Molecular Systematics of the Avian Schistosome Genus Trichobilharzia (Trematoda: Schistosomatidae) in North America

Abstract

Trichobilharzia is a genus of thread-like schistosomes with a cosmopolitan distribution in birds. Species of Trichobilharzia achieve notoriety as major etiological agents of cercarial dermatitis, or swimmer's itch. There are 40 species described in the literature, for which the majority lacks molecular sequence information. To better understand the phylogenetic relationships, diversity, species boundaries, host use, and geographic distribution of this genus, we surveyed 378 birds and over 10,000 snails from North America. The phylogenetic analysis was based on nuclear 18S, 28S rDNA, internal transcribed spacer region and mitochondrial cytochrome oxidase I sequence data. Specimens were recovered that could be related to 6 of the 14 described species of Trichobilharzia from North America (T. physellae, T. querquedulae, T. szidati, T. stagnicolae, T. franki, and T. brantae). An additional 5 lineages were found that could not be related directly to previously described species. Trichobilharzia brantae, transmitted by Gyraulus parvus, grouped outside the clade containing the recognized species of Trichobilharzia. A subgroup of the Trichobilharzia clade designated Clade Q was comprised of closely related species whose adults and eggs are similar, yet the European species use lymnaeids whereas the North American species use physids as snail hosts. This molecular phylogeny provides a useful framework to: 1) facilitate identification of worms, including those involved in dermatitis outbreaks; 2) test hypotheses about the evolution, diversification, host-parasite interactions and character evolution of Trichobilharzia; and 3) guide future taxonomic revision of Trichobilharzia.TrichobilharziaSkrjabin and Zakharov, 1920 is the most speciose genus within the Schistosomatidae Weinland 1858. The genus is comprised of 40 described species worldwide (Blair and Islam, 1983;Horák et al., 2002), of which 14 (Table I) have been described from North America. Members of this genus are reported to infect 5 orders of aquatic birds and 4 families of freshwater snails . Adult worms occur in the mesenteric or nasal veins of their definitive hosts, usually ducks, except in Africa where they also have been reported from other groups of aquatic birds such as grebes and ibises (Fain, 1956;Blair and Islam, 1983) and in Japan, from passerine birds (Oda, 1973). Blair and Islam (1983) and Horák et al. (2002) present the most recent reviews of this genus. The known snail intermediate hosts for most of the species are members of the basommatophoran families Lymnaeidae Rafinesque, 1815 and Physidae Fitzinger, 1833. Some species of Trichobilharzia also infect snails of Planorbidae Rafinesque, 1815, another basommatophoran family (Basch, 1966;Nassi, 1987;Rind, 1991), and the Pleuroceridae Fischer, 1885, a caenogastropod family (Ito, 1960a, b). The 14 described North American species of Trichobilharzia (Table I) Cercariae of species of Trichobilharzia were the first to be implicated in causing cercarial dermatitis or swimmer's itch (Cort, 1928...

Avian Schistosomes and Outbreaks of Cercarial Dermatitis

“…In North America and Europe, where most of the research has been focused, outbreaks occur in recreational ponds and reservoirs. These outbreaks have been reviewed extensively (7,8,70,71). Species of Trichobilharzia have been reported to cause dermatitis from other areas as well, such as Rwanda-Burundi (72), South Africa (73,74), New Zealand and Australia (75)(76)(77)(78)(79), Malaysia/Indonesia (80)(81)(82), Iran (65,(83)(84)(85)(86), United Arab Emirates (66), Thailand (87), and China (88,89) in the Eastern Hemisphere and Argentina (57,90,91), Chile (11), and El Salvador (92) in the Western Hemisphere.…”

“…Mammalian schistosomes use 3 families of snails, compared to 15 families used by avian schistosomes, as summarized in 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).…”

“…There is little evidence of schistosome species crossing snail families, naturally or experimentally (for an exception, see references 119 and 120). Trichobilharzia franki was reported to be widespread across Europe, but detailed molecular studies are showing that it may represent several species related to snail host use (70,121,122).…”

“…In freshwater, L. stagnalis is found commonly in the northern Eastern hemisphere, yet in the northern Western hemisphere it is only locally common. When L. stagnalis is found to be infected, the infecting species is related to a common European species, Trichobilharzia szidati (70,123). Interestingly, P. acuta is one of the most invasive pulmonate snails and can host at least four species of avian schistosomes in North America (10,70), yet there are no reports of this snail hosting schistosomes in their invasive range (outside North America).…”

“…When L. stagnalis is found to be infected, the infecting species is related to a common European species, Trichobilharzia szidati (70,123). Interestingly, P. acuta is one of the most invasive pulmonate snails and can host at least four species of avian schistosomes in North America (10,70), yet there are no reports of this snail hosting schistosomes in their invasive range (outside North America). It is also noteworthy that most of the schistosome species transmitted by physid snails have thus far been found only in North America (at least based on genetic comparisons) (e.g., G. huronensis, T. physellae, and one undescribed lineage of schistosome [10]).…”