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Apicomplexa: Eugregarinida: Actinocephalidae) Parasitizing Damselflies (Odonata: Zygoptera) in Belize, Central America

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Comp. Parasitol. 77(2), 2010, pp. 125–136 Nubenocephalus nickoli n. sp. and Nubenocephalus xunantunichensis n. sp. (Apicomplexa: Eugregarinida: Actinocephalidae) Parasitizing Damselflies (Odonata: Zygoptera) in Belize, Central America 1,4 2 3 RICHARD E. CLOPTON, TAMARA J. COOK, AND JOANNA J. CIELOCHA 1 Department of Natural Science, Peru State College, Peru, Nebraska 68421, U.S.A. (e-mail: [email protected]), 2 Department of Biological Sciences, Sam Houston State University, Huntsville, Texas 77341-2116, U.S.A. (e-mail: [email protected]), and 3 Department of Ecology and Evolutionary Biology and the Biodiversity Institute, University of Kansas, Lawrence, Kansas 66045, U.S.A. (e-mail: [email protected]) ABSTRACT: Two new species of Nubenocephalus (Apicomplexa: Eugregarinida: Actinocephalidae) are described from adult damselflies sampled in Cayo District, Belize, Central America. Nubenocephalus nickoli n. sp. is described from the American Rubyspot damselfly, Hetaerina americana, and the Smoky Rubyspot damselfly, Hetaerina titia (Odonata: Zygoptera: Hetaerinidae), and Nubenocephalus xunantunichensis n. sp. is described from the Comanche Dancer, Argia chelata (Odonata: Zygoptera: Coenagrionidae). New, complete morphological data sets are reported for populations of Nubenocephalus nebraskensis and Nubenocephalus secundus, and a complete, synoptic reevaluation of diagnostic morphological characters used to discriminate species within Nubenocephalus is presented for all known species of the genus in the New World. Nubenocephalus nebraskensis is reported from Argia apicalis for the first time. KEY WORDS: Acanthosporinae, Actinocephalidae, Apicomplexa, Argia apicalis, Argia chelata, Belize, Central America, Coenagrionidae, damselfly, Eugregarinida, Gregarine, Hetaerinidae, Hetaerina americana, Hetaerina titia, Nubenocephalus mutabilis, Nubenocephalus nebraskensis, Nubenocephalus nickoli n. sp., Nubenocephalus secundus, Nubenocephalus xunantunichensis n. sp., Odonata, Septatorina, Stylocephaloidea, Zygoptera. The eugregarine genus Nubenocephalus consists of 1 from adults of the American Rubyspot damselfly, 3 species parasitizing Nearctic and Palearctic dam- Hetaerina americana (Fabricius) (Odonata: Zygop- selflies. Known Nearctic species are reported from tera: Hetaerinidae), and the Smoky Rubyspot dam- hosts in the genus Argia (Odonata: Zygoptera: selfly, Hetaerina titia (Drury) (Odonata: Zygoptera: Coenagrionidae). The type species, Nubenocephalus Hetaerinidae). The gregarines recovered are referable nebraskensis Clopton, Percival and Janovy, 1993, is to the genus Nubenocephalus but are taxonomically described from the Seepage Dancer, Argia bipunctu- distinct from known species of Nubenocephalus. lata (Hagen) in Nebraska, U.S.A. Nubenocephalus Herein, we describe these new taxa and reevaluate secundus Hays, Clopton, T. J. Cook, 2007, is diagnostic morphological characters used to discrim- reported from the Blue-Ringed Dancer, Argia sedula inate species within Nubenocephalus. (Hagen), and the Dusky Dancer, Argia translata (Hagen in Selys), both in Texas, U.S.A. The single MATERIALS AND METHODS Palearctic species assigned to the genus, Nubenoce- Argia apicalis adults were collected with aerial nets along phalus mutabilis (K. Hoshide, 1977) Clopton and T. Long’s Creek, north of Auburn, Nemaha County, Nebraska, J. Cook, 2007 (5Ancyrophora mutabilis K. Hoshide, U.S.A. (40u24911.80N; 95u50981.80W), from July to August, 1977), is described from the Pied Bush Dart, Copera 2007 (n 5 71). Two specimens vouchering Argia apicalis are deposited in the Sam Houston State University Insect annulata (Selys) (Odonata: Zygoptera: Platycnemi- Collection (SHSUIC), Department of Biological Sciences, didae), in Yamaguchi, Yamaguchi Prefecture, Japan. Sam Houston State University, Huntsville, Texas, U.S.A. No species of Nubenocephalus is reported from the Individual accession numbers are not assigned by SHSUIC. Neotropics. These specimens can be distinguished by the following 5- During a survey of damselfly and eugregarine line determination labels: Line 1—‘‘Argia’’; Line 2— ‘‘apicalis (Say, 1839)’’; Line 3—‘‘MALE: REC070372’’ diversity in Belize, Central America, we collected 2 or ‘‘FEMALE: REC070465’’; Line 4—‘‘SYMBIOTYPE- heretofore unknown gregarine species: 1 from adults VOUCHER’’; Line 5—‘‘det. R E Clopton 2007.’’ of the Comanche Dancer, Argia chelata Calvert, and Argia chelata adults were collected in May 2008 with aerial nets near Hammock Bridge on the Mopan River at Branch Mouth, Cayo District, Belize, Central America (17u10965.60N; 89u4981.30W), and along Barton’s Creek at 4 Corresponding author. Caesar’s Place, Imperial Mile Marker 60, Western Highway 125 126 COMPARATIVE PARASITOLOGY, 77(2), JULY 2010 near Unitedville, Cayo District, Belize, Central America Damselflies were eviscerated, and their alimentary canals (17u12933.50N; 88u57920.50W) (n 5 22 and 4, respectively). were dissected in insect muscle saline (Belton and Argia sedula adults were collected with aerial nets along Grundfest, 1962). Permanent parasite preparations were Harmon Creek at the Sam Houston State University Center made following the techniques described by Clopton for Biological Field Studies, Walker County, Texas, U.S.A. (2004a). Observations of trophozoites, sporonts, and (30u44944.70N; 95u28946.20W), June to October 2006 (n 5 gamonts were made using an Olympus B-Max 41 compound 94). These are the original type collections for Nubeno- microscope with 310, 340, and 3100 universal planapo- cephalus secundus, and data provided herein for this species chromatic objectives with either bright field or phase are taken from the original type data set. Hetaerina contrast condensers. Digital photographs were taken using americana adults were collected using an aerial net from an Olympus DP-12 digital camera through the aforemen- the following localities in the U.S.A: Cedar Creek at the tioned microscope. Measurements were taken from digitized Paxton-Sarben Road, Keith County, Nebraska, U.S.A. images of preserved specimens using Image Pro Express v. (41u11902.80N; 101u21961.30W), July 1996 (n 5 47), June 4.5 image analysis software (Media Cybernetics, L.P., Silver 1997 (n 5 36), and September 2003 (n 5 17); Clear Creek Spring, Maryland). Images of preserved specimens used in at Highway 92, Keith County, Nebraska, U.S.A. the photographic plates were taken using the Olympus DP- (41u19920.90N; 102u02924.90W) in June 1998 (n 5 36), 70 digital camera attached to the Olympus B-Max 50 and June 1999 (n 5 28); Long’s Creek, north of Auburn, compound microscope described above. Photographic plates Nemaha County, Nebraska, U.S.A. (40u24911.80N; were processed and assembled using AdobeH PhotoShopH 95u50981.80W), July to August 2007 (n 5 92); Otter Creek 7.0.1 software (Adobe Systems Inc., San Jose, California, at Highway 92, Keith County, Nebraska, U.S.A. U.S.A.). (41u18908.30N; 101u55939.00W), June 1996 (n 5 30); and Individual gregarine gametocysts were preserved for Turkey Creek in Johnson County, Nebraska, U.S.A. future genetic analysis after transfer through 3 changes of (40u15975.30N; 96u21940.40W), July to August 2003 (n 5 TMS and 3 changes of distilled water sterilized by syringe 58). Hetaerina americana adults were collected in May filtration through a 0.2-mm membrane and transferred to 2008 with aerial nets near Hammock Bridge on the Mopan individual microcentrifuge tubes. A hypodermic needle was River at Branch Mouth, Cayo District, Belize, Central used to rupture each gametocyst, and the liberated contents America (17u10965.60N; 89u4981.30W), May 2008, and were dried at ,60uC before capping the microcentrifuge along Barton’s Creek at Caesar’s Place, Imperial Mile tube. All samples were stored at 4uC prior to DNA Marker 60, Western Highway near Unitedville, Cayo extraction. District, Belize, Central America (17u12933.50N; The DNA from each pooled sample of trophozoites and/or 88u57920.50W) (n 5 2 and 6, respectively). Hetaerina titia gamonts was isolated using a PureLink genomic DNA Mini adults were collected in June 2007 and May 2008 with aerial Kit (Invitrogen, Carlsbad, California, U.S.A.). Dried game- nets near Hammock Bridge on the Mopan River at Branch tocyst samples were extracted using the PureLink genomic Mouth, Cayo District, Belize, Central America DNA Mini Kit’s accompanying FTA protocol (Invitrogen, (17u10965.60N; 89u4981.30W) (n 5 29 and 19, respectively), Carlsbad, California, U.S.A.). Isolated DNA samples were and in May 2008 along Barton’s Creek at Caesar’s Place, resuspended in NE buffer (USB Corporation, Cleveland, Imperial Mile Marker 60, Western Highway near United- Ohio, U.S.A.) and stored by aliquot at 4uC for future ville, Cayo District, Belize, Central America (17u12933.50N; analysis. 88u57920.50W) (n 5 15). Adult damselflies were placed in Terminology for developmental stages generally follows 1-liter plastic containers held on ice until processed. that of Levine (1971) for Apicomplexa, with one notable Damselflies were isolated, abdomen-down, in 5-ml exception: Sporont is used herein to indicate a mature plastic test tubes with 1 ml of water. Fecal material in the individual lacking an epimerite that remains attached to the water was examined after 12–24 hr for gregarine host epithelium prior to forming an association (Clopton et gametocysts. Shed gametocysts were freed from feces, al., 1993). Terminology for association and gametocyst life- triple rinsed in Tenebrio molitor muscle saline (TMS) cycle characters follows that of Clopton (2009). Terminol-
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