Helminth Fauna of Bats of the Rostov Region: Review. 4. Acanthocephala. General Conclusions

Evsyukov A.P., Potapenko I.O., Tsygankova M.G.

Introduction. The class Cestoda is divided into two subclasses: the Cestodaria — unsegmented tapeworms, and the Eucestoda — true cestodes. The representatives of the orders Pseudophyllidea and Cyclophyllidae, which are part of the subclass of true cestodes parasitize in carnivorous mammals. At the same time, only representatives of the latter order parasitize in chiropterans. Data on the species composition and distribution of cestodes in the Rostov region have not been published yet. The list of bat species living in the Rostov region have been compiled previously. In this article, the authors study the cestode fauna parasitizing in chiropterans in the region under study. This review aims to analyse the current state of knowledge about the species composition of helminths parasitizing in bats in the Rostov region.Materials and Methods. The research materials have been obtained from the libraries and open access resources: PubMed (pubmed.ncbi.nlm.nih.gov), CyberLeninka (cyberleninka.ru), Google Scholar (scholar.google.com), BHL (www.biodiversitylibrary.org ), JSTOR (www.jstor.org), etc. Some data has been provided by the colleagues. Results. 17 species of cestodes of 4 genera, 1 family and 1 order can be found in 15 species of bats living in the Rostov region. Among them dominate the species of the genus Vampirolepis (11 species).Discussion and Conclusion. The results of the review carried out showed that maximum diversity of cestodes was found in one species of bats — the serotine bat (10 species). The smallest number of cestode species (1 per each) was found in the giant and lesser noctules. None of the cestode species found in bats in the Rostov region were recorded in companion animals or humans. However, some cestode species of the Hymenolepididae family, common in rodents, can infect the humans.

Evsyukov A.P., Tsygankova M.G.

Introduction. The class of Trematoda includes two subclasses — Aspidogastrea and Digenea. Representatives of the former do not parasitize in bats. The definitive hosts for digenetic trematodes (Digenea) are vertebrates, including bats, in which the sexual generation (maritae) parasitizes. Gastropods or bivalves are the intermediate hosts. Supplementary hosts for the trematodes of bats are larvae and imagos of flying insects. Since in most cases the development of parthenites and cercariae of trematodes is related to water environment, the supplementary hosts are the groups of insects whose larvae live in the water. The list of bat species living in the Rostov region has been compiled in the previous research. In the present article the authors investigate the trematode fauna parasitizing in bats of the region under study. The aim of this review is to analyse the current state of knowledge on the species composition of the helminth parasitizing in chiropterans of the Rostov region.Materials and Methods. The research materials have been obtained from the libraries and open access resources: PubMed (pubmed.ncbi.nlm.nih.gov), CyberLeninka (cyberleninka.ru), Google Scholar (scholar.google.com), BHL (www.biodiversitylibrary.org), JSTOR (www.jstor.org). Some data has been provided by the colleagues.Results. 42 trematode species from 10 genera, 5 families and 1 order can parasitize in 15 bat species living in the Rostov region. The Lecithodendriidae family (24 species) and the genus Paralecithodendrium (9 species) are represented by a large number of species. Of the listed trematodes, 33 species used to be recorded on the territory of Russia.Discussion and Conclusion. The results of the conducted systematic review have revealed that the largest number of trematode species parasitizes in two bat species living in the Rostov region: the common noctule (27 species) and the serotine bat (24 species). The smallest number of species (4 per each) is found in the giant noctule and the soprano pipistrelle bat. Two species (Plagiorchis elegans and Plagiorchis vespertilionis) have been found in the companion cats and dogs includingly, wheras a case of the latter parazitising in humans has also been recorded. The presence of bats in the urban environment enables the full life cycle of these trematodes. There exists possibility of the companion animals and people to get infected through incidental ingestion of the infested insects.

Kirillova N.Y., Kirillov A.A., Vekhnik V.A.

Various bat species often occupy the same habitats. Cohabitation should induce different preferences in spatial or trophic components of the bat ecological niche to reduce their competition. This determines the differences in the trematode fauna of Myotis spp. The purpose of our research was to study the biodiversity of trematodes in syntopic populations of five Myotis species in the Samarskaya Luka National Park. In the 2005–2007 period, we studied 867 bat specimens via the methods of complete helminthological dissection. In total, 11 trematode species from the families Plagiorchiidae (Plagiorchis koreanus, P. mordovii, P. muelleri, and P. vespertilionis), Pleurogenidae (Parabascus duboisi), and Lecithodendriidae (Prosthodendrium ascidia, Pr. chilostomum, Pr. cryptolecithum, Pr. hurkovaae, Pr. longiforme, and Lecithodendrium linstowi) were found in five Myotis species. Only three trematode species, P. koreanus, Pr. chilostomum, and P. duboisi, are common to all studied Myotis spp. Prosthodendrium cryptolecithum was recorded for the first time in Russia. Trematode species diversity is higher in Myotis daubentonii and M. dasycneme. The trematode fauna of M. brandtii, M. nattereri, and M. mystacinus is less diverse. The determining factor in the infection of bats with trematodes is feeding on semi-aquatic insects, possible second intermediate hosts of the parasites. The infection of bats with flukes occurs at different levels of host (Myotis spp.) abundance as a result of the realization of the main bat trophic relationships. Our results confirm the data that the ecological niches of the five Myotis species partially overlap. Analysis of the trematode fauna in Myotis spp. showed that, in the Samarskaya Luka, there may be weak competition for food items among bats.

Evsyukov A.P., Tsygankova M.G.

Introduction. Bats (Chiroptera) are the least studied group of mammals in many regions of Russia. At the same time, the chiropterans are known to be one of the largest orders of Mammalia, which can act as hosts and carriers of various pathogenic fungi, bacteria and viruses. However, the parasitic fauna of this group of animals is poorly investigated. The study of bat-parasitizing worms has great practical importance, since bats, due to their ancient origin, are a very detached order. Endoparasites, including the chiropteran helminths, have not been previously studied in the Rostov region. According to the available data, the up-to-date research on the bat parasites in Russia has been carried out only in the Saratov region and in the Republic of Mordovia. The aim of this series of articles is to study the helminth species composition parasitizing in chiropterans in the Rostov region. In the first report we present the data on nematodes.Materials and Methods. The materials for the research were the articles from the open access literature databases: PubMed (pubmed.ncbi.nlm.nih.gov), Cyberleninka (cyberleninka.ru), GoogleScholar (https://scholar.google.com ), etc. The main method used was the analysis of the collected data.Results. The authors were the first to reveal that 27 nematode species from 14 genera, 8 families, 4 orders and 2 classes can be found in 15 bat species living in the Rostov region. The numerous Chromadorea class is represented by 21 species, 12 of which are found in Russia.Discussion and Conclusion. The results of the literature sources analysis showed that the largest number of nematode species parasitize in two chiropteran species living in the Rostov region: in the Daubenton's bat (15 species) and in the common noctule (14 species). Only one species has been recorded in the northern bat. Most nematode species parasitize specifically in bats and have a direct life cycle. (e.g., species of the genus Molinostrongylus). For some species, such as Pterygodermatites bovieri and Litomosa spp., the intermediate hosts are arthropods and the definitive hosts are various bat species. For three nematode species: Ascarops strongylina, Physocephalus sexalatus and Spirocerca lupi, bats are the paratenic hosts.

Kirillova N.Y., Kirillov A.A., Vekhnik V.A., Shchenkov S.V., Fayzulin A.I., Ruchin A.B.

In this study, we present our dataset containing up-to-date information about occurrences of trematodes in small mammals in the Middle Volga region (European Russia). The dataset summarizes micromammals’ trematode occurrences obtained by long-term field helminthological studies of soricomorphs, erinaceomorphs, bats and rodents during a period of more than 20 years (1999–2022). Our studies of trematodes in micromammals were conducted using the method of complete helminthological necropsy. The dataset includes 7470 records of trematode occurrences in micromammals with 4483 digenean records in Samara Oblast, 2986 records in Republic of Mordovia and one trematode record in Ulyanovsk Oblast. Our dataset presents the data on 43 trematode species from 21 genera and 9 families found in the region studied. The data on trematodes from 28 species of micromammals belonging to 14 genera are presented. In total, the number of collected trematode specimens in our dataset is 153,050. Each occurrence record contains the trematode species name, basis of record, locality of finding, host species, site in host, date and authors of the record and species identification. All occurrence records are georeferenced. The dataset is based on the research of the staff of the Institute of Ecology of the Volga River basin of RAS and the Joint Directorate of the Mordovia Nature Reserve and National Park “Smolny”. The distribution and diversity of trematodes of small mammals in the Middle Volga region has not been completely studied, and further investigation may reveal both new occurrences of trematodes and new host records.

HODDA M.

A classification of the entire Phylum Nematoda is presented, based on current molecular, developmental and morphological evidence. The classification reflects the evolutionary relationships within the phylum, as well as significant areas of uncertainty, particularly related to the early evolution of nematodes.   It includes 3 classes, 8 subclasses, 12 superorders, 32 orders, 53 suborders, 101 superfamilies, 276 families, 511 subfamilies, 3030 genera, and 28537 species.   All valid species named from the time of publication of the previous classification and census (2010) to the end of 2019 are listed, along with the number of valid species in each genus.   Taxonomic authorities are provided for taxon names of all ranks.   The habitats where the species in each genus are found are listed, and an alphabetic index of genus names is provided.   The systematics of nematodes is reviewed, along with a history of nematode classification; evolutionary affinities and origins of nematodes; and the current diagnosis of the group.   Short overviews of the general biology, ecology, scientific and economic importance of the group are presented.  

Mathison B.A., Sapp S.G.

The classification of “parasites” in the medical field is a challenging notion, a group which historically has included all eukaryotes exclusive of fungi that invade and derive resources from the human host. Since antiquity, humans have been identifying and documenting parasitic infections, and this collective catalog of parasitic agents has expanded considerably with technology. As our understanding of species boundaries and the use of molecular tools has evolved, so has our concept of the taxonomy of human parasites. Consequently, new species have been recognized while others have been relegated to synonyms. On the other hand, the decline of expertise in classical parasitology and limited curricula have led to a loss of awareness of many rarely encountered species. Here, we provide a comprehensive checklist of all reported eukaryotic organisms (excluding fungi and allied taxa) parasitizing humans resulting in 274 genus-group taxa and 848 species-group taxa. For each species, or genus where indicated, a concise summary of geographic distribution, natural hosts, route of transmission and site within human host, and vectored pathogens are presented. Ubiquitous, human-adapted species as well as very rare, incidental zoonotic organisms are discussed in this annotated checklist. We also provide a list of 79 excluded genera and species that have been previously reported as human parasites but are not believed to be true human parasites or represent misidentifications or taxonomic changes.

Majewska A.A., Huang T., Han B., Drake J.M.

Helminths are parasites that cause disease at considerable cost to public health and present a risk for emergence as novel human infections. Although recent research has elucidated characteristics conferring a propensity to emergence in other parasite groups (e.g. viruses), the understanding of factors associated with zoonotic potential in helminths remains poor. We applied an investigator-directed learning algorithm to a global dataset of mammal helminth traits to identify factors contributing to spillover of helminths from wild animal hosts into humans. We characterized parasite traits that distinguish between zoonotic and non-zoonotic species with 91% accuracy. Results suggest that helminth traits relating to transmission (e.g. definitive and intermediate hosts) and geography (e.g. distribution) are more important to discriminating zoonotic from non-zoonotic species than morphological or epidemiological traits. Whether or not a helminth causes infection in companion animals (cats and dogs) is the most important predictor of propensity to cause human infection. Finally, we identified helminth species with high modelled propensity to cause zoonosis (over 70%) that have not previously been considered to be of risk. This work highlights the importance of prioritizing studies on the transmission of helminths that infect pets and points to the risks incurred by close associations with these animals. This article is part of the theme issue ‘Infectious disease macroecology: parasite diversity and dynamics across the globe’.

MONKS S.

Of 32 papers including Acanthocephala that were published in Zootaxa from 2001 to 2020, 5, by 11 authors from 5 countries, described 5 new species and redescribed 1 known species and 27 checklists from 11 countries and/geographical regions by 72 authors.  A bibliographic analysis of these papers, the number of species reported in the checklists, and a list of new species are presented in this paper. 

Guerreiro Martins N.B., del Rosario Robles M., Navone G.T.

The majority of species of Acanthocephala known thus far from South America have been recorded mostly in fish and wild birds. In particular, rodents in Argentina have been poorly studied for acanthocephalans. The genus Abrothrix (Sigmodontinae-Cricetidae) ranges from the Altiplano of southern Peru through the highlands of Bolivia, northern Chile, and Argentina south through Tierra del Fuego. The purpose of this paper was to study Acanthocephala species parasitizing different populations of Abrothrix from Santa Cruz province (Patagonia Argentina). Specimens of Acanthocephala were found in the small intestine of Abrothrix olivaceus, showing values of P 14.7%, IM = 2.8, and AM = 0.41. All the rodents parasitized were collected in Punta Quilla, Santa Cruz, Argentina. The specimens of Abrothrix longipilis were not parasitized. Moniliformis amini n. sp. is described with features such as the long, cylindrical, and pseudo-segmented body; proboscis receptacle double walled, outer wall with muscle fibers usually arranged spirally, and a combination of several morphometric characters, mainly the very small size of the proboscis receptacle and length of the testes and lemnisci. A marked proportion of arthropods was found in the diet of A. olivaceus, characterizing it as arthropodivorous. Possibly, a larger sampling effort and specific projects dealing with the study of acanthocephalans will shed light on several questions of the rodent-Moniliformis relationship.

Kirillova N.Y., Kirillov A.A.

Smales L.

Tinnin D.S., Ganzorig S., Gardner S.L.

PERKINS S., FENTON A.

Pathogens frequently use vectors to facilitate transmission between hosts and, for vertebrate hosts, the vectors are typically ectoparasitic arthropods. However, other parasites that are intimately associated with their hosts may also be ideal candidate vectors; namely the parasitic helminths. Here, we present empirical evidence that helminth vectoring of pathogens occurs in a range of vertebrate systems by a variety of helminth taxa. Using a novel theoretical framework we explore the dynamics of helminth vectoring and determine which host-helminth-pathogen characteristics may favour the evolution of helminth vectoring. We use two theoretical models: the first is a population dynamic model amalgamated from standard macro- and microparasite models, which serves as a framework for investigation of within-host interactions between co-infecting pathogens and helminths. The second is an evolutionary model, which we use to predict the ecological conditions under which we would expect helminth vectoring to evolve. We show that, like arthropod vectors, helminth vectors increase pathogen fitness. However, unlike arthropod vectors, helminth vectoring increases the pathogenic impact on the host and may allow the evolution of high pathogen virulence. We show that concomitant infection of a host with a helminth and pathogen are not necessarily independent of one another, due to helminth vectoring of microparasites, with profound consequences for pathogen persistence and the impact of disease on the host population.