Abstract

Résumé

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.

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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 ​and2.2. The map in Figure 5 was created using Carto-SI (https://www.carto-si.com/).