Taxonomía y sistemática

 

A new species of Mathevotaenia (Cestoda, Anoplocephalidae) parasitizing Tropidurus spinulosus (Reptilia, Squamata) from northeastern Argentina

 

Una especie nueva de Mathevotaenia (Cestoda, Anoplocephalidae) parásita de Tropidurus spinulosus (Reptilia, Squamata) del noreste de Argentina

 

Lía Inés Lunaschi^1*, Matías Fernando Lamas² and Fabiana Beatriz Drago¹

 

¹ Laboratorio de Helmintología, División Zoología Invertebrados, Museo de La Plata, Paseo del Bosque S/N°, 1900 La Plata, Buenos Aires, Argentina. *lunaschi@fcnym.unlp.edu.ar

² Laboratorio de Herpetología. Facultad de Ciencias Exactas y Naturales y Agrimensura. Universidad Nacional del Nordeste. Av. Libertad 5470, 3400 Corrientes, Argentina.

 

Recibido: 29 septiembre 2011.
Aceptado: 14 marzo 2012.

 

Abstract

Mathevotaenia chaquensis n. sp. (Cestoda, Anoplocephalidae, Linstowiinae) from a Spiny Lava Lizard, Tropidurus spinulosus, collected in Chaco Province, Argentina, is described. This is the second species of Mathevotaenia described from Neotropical reptiles. The new species is mainly characterized by having a relatively small strobila, 24 mm in total length, with about 100 craspedote proglottids, and 19–24 testes per proglottid. Among the South American species of Mathevotaenia, M. argentinensis is most similar to the new species by having similar body length and number of testes, but the major differences between both species include the size of suckers, neck, proglottids, testes and egg capsules, and the shape of the genital atrium and ovary (with 10–13 lobules on each side in M. argentinensis,, and 4–7 lobules in M. chaquensis n. sp.). A key to the species of the South American members of the Mathevotaenia Akumyan, 1946 is presented.

Key words: Mathevotaenia chaquensis n. sp., Linstowiinae, Spiny Lava Lizard, Tropiduridae, Chaco Province.

 

Resumen

Mathevotaenia chaquensis n. sp. (Cestoda, Anoplocephalidae, Linstowiinae) es descrita parasitando al lagarto de los quebrachales, Tropidurus spinulosus, procedente de la Provincia del Chaco, Argentina. Esta es la segunda especie de Mathevotaenia descrita parasitando reptiles Neotropicales. La nueva especie está caracterizada principalmente por tener un estróbilo relativamente pequeño, 24 mm de largo, con aproximadamente 100 proglótides craspedotas y 19–24 testículos por proglótide. Entre las especies sudamericanas de Mathevotaenia, M. argentinensis es la más semejante a la nueva especie por presentar similar longitud del cuerpo y número de testículos, pero difieren en el tamaño de las ventosas, cuello, proglótides, testículos y huevos. Además difieren en la forma del atrio genital y del ovario (10–13 lóbulos a cada lado enM. argentinensis vs. 4–7 lóbulos en M. chaquensis n. sp.). Se presenta una clave para la determinación de las especies sudamericanas de Mathevotaenia Akumyan, 1946.

Palabras clave: Mathevotaenia chaquensis n. sp., Linstowiinae, lagarto de los quebrachales, Tropiduridae, Provincia del Chaco.

 

Introduction

The Spiny Lava Lizard, Tropidurus spinulosus (Cope), is a tropidurid that is distributed from Brazil, Bolivia and Paraguay to central Argentina. It feeds mainly on insects Formicidae and Acrididae (Martori and Aun 1994). The helminth fauna of Spiny Lava Lizard is poorly known and the only record of helminths parasitizing it is that of Strongyluris oscari Travassos, 1923 (Nematoda–Heterakidae) (Sutton et al., 1998; ávila and Silva, 2010). During a helminthological study of lizards from Chaco Province, Argentina, one species of anoplocephalid cestode belonging to Mathevotaenia Akumyan, 1946, was collected from the small intestine of T. spinulosus; the aim of the present paper is to describe this new species.

The genus Mathevotaenia includes species that have been found parasitizing mainly mammals throughout the world (rodents, insectivores, edentates, carnivores, marsupials, bats, and primates), with isolated reports in reptiles and birds (Beveridge, 2008; Bursey et al., 2010; Goldberg et al., 2010). Also, Lamom and Greer (1986) reported one case of human infection by Mathevotaenia sp. in Bangkok, Thailand. According to Spasskii (1951) the life cycles of the species of Mathevotaenia involve insects, such as cockroaches and butterflies, as intermediate hosts in which amphicyst develop. Chervy (2002) analyzed the terminology applied to larval cestodes or metacestodes and considered that larvacyst of amphicyst type is a synonymous of precysticercus.

 

Materials and methods

Eleven specimens of Tropidurus spinulosus were collected between May 2005 and February 2010 during a survey of lizards in Pampa del Indio (26°16'33" S, 59°58' W), Chaco Province, Argentina. The lizards were dissected, the viscera fixed in 10% formalin and examined for helminths in the laboratory. One complete cestode specimen was collected, stained with hydrochloric carmine, dehydrated and mounted in Canada balsam. Measurements are given in micrometers (nm) unless otherwise stated, presented as the range. Drawings were made with the aid of a drawing tube. The hosts were deposited in the Herpetological Collection of the Universidad Nacional del Nordeste (UNNE), Corrientes Province, Argentina, and the parasite studied in the Helminthological collection of the Museo de La Plata (MLP), La Plata, Argentina.

The abbreviations of the measured features are as follows: Cpl – cirrus pouch length; Cpw – cirrus pouch width; Ecl – egg capsules length; Ecw – egg capsules width; Gad – genital atrium depth; Gaw – genital atrium width; Gpl – gravid proglottids length; Gpw – gravid proglottids width; Mpl – mature proglottids length; Mpw – mature proglottids width; Mw – maximum width; Nl – neck length; Nw – neck width; N° p – number of proglottids; N° te – number of testes; Onl – oncosphere length; Onw –oncosphere width; Onhl – oncospheral hooks length; Ovl – ovary length; Ovw – ovary width; Sl – scolex length; Sw – scolex width; Sul – suckers length; Suw – suckers width; Tgpl – terminal gravid proglottids length; Tgpw – terminal gravid proglottids width; Tel – testes length; Tew – testes width; Tl – total length; Vgl – vitelline gland length; Vgw – vitelline gland width.

 

Description

Family Anoplocephalidae Kholodkovskii, 1902

Subfamily Linstowiinae Fuhrmann, 1907

Mathevotaenia chaquensis n. sp. (Figs. 1–5; Table 1)

Diagnosis. Relatively small tapeworm. Scolex unarmed, poorly demarcated from strobila. Suckers oval with poorly muscular walls, each sucker inside a pocket that opens externally at most anterior part of structure through a slit. Neck long. Strobila apolytic with about 100 craspedote proglottids; velum up to 97 long. Immature proglottids protandric, wider than long. Mature proglottids wider than long, around 11; length–width ratio 1: 2–2.8. Gravid proglottids about 28 in number, wider than long; length–width ratio 1:0.5–1: 0.8; last 2 gravid proglottids longer than wide; length–width ratio 1:1.3–1:1.4. Developing genitalia first visible in 43th proglottid. Genital pores alternate irregularly, near the anterior margin of proglottid. Genital atrium small, surrounded by radially directed muscle fibres. Cirrus pouch slender, transversely elongated, extends beyond excretory canals, not reaching midline of proglottids; internal vas deferens coiled within cirrus–sac; cirrus without visible spines. Testes clearly visible in proglottid 52 arranged in single intervascular field, posterior and lateral to vitelline gland, reaching posterior margin of ovary. Ovary in medial portion of proglottid, bilobed, with transverse isthmus; ovarian lobes with 4–7 short lateral lobules. Lobes of ovary not quite reaching lateral excretory canals. Vitelline gland medial, posterior to ovarian isthmus, compact appearance or with variable number of small rounded lobules. Seminal receptacle absent. Vagina posterior to cirrus pouch. Female genitalia and testes involute progressively in gravid proglottids, cirrus pouch, duct with spermatozoids and vagina persist in last 3 proglottids. Eggs in egg capsules scattered in parenchyma, occupying most of proglottid. Oncospheral hooks 15–18 long; hook blade 5–7 long; hook base 10–11 long.

Taxonomic summary

Type host: Tropidurus spinulosus (Cope), Spiny Lava Lizard (Reptilia, Squamata)

Type locality: Pampa del Indio (26°16'33" S, 59°58' W), Libertador General San Martín, Chaco Province, Argentina.

Site of infection: small intestine.

Date of collection: December 2005.

Prevalence: 9% (1 of 11).

Type specimen: holotype MLP 6505.

Etymology: the species name refers to Chaco Province (chaquensis= of Chaco), the locality in which it was found.

Remarks

The genus Mathevotaenia contains an uncertain number of species due to complex synonymies and because descriptions of some species are too poor to determine correct generic assignment (Beveridge, 2008; Bursey et al., 2010).

In South America, 15 species of this genus have been reported parasitizing marsupials, armadillos, monkeys and bats, and there are also 2 reports in reptiles. The species described parasitizing small mammals from Argentina are: Mathevotaenia surinamensis (Cohn, 1902) Spasskii, 1951, Mathevotaenia diminuta Navone, 1988, Mathevotaenia matacus Navone, 1988, Mathevotaenia sanmartini Jiménez, Braun, Campbell and Gardner, 2008 in armadillos (Dasypodidae) from Chaco, Corrientes, Formosa and Jujuy Provinces, and Mathevotaenia bivittata (Janicki, 1904) and Mathevotaenia argentinensis Campbell, Gardner and Navone, 2003 parasitizing marsupials (Didelphidae) from Salta and Santiago del Estero Provinces, respectively (Navone, 1988; Campbell et al., 2003; Jiménez et al., 2008). Also, Ezquiaga et al. (2009) reported the presence of Mathevotaenia sp. parasitizing Zaedyus pichiy Desmarest (Dasypodidae) from Mendoza Province. This report was based on the microscopic identification of eggs in the stool, but the eggs of this genus are indistinguishable from those produced by other Linstowiinae; therefore we consider their identification doubtful. Among these species, M. chaquensis n. sp. is most similar to M. argentinensis, a parasite of Didelphis albiventris Lund, and M. bivittata described in Micoureus demerarae Thomas (as M. cinereus) and Marmosa murina L. These species are similar in having small strobila and a reduced number of testes. However, M. argentinensis differs from M. chaquensis n. sp. in having larger suckers, a longer neck, larger testes visible in more posterior proglottids, a pronounced sphincter–like genital atrium, vitelline gland and ovary with higher number of lobules (8 and 10–13, respectively) and larger egg capsules (Table 1). The specimens of M. bivittata described by Campbell et al. (2003) differ from the specimen studied here by possessing a larger scolex and suckers, smaller onchospheres, egg capsules, oncospheral hooks, and cirrus pouch; ovary with a higher number of lobules (10–15), by the distribution of mature eggs in the proglottids, concentrated along their lateral margins, and by the persistence of the female genitalia in gravid proglottids (Table 1). Also, the new species differs from the specimens of M. bivittata described by Baer (1927), Gomes (1979) and Campbell et al. (2003) by having a smaller number of testes (5–8, 8–10 and 10–13, respectively). The remaining species of Mathevotaenia from Argentinean mammals, M. sanmartini a parasite of Thylamys pallidior (Thomas); M. surinamensis reported in Dasypus novemcinctus L., Dasypus sp., Priodontes maximus Kerr (as P. gigas) (Dasypodidae), Didelphis aurita Wied–Neuwied, and Didelphis marsupialis L.(Didelphidae); M. diminuta described from Chaetophractus vellerosus Gray, and M. matacus found parasitizing Tolypeutes matacus (Desmarest), can be readily distinguished from M. chaquensis n. sp. by possessing a larger strobila and a higher number of testes (Table 1). The other South American species of Mathevotaenia described in mammals are: Mathevotaenia didelphidis (Rudolphi) Spasskii, 1951 found parasitizing Thylamys elegans Waterhouse (as Marmosa e.) and M. murina (Didelphidae); Mathevotaenia marmosae (Beddard) Spasskii, 1951 a parasite of T. elegans (as Marmosa e. ); Mathevotaenia tetragonocephala (Bremser) Spasskii, 1951 in Myrmecophaga tridactyla L. and Tamandua tetradactyla L. (Myrmecophagidae); Mathevotaenia paraguayae Schmidt and Martin, 1978 in Euphractus sexcinctus flavimanus Desmarest (Dasypodidae); Mathevotaenia megastoma (Diesing) Spasskii, 1951 from monkeys; Mathevotaenia brasiliensis Kugi and Sawada, 1970 in Saimiri sciureus L. (Primates: Cebidae); Mathevotaenia immatura Rego, 1963; Mathevotaenia boliviana Sawada and Harada, 1986 in Glossophaga soricina (Pallas) (Chiroptera: Phyllostomidae), and Mathevotaenia sp. in T. tetradactyla (Baer, 1927; Spasskii, 1951; Buchanan, 1956; Rego, 1963; Kugi and Sawada, 1970; Schmidt and Martin, 1978; Sawada and Harada, 1986; Beveridge, 2008; Bursey et al., 2010). Mathevotaenia marmosae, M. megastoma, M. brasiliensis and M. tetragonocephala differ from the new species in the total length of worms (84 mm to 650 mm) and number of testes (70 to 200). The specimens of M. immatura and M. boliviana can be distinguished from the specimen here described by having a smaller size (1.6–3.9 mm), fewer proglottids, larger suckers, smaller oncospheral hooks and egg capsules (Table 2). Mathevotaenia chaquensis n. sp. closely resembles M. paraguayae in the total length of strobila (24 mm vs. 20–25 mm), and number of testes (19–24 vs. 16–25). However, the major differences between the 2 species include the relative shape of mature proglottids, that is longer than wide in M. paraguayae according to the drawing of the proglottid (see Fig. 2 in Schmidt and Martin, 1978) vs. mature proglottids wider than long in M. chaquensis; presence of seminal receptacle in M. paraguayae vs. absence of seminal receptacle in M. chaquensis; an ovary not bilobed with about 21 digitiform lobules in M. paraguayae (see Fig. 2 in Schmidt and Martin, 1978) vs. ovary bilobed with 4–7 short lobules in M. chaquensis. In addition, M. chaquensis differs from these Paraguayan specimens in having smaller suckers, vitelline gland and egg capsules in M. chaquensis (115–145 x 105–126 vs. 150–200 x 140–190; 33–43 x 60–71 vs. 40–50 x 90–100; 41–45 vs. 60–80, respectively), a longer neck (580 vs. 400), a larger scolex and genital atrium (348 x 435 vs. 215–280 x 375–465; 53–79 x 48–71 vs. 40–50 x 10). A comparison of the 2 species is given in Table 2. In this paper, the new species is not compared with M. didelphidis since its scolex is unknown, and the descriptions provided by Baer (1927) and Spasskii (1951) disagree on the position of the testes (anterior to female gonad vs. posterior to it). Therefore, we believe that new studies of type material or of new specimens collected from type host are required.

At present, only 2 reports of Mathevotaenia have been made from Neotropical reptiles, Mathevotaenia sp. mentioned as parasite of Anolis humilis (Peters) (Squamata: Polychrotidae) from Nicaragua and Mathevotaenia panamensis Bursey, Goldberg and Telford, 2010 parasitizing Sceloporus malachiticus Cope (Squamata, Phrynosomatidae) from Panama (Goldberg et al., 2010; Bursey et al., 2010). The specimens of M. panamensis are similar in size to the specimen here described (22–29 mm vs. 24 mm), but differ by having fewer testes per proglottid (1016 vs. 19–24), persistence of female genitalia in gravid proglottids, mature eggs concentrated along the lateral margins of the proglottids, and also by significant morphometrical differences, i.e. larger size of ovary (51–78 x 120–154 vs. 82–116 x 266–271), vitelline gland (26–34 x 65–78 vs. 63 x 82), cirrus pouch (40–49 in diam. vs. 126178 x 44–48), genital atrium (25–30 x 8–12 vs. 53–79 x 48–71, oncosphere (15–18 vs. 24–29), egg capsules (27–30 vs. 41–45), oncospheral hooks (10–12 vs. 15–18).

This finding constitutes the first report of the genus Matevothaenia parasitizing reptiles from Argentina.

Key to the South American species of Mathevotaenia

 

Acknowledgments

The authors express their gratitude to Jorge Céspe–dez and José Ruiz–García for their help in sampling, and also thank Graciela T. Navone for providing part of the bibliography. The authors, L. Lunaschi and F. Drago are members of the Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC) and Universidad Nacional de La Plata (UNLP), respectively. The present study was funded by CIC (Res. No. 1535/10).

 

Literature cited

Ávila, R. W. and R. J. Silva. 2010. Checklist of helminths from lizards and amphisbaenians (Reptilia, Squamata) of South America. The Journal of Venomous Animals and Toxins including Tropical Diseases 16:543–572.         [ Links ]

Baer, J. G. 1927. Monographie des cestodes de la famille des Anophocephalidae. Bulletin Biologique de France et de Belgique, supp. 10:1–241.         [ Links ]

Beveridge, I. 2008. Mathevotaenia niuguiniensis n. sp. (Cestoda: Anoplocephalidae: Linstowiinae) from the water–rat Parahydromys asper (Thomas) in Papua New Guinea, with a list of species ofMathevotaenia Akumyan, 1946. Systematic Parasitology 71:189–198.         [ Links ]

Buchanan, G. D. 1956. Occurrence of the cestode Mathevotaenia surinamensis (Cohn, 1902) Spasskii, 1951 in a North American armadillo. Journal of Parasitology 42:34–38.         [ Links ]

Bursey, C. R., S. R. Goldberg and S. R. Telford. 2010. A new species of Mathevotaenia (Cestoda, Anoplocephalidae, Linstowiinae) from the lizard Sceloporus malachiticus (Squamata, Phrynosomatidae) from Panama. Acta Parasitologica 55:53–57.         [ Links ]

Campbell. M. L., S. L. Gardner and G. T. Navone. 2003. A new species of Mathevotaenia (Cestoda: Anoplocephalidae) and other tapeworms from marsupials in Argentina. Journal of Parasitology 89:1181–1185.         [ Links ]

Chervy, L. 2002. The terminology of larval cestodes or metacestodes. Systematic Parasitology 52:1–33.         [ Links ]

Ezquiaga, M. C., M. Superina and G. T. Navone. 2009. Parásitos intestinales de Zaedyus pichiy (Xenarthra: Dasypodidae) de Mendoza, Argentina. Mastozoología Neotropical 16:309–319.         [ Links ]

Goldberg, S. R., C. R. Bursey and L. J. Vitt. 2010. Helminths from 3 species of anoles: Lhe Humble Anole, Anolis humilis; the Border Anole, Anolis limifrons; and the Lion Anole, Anolis lionotus (Squamata: Polychrotidae), from Nicaragua. Comparative Parasitology 77:242–246.         [ Links ]

Gomes, D. C. 1979. Contribuição ao conhecimento dos helmintos parasitos de marsupiais no Brasil, da Coleção Helmintologica do Instituto Oswaldo Cruz (Cestoda, Archiacanthocephala e Linguatulida). Revista Ibérica de Parasitología 39:87–599.         [ Links ]

Jiménez, F. A., J. K. Braun, M. L. Campbell and S. L. Gardner. 2008: Endoparasites of fat–tailed mouse opossums (Thylamys: Didelphidae) from Northwestern Argentina and Southern Bolivia, with the description of a new species of tapeworm. Journal of Parasitology 94:1098–1102.         [ Links ]

Kugi, G. and I. Sawada. 1970. Mathevotaenia brasiliensis n. sp., a tapeworm from the squirrel monkey, Saimiri sciureus. Japanese Journal of Parasitology 19:467–470.         [ Links ]

Lamom, C. and G. J. Greer. 1986. Human Infection with an anoplocephalid tapeworm of the genus Mathevotaenia. The American Journal of Tropical Medicine and Hygiene 35:824-826.         [ Links ]

Martori, R. and L. Aun. 1994. Aspects of ecology of a population of Tropidurus spinulosus. Amphibia–Reptilia 15:317–326.         [ Links ]

Navone, G. T. 1988. Estudios parasitologicos en edentados argentinos. IV. Cestodes pertenecientes a la familia Anoplocephalidae Cholodkovsky, 1902, parásitos de dasypodidos. Neotropica 34:51–61.         [ Links ]

Rego, A. A. 1963. Nova espécie do gênero Mathevotaenia Akhumian, 1946 parasita de quirópteros (Cestoda: Anoplocephalidae). Revista Brasiliera de Biologia 23:31–34.         [ Links ]

Sawada, I. and M. Harada. 1986. Bat cestodes from Bolivia, South America, with descriptions of six new species. Zoological Science 3:367–377.         [ Links ]

Schmidt, G. D. and R. L. Martin. 1978. Tapeworms of the Chaco Boreal, Paraguay, with two new species. Journal of Helminthology 52:205–209.         [ Links ]

Spasskii, A. A. 1951. Anoplocephalate Tapeworms of Domestic and Wild Animals. In Essentials of cestodology. Vol. 1, K. I. Skrjabin (ed.). The Academy of Sciences of the USSR, Moscow. p. 515–634.         [ Links ]

Sutton, C. A., C. Mordeglia and F. Cruz. 1998. Strongyluris oscari Travassos, 1923 (Nematoda, Heterakidae) en Tropidurus spinulosus (Squamata, Tropiduridae) del noroeste de Argentina. Gayana, Zoología 62:171–175.         [ Links ]