. The distinguished feature of the species is the MCO as a broad tube with delicate walls, inconspicuous base and diagonal distal opening often with lateral spine-like projection. The three other species of the genus were also described from polynemid hosts.

Neodiplectanum mexicanum was found on the type host in the littoral of Rio de Janeiro and the morphology and morphometry of the present material are in agreement with previous descriptions (Mendoza-Franco et al. 2008Mendoza-Franco EF, Roche DG, Torchin ME (2008) New species of Diplectanum (Monogenoidea: Diplectanidae), and proposal of a new genus of the Dactylogyridae from the gills of gerreid fishes (Teleostei) from Mexico and Panama. Folia Parasitologica 55: 171-179., Domingues et al. 2011Domingues MV, Diamanka A, Pariselle A (2011) Monogenoids (Diplectanidae, Polyonchoinea) from the gills of mojarras (Perciformes, Gerreidae) with the resurrection of Neodiplectanum Mizelle & Blatz, 1941 and the proposal of Darwinoplectanum n. gen. Zootaxa 3010: 1-19.). The species is distinguished from other species of the genus by the morphology of the copulatory complex and the dorsal anchor. This species was originally described by Mendoza-Franco et al. (2008Mendoza-Franco EF, Roche DG, Torchin ME (2008) New species of Diplectanum (Monogenoidea: Diplectanidae), and proposal of a new genus of the Dactylogyridae from the gills of gerreid fishes (Teleostei) from Mexico and Panama. Folia Parasitologica 55: 171-179.) in Diplectanum from D. rhombeus collected from the coast of Campeche State, Gulf of Mexico. Domingues et al. (2011Domingues MV, Diamanka A, Pariselle A (2011) Monogenoids (Diplectanidae, Polyonchoinea) from the gills of mojarras (Perciformes, Gerreidae) with the resurrection of Neodiplectanum Mizelle & Blatz, 1941 and the proposal of Darwinoplectanum n. gen. Zootaxa 3010: 1-19.) transferred it to Neodiplectanum as N. mexicanum, because it shows all diagnostic features so far proposed for Neodiplectanum, including non-articulated male copulatory organ and accessory piece, vaginal atrium heavily sclerotized, squamodiscs spinelike rodlets, and dorsal anchors with conspicuous superficial and deep roots. These features led the authors to resurrect the genus and include the material referred as Diplectanum mexicanum by Domingues and Boeger (2008Domingues MV, Boeger WA (2008) Phylogeny and revision of Diplectanidae Monticelli, 1903 (Platyhelminthes: Monogenoidea). Zootaxa 1968(1): 1-40. https://doi.org/10.11646/zootaxa.1698.1.1
https://doi.org/10.11646/zootaxa.1698.1....
). Neodiplectanum mexicanum was reported from Guaratuba Bay, Municipality of Guaratuba, Paraná, Brazil on D. rhombeus.

AristocleidusMueller, 1936Mueller JF (1936) New gyrodactyloid trematodes from North American fishes. Transactions of the American Microscopic Society 55: 457-464 (Dactylogyridae) was proposed for A. hastatus from M. saxatilis from the Peace River near Fort Ogden, Florida, USA (Mueller 1936Mueller JF (1936) New gyrodactyloid trematodes from North American fishes. Transactions of the American Microscopic Society 55: 457-464). The specimens collected from D. rhombeus from the littoral of state of Rio de Janeiro are easily identified as A. hastatus by the distinguished feature of the ventral anchor, with deeply incised base forming deep and superficial roots and straight shaft and point form an angle of 90o. Kritsky and Mendoza-Franco (2008Mendoza-Franco EF, Roche DG, Torchin ME (2008) New species of Diplectanum (Monogenoidea: Diplectanidae), and proposal of a new genus of the Dactylogyridae from the gills of gerreid fishes (Teleostei) from Mexico and Panama. Folia Parasitologica 55: 171-179.) found A. hastatus on a new host, Diapterus peruvianus (Cuvier, 1830), and emended the diagnosis of Aristocleidus based on the newly collected material and the cotypes of A. hastatus. According to these authors, the possibility exists that A. hastatus was carried into the Peace River (type locality of the species) by its host from the marine environment and that the parasite species has marine rather than freshwater affinities. Kritsky and Mendoza-Franco (2008Kritsky DC, Mendoza-Franco EF (2008) Revision of Aristocleidus (Monogenoidea: Dactylogyridae), rediscovery of Aristocleidus hastatus, and description of Aristocleidus lamothei n. sp. from the Peruvian mojarra Diapterus peruvianus (Teleostei: Gerreidae) in Mexico. Revista Mexicana de Biodiversidad 79: 75-82.) and Mendoza-Franco et al. (2009Mendoza-Franco EF, Violante-González J, Roche DG (2009) Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research 105(3): 703-408. https://doi.org/10.1007/s00436-009-1442-9
https://doi.org/10.1007/s00436-009-1442-...
) provided measurements of A. hastatus from different gerreid hosts, showing differences in the morphometry of the specimens collected in the Atlantic and Pacific Oceans, as well as in the Panama Canal (Mendoza-Franco et al. 2009Mendoza-Franco EF, Violante-González J, Roche DG (2009) Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research 105(3): 703-408. https://doi.org/10.1007/s00436-009-1442-9
https://doi.org/10.1007/s00436-009-1442-...
, Table 1). They found differences in the length of the anchors between specimens of different host genus (35 to 39 in specimens from Diapterus spp. vs 40 to 48 in Gerres sp. and Eugerres sp.) The length of ventral anchor of the specimens collected from the littoral of Rio de Janeiro was smaller than those from Mexico, even in the same host (35 to 39 in specimens from Mexican D. rhombeus vs 28-33 in specimens from Brazilian D. rhombeus). Measurements of the bars in Brazilian material also show differences, with larger bars than Mexican and Panamanian material (Kritsky and Mendoza-Franco 2008, Mendoza-Franco et al. 2009Mendoza-Franco EF, Violante-González J, Roche DG (2009) Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research 105(3): 703-408. https://doi.org/10.1007/s00436-009-1442-9
https://doi.org/10.1007/s00436-009-1442-...
, 2015Mendoza-Franco EF, Osorio MT, Caspeta-Mandujano JM (2015) Two new species of Aristocleidus (Monogenea) from the gills of the Mexican mojarra Eugerres mexicanus (Perciformes, Gerreidae) from southwestern Mexico. Parasite 22: 33. https://doi.org/10.1051/parasite/2015033
https://doi.org/10.1051/parasite/2015033...
). The finding of A. hastatus in the coast of Angra dos Reis, littoral of Rio de Janeiro confirms the adaptation of Aristocleidus spp. to different environments, considering the occurrence in marine, brackish and freshwater hosts (Kritsky and Mendoza-Franco, 2008Kritsky DC, Mendoza-Franco EF (2008) Revision of Aristocleidus (Monogenoidea: Dactylogyridae), rediscovery of Aristocleidus hastatus, and description of Aristocleidus lamothei n. sp. from the Peruvian mojarra Diapterus peruvianus (Teleostei: Gerreidae) in Mexico. Revista Mexicana de Biodiversidad 79: 75-82., Mendoza-Franco et al. 2009Mendoza-Franco EF, Violante-González J, Roche DG (2009) Interoceanic occurrence of species of Aristocleidus Mueller, 1936 (Monogenoidea: Dactylogyridae) parasitizing the gills of gerreid fishes in the Neotropics. Parasitology Research 105(3): 703-408. https://doi.org/10.1007/s00436-009-1442-9
https://doi.org/10.1007/s00436-009-1442-...
, 2015Mendoza-Franco EF, Osorio MT, Caspeta-Mandujano JM (2015) Two new species of Aristocleidus (Monogenea) from the gills of the Mexican mojarra Eugerres mexicanus (Perciformes, Gerreidae) from southwestern Mexico. Parasite 22: 33. https://doi.org/10.1051/parasite/2015033
https://doi.org/10.1051/parasite/2015033...
).

ACKNOWLEDGEMENTS

The authors are grateful to Pedro José Diniz de Figueiredo from Central Nuclear Almirante Álvaro Alberto, Eletrobras, Eletronuclear, Angra dos Reis and Aderval Ferrari Vaz de Almeida from Laboratório de Monitoração Ambiental, Eletronuclear, Angra dos Reis, for the facilities and infrastructure offered to examine the fishes, and for the classification of the hosts and to Antonia Lucia dos Santos from FIOCRUZ for the assistance with the collection of parasites.

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ADDITIONAL NOTES

  • Zoobank register

    https://zoobank.org/2AF00088-9AC6-4626-81B8-7A24787937DE
  • How to cite this article

    Cohen SC, Justo MCN, Cárdenas MQ (2022) New records of Monogenoidea (Platyhelminthes) from three marine fish species from the coast of Angra dos Reis, Rio de Janeiro, Brazil. Zoologia (Curitiba) 39: e22024. https://doi.org/10.1590/S1984-4689.v39.e22024
  • Published by

    Sociedade Brasileira de Zoologia at Scientific Electronic Library Online (https://www.scielo.br/zool)

Edited by

Editorial responsibility

Antoine Pariselle

Publication Dates

  • Publication in this collection
    16 Dec 2022
  • Date of issue
    2022

History

  • Received
    05 May 2022
  • Accepted
    26 Oct 2022
Sociedade Brasileira de Zoologia Caixa Postal 19020, 81531-980 Curitiba PR Brasil, Tel./Fax: (55 41) 3266-6823 - Curitiba - PR - Brazil
E-mail: sbz@sbzoologia.org.br