Life cycle of Renylaima capensis, a brachylaimid trematode of shrews and slugs in South Africa: two-host and three-host transmission modalities suggested by epizootiology and DNA sequencing

Abstract

BackgroundThe life cycle of the brachylaimid trematode species Renylaima capensis, infecting the urinary system of the shrew Myosorex varius (Mammalia: Soricidae: Crocidosoricinae) in the Hottentots Holland Nature Reserve, South Africa, has been elucidated by a study of its larval stages, epizootiological data in local snails and mammals during a 34-year period, and its verification with mtDNA sequencing.MethodsParasites obtained from dissected animals were mounted in microscope slides for the parasitological study and measured according to standardized methods. The mitochondrial DNA cox1 gene was sequenced by the dideoxy chain-termination method.ResultsThe slugs Ariostralis nebulosa and Ariopelta capensis (Gastropoda: Arionidae) act as specific first and second intermediate hosts, respectively. Branched sporocysts massively develop in A. nebulosa. Intrasporocystic mature cercariae show differentiated gonads, male terminal duct, ventral genital pore, and usually no tail, opposite to Brachylaimidae in which mature cercariae show a germinal primordium and small tail. Unencysted metacercariae, usually brevicaudate, infect the kidney of A. capensis and differ from mature cercariae by only a slightly greater size. The final microhabitats are the kidneys and ureters of the shrews, kidney pelvis and calyces in light infections and also kidney medulla and cortex in heavy infections. Sporocysts, cercariae, metacercariae and adults proved to belong to R. capensis by analysis of a 437-bp-long cox1 fragment, which was identical except for three mutations in metacercariae, of which only one silent. Epizootiological studies showed usual sporocyst infection in A. nebulosa and very rare metacercarial infection in A. capensis, which does not agree with high prevalences and intensities in the shrews.ConclusionsThe presence of monotesticular adult forms and larval prevalences and intensities observed suggest that R. capensis may use two transmission strategies, a two-host life cycle by predation of A. nebulosa harbouring intrasporocystic cercariae may be the normal pattern, whereas a second mollusc host is just starting to be introduced. In shrews, a tissue-traversing, intraorganic migration followed by an interorganic migration to reach and penetrate the outer surface of either of both kidneys should occur. For first slug infection, the fluke takes advantage of the phenomenon that M. varius always urinate during defaecation. Consequently, in Brachylaimidae, the second intermediate mollusc host should evolutionarily be seen as a last addition to the cycle and their present adult stage microhabitat restricted to digestive tract and related organs as a loss of the tissue-traversing capacity of the metacercaria.

Parasitic infections of anurans from a freshwater creek community in Delta State, Niger Delta of Nigeria

“…One interesting fi nding in this study was the recovery of the metacercariae of a brachylaimid trematode from the rectum of H. galamensis. Members of the Brachylaimidae are parasitic mostly in domestic and wild birds as well as in some small mammals (Alicata, 1940;Ulmer, 1951a, b;Sirgel et al, 2012) and use terrestrial gastropods as fi rst and second intermediate hosts. The only brachylaimid trematode known so far to have an amphibian defi nitive host is Zeylanurotrema spearei, which is parasitic in the urinary bladder of Bufo marinus (see Cribb and Barton, 1991).…”

Brachylaima ezohelicis sp. nov. (Trematoda: Brachylaimidae) found from the land snail Ezohelix gainesi , with a note of an unidentified Brachylaima species in Hokkaido, Japan

“…Phylogenetic relationships of brachylaimids were inferred by sequences of 28S rDNA and cox1, using an unknown species found in this study and related taxa published in DNA databases [29,30,31,32]. The NJ phylogenetic trees of the two genes strongly suggested that the unknown species belongs to the genus Brachylaima, although the number of taxa available for the tree construction was insufficient ( Supplementary Fig.…”

Natural infection of the land snails Xerolenta obvia, Zebrina detrita, andMonacha samsunensis by Brachylaima sp. metacercariae in Kastamonu, Turkey

“…worldwide (Thiengo and Amato, 1995;Barger and Hnida, 2008;Barger, 2011;Sirgel et al, 2012;Valente et al, 2016;Gracenea and Gállego, 2017;Nakao et al, 2017), only sporocysts and cercariae have been reported in Helix aspersa as a first intermediate host in Turkey (Köse et al, 2015); metacercariae have not been reported.…”

“…Land snails and slugs are required as the first and second intermediate hosts in the life cycle of Brachylaima spp. (Yamaguti, 1975;Butcher and Grove, 2005;Barger and Hnida, 2008;Barger, 2011;Sirgel et al, 2012;Valente et al, 2016). First intermediate hosts have sporocysts and cercariae, and second intermediate hosts have metacercariae of Brachylaima spp.…”

“…First intermediate hosts have sporocysts and cercariae, and second intermediate hosts have metacercariae of Brachylaima spp. Infection occurs when the definitive hosts consume raw mollusks containing metacercariae Grove, 2001, 2005;González-Moreno and Gracenea, 2006;Barger and Hnida, 2008;Barger, 2011;Sirgel et al, 2012;Gracenea and Gállego, 2017;Nakao et al, 2017).…”