Nematode Parasites of 16 Lizard Species from the Area de Conservación Guanacaste, Costa Rica

Comp. Parasitol. 77(2), 2010, pp. 232–235

Research Note

Nematode Parasites of 16 Lizard Species from the Area de Conservacio´n Guanacaste, Costa Rica CHARLES R. BURSEY1,3

AND

DANIEL R. BROOKS2

1

Department of Biology, Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania 16146, U.S.A. (e-mail: [email protected]) and 2 Department of Ecology and Evolutionary Biology, University of Toronto, Ontario, Canada M5S 3G5 ABSTRACT:

Three hundred seventy lizards representing 6 families (16 species)—Corytophanidae: common basilisk, Basiliscus basiliscus (n 5 9); green basilisk, Basiliscus plumifrons (n 5 3); Smooth helmeted iguana, Corytophanes cristatus (n 5 8); Gekkkonidae: yellow-headed gecko, Gonatodes albogularis (n 5 63); common house gecko, Hemidactylus frenatus (n 5 53); yellowbelly gecko, Phyllodactylus tuberculosus (n 5 10); Iguanidae: Oaxacan spinytail iguana, Ctenosaura quinquecarinata (n 52); black iguana, Ctenosaura similis (n 5 37); Phrynosomatidae: rosebelly lizard, Sceloporus variabilis (n 5 18); Polychrotidae: water anole, Anolis aquaticus (n 5 5); neotropical green anole, Anolis biporcatus (n 5 7); copper anole, Anolis cupreus (n 5 51); humble anole, Anolis humilis (n 5 26); lion anole, Anolis lionotus (n 5 72); swift anole, Anolis tropidolepis (n 5 2); Teiidae: rainbow ameiva, Ameiva undulata (n 5 4)—collected in the Area de Conservacio´n Guanacaste, Costa Rica, were necropsied. Gravid nematodes representing 14 species—Africana telfordi, Cosmocercoides variabilis, Cyrtosomum penneri, Cyrtosomum scelopori, Falcaustra costaricae, Oswaldocruzia costaricensis, Ozolaimus monhystera, Physaloptera retusa, Piratuba digiticauda, Rhabdias nicaraguensis, Skrjabinelazia galliardi, Skrjabinodon scelopori, Spauligodon oxkutzcabiensis, Strongyluris panamaensis—and larvae representing 2 species—Acuariidae gen. sp. Ascarididae gen. sp.—were found. Thirty-two new host records are reported. KEY WORDS: Sauria, Nematoda, Costa Rica.

lepis Boulenger, 1885 (reported as Norops tropidolelpis); green spiny lizard, Sceloporus malachiticus Cope, 1864; brown forest skink, Sphenomorphus cherriei (Cope, 1893) (Bravo-Hollis and Brenes, 1959; Brenes and Bravo-Hollis, 1960; Goldberg and Bursey, 1992, 2004a, b, 2007, 2008a, 2009; Desser, 1997; Bursey and Goldberg, 2003, 2006; Bursey et al., 2004; Bursey et al., 2007a). Our work on Costa Rican lizards has produced additional hosts and nematode parasites, which we present herein. Host names follow Uetz and Hallermann (2009). Three hundred seventy lizards representing 6 families (16 species) collected in the Area de Conservacio´n Guanacaste, Costa Rica between April 2001 and August 2006 were necropsied—Corytophanidae: common basilisk, Basiliscus basiliscus (Linnaeus, 1768) (n 5 9); green basilisk, Basiliscus plumifrons Cope, 1876 (n 5 3); Smooth helmeted iguana, Corytophanes cristatus (Merrem, 1820) (n 5 8); Gekkkonidae: yellow-headed gecko, Gonatodes albogularis (Dume´ril and Bibron, 1836) (n 5 63); common house gecko, Hemidactylus frenatus Schlegel, 1836 (n 5 53); yellowbelly gecko, Phyllodactylus tuberculosus Wiegmann, 1834 (n 5 10); Iguanidae: Oaxacan spinytail iguana, Ctenosaura quinquecarinata (Gray, 1842) (n 52); Ctenosaura similis (n 5 37); Phrynosomatidae: rosebelly lizard, Sceloporus variabilis Wiegmann, 1834 (n 5 18); Polychrotidae: water anole, Anolis aquaticus Taylor, 1956 (n 5 5); neotropical green anole, Anolis biporcatus Wiegmann, 1834 (n 5 7); Anolis cupreus (n 5 51); humble anole, Anolis humilis Peters, 1863 (n 5 26); lion anole, Anolis lionotus Cope, 1861 (n 5 72); swift anole, Anolis tropidolepis Boulenger, 1885) (n 5 2); Teiidae: rainbow ameiva, Ameiva undulata (Wiegmann, 1834) (n 5 4). Hosts and helminths were deposited in Department of Zoology, University of Toronto, Ontario, Canada. A total of 7,434 nematodes was collected from 140 of the 370 lizards (38%) examined (Table 1). Of these, 7,430 were mature individuals representing 14 species;

Of the 73 lizard species found in Costa Rica (Savage, 2002), 10 (14%) have been reported to harbor nematodes, namely, black iguana, Ctenosaura similis (Gray, 1831); litter gecko, Lepidoblepharis xanthostigma (Noble, 1916); yellow-spotted night lizard, Lepidophyma flavimaculatum Dume´ril, 1851; Cope’s alligator lizard, Mesaspis monticola (Cope, 1878); copper anole, Anolis cupreus Hallowell, 1860 (reported as Norops cupreus); border anole, Anolis limifrons Cope, 1871 (reported as Norops limifrons); lichen anole, Anolis pentaprion Cope, 1863 (reported as Norops pentaprion); swift anole, Anolis tropido3

Corresponding author. 232

RESEARCH NOTES

233

Table 1. Prevalence of nematode infections in 16 lizard species from the Area de Conservacio´n Guanacaste, Costa Rica. Nematode species Africana Cosmocercoides Cyrtosomum Cyrtosomum Falcaustra Oswaldocruzia Ozolaimus Physaloptera N telfordi variabilis penneri scelopori costaricae costariensis monhystera retusa

Lizard species Corytophanidae Basiliscus basiliscus Basiliscus plumifrons Coryptophanes cristatus

9

—

—

—

—

—

—

—

11*

3

—

33*

—

—

—

—

—

—

8

25*

—

—

50*

—

—

—

—

63

—

—

—

—

—

—

—

67

53

—

—

—

—

—

—

—

13*

10

—

—

—

—

—

—

—

—

—

—

—

—

—

—

50*

—

—

—

—

—

—

3*

—

—

18

—

—

50

—

—

6*

—

22

5

—

—

—

—

—

20*

—

—

7 51 26 72

— — — 1*

— 4* 23* 6*

71 — — —

— — — —

— — — 17*

— — — 1*

— — — —

— 14 4* 1*

2

—

—

—

—

50

—

—

—

4

—

—

—

—

—

—

—

50

Gekkkonidae Gonatodes albogularis Hemidactylus frenatus Phyllodatylus tuberculosus Iguanidae Ctenosaura quinquecarinata 2 Ctenosaura similis 37 Phrynosomatidae Sceloporus variabilis Polychrotidae Anolis aquaticus Anolis biporcatus Anolis cupreus Anolis humilis Anolis lionotus Anolis tropidolepis Teiidae Ameiva undulata * New host record.

4 were larval forms representing 2 species. Although there were 16 nematode species in the sample, no host lizard harbored more than 4 species: 94 hosts (67%) harbored 1 nematode species, 38 hosts (27%) harbored 2 species, 6 hosts (4%) harbored 3 species, and 2 hosts (1%) harbored 4 species. On average, there were 1.40 6 0.65 SD (range, 1–4) nematode species per host individual and 51.30 6 181.86 SD (range, 1–1,548) nematode individuals per host. No lizard species harbored more than 7 helminth species; on average, there were 2.56 6 1.63 (range, 1–7) helminth species per lizard species. Thirty-two new host records are reported (Table 1).

Table 1 lists the species of nematodes collected in this study by host. Host lists for the nematode species found in this study are available elsewhere: Bursey et al. (2007b) for Africana telfordi, Cosmocercoides variabilis, Physaloptera retusa, Pirabuba digiticauda, Skrjabinelazia galliardi, Skrjabinodon scelopori, Spauligodon oxkutzcabiensis, and Strongyluris panamaensis; Bursey et al. (2003) for Cyrtosomum penneri and C. scelopori; Goldberg and Bursey (2008b) for Falcaustra costaricae and Oswaldocruzia costariensis; Baker (1987) for Ozolaimus monhystera; and Bursey, Goldberg, and Vitt (2007) for Rhabdias nicaraguensis. On the basis of this study

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COMPARATIVE PARASITOLOGY, 77(2), JULY 2010

Table 1. Extended.

Nematode species Piratuba digiticauda

Rhabdias nicaraguensis

Skrjabinelazia galliardi

Skrjabinodon scelopori

Spauligodon oxkutzcabiensis

Strongyluris panamaensis

Acuariidae gen. sp.

Ascarididae gen. sp.

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

13*

—

—

—

—

—

—

—

—

—

21

44

—

—

2*

—

—

—

—

—

—

—

—

—

—

—

20*

—

—

—

—

—

—

—

—

50*

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

—

14*

—

—

—

—

—

—

— 4* 17* —

— 4* — 50*

— — — —

— — — —

— — — —

— — — —

— — — —

— — 1* —

50*

—

—

—

—

—

—

50*

8*

9*

and the host lists above, none of these nematode species is restricted to a single host species, which is to suggest that Costa Rican lizards harbor a community of generalist nematodes. This is similar to the parasitic nematode community reported for lizards of Panama and Peru (Bursey et al., 2005; Bursey et al., 2007b) and is perhaps the typical structure of lizard nematode communities. We thank the scientific and technical staff of the Area de Conservacio´n Guanacaste (ACG) for support of this study, in particular: Elda Araya, Roger Blanco, Duvalier Bricen˜ o, Carolina Cano, Maria Marta Chavarrı´a, Felipe Chavarrı´a, Roberto Espinoza,

6*

Dunia Garcia, Guillermo Jimenez, Elba Lopez, Sigifredo Marin, Alejandro Masis, Calixto Moraga, Fredy Quesada, and Petrona Rios. Thanks also to Dan Janzen and Winnie Hallwachs, scientific advisers to the ACG, for their support. This study was funded by a Discovery Grant from the Natural Sciences and Engineering Research Council (NSERC) of Canada to D.R.B. LITERATURE CITED Baker, M. R. 1987. Synopsis of the Nematoda parasitic in amphibians and reptiles. Memorial University of Newfoundland, Occasional Papers in Biology 11:1–325.

RESEARCH NOTES

Bravo-Hollis, M., and R. R. Brenes. 1959. Helmintos de la Repu´blica de Costa Rica X. Nematoda 4. Sobre la posicio´n taxono´mica de los go´neros Ozolaimus Dujardin, 1845 y Macracis Gedoelst, 1916. Anales del Instituto de Biologı´a, Universidad Nacional Auto´noma de Me´xico 30:209–255. Brenes, R. R., and M. Bravo-Hollis. 1960. Helmintos de la Republica de Costa Rica IX. Nematoda 3. Algunos nematodos de reptiles, con descripcion de dos nuevas especies: Atractis caballeroi n. sp. y Cyrtosomum longicaudatum n. sp. Libro Homenaje al Dr. Eduardo Caballero y Caballero. Instituto Politechnico Nacional, Esquela Nacional de Ciencias Biologicas, Santo Toma´s, Hidalgo, Mexico. Pp 451–464. Bursey, C. R., and S. R. Goldberg. 2003. Acanthocephalus saurius n. sp. (Acanthocephala: Echinorhynchidae) and other helminths from the lizard Norops limifrons (Sauria: Polychrotidae) from Costa Rica. Journal of Parasitology 89:573–576. Bursey, C. R., and S. R. Goldberg. 2006. Helminths in Mesaspis monticola (Squamata: Anguidae) from Costa Rica, with the description of a new species of Entomelas (Nematoda: Rhabdiasidae) and a new species of Skrjabinodon (Nematoda: Pharyngodonidae). Parasite 13:183–191. Bursey, C. R., S. R. Goldberg, and C. L. Miller. 2004. Two new species of Falcaustra and comments on helminths of Norops tropidolepis (Sauria: Polychrotidae) from Costa Rica. Journal of Parasitology 90:598– 603. Bursey, C. R., S. R. Goldberg, and J. R. Parmelee. 2005. Gastrointestinal helminths from 13 species of lizards from Reserva Cuzco Amazo´nico, Peru. Comparative Parasitology 72:50–68. Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr. 2003. Strongyluris panamaensis n. sp. (Nematoda: Heterakidae) and other helminths from the lizard, Anolis biporcatus (Sauria: Polychrotidae), from Panama. Journal of Parasitology 89:118–123. Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr. 2007a. New species of Aplectana (Nematoda: Cosmocercidae) and Mesocoelium monas (Digenea: Brachycoeliidae) in Lepidophyma flavimaculatum (Squamata: Xantusiide) from Costa Rica. Caribbean Journal of Science 42:164–170.

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Bursey, C. R., S. R. Goldberg, and S. R. Telford, Jr. 2007b. Gastrointestinal helminths of 14 species of lizards from Panama with descriptions of five new species. Comparative Parasitology 74:108–140. Bursey, C. R., S. R. Goldberg, and L. J. Vitt. 2007. New species of Rhabdias (Nematoda: Rhabdiasidae) and other helminths from Norops capito (Sauria: Polychrotidae) from Nicaragua. Journal of Parasitology 93: 129–131. Desser, S. S. 1997. Blood parasites of the iguanid lizard, Ctenosaura similis from Costa Rica, with a description of Hepatozoon gamezi n. sp. Journal of Eukaryotic Microbiology 44:162–167. Goldberg, S. R., and C. R. Bursey. 1992. Gastrointestinal helminths of the lizard Sceloporus malachiticus (Sauria: Iguanidae) from Costa Rica. Journal of the Helminthological Society of Washington 59:125–126. Goldberg, S. R., and C. R. Bursey. 2004a. Lepidoblepharis xanthostigma (Orange-tailed gecko). Endoparasites. Herpetological Review 35:268. Goldberg, S. R., and C. R. Bursey. 2004b. Norops cupreus (Copper anole). Endoparasites. Herpetological Review 35:394. Goldberg, S. R., and C. R. Bursey. 2007. Sphenomorphus cherriei (Striped litter skink, Chirbala lisa). Endoparasites. Herpetological Review 38:82–83. Goldberg, S. R., and C. R. Bursey. 2008a. Lepidoblepharis xanthostigma (NCN). Endoparasites. Herpetological Review 39:350. Goldberg, S. R., and C. R. Bursey. 2008b. Helminths from 10 species of brachycephalid frogs (Anura: Brachycephalidae) from Costa Rica. Comparative Parasitology 75: 255–262. Goldberg, S. R., and C. R. Bursey. 2009. Ameiva undulata (Rainbow Ameiva). Endoparasites. Herpetological Review 40:82. Savage, J. M. 2002. The Amphibians and Reptiles of Costa Rica: A Herpetofauna Between Two Continents, Between Two Seas. University of Chicago Press, Chicago, Illinois. 934 pp. Uetz, P., J. Groll, and J. Hallermann. 2009. The Reptile Database [Internet]. Rockville, Maryland: Peter Uetz and J. Craig Venter Institute; 2009. http://www.reptiledatabase.org/. Accessed 2009 November 20.