Redescription of Protomagalhaensia Blaberae Peregrine, 1970
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Comp. Parasitol. 79(2), 2012, pp. 182–191 Redescription of Protomagalhaensia blaberae Peregrine, 1970 (Apicomplexa: Eugregarinida: Blabericolidae) Parasitizing the Bolivian Cockroach, Blaberus boliviensis (Dictyoptera: Blaberidae) R. E. CLOPTON Department of Natural Science, Peru State College, Peru, Nebraska, U.S.A. 68421 (e-mail: [email protected]) ABSTRACT: Protomagalhaensia blaberae Peregrine, 1970 is redescribed from the type host, the Bolivian cockroach Blaberus boliviensis. Complete morphometric data on all life cycle stages is presented, the taxon is stabilized with the deposition of new voucher specimen material, and P. blaberae is distinguished from all other species in the genus (Protomagalhaensia cerastes, Protomagalhaensia granulosae, and Protomagalhaensia wolfi). Species of Protomagalhaensia are distinguished by differences in relative metric ratios, morphology of oocysts, and by relative metric ratios of mature gamonts in association. The status of Protomagalhaensia serpentula is considered and the taxon is determined species inquirenda. KEY WORDS: Apicomplexa, Blabericolidae, Gregarine, Protomagalhaensia blaberae, Protomagalhaensia cerastes, Protomagalhaensia granulosae, Protomagalhaensia serpentula, Protomagalhaensia wolfi. The genus Protomagalhaensia (Apicomplexa: Eu- Monroe County, Florida, U.S.A. (Clopton, 2010). gregarinida: Blabericolidae) comprises 5 species of Protomagalhaensia serpentula has not been reported gregarines parasitic in the intestines of cockroaches. since its original description and remains enigmatic, a Protomagalhaensia serpentula (de Magalhaes 1900) problem compounded by confusion regarding the type Pinto 1918 (5Gregarina serpentula de Magalhaes host. Of the remaining 4 species in the genus, complete 1900) parasitizing Periplaneta americana (Linnaeus, taxonomic data sets and voucher specimens exist for 1758) (5Stylopyga americana Fischer, 1846) (Dic- all but P. blaberae (see Clopton and Hays, 2006; tyoptera: Blattaria: Blattidae: Blattinae) is the type of Clopton, 2010, 2011;). Herein, we complete the the genus and was described from material collected in stabilization of Protomagalhaensia by redescribing Rio de Janeiro, Brazil (Pinto, 1918, 1922). Proto- P. blaberae parasitizing B. boliviensis, differentiating magalhaensia granulosae Peregrine, 1970, parasitiz- it from existing species in the genus, discuss new ing Blaberus discoidalis Serville, 1839 (Dictyoptera: voucher material deposited to stabilize the taxon, and Blaberidae: Blaberinae), was described from cock- reconsider the taxonomic status of P. serpentula. roaches maintained in laboratory cultures in the Department of Zoology, University College Cardiff MATERIALS AND METHODS (Cardiff University), Cardiff, Wales, United Kingdom Blaberus boliviensis breeding colonies were established (Peregrine, 1970). Similarly, Protomagalhaensia bla- using stock obtained from commercial sources. Colonies berae Peregrine, 1970, parasitizing Blaberus bolivien- were maintained in 22-liter polycarbonate containers with sis Princis, 1946 (Dictyoptera: Blattaria: Blaberidae: coir bedding and cardboard egg-crate roosting habitat. Food (PurinaH Dog ChowH brand Dog Food Complete & Blaberinae), was also described from cockroaches Balanced [Nestle Purina Pet Care Company, St. Louis, maintained in laboratory cultures in the Department of Missouri, U.S.A.]) and water were provided ad libidum. Zoology, University College Cardiff (Peregrine, Adult or late-instar nymphal B. boliviensis individuals were 1970). Protomagalhaensia wolfi (Geus, 1969) Clopton examined for gregarine parasites as described by Clopton (2011). Likewise, preparation of permanent microscope and Hays, 2006 (5Gregarina wolfi Geus, 1969), slides, gametocyst collection and incubation protocols, parasitizing Nauphoeta cinerea (Olivier, 1789) (Dic- techniques for studying oocysts in monolayer and free- tyoptera: Blattaria: Blaberidae: Oxyhalinae: Nauphoe- rotational temporary mounts, and DNA extraction and tini), was described using material collected in storage protocols follow those detailed by Clopton (2011). Observations were made using an Olympus B-Max 50 Ndanda, Tanzania (Geus, 1969). Protomagalhaensia compound microscope with 310, 320, 340, and 360 cerastes Clopton, 2010, parasitizing Phoetalia pallida universal planapochromatic objectives, with either phase (Brunner von Wattenwyl 1865) Princis, 1967 (5Nau- contrast condensers or differential interference contrast phoeta pallida Brunner von Wattenwyl 1865) (Dic- prisms and an infinity-optics turret doubler. Digital tyoptera: Blattaria: Blaberidae: Blaberinae), was photographs were taken with an Olympus DP-70 digital camera through the aforementioned microscope. Measure- described from cockroaches maintained in laboratory ments were taken from the digitized images of preserved colonies established using wild stock from Key West, specimens using cellSens Dimension DesktopH v. 1.3 image 182 CLOPTON—REDESCRIPTION OF PROTOMAGALHAENSIA BLABERAE 183 analysis software (Olympus Corp., Silver Spring, Maryland, the anterior membranes of the satellite’s protomerite; U.S.A.). Photographic plates were processed and assembled oocysts dolioform, with or without spines or knobs at using AdobeH PhotoShopH CS5 Extended software (Adobe terminal apices, released in monete chains from Systems Inc., San Jose, California, U.S.A.). The extended morphometric character set for Protoma- gametocyst by extrusion. galhaensia delineated by Clopton and Hays (2006) and the Young solitary trophozoites (Figs. 5, 6): Young oocyst modifications described by Clopton (2011) are used herein, including the following metric characters and trophozoites solitary, extracellular forms attached to abbreviations: satellite acetabulum depth (AcD), satellite host ventricular epithelium. Holdfast a simple (i.e., acetabulum width (AcW), length of deutomerite (DL), lacking a diamerite) epimerite developing intracellu- distance from protomerite–deutomerite septum to deutom- larly in a single host epithelial cell. Epimerite very erite axis of maximum width (DLAM), distance from posterior end of deutomerite to deutomerite axis of narrowly obpyriform, expanding in distal half maximum width (DLPM), polar dehiscence plate length (Fig. 5), absent in older trophozoites (Fig. 6). Pro- (DPL), polar dehiscence plate width (DPW), width of tomerite broadly to shallowly ovoid in young deutomerite at equatorial axis (DWE), maximum width of trophozoites, becoming oblong in older solitary deutomerite (DWM), diameter of major karyosome (KD1), distance from nucleus to protomerite–deutomerite septum trophozoites, markedly constricted at protomerite– (NSD), length of nucleus (NL), width of nucleus (NW), deutomerite septum (cf. Figs. 5, 6). Deutomerite interior oocyst length (OLI), maximum exterior oocyst obovoid in young solitary trophozoites, becoming length (OLM), oocyst width (OW), width of protomerite– very narrowly to linearly oblong in older solitary deutomerite septum (PDSW), length of protomerite (PL), distance from anterior end of protomerite to protomerite axis trophozoites (cf. Figs. 5, 6). Nucleus orbicular with 1 of maximum width (PLAM), distance from protomerite– distinct, large, smooth-margined karyosome. deutomerite septum to protomerite axis of maximum width (PLPM), total length of primite (PTL), width of protomerite Association (Figs. 9–12): Presyzygial, gamontic; at equatorial axis (PWE), maximum width of protomerite gamonts anisomorphic due to structures involved in (PWM), oocyst residuum diameter (ResDia), and total association interface; association interface a shallow- length of satellite (STL). ly semi-obpanduriform interlock in which the poste- Measurements are presented in micrometers as mean rior end of the primite’s deutomerite is constricted values followed parenthetically by range values, standard deviations, and sample sizes. Metric differences between and clamped by an acetabulum formed from the species were identified using ANOVA protected Tukey’s anterior membranes of the satellite’s protomerite honestly significant difference (HSD) tests (a 5 0.05). (Figs. 9–12). Measurements taken from mature Parasite ontogenetic and anatomical nomenclature largely gamonts in association (cf. immature association of follows that proposed by Levine (1971) but defers to Clopton (2009) in reference to association, syzygy, Figs. 7, 8 and mature associations of Figs. 9–12). gametocyst development, and oocyst dehiscence. Nomen- Indices: PTL/STL 1.0 (0.9–1.2, 60.07, 30), PPL/SPL clature for the shapes of planes and solids follows Clopton 1.3 (1.0–2.6, 60.31, 30), PPWM/SPWM 1.1 (0.9– (2004). 1.4, 60.14, 30), PDL/SDL 1.0 (0.9–1.2, 60.08, 30), PDWM/SDWM 1.0 (0.8–1.3, 60.14, 30), PDWE/ RESULTS SDWE 1.0 (0.8–1.3, 60.12, 30). Protomagalhaensia blaberae Peregrine, 1970 Primite: Observations and data taken from mature (Figs. 1–16) primites in association. Epimerite absent; protomerite finely deltoid to deltoid; PL 88.1 (63.4–111.0, Generic diagnosis 611.71, 30), PWE 68.0 (50.5–94.5, 612.04, 30), Order Eugregarinida Le´ger, 1892, sensu Clopton PWM 75.1 (54.8–99.7, 611.40, 30), PLAM 58.4 (2002); Suborder Septatina Lankester, 1885, sensu (34.3–79.7, 612.22, 30), PLPM 30.9 (7.8–52.6, Clopton (2002); Superfamily Gregarinoidea, Chakar- 610.81, 30), PDSW 70.1 (52.6–91.7, 69.87, 30), avarty, 1960 sensu Clopton (2009); Family Blaber- PL/PWE 1.3 (1.0–1.7, 60.20, 30), PL/PWM 1.2 icolidae Clopton (2009); Genus Protomagalhaensia (1.0–1.6, 60.17, 30), PL/PDSW 1.3 (1.0–1.6, 60.18, Pinto, 1918 sensu Clopton