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Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. VI. the gray-checkered whiptail (Cnemidophorus dixoni).

ABSTRACT. -- Twenty-nine of 58 (50 percent) unisexual gray-checkered whiptails, Cnemidophorus dixoni (pattern class A), from Presidio County, Texas, were infected with one or more helminths, including linstowiid cestodes (Oochoristica sp.) in 12 (21 percent), larval spirurid nematodes (Physaloptera sp.) in 11 (19 percent), oxyurid nematodes (Parathelandros texanus) in three (five percent), and acanthocephalan cystacanths in 12 (21 percent). This note, the sixth in a series on helminths of species of Cnemidophorus, reports parasites in C. dixoni A for the second time. Key words: Acanthocephala; Cestoidea; Nematoda; Cnemidophorus dixoni A; helminths; lizards; Teiidae.

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The gray-checkered whiptail, Cnemidophorus dixoni, is a recently described parthenogenetic (all-female) lizard of the tesselatus species group that is restricted to three disjunct erosional bench habitats, two near the Rio Grande in Presidio County, Texas, and one near the Gila River in Hidalgo County, New Mexico (Scudday, 1973). The species inhabits areas of dry riverbeds and floodplains between roughland desert slopes and sandy desert floors that support sparse grasses, creosote bushes, and ocotillo. There is general agreement that C. dixoni is a diploid, cloned derivative of hybridization between the parental taxa C. gularis septemvittatus (sensu Walker and Cordes, 1991) and C. marmoratus marmoratus (sensu Hendricks and Dixon, 1986). However, it cannot be determined at present whether C. dixoni is a product of the same hybridization that produced the diploid color pattern classes (that is, morphotypes) of the Colorado checkered whiptail, C. tesselatus (sensu Zweifel, 1965) (see Wright and Lowe, 1967; Parker and Selander, 1976; Densmore et al., 1989). As a result, recent literature reflects little agreement on the appropriate taxonomic treatment for this parthenogen. For example, it may be regarded as a distinct species (Scudday, 1973; Densmore et al., 1989), a color pattern class of C. tesselatus (Zweifel, 1965; Parker and Selander, 1976), or a cloned hybrid lineage without taxonomic recognition (Walker, 1986). The species as defined by Scudday (1973) consists of two geographically disparate, ecologically distinctive color pattern classes designated A and B. The use of the name C. dixoni A in this report follows Scudday (1973), but is nonetheless a subjective choice and does not necessarily represent the final position of all coauthors on this controversy.

Except for the report by McAllister et al. (1991) on Mesocestoides sp. from C. dixoni, nothing else has been published on the helminth parasites of this whiptail lizard. The purpose of this note, the sixth in a series of reports on helminths of Cnemidophorus (McAllister 1990a, 1990b, 1990c, 1990d; McAllister et al., 1991), is to provide data on the identity, prevalence of infection, and intensity of other parasites harbored by this lizard, and to compare the information with that of the related C. tesselatus.

MATERIALS AND METHODS

Fifty-eight juvenile and adult C. dixoni A (mean [+ or -] 1 S.E. for snout-vent length, SVL = 81.8 [+ or -] 1.1, range 51-99 mm) were collected between June and September 1989 and again in May 1990 from "Campo Nuevo" in San Antonio Canyon, 45 km. N Presidio, Presidio Co. Texas (29[degrees] 53' N, 104[degrees] 29' W, elevation 900 to 1500 m). Lizards were collected with rubber bands or shot with .22-caliber rat shot, preserved in the field with 10 percent formalin, and stored in 70 percent ethanol. Methods for processing hosts and parasites have been described previously (McAllister, 1990a).

Representative helminths have been deposited in the United States National Museum (USNM) Helminthological Collection (USDA, Beltsville, Maryland 20705) as follows: Oochoristica sp. (USNM 81557), O. bivitellobata (USNM 81554-81556), Physaloptera sp. (USNM 81552), Parathelandros texanus (USNM 81553), acanthocephalan cystacanths (USNM 81550-81551). Voucher hosts are deposited in the University of Arkansas Department of Zoology (UADZ).

RESULTS AND DISCUSSION

Twenty-nine (50 percent) of the C. dixoni A were infected with at least one kind of helminth (Table 1). Twenty (69 percent) of these harbored a single species whereas nine (31 percent) were multiply infected with several helminths, including eight with two species and one had three species. There was a significant difference in size (SVL) between uninfected (78.2 [+ or -] 1.7, range 51-91 mm) and infected (85.3 [+ or -] 0.92, 77-99 mm) lizards (t = 3.69, 56 df, P < 0.0005). None of the six juvenile lizards (63.5 [+ or -] 2.9, 51-69 mm) was infected, whereas 56 percent of all adults ([greater than or equal to] 70 mm) harbored parasites. Nevertheless, if juvenile SVL measurements are deleted from the uninfected data, there still remains a significant difference, albeit a lesser one, between uninfected (82.0 [+ or -] 0.95 mm) and infected whiptails (t = 2.48, 50 df, P < 0.01). Indeed, examination of additional immature C. dixoni is necessary before definitive conclusions can be reached regarding prevalence among different size and age classes. However, this preliminary information appears to corraborate prevalence data reported by McAllister (1990c, 1990d), who noted that for large samples of C. exsanguis and C. gularis, which included different size classes, only 15 and 17 percent of immature lizards compared to 44 and 45 percent of the adults were infected, respectively.

The most common helminths were unidentified juvenile acanthocephalan cystacanths of the family Oligacanthorhynchidae. These spiny-headed worms were removed from the mesenteries and muscle fascia of 21 percent of the lizards (86.8 [+ or -] 1.2, 80-93 mm SVL). Interestingly, prevalence of infection was nearly 10-fold higher in C. dixoni A compared to other teiids reported previously to harbor these immature parasites. For example, McAllister (1990b, 1990d) reported cystacanths from two and four percent C. neomexicanus and C. gularis, respectively. In addition, Benes (1985) reported two percent of the C. tigris septentrionalis she examined were infected, whereas Goldberg and Bursey (1990) found only three percent of the C. uniparens they examined harbored cystacanths. Because all C. dixoni A reported herein came from a relatively small geographic area compared to hosts reported above, it is likely they had a greater opportunity to feed on similar food items and, hence, an invertebrate intermediate host required in the life cycle of the unknown acanthocephalan in question.

Larval Physaloptera sp. Rudolphi, 1819, were found in the stomach of 19 percent of the whiptails (85.3 [+ or -] 1.6, 80-99 mm SVL). This accords well with prevalence data on record from other species of Cnemidophorus harboring Physaloptera, which has been reported to range between one and 30 percent (Dyer, 1971; Specian and Whittaker, 1980; Goldberg and Bursey, 1989, 1990; McAllister et al., 1986; McAllister, 1990a, 1990b, 1990c, 1990d).

Two species of cyclophyllidean cestodes of the genus Oochoristica Luhe, 1898, were found in the duodenum of 11 of the whiptails (84.1 [+ or -] 1.7, 78-90 mm SVL). One of these, found in five percent of the lizards, could not be identified positively to species, whereas the other, recovered from 16 percent of the whiptails, was indistinguishable from O. bivitellobata Loewen, 1940. Mature proglottids of the former appeared to contain a single vitellaria, clearly distinguishing it from the latter species, which is characterized by two vitellaria (Loewen, 1940; Brooks and Mayes, 1976). Unfortunately, all specimens were unrelaxed and contracted due to in situ fixation when the host was killed. Examination of properly fixed specimens will be necessary to provide an adequate description and determine whether this cestode represents a new species. Prevalence of O. bivitellobata in other cnemidophorines is typically less than 15 percent but in some cases may be more than 60 percent (Loewen, 1940; Grundmann, 1959; Babero and Matthias, 1967; Telford, 1970; Dyer, 1971; Shoop and Janovy, 1978; Lyon, 1986; Goldberg and Bursey, 1989, 1990; McAllister, 1990b, 1990c, 1990d).

The least common helminth was the oxyurid, Parathelandros texanus Specian and Ubelaker, 1974. Three female worms each were found in the rectum of three lizards (UADZ 3628, 3663, 3783, 82-86 mm SVL) collected in June, July, and August 1989. Other teiids, including C. gularis, C. inornatus, C. tesselatus, and C. tigris, and several iguanid lizards are known to be hosts of this oxyurid (see McAllister, 1990d). Except for a single iguanid reported from Arizona (Walker and Matthias, 1973), the remaining hosts were collected at study sites in Brewster, Jeff Davis, and Presidio counties, Texas (Specian and Ubelaker, 1974; McAllister, 1990d).

An unexpected finding of this survey is the observation that Pharyngodon warneri Harwood, 1932, reported previously from at least eight species of Cnemidophorus, including the related C. tesselatus (see McAllister, 1990d), was not found in C. dixoni A. Inasmuch as P. warneri uses a life cycle not requiring intermediate hosts, it remains elusive why this nematode was absent in C. gularis septemvittatus at the Campo Nuevo study area (McAllister, unpublished observation).

In summary, except for P. warneri, all of the helminths reported from C. tesselatus (McAllister, 1990a; McAllister et al., 1991) are harbored by C. dixoni A. This might be expected given that C. dixoni is included in the tesselatus species group; however, C. dixoni A does not occur in sympatry with C. tesselatus in any part of its range. Rather, C. dixoni B is sympatric with C. tesselatus E in an area about 20 km. N Campo Nuevo at Pinto Canyon, Presidio Co., Texas, whereas C. dixoni A is found with its parental congeners, C. m. marmoratus and C. g. septemvittatus at San Antonio Canyon. Furthermore, C. dixoni A and C. dixoni B are not found in sympatry and whether their parasites are shared will require additional study.
TABLE 1. Helminths found in Cnemidophorus dixoni A. *

 Prevalence
 Number infected/
Helminth number examined Percent

Cestoidea
 Cyclophyllidea
 Oochoristica sp. ** 3/58 5
 O. bivitellobata 9/58 16
Nematoda
 Spirurida
 Physaloptera sp. 11/58 19
Oxyurida
 Parathelandros texanus 3/58 5
Acanthocephala
 Oligacanthorhynchida
 unidentified cystacanths 12/58 21

 Intensity
Helminth x [+ or -] SE (range)

Cestoidea
 Cyclophyllidea
 Oochoristica sp. ** 2.3 [+ or -] 1.3 (1-5)
 O. bivitellobata 4.7 [+ or -] 1.5 (1-13)
Nematoda
 Spirurida
 Physaloptera sp. 2.5 [+ or -] 0.9 (1-11)
Oxyurida
 Parathelandros texanus 1.0 [+ or -] - (1)
Acanthocephala
 Oligacanthorhynchida
 unidentified cystacanths 2.3 [+ or -] 0.8 (1-11)

*Mesocestoides sp. tetrathyridia (Cestoidea: Cyclophyllidea) reported
previously from three of 58 C. dixoni by McAllister et al. (1991).
**Immature adults with genital primordia and unidentifiable mature
adults.


ACKNOWLEDGMENTS

Cordes thanks A. Real, general manager of the Mesquite Ranch, Presidio County, Texas, for lodging and field assistance. Lizard collections were made under the authority of Texas Parks and Wildlife Department permit no. 61 provided through the assistance of D. Riskind, Texas Parks Division, and G. Adams, Texas Resource Protection Branch.

LITERATURE CITED

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Benes, E. S. 1985. Helminth parasites in some central Arizona lizards. Southwestern Nat., 30:467-473.

Bostic, D. L. 1965. Parasites recovered from the teiid lizard, Cnemidophorus hyperythrus beldingi. Southwestern Nat., 10:313.

Brooks, D. R., and M. A. Mayes. 1976. Morphological variation in natural infections of Oochoristica bivitellobata Loewen, 1940 (Cestoidea: Anoplocephalidae). Trans. Nebraska Acad. Sci., 3:20-21.

Densmore, L. D., J. W. Wright, and W. M. Brown. 1989. Mitochondrial DNA analysis and the origin and relative age of parthenogenetic lizards (genus Cnemidophorus). III. C. neomexicanus and the C. tesselatus complex. Evolution, 43:943-957.

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_____. 1990. Helminths of the Arizona striped whiptail, Cnemidophorus inornatus arizonae, and the desert grassland whiptail, Cnemidophorus uniparens (Sauria: Teiidae), from southeastern Arizona. Proc. Helminthol. Soc. Washington, 57:83-86.

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_____. 1990b. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. II. The New Mexico whiptail (Cnemidophorus neomexicanus). J. Wildlife Dis., 26:403-406.

_____. 1990c. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. III. The Chihuahuan spotted whiptail (Cnemidophorus exsanguis). J. Wildlife Dis., 26:544-546.

_____. 1990d. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. IV. The Texas spotted whiptail (Cnemidophorus gularis). Texas J. Sci., 42:381-388.

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Wright, J. W., and C. H. Lowe. 1967. Hybridization in nature between parthenogenetic and bisexual species of whiptail lizards (genus Cnemidophorus). Amer. Mus. Novit., 2286:1-36.

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CHRIS T. MCALLISTER, JAMES E. CORDES, AND JAMES M. WALKER

Renal-Metabolic Lab (151-G), Department of Veterans Affairs Medical Center, 4500 S. Lancaster Road, Dallas, Texas 75216, and Department of Zoology, University of Arkansas, Fayetteville, Arkansas 72701

Present address of Cordes: Department of Biology, Arkansas College, Batesville, Arkansas 72501.
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Author:McAllister, Chris T.; Cordes, James E.; Walker, James M.
Publication:The Texas Journal of Science
Geographic Code:100NA
Date:Aug 1, 1991
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