Short Communications

SALAMANDRA 45 2 125-128 Rheinbach, 20 May 2009 ISSN 0036-3375

Helminths from seven species of (: ) from Peru

Stephen R. Goldberg & Charles R. Bursey

Abstract. Seven species of Microlophus from Peru were examined for helminth parasites: M. koepckeorum, M. occipitalis, M. peruvianus, M. stolzmanni, M. theresiae, M. thoracicus and M. tigris. We found five species of Nematoda, mature individuals of Parapharyngodon sceleratus, Physalopera retusa, Spauligodon oxkutzcabiensis, Thubunaea parkeri, and larvae of Ascarididae gen. sp. On average, there were 2.0 ± .2 SD (range = -4) helminth species per Microlophus species. Nine new host records are re- ported. Key words. Reptilia, Tropiduridae, Microlophus, Nematoda, helminth, parasites, Peru.

The purpose of this paper is to report 2266-22622, 22625-22627, 22630, 22633, helminths from seven species of Microlophus 22634); M. peruvianus (n = ), SVL = 8.2 from Peru. The genus Microlophus consists mm ± 9.5 SD, range = 58-09 mm, Ancash of some 20 species restricted in distribution Department: Pativilca (LACM 4902, 49037), to South America and the Galapagos Islands Ica Department: Paracas (LACM 4908, (Peters & Donosos Barros 986). Microl- 4909, 49040, 49042, 49044, 49046, Lima ophus koepckeorum, M. peruvianus, M. ther- Department: Pavilca (LACM 49024, 49032), esiae, M. thoracicus, M. tigris are endemic to Cerro Azul (LACM 49057); M. stolzmanni Peru (Lehr 2002). Microlophus occipitalis (n = ), SVL = 68. mm ± 2.0 SD, range = is known from southwestern Ecuador and 49-89 mm, Cajamarca Department: Ochen- northern and central Peru; M. stolzmanni is tiuno (LACM 22652), Bellavista (LACM known from northwestern Peru and possibly 22655, 22659, 22660, 22667-22669, southwestern Ecuador (Peters & Donosos 2267, 22677, 22679, 2268); M. theresiae Barros 986). The only report, to our knowl- (n = 0), SVL = 66. mm ± 5.3 SD, range = 58- edge, of helminths from Microlophus is the 73 mm, Lima Department: El Paraiso Penin- description of Thubunaea parkeri from Mi- sula (LACM 22692-22694, 22699, 2270- crolophus occipitalis by Baylis (926). 22704, 2270, 227); M. thoracicus (n = Seventy-five Microlophus specimens from 0), SVL = 67.9 mm ± 6. SD, range = 56-78 Peru that had been deposited in the herpe- mm, Ica Department: Pisco Junction (LACM tological collection of the Natural History 2273-22736), Ancash Department: Cul- Museum of Los Angeles County (LACM), ebras (LACM 22739-2274, 22743); M. ti- Los Angeles, California, USA were examined gris (n = 0), SVL = 64.7 mm ± 4. SD, range for gastrointestinal helminths: M. koepck- = 42-80 mm, Lima Department: Asia Vieja eorum (n = 0), mean snout-vent length (LACM 2272, 2275-22723). (SVL) = 70.9 mm ± 6. SD, range 59-77 mm, The abdominal cavity of each was Lambayeque Department: Motupe (LACM opened and the digestive tract was removed. 22584, 22588-22590), Olmes (LACM The digestive tract was opened and exam- 2259, 22599, 22600), Zapote (LACM ined for helminths under a dissecting mi- 2262-2264); M. occipitalis (n = 3), SVL croscope. Nematodes were placed on a glass = 65.2 mm ± 8.4 SD, range = 50-78 mm, slide, cleared in a drop of lactophenol solu- Lambayeque Department: Motupe (LACM tion, covered with a cover slip and identified.

© 2009 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT) http://www.salamandra-journal.com 125 Short Communications

Tab. 1. Number (N), percent prevalence (P) and mean intensity ± SD (X) of Nematoda species for seven species of Microlophus from Peru.

Parapharyngodon Physaloptera Spauligodon Thubunaea Ascarididae scleratus retusa oxkutzcabiensis parkeri gen. sp. N P X N P X N P X N P X N P X M. koepckeorum 8 0 8  0  – – – – – – – – – M. occipitalis 9 23 3.0±2.7 – – – 3 8 3 – – – 2 8 2 M. peruvianus 4 8 2.0±.4  9  – – – – – – – – – M. stolzmanni 6 27 2.0±.7 2 8 .0±0.0 – – – 2 9 2 – – – M. theresiae – – – – – – – – – 4 20 2.0±.4 – – – M. thoracicus 8 30 6.0±5.6 – – – – – – – – – – – – M. tigris – – – 2 20 .0±0.0 – – – – – – – – – Selected nematodes were deposited in the Parapharyngodon scleratus was originally United States National Parasite Collection described as Thelandros sceleratus by Tra- (USNPC), Beltsville, Maryland: Microlophus vassos (923) from the iguanid Tropidurus koepckeorum: Parapharyngodon scleratus torquatus from Maguinhos, State of Rio de (USNPC 00775), Physaloptera sp. (USNPC Janeiro, Brazil. It was reassigned to Parap- 00776); Microlophus occipitalis: Parapharyn- haryngodon by Freitas (957). Parapharyn- godon scleratus (USNPC 00777), Spauligo- godon sceleratus is widely distributed in don oxkutzcabiensis (USNPC 00778), As- Brazil and has been reported from Ameiva carid larvae (USNPC 00779); Microlophus ameiva, Kentropyx altamazonicus, Mabuya peruvianus: Parapharyngodon scleratus (US- bistriata, Tropidurus scutipunctatus, T. spinu- NPC 00780), Physaloptera retusa (USN- losus, T. torquatus and the gekkonid Hemi- PC 0078); Microlophus stolzmanni: Para- dactylus mabouia (see Bursey et al. 2005). It pharyngodon scleratus (USNPC 00782), also is known from Microlophus albemarlen- Physaloptera retusa (USNPC 00783), Thubu- sis from the Galapagos Islands (Barus 973) naea parkeri (USNPC 00784); Microlo- and Tropidurus melanopleurus from Bolivia phus theresiae: Thubunaea parkeri (USNPC (Roca 997). Microlophus koepckeorum, M. 00785); Microlophus thoracicus: Thubunaea occipitalis M. peruvianus and M. stolzmanni parkeri (USNPC 00786); Microlophus tigris: represent new host records for Parapharyn- Physaloptera retusa (USNPC 00787). Identi- godon scleratus. fication was based on comparisons with the Spauligodon oxkutzcabiensis was de- original descriptions (see below) as well as scribed from the gecko Thecadactylus rapi- comparisons to reference specimens main- cauda from the Yucatan peninsula (Chit- tained in our laboratory. Parasite terminol- wood 938). It was recorded from scelop- ogy is in accordance with Bush et al. (997). orine lizards (Sceloporus malachiticus) from Five species of Nematoda were found: Costa Rica by Goldberg & Bursey (992a), gravid individuals of Parapharyngodon scel- S. formosus, S. grammicus, S. megalepidurus, eratus (Travassos, 923), Physaloptera retusa S. mucronatus from Mexico (Goldberg et al. Rudolphi, 89, Spauligodon oxkutzcabiensis 2003), and from the gecko Phyllodactylus re- (Chitwood, 938), Thubunaea parkeri Bay- issii from Peru (Goldberg & Bursey 2004). lis 926 and second stage larvae of Ascari- Spauligodon, a member of the Oxyuridae, has dae gen. sp. (Fig. , Table ). On average there a monoxenous (= direct life cycle) not involv- were 2.0 ± .2 SD (range = -4) helminth spe- ing an intermediate host (Anderson 2000). cies per Microlophus species. These nema- Infection occurs by contact with contami- todes are frequently found in South Ameri- nated substrate or possibly by ingesting eggs can lizards. from licking the substrate (see Goldberg &

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Fig. 1-5: Fig. 1a-d. Para- pharyngodon scleratus from Microlophus from Peru: (a) female; (b) female en face view; (c) male; (d) egg. Fig. 2a-d. Spauligodon oxkutz- cabiensis from Microlophus from Peru: (a) female; (b) fe- male en face view; (c) male; (d) egg. Fig. 3. Ascarididae gen. sp. (larva) from Micro- lophus from Peru. Fig. 4a- d. Physaloptera retusa from Microlophus from Peru: (a) female (anterior view); (b) female en face view; (c) male (posterior view); (d) female (posterior view). Fig. 5a-d. Thubunaea par- keri from Microlophus from Peru: (a) female (anterior view); (b) female en face view; (c) male (posterior view); (d) female (posterior view).

Bursey 992b). Microlophus occipitalis repre- and South America (see Goldberg et al. sents a new host record for Spauligodon ox- 2007). Insects serve as intermediate hosts kutzcabiensis. (Anderson 2000). Microlophus stolzmanni There are few reports of ascarid larvae in represents a new host record for Physalop- South American lizards (Vrcibradic et al. tera retusa. Thubunaea parkeriwas described 2002, Bursey et al. 2005) and ascarid trans- from M. occipitalis and Dicrodon heterolepis mission commonly involves terrestrial inver- from Peru (Baylis 926). The life cycle of T. tebrates (Anderson 2000). Thus, the pres- parkeri has not been studied, but Velikanov ence of ascarid larvae in M. occipitalis may (992) reported beetles to serve as intermedi- represent an accidental occurrence, a byprod- ate hosts for the congener Thubunaea baylisi. uct of diet. Physaloptera retusa was originally Microlophus stolzmanni and M. theresioides described from the teiid Tupinambis teguixin represent new host records for Thubunaea from Brazil by Rudolphi (89). Physalop- parkeri. tera retusa is widespread in the western hem- With at least 78 lizard species known from isphere and is known from North, Central Peru (Lehr 2002) and reports of helminths

127 Short Communications from only 5 (8%) much work needs to be – Journal of the Helminthological Society of done before the helminth diversity of Peru- Washington, 59: 25-27. vian lizards can be ascertained. Goldberg, S.R. & C.R. Bursey (992b): Preva- lence of the nematode Spauligodon giganticus (Oxyurida: Pharyngodonidae) in neonatal Yar- Acknowledgements row’s spiny lizards, Sceloporus jarrovii (Sauria: Iguanidae). – Journal of Parasitology 78: 539- We thank Christine Thacker (Natural History 54. Museum of Los Angeles County) for permission Goldberg, S.R. & C.R. Bursey (2004): Phyllo- to examine specimens, Peggy Firth for the illus- dactylus reissii (Peter’s Leaf-toed Gecko). En- trations and Tenzing Doleck (Whittier College) doparasites. – Herpetological Review, 35: 395. for assistance with dissections. Goldberg, S.R., C.R. Bursey & J.L. Camarillo- Rangel (2003): Gastrointestinal helminths of References seven species of sceloporine lizards from Mex- ico. – Southwestern Naturalist, 48: 208-27. Anderson, R.C. (2000): Nematode parasites of Goldberg, S.R., C.R. Bursey, J.P. Caldwell, L.J. vertebrates: their development and transmis- Vitt & G.C. Costa (2007): Gastrointestinal sion. – 2nd Ed., CABI Publishing, Wallingford, helminths from six species of frogs and three Oxfordshire, UK. species of lizards, sympatric in Pará State, Bra- Barus, V. (973): Some remarks on the Neotropi- zil. – Comparative Parasitology, 74: 327-342. cal species of the genera Parapharyngodon and Lehr, E. (2002). Amphibien und Reptilien in Batracholandros (Oxyuridae). – Folia Parasito- Peru. – Natur und Tier Verlag, Münster. logica, 20: 3-39. Peters. J.A. & R. Donoso-Barros (986): Cata- Baylis, H.A. (926): On a new species of the nem- logue of the Neotropical Squamata: Part II Liz- atode genus Thubunaea. – Annals and Maga- ards and Amphisbaenians. – Smithsonian In- zine of Natural History, ser 9, 7: 36-364. stitutution Press, Washington. Bursey, C.R., S.R. Goldberg & J.R. Parmelee Roca, V. (997): Tropidurus melanopleurus (NCN). (2005): Gastrointestinal helminths of 3 spe- Parasites. – Herpetological Review, 28: 204. cies of lizards from Reserva Cuzco Amazónico, Rudolphi, C. (89): Entozoorum Synopsis cui Peru. – Comparative Parasitology, 72: 50-68. Accedunt mantissa duplex et indices locu- Bush, A.O., K.D. Lafferty, J.M. Lotz & A.W. pletissimi. – August Rucker, Berlin, Germany. Shostak (997): Parasitology meets ecology 8 pp. on its own terms: Margolis et al. revisited. – Travassos, L. (923): Informações sôbre a fauna Journal of Parasitology, 83: 575-583. helmintológica de Mato Grosso. – Folha Med- Chitwood, B.G. (938): Some nematodes from ica, 4: 58-60. the caves of Yucatan. – Publications of the Velikanov, V.P. (992): Life-cycle of Thubunaea Carnegie Institute of Washington 49: 5-66. baylisi (Nematoda: Spirunia). – Parazitologiya, Freitas, J.F.T. (957): Sôbre os gêneros Thelandros 26: 436-440. Wedl, 862, e Parapharyngodon alvarengai sp. Vrcibradic, D., C.R.D. Rocha, C.R. Bursey & n. (Nematoda, Oxyuroidae). – Memórias do J.J. Vicente (2002): Helminth communities Instituto Oswaldo Cruz, 55: 2-45. of two sympatric skinks (Mabuya agilis and Goldberg, S.R. & C.R. Bursey (992a): Gastroin- Mabuya macrorhyncha) from two ‘restinga’ testinal helminths of the lizard, Sceloporus mal- habitats in southeastern Brazil. – Journal of achiticus (Sauria: Iguanidae), from Costa Rica. Helminthology, 76: 355-36.

Manuscript received: 10 May 2008 Authors’ addresses: Stephen R. Goldberg, Department of Biology, Whittier College, Whittier, Califor- nia 90608, USA, E-Mail: [email protected]; Charles R. Bursey, Pennsylvania State University, De- partment of Biology, Shenango Campus, Sharon, Pennsylvania 16146, USA, E-Mail: [email protected].

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