Strigea robusta causes polydactyly and severe forms of Rostand’s anomaly P in water frogs

Abstract

Background: Cases of polydactyly in natural populations of amphibians have attracted great interest from biologists. At the end of the 1940s, the French biologist Jean Rostand discovered a polymorphic syndrome in some water frog (Anura: Pelophylax) populations that included polydactyly and some severe morphological anomalies (he called it 'anomaly P'). The cause of this anomaly remains unknown for 70 years. In a previous study, we obtained anomaly P in the laboratory in tadpoles of water frogs that developed together with molluscs Planorbarius corneus (Mollusca: Gastropoda) collected in the field. We thus proposed the 'trematode hypothesis' , according to which the infectious agent responsible for anomaly P is a trematode species. Methods: Metacercariae from tadpoles with anomaly P were identified using ITS2 gene sequencing as Strigea robusta (Trematoda: Strigeidae). To verify teratogenic features of the species, cercariae of S. robusta were tested for the possibility to cause anomalies. Identification of cercariae species was made using morphological and molecular methods (sequencing of ITS2 and 28S rRNA). The tadpoles were exposed to parasites at four doses of cercariae (control, low, medium and high) and divided into two groups: "early" (at 25-27 Gosner stages) and "late" (at 29-34 Gosner stages) exposure. Results: A total of 58 (72.5%) tadpoles survived until metamorphosis under the dose-dependent experiment with the trematode S. robusta. Differences in the survival rates were observed between the exposed and unexposed tadpoles both in the group of "early" tadpoles and "late" tadpoles. The exposure of tadpoles to the cercariae of S. robusta induced anomaly P in 82% of surviving tadpoles. The severe forms developed only in "early" stages under all doses of cercariae exposure. Polydactyly predominantly developed in the "late" stages; under a light exposure dose, polydactyly also developed in "early" tadpoles. Laboratory-hatched tadpoles reared together with infected snails had different rates of survival and complexity of deformations associated with the period of coexistence. Conclusions: The experiments with direct cercariae exposure provide compelling evidence that S. robusta leads to anomaly P in tadpoles of water frogs. The manifestation of anomaly P turned out to be dependent on the stage of development, cercariae dose, and the location of the cysts.

Helminth communities in amphibians from Latvia, with an emphasis on their connection to host ecology

“…In amphibians, disease or infection is usually accompanied by emaciation and weight loss (Bancila et al, 2010). Diplostomid trematode (A. alata, S. strigis) larvae and gastrointestinal nematode infections were better correlated with host length than with weight, probably due to their adverse effect on host body condition (Hendrikx & Van Moppes, 1983;Svinin et al, 2020) and accompanying weight loss that increased data dispersion. A similar pattern was also observed in trematode species richness.…”

High prevalence of anomalies in Nyctimantis brunoi (Anura: Hylidae) from a restinga protected area in southeastern Brazil

“…In addition to the potential causes aforementioned, UV-B radiation, viral infections, infection caused by the trematodes Ribeiroia ondatrae (Price, 1931) Price, 1942, Acanthostomum burminis (Bhalerao, 1926) Bhalerao, 1936, and Strigea robusta (Szidat, 1928, and parasitic copepod invasion [Lernaea cyprinacea (Linnaeus, 1758)] are also associated with developing of limb malformations in amphibians (Stocum 2000, Blaustein and Johnson 2003, Johnson et al 2004, Burton et al 2008, Rajakaruna et al 2008, Kupferberg et al 2009, Svinin et al 2020.…”

An overview of helminths of the European fire-bellied toad Bombina bombina (Amphi-bia, Anura) in the Volga River Basin

“…Among other dangers for amphibians, we should note the emergence of a new type of threat in the XXI century such as infectious diseases caused by parasites -fungi (Narayan et al, 2011;Meurling, 2019;Sewell et al, 2021) and helminths (Jayawardena et al, 2013). The pathogenic effect of helminthic infection in amphibians has a wide range of manifesttations: from a number of skeletal anomalies (Schotthoefer et al, 2003;Szuroczki et al, 2011) and limb malformations (Svinin et al, 2020a(Svinin et al, , 2020b till the dysfunction of internal organs (Vedernikov et al, 2020), suppression of behavioral reactions, life instincts and death (Ivanov et al, 2012). Unfortunately, amphibian helminths are not given due attention nowadays, despite the fact that the relevance of research in this direction is obvious.…”