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Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. VIII. the Gila spotted whiptail (Cnemidophorus flagellicaudus), Sonoran spotted whiptail (Cnemidophorus sonorae), and plateau striped whiptail (Cnemidophorus velox).

ABSTRACT. -- Sixteen of 76 (22 percent) parthenogenetic whiptail lizards (Cnemidophorus) were infected with one or more helminths, including eight of 23 (35 percent) C. flagellicaudus from Arizona and New Mexico, five of 16 (31 percent) C. sonorae from Arizona, and three of 37 (eight percent) C. velox from New Mexico. The following helminths were found: Oochoristica bivitellobata Loewen, 1940, in five (22 percent) C. flagellicaudus, one (six percent) C. sonorae, and two (five percent) C. velox; Physaloptera sp. Rudolphi, 1819, in two (nine percent) C. flagellicaudus, four (25 percent) C. sonorae, and two (five percent) C. velox; Parathelandros texanus Specian and Ubelaker, 1974, in one (four percent) C. flagellicaudus; and acanthocephalan cystacanths in one (four percent) C. flagellicaudus and a single (six percent) C. sonorae. This note, the eighth in a series on helminths of the genus Cnemidophorus, reports parasites in C. flagellicaudus and C. sonorae for the first time and in C. velox for the second time. Key words: Acanthocephala; Cestoidea; Nematoda; Cnemidophorus flagellicaudus, Cnemidophorus sonorae, Cnemidophorus velox; helminths; lizards; survey; Teiidae.

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The New World genus Cnemidophorus contains approximately 55 species of whiptail lizards that occur throughout much of the Americas. Numerous unisexual (parthenogenetic) taxa are common inhabitants of the desert areas of the southwestern United States and adjacent Mexico. Three of these all-female species with restricted ranges include the Gila spotted whiptail, Cnemidophorus flagellicaudus Lowe and Wright, 1964, found in pinon-juniper, oak woodland, open chaparral, streamside grassland, and upper edge of desert grassland from Mohave County, Arizona, to extreme southwestern New Mexico, the Sonoran spotted whiptail, Cnemidophorus sonorae Lowe and Wright, 1964, which occurs in upland habitats of oak woodland, oak and desert grassland, desert shrub, and streamside woodland from southeastern Arizona to northeastern Sonora, Mexico, and the plateau spotted whiptail, Cnemidophorus velox Springer, 1928, that ranges on mountains in pinonjuniper grassland, oak woodland, open chaparral, and lower edges of ponderosa pine and fir forest from central and northern Arizona and northern New Mexico to southern Utah and western Colorado (Stebbins, 1985). The ancestry of these triploid unisexual whiptails indicated by protein electrophoresis (Dessauer and Cole, 1989) is C. burti x C. inornatus x C. burti for C. flagellicaudus and C. sonorae, and C. burti x C. inornatus x C. inornatus for C. velox.

Although some information is available on the natural history and ecology of these three taxa (see Price, 1983), little is known regarding their endoparasites--see Douglas (1966) for data on helminths of 16 C. velox from Colorado. The purpose of this paper, the eighth in a series of reports on helminth parasites of Cnemidophorus (McAllister et al, 1991b), is to provide data on the identity, prevalence, and intensity of parasites infecting these three whiptail lizards and to compare the information with that of their bisexual ancestral species, C. burti and C. inornatus.

MATERIALS AND METHODS

Seventy-six hatchling, juvenile, and adult female whiptails, including 23 C. flagellicaudus--mean [+ or -] 1 SE for snout-vent length (SVL) = 57.8 [+ or -] 3.6, range 36-87 mm, 16 C. sonorae (67.0 [+ or -] 2.5, 51-88 mm), and 37 C. velox (64.2 [+ or -] 2.9, 39-80 mm) were collected between July 1958 and July 1962 and again between May 1974 and July 1990. Sample sizes (in parentheses) were as follows: C. flagellicaudus, Catron (21) and Hidalgo (2) counties, New Mexico; C. sonorae, Cochise (3), Pima (3), and Santa Cruz (8) counties, Arizona, and Hidalgo (2) County, New Mexico; and C. velox, Guadalupe (6), Grant (2), Harding (1), Los Alamos (4), Rio Arriba (8), Sandoval (9), Santa Fe (3), San Juan (3), Socorro (1), and Torrance (1) counties, New Mexico. These lizards previously had been fixed in 10 percent formalin, stored in 70 percent ethanol, and borrowed from the following museum collections: C. flagellicaudus (Museum of Southwestern Biology of the University of New Mexico, UNM 6706, 6720-23, 6725, 9152-53, 9156, 9159-60, 9162-63, 10281, 10334-37, 10363-64, 10441, 30639-40); C. sonorae (University of Colorado Museum, Boulder, UCM 56291-98, and Texas Cooperative Wildlife Collections of Texas A & M University, TCWC 62777-79, 64536, and UNM 39268, 41123, 43965, 50148); and C. velox (UNM 21000, 21713-14, 22024, 22031-32, 22050, 23085, 23103, 23585, 30672-78, 32089-91, 32140, 32467-68, 32956, 36406, 36408-10, 36952-55, 37064-65, 37857, 40951, 40953). Detailed methods for processing hosts and parasites have been described previously (McAllister, 1990a).

Representative helminths have been deposited in the United States National Museum (USNM) Parasite Collection (USDA) at Beltsville, Maryland 20705, as follows: Oochoristica bivitellobata (USNM 81961-63), Physaloptera sp. (USNM 81966-68), Parathelandros texanus (USNM 81969), acanthocephalan cystacanths (USNM 81964-65).

RESULTS AND DISCUSSION

Of 76 individual Cnemidophorus examined, 16 (22 percent) were infected with at least one kind of helminth (Table 1). These included eight (35 percent) of the C. flagellicaudus, five (31 percent) of the C. sonorae, and three (eight percent) of the C. velox. Multiple infections of two helminths were found in all three species of whiptail lizards.

Third stage larvae of the spirurid nematode, Physaloptera sp. Rudolphi, 1819, were found in stomachs of all three whiptails (combined mean intensity = 1.3 [+ or -] 0.3, range 1-3), including two C. flagellicaudus (UNM 9152, 10363; 47 and 70 mm SVL) collected in April and July 1962 in Catron County, New Mexico, four C. sonorae (UCM 56292-93, 56297, TCWC 64536; 70-73 mm SVL) collected in June 1986 and August 1990 in Santa Cruz and Pima counties, Arizona, and two C. velox (UNM 22031, 40953; 75 and 77 mm SVL) taken in July 1958 and June 1970 in Grant and Santa Fe counties, New Mexico. These spirurids are common helminths of North and South American whiptail lizards (see McAllister et al., 1991b) and have been reported from C. inornatus and C. burti (Goldberg and Bursey, 1989, 1990).

Twenty-eight linstowiid tapeworms, Oochoristica bivitellobata Loewen, 1940, were recovered from the duodenum of eight whiptails (combined mean intensity = 3.5 [+ or -] 0.5, range 2-5), including 19 from five C. flagellicaudus (UNM 9159-60, 9162-63, 10441; 82.4 [+ or -] 2.3, 74-87 mm SVL) taken in July 1962 in Catron County, New Mexico, five specimens from a single C. sonorae (TCWC 12777, 51 mm SVL) obtained in May 1984 in Cochise County, Arizona, and two each from two C. velox (UNM 22031, 30676; 48 and 77 mm SVL) collected in July 1958 and June 1973 in Sandoval and Grant counties, New Mexico. Mean intensity was 3.8 [+ or -] 0.5 (3-5) for C. flagellicaudus, 5.0 [+ or -] 0.0 (5) for C. sonorae, and 2.0 [+ or -] 1.4 (2) for C. velox. This cestode is apparently one of the most ubiquitous and apparently host specific of the genus as it now has been reported from 14 species of Cnemidophorus from various localities in 11 states (Table 2); overall prevalence of infection is low in that 206 of 1293 (16 percent) of the lizards harbored this tapeworm. When whiptails are divided into bisexual and unisexual taxa, prevalence of O. bivitellobata in six bisexual species is 164 of 953 (17 percent) and in eight unisexual species is 42 of 340 (12 percent). In addition, Douglas (1966) reported O. bivitellobata from northern plateau lizards, Sceloporus undulatus elongatus Stejneger, 1890, from Mesa Verde National Park, Colorado. However, voucher specimens were not mentioned and apparently are not available for verification (J. E. Ubelaker, personal communication). Interestingly, the only Oochoristica previously reported from sceloporiine lizards is O. scelopori Voge and Fox, 1950 (see McAllister et al., 1985). For these reasons, S. u. elongatus is not included in the table.

Specimens of the oxyurid nematode, Parathelandros texanus Specian and Ubelaker, 1974, were found in the rectum of a single juvenile C. flagellicaudus (UNM 6723, SVL 48 mm) obtained in April 1962 in Catron County, New Mexico. Five other whiptails (including C. inornatus) and five iguanids from southwestern Texas (Specian and Ubelaker, 1974; McAllister et al., 1991b) and Urosaurus ornatus from Arizona (Walker and Matthias, 1973; Specian and Ubelaker, 1974) have been reported as hosts. Thus, New Mexico represents a new geographic locality for this helminth.

Oligacanthorychid acanthocephalan cystacanths were recovered from the body cavity and muscle fascia of a single C. flagellicaudus (UNM 9162, SVL 82 mm) obtained in July 1962 in Catron County, New Mexico, and a C. sonorae (TCWC 64536, SVL 71 mm) taken in June 1986 in Pima County, Arizona. Cystacanths are apparently common helminths of whiptails as they have been reported previously from C. neomexicanus (McAllister, 1990b), C. gularis (McAllister, 1990d), C. dixoni (McAllister et al., 1991a), C. tigris (Benes, 1985), and C. uniparens (Goldberg and Bursey, 1990).

In accordance with data from helminth surveys on other whiptail lizards, C. flagellicaudus, C. sonorae, and C. velox have a depauperate parasite fauna and share parasites with most other congeners, regardless of geographic location or even ancestry. As noted by Goldberg and Bursey (1990) for C. uniparens and McAllister et al. (1991a) for C. dixoni, it is unknown why Pharyngodon warneri Harwood, 1932, a common oxyurid in other whiptails (see McAllister, et al., 1991b), was not recovered from C. flagellicaudus, C. sonorae, or C. velox. Indeed, this was not expected because P. warneri has been reported from the parental C. inornatus (Specian and Ubelaker, 1974; Goldberg and Bursey, 1990), whereas a similar species, P. cnemidophori Read and Amrein, 1953, was reported from the other parental form, C. burti (Goldberg and Bursey, 1989). In addition, C. flagellicaudus and C. exsanguis (a host for P. warneri--see McAllister 1990c), are sympatric in Catron County, New Mexico (Cueller, 1979), and C. velox is sympatric with C. inornatus and C. uniparens (Wright, 1968). Thus, opportunity should exist for direct infection by P. warneri, but experimental transmission studies will be necessary to determine why some whiptail lizards may not serve as hosts of P. warneri.
TABLE 1. Helminths found in Cnemidophorus flagellicaudus from New
Mexico, C. sonorae from Arizona, and C. velox* from New Mexico.

 Host
 C. flagellicaudus C. sonorae C. velox
Helminth Number infected/number examined (percent)

Cestoidea
 Cyclophyllidea
 Oochoristica bivitellobata 5/23 (22)** 1/16 (6)** 2/37 (5)
Nematoda
 Spirurida
 Physaloptera sp. 2/23 (9)** 4/16 (25)** 2/37 (5)**
Oxyurida
 Parathelandros texanus 1/23 (4)** -- --
Acanthocephala
 Oligacanthorhynchida
 unidentified cystacanths 1/23 (4)** 1/16 (6)** --

*Douglas (1966) previously reported O. bivitellobata, Phyllodistomum sp.
Braun, 1899, and Spauligodon (syn. Pharyngodon) giganticus (Read and
Amrein, 1953) Skrjabin, Schikhobalova, and Lagodovskaja, 1960, from C.
velox.
**New host record.

TABLE 2. A summary of the bisexual and unisexual whiptail lizards
reported to be hosts of Oochoristica bivitellobata Loewen, 1940.

Host Locality Prevalence* Reference

Bisexual taxa
 Cnemidophorus burti Arizona 1/57 (2) Goldberg and
 Bursey, 1989
 C. gularis New Mexico, Texas 3/289 (1) McAllister, 1990d
 C. hyperythrus California 5/104 (5) Bostic, 1965
 C. inornatus Arizona 10/78 (13) Goldberg and
 Bursey, 1990
 C. sexlineatus Kansas 91/147 (62) Loewen, 1940
 Nebraska 3/3 (100) Brooks and Mayes,
 1976
 2/64 (3) Shoop and Janovy,
 1978
 South Dakota 13/26 (50) Dyer, 1971
 C. tigris California 13/49 (27) Telford, 1970
 Idaho 13/32 (41) Lyon, 1986
 Nevada 5/97 (5) Babero and
 Matthias, 1967
 Utah 5/7 (71) Grundmann, 1959
Unisexual taxa
 C. dixoni Texas 9/58 (16) McAllister et
 al., 1991
 C. exsanguis New Mexico, Texas 7/87 (8) McAllister, 1990c
 C. flagellicaudus New Mexico 5/23 (22) This report
 C. neomexicanus New Mexico, Texas 7/61 (11) McAllister, 1990b
 C. sonorae Arizona 1/16 (6) This report
 C. tesselatus** Texas 3/27 (11) McAllister, 1990a
 C. uniparens Arizona 8/31 (26) Goldberg and
 Bursey, 1990
 C. velox Colorado ? Douglas, 1966
 New Mexico 2/37 (5) This report

*Number infected/number examined (percent).
**Probable host.


ACKNOWLEDGMENTS

I thank A. L. Schueler and H. L. Snell (UNM), J. R. Dixon (TCWC), and H. M. Smith (UMC) for loaning specimens used in this study.

LITERATURE CITED

Babero, B. B., and D. V. Matthias. 1967. Thubunaea cnemidophorus n. sp., and other helminths from lizards, Cnemidophorus tigris, in Nevada and Arizona. Trans. Amer. Micros. Soc., 86:173-177.

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.

Cueller, O. 1979. On the ecology of coexistence in parthenogenetic and bisexual lizards of the genus Cnemidophorus. Amer. Zool., 19:773-786.

Dessauer, H. C., and C. J. Cole. 1989. Diversity between and within nominal forms of unisexual teiid lizards. Pp. 49-71, in Evolution and ecology of unisexual vertebrates (R. M. Dawley and J. P. Bogart, eds.), Bull. New York State Mus., Albany, 466: iv + 1-302.

Douglas, C. L. 1966. Amphibians and reptiles of Mesa Verde National Park, Colorado. Univ. Kansas Publ., Mus. Nat. Hist., 15:711-744.

Dyer, W. G. 1971. Some helminths of the six-lined lizard, Cnemidophorus sexlineatus, in South Dakota. Proc. Helminth. Soc. Washington, 38:256.

Goldberg, S. R., and C. R. Bursey. 1989. Helminths of the giant spotted whiptail, Cnemidophorus burti stictogrammus (Sauria: Teiidae). Proc. Helminth. Soc. Washington, 56:86-87.

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

Grundmann, A. W. 1959. Parasites recovered from six species of Utah lizards. J. Parasitol., 45:394.

Loewen, S. L. 1940. On some reptilian cestodes of the genus Oochoristica (Anoplocephalidae). Trans. Amer. Micros. Soc., 59:511-518.

Lyon, R. E. 1986. Helminth parasites of six lizard species from southern Idaho. Proc. Helminth. Soc. Washington, 53:291-293.

McAllister, C. T. 1990a. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. I. The Colorado checkered whiptail (Cnemidophorus tesselatus). J. Wildlife Dis., 26:139-142.

_____. 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.

McAllister, C. T., J. E. Cordes, and J. M. Walker. 1991a. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. VI. The gray-checkered whiptail (Cnemidophorus dixoni). Texas J. Sci., 43:309-314.

McAllister, C. T., S. E. Trauth, and D. B. Conn. 1991b. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. VII. The six-lined racerunner, Cnemidophorus sexlineatus. Texas J. Sci., 43:391-397.

McAllister, C. T., S. E. Trauth, and J. E. Ubelaker. 1985. Oochoristica crotaphyti n. sp. (Eucestoda: Linstowiidae) from Crotaphytus collaris (Lacertilia: Iguanidae) in northern Arkansas. J. Parasit., 71:803-807.

Price, A. H. 1983. Annotated bibliography of the genus Cnemidophorus in New Mexico. Smithsonian Herp. Inf. Serv., 58:1-92.

Shoop, W. L., and J. Janovy, Jr. 1978. Adult cestodes from the coelomic cavity of the teiid lizard, Cnemidophorus sexlineatus. J. Parasitol., 64:561-562.

Specian, R. D., and J. E. Ubelaker. 1974. Parathelandros texanus n. sp. (Nematoda: Oxyuridae) from lizards in west Texas. Trans. Amer. Micros. Soc., 93:413-415.

Stebbins, R. C. 1985. A field guide to western reptiles and amphibians. Houghton Mifflin, Boston, 336 pp.

Telford, S. R. 1970. A comparative study of endoparasitism among some California lizard populations. Amer. Midland Nat., 83:516-554.

Walker, K. A., and D. V. Matthias. 1973. Helminths of some northern Arizona lizards. Proc. Helminth. Soc. Washington, 40:168-169.

Wright, J. W. 1968. Variation in 3 sympatric sibling species of whiptail lizards (genus Cnemidophorus). J. Herp., 1:1-20.

CHRIS T. MCALLISTER

Renal-Metabolic Laboratory (151-G), Department of Veterans Affairs Medical Center, 4500 S. Lancaster Road, Dallas, Texas 75216
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Date:May 1, 1992
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