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Phylogenetic relationships of a novel bat fly species infesting the geographically widespread Old World fruit bat, Rousettus leschenaultii, in Southern Asia

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Abstract

The global epidemiological significance of bats and their blood-sucking ectoparasites is increasingly recognized. However, relevant data are scarce from Pakistan where the Palearctic and Oriental zoogeographic regions meet. In this study, 200 bats belonging to five species were examined for the presence of ectoparasites in Pakistan. Bat flies were found only on Leschenault’s fruit bat (Rousettus leschenaultii). The prevalence of infestation did not correlate with habitat type and host traits including age, reproductive status, and sex. All bat flies represented the same Eucampsipoda species which was shown to be morphologically different from all species of its genus with known south Asian distribution and belonged to a separate phylogenetic group. These results highlight the existence of a hitherto undescribed bat fly species in southern Asia, which is not shared by the fruit bat species (R. leschenaultii) and insectivorous ones (e.g., Rhinopoma microphyllum) thus probably playing a role only in intraspecific transmission of pathogens.

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References

  • Akhtar N, Saeed K, Khan S (2014) Current status of mammals in district Buner Khyber Pakhtunkhwa, Pakistan. Int J Mol Evol Biodiversity 1:1–5

    Google Scholar 

  • Attaullah AS, Javid A, Imran M, Khan TM, Phelps K, Olival KJ (2022) Knowledge, perceptions, and attitudes by residents in Punjab and Khyber Pakhtunkhwa, Pakistan in connection with bats. J Ethnobiol Ethnomed 18:10–10

    Article  Google Scholar 

  • Azhar I, Khan FAA, Ismail N, Abdullah MT (2015) Checklist of bat flies (Diptera: Nycteribiidae and Streblidae) and their associated bat hosts in Malaysia. Check List 11:1–12

    Article  Google Scholar 

  • Bai Y, Kosoy M, Recuenco S, Alvarez D, Moran D, Turmelle A, Ellison J, Garcia DL, Estevez A, Lindblade K, Rupprecht C (2011) Bartonella spp. in Bats, Guatemala. Emerg Infect Dis 17:1269–1272

    Article  PubMed  PubMed Central  Google Scholar 

  • Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83: 575-583

  • Çetin H, Coşkun G, Dick CW (2020) Ectoparasitic Bat Flies (Eucampsipodahyrtlii) Detected on the Egyptian Fruit Bat (Rousettusaegyptiacus) in Antalya. Turkey Turkiye Parazitol Derg 44:115–117

    Article  PubMed  Google Scholar 

  • Combes C (2001) Parasitism. The ecology and evolution of intimate interactions. Chicago: University of Chicago Press 699.

  • Dick CW (2007) High host specificity of obligate ectoparasites. Ecol Entomol 32:446–450

    Article  Google Scholar 

  • Dick CW, Patterson BD (2006) Bat flies: obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and Macroparasites. Springer, New York NY USA, pp 179–194

    Chapter  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Fritz GN (1983) Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. J Med Entomol 20:1–10

    Article  CAS  PubMed  Google Scholar 

  • Ikeda P, Marinho Torres J, Perles L, Lourenço EC, Herrera HM, de Oliveira CE, Zacarias Machado R, André MR (2020) Intra- and inter-host assessment of Bartonella diversity with focus on non-hematophagous bats and associated ectoparasites from Brazil. Microorganisms 8:1822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen van Vuren P, Wiley M, Palacios G, Storm N, McCulloch S, Markotter W, Birkhead M, Kemp A, Paweska JT (2016) Isolation of a novel Fusogenic Orthoreovirus from Eucampsipodaafricana Bat Flies in South Africa. Viruses 8:65

    Article  PubMed  PubMed Central  Google Scholar 

  • Jansen van Vuren P, Wiley MR, Palacios G, Storm N, Markotter W, Birkhead M, Kemp A, Paweska JT (2017) Isolation of a novel orthobunyavirus from bat flies (Eucampsipodaafricana). J Gen Virol 98:935–945

    Article  PubMed  PubMed Central  Google Scholar 

  • Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endangered Species Res 8:93–115

    Article  Google Scholar 

  • Khan W, Nisa NN, Ullah S, Rehbar B, Ahmad S, Siyal GB, Ahmad A, Khalid S, Zada K, Ullah N (2020) Morphology and ectoparasite spectrum of Pteropusvampyrus (the flying fox) in different parts of Malakand Division, Pakistan. Braz J Biol 80:523–528

    Article  CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7 Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwiecinski GG, Griffiths TA (1999) Rousettus Aegyptiacus Mamm Species 611:1–9

    Google Scholar 

  • Lei BR, Olival KJ (2014) Contrasting patterns in mammal-bacteria coevolution: Bartonella and Leptospira in bats and rodents. PLoS Negl Trop Dis 8:2738

    Article  Google Scholar 

  • Loftis AD, Gill JS, Schriefer ME, Levin ML, Eremeeva ME, Gilchrist MJ, Dasch GA (2005) Detection of Rickettsia, Borrelia, and Bartonella in Carioskelleyi (Acari: Argasidae). J Med Entomol 42:473–480

    CAS  PubMed  Google Scholar 

  • Lučan RK, Bartonička T, Jedlička P, Řeřucha S, Šálek M, Čížek M, Nicolaou H, Horáček I (2016) Spatial activity and feeding ecology of the endangered northern population of the Egyptian fruit bat (Rousettusaegyptiacus). J Mammal 97:815–822

    Article  Google Scholar 

  • Maa T (1971) Revision of the Australian bat flies. Pac Insects Monogr 28:1–118

    Google Scholar 

  • Mahmood-ul-Hassan M, Jones G, Dietz C (2009) the bats of Pakistan – the least known mammals. Saarbrücken, Germany: Verlag Dr. Muller 168

  • Morse SF, Olival KJ, Kosoy M, Billeter S, Patterson BD, Dick CW, Dittmar K (2012) Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infect Genet Evol 12:1717–1723

    Article  PubMed  Google Scholar 

  • Nordin J, Chew TH, Lim LS, Shamsir MS (2021) Temporal changes of bat diversity in the urban habitat island of Batu Caves, Malaysia. Conf Ser Earth Environ Sci 736:012–051

    Google Scholar 

  • Obame-Nkoghe J, Rahola N, Bourgarel M, Yangari P, Prugnolle F, Maganga GD, Leroy EM, Fontenille D, Ayala D, Paupy C (2016) Bat flies (Diptera: Nycteribiidae and Streblidae) infesting cave-dwelling bats in Gabon: diversity, dynamics and potential role in Polychromophilusmelanipherus transmission. Parasit Vectors 9:333

    Article  PubMed  PubMed Central  Google Scholar 

  • Patterson BD, Dick CW, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23:177–189

    Article  Google Scholar 

  • Perveen F, Faiz-ur R (2015) Characteristics of the first record of bat (Mammalia: Chiroptera) fauna from Peshawar and adjacent areas, Khyber Pakhtunkhwa. Pakistan Global J Anim Sci Res 3:148–160

    Google Scholar 

  • Perveen F, Rahman F (2012) Checklist of first recorded bats species in Peshawar and adjacent areas, Khyber Pakhtunkhwa. Int J Farm Allied Sci 1:97–100

    Google Scholar 

  • Postawa T, Nagy Z (2016) Variation of parasitism patterns in bats during hibernation: the effect of host species, resources, health status, and hibernation period. Parasitol Res 115:3767–3778

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu Y, Kajihara M, Nakao R, Mulenga E, Harima H, Hang’ombe BM, Eto Y, Changula K, Mwizabi D, Sawa H, Higashi H, Mweene A, Takada A, Simuunza M, Sugimoto C (2020) Isolation of Candidatus Bartonella rousetti and other bat-associated Bartonellae from bats and their flies in Zambia. Pathogens 9:469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramanantsalama RV, Goodman SM, Dietrich M (2022) Lebarbenchon, C. Interaction between Old World fruit bats and humans: from large scale ecosystem services to zoonotic diseases. Acta Trop 231:2–18

    Article  Google Scholar 

  • Reeves WR, Lloyd JE (2019) Louse Flies, Keds, and Bat Flies (Hippoboscoidea). In Medical and Veterinary Entomology, 3rd ed Mullen GR, Durden LA, Eds Academic Press London UK pp 421–438.

  • Samoh A, Pantip V, Soisook PA (2021) Checklist of Nycteribiid and Streblid Bat Flies (Diptera: Nycteribiidae and Streblidae) from Thailand with Thirteen New Records for the Country. Trop Nat 21:244–262

    Google Scholar 

  • Szentiványi T, Markotter W, Dietrich M, Clément L, Ançay L, Brun L, Genzoni E, Kearney T, Seamark E, Estók P, Christe P, Glaizot O (2020) Host conservation through their parasites: molecular surveillance of vector-borne microorganisms in bats using ectoparasitic bat flies. Parasite 27:72

    Article  PubMed  PubMed Central  Google Scholar 

  • Theodor O (1967) Illustrated catalogue of the Rothschild collection of Nycteribiidae (Diptera) in the British Museum (Natural History); with keys and short descriptions for the identification of subfamilies, genera, species and subspecies. British Museum (Natural History). Publication 665:1–506

    Google Scholar 

  • Tortosa P, Dsouli N, Gomard Y, Ramasindrazana B, Dick CW, Goodman SM (2013) Evolutionary history of Indian Ocean nycteribiid bat flies mirroring the ecology of their hosts. PLoS ONE 8:1–8

    Article  Google Scholar 

  • Ullah H, Kontschán J, Takács N, Wijnveld M, Schötta AM, Boldogh SA, Sándor AD, Szekeres S, Görföl T, Rasheed SB, Javid A, Hornok SA (2019) new Rickettsia honei-related genotype, two novel soft tick haplotypes and first records of three mite species associated with bats in Pakistan. Syst Appl Acarol 24:2106–2118

    Google Scholar 

  • Welbergen JA, Meade J, Field HE, Edson D, McMichael L, Shoo LP, Praszczalek J, Smith C, Martin JM (2020) Extreme mobility of the world’s largest flying mammals creates key challenges for management and conservation. BMC Biol 18:2–13

    Article  Google Scholar 

  • Wenzel RL, Tipton VJ (1966) Some relationships between mammal hosts and their ectoparasites. In Ectoparasites of Panama; Wenzel RL Tipton VJ Eds. Field Museum of Natural History: Chicago IL USA pp 677–723.

  • Yadav PD, Shete-Aich A, Nyayanit DA, Pardeshi P, Majumdar T, Balasubramanian R, Ullas PT, Mohandas S, Dighe H, Sawant P, Patil S, Patil D, Gokhale MD, Mathapati B, Sudeep AB, Baradkar S, Kumar A, Kharde R, Salve M, Joshi Y, Gupta N, Mourya DT (2020) Detection of coronaviruses in Pteropus & Rousettus species of bats from different States of India. Indian J Med Res 151:226–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This study was partially funded by the US Department of the Defense, Defense Threat Reduction Agency (DTRA), under the award HDTRA1-17–0064 (“Understanding the Risk of Bat-Borne Zoonotic Disease Emergence in Western Asia”). The content of the information does not necessarily reflect the position or the policy of the US federal government, and no official endorsement should be inferred.

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Authors and Affiliations

  1. Wildlife Epidemiology and Molecular Microbiology Laboratory (One Health Research Group), Discipline of Zoology, Department of Wildlife & Ecology, University of Veterinary and Animal Sciences, Ravi Campus, Lahore, Pattoki, Pakistan

    Attaullah & Shahzad Ali

  2. Department of Wildlife & Ecology, University of Veterinary and Animal Sciences, Ravi Campus, Lahore, Pattoki, Pakistan

    Attaullah, Shahzad Ali & Arshad Javid

  3. Institute of Biochemistry and Biotechnology, University of Veterinary and Animal Sciences, Ravi Campus, Lahore, Pakistan

    Muhammad Imran

  4. Institute of Pharmaceutical Science, University of Veterinary and Animal Sciences, Lahore, Pakistan

    Tahir Mehmood Khan

  5. EcoHealth Alliance, New York, NY, USA

    Kendra Phelps & Kevin J. Olival

  6. Plant Protection Institute, Centre for Agricultural Research, Budapest, Hungary

    Jenő Kontschán

  7. Department of Plant Sciences, Albert Kázmér Faculty of Mosonmagyaróvár, Széchenyi István University, Mosonmagyaróvár, Hungary

    Jenő Kontschán

  8. Department of Parasitology and Zoology, University of Veterinary Medicine, István u. 2., 1078, Budapest, Hungary

    Sándor Hornok

  9. Climate Change: New Blood-Sucking Parasites and Vector-Borne Pathogens Research Group, ELKH-ÁTE, Budapest, Hungary

    Sándor Hornok

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  1. Attaullah
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Contributions

AU, SA, SH, KP, JK, and KO performed the statistical analyses, evaluated the results and drafted the paper. AU, SA, AJ, MI, and TK participated in the conception and design of the study. AU, SA, KP, JK, and KO contributed to analyzing data. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Shahzad Ali.

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Ethical statement

This study was carried according to instructions of Animal Ethics Committee of the University of Veterinary and Animal Sciences (UVAS), Lahore, Pakistan (No. 120/IRC/BMR; Dated 14/04/2021).

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Section Editor: Van Lun Low

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Attaullah, Ali, S., Javid, A. et al. Phylogenetic relationships of a novel bat fly species infesting the geographically widespread Old World fruit bat, Rousettus leschenaultii, in Southern Asia. Parasitol Res 122, 2101–2107 (2023). https://doi.org/10.1007/s00436-023-07909-0

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