Gastrointestinal Helminths of the Tree Lizard, Urosaurus Ornatus (Phrynosomatidae)

Home , Granite spiny lizard, Phrynosomatidae, Urosaurus, Urosaurus ornatus

J. Helminthol. Soc. Wash. 60(1), 1993, pp. 118-121

Research Note Gastrointestinal Helminths of the Tree Lizard, Urosaurus ornatus (Phrynosomatidae)

STEPHEN R. GOLDBERG,' CHARLES R. BuRSEY,2 AND NAIDA ZucKER3 1 Department of Biology, Whittier College, Whittier, California 90608, 2 Department of Biology, Pennsylvania State University, Shenango Valley Campus, 147 Shenango Avenue, Sharon, Pennsylvania 16146, and 3 Department of Biology, Box 30001, New Mexico State University, Las Cruces, New Mexico 88003-0001

ABSTRACT: The gastrointestinal tracts of 205 Urosau- and Cochise counties, Arizona. By ANOVA, there rus ornatus were examined for helminths: 117 from was no significant difference in snout-vent length Aguirre Spring, New Mexico; 73 from Dona Ana Mountains, New Mexico; and 15 from southern Ari- for the 3 populations (P > 0.05). zona. Spauligodon giganticus was the most prevalent Aguirre Spring Recreation Area is a relatively helminth (prevalence 24.8%, mean intensity 5.6) and mesic environment located at 1,700 m elevation occurred in all 3 samples. The Aguirre Spring sample on a northeast slope of the Organ Mountains had significantly higher prevalences of S. giganticus (32°22'N, 106°33'W, Dona Ana County, New (38.5%) than the other 2 samples. In addition, third- stage larvae of Physaloptera sp. (prevalence 4.2%, mean Mexico). Boulders tend to be clumped, resulting intensity 3.5) and Oochoristica sp. (prevalence 4.2%, in discontinuous habitats for U. ornatus. Most mean intensity 1.6) and tetrathyridia of Mesocestoides lizards are found on boulders or in trees or bushes sp. (prevalence 3.2%, mean intensity 103.8) were re- overhanging boulders. In this habitat, the lizards covered from the New Mexico samples. The finding of Mesocestoides sp. within skeletal muscle in 1 spec- are both saxicolous and arboreal. The Dona Ana imen is noteworthy because it demonstrates that this Mountains have a more xeric environment. The parasite can migrate out of the body cavity. All findings major collecting site (Mount Summerford) lies represent new host records. on a southwest-facing slope at 1,475 m elevation KEY WORDS: Urosaurus ornatus, Phrynosomatidae, (32°30'N, 106°49'W) in Dona Ana County, New cestode, Oochoristica sp., Mesocestoides sp., nematode, Spauligodon giganticus, Physaloptera sp., prevalence, Mexico. Some lizards were collected from neigh- intensity. boring mounts. These sites are strewn with cubic- meter-sized and larger, lichen-covered boulders. The tree lizard, Urosaurus ornatus (Baird and Shade-creating vegetation is mostly lacking. The Girard, 1852), is one of the most abundant liz- lizards at these localities are strictly saxicolous. ards in the American Southwest. It is an ovip- Infected specimens from Arizona were from Kitt arous lizard that occupies a wide variety of hab- Peak, Baboquivari Mountains (31°95'N, itats from riparian environments to dry, rocky 111°59'W, elevation 1,885 m), Pima County, Ar- areas (Dunham, 1982). It ranges from south- izona. Here the topography consists of granite western Wyoming to southern Sinaloa and boulders and outcroppings. In this habitat U. northern Coahuila, Mexico, and from south- ornatus is arboreal. eastern California to central Texas occurring from Specimens from New Mexico were collected sea level to 2,770 m (Stebbins, 1985). To our 1985-1986; Arizona specimens were collected knowledge there are 3 previous reports of hel- 1967-1969. Specimens were preserved in 10% minths from U. ornatus: Walker and Matthias formalin and stored in 95% ethanol prior to ex- (1973) and Specian and Ubelaker (1974) recov- amination. The body cavity was opened and the ered the nematode Parathelandros texanus; Benes gastrointestinal tract was excised by cutting across (1985) found cestode tetrathyridia. This report the anterior esophagus and the rectum. The contains helminth prevalence and intensity data esophagus, stomach, small intestine, and large for populations of U. ornatus from New Mexico intestine were examined separately. The body and Arizona. cavity was examined for cestode tetrathyridia. Two hundred five Urosaurus ornatus were ex- Each helminth was removed and identified uti- amined: 117 from Aguirre Spring Recreation Area lizing a glycerol wet mount and then returned to and 73 from Dona Ana Mountains, Dona Ana alcohol storage. Selected cestodes were stained County, New Mexico; and 15 from Pima, Final with hematoxylin and mounted in balsam. After

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dissection, all lizards were deposited in the herpetology collection of the Natural History Mu- seum of Los Angeles County (Aguirre Spring o o 139449-139565; Dona Ana Mountains 139566- 139638; Arizona 139438-139448, 139639- o o 139642). Representative helminths in vials of alcohol were deposited in the USNM Helmin- thological Collection, USDA, Beltsville, Mary- land 20705: Spauligodon giganticus (82180- 82182), Physaloptera sp. (82184), Mesocestoides sp. (82185), and Oochoristica sp. (82183). Two species of nematodes, Spauligodon giganticus (Read and Amrein, 1953) Skrjabin, O — r-i —i Schikhobalova, and Lagodovskaja, 1960, and Physaloptera sp., and 2 species of cestodes, Me- socestoides sp. and Oochoristica sp., were found. Location of infection, prevalence, and intensity

(by host sex) are shown in Table 1. All of these cs <* o helminths represent new host records for U. ornatus. The most prevalent helminth was S. giganticus, which was found in lizards of all 3 populations. For all samples, prevalence was 24.8% and mean intensity 5.6. There was no significant difference for prevalence of S. giganticus infection between males and females at Aguirre Spring O O in o (Kruskal-Wallis statistic, P > 0.05). Because of low prevalences, tests of significant difference between males and females in the other 2 samples O O TT O were not done. Third-stage larvae of Physaloptera sp. were recovered from the New Mexico populations only (prevalence 4.2%, mean intensity 3.5) as were Oochoristica sp. (prevalence 4.2%, mean intensity 1.6) and tetrathyridia of Mesocestoides sp. (prevalence 3.2%, mean intensity 103.8). Tet- rathyridia had lodged in skeletal musculature of the forelimbs, chest, and tail of a single Aguirre Spring female, making it impossible to obtain an accurate count. The prevalence of infection of 5". giganticus at Aguirre Spring was significantly different from the other sites (Chi-square = 25.7, P < 0.001); however, mean intensity of infection was not sig- oa -c~ •—e -yg nificantly different at the 3 sites (Kruskal-Wallis 56 statistic, P > 0.05). The Aguirre Spring site is 09 (X3 more moist, with greater vegetation and shade than the Dona Ana sites. In addition, the population density of U. ornatus at Aguirre Spring is much higher than the other sites. Boulders are found in clusters, and there is often 1 dominant male lizard and several subordinate males around 2 « * the periphery of a boulder cluster as well as sev- "§ I « 0 Z

sey and Goldberg (1992a) estimated that 91-98 days were required for completion of the S. giganticus life cycle. It is likely that the August

5s 30. drop in monthly prevalence (Fig. 1) represents the completion of the life cycle by the first generation of nematodes. The prevalence seen in August and September would represent infection by the second generation, which would mature during the lizard hibernation period. Spauligo- don giganticus did not appear in the Dona Ana I Mountains population of U. ornatus until July; Ajg Apr only 3 lizards of that population were infected. Figure 1. Prevalence of Spauligodon giganticus by It is plausible that the difference in infection rates month in the Aguirre Spring population, Dona Ana County, New Mexico. of the New Mexico samples may result primarily from differences in density of the lizard populations. The greater density of U. ornatus at eral females in each dominant male's territory Aguirre Spring leads to more substrate fecal con- (Zucker, 1989). At the Dona Ana Mountains, tamination. This increases chance of egg inges- where granite boulders dominate the terrain, liz- tion and results in higher prevalence and inten- ards are less dense with generally only 1 male sity of S. giganticus infection. and 1 female in overlapping territories (N. Zuck- Other phrynosomatid lizards reported as hosts er, pers. obs.). Male territories often do not lie for S. giganticus are Callisaurus draconoides by adjacent to each other. Urosaurus ornatus is un- Telford (1970); Sceloporus graciosus by Telford common in the Baboquivari Mountains, where (1970) and White and Knapp (1979); S. jarrovii it is restricted to oak trees. It apparently cannot by Goldberg and Bursey (1990b); Sceloporus oc- compete with the larger Yarrow's spiny lizard, cidentalis by Telford (1970), Pearce and Tanner Sceloporus jarrovii, which occupies the rocks. (1973), White and Knapp (1979), and Lyon When infection in the Aguirre Spring popu- (1986); Sceloporus orcutti by Telford (1970) and lation was examined by month (Fig. 1), there was Goldberg and Bursey (1991); Sceloporus undu- an increase in prevalence May through July and latus by Pearce and Tanner (1973); and Uta then a sharp decrease in August. Spauligodon stansburiana by Telford (1970). giganticus has a direct life cycle with infection Physaloptera spp. occur in the stomach of a spread by fecal contamination (Telford, 1971). number of terrestrial vertebrates with such reg- In a 51. jarrovii population, sympatric with the ularity that the genus is commonly called "the Baboquivari Mountain population of U. ornatus, stomach worm." Telford (1970) found this hel- Bursey and Goldberg (1992a) found monthly minth to be the most common nematode recov- prevalences of S. giganticus to range from 86 to ered from southern California lizard species. It 100%. Infections occurred in all seasons but with is of interest that only third-stage larvae of no annual pattern of infection. Sceloporus jar- Physaloptera were found in the New Mexico rovii has been observed to lick the ground populations of U. ornatus. Third-stage but not (DeFazio et al., 1977) and is thought to obtain adult Physaloptera sp. have been found in a num- environmental cues through this behavior. Sub- ber of other species of lizards. strate licking plays an important role in the ep- Eight species of Oochoristica have been recov- idemiology of S. giganticus (see Goldberg and ered from North American lizards (Bursey and Bursey, 1992). There are no reports of substrate Goldberg, 1992b). The species found in U. or- licking in U. ornatus; however, this lizard fre- natus is apparently undescribed. It differs from quently "snout-wipes." That is, with the back of the previously described species in length, pro- the lizard arched upward, the tip of the snout is glottid number, scolex width, sucker measure- rubbed back and forth on the substrate several ments, and number of testes. times (Delahunt, 1976). It is possible that eggs Tetrathyridia of Mesocestoides sp. are most of S. giganticus are ingested when U. ornatus commonly seen in the body cavity. The occur- performs this behavior. Infection may occur soon rence of tetrathyridia in North American lizards after U. ornatus becomes active in the spring with has been compiled by McAllister (1988) and more lizards acquiring infection over time. Bur- Goldberg and Bursey (1990b). While there have

Copyright © 2011, The Helminthological Society of Washington OF WASHINGTON, VOLUME 60, NUMBER 1, JANUARY 1993 121 been reports of tetrathyridia in the liver, heart, ard, Sceloporus occidentalis biseriatus (Iguanidae), and mesenteries (McAllister, 1988), this is ap- from southern California. Bulletin of the Southern parently the first report of skeletal muscle in- California Academy of Sciences 89:42^8. —, and . 1991. Intestinal helminths of the vasion and suggests that migration out of the granite spiny lizard (Sceloporus orcutti). Journal body cavity is possible when large numbers of of Wildlife Diseases 27:355-357. tetrathyridia are present. Tetrathyridia of Me- -, and . 1992. Prevalence of the nema- socestoides sp. were recovered from the sympat- tode Spauligodon giganticus (Oxyurida: Pharyn- godonidae) in neonatal Yarrow's spiny lizards, ric Baboquivari Mountain (Kitt Peak) S. jarrovii Sceloporus jarrovii (Sauria: Iguanidae). Journal of population by Goldberg and Bursey (1990a). Parasitology 78:539-541. We thank Rana Tawil for assistance in recov- Lyon, R. E. 1986. Helminth parasites of six lizard ery of helminths. species from southern Idaho. Proceedings of the Helminthological Society of Washington 53:291- Literature Cited 293. McAllister, C. T. 1988. Mesocestoides sp. tetrathy- Benes, E. S. 1985. Helminth parasitism in some cen- ridia (Cestoidea: Cyclophyllidea) in the iguanid tral Arizona lizards. Southwestern Naturalist 30: lizards, Cophosaurus texanus texanus and Scelop- 467^73. orus olivaceous, from Texas. Journal of Wildlife Bursey, C. R., and S. R. Goldberg. 1992a. Monthly Diseases 24:160-163. prevalences of Spauligodon giganticus (Nemato- Pearce, R. C., and W. W. Tanner. 1973. Helminths da, Pharyngodonidae) in naturally infected Yar- of Sceloporus lizards in the Great Basin and upper row's spiny lizard Sceloporus jarrovii jarrovii Colorado Plateau of Utah. Great Basin Naturalist (Iguanidae). American Midland Naturalist 127: 33:1-18. 204-207. Specian, R. D., and J. E. Ubelaker. 1974. Parathe- , and . 19925. Oochoristica bezyi' n. sp. landros texanus n. sp. (Nematoda: Oxyuridae) from (Cestoda: Linstowiidae) from the desert night liz- lizards in west Texas. Transactions of the Amer- ard, Xantusia vigilis vigilis (Xantusiidae). Trans- ican Microscopical Society 93:413-415. actions of the American Microscopical Society 111: Stebbins, R. C. 1985. A Field Guide to Western Rep- 36-43. tiles and Amphibians. Houghton Mifflin Co., Bos- DeFazio, A., C. A. Simon, G. A. Middendorf, and D. ton, Massachusetts. 336 pp. Romano. 1977. Iguanid substrate licking: a re- Telford, S. R., Jr. 1970. A comparative study of en- sponse to novel situations in Sceloporus jarrovi. doparasitism among some southern California liz- Copeia 1977:706-709. ard populations. American Midland Naturalist 83: Delahunt, R. A. 1976. Summer activity cycles of Uro- 516-554. saurus ornatus in field and laboratory. M.S. The- . 1971. Parasitic diseases of reptiles. Journal sis, New Mexico State University, Las Cruces, New of the American Veterinary Medical Association Mexico. 30 pp. 159:1644-1652. Dunham, A. E. 1982. Demographic and life-history Walker, K. A., and D. V. Matthias. 1973. Helminths variation among populations of the iguanid lizard of some northern Arizona lizards. Proceedings of Urosaurus ornatus: implications for the study of the Helminthological Society of Washington 40: life-history phenomena in lizards. Herpetologica 168-169. 38:208-221. White II, R. L., and S. E. Knapp. 1979. Helminth Goldberg, S. R., and C. R. Bursey. 1990a. Gastro- parasites of sceloporine (Iguanidae) lizards from intestinal helminths of the Yarrow spiny lizard, central Oregon. Proceedings of the Helmintholog- Sceloporus jarrovii jarrovii Cope. American Mid- ical Society of Washington 46:270-272. land Naturalist 124:360-365. Zucker, N. 1989. Dorsal darkening and territoriality , and . 1990b. Prevalence of larval ces- in a wild population of the tree lizard, Urosaurus todes (Mesocestoides sp.) in the western fence liz- ornatus. Journal of Herpetology 23:389-398.