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Life-Cycle of Oxyspirura Petrowi (Spirurida: Thelaziidae), An

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Life-Cycle of Oxyspirura Petrowi (Spirurida: Thelaziidae), An Kalyanasundaram et al. Parasites Vectors (2019) 12:555 https://doi.org/10.1186/s13071-019-3802-3 Parasites & Vectors RESEARCH Open Access Life-cycle of Oxyspirura petrowi (Spirurida: Thelaziidae), an eyeworm of the northern bobwhite quail (Colinus virginianus) Aravindan Kalyanasundaram, Matthew Z. Brym, Kendall R. Blanchard, Cassandra Henry, Kalin Skinner, Brett J. Henry, Jessica Herzog, Alyssa Hay and Ronald J. Kendall* Abstract Background: Oxyspirura petrowi (Spirurida: Thelaziidae), a heteroxenous nematode of birds across the USA, may play a role in the decline of the northern bobwhite (Colinus virginianus) in the Rolling Plains Ecoregion of West Texas. Previous molecular studies suggest that crickets, grasshoppers and cockroaches serve as potential intermediate hosts of O. petrowi, although a complete study on the life-cycle of this nematode has not been conducted thus far. Conse- quently, this study aims to improve our understanding of the O. petrowi life-cycle by experimentally infecting house crickets (Acheta domesticus) with O. petrowi eggs, feeding infected crickets to bobwhite and assessing the life-cycle of this nematode in both the defnitive and intermediate hosts. Methods: Oxyspirura petrowi eggs were collected from gravid worms recovered from wild bobwhite and fed to house crickets. The development of O. petrowi within crickets was monitored by dissection of crickets at specifed intervals. When infective larvae were found inside crickets, parasite-free pen-raised bobwhite were fed four infected crickets each. The maturation of O. petrowi in bobwhite was monitored through fecal foats and bobwhite necropsies at specifed intervals. Results: In this study, we were able to infect both crickets (n 45) and bobwhite (n 25) with O. petrowi at a rate of 96%. We successfully replicated and monitored the complete =O. petrowi life-cycle in vivo= , recovering embryonated O. petrowi eggs from the feces of bobwhite 51 days after consumption of infected crickets. All life-cycle stages of O. petrowi were confrmed in both the house cricket and the bobwhite using morphological and molecular techniques. Conclusions: This study provides a better understanding of the infection mechanism and life-cycle of O. petrowi by tracking the developmental progress within both the intermediate and defnitive host. To our knowledge, this study is the frst to fully monitor the complete life-cycle of O. petrowi and may allow for better estimates into the potential for future epizootics of O. petrowi in bobwhite. Finally, this study provides a model for experimental infection that may be used in research examining the efects of O. petrowi infection in bobwhite. Keywords: Eyeworm, Bobwhite, Crickets, Life-cycle, Intermediate, Defnitive *Correspondence: [email protected] The Wildlife Toxicology Laboratory, Texas Tech University, Lubbock, TX 79409-3290, USA © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kalyanasundaram et al. Parasites Vectors (2019) 12:555 Page 2 of 10 Background Although many studies have investigated the efects of Te eyeworm (Oxyspirura petrowi) is a heteroxenous O. petrowi on bobwhite, there is a lack of research into nematode found in birds of the USA. In the USA, it was how bobwhite are infected with this nematode. Tus, frst reported in Galliformes and Passeriformes in Michi- understanding the full life-cycle of O. petrowi could pro- gan during 1937 [1]. Since then, it has been identifed in vide valuable insight to transmission dynamics in wild numerous other species from these orders, including the bobwhite. Telazia callipaeda, for example, utilizes a fy lesser-prairie chicken (Tympanuchus pallidicinctus) [2], as an intermediate host to transmit third-stage larvae to northern cardinal (Cardinalis cardinalis) [3], northern the defnitive host [19, 22, 23], while the chicken eye- mockingbird (Mimus polyglottos), curve-billed thrasher worm (Oxyspirura mansoni) utilizes the Surinam cock- (Toxostoma curvirostre) [4], Gambel’s quail (Callipepla roach (Pycnoscelus surinamensis) for this purpose [24]. gambelii) [5], scaled quail (Callipepla squamata) and It is known that O. petrowi also requires an intermedi- northern bobwhite quail (Colinus virginianus; hereafter, ate host and multiple insect species have been identifed bobwhite) [6]. Oxyspirura petrowi has gained particular in this capacity, including the diferential grasshopper notoriety in the Rolling Plains Ecoregion of West Texas, (Melanoplus diferentialis), wood cockroach (Parcoblatta as this area is reported to be the epicenter of infection spp.) and red-legged grasshopper (Melanoplus femur- [7]. Te West Texas Rolling Plains is also considered to rubrum) [25]. Furthermore, pioneering research by Kis- be a stronghold of bobwhite hunting [5], which provides tler et al. [26] reported the plains lubber grasshopper an important source of seasonal revenue for many local (Brachystola magna) as an intermediate host, with O. communities [8]. Unfortunately, bobwhite populations petrowi larvae being found in the body cavity of various throughout the West Texas Rolling Plains have been specimens. Kistler et al. [26] confrmed the identity of O. declining, with O. petrowi infection being purported as a petrowi in B. magna by experimentally infecting house potential mechanism contributing to this decline [9–11]. crickets (Acheta domesticus; hereafter, cricket) with O. In the Rolling Plains, there have been extensive studies petrowi and comparing the morphology of third-stage investigating the efects of O. petrowi on bobwhite and larvae recovered from both orthopterans. Kistler et al. surveys have identifed it to be highly prevalent through- [26] also fed infected B. magna to pen-raised bobwhite, out the ecoregion [7, 12]. For instance, Dunham et al. recovering sexually mature O. petrowi from these birds. [13] found 58.7% of adult bobwhite across 29 counties in However, Kistler et al. [26] achieved only low (16.6%) the Rolling Plains to be infected with O. petrowi, while infection rates in crickets and were unable to observe others have found some areas with a prevalence of 100% the complete development of O. petrowi, recovering only [10, 11]. Oxyspirura petrowi is typically found on the sur- third-stage larva and adults. In order to better under- face of the eye, under the nictitating membrane, as well stand the development of O. petrowi larvae within both as in the lacrimal ducts and other glands of the eye [9]. the intermediate and defnitive host, this study expands Oxyspirura petrowi infections have been correlated with upon research done by Kistler et al. [26] by providing a infammation of the lacrimal ducts, keratitis and lesions more efective means of infection and detailed exami- on the Harderian gland [9, 14], leading to suspicions that nation of each stage of the O. petrowi life-cycle in both infection may adversely afect bobwhite [9–11]. Patho- crickets and bobwhite. logical investigations have further increased concerns of O. petrowi infection, as the Harderian gland is associ- Methods ated with immune function [15]; although more research Cricket colonies is needed to elucidate links between infection and these Adult crickets were maintained in two standard 10-gal- immune system processes. Moreover, phylogenetic anal- lon glass aquariums (50.80 × 25.40 × 30.48 cm; here- yses have revealed the close relation of O. petrowi to the after, maintenance aquariums), which were ftted human eyeworm (Loa loa) [16, 17] and the human and with screen aquarium covers (50.8 × 25.4 cm) to pre- carnivore eyeworm (Telazia callipaeda) [17], which vent escapes and high humidity, which is sub-optimal have been associated with impaired vision [18] and ulcer- for adults [27]. A third 10-gallon aquarium was used ative keratitis [19] in their hosts, respectively. While the as a rearing container for cricket nymphs (1st to 4th phylogenetic similarity of O. petrowi to L. loa and T. cal- instars). Because cricket nymphs are vulnerable to des- lipaeda does not necessarily imply similar pathology, the iccation [27], the rearing aquarium was covered with documented pathological consequences of O. petrowi a tempered-glass lid (50.8 × 25.4 cm), which increased infection alongside reports of bobwhite fying into sta- humidity and could withstand the temperatures gener- tionary objects [20, 21] suggest that impaired vision may ated by heat lamps used to warm the colonies. As an occur in birds infected with this parasite. additional measure of safety, a welded wire screen was Kalyanasundaram et al. Parasites Vectors (2019) 12:555 Page 3 of 10 placed between the lid and heat lamp on the rearing growth of bacteria and mold. Te complete setup for aquarium to prevent the lamp from falling into the col- cricket colonies is illustrated in Fig. 1. ony if the tempered-glass failed. A heat lamp with an incandescent infrared bulb Experimental crickets (120 V, 50 W) was set on top of each aquarium cover to A total of 200 adult crickets were purchased from attain temperatures (~ 30 °C)
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