Introduction
Peru harbours the fifth highest diversity of reptile species among the world's countries, with 524 species, distributed in three orders, 32 families and 127 genera (Uetz et al., Reference Uetz, Freed, Aguilar and Hošek2021). Many of these species are endemic in Peruvian territory and are in a vulnerable or critically endangered situation according to the International Union for Conservation of Nature, mainly due to the loss of habitat, anthropogenic disturbance and illegal hunting (Peres & Nascimento, Reference Peres and Nascimento2006). Most of these species are found on the eastern side of the Andes and the Amazon basin (Koch et al., Reference Koch, Venegas, Santa Cruz and Böhme2018).
Reptiles play an important ecological role by being part of the food web, as prey for mammals, amphibians and birds, as well as being predators themselves of various invertebrates and vertebrates. They also act as seed dispersers and their presence indicates good ecosystem health (Klemens & Thorbjarnarson, Reference Klemens and Thorbjarnarson1995; Benítez-Malvido et al., Reference Benítez-Malvido, Tapia, Suazo, Villaseñor and Alvarado2003; Castro & Galetti, Reference Castro and Galetti2004; Stevenson & Guzmán, Reference Stevenson and Guzmán2008). One of their ecological roles involves serving as hosts to a range of parasitic helminths with both direct and indirect life cycles, contributing to their population dynamics and community structure (Fernandes & Kohn, Reference Fernandes and Kohn2014; Gómez-Puerta et al., Reference Gómez-Puerta, Bachmann, Quiñones, Quispe, Torres and Macalupu2017; Huancachoque et al., Reference Huancachoque, Sáez, Cruces, Mendoza, Luque and Chero2020).
Some compilation studies on reptile helminths were published by Tantaleán et al. (Reference Tantaleán, Sarmiento and Huiza1992), Sarmiento et al. (Reference Sarmiento, Tantaleán and Huiza1999) and McAllister et al. (Reference McAllister, Bursey and Freed2010), focused on some helminth groups and limited to some geographical regions of the country. Considering the great diversity of reptile hosts in Peru, many helminth species have not yet been described by specialists, and others are neglected in their studies. Here, we present a current record of helminth parasites (Platyhelminthes, Nematoda and Acanthocephala) that infect reptile species and their geographical distribution in Peruvian territory, which increases knowledge about parasites in the Neotropical region.
Materials and methods
The checklist was compiled based on information from three sources: (1) an extensive bibliographical review of helminth parasites reported from reptiles in Peru, using different databases such as CAB Abstracts, Biological Abstracts, Helminthological Abstracts and Zoological Records (Web of Knowledge); (2) a search in the database of the Helminthological and Minor Invertebrates Collection of the Museum of Natural History at San Marcos University, Peru and in the Collection of Protozoa and Metazoan Parasites of Federico Villarreal University, Peru; and (3) a bibliographical search of articles published in Spanish that were not indexed by electronic databases. Undergraduate theses and scientific meetings do not constitute formal publications and were thus not considered. The parasite–host list is presented in phylogenetic order starting with the phylum Platyhelminthes (Trematoda and Cestoda) and followed by the phyla Acanthocephala and Nematoda. Each group contains families, genera and species in alphabetical order. The classification of helminths is based on the following references: Gibson et al. (Reference Gibson, Jones and Bray2002), Jones et al. (Reference Jones, Bray and Gibson2005), and Bray et al. (Reference Bray, Gibson and Jones2008) for Trematoda; Khalil et al. (Reference Khalil, Jones and Bray1994) for Cestoda; Anderson et al. (Reference Anderson, Chabaud and Willmott2009) for Nematoda and Amin (Reference Amin2013) for Acanthocephala. The nomenclatural changes of the names of helminths are based on particular references indicated in the notes section. Information for each species includes scientific name, authority and year, host species, developmental stage, site of infection, locality, and the respective reference. Type locality, type host, and original reference of a new species are indicated in parentheses. When one record obtained from a collection database has not been published, we include the acronym of this collection after the record. Finally, for each record the acronym and accession number of the collections where the specimens were deposited, is included. Acronyms are as follows: Collection of Protozoa and Metazoan Parasites of Federico Villarreal University (CPMP), Peru; Helminthological and Minor Invertebrates Collection of the Museum of Natural History at San Marcos University (MUSM), Peru; Helminthological Collection of Oswaldo Cruz Institute (CHIOC), Brazil; Helminthological Collection of the National Museum of Natural History, Smithsonian Institution (USNM), USA; United States National Parasite Collection (USNPC), USA; Collection of the Parasitology of Wild Animal and Zoonoses of the Biological Sciences Faculty at San Marcos University (Col. PAS–FCB), Peru; and State Museum of Natural History Karlsruhe (SMNK), Germany. The names of host species follow Uetz et al. (Reference Uetz, Freed, Aguilar and Hošek2021). The names of species of reptiles in the host–parasite list is arranged according to the higher-level classification of Uetz et al. (Reference Uetz, Freed, Aguilar and Hošek2021). Parasite names are updated in agreement with the recent literature, but inclusion in the parasite or host lists does not necessarily imply that authors agree with their validity.
Results
To date, a total of 106 helminth parasites (82 nominal species and 24 taxa identified at generic level) have been recorded in reptiles from Peru, the majority in the adult stage. Nematodes have the highest species richness in number and percentage (n = 79, 74.52%), followed by trematodes (n = 17, 16.03%) and cestodes (n = 9, 8.49%). The acanthocephalans are represented by only one species. The parasites with the highest numbers of records are the nematodes Physaloptera retusa Rudolphi, 1819 (n = 11), Physalopteroides venancioi (Lent, Freitas & Proença, 1946) (n = 9) and Strongyluris oscari Travassos, 1923 (n = 7). The 106 taxa of helminth parasites have been recorded from 55 species of reptiles in Peru, distributed in 34 genera and 14 families. The reptiles with the most reports of helminths in Peru are the yellow-footed tortoise Chelonoidis denticulatus (Linnaeus, 1766) (Testudinidae) with 18 species (three trematodes and 15 nematodes), followed by the Peru desert tegu Dicrodon guttulatum Duméril & Bibron, 1839 (Teiidae) with 11 species (three cestodes and eight nematodes) and the yellow-spotted Amazon River turtle Podocnemis unifilis Troschel, 1848 (Podocnemididae) with 10 species (five trematodes and five nematodes).
Parasite–host list
PHYLUM PLATYHELMINTHES GEGENBAUR, 1859
CLASS TREMATODA RUDOLPHI, 1808
SUB CLASS DIGENEA CARUS, 1863
SUPERFAMILY CLINOSTOMOIDEA LÜHE, 1901
FAMILY LIOLOPIDAE ODHNER, 1912
Helicotrema spirale (Diesing, 1850) Odhner, 1912
Chelonoidis denticulatus; adult; intestine; Loreto (03°43′S, 73°14′W) (Tantaleán & Forlong, Reference Tantaleán and Forlong2013).
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3052) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine; Loreto (MUSM-HEL 57) (Present study).
SUPERFAMILY GORGODEROIDEA LOOSS, 1899
FAMILY DICROCOELIIDAE LOOSS, 1899
Paradistomum sp1.
Hemidactylus mabouia; adult; gallbladder; San Martín (6°24′S, 76°30′W) (CPMP 208a–f, 209) (Present study).
Paradistomum sp2.
H. mabouia; adult; gallbladder; San Martín (6°24′S, 76°30′W) (CPMP 210a–c, 211) (Present study).
FAMILY MESOCOELIIDAE DOLLFUS, 1929
Mesocoelium sp.
Dipsas catesbyi; adult; intestine; San Martin (6°24′S, 76°30′W) (CPMP 200) (Present study).
SUPERFAMILY MICROSCAPHIDIOIDEA LOOSS, 1900
FAMILY MICROSCAPHIDIIDAE LOOSS, 1900
Podocnemitrema papillosus Alho & Vicente, 1964
Podocnemis expansa, Podocnemis unifilis; adult; intestine; Loreto (MUSM-HEL 2977) (Tantaleán et al., Reference Tantaleán, Sánchez and Pineda Catalan2011).
SUPERFAMILY PARAMPHISTOMOIDEA FISCHOEDER, 1901
FAMILY CLADORCHIIDAE FISCHOEDER, 1901
Halltrema avitellina Lent & Freitas, 1939
P. expansa, P. unifilis; adult; intestine; Loreto (MUSM-HEL 2976) (Tantaleán et al., Reference Tantaleán, Sánchez and Pineda Catalan2011).
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3051) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine, stomach; Ucayali (MUSM-HEL 26) (Present study).
Halltrema heteroxenum (Cordero & Vogelsang, 1940) Jones, 2005
P. unifilis; freshwater, adult; intestine; Loreto (Tantaleán & Forlong, Reference Tantaleán and Forlong2013).
Nematophila grandis (Diesing, 1839) Travassos, 1934
Peltocephalus dumerilianus; adult; intestine; Ucayali (USNM 1351577) (unpublished data, USNM).
P. unifilis; adult; stomach; Loreto, Madre de Dios (MUSM-HEL 77, 230, 489, 563) (Salizar & Sánchez, Reference Salizar and Sánchez2004).
P. unifilis; adult; intestine, stomach; Loreto (05°20′S, 74°19′W) (Sánchez et al., Reference Sánchez, Tantaleán, Vela and Méndez2006).
P. expansa, P. unifilis; adult; stomach, Loreto (MUSM-HEL 2975) (Tantaleán et al., Reference Tantaleán, Sánchez and Pineda Catalan2011).
P. unifilis; adult; stomach; Loreto (MUSM-HEL 3037) (Present study).
C. denticulatus; adult; stomach, San Martín (6°24′S, 76°30′W) (CPMP 202) (Present study).
SUPERFAMILY PLAGIORCHIOIDEA LÜHE, 1901
FAMILY PLAGIORCHIIDAE LÜHE, 1901
Glossidiella peruensis Huancachoque et al., Reference Huancachoque, Sáez, Cruces, Mendoza, Luque and Chero2020
Atractus major (type host); adult; lung; San Martin (6°11′S, 76°50′W) (type locality) (holotype, MUSM-HEL 4029; paratypes, MUSM-HEL 4030a–f) (Huancachoque et al., Reference Huancachoque, Sáez, Cruces, Mendoza, Luque and Chero2020).
FAMILY RENIFERIDAE PRATT, 1902
Renifer heterocoelium (Travassos, 1921) Caballero & Vogelsang, 1947
Chironius sp.; adult; oral cavity; San Martin (6°24′S, 76°30′W) (CPMP 201) (Present study).
FAMILY TELORCHIIDAE (LOOSS, 1899) DOLLFUS, 1925
Orchidasma amphiorchis (Braun, 1899) Looss, 1900
Chelonia mydas agassizii; adult; intestine; Ica (Tantaleán et al., Reference Tantaleán, Sarmiento and Huiza1992; Fernandes & Kohn, Reference Fernandes and Kohn2014; Werneck & Da Silva, Reference Werneck and Da Silva2016).
Telorchis hagmanni Lent & Freitas, 1937
P. unifilis; adult; intestine; Loreto (Col. PAS–FCB 256) (Tantaleán et al., Reference Tantaleán, Sánchez and Pineda Catalan2011).
SUPERFAMILY PRONOCEPHALOIDEA LOOSS, 1899
FAMILY PRONOCEPHALIDAE LOOSS, 1902
Adenogaster serialis Looss, 1899
C. mydas agassizii; adult; intestine; Ica (Tantaleán et al., Reference Tantaleán, Sarmiento and Huiza1992; Fernandes & Kohn, Reference Fernandes and Kohn2014; Werneck & Da Silva, Reference Werneck and Da Silva2016).
Cricocephalus albus (Kühl & van Hasselt, 1822) Looss, 1899
C. mydas agassizii; adult; intestine; Piura (05°48′S, 80°51′W) (MUSM-HEL 3661) (Gómez-Puerta et al., Reference Gómez-Puerta, Bachmann, Quiñones, Quispe, Torres and Macalupu2017).
SUPERFAMILY SCHISTOSOMATOIDEA STILES & HASSALL, 1898
FAMILY SPIRORCHIIDAE STUNKARD, 1921
Atamatam amazoniensis Bullard & Roberts, 2019
Chelus fimbriata; adult; blood vessels of kidney and mesentery; Loreto (03°45′S, 73°14′W) (holotype, USNM 1557310; paratypes, USNM 1557311–1557312) (Bullard et al., Reference Bullard, Roberts and Warren2019).
Note: Sequence of partial 28S in the GenBank database MK775718.
Paratamatam iquitosiensis Bullard & Roberts, 2019
C. fimbriata; adult; blood vessels of kidney and mesentery; Loreto (03°45′S, 73°14′W) (holotype, USNM 1557313; paratype, USNM 1557314–1557319) (Bullard et al., Reference Bullard, Roberts and Warren2019).
Note: Sequence of partial 28S in the GenBank database MK775719 and MK775720.
Pitiutrema revelae Dutton & Bullard, 2019
Podocnemis sextuberculata; adult; heart; Loreto (03°45′S, 73°14′W) (holotype, USNM 1578590; paratypes, USNM 1578591–1578593) (Dutton et al., Reference Dutton, Warren and Bullard2019).
Note: Sequence of partial 28S in the GenBank database MN244241.
CLASS CESTODA VAN BENEDEN, 1849
ORDER CYCLOPHYLLIDEA VAN BENEDEN IN BRAUN, 1900
FAMILY ANOPLOCEPHALIDAE CHOLDKOVSKY, 1902
Oochoristica ameivae (Beddard, 1914) Baer, 1924
Ameiva ameiva; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93228) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Oochoristica freitasi Rego & Ibañez, Reference Rego and Ibañez1965
Dicrodon heterolepis (type host); adult; intestine; La Libertad (type locality) (holotype, CHIOC 29203-29259; paratype, CHIOC 29197-29202) (Rego & Ibañez, Reference Rego and Ibañez1965).
D. heterolepis; adult; intestine; Ancash (10°05′S, 78°05′W) (USNPC 100637) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
Dicrodon guttulatum; adult; intestine; Piura, Tumbes (MUSM-HEL 2301, 2308) (Ávila & Silva, Reference Ávila and Silva2010).
D. heterolepis; adult; intestine; Lima (MUSM-HEL 346) (Present study).
Oochoristica iguanae Bursey & Goldberg, 1996
D. guttulatum; adult; intestine; Piura, Lambayeque (MUSM-HEL 2278, 2307) (Ávila & Silva, Reference Ávila and Silva2010).
Oochoristica sp.
Microlophus peruvianus; adult; intestine; Moquegua (Cordova et al., Reference Cordova, Rego and Vicente1980).
D. guttulatum; adult; intestine; Piura (MUSM-HEL 2848) (Present study).
D. guttulatum; adult; intestine; Tumbes (MUSM-HEL 2845) (Present study).
Oochoristica travassosi Rego & Ibañez, Reference Rego and Ibañez1965
Leiocephalus sp. (type host); adult; intestine; La Libertad (type locality) (holotype, CHIOC 29207-29210; paratype, CHIOC 29211-29214; paratype, CHIOC 29257) (Rego & Ibañez, Reference Rego and Ibañez1965).
Phyllodactylus johnwrighti; adult; intestine; Cajamarca (USNPC 100809) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
Oochoristica vanzolinii Rego & Rodrigues, 1965
H. mabouia; adult; intestine; San Martín (6°24′S, 76°30′W) (CPMP 207a–d) (Present study).
ORDER PROTEOCEPHALIDEA MOLA, 1928
FAMILY PROTEOCEPHALIDAE LA RUE, 1911
Crepidobothrium gerrardii Baird, 1860
Boa constrictor; adult; intestine; Loreto (4°29′S, 73°35′W) (MUSM-HEL 2978) (Gómez-Puerta, Reference Gómez-Puerta2011).
Ophiotaenia flava Rudin, 1917
Kentropyx pelviceps; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93244) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Ophiotaenia sp.
B. constrictor; adult; intestine; Ucayali (MUSM-HEL 222) (Present study).
PHYLUM NEMATODA RUDOLPHI, 1808
FAMILY DIAPHANOCEPHALIDAE TRAVASSOS, 1920
Kalicephalus sp.
Bothrops atrox; adult; intestine, stomach; Cusco (MUSM-HEL 1538) (Present study).
Xenodon sp.; adult; intestine; Loreto (Tantaleán, Reference Tantaleán1976).
Kalicephalus inermis Molin, 1861
B. atrox; adult; intestine, stomach; Amazonas (Tantaleán & Gónzalo, Reference Tantaleán and Gónzalo1985)
Lachasis muta; adult; intestine, stomach; Loreto (Present study) (MUSM-HEL 1392)
Kalicephalus subulatus Molin, 1861
B. constrictor; adult; intestine; Loreto, San Martin (03°45′S, 73°15′W; 06°02′S, 76°58′W) (MUSM-HEL 2214) (Gómez & Sánchez, Reference Gómez and Sánchez2007).
B. constrictor; adult; intestine, San Martín (6°24′S, 76°30′W) (CPMP 216) (Present study).
Diaphanocephalus jacuruxi Alho, 1965
Dracaena guianensis; adult; intestine; Loreto (03°43′S, 73°14′W) (Col. PAS–FCB 659) (Tantaleán, Reference Tantaleán2016).
FAMILY PHYSALOPTERIDAE (RAILLIET, 1893) LEIPER, 1908
Physaloptera obtusissima Molin, 1860
K. pelviceps; adult; stomach; Ucayali (07°35′N, 73°45′W) (USNPC 84986) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Physaloptera retusa Rudolphi, 1819
A. ameiva; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93231) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Anolis punctatus; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93236) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Kentropyx altamazonicus; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93242) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
K. pelviceps; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93246) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Varzea bistriata; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93250) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Plica plica; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93253) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Plica umbra; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93255) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Stenocercus roseiventris; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93262) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Thecadactylus rapicauda; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93264) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Tupinambis teguixin; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93267) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Thecadactylus solimoensis; adult; stomach; Peruvian Amazon (MUSM-HEL 2135) (Jordán et al., Reference Jordán, Suárez and Sánchez2011).
Physaloptera sp.
D. guttulatum; larvae; stomach; Lima (MUSM 2314) (Ávila & Silva, Reference Ávila and Silva2010).
H. mabouia; larvae; intestine; San Martín (6°24′S, 76°30′W) (CPMP 214) (Present study).
B. constrictor; larvae; intestine, San Martín (6°24′S, 76°30′W) (CPMP 218) (Present study).
C. denticulatus; larvae; intestine, San Martín (6°24′S, 76°30′W) (CPMP 205) (Present study).
Physalopteridae gen. sp.
Ophidia gen. sp.; adult; stomach, San Martín (6°24′S, 76°30′W) (CPMP 222) (Present study).
Physalopteroides venancioi (Lent, Freitas & Proença, 1946)
Cercosaura ocellata; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93241) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Imantodes cenchoa; adult; stomach; Ucayali (07°35′N, 73°45′W) (USNPC 84986) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Kentropyx altamazonicus; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93243) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
K. pelviceps; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93247) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
V. bistriata; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93251) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
T. rapicauda; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93265) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
T. solimoensis; adult; stomach; Peruvian Amazon (MUSM-HEL 2136) (Jordán et al., Reference Jordán, Suárez and Sánchez2011).
T. teguixin; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93268) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005)
Xenoxybelis argenteus; adult; stomach; Ucayali (07°35′N, 73°45′W) (USNPC 84995) (McAllister et al., Reference McAllister, Bursey and Freed2010)
Thubunaea iguanae Telford, 1965
M. peruvianus; adult; stomach; Ica (MUSM-HEL 2187) (Pérez et al., Reference Pérez, Balta, Salizar and Sánchez2007).
Microlophus thoracicus thoracicus; adult; stomach; Ica (MUSM-HEL 2188) (Pérez et al., Reference Pérez, Balta, Salizar and Sánchez2007).
Thubunaea parkeri Baylis, 1926
D. heterolepis; adult, stomach; Ancash (10°05′S, 78°05′W) (USNPC 100639) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
D. heterolepis; adult, stomach; Ancash (MUSM-HEL 2303) (Present study).
FAMILY PHARYNGODONIDAE TRAVASSOS, 1920
Alaeuris caudatus Lent & Freitas, 1948
Iguana iguana; adult; intestine; Tumbes (Tantaleán, Reference Tantaleán1998).
Alaeuris sp.
I. iguana; adult; intestine; Piura (MUSM-HEL 272) (Present study).
Ozolaimus cirratus Linstow, 1906
I. iguana; adult; intestine; Lima (Arrojo, Reference Arrojo2002).
Ozolaimus megatyphlon (Rudolphi, 1819) Dujardin, 1845
I. iguana; adult; intestine; Piura (CHIOC 29993,) (unpublished data, CHIOC).
I. iguana; adult; intestine; Piura (MUSM-HEL 48) (Present study).
I. iguana; adult; intestine; Tumbes (MUSM-HEL 1365) (Present study).
I. iguana; adult; intestine; Tumbes (MUSM-HEL 1365) (Present study).
I. iguana; adult; intestine; Lima (Arrojo, Reference Arrojo2002).
Parapharyngodon arequipensis Calisaya & Cordova, Reference Calisaya and Cordova1997
M. peruvianus (type host); adult; intestine; Moquegua (type locality) (holotype, MUSM-HEL 1441; paratype, MUSM-HEL 1443) (Calisaya & Cordova, Reference Calisaya and Cordova1997).
D. heterolepis; adult; intestine; La Libertad (MUSM-HEL 2305) (Present study).
D. guttulatum; adult; intestine; Ancash (MUSM-HEL 2310) (Present study).
D. guttulatum; adult; intestine; Lima (MUSM-HEL 2313) (Present study).
D. guttulatum; adult; intestine; La Libertad (MUSM-HEL 2316, 2318) (Present study).
D. guttulatum; adult; intestine; Lambayeque (MUSM-HEL 2313, 2323, 2325) (Present study).
D. guttulatum; adult; intestine; Tumbes (MUSM-HEL 2328) (Present study).
Parapharyngodon lagitor Alho & Rodrigues, 1963
D. guttulatum; adult; intestine; Lambayeque (MUSM-HEL 2324) (Ávila & Silva, Reference Ávila and Silva2010).
Parapharyngodon moqueguensis Calisaya & Cordova, Reference Calisaya and Cordova1997
M. peruvianus (type host); adult; intestine; Moquegua (type locality) (holotype, MUSM-HEL 1444; Alotype, MUSM-HEL 1445; paratype, MUSM-HEL 1446) (Calisaya & Cordova, Reference Calisaya and Cordova1997).
D. guttulatum; adult; intestine; Tumbes (MUSM-HEL 2843) (Present study).
D. guttulatum; adult; intestine; Piura (MUSM-HEL 2847) (Present study).
Parapharyngodon scleratus Travassos, 1923
A. ameiva; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93230) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
K. pelviceps; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93245) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
K. pelviceps; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84985) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Copeoglossum nigropunctatum; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84987) (McAllister et al., Reference McAllister, Bursey and Freed2010).
V. bistriata; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93245) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
P. johnwrighti; adult; intestine; Cajamarca (USNPC 100810) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
T. solimoensis; adult; intestine; Peruvian Amazon (MUSM-HEL 2134) (Jordán et al., Reference Jordán, Suárez and Sánchez2011).
Parapharyngodon sp.
D. guttulatum; adult; intestine; Lambayeque (MUSM-HEL 2321, 2322) (Present study).
D. guttulatum; adult; intestine; Lima (MUSM-HEL 2331) (Present study).
D. guttulatum; adult; intestine; Tumbes (MUSM-HEL 2330, 2844) (Present study).
Parapharyngodon yurensis Calisaya & Cordova, Reference Calisaya and Cordova1997
M. peruvianus (type host); adult; intestine; Arequipa (type locality) (holotype, MUSM-HEL 1447; Alotype, MUSM-HEL 1448; paratype, MUSM-HEL 1449) (Calisaya & Cordova, Reference Calisaya and Cordova1997).
Pharyngodon sp.
H. mabouia; adult; intestine; San Martín (6°24′S, 76°30′W) (CPMP 213) (Present study).
Pharyngodon micrurus Freitas & Ibañez, Reference Freitas and Ibañez1963
D. guttulatum; adult; intestine; Lambayeque (06°09′S, 79°43′W) (USNPC 100635) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
D. guttulatum; adult; intestine; Ancash (MUSM-HEL 2309) (Present study).
D. guttulatum; adult; intestine; Lima (MUSM-HEL 2312) (Present study).
D. guttulatum; adult; intestine; La Libertad (MUSM-HEL 2315) (Present study).
D. guttulatum; adult; intestine; Lambayeque (MUSM-HEL 2326) (Present study).
D. guttulatum; adult; intestine; Loreto (MUSM-HEL 2759) (Present study).
D. guttulatum; adult; intestine; Piura (MUSM-HEL 2846) (Present study).
D. guttulatum; adult; intestine; Tumbes (MUSM-HEL 2329) (Present study).
D. heterolepis (type host); adult; intestine; La Libertad (type locality) (CHIOC 29180-29261) (Freitas & Ibañez, Reference Freitas and Ibañez1963).
D. heterolepis; adult; intestine; Ancash (10°05′S, 78°05′W) (USNPC 100638) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
D. heterolepis; adult; intestine; Ancash (MUSM-HEL 2302) (Present study).
Skrjabinodon dixoni Bursey & Goldberg Reference Bursey and Goldberg2007
Uracentron flaviceps (type host); adult; intestine; Loreto (type locality) (holotype, USNPC 98997; Allotype, USNPC 98998; paratype, USNPC 98999; MUSM-HEL 2756) (Bursey & Goldberg, Reference Bursey and Goldberg2007, Present study).
Thelandros capacyupanquii (Freitas, Vicente & Ibáñez, 1968)
Dicrodon holmbergi (type host); adult; intestine; La Libertad (type locality) (holotype, CHIOC 30303) (Freitas et al., Reference Freitas, Vicente and Ibañez1968a).
D. holmbergi; adult; intestine; La Libertad (08°31′S, 78°48′W) (USNPC 100640) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
D. holmbergi; adult; intestine; La Libertad (MUSM-HEL 2304) (Present study).
D. holmbergi; adult; intestine; La Libertad (MUSM-HEL 733) (Present study).
D. holmbergi; adult; intestine; Loreto (MUSM-HEL 2760) (Present study).
D. guttulatum; adult; intestine; Lambayeque (06°09′S, 79°43′W) (USNPC 100636) (Goldberg & Bursey, Reference Goldberg and Bursey2008).
D. guttulatum; adult; intestine; La Libertad (MUSM-HEL 2317) (Present study).
D. guttulatum; adult; intestine; Loreto (MUSM-HEL 2761) (Present study).
D. guttulatum; adult; intestine; Ancash (MUSM-HEL 2761) (Present study).
Note: This species was originally determined as Parathelandros capacyupanquii, but this species was transferred to Thelandros by Vicente et al. (Reference Vicente, Vrcibradis, Muniz-Pereira and Magalhaes2000).
Thelandros capacyupanquii (Freitas, Vicente & Ibáñez, 1968) Type A
D. guttulatum; adult; intestine; La Libertad (MUSM-HEL 2319) (Present study).
Thelandros capacyupanquii (Freitas, Vicente & Ibáñez, 1968) Type B
D. guttulatum; adult; intestine; Ancash (MUSM-HEL 2311) (Present study).
Thelandros capacyupanquii (Freitas, Vicente & Ibáñez, 1968) Type A and B
D. guttulatum; adult; intestine; Ancash (MUSM-HEL 2332) (Present study).
Spauligodon maytacapaci (Vicente & Ibáñez, 1968)
Leiocephalus sp. (type host); adult; intestine; Cajamarca (type locality) (holotype, CHIOC 30042; CHIOC 30111) (Vicente & Ibañez, Reference Vicente and Ibañez1968).
Note: The original determination of this material was Parathelandros maytacapaci, but this species was transferred to Spauligodon by Barus & Coy-Otero (Reference Barus and Coy-Otero1974).
Spauligodon oxkutzcabiensis Chitwood, 1938
T. rapicauda; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93266) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Phyllodactylus inaequalis; adult; intestine; Lambayeque (USNPC 100808) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
P. johnwrighti; adult; intestine; Cajamarca (USNPC 100811) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
Phyllodactylus microphyllus; adult; intestine; Ancash (USNPC 100813) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
Spauligodon sp.
H. mabouia; adult; intestine; San Martín (6°24′S, 76°30′W) (CPMP 212) (Present study).
Spauligodon viracochai (Freitas, Vicente & Ibáñez, 1968)
Phyllodactylus angustidigitus; adult; stomach; Ica (MUSM-HEL 2300) (Pérez et al., Reference Pérez, Balta, Salizar and Sánchez2007).
Phyllodactylus gerrhopygus (type host); adult; intestine; La Libertad (type locality) (holotype, CHIOC 30315) (Freitas et al., Reference Freitas, Vicente and Ibañez1968b).
P. gerrhopygus; adult; intestine; Lima (MUSM-HEL 1366) (Present study).
Note: This species was originally described as Parathelandros viracochai, but this species was transferred to Spauligodon by Barus & Coy-Otero (Reference Barus and Coy-Otero1974).
Thelandros bulbosus Linstow, 1899
M. peruvianus; adult; intestine; Arequipa (Sarmiento et al., Reference Sarmiento, Tantaleán and Huiza1999)
FAMILY COSMOCERCIDAE TRAVASSOS, 1925
Aplectana sp.
Cercosaura argulus; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84991) (McAllister et al., Reference McAllister, Bursey and Freed2010).
FAMILY HETERAKIDAE RAILLIET & HENRY, 1912
Spinicauda sp.
A. ameiva; adult; intestine; Madre de Dios (Sarmiento et al., Reference Sarmiento, Tantaleán and Huiza1999).
D. guttulatum; adult; intestine; Piura (MUSM-HEL 293) (Present study).
Spinicauda spinicauda (Olfers in Rudolphi, 1819) Travassos, 1923
A. ameiva; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93232) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Enyalioides laticeps; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84983) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Strongyluris oscari Travassos, 1923
Anolis fuscoauratus; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93233) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
A. punctatus; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93240) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Anolis trachyderma; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84982) (McAllister et al., Reference McAllister, Bursey and Freed2010).
I. cenchoa; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84994) (McAllister et al., Reference McAllister, Bursey and Freed2010).
P. plica; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93254) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
P. umbra; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93257) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
S. roseiventris; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93257) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY KATHLANIIDAE CARRIL, 1914
Cruzia rudolphi Ruiz, 1947
D. catesbyi; adult; rectum; Ucayali (07°35′N, 73°45′W) (USNPC 84992) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Falcaustra belemensis Baker & Bain, 1981
Potamites ecpleopus; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84990) (McAllister et al., Reference McAllister, Bursey and Freed2010).
FAMILY MOLINEIDAE DURETTE-DESSERT & CHABAUD, 1977
Kentropyxia sauria Baker, 1982
K. pelviceps; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84984) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Oswaldocruzia brasiliensis Lent & Freitas, 1935
C. nigropunctatum; adult; intestine; Ucayali (07°35′N, 73°45′W) (USNPC 84989) (McAllister et al., Reference McAllister, Bursey and Freed2010).
Oswaldocruzia peruensis Ben-Slimane et al., Reference Ben-Slimane, Verhaagh and Durette-Desset1995
S. roseiventris (type host); adult; rectum; Huánuco (type locality) (09°37′S, 74°56′W) (holotype and Allotype, MNHN 758; paratypes, MNHN 758; paratypes, SMNK 172) (Ben-Slimane et al., Reference Ben-Slimane, Verhaagh and Durette-Desset1995).
S. roseiventris; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93260) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
A. punctatus; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93235) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Oswaldocruzia sp.
H. mabouia; adult; intestine; San Martín (6°24′S, 76°30′W) (CPMP 215) (Present study).
Oswaldocruzia vitti Bursey & Goldberg, 2004
Cercosaura eigenmanni; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93259) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY ONCHOCERCIDAE CHABAUD & ANDERSON, 1959
Oswaldofilaria azevedoi Bain, 1974
S. roseiventris; adult; body cavity; Madre de Dios (12°35′S, 69°05′W) (USNPC 93261) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Piratuba digiticauda Lent & Freitas, 1941
P. umbra; adult; body cavity; Madre de Dios (12°35′S, 69°05′W) (USNPC 93256) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Piratuba lainsoni Bain, 1974
A. punctatus; adult; body cavity; Madre de Dios (12°35′S, 69°05′W) (USNPC 93237) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Piratuboides zeae (Bain, 1974) Bain & Sulahian, 1974
V. bistriata; adult; body cavity; Madre de Dios (12°35′S, 69°05′W) (USNPC 93252) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
C. nigropunctatum; adult; body cavity; Ucayali (07°35′N, 73°45′W) (USNPC 84988) (McAllister et al., Reference McAllister, Bursey and Freed2010).
FAMILIA ACUARIIDAE RAILLIET, HENRY & SISOFF, 1912
Acuariidae gen. sp.
Phyllodactylus lepidopygus; larva; intestine; Lima (USNPC 100812) (Goldberg & Bursey, Reference Goldberg and Bursey2010).
FAMILY ATRACTIDAE RAILLIET, 1917
Cyrtosomum longicaudatum Brenes & Bravo Hollis, 1960
A. punctatus; adult; intestine; Madre de Dios (12°35′S, 69°05′W) (USNPC 93234) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY RHABDIASIDAE RAILLIET, 1916
Rhabdias anolis Bursey, Goldberg & Telford, 2003
A. punctatus; adult, lungs; Madre de Dios (12°35′S, 69°05′W) (USNPC 93238) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Serpentirhadias sp.
B. atrox; adult; lungs; Amazonas (Tantaleán & Gónzalo, Reference Tantaleán and Gónzalo1985).
Serpentirhabdias filicaudalis (Barella, dos Santos & da Silva, 2009)
Spilotes pullatus; adult, lungs; San Martin (6°24′S, 76°30′W) (CPMP 220, 221) (Present study).
FAMILY SEURATIDAE HALL, 1916
Skrjabinelazia intermedia (Freitas, 1940) Chabaud, 1973
A. punctatus; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93239) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY TRICHURIDAE RESCATE, 1911
Amphibiocapillaria freitasilenti (Araujo & Gandra, 1941) Moravec, 1986
A. ameiva; adult; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93229) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY ASCARIDIDAE BAIRD, 1853
Angusticaecum brevispiculum Chapin, 1925
C. denticulatus; adult; intestine; Ucayali (MUSM-HEL 747) (Salizar & Sánchez, Reference Salizar and Sánchez2007).
C. denticulatus; adult; intestine; Loreto (MUSM-HEL 356, 490) (Salizar & Sánchez, Reference Salizar and Sánchez2007).
C. denticulatus; adult; intestine; San Martin (CPMP 2003) (Present study).
Angusticaecum holopterum Chapin, 1924
C. denticulatus; adult; intestine; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3049) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
Angusticaecum sp.
C. denticulatus; adult; intestine; Loreto (MUSM-HEL 1358) (Tantaleán et al., Reference Tantaleán, Juárez and Cruz1983).
Dujardinascaris sp.
K. pelviceps; larva; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93248) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
T. teguixin; larva; stomach; Madre de Dios (12°35′S, 69°05′W) (USNPC 93269) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
Ophidascaris arndti Sprehn, 1929
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3050) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
Ophidascaris sp.
C. denticulatus; adult; intestine; Ucayali (MUSM-HEL 14) (Present study).
FAMILY DIPLOTRIAENOIDEA ANDERSON, 1958
Hastospiculum onchocercum Chitwood, 1932
L. muta; adult; lungs; Amazonas (Tantaleán & Gónzalo, Reference Tantaleán and Gónzalo1992).
L. muta; adult; lungs; Loreto (MUSM-HEL 1391) (Tantaleán & Gónzalo, Reference Tantaleán and Gónzalo1992).
Hastospiculum sp.
P. umbra; larva; coelom, under peritoneum; Madre de Dios (12°35′S, 69°05′W) (USNPC 93258) (Bursey et al., Reference Bursey, Goldberg and Parmelee2005).
FAMILY CAMALLANIDAE RAILLIET & HEORY, 1915
Procamallanus (Procamallanus) sp.
B. constrictor; adult; intestine, San Martín (6°24′S, 76°30′W) (CPMP 217) (Present study).
Serpinema amazonicus (Ribeiro, 1941) Yeh, 1960
P. expansa; adult; intestine; Loreto (Tantaleán, Reference Tantaleán1998).
P. unifilis; adult; intestine; Loreto (Sánchez et al., Reference Sánchez, Tantaleán, Vela and Méndez2006).
Podocnemis sp.; adult; intestine; Loreto (MUSM-HEL 79) (Present study).
Podocnemis sp.; adult; intestine; Ucayali (MUSM-HEL 309) (Present study).
FAMILY GNATHOSTOMATIDAE RAILLIET, 1895
Ancyracanthus pinnatifidus Diesing, 1839
P. unifilis; adult; intestine; Loreto (Sánchez et al., Reference Sánchez, Tantaleán, Vela and Méndez2006)
FAMILY ATRACTIDAE TRAVASSOS, 1919
Atractis impura Caballero, 1944
C. denticulatus; adult; intestine; Loreto, Ucayali (MUSM-HEL 34, 1038) (Salizar & Sánchez, Reference Salizar and Sánchez2007)
Atractis marquezi Bursey & Flanagan, 2002
C. denticulatus; adult; intestine; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3045) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
P. unifilis; adult; intestine; Pasco (MUSM-HEL 3673) (Present study).
Phrynops geoffroanus; adult; intestine; Pasco (MUSM-HEL 3680) (Present study).
Mesoclemmys gibba; adult; intestine; Pasco (MUSM-HEL 3683) (Present study).
Atractis trematophila Travassos 1934
P. unifilis; adult; intestine; Pasco (MUSM-HEL 3674) (Present study).
M. gibba; adult; intestine; Pasco (MUSM-HEL 3684) (Present study).
Klossinemella conciliatus Alho, 1964
P. unifilis; adult; stomach; Loreto (MUSM-HEL 564) (Salizar & Sánchez, Reference Salizar and Sánchez2007).
Klossinemella travassosi Costa, 1961
C. denticulatus; adult; intestine; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3046) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine; Loreto (MUSM-HEL 3046) (Present study).
P. unifilis; adult; intestine; Pasco (MUSM-HEL 3677) (Present study).
Labiduris gulosa Rudolphi, 1819
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3042) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine, San Martín (6°24′S, 76°30′W) (CPMP 206) (Present study).
C. denticulatus; adult; intestine, stomach; Ucayali (03°77′S, 73°27′W) (MUSM-HEL 25, 35) (Present study).
Labiduris zschokkei Linstow 1899
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3043) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine, stomach; Ucayali (03°77′S, 73°27′W) (MUSM-HEL 24, 36) (Present study).
Labiduris irineuta Costa, 1961
C. denticulatus; adult; intestine, stomach; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3044) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
Paratractis hystrix (Diesing, Reference Diesing1851) Sarmiento, Reference Sarmiento1959
P. dumerilianus; adult; intestine; Ucayali (Syntype, USNM 1338611) (Sarmiento, Reference Sarmiento1959).
Podocnemis sp.; adult; intestine, stomach; Loreto (MUSM-HEL 78) (Present study).
P. unifilis; adult; intestine; Loreto (MUSM-HEL 562) (Present study).
Note: The original determination of this material was Ascaris hystrix Diesing, 1851 (Diesing, Reference Diesing1851). Later was transferred to Atractis by Von Drasche (Reference Von Drasche1883). Finally, was transferred to genus Paratractis by Sarmiento et al. (Reference Sarmiento1959).
Paraorientatractis semiannulata Gibbons, Khalil & Marinkelle, 1997
P. unifilis; adult; intestine; Ucayali (MUSM-HEL 2685) (Salizar & Sánchez, Reference Salizar and Sánchez2007).
P. unifilis; adult; intestine; Pasco (MUSM-HEL 3672) (Present study).
P. geoffroanus; adult; intestine; Pasco (MUSM-HEL 3681) (Present study).
M. gibba; adult; intestine; Pasco (MUSM-HEL 3682) (Present study).
FAMILY STRONGYLIDAE BAIRD, 1853
Chapiniella variabilis Chapin, 1924
C. denticulatus; adult; intestine, stomach; Loreto (Tantaleán et al., Reference Tantaleán, Juárez and Cruz1983).
C. denticulatus; adult; intestine; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3048) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
C. denticulatus; adult; intestine; San Martin (6°24′S, 76°30′W) (CPMP 204) (Present study).
C. denticulatus; adult; intestine; Ucayali (MUSM-HEL 1372) (Present study).
Sauricola sauricola Chapin, 1924
C. denticulatus; adult; intestine; Loreto (03°77′S, 73°27′W) (MUSM-HEL 3047) (Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014).
Sauricola sp.
C. denticulatus; adult; intestine, stomach; Ucayali (03°77′S, 73°27′W) (MUSM-HEL 37) (Present study).
PHYLUM ACANTHOCEPHALA KOHLREUTHER, 1771
CLASS PALAEACANTHOCEPHALA MEYER, 1931
ORDER POLYMORPHIDA PETROCHENKO, 1956
FAMILY CENTRORHYNCHIDAE VAN CLEAVE, 1916
Centrorhynchus sp.
S. pullatus; larvae; intestine; San Martin (6°24′S, 76°30′W) (CPMP 219) (Present study).
Chironius scurrulus; larvae; intestine; San Martin (6°24′S, 76°30′W) (CPMP 223) (Present study).
Host–parasite list
ORDER SQUAMATA OPPEL, 1811
SUBORDER OPHIDIA LATREILLE, 1804
FAMILY BOIDAE GRAY, 1825
Boa constrictor Linnaeus
Trematoda: Crepidobothrium gerrardii; Cestoda: Ophiotaenia sp.; Nematoda: Kalicephalus subulatus, Physaloptera sp., Procamallanus (Procamallanus) sp.
FAMILY COLUBRIDAE OPPEL, 1811
Chironius sp.
Trematoda: Renifer heterocoelium.
Chironius scurrulus (Wagler)
Acanthocephala: Centrorhynchus sp.
Dipsas catesbyi (Sentzen)
Trematoda: Mesocoelium sp.; Nematoda: Cruzia rudolphi.
Imantodes cenchoa (Linnaeus)
Nematoda: Physalopteroides venancioi, Strongyluris oscari.
Philodryas argentea (Daudin)
Nematoda: P. venancioi.
Spilotes pullatus (Linnaeus)
Nematoda: Serpentirhabdias filicaudalis; Acanthocephala: Centrorhynchus sp.
Xenodon sp.
Nematoda: Kalicephalus sp.
FAMILY DIPSADIDAE BONAPARTE 1838
Atractus major Boulenger
Trematoda: Glossidiella peruensis.
FAMILY VIPERIDAE OPPEL, 1811
Bothrops atrox (Linnaeus)
Nematoda: Kalicephalus inermis, Kalicephalus sp., Serpentirhadias sp.
Lachesis muta (Linnaeus)
Nematoda: Hastospiculum onchocercum, Kalicephalus inermis.
SUBORDER SAURIA MACARTNEY, 1802
FAMILY DACTYLOIDAE FITZINGER, 1843
Anolis fuscoauratus D'Orbigny
Nematoda: S. oscari.
Anolis punctatus Daudin
Nematoda: Cyrtosomum longicaudatum, O. peruensis, Physaloptera retusa, Piratuba lainsoni, Rhabdias anolis, Skrjabinelazia intermedia, S. oscari.
Anolis trachyderma Cope
Nematoda: S. oscari.
FAMILY GEKKONIDAE GRAY, 1825
Hemidactylus mabouia (Moreau de Jonnès)
Trematoda: Paradistomum sp1., Paradistomum sp2.; Cestoda: Oochoristica vanzolinii; Nematoda: Oswaldocruzia sp., Pharyngodon sp., Physaloptera sp., Spauligodon sp.
FAMILY GYMNOPHTHALMIDAE FITZINGER, 1826
Cercosaura argulus Peters
Nematoda: Aplectana sp.
Cercosaura eigenmanni (Griffin)
Nematoda: Oswaldocruzia vitti.
Cercosaura ocellata Wagler
Nematoda: P. venancioi.
Potamites ecpleopus (Cope)
Nematoda: Falcaustra belemensis.
FAMILY HOPLOCERCIDAE FROST & ETHERIDGE, 1989
Enyalioides laticeps (Guichenot)
Nematoda: Spinicauda spinicauda.
FAMILY IGUANIDAE OPPEL, 1811
Iguana iguana (Linnaeus)
Nematoda: Alaeuris caudatus, Alaeuris sp., Ozolaimus cirratus, Ozolaimus megatyphlon.
FAMILY LEIOCEPHALIDAE FROST & ETHERIDGE, 1989
Leiocephalus sp.
Cestoda: Oochoristica travassosi; Nematoda: Spauligodon maytacapaci, Thelandros bulbosus, Thubunaea iguana.
FAMILY PHYLLODACTYLIDAE GAMBLE, BAUER, GREENBAUM & JACKMAN, 2008
Phyllodactylus angustidigitus Dixon & Huey
Nematoda: Spauligodon viracochai.
Phyllodactylus gerrhopygus (Wiegmann)
Nematoda: Spauligodon viracochai.
Phyllodactylus inaequalis Cope
Nematoda: Spauligodon oxkutzcabiensis.
Phyllodactylus johnwrighti Dixon & Huey
Cestoda: Oochoristica travassosi; Nematoda: Parapharyngodon scleratus, Spauligodon oxkutzcabiensis.
Phyllodactylus lepidopygus (Tschudi)
Nematoda: Acuariidae gen. sp.
Phyllodactylus microphyllus Cope
Nematoda: Spauligodon oxkutzcabiensis.
Thecadactylus rapicauda (Houttuyn)
Nematoda: Physaloptera retusa, P. venancioi, Spauligodon oxkutzcabiensis.
Thecadactylus solimoensis Bergmann & Russell
Nematoda: Parapharyngodon scleratus, Physaloptera retusa, P. venancioi.
FAMILY SCINCIDAE GRAY, 1825
Copeoglossum nigropunctatum (Spix)
Nematoda: Piratuboides zeae, Oswaldocruzia brasiliensis, Parapharyngodon scleratus.
Varzea bistriata (Spix)
Nematoda: Oswaldocruzia brasiliensis, Parapharyngodon scleratus, Physaloptera retusa, P. venancioi, Piratuboides zeae.
FAMILY TEIIDAE GRAY, 1827
Ameiva ameiva (Linnaeus)
Cestoda: Oochoristica ameivae; Nematoda: Amphibiocapillaria freitasilenti, Parapharyngodon scleratus, Physaloptera retusa, Spinicauda sp., Spinicauda spinicauda.
Dracaena guianensis Daudin
Nematoda: Diaphanocephalus jacuruxi.
Dicrodon guttulatum Duméril & Bibron
Cestoda: Oochoristica freitasi, Oochoristica iguanae, Oochoristica sp.; Nematoda: Parapharyngodon arequipensis, Parapharyngodon lagitor, Parapharyngodon moqueguensis, Parapharyngodon sp., Pharyngodon micrurus, Physaloptera sp., Spinicauda sp., Thelandros capacyupanquii, Thelandros capacyupanquii Type A, Thelandros capacyupanquii Type B, Thelandros capacyupanquii Type A and B.
Dicrodon heterolepis (Tschudi)
Cestoda: Oochoristica freitasi; Nematoda: Parapharyngodon arequipensis, Pharyngodon micrurus, Thubunaea parkeri.
Dicrodon holmbergi Schmidt
Nematoda: Thelandros capacyupanquii.
Kentropyx altamazonica (Cope)
Nematoda: Physaloptera retusa, P. venancioi.
Kentropyx pelviceps (Cope)
Cestoda: Ophiotaenia flava; Nematoda: Dujardinascaris sp., Kentropyxia sauria, Parapharyngodon scleratus, Physaloptera obtusíssima, Physaloptera retusa, P. venancioi.
Tupinambis teguixin (Linnaeus)
Nematoda: Dujardinascaris sp., Physaloptera retusa, P. venancioi.
FAMILY TROPIDURIDAE BELL, 1843
Microlophus peruvianus (Lesson)
Cestoda: Oochoristica sp.; Nematoda: Parapharyngodon arequipensis, Parapharyngodon moqueguensis, Parapharyngodon yurensis.
Microlophus thoracicus thoracicus (Tschudi)
Nematoda: Thubunaea iguanae.
Plica plica (Linnaeus)
Nematoda: Physaloptera retusa, S. oscari.
Plica umbra (Linnaeus)
Nematoda: Hastospiculum sp., Physaloptera retusa, Piratuba digiticauda, S. oscari.
Stenocercus roseiventris D'Orbigny in Duméril & Bibron
Nematoda: Oswaldocruzia peruensis, Oswaldofilaria azevedoi, Physaloptera retusa, S. oscari.
Uracentron flaviceps (Guichenot)
Nematoda: Skrjabinodon dixoni.
ORDER TESTUDINES BATSCH, 1788
FAMILY CHELIDAE GRAY 1825
Chelus fimbriata (Schneider)
Trematoda: Atamatam amazoniensis, Paratamatam iquitosiensis.
Mesoclemmys gibba (Schweigger)
Nematoda: Atractis marquezi, Atractis trematophila, Paraorientatractis semiannulata.
FAMILY CHELONIIDAE OPPEL, 1811
Chelonia mydas agassizi Bocourt
Trematoda: Adenogaster serialis, Cricocephalus albus, Orchidasma amphiorchis.
FAMILY PODOCNEMIDIDAE COPE, 1888
Peltocephalus dumerilianus (Schweigger)
Trematoda: Nematophila grandis; Nematoda: P. hystrix.
Podocnemis expansa (Schweigger)
Trematoda: Halltrema avitellina, N. grandis; Nematoda: Podocnemitrema papillosus, Serpinema amazonicus.
Podocnemis sp.
Nematoda: P. hystrix, S. amazonicus.
Podocnemis unifilis Troschel
Trematoda: H. avitellina, Halltrema heteroxenum, N. grandis, P. papillosus, Telorchis hagmanni; Nematoda: Ancyracanthus pinnatifidus, A. trematophila, P. hystrix, P. semiannulata, S. amazonicus.
Podocnemis sextuberculata Cornalia
Trematoda: Pitiutrema revelae.
FAMILY TESTUDINIDAE GRAY, 1825
Chelonoidis denticulatus (Linnaeus)
Trematoda: Helicotrema spirale, H. avitellina, N. grandis; Nematoda: Angusticaecum brevispiculum, Angusticaecum holopterum, Angusticaecum sp., Atractis impura, A. marquezi, Chapiniella variabilis, Klossinemella conciliatus, Klossinemella travassosi, Labiduris gulosa, Labiduris zschokkei, Labiduris irineuta, Ophidascaris arndti, Ophidascaris sp., Physaloptera sp., Sauricola sauricola.
Discussion
The checklist presented here includes 82 nominal species and 24 taxa identified at the generic level of helminths associated with 55 reptile host species from Peru. They come from 18 of the 25 official Peruvian regions. Most of the parasitological studies were carried out in the Peruvian Amazon, with 145 reports, followed by the Peruvian Coast and the Andes Mountains with 64 and 15 reports, respectively. In seven Peruvian regions (Apurimac, Ayacucho, Callao, Huancavelica, Junín, Puno and Tacna), no parasitological studies have been carried out in reptiles, which indicates evident under-registration compared to the diversity of reptile helminths existing in other geographical regions with similar characteristics.
The phylum Nematoda contributes the highest proportion (79/106) of parasitic helminths of reptiles in Peru. Lower proportion of trematodes (17/106) and cestodes (9/106) have been recorded. The acanthocephalans are the least frequent group, with only one species (1/106) recovered. The lower numbers of trematode, cestode and acanthocephalan species registered in reptiles from Peru could be related to the low number of helminthologists studying parasites of this group of hosts. The highest number of taxa of helminths (22/106) is recorded in the family Pharyngodonidae with 18 nominal species and four taxa identified at the generic level. The nematode Pharyngodon micrurus Freitas & Ibañez, Reference Freitas and Ibañez1963 was the first helminth species described from reptiles in Peru and was found in the intestine of the desert tegu D. heterolepis (Tschudi) in La Libertad (Freitas & Ibañez, Reference Freitas and Ibañez1963). Since then, 15 new species of helminths (three trematodes, two cestodes and nine nematodes) have been described infecting reptiles from Peru with Glossidiella peruensis Huancachoque et al., Reference Huancachoque, Sáez, Cruces, Mendoza, Luque and Chero2020 being the most recent species described (Huancachoque et al., Reference Huancachoque, Sáez, Cruces, Mendoza, Luque and Chero2020).
A little more than 10% of reptile species, not necessarily the most abundant, currently inhabiting Peru (55/524 species) have a record of parasitism by helminths, representing a small proportion considering the great variety of reptiles that inhabit the various tropical and subtropical geographical areas of Peru (Koch et al., Reference Koch, Venegas, Santa Cruz and Böhme2018). The families of reptiles found harbouring the highest number of reported taxa are Teiidae, Testudinidae and Podocnemidae with 24, 18 and 14 taxa, respectively. The reptile species with the highest number of taxa of helminths reported are C. denticulatus with 18 species (three trematodes and 15 nematodes), followed by D. guttulatum with 11 species (three cestodes and eight nematodes) and P. unifilis with 10 species (five trematodes and five nematodes). The helminths associated with C. denticulatus have rarely been studied (Tantaleán et al., Reference Tantaleán, Juárez and Cruz1983; Salizar & Sánchez, Reference Salizar and Sánchez2007; Tantaleán & Forlong, Reference Tantaleán and Forlong2013; Julca et al., Reference Julca, Casas, Chavera, Sánchez, Sánchez and Batalla2014). Despite this, C. denticulatus is considered the host that harbours the highest number of helminth species reported in Peru. The yellow-footed tortoise, or C. denticulatus, is a terrestrial species that inhabits a great diversity of environments (Carvajal-Campos & Rodríguez-Guerra, Reference Carvajal-Campos and Rodríguez-Guerra2019). This could explain its great variety of helminths, principally those with direct life cycles. The yellow-spotted Amazon River turtle, P. unifilis is also a species that lives in a wide variety of habitats, such as rivers and lakes (Cisneros-Heredia, Reference Cisneros-Heredia2006). However, its helminth parasites have been poorly studied (Salizar & Sánchez, Reference Salizar and Sánchez2004; Sánchez et al., Reference Sánchez, Tantaleán, Vela and Méndez2006; Salizar & Sánchez, Reference Salizar and Sánchez2007; Tantaleán et al., Reference Tantaleán, Sánchez and Pineda Catalan2011; Tantaleán & Forlong, Reference Tantaleán and Forlong2013). Considering the high diversity of reptile hosts in Peruvian territory with very diverse regions and microclimates, it is possible that a significant number of new species may emerge in future parasitological studies.
On the other hand, 24 of the 106 registered helminth specimens have not been identified up to the specific epithet, either due to the lack of specialists or the lack of a more detailed review of the existing scientific collections of helminths. Pollution, anthropization and degradation of habitats threaten the ecosystems where reptiles live, increasing the chances of breaking the usual parasite–host balance and parasitic diversity regulated by external factors in nature, with potentially detrimental outcomes to the health of the reptile hosts (Peres & Nascimento, Reference Peres and Nascimento2006). This is a compilation report of the parasitic helminths observed in reptiles of Peru and serves as a basis for future studies on the diversity, ecology and parasitism of wild animals.
Acknowledgement
We thank Mr. Guy Emmet Fulkerson for reading the manuscript and editing the language.
Funding
Jhon D. Chero and Celso L. Cruces were supported by a student fellowship from the Coordenação de Aperfeiçoamento de Pessoal do Ensino Superior, Brazil (CAPES) – Finance Code 001. José L. Luque were supported by Researcher fellowships from the Conselho Nacional de Desenvolvimento Científico e Tecnológico, Brazil (CNPq).
Conflicts of interest
None.
Ethical standards
The authors declare that all applicable international, national and/or institutional guidelines for the care and use of animals were followed.