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Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. VII. The six-lined racerunner, Cnemidophorus sexlineatus.

ABSTRACT. -- Fifty-one six-lined racerunners, Cnemidophorus sexlineatus, from 17 counties of Arkansas were examined for parasites. Twenty-five (49 percent) were infected with one or more helminths: two (four percent) with tetrathyridia of Mesocestoides Vaillant, 1863; 10 (20 percent) with larval spirurid nematodes, Abbreviata sp.; three (six percent) with Thubunaea cnemidophorus Babero and Matthias, 1967; and 15 (29 percent) with oxyurid nematodes, Pharyngodon warneri Harwood, 1932. Prevalence of infection varied among different age, sex, and size classes of C. sexlineatus--62 percent of adult males, 38 percent of adult females, and 25 percent immatures harbored parasites. This paper, the seventh in a series of reports on parasites of Cnemidophorus, represents the first time C. sexlineatus from Arkansas have been surveyed for helminths. Key words: cestodes; helminths; nematodes; parasites; racerunners; whiptail lizards; Cnemidophorus sexlineatus.

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The six-lined racerunner, Cnemidophorus sexlineatus (Linnaeus, 1766), is a moderately-sized bisexual whiptail lizard that ranges both east and west of the Mississippi River from Maryland to Florida westward to New Mexico and north to Wyoming, South Dakota, Minnesota, and Wisconsin (Conant, 1975). This teiid occupies a variety of habitats including river floodplains, open grasslands, rocky outcrops, and open woody fields. Much has been documented on the biology of C. sexlineatus (Fitch, 1958; Hoddenbach, 1966; Clark, 1976; Trauth, 1983), including information on its helminth parasites (Harwood, 1932; Loewen, 1940; Dyer, 1971; Brooks and Mayes, 1976; Shoop and Janovy, 1978). However, with the exception of Harwood's (1932) report on six-lined racerunners from southeastern Texas, which involved only six lizards, the remaining studies were focused on northern populations of C. sexlineatus.

The purposes of this paper, the seventh in a series of reports on helminths of Cnemidophorus, is to provide data on the prevalence, intensities, and identities of endoparasites from a survey on southern populations of C. sexlineatus, compare those data with previously published information on more northern populations, and present a summary on the parasites of this common whiptail lizard.

MATERIALS AND METHODS

A total of 51 juvenile and adult C. sexlineatus--27 males, 24 females; mean [+ or -] snout-vent length (SVL) = 69.9 [+ or -] 1.3, range 41-90 mm--was collected monthly between 1973 and 1980 and again between August 1989 and November 1990 from the following counties in Arkansas (sample sizes in parentheses): Baxter (11), Boone (1), Cleburne (1), Conway (9), Crawford (1), Dallas (1), Johnson (5), Logan (1), Marion (5), Montgomery (1), Polk (1), Pope (3), Scott (1), Sebastian (1), Searcy (2), Washington (4), and Yell (3). Of these, 31 were specimens previously stored in 70 percent ethanol and housed in the Arkansas State University Museum of Zoology (ASUMZ); the remainder (N = 20) were collected alive and examined for fresh material. Methods for processing museum specimens and live hosts and staining and preparation of parasites have been described in detail (McAllister, 1990d).

Representative helminths have been deposited in the United States National Parasite Collection (USDA, Beltsville, Maryland 20705) as follows: Mesocestoides sp. (USNM 81900), Abbreviata sp. (USNM 81910-81911), Thubunaea cnemidophorus (USNM 81908-81909), Pharyngodon warneri (USNM 81907). All voucher hosts are deposited in the ASUMZ.

RESULTS AND DISCUSSION

Twenty-five (49 percent) C. sexlineatus were infected with at least one kind of helminth (Table 1). The majority (84 percent) harbored a single species, whereas multiple infections of two species were found in three (12 percent) lizards; one (four percent) had three species. The overall snoutvent lengths of infected lizards (72.3 [+ or -] 1.2, range 62-84 mm) and uninfected lizards (67.3 [+ or -] 2.2, 41-90 mm) were significantly different (t = 2.03, 49 df, P < 0.01). Of the 20 lizards collected alive, blood was negative for plasmodial or trypanosomal parasites, and feces were negative for coccidian oocysts.

There was a two-fold difference in prevalence among the sexes as 17 or 65 percent of all males and eight or 32 percent of all females harbored parasites. Prevalence also varied among different age, sex, and size classes of C. sexlineatus; 62 percent of adult males and 38 percent of adult females were infected, whereas only a single immature lizard was infected (Table 2). These data accord well with prevalence information from a survey on a large sample of C. gularis (McAllister, 1990d).

As with other species of Cnemidophorus (McAllister, 1990a, 1990b, 1990c, 1990d), the most common parasite of C. sexlineatus was the oxyurid nematode, Pharyngodon warneri Harwood, 1932. This pinworm was found in the colon and rectum of 15 lizards (71.3 [+ or -] 1.6, 59-79 mm SVL), including 11 (41 percent) of the males and four (17 percent) of the females. Harwood (1932) originally described P. warneri from C. sexlineatus from Huntsville, Walker Co., Texas. The only other report of the parasite from this host was by Dyer (1971). Arkansas represents a new distributional record for P. warneri (see McAllister, 1990d, for other localities).

Larval spirurid nematodes, Abbreviata sp., were found in the stomach of 20 percent of the racerunners (75.0 [+ or -] 1.5, 69-84 mm SVL), including six (22 percent) of the males and four (17 percent) of the females. The majority of Abbreviata have been reported from hosts that occur outside of North America (Baker, 1987). However, four turtles and two lizards from the United States have been reported to harbor Abbreviata, including Terrapene ornata from Oklahoma (Hill, 1941), Chrysemys picta marginata, Chelydra serpentina, and Emydoidea blandingii from Wisconsin (Morgan, 1945), Sceloporus undulatus from Illinois, Maryland, New York, and Wisconsin (Morgan, 1945), and Crotaphytus collaris from Arkansas (McAllister and Trauth, 1985). One species, A. ranae (Walton, 1931) Morgan, 1941, from anuran amphibians, has been designated a species inquirenda (see Baker, 1987). Indeed, the genus is badly in need of revision.

Another spirurid, Thubunaea cnemidophorus Babero and Matthias, 1967, was recovered from the stomach of only three C. sexlineatus (68.3 [+ or -] 2.0, 65-72 mm SVL). The species was originally described from western whiptails, C. tigris from Nevada (Babero and Matthias, 1967). In addition, T. cnemidophorus has been reported from C. burti stictogrammus from Arizona (Goldberg and Bursey, 1989) and the rattlesnakes, Crotalus cerastes, C. mitchellii, and C. scutulatus (Babero and Emmerson, 1974). However, these snakes may be incidental hosts that were secondarily infected from eating parasitized lizard prey. The present report represents a new host and locality record for T. cnemidophorus.

[FIGURES 1-2 OMITTED]

Tetrathyridia of Mesocestoides sp. were found encapsulated in the liver, intestinal mesenteries, and musculature of an adult male and female C. sexlineatus (72 and 84 mm SVL) from Baxter and Johnson counties. Tetrathyridia were encapsulated either in groups (Fig. 1) or individually (Fig. 2) throughout the infected tissues. In addition, one of these hosts contained numerous free tetrathyridia in its coelomic cavity. None of the tetrathyridia showed any morphological evidence of asexual proliferation such as buds or multiple or split scoleces. Thus, as with the vast majority of Mesocestoides tetrathyridia (Conn, 1990), including those from other Cnemidophorus sp. (McAllister et al., 1991b), these appear to be of the nonproliferative type. Dyer (1971) reported Mesocestoides sp. from C. sexlineatus from South Dakota. Other species of Cnemidophorus have been reported to harbor Mesocestoides sp. tetrathyridia, including C. tigris from Arizona (Babero and Matthias, 1967; Benes, 1985), California (Mankau and Widmer, 1977), and Nevada (Babero and Matthias, 1967), C. b. stictogrammus from Arizona (Goldberg, 1987), and C. dixoni, C. gularis septemvittatus, C. marmoratus, and C. tesselatus from Texas and Colorado (McAllister et al., 1991b). This investigation represents the first time Mesocestoides sp. tetrathyridia has been reported from Arkansas.

A summary of the parasites thus far reported from C. sexlineatus is presented in Table 3. As expected, there is some similarity between the helminth parasites of southern and northern populations of C. sexlineatus. Fifty percent of the helminths reported herein have been reported previously from C. sexlineatus, whereas two others are reported for the first time in this host. Interestingly, the cyclophyllidean tapeworm, Oochoristica bivitellobata Loewen, 1940, was not recovered during the present study but has been found in C. sexlineatus from other localities (Table 3). Indeed, this helminth has been reported from a total of 109 of 240 (45 percent) C. sexlineatus. However, prevalence of O. bivitellobata in other Cnemidophorus can range between one and 16 percent (McAllister, 1990b, 1990c, 1990d; McAllister et al., 1991a) and its prevalence in Arkansas C. sexlineatus also may be low.

Lastly, Werth (1972) reported "an unidentified nematode" from C. sexlineatus as well as three other sympatric lizards (C. collaris, Sceloporus undulatus, and Holbrookia maculata) in Kansas. Assuming the nematode was found in stomach contents, it likely represented a species of spirurid. However, without having voucher specimens for examination, their identity will never be known. This further emphasizes the need for depositing parasite vouchers in a museum collection so they may examined at a later date.
TABLE 1. Helminths found in Cnemidophorus sexlineatus from Arkansas.

 Prevalence
 Number infected/
Helminth number examined Percent

Cestoidea
 Cyclophyllidea
 Mesocestoides sp. 2/51 4
Nematoda
 Spirurida
 Abbreviata sp. 10/51 20
 Thubunaea cnemidophorus 3/51 6
 Oxyurida
 Pharyngodon warneri 15/51 29

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

Cestoidea
 Cyclophyllidea
 Mesocestoides sp. --*
Nematoda
 Spirurida
 Abbreviata sp. 5.7 [+ or -] 1.6 (1-16)
 Thubunaea cnemidophorus 24.0 [+ or -] 13.8 (1-45)
 Oxyurida
 Pharyngodon warneri 40.8 [+ or -] 10.5 (1-100)

*Numerous tetrathyridia were encapsulated in tissues and impossible to
count.

TABLE 2. Prevalence of helminths infecting different age, sex, and size
classes of C. sexlineatus from Arkansas.

Age, sex, and size class* Prevalence

Juveniles (41-59 mm SVL) 1/4 (25%)
Adult females (60-90 mm SVL) 8/21 (38%)
Adult males (60-85 mm SVL) 16/26 (62%)
All adults (60-90 mm SVL) 24/47 (51%)
All lizards (41-90 mm SVL) 25/51 (49%)

*Lizards that reached SVL's [greater than or equal to] 60 mm were
considered sexually mature (see Trauth, 1983).

TABLE 3. Parasites reported from Cnemidophorus sexlineatus from various
localities of North America.

Parasite Locality Prevalence Reference

Cestoidea
 Cyclophyllidea
 Mesocestoides sp. South Dakota 2/23 (9%) Dyer, 1971
 Arkansas 2/51 (4%) This report
 Oochoristica
 bivitellobata Kansas 91/147 (62%) Loewen, 1940
 South Dakota 13/26 (50%) Dyer, 1971
 Nebraska 3/3 (100%) Brooks and Mayes, 1976
 2/64 (3%) Shoop and Janovy, 1978
Nematoda
 Spirurida
 Abbreviata sp. Arkansas 10/51 (20%) This report
 Physaloptera sp. South Dakota 7/26 (27%) Dyer, 1971
 Thubunaea
 cnemidophorus Arkansas 3/51 (6%) This report
 Oxyurida
 Pharyngodon
 warneri Texas 2/6 (33%) Harwood, 1932
 South Dakota 19/26 (73%) Dyer, 1971
 Arkansas 15/51 (29%) This report
Arthropoda
 Acari
 Eutrombicula
 alfreddugesi Kansas 98/108 (91%) Loomis, 1956
 Texas -- Loomis and Crossley,
 1963


ACKNOWLEDGMENTS

C.T.M. and S.E.T. thank the Arkansas State Game and Fish Commission for Scientific Collecting Permits Nos. 775 and 831, respectively.

LITERATURE CITED

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Hill, W. 1941. Physaloptera terrapenis, a new nematode from a tortoise. Trans. Amer. Microsc. Soc., 90:59-64.

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

Loomis, R. B. 1956. The chigger mites of Kansas (Acarina, Trombiculidae). Univ. Kansas Sci. Bull., 37:1195-1443.

Loomis, R. B., and D. A. Crossley. 1963. New species and new records of chiggers (Acarina: Trombiculidae) from Texas. Acarologia, 5:371-385.

Mankau, S. K., and E. A. Widmer. 1977. Prevalence of Mesocestoides (Eucestoda: Mesocestoididea) tetrathyridia in southern California reptiles with notes on the pathology in the Crotalidae. Japanese J. Parasitol., 26:256-259.

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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.

McAllister, C. T., and S. E. Trauth. 1985. Endoparasites of Crotaphytus collaris collaris (Sauria: Iguanidae) from Arkansas. Southwestern Nat., 30:363-370.

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., J. E. Cordes, D. B. Conn, J. Singleton, and J. M. Walker. 1991b. Helminth parasites of unisexual and bisexual whiptail lizards (Teiidae) in North America. V. Mesocestoides sp. tetrathyridia (Cestoidea: Cyclophyllidea) from four species of Cnemidophorus. J. Wildlife Dis., 27:494-497.

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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.

Trauth, S.E. 1983. Nesting habitat and reproductive characteristics of the lizard Cnemidophorus sexlineatus (Lacertilia: Teiidae). Amer. Midland Nat., 109:289-299.

Werth, R. J. 1972. Lizard ecology: evidence of competition. Trans. Kansas Acad. Sci., 75:285-300.

CHRIS T. MCALLISTER, STANLEY E. TRAUTH, AND DAVID BRUCE CONN

Renal-Metabolic Laboratory (151-G), Department of Veterans Affairs Medical Center, 4500 S. Lancaster Road, Dallas, Texas 75216; Department of Biological Sciences, Arkansas State University, State University, Arkansas 72467; and Department of Biology, St. Lawrence University, Canton, New York 13617
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Author:McAllister, Chris T.; Trauth, Stanley E.; Conn, David Bruce
Publication:The Texas Journal of Science
Geographic Code:100NA
Date:Nov 1, 1991
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