An Approach to Revealing Blood Fluke Life Cycles, Taxonomy, and Diversity: Provision of Key Reference Data Including Dna Sequence From Single Life Cycle Stages

Abstract

Revealing diversity among extant blood flukes, and the patterns of relationships among them, has been hindered by the difficulty of determining if specimens described from different life cycle stages, hosts, geographic localities, and times represent the same or different species. Persistent collection of all available life cycle stages and provision of exact collection localities, host identification, reference DNA sequences for the parasite, and voucher specimens eventually will provide the framework needed to piece together individual life cycles and facilitate reconciliation with classical taxonomic descriptions, including those based on single life cycle stages. It also provides a means to document unique or rare species that might only ever be recovered from a single life cycle stage. With an emphasis on the value of new information from field collections of any available life cycle stages, here we provide data for several blood fluke cercariae from freshwater snails from Kenya, Uganda, and Australia. Similar data are provided for adult worms of Macrobilharzia macrobilharzia and miracidia of Bivitellobilharzia nairi. Some schistosome and sanguinicolid cercariae that we recovered have peculiar morphological features, and our phylogenetic analyses (18S and 28S rDNA and mtDNA CO1) suggest that 2 of the new schistosome specimens likely represent previously unknown lineages. Our results also provide new insights into 2 of the 4 remaining schistosome genera yet to be extensively characterized with respect to their position in molecular phylogenies, Macrobilharzia and Bivitellobilharzia. The accessibility of each life cycle stage is likely to vary dramatically from one parasite species to the next, and our examples validate the potential usefulness of information gleaned from even one such stage, whatever it might be.The Schistosomatidae is one of the best known of parasite families, yet even within this group much remains to be learned about global species diversity, biogeography, patterns of vertebrate and snail host usage, and evolutionary relationships. Our knowledge of schistosome origins and diversification also will be improved by better understanding the diversity inherent in closely-related digenean families, including the 2 other families of blood flukes (the Spirorchiidae of turtles and the Sanguinicolidae of fishes), and the Clinostomidae. Blood fluke systematics, particularly of schistosomes, has received considerable attention in the last several years (e.g., Carmichael, 1984;Rollinson et al., 1997;Snyder and Loker, 2000;Attwood et al., 2002;Lockyer et al., 2003;Morgan et al., 2003; Agatsuma et al., 2004). These studies have examined morphology, DNA sequence diversity, and patterns of host use. The molecular studies, in particular, have yielded intriguing new hypotheses that delineate the broad patterns of relationships within the family and have provided an invaluable framework to examine overall schistosome and blood fluke diversity.One of the long-standing impediments to assessing diversi...

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…The genus Bivitellobilharzia is considered a schistosome of elephants, but it has also been reported from wild rhinoceroses in Nepal (38)(39)(40)(41). There are no known reports of cercarial dermatitis in humans from areas inhabited by African elephants (with the Bivitellobilharzia loxodontae schistosome), but in areas where domesticated Asian elephants are used, there have been cases of dermatitis in the mahouts, or elephant handlers, when the elephants are taken for bathing (e.g., in Sri Lanka [40]).…”

“…There are no known reports of cercarial dermatitis in humans from areas inhabited by African elephants (with the Bivitellobilharzia loxodontae schistosome), but in areas where domesticated Asian elephants are used, there have been cases of dermatitis in the mahouts, or elephant handlers, when the elephants are taken for bathing (e.g., in Sri Lanka [40]). In Nepal, Bivitellobilharzia nairi has thus far been found in wild, not domesticated, elephants (38).…”

“…At the base of clade D is an unresolved group of avian schistosomes, most of which have been implicated in dermatitis outbreaks and comprise the most diverse range of both bird and snail (9 families) host use (13,40,(56)(57)(58)(59)(60)(61)(62)(63)(64)(65)(66). Current results based on all of the available sequence data in GenBank for the internal transcribed spacer (ITS) region indicate that there are about nine distinct lineages, only two of which are described: Gigantobilharzia and Dendritobilharzia (40,(64)(65)(66)(67)(68)(69).…”

“…Current results based on all of the available sequence data in GenBank for the internal transcribed spacer (ITS) region indicate that there are about nine distinct lineages, only two of which are described: Gigantobilharzia and Dendritobilharzia (40,(64)(65)(66)(67)(68)(69). Most of the lineages in this part of clade D have one to a few species and have been seen in only a few cases, many related to dermatitis outbreaks (12) ( Table 1).…”

“…The majority of schistosome species are transmitted by the pulmonate snail families Physidae, Lymnaeidae, and Planorbidae (10,70,105). Interestingly, two snail families contain species (e.g., Biomphalaria and Indoplanorbis in the Planorbidae family and Stagnicola in the Lymnaeidae family) that can host both avian and mammalian schistosomes that cause dermatitis (40,51,70,104,106).…”