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

Wilhelm F Sirgel,M Dolores Bargues,Santiago Mas-Coma,Patricio Artigas

doi:10.1186/1756-3305-5-169

Wilhelm F Sirgel, M Dolores Bargues + Show 2 more

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https://doi.org/10.1186/1756-3305-5-169

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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.

Highlights

The 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
Life cycle A total of 34 years work in the small area where R. capensis occurs, leads to several conclusions: (i) this fluke species appears to be specific for M. varius, as no brachylaimid has ever been found in any of the other vertebrates inhabiting the same area; (ii) the slug Ariostralis nebulosa is the first intermediate host of this fluke species, as branched, cercariogenous sporocysts resembling those typical of brachylaimids [14,16,24,25] were frequently found but only in this slug among the five terrestrial mollusc species inhabiting the area; this means that this fluke is highly specific at first
Epizootiological data, several morphological features, comparisons with other archaic and modern brachylaimids, and intraspecific mtDNA cox1 gene sequence variability suggest that R. capensis may use two transmission strategies in the study area of the Hottentots Holland Nature Reserve, South Africa

Summary

Introduction

The 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. They affect domestic animals [3], poultry [4,5,6,7,8] and wild game birds [9,10]. They have proved to be useful as biological tags in studies of postfire ecosystem regeneration processes [11,12]. While the great majority of digenean trematodes follow an aquatic life cycle [13], brachylaimids are one of the very few trematode groups (the only other one is Dicrocoeliidae) that have succeeded in colonizing the terrestrial milieu, in some instances even very arid, xerophilic habitats [14]

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