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Urocleidoides
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Neotropical Helminthology
Neotropical Helminthology, 2023, vol. 17 (2), 101-116
ORIGINAL ARTICLE / ARTÍCULO ORIGINAL
A
NEW SPECIES OF
UROCLEIDOIDES
(MONOGENOIDEA: DACTYLOGYRIDAE)
PARASITE OF
PSECTROGASTER AMAZONICA
(CHARACIFORMES:
CURIMATIDAE) AND
CAENOTROPUS LABYRINTHICUS
(CHARACIFORMES:
CHILODONTIDAE) FROM TOCANTINS RIVER, MARANHÃO STATE, BRAZIL
WITH CHECKLIST OF THE GENUS
UNA NUEVA ESPECIE DE PARÁSITO
UROCLEIDOIDES
(MONOGENOIDEA:
DACTYLOGYRIDAE) DE
PSECTROGASTER AMAZONICA
(CHARACIFORMES:
CURIMATIDAE) Y
CAENOTROPUS LABYRINTHICUS
(CHARACIFORMES:
CHILODONTIDAE) DEL RÍO TOCANTINS, ESTADO DE MARANHÃO, BRASIL Y
UNA LISTA DE VERIFICACIÓN DEL GÉNERO
Carine Almeida Miranda Bezerra
1
, Álvaro José Bittencourt de Freitas
2
, Diego Carvalho Viana
3
,
Simone Chinicz Cohen
2*
& Marcia Cristina Nascimento Justo
2
ISSN Versión Impresa 2218-6425 ISSN Versión Electrónica 1995-1403
DOI: https://dx.doi.org/10.24039/rnh20231721591
Volume 17, Number 2 (jul - dec) 2023
Este artículo es publicado por la revista Neotropical Helminthology de la Facultad de Ciencias Naturales y Matemática, Universidad Nacional Federico
Villarreal, Lima, Perú auspiciado por la Asociación Peruana de Helmintología e Invertebrados Af nes (APHIA). Este es un artículo de acceso abierto,
distribuido bajo los términos de la licencia Creative Commons Atribución 4.0 Internacional (CC BY 4.0) [https:// creativecommons.org/licenses/by/4.0/
deed.es] que permite el uso, distribución y reproducción en cualquier medio, siempre que la obra original sea debidamente citada de su fuente original.
ABSTRACT
Parasites are important components of global biodiversity and among them, the Monogenoidea stands out as a parasites
of f shes, commonly af ecting the gills of their hosts. T e present study aimed to analyze the presence of species of
Urocleidoides
parasitizing characiform f shes from the Tocantins River. During the study, specimens of
Psectrogaster
amazonica
Eigenmann & Eigenmann and
Caenotropus labyrinthicus
(Kner) were collected from the urban zone of the
municipality of Imperatriz, state of Maranhão. T e gills of the f sh were removed and placed in vials containing hot
1
Programa de Pós-Graduação em Ciência Animal, Universidade Estadual do Maranhão (UEMA). Cidade Universitária Paulo
VI, Avenida Lourenço Vieira da Silva 1000, 65055-310 São Luís, MA, Brazil.
2
Laboratório de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz (IOC), FIOCRUZ. Avenida Brasil 4365, 21040-900
Rio de Janeiro, RJ, Brazil.
3
Núcleo de Estudos Morfof siológicos Avançados (NEMO), Universidade Estadual da Região Tocantina do Maranhão
(UEMASUL). Campus Imperatriz, Rua Godofredo Viana 1300, 65901-480 Imperatriz, MA, Brazil.
* Corresponding author
: scohen@ioc.f ocruz.br
Carine A. M. Bezerra:
https://orcid.org/0000-0003-4842-1595
Álvaro José B. de Freitas:
https://orcid.org/0000-0003-4338-7893
Diego C. Viana:
https://orcid.org/0000-0002-3302-9892
Simone C. Cohen:
https://orcid.org/0000-0001-8204-336X
Marcia C. N. Justo:
https://orcid.org/0000-0002-0684-3389
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Bezerra
et al.
water (65°C), and posteriorly, absolute ethanol was added to reach a concentration of 70%. A new species of
Urocleidoides
was described parasitizing both hosts.
Urocleidoides psectrogasteri
n. sp. can be distinguished by its congeners species
principally by the morphology of the MCO. Besides, the known species
U. tocantinensis
also was found parasitizing
C. labyrinthicus
, which was reported as a new host for this species. In addition, a checklist containing all species of
Urocleidoides
is presented to compile the known data on this monogenoid genus.
Keywords:
Fish parasites –
Monogenoidean – Neotropical Region – Tocantins-Araguaia Basin –
Urocleidoides
psectrogasteri
n. sp.
RESUMEN
Los parásitos son componentes importantes de la biodiversidad global y entre ellos, se destacan los Monogenoidea como
parásitos de los peces, afectando comúnmente las branquias de sus hospederos. El objetivo del presente estudio fue
analizar la presencia de especies de
Urocleidoides
que parasitan peces Characiformes del río Tocantins. Durante el estudio,
se recolectaron ejemplares de
Psectrogaster amazonica
Eigenmann & Eigenmann y
Caenotropus labyrinthicus
(Kner) de
la zona urbana del municipio de Imperatriz, estado de Maranhão, Brasil. Se extrajeron las branquias de los peces y se
colocaron en viales con agua caliente (65°C), y posteriormente se añadió etanol absoluto hasta alcanzar una concentración
del 70%. Se describió una nueva especie de
Urocleidoides
que parasita a ambos hospedadores.
Urocleidoides
psectrogasteri
n. sp. se puede distinguir por sus especies congéneres principalmente por la morfología de la MCO. Además, la especie
conocida
U. tocantinensis
, también fue encontrada parasitando a
C. labyrinthicus
, la cual fue reportada como un nuevo
hospedero para esta especie. Además, se presenta una lista de verifcación que contiene todas las especies de
Urocleidoides
para recopilar los datos conocidos sobre este género monogenoideo.
Palabras clave:
Bacia del Tocantins-Araguaia –
Monogenoideos – Parásitos de peces – Region Neotropical –
Urocleidoides
psectrogasteri
n. sp.
INTRODUCTION
Urocleidoides
Mizelle & Price, 1964 was proposed
to accommodate the species
U. reticulatus
Mizelle &
Price, 1964 from the gills of
Poecilia reticulata
Peters,
1859 (Poeciliidae), which was collected from Capitol
Aquarium, Sacramento, California, USA (Mizelle &
Price, 1964). Kritsky & Tatcher (1983) listed 30 species
of the genus described from four diferent orders of hosts:
Characiformes, Cyprinodontiformes, Gymnotiformes
e Siluriformes (Mizelle
et al
., 1968; Mizelle & Kritsky,
1969; Molnar
et al.
,1974; Kritsky & Tatcher 1974,
1976, 1983). Kritsky
et al
. (1986) revised the genus,
described two new species,
U. eremitus
Kritsky, Tatcher
& Boeger, 1986 and
U. paradoxus
Kritsky, Tatcher &
Boeger, 1986 and added new morphological details in
species described previously:
U. reticulatus
,
U. anops
Kritsky & Tatcher 1974
and
U. curimatae
Molnar,
Hanek & Fernando, 1974. Te authors emended the
diagnosis of the genus, characterizing the species by the
presence of vaginal sclerite, male copulatory organ with
counterclockwise ring, tandem gonads, no modifcated
anchors, hook with dilated shank and pairs 1 and 5
of hooks usually reduced in size. Kritsky
et al.
(1986)
considered 22 species as
incertae sedis
, mainly by the
absence of the vaginal sclerite
.
Posteriorly, Ferreira
et
al
. (2017) added
U. advenai
Mendoza-Franco & Reina,
2008 to this status of
incertae sedis
.
Further studies reallocate some of these species on newly
described genera as
Ameloblastella
Kritsky, Mendoza-
Franco & Scholz, 2000,
Aphanoblastella
Kritsky, Mendoza-
Franco & Scholz, 2000,
Characithecium
Mendoza-Franco,
Reina & Torchin, 2009,
Diaphorocleidus
Jogunoori,
Kritsky & Venkatanarasaiah, 2004,
Nanayella
Acosta,
Mendoza-Palmero, Silva & Scholz, 2019,
Philocorydoras
Suriano, 1986 and
Sciadicleithrum
Kritsky, Boeger &
Tatcher, 1989 (Price & Bussing, 1968; Kritsky
et al
.,
1989, 2000; Jogunoori
et al
., 2004; Mendoza-Franco
et
al
., 2009; Yamada
et al
., 2015; Acosta
et al
., 2019).
Recently, Santos-Neto & Domingues (2023) proposed
four new species of
Urocleidoides
from Characiformes and
Gymnotiformes and revalidate the
incertae sedis
species,
Urocleidoides gymnotus
Mizelle, Kritsky & Crane, 1968
and
Urocleidoides carapus
Mizelle, Kritsky & Crane,
1968, based in molecular sequences. One of the new
species,
Urocleidoides vanini
Santos-Neto & Domingues,
2023 did not present vaginal sclerite as the
incertae sedis
revalidated by these authors. From the species previously
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assigned as
incertae sedis
by Kritsky
et al.
(1986), six have
not yet been relocated to other genera.
Species of
Urocleidoides
have been described from
Psectrogaster amazonica
Eigenmann & Eigenmann and
Caenotropus labyrinthicus
(Kner), as
U. tocantinensis
Freitas, Bezerra, Meneses, Justo, Viana & Cohen,
2021
and
U. paratriangulus
Freitas, Bezerra, Meneses,
Viana, Justo & Cohen 2021 and the latter also from
C.
labyrinthicus
(Freitas
et al
., 2021)
.
In this present study, a new species of
Urocleidoides
was
found parasitizing
P. amazonica
and
C. labyrinthicus
and is described herein. In addition,
C. labyrinthicus
is
reported as new host for
U. tocantinensis
and a checklist
of
Urocleidoides
species with all current information
about their hosts, localities and validity is presented.
MATERIAL AND METHODS
Fishes were collected in Tocantins River at the urban
zone of Imperatriz municipality, state of Maranhão
,
129
specimens of
P. amazonica
(standard length 11.5–16.1 cm;
total weight 42–100 g)
and 20 specimens
C. labyrinthicus
(standard length 12.1–14.5 cm; total weight 38–70 g).
Te fshes were caught with the aid of local fshermen
and were carried to the “Núcleo de Estudos Morfológicos
Avançados (NEMO)” at the Universidade Estadual da
Região Tocantina do Maranhão (UEMASUL), Maranhão
State, Brazil, where they were identifed.
Te gills of fsh were removed and placed in vials containing
hot water (65°C), and vigorously shaken to detach the
parasites from the gill flaments. Posteriorly, absolute
ethanol was added to reach a concentration of 70%. Tose
vials containing the gills were then sent to the “Laboratório
de Helmintos Parasitos de Peixes, Instituto Oswaldo Cruz,
FIOCRUZ”, Rio de Janeiro state, Brazil. Te gills and
sediments were analyzed in Petri dishes. Monogenoids
were collected under a stereoscopic microscope, and the
specimens mounted in Hoyer’s medium to study the
sclerotized structures (Humason, 1979).
Parasitological indexes were calculated as proposed
by Bush
et al
. (1997), followed by standard deviation.
Measurements are presented in micrometers; range values
are followed by mean and number of structures measured
in parentheses. Morphometric studies were performed
through ImageJ software (Wayne, 2010), distributed by
the National Institutes of Health (NIH), and available at
https://imagej.nih.gov/ij/download.html. Te authorship
of the taxa followed the recommendation of Article 50.1
of the International Code of Zoological Nomenclature
(ICZN), which deals with the identity of the authors.
A checklist of valid
Urocleidoides
species is presented
herein, providing information about hosts and
geographical distribution. For construction of this
checklist, published papers with original descriptions
and/or reports of species, taxonomic revisions, and
checklists were used and online biodiversity databases as
Taxonomic Catalog of Brazilian Fauna, PubMed, Scopus,
Google Scholar and CAB Abstracts.
Posgraduate theses and abstract scientifc meetings do
not constitute formal publications and were thus not
considered.
For Brazilian states, abbreviations are presented as follows:
AC
: Acre;
AL
: Alagoas;
AM
: Amazonas;
AP
: Amapá;
BA
:
Bahia;
CE
: Ceará;
DF
: Distrito Federal;
ES
: Espírito
Santo;
GO
: Goiás;
MA
: Maranhão;
MG
: Minas Gerais;
MS
: Mato Grosso do Sul;
MT
: Mato Grosso;
PA
: Pará;
PB
: Paraíba;
PE
: Pernambuco;
PI
: Piauí;
PR
: Paraná;
RO
: Rondônia;
RJ
: Rio de Janeiro;
RN
: Rio Grande do
Norte;
RR
: Roraima;
RS
: Rio Grande do Sul;
SC
: Santa
Catarina;
SE
: Sergipe;
SP
: São Paulo;
TO
: Tocantins.
Ethic aspects
: Te fsh sample collection protocol and
laboratory procedures were approved by the Research
Ethics Committee of “Universidade Estadual do
Maranhão” (UFMA), Maranhão State, Brazil under
protocol number 43/2021, and the environmental
collection license was obtained from the System for
Authorization and Information on Biodiversity (SISBIO),
under protocol number 79538-1.
RESULTS
TAXONOMY
Class Monogenoidea Bychowsky, 1937
Subclass Polyonchoinea Bychowsky, 1937
Order Dactylogyridea Bychowsky, 1937
Dactylogyridae Bychowsky, 1933
Urocleidoides
Mizelle & Price, 1964
Urocleidoides psectrogasteri
sp. nov Bezerra, Freitas, Cohen
& Justo
(Fig. 1)
Type host.
Psectrogaster amazonica
Eigenmann &
Eigenmann (Curimatidae).
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Type locality.
Tocantins River (5°27’50’S; 47°33’48’W),
at the urban zone of Imperatriz municipality.
Other hosts
:
Caenotropus labyrinthicus
(Kner)
(Chilodontidae)
Infestation parameters.
P. amazonica
: Total number of
hosts: 129; prevalence: 17%; total number of parasites:
25; mean intensity: 1.14 (±0.34); mean abundance: 0.19
(±0.45); range of intensity: 1–2.
C. labyrinthicus
: Total
number of hosts: 20; prevalence: 5%; intensity: 3 (only
one host was parasitized); mean abundance: 0.15 (±0.67).
Deposited material.
Holotype CHIOC 40210.
Paratypes CHIOC 40211, 40212, 40213, 40214, 40215,
40216, 40217 a-c.
Etymology
: Te specifc name refers to the scientifc
name of the host
Psectrogaster amazonica
Figure 1.
Urocleidoides psectrogasteri
sp. nov from
Psectrogaster amazonica
(Curimatidae) from Tocantins
River, at the urban zone of Imperatriz municipality. A. Total, ventral view (composite). B. Copulatory
complex; C. Vaginal sclerite; D. Dorsal bar; E. Ventral Bar; F. Ventral anchor; G. Dorsal anchor; H. Hook.
Description based on 23 specimens mounted in Hoyer’s
medium: Body fusiform, 250–564 (384, n= 23) long
by 97–201 (139, n= 23) wide. Tree pairs of cephalic
glands. Two pairs of eyespots, equidistant, anterior pair
smaller than posterior. Pharynx 14–22 (18, n=5) ovate
and muscular. Peduncle short. Haptor sub-hexagonal
75–184 (117, n= 22) wide. Anchors robust, dissimilar
in shape. Ventral anchor with well-developed roots,
protruding superfcial root, semi-circular shape, rounded
deep root, evenly curved shaft and short point, 24–53
(39, n=46) long and base 15–22 (18, n=46); Dorsal
anchor with rectangular-shaped superfcial root and
deep root distally round, evenly curved shaft and acute
point 23–34 (29, n= 44) long and base 12–19 (16, n=
44). Ventral bar robust, slightly curved, with enlarged
extremities, concave posteromedial 27–77 (46, n=9) and
drop-like shaped posteromedian projection, short and
thin 5–14 (8, n= 21) long. Dorsal bar slender V-shaped,
slightly curved, 37–70 (54, n= 23) long. Seven pairs of
marginal hooks, with distribution of ancyrocephaline,
fve pairs ventral and two dorsal. Hooks similar in
shape, divided in two subunits, protruded thumb, curved
point, shank straight with proximal dilation, comprising
⅔ of shank length; FH loop ¼ of shank length; pairs
1 and 5 slightly smaller than others, pair 1 12–27 (19,
n = 34); pair 2 19–30 (25, n= 35); pair 3 19–34 (26,
n= 33); pair 4 19–39 (28, n= 33); pair 5 14–28 (21, n=
28); pair 6 19–35 (27, n= 32); pair 7 19–34 (27, n= 34)
long. Copulatory complex composed of male copulatory
organ (MCO) with auriculate base, sickle shape, 28–44
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(36, n=18) and accessory piece bifurcated, with two
elongated parts, articulated to MCO base, 27–41 (33,
n=18) long. Testis dorsal to germarium; seminal vesicle
a distal dilation of vas deferens; single prostatic reservoir
present. Germarium elongated. Vaginal pore sinistral;
vagina comprising a vaginal vestibule cup-shaped,
sclerotized and a vaginal canal long; seminal receptacle
round. Vaginal sclerite present in the middle of the body,
with a longitudinal groove in the middle, erected thumb,
18–44 (29, n= 18) long. Eggs not observed. Vitellaria
present, heavily distributed throughout the body, except
in reproductive organs.
Remarks
: Te new species is allocated in
Urocleidoides
by the presence of vaginal sclerite, vagina in sinistral
position, and hook pairs 1 and 5 reduced in size. Te
MCO of the new species is similar to those of some
species by the absence of coils on the MCO, as observed
in
U. surianoae
Rossin & Timi, 2016,
U. falxus
Zago,
Yamada, Yamada, Franceschini, Bongiovani & Silva,
2020
and
U. tocantinensis
. Te new species is evidently
distinguished from these species by the morphology
of the male copulatory organ, which is pincer-shaped
(reverse J-shaped, with expanded proximal end in
U.
surianoae
, male copulatory organ appearing to twist
into itself and resembling the shape of a sickle and base
enlarged in
U. falxus
and straight tube with enlarged base
in
U
.
tocantinensis
). Te new species also resembles
U.
tocantinensis
considering the bifurcation of the accessory
piece and morphology of vagina. Considering the
projection of the ventral bar, the new species is similar
to
Urocleidoides boullengerelae
Freitas, Bezerra, Meneses,
Justo, Viana & Cohen, 2021,
Urocleidoides piriatiu
Mendoza-Franco & Reina, 2008 and
U. tocantinensis
,
difering that in
Urocleidoides psectrogasteri
sp. nov. the
posteromediam projection is reduced in size. Despite
the projection in
Urocleidoides surianoae
Rossim &
Timi, 2016
is similar in shape and size, it difers from
U
.
psectrogasteri
sp. nov. by the anteromedial position.
Checklist of
Urocleidoides
spp. from Neotropical
Region
Urocleidoides
spp. have been recorded from 3 diferent
orders (34 in Characiformes, eight in Gymnotiformes
and four in Cyprinodontiformes), associated with 14
families and 48 species of fshes (Fig. 2). Most of them
were reported from fshes belonging to Characiformes,
from eight diferent families with predominance of
Erythrinidae, mainly from
Hoplias malabaricus
(Bloch).
Regarding the geographical distribution, most species are
reported from Brazil, followed by Mexico and Panama,
and records in Argentina, Colômbia, El Salvador,
Honduras and Trindad and Tobago, thus presenting
a broad host and locality spectrum. Until now, thirty-
one species of
Urocleidoides
are referred from Brazil in
diferent localities, rivers and basins within the country.
Figure 2. Distribution of
Urocleidoides
spp. within host families of three orders
of freshwater fshes. Blue: Characiformes, Orange: Cyprinodontiformes, Grey:
Gymnotiformes.
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Urocleidoides aimarai
Moreira, Scholz & Luque, 2015
Type-host and locality
:
Hoplias aimara
(Valenciennes)
(Characiformes: Erythrinidae) [Xingu River, around
Altamira, PA,
Brazil
].
Other hosts and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae);
Leporinus friderici
(Bloch) (Characiformes, Anostomidae) [Batalha River,
SP,
Brazil
].
Records
: Moreira
et al.
(2015); Dias
et al.
(2017); Gião
et al.
(2020).
Urocleidoides anops
Kritsky & Tatcher, 1974
Type-host and locality
:
Characidium caucanum
Eigenmann (Characiformes: Crenuchidae) [Pance River,
Cali, Valle,
Colombia
].
Other host and localiy
:
Psalidodon fasciatus
(Cuvier)
(Characiformes: Characidae) [Noc-choncunchey and
Dzonot Cervera cenotes,
Mexico
].
Record
: Kritsky & Tatcher (1974); Mendoza-Franco
et
al.
(1999).
Urocleidoides atilaiamarinoi
Santos-Neto &
Domingues, 2023
Type host and locality
:
Hoplerythrinus unitaeniatus
(Agassiz) (Characiformes: Erythinidae) [Igarapé
Maratininga (Moju River Basin), municipality of
Tailândia, PA,
Brazil
].
Other locality:
Balneário Aracu (Guamá River Basin),
municipality of Ourém, Pará,
Brazil
.
Record:
Santos-Neto & Domingues (2023).
Urocleidoides boulengerellae
Freitas, Bezerra,
Meneses, Justo, Viana & Cohen, 2021
Type-host and locality
:
Boulengerella cuvieri
(Spix &
Agassiz) (Characiformes: Ctenoluciidae) [Tocantins
River, near the municipality of Tupiratins, TO,
Brazil
].
Other localities
: Arraias River, close to the municipality
of Babaçulândia; Tocantins River, close to the
municipalities of Aguiarnópolis and Estreito; at the
mouth of the Itaueiras River, in the municipality of
Estreito, MA,
Brazil
.
Record
: Freitas
et al.
(2021).
Urocleidoides brasiliensis
Rosim, Mendoza-Franco &
Luque, 2011
Type-host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Cuiabá River, MT,
Brazil
].
Other
localities
: Cristalino River, MT; Caeté River,
Bragança; Maracanã River, Nova Timboteua; Piriá and
Guripi Rivers,Viseu; Maparanim River, Municipality of
Terra Alta; Itabocal River, Irituia, PA; Upper Paraná River
Floodplain, PR, MS; Paraná River, PR; Guandú River,
RJ,
Brazil
.
Records
: Rosim
et al.
(2011); Graça
et al.
(2013); Ferreira
et al.
(2017).
Urocleidoides bulbophallus
Ferreira, Rodrigues,
Cunha & Domingues, 2017
Type-host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Caeté River, Bragança,
PA,
Brazil
].
Other localities:
Itabocal River, Irituia; Piriá River,
Viseu; Maparanim River, Terra Alta; Gurupi River, Viseu,
PA,
Brazil.
Records
: Ferreira
et al.
(2017).
Urocleidoides carapus
Mizelle, Kritsky & Crane,
1968
Type-host and locality
:
Gymnotus carapo
(Linnaeus)
(Gymnotiformes, Gymnotidae) [Amazon Basin,
Brazil
].
Other host and locality
:
Sternopygus macrurus
(Bloch
& Schneider) (Gymnotiformes, Gymnotidae) [Guamá
River, Ourém, PA,
Brazil
].
Records
: Mizelle
et al.
(1968); Santos-Neto & Domingues
(2023).
Urocleidoides cuiabai
Rosim, Mendoza-Franco &
Luque, 2011
Type host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Cuiabá River, MT,
Brazil
].
Other localities
: Maracanã River, Nova Timboteua;
Gurupi and Piriá Rivers, Viseu, PA; Araguaia River,
MT; Jaguari-Mirim River, MG, SP; Upper Paraná River
Floodplain, PR, MS; Paraná River, PR; Guandu River,
RJ; Batalha River, SP,
Brazil
.
Records
: Rosim
et al.
(2011); Graça
et al.
(2013);
Gasques
et al.
(2016); Ferreira
et al.
(2017); Dias
et al.
(2017); Gião
et al.
(2020).
Urocleidoides cultellus
Mendoza-Franco & Reina,
2008
Type-host and locality:
Brachyhypopomus occidentalis
(Regan) (Gymnotiformes: Hypopomidae) [Águas Claras
River at its confuence with the Bayano Lake,
Republic
of Panama
].
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Record
: Mendoza-Franco & Reina (2008).
Urocleidoides curimatae
Molnár, Hanek & Fernando,
1974
Type-host and locality:
Steindachnerina argentea
(Gill)
(=
Curimata argentea
) (Characiformes: Curimatidae)
[Arouca River near D’Abadie] after
Trinidad
.
Record
: Molnar
et al.
(1974).
Urocleidoides digitabulum
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva, 2020
Type-host and locality
:
Leporinus friderici
(Characiformes: Anostomidae) [Sapucaí-Mirim River,
Upper Parana River Basin, SP,
Brazil
].
Other hosts and localities
:
Leporinus octofasciatus
Steindachner;
Megaleporinus elongatus
(Valenciennes)
(Characiformes: Anostomidae)
[Jurumirim Reservoir,
Paranapanema River, Upper Paraná River Basin, SP,
Brazil
].
Record
: Zago
et al.
(2020).
Urocleidoides eremitus
Kritsky, Tatcher & Boeger,
1986
Type-host and locality
:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Janauaca Lake near
Manaus, AM,
Brazil
].
Other hosts and localities:
Leporinus friderici
;
Megaleporinus macrocephalus
(Garavello & Britski)
(Characiformes: Anostomidae) [Chascomus Lake,
Buenos Aires province,
Argentina;
fsh farms in
Cruzeiro
do Sul and Rio Branco, AC; Igarapé Fortaleza basin,
in the municipality of Macapá, AP; Jaguari Mirim
River, MG and SP; Machado River, MG; Cuiabá River,
MT; Maracanã River, Nova Timboteua; Piriá River,
Viseu; Caeté River, Bragança, PA; Upper Paraná River
Floodplain in the PR, MS; Guandu River, RJ; Batalha
River, Peixe River; Pirassununga lagoons, SP,
Brazil;
Tambopata River, Madre de Dios,
Perú
].
Records
: Kritsky
et al.
(1986); Iannacone & Luque
(1993); Suriano (1997a); Rosim
et al.
(2011); Corrêa
et
al.
(2013), Alcântara & Tavares-Dias (2015); Dias
et al.
(2017); Ferreira
et al.
(2017); Martins
et al.
(2017 a, b);
Gião
et al.
(2020); Negreiros
et al.
(2021).
Urocleidoides falxus
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva, 2020
Type-host and locality:
Megaleporinus elongatus
(Characiformes: Anostomidae) [Sapucaí-Mirim River,
Upper Paraná River basin, SP,
Brazil
].
Other locality
: Jurumirim Reservoir, Paranapanema
River, Upper Paraná River basin, SP,
Brazil
.
Record
: Zago
et al.
(2020).
Urocleidoides fegomai
Mendoza-Franco, Aguirre-
Macedo & Vidal-Martínez, 2007
Type-host and locality
:
Piabucina panamensis
Gill
(Characiformes: Lebiasinidae) [Frijolito River,
Panama].
Record
: Mendoza-Franco
et al.
(2007).
Urocleidoides gymnotus
Mizelle, Kritsky & Crane, 1968
Type-host and locality
:
Gymnotus carapo
(Gymnoti-
formes, Gymnotidae) [Amazon Basin,
Brazil
].
Other host and locality
:
Sternopygus macrurus
(Gymnotiformes, Gymnotidae) [Guamá River, Ourém,
PA,
Brazil
].
Records
: Mizelle
et al.
(1968); Santos-Neto &
Domingues (2023).
Urocleidoides hypopomi
Suriano, 1997
Type-host and locality:
Brachyhypopomus brevirostris
(Steindachner) (Gymnotiformes: Hypopomidae) [Paraná
River, Puerto Italia, Corrientes Province,
Argentina
].
Record
: Suriano (1997a).
Urocleidoides indianensis
Oliveira, Silva, Vieira &
Acosta, 2021
Type-host and locality
:
Parodon nasus
Kner
(Characiformes: Parodontidae) [Indiana stream (Capivara
River, Tietê River, Upper Paraná River basin), Botucatu,
SP,
Brazil
].
Record
: Oliveira
et al.
(2021).
Urocleidoides jariensis
Oliveira, Santos-Neto,
Tavares-Dias & Domingues, 2020
Type-host and locality:
Schizodon fasciatus
Spix &
Agassiz (Characiformes: Anostomidae) [Lower Jari River,
near Jarilândia district, in municipality of Vitória do Jari,
AP,
Brazil
].
Record
: Oliveira
et al.
(2020).
Urocleidoides macrosoma
Santos-Neto & Domingues,
2023
Type host and locality
:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Vila Segredo – Segredo
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Bezerra
et al.
River (Quatipuru River Basin), Tauari, municipality of
Capanema, PA,
Brazil
].
Record
: Santos-Neto & Domingues (2023).
Urocleidoides malabaricusi
Rosim, Mendoza-Franco
& Luque, 2011
Type-host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Cuiabá River, MT,
Brazil
].
Other localities
: Caeté River, Bragança; Gurupi River,
Viseu; Maracanã River, Nova Timboteua; Maparanim
River, Terra Alta; Piriá River, Viseu; Itabocal River,
Irituia, PA; Upper Paraná River Floodplain PR, MS;
Batalha River, SP; Paraná River, PR,
Brazil.
Records
: Rosim
et al.
(2011); Graça
et al.
(2013);
Gasques
et al.
(2016); Ferreira
et al.
(2017); Dias
et al.
(2017); Gião
et al.
(2020).
Urocleidoides naris
Rosim, Mendoza-Franco &
Luque, 2011
Type-host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Cuiabá River, MT,
Brazil
].
Other localities:
Guandu River, RJ; Jaguari-Mirim River,
MG and SP; Machado River, MG,
Brazil
.
Record
: Rosim
et al.
(2011).
Urocleidoides nataliapasternakae
Santos-Neto &
Domingues, 2023
Type host and locality
:
Brachyhypopomus brevirostris
(Steindachner) (Gymnotiformes: Hypopomidae)
[Balneário Aracu (Guamá River Basin), municipality of
Ourém, PA,
Brazil
].
Record
: Santos-Neto & Domingues (2023).
Urocleidoides neotropicalis
Mendoza -Franco &
Reina, 2008
Type-host and locality:
Saccodon dariensis
Meek &
Hildebrand (Characiformes: Parodontidae) [Piriati River
at its confuence with the Chagres River Basin,
Republic
of Panama
].
Record
: Mendoza-Franco & Reina (2008).
Urocleidoides paradoxus
Kritsky, Tatcher & Boeger,
1986
Type-host and loca
Õ
lity:
Rhytiodus microlepis
Kner
(Characiformes, Anostomidae) [Solim
Õ
es River near Ilha
Marchantaria, Manaus, AM,
Brazil
].
Other hosts and localities
:
Leporinus friderici
;
Leporinus
lacustris
Amaral Campos;
Megaleporinus elongatus
;
Megaleporinus macrocephalus
,
Megaleporinus obtusidens
(Valenciennes) (Characiformes, Anostomidae) [Parana
River, Puerto Italia, Corrientes province,
Argentina
;
fsh farms in Cruzeiro do Sul and Rio Branco, AC; Furo
do Catalão, near Encontro das Aguas, Manaus; Coari
Manaus section, Lake Baixio; Lake Ananá, Lake Preto
and Lake Catalão, Iranduba, AM; lower Jari River, near
Jarilândia district, in municipality of Vitória do Jari, AP;
Upper Paraná River foodplain, PR; Lake Guaiba, RS;
Batalha River, SP;
Brazil
].
Records
: Kritsky
et al.
(1986); Suriano (1997a); Guidelli
et al.
(2006, 2011); Takemoto
et al.
(2009); Souza
et al.
(2017); Martins
et al.
(2017a,b); Wendt
et al.
(2018);
Oliveira
et al.
(2020); Negreiros
et al.
(2021).
Urocleidoides paranae
Ferreira, Rodrigues, Cunha &
Domingues, 2017
Type-host and locality:
Hoplias malabaricus
(Characiformes: Erythrinidae) [Upper Paraná River
foodplain (Paraná River Basin; Paraná, Paranapanema
Sub-basin), PR and MS,
Brazil
].
Records
: Graça
et al.
(2013); Ferreira
et al.
(2017).
Remarks: Te authors examined vouchers of
U. eremitus
collected from
H. malabaricus
from the Upper Paraná
River foodplain of Graça
et al.
(2013) and indicated that
these specimens are members of
U. paranae
.
Urocleidoides paratriangulus
Freitas, Bezerra,
Meneses, Justo, Viana & Cohen, 2021
Type host
and locality
:
Psectrogaster amazonica
(Characiformes: Curimatidae) [Tocantins River, close to
the municipality of Embiral, MA,
Brazil
].
Other hosts and localities:
Cyphocharax gouldingi
Vari (Characiformes: Curimatidae);
Caenotropus
labyrinthicus
(Chraciformes: Chilodontidae);
Mylesinus
pauscisquamatus
Jégu & Santos (Characiformes:
Serrasalmidae) [Farinha River, close to the municipality
of Estreito, MA; Tocantins River, close to the urban
perimeter of Imperatriz, MA; Tocantins River, close to
the municipalities of Aguiarnópolis and Estreito, MA; at
the mouth of the Itaueiras River, in the municipality of
Estreito, MA; Tocantins River, close to the municipalities
of Aguiarnópolis and Estreito, MA; at the mouth of the
Itaueiras River, municipality of Estreito, MA; João Aires
River, close to the municipality of Palmeirantes, TO;
Arraias River, close to the municipality of Babaçulândia,
TO,
Brazil
].
Record
: Freitas
et al.
(2021).
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Urocleidoides parodoni
Oliveira, Silva, Vieira &
Acosta, 2021
Type-host and locality:
Parodon nasus
(Characiformes:
Parodontidae) [Indiana stream (Capivara River, Tietê
River, Upper Paraná River basin), Botucatu, SP,
Brazil
].
Record
: Oliveira
et al.
(2021).
Urocleidoides piriatiu
Mendoza-Franco & Reina,
2008
Type-host and locality:
Ctenolucius beani
(Fowler)
(Characiformes: Ctenoluciidae) [Piriati River at its
confuence with the Chagres River Basin,
Republic of
Panama
].
Record
: Mendoza-Franco & Reina (2008).
Urocleidoides psectrogasteri
Bezerra, Freitas, Cohen
& Justo 2023
Type-host and locality
:
Psectrogaster amazonica
(Characiformes: Curimatidae); [Tocantins River, at the
urban zone of Imperatriz municipality, MA;
Brazil
].
Other hosts:
Caenotropus labyrinthicus
(Chraciformes:
Chilodontidae)
Record
:
Present study
Urocleidoides ramentacuminatus
Oliveira, Santos-
Neto, Tavares-Dias & Domingues, 2020
Type-host and locality:
Schizodon fasciatus
(Characiformes: Anostomidae) [Lower Jari River, near
Jarilândia district, in municipality of Vitória do Jari, AP,
Brazil
].
Other host:
Laemolyta proxima
Garman (Characiformes:
Anostomidae).
Record:
Oliveira
et al.
(2020).
Urocleidoides reticulatus
Mizelle & Price, 1964
Type-Host and locality:
Poecilia reticulata
(Peters)
[=
Lebistes reticulatus
(Peters)] (Cyprinodontiformes:
Poeciliidae) [Host obtained from Capitol Aquarium,
Sacramento, California,
United States
].
Other hosts and localities:
Belonesox belizanus
Kner;
Poecilia mexicana
Steindachner;
Poecilia petenensis
Gunther;
Xiphophorus helleri
Heckel;
Xiphophorus
maculatus
(Günther) (Cyprinodontiformes: Poeciliidae)
[Private Aquaria, Prague and Ceske Budejovice,
Czech
Republic,
imported freshwater ornamental fsh,
Australia;
Imported freshwater ornamental fsh,
Sri
Lanka
].
Records
: Mizelle & Price (1964); Evans & Lester (2001);
Pineda-López
et al.
(2005); Trujillo-González
et al.
(2018).
Urocleidoides sapucaiensis
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva 2020
Type-host and locality:
Megaleporinus elongatus
(Characiformes: Anostomidae) [Sapucaí-Mirim River,
Upper Paraná River basin, SP,
Brazil
].
Other locality
: Jurumirim Reservoir, Paranapanema
River, Upper Paraná River basin, SP,
Brazil
.
Record
: Zago
et al.
(2020).
Urocleidoides similuncus
Mendoza-Franco, Aguirre-
Macedo, & Vidal-Martínez, 2007
Type-host and locality:
Poecilia gillii
(Cyprinodon-
tiformes, Poeciliidae) [Frijolito River,
Panama
].
Record:
Mendoza-Franco
et al.
(2007).
Urocleidoides simonae
Mendoza-Franco, Caspeta-
Mandujano, Salgado-Maldonado & Matamoros,
2015
Type-host and locality:
Profundulus punctatus
(Günther)
(Cyprinodontiformes: Profundulidae) [Nandalumi River,
Chiapa de Corso, Chiapas,
Mexico
].
Other hosts and localities
:
Profundulus punctatus
(=
Profundulus balsanus
);
Profundulus guatemalensis
(Günther),
Profundulus kreiseri
Matamoros, Shaefer,
Hernández & Chakrabarty,
Tlaloc labialis (=Profundulus
labialis)
(Günther),
Profundulus oaxacae
(Meek);
Profundulus
sp. 1,
Profundulus
sp. 2. (Cyprinodontiformes:
Profundulidae) [Cauta River (Lempa River Basin);
Cauca River, Nonoalpa River, Quebrada Los Tecomates
(Lempa River Basin),
El Salvador;
Nil River (Guacalate
River Basin); El Cantil River (Guacalate Rivr Basin);
Creek El Platanar (Guacalate River basin),
Guatemala
;
River at rancho San Antonio, Chicoasén; Arroyo Ojo
de Agua, El Canelar, La Frailesca, Chiapas, Creek Tres
Picos, Copainalá and River Nandalumi, Chiapa de
Corso, Chiapas State; Ahl from La Laca River (Papagayo
River Basin); Cahoapan River, Tamarindo River (Nexpa
River basin), Guerrero State; Creek Los Sabinos (Atoyac-
Verde River Basin), Chicaguaxtla River, Concepción
del Progreso (Atoyac-Verde River Basin), Chico River,
San Lorenzo Albarradas (Atoyac-Verde basin), Aguacate
River, Juquilá, Manialtépec River Basin, Oaxaca State;
Mexico
].
Record
: Mendoza-Franco
et al.
(2015).
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Bezerra
et al.
Urocleidoides sinus
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva, 2020
Type-host and locality:
Schizodon nasutus
Kner
(Characiformes: Anostomidae) [Sapucaí-Mirim River,
Upper Paraná River basin, SP,
Brazil
].
Other hosts and localities
:
Leporinus striatus
Kner,
Schizodon intermedius
Garavello & Britski (Characiformes:
Anostomidae) [Jurumirim Reservoir, Paranapanema
River, Upper Paraná River basin, SP,
Brazil
].
Record
: Zago
et al.
(2020).
Urocleidoides solarivaginatus
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva, 2020
Type-host and locality
:
Leporinus friderici
(Characiformes: Anostomidae) [Sapucaí-Mirim River,
Upper Paraná River basin, SP,
Brazil
].
Other hosts and locality
:
Leporinus octofasciatus
,
Leporinus striatus
(Characiformes: Anostomidae)
[Jurumirim Reservoir, Paranapanema River, Upper
Paraná River basin, SP,
Brazil
].
Record
: Zago
et al.
(2020).
Urocleidoides surianoae
Rossin & Timi, 2016
Type-host and locality:
Cyphocharax voga
(Hensel)
(Characiformes: Curimatidae) [Chascomus Lake, Buenos
Aires province,
Argentina
].
Record
: Rossin & Timi (2016).
Urocleidoides tenuis
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva 2020
Type-host and locality
Apareiodon piracicabae
(Eigenmann) (Characiformes: Parodontidae) [Streams
of the Middle Paranapanema River, Upper Paraná River
basin, SP,
Brazil
].
Other hosts and localities
:
Apareiodon afnis
(Steindachner),
Parodon nasus
(Characiformes:
Parodontidae) [Jurumirim Reservoir, Paranapanema
River, Upper Paraná River basin; Indiana stream
(Capivara River, Tietê River, Upper Paraná River basin),
Botucatu, SP,
Brazil
].
Records
: Zago
et al.
(2020); Oliveira
et al.
(2021).
Urocleidoides tocantinensis
Freitas, Bezerra, Meneses,
Justo, Viana & Cohen, 2021
Type host and locality:
Psectrogaster amazonica
(Characiformes, Curimatidae) [Tocantins River, close to
the municipality of Embiral, MA,
Brazil
].
Other host and localities:
Caenotropus labyrinthicus
(Characiformes, Chilodontidae);
Mylesinus
pauscisquamatus
(Characiformes, Serrasalmidae)
[Farinha River, close to the municipality of municipality
of Estreito, MA; Tocantins River, close to the urban
perimeter of Imperatriz; Tocantins River, at the urban
zone of Imperatriz municipality, MA; Arraias River, close
to the municipality of Babaçulândia, TO;
Brazil
].
Records:
Freitas
et al.
(2021);
Present study
.
Urocleidoides triangulus
(Suriano, 1981) Rossin &
Timi, 2016
Type host and locality
:
Cyphocharax gilbert
(Quoy &
Gaimard) (Characiformes: Curimatidae) [Chascomus
Lake, Buenos Aires province,
Argentina
].
Other hosts and localities:
Cyphocharax modestus
(Fernández-Yépez);
Cyphocharax nagelii
(Steindachner);
Cyphocharax voga
(Characiformes: Curimatidae) [Guandu
River, RJ; Batalha River and Peixe River, Anhembi, SP,
Brazil
].
Records
: Suriano (1981); Suriano (1997b); Vieira
et al.
(2013); Abdallah
et al.
(2015); Rossin & Timi (2016);
Dias
et al.
(2017); Freitas
et al.
(2021).
Urocleidoides uncinus
Zago, Yamada, Yamada,
Franceschini, Bongiovani & Silva
2020
Type-host and locality:
Gymnotus sylvius
Albert &
Fernandes-Matioli (Gymnotiformes: Gymnotidae)
[Sapucaí-Mirim River, Upper Paraná River basin, SP,
Brazil
]
.
Other locality
: Jurumirim Reservoir, Paranapanema
River, Upper Paraná River basin, SP,
Brazil.
Record
: Zago
et al.
(2020).
Urocleidoides vaginoclaustroides
Mendoza-Franco,
Caspeta-Mandujano, Salgado-Maldonado &
Matamoros, 2015
Type-host and locality
:
Pseudoxiphophorus bimaculatus
(Heckel) (Cyprinodontiformes: Poeciliidae) [Danta
River, a tributary of the Río Lacantún basin in the
Biosphere Reserve of Montes Azules (BRMA), Chiapas,
Mexico
].
Other host and locality
:
Poeciliopsis retropinna
(Regan)
(Cyprinodontiformes: Poeciliidae) [Arroyo Jose,
Chiriquicito River,
Panama
].
Record:
Mendoza-Franco
et al.
(2015).
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Urocleidoides vaginoclaustrum
Jogunoori, Kritsky
& Venkatanarasaiah, 2004
Type-host and locality:
Xiphophorus hellerii
(Cyprinodontiformes: Poeciliidae) [Aquarium fshes in
the twin cities of Hyderabad and Secunderabad,
India
].
Other hosts and localities
:
Pseudoxiphophorus bimaculatus
(=
Heterandria bimaculata
),
Xiphophorus birchmanni
;
Xiphophorus malinche
(Cyprinodontiformes, Poeciliidae),
Tlaloc labialis
(=
Profundulus labialis
);
Tlaloc portillorum
(=
Profundulus portillorum
) (Cyprinodontiformes,
Profundulidae) [Creek at Ojojona, Francisco Morazán
(Nacaome River basin); Lepaterique, Francisco Morazán
(Nacaome River basin),
Honduras
. Danta River, a
tributary of the Lacantún River, Chiapas; River at rancho
San Antonio, Chicoasén, Chiapas; Los Berros Spring, San
Pedro River Mezquital basin, Durango; Arroyo Xontla
and Conzintla River, Pánuco drainage, Hidalgo; Benito
Juárez, part of Zontecomatlán River; La Antigua River
basin, Veracruz,
Mexico
].
Records
: Jogunoori
et al.
(2004); Salgado-Maldonado
et al.
(2014, 2016) Mendoza-Palmero & Aguilar-
Aguilar (2008); Mendoza-Franco
et al.
(2015); Bautista-
Hernández
et al.
(2014; 2019); Mendoza-Garfas
et al.
(2017).
Remarks:
Tis species was referred by Rodríguez-
Santiago
et al.
(2016) parasitizing
Pterygoplichthys
pardalis
(Siluriformes, Loricariidae). Considering that
Urocleidoides
spp. are not reported from Siluriformes
and these authors stated that only three specimens were
collected, we did not consider this report.
Urocleidoides vanini
Santos-Neto & Domingues,
2023
Type host and locality
:
Erythrinus erythrinus
(Bloch
& Schneider) (Characiformes, Erythrinidae) [Vila
Perseverança, Palheta River (Guamá River Basin),
municipality of São Domingos do Capim, PA,
Brazil
].
Record
: Santos-Neto & Domingues (2023).
Urocleidoides visiofortatus
Mendoza-Franco & Reina,
2008
Type-host and locality:
Brachyhypopomus occidentalis
(Regan) (Gymnotiformes: Hypopomidae) [Águas Claras
River at its confuence with the Bayano Lake,
Panama
].
Record
: Mendoza-Franco & Reina (2008).
Urocleidoides xinguensis
Moreira, Scholz & Luque,
2015
Type-host and locality:
Hoplias aimara
(Characiformes,
Erythrinidae) [Xingu River, near Altamira, PA,
Brazil
].
Record
: Moreira
et al.
(2015).
DISCUSSION
Urocleidoides
was originally described by Mizelle & Price
(1964) to accommodate the type species,
U. reticulatus
.
Te authors proposed that species of the genus are
restricted to those that present, besides vaginal sclerite,
overlapping (tandem) gonads, counterclockwise cirrus
rings, unmodifed anchors and hooks (pairs 1, 5 usually
reduced) with enlarged shanks. Afterwards, some authors
identifed diferent characteristics to the genus, Rosim
et al
. (2011) stated that the ventral bar with enlarged
extremities may be considered a generic character
for this genus. Zago
et al
. (2020) added an amended
diagnosis, considering the recent discovery of new
species of
Urocleidoides
, including “vagina lateral (dextral
or sinistral) sclerotized; receptacle seminal present”.
Besides these characteristics, Rossim & Timi (2016),
Zago
et al.
(2020) and Freitas
et al.
(2021) described
species with absence of coils in the male copulatory
organ, and this character may be included as diagnostic
for the genus, according to the amendment made by
Zago
et al.
(2020). Santos-Neto & Domingues (2023)
postulated that, although the presence of vaginal sclerite
is a diferential character for
Urocleidoides
, it cannot be
considered a main characteristic for the species of the
genus. According to these authors, the species described
from gymnotiform hosts, even without vaginal sclerite,
share some morphological characteristics.
Te type species of
Urocleidoides
have been described
from aquarium fshes, found in native habitats in the
Neotropical Region, as
U. reticulatus
from
Poecilia
reticulata
from Capitol Aquarium, Sacramento,
California, USA, and another species of this genus was
also reported from aquarium fshes,
U. vaginoclaustrum
,
described from
Xiphophorus hellerii
. Te hosts from both
species were collected from Neotropical Region and are
available in aquarium in diferent countries: Israel, Czech
Republic, India, California (USA) and in Central Mexico
(Kritsky
et al
., 1986; Jogunoori
et al
., 2004; Mendoza-
Palmero & Aguilar-Aguilar, 2008).
From the total number of species, 27 were reported
parasitizing a single host species, while 19 species are
image/svg+xml
112
Neotropical Helminthology (Lima). Vol. 18, N
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2, jul - dic 2023
Bezerra
et al.
found in more than one host species, ranging from 2 to
6 species, belonging or not to the same family. All species
of
Urocleidoides
found in more than one host species are
specifc to the fsh order that they parasitize, and within
the order, 12 species are restricted to one family, while
7 were recorded in more than one family, mainly in 2
diferent families from the same order, with emphasis in
U
.
paratriangulus
and
U. tocantinensis
, the only species
recorded in 3 diferent families. Tis demonstrated that,
despite the generalist behavior of
Urocleidoides
, in which
all known species are found in 3 diferent orders, each
species shows a specifcity to the host.
Hoplias malabaricus
is the host species which present
the highest diversity in species: seven species from
Urocleidoides
were described from diferent river basins in
Brazil (Rosim
et al.
2011; Ferreira
et al.,
2017; Santos-
Neto & Domingues, 2023). Variations in size and shape
of haptoral structures were observed by Rosim
et al.
(2011) from diferent river basins and were considered
to be intraspecifc variation. According to Ferreira
et
al.
(2017), this is probably due to geographic distance,
phenotypic plasticity of parasites or host induced
morphological change. Rosim
et al.
(2011) found their
new species in
H. malabaricus
from diferent basins.
Nevertheless,
H. malabaricus
appears to be a species
complex when comparing cytogenetic and molecular
studies. Tus, the diversity of species presented in this
host may be artifcial, considering that they represent
diferent
Hoplias
species that may harbour diferent
Urocleidoides
spp. Considering
Hoplias
, nine species were
reported in 10 associations from
H. malabaricus
and
H.
aimara.
Anostomidae is the most representative family housing
Urocleidoides
spp., represented by 12 diferent species in
23 associations host-parasite, followed by Poeciliidae,
with 11 species in 13 associations and Curimatidae, with
8 species and 10 associations.
Previous studies reported
Urocleidoides
spp. as parasites
of
P. amazonica
and
C. labyrinthicus.
In the present study,
besides the new species,
Urocleidoides tocantinensis
were
found parasitizing
C. labyrinthicus
, amplifying the host
spectrum of this monogenoidean.
In this paper, the number of valid species in genus
Urocleidoides sensu stricto
was increased to 46, as well
as that of monogenoids in the Tocantins River basin,
contributing to knowledge of the diversity of these
parasites in this important region, which includes
an endemic diversity of fsh and consequently,
monogenoideans parasites. Further studies on other
host species from this basin, whose fauna of parasites
is underestimated, will provide interesting and valuable
information about biogeographical and evolutionary
research on dactylogyrids in the Neotropics.
Author contributions
:
CRediT (Contributor Roles
Taxonomy)
CAMB
= Carine A. M. Bezerra
AJBF
= Álvaro José B. de Freitas
DCV
= Diego C. Viana
SCC
= Simone C. Cohen
MCNJ
= Marcia C. N. Justo
Conceptualization
:CAMB, AJBF, SCC, MCNJ
Data curation:
CAMB, AJBF
Formal Analysis
: SCC, MCNJ
Funding acquisition
: SCC, MCNJ, DCV
Investigation
: CAMB, AJBF, SCC, MCNJ
Methodology
: CAMB, AJBF
Project administration
: SCC, MCNJ
Resources
: SCC, MCNJ, DCV
Supervision
: SCC, MCNJ
Validation
: SCC, MCNJ
Writing – original draft
: CAMB, AJBF
Writing – review & editing
: SCC, MCNJ
image/svg+xml
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New species of
Urocleidoides
Neotropical Helminthology (Lima). Vol. 17, N
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2, jul - dic 2023
BIBLIOGRAPHIC REFERENCES
Abdallah, V.D., Azevedo, R.K., & Luque, J.L. (2015).
First record of
Palombitrema triangulum
(Suriano, 1981) Suriano,
1997 (Monogenea: Dactylogyridae) from freshwater fshes in Brazil.
Brazilian Journal of Biology, 75,
229-233.
Acosta, A.A., Mendoza-Palmero, C.A., Silva, R.J., & Scholz, T. (2019). A new genus and four new species of
Dactylogyrids (Monogenea), gill parasites of pimelodid catfshes (Siluriformes: Pimelodidae) in South America
and the reassignment of
Urocleidoides
megorchis
Mizelle et Kritsky, 1969.
Folia Parasitologica, 66
, 4.
Alcântara, N.M., & Tavares-Dias, M. (2015). Structure of the parasites communities in two Erythrinidae fsh from
Amazon River system (Brazil).
Revista Brasileira de Parasitologia Veterinária, 24,
183-190.
Bautista-Hernández, C.E., Pulido-Flores, G., Violante-González, J. & Monks, S. (2019). Helminth parasites of
Xiphophorus birchmanni
(Teleostei: Poeciliidae) from two localities of the Pánuco River drainage, Mexico.
Revista
Mexicana de Biodiversidad, 90
, e901577.
Bautista-Hernández, C.E., Violante-González, J., Monks, S., & Pulido-Flores, G. (2014). Helminth communities of
Xiphophorus malinche
(Pisces: Poeciliidae), endemic freshwater fsh from the Pánuco River, Hidalgo, Mexico.
Revista Mexicana de Biodiversidad, 85,
838-844.
Bush, A.O., Laferty, K.D., Lotz, J.M., & Shostak, A.W. (1997). Parasitology meets ecology on its own terms: Margolis
et al. revisited.
Te Journal of Parasitology, 83
, 575-583.
Corrêa, L.L., Karling, L.C., Takemoto, R.M., Ceccarelli, P.S., & Ueta, M.T. (2013). Hematological parameters of
Hoplias malabaricus
(Characiformes: Erythrinidae) parasitized by Monogenea in lagoons in Pirassununga, Brazil.
Revista Brasileira de Parasitologia Veterinária, 22
, 457-462.
Dias, K.G.A., Vieira, D.H.M.D., Camargo, A.D.A., Silva, R.J., Azevedo, R.K., & Abdallah, V.D. (2017). Diversity
of monogeneans parasites from Characiformes fshes in the Batalha River and Peixe’s River, State of São Paulo,
Brazil.
Neotropical Helminthology, 11
, 317-330.
Evans, B.B., & Lester, R.J. (2001). Parasites of ornamental fsh imported into Australia.
Bulletin-European Association of
Fish Pathologists, 21
, 51-55.
Ferreira, K.D.C., Rodrigues, A.R.O., Cunha, J.M., & Domingues, M.V. (2017). Dactylogyrids (Platyhelminthes,
Monogenoidea) from the gills of
Hoplias malabaricus
(Characiformes: Eryhtrinidae) from coastal rivers of the
Oriental Amazon Basin: species of
Urocleidoides
and
Constrictoanchoratus
n. gen.
Journal of Helminthology, 92
,
353-368.
Freitas, A.J., Bezerra, C.A.M., Meneses, Y.C., Justo, M.C.N., Viana, D.C., & Cohen, S.C. (2021). Tree new species
of
Urocleidoides
(Monogenoidea: Dactylogyridae) parasitizing characiforms (Actinopterygii: Characiformes) in
Tocantins River, states of Tocantins and Maranhão, and new record for
U. triangulus
in Guandu River, state of
Rio de Janeiro, Brazil.
Zoologia, 38
, e65001.
Gasques, L.S., Graça, R.J., Prioli, S.M.A.P., Takemoto, R.M., & Prioli, A.J. (2016). Molecular characterization of
Urocleidoides cuiabai
and
U. malabaricusi
(Monogenea: Dactylogyridae) from the trahira fsh
Hoplias
af.
malabaricus
in the Paraná River, Brazil.
Journal of Helminthology, 90
, 693-697.
Gião, T., Pelegrini, L.S., Azevedo, R.K., & Abdallah, V.D. (2020). Biodiversity of parasites found in the trahira,
Hoplias
malabaricus
(Bloch, 1794), collected in the Batalha River, Tietê-Batalha drainage basin, SP, Brazil.
Anais da
Academia Brasileira de Ciências, 92
, e20180610.
Graça, R.J., Ueda, BH., Oda, F.H., & Takemoto, R.M. (2013). Monogenea (Platyhelminthes) parasites from the gills
of
Hoplias
af.
malabaricus
(Bloch, 1794) (Pisces: Erythrinidae) in the upper Paraná River foodplain, States of
Paraná and Mato Grosso do Sul, Brazil.
Check List, 9
, 1484-1487.
Guidelli, G., Tavechio, W.L.G., Takemoto, R.M., & Pavanelli, G.C. (2006). Fauna parasitária de
Leporinus lacustris
e
Leporinus friderici
(Characiformes, Anostomidae) da planície de inundação do alto rio Paraná, Brasil.
Acta
Scientiarum. Biological Sciences, 28,
281-290.
image/svg+xml
114
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dic 2023
Bezerra
et al.
Guidelli, G., Tavechio, W.L.G., Takemoto, R.M., & Pavanelli, G.C. (2011). Relative condition factor and parasitism
in anostomid fshes from the foodplain of the Upper Paraná River, Brazil.
Veterinary Parasitology, 177
, 145-151.
Humason, G.L. (1979).
Animal tissue techniques.
W.N. Freeman & Company.
Iannacone, J.A., & Luque, J.L. (1993). New records of helminths parasitic on Peruvian Amazonian. fshes (Osteichthyes).
Revista de Biología Tropical, 41
, 303-305.
Jogunoori, W., Kristky, D.C., & Venkatanarasaiah, J. (2004). Neotropical Monogenoidea. 46. Tree new species from
the gills of introduced aquarium fshes in India, the proposal of
Heterotylus
n. g. and
Diaphorocleidus
n. g., and
the reassignment of some previously described species of
Urocleidoides
Mizelle & Price, 1964 (Polyonchoinea:
Dactylogyridae).
Systematic Parasitology, 58
, 115–124.
Kritsky, D.C., & Tatcher, V.E. (1974). Monogenetic trematodes (Monopisthocotylea: Dactylogyridae) from freshwater
fshes of Colombia, South America.
Journal of Helminthology, 48
, 59–66.
Kritsky, D.C., & Tatcher, V.E. (1976). New monogenetic trematodes from freshwater fshes of western Colombia with
the proposal of
Anacanthoroides
gen. n. (Dactylogyridae).
Proceedings of the Helminthological Society of Washington,
43
, 129-134.
Kritsky, D.C., & Tatcher, V.E. (1983). Neotropical Monogenoidea. 4.
Linguadactyloides brinkmanni
gen. et sp. n.
(Dactylogyridae: Linguadactyloidinae subfam. n.) with observations on its pathology in a Brazilian freshwater
fsh,
Colossoma macropomum
(Cuvier).
Proceedings of the Helminthological Society of Washington, 50
, 305-311.
Kritsky, D.C., & Tatcher, V.E. (1983). Neotropical Monogenea. 5. Five new species from the aruana,
Osteoglossum
bicirrosum
Vandelli, a freshwater teleost from Brazil, with the proposal of
Gonocleithrum
n. gen. (Dactylogyridae:
Ancyrocephalinae).
Proceedings of the Biological Society of Washington, 96
, 581–597.
Kritsky, D.C., Tatcher, V.E., & Boeger, W.A. (1986). Neotropical Monogenea. 8. Revision of
Urocleidoides
(Dactylogyridae, Ancyrocephalinae).
Proceedings of the Helminthological Society of Washington, 53
, 1-37.
Kritsky, D.C., Tatcher, V.E., & Boeger, W.A. (1989)
.
Neotropical Monogenea. 15. Dactylogyrids from the gills of
Brazilian Cichlidae with proposal of
Sciadicleithrum
gen. n. (Dactylogyridae).
Proceeding of the Helminthological
Society of Washington, 56
, 128-140.
Kristky, D.C., Mendoza-Franco, E.F., & Scholz, T. (2000). Neotropical Monogenoidea. 36. Dactylogyrids from the
gills of
Rhamdia guatemalensis
(Siluriformes: Pimelodidae) from cenotes of the Yucatan Peninsula, Mexico with
proposal of
Ameloblastella
gen. n. and
Aphanoblastella
gen. n. (Dactylogyridae, Ancyrocephalinae).
Comparative
Parasitology, 67
, 76–84.
Martins, W.M.O., Justo, M.C.N., Cárdenas, M.Q., & Cohen, S.C. (2017a). Metazoan parasite communities of
Leporinus macrocephalus
(Characiformes: Anostomidae) in cultivation systems in the western Amazon, Brazil.
Acta Amazonica, 47
, 301-310.
Martins, W.M.O., Justo, M.C.N., Cárdenas, M.Q., & Cohen, S.C. (2017b). Seasonality of parasitic helminths of
Leporinus macrocephalus
and their parasitism rates in farming systems in the Amazon.
Brazilian Journal of
Veterinary Parasitology, 26
, 419-425.
Mendoza-Franco, E.F., & Reina, R.G. (2008). Five new species of Urocleidoides (Monogenoidea) (Mizelle and Price
1964) Kritsky, Tatcher and Boeger, 1986, parasitizing the gills of panamanian freshwater fshes.
Te Journal of
Parasitology, 94
, 793-802.
Mendoza-Franco, E.F., Aguirre-Macedo, M.L., & Vidal-Martínez, V.M. (2007). New and previously described species
of Dactylogyridae (Monogenoidea) from the gills of Panamanian freshwater fshes (Teleostei).
Te Journal of
Parasitology, 93
, 761-771.
Mendoza-Franco, E.F., Caspeta-Mandujano, J.M., Salgado-Maldonado, G., & Maramoros, W.A. (2015). Two new
species of
Urocleidoides
Mizelle et Price, 1964 (Monogenoidea) from the gill lamellae of profundulids and
poeciliids from Central America and southern Mexico.
Folia Parasitologica, 62
, 059.
image/svg+xml
115
New species of
Urocleidoides
Neotropical Helminthology (Lima). Vol. 17, N
º
2, jul - dic 2023
Mendoza-Franco, E.F., Reina, R.G., & Torchin, M.E. (2009). Dactylogyrids (Monogenoidea) parasitizing the gills of
Astyanax
spp. (Characidae) from Panama and Southeast Mexico, a new species of
Diaphorocleidus
and a proposal
for
Characithecium
n. gen.
Te Journal of Parasitology, 95
, 46-55.
Mendoza-Franco, E.F., Scholz, T., Vivas-Rodríguez, C., & Vargas-Vázquez, J. (1999). Monogeneans of freshwater fshes
from cenotes (sinkholes) of the Yucatan Peninsula, Mexico.
Folia Parasitologica, 46
, 267-273.
Mendoza-Garfas, B., Garcia-Prieto, L., & De León, G.P.P. (2017). Checklist of the Monogenea (Platyhelminthes)
parasitic in Mexican aquatic vertebrates.
Zoosystema, 39
, 501-598.
Mendoza-Palmero, C.A., & Aguilar-Aguilar, R. (2008). Record of
Urocleidoides vaginoclaustrum
Jogunoori, Kritsky and
Venkatanarasaiah, 2004 (Monogenea: Dactylogyridae) from a freshwater fsh in Mexico.
Parasitology Research, 10
,
1235-1236.
Mizelle, J.D., & Price, C.E. (1964). Studies on monogenetic trematodes. XXVII. Dactylogyrid species with the proposal
of
Urocleidoides
gen. n.
Te Journal of Parasitology, 50
, 579-584.
Mizelle, J.D., Kritsky, D.C., & Crane, J.W. (1968).
Studies on monogenetic trematodes. XXXVIII. Ancyrocephalinae
from South America with the proposal of
Jainus
gen. n.
American Midland Naturalist, 80
, 186-198.
Mizelle, J.D., & Kritsky, D.C. 1969. Studies on monogenetic trematodes. XXXIX. Exotic species of Monopithocotylea
with the proposal of
Archidiplectanum
gen. n. and
Longihaptor
gen. n.
American Midland Naturalist, 81
, 370–386.
Molnar, K., Hanek, G. & Fernando, C.H. (1974).
Ancyrocephalids (Monogenea) from freshwater fshes of Trinidad.
Te
Journal of Parasitology, 60
, 914-920.
Moreira, J., Scholz, T., & Luque, J.L. (2015). First data on the parasites of
Hoplias aimara
(Characiformes): description
of two new species of gill monogeneans (Dactylogyridae).
Acta Parasitologica, 60
, 254–260.
Negreiros, L.P., Neves, L.R., & Tavares-Dias, M. (2021). Parasites in
Leporinus macrocephalus
(Anostomidae) of four fsh
farms from the western Amazon (Brazil).
Anais da Academia Brasileira de Ciências, 93
, e20190988.
Oliveira, M.S.B., Santos-Neto, J.F., Tavares-Dias, M., & Domingues, M.V. (2020). New species of
Urocleidoides
(Monogenoidea: Dactylogyridae) from the gills of two species of Anostomidae from the Brazilian Amazon.
Brazilian Journal of Veterinary Parasitology, 29
, e007820.
Oliveira, G.S., Silva, R.J., Vieira, F.E.G., & Acosta, A.A. (2021).
Urocleidoides
spp. (Monogenea: Dactylogyridae) from
the gills of
Parodon nasus
(Characiformes: Parodontidae) from a Brazilian stream with descriptions of two new
species.
Zootaxa, 5081
, pp. 535-550.
Pineda-López, R., Salgado-Maldonado, G., Soto-Galera, E., Hernández-Camacho, N., Orozco-Zamorano, A.,
Contreras-Robledo, S., Cabañas-Carranza, G., & Aguilar-Aguilar, R. (2005). Helminth parasites of viviparous
fshes in Mexico.
In
: Uribe, MC; Grier, HJ (Eds).
Viviparous fshes.
New Life Publications, Florida, pp 437–456.
Price, C.E., & Bussing, W.A. (1968). Monogenean parasites of Costa Rican fshes. II. Proposal of
Palombitrema
heteroancistrium
n. gen., n. sp.
Proceedings of the Helminthological Society of Washington, 35
, 54-57.
Rodríguez-Santiago, A, García-Prieto, L., Mendoza-Garfas, B., González-Solís, D., & Grano-Maldonado, M. (2016).
Parasites of two coexisting invasive sailfn catfshes (Siluriformes: Loricariidae) in a tropical region of Mexico.
Neotropical Ichthyology, 14
, e160021.
Rosim, D.F., Mendoza-Franco, E.F., & Luque, J.L. (2011). New and previously described species of
Urocleidoides
(Monogenoidea: Dactylogyridae) infecting the gills and nasal cavities of
Hoplias malabaricus
(Characiformes:
Erythrinidae) from Brazil.
Te Journal of Parasitology, 97
, 406-417.
Rossin, M.A., & Timi, J.T. (2016). Dactylogyrid monogeneans parasitising
Cyphocharax voga
(Hensel) (Teleostei:
Curimatidae) from the Pampas region, Argentina: new and previously described species.
Systematic Parasitology,
93
, 701-714.
Salgado-Maldonado, G., Novelo-Turcotte, M.T., Caspeta-Mandujano, J.M., Vazquez-Hurtado, G., Quiroz-Martínez,
B., Mercado-Silva, N., & Favila, M. (2016). Host specifcity and the structure of helminth parasite communities
of fshes in a Neotropical River in Mexico.
Parasite, 23
, 1–11.
image/svg+xml
116
Neotropical Helminthology (Lima). Vol. 18, N
º
2, jul - dic 2023
Bezerra
et al.
Salgado-Maldonado, G., Novelo-Turcotte, M.T., Vázquez, G., Caspeta-Mandujano, J.M., Quiróz-Martínez, B., &
Favila, M. (2014). Te communities of helminth parasites of
Heterandria bimaculata
(Teleostei: Poeciliidae) from
the upper Río La Antigua basin, east-central Mexico show a predictable structure.
Parasitology, 141
, 970-980.
Santos-Neto, J.F., & Domingues, M.V. (2023). Integrative taxonomy of
Urocleidoides
spp. (Monogenoidea: Dactylogyridae)
parasites of characiform and gymnotiform fshes from the coastal drainages of the Eastern Amazon, Brazil.
Journal
of Helminthology
, 97, https://doi.org/10.1017/S0022149X2300041X
Souza, A.K.S., Porto, D.B., Silva, E.A., & Malta, J.C.O. (2017). Parasites of
Rhytiodus microleps
Kner, 1859 (Characiformes:
Anostomidae) collected in lakes of the Amazonian food plain.
Neotropical Helminthology, 11
, 37-43.
Suriano, D.M. (1981).
Androspira
gen. nov. (Monogenea Ancyrocephalinae) parasito branquial de
Pseudocurimata
gilberti
(Quoy & Gaimard, 1824) Fernández-Yepes, 1948 (Pisces Tetragonopteridae) de la Laguna de Chascomús,
República Argentina.
Neotropica, 27
, 67–78.
Suriano, D.M. (1997a). Te genus
Urocleidoides
Mizelle and Price, 1964 (Monogenea: Ancyrocephalidae) parasitizing
Characoidei fshes in Argentina.
Physis, 53
, 2-6.
Suriano, D.M. (1997b).
Palombitrema heteroancistrium
Price and Bussing, 1968 (Monogenea: Ancyrocephalidae) from
Astyanax
(
A
.)
fasciatus fasciatus
(Cuvier, 1819) (Pisces: Characidae) in Chascomu’s Lake, Argentina: anatomy and
systematic position.
Physis, 53
, 7-10.
Takemoto, R.M., Pavanelli, G.C., Lizama, M.L.A., Lacerda, A.C.F., Yamada, F.H., Moreira, L.H., & Bellay, S. (2009).
Diversity of parasites of fsh from the Upper Paraná River foodplain, Brazil. Brazilian.
Journal of Biology, 69
,
691-705.
Trujillo-González, A., Becker, J.A., Vaughan, D.B., & Hutson, K.S. (2018). Monogenean parasites infect ornamental
fsh imported to Australia.
Parasitology research, 117
, 995-1011.
Vieira, D.H., Caramello, L.E., Abdallah, V.D., Silva, R.J., & Azevedo, R.K. (2013). Community ecology of metazoan
parasites of the sairú
Cyphocharax nagelii
from the Peixe River.
Revista Brasileira de Parasitologia Veterinária, 22
,
611-615.
Wayne R. (2010).
NIH: imageJ.
https://imagej.nih.gov/ij/download.html
Wendt, E.W., Monteiro, C.M., & Amato, S.B. (2018). Helminth fauna of Megaleporinus obtusidens (Characiformes:
Anostomidae) from Lake Guaíba: analysis of the parasite community.
Parasitology Research, 117
, 2445-2456.
Yamada, F.H., Brandão, H., Yamada, P.O.F., & Silva, R.J. (2015).
Philocorydoras longus
sp. n. (Monogenea, Dactylogyridae)
from the gills of
Hoplosternum littorale
(Siluriformes, Callichthyidae) in Southeastern Brazil and the reassignment
of two species from the genus
Urocleidoides
to
Philocorydoras
.
Helminthologia, 52
, 331- 335.
Zago, A.C., Yamada, F.H., Yamada, P.O.F., Franceschini, L., Bongiovani, M.F., & Silva, R.J. (2020). Seven new species
of
Urocleidoides
(Monogenea: Dactylogyridae) from Brazilian fshes supported by morphological and molecular
data.
Parasitology Research,
119
, 3255-3283.
Received June 6, 2023.
Accepted August 30, 2023.