DOI: 10.7589/2017-11-275 Journal of Wildlife Diseases, 54(3), 2018, pp. 612–616 Ó Wildlife Disease Association 2018

Mesocestoides sp. in Wild Northern Bobwhite (Colinus virginianus) and Scaled Quail (Callipepla squamata)

Bradley W. Kubecˇka,1,2,4 Nicole J. Traub,1 Vasyl V. Tkach,3 Taylor R. Shirley,1 Dale Rollins,2 and Alan Fedynich1 1Caesar Kleberg Wildlife Research Institute, Texas A&M University–Kingsville, 700 University Boulevard, MSC 218, Kingsville, Texas 78363, USA; 2Rolling Plains Quail Research Foundation, PO Box 220, Roby, Texas 79543, USA; 3Department of Biology, University of North Dakota Grand Forks, PO Box 9019, Grand Forks, North Dakota 58202, USA; 4Corresponding author (email: [email protected])

ABSTRACT: Mesocestoides spp. have a cosmopoli- Odontophoridae known for its precipitous tan distribution with zoonotic potential. Mesoces- population decline over the past century. toides tetrathyridia were found under the Their geographic range extends from northern pericardial sac, on the surface of the crop, and in the peritoneal cavity of a hunter-harvested Mexico to Wisconsin, and Colorado to the Northern Bobwhite (Colinus virginianus) and a Carolinas (Guthery 2000). Scaled Quail (Cal- Scaled Quail (Callipepla squamata) collected lipepla squamata) occur sympatrically with during the 2016–17 quail hunting season in bobwhites in Texas, and are the most closely northwest and southern Texas, US respectively. related taxon to the genus Colinus (Hosner et Molecular analysis indicated that the tetrathyridia from the birds likely belonged to an undescribed al. 2015). species and are identical to pretetrathyridium A Bobwhite and Scaled Quail harvested stages recently found in Scincella lateralis skinks during the 2016–17 hunting season in north- in Oklahoma. This is the first report of Mesoces- western Texas (3281503500 N, 10084302300 W) and toides from North American birds. southern Texas (2685205300 N, 9980402000 W), Key words: Callipepla squamata, Colinus respectively, were infected with tetrathyridia virginianus, Mesocestoides, molecular analysis, of the genus Mesocestoides. The condition of Northern Bobwhite, Scaled Quail, tetrathyridia, Texas. the quails was within normal limits on gross examination (i.e., no lesions or morphological aberrations). Tetrathyridia were present on the Tetrathyridia are the second larval stage (or surface of the crop, under the pericardial sac metacestode) of cestodes belonging to the (Fig. 1), and attached to the serous membrane genus Mesocestoides (Mesocestoididae), which of (and free-floating throughout) the coelomic are characterized by a three-host life cycle cavity. Identification to genus was performed (Khalil et al. 1994; Skirnisson et al. 2016). The by J. M. Kinsella (HelmWest Laboratory, first intermediate host is unknown but pre- Missoula, Montana, USA) using morphological sumed to be a copraphagous arthropod (For- characteristics. Metacestodes had all morpho- onda et al. 2007). Tetrathyridia have been logical characteristics typical of Mesocestoides found in .200 vertebrate hosts, including tetrathyridia with apical end and suckers birds, mammals, reptiles, and amphibians on invaginated (Fig. 2). every continent except Australia (Chertkova Morphological features of tetrathyridia do and Kosupko 1978; Padgett et al. 2013). Of the not allow for their reliable identification; seven avian orders known to host Mesocestoi- therefore, molecular techniques are recom- des, Galliformes and Passeriformes are the mended to be utilized for identification most frequently documented (Chertkova and (Padgett et al. 2005). Moreover, this is also Kosupko 1978; Litera´k et al. 2004). Known true for adult stages and there is disagreement definitive hosts include, but are not limited to, on the number of valid species in this genus arctic fox (Vulpes lagopus), domestic dogs (Webster 1949; Zales´ny and Hildebrand (Canis familiaris), and domestic cats (Felis 2012). Therefore, we obtained partial se- silvestris catus; Skirnisson et al. 1993, 2016). quences of mitochondrial 12S, cox1,and The Northern Bobwhite (Colinus virgin- nad1 genes from the tetrathyridia obtained ianus) is a popular game bird of the family from the bobwhite following the procedures

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FIGURE 1. Northern Bobwhite (Colinus virginianus) heart with tetrathyridia of Mesocestoides sp. under the pericardial sac collected during February 2017 in Mitchell County, Texas, USA.

FIGURE 2. Total mount of tetrathyridium of Mesocestoides sp. from a Northern Bobwhite (Colinus virginianus) collected during February 2017 in Mitchell County, Texas, USA. Note the invaginated anterior (indicated by arrow) and posterior end, and numerous calcareous corpuscles in parenchyma of the metacestode that appear as dark inclusions in the stained specimen. Bar¼1 mm. 614 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 3, JULY 2018

FIGURE 3. Phylogenetic tree resulting from Bayesian analysis and maximum likelihood analysis of 12S alignment of Mesocestoides showing the position of the specimens found in Northern Bobwhite (Colinus virginianus) collected during February 2017 in Mitchell County, Texas, USA. Branch support values are shown at internodes as Bayesian analysis posterior probabilities/maximum likelihood bootstrap percentages. Only posterior probabilities greater than 0.75 and bootstraps greater than 50% are shown. The scale bar indicates the number of substitutions per site. described by McAllister et al. (2018). Se- ed in MEGA 7 (Kumar et al. 2016). All quences were submitted to the GenBank analyses were performed as described by under accession numbers MG214761– McAllister et al. (2018); the only difference MG214763. Phylogenetic analysis of 12S data was the addition of the new sequence of was carried out using Bayesian inference as Mesocestoides from the bobwhite. implemented in the MrBayes program version Pairwise sequence comparisons as well as 3.1 (Ronquist and Huelsenbeck 2003) and the results of molecular phylogenetic analysis maximum likelihood algorithm as implement- (Fig. 3) have confirmed identification of our SHORT COMMUNICATIONS 615 metacestodes from quail as Mesocestoides sp. these studies have documented Mesocestoides Interestingly, these larvae were conspecific spp. in quails. It is likely that the occurrence with the pretetrathyridium stages recently of Mesocestoides in quail, or any New World reported from the ground skink Scincella birds, is rare and incidental. lateralis in Oklahoma (McAllister et al. The pathogenicity of Mesocestoides is low 2018). The two forms were nearly completely (Atkinson et al. 2009); however, human identical genetically with only 0.7% (only two infections have been documented to occur nucleotides) divergence in the 12S gene, 0.8% from eating raw or undercooked meat con- divergence in cox1 gene, and 1.6% divergence taining tetrathyridia (Eom et al. 1992; Fuentes in the highly variable nad1 gene. According to et al. 2003; Centers for Disease Control and McAllister et al. (2018), these metacestodes Prevention 2016). Hunters should assure their do not have a match among currently harvest is washed and cooked thoroughly sequenced adult or metacestode stages of before consumption. Additionally, we suggest Mesocestoides and might represent a yet that internal organs be disposed in a place not undescribed species that is closely related accessible to pets or other wildlife. (Fig. 3) to two lineages previously reported as This study was funded by the Rolling Plains Mesocestoides sp. C by Padgett et al. (2005). Quail Research Foundation, Caesar Kleberg The important difference between our spec- Wildlife Research Institute, South Texas and imens and those described by McAllister et al. Park Cities Chapters of Quail Coalition, and (2018) is that the specimens from the quail the Rene´ Barrientos Fund for Graduate were fully-formed tertrathyridia with invagi- Student Tuition. We thank Mike Kinsella for nated apical ends (Fig. 2), whereas the morphological identification of specimens and specimens from the skinks were pretetrathyr- appreciate the studious nature of the hunters idia with evaginated scolex and neck region. who submitted their harvested samples. Nec- Adult Mesocestoides vogae (reported as

ropsies were conducted in accordance to the Mesocestoides corti)andMesocestoides line- TAMUK Institutional Biosafety Committee atus have been documented in canids, felids, protocol 2015-12-01. This is manuscript 18- and mustelids from Texas (Custer and Pence 111 of the Caesar Kleberg Wildlife Research 1981; Pence and Windberg 1984; Pence et al. Institute. 2003). In South Texas, coyotes (Canis latrans) and ocelots (Leopardus pardalis) had 48% LITERATURE CITED and 7% prevalence of M. lineatus, respectively Atkinson CT, Thomas NJ, Hunter DB. 2009. Parasitic (Pence and Windberg 1984; Pence et al. diseases of wild birds.JohnWileyandSons, 2003), whereas bobcats (Lynx rufus)and Hoboken, New Jersey, 592 pp. American badgers had 36% and 23% preva- Centers for Disease Control and Prevention. 2016. DPDx- lence of M. vogae (reported as M. corti)in Laboratory identification of parasitic diseases of northern Texas, respectively (Stone and Pence public health concern, Mesocestoidiasis.https:// www.cdc.gov/dpdx/mesocestoidiasis/index.html. Ac- 1978; Pence and Dowler 1979; Etges 1991). cessed November 2017. Our study appears to be the first record of Chertkova AN, Kosupko GA. 1978. The suborder tetrathyridia in wild North American birds. Mesocestoidata Skryabin, 1940. In: Principles of During the 2016–17 hunting season we noted cestodology, Ryzhikov KM, editor. Nauka Publishers, two other instances of tetrathyridia in bob- Moscow, Russia, pp. 118–229. Custer JW, Pence DB. 1981. Ecological analyses of whites from North Texas, but disregarded helminth populations of wild canids from the Gulf their occurrence as proglottids of more robust coastal prairies of Texas and Louisiana. J Parasitol 67: cestodes. Recent helminth surveys of quails 289–307. from Texas have been extensive, and compre- Davidson WR, Kellogg FE, Doster GL, Moore CT. 1991. hensive helminth surveys have been conduct- Ecology of helminth parasitism in bobwhites from northern Florida. J Wildl Dis 27:185–205. ed across their geographic range (Stoddard Eom KS, Kim SH, Rim HJ. 1992. Second case of human 1931; Kellogg and Calpin 1971; Moore et al. infection with Mesocestoides lineatus in Korea. 1986; Davidson et al. 1991). However, none of Korean J Parasitol 30:147–150. 616 JOURNAL OF WILDLIFE DISEASES, VOL. 54, NO. 3, JULY 2018

Etges FJ. 1991. The proliferative tetrathyridium of Padgett KA, Nadler SA, Munson L, Sacks B, Boyce WM. Mesocestoides vogae sp. n. (Cestoda). J Helminthol 2005. Systematics of Mesocestoides (Cestoda: Meso- Soc Wash 58:181–185. cestoididae): Evaluation of molecular and morpho- Foronda P, Rivero AP, Santana Morales MA, Kabdur A, logical variation among isolates. J Parasitol 91:1435– Gonza´lez AC, Quispe Ricalde MA, Feliu C, Valla- 1443. dares B. 2007. First larval record of Mesocestoides in Pence DB, Dowler RC. 1979. Helminth parasitism in the Carnivora of Tenerife (Canary Islands). J Parasitol badger, Taxidea taxus (Schreber, 1778), from the 93:138–142. western Great Plains. J Helminthol Soc Wash 46:245– Fuentes MV, Galan-Puchades MT, Malone JB. 2003. A 253. new case report of human Mesocestoides infection in Pence DB, Tewes ME, Laack LL. 2003. Helminths of the United States. Am J Trop Med Hyg 68:566–567. the ocelots from southern Texas. JWildDis39:683– Guthery FS. 2000. On bobwhites. Texas A&M University 689. Press, College Station, Texas, 213 pp. Pence DB, Windberg LA. 1984. Population dynamics Hosner PA, Braun EL, Kimball RT. 2015. Land across selected habitat variables of the helminth connectivity changes and global cooling shaped the community in coyotes, Canis latrans, from south colonization history and diversification of New World quail (Aves: Galliformes: Odontophoridae). J Bio- Texas. J Parasitol 70:735–746. geogr 42:1883–1895. Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian Kellogg FE, Calpin JP. 1971. A checklist of parasites and phylogenetic inference under mixed models. Bio- diseases reported from the bobwhite quail. Avian Dis informatics 19:1572–1574. 15:704–715. Skirnisson K, Eydal M, Gunnarsson E, Hersteinsson P. Khalil LF, Jones A, Bray RA. 1994. Keys to the cestode 1993. Parasites of the arctic fox Alopex lagopus in parasites of vertebrates. CAB International, Walling- Iceland. J Wildl Dis 29:440–446. ford, UK, 751 pp. Skirnisson K, Siguroard¨ ottir´ OG,´ Nielsen OK.´ 2016. Kumar S, Stecher G, Tamura K. 2016. MEGA7: Morphological characteristics of Mesocestoides can- Molecular evolutionary genetics analysis version 7.0 islagopodis (Krabbe 1865) tetrathyridia found in rock for bigger datasets. Mol Biol Evol 33:1870–1874. ptarmigan (Lagopus muta) in Iceland. Parasitol Res Litera´k I, Olson PD, Georgiev BB, Spakulova M. 2004. 115:3099–3106. First record of metacestodes of Mesocestoides sp. in Stoddard HL. 1931. The bobwhite quail: Its habits, the common starling (Sturnus vulgaris) in Europe, preservation, and increase. Charles Scribner’s Sons,

with an 18S rDNA characterization of the isolate. New York, New York, 559 pp. Folia Parasitol 51:45–49. Stone JE, Pence DB. 1978. Ecology of helminth McAllister CT, Tkach VV, Conn DB. 2018. Morphological parasitism in the bobcat from west Texas. J Parasitol and molecular characterization of post-larval pre- 64:295–302. tetrathyridia of Mesocestoides sp. (Cestoidea: Cyclo- Webster D. 1949. Fragmentary studies on the life history phyllidea) from ground skink, Scincella lateralis of the cestode Mesocestoides latus. J Parasitol 35:83– (Sauria: Scincidae), from southeastern Oklahoma, 90. USA. J Parasitol doi: 10.1645/17-178. Zales´ny G, Hildebrand J. 2012. Molecular identification of Moore J, Freehling M, Simberloff D. 1986. Gastrointes- Mesocestoides spp. from intermediate hosts (rodents) tinal helminths of the northern bobwhite in Florida: 1968 and 1983. J Wild Dis 22:497–501. in central Europe (Poland). Parasitol Res 110:1055– Padgett KA, Crosbie PR, Boyce WM. 2013. Mesocestoi- 1061. des. In: Molecular detection of human pathogens, Liu D, editor. CRC Press, Taylor and Francis Group, Submitted for publication 15 November 2017. Boca Raton, Florida, pp. 277–285. Accepted 1 February 2018.