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Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil
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Hudson A. Pinto a,∗ , Sara V. Brant b , Alan L. de Melo a a Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Brazil b University of New Mexico, Department of Biology, Albuquerque, NM 87111, USA
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Article history: Received 7 March 2014 Received in revised form 22 May 2014 Accepted 4 June 2014 Available online xxx
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Keywords: Brazil Cercariae Schistosomes Physa Trichobilharzia
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1. Introduction
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Species of Trichobilharzia are the main etiological agents of cercarial dermatitis in humans, which is considered a re-emerging disease. Despite the diversity and global distribution of this genus, studies of Trichobilharzia are scarce in South America. The goal of our investigations is better understand the diversity, distribution and life cycle of avian schistosomes and their likely role in causing dermatitis in Brazil. As part of this effort, cercariae found in naturally infected Physa marmorata were identified by morphological and molecular (mitochondrial cox1, nuclear ITS1 and 28S gene regions) methods as Trichobilharzia sp. These cercariae are similar morphologically to T. jequitibaensis described previously from Brazil and similar genetically to the North American physid transmitted species T. querquedulae and T. physellae. This is the first report of a potential agent of cercarial dermatitis from naturally infected snails from Brazil and first molecular characterization of a South America species of Trichobilharzia. A discussion follows concerning the potential role this species has in outbreaks of dermatitis in Brazil. © 2014 Published by Elsevier B.V.
The globally distributed Trichobilharzia Skrjabin and Zakharov, 1920, that currently includes 35 nominal species, is the most speciose genus of digenetic trematodes in the family Schistosomatidae. They have a two-host life cycle with an aquatic snail as intermediate and birds as definitive hosts. The adult worms live in the portal and mesenteric veins (most species) or nasal tissue. Verified species of Trichobilharzia have been reported from two families of aquatic pulmonate snails, Lymnaeidae and Physidae, and their definitive hosts include ducks in the family Anatidae. Though there are a few reports of Trichobilharzia from other avian and snail families, current knowledge, host use, and morphological characteristics of these species suggest that they may represent different genera or are aberrant occurrences (Fain, 1956; Blair and Islam, 1983; Horák et al., 2002; Brant and Loker, 2009). Added to the problem of identification, when examining snails, it was common in the
∗ Corresponding author at: Laboratório de Taxonomia e Biologia de Invertebrados, Departamento de Parasitologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, C.P. 486, Belo Horizonte, Minas Gerais 30123-970, Brazil. Tel.: +55 031 3409 2978. E-mail address:
[email protected] (H.A. Pinto).
past to identify almost any furcocercariae with pigmented eyespots as Trichobilharzia, often incorrectly. Thus far there are described about 14 species of Trichobilharzia from North America from anatid ducks and both physid and lymnaeid snails (Brant and Loker, 2009), which is in stark contrast, given the duck diversity, to the one species reported from South America, Trichobilharzia jequitibaensis Leite, Costa and Costa, 1978. This species was described in Brazil from naturally infected domesticated ducks, Cairina moschata domestica Donkin, 1989, and during laboratory life cycle studies, lymnaeid and physid snails were permissive experimental hosts (Leite et al., 1978, 1979). However, the natural intermediate hosts of T. jequitibaensis are still unknown. These 2 studies remain the only ones relating to the occurrence of Trichobilharzia in Brazil, even though a large number of trematode species were identified in molluscs (reviewed by Pinto and Melo, 2013) and birds (reviewed by Travassos et al., 1969) in Brazil. A putative Trichobilharzia sp. was described from Chilina dombeiana (Bruguière, 1789) from Chile related to an outbreak of cercarial dermatitis (Valdovinos and Balboa, 2008), but morphological features Q2 of the cercariae are not consistent with species of Trichobilharzia (Brant and Loker, 2009) and thus probably represent a different genus of avian schistosome. Species of Trichobilharzia are probably best known as the major etiological agents of cercarial dermatitis, or ‘swimmer’s itch’ in
http://dx.doi.org/10.1016/j.actatropica.2014.06.002 0001-706X/© 2014 Published by Elsevier B.V.
Please cite this article in press as: Pinto, H.A., et al., Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.06.002
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humans. Recent reviews have considered cercarial dermatitis as a re-emerged neglected disease, mainly in Europe and North America where they have been most well studied (Horák et al., 2002; Koláˇrová et al., 2013; Soldánová et al., 2013). Much of these studies have focused on the biology, systematics, evolution, and pathology of this genus to better understand the epidemiology not just of dermatitis, but avian schistosomes in general (Horák et al., 2002; Rudolfová et al., 2005, 2007; Koláˇrová et al., 2005; Koláˇrová, 2007; Jouet et al., 2008, 2010; Brant and Loker, 2009, 2013; Brant et al., 2006, 2011; Horák & Koláˇrová, 2011; Cipriani et al., 2011; Lichtenbergová and Horák, 2012). In contrast to these many recent studies of Trichobilharzia and other avian schistosomes in North America and Europe, little is known about these parasites in other continents, despite the global affliction of dermatitis in people, including in South America (Szidat, 1951, 1958; De Meillon and Stoffberg, 1954; Bosq et al., 1955; Szidat and Szidat, 1960; Leite et al., 1979; Appleton and Brock, 1986; Wooi et al., 2007; Valdovinos and Balboa, 2008; Pinto et al., 2012). Moreover, the prevalence of cercarial dermatitis by avian schistosomes is unknown or neglected in Brazil (Pinto et al., 2012). As part of our goal to increase our knowledge of schistosome diversity within molluscs in Brazil, we report the first morphological and genetic characterization of cercariae of Trichobilharzia in naturally infected snails in South America.
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2. Materials and methods
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Cercariae of Trichobilharzia were collected from Physa marmorata Guilding, 1828 (2/7; 29%) in an aquatic pond in the city of Alegre (20◦ 45 50 S, 41◦ 31 58 W), state of Espírito Santo, in southeastern Brazil, in July 2011. These cercariae were heat killed in water at 70 ◦ C and fixed in 10% formalin for morphological analysis. In addition, a subsample of cercariae were preserved in 95% ethanol and kept cold for molecular analyses. Morphological characterization of the cercariae was completed by cercarial measurements to compare with other species of Trichobilharzia, in particular, those collected from species of Physa (Talbot, 1936; Macfarlane and Macy, 1946; Wu, 1953; Edwards and Jansch, 1955; ˜ Ostrowski de Núnez, 1978; Leite et al., 1979; Brant and Loker, 2009). The morphometric analysis was performed with the aid of ocular micrometer in an optical microscope, and the photographs were taken with a digital camera attached to a Leica microscope. Cercariae were stained with alum acetocarmine, dehydrated in increasing grades of ethanol, cleared in beechwood creosote, and mounted on permanent slides in Canada balsam. Specimens of stained cercariae were deposited in the collections of the Laboratory of Taxonomy and Biology of Invertebrates, Brazil (accession number DPIC 6245a-c) and Museum of Southwestern Biology Division of Parasitology, University of New Mexico, USA (accession number MSB:Para:19006). Molecular characterization of the cercariae was performed by polymerase chain reaction (PCR) of the mitochondrial cytochrome oxidase subunit I (cox1; 824 bp), the internal transcribed spacer region 1 (ITS1; 1340 bp) and a 5 prime section (1185 bp) of 28S ribosomal DNA. DNA extraction, PCR conditions, sequencing and sequence analysis methods were as described by Brant and Loker (2009). The sequences obtained were compared with those reported for other species of avian schistosomes available in GenBank, including the North American T. physellae and T. querquedulae, two species that have also been reported in Physa spp. Phylogenetic analyses of the genetic data were performed using the methods of maximum parsimony (MP), maximum likelihood (ML), minimum evolution (ME) using the software PAUP* 4.0b10. Nodal support was estimated using the bootstrap method with over 500 replicates for ME and MP, and 200 replicates for ML. The sequences obtained
Fig. 1. Cercariae of Trichobilharzia sp. found in Physa marmorata from Brazil. Vital staining by neutral red. Scale bar: 100 m.
were deposited in GenBank under the accession numbers KJ855994 to KJ855997. 3. Results and discussion The general morphological traits and measurements of the cercariae obtained in this study (Fig. 1) are in agreement with those reported for species of Trichobilharzia transmitted by physid snails by several authors (Table 1). The cercariae of Trichobilharzia sp. reported in the present study resemble those reported for T. jequitibaensis by Leite et al. (1979), though some measurements are smaller. Relative to the species from physid snails, our sample had body and tail stem measurements much smaller to those described for T. querquedulae, T. cameroni, T. oregonensis (Macfarlane and Macy, 1946; Wu, 1953; Brant and Loker, 2009). Regarding T. physellae, although less clear, the measurements of tail stem are also longer than our Brazilian Trichobilharzia sp., and with the exception of the anterior organ, the range of the other morphological traits ˜ overlap (Talbot, 1936). Cercaria I described by Ostrowski de Núnez (1978) also collected from P. marmorata in Argentina is smaller than Brazilian Trichobilharzia sp. Interestingly, all available measurements for T. adamsi overlap with our species (Edwards and Jansch, 1955). Nevertheless, the conclusive study of the sizes of cercariae with the aim of specific identification is extremely difficult, since factors such as host-induced size differences, intraspecific variation, methodological differences in fixation methods, all have
Please cite this article in press as: Pinto, H.A., et al., Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.06.002
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265 ± 8 60 ± 5 374 ± 11 40 ± 4 196 ± 8 32 ± 9 0.71 1.9 95 ± 5 39 ± 2 29 ± 2 – – – – – VS – anterior VS – posterior Eye spots
Ventral sucker
L W L W L L L W Body:tail Tail:furcae Anterior organ
Furcae
Tail stem
Body
L W L W L W
216 ± 10 (201–240) 82 ± 8 (64–93) 336 ± 28 (249–376) 44 ± 5 (35–60) 217 ± 14 (177–236) 19 ± 3 (11–27) 0.64 (0.54–0.77) 1.56 (1.29–1.72) 66 ± 3 (60–71) 51 ± 4 (45–59) 24 ± 3 (19–29) 23 ± 3 (17–27) 113 ± 9 (95–134) 82 ± 7 (71–103) 11 ± 1 (9–13) 10 ± 1 (8–14)
P. gyrina USA Hot formalin Physa marmorata Brazil Hot formalin + staining Host Locality Fixation
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270 ± 19 (227–302) 66 ± 6.5 (53–76) 282 ± 27 (213–320) 38 ± 5.7 (28–52) 183 ±13 (148–210) 18 ± 3 (13–27) 0.96 1.54 87 ± 6.4 (72–101) 46 ± 4.7 (37–58) 25 ± 2.6 (20–32) 28 ± 2.3 (20–33) 172 ± 14 (140–197) 72 ± 2 (57–66) 8 ± 0.9 (6.6–9.3) 6 ± 0.9 (5.3–9.3) 230 ± 6.9 80 ± 1.4 341 ± 2.3 44 ± 0.8 201 ± 5.4 – 0.67 1.69 – 52 ± 0.7 37 ± 0.6 – – 97 ± 5.9 – – 319 ± 26 (257–361) 57 ± 4 (52–70) 369 ± 24 (347–424) 38 ± 1.5 (35–42) 225 ± 11 (195–253) 23 ± 1.4 (19–26) 0.86 1.64 108 ± 11 (80–132) 38 ± 4 (28–46) 30 ± 2 (24–31) 32 ± 2 (28–35) 187 ± 22 (187–219) 90 ± 12 (73–111) – – 315 69 426 47 222 – 0.74 1.92 97 48 28
P. gyrina Canada Hot formalin
P. marmorata Brazil Hot formalin
T. querquedulae
Brant and Loker (2009) P. gyrina USA 95% ethanol Ostrowski de ˜ (1978) Núnez P. marmorata Argentina Hot formalin
Cercaria I T. jequitibaensis
Edwards and Jansch (1955) P. coniformis Canada Hot formalin Macfarlane and Macy (1946) P. ampullacea USA Hot formalin
Leite et al. (1979)
T. adamsi T. cameroni
Wu (1953)
T. oregonensis
Pence and Rhodes (1982) P. anatina USA Hot AF A +staining 244 ± 15 60 ± 4 301 ± 7 36 ± 4 157 ± 4 18 ± 1 0.81 1.92 – – 18 ± 3 – – 68 ± 6 – – T. physellae
Talbot (1936) Present study
Trichobilharzia sp. Species
Table 1 Morphometric data of larval stages of Trichobilharzia sp. that emerged from Physa marmorata from Brazil, and other similar larvae described by different authors. Measurements are presented in micrometers as the means followed by standard deviation and range in parentheses. Abbreviations: L = length, W = width.
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Fig. 2. Maximum likelihood tree of Schistosomatidae based on the 5 region 28S nuclear DNA sequence. Outgroups for the family are the marine turtle spirorchiids, Carettacola hawaiiensis, Learedius learedi, and Hapalotrema mehrai. The box indicates ‘Clade Q’ within the genus Trichobilharzia. The specimen in bold is Trichobilharzia sp. from Physa marmorata from Brazil collected for this study. Node support is indicated by MP/ME/ML bootstrap values, respectively. The dash indicates no significant node support.
been reported for the study of larval trematodes including Schistosomatidae (Blair and Islam, 1983; Horák et al., 2002). Indeed, Jouet et al. (2010) showed that depending on the intermediate host (Radix auricularia or Radix peregra), the larvae of T. franki, a European species from the ‘Clade Q’ sensu Brant and Loker (2009) have distinct measurements. The molecular data confirm that the cercariae collected from naturally infected P. marmorata from Brazil are members of the genus Trichobilharzia (Figs. 2 and 3). Furthermore the Brazilian sample is most closely related to the physid-transmitted species of Trichobilharzia than the lymnaeid transmitted species and places it as a member of ‘Clade Q’ sensu Brant and Loker (2009) (Fig. 3 and Table 2). A pairwise comparison of the sequences obtained in this study and those reported for other species of Trichobilharzia is reported in Table 2 and shows that the Brazil sample is as different from the other species of Trichobilharzia as they all are from each other lending support to its status of a distinct species. A comparison of the cox1 and ITS1 tree show the Brazilian Trichobilharzia in two different positions. There is strong support in the cox1 tree placing our sample sister to the North America physid transmitted T. physellae. However, there is some support in the ITS1 tree placing out sample as sister the other North America physid transmitted species, T. querquedulae. In the 28S tree, also a nDNA tree, our sample grouped with T. physellae, though there was no bootstrap support, lending more support perhaps for the cox1 tree. There are a couple of hypotheses to consider reconciling the conflicting phylogenetic results of the mtDNA versus the nDNA. One hypothesis is that this species is of hybrid origin probably
Please cite this article in press as: Pinto, H.A., et al., Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.06.002
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Fig. 3. Maximum likelihood trees focused on Clade Q of Trichobilharzia (A) based on cox1 mitochondrial DNA sequence and (B) based on ITS1 internal transcribed spacer region of nuclear DNA. The specimen in bold is Trichobilharzia sp. from Physa marmorata from Brazil collected for this study. Node support is indicated by MP/ME/ML bootstrap values, respectively. The taxonomic names in the tree are as follow: species, individual code, continent (sometimes country) codes, GenBank accession number. Codes are as follow NA = North America, EU = Europe (IS = Iceland, FN = Finland).
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from ducks migrating from North to South America. Anas discors (bluewinged teal) and Anas cyanoptera (cinnamon teal) are common species in North America that are known to migrate as far south as Brazil. These are also two of three species that are each other’s closest relatives and have been found as exclusive wild hosts for T. querquedulae (Johnson and Sorenson, 1999; Brant and Loker, 2009). The presence of T. querquedulae in migrating ducks from North America is a possible source. Trichobilharzia physellae is found in diving ducks (Bucephala, Aythya, Mergus, Clangula), an ecological group of ducks, rather than phylogenetic lineage within Anatidae. Several species of diving ducks are native from Brazil, and while it is not common for these divers in North America to migrate as far south as Brazil, some make it to northern Central America. Physids are widely distributed, particularly P. acuta and thus a suitable snail host would be available. Because T. physellae is not as bird host specific as T. querquedulae, perhaps local migrating populations of ducks are able to maintain infections. A second hypothesis is that there are multiple different copies of ITS1 in a
single individual (e.g. Koch et al., 2003; Brant, unpublished results), Q3 although this would need additional testing for trematodes. Additional specimens of the species of Trichobilharzia from P. marmorata would also provide more robust affiliations. Here we present only one sample from one locality. The patterns found here may be a result of having only a single specimen and the genetic differences (Table 2) are not distant enough to strongly support a single pattern across the two genes compared here. Thus, given the complexity inherent in the genus Trichobilharzia, a thorough study is necessary taking into account the different species currently referenced, their hosts, but also the validity of the evolutionary histories of the domains used for molecular analyses. The first report of brevifurcated cercariae (Cercaria segmentata), perhaps a species of Trichobilhariza, in P. marmorata from Brazil was done by Lutz (1933). Later, Leite et al. (1979) described the cercariae of T. jequitibaensis infecting laboratory-reared P. marmorata and Lymnaea columella Say, 1817. There was an additional report of P. marmorata with a Trichobilharzia-like cercariae from
Table 2 Percent uncorrected p genetic distances for cox1 and ITS1, respectively, among species of Trichobilharzia (Clade Q) from North America and Europe and to the Trichobilharzia sp. from Brazil. The dash indicates that no comparisons were made. Species isolates, origin (country), hosts and GenBank accession numbers can be found in Fig. 3.
(1) Trichobilharzia regenti (2) W701 Trichobilharzia Brazil (3) Trichobilharzia querquedulae (4) Trichobilharzia physellae (5) Trichobilharzia franki (6) Trichobilharzia sp. A (7) Trichobilharzia sp. C (8) Trichobilharzia Francea (9) Trichobilharzia franki Ab (10) Trichobilharzia franki Bc a b c
(1)
(2)
(3)
(4)
(5)
(6)
(7)
(8)
(9)
(10)
0.2/– 10.6/– 11.4/– 10.6/– 10.6/– 9.9/– 11.6/– 9.1/– – –
– 9.0/1.3 7.0/1.3 9.7/1.6 8.6/1.3 10.5/– 9.6/– –/2.2 –/2.0
0.8/0.2 8.6/1.8 8.1/1.9 8.7/1.7 8.8/– 9.2/– –/2.6 –/2.3
0.16/0.1 9.1/1.0 8.8/0.9 9.2/– 9.7/– –/2.1 –/1.8
0.7/0.8 8.6/0.7 8.8/– 9.9/– –/2.1 –/1.7
1.5/0.6 9.1/– 9.3/– –/2.0 –/1.7
– 10.5/– –/– –/–
1.1/– –/– –/–
–/1.5 –/0.4
–/1.1
Samples from France from Radix peregra: Trichobilharzia EAN57, Trichobilharzia EAN31, Trichobilharzia DOUC1 in Fig. 3A. Trichobilharzia franki A includes: Trichobilharzia franki ls25, Trichobilharzia franki ls19, Trichobilharzia franki Ra3 in Fig. 3B. Trichobilharzia franki B includes: Trichobilharzia franki 08, Trichobilharzia franki 014, Trichobilharzia franki M2, Trichobilharzia franki LS1 in Fig. 3B.
Please cite this article in press as: Pinto, H.A., et al., Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.06.002
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˜ Argentina described as Cercaria I by Ostrowski de Núnez (1978). The samples in these three reports plus our new report may represent conspecifics. Moreover, similar cercariae were also found in P. marmorata from locations from the state of Minas Gerais, Brazil in the mid-1990s (unpublished results). Given the wide distribution of P. marmorata in the neotropics, it is possible that this snail species is involved in the transmission of Trichobilharzia elsewhere in the country. Both experimental studies exposing these cercariae to duck hosts and examination of wild and domestic ducks to obtain adult parasites followed with molecular confirmation are necessary to solidify the links in the life cycle and specific identification of this Trichobilharzia species. There is the possibility that a species of North American schistosomes arriving via a migratory bird might expose these snails, though comparison to data generated from samples across North America have so far not matched the sample from Brazil (Brant, unpublished). However, in view of the dissemination of Physa spp., including P. acuta that is an invasive species, the possibility of North American species of Trichobilharzia found in Brazil cannot be ruled out. The snail host, P. marmorata, is interesting because while it is a physid snail, it is in a different clade of physid snails than those snails used by the North American species of Trichobilharzia. It is considered to belong to the Aplexa 3 clade of physid snails according to the molecular phylogenetic analyses of Wethington and Lydeard (2007). It also belongs to groups of physids that have not been reported outside of South America as hosts of Trichobilharzia. There are few reports of schistosomes from aplexid physids but their generic affiliations remain unknown (e.g. Gerard, 2004). Physa marmorata has a native range in the Caribbean, Central America and northern South America but also has been a relatively successful invasive species in Africa (e.g. Paraense, 1986; Taylor, 2003; Dana and Appleton, 2007; Bony et al., 2008). In comparison, the North America species Physa acuta (Draparnaud, 1805) and P. gyrina (both hosts of avian schistosomes, Trichobilharzia in particular) are probably the most abundant physids. Currently, the North American native P. acuta is the single most widely distributed physid worldwide (Paraense and Pointier, 2003). The commonality among at least these three species of physids are that they are habit generalists, thriving in both natural and altered environments with a wide tolerance for water temperature and chemistry – ponds, drainage ditches, rivers, marshes, ephemeral water (Taylor, 2003; Dana and Appleton, 2007; Bony et al., 2008). Physa acuta is also an invasive and widespread species in South America, where it has attained high densities mainly in disturbed environments, includ˜ ing areas in which it occurs in sympatry with P. marmorata (Núnez, 2010). Although specimens of P. acuta are commonly evaluated for trematode larval infection, it has not yet been found infected with Trichobilharzia (or other schistosomes) in Brazil. This raises an interesting set of question relative to snail host specificity of at least the now three known lineages of Trichobilharzia that use physid snails. Are T. physellae or T. querquedulae able to infect P. marmorata? Is the species of Trichobilharzia found in this work able to infect P. gyrina or P. acuta? These questions are even more compelling because the results of Leite et al. (1979) showed the experimental infection of physid and lymnaeid by T. jequitibaensis, thus bringing in the question of snail host use and transmission of species of Trichobilharzia, at least those in Clade Q. On the other hand, it is possible that specificity for the first intermediate host does not exist at least in some species of Trichobilharzia, given that T. physellae has been reported from 4 species (P. acuta, P. gyrina, P. parkeri, P. magnalacustris) of North American physids (Talbot, 1936; Pence and Rhodes, 1982; Brant and Loker, 2009). The results obtained in this study should serve as a warning about the possibility of occurrence of cercarial dermatitis by larvae Trichobilharzia in Brazil. In fact, in North America, the involvement of Physa spp. in the transmission of Trichobilharzia and in
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maintenance of outbreaks of cercarial dermatitis by species of this genus was reported and is not uncommon (Cort, 1950; Wu, 1953; Edwards and Jansch, 1955; Brant and Loker, 2009). In South America, cercarial dermatitis in humans by non-S. mansoni larval trematodes were diagnosed in Argentina between the 1950s and 1960s (Szidat, 1951, 1958; De Meillon and Stoffberg, 1954; Bosq et al., 1955; Szidat and Szidat, 1960) and more recently in Chile (Valdovinos and Balboa, 2008). In Brazil, cases of cercarial dermatitis by bird schistosomes have not been identified, possibly due to the lack of studies and difficulties related to differential diagnosis with dermatitis caused by larvae of S. mansoni (Pinto et al., 2012). On the other hand, cercariae with morphology compatible with other larval avian schistosomes have been found frequently in other mollusc species from different regions of this country (unpublished data). Accordingly, future studies on avian schistosomes, both biological and epidemiological, may reveal the occurrence of human cases of cercarial dermatitis by these parasites in Brazil, as well as increasing knowledge about the diversity of schistosomatids in South America. Acknowledgements We would like to thank Miss Ana Paula Martins Oliveira from our library for helping us with bibliographies, and to National Council for Scientific and Technological (CNPq), Brazil. The work was also supported by a National Science Foundation (NSF) grant to Q4 (SVB) DEB 1021427 and technical assistance at the University of New Mexico Molecular Biology Facility was supported by NIH grant 1P20RR18754 from the Institute Development Award Program of the National Center for Research Resources. References Appleton, C.C., Brock, K., 1986. The penetration of mammalian skin by cercariae of Trichobilharzia sp. (Trematoda: Schistosomatidae) from South Africa. Onderstepoort J. Vet. Res. 53, 209–211. Blair, D., Islam, K.S., 1983. The life cycle and morphology of Trichobilharzia australis n. sp. (Digenea: Schistosomatidae) from the nasal blood vessels of the black duck (Anas superciliosa) in Australia, with a review of the genus Trichobilharzia. Syst. Parasitol. 5, 89–117. Bony, Y.K., Kouassi, N.C., Diomandé, D., Gourene, G., Verdoit-Jarraya, M., Pointier, J.P., 2008. Ecological conditions for spread of the invasive snail Physa marmorata (Pulmonata: Physidae) in the Ivory Coast. Afr. Zool. 43, 53–60. Bosq, P., Szidat, L., Soria, M.F., 1955. Dermatitis schistosomica por Cercaria chascomusi. Prensa Méd. Argent. 42, 3500–3504. Brant, S.V., Loker, E.S., 2009. Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. J. Parasitol. 95, 941–963. Brant, S.V., Loker, E.S., 2013. Discovery-based studies of schistosome diversity stimulate new hypotheses about parasite biology. Trends Parasitol. 29, 449–459. Brant, S.V., Bochte, C.A., Loker, E.S., 2011. New intermediate host records for the avian schistosomes Dendritobilharzia pulverulenta, Gigantobilharzia huronensis, and Trichobilharzia querquedulae from North America. J. Parasitol. 97, 946–949. Brant, S.V., Morgan, J.A.T., Mkoji, G.M., Snyder, S.D., Rajapakse, J.R.P.V., Loker, E.S., 2006. An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. J. Parasitol. 92, 77–88. Cipriani, P., Mattiucci, S., Paoletti, M., Scialanca, F., Nascetti, G., 2011. Molecular evidence of Trichobilharzia franki Müller and Kimmig, 1994 (Digenea: Schistosomatidae) in Radix auricularia from Central Italy. Parasitol. Res. 109, 935–940. Cort, W.W., 1950. Studies on schistosome dermatitis XI. Status of knowledge after more than twenty years. Am. J. Hyg. 52, 251–307. Dana, P., Appleton, C.C., 2007. Observations on the population dynamics of the invasive freshwater snail Aplexa marmorata (Pulmonata: Physidae) in Durban, South Africa. S. Afr. J. Sci. 103, 493–496. De Meillon, B., Stoffberg, N., 1954. Swimmer’s Itch in South Africa. S. Afr. Med. J. 28, 1062–1064. Edwards, D.K., Jansch, M.E., 1955. Two new species of dermatitis producing schistosome cercariae from Cultus lake, British Columbia. Can. J. Zool. 33, 182–194. Fain, A., 1956. Les Schistosomes d’Oiseaux du Genre Trichobilharzia Skrjabin et Zakharow, 1920 au Ruanda Urundi. Rev. Zool. Bot. Afr. 54, 147–178. Gerard, C., 2004. First occurrence of Schistosomatidae infecting Aplexa hypnorum (Gastropoda, Physidae) in France. Parasite 11, 231–234. Horák, P., Koláˇrová, L., Adema, C.M., 2002. Biology of the schistosome genus Trichobilharzia. Adv. Parasitol. 52, 155–233.
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Please cite this article in press as: Pinto, H.A., et al., Physa marmorata (Mollusca: Physidae) as a natural intermediate host of Trichobilharzia (Trematoda: Schistosomatidae), a potential causative agent of avian cercarial dermatitis in Brazil. Acta Trop. (2014), http://dx.doi.org/10.1016/j.actatropica.2014.06.002
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