New species of Urocleidoides (Monogenoidea: Dactylogyridae) from the gills of two species of Anostomidae from the Brazilian Amazon

Novas espécies de Urocleidoides (Dactylogyridae) das brânquias de duas espécies de Anostomidae da Amazônia brasileira

Abstract

Three species (2 new) of Urocleidoides are described and/or reported from the gills of Schizodon fasciatus and Laemolyta proxima (Anostomidae) from the Jari River in the eastern Brazilian Amazon. Urocleidoides jariensis n. sp. presents a sclerotized, tubular, spiral male copulatory organ (MCO) with one counterclockwise coil, a circular sclerotized tandem brim associated with the base of the MCO; a heavily sclerotized, funnel-shaped vaginal vestibule; and a broadly V-shaped ventral bar with anteromedial constriction and enlarged ends. Urocleidoides ramentacuminatus n. sp. has a sclerotized, tubular, spiral MCO with one counterclockwise coil; an accessory piece with a hook-shaped distal portion; and a dorsal anchor with a short, straight shaft; anchor point with ornamentation as sclerotized shredded filaments. Urocleidoides paradoxus is reported for the first time parasitizing S. fasciatus.

Keywords:
Amazon; anostomidae; monogenoids; parasites; freshwater fish

Resumo

Três espécies (2 novas) de Urocleidoides são descritas e/ou reportadas das brânquias de Schizodon fasciatus e Laemolyta proxima (Anostomidae) da bacia do Rio Jari, na Amazônia oriental brasileira. Urocleidoides jariensis n. sp. apresenta um órgão copulatório masculino (OCM) convoluto, com uma volta no sentido anti-horário, uma borda em tandem esclerotizada circular, associada à base do OCM; um vestíbulo vaginal fortemente esclerotizado e em forma de funil; um canal vaginal esclerotizado na porção proximal; e uma barra ventral em forma de V com constrição anteromedial e ampliações terminais. Urocleidoides ramentacuminatus n. sp. tem um OCM convoluto com, aproximadamente, uma volta no sentido anti-horário; uma peça acessória com uma porção distal em forma de gancho; uma âncora dorsal com haste curta e reta; e ponta da âncora com ornamentação como filamentos desfiados esclerotizados. Urocleidoides paradoxus é relatada pela primeira vez parasitando S. fasciatus.

Palavras-chave:
Amazônia; anostomidae; monogenoideos; parasitos; peixes de água doce

Introduction

Neotropical characiforms fish of the Anostomidae family have wide distribution in the watersheds of South and Central America (Nelson et al., 2016). This family currently comprises 14 genera and 155 species, many of which occur in the Amazon basin, with species of Schizodon Agassiz, 1829 and Laemolyta Cope, 1872 representing approximately 16% of the diversity (Nelson et al., 2016). Members of this family are important hosts for the life cycle of a broad diversity of parasites (Guidelli et al., 2006; Oliveira et al., 2017; Yamada et al., 2017), including platyhelminths belonging to the Class Monogenoidea (Cohen et al., 2013). Among anostomid species, only 7.7% has been investigated for monogenoidean parasites. Currently, 12 species of monogenoids are known to parasitize the gills, nostrils, body surface, urinary bladder, and ureter of members of 13 species of Anostomidae (see Table 1).

Table 1
Checklist of monogenoid species in fish of the family Anostomidae in Brazil.

Parasite species	Host species	Infection site	Locality	Reference
Jainus leporini	Leporinus copelandii	Gill filaments	Guandu River, Rio de Janeiro state	Abdallah et al. (2012)
Jainus leporini	Leporinus microcephalus	Gill filaments	Cruzeiro do Sul city, Acre state	Abdallah et al. (2012)
Jainus leporini	Leporinus friderici	Gill filaments	Jari and Igarapé Fortaleza rivers, Amapá State	Oliveira et al. (2017)
Jainus piava	Leporinus friderici	Gill filaments	Paranapanema, Taquari and Viados rivers, São Paulo state	Yamada et al. (2017)
Jainus piava	Schizodon borellii	Gill filaments	Paraná River, Paraná state	Karling et al. (2011)
Jainus piava	Megaleporinus obtusidens	Gill filaments	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)
Rhinoxenus arietinus	Leporinus elongates	Nostrils	Paraná River, Paraná state	Takemoto et al. (2009)
Rhinoxenus arietinus	Leporinus friderici	Nostrils	Paraná River, Paraná state	Guidelli et al. (2006)
Rhinoxenus arietinus	Leporinus lacustris	Nostrils	Paraná River, Paraná state	Guidelli et al. (2006)
Rhinoxenus arietinus	Leporinus obtusidens	Nostrils	Paraná River, Paraná state	Takemoto et al. (2009)
Rhinoxenus arietinus	Rhytiodus argenteofuscus	Nostrils	Solimões River, Amazonas state	Kritsky et al. (1988)
Rhinoxenus arietinus	Schizodon fasciatus	Nostrils	Solimões River, Amazonas state	Kritsky et al. (1988)
Rhinoxenus nyttus	Schizodon fasciatus	Nostrils	Solimões River, Amazonas state	Kritsky et al. (1988)
Rhinoxenus nyttus	Megaleporinus obtusidens	Nostrils	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)
Scleroductus yuncensi	Leporinus copelandii	Body	Guandu River, Rio de Janeiro state	Azevedo et al. (2010)
Tereancistrum flabellum	Leporinus friderici	Gill filaments	Sapucaí-Mirim and Paranapanema rivers, São Paulo state	Zago et al. (2017)
Tereancistrum flabellum	Leporinus amblyrhynchus	Gill filaments	Sapucaí-Mirim and Paranapanema rivers, São Paulo state	Zago et al. (2017)
Tereancistrum parvus	Leporinus obtusidens	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Tereancistrum parvus	Leporinus lacustris	Gill filaments	Paraná River, Paraná state	Guidelli et al. (2006), Takemoto et al. (2009)
Tereancistrum parvus	Leporinus friderici	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Tereancistrum parvus	Leporinus friderici	Gill filaments	Jari and Igarapé Fortaleza rivers, Amapá state	Oliveira et al. (2017)
Tereancistrum parvus	Leporinus elongates	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Tereancistrum parvus	Leporinus fasciatus	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Tereancistrum parvus	Megaleporinus obtusidens	Gill filaments	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)
Tereancistrum parvus	Leporinus microcephalus	Gill filaments	Cruzeiro do Sul, Acre state	Martins et al. (2017)
Tereancistrum paranaensis	Leporinus microcephalus	Gill filaments	Cruzeiro do Sul, Acre state	Martins et al. (2017)
Tereancistrum paranaensis	Megaleporinus obtusidens	Gill filaments	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)
Trinibaculum rotundus	Schizodon borellii	Gill filaments	Paraná River, Paraná state	Karling et al. (2011)
Urocleidoides paradoxus	Leporinus elongates	Gills filament	Paraná River, Paraná state	Takemoto et al. (2009)
Urocleidoides paradoxus	Leporinus lacustris	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Urocleidoides paradoxus	Leporinus obtusidens	Gill filaments	Paraná River, Paraná state	Takemoto et al. (2009)
Urocleidoides paradoxus	Rhytiodus microlepis	Gill filaments	Solimões River, Amazonas state	Kritsky et al. (1986)
Urocleidoides paradoxus	Leporinus friderici	Gill filaments	Paraná River, Paraná state	Guidelli et al. (2006)
Urocleidoides paradoxus	Leporinus friderici	Gill filaments	Jari River and Igarapé Fortaleza, Amapá state	Oliveira et al. (2017)
Urocleidoides paradoxus	Leporinus microcephalus	Gill filaments	Cruzeiro do Sul, Acre state	Martins et al. (2017)
Urocleidoides paradoxus	Megaleporinus obtusidens	Gill filaments	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)
Urocleidoides eremitus	Leporinus microcephalus	Gill filaments	Cruzeiro do Sul, Acre state	Martins et al. (2017)
Kritskyia eirasi	Leporinus microcephalus	Urinary bladder and ureter	Cruzeiro do Sul, Acre state	Martins et al. (2017)
Kritskyia eirasi	Leporinus friderici	Urinary bladder and ureter	Paraná River, Paraná state, Brazil	Guidelli et al. (2006)
Kritskyia eirasi	Leporinus lacustris	Urinary bladder and ureter	Paraná River, Paraná state	Guidelli et al. (2006)
Kritskyia eirasi	Megaleporinus obtusidens	Urinary bladder and ureter	Guaíba Lake, Rio Grande do Sul state	Wendt et al. (2018)

During a field survey of parasites from the gills of Schizodon fasciatus Spix & Agassiz, 1829 and Laemolyta proxima Garman, 1890 (Anostomidae) from the Jari River, a tributary of the Amazon River basin (northern Brazil), two new species of Urocleidoides Mizelle & Price, 1964 were found and are described herein. We also recorded for the first time Urocleidoides paradoxus Kritsky, Thatcher & Boeger, 1986 parasitizing the gills of S. fasciatus from the eastern Amazon.

Materials and Methods

Host fish collection

In March 2018, 15 specimens of S. fasciatus and 3 specimens of L. proxima were collected with fishing nets in the lower Jari River, near Jarilândia district, in municipality of Vitória do Jari, State of Amapá, Brazil (1°9'4.01”S; 52°0'53.22” W). Host scientific names were validated in accordance with Fricke et al. (2019), and identification was carried out in accordance with specialized literature (Queiroz et al., 2013).

This study was developed in accordance with the principles adopted by the Brazilian College of animal Experimentation (COBEA). Authorization from Ethic Committee in the Use of Animal of the Embrapa Amapá (Protocol N^o 014/2018) was also carried out.

Parasitological procedures

Gill arches were removed and placed in vials containing hot water (65° C). Each vial was vigorously shaken, and formalin was added to obtain a 5% solution. In the laboratory, the contents of each vial were examined under a dissecting microscope (Leica S6D) and monogenoids were removed from the gills or sediment using small probes. Some specimens were stained with Gomori’s trichrome (Humason, 1979; Boeger & Vianna, 2006) and mounted in Damar Gum or Canada balsam to determine the internal soft structures, while others were mounted in Hoyer’s or Gray & Wess medium (Humason, 1979) for the study of the sclerotized structures. Measurements, all in micrometers, were obtained according to the procedures described by Mizelle & Klucka (1953). The measurements inner and outer for the anchors follow the scheme illustrated in Figures 1j. Dimensions of organs and structures represent the straight line distances between the extreme ends, the total lengths of the male copulatory organ were carried out using ImageJ (Rasband, 1997) on drawing tube images. The mean is followed by the range and the number (n) of specimens measured in parentheses. Illustrations were prepared with the aid of a drawing tube on a Leica DM 2500 microscope with differential interference contrast and phase contrast optics. Illustrations of the soft and hard structures were prepared using pen and ink. Plates were prepared using PhotoPaint software. Prevalence and mean intensity follow Bush et al. (1997). Type specimens and vouchers were deposited in the Invertebrate Collection of the Museu Paraense Emílio Goeldi (MPEG), Belém, Pará state, Brazil.

Figure 1
Urocleidoides jariensis n. sp. (a) Holotype, whole-mount (ventral view). (b) Male copulatory organ. (c) Vagina. (d) Vaginal sclerite. (e) Ventral bar. (f) Dorsal bar. (g) Hook (pair 5). (h) Hook (pair 1). (i) (pairs 2, 3, 4, 6 and 7). (j) Ventral anchor. (k) Dorsal anchor.

Results

Taxonomic summary:

Class Monogenoidea Bychowsky, 1937

Subclass Polyonchoinea Bychowsky, 1937

Order Dactylogyridea Bychowsky, 1937

Dactylogyridae Bychowsky, 1933

Urocleidoides Mizelle & Price, 1964

Urocleidoides jariensis n. sp. (Figure 1ak)

Description: Based on nine specimens; three mounted in Gomori’s trichrome, six mounted in Hoyer’ medium. Body fusiform (Figure 1a) total length excluding haptor 255 (218–298; n = 9) long, 107 (59–154; n = 9) wide at level of gemarium. Tegument smooth. Cephalic margin tapered; moderately developed terminal lobes; three bilateral pairs of head organs with rod-shaped secretion; cephalic glands unicellular, posterolateral to pharynx (observed only in paratypes). Four eyes (two pairs); posterior pair larger than anterior pair; accessory chromatic granules present in cephalic area, elliptical (Figure 1a). Mouth subterminal, midventral; pharynx 21 (17–25; n = 8) long, 23 (13–30; n = 8) wide, muscular, glandular; moderately elongated esophagus. Two intestinal caeca, posteriorly confluent to gonads, lacking diverticula. Genital pore opening midventral; genital atrium muscular. Testis, seminal vesicle, vas deferens, prostatic reservoir not observed. Copulatory complex comprising male copulatory organ (MCO) and accessory piece (Figure 1b); MCO sclerotized, tubular, spiral, counterclockwise, with one coil, 39 (28–49; n = 6) long; circular sclerotized tandem brim associated with base of MCO; proximal portion of MCO slightly expanded, distal aperture slightly acute. Accessory piece sclerotized, non-articulated with MCO, comprising a variable distal sheath, surrounding the MCO (Figure 1b). Germarium elongate 68 (44–94; n = 6) long, 28 (15–45; n = 6) wide (Figure 1a). Mehlis glands, ootype and seminal receptacle not observed. Vagina single (Figure 1c), heavily sclerotized; vaginal aperture dextro-ventral, marginal; vagina comprising vaginal vestibule, funnel-shaped with short vaginal canal. Vaginal sclerite (Figure 1d) 30 (25–35; n = 4) long, hook-shaped with longitudinal superficial groove. Vitellaria dense throughout trunk, except in region of reproductive organs. Eggs not observed. Peduncle short; haptor hexagonal 68 (45–105; n = 9) long, 71 (11–106; n = 9) wide (Figure 1a). Anchors similar; well-developed superficial root, short deep root, slightly curved elongate shaft, recurved and acute point. Ventral anchor (Figure 1j), outer 38 (36–40; n = 7) long, inner 38 (35–41; n = 7) long, base 14 (13–15; n = 7) wide, evenly curved shaft and point, point acute, extending at level of tip of superficial root. Dorsal anchor smaller than ventral anchor (Figure 1k) outer 31 (31–33; n =7) long, inner 33 (31–38; n = 7) long, base 11 (10–12; n = 7) wide, shaft elongate, point not extending level of tip of superficial root. Ventral bar (Figure 1e) 48 (30–55; n = 8) long, slightly curved, broadly V-shaped with anteromedial constriction and enlarged ends. Dorsal bar (Figure 1f) 45 (33–55; n = 8) long, U-shaped, with slightly enlarged ends, slightly curved in posterior direction. Hook pair 1, 21 (19–23; n = 8) long (Figure 1h) and hooks pairs 2–4, 6–7, 27 (21–32; n = 8) long (Figure 1i), similar in shape, composed of two subunits, shank with inflation comprising approximately 2/3 of total shank length; erected thumb, lightly curved long shaft, delicate point; filamentous hook (FH) with loop extending to union of shank subunits; pair 5 smaller than other hooks, 15 (13–16; n = 8) long, composed of single unit and inflated base (Figure 1g).

Type host:Schizodon fasciatus Spix & Agassiz, 1829.

Prevalence: 100%.

Mean intensity: 14.0 (11–21).

Site of infection: Gill filaments.

Type locality: Jari River, municipality of Vitória do Jari, in Amapá state, Brazil (1°9'4.01”S; 52°0'53.22”W).

Specimens deposited: Holotype MPEG Nº 00206 and 8 paratypes MPEG Nº 00207–00214.

Etymology: The specific name refers to the locality.

Remarks

The new species resembles Urocleidoides malabaricusi Rosim, Mendoza-Franco & Luque, 2011 reported from the gills of Hoplias malabaricus (Characiformes: Erythrinidae) based on the morphology of the MCO, anchors and bars. Both species possess MCO with one ring, bars with enlarged ends, ventral bar V-shaped, dorsal bar U-shaped, and anchors with well-developed roots. However, Urocleidoides jariensis n. sp. differs from U. malabaricusi in the absence of a muscular pad on the right side of the body that surrounds the copulatory complex as reported in U. malabaricusi. The new species also differs from U. malabaricusi by possessing a dextro-ventral vagina (sinistral in U. malabaricusi).

Urocleidoides ramentacuminatus n. sp. (Figure 2aj)

Figure 2
Urocleidoides ramentacuminatus n. sp. (a) Holotype, whole-mount (dorsal view). (b) Male copulatory organ. (c) Vagina. (d) Vaginal sclerite. (e) Ventral bar. (f) Dorsal bar. (g) Hooks (pair 2, 3, 4, 6 and 7). (h) Hooks (pair 1 and 5). (i) Ventral anchor. (j) Dorsal anchor.

Description: Based on 14 specimens; nine mounted in Gomori’s trichrome, five mounted in Hoyer’s. Body fusiform (Figure 2a), total length excluding haptor 259 (178–323; n = 14) long, 79 (51–130; n = 14) wide at level of gemarium. Tegument smooth or scaled (Figure 2a). Cephalic margin tapered; moderately developed terminal lobes; three bilateral pairs of head organs with rod-shaped secretion; cephalic glands unicellular, posterolateral to pharynx (observed only in paratypes). Four eyes (two pairs), posterior pair larger than anterior pair; accessory chromatic granules present in cephalic area, elliptical (Figure 2a). Mouth subterminal, midventral; pharynx 14 (10–17; n = 8) long, 15 (17–18; n = 8) wide, muscular, glandular; esophagus short. Two intestinal caeca, posteriorly confluent to gonads, lacking diverticula. Genital pore opening midventral; genital atrium muscular. Testis, seminal vesicle, vas deferens, prostatic reservoir not observed. Copulatory complex comprising MCO and accessory piece (Figure 2b); MCO sclerotized, one counterclockwise coil, 56 (40–73; n = 7) long, sclerotized expansion at the base of MCO, flange-like; proximal portion of MCO slightly expanded, distal aperture acute (Figure 2b). Accessory piece sclerotized, non-articulated with the MCO, distal portion hook shaped. Germarium fusiform 43 (27–61; n = 5) long, 17 (12–25; n = 5) wide. Mehlis glands, ootype and seminal receptacle not observed. Vagina single (Figure 2c), heavily sclerotized; vaginal aperture dextro-ventral, marginal; vagina comprising vaginal vestibule, bulb-shaped with short vaginal canal. Vaginal sclerite (Figure 2d) 28 (20–42; n = 10) long, robust, with proximal portion curved, distally straight, acute, thumb rounded. Vitellaria dense throughout trunk, except in region of reproductive organs. Eggs not observed. Peduncle short; haptor hexagonal, 49 (35–75; n = 14) long, 63 (32–104; n = 14) wide. Anchors dissimilar. Ventral anchor (Figure 2i), outer 24 (21–27; n = 7) long, inner 24 (19–30; n = 7) long, base 9 (n = 7) well-developed superficial root, short deep root; evenly curved shaft and point; point acute, extending just past level of tip of superficial root. Dorsal anchor (Figure 2j) outer 20 (17–25; n = 7) long, inner 24 (20–28; n = 7) long, base 9 (8–9; n = 7) wide, subtriangular superficial root, short deep root; straight shaft, short; anchor point presents ornamentation as sclerotized shredded filaments, extending just past level of tip of superficial root. Ventral bar (Figure 2e) 34 (24–40; n = 13) long, rod-shape. Dorsal bar (Figure 2f) 29 (21–45; n = 12) long, narrow, U-shaped, with small terminal enlargement ends, slightly curved in posterior direction. Hooks pairs 2–4, 6–7, 24 (10–43; n = 10) long (Figure 2g), similar in shape, shank elongated with inflation; erected thumb, lightly curved shaft, delicate curved point; filamentous hook (FH) not observed; hooks pairs 1 and 5 smaller than other hooks with inflation comprising approximately 1/2 of the total shank length, pair 1, 14 (10–17; n = 10) long (Figure 2h); pair 5, 13 (10–18; n = 10) long (Figure 2h).

Type host:Schizodon fasciatus Spix & Agassiz, 1829.

Prevalence: 100%

Mean intensity: 7.0 (5–17).

Site of infection: Gill filaments.

Type locality: Jari River, municipality of Vitória do Jari, Amapá state, Brazil (1°9'4.01”S; 52°0'53.22”W).

Other records:Laemolyta proxima Garman, 1890.

Locality: Jari River, municipality of Vitória do Jari, Amapá state, Brazil (1°9'4.01”S; 52°0'53.22”W).

Prevalence: 66.6%.

Mean intensity: 2.0 (1–4).

Specimens deposited: Holotype MPEG Nº 002015; 6 paratypes MPEG Nº 00216–00221 and 7 vouchers MPEG Nº 00222–00228.

Etymology: The specific epithet derives from the Latin (rament = shreds + acumin = point) and refers to the dorsal anchor morphology with ornamentation as sclerotized shredded filaments.

Remarks

Urocleidoides ramentacuminatus sp. n. is similar to Urocleidoides carapus Mizelle, Kritsky & Crane, 1968 from Gymnotus carapo (Gymnotidae: Gymnotiformes) and Urocleidoides cultellus Mendoza-Franco & Reina, 2008 from Brachyhypopomus occidentalis (Gymnotiformes: Hypopomidae) due to the morphology of the dorsal anchor. However, U. ramentacuminatus sp. n. can be easily distinguished from both species by possessing a robust vaginal sclerite (absent in U. carapus; grooved rod distally hooked in U. cultellus); a dextro-ventral vagina (vagina sinistral or sinistral-ventral in U. carapus; midventral, long and coiled in U. cultellus), and MCO with one counterclockwise ring (more than one ring in U. carapus and U. cultellus).

Urocleidoides paradoxus Kritsky, Thatcher & Boeger, 1986 (Figure 3ai)

Figure 3
Urocleidoides paradoxus Kritsky, Thatcher & Boeger, 1986. (a) Whole mount. (b) Male copulatory organ. (c) Vaginal sclerite. (d) Ventral bar. (e) Dorsal bar. (f) Hook pair 1 and 5. (g) Hooks (pairs 2, 3, 4, 6 and 7). (h) Ventral anchor. (i) Dorsal anchor.

Urocleidoides paradoxusKritsky, Thatcher & Boeger (1986): 5–8, Figure 10–18 (descr); Cohen et al. (2013): 67, 120–121, Figure 343 (citat).

Type host:Rhytiodus microlepis Kner 1858.

Site of infection: Gill filaments.

Type locality: Solimões River near Ilha Marchantaria, municipality of Manaus, Amazonas state, Brazil.

Other records:Leporinus elongatus (Takemoto et al., 2009), Leporinus lacustris (Guidelli et al., 2006; Takemoto et al., 2009); Leporinus obtusidens (Takemoto et al., 2009), Rhytiodus microlepis (Kritsky et al., 1986), Leporinus friderici (Guidelli et al., 2006; Oliveira et al., 2017), Leporinus macrocephalus (Martins et al., 2017) and Schizodon fasciatus (present study).

Prevalence: 100%.

Mean intensity: 10.5 (10–24).

Specimens deposited: 9 vouchers MPEG Nº 00229–00237.

Comparative measurements: These are shown in Table 2.

Table 2
Comparative measurements between specimens of Urocleidoides paradoxus.

	Urocleidoides paradoxus Solimões River (type locality)	N	Urocleidoides paradoxus Jari River (present study)	N
Body
Length	230 (166– 291)	7	353 (295–463)	20
Width	139 (86–191)	7	83 (67–94)	20
Pharynx
Length	15 (12–19)	7	19 (17–21)	20
Width	15 (12–20)	7	-
Haptor
Length	47 (37–55)	7	59 (53–67)	20
Width	101 (76–134)	7	75 (66–83)	20
Ventral anchor
Outer	21 (18–25)	7	-
Inner	22 (920–29)	7	-
Base	15 (13–16)	7	-
Dorsal anchor
Outer	25 (24–26)	7	-
Inner	25 (22–25)	7	-
Base	16 (16–18)	7	-
Ventral bar
Length	37 (28–40)	7	39 (37-40)	20
Width	4 (4–4)	7	-
Dorsal bar
Length	37 (28–42)	7	37 (35-40)	20
Width	4 (4–4)	7	-
Hook pair 1	15 (13–16)	7	(21–22)	20
Hook pair 2, 3, 4, 6, 7	31 (25–40)	7	27 (25–30)	20
Hook pair 5	23 (19–28)	7	(18–19)	20
Germarium
Length	68 (60–72)	7	-
Width	15 (14–18)	7	-
MCO	43 (34–60)		77	20
Vaginal sclerite length	34 (30–37)	7	31 (28–32)	20

• N: Number of samples.

Remarks

The specimens available are conspecific with U. paradoxus, mainly due to sharing the morphology of the anchors, bars, hooks, copulatory complex, vagina dextral and vaginal sclerite. The specimens studied here differ morphometrically in some measurements from specimens from the type locality (Table 2).

Discussion

Species of monogenoids belonging to Urocleidoides Mizelle & Price, 1964, Jainus Kritsky & Crane, 1968; Tereancistrum Kritsky, Thatcher & Kayton, 1980; Trinibaculum Kritsky, Thatcher & Kayton, 1980; Rhinoxenus Kritsky, Boeger & Thatcher, 1988; Scleroductus Jara & Cone, 1989 and Kritskyia Kohn, 1990 have been reported parasitizing Anostomidae species (Table 1). However, none of these taxa seems to be restrict to anostomid fish. Except by species of Jainus, Tereancistrum, Trinibaculum and Rhinoxenus that are restrict to characiform hosts, the other genera are reported from at least two different Neotropical fish order. Species of Kritskya and Scleroductus are parasites of ureters and body surface, respectively, from characiform and siluriform hosts, whereas members of Urocleidoides can be found parasitizing the gills of species of 13 families from 4 different host fish orders (i.e., Characiformes, Cyprinodontiformes, Gymnotiformes and Siluriformes). In the present study, U. paradoxus is reported for the first time on the S. fasciatus gills, which has two new species of Urocleidoides described herein.

Urocleidoides Mizelle & Price, 1964 was proposed to accommodate Urocleidoides reticulatus Mizelle & Price, 1964 from Poecilia reticulata Peters, 1859. Twenty-six species of Urocleidoides are currently known parasitizing Characiformes (Erythrinidae, Lebiasinidae, Anostomidae, Crenuchidade, Ctenolucidae, Parodontidae and Curimatidae), Cyprinodontiformes (Poeciliidae, Profundulidae) and Gymnotiformes (Hypopomidae) from North, South and Central America (see Table 3). Urocleidoides sensuKritsky et al. (1986) is distinguished from other dactylogyrid species by a combination of characters, including the morphology of MCO with counterclockwise rings, the presence of a sinistral vaginal sclerite, unmodified anchors, according to Kritsky et al. (1986), and hook pair 1 and 5 usually reduced with enlarged shanks. In this study, Urocleidoides jariensis n. sp. and Urocleidoides ramentacuminatus n. sp. present all these morphological characters for the diagnosis of Urocleidoides sensu stricto.

Table 3
List of species of Urocleidoides sensu stricto.

Parasite species	Host species	Infection site	Locality	Reference
Urocleidoides advenai	Brachyhypopomus occidentalis	Gill filaments	Aguas Claras River (Panamá)	Mendoza-Franco & Reina (2008)
Urocleidoides aimarai	Hoplias aimara	Gill filaments	Xingú River, Altamira, Pará state (Brazil)	Moreira et al. (2015)
Urocleidoides anops	Characidium caucanum	Gill filaments	Pance River, Cáli (Colombia)	Kritsky & Thatcher (1974)
Urocleidoides brasiliensis	Hoplias malabaricus	Gill filaments	Cuibá River (Brazil)	Rosim et al. (2011)
Urocleidoides bulbophallus	Hoplias malabaricus	Gill filaments	Caeté River, Bragança, Pará state (Brazil)	Ferreira et al. (2017)
Urocleidoides cuiabai	Hoplias malabaricus	Gill filaments	Cuibá River (Brazil)	Rosim et al. (2011)
Urocleidoides cultellus	Brachychypopomus occidentalis	Gill filaments	Aguas Claras River (Panamá)	Mendoza-Franco & Reina (2008)
Urocleidoides curimatae	Steindachnerina argentea	Gill filaments	Arouca River, D'Abadie (Trinidad and Tobago)	Molnar et al. (1974)
Urocleidoides eremitus	Hoplias malabaricus	Gill filaments	Janauaca Lake, Manaus, Amazonas state (Brazil)	Kritsky et al. (1986)
Urocleidoides flegomai	Piabucina panamensis	Gill filaments	Frijolito River (Panamá)	Mendoza-Franco et al. (2007)
Urocleidoides hypopomi	Brachyhypopomus brevirostris	Gill filaments	Paraná River (Argentina)	Suriano (1997)
Urocleidoides malabaricusi	Hoplias malabaricus	Gill filaments	Cuibá River (Brazil)	Rosim et al. (2011)
Urocleidoides naris	Hoplias malabaricus	Nostrils	Cuibá River (Brazil)	Rosim et al. (2011)
Urocleidoides neotropicalis	Saccodon dariensis	Gill filaments	Piriati River (Panamá)	Mendoza-Franco & Reina (2008)
Urocleidoides paradoxus	Rhytiodus microlepis	Gill filaments	Amazon River, Amazonas state (Brazil)	Kritsky et al. (1986)
Urocleidoides paranae	Hoplias malabaricus	Gill filaments	Paraná River, Mato Grosso do Sul state (Brazil)	Ferreira et al. (2017)
Urocleidoides piriatiu	Ctenolucius beani	Gill filaments	Piriati River (Panamá)	Mendoza-Franco & Reina (2008)
Urocleidoides reticulatus	Poecilia reticulata	Gill filaments	Aquarium, Sacramento (California, USA)	Mizelle & Price (1964)
	Actinopterygii	Gill filaments	México
Urocleidoides similuncus	Poecilia gillii	Gill filaments	Frijolito River (Panamá)	Mendoza-Franco et al. (2007)
Urocleidoides simonae	Profundulus punctatus	Gill filaments	Nandalumi River, Chiapas (Mexico)	Mendoza-Franco et al. (2015)
Urocleidoides surianoae	Cyphocharax voga	Gill filaments	Lake Chascomús, Buenos Aires (Argentina)	Rossin & Timi (2016)
Urocleidoides triangulus	Cyphocharax voga	Gill filaments	Lake Chascomús, Buenos Aires (Argentina)	Rossin & Timi (2016)
Urocleidoides vaginoclaustroides	Pseudoxiphophorus bimaculatus	Gill filaments	Danta River, Chiapas (Mexico)	Mendoza-Franco et al. (2015)
Urocleidoides vaginoclaustrum	Xiphophorus hellerii	Gill filaments	Hyderabad and Secunderabad (India)	Jogunoori et al. (2004)
Urocleidoides visiofortatus	Brachychypopomus occidentalis	Gill filaments	Aguas Claras River (Panamá)	Mendoza-Franco & Reina (2008)
Urocleidoides xinguensis	Hoplias aimara	Gill filaments	Xingú River, Altamira, Pará state (Brazil)	Moreira et al. (2015)
Urocleidoides jariensis n. sp.	Schizodon fasciatus	Gill filaments	Jari River, Amapá state (Brazil)	Present study
Urocleidoides ramentacuminatus n. sp.	Schizodon fasciatus and Laemolyta proxima	Gill filaments	Jari River, Amapá state (Brazil)	Present study

Some species of Urocleidoides have been described and posteriorly relocated to other genera: Demidospermus lebedevi (Kritsky & Thatcher, 1976); Diaphorocleidus affinis (Mizelle, Kritsky & Crane, 1968); Diaphorocleidus kabatai (Molnar, Hanek & Fernando, 1974); Diaphorocleidus microstomus (Mizelle, Kritsky & Crane, 1968); Philocorydoras corydori (Molnar, Hanek & Fernando, 1974); Philocorydori margolisi (Molnar, Hanek & Fernando, 1974); Palombitrema heteroancistrium (Price & Bussing, 1968); Characithecium costaricensis (Price & Bussing, 1967) and Nanayella megorchis (Mizelle & Kritsky, 1969) (Price & Bussing, 1968; Kritsky et al., 2000; Jogunoori et al., 2004; Mendoza-Franco et al., 2009; Yamada et al., 2015; Acosta et al., 2019), due to the absence of morphological characters (i.e., presence of vaginal sclerite, MCO rolled counterclockwise, hook pair 1 and 5 reduced) that define this genus.

Urocleidoides paradoxus was described in Rhytiodus microlepis Kner, 1858 from the Solimões River, in Amazonas State, Brazil. This unique species of genus with a vagina that present dextral opening, and this characteristic was added for diagnose of this genus (see Kritsky et al., 1986). Urocleidoides jariensis n. sp. and Urocleidoides ramentacuminatus n. sp. resemble U. paradoxus because both species share the presence of the vaginal dextral opening, a characteristic present only in the species of Urocleidoides reported to members of Anostomidae family. Studies suggest that most monogenoids species are restricted to their hosts at highest taxonomic levels (i.e., family or order), probably due to broad historical restrictions (e.g., immunological, morphological and/or evolution), which acts at a large scale (Boeger & Kritsky, 1997; Desdevises et al., 2002).

The present study increased the species number of Urocleidoides sensu stricto to 27, as well as that of monogenoids in Amazonian fish, thus contributing to knowledge of the diversity of these parasites in this important Neotropical region, which includes a great, yet underestimated diversity of monogenoids. However, Urocleidoides is one of the most specious and taxonomically problematic genera among Neotropical dactylogyrids. It is possible that, in the future, the taxonomic position of incertae sedis species are clarified with the aid of molecular studies together with morphological analyses of holotypes and paratypes.

Acknowledgements

We would like to thank Mr. João Pena de Oliveira for assistance during the collection of fishes and for research grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) (# 303013/2015-0) for Marcos Tavares-Dias. This work was partially supported by Programa de Pós-Graduação em Biodiversidade Tropical (PPGBio) for granting a Ph.D. Scholarship grant to Marcos S.B. Oliveira.

• How to cite: Oliveira MSB, Santos-Neto JF, Tavares-Dias M, Domingues MV. New species of Urocleidoides (Monogenoidea: Dactylogyridae) from the gills of two species of Anostomidae from the Brazilian Amazon. Braz J Vet Parasitol 2020; 29(3); e007820. https://doi.org/10.1590/S1984-29612020039

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Publication Dates

• Publication in this collection
  28 Aug 2020
• Date of issue
  2020

History

• Received
  05 Apr 2020
• Accepted
  29 Apr 2020