Research

22 pages, 1807 KiB

Open AccessArticle

Phylogenomics and Diversification of the Schistosomatidae Based on Targeted Sequence Capture of Ultra-Conserved Elements

by Erika T. Ebbs, Eric S. Loker, Lijing Bu, Sean A. Locke, Vasyl V. Tkach, Ramesh Devkota, Veronica R. Flores, Hudson A. Pinto and Sara V. Brant

Pathogens 2022, 11(7), 769; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11070769 - 05 Jul 2022

Cited by 2 | Viewed by 2356

Abstract

Schistosomatidae Stiles and Hassall 1898 is a medically significant family of digenetic trematodes (Trematoda: Digenea), members of which infect mammals or birds as definitive hosts and aquatic or amphibious gastropods as intermediate hosts. Currently, there are 17 named genera, for many of which [...] Read more.

Schistosomatidae Stiles and Hassall 1898 is a medically significant family of digenetic trematodes (Trematoda: Digenea), members of which infect mammals or birds as definitive hosts and aquatic or amphibious gastropods as intermediate hosts. Currently, there are 17 named genera, for many of which evolutionary interrelationships remain unresolved. The lack of a resolved phylogeny has encumbered our understanding of schistosomatid evolution, specifically patterns of host-use and the role of host-switching in diversification. Here, we used targeted sequence capture of ultra-conserved elements (UCEs) from representatives of 13 of the 17 named genera and 11 undescribed lineages that are presumed to represent either novel genera or species to generate a phylogenomic dataset for the estimation of schistosomatid interrelationships. This study represents the largest phylogenetic effort within the Schistosomatidae in both the number of loci and breadth of taxon sampling. We present a near-comprehensive family-level phylogeny providing resolution to several clades of long-standing uncertainty within Schistosomatidae, including resolution for the placement of the North American mammalian schistosomes, implying a second separate capture of mammalian hosts. Additionally, we present evidence for the placement of Macrobilharzia at the base of the Schistosoma + Bivitellobilharzia radiation. Patterns of definitive and intermediate host use and a strong role for intermediate host-switching are discussed relative to schistosomatid diversification. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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12 pages, 1019 KiB

Open AccessArticle

The Tails of Two Avian Schistosomes: Paired Exposure Study Demonstrates Trichobilharzia stagnicolae Penetrates Human Skin More Readily than a Novel Avian Schistosome from Planorbella

by Nathaniel J. Anderson, Curtis L. Blankespoor and Randall J. DeJong

Pathogens 2022, 11(6), 651; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11060651 - 04 Jun 2022

Cited by 1 | Viewed by 3579

Abstract

A novel schistosome from Planorbella snails currently known as avian schistosomatid sp. C (ASC) was recently described as being capable of causing the papules associated with swimmer’s itch. We conducted a paired study with 24 human volunteers, exposing each of their forearms to [...] Read more.

A novel schistosome from Planorbella snails currently known as avian schistosomatid sp. C (ASC) was recently described as being capable of causing the papules associated with swimmer’s itch. We conducted a paired study with 24 human volunteers, exposing each of their forearms to five drops of water containing cercariae of ASC or Trichobilharzia stagnicolae, and examined the skin for papules 1–3 days later. A mixed effects model showed that only the parasite species significantly affected the number of papules, while prior experimental exposure, swimming history, and swimmer’s itch experience did not. The total number of papules produced by the two species were very different: ASC produced a total of 2 papules from the 298 cercariae used, compared to 49 papules from 160 T. stagnicolae cercariae, a difference factor of more than 43X, which was comparable to the odds ratio of 45.5 computed using the statistical model. A well-known agent of swimmer’s itch, T. stagnicolae, is able to penetrate human skin more frequently than ASC, likely meaning that ASC is only a minor cause of swimmer’s itch where T. stagnicolae is present. We also completed limited experiments that compared the cercarial behavior of the two species in vitro and in situ. A known stimulant of schistosome cercarial penetration, α-linolenic acid, did not stimulate ASC cercariae to initiate penetration-associated behaviors as frequently as T. stagnicolae. However, when placed on esophageal tissue of the known vertebrate host for ASC, Canada goose (Branta canadensis), ASC cercariae were observed penetrating the esophageal epithelium quickly, whereas T. stagnicolae cercariae did not exhibit any penetration behaviors. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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23 pages, 3544 KiB

Open AccessArticle

Cercariae of a Bird Schistosome Follow a Similar Emergence Pattern under Different Subarctic Conditions: First Experimental Study

by Miroslava Soldánová, Ana Born-Torrijos, Roar Kristoffersen, Rune Knudsen, Per-Arne Amundsen and Tomáš Scholz

Pathogens 2022, 11(6), 647; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11060647 - 03 Jun 2022

Cited by 4 | Viewed by 1747

Abstract

The emergence of cercariae from infected mollusks is considered one of the most important adaptive strategies for maintaining the trematode life cycle. Short transmission opportunities of cercariae are often compensated by periodic daily rhythms in the cercarial release. However, there are virtually no [...] Read more.

The emergence of cercariae from infected mollusks is considered one of the most important adaptive strategies for maintaining the trematode life cycle. Short transmission opportunities of cercariae are often compensated by periodic daily rhythms in the cercarial release. However, there are virtually no data on the cercarial emergence of bird schistosomes from freshwater ecosystems in northern latitudes. We investigated the daily cercarial emergence rhythms of the bird schistosome Trichobilharzia sp. “peregra” from the snail host Radix balthica in a subarctic lake under both natural and laboratory seasonal conditions. We demonstrated a circadian rhythm with the highest emergence during the morning hours, being seasonally independent of the photo- and thermo-period regimes of subarctic summer and autumn, as well as relatively high production of cercariae at low temperatures typical of northern environments. These patterns were consistent under both field and laboratory conditions. While light intensity triggered and prolonged cercarial emergence, the temperature had little effect on cercarial rhythms but regulated seasonal output rates. This suggests an adaptive strategy of bird schistosomes to compensate for the narrow transmission window. Our results fill a gap in our knowledge of the transmission dynamics and success of bird schistosomes under high latitude conditions that may serve as a basis for elucidating future potential risks and implementing control measures related to the spread of cercarial dermatitis due to global warming. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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23 pages, 2723 KiB

Open AccessArticle

Morphological, Behavioral, and Molecular Characterization of Avian Schistosomes (Digenea: Schistosomatidae) in the Native Snail Chilina dombeyana (Chilinidae) from Southern Chile

by Pablo Oyarzún-Ruiz, Richard Thomas, Adriana Santodomingo, Gonzalo Collado, Pamela Muñoz and Lucila Moreno

Pathogens 2022, 11(3), 332; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11030332 - 09 Mar 2022

Cited by 5 | Viewed by 2330

Abstract

Avian schistosomes are blood flukes parasitizing aquatic birds and snails, which are responsible for a zoonotic disease known as cercarial dermatitis, a hypersensitive reaction associated to the cutaneous penetration of furcocercariae. Despite its worldwide distribution, its knowledge is fragmentary in the Neotropics, with [...] Read more.

Avian schistosomes are blood flukes parasitizing aquatic birds and snails, which are responsible for a zoonotic disease known as cercarial dermatitis, a hypersensitive reaction associated to the cutaneous penetration of furcocercariae. Despite its worldwide distribution, its knowledge is fragmentary in the Neotropics, with most of data coming from Argentina and Brazil. In Chile, there are only two mentions of these parasites from birds, and one human outbreak was associated to the genus “Trichobilharzia”. However, the identity of such parasites is pending. The aim of this study was to identify the furcocercariae of avian schistosomes from Southern Chile using an integrative approach. Thus, a total of 2283 freshwater snails from different families were collected from three different regions. All snails were stimulated for the shedding of furcocercariae, but only Chilina dombeyana (Chilinidae) from the Biobío region was found to be parasitized. The morphology and phylogenetic analyses of 28S and COI genes stated two lineages, different from Trichobilharzia, shared with Argentina. This study provides new information on Neotropical schistosomes, highlighting the need for major research on these neglected trematodes, which are considered to be emerging/re-emerging parasites in other parts of the globe as consequence of anthropogenic disturbances and climatic change. Highlights: 1. Two different lineages (Lineage I and II) were described and molecularly characterized (28S and COI genes); 2. Cercaria chilinae I y II are proposed as a synonymous of Lineage II. Thus, a total of four different lineages of avian schistosomes are related to Chilina spp.; 3. Chilina spp. represents an important intermediate host for avian schistosomes in South America, constituting a reservoir de schistosomes with zoonotic potential; 4. Coinfection between the two different lineages was found, a finding previously not reported for avian schistosomes; 5. Expansion in the geographic distribution of Nasusbilharzia melancorhypha from its original record in Argentina, with Chilina dombeyana as an additional intermediate host. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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14 pages, 1648 KiB

Open AccessArticle

Somatic Dimorphism in Cercariae of a Bird Schistosome

by Miroslava Soldánová, Petra Kundid, Tomáš Scholz, Roar Kristoffersen and Rune Knudsen

Pathogens 2022, 11(3), 290; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11030290 - 24 Feb 2022

Cited by 3 | Viewed by 2095

Abstract

Phenotypic polymorphism is a commonly observed phenomenon in nature, but extremely rare in free-living stages of parasites. We describe a unique case of somatic polymorphism in conspecific cercariae of the bird schistosome Trichobilharzia sp. “peregra”, in which two morphs, conspicuously different in their [...] Read more.

Phenotypic polymorphism is a commonly observed phenomenon in nature, but extremely rare in free-living stages of parasites. We describe a unique case of somatic polymorphism in conspecific cercariae of the bird schistosome Trichobilharzia sp. “peregra”, in which two morphs, conspicuously different in their size, were released from a single Radix balthica snail. A detailed morphometric analysis that included multiple morphological parameters taken from 105 live and formalin-fixed cercariae isolated from several naturally infected snails provided reliable evidence for a division of all cercariae into two size groups that contained either large or small individuals. Large morph (total body length of 1368 and 1339 μm for live and formalin-fixed samples, respectively) differed significantly nearly in all morphological characteristics compared to small cercariae (total body length of 976 and 898 μm for live and formalin samples, respectively), regardless of the fixation method. Furthermore, we observed that small individuals represent the normal/commonly occurring phenotype in snail populations. The probable causes and consequences of generating an alternative, much larger phenotype in the parasite infrapopulation are discussed in the context of transmission ecology as possible benefits and disadvantages facilitating or preventing the successful completion of the life cycle. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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16 pages, 1576 KiB

Open AccessEditor’s ChoiceArticle

First Record of Trichobilharzia physellae (Talbot, 1936) in Europe, a Possible Causative Agent of Cercarial Dermatitis

by Nikolaus Helmer, Hubert Blatterer, Christoph Hörweg, Susanne Reier, Helmut Sattmann, Julia Schindelar, Nikolaus U. Szucsich and Elisabeth Haring

Pathogens 2021, 10(11), 1473; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10111473 - 12 Nov 2021

Cited by 9 | Viewed by 3237

Abstract

Several species of avian schistosomes are known to cause dermatitis in humans worldwide. In Europe, this applies above all to species of the genus Trichobilharzia. For Austria, a lot of data are available on cercarial dermatitis and on the occurrence of Trichobilharzia [...] Read more.

Several species of avian schistosomes are known to cause dermatitis in humans worldwide. In Europe, this applies above all to species of the genus Trichobilharzia. For Austria, a lot of data are available on cercarial dermatitis and on the occurrence of Trichobilharzia, yet species identification of trematodes in most cases is doubtful due to the challenging morphological determination of cercariae. During a survey of trematodes in freshwater snails, we were able to detect a species in the snail Physella acuta (Draparnaud, 1805) hitherto unknown for Austria, Trichobilharzia physellae; this is also the first time this species has been reported in Europe. Species identification was performed by integrative taxonomy combining morphological investigations with molecular genetic analyses. The results show a very close relationship between the parasite found in Austria and North American specimens (similarity found in CO1 ≥99.57%). Therefore, a recent introduction of T. physellae into Europe can be assumed. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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Review

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27 pages, 2454 KiB

Open AccessEditor’s ChoiceReview

Scratching the Itch: Updated Perspectives on the Schistosomes Responsible for Swimmer’s Itch around the World

by Eric S. Loker, Randall J. DeJong and Sara V. Brant

Pathogens 2022, 11(5), 587; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050587 - 16 May 2022

Cited by 8 | Viewed by 5515

Abstract

Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they [...] Read more.

Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they penetrate human skin. Recent years have witnessed a dramatic increase in our understanding of schistosome diversity, now encompassing 17 genera with eight more lineages awaiting description. Collectively, schistosomes exploit 16 families of caenogastropod or heterobranch gastropod intermediate hosts. Basal lineages today are found in marine gastropods and birds, but subsequent diversification has largely taken place in freshwater, with some reversions to marine habitats. It seems increasingly likely that schistosomes have on two separate occasions colonized mammals. Swimmer’s itch is a complex zoonotic disease manifested through several different routes of transmission involving a diversity of different host species. Swimmer’s itch also exemplifies the value of adopting the One Health perspective in understanding disease transmission and abundance because the schistosomes involved have complex life cycles that interface with numerous species and abiotic components of their aquatic environments. Given the progress made in revealing their diversity and biology, and the wealth of questions posed by itch-causing schistosomes, they provide excellent models for implementation of long-term interdisciplinary studies focused on issues pertinent to disease ecology, the One Health paradigm, and the impacts of climate change, biological invasions and other environmental perturbations. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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9 pages, 305 KiB

Open AccessReview

Simplifying Schistosome Surveillance: Using Molecular Cercariometry to Detect and Quantify Cercariae in Water

by Brooke A. McPhail, Kelsey Froelich, Ronald L. Reimink and Patrick C. Hanington

Pathogens 2022, 11(5), 565; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens11050565 - 10 May 2022

Cited by 5 | Viewed by 1891

Abstract

Avian schistosomes are considered a public health nuisance due to their ability to cause swimmer’s itch when accidentally encountering humans rather than their intended avian hosts. Researchers have been monitoring their presence and abundance through snail collections and cercariometry. Cercariometry methods have evolved [...] Read more.

Avian schistosomes are considered a public health nuisance due to their ability to cause swimmer’s itch when accidentally encountering humans rather than their intended avian hosts. Researchers have been monitoring their presence and abundance through snail collections and cercariometry. Cercariometry methods have evolved over the last several decades to detect individual schistosome species from a single water sample, simplifying the monitoring of these parasites. This methodological evolution coincides with the development of the field of environmental DNA (eDNA) where genetic material is extracted from environmental samples, rather than individual organisms. While there are some limitations with using molecular cercariometry, notably the cost and its inability to differentiate between life cycle stages, it substantially reduces the labor required to study trematode populations. It also can be used in complement with snail collections to understand the composition of avian schistosomes in an environment. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

Other

Jump to: Research, Review

10 pages, 1395 KiB

Open AccessBrief Report

Invaders as Diluents of the Cercarial Dermatitis Etiological Agent

by Anna Stanicka, Łukasz Migdalski, Katarzyna Szopieray, Anna Cichy, Łukasz Jermacz, Paola Lombardo and Elżbieta Żbikowska

Pathogens 2021, 10(6), 740; https://0-doi-org.brum.beds.ac.uk/10.3390/pathogens10060740 - 11 Jun 2021

Cited by 7 | Viewed by 2087

Abstract

Research on alien and invasive species focuses on the direct effects of invasion on native ecosystems, and the possible positive effects of their presence are most often overlooked. Our aim was to check the suitability of selected alien species (the snail Physa acuta [...] Read more.

Research on alien and invasive species focuses on the direct effects of invasion on native ecosystems, and the possible positive effects of their presence are most often overlooked. Our aim was to check the suitability of selected alien species (the snail Physa acuta, the bivalve Dreissena polymorpha, and the gammarid Dikerogammarus villosus) as diluents for infectious bird schistosome cercariae—the etiological factor of swimmer’s itch. It has been hypothesized that alien species with different feeding habits (scrapers, filterers and predators) that cohabit the aquatic environment with intermediate hosts of the schistosomatid trematodes are capable of feeding on their free-swimming stages—cercariae. In the laboratory conditions used, all experimental animals diluted the cercariae of bird schistosome. The most effective diluents were P. acuta and D. villosus. However, a wide discrepancy in the dilution of the cercariae between replicates was found for gammarids. The obtained results confirm the hypothesis that increased biodiversity, even when alien species are involved, creates the dilution effect of the free-living stages of parasites. Determining the best diluent for bird schistosome cercariae could greatly assist in the development of current bathing areas protection measures against swimmer’s itch. Full article

(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)

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