Introduction
Didelphimorphia (opossums) is the most diverse order of marsupials present in the New World with over 125 extant species (Gardner, Reference Gardner2007; Teta et al., Reference Teta, D'Elía, Flores and de la Sancha2009; Voss and Jansa, Reference Voss and Jansa2009; Gutiérrez et al., Reference Gutiérrez, Jansa and Voss2010; Rossi et al., Reference Rossi, Voss and Lunde2010; Jansa et al., Reference Jansa, Barker and Voss2014; Voss, Reference Voss and Knight2022). This group includes arboreal, terrestrial, semiaquatic and scansorial representatives (Astúa, Reference Astúa2009; Flores, Reference Flores2009; Voss and Jansa, Reference Voss and Jansa2009). Most of them occur in moderate densities in non-disturbed forests throughout the Neotropics (Lima et al., Reference Lima, Stenseth, Yoccoz and Jaksic2001; Gentile et al., Reference Gentile, Finotti, Rademaker and Cerqueira2004; Püttker et al., Reference Püttker, Meyer-Lucht and Sommer2008; Pires et al., Reference Pires, Martins, Silva and Reis2010). Several aspects of their ecology remain unknown, perhaps, because a large number of species is arboreal making their collection infrequent (Fontúrbel and Jiménez, Reference Fontúrbel and Jiménez2009; Caceres et al., Reference Caceres, Nápoli and Hannibal2011; José et al., Reference José, Macedo and Loss2019). The territory of Bolivia sits at the juncture of high-altitude desserts, mountainous, temperate, tropical forest and lowland savannah biomes. This results in a large diversity of mammals that includes 24% of the extant species of opossums (Anderson, Reference Anderson1997; Gutiérrez et al., Reference Gutiérrez, Jansa and Voss2010; Rossi et al., Reference Rossi, Voss and Lunde2010; Voss et al., Reference Voss, Pine and Solari2012). This diversity includes representatives of all 4 subfamilies and major clades in the Didelphidae Gray and species that inhabit humid and dry forests (Voss and Jansa, Reference Voss and Jansa2009; Jansa et al., Reference Jansa, Barker and Voss2014; Voss, Reference Voss and Knight2022).
From 1984 to 2000, the American Museum of Natural History (AMNH, New York City, USA), the Mammal Division of the Museum of Southwestern Biology (MSB:Mamm, University of New Mexico, Albuquerque New Mexico, USA), the Harold W. Manter Laboratory of Parasitology (HWML, University of Nebraska-Lincoln, Lincoln Nebraska, USA), and the Bolivian National Museum of Natural History in La Paz (Colección Nacional de Fauna Sección Mastozoología, CBF, La Paz, Bolivia) mounted joint US National Science Foundation funded collecting expeditions throughout Bolivia to survey and inventory sylvatic mammals and their parasites. A major part of the work on the mammals has been published by Anderson (Reference Anderson1997) and many groups of parasites that were collected from these mammals are still being studied in earnest. From most of the mammals that were collected by these expeditionary research teams in Bolivia, data on habitat, habits and biological associates were also collected and archived in museums. All of the parasites are on deposit in the HWML within the Bolivian Mammal Parasite Collection (BMPC). The BMPC includes all specimens of helminths and parasitic arthropods that were recovered from the more than 16 000 mammals collected and preserved in museums during the course of our work.
Species of helminths that occur in opossums can be grouped in families that include opossum dwelling species, such as Rhopaliidae (Radev et al., Reference Radev, Gardner, Kanev, Jones, Bray and Gibson2005; Haverkost and Gardner, Reference Haverkost and Gardner2008) or in families that include species occurring in distantly related groups of mammals, i.e. Aspidoderidae, Onchocercidae, Viannaidae (Brant and Gardner, Reference Brant and Gardner2000; Jiménez et al., Reference Jiménez, Gardner, Navone and Ortí2012; Scheibel et al., Reference Scheibel, Catzeflis and Jiménez2014). However, the establishment of their specificity or host range is difficult to assess without the existence of a database that relates the distribution of parasite species across several species of mammals. Herein, we present the recorded species of gastrointestinal helminths infecting opossums in Bolivia.
Materials and methods
All mammals were collected using Sherman™ live traps baited with a mixture of oatmeal, vanilla, tuna and sardines, or with snap traps baited with peanut butter. Traps were placed in suitable habitat each evening and checked at first daylight the following morning. Details of each mammal collected were recorded in a field-collection catalog book and in the trap data book, copies of which are maintained in the HWML, the originals are in the Department of Mammalogy, AMNH. Mammal voucher specimens are deposited in the AMNH, MSB:Mamm and CBF.
In the field, each organ of the digestive system was examined separately. Platyhelminths found were placed in distilled water until they relaxed and were killed and fixed in either 70% EtOH or hot or cold 10% formalin. Nematodes were either placed directly in 70% ethanol or killed with glacial acetic acid then transferred to either 70% ethanol or 10% formalin solution. Some samples were preserved in 95% ethanol or in liquid nitrogen and then stored in −85°C freezers in the Manter Laboratory Parasite Genomic Research Facility.
Digenetic trematodes, cestodes and acanthocephalans were stained in Semichon's acetocarmine, dehydrated in a graded series of ethanol, cleared in xylene and mounted in Canada balsam or Damar Gum. Nematodes were cleared in lactophenol and mounted on temporary slides. Vouchers for this study were deposited in the HWML. Specimens used for comparison were borrowed from the HWML and 7 additional institutions including:
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CHIOC: Coleção Helmintológica do Instituto Oswaldo Cruz, Oswaldo Cruz Institute, Rio de Janeiro Brazil.
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CHLP: Collection of Helminths of the Division of Invertebrates of the Museum of Natural History of the National University of La Plata.
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CMNA: Canadian Museum of Nature Parasite Collection, Ottawa, Canada
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CNHE: Colección Nacional de Helmintos of the National Autonomous University of Mexico, Mexico City.
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CHIAUMSM: Colección de Helmintos e Invertebrados Afines, Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima.
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UCDNC: University of California Davis Nematode Collection, University of California, Davis, USA.
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USNPC: United States National Parasite Collection of the Smithsonian Institution. Washington D.C. U.S.A.
The list follows current systems of classification (Radev et al., Reference Radev, Gardner, Kanev, Jones, Bray and Gibson2005; Beveridge et al., Reference Beveridge, Spratt, Durette-Desset and Schmidt-Rhaesa2014; Mariaux et al., Reference Mariaux, Tkach, Vasileva, Waeschenbach, Beveridge, Dimitrova, Haukisalmi, Greiman, Littlewood, Makarikov, Phillips, Razafiarisolo, Widmer, Georgiev, Caira and Jensen2017; Hodda, Reference Hodda2022). The helminthological record for most of the marsupials examined is available at http://opensiuc.lib.siu.edu/zool_data/23/. The relation of voucher specimens, numbers and collections is presented below.
Results
A total of 32 taxa of helminths were recovered from 17 species of marsupials collected from 23 localities. The total includes 3 species of digenetic trematodes, 6 species of tapeworms, 22 species of nematodes, 2 of which remain unidentified and an acanthocephalan. The association of parasites and their didelphiomorph hosts is detailed in Tables 1–3. We present this association using the tribe of the mammals.
Table 1. Helminthological records in Bolivia for species of marsupials included in the tribe Thylamini
Collection number for a representative and prevalence are provided.
Table 2. Helminthological records in Bolivia for species of marsupials included in the tribe Marmosini
Monodelphis kunsi was infection free. Collection number for a representative and prevalence are provided.
Table 3. Helminthological records in Bolivia for species of marsupials included in the tribe Didelphini
Collection number for a representative and prevalence are provided.
Phylum Platyhelminthes Gegenbaur, 1859
Class Trematoda Rudolphi, 1808
Order Diplostomida Olson, Cribb, Tkach, Bray and Littlewood, 2003
Superfamily Echinostomoidea Looss, 1902
Family Rhopaliidae Looss, 1899
Rhopalias Stiles and Hassall, 1898
1. Rhopalias caballeroi Kifune and Uyema, 1982
Site of infection: Small intestine
Type host and locality: Didelphis marsupialis L., Huanuco, Peru
Other reported hosts: Chironectes minimus (Zimmermann), Didelphis sp., Philander opossum (L.), Lutreolina crassicaudata (Desmarest)
Locality records: Argentina: Buenos Aires, Berisso. Colombia: undetermined. Mexico: Veracruz: Los Tuxtlas. Panama: Panama Canal. Peru: Cusco: Pilcopata; San Martín: Bella Vista; Llamas. Venezuela: Aragua (Tantaleán and Chavez, Reference Tantaleán and Chavez2004; Haverkost and Gardner, Reference Haverkost and Gardner2008; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017)
Records in Bolivia: Chironectes minimus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML70021 (274 specimens) from MSB:MAMM:68330. Didelphis marsupialis: Santa Cruz: San Rafael de Amboró, 17°21′S, 63°43′W, 400 m, 24 July 1985, HWML70025 (3 specimens) from MSB:MAMM:55833. Philander opossum: Santa Cruz: San Miguel del Rincón, 17°23′S, 63°32′W, 300 m; 13 August 1984, HWML70018 (3 specimens) from MSB:MAMM:55074; Estancia Cachuela Esperanza, 16°46′59.99″S, 63°13′59.99″W, 300 m, 22 August 1984, HWML70021 (18 specimens) from MSB:MAMM:210569.
Additional specimens examined: HWML70014 (1 specimen) from Lutreolina crassicaudata, Berisso, Buenos Aires, Argentina; CNHE 4081 (1 specimen) from Didelphis sp., Catemaco, Veracruz, Mexico; CNHE965 (1 specimen) from Didelphis marsupialis, Aragua, Venezuela.
2. Rhopalias coronatus (Rudolphi, 1819) Stiles and Hassall, 1898
Synonyms: Rhopalias dobbini Prod'Hon, 1968
Site of infection: Small intestine
Type host and locality: Didelphis marsupialis, Brazil.
Other reported hosts: Didelphis albiventris Lund, Didelphis pernigra (J.A. Allen), Lutreolina crassicaudata, Metachirus myosurus (Temminck) and Philander opossum.
Locality records: Argentina: Buenos Aires: Berisso. Brazil: Bahía: Igrapiúna; Minas Gerais: Belo Horizonte. Costa Rica: Cariai. Mexico: Chiapas: Motozintla; Oaxaca: Cuicatlán; Quintana Roo: La Ceiba; Veracruz: Alvarado and Los Tuxtlas. Panama: Canal Zone. Paraguay: undetermined. Peru: Ancash: Marca; Cajamarca: undetermined; Huánuco: undetermined; Pasco: Villa Rica; San Martin: Llamas. Venezuela: El Tacal (Siebert, Reference Siebert1970; Silva and Costa, Reference Silva and Costa1999; Haverkost and Gardner, Reference Haverkost and Gardner2008; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017; Polo-Gonzales et al., Reference Polo-Gonzales, Sánchez and Pacheco2019; Cirino et al., Reference Cirino, Neto, Maldonado and Gentile2020).
Records in Bolivia: Philander opossum: Santa Cruz: Estancia Cachuela Esperanza, 16°47″, 63°14′, 300 m, 22 August 1984, HWML70000 (108 specimens) from MSB:MAMM:210569; 15 km S of Santa Cruz, 17°53′S, 63°07′W, 2 August 1987, HWML70002 (39 specimens), from AMNH263965; 3 km SE of Montero, 1 km N of Villa Copacabana, 17°23′S, 63°14′W, 250 m, 26 June 1991, HWML70009 (21 specimens), from AMNH263963.
Additional specimens examined: HWML34950 (1 specimen) from Didelphis albiventris, Paraguay. HWML70013 (1 specimen) from Lutreolina crassicaudata, Berisso, Buenos Aires, Argentina.
3. Rhopalias macracanthus Chandler, 1932
Synonyms: Rhopalias louisiana Hearin, 1937
Site of infection: Small intestine
Type host and locality: Didelphis virginiana Kerr, Houston, Texas
Other reported hosts: Didelphis marsupialis.
Locality Records: Costa Rica: Cariai. Mexico: Colima: Comala, La Esperanza. Chiapas: Jaltengo, Motozintla, and Pueblo Nuevo; Oaxaca: Temazcal; Quintana Roo: Rancho La Ceiba; Veracruz: Alvarado, and Los Tuxtlas. United States: Florida: Tallahasee; Illinois: Jackson Co.; Maryland: Beltsville; Texas: Houston (Siebert, Reference Siebert1970; Alden, Reference Alden1995; Haverkost and Gardner, Reference Haverkost and Gardner2008).
Records in Bolivia: Philander opossum: Santa Cruz: Santa Cruz, 16°28′12″S, 63°08′24″W, HWML70001 (1 specimen); 15 km S of Santa Cruz, 17°53′S, 63°07′W, 2 August 1987, HWML70003 (7 specimens), from AMNH263965 and 263966; 3 km SE of Montero, 1 km N of Villa Copacabana, 17°23′S, 63°14′W, 250 m, 26 June 1991, HWML70010, (3 specimens) from AMNH263963; 10 km N of San Ramón, 16°36′S, 62°42′W, 250 m, 7 August 1985, HWML70028 (1 specimen), from host MSB:MAMM:55857.
Additional specimens examined: USNPC8548 (1 specimen) from Didelphis marsupialis, Houston.
Remarks: Rhopalias macracanthus and R. coronatus cause co-infections in the Gray four-eyed opossum, Philander opossum. Haverkost and Gardner (Reference Haverkost and Gardner2008) reviewed species in the family across the continent, making observations and identifying reliable characters based on morphometric analyses.
Class Cestoda Rudolphi, 1808
Order Cyclophyllidea van Beneden in Braun, 1900
Family Anoplocephalidae Blanchard, 1891
Subfamily Linstowiinae Fuhrmann, 1907
Mathevotaenia Akhumyan, 1946
4. Mathevotaenia bivittata (Janicki, 1904) Yamaguti, 1959
Synonyms: Oochoristica bivittata Janicki, 1904; Linstowia (Opossumia) bivittata (Janicki, 1904) Spasskii, 1951; Opossumia bivittata Spasskii, 1981.
Site of infection: Small intestine
Type host and locality: Marmosa sp., Brazil.
Other reported hosts: Caluromys derbianus (Waterhouse), Didelphis albiventris, Didelphis marsupialis, Marmosa paraguayana Tate (as Micoreus cinereus), Marmosa murina (L.), Marmosa demerarae (Thomas), Metachirus nudicaudatus (É. Geoffreoy), Monodelphis domestica (Wagner), Philander opossum, and Thylamys sp.
Locality records: Argentina: Salta: Orán. Brazil: Pará: Belém, Bassuquara and Bacia de Agua Preta; Mato Grosso do Sul: Bodoquena; Espirito Santo: Santa Teresa; Rio de Janeiro: Angra dos Reis. Panama: Canal Zone. Trinidad and Tobago: Rio Claro, Sangre Grande. French Guiana: Cayenne, Nouragues, Saut Pararé and Saül, Pic Matecho (Foster, Reference Foster1939; dos Santos, Reference dos Santos1968; Campbell et al., Reference Campbell, Gardner and Navone2003; Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013).
Records in Bolivia: Thylamys sp.: Tarija: 3 km S of Cuyambuyo, 22°16′S, 64°33′W, 900 m, 3 and 4 August 1991, HWML118719 (207 specimens) from MSB:MAMM:240043.
Additional specimens examined: HWML 17712 from Marmosa cinerea (Temminck), Argentina, Salta, Orán. HWML 49769 from Marmosa murina French Guiana, Cayenne, Montagne du Tigre.
5. Mathevotaenia sanmartini Jiménez, Braun, Campbell and Gardner, Reference Jiménez, Braun, Campbell and Gardner2008
Site of infection: Small intestine
Type host and locality: Thylamys pallidior (Thomas), OMNH 34911, Argentina: Jujuy: Susques, 8.2 km south of Sey (by road), 24°00′48.8″S, 66°30′52.8″W, 4167 ± 10 m (31 March and 1 April 2006).
Locality and host records: No additional records available.
Records in Bolivia: Thylamys pallidior: Cochabamba: Curubamba, 7.5 km southeast of Rodeo (by road), 17°40′31″S, 65°36′04″W, 4000 m, 24 and 26 July 1993, HWML70016–19 (1 and 3 specimens) from MSB:MAMM:87100 and MSB:MAMM:87102.
Additional specimens examined: CHLP5727 (1 specimen) holotype from Thylamys pallidior, Argentina.
Remarks: Several of these specimens were reported in the original description of the species (Jiménez et al., Reference Jiménez, Braun, Campbell and Gardner2008).
6. Mathevotaenia sp.
Site of infection: Small intestine
Type host and locality: Not yet named.
Records in Bolivia: Marmosops bishopi (Pine): La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 27 July 1992, HWML118786 (1 specimen) from MSB:MAMM:235887. Marmosops noctivagus (Tschudi): Cochabamba: 9.5 km by road NE of Tablas Monte, Río Jatún Mayu; 17°2′S, 65°59′W, HWML49845 from MSB:MAMM:70278. Thylamys pusillus (Desmarest): Santa Cruz: 53 km E Boyuibe, 20°27′S, 62°50′W, 600 m, 6 July 1991, HWML 118788 (6 specimens) from MSB:MAMM:87105. Thylamys venustus: Tarija: Tapecua, 21°26′S, 63°55′W, 1500 m, 12 July 1991, HWML 118787 (2 specimens) from AMNH275439.
7. Paralinstowia schmidti (Gardner and Campbell, 1992) Beveridge and Spratt, 2003
Site of infection: Small intestine
Type host and locality: Thylamys elegans venusta (Thomas), Bolivia: Chuquisaca, El Porvenir 20°45′S, 63°13′W, 675 m, 6 July, 1985, symbiotype: AMNH261257.
Other reported hosts: Monodelphis domestica (Wagner)
Locality records: None available.
Records in Bolivia: Chuqisaca: El Porvenir, 20°27′W, 63°07′48″S, 675 m, 15 July 1985, UCDNC2831 (32 specimens) from host MSB:MAMM:211200.
Remarks: Both Monodelphis domestica and Thylamys elegans venusta -junior synonym of Thylamys venustus (Thomas)- were the only marsupials collected in El Porvenir. The species was not found in the other three localities were specimens of Monodelphis domestica were collected.
8. Pritchardia boliviensis Gardner, Jiménez and Campbell, Reference Gardner, Jiménez and Campbell2013
Site of infection: Small intestine
Type host and locality: Marmosops noctivagus: Cochabamba: 9.5 km by road NE of Tablas Monte, Río Jatun Mayu 17°02′29″S, 65°59′05″W, 1500 m, 14 July 1993, symbiotype MSB:MAMM:70278.
Other reported hosts: Marmosa paraguayana, Metachirus nudicaudatus, Gracilinanus sp., Marmosops ocellatus (Tate)
Locality records: Brazil: Paraná: between Corbélia and Cascavel. Paraguay: Alto Paraná: Estación Biológica Limoy (Gardner et al., Reference Gardner, Jiménez and Campbell2013; Benatti et al., Reference Benatti, Moraes, Pacheco, Machado, Oliveira, Perin, Andrietti, Cândido Júnior, Vogliotti, Tebaldi and Hoppe2023).
Records in Bolivia: Marmosa sp.: Santa Cruz: 53 km E of Boyuibe, 20°27′S, 62°50′W, 600 m, 8 July 1991, HWML118801 (139 specimens) from MSB:MAMM:239772. Marmosops noctivagus: Cochabamba: 9.5 km by road NE Tablas Monte, 17°02′S, 65°59″W, 14 and 16 July 1993, HWML118790 and HWML118791 (98 and 65 specimens) from MSB:MAMM:70278 and MSB:MAMM: 30279; La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWML61763 (19 specimens) from host MSB:MAMM:235553. Marmosops ocellatus: Santa Cruz: 3.5 km W, Estación El Pailón, 17°39′S, 62°45′W; 300 m, 21 September 1984, HWML118789 from MSB:MAMM:55070. Metachirus nudicaudatus: La Paz: La Reserva, 15°44′S, 67°31′W; 840 m. 24 July 1992, CNHE6422, CHIOC37318, USNPC103071, from CBF2310. Monodelphis domestica: Santa Cruz: 1 km S and 3 km W of Estancia Isibolos, 19°31′S, 63°36′W, 930 m, 5 July 1991, HWML118800 (52 specimens) from MSB:MAMM:239734. Philander opossum: Santa Cruz: 3 km SE Montero, 1 km N Villa Copacabana, 17°23′S, 63°14′W, 250 m, 26 June 1991, HWML118809 (1 specimen) from MSB:MAMM:239685.
Remarks: The holotype for this species was examined and used as a comparative reference.
9. Atriotaenia sp.
Site of infection: Small intestine
Records in Bolivia: Marmosops noctivagus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 24 July 1992, HWML118724 (4 specimens) from MSB:MAMM:235815. Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118720 (2 specimens) from MSB:MAMM:140296. Thylamys sponsorius (Thomas): Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118760 (1 specimen) from MSB:MAMM:67014, HWML118784 (365 specimens from MSB:MAMM:67015).
Remarks: Most of the specimens were contracted, making it difficult to identify to species level.
Phylum Nematoda Cobb, 1932
Class Chromadoria Pearse, 1936
Order Rhabditida Chitwood, 1933
Superfamily Ancylostomatoidea Looss, 1905
Family Ancylostomatidae Looss, 1905
Subfamily Bunostominae Railliet and Henry, 1909
Monodontus Molin, 1860
10. Monodontus sp.
Site of infection: Small intestine
Records in Bolivia: Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118720 (1 specimen) from MSB:MAMM:140296.
Remarks: This is a single mature female. Species of the genus are known to typically infect rodents.
Superfamily Molineoidea Skrjabin and Shulz, 1937
Family Molineidae Skrjabin and Shulz, 1937
Subfamily Anoplostrongylinae Chandler, 1938
Moennigia Travassos, 1935
11. Moennigia sp.
Site of infection: Small intestine
Records in Bolivia: Monodelphis domestica: Chuquisaca: Río Limón, 19°33′S, 64°08′W, 1300 m, 3 August 1990 HWML118764 (1 specimen) from MSB:MAMM:63278. Monodelphis glirina: Pando: Santa Rosa, 12°07′48″S, 68°14′24″W, 800 m, 1 August 1986, HWML118765 (11 specimens) AMNH M 262399. Marmosops noctivagus: Cochabamba: 9.5 km by road NE Tablas Monte, 17°02′S, 65°59″W, 14 and 15 July 1993, HWML118766 and HWML118767 (1 specimen each) from MSB:MAMM:70278 and MSB:MAMM:238453.
Remarks: These individuals belong to a single species which may be new to science. The senior author is attempting to work in the precise identification and description.
Superfamily Heligmosomoidea Cram, 1927
Family Viannaiidae Neveu-Lemaire, 1944
Subfamily Viannaiinae Neveu-Lemaire, 1944
Travassostrongylus Orloff, 1933
12. Travassostrongylus callis (Travassos, 1914) Orloff, 1933
Synonyms: Trichostrongylus callis Travassos 1914; Ostertagia callis (Travassos, 1914) Travassos 1918
Site of infection: Small intestine
Type host and locality: Didelphis aurita (Wied-Neuwied), Brazil: Rio de Janeiro: Manguinhos CHIOC 724.
Other reported hosts: Didelphis marsupialis, Philander opossum.
Locality records: Brazil: Espirito Santo: Sooretama; Rio de Janeiro: Petrópolis. French Guiana: undetermined. Panama: Panama City (Diaw, Reference Diaw1976a, Reference Diaw1976b; Scheibel et al., Reference Scheibel, Catzeflis and Jiménez2014).
Records in Bolivia: Chironectes minimus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118721 (6 specimens) from MSB:MAMM:68330.
Additional specimens examined: From Didelphis aurita, Brazil: Rio de Janeiro: CHIOC 8426, 8584, 8589, 9608 Manguinhos; CHIOC 9118 Petrópolis; CHIOC 29504, 29505 Espirito Santo: Sooretama.
Viannaia Travassos, 1914
13. Viannaia didelphis (Travassos, 1914) Durette-Desset, 1968
Synonyms: Nematodirus (Mecistocirrus) didelphis Travassos, 1914
Site of infection: Small intestine
Type host and locality: Didelphis aurita, Brazil, Rio de Janeiro, Manguinhos CHIOC 942.
Other reported hosts: Didelphis marsupialis and Didelphis virginiana.
Locality records: Costa Rica: Guanacaste, Colonia Bolaños. Mexico: Colima: La Esperanza, Madrid. Panama: Panama City. United States: Georgia: Enigma, Bulloch Co.; Louisiana: Jeanerette; Illinois: Urbana, Jackson Co.; North Carolina: undetermined; Tennessee: Reelfoot Lake. Trinidad and Tobago: undetermined; Venezuela: Maracaibo (Guerrero, Reference Guerrero1985; Alden, Reference Alden1995; Monet-Mendoza et al., Reference Monet-Mendoza, Osorio-Sarabia and García-Prieto2005; Scheibel et al., Reference Scheibel, Catzeflis and Jiménez2014).
Records in Bolivia: Marmosa sp.: La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWML118722, HWML61763 from host MSB:MAMM:235553.
Remarks: Species in Viannaia have been reported in several species of marsupials across the Americas (Dikmans, Reference Dikmans1931; Cañeda-Guzmán, Reference Cañeda-Guzmán1997; Ellis et al., Reference Ellis, Pung and Richardson1999; Silva and Costa, Reference Silva and Costa1999; Gomes et al., Reference Gomes, Cruz, Vicente and Pinto2003; Antunes, Reference Antunes2005; Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013). A few studies suggest some infections are caused by multiple species (Diaw, Reference Diaw1976a; Guerrero, Reference Guerrero1985; Scheibel et al., Reference Scheibel, Catzeflis and Jiménez2014), thus, individual identification of these nematodes is recommended.
14. Viannaia hamata Travassos, 1914
Site of infection: Small intestine
Type host and locality: Didelphis aurita, Brazil, Rio de Janeiro, Manguinhos CHIOC 942
Other reported hosts: Didelphis albiventris, Didelphis marsupialis, Didelphis virginiana, Philander opossum, Marmosa cinerea, Marmosa murina.
Locality records: Brazil: Minas Geráis, Belo Horizonte; Pará: Belém; Río de Janeiro: Glicêrio, Petrópolis; Paraná: between Corbélia and Cascavel; Río Grande do Sul: Pelotas; Peru: Pasco: Villa Rica; San Martín: Bella Vista, Lamas. Trinidad and Tobago, undetermined; United States: Georgia, Macintosh Co., Bulloch Co.; North Carolina. Venezuela: Miranda, Guatopo (Wolfgang, Reference Wolfgang1951; Guerrero, Reference Guerrero1985; Ellis et al., Reference Ellis, Pung and Richardson1999; Silva and Costa, Reference Silva and Costa1999; Gomes et al., Reference Gomes, Cruz, Vicente and Pinto2003; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017; Polo-Gonzales et al., Reference Polo-Gonzales, Sánchez and Pacheco2019; Benatti et al., Reference Benatti, Moraes, Pacheco, Machado, Oliveira, Perin, Andrietti, Cândido Júnior, Vogliotti, Tebaldi and Hoppe2023).
Records in Bolivia: Didelphis marsupialis: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118723 (2 specimens) from MSB:MAMM:235674.
Additional specimens examined: CHIOC 29289 and 29290 from Didelphis sp. Brazil, Rio de Janeiro, Usina da Tijuca.
15. Viannaia metachirops Durette-Desset, 1974
Site of infection: Small intestine
Type host and locality: Philander opossum, French Guiana
Other reported hosts: None available
Locality records: None available
Records in Bolivia: Marmosops noctivagus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 24 July 1992, HWML118724 (5 specimens) from MSB:MAMM:235815. Marmosa sp., La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWM118725 (3 specimens) from host MSB:MAMM:235553.
Additional specimens examined: None, identification made based on diagnostic traits.
16. Viannaia minispicula Guerrero, Reference Guerrero1985
Site of infection: Small intestine
Type host and locality: Marmosa murina, Venezuela: Amazonas, Caño Yaguá
Other reported hosts: Marmosa demerarae, Philander opossum
Locality records: French Guiana: Guyanne, Cacao.
Records in Bolivia: Marmosops noctivagus: Cochabamba: 9.5 km by road NE Tablas Monte, 17°02′S, 65°59″W, 15 July 1993, HWML118726 (1 specimen) from MSB:MAMM:238453.
Additional specimens examined: None, identification made based on diagnostic traits.
17. Viannaia philanderi (Wolfgang, Reference Wolfgang1951) Durette-Desset, 1968
Site of infection: Small intestine
Type host and locality: Caluromys philander, Trinidad.
Other reported hosts: None available
Locality records: None available
Records in Bolivia: Marmosa sp.: Santa Cruz: Estancia Cachuela Esperanza, 16°46′59.99″S, 63°13′59.99″W, 300 m, 24 August 1984, HWML118727 (3 specimens) from MSB:MAMM:211050. Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118728 (13 specimens) from MSB:MAMM:140297.
Additional specimens examined: None, identification made based on diagnostic traits.
18. Viannaia simplicispicula (Navone, Suriano and Pujol, Reference Navone, Suriano and Pujol1991) Jiménez et al., 2024
Synonyms: Hoineffia simplicispicula Navone, Suriano and Pujol, Reference Navone, Suriano and Pujol1991
Site of infection: Small intestine
Type host and locality: Thylamys venustus cinderellus (Thomas 1902): Argentina: Tucumán: Quebrada Los Sosa, Museo Argentino Bernardino Rivadavia No. 360.
Other reported hosts: Tlacuatzin canescens (J.A. Allen).
Locality records: Argentina: Jujuy: Dr Manuel Belgrano, Las Capillas and El Palmar; Salta: Mosconi. Mexico: Oaxaca: Santa Catarina Juquila (Jiménez et al., Reference Jiménez, Braun, Campbell and Gardner2008; Guzmán-Cornejo et al., Reference Guzmán-Cornejo, Garciá-Prieto, Acosta-Gutiérrez, Falcón-Ordaz and León-Paniagua2012).
Records in Bolivia: Didelphis marsupialis: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118758 (1 specimen) from MSB:MAMM:235674. Thylamys sp.: Tarija: 3 km S of Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118759 (18 specimens) from MSB:MAMM:240043. Thylamys sponsorius: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118760 (1 specimen) from MSB:MAMM:67015. Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118761 (18 specimens) from MSB:MAMM:140296, HWML118762 (10 specimens) from MSB:MAMM:140297; Tapecua, 21°26′S, 63°55′W, 1500 m, 12 July 1991, HWML118763 (4 specimens) from AMNH275439.
Remarks: Guerrero (Reference Guerrero1985) transferred Hoineffia cayennensis Diaw, 1976 to Viannaia. This recommendation was based on the observation that the transversally elongated bursa – diagnostic for Hoineffia Diaw, 1976 – also occurs in other species featuring a gubernaculum such as Viannaia venezuelensis Guerrero, Reference Guerrero1985 and Viannaia barusi Guerrero, Reference Guerrero1985. Furthermore, other species in the genus feature the combination of cordiform bursa and lack of gubernaculum, such as Viannaia viannai. The phenotypic plasticity of the bursa is shown in a subset of species of Viannaia collected across Mexico (Ramírez-Cañas et al., Reference Ramírez-Cañas, López-Caballero and Mata-López2021). Hoinneffia simplicispicula Navone, Suriano and Pujol, Reference Navone, Suriano and Pujol1991 was proposed as the second species in the genus; further, the species was recorded in in Mexico and in Argentina (Jiménez et al., Reference Jiménez, Braun, Campbell and Gardner2008; Guzmán-Cornejo et al., Reference Guzmán-Cornejo, Garciá-Prieto, Acosta-Gutiérrez, Falcón-Ordaz and León-Paniagua2012). Apparently, Navone et al. (Reference Navone, Suriano and Pujol1991) were not familiar with the change proposed by Guerrero (Reference Guerrero1985). We herein consider that the differences in the shape of the caudal bursa, the relative length of the dorsal lobe, dorsal ray and ray 8 are consistent with the intraspecific variability documented by Guerrero (Reference Guerrero1985). Further this variability is observed in specimens from Argentina, Bolivia and French Guiana. Rather than proposing an amended diagnosis, we refer readers to the diagnosis proposed by Dikmans (Reference Dikmans1945), who only missed the presence of three ventral ridges proposed by Durette-Desset (Reference Durette-Desset1971) in his definition of the genus.
Additional specimens examined: HWML63395 from Thylamys venustus, 24.8 km N of Santa Clara (by road), Jujuy, Argentina.
19. Viannaia skrjabini Lent and Freitas, 1937
Site of infection: Small intestine
Type host and locality: Philander opossum, Brazil: Río de Janeiro: Petrópolis. CHIOC 7721
Other reported hosts: Didelphis albiventris, Didelphis marsupialis and Marmosa robinsoni Bangs.
Locality records: Brazil: Pernambuco, Exu. Venezuela: Amazonas, Caño Yaguá; Miranda: Río Negro; Distrito Federal: Naiguatá (Guerrero, Reference Guerrero1985).
Records in Bolivia: Didelphis marsupialis: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118729 (from HWML61838) (3 specimens) from MSB:MAMM:235674.
Additional specimens examined: Holotype CHIOC7721, from Philander opossum, Brazil: Río de Janeiro, Petrópolis
20. Viannaia viannai Travassos, 1914
Site of infection: Small intestine
Type host and locality: Didelphis aurita, Brazil, Rio de Janeiro, Manguinhos CHIOC 922.
Other reported hosts: Didelphis marsupialis, Didelphis virginiana, Philander opossum.
Locality records: Brazil: Pernambuco: Exu; Rio de Janeiro: Morro São João, Casimiro de Abreu. Costa Rica: Guanacaste, Colonia Baños. French Guiana: Camp du Tigre. Mexico: Guerrero: Taxco El Viejo. Panama: Panama City. Peru: San Martín: Bella Vista. United States: Illinois, Carbondale; Maryland, Beltsville. Venezuela: Miranda: Caño Yagua, Río Negro and San Antonio (Guerrero, Reference Guerrero1985; Monet-Mendoza et al., Reference Monet-Mendoza, Osorio-Sarabia and García-Prieto2005; Scheibel et al., Reference Scheibel, Catzeflis and Jiménez2014; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017).
Records in Bolivia: Didelphis marsupialis: La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 6 July 1992, HWML118730 (1 specimen) from MSB:MAMM:235570; La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118731 (1 specimen) from MSB:MAMM:235674. Marmosa sp.: La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWML118732 (3 specimens) from host MSB:MAMM:235553; Santa Cruz: Estancia Cachuela Esperanza, 16°46′59.99″S, 63°13′59.99″W, 300 m, 24 August 1984, HWML118733 (7 specimens) from MSB:MAMM:211050. Marmosops noctivagus: Cochabamba: 9.5 km by road NE Tablas Monte, 17°02′S, 65°59″W, 14, 15 and 16 July 1993, HWML62620, HWML118734–36 (11, 13 and 10 specimens) from MSB:MAMM:70278, MSB:MAMM:238453 and MSB:MAMM:30279; La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 24 July 1992, HWML61852 (10 specimens) from MSB:MAMM:235815. Monodelphis peruviana: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 25 July 1992, HWML118737 (3 specimens) from MSB:MAMM:68336. Thylamys sp.: Tarija: Tapecua, 21°26′S, 63°55′W, 1500 m, 1 June 1991, HWML118794 (5 specimens) from MSB:MAMM:238757.
Additional specimens examined: From Didelphis marsupialis, HWML67179–81, Panama City, Panama and Colonia Baños, Costa Rica. From Didelphis virginiana HWML61798 from Carbondale Illinois, U.S.A.
Order Spirurida Railliet, 1915
Suborder Ascaridina Inglis, 1983
Superfamily Heterakoidea Railliet and Henry, 1912
Family Aspidoderidae Skrjabin and Shikhobalova, 1947
Aspidodera Railliet and Henry, 1912
21. Aspidodera raillieti Travassos, 1913
Synonyms: Aspidodera harwoodi Chandler, 1932, Aspidodera vicentei Pinto, Kohn, Fernandes and Mello, 1981, Aspidodera diaz-ungriai Masí-Pallarés and Benítez-Uscher, 1971
Site of infection: Caecum and large intestine
Type host and locality: Didelphis aurita, Manguinhos, Brazil
Other reported hosts: Didelphis marsupialis, Didelphis virginiana, Didelphis pernigra, Gracilinanus agilis (Burmeister), Marmosa demerarae, Marmosa murina, Marmosops ocellatus, Metachirus nudicaudatus, Metachirus myosurus, Philander opossum, Sigmodontinae: Nectomys squamipes (Brants), Euoryzomys nitidus (Thomas).
Locality records: Brazil: Bahía: Igrapiúna; São Paulo, Piauí, Formosa. French Guiana: Montagne du Tigre, Nouragues, Saül, Petit Saut, Route de Kaw. Guatemala: Santa Rosa. Mexico: Motozintla; Panama: Panama Canal. Paraguay: Puerto Ibapobó. Suriname. Peru: La Libertad, Bosque del Cachil; San Martín: Bella Vista; Llamas. United States: Texas, Houston; Illinois, Jackson Co., Union Co., (Santos et al., Reference Santos, Lent and Gomes1990; Alden, Reference Alden1995; Jiménez-Ruiz et al., Reference Jiménez-Ruiz, Gardner, Noronha and Pinto2008; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017; Polo-Gonzales et al., Reference Polo-Gonzales, Sánchez and Pacheco2019; Varella et al., Reference Varella, Vilela, Gentile, Cardoso, da Costa-Neto and Maldonado Júnior2022)
Records in Bolivia: Didelphis albiventris: Tarija: Tapecua, 21°26′S, 63°55′W, 1500 m, 14 July 1991, 1500 m, HWML118738 (36 specimens) from CBF2379. Didelphis marsupialis: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 and 25 July 1992, HWML118810 (7 specimens) from MSB:MAMM:235674, HWML61882 (2 specimens) from MSB:MAMM:235838. Marmosops ocellatus: Santa Cruz: 15 km S of Santa Cruz, 17°53′S, 63°07′W, 2 August 1984, HWML118739 (2 specimens) from MSB:MAMM:58514. Monodelphis domestica: Chuquisaca: El Porvenir, 20°45′S, 63°13′W, 675 m, 7 July 1985, HWML60236 (1 specimen) from MSB:MAMM:55847. Monodelphis sanctarosae: Santa Cruz: Santa Rosa de la Roca, 15°30′00″S, 61°16′12″W, 250 m, 6 June 1990, HWML118802 (2 specimens) from MSB:MAMM:237023. Philander opossum: Santa Cruz: San Miguel Rincón, 17°22′59″S, 63°31′59″W, 300 m, 14 August 1984, HWML118740 (1 specimen) from MSB:MAMM:210528; 6 km by road W Ascención, 15°25′47″S, 63°53′59″W, 240 m, 13 August 1985, HWML118741 (6 specimens) from MSB:MAMM:211436.
Additional specimens examined: CHIOC12 (holotype) from Didelphis aurita, Rio de Janeiro Brazil.
CHIOC18356, CHIOC19115, from Didelphis azarae, Puerto Ibapobó, Paraguay. CHIOC4446 from Tolypeutes tricninctus (L.) Tanque, Brazil. CHIOC31879 from Nectomys squamipes Formosa, Goiás, Brazil. USNPC8550 from Didelphis virginiana, Houston, Texas, U.S. A.CMNA408 from Didelphis marsupialis, Saint Vincent, Trinidad, Trinidad and Tobago. CNHE2110 from Didelphis marsupialis, Motozintla, Mexico.
Superfamily Cosmocercoidea Railliet, 1916
Family Kathlaniidae Lane, 1914
Cruzia Travassos, 1917
22. Cruzia tentaculata (Rudolphi, 1819) Travassos, 1917
Synonyms: Ascaris tentaculata Rudolphi, 1819; Oxysoma tentaculata Schneider, 1866
Site of infection: Large intestine and caecum
Type host and locality: Didelphis marsupialis, Brazil
Other reported hosts: Didelphis albiventris, Didelphis aurita, Didelphis pernigra, Didelphis virginiana, Metachirus nudicaudatus, Metachirus myosurus, Philander opossum, Philander quica (Temminck).
Locality Records: Brazil: Bahía: Igrapiúna; Minas Gerais: Belo Horizonte, Conceição dos Ouros; Paraibá: Santa Rita; Paraná: Curitiba, Ponta Grossa; São Paulo: São Paulo; Rio Grande do Sul: Porto Alegre; Rio de Janeiro: Glicério, Barra de Marica, Casimiro de Abreu, Serra dos Orgãos, Sumidouro, Petrópolis; Santa Catarina: Santa Catarina Island; Sergipe: Capela, São Cristovão. Colombia: Valle del Cauca: Meléndez. Mexico: Chiapas; Colima; Distrito Federal; Estado de México; Hidalgo: Tasquillo; Guerrero; Jalisco; Morelos; Oaxaca; Veracruz; Yucatán. Peru: Ancash: Marca, Huanchoc; Loreto: Iquitos; Piura: valle del Huancabamba; San Martín: Bella Vista; Cajamarca: Cajamarca. United States: Louisiana, North Carolina, Pennsylvania, Tennessee, Texas, Wisconsin (Alden, Reference Alden1995; Silva and Costa, Reference Silva and Costa1999; Monet-Mendoza et al., Reference Monet-Mendoza, Osorio-Sarabia and García-Prieto2005; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017; Polo-Gonzales et al., Reference Polo-Gonzales, Sánchez and Pacheco2019; Cirino et al., Reference Cirino, Neto, Maldonado and Gentile2020).
Records in Bolivia: Didelphis albiventris: Tarija: Tapecua, 21°06′S, 63°55′W, 1500 m, 14 July 1991, HWML 118741 (39 specimens) from MSB:MAMM:239823; La Paz: Saynami Rio Zongo, 16°07′39″S, 68°05′59″W, 4 June 1993, HWML118742 (153 specimens) from MSB:MAMM:236299. Didelphis pernigra: La Paz: Yanacachi, Valle Aceromarka 16°19′35″S, 67°53′21″W, 3085 (Mollericona and Nallar, Reference Mollericona and Nallar2014). Philander opossum: Santa Cruz: 6 km by road W Ascención, 15°25′47″S, 63°53′59″W, 240 m, 13 August 1985, HWML118743 (99 specimens) from MSB:MAMM:211436.
Remarks: The species has an almost continental distribution and it is known to occur in armadillos and opossums (Ruiz, Reference Ruiz1947; Fujita et al., Reference Fujita, Abe, Oku, Sanabria, Inchaustti and Kamiya1995; Adnet et al., Reference Adnet, Anjos, Menezes-Oliveira and Lanfredi2009; Souza et al., Reference Souza, Vilela, Gentile, Lopes-Torres, Cordeiro-Estrela, Moratelli, da Costa-Neto, Cardoso, Varella and Maldonado Júnior2022). The material of this species across its putative range needs to be reviewed.
Suborder Spirurina Railliet and Henry, 1915
Superfamily Rictularioidea Hall, 1913
Family Rictulariidae Hall, 1913
Pterygodermatites Wedl, 1861
23. Pterygodermatites (Paucipectines) elegans (Travassos, 1928) Quentin, 1969
Synonyms: Rictularia elegans Travassos, 1928
Site of infection: Small intestine
Type host and locality: Eumops perotis (Schinz): Engenheiro Gomide, São Paulo, Brazil.
Other reported hosts: Marmosa cinerea, Marmosa demerarae.
Locality Records: Brazil: Cafezal, Belém. French Guiana: Macouria, Montagne du Tigre, Pic Matecho, Saül (Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013).
Records in Bolivia: Marmosa sp.: Santa Cruz: Estancia Cachuela Esperanza, 16°46′59.99″S, 63°13′59.99″W, 300 m, 24 August 1984, HWML60078 (15 specimens) from MSB:MAMM:211050; La Paz: Chijchijpa: 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWML118744 (1 specimen) from host MSB:MAMM:235553. Marmosops bishopi: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 27 July 1992, HWML118745 (1 specimens) from MSB:MAMM:235887.
Additional specimens examined: HWML67202 from Marmosa demerarae, Montagne du Tigre, Cayenne, French Guiana.
24. Pterygodermatites (Paucipectines) jaegerskioldi (Lent and Freitas, Reference Lent and Freitas1935) Quentin, 1969
Site of infection: Small intestine
Type host and locality: Caluromys philander (L.), Rio de Janeiro, Tijuca, Brazil.
Other reported hosts: Gracilinanus agilis, Gracilinanus microtarsus (Wagner).
Locality records: Brazil: Mato Grosso do Sul, Nhecolândia; Rio de Janeiro: Parque Nacional da Serra dos Orgãos (Lent and Freitas, Reference Lent and Freitas1935; Torres et al., Reference Torres, Maldonado and Lanfredi2007, Reference Torres, Maldonado and Lanfredi2009).
Records in Bolivia: Monodelphis domestica: Santa Cruz: 27 km S of Santa Cruz, 3 km E and 1 km S Brecha Tres, 18°01′59″S, 63°10′01″W, 20 June 1992, HWML118746 (1 specimen) from MSB:MAMM:67022; 1 km S and 3 km W of Estancia Isibolos, 19°31′S, 63°36′, 930 m, 5 July 1991, HWML118747 (5 specimens) from MSB:MAMM:239734.
Superfamily Spiruroidea Oerley, 1885
Family Spiruridae Oerley, 1885
Spirura Blanchard, 1849
25. Spirura guianensis (Ortlepp, 1924) Chitwood, 1938
Site of infection: Stomach
Type host and locality: Monki monki (Scientific name not disclosed), Suriname.
Other reported hosts: Didelphis marsupialis, Gracilinanus agilis, Marmosa cinerea, Marmosa demerarae, Marmosa murina, Metachirops opossum, Philander opossum, Saguinus geoffroyi (Pucheran), Saguinus nigricollis (Spix), and Tamarinus nigricollis (Spix)
Locality Records: French Guiana: Montagne du Tigre. Brazil: Rio de Janeiro, Itaguaí; Mato Grosso do Sul, Nhecolândia. Panama: Panama Canal (Torres et al., Reference Torres, Maldonado and Lanfredi2009; Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013).
Records in Bolivia: Chironectes minimus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 22 July 1992, HWML118748 (34 specimens) from MSB:MAMM:68330. Monodelphis domestica: Chuqisaca: El Porvenir, 20°27′W, 63°07′48″S, 675 m, 15 July 1985, HWML 118756 (1 specimen) from host MSB:MAMM:211199
Family Gongylonematidae Hall, 1916
Gongylonemoides Lent and Freitas, 1937
26. Gongylonemoides marsupialis (Vaz and Pereira, 1934) Freitas and Lent, 1937
Synonym: Gongylonema marsupialis Vaz and Pereira, 1934
Site of infection: Esophagus
Type host and locality: Didelphis aurita, São Paulo, Brazil
Other reported hosts: Didelphis aurita, Metachirops opossum.
Locality Records: Brazil: Rio de Janeiro; São Paulo: undetermined. Peru: San Martín: Llamas (Gomes et al., Reference Gomes, Cruz, Vicente and Pinto2003; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017).
Records in Bolivia: Marmosa sp.: La Paz: Chijchijpa, 16°09′S, 67°45′W, 1114 m, 8 July 1992, HWML118749 (55 specimens) from host MSB:MAMM:235553; Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML118750 (3 specimens) from MSB:MAMM:140296.
Superfamily Physalopteroidea Railliet, 1893
Family Physalopteridae Railliet, 1893
Turgida Travassos, 1920
27. Turgida turgida (Rudolphi, 1819) Travassos, 1919
Synonyms: Physaloptera turgida Rudolphi, 1819; Spiroptera turgida Dujardin, 1845; Physaloptera didelphidis Leidy, 1851.
Site of infection: Stomach
Type host and locality: Brazil
Other reported hosts: Caluromys derbianus, Didelphis aurita, Didelphis albiventris, Didelphis marsupialis and Didelphis virginiana, Metachirus nudicaudatus, and Philander opossum.
Locality Records: Argentina: Santiago del Estero. Brazil: Goías: Nerópolis; Río de Janeiro: Casimiro de Abreu, Angra dos Reis, Sumidouro; Santa Catarina: Santa Catarina Island. Mexico: Chiapas: Motozintla, Tonalá; Colima: Colima, Comala, Dos Amates, La Esperanza, Madrid; Distrito Federal; Estado de México: Tequesquinahuac; Guerrero: Coyuquilla, Taxco El Viejo; Hidalgo: Tasquillo; Jalisco: Chamela; Michoacán, El Hortigal; Morelos; Oaxaca: Temazcal; Veracruz, Los Tuxtlas. Panama: Panama Canal. Peru: Loreto: Iquitos; Piura: San Felipe de Vichayal; San Martín: Bella Vista. United States: California, Connecticut, Colorado, Florida, Georgia, Illinois, Kansas, Louisiana, Oklahoma, New York, North Carolina, Pennsylvania, Tennessee, Texas, Virginia, Wisconsin. Trinidad and Tobago. Venezuela: Maracaibo (Alden, Reference Alden1995; Monet-Mendoza et al., Reference Monet-Mendoza, Osorio-Sarabia and García-Prieto2005; Chero et al., Reference Chero, Sáez, Mendoza-Vidaurre, Iannacone and Cruces2017; Polo-Gonzales et al., Reference Polo-Gonzales, Sánchez and Pacheco2019).
Records in Bolivia: Didelphis albiventris: Tarija: Tapecua, 21°06′S, 63°55′W, 1500 m, 14 July 1991, HWML118751 (69 specimens) from MSB:MAMM:239823; Philander opossum: Pando: Bella Vista, 11°13′48″W, 67°07′12″W, 170 m, 26 July 1986, HWML118752 (2 specimens) from MSB:MAMM:211891.
Suborder Oxyurinae Railliet, 1895
Superfamily Oxyuroidea Cobbold, 1864
Family Oxyuridae Cobbold, 1864
Didelphoxyuris Gardner and Hugot, 1995
28. Didelphoxyuris thylamisis Gardner and Hugot, 1995
Site of infection: Large intestine and caecum
Type host and locality: Thylamys venustus: Santa Cruz, 5 km NE Quiñe, 18°03′S, 64°19′W, 1900 m, 27 May 1991.
Other reported hosts: Other than symbiotype, none available
Locality records: Other than type locality, none available
Records in Bolivia: Marmosa sp.: Santa Cruz: 53 km E Boyuibe, 20°27′S, 62°50′W, 600 m, 6 July 1991, HWML118755 (12 specimens) from MSB:MAMM:239772. Thylamys venustus: Tarija: 3 km SE Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 August 1991, HWML117853 from MSB:MAMM:140296, HWML117854 (256 specimens) from MSB:MAMM:140297; Tarija: Tapecua, 21°26′S, 63°55′W, 1500 m, 12 July 1991, HWML61315 (17 specimens) from AMNH275439; Santa Cruz: 5 km NE Quiñe, 18°03′S, 64°19′W, 1900 m, 27 May 1991, HWML61086 NK22813 MSB:MAMM:87107 (360 specimens). Thylamys pusillus: Santa Cruz: 53 km E Boyuibe, 20°27′S, 62°50′W, 600 m, 6 July 1991, HWML61267 (28 specimens) from MSB:MAMM:87105
Additional specimens examined: HWML39072 holotype
Remarks: The symbiotype was originally identified as Thylamys elegans Waterhouse. However, a systematic review of the genus revealed that this species is restricted to the western slope of the Andean Cordillera; furthermore, fat-tailed opossusms infected with pinworms used in the species description belong to Thylamys venustus (Giarla et al., Reference Giarla, Voss and Jansa2010).
Monodelphoxyuris Guerrero and Hugot, 2003
29. Monodelphoxyuris dollmeiri Guerrero and Hugot, 2003
Site of infection: Large intestine and caecum
Type host and locality: Monodelphis emiliae (Thomas): San Martín, Rio Camisea, Cusco, Peru, 11°47′10″S, 72°42′5″W, 474 m; May 08, 1997. Accession number CHIAUMSM1175. Symbiotype 14149 Mammal Collection of the Museo de Historia Natural, Universidad Nacional Mayor de San Marcos, Lima.
Other reported hosts: None available
Locality records: Other than type locality, none available
Records in Bolivia: Monodelphis domestica: Chuqisaca: El Porvenir, 20°27′W, 63°07′48″S, 675 m, 15 July 1985, HWML 118756 (158 specimens) from host MSB:MAMM:211199; HWML 60229 (88 specimens) from host AMNH M 261233. Thylamys venustus: Chuqisaca: El Porvenir, 20°27′W, 63°07′48″S, 675 m, 13 July 1985, HWML 60130 (2 specimens) from host MSB:MAMM:211181
Neohilgertia Navone, Suriano and Pujol, 1990
30. Neohilgertia venusti Navone, Suriano and Pujol, 1990
Site of infection: Large intestine and caecum
Type host and locality: Thylamys venustus, Tucuman, Burruyacu. Bernardino Rivadavia Helminthological Collection 362.
Other reported hosts: None available
Locality records: Other than type locality, none available
Records in Bolivia: Thylamys sp.: Tarija: 3 km S of Cuyambuyo, 22°16′S, 64°33′W, 900 m, 4 and 5 August 1991, HWML61553 (36 specimens) from MSB:MAMM:240043; HWML118792 (42 specimens) from MSB:MAMM:240056
Class Dorylaimea Hodda, 2007
Order Trichocephalida Spasski, 1954
Family Trichuridae Ransom, 1911
Trichuris Roederer, 1761
31. Trichuris reesali Wolfgang, Reference Wolfgang1951
Site of infection: Large intestine and caecum
Type host and locality: Didelphis marsupialis, Trinidad
Other reported hosts: Didelphis marsupialis, Marmosa demerarae, Marmosa murina, Philander opossum (Wolfgang, Reference Wolfgang1951; Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013).
Locality Records: French Guiana: Camp du Tigre, Saül, Macouria.
Records in Bolivia: Marmosa sp.: Santa Cruz: Estancia Cachuela Esperanza, 16°46′59.99″S, 63°13′59.99″W, 300 m, 24 August 1984, HWML118807 (2 specimens) from MSB:MAMM:211050; Marmosops noctivagus: La Paz: La Reserva, 15°44′S, 67°31′W, 850 m, 24 July 1992, HWML118757 (7 specimens) from MSB:MAMM:235815.
Phylum Acanthocephala Rudolphi, 1808
Class Archiacanthocephala Meyer, 1931
Order Moniliformida Schmidt, 1972
Family Oligoacanthorhynchidae Southwell and McPhie, 1925
Oligacanthorhynchus Travassos, 1915
32. Oligacanthorhynchus microcephalus (Rudolphi, 1819) Schmidt, 1972
Synonyms: Echinorhynchus microcephalus Rudolphi, 1819; Echinorhynchus tortuosa Leidy, 1850; Hamanniella microcephalus (Rudolphi, 1819) Travassos, 1915; Hamanniella tortuosa (Leidy, 1850) Van Cleave, 1924; Hamanniella tumida (Van Cleave, 1947) Van Cleave, 1953; Oligacanthorhynchus tortuosa (Leidy, 1850) Schmidt, 1972; Oligacanthorhynchus tumida (Van Cleave, 1947) Schmidt, 1972; Travassosia tumida Van Cleave, 1947
Site of infection: Small intestine
Type host and locality: Caluromys philander, Brazil
Other reported hosts: Didelphis albiventris, Didelphis marsupialis, Didelphis virginiana, Marmosa demerarae, Marmosa murina, Metachirus myosurus, Philander opossum. Dasypus novemcinctus L., Euphractus sexcinctus (L.).
Locality Records: Brazil: Bahía: Igrapiúna; Rio de Janeiro: Rio de Janeiro; São Paulo: São Paulo. Colombia: Chocó. Mexico: Campeche, Colima, Michoacán, Guanajuato, Morelos, Oaxaca, Tabasco, Veracruz, Yucatán. French Guiana: Montagne du Tigre, Macouria, Pic Matecho. Paraguay: Chaco Boreal. Suriname. United States: Alabama, Arkansas, Florida, Georgia, Illinois, Louisiana, Mississippi, Oklahoma, South Carolina, Texas. Venezuela (Richardson et al., Reference Richardson, Gardner and Allen2014; Acosta-Virgen et al., Reference Acosta-Virgen, Lopez-Caballero, Garcia-Prieto and Mata-Lopez2015; Cirino et al., Reference Cirino, Neto, Maldonado and Gentile2020).
Remarks: Oligacanthorhynchus microcephalus was collected from Metachirops opossum and Philander opossum from Santa Cruz, Bolivia and used for a redescription of the species (Richardson et al., Reference Richardson, Gardner and Allen2014).
Discussion
Bolivia contains a large variety of biomes and it is rich in natural resources (Ergueta and Salazar, Reference Ergueta and Salazar1991; Auty, Reference Auty1994; Anderson, Reference Anderson1997; Hancock et al., Reference Hancock, Ralph and Ali2018). Among these resources, some minerals are used in high demand (Finer et al., Reference Finer, Jenkins, Pimm, Keane and Ross2008; Hancock et al., Reference Hancock, Ralph and Ali2018), and vast areas of the country have been converted to agricultural use (Cuellar and Noss, Reference Cuellar and Noss2014). The exploitation of these natural resources wipes out natural habitats and causes extinction of native biodiversity (Finer et al., Reference Finer, Jenkins, Pimm, Keane and Ross2008; Cuellar and Noss, Reference Cuellar and Noss2014; Gardner et al., Reference Gardner, Botero-Cañola, Aliaga-Rossel, Dursahinhan and Salazar-Bravo2021). These abrupt modifications change the interactions among species occurring in the biome, which includes the dynamics that regulate the interactions between parasites and hosts (Gardner and Campbell, Reference Gardner and Campbell1992b). The parasite checklist herein presented is a historical document that summarizes the marsupial parasite association present in Bolivia by the end of the Twentieth Century.
Of the 35 species of marsupials recorded for Bolivia we document the helminthological record for 17. Most of the specimens were collected in localities across the Chaco, and Yungas, with few individuals collected from the Amazon basin. The majority of the specimens representing both parasites and hosts were preserved and archived in relevant repositories for biodiversity, which include the Harold W. Manter Laboratory of Parasitology (Lincoln, Nebraska), the Museum of Southwestern Biology (Albuquerque, New Mexico), and the American Museum of Natural History (New York, New York). The records resulted from the synergistic effort of mammalogists and parasitologists participating in the Bolivian Faunistic Inventories completed by the end of the previous century (Anderson, Reference Anderson1997). The present checklist includes the helminths collected from didelphiomorphs and it expands on other published checklists that document the diversity of parasites in mammals present in Bolivia (Dick et al., Reference Dick, Gettinger and Gardner2007; Pucu et al., Reference Pucu, Lareschi and Gardner2014; Sanchez et al., Reference Sanchez, Lareschi, Salazar-Bravo and Gardner2018).
A greater effort is necessary to complete the inventory of the parasites of marsupials present in Bolivia, since 17 species of didelphiomorphs, plus Lestoros inca (Thomas), representative of Coenolestidae, have not been surveyed for helminths. Furthermore, the assessment of the helminth fauna associated with each species may be hindered by the relatively large sample size necessary to survey the parasite species richness in marsupials (Jiménez et al., Reference Jiménez, Gardner and Catzeflis2011; Byles et al., Reference Byles, Catzeflis, Scheibel and Jiménez2013).
Nematodes represent the most diverse group in this checklist; it includes 22 species of which 9 are included in Viannaiidae and only occur in didelphiomorph marsupials. The second largest group includes cyclophyllidean tapeworms (6 species) followed by rhopaliid trematodes (3 species) and 1 species of acanthocephalan. From the total of parasite species, 16 are monoxenous, and include nematodes of the Viannaiidae, Oxyuridae, Trichuridae, Molineidae and Ancylostomatidae. The other 16 species are heteroxenous, and they depend on molluscs or insects to infect their definitive hosts. Heteroxenous species may be used as indicators of the local biodiversity by revealing the taxonomic and trophic levels that still function in any given locality (Gardner and Campbell, Reference Gardner and Campbell1992b). A modest fraction of the organisms used in this checklist have served as the foundation for systematic reviews and species descriptions for trematodes, cestodes and nematodes (Gardner and Campbell, Reference Gardner and Campbell1992a; Haverkost and Gardner, Reference Haverkost and Gardner2008; Jiménez et al., Reference Jiménez, Braun, Campbell and Gardner2008; Gardner et al., Reference Gardner, Jiménez and Campbell2013), underscoring the relevance of species descriptions as the sole records documenting biodiversity.
As a consequence, the present checklist incorporates additional localities that better represent the distribution of parasites and their host spectrum. The results listed in this checklist should act as a starting point to build upon the diversity of mutualists, micropredators or parasites associated with marsupials. As stated elsewhere (Gardner and Campbell, Reference Gardner and Campbell1992b; Wood et al., Reference Wood, Welicky, Preisser, Leslie, Mastick, Greene, Maslenikov, Tornabene, Kinsella and Essington2023), the changes in the quality of the habitat and the diversity of organisms will determine the likelihood of heteroxenous species to complete their life cycle.
The identification of helminths herein presented documents their distribution in nearly 50% of the marsupial biodiversity of Bolivia. None of the species included in this checklist are known to have a zoonotic potential. Nevertheless this list should complement the efforts to screen these organisms for microparasites, which may be of zoonotic relevance and have been documented across Bolivia (Messenger et al., Reference Messenger, Garcia, Vanhove, Huaranca, Bustamante, Torrico, Torrico, Miles and Llewellyn2015). This is important because several species of marsupials are synanthropic and thrive in human altered environments (Bezerra-Santos et al., Reference Bezerra-Santos, Ramos, Campos, Dantas-Torres and Otranto2021; Voss, Reference Voss and Knight2022). This innate ability makes it important to continue the surveillance of parasites in these mammals, since they can expose human populations to unanticipated outbreaks. The surveillance is an important component of proposed novel protocols to prevent outbreaks resulting from anthropogenic alterations (Hoberg et al., Reference Hoberg, Boeger, Molnár, Földvári, Gardner, Juarrero, Kharchenko, Ortiz, Preiser, Trivellone and Brooks2022; Gardner et al., Reference Gardner, Brooks, Boeger and Hoberg2023).
Data availability statement
The helminthological record for most of the marsupials examined is available at http://opensiuc.lib.siu.edu/zool_data/23/.
Acknowledgements
The following organizations provided logistic support in the field: Museo Nacional de Historia Natural, La Paz; The Museum of Southwestern Biology, University of New Mexico and Instituto Boliviano de Biología de la Altura, La Paz. We also thank the students and staff of Museums in Bolivia who are working hard to learn and conserve their biodiversity heritage. Dr Gabor Racz of the H.W. Manter Laboratory assisted in work in the laboratory, loans and deposition of specimens. Cristina Damborenea (CHLP), Luis García Prieto (CNHE), Eric Hoberg (USNPC), Luis Muniz (CHIOC), Graciela Navone, Judith Price (CMNA), and Lidia Sánchez (CHIAUMSM) made part of the material they have under their care available for comparisons.
Author contributions
S. L. G. conceived and designed the logistics to secure specimens in the field. S. L. G. M. L. C. and F. A. J. conducted data gathering. F. A. J., M. L. C., B. B. and R. P. S. performed analyses. F. A. J. and S. L. G. wrote the article.
Financial support
This work was supported by United States National Science Foundation Grants BSR8612329, BSR8612329, BSR9024816, DEB9496263, and DEB9631295 to S. L. G. BSR8408923 to T. L. Yates; BSR8316740 to S. Anderson. Additional support was provided directly by the American Museum of Natural History, The Museum of Southwestern Biology, the Tinker Foundation, SIU-Carbondale and the Harold W. Manter Laboratory of Parasitology.
Competing interests
The authors declare that there is no competing interest.
Ethical standards
Most recent version of protocols describing the use of vertebrates includes protocol 21-017 approved by IACUC of SIUC.
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