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Home , Pantherophis obsoletus, Reptile Database, Sarcocystidae, Sarcocystis, Tantilla gracilis

33

First Report of sp. (: ) from (Ophidia: )

Chris T. McAllister Science and Mathematics Division, Eastern Oklahoma State College, Idabel, OK 74745

William G. Palmer Department of Biology, University of Oklahoma, Norman, OK 73019

R. Scott Seville Department of Zoology and Physiology, University of Wyoming/Casper Center, 125 Col- lege Drive, Casper, WY 82601

Coccidia of the Sarcocystis exhibit Levine and Tadros, 1980 from bullsnakes (P. an obligate predator/prey or scavenger/ c. sayi) from (Roudabush 1937; Bled- prey life cycle. In a definitive host, soe 1980; Duszynski and Upton 2009). We sexual reproduction occurs in the epithelial know of no previous reports of Sarcocystis cells of the small intestine and oocysts and sp. in any from Oklahoma. Here we free sporocysts are passed in feces; in the provide the first report of Sarcocystis sp. in intermediate host (often a rodent), asexual two common snakes from the state. development takes place, usually as cyst Between September 2002 and Sep- (sarcocyst) stages in skeletal musculature tember 2013, we collected by hand, snake (Duszynski and Upton 2009). In order to tong, or from fresh specimens found dead adequately identify Sarcocystis , it is on the road (DOR), 42 colubrid and five necessary to examine their life cycle through viperid snakes from five counties (Figure experimental transmission studies. Indeed, 1) of southeastern Oklahoma (Atoka, Choc- McAllister et al. (1996) stated, “tissue stages taw, LeFlore, McCurtain, Pushmataha), recovered in the intermediate host are neces- including: two A. c. contortrix, one western sary for species identification.” cottonmouth ( leucos- Duszynski and Upton (2009) provide toma), two black racers (Coluber constrictor the most recent summation of Sarcocystis priapus), two timber (Crotalus spp. from snakes of the world. In the fam- horridus), five prairie ring neck snakes Di( - ily Colubridae, only 10 species of Sarcocystis adophis punctatus arnyi), one western mud have been adequately described. Of these, snake (Farancia abacura reinwardtii), two four species are known from eastern hognose snakes (Heterodon platirhi- as follows: Sarcocystis lampropeltii Duszynski nos), four prairie king snakes (Lampropeltis and Upton, 2009, formerly Sarcocystis mon- calligaster calligaster), one blotched water tanaensis Dubey, 1983 from a speckled king- snake ( transversa), one snake (Lampropeltis holbrookii) from broad- (Nerodia fasciata (see Lindsay et al., 1992), S. montanaensis confluens), 11 diamondback water snakes from a southern copperhead (Agkistrodon (), 13 western snakes contortrix contortrix) from Arkansas (Lind- (Panterophis obsoletus obsoletus), one midland say et al., 1991), Sarcocystis idahoensis Bled- brown snake ( wrightorum), soe, 1980 from Great Basin gopher snakes one flathead snake ( gracilis), and one ( deserticola) from Idaho, western ribbon snake ( and Sarcocystis roundabushi (Pellérdy, 1974) proximus). Fresh fecal samples were col-

Proc. Okla. Acad. Sci. 93: pp 33-36 (2013) 34 C.T. McALLISTER, W.G. PALMER and R.S. SEVELLE

Figure 1. Five Oklahoma counties where snakes were collected and surveyed for Sar- cocystis spp.

lected from the rectum of each individual 95.042542ºW) and another adult male (1,135 for examination of and placed in mm SVL, ASUMZ 32766) collected on 9 Au- individual vials containing 2.5% (w/v) gust 2013 from off US 271, S of Talihina, Le aqueous potassium dichromate (K2Cr2O7). Flore County (34.623603ºN, 94.652138ºW); They were examined by light microscopy and two of four (50%) L. c. calligaster (adult after flotation in Sheather’s sugar solution males, 850 and 745 mm SVL, ASUMZ 32766, (specific gravity = 1.30). Measurements uncatalogued-DOR) collected on 21 July were taken on 10 sporocysts using a cali- 2013 and 19 September 2013 from 1.6 km brated ocular micrometer and reported in W of Broken Bow off St. Hwy. 3, McCurtain micrometers with means followed by the County (34.032217ºN, 94.756866ºW) and ranges in parentheses. Photographs were 3.2 km SE of Smithville off St. Hwy. 4, Mc- taken using Nomarski interference-contrast Curtain County (34.450335°N,94.6271°W). (DIC) optics. Photovouchers of the parasites Sporocysts from P. o. obsoletus (ASUMZ are deposited in the National 32765) measured L × W (mean [range]) = 11.2 Parasite Collection (USNPC), Beltsville, Mary- × 9.0 (10–12 × 8–10) with a shape index of 1.3 land. Host vouchers are deposited in the (1.2–1.4); the sporocyst wall was ca. 0.5 thick, Arkansas State University Museum of Zo- lacked a , and enclosed four spo- ology (ASUMZ) Herpetological Collection, rozoites and a granular sporocyst residuum. State University, Arkansas. Snake These measurements accord well with those follows the TIGR (Uetz 2013). previously reported from L. holbrookii from Four of 47 (9%) of the snakes were found Arkansas and originally reported as Sarco- to be passing fully sporulated oocysts and cystis montanaensis (Lindsay et al. 1992) but free sporocysts of Sarcocystis sp. (Figures now referred to as Sarcocystis lampropeltii 2A-C) in feces as follows: two of 13 (15%) (see Duszynski and Upton 2009). Unfortu- P. o. obsoletus, an adult male (snout-vent nately, there were not enough sporocysts to length [SVL] = 1,230 mm, ASUMZ 32765) attempt to establish experimental infections collected on 23 May 2013 from the vicinity in rodents and therefore, a description of of Three Sticks National Forest Monument a new or previously known species using off US 259, Le Flore County (34.730637ºN, microscopy alone is not possible.

Proc. Okla. Acad. Sci. 93: pp 33-36 (2013) FIRST REPORT OF SARCOCYSTIS FROM OKLAHOMA SNAKES 35

Figure 2. Photomicrographs of oocysts of three isolates of Sarcocystis sp. from Oklahoma snakes. A. Oocyst (USNPC 107154) from obsoletus obsoletus, Le Flore County, Three Sticks National Forest Monument. B. Oocyst (USNPC 107155) from P. o. obsoletus, Le Flore County, Talihina. C. Oocyst (USNPC 107156) from cal- ligaster, McCurtain County, Broken Bow. Oocyst from other L. c. calligaster, McCurtain County, Smithville, not shown. Bar = 10 µm for all figs.

This is not the first time that a western LITERATURE CITED or prairie king snake has been re- Anderson DR, Duszynski DW, Marquardt WC. 1968. Three new coccidia (: Teleosporea) from ported to harbor Sarcocystis sp. McAllister kingsnakes, Lampropeltis spp., in , with a et al. (1995) reported a Sarcocystis sp. from description of zamenis Phisalix, 1921. J. one of 13 (8%) P. o. obsoletus and a single L. Parasitol. 54:577-581. Sarcocystis idahoensis c. calligaster from Arkansas. In addition, Bledsoe B. 1980. sp. n. in deer mice Peromyscus maniculatus (Wagner) and gopher a Sarcocystis sp. (termed Sarcocystis sp. 2, snakes (Daudin). J. Protozool. formerly S. roudabushi, see Duszynski and 27:93-102. Upton 2009) and S. cleithrionomyelapis (Ma- Duszynski DW, Upton SJ. 2009. The biology of the coccidia (Apicomplexa) of snakes of the world. A tuschka 1986) have been previously reported scholarly handbook for identification and treat- from P. obsoletus and a Sarcocystis sp. (syn. ment. Available from: CreateSpace.com. 422 p. lampropeltis) was reported Lindsay DS, Upton SJ, Blagburn BL, Toivio-Kinnucan M, Dubey JP, McAllister CT, Trauth SE. 1992. by Anderson et al. (1968) from L. c. calligaster Demonstration that Sarcocystis montanaensis has a from Illinois. However, we document the -prairie life cycle. J. Helm. initial report of Sarcocystis sp. from two spe- Soc. Wash. 59:9-15. cies of Oklahoma . Lindsay DS, Upton SJ, Blagburn BL, Toivio-Kinnucan M, Dubey JP, McAllister CT, Trauth SE. 1991. Sporocysts isolated from the southern copperhead ACKNOWLEDGMENTS ( contortrix) produce Sarcocystis The Oklahoma Department of Wildlife montanaensis-like sarcocysts in prairie (Micro- tus ochrogaster). J. Wildl. Dis. 27:148-152. Conservation and USDA Forest Service Matuschka F-R. 1986. Sarcocystis cleithrionmyelaphis (Ouachita National Forest) provided scien- n. sp. from snakes of the genus and differ- tific collecting permits to C. T. McAllister. ent voles of the family Arvicolidae. J. Parasitol. We thank Dr. S. E. Trauth (ASUMZ) and P. 72:226-231. McAllister CT, Upton SJ, Barker DG, Painter CW. 1996. A. Pilitt (USNPC) for expert curatorial as- Sarcocystis sp. (Apicomplexa) from the New Mexico sistance. This project was, in part, supported ridgenose , obscurus. J. by grants from the National Center for Research Helm. Soc. Wash. 63:128-130. McAllister CT, Upton SJ, Trauth SE, Dixon JR. 1995. Resources (5P20RR016474-12) and the National Coccidian parasites (Apicomplexa) from snakes in Institute of General Medical Sciences (8 P20 the southcentral and southwestern United States. GM103432-12) from the National Institutes of J. Parasitol. 81:63-68. Roudabush RL. 1937. Some coccidia of reptiles found Health. The content is solely the responsibility in North America. J. Protozool. 23:354-359. of the authors and does not necessarily represent Uetz P. 2013. The TIGR Reptile Database. World Wide Web the official views of the National Institutes of electronic publication. http://www.reptile-database. Health. org/. (Accessed 11 July 2013). Received: August 14th, 2013, Accepted: November 3rd, 2013

Proc. Okla. Acad. Sci. 93: pp 33-36 (2013) 36 C.T. McALLISTER, W.G. PALMER and R.S. SEVELLE

Proc. Okla. Acad. Sci. 93: pp 33-36 (2013)