Introduction

With 508 species of native mammals, Peru is the third most diverse country in the New World, after Brazil and Mexico, and the fifth most diverse for mammals in the world (^{Pacheco, Cadenillas, Salas, Tello, & Zeballos, 2009}). In Peru, the order Didelphimorphia is represented by the family Didelphidae with 40 species in 13 recognized genera (^{Pacheco et al., 2009}). However, despite this great diversity, the information on its helminth parasites is still very scarce (^{Tantaleán, Díaz, Sánchez, & Portocarrero, 2010}).

The common opossum, Didelphis marsupialis Linnaeus, 1758, is a marsupial species in the family Didelphidae, living in rainforest and subtropical forest, secondary forest, and near human settlements. This species is widely distributed from Mexico, south to Peru, Bolivia, Paraguay and northeastern Argentina, including Trinidad and the Lesser Antilles (^{Aponte, 2013}, ^{Emmons and Feer, 1997}, ^{Rueda et al., 2013}). It is listed as presenting Least Concern status by the International Union for Conservation of Nature and Natural Resources (IUCN Red List). Information about parasite diversity of this species in different countries along its geographical distribution is scarce (^{Acosta-Virgen et al., 2015}, ^{Fernandes et al., 2015}, ^{García-Prieto et al., 2012}, ^{Jiménez et al., 2011}, ^{Rodríguez-Ortiz et al., 2004}). Although there are some reports of digeneans (^{Kifune and Uyema, 1982}, ^{Miyazaki et al., 1978}, ^{Tantaleán et al., 1992}), nematodes (^{Arrojo, 2002}, ^{Sarmiento et al., 1999}, ^{Tantaleán et al., 2010}) and acanthocephalans (^{Tantaleán, Sánchez, Gómez, & Huiza, 2005}) from D. marsupialis in Peru, the knowledge of the helminth richness associated with this host species is still incomplete due to the wide distribution of this host in Peru.

In the present study, we report new records of helminth species parasitizing D. marsupialis in Peru. In addition, a checklist of helminth parasites of Peruvian marsupials is presented.

Materials and methods

Between May and November 2015, 8 specimens of D. marsupialis (Didelphidae) were found dead in the jungle of San Martín, Peru (Fig. 1). The specimens were collected and transferred to the laboratory of Clinical Analysis Morales Lab. for the respective necropsy. During the necropsy of hosts, trematodes and nematodes were extracted from the gastrointestinal tract, placed in Petri dishes with tap water, fixed in 4% hot formaldehyde and preserved in 70% ethanol. For morphological study, trematodes were stained with Semichon's carmine, dehydrated in successive series of ethanol (up to absolute ethanol), cleared in Eugenol and mounted in Canada balsam. Nematodes were cleared in Amman's lactophenol and temporarily mounted for morphological study (^{Lamothe-Argumedo, 1997}). The parasites were analyzed and measured using a Leica-DM500 microscope with LEICA-ICC50 HD camera and Software LAS (Leica Application Suite), EZ versión 1.80, 2009, Switzerland. Measurements are in millimeters (mm). The taxonomic determination of the parasites was in accordance with the diagnosis proposed by ^{Gibson, Jones, and Bray (2002)} and ^{Haverkost and Gardner (2008)} for trematodes, and ^{Chagas-Moutinho, Oliveira-Menezes, Cárdenas, and Lanfredi (2007)}, Lent and ^{Freitas, 1937a}, ^{Lent and Freitas, 1937b}, ^{Santos, Lent, and Gomes (1990)}, ^{Travassos (1922)}, ^{Vicente (1966)}, and ^{Vicente, Rodrigues, Gomes, and Pinto (1997)} for nematodes. The terms prevalence and mean intensity were used according to ^{Bush, Lafferty, Lotz, and Shostak (1997)}.

Vouchers of all helminth species were deposited in the Helminthological and Minor Invertebrates Collection of the Museum of Natural History at the San Marcos University (MUSM), Peru.

Furthermore, a checklist was compiled based on the new and previous reports of helminths parasites of marsupials from Peru. Undergraduate theses and scientific meetings do not constitute formal publications, and thus were not considered. Records published until April 2016 were included. The checklist consists of 2 sections: the first part is the list of helminth parasites of marsupials, indicating host, site of infection, locality and reference. The taxonomy of helminths follows ^{Amin (2013)} for Acanthocephala, ^{Anderson, Chabaud, and Willmott (2009)} for Nematoda, and ^{Gibson et al. (2002)} for Trematoda. The second part includes the list of hosts and their respective parasites. Marsupial species are in alphabetical order. The updated name of marsupials follows ^{Pacheco et al. (2009)}.

In this work, all applicable institutional, national and international guidelines for the care and use of wild animals were followed. Furthermore, all individuals of the host D. marsupialis were found dead and are not considered as Critically Endangered by IUCN.

Results

A total of 582 endoparasites were collected in the study specimens and the total prevalence was 100%. Morphological analyses of parasites permitted the identification of 11 taxa (2 digeneans and 9 nematodes) belonging to 9 genera and 8 families.

Phylum Platyhelminthes Gegenbaur, 1959

Class Trematoda Rudolphi, 1808

Family Plagiorchiidae Ward, 1917

Plagiorchis didelphidis (Parona, 1869) Stossich, 1904

Description: based on 5 adult specimens. Body 4.754–6.455 (5.452) long, maximum width 1.383–1.724 (1.583). Tegument covered with numerous small spines. Oral sucker subterminal, 0.420–0.564 (0.518) long by 0.537–0.708 (0.649) wide. Pharynx 0.239–0.333 (0.303) long by 0.260–0.393 (0.348) wide. Acetabulum 0.676–0.956 (0.837) long by 0.708–1.026 (0.872) wide. Anterior testis 0.421–0.611 (0.513) long by 0.475–0.703 (0.554) wide. Posterior testis 0.444–0.640 (0.528) long by 0.455–0.655 (0.535). Ovary 0.268–0.328 (0.289) long by 0.213–0.337 (0.289) wide. Eggs numerous, 0.042–0.046 long by 0.019–0.021 wide.

Taxonomic summary

Infection site: small intestine.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W).

Specimens deposited: MUSM 3400.

Prevalence: 25% (2 infected marsupials of 8).

Mean intensity: 8.

Mean abundance: 2.

Remarks

Species of Plagiorchis Luehe, 1899 are intestinal trematodes of amphibians, reptiles, birds and mammals (^{Rodrigues, 1994}). In Peru, 2 species are currently known: P. didelphidis from D. marsupialis, Didelphis albiventris Lund, 1840, Metachirus nudicaudatus (É. Geoffroy, 1803) and Philander opossum (Linnaeus, 1758) and Plagiorchis sp. from Leucophaeus pipixcan (Wagler, 1831) (^{Tantaleán et al., 1992}). This species is also described for Brazil and Paraguay (^{Fernandes et al., 2015}).

Family Rhopaliasidae (Looss, 1899) Yamaguti, 1958

Rhopalias caballeroi ^{Kifune & Uyema, 1982}

Description: based on 5 adult specimens. Body 3.489–4.090 (3.79) long, maximum width 0.820–1.074 (0.95). Oral sucker 0.058–0.254 (0.130) long by 0.070–0.283 (0.130) wide. Pharynx 0.053–0.223 (0.121) long by 0.030–0.149 (0.077) wide. Esophagus 0.097 long. Acetabulum 0.319–0.370(0.345) long by 0.289–0.341 (0.315) wide. Cirrus sac 0.230–0.938 (0.512) long. Anterior testis 0.488–0.541 (0.515) long by 0.515–0.547 (0.531) wide. Posterior testis 0.582–0.924 (0.750) long by 0.438–0.448 (0.440) wide. Ovary 0.120–0.229 (0.169) long by 0.233–0.238 (0.236) wide. Eggs 0.093–0.099 (0.096) long by 0.057–0.060 (0.058) wide.

Taxonomic summary

Infection site: small intestine and tongue.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W); Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3401.

Prevalence: 50% (4 infected marsupials of 8).

Mean intensity: 2.5.

Mean abundance: 0.625.

Remarks

Species of Rhopalias (Rudolphi, 1819) are parasites of the small intestines of marsupials from the Nearctic and Neotropical regions (^{Haverkost and Gardner, 2008}, ^{Fernandes et al., 2015}). Five species, namely R. baculifer Braun, 1900, R. caballeroi, R. coronatus ^{Kifune & Uyema, 1982}, R. horridus (Diesing, 1850) and Rhopalias sp. have been reported in Peru (^{Miyazaki et al., 1978}, ^{Morales et al., 2005}, ^{Tantaleán and Chávez, 2004}, ^{Tantaleán et al., 1992}). According to ^{Haverkost and Gardner (2008)}, R. caballeroi is distinguished by the absence of oral and flanking spines, and because it has between 4 and 11 spines visible within tentacle sacs. This species has also been reported for Argentina, Bolivia, Brazil, Colombia, Mexico, and Paraguay (^{Acosta-Virgen et al., 2015}, ^{Fernandes et al., 2015}).

Rhopalias coronatus (Rudolphi, 1819) Stiles & Hassall, 1898

Description: based on 5 adult specimens. Body 2.452–9.352(4.436) long, maximum width 0.212–1.581(0.733). Oral sucker 0.120–0.344 (0.183) long by 0.088–0.325 (0.178) wide. Pharynx 0.111–0.421 (0.201) long by 0.042–0.244 (0.121) wide. Acetabulum 0.149–0.821 (0.376) long by 0.156–0.800 (0.352) wide. Cirrus sac 0.562–2.198 (0.966) long. Anterior testis 0.158–0.624 (0.336) long by 0.102–0.263 (0.160) wide. Posterior testis 0.249–0.900 (0.500) long by 0.075–0.276 (0.149) wide. Ovary 0.070–0.345 (0.164) long by 0.089–0.351 (0.177) wide. Eggs 0.069–0.105 (0.092) long by 0.031–0.068 (0.048) wide.

Taxonomic summary

Infection site: small intestine and tongue.

Locality: Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3402.

Prevalence: 25% (2 infected marsupials of 8).

Mean intensity: 11.

Mean abundance: 2.75.

Remarks

This species is a common intestinal parasite of marsupials from North, Central and South America (^{Fernandes et al., 2015}, ^{Haverkost and Gardner, 2008}, ^{Rivillas et al., 2004}). According to ^{Haverkost and Gardner (2008)}, R. coronatus is distinguished by the presence of flanking and oral spines, between 3 and 11 spines visible within tentacle sacs, which extend far beyond the posterior margin of the pharynx. In Peru, R. coronatus has been registered in four marsupial hosts. This species has also been recorded from Argentina, Bolivia, Brazil, Costa Rica, Ecuador, Mexico, Paraguay, and Venezuela (^{Acosta-Virgen et al., 2015}, ^{Fernandes et al., 2015}, ^{Rodríguez-Ortiz et al., 2004}).

Phylum Nematoda Rudolphi, 1808

Family Aspidoderidae Skrjabin & Schikhobalova, 1947

Aspidodera raillieti^{Travassos, 1913}

Description: based on 12 adult specimens (6 male and 6 female). Male: Body 5.78–7.91 (7.10) long by 0.22–0.32 (0.28) wide. Cephalic expansion 0.12–0.16 (0.14) long. Esophagus 0.75–0.89 (0.84) long, bulb 0.22–0.27 (0.25) long by 0.17–0.21 (0.19) wide. Excretory pore at 0.60–0.76 (0.68) from anterior end. Spicules 0.84–1.07 (0.94) long. Gubernaculum 0.20–0.23 (0.21) long. Cloaca at 0.41–0.51 (0.47) from posterior end. Female: Body 7.60–8.67 (8.05) long by 0.41–0.49 (0.45) wide. Cephalic expansion 0.15–0.18 (0.16) long. Esophagus 0.85–1.06 (0.98) long, bulb 0.25–0.30 (0.27) long by 0.22–0.25 (0.24) wide. Excretory pore at 0.61–0.73 (0.68) from anterior end. Vulva located at the middle of the body 2.93–3.09 (3.02) from the anterior end. The anal opening at 1.03–1.13 (1.08) from the posterior end. Eggs 0.06–0.07 (0.068) long by 0.04–0.05 (0.043) wide.

Taxonomic summary

Infection site: small intestine.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W); Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3251.

Prevalence: 63% (5 infected marsupials of 8).

Mean intensity: 18.2.

Mean abundance: 11.37.

Remarks

Nematodes of the family Aspidoderidae are widely distributed in the Americas, in countries such as Brazil, Mexico, Panama, Paraguay, Trinidad, Argentina, USA, Peru, Bolivia, Guatemala, Venezuela, and Suriname (^{Chagas-Moutinho et al., 2007}). These nematodes are parasites of mammals of the orders Edentata, Marsupialia, and Rodentia (^{Chagas-Moutinho et al., 2007}, ^{Jiménez-Ruiz et al., 2006}, ^{Santos et al., 1990}). ^{Santos et al. (1990)} reviewed the genus and established some characters to identify these nematodes to the level of species, which include the cephalic cordons, the shape and length of the spicules, the shape of the spinneret, and the number of caudal papillae (^{Gomes et al., 2003}, ^{Jiménez-Ruiz et al., 2006}). Aspidodera raillieti was described by ^{Travassos (1913)} on the basis of specimens collected in the caecum from the Brazilian Common Opossum Didelphis aurita (Wied-Neuwi, 1826) from Brazil. The taxonomic characters were performed by ^{Chagas-Moutinho et al. (2007)} and ^{Santos et al. (1990)}. According to ^{Sarmiento et al. (1999)} specimens of Aspidodera harwoodi Chandler, 1932 have been recorded from D. marsupialis in Peru. However, ^{Santos et al. (1990)} considered A. harwoodi synonymous of A. raillieti. Other hosts of A. raillieti include Caluromys lanatus (Olfers, 1818); Didelphis virginiana Allen, 1900; D. albiventris; D. aurita; Chironectes minimus (Zimmermann, 1780); Chiropotes satanas (Hoffmannsegg, 1807); P. opossum and Nectomys squamipes (Brants, 1827) and Tolypeutes tricinctus (Linnaeus, 1758); T. apereoides in Brazil and D. virginiana in Mexico (^{Acosta-Virgen et al., 2015}, ^{Pinto et al., 2011}, ^{Vicente et al., 1997}). This species is also listed in Brazil and Mexico, in D. marsupialis (^{Chagas-Moutinho et al., 2007}, ^{Jiménez et al., 2011}).

Family Kathlaniidae Travassos, 1918

Cruzia tentaculata (Rudolphi, 1819) ^{Travassos, 1917}

Description: based on 10 adult specimens (5 male and 5 female). Male: Body 11.78–12.91 (12.30) long by 0.54–0.71 (0.68) wide. Esophagus 2.75–2.89 (2.84) long, bulb 0.29–0.30 (0.25) long by 0.27–0.30 (0.28) wide. Excretory pore at 1.18–1.30 (1.20) from anterior end. Spicules 0.80–0.93 (0.89) long. Gubernaculum 0.16–0.20 (0.19) long. Cloaca at 0.15–0.20 (0.18) from posterior end. Female: Body 11.60–12.67 (10.05) long by 0.50–0.58 (0.51) wide. Oral capsule 0.18–0.26 (0.22) long. Esophagus 1.85–2.06 (1.98) long, bulb 0.25–0.28 (0.27) long by 0.26–0.29 (0.27) wide. Excretory pore at 1.18–1.30 (1.23) from anterior end. Vulva located at the middle of the body 5.24–5.34 (5.26) from the anterior end. The anal opening at 0.70–1.09 (0.98) from the posterior end. Eggs 0.1–0.12 (0.11) long by 0.04–0.05 (0.04) wide.

Taxonomic summary

Infection site: small intestine.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W); Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3253.

Prevalence: 63% (5 infected marsupials of 8).

Mean intensity: 15.2.

Mean abundance: 9.5.

Remarks

Species of Cruzia are parasites of the large intestine of marsupials, reptiles, amphibians, and mammals (^{Adnet, Anjos, Menezes-Oliveira, & Lanfredi, 2009}). The specimens collected from the small intestine of D. marsupialis belonging to the genus Cruzia^{Travassos, 1917} by having a mouth with three well-developed triangular lips, pharynx with three longitudinal rows of hooks and three structures truncated like tooth at the base, esophagus with well-developed bulb and with anterior blind intestine (^{Vicente et al., 1997}). Morphometric characteristics of the specimens studied in the present paper fit with the aforementioned by Travassos (1917) and ^{Vicente et al. (1997)} for Cruzia tentaculata (Rudolphi, 1819) Travassos, 1917. Cruzia tentaculata is a common parasite of marsupials in South and Central America (^{Gomes et al., 2003}, ^{Pinto et al., 2011}). In Peru, C. tentaculata has been found parasitizing the intestine of D. marsupialis and M. nudicaudatus (Geoffroy, 1803) from Cajamarca and Iquitos, respectively (^{Sarmiento et al., 1999}, ^{Tantaleán et al., 2010}).

Family Gongylonematidae Sobolev, 1949

Gongylonemoides marsupialis (^{Vaz & Pereira, 1934}) ^{Freitas & Lent, 1937}

Description: based on 10 adult specimens (6 male and 4 female). Male: Body 20.64–22.32 (21.10) long by 0.22–0.27 (0.24) wide. Muscular and glandular esophagus 0.50–0.64 (0.52) and 3.60–3.7 (3.65) long, respectively. Excretory pore at 0.60–0.68 (0.66) from anterior end. Right and left spicules 0.28–0.30 (0.29) and 0.154–0.180 (0.16) long, respectively. Cloaca at 0.205–0.208 (0.207) from posterior end. Female: Body 45.60–46.67 (46.05) long by 0.30–0.32 (0.31) wide. Muscular and glandular esophagus 0.60–0.71 (0.68) and 6.48–6.72 (6.65) long, respectively. Excretory pore at 0.65–0.72 (0.66) from anterior end. Vulva located at the middle of the body 5.60–6.09 (5.80) from the posterior end. The anal opening at 0.237–0.263 (0.240) from the posterior end. Eggs 0.04–0.05 (0.04) long by 0.01–0.02 (0.01) wide.

Taxonomic summary

Infection site: trachea.

Locality: Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3254.

Prevalence: 25% (2 infected marsupials of 8).

Mean intensity: 15.

Mean abundance: 3.75.

Remarks

The species was described as Gongylonema marsupialis by ^{Vaz and Pereira (1934)} based on a female specimen collected from D. aurita from Brazil. ^{Freitas and Lent (1937)} created the genus Gongylonemoides to include this species, considering the absence of the gubernaculum, the most outstanding character. The specimens studied herein were closer to these referred by ^{Freitas and Lent (1937)}. Gongylonemoides marsupialis has been registered in D. aurita, D. marsupialis, and M. opossum from Brazil (^{Gomes et al., 2003}, ^{Vicente et al., 1997}). This paper constitutes the first register of this nematode species in Peru.

Family Physalopteridae Leiper, 1908

Physaloptera mirandai ^{Lent & Freitas, 1937}

Description: based on 10 adult specimens (5 male and 5 female). Male: Body 29.75–37.55 (32.05) long by 0.45–0.99 (0.77) wide. Muscular and glandular esophagus 064–0.89 (0.78) and 4.33–7.08 (5.84) long, respectively. Excretory pore at 1.01–1.21 (1.13) from anterior end. Spicules, 0.46–0.62 (0.55) long. Cloacal aperture at 1.47–2.04 (1.71) from posterior end. Female: Body 30.87–46.31 (37.80) long by 0.64–1.03 (0.84) wide. Muscular and glandular esophagus 0.67–0.94 (0.76) and 7.49–8.40 (7.74) long, respectively. Excretory pore at 1.07–1.37 (1.20) from anterior end. Vulva located at 10.31–11.29 (10.83) from anterior end. Cloacal aperture at 1.47–2.04 (1.71) from posterior end. Anal aperture at 0.78–0.96 (0.84) from the posterior end.

Taxonomic summary

Infection site: stomach.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W).

Specimens deposited: MUSM 3252.

Prevalence: 25% (2 infected marsupials of 8).

Mean intensity: 11.5.

Mean abundance: 2.87.

Remarks

^{Lent and Freitas (1937a)} described Physaloptera mirandai recovered from the brown four-eyed opossum M. nudicaudatus in Brazil. Our specimens show morphometric characteristics similar to those indicated in the original description of P. mirandai by ^{Lent and Freitas (1937a)}. This species has been previously registered in Peru by ^{Tantaleán et al. (2010)} in M. nudicaudatus. This paper constitutes the first record of P. mirandai parasitizing to D. marsupialis (^{Vicente et al., 1997}).

Turgida turgida (Rudolphi, 1819) Travassos, 1919

Taxonomic summary

Infection site: stomach.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W).

Specimens deposited: MUSM 3403.

Prevalence: 13% (1 infected marsupial of 8).

Mean intensity: 2.

Mean abundance: 0.25.

Remarks

Turgida turgida (Rudolphi, 1819) Travassos, 1919, is a common parasite of marsupials from North and South America (^{Gomes et al., 2003}). Adult worms are found parasitizing the stomach, mainly the greater curvature, producing a large fibrous ulceration at the point of attachment (^{Alden, 1995}, ^{Gray and Anderson, 1982}, ^{Humberg et al., 2011}). The taxonomic characters used by us to identify our specimens follow ^{Matey, Kuperman, and Kinsella (2001)} and ^{Travassos (1920)}. According to ^{Gomes et al. (2003)}, ^{Humberg et al. (2011)}, ^{Pinto et al. (2011)} and ^{Vicente et al. (1997)}, T. turgida is parasitie of D. albiventris, D. aurita, D. marsupialis, D. virginiana, Caluromys philander, Ch. minimus, and M. nudicaudatus from Brazil. In Peru, ^{Tantaleán et al. (2010)} recorded this species from P. opossum.

Family Trichuridae Railliet, 1915

Trichuris marsupialis (Rud, 1819) Hall, 1916

Description: based on 10 adult specimens (5 male and 5 female). Male: Body 12.5–15.5 (14.65) long. Spicules 0.90–1.30 (0.97) long. Cloaca at 1.26–1.50 (1.30) from posterior end. Female: Body 13.6–20.23 (17.45) long. Eggs 0.062–0.068 (0.066) long by 0.031–0.032 (0.031) wide.

Taxonomic summary

Infection site: stomach.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W); Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3256.

Prevalence: 50% (4 infected marsupials of 8).

Mean intensity: 12.

Mean abundance: 6.

Remarks

Trichuris marsupialis has been found parasitizing the intestine of D. virginiana in the United States of America by ^{Babero (1960)}; D. marsupialis, Didelphis sp., D. virginiana, and P. opossum from Mexico by ^{Acosta-Virgen et al. (2015)} and ^{Monet-Mendoza, Osorio-Sarabia, and García-Prieto (2005)}, and in D. albiventris from Brazil by ^{Pinto et al. (2011)}. In Peru, Trichuris sp. has been registered in the intestine of four marsupial hosts (^{Tantaleán et al., 2010}). Thus, T. marsupialis represents the first species recorded from marsupials of Peru.

Family Viannaiidae Durette-Desset & Chabaud, 1981

Viannaia hamata^{Travassos, 1914}

Description: based on 10 adult specimens (5 male and 5 female). Male: Body 2.65–2.82 (2.79) long by 0.130–0.172 (0.154) wide. Cephalic expansion 0.045–0.047 (0.046) long. Esophagus 0.305–0.320 (0.316) long. Excretory pore at 0.312–0.340 (0.320) from anterior end. Spicules 0.133–0.140 (0.138) long. Gubernaculum 0.019–0.023 (0.022) long. Female: Body 2.42–3.80 (3.29) long by 0.175–0.220 (0.200) wide. Cephalic expansion 0.040–0.047 (0.046) long. Esophagus 0.250–0.352 (0.322) long. Excretory pore at 0.282–0.354 (0.334) from anterior end. Vulva located at the middle of the body 0.073–0.103 (0.099) from the anterior end. Eggs 0.054–0.062 (0.059) long by 0.04–0.06 (0.05) wide.

Taxonomic summary

Infection site: stomach.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W); Lamas, San Martín, Peru (6°25′ S, 76°30′ W).

Specimens deposited: MUSM 3404.

Prevalence: 38% (3 infected marsupials of 8).

Mean intensity: 41.3.

Mean abundance: 15.5.

Remarks

Our specimens show morphometric characteristics similar to those indicated in the redescription of V. hamata by ^{Guerrero (1985)}. Viannaia hamata had been recorded only in D. marsupialis and D. aurita from Brazil (^{Gomes et al., 2003}, ^{Pinto and Gomes, 1980}, ^{Pinto et al., 2011}); therefore, Viannaia hamata represents a new record in Peru.

Viannaia viannaia^{Travassos, 1914}

Description: based on 10 adult specimens (5 male and 5 female). Male: Body 1.650–2.720 (2.360) long by 0.077–0.16 (0.106) wide. Cephalic expansion 0.035–0.050 (0.047) long. Esophagus 0.221–0.290 (0.278) long. Excretory pore at 0.270–0.355 (0.320) from anterior end. Spicules 0.097–0.117 (0.108) long. Female: Body 2.30–3.13 (3.09) long by 0.140–0.210 (0.180) wide. Cephalic expansion 0.030–0.048 (0.044) long. Esophagus 0.251–0.352 (0.320) long. Excretory pore at 0.284–0.350 (0.330) from anterior end. Vulva located at the middle of the body 0.072–0.102 (0.097) from the anterior end. Eggs 0.052–0.062 (0.057) long by 0.04–0.06 (0.05) wide.

Taxonomic summary

Infection site: stomach.

Locality: Bella Vista, San Martín, Peru (7°15′ S, 76°28′ W).

Specimens deposited: MUSM 3255.

Prevalence: 25% (2 infected marsupials of 8).

Mean intensity: 72.5.

Mean abundance: 18.2.

Remarks

The genus Viannaia was erected by ^{Travassos (1914)} to accommodate those species of neotropical Trichostrongylidae with short spicules (^{Guerrero, 1985}). Our specimens completely correspond with the original description given by ^{Travassos (1914)} and the redescription made by ^{Guerrero (1985)} for Viannaia viannaia. This nematode was recorded in D. marsupialis, D. aurita, P. opossum, and Akodon cursor (Winge, 1887) from Brazil; D. virginiana in USA, D. marsupialis and P. opossum in Venezuela and D. marsupialis and P. opossum in Mexico (^{Jiménez et al., 2011}, ^{Vicente et al., 1997}). This paper constitutes the first record of V. viannaia in Peru.

To date, a total of 38 helminth parasites have been recorded in Peruvian marsupials (Table 1), all in adult stage. Digeneans have the highest species richness in number and percentage (n = 19, 50%), followed by nematodes (n = 17, 45%) and acanthocephalans (n = 2, 5%). The parasites with the highest numbers of records were the digeneans Plagiorchis didelphidis (Parona, 1896) Stossich, 1904 (n = 4) and Rhopalias coronatus ^{Kifune & Uyema, 1982} (n = 4), and the nematode Aspidodera sp. (n = 4). For Peru information exists on the parasites of 10 marsupials, distributed in 7 genera: Chironectes (1 sp.), Didelphis (2 spp.), Marmosa (1 sp.), Marmosops (1 sp.), Metachirus (1 sp.), Monodelphis (2 spp.) and Philander (2 spp.) (Table 2). Marsupials that harbored the highest number of parasites were D. marsupialis (n = 22) followed by P. opossum (n = 15), M. nudicaudatus (n = 13) and D. albiventris (n = 6) (Table 2). The localities with the highest number of records were Huánuco (28%, n = 15), Loreto (21%, n = 11) and San Martín (21%, n = 11) (Table 1).

Discussion

As a result of this study, we report 11 helminth species (3 digeneans and 9 nematodes) in the helminth communities of D. marsupialis from San Martín region, Peru. Species of parasites that represent new records for the country include V. viannaia, V. hamate, and G. marsupialis. All parasites recorded in this study are reported for the first time from the San Martín region.

In the present study, nematodes represented 82% of the total species in the component community of D. marsupialis. The composition of the majority of parasite communities of didelphid marsupials show a higher number of nematode species (^{Acosta-Virgen et al., 2015}, ^{Alden, 1995}, ^{Grover and Harkema, 1970}, ^{Jiménez et al., 2011}, ^{Monet-Mendoza et al., 2005}). According to ^{Acosta-Virgen et al. (2015)}, the structuring factor of the helminthofauna in marsupials is the diet; most of the nematode species infect these host species through ingestion of eggs, larvae or intermediate hosts.

In the present work, 6 of 11 helminth species collected in D. marsupialis have indirect patterns of transmission by intermediate host ingestion (G. marsupialis, P. didelphidis, R. caballeroi, R. coronatus, P. mirandai, and T. turgida) and 5 are transmitted directly by ingestion of eggs (A. raillieti, C. tentaculata, T. marsupialis, V. hamate, and V. viannaia). The helminthfauna of D. marsupialis in San Martín seemed to be dominated by helminths with direct patterns of transmission. This is indicated by the highest values of prevalence of A. raillieti, C. tentaculata, and T. marsupialis, which exceeded 49%. In contrast, helminths with indirect patterns of transmission had low values of prevalence. ^{Jiménez et al. (2011)} mention 2 hypotheses to explain the low prevalence values in helminths with indirect patterns of transmission, including as the main reason the wide spectrum of food items used by marsupials such as D. marsupialis.

The checklist presented herein includes 32 named and 6 undetermined species of helminths associated with 10 marsupial host species from Peru; these come from 7 of the 26 Peruvian regions. The greatest richness of parasites was registered among digeneans (19 spp.) and nematodes (17 spp.), in contrast to what was observed by ^{Jiménez, Scheibel, Byles, and Gardner (2013)} in the parasites of marsupials in Bolivia, where nematodes and cestodes are the dominant group of parasites, while digeneans barely are represented by 2 species; this situation also was observed by ^{Pérez-Ponce de León, García-Prieto, and Mendoza-Garfias (2007)} in digeneans of marsupials from Mexico, where digeneans showed a low species richness. The large number of species being represented by digeneans in this work could be a result of the extraordinary diversification of sites of infection, life-cycles, and in the modes of feeding (^{Pérez-Ponce de León et al., 2007}).

The second species-richest taxon was Nematoda, represented by 17 species, similar to compiled by ^{García-Prieto et al. (2012)}, who listed 14 named and 7 unidentified nematode species in marsupials from Mexico, but it is a different number to that reported from Bolivia (21 nematode species) (^{Jiménez et al., 2013}). According to ^{Garrido-Olvera, García-Prieto, and Pérez-Ponce de León (2006)}, nematodes are probably the second largest taxon in the Animal kingdom after arthropods, when considering the number of described and estimated unknown species.

The other group of parasites, Acanthocephala, was represented by only a few species, which corresponds to the situation in Mexico (^{García-Prieto, García-Varela, Mendoza-Garfias, & Pérez-Ponce de León, 2010}).

The digeneans Amphimerus neotropicales Caballero, Montero, Gei & Caballero, 1963, Duboisiella proloba Baer, 1938, P. didelphidis, Rhopalias baculifer Braun, 1900, R. coronatus and Rhopalias horridus (Diesing, 1850) Stiles & Hassall, 1898 and the nematode Gnathostoma turgidum Stossich, 1902 were the first species of helminths recorded from Peruvian marsupials (^{Miyazaki et al., 1978}).

In Peru, there are 40 known marsupial species (^{Pacheco et al., 2009}), of which only 25% (10 hosts of one family) have parasitological records; this information likely corresponds to only a small proportion of the true richness of parasites with a high amount of diversity remaining untouched. The marsupial species D. marsupialis, P. opossum, M. nudicaudatus, and D. albiventris presented the highest richness of parasites. This is similar to that reported from Mexico, where D. marsupialis and P. opossum are the hosts with the highest number of helminth parasites after D. virginiana (^{Pérez-Ponce de León & García-Prieto, 2001}).