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First records of bat ectoparasites from Chrea National Park, Algeria, with notes on guano-based endoparasite traces

Published online by Cambridge University Press:  28 April 2026

Djamel Bendjoudi ,
Faiza Marniche ,
Sarah Banat ,
Hichem Zaoui  and
Haroun Chenchouni Open the ORCID record for Haroun Chenchouni [Opens in a new window]
Djamel Bendjoudi
Affiliation:
Laboratory of Biotechnology, Environment and Health, Faculty of Nature and Life Sciences, University of Blida 1, Blida, Algeria
Faiza Marniche
Affiliation:
Research Laboratory on the Management of Local Animal Resources (GRAL), Higher National Veterinary School (ENSV), Algiers, Algeria
Sarah Banat
Affiliation:
Laboratory of Biotechnology, Environment and Health, Faculty of Nature and Life Sciences, University of Blida 1, Blida, Algeria
Hichem Zaoui
Affiliation:
Laboratory of Biotechnology, Environment and Health, Faculty of Nature and Life Sciences, University of Blida 1, Blida, Algeria
Haroun Chenchouni*
Affiliation:
Department of Ecology and Environment, Faculty of Nature and Life Sciences, University of Batna 2, Batna, Algeria Laboratory of Natural Resources and Management of Sensitive Environments (LRNAMS), University of Oum El Bouaghi, Oum El Bouaghi, Algeria
*
Corresponding author: Haroun Chenchouni; Email: chenchouni@gmail.com
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Abstract

Content of image described in text.

Field sampling was conducted in the Chiffa tunnel area of the El Hamdania sector within Chrea National Park (CNP), Algeria. A total of 20 bats were captured and examined for ectoparasite infestations. Additionally, coprological analysis of guano was performed to investigate the possible presence of traces of internal parasites, subject to the methodological limitations described herein. The captured bats belonged to 2 distinct families. The family Rhinolophidae included Rhinolophus blasii Peters, 1866, represented by 18 individuals, and the greater horseshoe bat, Rhinolophus ferrumequinum (Schreber, 1774), represented by a single individual. The family Vespertilionidae was represented by Nyctalus leisleri (Kühl, 1817), also by a single individual; this constitutes the first documented record of this species in CNP. Examination of ectoparasites from 19 rhinolophid bats identified 3 dipteran ectoparasite species. Brachytarsina (Brachytarsina) flavipennis Macquart, 1851 (Streblidae) was the most prevalent (66.7%), followed by Phthiridium biarticulatum Hermann, 1804 and Nycteribia schmidlii Schiner, 1853 (Nycteribiidae), each at 16.7%. The study documents, for the first time in Algeria, N. schmidlii parasitizing R. blasii. Coprological analysis of guano revealed the presence of structures belonging to 3 phyla; these data are preliminary and should be interpreted with caution. The findings contribute to knowledge of chiropteran ectoparasite–host associations in North Africa and highlight CNP as a significant locality for bat biodiversity.

Keywords

bats (Chiroptera)Chrea National Parkectoparasitesendoparasitesguano analysisRhinolophidaespecies diversityVespertilionidae

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Type
Research Article
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Parasitology , First View , pp. 1 - 11
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© The Author(s), 2026. Published by Cambridge University Press.

Introduction

Bats (Chiroptera) represent the second most diverse order of mammals after rodents, constituting approximately 22% of all mammalian species, with around 1420 species documented globally (Burgin et al., Reference Burgin, Colella, Kahn and Upham2018; Letko et al., Reference Letko, Seifert, Olival, Plowright and Munster2020). They inhabit all continents except Antarctica (Letko et al., Reference Letko, Seifert, Olival, Plowright and Munster2020), with particularly high densities noted in Mediterranean regions, including Southern Europe and North Africa (Rose, Reference Rose2006; Aulagnier et al., Reference Aulagnier, Haffner, Mitchell-Jones and Moutou2017). While bats have been associated with various disease outbreaks, their ecological importance is significant, as they fulfil critical roles in ecosystems, such as regulating arthropod populations and facilitating plant pollination (Aggrey et al., Reference Aggrey, Rwego, Sande, Khayiyi, Kityo, Masembe and Kading2024).

Despite their ecological benefits, bats are recognized as natural reservoirs for several zoonotic pathogens, including viral, bacterial, parasitic and fungal agents (Smith and Wang, Reference Smith and Wang2012; Allocati et al., Reference Allocati, Petrucci, Di Giovanni, Masulli, Di Ilio and De Laurenzi2016). These pathogens can be disseminated over considerable distances, aided by the migratory behaviour of certain bat species (Messenger et al., Reference Messenger, Rupprecht, Smith, Kunz and Fenton2003). Algeria, with its favourable ecological conditions (Yeddou and Lammari, Reference Yeddou and Lammari2017), hosts a remarkable diversity of bat species, ranking second in Africa after Sudan. The bat fauna of Algeria includes 25 species across 7 families, with 6 species from the Rhinolophidae family and 13 species from the Vespertilionidae family (Ahmim, Reference Ahmim2013, Reference Ahmim2017, Reference Ahmim2019).

Research on chiropteran parasites, particularly ectoparasites and endoparasites, has garnered increased interest in recent years due to their relevance in modelling the emergence and transmission of diseases (Dick and Patterson, Reference Dick and Patterson2007; Wibbelt et al., Reference Wibbelt, Moore, Schountz and Voigt2010; Attia-Hili, Reference Attia-Hili2015). However, studies on bat parasites in Algeria remain limited and fragmented (Bendjeddou et al., Reference Bendjeddou, Khelfaoui, Abiadh, Mechouk, Mihalca and Sándor2024). Notable efforts include investigations into the seasonal infestation of Myotis punicus Felten, 1977 by Ixodes vespertilionis Koch, 1844 (Bendjeddou et al., Reference Bendjeddou, Bouslama, Amr and Bani Hani2016) and inventories of bat ectoparasites (Ter Hofstede and Fenton, Reference Ter Hofstede and Fenton2005; Bendjeddou et al., Reference Bendjeddou, Bitam, Abiadh, Bouslama and Amr2013, Reference Bendjeddou, Bouslama, Amr and Bani Hani2016, Reference Bendjeddou, Loumassine, Scheffler, Bouslama and Amr2017).

Bats are known to host a wide variety of ectoparasites (Anciaux de Faveaux, Reference Anciaux de Faveaux1965, Reference Anciaux de Faveaux1976; Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993; Stanyukovich, Reference Stanyukovich1997; Imaz et al., Reference Imaz, Aihartza and Totorika1999; Bitam et al., Reference Bitam, Dittmar, Parola, Whiting and Raoult2010; Camilotti et al., Reference Camilotti, Graciolli, Weber, Arruda and Cáceres2010; Orlova, Reference Orlova2011, Reference Orlova2013; Tsai et al., Reference Tsai, Chang, Chuang and Chomel2011; Krištofík and Danko, Reference Krištofík and Danko2012; Morse et al., Reference Morse, Olival, Kosoy, Billeter, Patterson, Dick and Dittmar2012; Klimpel and Mehlhorn, Reference Klimpel and Mehlhorn2014; Morand, Reference Morand2014; Burazerović et al., Reference Burazerović, Ćakić, Mihaljica, Sukara, Ćirović and Tomanović2015; Sponchiado et al., Reference Sponchiado, Melo, Martins, Krawczak, Labruna and Căcere2015; Leulmi et al., Reference Leulmi, Aouadi, Bitam, Bessas, Benakhla, Raoult and Parola2016; Khelfaoui et al., Reference Khelfaoui, Kebaci and Benyacoub2018). In Algeria’s Chrea National Park (CNP), 2 significant studies on bat ectoparasites were conducted in the El Hamdania sector (Yeddou and Lammari, Reference Yeddou and Lammari2017; Bendjoudi et al., Reference Bendjoudi, Yedou, Beneldjouzi, Mechouk and Bendjeddou2019). In addition to ectoparasites, bats harbour various endoparasites, including cestodes, trematodes and nematodes (Theodorides, Reference Theodorides1953; Combes and Clerc, Reference Combes and Clerc1970; Gardner and Jiménez-Ruiz, Reference Gardner and Jiménez-Ruiz2009; Horvat et al., Reference Horvat, Čabrilo, Paunović, Karapandža, Jovanović, Budinski and Čabrilo2015; Singh et al., Reference Singh, Barolia and Sharma2015; Hadjouti and Mamouni, Reference Hadjouti and Mamouni2016; Webber and Willis, Reference Webber, Willis and Ortega2016; Léger, Reference Léger2019). However, knowledge regarding the endoparasites of Algerian bats remains limited.

This study aimed to document the ectoparasites and endoparasites associated with bats in CNP, thereby contributing valuable insights into the parasitic fauna of Algerian bats and their ecological interactions. Specifically, we sought to: (i) identify the bat species present in tunnels of CNP and confirm potential new records for the park and the region; (ii) inventory the ectoparasitic Diptera and Acari species colonizing bat hosts and assess their relative abundance (RA) across different bat species; (iii) conduct coprological analyses of guano samples to identify helminth and arthropod endoparasites, determine their prevalence and quantify their RA; (iv) evaluate whether ectoparasite composition is associated with host species using statistical methods; and (v) provide the first baseline data for ectoparasite–host associations in CNP, thereby establishing a foundation for future faunistic, epidemiological and ecological studies on the role of bats in regional biodiversity and potential pathogen transmission.

Materials and methods

Study area

The CNP, located between latitudes 36°19′ N–36°30′ N and longitudes 02°38′ E–03°02′ E (Figure 1), encompasses an area of 26 587 hectares (BNEF, 1984). The park is recognized for its rich biodiversity, hosting a diverse range of flora and fauna, including a notable variety of chiropteran species. In the western region of the park, bats have been observed inhabiting disused railway tunnels and abandoned mines (Figure 2) along the Chiffa River (36°24′0.01″ N, 2°46′0.01″ E; elevation: 239 m a.s.l.) (Meddour, Reference Meddour2002). CNP is predominantly characterized by montane forests and shrublands, dominated by Atlas cedar (Cedrus atlantica (Endl.) Manetti ex Carrière), holm oak (Quercus ilex L.) and mixed broadleaved woodlands. The main woodland areas are distributed across Oued El Marja, Tibenkent, Beni-Selmen, Tamesguida and the central Chréa region (Bendjoudi et al., Reference Bendjoudi, Marniche, Takdjout, Epalanga and Chenchouni2023).

Figure 1.

Vegetation map and geographic location of Chrea National Park in Algeria.

A map showing the vegetation distribution in Chrea National Park, Algeria, with a detailed legend indicating various forest types and cultivated lands. See long description.
Figure 2.

Photos of Chiffa Tunnel at the Chrea National Park in Algeria. Left: outside the tunnel, right: inside the tunnel, near the entrance.

Two images of Chiffa Tunnel: left shows people on a bridge outside, right shows railway tracks inside the tunnel. See long description.

Bat sampling

Field sampling was conducted between May and June 2019 in the El Hamdania tunnel (Figure 2). Bats were captured using hand nets (Figure 3), a method compliant Algerian Law and preferred in chiropteran research (Kunz and Kurta, Reference Kunz, Kurta and Kunz1988; Mitchell-Jones and Robertson, Reference Mitchell-Jones, Robertson, Mitchell-Jones and McLeish2004). Captured bats were placed in thick, aerated capture bags and transported to the Zoology Laboratory of the National Veterinary School of El Alia (Algiers) for further examination.

Figure 3.

Capture bats with a hand net.

Two images showing a bat in a tunnel and a person capturing bats with a hand net.

Bat species identification was conducted using the determination keys of Dietz and von Helversen (Reference Dietz and von Helversen2004) and Dietz (Reference Dietz2005), by Prof Faiza Marniche at National Veterinary School of El Alia (Algeria) and Prof Djamel Bendjoudi at the Laboratory of Biotechnology, Environment, and Health in Blida 1 University. Following identification and examination, all bats were released back into their natural habitats by the end of the same day.

Collection and identification of endoparasites in guanos

For parasitological analysis, 150 g of guano was collected from each individual of 2 Rhinolophidae species (Rhinolophus blasii and Rhinolophus ferrumequinum). Parasites were identified using the flotation technique (Sivajothi et al., Reference Sivajothi, Reddy and Rayulu2014; Hendrix and Robinson, Reference Hendrix and Robinson2023) and the direct smear method. Microscopic examination was conducted at magnifications of 10×, 40× and 100×, with parasite identification guided by standard taxonomic keys (Sonin, Reference Sonin1975; Bray et al., Reference Bray, Gibson and Jones2008; Anderson et al., Reference Anderson, Chabaud and Willmott2009; Léger, Reference Léger2019; Zajac et al., Reference Zajac, Conboy, Little and Reichard2021).

Collection and identification of ectoparasites on bats

Each bat was individually examined for ectoparasites, which were carefully removed with fine forceps following macroscopic examination of all body regions (Hutson et al., Reference Hutson, Mickleburgh and Racey2001). Collected ectoparasites were preserved in 70% ethanol and processed through a series of preparatory steps: immersion in a 10% potassium hydroxide (KOH) solution for 24 h, rinsing in distilled water for 30 min and subsequent dehydration in 100% ethanol. Prepared specimens were mounted on slides and examined under a Leica DM500 optical microscope at 100× magnification.

Ectoparasite identification was performed using established taxonomic references (Arthur, Reference Arthur1956; Hopkins and Rothschild, Reference Hopkins and Rothschild1956; Rudnick, Reference Rudnick1960; Dusbabek, Reference Dusbabek1962; Radovsky, Reference Radovsky1967; Theodor, Reference Theodor1967; Hůrka, Reference Hůrka1982; Dietz and von Helversen, Reference Dietz and von Helversen2004). Additional verification was provided by Prof Faiza Marniche at the National Veterinary School (Algiers, Algeria) and Prof Carl Dick (Department of Biology, Western Kentucky University, Kentucky, USA), utilizing dichotomous keys.

Data analysis

The results obtained from our study on ectoparasites and endoparasites were analysed using the positivity index applied to ectoparasite samples collected from bats and guano. The positivity index represents the percentage of samples containing a parasite, calculated as P% = (P+ /Pt) × 100, where P% is the positivity index, P+ is the number of positive samples and Pt is the total number of samples (El Guamri et al., Reference El Guamri, Belghity, Achicha, Tiabi, Aujjar and Barkia2009). Parasite abundance (A) is defined as the ratio of the total number of individuals of a parasite species (n) to the total number of individuals host examined (H) (Margolis et al., Reference Margolis, Esch, Holmes, Kuris and Schad1982). In this context, H denotes the number of host samples examined, and A is calculated as A = n/H, where n represents the number of individuals of the parasite species. Finally, statistical analyses were conducted using the software Quantitative Parasitology V 3.0 (Rózsa et al., Reference Rózsa, Reiczigel and Majoros2000) to process prevalence and other relevant parameters. The package {ggalluvial} version 0.12.5 under the statistical environment R was used to generate to generate alluvial diagram depicting the distribution of dipteran ectoparasites across their bat hosts.

Results

Bat species

During field sampling events around the El Hamdania tunnels in April and June 2019, we collected 20 bats from 2 different families: 2 species from the Rhinolophidae family and 1 species from the Vespertilionidae family. The captured bat species included Blasius’s Horseshoe Bat (Rhinolophus blasiiblasii Peters, 1866) with 18 individuals (13 males and 5 females), the Greater Horseshoe Bat (Rhinolophus ferrumequinum (Schreber, 1774)) which comprised 1 male and Leisler’s Bat (Nyctalus leisleri (Kühl, 1817)) also represented by 1 male (Figure 4). It is noteworthy that N. leisleri (Vespertilionidae) is a new species that has not been previously reported in the CNP.

Figure 4.

Bat species found in the Chiffa tunnel around the Chrea National Park. (A) Leisler’s Noctule Nyctalus leisleri, (B) Blasius’s horseshoe bat Rhinolophus blasii, and (C) greater horseshoe bat Rhinolophus ferrumequinum.

Composite photograph with three close-up bat photographs labeled A, B and C. See long description.

Ectoparasites

The identification of ectoparasites found in the 2 species of Rhinolophidae revealed 30 ectoparasites were collected from 18 R. blasii (14 males and 4 females) and 1 R. ferrumequinum (male) between April and June 2019. We noted the presence of a single class, a single order with 2 families, namely 20 Streblidae flies including Brachytarsina (Brachytarsina) flavipennis Macquart, 1851 [= Nycteribosca africana] and 10 Nycteribiidae flies including Phthiridium biarticulatum Hermann, 1804 (n = 5 flies) and Nycteribia schmidlii Schiner, 1853 (n = 5 flies) (Figure 5).

Figure 5.

Microscopic views (40× magnification) of Nycteribia (Listropoda) schmidlii schmidlii Schiner, 1853 (Diptera: Nycteribiidae): (A) female ventral view; (B) male ventral view; (C) male ventral extremity; (D) dorsal view of Nycteribosca africana = Brachytarsina (Brachytarsina) flavipennis Macquart, 1851 (Diptera: Streblidae) and (E) ventral view of Phthiridium biarticulatum (Diptera: Nycteribiidae) Hermann, 1804.

Composite micrograph figure with five microscope photographs labeled A to E, showing ventral and dorsal views and close-ups of wingless and winged flies at 40 times magnification. See long description.

These ectoparasites were collected from the patagium of R. blasii females and R. ferrumequinum male. The ectoparasite community associated with the captured bats showed varying levels of RA among host species. In R. blasii, Nycteribosca africana was the dominant parasite (75%), followed by N. schmidlii (15%) and Phthiridium biarticulatum (10%). In R. ferrumequinum, N. africana also prevailed but at a lower proportion (50%), while P. biarticulatum (30%) and N. schmidlii (20%) were relatively more common compared to their occurrence in R. blasii (Figure 6). The Pearson chi-square test of independence revealed no significant association between bat host species and ectoparasite composition (χ 2 = 2.00, df = 2, p = 0.37), indicating that ectoparasite distribution was relatively similar between R. blasii and R. ferrumequinum.

Figure 6.

Alluvial plot illustrating the distribution of dipteran ectoparasites across their bat hosts. The proportions (%) are relative abundances.

An alluvial plot showing the distribution of dipteran ectoparasites across bat host species. See long description.

Endoparasites

Coprological analysis results

A study of the parasitic fauna of the bats revealed the presence of a species of cestode and 2 species of nematodes within 150 g of guano samples (Table 1). A substantial presence of arthropods was also recorded, represented by adult mites and eggs (n = 255) (Figure 7). We observed a high RA for the arthropod phylum (55.7%). The species Alabidocarpus sp. (adults) dominated with a rate of 43.7%. The nematode Strongylacantha sp. (non-embryonated eggs) ranked second with 118 individuals (RA = 25.8%), followed by Acari sp. (eggs) with 55 individuals (RA = 12.0%). Rhabditida sp. (embryonated eggs) was observed with an RA of 13.8% (63 individuals), while the cestode Milina (Hymenolepis) sp. (eggs) was represented by 11 individuals (RA = 2.4%) (Table 1).

Table 1.

Inventory and abundance of parasites found in bat guanos studied in Chrea National Park

Alabidocarpus sp. adults dominate bat guano parasites (200 individuals; 43.7%), followed by Strongylacantha sp. non-embryonated eggs (118; 25.8%) out of 458 total. See long description.

S = Total richness, n = number of individuals (per 150 g guanos), RA = relative abundance in %.

Figure 7.

Parasites found in bat guanos observed under light microscope at 40× magnification. (A) Non-embryonated egg of Strongylacantha sp.; (B) embryonated egg of Rhabditida sp.; (C) larva Rhabditida sp.; (D) egg of Milina (Hymenolepis) sp.; (E) egg Acari and (F) adult Alabidocarpus sp.

Six micrographs labeled A to F of oval structures and curved worm-like forms. See long description.

Prevalence of endoparasites

The prevalence of endoparasites found in the guanos of the Rhinolophidae studied is presented in Table 2. Out of a total of 150 g of Rhinolophidae guano, a prevalence of 100% was infested by Alabidocarpus sp. (adults), followed by Strongylacantha sp. (non-embryonated eggs) with a prevalence rate of 78.7%. Rhabditida sp. (embryonated eggs) has a prevalence rate of 42.0%, while Acari sp. (eggs) shows a prevalence rate of 36.7%. Both Rhabditida sp. (larvae) and Milina (Hymenolepis) sp. (eggs) represent a prevalence rate of 7.3% each. We also note the presence of 2 dominant species: Alabidocarpus sp. (adults) and Strongylacantha sp. (non-embryonated eggs). Additionally, there are satellite species, including Rhabditida sp. (embryonated eggs) and Acari sp. (eggs), as well as rare species such as Rhabditida sp. (larvae) and Milina (Hymenolepis) sp. (eggs) (Table 2).

Table 2.

Abundance (A), positivity index (P+) and prevalence of parasites found in bat guanos studied in Chrea National Park (Algeria)

Alabidocarpus adults were most common (A 100; 100% prevalence), with Strongylacantha eggs also high (A 59; 78.7%), while Rhabditida larvae and Milina eggs were rare (7.3%). See long description.

n = number of individuals, A = parasite abundance, H = number of parasitized hosts.

Discussion

The present study provides the first survey of bat ectoparasites, with supplementary coprological data, in CNP, Algeria, thereby filling a significant gap in the regional knowledge of chiropteran ecology. Three bat species were recorded, including R. blasii and R. ferrumequinum, with N. leisleri reported for the first time in the park, marking an extension of its known distribution in North Africa. Parasitological analyses revealed a remarkable diversity of metazoan parasites, encompassing both ectoparasites (Diptera and Acari) and endoparasites (Nematoda and Cestoda). Among the most noteworthy findings, N. schmidlii parasitizing R. blasii was reported for the first time in Algeria, as well as a distinct composition of helminth communities, which varied across host species. These results underscore not only the ecological complexity of bat-parasite interactions in this understudied region but also the originality of the faunistic data presented here, which contribute novel records at both national and local levels.

Bat species

Leisler’s Noctule (N. leisleri) is a migratory species found in Europe and has been documented in the northern Himalayan region of Pakistan (Walker et al., Reference Walker, Warnick, Lange, Uible, Hamlet, Davis and Wright1964). It is recognized as a Mediterranean species and appears to be the most prevalent Nyctalus species in Africa. This species has been recorded only in Yakouren, located in northern Algeria (Tizi Ouzou), as noted by Hanak and Gaisler (Reference Hanak and Gaisler1983), Gaisler (Reference Gaisler1983) and Gaisler and Kowalski (Reference Gaisler and Kowalski1986). Hanak and Gaisler conducted a biometry study of the 4 individuals discovered in 1983 in Northern Cyrenaica, Libya and Morocco (El Ibrahimi and Idrissi, Reference El Ibrahimi and Idrissi2015), as well as in Bekrite in the Middle Atlas (Benda et al., Reference Benda, Ruedi and Aulagnier2004, Reference Benda, Červený, Konečný, Reiter, Ševčík, Uhrin and Vallo2010). N. leisleri was first recorded in CNP. While its current distribution and demographic data are not available, its presence has been confirmed. This locality represents the southernmost point for this species in the Maghreb and is also the most continental site in Africa.

Ectoparasites

Bats host a diverse array of ectoparasites and serve as crucial food sources for numerous haematophagous arthropods. These ectoparasites can negatively impact the fitness of their bat hosts, affecting both survival and reproductive success. Such fitness costs drive the evolution of host behavioural defences to mitigate parasitism (Ter Hofstede and Fenton, Reference Ter Hofstede and Fenton2005). In Algeria, studies on bat ectoparasites remain relatively limited. Our findings concerning ectoparasites from the Nycteribiidae family align with the work of Bendjeddou et al. (Reference Bendjeddou, Loumassine, Scheffler, Bouslama and Amr2017), who compiled a systematic list of bat ectoparasites in Algeria, documenting 25 species, including 3 bat fly species from the Nycteribiidae family.

The bat fly N. schmidlii exhibits a broad distribution, spanning southern Europe, North Africa, southwestern Asia and parts of Central Asia, including Afghanistan (Hůrka, Reference Hůrka1964). In Algeria, this species has been reported on various bat hosts, including Miniopterus schreibersii and Rhinolophus mehelyi (Falkoz, 1923), R. ferrumequinum (Theodor and Moscona, Reference Theodor and Moscona1954), Myotis blythi (Rotrou, Reference Rotrou1939; Aellen, Reference Aellen1955), M. schreibersii, M. blythi and R. euryale (Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993). Elsewhere, N. schmidlii has been documented on Asellia tridens in Palestine (Theodor and Moscona, Reference Theodor and Moscona1954) and on M. schreibersii in Turkey (Albayrak, Reference Albayrak2003). Hůrka (Reference Hůrka1964) identified M. schreibersii as the principal host of N. schmidlii, while also listing secondary hosts such as M. blythi, M. capaccinii, M. emarginatus, Myotis myotis, Rhinolophus euryale, R. ferrumequinum and R. mehelyi. These bats are typically social, and residing in caves (Scheffler et al., Reference Scheffler, Dolch, Ariunbold, Stubbe, Abraham and Thiele2012). Notably, this study reports N. schmidlii schmidlii parasitizing R. blasii in Algeria for the first time.

Phthiridium biarticulatum is a circum-Mediterranean species associated primarily with cave-dwelling bats. It demonstrates a strong preference for Rhinolophus species (Ševčík et al., Reference Ševčík, Benda and Lucan2013), particularly R. ferrumequinum and R. euryale (Beaucournu and Noblet, Reference Beaucournu and Noblet1996). In this study, this bat fly was collected from R. blasii and R. ferrumequinum. In Algeria, P. biarticulatum has been reported on R. ferrumequinum (Theodor and Moscona, Reference Theodor and Moscona1954) and R. blasii (Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993; Bendjeddou et al., Reference Bendjeddou, Bitam, Abiadh, Bouslama and Amr2013, Reference Bendjeddou, Loumassine, Scheffler, Bouslama and Amr2017). Beyond Algeria, it has been recorded on R. mehelyi in Libya (Hůrka, Reference Hůrka1982; Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993), R. blasii, R. euryale and R. ferrumequinum in Iran (Nader and Kock, Reference Nader and Kock1983; Benda et al., Reference Benda, Spitzenberger, Hanák, Andreas, Reiter, Ševčík, Šmíd and Uhrin2014), and R. blasii, R. clivosus, R. euryale and R. ferrumequinum in Jordan (Benda et al., Reference Benda, Červený, Konečný, Reiter, Ševčík, Uhrin and Vallo2010).

Nycteribosca africana is the sole representative of the Streblidae family in Western Europe. This small-winged, thermophilic fly is predominantly associated with troglophilic and gregarious bats of the genera Myotis and Rhinolophus (Beaucournu and Noblet, Reference Beaucournu and Noblet1996). Previously referred to as Nycteribosca kollari, this species thrives along winter isotherms of +8 to +10 °C (Hůrka, Reference Hůrka1962). Although primarily parasitizing Mediterranean Rhinolophus species, N. africana is also common on Myotis species (Hůrka, Reference Hůrka1962; Scheffler et al., Reference Scheffler, Dolch, Ariunbold, Stubbe, Abraham and Thiele2012). It has been documented on R. blasii, R. ferrumequinum, R. hipposideros and R. mehelyi in regions such as Cyprus, Jordan and Syria (Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993; Walter and Ebenau, Reference Walter and Ebenau1997; Ševčík et al., Reference Ševčík, Benda and Lucan2013).

On the island of Crete, Brachytarsina flavipennis Macquart, 1851 was reported on R. blasii for the first time by Scaravelli et al. (Reference Scaravelli, Priori and Georgiakakis2014). Additionally, N. africana has been recovered from R. blasii in Iran and Jordan (Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993; Benda et al., Reference Benda, Spitzenberger, Hanák, Andreas, Reiter, Ševčík, Šmíd and Uhrin2014), from R. ferrumequinum and R. blasii in Cyprus (Ševčík et al., Reference Ševčík, Benda and Lucan2013) and from R. mehelyi in Libya and Syria (Hůrka, Reference Hůrka1982; Walter and Ebenau, Reference Walter and Ebenau1997). One female specimen was captured on R. ferrumequinum at El-Haouaria, Tunisia, in April 1955 (Vermeil, Reference Vermeil1960).

Although the chi-square test showed no significant association between host species and ectoparasite composition, some differences in relative prevalence were observed. Nycteribosca africana was more common on R. blasii, while Phthiridium biarticulatum occurred more frequently on R. ferrumequinum. These patterns may reflect subtle differences in roosting behaviour, microhabitat use or host physiology rather than strict host specificity. Similar non-exclusive associations have been reported in Mediterranean and North African bat–ectoparasite systems, where parasite prevalence varied among host species without clear statistical segregation (Bain, Reference Bain1966; Burazerović et al., Reference Burazerović, Ćakić, Mihaljica, Sukara, Ćirović and Tomanović2015; Frank et al., Reference Frank, Kuhn, Werblow, Liston, Kochmann and Klimpel2015; Khelfaoui et al., Reference Khelfaoui, Kebaci and Benyacoub2018). Such findings suggest that the distribution of bat ectoparasites is often influenced by ecological factors such as roost type, host colony size and microclimatic conditions, rather than strict host specialization (Amr and Qumsiyeh, Reference Amr and Qumsiyeh1993; Patterson et al., Reference Patterson, Dick and Dittmar2007; Bendjeddou et al., Reference Bendjeddou, Bouslama, Amr and Bani Hani2016, Reference Bendjeddou, Khelfaoui, Abiadh, Mechouk, Mihalca and Sándor2024; Webber and Willis, Reference Webber, Willis and Ortega2016). This highlights the ecological plasticity of bat flies and streblid parasites, which may exploit multiple sympatric hosts within the same habitat.

Endoparasites

The present study provides preliminary coprological data on helminths and arthropods found in bat guano in the El Hamdania sector of CNP. It should be noted that this coprological approach has important limitations: it yields only qualitative presence–absence data, does not permit estimation of parasite burden and cannot detect trematodes, which are among the most common bat endoparasites. A full helminthological necropsy involving dissection of all organ systems would be required to obtain comprehensive data on the endoparasite fauna. All species reported represent new records for the country.

Previous studies have demonstrated that flukes (digeneans) and roundworms (nematodes) are prevalent in horseshoe bat populations (Esteban et al., Reference Esteban, Oltra-Ferrero, Botella and Mas-Coma1991, Reference Esteban, Botella and Toledo1999; Ricci, Reference Ricci1995). Esteban et al. (Reference Esteban, Oltra-Ferrero, Botella and Mas-Coma1991) attributed this high prevalence to factors such as bat lifestyle, habitat preferences and diet. For instance, Strongylacantha spp. have simple life cycles, whereas Rhabditida spp. exhibit more complex parasitic cycles involving blood-sucking insect vectors (Bain, Reference Bain1966; Mészáros, Reference Mészáros1971). These insects consume larvae produced by mature female nematodes within bat hosts.

In related studies, Horvat et al. (Reference Horvat, Čabrilo, Paunović, Karapandža, Jovanović, Budinski and Čabrilo2015) analysed helminth infections in 17 individuals of the greater horseshoe bat (R. ferrumequinum) collected across 8 localities in Serbia. Helminth prevalence was high, with 88.2% of bats infected. Among the parasites identified, Strongylacantha glycirrhiza showed the highest prevalence (76.5%), comprising 65 of the 108 helminth individuals recovered. This study highlights the importance of both helminths and protozoa as common endoparasites in bats (Gardner and Jiménez-Ruiz, Reference Gardner and Jiménez-Ruiz2009; Klimpel and Mehlhorn, Reference Klimpel and Mehlhorn2014). For instance, Mühldorfer et al. (Reference Mühldorfer, Speck, Kurth, Lesnik, Freuling, Müller, Kramer-Schadt and Wibbelt2011) identified protozoan infections, such as Eimeriidae and Sarcocystidae, in Pipistrellus pipistrellus bats in Germany.

The observed helminth diversity in our study differs from those reported in the literature, potentially due to host species differences, dietary diversity or unique immune characteristics. For example, R. ferrumequinum exhibited consistently high parasitism levels, contrasting with the lower parasitism observed in R. blasii. This disparity mirrors findings by Mituch (Reference Mituch1964) in Czechoslovakia, where R. euryale displayed impoverished helminthofauna (14% parasitism) compared to R. ferrumequinum (43%). These differences may reflect variations in host immunity or ecological and behavioural factors, such as prey selection or activity patterns. It must be emphasized, however, that meaningful statistical comparison of endoparasite levels between R. ferrumequinum and R. blasii is not possible in the present study, given that only a single individual of R. ferrumequinum was sampled.

Cestodes in bats, particularly in Algeria, remain understudied. Comparative literature from France, Poland, Hungary, Germany and Austria reveals diverse Cestoda communities, with species of the Hymenolepididae family representing 4% of bat-associated taxa (Frank et al., Reference Frank, Kuhn, Werblow, Liston, Kochmann and Klimpel2015; Léger, Reference Léger2019). Differences in dietary composition, such as consumption of aquatic larvae – essential vectors for trematodes – may influence infection prevalence (Holmes, Reference Holmes1966). Such ecological nuances warrant further investigation to better understand host-parasite dynamics.

Additionally, mites are well-documented ectoparasites in bats, including ticks (Kolonin, Reference Kolonin2007; Hornok et al., Reference Hornok, Kontschán, Kovács, Angyal, Görföl, Polacsek, Kalmár and Mihalca2014) and other mite species (Tsai et al., Reference Tsai, Chang, Chuang and Chomel2011). At our study site, adult mites of the genus Alabidocarpus were identified in bat guano, underscoring the complex ecological interactions between bats and their parasites. Host-parasite relationships are deeply influenced by the behaviour and ecology of both parties (Patterson et al., Reference Patterson, Dick and Dittmar2007).

The helminth species reported here are consistent with those expected in greater horseshoe bats, and El Hamdania represents a newly confirmed locality for their geographical distribution. This study provides a foundational contribution to the parasitic fauna of bats in Algeria and lays the groundwork for future research. Such work could explore faunistic, epizootiological and biocenotic aspects, which offers valuable insights into regional and local biodiversity, as well as the intricate relationships within these ecosystems (Altringham, Reference Altringham2011; Fenton and Simmons, Reference Fenton and Simmons2014).

Conclusion

This study provides new data on the ectoparasite communities associated with cave-dwelling bats in CNP, together with supplementary coprological observations on endoparasite traces in guano. The findings should be interpreted in light of the methodological limitations inherent to the coprological approach, which yields only qualitative, fragmentary data and does not permit detection of trematodes or estimation of parasite burdens. Among the bat species captured in the Chiffa Tunnel (El Hamdania region), R. blasii (Blasius’ horseshoe bat) was the most abundant, followed by R. ferrumequinum (greater horseshoe bat) and N. leisleri (Leisler’s noctule), the latter newly reported in CNP.

Data availability statement

The datasets used and analysed during the current study are available from the corresponding author on reasonable request.

Acknowledgements

This work could not have been carried out without the help of Mr Ramdane Dehal (Director of the Chrea National Park ‘CNP’, Algeria), Mrs Salima Rahmouni (Veterinary Inspector at CNP), Mr Reda El-Ferroudji (Head of the El Hamdania Sector, CNP) and his team. We thank Prof Amel Milla (Higher National Veterinary School, Algiers) for her availability and the laboratory technician Mr Khaled Dalil for his help at the Zoology Laboratory of the Higher National Veterinary School.

Author contributions

Djamel Bendjoudi (conceptualization, methodology, investigation, data curation, resources, writing – original draft, writing – review & editing). Faiza Marniche (conceptualization, methodology, data curation, resources, writing – original draft). Sarah Banat (investigation). Hichem Zaoui (investigation). Haroun Chenchouni (visualization, writing – review & editing).

Financial support

This study was not funded by any source.

Competing interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical standards

The study received approval from the Scientific Committee of the Faculty of Nature and Life Sciences at the University of Blida 1 in Algeria. All procedures were conducted in accordance with the standards and regulations established by the Ethics Committee of the SNV Faculty. Additionally, the study adhered to the Animal Research: Reporting of In Vivo Experiments (ARRIVE) guidelines, and the U.K. Animals Act 1986 guidelines.

Statement of animal rights

No animal suffered during the course of the studied. All the animal studies were conducted with the utmost regard for animal welfare, and all animal rights issues were appropriately observed.

References

Aellen, V (1955) Rhinolophus blasii Peters, 1866: Chauve-souris nouvelle pour l’Afrique du Nord. Mammalia 19, 361–366. https://doi.org/10.1515/mamm.1955.19.3.361.Google Scholar
Aggrey, S, Rwego, IB, Sande, E, Khayiyi, JD, Kityo, RM, Masembe, C and Kading, RC (2024) Socioeconomic benefits associated with bats. Journal of Ethnobiology and Ethnomedicine 20, 78. https://doi.org/10.1186/s13002-024-00720-w.Google Scholar
Ahmim, M (2013) Presence of a small population of polecat-like mustelid in North Algeria: Potentially the wild progenitor of domestic ferret (Mustela putorius furo). Small Carnivore Conservation 48, 87–88.Google Scholar
Ahmim, M (2017) Current status, distribution, and conservation status of Algerian bats (Mammalia: Chiroptera). Journal of Threatened Taxa 9(1), 9723–9733. https://doi.org/10.11609/jott.2576.9.1.9723-9733.Google Scholar
Ahmim, M (2019) Les mammifères sauvages d’Algérie: Répartition et biologie de la conservation. Les Editions du Net. https://hal.archives-ouvertes.fr/hal-02375326.Google Scholar
Albayrak, I (2003) The bats of the eastern Black Sea region in Turkey (Mammalia: Chiroptera). Turkish Journal of Zoology 27(4), 269–273.https://journals.tubitak.gov.tr/zoology/vol27/iss4/2.Google Scholar
Allocati, N, Petrucci, AG, Di Giovanni, P, Masulli, M, Di Ilio, C and De Laurenzi, V (2016) Bat–man disease transmission: Zoonotic pathogens from wildlife reservoirs to human populations. Cell Death Discovery 2, 16048. https://doi.org/10.1038/cddiscovery.2016.48.Google Scholar
Altringham, JD (2011) Bats: From Evolution to Conservation, 2nd Edn. New York: Oxford University Press.Google Scholar
Amr, ZS and Qumsiyeh, MB (1993) Records of bat flies from Jordan, Libya, and Algeria. Entomological News 104(1), 43–46.Google Scholar
Anciaux de Faveaux, M (1965) Les parasites des chiroptères: Rôle épidémiologique chez les animaux et l’homme au Katanga. Annales de Parasitologie 40(1), 21–38. https://doi.org/10.1051/parasite/1965401021.Google Scholar
Anciaux de Faveaux, M (1976) Distribution des chiroptères en Algérie: Avec notes écologiques et parasitologie. 80 pGoogle Scholar
Anderson, RC, Chabaud, AG and Willmott, S (2009) Keys to the Nematode Parasites of Vertebrates: Archival Volume. Wallingford: CAB International.Google Scholar
Arthur, DR (1956) The Ixodes ticks of Chiroptera (Ixodoidea: Ixodidae). Journal of Parasitology 42, 180. https://doi.org/10.2307/3274734.Google Scholar
Attia-Hili, R (2015) Les ectoparasites des chiroptères: Taxinomie et relations hôte-parasite. Master thesis, Tunisia: Univ. Sfaxx.Google Scholar
Aulagnier, S, Haffner, P, Mitchell-Jones, AJ and Moutou, F (2017) Mammifères d’Europe, d’Afrique du Nord et du Moyen-Orient: Guide Delachaux. Paris: Delachaux et Niestlé.Google Scholar
Bain, O (1966) Diversité et étroite spécificité parasitaire des Filaires de chauves-souris, confondues sous le nom de Litomosa filaria (Van Beneden, 1872). Bulletin du Museum National d’Histoire Naturelle 38, 928–939.Google Scholar
Beaucournu, JC and Noblet, JF (1996) Les diptères pupipares parasites de chauves-souris dans les Alpes et les Préalpes françaises (Diptera: Streblidae et Nycteribiidae). Bulletin de la Société Entomologique de France 101(3), 235–240.Google Scholar
Benda, P, Červený, J, Konečný, A, Reiter, A, Ševčík, M, Uhrin, M and Vallo, P (2010) Some new records of bats from Morocco (Chiroptera). Lynx (Praha) 41, 151–166.Google Scholar
Benda, P, Ruedi, M and Aulagnier, S (2004) New data on the distribution of bats (Chiroptera) in Morocco. Vespertilio 8, 13–44. https://www.ceson.org/vespertilio/8/8_02.pdf.Google Scholar
Benda, P, Spitzenberger, F, Hanák, V, Andreas, M, Reiter, A, Ševčík, M, Šmíd, J and Uhrin, M (2014) Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 11. On the bat fauna of Libya II. Acta Societatis Zoologicae Bohemicae 78, 1–162.Google Scholar
Bendjeddou, ML, Bitam, I, Abiadh, A, Bouslama, Z and Amr, ZS (2013) New records of arthropod ectoparasites of bats from north-eastern Algeria. Jordan Journal of Biological Sciences 6, 324–327.Google Scholar
Bendjeddou, ML, Bouslama, Z, Amr, ZS and Bani Hani, R (2016) Infestation and seasonal activity of Ixodes vespertilionis Koch, 1844 (Acari: Ixodidae) on the Maghreb Mouse-Eared Bat (Myotis punicus (Felten, 1977)) in northeastern Algeria. Journal of Vector Ecology 41, 110–113. https://doi.org/10.1111/jvec.12201.Google Scholar
Bendjeddou, ML, Khelfaoui, F, Abiadh, A, Mechouk, N, Mihalca, AD and Sándor, AD (2024) Bat ectoparasites (Acari, Diptera, Hemiptera, Siphonaptera) in the Grand Maghreb (Algeria, Libya, Mauritania, Morocco and Tunisia): A literature review and new data. Acta Parasitologica 69(1), 106–120. https://doi.org/10.1007/s11686-023-00732-8.Google Scholar
Bendjeddou, ML, Loumassine, HA, Scheffler, I, Bouslama, Z and Amr, Z (2017) Bat ectoparasites (Nycteribiidae, Streblidae, Siphonaptera, Heteroptera, Mesostigmata, Argasidae, and Ixodidae) from Algeria. Journal of Vector Ecology 42, 13–23. https://doi.org/10.1111/jvec.12235.Google Scholar
Bendjoudi, D, Marniche, F, Takdjout, L, Epalanga, M and Chenchouni, H (2023) Copro-parasitological survey of striped hyena (Hyaena hyaena), African golden Wolf (Canis lupaster), and red Fox (Vulpes vulpes) in Algeria. Euro-Mediterranean Journal for Environmental Integration 8(3), 691–703. https://doi.org/10.1007/s41207-023-00388-w.Google Scholar
Bendjoudi, D, Yedou, W, Beneldjouzi, A, Mechouk, N and Bendjeddou, ML (2019) On bat ectoparasites (Nycteribidae, Streblidae, Siphonaptera, Mesostigmata, and Ixodidae) from Chréa National Park (central parts of the Atlas Mountains), Algeria. Bulletin de la Société Zoologique de France 144(2), 63–72.Google Scholar
Bitam, I, Dittmar, K, Parola, P, Whiting, MF and Raoult, D (2010) Fleas and flea-borne diseases. International Journal of Infectious Diseases 14, 667–676. https://doi.org/10.1016/j.ijid.2009.11.011.Google Scholar
BNEF (Bureau National des Etudes Forestières) (1984) Étude du milieu du Parc National de Chréa. Blida: BNEF.Google Scholar
Bray, RA, Gibson, DI and Jones, A (2008) Keys to the Trematoda (Vol. 3). London: CABI Publishing and the Natural History Museum. https://doi.org/10.1079/9780851995885.0000.Google Scholar
Burazerović, J, Ćakić, S, Mihaljica, D, Sukara, R, Ćirović, D and Tomanović, S (2015) Ticks (Acari: Argasidae, Ixodidae) parasitizing bats in the central Balkans. Experimental and Applied Acarology 66, 281–291. https://doi.org/10.1007/s10493-015-9891-6.Google Scholar
Burgin, CJ, Colella, JP, Kahn, PL and Upham, NS (2018) How many species of mammals are there? Journal of Mammalogy 99, 1–14. https://doi.org/10.1093/jmammal/gyx147.Google Scholar
Camilotti, VL, Graciolli, G, Weber, MW, Arruda, JLS and Cáceres, NC (2010) Batflies from the deciduous Atlantic Forest in southern Brazil: Host-parasite relationships and parasitism rates. Acta Parasitologica 55(2), 194–200. https://doi.org/10.2478/s11686-010-0026-2.Google Scholar
Combes, C and Clerc, B (1970) Recherches éco-parasitologiques sur l’helminthofaune des Chiroptères dans l’est des Pyrénées. Annales de Parasitologie 45(5), 537–561. https://doi.org/10.1051/parasite/1970455537.Google Scholar
Dick, CW and Patterson, BD (2007) Against all odds: Explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37(8–9), 871–876. https://doi.org/10.1016/j.ijpara.2007.02.004.Google Scholar
Dietz, C (2005) Illustrated identification key to the bats of Egypt. Electronic publication (Version 1.0), 1–37.Google Scholar
Dietz, C and von Helversen, O (2004) Illustrated identification key to the bats of Europe (Version 1.0). Electronic publication. https://www.mammalwatching.com/Palearctic/Otherreports/batkey.pdf.Google Scholar
Dusbabek, F (1962) Parasitische Fledermausmilben der Tschechoslowakei I. Fam. Spinturnicidae Oudms., 1901 (Acarina, Gamasides). Acta Societatis Entomologicae Czechoslovaniae 59(4), 357–379.Google Scholar
El Guamri, Y, Belghity, D, Achicha, A, Tiabi, M, Aujjar, N, Barkia, A, et al (2009) Enquête épidémiologique rétrospective sur les parasitoses intestinales au Centre hospitalier provincial El Idrissi (Kénitra, Maroc): Bilan de 10 ans (1996–2005). Annales de Biologie Clinique 67(2), 191–202. https://doi.org/10.1684/abc.2009.0313.Google Scholar
El Ibrahimi, S and Idrissi, HR (2015) Nouveau bilan de connaissances des chauves-souris au Maroc. In 11e Rencontres Bourgogne-Nature et 37e Colloque francophone de Mammalogie Les Mammifères sauvages - Recolonisation et réémergence. Revue Scientifique Bourgogne-Nature 21–22, 359–368.Google Scholar
Esteban, JG, Botella, P and Toledo, R (1999) Helminth fauna of bats in Spain IV. Parasites of Rhinolophus ferrumequinum (Chiroptera: Rhinolophidae). Research and Reviews in Parasitology 59(1–2), 57–68.Google Scholar
Esteban, JG, Oltra-Ferrero, JL, Botella, P and Mas-Coma, S (1991) Helmintos de quiropteros en España: Espectro faunístico e interés aplicado de su estudio. In J Benzal and O de Paz (eds), Los Murciélagos de España y Portugal. Madrid: ICONA, Ministerio de Agricultura, Pesca y Alimentación, pp. 280–304Google Scholar
Fenton, MB and Simmons, NB (2014) Bats: A World of Science and Mystery. Chicago, IL, USA: The University of Chicago Press.Google Scholar
Frank, R, Kuhn, T, Werblow, A, Liston, A, Kochmann, J and Klimpel, S (2015) Parasite diversity of European Myotis species with special emphasis on Myotis myotis (Microchiroptera, Vespertilionidae) from a typical nursery roost. Parasites & Vectors 8, 101–114. https://doi.org/10.1186/s13071-015-0726-7.Google Scholar
Gaisler, J (1983) Nouvelles données sur les Chiroptères du Nord Algérien. Mammalia 47(3), 360–369. https://doi.org/10.1515/mamm-1983-0308.Google Scholar
Gaisler, J and Kowalski, K (1986) Results of the netting of bats in Algeria (Mammalia: Chiroptera). Věstník Československé Společnosti Zoologické 50(3), 161–173.Google Scholar
Gardner, SI and Jiménez-Ruiz, A (2009) Methods for the study of bat endoparasites. In TH Kunz and S Parsons (eds), Ecological and Behavioral Methods for the Study of Bats. Baltimore, Maryland: Johns Hopkins University Press, pp. 795–805.Google Scholar
Hadjouti, R and Mamouni, I (2016) Contribution au répertoire des agents microbiens et à l’inventaire des ectoparasites des chauves-souris de la région nord de la wilaya de Bouira. Master Dissertation. Algeria: University of Boumerdes.Google Scholar
Hanak, V and Gaisler, J (1983) Nyctalus leisleri (Kühl, 1818): Une espèce nouvelle pour le continent africain. Mammalia 47(4), 585–587.Google Scholar
Hendrix, CM and Robinson, N (2023) Diagnostic Parasitology for Veterinary Technicians, 6th Edn. St. Louis, MO: Mosby Inc., Elsevier Inc.Google Scholar
Holmes, RT (1966) Breeding ecology and annual cycle adaptations of the red-backed sandpiper (Calidris alpina) in northern Alaska. The Condor 68(1), 3–46. https://doi.org/10.2307/1365381.Google Scholar
Hopkins, GH and Rothschild, M (1956) An Illustrated Catalogue of Rothschild Collection of Fleas (Siphonaptera) in the British Museum (Natural History. Vol. II. London: The Trustees of the British Museum.Google Scholar
Hornok, S, Kontschán, J, Kovács, R, Angyal, D, Görföl, T, Polacsek, Z, Kalmár, Z and Mihalca, AD (2014) Bat ticks revisited: Ixodes ariadnae sp. nov. and allopatric genotypes of I. vespertilionis in caves of Hungary. Parasites & Vectors 7, 202. https://doi.org/10.1186/1756-3305-7-202.Google Scholar
Horvat, Ž, Čabrilo, B, Paunović, M, Karapandža, B, Jovanović, J, Budinski, I and Čabrilo, OB (2015) The helminth fauna of the greater horseshoe bat (Rhinolophus ferrumequinum) (Chiroptera: Rhinolophidae) on the territory of Serbia. Biologia Serbica 37(1–2), 64–67.Google Scholar
Hůrka, K (1962) Beitrag zu Nycteribiden- und Streblidenfauna Albaniens nebst Bemerkungen zur Fauna von Bulgarien, Ungarn und UdSSR. Časopis Československé Společnosti Entomologicé 59, 156–164.Google Scholar
Hůrka, K (1964) Distribution, bionomy and ecology of the European bat flies with special regard to the Czechoslovak fauna (Diptera, Nycteribidae). Acta Universitatis Carolinae: Biologica 1964, 167–231.Google Scholar
Hůrka, K (1982) On the insect bat ectoparasites of coastal Libya (Cimicidae, Nycteribiidae, Streblidae, Ischnopsyllidae). Věstník Československé Společnosti Zoologické 46(2), 85–91.Google Scholar
Hutson, AM, Mickleburgh, SP and Racey, PA (2001) Microchiropteran bats: Global status survey and conservation action plan. Gland, Switzerland Cambridge, UK: Species Survival Commission Chiroptera Specialist Group, IUCN. https://doi.org/10.2305/IUCN.CH.2001.SSC-AP.1.en.Google Scholar
Imaz, E, Aihartza, JR and Totorika, MJ (1999) Ectoparasites on bats (Gamasida, Ixodida, Diptera) in Biscay (Northern Iberian Peninsula). Miscel·lània Zoològica 22(2), 21–30.Google Scholar
Khelfaoui, F, Kebaci, A and Benyacoub, S (2018) New data on Insecta and Acarina parasitizing bats (Mammalia: Chiroptera) in Numidia, Eastern Algeria. Bulletin de la Société Zoologique de France 143(2), 63–73.Google Scholar
Klimpel, S and Mehlhorn, H (2014) Bats (Chiroptera) as Vectors of Diseases and Parasites: Facts and Myths (Vol. 5). Parasitology Research Monographs, Berlin, Heidelberg: Springer. https://doi.org/10.1007/978-3-642-39333-4Google Scholar
Kolonin, GV (2007) Mammals as hosts of ixodid ticks (Acarina: Ixodidae). Entomological Review 87(4), 401–412. https://doi.org/10.1134/S0013873807040033.Google Scholar
Krištofík, J and Danko, Š (2012) Arthropod ectoparasites (Acarina, Heteroptera, Diptera, Siphonaptera) of bats in Slovakia. Vespertilio 16, 167–189. https://ceson.org/vespertilio/16/167_189_Kristofik.pdf.Google Scholar
Kunz, TH and Kurta, A (1988) Capture methods and holding devices. In Kunz, TH (ed.), Ecological and Behavioral Methods for the Study of Bats. Washington, DC: Smithsonian Institution Press, pp. 1–30.Google Scholar
Léger, C (2019) Les parasites métazoaires des chiroptères en Lorraine (Acari, Anoplura, Cestoda, Diptera, Hemiptera, Nematoda, Siphonaptera): état des lieux bibliographique (1862–2018) et nouvelles observations. Neuves-Maisons: CPEPESC Lorraine Publications.Google Scholar
Letko, M, Seifert, SN, Olival, KJ, Plowright, RK and Munster, VJ (2020) Bat-borne virus diversity, spillover, and emergence. Nature Reviews Microbiology 18, 461–471. https://doi.org/10.1038/s41579-020-0394-z.Google Scholar
Leulmi, H, Aouadi, A, Bitam, I, Bessas, A, Benakhla, A, Raoult, D and Parola, P (2016) Detection of Bartonella tamiae, Coxiella burnetii, and rickettsiae in arthropods and tissues from wild and domestic animals in northeastern Algeria. Parasites & Vectors 9, 27. https://doi.org/10.1186/s13071-016-1316-9.Google Scholar
Margolis, L, Esch, GW, Holmes, JC, Kuris, AM and Schad, GA (1982) The use of ecological terms in parasitology: Report of an ad hoc committee of the American Society of Parasitologists. The Journal of Parasitology 68(1), 131–133. https://doi.org/10.2307/3281335.Google Scholar
Meddour, R (2002) Bioclimats étages et séries de végétation de l’Atlas Blidéen (Algérie). Phytocoenologia 32(1), 101–128. https://doi.org/10.1127/0340-269X/2002/0032-0101.Google Scholar
Messenger, SL, Rupprecht, C and Smith, C (2003) Bats, emerging virus infections, and the rabies paradigm. In Kunz, TH and Fenton, MB (eds.), Bat Ecology. Chicago, IL, USA: The University of Chicago Press, pp. 79–622.Google Scholar
Mészáros, F (1971) Vizsgalatok a hazai deneverek előskodő fonalfergein (Nematoda): [Investigation on nematodes of Hungarian bats]. Állattani Közlemények 58(1–4), 78–86.Google Scholar
Mitchell-Jones, AJ and Robertson, CJ (2004) Bats and the law. In Mitchell-Jones, AJ and McLeish, AP (eds.), Bat Worker’s Manual, 3rd Edn. Peterborough, UK: Joint Nature Conservation Committee, pp. 11–22.Google Scholar
Mituch, J (1964) Nález trematóda Plagiorchis (Plagiorchis) amplehaustoria sp. nov. z netopierov (Chiroptera) zo Slovenska. Biologia 19(2), 122–125.Google Scholar
Morand, CMEH (2014) La punaise de lit (Cimex lenticularus): Résurgence d’un nuisible. Doctoral thesis. École Nationale Vétérinaire d’Alfort.Google Scholar
Morse, SF, Olival, KJ, Kosoy, M, Billeter, S, Patterson, BD, Dick, CW and Dittmar, K (2012) Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea: Streblidae, Nycteribiidae). Infection Genetics and Evolution 12(8), 1717–1723. https://doi.org/10.1016/j.meegid.2012.06.009.Google Scholar
Mühldorfer, K, Speck, S, Kurth, A, Lesnik, R, Freuling, C, Müller, T, Kramer-Schadt, S and Wibbelt, G (2011) Diseases and causes of death in European bats: Dynamics in disease susceptibility and infection rates. PLoS ONE 6(12), e29773. https://doi.org/10.1371/journal.pone.0029773.Google Scholar
Nader, IA and Kock, D (1983) Notes on Some Bats from the near East (Mammalia: Chiroptera). Frankfurt: Forschungsinstitut Senckenberg.Google Scholar
Orlova, MV (2011) Ectoparasite associations of bats from the Urals (Russia). Hystrix, the Italian Journal of Mammalogy 22(1), 105–110. https://doi.org/10.4404/hystrix-22.1-4470.Google Scholar
Orlova, MV (2013) Ectoparasites of the particolored bat (Vespertilio murinus Linnaeus, 1758, Chiroptera, Mammalia) in the Urals and adjacent regions. Entomological Review 93(9), 1236–1242. https://doi.org/10.1134/S0013873813090169.Google Scholar
Patterson, BD, Dick, CW and Dittmar, K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23, 177–189. https://doi.org/10.1017/S0266467406003816.Google Scholar
Radovsky, FJ (1967) The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic in bats. University of California Publications in Entomology 46, 1–288.Google Scholar
Ricci, M (1995) Report on trematode parasites of bats in Italy. Parasitologia 37(2–3), 199–214.Google Scholar
Rose, E (2006) Grand Rhinolophe fer à cheval – Rhinolophus ferrumequinum. Gland, Switzerland: World Wide Fund for Nature (WWF).Google Scholar
Rotrou, M (1939) La grotte de la Tafna: Historique, description, faune. Bulletin de la Société d’Histoire Naturelle d’Alger 80, 399–408.Google Scholar
Rózsa, L, Reiczigel, J and Majoros, G (2000) Quantifying parasites in samples of hosts. Journal of Parasitology 86(2), 228–232. https://doi.org/10.1645/0022-3395(2000)086[0228:qpisoh]2.0.co;2.Google Scholar
Rudnick, A (1960) A revision of the mites of the family Spinturnicidae (Acarina). University of California Publications in Entomology 17(2), 157–283.Google Scholar
Scaravelli, D, Priori, P and Georgiakakis, P (2014) Brachytarsinia flavipennis (Diptera: Streblidae) on Rhinolophus blasii (Mammalia: Rhinolophidae) in the Island of Crete. Natura Rerum 3, 35–36.Google Scholar
Scheffler, I, Dolch, D, Ariunbold, J, Stubbe, A, Abraham, A and Thiele, K (2012) Ectoparasites of Bats in Mongolia, Part 2 (Ischnopsyllidae, Nycteribiidae, Cimicidae, and Acari). Exploration into the Biological Resources of Mongolia, Institut für Biologie der Martin-Luther-Universität Halle-Wittenberg. https://core.ac.uk/download/33148092.pdfGoogle Scholar
Ševčík, M, Benda, P and Lucan, RK (2013) Diptera Pupipara from bats of two large eastern Mediterranean islands, Crete and Cyprus. Turkish Journal of Zoology 37(1), 31–37. https://doi.org/10.3906/zoo-1112-20.Google Scholar
Singh, P, Barolia, SK and Sharma, DK (2015) Identification, Isolation and Characterization of Enterococcus species (Gen Bank Accession No: KF777815) from Fecal Contents of Pteropus giganteus. International Journal of Current Microbiology and Applied Sciences 4(3), 143–149.Google Scholar
Sivajothi, S, Reddy, BS and Rayulu, VC (2014) Intestinal coccidiosis infection in domestic rabbits. International Journal of Biological Research 2(2), 48–50. https://doi.org/10.14419/ijbr.v2i2.2540.Google Scholar
Smith, I and Wang, LF (2012) Bats and their virome: An important source of emerging viruses capable of infecting humans. Current Opinion in Virology 3(1), 84–91. https://doi.org/10.1016/j.coviro.2012.11.006.Google Scholar
Sonin, MD (1975) Osnovi nematologii [The Basics of Nematology]. Moscow: Akademii Nauk SSSR.Google Scholar
Sponchiado, J, Melo, GL, Martins, TF, Krawczak, FS, Labruna, MB and Căcere, NC (2015) Association patterns of ticks (Acari: Ixodida: Ixodidae, Argasidae) of small mammals in Cerrado fragments, western Brazil. Experimental and Applied Acarology 65(3), 389–401. https://doi.org/10.1007/s10493-014-9877-9.Google Scholar
Stanyukovich, MK (1997) Keys to the gamasid mites (Acari: Parasitiformes: Mesostigmata: Macronyssoidea and Laelaptoidea) parasitizing bats (Mammalia: Chiroptera) from Russia and adjacent countries. Rudolf Natschinsky School 7, 13–46.Google Scholar
Ter Hofstede, HM and Fenton, MB (2005) Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. Journal of Zoology 266(1), 333–340. https://doi.org/10.1017/S095283690500693X.Google Scholar
Theodor, O (1967) An Illustrated Catalogue of the Rothschild Collection of Nycteribiidae (Diptera) in the British Museum (Natural History). London: Whitefriars Press Ltd.Google Scholar
Theodor, O and Moscona, A (1954) On the bat parasites in Palestine I. Nycteribiidae, Streblidae, Hemiptera, Siphonaptera. Parasitology 44, 157–245. https://doi.org/10.1017/S0031182000018862.Google Scholar
Theodorides, J (1953) Contribution à l’étude des parasites et phorétiques de Coléoptères terrestres. Doctoral dissertation. Paris: Faculty of Science.Google Scholar
Tsai, YL, Chang, CC, Chuang, ST and Chomel, BB (2011) Bartonella species and their ectoparasites: Selective host adaptation or strain selection between the vector and the mammalian host? Comparative Immunology, Microbiology & Infectious Diseases 34(4), 299–314. https://doi.org/10.1016/j.cimid.2011.04.005.Google Scholar
Vermeil, C (1960) Contribution à l’étude des Nycteribiidae et des Streblidae (Diptera, Pupipara) de Tunisie. Parasite 35, 573–577. https://doi.org/10.1051/parasite/1960355737.Google Scholar
Walker, EP, Warnick, F, Lange, KI, Uible, HE, Hamlet, SE, Davis, MA and Wright, PE (1964) Mammals of the World (Vol. 1). Baltimore: Johns Hopkins Press, i–xlviii, 1644.Google Scholar
Walter, VG and Ebenau, C (1997) Nachweise von Fledermausfliegen aus Syrien (Diptera: Streblidae, Nycteribiidae). Zoology in the Middle East 14(1), 115–119. https://doi.org/10.1080/09397140.1997.10637712.Google Scholar
Webber, QMR and Willis, CKR (2016) Sociality, parasites, and pathogens in bats. In Ortega, J (ed), Sociality in Bats. Cham: Springer, pp. 105–139.Google Scholar
Wibbelt, G, Moore, MS, Schountz, T and Voigt, CC (2010) Emerging diseases in Chiroptera: Why bats? Biology Letters 6(4), 438–440. https://doi.org/10.1098/rsbl.2010.0267.Google Scholar
Yeddou, W and Lammari, A (2017) Contribution à l’étude des ectoparasites des Chiroptères dans le secteur d’El Hamdania (Parc National de Chréa). Master dissertation. Algeria: University of Blida.Google Scholar
Zajac, AM, Conboy, GA, Little, SE and Reichard, MV (2021) Veterinary Clinical Parasitology, 9th Edn. Chichester, West Sussex, UK: Wiley-Blackwell.Google Scholar
Figure 0

Figure 1. Vegetation map and geographic location of Chrea National Park in Algeria.Figure 1 long description.

Figure 1

Figure 2. Photos of Chiffa Tunnel at the Chrea National Park in Algeria. Left: outside the tunnel, right: inside the tunnel, near the entrance.Figure 2 long description.

Figure 2

Figure 3. Capture bats with a hand net.Figure 3 long description.

Figure 3

Figure 4. Bat species found in the Chiffa tunnel around the Chrea National Park. (A) Leisler’s Noctule Nyctalus leisleri, (B) Blasius’s horseshoe bat Rhinolophus blasii, and (C) greater horseshoe bat Rhinolophus ferrumequinum.Figure 4 long description.

Figure 4

Figure 5. Microscopic views (40× magnification) of Nycteribia (Listropoda) schmidlii schmidlii Schiner, 1853 (Diptera: Nycteribiidae): (A) female ventral view; (B) male ventral view; (C) male ventral extremity; (D) dorsal view of Nycteribosca africana = Brachytarsina (Brachytarsina) flavipennis Macquart, 1851 (Diptera: Streblidae) and (E) ventral view of Phthiridium biarticulatum (Diptera: Nycteribiidae) Hermann, 1804.Figure 5 long description.

Figure 5

Figure 6. Alluvial plot illustrating the distribution of dipteran ectoparasites across their bat hosts. The proportions (%) are relative abundances.Figure 6 long description.

Figure 6

Table 1. Inventory and abundance of parasites found in bat guanos studied in Chrea National ParkTable 1 long description.

Figure 7

Figure 7. Parasites found in bat guanos observed under light microscope at 40× magnification. (A) Non-embryonated egg of Strongylacantha sp.; (B) embryonated egg of Rhabditida sp.; (C) larva Rhabditida sp.; (D) egg of Milina (Hymenolepis) sp.; (E) egg Acari and (F) adult Alabidocarpus sp.Figure 7 long description.

Figure 8

Table 2. Abundance (A), positivity index (P+) and prevalence of parasites found in bat guanos studied in Chrea National Park (Algeria)Table 2 long description.