Bat parasites (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera, Trematoda) in France (1762–2018): a literature review and contribution to a checklist

This paper is a bibliographical survey of records of bat parasites in France (including Corsica) between 1762 and 2018. In total, 237 scientific publications were analysed. They show that bats are infected with a large diversity of endoparasites and ectoparasites. A total of 113 parasite taxa were identified from 27 host species; in addition, six bats were not identified to the species-level. The helminth fauna of bats comprises three species of Cestoda, 15 of Trematoda, and 13 of Nematoda. Acari parasites include 53 species (in addition to 22 invalid species). Finally, insect parasites comprise 13 species of Diptera (bat flies), 12 of Siphonaptera (fleas), 3 of Hemiptera (bugs), and 1 Anoplura species. Bat taxa reported with parasites were Barbastella barbastellus, Eptesicus serotinus, Hypsugo savii, Miniopterus schreibersii, Myotis bechsteinii, M. blythii, M. capaccinii, M. dasycneme, M. daubentonii, M. emarginatus, M. myotis, M. mystacinus, M. nattereri, M. punicus, Nyctalus lasiopterus, N. leisleri, N. noctula, Pipistrellus kuhlii, P. nathusii, P. pipistrellus, Plecotus auritus, P. austriacus, Rhinolophus euryale, R. ferrumequinum, R. hipposideros, R. mehelyi, Tadarida teniotis, Eptesicus sp., Myotis sp., Pipistrellus sp., Plecotus sp., Rhinolophus sp. and the species complex Pipistrellus pipistrellus/kuhlii/nathusii. As regards E. nilssonii, Vespertilio murinus (Particoloured Bat), M. alcathoe, M. escalerai, P. macrobullaris and P. pygmaeus, no records were found. These published field data originated from 72 of the 96 departments in metropolitan France. The most commonly cited were Ardèche, Ariège, Bouches-du-Rhône, Haute-Savoie, Maine-et-Loire, Moselle, Meurthe-et-Moselle, Pyrénées-Orientales, Sarthe, Haute-Corse and Corse-du-Sud.


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.

Methods
Initially, I used the works of nine authors: Anciaux de Faveaux [5][6][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][107][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.
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].

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].

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).  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].
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 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]).

Conflict of interest
The author declares no conflict of interest.
Acknowledgements. 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.