Update of Dicrocoeliidae (Digenea) parasitizing rodents from the Americas with a description of a new Platynosomoides species from Argentina

Abstract

Digeneans are common parasites of small mammals. Dicrocoeliidae is a family with a cosmopolitan distribution, with 18 genera previously recorded from mammals in the Americas, six of them parasitizing rodents in Argentina. In this study, an updated compilation is provided of Dicrocoeliidae from rodents in the Americas. Also, a new Platynosomoides species is described parasitizing the cricetid rodent Akodon montensis of the Atlantic Forest in Argentina. Digital repositories were used to search for Dicrocoeliidae from rodents in the Americas. Rodents were collected in four localities of the Atlantic Forest, Argentina. Digeneans were removed from the rodent’s bile duct, and conventional studies were used for the morphological description. A total of 15 Dicrocoeliidae species were found parasitizing 18 rodent species from eight countries in the Americas. The new species of Platynosomoides from Akodon montensis differs from the other two species of genus by the size of body, testes, ovary, cecum length and position and length of the vitelline bands. Dicrocoeliidae show growing diversity, and the compilation of species in a rodent host base allows a clearer comparison and identification of new taxa in the future.

Key words
Akodon montensis; Argentina; Cricetidae; Dicroceliidae; Platynosomoides; Sigmodontinae

INTRODUCTION

The family Dicrocoeliidae Looss 1899, has a worldwide distribution, being composed of more than 400 species included in 48 genera, parasitizing the bile ducts and gall bladders of birds and placental mammals and, more rarely, reptiles and marsupials. Their life cycles usually involve snails and arthropods as first and second intermediate hosts, respectively (Yamaguti 1971, Pojmańska 2008). To date, 29 genera within this family were recorded in mammals, 18 of them distributed in the Americas. Among these, 11 genera have been previously registered in rodents, six of them in Argentina (Pojmańska 2008, Fernandes et al. 2015, Panisse et al. 2017, Guerreiro Martins et al. 2019b).

Regarding dicrocoelids, the diagnosis of the genera is based on a combination of morphological characters, such as location of genital pore, testes, vitelline bands, and size of the ventral sucker (Pojmańska 2008). In the last revision of this family, Pojmańska (2008) distinguished four subfamilies based on the relative position of gonads, vitelline bands, and uterus. However, molecular phylogeny does not support this proposal (Tkach et al. 2018, Hildebrand et al. 2019).

Despite several representative taxa of Dicrocoeliidae being included in molecular studies, only three species parasitic of American rodents have sequences available in GenBank (Martínez-Ibeas et al. 2011, Pinto et al. 2018, Hildebrand et al. 2019). Several taxonomic keys have compiled digenean diversity around the world, with few of them mentioning the species (Yamaguti 1971, Gibson et al. 2002, Jones et al. 2005, Bray et al. 2008). The cricetid rodents deserve greater attention as hosts of these parasites, since in recent years there has been a growing diversity of genera and species not yet registered (Panisse et al. 2017, Guerreiro Martins et al. 2019a, b, Preisser & Falcón-Ordaz 2019).

In this study, an updated compilation is provided of Dicrocoeliidae from rodents in the Americas. Also, a new Platynosomoides species is described based on morphological characteristics, parasitizing the cricetid rodent Akodon montensis Thomas 1913 of the Atlantic Forest in Argentina.

The ZooBank Life Science Identifier (LSID) of this publication is: urn:lsid:zoobank.org:pub:058703F3-DDC4-42CF-8648-9EEF8548391F.

MATERIALS AND METHODS

The compilation of species data of Dicrocoeliidae from American rodents was performed using the digital repositories Scielo, Redalyc, Scopus, Dialnet, Pubmed, and Google Academic. Reports were found using the descriptor words: Dicrocoeliidae, Platynosomoides sp., and Rodentia.

A total of 190 Akodon montensis specimens were collected by several collaborators (see Acknowledgments) between 2009 and 2013 in Misiones Province, Argentina: 80 from Campo Anexo M. Belgrano, INTA (26º 02’54.21”S; 53º 46’32.40”W); 82 from Parque Provincial Urugua-í (25º51’25.58”S; 54º09’59.87”W); 4 from Sendero de la Gruta, Parque Provincial Moconá (27°9’23.52”S; 53°54’10.26”W); and 24 from Reserva de Vida Silvestre Urugua-í, Fundación Vida Silvestre (25º58’32.29”S; 54º 07’00.08”W).

The research has been conducted according to Argentine laws. Sample collection was carried out during fieldwork under official permits granted by Ministerio de Ecología, RNR y Turismo, Provincia de Misiones (authorization #23 and #27. Guía Tránsito 000316, 000685 and 000699), in accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. Rodent specimens were collected following the procedures and protocols approved by national laws (Animal Protection National law 14.346 and references in the provincial permits) and Ethics Committee for Research on Laboratory Animals, Farm and Obtained from Nature of National Council of Scientific and Technical Research (CONICET). No endangered species were involved in this study.

Dicrocoelids were removed from the rodent’s bile duct, subsequently fixed in 10% formalin, preserved in 70% ethanol, stained with hydrochloric carmine, dehydrated through an alcohol series, cleared in eugenol, and studied by light microscopy (Leica MZ6® and Olympus BX51®). Drawings were made with the aid of a drawing tube. One specimen was dried using the critical point method, examined using the scanning electron microscope (JEOL/JSMT 6360 LV®). Family and generic identification were made following the keys of Yamaguti (1971) and Bray et al. (2008).

Prevalence (P), mean intensity (MI), and mean abundance (MA) were calculated according to Bush et al. (1997). In the description, measurements of specimens are presented as follows: mean, standard deviation, and range in parentheses. All measurements are given in millimeters (mm) unless otherwise indicated. The scales of figures are given in micrometers (μm).

The nomenclatural acts have been registered in ZooBank, the online registration system for the ICZN. Type specimens were deposited in the helminthological collection of Museo de La Plata (MLP-He), La Plata, Buenos Aires, and hosts in the mammalogy collection of Centro Nacional Patagónico (CNP), Puerto Madryn, Chubut.

RESULTS

An updated compilation of Dicrocoeliidae species parasitizing rodents in the Americas is provided in Table I. A total of 14 species were recorded from 18 host species in eight countries.

Table I
Morphological features and measurements (mm) of Dicrocoeliidae species from rodents in the Americas.

Species	Athesmia heterolecithodes	Caballerolecythus ibunami	Canaania obesa a	Conspicuum minor b	Conspicuum pulchrum	Conspicuum thatcheri	Concinnum peromysci
Author	(Braun 1899) Looss 1899	Lamothe-Argumedo, Falcón-Ordaz, García-Prieto & Fernández-Fernández 2005	Travassos 1944	Mañé-Garzón & Holcman-Spector 1975	(Travassos 1919) Bhalerao 1936	Rivillas, Caro, Carvajal & Vélez 2004	Neidert & Macy 1968
Reference	Martínez & Binda 1992	Lamothe-Argumedo et al. 2005	Maldonado Junior et al. 2010, Guerreiro Martins et al. 2019a	Sutton 1998	Travassos et al. 1969	Rivillas et al. 2004	Neidert & Ralph 1968
Synonymous	Distomum heterolecithodes	-	-	-	Eurytrema pulchrum	-	-
Host species	Myocastor coypus (Myocastoridae)	Liomys irroratus (Heteromyidae)	Akodon azarae, A. cursor, A. montensis, Nectomys squamipes, Oligoryzomys nigripes (Cricetidae)	Scapteromys aquaticus, S. tumidus (Cricetidae)	Oxymycterus quaestor (Cricetidae)	Melanomys caliginosus (Cricetidae)	Peromyscus maniculatus (Cricetidae)
Country	Argentina	Mexico	Argentina, Brazil	Argentina, Uruguay	Brazil	Colombia	United State
Site of infection	Bile duct	Bile duct	Bile ducts and the first part of small intestine	Bile duct	Bile duct	Liver	Pancreatic ducts and a few in the small intestine
Body length	6.95-7.50	6.00-6.90	2.20	0.83-1.62	3.00-3.80	1.12-2.66	2.66-3.19
Body width	1.77-1.96	0.26-0.40	1.30	0.35-0.63	1.50-20	0.49-1.13	0.86-1.10
Oral sucker diameter max	0.32	0.11-0.19	0.28	0.13-0.21	0.43-0.45	0.08-0.36	0.20-0.23
Oral sucker diameter min	0.32	0.10-0.16	0.22	0.13-0.20	0.43-0.45	0.13-0.37	0.19-0.23
Ventral sucker diameter max	0.36	0.10-0.19	0.84	0.24-0.44	0.62-0.70	0.15-0.63	0.23-0.32
Ventral sucker diameter min	0.36	0.09-0.19	0.73	0.23-0.35	0.62-0.70	0.28-0.69	0.23-0.30
Cirrus sac length	-	0.17-0.40	-	0.07-0.17	-	0.17-0.30	0.15-0.24
Cirrus sac width	-	0.04-0.10	-	0.07-0.09	-	0.10	0.06-0.10
Pharynx length	0.12	0.04-0.06	0.17	0.06-0.09	0.17-0.22	0.09-0.37	0.10-0.13
Pharynx width	-	0,04-0,07	-	0.08-0.12	0.17-0.22	0.07-0.38	0.10-0.13
Testes length	AT: 0.64-0.68 PT: 0.72-0.74	AT: 0.28-0.40; PT: 0.31-0.47	0.24-0.28	0.08-0.15	-	LT: 0.07-0.35; RT: 0.05-0.38	-
Testes width	-	AT: 0.16-0.25; PT: 0.18-0.28	0.31-0.33	0.06-0.09	-	LT: 0.06-0.22; RT: 0.05-0.24	-
Ovary length	0.21-0.36	0.21-0.28	0.26	0.06-0.10	-	0.12-0.17	0.11-0.16
Ovary width	-	0.15-0.20	0.33	0.04-0.11	-	0.12-0.17	0.13-0.21
Eggs length	0.031-0.036	0.024-0.030	0.02	0.027-0.034	0.041-0.045	0.030-0.038	0.05-0.06
Eggs width	0.020	0.013-0.017	0.03	0.016-0.020	0.018-0.022	0.013-0.019	0.033-0.039

Species	Dicrocoelium dendriticum	Lyperosomum intermedium	Platynosomum illiciens	Platynosomum minutum	Yungasicola travassosi	Zonorchis komareki	Zonorchis oxymycterae c
Author	(Rudolphi 1819) Looss 1899	Denton & Kinsella 1972	(Braun 1901) Kossak 1910	Kifune & Uyema 1982	Gardner & Pérez-Ponce de Léon 2002	(McIntosh 1939) Travassos 1944	Sutton 1983
Reference	Martino et al. 2012	Denton & Kinsella 1972	Pinto et al. 2016	Kifune & Uyema 1982	Gardner & Pérez-Ponce de Léon 2002	McIntosch 1939	Sutton 1983, Guerreiro Martins et al. 2019a
Synonymous	Distoma dendriticum,	-	Eurytrema fastosum, Platynosomum fastosum, P. concinnum	-	-	Eurytrema komareki	Skrjabinus oxymycterae
Host species	Myocastor coypus (Myocastoridae)	Oryzomys palustris (Cricetidae)	Mus musculus (Muridae)	Proechimys longicaudatus (Echimyidae)	Akodon fumeus (Cricetidae)	Peromyscus gossypinus (Cricetidae)	Akodon azarae; Oxymycterus rufus (Cricetidae)
Country	Argentina	United State	Brazil	Peru	Bolivia	United State	Argentina
Site of infection	Liver	Pancreas	Bile duct	Bile duct, gall bladder	Gall bladder and bile ducts	Liver	Bile duct and small intestine
Body length	5.00-12.00	1.65-4.20	2.23-4.98	1.88-2.74	1.97-3.33	2.82	1.77-3.68
Body width	1.00-2.50	0.33-0.42	0.86-1.72	0.58-0.86	0.71-1.45	0.80	0.66-0.78
Oral sucker diameter max	0.40	0.13-0.15	0.24-0.42	0.23-0.28	0.21-0.34	0.20	0.19-0.29
Oral sucker diameter min	0.30	0.12-0.14	0.24-0.35	0.22-0.26	0.19-0.36	0.20	0.13-0.24
Ventral sucker diameter max	0.45	0.21	0.20-0.43	0.27-0.34	0.19-0.34	0.37	0.49-0.66
Ventral sucker diameter min	0.40	0.16	0.24-0.39	0.27-0.34	0.18-0.34	0.32	0.49-0.61
Cirrus sac length	0.50-0.60	0.11-0.15	0.28-0.48	-	0.10-0.28	-	-
Cirrus sac width	-	0.05-0.65	0.10-0.17	-	0.02-0.07	-	-
Pharynx length	0.13	0.07	0.08-0.15	-	0.09-0.16	0.10	0.12-0.16
Pharynx width	0.12	0.06	0.07-0.14	-	0.07-0.14	0.10	0.13-0.16
Testes length	1.00	0.24	LT: 0.34-0.88; RT: 0.35-0.89	-	LT: 0.11-0.23; RT: 0.09-0.21	0.09-0.20	0.14-0.18
Testes width	0.70	0.11	LT: 0.24-0.58; RT: 0.23-0.54	-	LT: 0.09-0.19; RT: 0.11-0.18	0.09-0.20	0.16-0.19
Ovary length	0.25	0.06-0.14	0.10-0.29	-	0.05-0.13	0.13-0.14	0.11-0.14
Ovary width	0.35	0.07-0.15	0.17-0.39	-	0.62-0.13	0.13-0.14	0.11-0.16
Eggs length	0.038-0.045	0.04-0.05	-	0.03-0.04	0.019-0.031	0.030	0.02
Eggs width	0.022-0.030	0.02-0.027	-	0.02	0.012-0.020	0.023	0.02-0.04

• AT: Anterior testis; PT: Posterior testis; RT: Right testis; LT: left testis. Measurements from ^aMaldonado Junior et al. (2010) in A. montensis and from ^bSutton (1998) in S. aquaticus.
  RT: Right testis; LT: left testis. Measurements from ^c Sutton (1983) in O. rufus.

A total of 47 dicrocoelid specimens were found in the bile duct of 10 Akodon montensis and were identified as a new species of Platynosomoides described below.

Platynosomoides lunaschiae sp. nov. (Table II, Figs. 1-2)

Description (based on 15 complete stained specimens): Plagiorchiida: Dicrocoeliidae. Fusiform body (Fig. 1a), 2.18 ± 0.33 (1.79-2.84) long by 1.16 ± 0.21 (0.92-1.59) wide. Tegument unspined covered by papillae (Figs. 2a-b). Oral sucker rounded, 0.31 ± 0.05 (0.19-0.39) long by 0.29 ± 0.06 (0.21-0.38) wide. Ventral sucker rounded, 0.38 ± 0.06 (0.29-0.48) long by 0.34 ± 0.06 (0.23-0.44) wide. Pharynx, 0.13 ± 0.01 (0.11-0.15) long by 0.12 ± 0.01 (0.9-0.13) wide. Esophagus short. Cecal bifurcation in the forebody, just anterior to the ventral sucker. Long ceca, extending up to three-quarters of the body (Fig. 1a). Rounded testis located immediately posterolateral to the ventral sucker. Right testis 0.16 ± 0.03 (0.07-0.20) long by 0.15 ± 0.03 (0.06-0.18) wide; left testis 0.14 ± 0.03 (0.06-0.18) long by 0.13 ± 0.02 (0.05-0.15) wide (Fig. 1a). Cirrus sac short, located between the ventral sucker and the cecal bifurcation, 0.22 long by 0.1 wide. Genital pore at level of pharynx (Fig. 1b). Ovary rounded, 0.14 ± 0.03 (0.11-0.2) long by 0.12 ± 0.02 (0.09-0.18) wide, located posterior to the right or left testis (Fig. 1c). Uterus intercecal, occupying the entire hindbody (Fig. 1a). Vitelline bands extracecal, extending from the level of the ventral sucker up to 2/3 of the body length, not overlapping the end of the ceca (Fig. 1a). Eggs 32.43 ± 1.69 (29.04-34.98) µm long by 17.62 ± 2.02 (14.51-20.8) µm wide.

Figure 1
Drawing of Platynosomoides lunaschiae sp. nov. a) Complete adult specimen, ventral view. b) Detail of cirrus sac, with internal seminal vesicle (isv) and cirrus (ci). c) Detail of the ovarian complex, showing ovary (ov), oviduct (ovd), seminal receptacle (sr) and ootype (oo).

Figure 2
SEM images of Platynosomoides lunaschiae sp. nov. a), b) Details of tegument papillae, lateral view.

Taxonomic summary

Type host: Akodon montensis Thomas 1913

Symbiotype: with collection number in process, field numbers: CG 159. Other hosts: CNP 3724, 4069, 5191, 5255, 5274

Site of infection: Bile duct

Type locality: Parque Provincial Urugua-í, Misiones province, Argentina (25º51’25.58” S; 54º09’59.87” W)

Other localities: Campo Anexo M. Belgrano, Parque Provincial Moconá and Reserva de Vida Silvestre Urugua-í, Misiones province, Argentina

Specimens deposited: Holotype (No. 7324), Paratype (No. 7709) and a total of three Voucher specimens (Nos. 7573, 7710, 7711) were deposited at MLP-He

Host-parasite data: P=5.26%, IM=4.7 and AM=0.25. The values of P, MI, and MA in the different sampling areas were: Campo Anexo M. Belgrano P=1.2% (1/80), IM=5, and AM-0.1; Parque Provincial Urugua-í P=7.3% (6/82), IM=5.2, and AM=0.4; Sendero La Gruta, Parque Provincial Moconá P=25% (1/4), IM=2, and AM= 0.5; and Reserva de Vida Silvestre Urugua-í P=8.3% (2/24), IM=4.5, and AM=0.4

Etymology: to Dr. Lía I. Lunaschi in recognition of her work in the helminthological collection of Museo de La Plata and valuable contributions to knowledge of the digenean

Recorded in URN as: urn:lsid:zoobank.org:act:E3261D6F-09DC-45E2-B4FD-87253620B7F1

Remarks: Only two nominal species are located in Platynosomoides: P. muris (Shcherbakova 1942) and P. verschureni (Baer 1901) (Pojmańska 2008) (Table II). Platynosomoides lunaschiae sp. nov. is distinguished from these two species by the body length (1.79-2.84 vs. 3.27-3.41; 3-4.5, respectively), length and width of testis (0.06-0.20 x 0.05-0.18 vs. 0.24-0.41 x 0.25-0.36; 0.32 x 0.23, respectively). The ovary in the new species is smaller than in P. muris (0.09-0.18 vs. 0.23-0.24). Also, in the new species the ovary and testis have similar size, whereas in P. muris the testes are larger than the ovary. In addition, P. lunaschiae sp. nov. has ceca and vitelline bands extending to three-quarters of the body, while in P. muris the ceca extend to the end of the body and the vitelline bands reach up to two-thirds of the body, and in P. verschureni the ceca and vitelline bands extend up to the middle of the body.

Table II
Morphological features and measurements (mm) of Platynosomoides species.

Species	Platynosomoides muris	Platynosomoides verschureni	Platynosomoides lunaschiae sp. nov.
Author	(Stcherbakova 1942)	(Baer 1959)	This paper
Species hosts	Apodemus sylvaticus; Leopoldamys siporanus (Muridae)	Crocidura olivieri (Soricidae)	Akodon montensis (Cricetidae)
Country	Armenia; Russia; Malaysia	Democratic Republic of the Congo	Argentina
Continent	Asia	Africa	America
Site of infection	Liver	Bile duct	Bile duct
Body length	3.27-3.41	3.00-4.50	2.18 ± 0.33 (1.79-2.84)
Body width	1.22-1.80	0.71-0.90	1.16 ± 0.21 (0.92-1.59)
Oral sucker diameter max	0.23-0.27	0.25	0.31 ± 0.05 (0.19-0.39)
Oral sucker diameter min	0.22	0.23	0.29 ± 0.06 (0.21-0.38)
Ventral sucker diameter max	0.28	0.39-0.41	0.38 ± 0.06 (0.29-0.48)
Ventral sucker diameter min	0.25	-	0.34 ± 0.06 (0.23-0.44)
Cirrus sac length	0.23-0.28	0.23-0.26	0.22
Cirrus sac width	-	0.06-0.14	0.10
Pharynx length	-	0.14-0.15	0.13 ± 0.01 (0.11-0.15)
Pharynx width	-	0.12-0.14	0.12 ± 0.01 (0.09-0.13)
Right testis length	0.24-0.41	0.32	0.16 ± 0.03 (0.07-0.20)
Left testis length	0.24-0.41	0.32	0.14 ± 0.03 (0.06-0.18)
Right testis width	0.25-0.36	0.23	0.15 ± 0.03 (0.06-0.18)
Left testis width	0.25-0.36	0.23	0.13 ± 0.02 (0.05-0.15)
Ovary length	0.16-0.18	-	0.14 ± 0.03 (0.11-0.20)
Ovary width	0.23-0.24	0.18	0.12 ± 0.02 (0.09-0.18)
Eggs length	0.030-0.035	0.032-0.034	0.032 ± 0.001 (0.029-0.034)
Eggs width	0.018-0.020	0.018-0.021	0.017 ± 0.002 (0.014-0.020)

DISCUSSION

Dicrocoeliidae shows a high morphological diversity with 18 genera parasitizing mammals of the Americas, 11 of them in rodents (McIntosch 1939, Neidert & Ralph 1968, Lamothe-Argumedo et al. 2005, Pojmańska 2008, Fernandes et al. 2015, Panisse et al. 2017). Nine of these genera were registered from the Neotropical region: Athesmia Looss 1899, Caballerolecythus Lamothe-Argumedo, Falcón-Ordaz, García-Prieto & Fernandez-Fernandez 2005, Canaania Travassos 1944, Conspicuum Bhalerao 1936, Dicrocoelium Dujardin 1845, Platynosomoides Yamaguti 1971, Platynosomum Looss 1907, Yungasicola Gardner & Pérez-Ponce de Leon 2002, and Zonorchis Travassos 1944.

Dicrocoelids of American rodents are distributed in five host families: Cricetidae, Echimyidae, Heteromyidae, Muridae, and Myocastoridae, the first being the most frequent (Sutton 1983, Sutton & Damborenea 1996, Navone et al. 2009, Fernandes et al. 2015, Panisse et al. 2017, Guerreiro Martins et al. 2019b). Six dicrocoelid species (Canaania obesa Travassos 1944, Conspicuum minor Mañé-Garzón & Holcman-Spector 1975, Conspicuum pulchrum (Travassos 1919), Platynsomoides sp., Yungasicola travassosi Gardner & Pérez-Ponce de León 2002, Zonorchis oxymycterae Sutton 1983) were recorded parasitizing Akodontini rodents (Cricetidae) (Travassos et al. 1969, Sutton 1983, Sutton 1998, Maldonado Junior et al. 2010 Panisse et al. 2017).

Four dicrocoelid species have been recorded parasitizing the genus Akodon: C. obesa from A. azarae, Akodon cursor (Winge 1887) and A. montensis in Argentina and Brazil; Platynosomoides sp. from A. montensis in Argentina (Maldonado Junior et al. 2010 Panisse et al. 2017, Guerreiro Martins et al. 2019b); Y. travassosi from Akodon fumeus Thomas 1902 in Bolivia (Gardner & Pérez-Ponce de Léon 2002); and Z. oxymycterae from A. azarae in Argentina (Sutton 1983). Although Platynosomoides sp. was mentioned by Panisse et al. (2017) as the first record of this genus in Cricetidae and in America, no description was provided. Notably, the genus Platynosomoides has been reported parasitizing only two families of rodents, Muridae from Asia, and Soricidae from Africa (Stcherbakova 1942, Baer 1959).

The main morphological differences between P. lunaschiae sp. nov. and the other three dicrocoelid species reported from Akodon spp. are the distribution and length of the vitelline bands, and the position of the testes. The new species is distinguished from C. obesa and Z. oxymycterae by the size of the ventral and oral suckers. Platynosomoides lunaschiae sp. nov. is also differentiated from Y. travassosi by cecum length and the size of the uterus. Platynosomoides lunaschiae sp. nov. was found in four geographic localities of the Atlantic Forest in Misiones Province, with low prevalence similar to those recorded for other dicrocoelids in the Akodon species (Navone et al. 2009, Maldonado Junior et al. 2010, Simões et al. 2011).

To date, few molecular studies have been performed on dicrocoelid species parasitizing rodents in the Americas (Table I). The only three species with data available in GenBank are Dicrocoelium dendriticum, Lyperosomum intermedium Denton & Kinsella 1972, and Platynosomum illiciens (Braun 1901) (Martínez-Ibeas et al. 2011, Pinto et al. 2018, Hildebrand et al. 2019). Regarding the new species, despite extracting DNA, no molecular results were obtained, possibly due to inadequate conservation of the specimens. However, the morphological and morphometric comparison of the present specimens and the previously described species support the erection of a new species.

The taxonomy of the Dicrocoeliidae has been controversial, with many species being transferred from one genus to another. For example, Pojmańska (2008) suggested the synonymy of Zonorchis with Skrjabinus. However, considering the position of the reproductive organs and the morphology and size of the ventral sucker, the present study considers both genera as valid, following Sitko (2013) and Hildebrand et al. (2019). In turn, Nguyen & Pham (2004) suggested that Platynosomoides muris should be transferred to the genus Dictyonograptus. This paper does not follow that proposal, since that species presents diagnostic features of Platynosomoides that agree with Pojmańska (2008), such as vitelline bands extending from ventral sucker level to far beyond the ovary. Platynosomoides verschureni was originally described in the genus Platynosomum (Baer 1959), and Yamaguti (1971) later suggested that it should be referred to as Platynosomoides. Pojmańska (2008) agrees with this proposal, including the geographic distribution of the two species within the Platynosomoides genus.

Digenean-host associations occur within a complex system of biotic and abiotic factors. Three types of life cycle have been suggested for the family Dicrocoeliidae (Pojmańska 2008). Ecological aspects of the Platynosomoides species, such as dispersal ability, survival conditions, and adequate hosts, have not yet been studied. However, considering that the host species are terrestrial and omnivorous, feeding mainly on green vegetation, leaves, fruit, seeds, and arthropods (Houemenou et al. 2014, Latinne et al. 2014, Pardiñas et al. 2017, Schlitter et al. 2021), some invertebrates, such as mollusks and arthropods, may act as intermediate hosts of P. lunaschiae sp. nov. as occurs in other dicrocoelid species.

To date, Athesmia heterolecithodes (Braun 1899), Canaania obesa, Conspicuum minor, Dicrocoelium dendriticum (Rudolphi 1819), Platynosomoides lunaschiae sp. nov. and Zonorchis oxymycterae are the only Dicrocoellidae of rodents recorded from Argentina (Martínez & Binda 1992, Sutton 1998, Martino et al. 2012, Panisse et al. 2017, Guerreiro Martins et al. 2019b). The records show a growth in knowledge of the diversity of digeneans from rodents in recent years. This is encouraging, since it may indicate that this increase is related to greater interest of taxonomists in these less-explored groups of helminths. This study provides an updated compilation of dicrocoelid species parasitizing rodents in the Americas with the description of a new species of Platynosomoides from the Atlantic Forest, enlarging the host and geographic distribution for this family of Digenea.

ACKNOWLEDGMENTS

We thank Carlos Galliari, Ulyses Pardiñas, Marcela Lareschi, Juliana Notarnicola, Cecilia Ezquiaga, Juliana Sanchez, Ezequiel Palumbo, Jorge Barneche, Julio Torres for their essential help and cooperation in the field tasks and host collections, mainly to the first four specialists mentioned, who were part of most of the samplings carried out; to Carlos Galliari and Ulyses Pardiñas for the identification of the hosts, to Patricia Sarmiento for the SEM photographs. The work in Misiones province was authorized by Ernesto Kraucsuk and Facundo Tejeda Cajas (Dirección de Biodiversidad) and Mónica Schroder (Dirección Áreas Naturales Protegidas), both from Ministerio de Ecología y Recursos Naturales Renovables de la Provincia de Misiones. We thank Mariano Chudi by kindness and assistance in P.P.Urugua-í at Seccional Uruzú; Luis Marmelicz, Hugo Fassola and Martín Pinazo for their hospitality and support during the field work at the Campo Anexo Manuel Belgrano-INTA Montecarlo; Pablo Herrera, Manuel Jaramillo and Ariel Tombo for allowance to work at Reserva de Vida Silvestre Urugua-í.

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Publication Dates

• Publication in this collection
  21 Nov 2022
• Date of issue
  2022

History

• Received
  23 Oct 2021
• Accepted
  6 Feb 2022