Dactylosoma, Labbe, 1894

Netherlands, Edward C., Cook, Courtney A., Du Preez, Louis H., Vanhove, Maarten P. M., Brendonck, Luc & Smit, Nico J., 2020, An overview of the Dactylosomatidae (Apicomplexa: Adeleorina: Dactylosomatidae), with the description of Dactylosoma kermiti n. sp. parasitising Ptychadena anchietae and Sclerophrys gutturalis from South Africa, International Journal for Parasitology: Parasites and Wildlife 11, pp. 246-260 : 247-248

1.3. The genus Dactylosoma

Members of the genus Dactylosoma have undergone a fair number of taxonomic disputes, with D. ranarum being the first described species of the genus. Although Lankester (1871) is often given credit for the discovery of D. ranarum (see Saunders, 1960; Levine, 1971; Barta et al., 1987; Barta, 1991; Davies and Johnston, 2000), it is clear from the original descriptions ( Lankester, 1871, 1882) that he was working with a species of Lankesterella Labbé 1899 (initially known as “ Drepanidium ” erected by Lankester (1871, 1882) however, this name had already been used by Ehrenberg (1861) for a ciliate). Nöller (1913) clarified that the first description of D. ranarum was by Kruse (1890) who believed he was describing additional developmental stages of the “ Drepanidium ” parasite that was Lankesterella minima ( Chaussat, 1850) . Kruse (1890) suggested that the parasite should be grouped with the haemogregarines, proposing the name Haemogregarina ranarum ( Kruse, 1890) if the generic name “ Drepanidium ” was to fall away. Celli and San Felice (1891) also regarded it as H. ranarum , and Grassi and Feletti (1892) as a malarial parasite, due to its resemblance to human malaria. However, Labbé (1894) recognised differences between these genera, subsequently erecting Dactylosoma based on: (1) different elongated and amoeboid body forms; (2) areolar structure, vesicular nucleus and hyaline appearance of the protoplasm; (3) lack of pigment, but presence of retractile granules; (4) minimal effect on the host cell and nucleus; and (5) merogony (“sporulation”) that gives rise to between 5 and 12 merozoites (“sporozoites”) grouped in a rosette- or fan-like appearance. Labbé (1894) named the species he placed in this newly erected genus, Dactylosoma splendens Labbé 1894 , however, according to Wenyon (1926) who supported the designation of Nöller (1913), Kruse (1890) had first used the species name “ ranarum ” for this parasite, thus Dactylosoma splendens was renamed Dactylosoma ranarum ( Kruse, 1890) .

Currently there are five recognised species of Dactylosoma , two of which infect fish hosts, namely Dactylosoma iethrinorum Saunders, 1960 , and Dactylosoma salvelini Fantham, Porter and Richardson, 1942 (see Table 1 ). The remaining three species were described from anuran hosts. The first, Dactylosoma ranarum , is the most common and a cosmopolitan species reported from several anuran species. According to Barta (1991), this species has been recorded from Pelophylax kl. esculentus (Linnaeus, 1758) in France ( Laveran, 1899), the Caucasus ( Finkelstein, 1908), and Corsica ( Boulard et al., 1982) and other European countries ( França, 1908; Nöller, 1913). Furthermore, this species has also been recorded from Central and South America in Rhinella marina (Linnaeus, 1758) (see Walton, 1946) and in an unidentified toad from Pará, Brazil ( Durham, 1902). Additionally, there have been reports in Africa from Pel. kl. esculentus collected in Constantine, Algeria ( Billet, 1904), Pelophylax saharicus (Boulenger in Hartert, 1913) from Morocco ( Seabra-Babo et al., 2015), and Pelophylax ridibundus (Pallas, 1771) (syn. Rana ridibunda ) from North Africa ( Walton, 1947, 1949), all included within the Palearctic realm. From the Ethiopian realm, hosts include Hyperolius sp. (syn. Rappia marmorata ), Amnirana galamensis (Dumeril and Bibron, 1841) (syn. Hylarana galamensis , Rana galamensis ), Ptychadena oxyrhynchus (Smith, 1849) (syn. Rana oxyrhynchus ), Ptychadena submascareniensis (Guibé and Lamotte, 1953) (syn. R. mascareniensis ) and Sclerophrys regularis (Reuss, 1833) (syn. Amietophrynus regularis , Bufo regularis ) from the Gambia ( Dutton et al., 1907). It is clear from the illustrations provided that the latter hosts were infected with several different blood parasites, all grouped as “ Drepanidia ” ( Dutton et al., 1907; Walton, 1948). Amnirana albolabris (Hallowell, 1856) (syn. Hylarana albolabris , Rana albolabris ) is reported as a host for D. ranarum from the Democratic Republic of the Congo ( Schwetz, 1930; Walton, 1947) in Central Africa, and Scl. gutturalis (syn. Scl. regularis ) in South Africa ( Fantham et al., 1942). The giant bullfrog, Pyxicephalus adspersus Tschudi, 1838 is also reported to be infected with D. ranarum from an unspecified location possibly in sub-Saharan Africa ( Walton, 1947). Lastly, there are also reports from Sylvirana guentheri (Boulenger, 1882) from Tonkin, northern Vietnam ( Mathis and Léger, 1911) and Yung Foh Lee, Yang Ming Shan, Taiwan ( Manwell, 1964). The type host and type locality for D. ranarum is Pel. kl. esculentus and probably Naples, Italy, respectively ( Kruse, 1890). The second species, Dactylosoma sylvatica Fantham, Porter and Richardson, 1942 was described from the wood frog Lithobates sylvaticus (LeConte, 1825) (syn. Rana sylvatica ) collected in the Province of Quebec, Canada. The third species is Dactylosoma taiwanensis Manwell, 1964 , described from the Alpine cricket frog, Fejervarya limnocharis (Gravenhorst, 1829) (syn. Rana Iimnocharis ) in Hualien, Hua Lien Hsien, Taiwan (see Table 1 ). In addition to the summary of reported species of Dactylosoma mentioned above, Netherlands et al. (2015) reported on an unidentified species of Dactylosoma in Ptychadena anchietae (Bocage, 1868) from northern KwaZulu-Natal, South Africa.

Species previously regarded as members of Dactylosoma are Babesiosoma mariae ( Hoare, 1930) and Babesiosoma jahni ( Nigrelli, 1929) . Two enigmatic species previously assigned to Dactylosoma , Dactylosoma tritonis ( Fantham, 1905) and D. amaniae ( Awerinzew, 1914) are more likely inclusions of rickettsial organisms according to Levine (1988) and Barta (1991). Dactylosoma clariae ( Haiba, 1962) (syn. Cytauxzoon clariae and Haemohormidium clariae ) and Dactylosoma tilapiae Imam, Marzouk, Hassan, Derhall and Itman, 1985 were considered by Negm-Eldin (1998) to not contain sufficient proof to document the validity of these species ( Smit et al., 2003). Species of Dactylosoma are characterised by similar merogonic development as for species of Babesiosoma , except for the morphologically distinct primary and secondary meronts and a varying number of merozoites produced in these cycles. In summary, D. ranarum undergoes primary merogony when a merozoite enters the host frogs’ erythrocytes. Within erythrocytes, merozoites undergo simultaneous peripheral budding, transforming into a large multinucleate meront producing up to 16 merozoites arranged in the characteristic rosette- or hand-like nature for which the genus was named (see Labbé, 1894; Nöller, 1913; Barta, 1991; Lainson, 2007). Merozoites then separate and penetrate other erythrocytes, either repeating the cycle of primary merogony or initiating secondary merogony. The cycle is repeated in secondary merogony with meronts producing up to eight merozoites that either repeat secondary merogony or mature into gamonts (see Nöller, 1913; Barta et al., 1987). To date, no complete cycles for any species of Dactylosoma have been elucidated. However, Barta (1991) used frogs captured on the island of Corsica, France, to experimentally infect the North American glossiphoniid leech Desserobdella picta (Verrill, 1872) , the natural vector of B. stableri (see below) with D. ranarum . In his study, although no observations on the development of gametes or zygote formation were made, D. ranarum was found to undergo sporogonic development within the intestinal epithelium of this experimentally infected leech host. The oocysts observed appear to be polysporoblastic producing 30 or more sporozoites by a process of exogenous budding directly into the cytoplasm of the epithelial cell ( Barta, 1991). Other haematophagous invertebrates have also been considered as potential vectors. Nöller (1913) was the first to experimentally attempt transmission of D. ranarum using the glossiphoniid leech Hemiclepsis margmata (Müller, 1774) , however, this was unsuccessful despite repeated attempts. Boulard et al. (1982) also tested the mosquito Culicoides nubeculosus (Meigen, 1830) as the potential vector of D. ranarum , but the experiments yielded no results. Although phlebotomine sand flies are the known vectors for different blood parasites of anurans ( Feng and Chung, 1940; Desportes, 1942), none thus far have been tested as potential vectors for any species of Dactylosoma .