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

Tetrathyridia are the second larval stage (or metacestode) of cestodes belonging to the genus Mesocestoides (Mesocestoididae), which are characterized by a three-host life cycle (Khalil et al. 1994; Skirnisson et al. 2016). The first intermediate host is unknown but presumed to be a copraphagous arthropod (Foronda et al. 2007). Tetrathyridia have been found in >200 vertebrate hosts, including birds, mammals, reptiles, and amphibians on every continent except Australia (Chertkova and Kosupko 1978; Padgett et al. 2013). Of the seven avian orders known to host Mesocestoides, Galliformes and Passeriformes are the most frequently documented (Chertkova and Kosupko 1978; Literák et al. 2004). Known definitive hosts include, but are not limited to, arctic fox (Vulpes lagopus), domestic dogs (Canis familiaris), and domestic cats (Felis silvestris catus; Skirnisson et al. 1993, 2016).

The Northern Bobwhite (Colinus virginianus) is a popular game bird of the family Odontophoridae known for its precipitous population decline over the past century. Their geographic range extends from northern Mexico to Wisconsin, and Colorado to the Carolinas (Guthery 2000). Scaled Quail (Callipepla squamata) occur sympatrically with bobwhites in Texas, and are the most closely related taxon to the genus Colinus (Hosner et al. 2015).

A Bobwhite and Scaled Quail harvested during the 2016–17 hunting season in northwestern Texas (32°15′35″N, 100°43′23″W) and southern Texas (26°52′53″N, 99°04′20″W), respectively, were infected with tetrathyridia of the genus Mesocestoides. The condition of the quails was within normal limits on gross examination (i.e., no lesions or morphological aberrations). Tetrathyridia were present on the surface of the crop, under the pericardial sac (Fig. 1), and attached to the serous membrane of (and free-floating throughout) the coelomic cavity. Identification to genus was performed by J. M. Kinsella (HelmWest Laboratory, Missoula, Montana, USA) using morphological characteristics. Metacestodes had all morphological characteristics typical of Mesocestoides tetrathyridia with apical end and suckers invaginated (Fig. 2).

Morphological features of tetrathyridia do not allow for their reliable identification; therefore, molecular techniques are recommended to be utilized for identification (Padgett et al. 2005). Moreover, this is also true for adult stages and there is disagreement on the number of valid species in this genus (Webster 1949; Zaleśny and Hildebrand 2012). Therefore, we obtained partial sequences of mitochondrial 12S, cox1, and nad1 genes from the tetrathyridia obtained from the bobwhite following the procedures described by McAllister et al. (2018). Sequences were submitted to the GenBank under accession numbers MG214761–MG214763. Phylogenetic analysis of 12S data was carried out using Bayesian inference as implemented in the MrBayes program version 3.1 (Ronquist and Huelsenbeck 2003) and maximum likelihood algorithm as implemented in MEGA 7 (Kumar et al. 2016). All analyses were performed as described by McAllister et al. (2018); the only difference was the addition of the new sequence of Mesocestoides from the bobwhite.

Pairwise sequence comparisons as well as the results of molecular phylogenetic analysis (Fig. 3) have confirmed identification of our metacestodes from quail as Mesocestoides sp. Interestingly, these larvae were conspecific with the pretetrathyridium stages recently reported from the ground skink Scincella lateralis in Oklahoma (McAllister et al. 2018). The two forms were nearly completely identical genetically with only 0.7% (only two nucleotides) divergence in the 12S gene, 0.8% divergence in cox1 gene, and 1.6% divergence in the highly variable nad1 gene. According to McAllister et al. (2018), these metacestodes do not have a match among currently sequenced adult or metacestode stages of Mesocestoides and might represent a yet undescribed species that is closely related (Fig. 3) to two lineages previously reported as Mesocestoides sp. C by Padgett et al. (2005). The important difference between our specimens and those described by McAllister et al. (2018) is that the specimens from the quail were fully-formed tertrathyridia with invaginated apical ends (Fig. 2), whereas the specimens from the skinks were pretetrathyridia with evaginated scolex and neck region.

Adult Mesocestoides vogae (reported as Mesocestoides corti) and Mesocestoides lineatus have been documented in canids, felids, and mustelids from Texas (Custer and Pence 1981; Pence and Windberg 1984; Pence et al. 2003). In South Texas, coyotes (Canis latrans) and ocelots (Leopardus pardalis) had 48% and 7% prevalence of M. lineatus, respectively (Pence and Windberg 1984; Pence et al. 2003), whereas bobcats (Lynx rufus) and American badgers had 36% and 23% prevalence of M. vogae (reported as M. corti) in northern Texas, respectively (Stone and Pence 1978; Pence and Dowler 1979; Etges 1991).

Our study appears to be the first record of tetrathyridia in wild North American birds. During the 2016–17 hunting season we noted two other instances of tetrathyridia in bobwhites from North Texas, but disregarded their occurrence as proglottids of more robust cestodes. Recent helminth surveys of quails from Texas have been extensive, and comprehensive helminth surveys have been conducted across their geographic range (Stoddard 1931; Kellogg and Calpin 1971; Moore et al. 1986; Davidson et al. 1991). However, none of these studies have documented Mesocestoides spp. in quails. It is likely that the occurrence of Mesocestoides in quail, or any New World birds, is rare and incidental.

The pathogenicity of Mesocestoides is low (Atkinson et al. 2009); however, human infections have been documented to occur from eating raw or undercooked meat containing tetrathyridia (Eom et al. 1992; Fuentes et al. 2003; Centers for Disease Control and Prevention 2016). Hunters should assure their harvest is washed and cooked thoroughly before consumption. Additionally, we suggest that internal organs be disposed in a place not accessible to pets or other wildlife.

This study was funded by the Rolling Plains Quail Research Foundation, Caesar Kleberg Wildlife Research Institute, South Texas and Park Cities Chapters of Quail Coalition, and the Reńe Barrientos Fund for Graduate Student Tuition. We thank Mike Kinsella for morphological identification of specimens and appreciate the studious nature of the hunters who submitted their harvested samples. Necropsies were conducted in accordance to the TAMUK Institutional Biosafety Committee protocol 2015-12-01. This is manuscript 18-111 of the Caesar Kleberg Wildlife Research Institute.