Great Basin Naturalist

Volume 57 | Number 3 Article 12

7-31-1997 Helminths from the Sonoran spotted whiptail, Cnemidophorus sonorae, and the , Cnemidophorus tigris (Sauria: ), from southern with comments on Abbreviata terrapenis (Nematoda: Physalopteridae) Stephen R. Goldberg Whittier College, Whittier,

Charles R. Bursey Pennsylvania State University, Shenango Campus, Sharon, Pennsylvania

Hay Cheam Whittier College, Whittier, California

Follow this and additional works at: http://scholarsarchive.byu.edu/gbn

Recommended Citation Goldberg, Stephen R.; Bursey, Charles R.; and Cheam, Hay (1997) "Helminths from the Sonoran spotted whiptail, Cnemidophorus sonorae, and the western whiptail, Cnemidophorus tigris (Sauria: Teiidae), from southern Arizona with comments on Abbreviata terrapenis (Nematoda: Physalopteridae)," Great Basin Naturalist: Vol. 57: No. 3, Article 12. Available at: http://scholarsarchive.byu.edu/gbn/vol57/iss3/12

This Note is brought to you for free and open access by the Western North American Naturalist Publications at BYU ScholarsArchive. It has been accepted for inclusion in Great Basin Naturalist by an authorized administrator of BYU ScholarsArchive. For more information, please contact [email protected]. Creat Ba.<;in Katul'albi( 57(3), © 1997, pp. 273-277

HELMINTHS FROM THE SONORAN SPOTTED WHIPTAIL, CNEMlDOPHORUS SONORAE, AND THE WESTERN WHIPTAIL, CNEMIDOPHORUS TIGRIS (SAURIA: TEIIDAE), FROM SOUTHERN ARIZONA WITH COMMENTS ON ABBREVIATA TERRAPENIS (NEMATODA: PHYSALOPTERIDAE)

Stephen R. Goldbergl , Charles R. Bursey2, and Hay Cheaml

Key words: Cn.t:miduphorus SOlLorae, Cnemidophorus tigris, Teiidae, helrnilltJu, Nematoda, c&"Uxla, Acanthocephala, Arizo116.

Cnemido-phorus sonorae Lowe and \Vright, (LAGM) and the University of Arizona (UAZ) 1964, the Sonoran spotted whiptail, occurs and examined; collection data are given in the fl"om southeastern Arizuna to northeastern Appendix. The were originally pre­ Sonora and east to western ; Cne­ served in 10% formalin or BOllin's fixative and midophorus tigris Baird and Girard, 1852, the stored in 70% ethanol. The body cavity was western whiptail, ranges from and opened and the gastrointestinal tract was south through California to Baja Califor­ excised by cutting across the esophagus and nia and Coahuila, Mexico, and eastward to rectum. The esophagus, stomach, small intes­ western , New Mexico, and Texas tines, and large intestines were slit longitudi­ (Stebhins 1985). Helminths have been previ­ nally and examined separately under a dissect­ ously reported from Cnemidophorus sonorae ing microscope. The body cavity and liver were by McAllister (1992) and Cnemidophorus tigris also examined. Each helminth was removed by Grundmann (1959), Babero and Matthias and initially placed in a drop of glycerol on a (1967), Telford (1970), Specian and Ubelaker glass slide. Nematodes were identified Ii'om (1974a, 1974b), Benes (1985), and Lyon (1986). these temporary mounts. ecstacies were stained Abbreviata ten'apenis (Hill 1945) Morgan, with hematoxylin, mounted in balsam, and iden­ 1945 was originally deseribcd from specimens tified. AcanthlK.-ephalans were cleared. in xylene, taken from 7 ornate box turtles (TefTapene mounted in balsam, and assigned to . arnata) collected fi-om widely separated points Tenninology usage is in accordance with Mar­ in Oklahoma (Hill 1945). The 1st host to golis et al. (1982). be repol'ted fol' this helminth was ScelOl'orus Cnemido-p/lOTUs Sonorae was found to har­ jarrovii, also collected from widely separated bor 2 ofcestodcs, OochOlistica bioitel­ points in Arizona, New Mexico, and Mexico labala Loewen, 1940 aod 0. 1IUICf1IUsteri Bursey (Goldberg et al. 1995, 1996). The purpose of and Goldberg, 1996; and 3 species of nema­ this paper is to report on a helminthological todes, Abbreoiala ten'apenis, Pharyngodon examination of Cnem.idophorus S01lorae and wameli Harwood, 1932, and Thub"naea ene­ Cflemia.ophoru.s tigris from southern Alizona rnidophorus Babero aod Matthias, 1967. Cn"mi­ and the presence of A. terrapenis in these 2 dophorus tigris was found to harbor 1 species addilinnal lizard hosts. of cestode, 0. hivitellobutu; 2 species of nema­ Twenty-one female Cnetnidophorus SOllorae todes, A. terrapellis and P. warneli; and cysta­ (mean snout-vent length [SVL] = 73.2 rom + canths of a species of Acanthocephala, Cmtro­ 5.6 s, range 60-80) and 82 Cllemidophorus rhynchus sp. Prevalences and mean intensities tigris (28 females, 54 males; mean SVL = 65.6 for these helminths are given in Table I. The in­ mm + 10.1 s, I'ange 34-82 mrn) were harrowed fection prevalence between males and females fi-om the herpctology collections of the Nat­ of C. tigris was not significantly diffcrent (for ural History Museum of Los Angeles County A. terrape"is, X2 = 0.17, 1 dE, P > 0.05; for P.

IDcpa.tl1W1lt of Biolugy, Whittier C"llc~, Wloinier, CA 9OGO.'l. 2\)epm1mOIlt of Biology. Penllsyh·""i3 Slllte UJlivenily, Sheua'lgfl Campu... 147 Shell~'ll;<) A'~lue. Sh:!.mo. PA 16146.

273 274 GREAT BASIN NATURALIST [Volume 57

TABLE 1. Gastrointestinal helminths of21 Cnemidophorus sonorae and 82 C. tigris from Pima County; AZ.

Helminth

Oochoristica bivitellobata Oochoristica macallisferi Abbreviata terrapenis Pharyngodon warneri Thubunaea cnemidoplwru.s Centrorhynchus sp.

III _ estlplmgus, 1, _ ,tomach, c - small intestine, d ,. large intestine 2""w h()'l re<.~)rd

wameri, x2 = 0.21, 1 df, P > 0.05). Cnemi­ lizard Scelopoms undulatus (M organ 1941, dophorus sonorae is a new host record for 0. McAllister and Trauth 1985). Adults ofAbbre­ macallisteri, A. terrapenis, P. wamen, and T. viata terrapenis have previously been reported cnemidophorus; C tigris is a new host record from Sceloporus jarrovii in Arizona, New Mex­ for A. terrapenis. Helminths were placed in vials ieo, and Mexico (Goldberg et al. 1995, 1996). of alcohol and deposited in the u.s. National This is also the 1st report of 0. macallisteri Parasite Collection (USNPC), Beltsville, Mary­ from a teiid lizard, although unidentified species land (accession numbers in Appendix). of Oochoristica have heen reported from Cne­ Oochoristica bivitellobata, Pharyngodon midophoms dixoni, C. gularis, and C. tesselatus wameri, and Thuhunaea cnemidophorus have (McAllister 1990a, 1990d, McAllister, Cordes, been previously reported in North American and Walker 1991). ln Arizona, Benes (1985) re­ lizards (Table 2) and may be limited to teiid ported OachoJistica from Cnemidophorus tigJis, lizards. The occurrence of T. cnemidophorus Coleonyx variegatus, Phrynosoma solare, Scelo­ in the crotalid snakes Crotalus cerastes, C. porus magister, and Uta stansburiana, but did mitchelli, and C. scutulatus by Babero and not identify the species. Emmerson (1974) needs further study to Abbreviata terrapenis is a heteroxenous determine if the snakes are indeed hosts, or if physalopterid helminth with an indirect life the parasites were present in lizards that the cycle involving an insect intermediate host snakes had ingested. McAllister (1992) ques­ (Anderson 1992). Echternacht (1967) reported tioned the determination of 0. bivitellobata in that termites are the major dietroy component Sceloporus undulatus and suggested that it for C. sonorae and C. tigris from the Santa Rita probably is Oochoristica scelopori; thus, S. un­ Mountains, Pima County, Arizona, represent­ dulatus is not included in Table 2. Species of ing over 90% of all prey organisms consumed. Centrorhynchus typically use arthropods (prob­ Mitchell (1979) reported a predominance of ahly insects) as intermediate hosts and primar­ termites in the diets of C. sonorae and C. tigris ily birds of prey as definitive hosts (Petro­ in Cochise County, southeastern Arizona. Vitt chenko 1958). The occasional presence of a and Ohmart (1977) similarly found that ter­ cystacanth in the stomach of an insectivore mites compose 76% of the diet of C. tigris could be expected. One nematode not found living along the Colorado River in western in these lizards, but frequently associated with Arizona. Pianka (1970) reported that, while teiid lizards, is Parathelandros texanus Specian southern c. tigris populations eat large quanti­ and Ubelaker, 1974. This helminth may be ties of termites, northern populations (Idaho, limited to west Texas (see Baker 1987). , ) utilize other food types and This is the first report of adult Abbreviata consume few termites. Iftermites serve as inter­ terrapenis from teiid lizards, although larvae mediate hosts for Abbreviata terrapenis, low of Abbreviata sp. have been reported from C. frequencies of these insects in the diets of C. sexlineatus by McAllister, Trauth, and Conn tigris from northern populations might account (1991). Larvae of Abbreviata sp. have also for the ahsence of A. terropenis in the studies been reported from the crotaphytid lizard of these populations by Grundmann (1959), Crotaphytus collaris and the phrynosomatid Babero and Matthias (1967), and Lyon (1986). 1997] NOTES 275

TABLE 2. Reports of Oochoristica biviteUobata, Phnryngodon warner£, and Thubunaea cnemidophorus from teiicl lizards.

Helminth Host Locality Prevalence Reference Oochoristica biviteUobata Cnemidophorus burn Arizona 1;57 (2%) Goldberg and Bursey 1989 C. dixoni Texas 9158 (16%) McAllister, Cordes, and Walker 1991 C. exsanguis New Mexico, Texas 7/87 (8%) McAllister 199Qc C. flageUicaudus New Mexico 5/2:3 (22%) McAllister 1992 C. gularis New Mexico, Texas 3/289 (1%) McAllister 1990d Texas 1;133 (1%) McAllister et al. 1995 C. hyperythrus California 5/104 (5%) Bostic 1965 C. inornatus Arizona 10(78 (13%) Goldberg and Bursey 1990 C. neomexicanus New Mexico, Texas 7/61 (11%) McAllister 1990b C. sexlineatus Kansas 911144 (63%) Loewen 1940 Nebraska 3/3 (100%) Brooks and Mayes 1976 2/64 (3%) Shoop and JanoV)' 1978 South Dakota 13/23 (57%) Dyer 1971 C. sonorae Arizona 1116 (6%) McAllister 1992 C. tesselatus Texas 3/27 (11%) McAllister 1990a 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 C. uniparens Arizona 8/31 (26%) Goldberg and Bursey 1990 C. velox Colorado not stated Douglas 1966 New Mexico 2/37 (5%) McAllister 1992 Pharyngodon warned C. exsanguis New Mexico, Texas 10/87 (11%) McAllister 1990c C. guiaris Oklahoma, Texas, Mexico 69/289 (24%) McAllister 1990d Texas 2/83 (2%) McAllister et al. 1995 C. inomatus Arizona 18(78 (23%) Goldberg and Bursey 1990 Texas not stated Specian and Ubelaker 1974a C. laredoensis Texas 5;22 (23%) McAllister et al. 1986 C. neomexicanus New Mexico, Texas 2/61 (3%) McAllister 1990b C. scxlineatus Texas 2/4 (50%) Harwood 1932 South Dakota 19/23 (83%) Dyer 1971 Arkansas 15151 (29%) McAllister, Trauth, and Conn 1991 C. tesselatus Texas 4/27 (15%) McAllister 1990a C. tigris Utah 5(7 (71%) Grundmann 1959 Arizona, Nevada 63/100 (63%) Babero and Matthias 1967 Thubunaea cnemidophorus c. tigris Nevada 9/87 (10%) Babero and Matthias 1967 C. burti Arizona 2157 (4%) Goldberg and Bursey 1989 C. sexlineatus Arkansas 3/51 (6%) McAllister, Trauth, and Conn 1991

It has been shown that Skrjahinoptera phryno­ ine CnemidopMrus sanorae, and Jeffrey Feng, 80nw, also a member of the Physalopteridae Whittier College, for technical assistance. and a common parasite of Phrynosoma spp., is dependent upon ants (Pogonomyrmex sp.) as LITERATURE CITED intermediate hosts (Lee 1957). The possibility that termites may serve as intermediate hosts ANDERSON, R.C. 1992. Nematode parasites of vertebrates. ofA. terrapenis needs to be investigated. Sucb Their development and transmission. C.A.B. Inter­ national, Wallingford, Oxon, u.K. 578 pp. information would be helpful in determining BABERO, B.B., AND RH. EMMERSON. 1974. Tlwbunaea cne­ distribution patterns ofA. terrapenis. mw.ophorus in Nevada rattlesnakes. Journal of Para­ sitology 60:595. ACKNOWLEDGMENTS BABERO, B.B., AND D. MATTHIAS. 1967. Thuhunaea cnemi­ dophorus n. sp., and other helminths from lizards, H. Cnemidophorus tigris, in Nevada and Arizona. Trans­ 'The authors thank Charles Lowe, Depart­ actions of the American Microscopical Society 86: ment of Ecology and Evolutionary Biology, 173-177. University ofArizona, for permission to exam- BAKER, M.R. 1987. Synopsis of the nematoda parasitic in 276 GREAT BASIN NATURALIST [Volume 57

ampJlibiaru; and . Memmial University of New­ ua} whiptail lizards (felidae) i.n North America. II. foundland. Occasional Papers in Biology 11;1-325. The (Cnemidophorus neotneJ:i. BENES, B.S. 1985. Helminth parasitism in some central conus). Journal ofWildlife Diseases 26:403-406. Arizona lizards. Southwestern Naturalist 30:467--473. · 199Oc, Helminth parasites ofunisexual and bisex.­ BOSfJ(;. D.L. 1965. Parasites of the leiid lizard, Cncmi­ --u-al whiptail lizards (Teiidae) in North America lil. dophorus hyperythrw beldingi. Soulhwestem Natu­ The Chihuahuan spotted whiptail (Cnemidvph0ru3 ralist 10:313. exsanguis). Journal ofWildlife Diseases 26:544-546. BROOKS, D.R.. ANIJ M.A. MAVES. 1976. Morphological vari­ ___. 199Od. Helminth parasites ofunisexual and bisex­ ation in natural infections ofOoc1lOristica bivitellobata ual whiptaillizards (Teiidae) in North America. IV. Loewen. 1940 (Ce,o,toidea: Anoplocephalidae). Trans­ The Texas spotted whiptaU (Cnemidoplwros guLJris). uctions ofthe NebrdsXa Academy ofScience 3:20-21. Texas Journal ofScience 42:381-388. DOUGLA~, C.L. 1966. Amphibians and reptiles of Mesa · 1992. Helminth parasites of unisexual and bisex- Verde National Park, Colorado. University of Kansas --ual- whiptaiI lizards (Teiidae) in orth America. VIII. Publications, Museum of Natural History 15:711-744. The Gil. spotted whiptail (Cnpecies of Utah lizards. Journal ofPell'asitology 45:394. MITCHELL, J.e. 1979. Ecology of southeastem Arizona HARWIXlI). po. 1002. The helminths parasitic in the Am­ whiptail lizards (Cnemidophorus: Teiidae): popula· phibi

asitism among some Southern Califomia lizard pop­ (2061XH;7, 20677, 20681, 20667, 29637, 30087, 30090, ulations. American Midland ~ aturalist 83:516-554. 3(682). VITI, L.J., Al'm R.D. OHMAJI,T. 1977. Ecology and repro­ duction of Lower Colorado River lizards; II. C'wmi­ Natural History Museum ofLos Angeles County dophorus tiooris (Teiidae), with comparisons. Herpe. Cnemidoplwru.s tigris W = 77 [27 females, 50 males]} tologica 33:223--234. foothills Santa Calalina Mountains (822 m elevation, 32°2O'N, llO"07'W), Pima County, Arizona, collected 1962 Receil;ed 1 Octobe,.. 1996 (LACM 143588), 1963 (LACM 143587, 143589), 1964 Accepted 5 December 1996 (LACM 143590-93), 1966 (LACM 143586, 143594-034), 1969 (LACM 143558-85); (N ~ 5 [1 female, 4 males]) Avra Valley (457 m elevation, 32°20'N, 1l1·20'\\~, Pima County, collected 1964 (LACM 14365-69).

ApPENDIX u.s. National Parasite Collection MUSEUM ACCESSION NUMBERS Cnemidophorus sonorae; Oochoristica hidtellobatll, 86861; Ooclwristica macaUisleri, 86862; Abbrcviata ter­ Universit).· o( Arizona ropenis, 86863; Pharyngodon wameri, 86864; Thubuflllea Cnemidophorw sonorae (N = 21 [aU females]) Sabino cnemidophonls, 86865. Canyon (883 m elevation, 32°2O'N, 110°49'\\'), Santa Cata­ Cnemidophorw tigris; Oochoristica bivitellobatl', 86866; lina Mountains, Pima County, Arizona, coUeded 1953 Abln-eciam terrap.,,", 86867; Phnnp.godon ""'""'", 86868; (UAZ 4810-12, 48(1), 1960 (lOWJ, 1(971), 1961 (11034), Centrorltynch... 'po (cy,tacanth), 86869. 1964 (15252, 15258, 15471, 15541, 15708), 1967-1969