ORIGINAL ARTICLE /ARTÍCULO ORIGINAL

A TAXONOMIC STUDY OF ASPIDOGASTREANS OF THE GENUS LOBATOSTOMA

ECKMANN, 1932 (TREMATODA) DEPOSITED IN THE UNITED STATES NATIONAL

PARASITE COLLECTION (USNPC)

ESTUDIO TAXONÓMICO SOBRE LOS ASPIDOGASTREOS DEL GÉNERO

LOBATOSTOMA ECKMANN, 1932 (TREMATODA) DEPOSITADOS EN LA UNITED

STATES NATIONAL PARASITE COLLECTION (USNPC)

1 2 3

Philippe Vieira Alves , Cláudia Portes Santos & José Luis Luque

1 2 3

Philippe Vieira Alves , Cláudia Portes Santos & José Luis Luque

1Programa de Pós-Graduação em Biologia Animal, Universidade Federal Rural do Rio de Janeiro, BR 465, Km 7,

Seropédica, Rio de Janeiro, 23890-000, Brasil. Laboratório de Avaliação e Promoção da Saúde Ambiental, Instituto Oswaldo

Cruz, Av. Brasil, 4365, Manguinhos, Rio de Janeiro, RJ, 21040-360, Brasil. Departamento de Parasitologia Animal,

Universidade Federal Rural do Rio de Janeiro, CP 74.540, Seropédica, Rio de Janeiro, 23851-970, Brasil. E-mail:

luqueufrrj@gmail.com

Neotropical Helminthology, 2015, 9(1), jan-jun: 29-40.

The helminthological collections are depository of the type/voucher specimens and contribute to the

maintenance of the history of the species. In this study, a reassessment of the taxonomic status of

Lobatostoma (a priori) species is performed based on specimens deposited in the United States

National Parasite Collection (USNPC). Nine slides (six species) of stained specimens of L. albulae

Yamaguti, 1968; L. kemostoma (MacCallum & MacCallum, 1913); L. manteri Rohde, 1973; L.

pacificum Manter, 1940; L. ringens (Linton, 1905); L. veranoi Oliva & Luque, 1989, including the

photomicrographs from the USNPC, were analyzed. The specimens under accession numbers

USNPC 36394.02 (assumed to be L. ringens) and USNPC 083016/B7.30, B7.36 (assumed to be L.

kemostoma), are identified herein as Cotylogaster sp. and Lobatostoma sp., respectively. Further, we

provide taxonomic comments on each taxon studied and outline the need of caution when assessing

the taxonomic identification of deposited material in the helminthological collections.

ABSTRACT

Keywords: Aspidogastrea – Cotylogaster - helminthological collections – Lobatostoma – taxonomy - USNPC.

RESUMEN

Palabras clave: Aspidogastrea - colecciones helmintológicas – Cotylogaster – Lobatostoma – taxonomía - USNPC.

Las colecciones helmintológicas son depositarios de los especímenes tipo/muestras representativas y

contribuyen al mantenimiento de la historia de la especie. En este estudio, se proporciona una

reevaluación de la situación taxonómica de las especies de Lobatostoma (a priori) basado en

especímenes depositados en la United States National Parasite Collection (USNPC). Nueve láminas

(seis especies) con muestras teñidas de L. albulae Yamaguti, 1968; L. kemostoma (MacCallum &

MacCallum, 1913); L. manteri Rohde, 1973; L. pacificum Manter, 1940; L. ringens (Linton, 1905); L.

veranoi Oliva & Luque, 1989, incluyendo las fotos enviadas por USNPC, fueron analizadas. Los

especímenes bajo los números de acceso USNPC 36394.02 (que se supone L. ringens) y USNPC

083016/B730, B7.36 (que se supone L. kemostoma), se identificaron en este estudio como

Cotylogaster sp. y Lobatostoma sp., respectivamente. Además, se proporcionan comentarios

taxonómicos acerca de cada taxón estudiado y se enfatiza la necesidad de evaluar conservadoramente

la identificación taxonómica de material depositado en las colecciones helmintológicas.

ISSN Versión impresa 2218-6425 ISSN Versión Electrónica 1995-1043

INTRODUCTION

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015

Aspidogastrea Faust & Tang, 1936 is a small

group of trematodes parasitizing molluscs as

obligate hosts and vertebrates (fishes and

turtles) as facultative or obligate final hosts

(Rohde, 2002). It represents the most basal

group of flukes (Olson et al., 2003). The

aspidogastreans are characterized by having a

ventral holdfast organ with rows of alveoli or

suckerlets, or just presenting a row of rugae or

suckers (Rohde, 2002).

Lobatostoma Eckmann, 1932 is one of the

most speciose aspidogastreans and their

members are found in molluscs and teleost fish

distributed worldwide (Rohde, 1994). Alves et

al. (2015a) listed nine valid species in the

genus, namely, L. anisotremum Oliva &

Carvajal, 1984; L. hanumanthai Narasimhulu

& Madhavi, 1980; L. jungwirthi Kritscher,

1974; L. kemostoma (MacCallum &

MacCallum, 1913); L. manteri Rohde, 1973;

L. pacificum Manter, 1940; L. platense Mañé-

Garzon & Holcman-Spector, 1976; L. ringens

(Linton, 1905); and L. veranoi Oliva & Luque,

1989. Of them, six have been described from

carangid fish, while the remaining have been

described from fish of the families

Haemulidae, Sciaenidae and Cichlidae (only

freshwater host). All species possesses head

lobes, single testis and the presence of a cirrus-

sac as differential diagnosis of the genus

(Rohde, 2002).

Alves et al. (2015b) redescribed L. kemostoma,

based on the type and newly collected material

from the type host Trachinotus carolinus

(Linnaeus, 1766) (Carangidae) off the

Brazilian coast. They also designated a

lectotype from the syntypes deposited in the

United States National Parasite Collection

(USNPC), Beltsville, Maryland. So far, this

collection has been of assistance for

parasitologists all over the world with loan of

specimens, lots of which serve as source of

information on biodiversity and systematics of

parasites (see Hoberg, 2002). Recently, the

operational responsibility for curation and the

management of specimens deposited in the

USNPC has been transferred to the National

Museum of Natural History (NMNH),

Washington, D.C. (Hoberg & Phillips, 2014).

As a part of an ongoing research project on

Lobatostoma, we had access to specimens

deposited in the USNPC/NMNH. Herein, we

reassess the taxonomic identification of some

species, with comments on each taxon.

The type and voucher specimens of

Lobatostoma examined were lent by the staff

of USNPC. Photomicrographs of holotypes,

kindly sent by Ms. Patricia A. Pilitt (Associate

Curator of USNPC), were also studied. A list of

the material examined is shown in Table 1.

The specimens were studied according to their

original descriptions and the present literature

on aspidogastreans. Photomicrographs were

taken using a CELL D™ software set up in the

Olympus™ BX51 microscope. The names of

fish follow FishBase (Froese & Pauly, 2014).

A total of nine slides containing stained

specimens of Lobatostoma spp. (a priori),

including those photographs sent by the staff of

USNPC, were analyzed. Taxonomic

inconsistencies were observed in the

specimens under accession number USNPC

36394.02 labeled as L. ringens. In fact, the five

specimens on the slide are reassigned to

Cotylogaster Monticelli, 1892. Similarly, the

two slides USNPC 083016/B7.30, B7.36 with

two specimens on each, previously labeled as

MATERIAL AND METHODS

RESULTS

Alves et al.

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015

L. kemostoma are now identified as

Lobatostoma sp. The comments on each taxon

are provided below:

Lobatostoma albulae Yamaguti, 1968 (Fig.

1A)

This species was briefly described based on

two specimens from Albula vulpes (Linnaeus,

1758) (Albuliformes: Albulidae) off the

Pacific Ocean. Several important

morphological features, such as the

arrangement and the total number of alveoli on

the ventral disc were incompletely described.

In addition, the holotype (Fig. 1A) illustrated

in the original description was deformed due

the excessive number of eggs, which made

impossible its specific identification.

Apparently, the second specimen studied by

Yamaguti was not deposited (see Yamaguti,

1968).

Narasimhulu & Madhavi (1980) suggested

that L. albulae is probably junior synonym of

L. ringens, but there is no evidence for this and

Oliva & Luque (1989) considered as valid only

nine species, excluding L. albulae. Despite of

that, new material from the type host is

necessary to reassess the taxonomic status of

this doubtful species. Therefore, L. albulae is

considered to be a species inquirenda.

Lobatostoma from a helminthological collection

Figure 1. Holotypes of Lobatostoma deposited in the USNPC: A) L. albulae from Albula vulpes – ventral view (USNPC

063691.00); B) L. pacificum from Trachinotus paitensis – ventro-lateral view (USNPC 09321.00); C) L. manteri from T. blochii –

ventral view (USNPC 71056.00).

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Alves et al.

Lobatostoma pacificum Manter, 1940 (Fig.

1B)

Lobatostoma pacificum was the first species of

the genus described from the Pacific Ocean

parasitizing Trachinotus paitensis (Cuvier,

1832) (syn. of T. paloma) in the Galapagos

Islands. It is differentiated from the similar L.

kemostoma, by having higher number of

marginal alveoli on the ventral disc (32–34 vs

30), cephalic lobes with different shape and

size and by having a hindbody (from distal

base of the ventral disc to posterior end)

smaller than the ventral disc. L. pacificum is

also differentiated from the other species of the

genus by possessing the hindbody at least one

third of the body length.

The specimen USNPC 09321.00 is registered

in the USNPC as “type”, without any mention

of what kind of type it is, recognized by the

International Commission on Zoological

Nomenclature (ICZN), article 72.1. (ICZN,

1999). Manter deposited all holotypes of the

several described species in the USNPC and

the paratypes in the Allan Hancock Foundation

at The University of Southern California,

consequently the studied specimen is the

holotype (see pag. 329 in Manter, 1940).

Lobatostoma manteri Rohde, 1973 (Fig. 1C)

This species was described from Trachinotus

blochii (Lacepède, 1801) off the Australian

coast (Pacific Ocean part). It differs from the

other eight congeneric species by having

56–62 marginal alveoli on the ventral disc

(Rohde, 1973). Despite of the author also

differentiates the species by the ratio between

the cirrus sac and pharynx, L. platense shows

similarly the cirrus sac twice the size, at least,

of the pharynx (Mañé-Garzon & Holcman-

Spector, 1976).

Among the Lobatostoma species, L. manteri

has been widely studied regarding the biology

of the genus. For instance, studies on life cycle

(Rohde, 1973), morphology (Rohde, 1973),

including ultrastructure (Rohde, 1989; Rohde

& Watson, 1989a; Rohde et al., 1991),

sensorial system (Rohde & Watson, 1989b,

1992), parasite-host system (Rohde &

Sandland, 1973; Rohde, 1981) and

pathogenicity (Rohde, 1975) were performed

on this species.

Lobatostoma ringens (Linton, 1905) (Fig. 2

A–B)

The species was described as Aspidogaster

ringens Linton, 1905 from T. carolinus and

Micropogonias undulatus (Linnaeus, 1766) in

the North Atlantic Ocean; the type host was not

given. Eckmann (1932) erected Lobatostoma

to accommodate L. ringens and L. kemostoma

based on features already mentioned. Since

then, L. ringens has been reported from several

unrelated groups of fishes (nine different

families) across the western Atlantic Ocean,

with the major number of records in the genus

(Hendrix & Overstreet, 1977; Chinchilla &

Mago, 2005). Moreover, there are two records

on molluscs, although its life cycle has not

been completely elucidated as for L. manteri

and L. jungwirthi (Rohde, 1973; Zylber &

Ostrowski de Núñez, 1999).

The identification of the species has been

broadly based on the relative position of testis,

the ratio hindbody/ventral disc and

pharynx/cirrus sac, number of marginal alveoli

and the arrangement of the vitellaria (Rohde,

1973; Mañé-Garzon & Holcman-Spector,

1976; Lunaschi, 1984; Oliva & Carvajal,

1984). However, the intraspecific variation,

the degree of contraction, as well as the

mounting of the material, can alter some of

these features (Oliva & Luque, 1989; Alves et

al., 2015a). Therefore, L. ringens can be

differentiated from its congeners, but three by

having 32–40 marginal alveoli. It differs from

L. pacificum and L. kemostoma by a smaller

hindbody (less than one third of the body vs at

least one third of the body). It is also

differentiated from L. jungwirthi, the only

freshwater species of the genus, due to the

lacking of a hindbody in the last taxon.

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015

The unique specimen which bears the name of

the taxon, as recommended by ICZN, is still

lacking. According to records of USNPC, in

1996, Ms. Meryl A. Ferguson redetermined the

specimens of L. ringens USNPC 035556.02,

035557.02, 035559.02 deposited by G.W.

MacCallum in 1911 and 1912 as “types”,

although she has not published any work to

validate it (P. Pilitt, personal communication).

A redescription of L. ringens, based on

morphological and molecular studies of

specimens collected across the western

Atlantic Ocean, is needed along with a critical

review of the material deposited in the

USNPC.

Gomes & Fábio (1976) redescribed L. ringens

arguing that there were no records of this

species in the South America, but Szidat

(1961) and Suriano (1966) have already

reported it (with taxonomic description) from

Oncopterus darwinii Steindachner, 1874 and

Micropogonias furnieri (Desmarest, 1823),

respectively, in the Argentine waters.

Moreover, they overlooked the number of

median alveoli on the ventral disc, thus

underestimating the total number of them.

Lobatostoma veranoi Oliva & Luque, 1989

(Fig. 3 A–C)

Lobatostoma veranoi was described from

Menticirrhus ophicephalus (Jenyns, 1840) in

the Peruvian coast. It represents the third

species described from a host which does not

belong to the Trachinotus genus. This species

is distinguished from the others but one by

having a higher number of marginal alveoli

(64–66 vs 62 at maximum). Oliva & Luque

(1989) pointed out that L. veranoi differs from

the similar species in the number of marginal

alveoli L. anisotremum (64), by its smaller

cirrus sac than the pharynx, but they did not

Lobatostoma from a helminthological collection

Figure 2. Vouchers and type specimens of Lobatostoma ringens deposited in the USNPC: A) Young adult from Calamus calamus

– ventral view (USNPC 08538.02); B) Adult from Trachinotus carolinus – ventral view (USNPC 035560.00).

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Alves et al.

provide any measurement of the cirrus sac to

corroborate this statement.

In the present study, new measurements were

taken from the paratype under accession

number USNPC 80460.00. Indeed, the cirrus

sac (160µm long) is smaller than the pharynx

(217 µm long), leading us to agree with Oliva

& Luque (1989).

Lobatostoma sp. (Fig. 4 A–B)

Bunkley-Williams et al. (1996) reported L.

kemostoma from T. carolinus off the

Caribbean Sea and also off the Dauphin Island,

northern Gulf of Mexico. However, the

specimens do not have any autapomorphic

character of the referred species as stated by

Alves et al. (2015a). Thus, they were identified

in the present study just as Lobatostoma sp.

since its degree of contraction and preservation

precluded the observation of the main

morphological characters.

Cotylogaster sp. (Fig. 5)

The five specimens on the slide (USNPC

36394.02) were identified as L. ringens by Ms.

M. A. Ferguson, but further analysis on this

material showed that they do not belong to the

Figure 3. Paratype of Lobatostoma veranoi (USNPC 80460.00) deposited in the USNPC: A) Whole-mount – ventral view; B)

Detail of the internal organs, second quarter of the body – ventral view; C) Detail of the internal organs, first quarter of the body –

ventral view. Abbreviations: cirrus sac (cs), intestinal caecum (ic), pharynx (p), seminal vesicle (sv), vitellaria follicular (vf).

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Lobatostoma from a helminthological collection

subfamilyAspidogastrinae. These specimens

are now placed in Cotylaspidinae Chauhan,

1954 because they have three longitudinal

rows of alveoli on the ventral disc as stated by

Rohde (2002). In this subfamily, just

Cotylogaster Monticelli, 1892 is found in

teleost fish; Cotylaspis Leidy, 1857 and

Lissemysia Sinha, 1935 are primarily parasites

of molluscs and turtles (Rohde, 2002),

although L. pandei Rai, 1970 and L. agrawali

Singh and Tewari, 1985 have been described in

teleost fish (Rai, 1970; Singh & Tewari, 1985).

The morphology of the specimens agrees with

Cotylogaster which is characterized by

possessing two testes; the presence of the

cirrus sac in the genus is controversial. Rohde

(2002) pointed out that this feature is present in

the group and Yamaguti (1963) differentiated

Cotylogaster from Cotylogasteroides

Yamaguti, 1963 (synonym of the former), by

the presence or absence of the cirrus sac,

respectively. However, following works on

redescription and description of new species

did not mention a true cirrus sac. Rather, it

corresponds to the prostatic complex

(Fredericksen, 1972; Hendrix & Overstreet,

1977), which is the case of the present forms.

Four species are currently recognized in the

genus, C. basiri Siddiqi and Cable, 1960; C.

dinosoides Hendrix and Overstreet, 1977; C.

michaelis Monticelli, 1892; and C.

occidentalis Nickerson, 1902. Of these, three

have been reported from marine fish, only C.

occidentalis have been found in molluscs and

Figure 4. Lobatostoma sp. deposited in the USNPC: A) Young adult – ventral view (USNPC 083016. B7.36); B) Adult – ventral

view (USNPC 083016.B7.30).

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Alves et al.

in the freshwater fish Aplodinotus grunniens

Rafinesque, 1019 from North America

(Fredericksen, 1972).

The specimens studied herein resemble C.

dinosoides by possessing a simple buccal

funnel with acuminate end without lateral

lobes, but they are similar with C. basiri by the

presence of eyespots in the anterior end; these

features are unique for each taxon. Regardless

of records of C. basiri in T. carolinus, C.

dinosoides was described based on immature

specimens (Hendrix & Overstreet, 1977),

which may explain the absence of eyespots

near to the pharynx. Thus, new sampling effort

focused on aspidogastreans from T. carolinus

and Pogonias cromis (Linnaeus, 1766) (type

host of C. dinosoides) in the North Atlantic are

needed in order to elucidate these taxonomic

divergences.

Figure 5. Cotylogaster sp. (USNPC 36394.02) deposited in the USNPC.

Table 1. Collection data from the United States National Parasite Collection (USNPC), with accession number of the

studied material. Abbreviations: H = holotype, P = paratype, S = syntype, V = voucher.

Species Hosts (Family host) Accession number References

L. ringens (Linton,

1905)

Trachinotus carolinus

(Linnaeus, 1766)

(Carangidae)

035560 (S)

MacCallum &

MacCallum

(1913)

Calamus calamus

(Valenciennes, 1830)

(Sparidae)

08538.02 (V)a Linton (1910)

L. pacificum

Manter, 1940

Trachinotus paitensis

(Cuvier, 1832)

(Carangidae)

09321.00 (H)a Manter (1940)

L. albulae

Yamaguti, 1968

Albula vulpes (Linnaeus,

1758) (Albulidae)

063691.00 (H)a Yamaguti (1968)

L. manteri Rohde,

1973

Trachinotus blochii

(Lacepède, 1801)

(Carangidae)

71056.00 (H)a Rohde (1973)

L. veranoi Oliva &

Luque, 1989

Menticirrhus

ophicephalus (Jenyns,

1840) (Sciaenidae)

80460.00 (P) Oliva & Luque

(1989)

Cotylogaster sp. as

L. ringens

Trachinotus carolinus

(Linnaeus, 1766)

(Carangidae)

36394.02 (V) Dataset of

USNPC.

Lobatostoma sp. as

L. kemostoma Trachinotus carolinus

(Linnaeus, 1766)

(Carangidae)

083016/B7.30, B7.36 (V)

Bunkley-Williams

et al. (1996)

aPhotomicrographs released by Ms Patricia Pillit.

DISCUSSION

The relevance of parasites within studies on

conservation and management of the

biodiversity have been increased since the last

decade, due to the recognition of the essential

role that these organisms play in the

ecosystems (Brooks & Hoberg, 2000; Pérez-

Ponce de León & García-Prieto, 2001; Nichols

& Gómez, 2011; Gómez et al., 2012).

Moreover, Marcogliese (2005) stated that

resource managers interested in environmental

quality should consider the studies on

parasitology along with other disciplines in

ecosystem assessments.

In this context, the helminthological

collections or museums repositories are very

useful to maintain the type and voucher

specimens as an empirical record, which

validates all taxonomic research (Hoberg et al.,

2009). In addition, taxonomic works on

specimen-based data can improve the

knowledge about the global composition,

spatial distribution, ecology, systematics, and

organismal history (Krishtalka & Humphrey,

2000; Hoberg et al., 2009). Despite of its

importance, shortcomings of the data

deposited or gaps in the information can

appear in the museums dataset (Ponder et al.,

2001) as well as presented by the specimens

under accession numbers USNPC 36394.02

and USNPC 083016/B7.30, B7.36.

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Lobatostoma from a helminthological collection

Neotropical Helminthology. Vol. 9, Nº1, jan-jun 2015 Alves et al.

In this work, we added new information on

morphology of some species of Lobatostoma

and one of Cotylogaster deposited in the

USNPC, but further studies using both fresh

and deposited material of the genera are

warranted to better clarify our knowledge on

the group. It is clear that type/voucher

materials are very useful for taxonomic

studies, even though they must be critically

examined since specimens with questionable

identification can be found among the

deposited material.

We thank Patricia Pilitt and Eric Hoberg for the

loan of specimens of Lobatostoma available at

USNPC. This study was supported financially

by Conselho Nacional de Desenvolvimento

Científico e Tecnológico (CNPq),

Coordenação de Aperfeiçoamento de Pessoal

de Ensino Superior (CAPES) and Fundação

Oswaldo Cruz-PROEP.

marine fishes. Journal of Aquatic Animal

Health, vol. 8, pp. 87-92. Triage for the

biosphere: the need and rationale for

taxonomic inventories and phylogenetic

studies of parasites. Comparative

Parasitology, vol. 67, pp. 1-25. Hallazgo

de Lobatostoma ringens (Linton, 1907)

Eck m an n, 1 9 32 ( Tre ma toda :

Aspidogasteridae) en Umbrina coroides

Cuvier, 1830 (Pisces: Sciaenidae) en

Venezuela. Boletín del Instituto de

Oceanografía de la Universidad Oriente,

vol. 44, pp. 105-110.

Über zwei neue

Trematoden der Gattung Aspidogaster.

Zeitschrift für Parasitenkunde, vol. 4,

pp. 395-399. Morphology and

taxonomy of Cotylogaster occidentalis

(Trematoda: Aspidogastridae). The

Journal of Parasitology, vol. 58, pp.

1110-1116. FishBase. World

Wide Web electronic publication,

accessed in April 15, 2014,

<http://www.fishbase.org>

Ocorrência de

Lobatostoma ringens (Linton, 1905) no

Brasil. Atas da Sociedade de Biologia do

Rio de Janeiro, vol. 18, pp. 83-85.

Parasite conservation, conservation

medicine, and ecosystem health. In: AA

Aguirre, RS Ostfeld & P Daszak, (eds.).

New directions in conservation

Medicine: applied cases of ecological

health. New York, Oxford. pp. 67-81.

Marine

Aspidogastrids (Trematoda) from fishes

in the Northern Gulf of Mexico. The

Journal of Parasitology, vol. 63, pp. 810-

817. Foundations for an

Integrative Parasitology: collections,

archives, and biodiversity informatics.

Brooks, RD & Hoberg, EP. 2000.

Chinchilla, OL & Mago, YG. 2005.

Eckmann, F. 1932.

Fredericksen, DW. 1972.

Froese, R & Pauly, D. 2014.

Gomes, DC & Fábio, SP. 1976.

Gómez, A, Nichols, E & Perkins, SL. 2012.

Hendrix, SS & Overstreet, RM. 1977.

Hoberg, EP. 2002.

ACKNOWLEDGEMENTS

Alves, PV, Borges, JN, Santos, CP & Luque,

JL. 2015a.

Alves, PV, Vieira, FM, Santos, CP, Scholz, T &

Luque, JL. 2015b.

Bunkley-Williams, L, Dyer, WG & Williams

Jr, EH. 1996.

A redescription of

Lobatostoma kemostoma (MacCallum

& MacCallum, 1913) (Trematoda:

Aspidogastrea) from the Florida

pompano fish Trachinotus carolinus

(Linnaeus, 1766) off the Brazilian coast.

Journal of Helminthology, vol. 89, pp.

335-344.

A Checklist of the

Aspidogastrea (Platyhelminthes:

Trematoda) of the World. Zootaxa, vol.

3918, pp. 339-396.

Some aspidogastrid and

digenean trematodes of Puerto Rican

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