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All issues Volume 27 (2020) Parasite, 27 (2020) 61 Full HTML
Open Access
Review
Issue
Parasite
Volume 27, 2020
Article Number 61
Number of page(s) 42
DOI https://doi.org/10.1051/parasite/2020051
Published online 17 November 2020

© C. Léger, published by EDP Sciences, 2020

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Introduction

Bats (Mammalia: Chiroptera) represent the second-most diverse order of mammals, after rodents. As of 2007, 42 bat species have been reported from Europe (Dietz et al. [84]). According to Arthur & Lemaire [16], 35 species have been unambiguously identified in France. Many aspects of the ecology of bats are under study (e.g. swarming, hunting sites, flight routes, habitat studies, acoustic ecology). One of these aspects is the study of bat parasites, which has a long history in Europe, for instance in French-speaking areas (France, Belgium). Bats are infected with a large diversity of parasites. Around the year 1999, c. 756 taxa were known to be associated with bats worldwide [167]. In Lanza’s book, a wide range of parasitic organisms were presented, belonging to 13 groups: Myconta (two taxa), Acanthocephala (three taxa), Mallophaga (one taxon, accidental exposure), Anoplura (two taxa), Heteroptera (11 taxa), Neobacteria (c. 31 taxa), Protozoa (25 taxa), Cestoda (55 taxa), Digenea (105 taxa), Nematoda (62 taxa), Acari (324 taxa), Diptera (65 taxa) and Siphonaptera (64 taxa). This includes at least ten phyla: Acanthocephala (Spiny-headed worms), Apicomplexa, Arthropoda, Ascomycota (Ascomycete fungi), Euglenozoa, Firmicutes, Nematoda, Platyhelminthes, Protobacteria and Spirochaetes. Similar findings were noted by Stiles & Nolan [235] in their “key catalogue” of bat parasites. In addition to the high diversity of bat parasites, these findings point out the predominant share, in the published records, of metazoan parasites. They also point out the issue of diseases in bats and the issue of bat parasites as disease vectors for their hosts. Indeed, we know that bats are hosts to a large range of infections (transmission linked with their ecology) and they seemingly are able to control these infections so that they are mostly asymptomatic. Some bat parasites (e.g. bat flies) are known to be disease vectors for their hosts [83, 129, 181, 184, 192, 261].

Among the earliest works on bat parasites in France is Étienne-Louis Geoffroy’s Histoire abrégée des insectes [123], published in 1762 (Fig. 1). This book marks the starting point for research on bat parasites in France. The present paper reviews metazoan parasites reported on bats in France between 1762 and 2018, with the exception of acanthocephalans. According to the Host-Parasite Database of the Natural History Museum, London [125], no bat parasites belonging to the Acanthocephala phylum are currently known in France. In addition, hyperparasites are excluded from this paper. Nevertheless, it should be noted that bat parasites have their own parasites, such as Laboulbeniales fungi associated with bat flies or viruses of haemosporidian parasites. Some of these hyperparasites have reports from France, specifically in the department of Gard (Arthrorhynchus eucampsipodae Thaxt., 1901 and A. nycteribiae (Peyr.) Thaxt., 1931) [55, 129, 238]. The purpose of the present paper is twofold: the primary aim is to summarize the large body of published field data; and secondly to inform the reader about the geographical origin of the data and to contribute to a general overview and checklist of bat-parasite associations in France.

thumbnail Figure 1

Number of studies (n = 237) that include bat parasites observed in France since 1760, by decade.

Methods

Initially, I used the works of nine authors: Anciaux de Faveaux [5–7], Beaucournu [28, 29], Beaucournu and Launay [37], Hůrka [149], Lanza [167], Maa [185] and Szentiványi et al. [237]. The list of all the sources used in these papers offers an essential bibliographical guide. The online catalog of the Library of the Muséum National d’Histoire Naturelle (MNHN) was also used. I checked all available publications on each of the searched terms including a combination of France or the name of administrative departments (n = 111) or the names of former administrative regions of France (n = 22) with one of the generic names of the bat parasites, as mentioned in I parassiti dei pipistrelli (Mammalia, Chiroptera) della fauna italiana [167], Parasite diversity of European Myotis species with special emphasis on Myotis myotis (Microchiroptera, Vespertilionidae) from a typical nursery roost [121], Les puces de France et du basin méditerranéen occidental [37], and Checklist of host associations of European bat flies (Diptera: Nycteribiidae, Streblidae) [237]. For the study area, see Figure 5. I searched Google Scholar, ISI Web of Science, Hyper-Article en Ligne (HAL), Biodiversity Heritage Library (BHL), Gallica, and Archives. The collated sources (n = 237) were then analysed. I then proceeded to index them in terms of their chronology, taxonomy, and geography. The validity of all the taxa found was checked using the comprehensive synonymies provided by the Host-Parasite Database of the Natural History Museum, London [125] and the Inventaire National du Patrimoine Naturel of the Muséum National d’Histoire Naturelle (MNHN) [153]. The taxonomic works of Fain [106–108], Lanza [167], Neumann [197], Da Fonseca [72], Radovsky [212], Roy and Chauve [221, 222], Rudnick [223], Stiles and Nolan [235] and Theodor & Moscona [241] were also used. The bat classification and taxonomy, in this paper, is based on Dietz et al. (2009) and Arthur and Lemaire (2015). Authorities for the host taxa and parasites species are given in Tables 1 and 2. The map in Figure 5 was created using Carto-SI (https://www.carto-si.com/).

Results and discussion

Based on published data, eight groups of bat parasites reported from France have been identified (Fig. 2). The majority of the analysed papers (94%) were published between 1762 and 1999 (Fig. 1). All host-parasite associations are listed in Tables 1 and 2. What follows is an overview of all bat parasites, arranged by higher taxonomic group.

thumbnail Figure 2

Overview of the 113 generally recognised parasite taxa that are mentioned in the analysed papers (n = 237) per host taxonomic group. Invalid species (n = 22 Acari and 3 Diptera) recorded in the literature, records reported from France without identification to species level (n = 6 Acari; 1 Cestoda; 2 Diptera; 1 Hemiptera; 2 Nematoda and 2 Trematoda) and species only noted as absent (n = 3 Acari and 1 Diptera) are not included here.

1 Phylum Arthropoda Latreille, 1829

1.1 Subphylum Chelicerata Heymons, 1901

1.1.1 Subclass Acari Leach, 1817

Most of the studied papers (n = 112) deal with 75 species (53 generally recognised species and 22 invalid species) of Acari of four groups: Ixodida, Mesostigmata, Trombidiformes (suborder Prostigmata), and Sarcoptiformes (Fig. 3). A total of 53 recognised species (including two subspecies) of mites and ticks were reported to be parasites of bats in France prior to 2018. Of these, two species have only been collected from the border between Switzerland and the French department of Haute-Savoie (Col de Bretolet): Spinturnix helvetiae and S. acuminatus.

thumbnail Figure 3

Number of recognised species of Acari (n = 53), per host order (n = 4) and genus (n = 23). Invalid species (n = 22 Acari) recorded in the literature (n = 237 papers) and species only noted as absent (n = 3 Acari) are not included here.

These recognised species found in the literature (n = 53) reported from France belong to 23 genera: Acanthophthirius, Alabidocarpus, Argas, Calcarmyobia, Eyndhovenia, Hirstionyssus, Ichoronyssus, Ixodes, Labidocarpus, Leptotrombidium, Macronyssus, Neomyobia, Neotrombicula, Notoedres, Nycteridocoptes, Oudemansidium, Paraperiglischrus, Pteracarus, Psorergates, Riedlinia, Sasatrombicula, Steatonyssus and Spinturnix. Among this group, the most diverse genera reported in France are Spinturnix and Macronyssus (Fig. 3): these genera account for 30% of all documented Acari infections involving valid species.

Six more records reported from France without identification to species level were found. These comprise Dermanyssus sp. [86], Ichoronyssus sp. [25], Ixodes sp. [178], Neomyobia sp. [126], Steatonyssus sp. [152, 212] and Spinturnix sp. [133]. Three other species are noted as absent from bats in western France, namely Ixodes canisuga, I. ricinus, and Pholeoixodes hexagonus [28]. Finally, 22 invalid taxa reported from France were found in the analysed papers. Examples for this category are Dermanyssus murinus (Lucas, 1840) [101, 104, 167, 183, 195], D. vespertilionis Dugès, 1834 [94], Pteroptus vespertilionis, and Spinturnix vespertilionis (C.L. Koch)] [70].

Table 1

List of bat species and their associated metazoan parasites in France (including Corsica), based on the published literature. Authors are listed in the bibliography. See also the work titled Les parasites métazoaires des Chiroptères de France (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) : contribution à un état des lieux bibliographique (1762–2018) et à l’établissement d’une liste nationale (2019). Invalid species are listed in brackets. Records marked with an exclamation mark (!) are invalid. Records marked with a question mark (?) are dubious. They may require further clarification.

A large host group comprising the following taxa was identified with Acari infections: Barbastella barbastellus, Eptesicus serotinus, Eptesicus sp., Hypsugo savii, Miniopterus schreibersii, Myotis bechsteinii, M. blythii, M. blythii oxygnathus, M. capaccinii, M. dasycneme, M. daubentonii, M. emarginatus, M. myotis, M. mystacinus, M. nattereri, M. punicus, Myotis sp., Nyctalus lasiopterus, N. leisleri, N. noctula, Pipistrellus kuhlii, P. nathusii, P. pipistrellus, Pipistrellus sp., Plecotus auritus, P. austriacus, Rhinolophus euryale, R. ferrumequinum, R. hipposideros and Rhinolophus sp. (see Tables 1 and 2). The oldest works dealing with Acari parasitising bats in France are Geoffroy’s Histoire abrégée des insectes [123] and Latreille’s Précis des caractères génériques des insectes, disposés dans un ordre naturel [168], dated 1762 and 1797. Geoffroy mentioned the tick (found on an unidentified bat) as Acarus fuscus ovatus, pedibulus pallidis, vespertilionis, a taxon treated as Caris vespertilionis by Lamarck in the Histoire naturelle des animaux sans vertèbres (1839). The book of Latreille contains an observation of Carios on “la Chauve-Souris noctule” (=Nyctalus noctula or Nyctalus sp.). This taxon is very likely Argas (Carios) vespertilionis (Latreille, 1802). Descriptions of some species and subspecies are based on type material from France (e.g. Spinturnix nobleti [81], S. bechsteini [82], Pteracarus pipistrellius maximis [251], Myobia poppei (= Acanthophthirius (Acanthophthirius) poppei) [249] and Spinturnix andegavinus [76]). The majority of published data on parasites of chiropteran populations in France deal with Arachnida and similar findings were noted by Lanza [167], Krištofík & Danko [165] and Frank et al. [121] in Italy, Slovakia and other European countries.

Table 2

List of bat parasites (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) and their hosts in France (including Corsica), based on the published literature, with reported synonyms. Authors are listed in the bibliography. See also the work entitled Les parasites métazoaires des Chiroptères de France (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) : contribution à un état des lieux bibliographique (1762-2018) et à l’établissement d’une liste nationale (2019). Invalid species are listed in brackets. Records marked with an exclamation mark (!) are invalid. Records marked with a question mark (?) are dubious. They may require further clarification.

1.2 Subphylum Hexapoda Latreille, 1825

1.2.1 Suborder Anoplura Leach, 1815 (order Phthiraptera Haeckel, 1896)

Only one species has been reported as a bat parasite in France, i.e. Polyplax serrata. The scientist Paul Rémy (1894–1962) published in 1948 the only record; this was from R. hipposideros (Borkhausen, 1797) in north-eastern France at Trémont-sur-Saulx (Meuse area [177, 216]). The mentioned locality in the original paper, “Frémont-sur-Saulx” [216], contains a typographical error. These field data, dated 1925–1926, and published in the journal La Feuille des Naturalistes, are surprising and dubious [Beaucournu, in litt.]. In fact, this species is more likely to be an ectoparasite of mammals of the Rodentia order (e.g. Apodemus, Clethrionomys and Mus genera) and Eulipotyphla (Crocidura leucodon) [98, 234]. It should be noted, however, that Polyplax sp. was also reported on Rhinolophus mehelyi by Gadžiev et al. in 1990 in Eastern Europe. These are the only data on Polyplax sp. in Lanza’s analysis [167] and hence they may be unreliable. Rémy’s observation is not mentioned in the works of Durden & Musser [98], Ferris [119] and Hopkins [140].

1.2.2 Order Diptera Linnaeus, 1758

According to Szentiványi et al., 17 species of bat flies are currently known in Europe [237]. Thirteen species of bat flies have been reported from France and two more records without identification to species level have been found. These are Basilia (Basilia) italica, B. (Basilia) mediterranea, B. (Basilia) nana, 1954, B. (Basilia) nattereri, Brachytarsina flavipennis, Nycteribia (Achrocholidia) vexata, N. (Nycteribia) kolenatii, N. (Nycteribia) latreillii, N. (Nycteribia) pedicularia, N. (Nycteribia) schmidlii, Penicillidia (Neopenicillidia) conspicua, P. (Penicillidia) dufourii, Phthiridium biarticulatum, Nycteribia sp. and Nycteribia kolenatii/latreillii/pedicularia [1, 4, 12, 22–30, 34, 35, 38–41, 43, 45, 47, 53, 73, 74, 86, 91, 93, 115–117, 126, 135, 146–152, 154, 156, 167, 170, 172, 173, 175, 177, 179, 186, 187, 200, 203, 204, 206, 214, 215, 237, 240–242, 247, 248, 260]. Three invalid taxa reported from France were found in the analysed papers: Nycteribia eparticulata, N. vespertilionis Meig., and N. vespertilionis Latreille. Penicillidia (Penicillidia) monoceros is noted as absent in western France [28]. Another species, B. (Basilia) daganiae could be distributed in France [28, 34]. As far as hosts of the bat flies (Diptera: Nycteribiidae and Streblidae) are concerned, E. serotinus, H. savii, M. schreibersii, M. bechsteinii, M. blythii, M. capaccinii, M. daubentonii, M. emarginatus, M. myotis, M. mystacinus, M. nattereri, M. species, P. pipistrellus, Pipistrellus sp., P. auritus, R. euryale, R. ferrumequinum, R. hipposideros, and R. mehelyi have been recorded in the literature. Jean-Frédéric Hermann’s record of Phthiridium vespertilionis, dated 1804, is the oldest French record of a dipteran as a bat parasite [135]. The bibliographical survey of the published data (n = 111 papers) written by Szentiványi et al. has shown that ten bat fly species are known to be associated with bats in Albania, Romania, and Italy [237]. Europe’s most species-rich communities have been reported in Spain (11 species), Switzerland (11 species), Hungary (11 species) and France (13 species). As such, France has the most diverse community reported in the literature.

1.2.3 Order Hemiptera Linnaeus, 1758

The literature provides well-documented cases for Cimex dissimilis, C. lectularius, and C. pipistrelli on M. myotis, M. emarginatus, R. euryale, and R. ferrumequinum [28, 167, 177, 207, 236, 253, 254]. In addition to these species, records reported from France without identification to species level have been found (Cimex sp. on M. myotis, M. emarginatus, R. euryale, and R. ferrumequinum) [28, 177]. The first published data in the analysed literature are dated 1961 [28] when Beaucournu published his observations on Cimex sp. in the department of Maine-et-Loire. True bugs (Hemiptera: Cimicidae) using bats as hosts have not been well studied in France. Studies on bat guano deposits could provide data on the species distribution. For instance, this method provided new records of Cimex sp. and Cimex dissimilis (Horváth, 1910) in a roosting colony of M. myotis in June 2017 and June 2018 in north-eastern France [177] (about C. dissimilis in roosting colony of M. myotis, see also [121] and [224]).

1.2.4 Order Siphonaptera Latreille, 1825

Twelve species are known to be associated with bats in France. They belong to the family Ischnopsyllidae Wahlgren, 1907. The species are Araeopsylla gestroi, Ischnopsyllus (Hexactenopsylla) hexactenus, I. (Ischnopsyllus) elongatus, I. (Ischnopsyllus) intermedius, I. (Ischnopsyllus) octactenus, I. (Ischnopsyllus) simplex, I. (Ischnopsyllus) variabilis, Nycteridopsylla ancyluris ancyluris, N. eusarca, N. longiceps, N. pentactena, and Rhinolophopsylla unipectinata unipectinata. According to Beaucournu and Launay [37], the published records of Nycteridopsylla dictena are dubious [146, 227]. Bat fleas have been observed on 20 hosts in France [3, 14, 23, 29, 33, 36–38, 42–44, 46, 85, 86, 90, 95, 141, 142, 152, 156, 157, 167, 177, 200, 204, 219, 227, 228, 231, 242, 257]. These hosts are E. serotinus, M. schreibersii, M. blythii, M. capaccinii, M. daubentonii, M. emarginatus, M. myotis, M. mystacinus, M. nattereri, Myotis sp., N. leisleri, N. noctula, P. kuhlii, P. nathusii, P. pipistrellus, P. auritus, P. austriacus, R. euryale, R. ferrumequinum, R. hipposideros, Rhinolophus sp., and Tadarida teniotis. Studies on bat fleas have a long history in France and the book of Walckenaer on insects, entitled Faune parisienne, insectes ou Histoire abrégée des insectes des environs de Paris [257], may be among the earliest such works. According to the Inventaire National du Patrimoine Naturel, 91 autochthonous (indigenous) species of the Siphonaptera order have been reported in France. Species of the Ischnopsyllidae found in France represent almost 13% of fleas in the country [153].

2 Phylum Nematoda Diesing, 1861

In France, the helminth fauna of bats is varied, with more than 30 species. Nematodes recorded in bats in France are divided into three orders: Muspiceida Bain & Chabaud, 1959, Rhabditida Chitwood, 1933, and Strongylida Molin, 1861; and six families: Onchocercidae Leiper, 1911 (three species), Molineidae Skrjabin & Schulz, 1937 (four species), Rictulariidae Railliet, 1916 (one species), Muspiceidae Bain & Chabaud, 1959 (two species), Seuratidae Hall, 1916 (one species), and Strongylacanthidae (Yorke & Maplestone, 1926, subfamily) Chabaud, 1960 (one species). Thirteen species and two nematodes identified to genus-level have been reported: Litomosa dogieli, L. filaria, L. ottavianii, Molinostrongylus alatus, M. ornatus, M. panousei, M. tipula, Pterygodermatites (Neopaucipectines) bovieri, Riouxgolvania nyctali, R. rhinolophi, Seuratum mucronatum, Strongylacantha glycirrhyza, Rictularia sp., Riouxgolvania sp., and Trichosomum speciosum. These parasites were documented in the following bat species: M. schreibersii, M. blythii, M. emarginatus, M. myotis, Plecotus sp., Rhinolophus sp. and three species of the genus Rhinolophus (R. euryale, R. ferrumequinum, and R. hipposideros) [19–21, 54, 56, 57, 68, 75, 86, 97, 99, 167, 177, 194, 200, 211, 233, 235, 243, 245]. The original description of the rare nematode P. (Neopaucipectines) bovieri is based on material from M. myotis in France. To my knowledge, it is the first published observation in the country (dated September 1885) [56, 66, 230]. The original descriptions of Riouxgolvania nyctali and R. rhinolophi are based on material from M. blythii and R. euryale in the Netherlands and the French departments of Ariège and Pyrénées-Orientales [20, 21]. A re-description of Seuratum mucronatum was based on material from Plecotus auritus (dated 1950) in the French department of Indre-et-Loire [54]. As a comparison, according to Horvat et al. [144, 145], two Nematode species (associated with M. myotis and R. ferrumequinum) are known in Serbia to be associated with bats, whilst in Croatia, these authors noted three species.

3 Phylum Platyhelminthes Minot, 1876

3.1 Class Trematoda

Records of 15 recognised species of trematodes from bats have been found from over 17 published papers. They belong to the order Plagiorchiida La Rue, 1957 and are divided into three families: Lecithodendriidae Lühe, 1901 (13 species), Mesotretidae Poche, 1926 (one species), and Plagiorchiidae Lühe, 1901 (one species). These species are Allassogonoporus amphoraeformis, Lecithodendrium granulosum, L. linstowi, L. moedlingeri, Mesotretes peregrinus, Parabascus duboisi, P. lepidotus, P. semisquamosus, Plagiorchis vespertilionis, Prosthodendrium (Prosthodendrium) carolinum, P. (Prosthodendrium) hurkovaae, P. (Prosthodendrium) chilostomum, P. (Prosthodendrium) longiforme, P. parvouterus, and Pycnoporus heteroporus [1, 57, 60, 61, 68, 71, 86–89, 97, 163, 167, 177, 188, 200, 202, 243]. Two trematodes identified to genus-level have been reported (Lecithodendrium sp. and Prosthodendrium sp.) [86]. These parasites were documented in the following bat species: Eptesicus serotinus [68, 88, 167], Miniopterus schreibersii [68, 167, 188, 200, 235], Myotis daubentonii [89, 167], M. capaccinii [68, 167], M. emarginatus [68, 86, 167], M. myotis [57, 61, 68, 167], Pipistrellus kuhlii [86], P. pipistrellus [57, 60, 61, 68, 86, 97, 163, 167, 235], Plecotus auritus [86, 167], P. austriacus [68, 167], Rhinolophus euryale [68, 167], R. ferrumequinum [68, 86–88, 167, 188, 200, 243], and R. hipposideros [68, 86, 167, 188, 200, 235].

As a comparison, in the United Kingdom, Lord et al. [181, 182] noted four trematode species and one trematode identified to genus-level in bats. In Serbia, Horvat et al. [144, 145] noted a total of seven trematode taxa associated with bats, and only one species in Croatia. According to the Inventaire National du Patrimoine Naturel, 28 species of the family Lecithodendriidae and 27 species of the family Plagiorchiidae have been reported in France. Species of the Lecithodendriidae found in bats represent almost 46% of the family [153]. The observations on Mesotretes peregrinus (Braun, 1900), published by Combes & Clerc, Dubois and Matskási [68, 88, 188], are of particular interest since this is the only species of the family Mesotretidae reported in Europe [125, 153]. As regards Plagiorchis vespertilionis (O.F. Müller, 1784) [68, 86–89, 200, 235], it is worth noting that this species is the only member of the family Plagiorchiidae reported from bats in France. According to Lanza [167], 18 taxa of the Plagiorchiidae family have been reported worldwide. The Histoire naturelle des helminthes ou vers intestinaux (1845) by Félix Dujardin (1801–1860) appears to be the earliest French source mentioning bat-associated trematodes [93]. The first documented reports from France, P. (Prosthodendrium) chilostomum and P. heteroporus, were published in the Notices helminthologiques (deuxième série) by Raphaël Blanchard (1857–1919) [57].

3.2 Class Cestoda

Three recognised and one innominate species of cestodes have been reported in bats in France, which makes it the richest community reported in Europe. These species are Milina grisea, Vampirolepis acuta, and V. balsacii [68, 86, 158, 159, 167, 177, 180, 196, 200, 243, 255, 262]. They belong to one family: Hymenolepididae Ariola, 1899 (Cyclophyllidea van Beneden in Braun, 1900 order). In addition to these species, one cestode identified to genus-level has been reported (Vampirolepis sp.) [86]. The description of H. balsacii is based on material from Myotis bechsteinii and Eptesicus serotinus from north-eastern France collected by the naturalist Henri Heim de Balsac (1899–1979) at a place called Buré d’Orval in Allondrelle-la-Malmaison [158, 159]. Some authors have noted that the observation was made at “Buré” ([158] see also [142]). Joyeux & Baer’s paper on cestodes, entitled Sur quelques Cestodes de France, is the first work on the bat cestodes in France (published in 1934 in the journal Archives du Muséum national d’Histoire naturelle). Bat cestodes are not well studied, especially in France, where the most recent data from field research is almost 50 years old [68, 86, 158, 159, 167, 177, 180, 196, 200, 243, 255, 262]. France has the most diverse community reported in the literature. According to Frank et al. [121], three species are known to be associated with bats in Poland and Hungary. These authors also reported one species in Germany and two species in Austria. It is worth noting that, according to the Inventaire National du Patrimoine Naturel, 75 species of the family Hymenolepididae have been reported in France and species of the family found in bats represent 4% of the family [153].

4 Hosts and geographical distribution of bat-parasite associations

Over a 256-year period, the 113 recognised taxa of bat parasites from France were collected from 27 bats species and six other bats that were not identified to species-level (five genera and the Pipistrellus species complex) (Figs. 2 and 4). The taxa are B. barbastellus, E. serotinus, H. savii, M. schreibersii, M. bechsteinii, M. blythii, M. capaccinii, M. dasycneme, M. daubentonii, M. emarginatus, M. myotis, M. mystacinus, M. nattereri, M. punicus, N. lasiopterus, N. leisleri, N. noctula, P. kuhlii, P. nathusii, P. pipistrellus, P. auritus, P. austriacus, R. euryale, R. ferrumequinum, R. hipposideros, R. mehelyi, T. teniotis, Eptesicus sp., Myotis sp., Pipistrellus sp., Plecotus sp., Rhinolophus sp., and the species complex Pipistrellus pipistrellus/kuhlii/nathusii. These species represent almost 79% of the bat fauna of France (including Corsica). The most commonly reported hosts, which are mentioned in more than 29 papers, are E. serotinus, R. euryale, R. hipposideros, M. schreibersii, P. pipistrellus, M. myotis, and R. ferrumequinum. However, the most cited species is the Greater horseshoe bat (R. ferrumequinum); 30% of the analysed publications deal with this species. Some bat species have no records of associated metazoan parasites in the analysed publications (n = 237), because the ecology of the host is poorly studied (E. nilssonii, Vespertilio murinus (Particoloured Bat), M. alcathoe, M. escalerai and P. macrobullaris). In addition to this, since P. pygmaeus was identified in the 1990’s, we cannot rule out that some of the records of Pipistrellus sp. or P. pipistrellus may refer to P. pygmaeus [41, 45, 53, 58, 142].

thumbnail Figure 4

Histogram showing the number of studies (n = 237) per host taxon (n = 34; species: 27; complex: 1; genera: 6) during the period 1762–2018.

Published field data originated from 72 French departments (Fig. 5). One of them is mentioned as a non-prospected area (department of Vosges). Indeed, there is no publication about bat parasites in this department. Associations with specified geographical locations were most commonly from Ardèche (11 papers), Ariège (13 papers), Bouches-du-Rhône (15 papers), Haute-Savoie (12 papers), Maine-et-Loire (19 papers), Moselle (11 papers), Meurthe-et-Moselle (23 papers), Pyrénées-Orientales (24 papers), Sarthe (12 papers), Haute-Corse, and Corse-du-Sud (23 papers). Importantly, these distribution patterns are influenced more by biased sampling efforts than by actual geographical and ecological patterns. This distribution map only helps to point to well-studied areas. The relative prominence of the departments Ardèche, Ariège, Pyrénées-Orientales, Haute-Corse and Corse-du-Sud compared to other departments is most likely a result of the attention given to karstic areas by European biospeleology (for instance [14, 23–25, 48–53, 69, 70, 115, 118, 120, 126, 131–133, 136, 137, 151, 152, 154, 178, 186, 214–216, 246]). This is closely linked to the success and prevalence of M. schreibersii, R. euryale, and R. ferrumequinum compared to other bat species. This prevalence could be the result of their ability to roost in the summer in limestone areas and underground sites. The focus on E. serotinus, R. ferrumequinum, R. hipposideros, P. pipistrellus, and M. myotis is the result of their ability to exploit anthropogenic environments (i.e. farmland, urban areas). As a consequence of this, these species have more contact with human populations (about P. pipistrellus, see [182]) and were the first to be studied in France (for the 1762–1844 period see [11, 13, 18, 90–92, 94–97, 124, 183, 220, 258, 260]).

thumbnail Figure 5

Study area and the number of publications that include data on parasites of bats in each French administrative region (department).

Conflict of interest

The author declares no conflict of interest.

Acknowledgments

One of the most pleasant parts of finishing a paper is to thank those who have contributed to the making of it. My thanks first of all to Professor Jean-Lou Justine, Editor-in-chief of Parasite. I have every reason to be grateful for the help and advice of the highly esteemed naturalist Professor Jean-Claude Beaucournu. I would like to express my warmest thanks to the Parasite journal reviewers for proofreading the manuscript and for their valuable comments and suggestions, and to Gilles Le Guillou. My thanks to my father François Léger and Jean-Baptiste Schweyer (Agence Française pour la Biodiversité), who provided me opportunities to deal with biased sampling efforts issues. I extend my warm thanks to Valeria Dragoni and to my friends and colleagues Clément Chardon and Hugo Weissbart (Imperial College London, Department of Bioengineering). I want to thank especially two librarians and colleagues: Lucien Gournay, a fine librarian at the Bibliothèque Mammifères et Oiseaux in Paris (MNHN, service Recherche, enseignement, expertise), who read and commented on the completed manuscript; Ann Qualtrough (Bibliothèque centrale du MNHN, service Collecte, traitement et flux), who took the time to read the manuscript and make numerous valuable suggestions. Of course, it needs to be added that responsibility for any remaining errors is my own.

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Cite this article as: Léger C. 2020. Bat parasites (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) in France (1762–2018): a literature review and contribution to a checklist. Parasite 27, 61.

All Tables

Table 1

List of bat species and their associated metazoan parasites in France (including Corsica), based on the published literature. Authors are listed in the bibliography. See also the work titled Les parasites métazoaires des Chiroptères de France (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) : contribution à un état des lieux bibliographique (1762–2018) et à l’établissement d’une liste nationale (2019). Invalid species are listed in brackets. Records marked with an exclamation mark (!) are invalid. Records marked with a question mark (?) are dubious. They may require further clarification.

In the text
Table 2

List of bat parasites (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) and their hosts in France (including Corsica), based on the published literature, with reported synonyms. Authors are listed in the bibliography. See also the work entitled Les parasites métazoaires des Chiroptères de France (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) : contribution à un état des lieux bibliographique (1762-2018) et à l’établissement d’une liste nationale (2019). Invalid species are listed in brackets. Records marked with an exclamation mark (!) are invalid. Records marked with a question mark (?) are dubious. They may require further clarification.

In the text

All Figures

thumbnail Figure 1

Number of studies (n = 237) that include bat parasites observed in France since 1760, by decade.
In the text
thumbnail Figure 2

Overview of the 113 generally recognised parasite taxa that are mentioned in the analysed papers (n = 237) per host taxonomic group. Invalid species (n = 22 Acari and 3 Diptera) recorded in the literature, records reported from France without identification to species level (n = 6 Acari; 1 Cestoda; 2 Diptera; 1 Hemiptera; 2 Nematoda and 2 Trematoda) and species only noted as absent (n = 3 Acari and 1 Diptera) are not included here.
In the text
thumbnail Figure 3

Number of recognised species of Acari (n = 53), per host order (n = 4) and genus (n = 23). Invalid species (n = 22 Acari) recorded in the literature (n = 237 papers) and species only noted as absent (n = 3 Acari) are not included here.
In the text
thumbnail Figure 4

Histogram showing the number of studies (n = 237) per host taxon (n = 34; species: 27; complex: 1; genera: 6) during the period 1762–2018.
In the text
thumbnail Figure 5

Study area and the number of publications that include data on parasites of bats in each French administrative region (department).
In the text

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