Abstract
Purpose
Neotropical bats are infested by multiple ectoparasites (like bat fly and mite species) and investigations on these invertebrates on their hosts are crucial to better understand the ectoparasite-ectoparasite and ectoparasite-host associations. The goal of this study was to report ectoparasites species (bat flies and mites) on bats, emphasizing ectoparasite co-occurrences and host-ectoparasite associations. We also test if there is relationship between bat flies and mites on their hosts.
Methods
This study occurred twice a month from September 2011 to September 2012 in an Atlantic Forest remnant in Rio de Janeiro State, Brazil. Spearman correlation was used to test relationship between bat flies and mites.
Results
We found 27 species of ectoparasites on 13 species of bats. Ectoparasites belonged to the bat fly families Streblidae and Nycteribiidae, and the mite families Spinturnicidae, Macronyssidae, Sarcoptidae, and Trombiculidae. Streblid-streblid association was more frequent, but we also recorded streblid-spinturnicid, streblid-sarcoptid and spinturnicid-spinturnicid associations. The abundance of spinturnicid species was negatively related to the abundance of streblid species. We record the first occurrence of Strebla chrotopteri associated with Chrotopterus auritus, Periglischrus paracutisternus associated with Trachops cirrhosus and Basilia juquiensis associated with Myotis riparius for Rio de Janeiro State.
Conclusion
There were several co-occurrences between different taxa and between species of the same family. These results show the importance of the integrated taxonomic record. The negative interspecific interactions between spinturnicid and streblid may affect distributions, structuring ectoparasite communities on hosts.
Similar content being viewed by others
References
Whitaker JO, Ritzi CM, Dick CW, Kunz TH, Parsons S (2009) Collecting and preserving bat ectoparasites for ecological study. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats. Johns Hopkins University Press, Baltimore, pp 806–827
Marshall AG (1982) Ecology of insect parasitic on bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 369–401
Bush AO, Lafferty KD, Lotz JM, Shostak AW et al (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 83:575–583
Bertola PB, Aires CC, Favorito SE, Graciolli G, Amaku M, Pinto-Da-Rocha R (2005) Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque Estadual da Cantareira, São Paulo, Brazil: Parasitism rates and host-parasite associations. Mem Inst Oswaldo Cruz 100:25–32. https://doi.org/10.1590/S0074-02762005000100005
Aguiar LMS, Antonini Y (2016) Prevalence and intensity of Streblidae in bats from a Neotropical savanna region in Brazil. Folia Parasitol 63:024. https://doi.org/10.14411/fp.2016.024
ter Hofstede HM, Fenton MB, Whitaker JO (2004) Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Can J Zool 82(4):616–626. https://doi.org/10.1139/z04-030
Dick CW (2005) Ecology and host specificity of bat flies (Diptera: Streblidae) and their chiropteran host. Thesis. Texas Tech University, Lubbock
Tello SJ, Stevens RD, Dick CW (2008) Patterns of species co-occurrence and density compensation: a test for interspecific competition in bat ectoparasite infracommunities. Oikos 117(5):693–702. https://doi.org/10.1111/j.0030-1299.2008.16212.x
Hiller T, Honner B, Page RA, Tschapka M (2018) Leg structure explains host site preference in bat flies (Diptera: Streblidae) parasitizing neotropical bats (Chiroptera: Phyllostomidae). Parasitol. https://doi.org/10.1017/S0031182018000318
Graciolli G (2019) Nycteribiidae in Catálogo Taxonômico da Fauna do Brasil. PNUD. https://fauna.jbrj.gov.br/fauna/faunadobrasil/1145 Accessed 15 May 2019.
Graciolli G (2019) Streblidae in Catálogo Taxonômico da Fauna do Brasil. PNUD. https://fauna.jbrj.gov.br/fauna/faunadobrasil/2624 Accessed 15 May 2019.
Almeida JC, Gettinger DD (2019) Spinturnicidae in Catálogo Taxonômico da Fauna do Brasil. PNUD. https://fauna.jbrj.gov.br/fauna/faunadobrasil/2529 Accessed 15 May 2019.
Presley SJ (2004) Ectoparasitic assemblages of Paraguayan bats: ecological and evolutionary perspectives. Thesis. Texas Tech University, Lubbock
Almeida J, Serra-Freire N, Peracchi A (2015) Anatomical location of Periglischrus iheringi (Acari: Spinturnicidae) associated with the great fruit-eating bat (Chiroptera: Phyllostomidae). Braz J Vet Parasitol Vet 24(3):361–364. https://doi.org/10.1590/S1984-29612015022
Almeida JC, Silva SSP, Serra-Freire NM, Valim MP (2011) Ectoparasites (Insecta and Acari) associated with bats in southeastern Brazil. J Med Entomol 48:753–757
Moras LM, Ferreira L, Bernardi DO, Graciolli G, Gregorin R (2013) Bat flies (Diptera: Streblidae, Nycteribiidae) and mites (Acari) associated with bats (Mammalia: Chiroptera) in a high-altitude region in southern Minas Gerais. Brazil Acta Parasitol 58(4):556–563. https://doi.org/10.2478/s11686-013-0179-x
Bezerra RHS, de Vasconcelos PF, Bocchiglieri A (2016) Ectoparasites of bats (Mammalia: Chiroptera) in Atlantic forest fragments in north-eastern Brazil. Parasitol Res 115(10):3759–3765. https://doi.org/10.1007/s00436-016-5137-8
Bezerra RHS, Bocchiglieri A (2018) Association of ectoparasites (Diptera and Acari) on bats (Mammalia) in a restinga habitat in northeastern Brazil. Parasitol Research 117:3413–3420. https://doi.org/10.1007/s00436-018-6034-0
Gomes LAC, Pires ADS, Martins MA, Lourenço EC, Peracchi AL (2015) Species composition and seasonal variation in abundance of Phyllostomidae bats (Chiroptera) in an Atlantic Forest remnant, southeastern Brazil. Mammalia 79(1):61–68. https://doi.org/10.1515/mammalia-2013-0108
Walter DE, Krantz GW (2009) Collecting, rearing, and preparing specimens. In: Krantz GW, Walter DE (eds) A manual of acarology, Texas Tech. University Press, Lubbock, pp 83–95
Wenzel RL, Tipton VJ, Kiewlicz A (1966) The streblid bat flies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp 405–675
Wenzel RL (1976) The Streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young Univ Sci Bull 20(4):1–175
Guerrero R (1994) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: pallidus, caecus, major, uniformis y longipes del gênero Trichobius Gervais, 1844. Acta Biol Venez 15(1):1–18
Guerrero R (1995) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. III. Los grupos: dugesii, dunni y phyllostomae del genero Trichobius Gervais, 1844. Acta Biol Venez 15(3–4):1–27
Guerrero R (1996) Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. VI Streblinae Acta Biol Venez 16:1–26
Guerrero R (1998) Notes on Neotropical batflies (Diptera, Streblidae). I. The genus Trichobius, with description of two new species and one new subspecies from Venezuela. Acta Parasitol 43:86–93
Miller J, Tschapka M (2001) The bat flies of La Selva (Diptera: Nycteribiidae, Streblidae). Systematic Entomology Lab, USDA, Washington, DC. https://www.biologie.uni-ulm.de/bio3/Batfly/key.html#Families. Acessed 09 Jan 2020.
Guimarães LR, Andretta MAVD (1956) Sinopse dos Nycteribiidae (Diptera) (Diptera) do Novo Mundo. Arq Zool 9:1–175
Guimarães LR (1966) Nycteribiid batflies from Panama (Diptera: Nycteribiidae). In: Wenzel RL, Tipton VJ (eds) Ectoparasites of panama. Field Museum of Natural History, Chicago, pp 393–404
Guimarães LR (1977) Supplemantary note on Venezuelan bat flies (Diptera: Nycteribiidae). Great Basin Nat 37:221–224
Graciolli G (2004) Nycteribiidae (Diptera, Hippoboscoidea) no Sul do Brasil. Rev Bras Zool 21 (4): 971–985. https://www.scielo.br/scielo.php?pid=S0101-81752004000400035&script=sci_arttext Acessed 7 June 2019.
Furman D (1966) The spinturnicid mites of Panama (Acarina: Spinturnicidae). In: Wenzel RL, Tipton VJ (eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp 125–166
Herrin CS, Tipton VJ (1975) Spinturnicid mites of Venezuela. Brigham Young Univ Sci Bull 20:1–72
Morales-Malacara JB (2001) New morphological analysis of the bat wing mites of the genus Periglischrus (Acari: Spinturnicidae). In: Acarology: Proceedings of the 10th International Congress, Canberra, Australia, 5–10 July 1998 Canberra, Australia. pp 185–195.
Radovsky FJ (1967) The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic on bats. Univ Calif Publ Entomol 46:153–159
Radovsky FJ (2010) Revision of genera of the parasitic mite family Macronyssidae (Mesostigmata: Dermanyssoidea) of the world. Indira Publishing House, Michigan
Fain A (1959) Les acariens psoriques parasites des chauves-souris. X. Le genre Chirnyssoides g.n. chez les chauves-souris sud-américaines (Sarcoptiformes: Sarcoptidae). Bull Inst Roy Sci Nat Belg 35(31):1–19
Fain A, Lukoschus FS (1975) Parasitic mites of Surinam. XXX. New observations on the genera Chirnyssoides and Notoedres from bats (Sarcoptiformes: Sarcoptidae). Acta Zool Pathol Antverp 61:91–118
Klompen JSH (1992) Phylogenetic relationships in the mite family Sarcoptidae (Acari: Astigmata). University of Michigan, Michigan
Brennan JM (1969) New bat chiggers of the genus Perissopalla from Venezuela and Northeastern Brazil (Acarina: Trombiculidae). J Med Entomol 6(4):427–431. https://doi.org/10.1093/jmedent/6.4.427
Brennan JM, Reed JT (1975) A list of Venezuela chiggers, particularly of small mammalian hosts (Acarina: Trombiculidae). Brigham Young Univ Sci Bull Biol Ser 20(1):45–75
Brennan JM, Goff ML (1977) Keys to the genera of chiggers of the western hemisphere (Acarina: Trombiculidae). J Parasit 63(3):554–566. https://doi.org/10.2307/3280021
Barabási AL (2016) Network Science. Cambridge University Press, Cambridge
Dormann CF, Gruber B, Fruend J (2008) Introducing the bipartite Package: Analysing Ecological Networks. R news 8/2: 8–11. https://www.biom.uni-freiburg.de/Dateien/PDF/dormann2008rnews.pdf Accessed 09 Jan 2020.
Teixeira ALM, Ferreira RL (2010) Fauna de dípteros parasitas (Diptera: Streblidae) e taxa de infestação em morcegos presentes em cavidades artificiais em Minas Gerais. Chiropt Neotrop 16:748–754
Barbier E, Graciolli G (2016) Community of bat flies (Streblidae and Nycteribiidae) on bats in the Cerrado of Central-West Brazil: hosts, aggregation, prevalence, infestation intensity, and infracommunities. Stud Neotrop Fauna E 51(3):176–187. https://doi.org/10.1080/01650521.2016.1215042
Prevedello JA, Graciolli G, Carvalho CJB (2005) A fauna de dípteros (Streblidae e Nycteribiidae) ectoparasitos de morcegos (Chiroptera) do estado do Paraná, Brasil: Composição, distribuição e áreas prioritárias para novos estudos. Biociências 13(2):193–209
Reis NR, Peracchi AL, Batista CB, Lima IP, Pereira AD (2017) História Natural dos morcegos brasileiros. Chave de identificação de espécies. Technical Books, Rio de Janeiro
Graciolli G, Carvalho CJB (2001) Moscas ectoparasitas (Diptera, Hippoboscoidea, Nycterybiidae) de morcegos (Mammalia: Chiroptera) do Estado do Paraná, Brasil. II. Streblidae. Chave pictórica para os gêneros e espécies. Rev Bras Zool 18:907–960. https://doi.org/10.1590/S0101-81752001000300026
Graciolli G, Passos FC, Pedro WA, Lim BK (2006) Moscas ectoparasitas (Diptera, Streblidae) de morcegos filostomídeos (Mammalia, Chiroptera) na Estação Ecológica dos Caetetus, São Paulo. Brasil Rev Bras Zool 23(1):298–299. https://doi.org/10.1590/S0101-81752006000100025
Coimbra CEA, Guimarães LR, Mello DA (1984) Ocorrência de Streblidae (Diptera: Pupipara) em morcegos capturados em regiões de cerrado do Brasil Central. Rev Bras Entomol 28:547–550
Eriksson A, Graciolli G, Fischer E (2011) Bat flies on phyllostomid hosts in the cerrado region: component community, prevalence and intensity of parasitism. Mem Inst Oswaldo Cruz 106(3):274–278. https://doi.org/10.1590/S0074-02762011000300004
Vasconcelos PF, Falcão LAD, Graciolli G, Borges MAZ (2016) Parasite-host interactions of bat flies (Diptera: Hippoboscoidea) in Brazilian tropical dry forests. Parasitol Res 115(1):367–377. https://doi.org/10.1007/s00436-015-4757-8
Graciolli G, Autino AG, Claps GL (2007) Catalogue of American Nycteribiidae (Diptera, Hippoboscoidea). Rev Bras Entomol 51:142–159. https://doi.org/10.1590/S0085-56262007000200004
Guimarães LR (1972) Venezuelan nycteribiid bat flies (Diptera: Nycteribiidae). Brigham Young Univ Sci Bull Biol Ser 17:1–11
Graciolli G, Passos FC, Pedro WA, Lim BK (2002) Records of Streblidae and Nycteribiidae (Diptera) on Vespertilionid Bats (Chiroptera: Vespertilionidae) from São Paulo State, Brazil. J New York Entomol Soc 110:402–404
Dick CW, Patterson BD (2006) Bat flies: Obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and Macroparasites. Springer, Tokyo, pp 179–194
Almeida JCD, Martins MA, Guedes PG, Peracchi AL, Serra-Freire NM (2016) New records of mites (Acari: Spinturnicidae) associated with bats (Mammalia, Chiroptera) in two Brazilian biomes: Pantanal and Caatinga. Rev Bras Parasitol Vet 25(1):18–23. https://doi.org/10.1590/S1984-29612016005
Machado-Allison CE, Antequera R (1971) Notes on Neotropical Mesostigmata VI: four new Venezuelan species of the genus Periglischrus (Acarina: Spinturnicidae). Smithson Contrib Zool 93:1–16
Lourenço EC, Gomes LAC, Pinheiro MC, Patrício PMP, Famadas KM (2014) Composition of bat assemblages (Mammalia: Chiroptera) in tropical riparian forests. Zool 31(4):361–369. https://doi.org/10.1590/S1984-46702014000400007
Azevedo AA, Linardi MP, Coutinho MTZ (2002) Acari ectoparasites of bats from Minas Gerais, Brazil. J Med Entomol 39:553–555. https://doi.org/10.1603/0022-2585-39.3.553
Silva CL, Valim MP, Graciolli G (2017) Ácaros ectoparasitos de morcegos no estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zool 107(suppl):1–6. https://doi.org/10.1590/1678-4766e2017111
Jacinavicius F, Bassini-Silva R, Mendoza-Roldan JA, Pepato AR, Ochoa R, Welbourn C, Barros-Battesti DM (2018) A checklist of chiggers from Brazil, including new records (Acari: Trombidiformes: Trombiculidae and Leeuwenhoekiidae). ZooKeys 743:1–41
Silveira PSA, Bernardi LFO, Pepato AR (2015) New records of the genus Whartonia (Acari, Leeuwenhoekiidae) associated with the bat Carollia perspicillata from southeastern Brazil. Check List 11(6):1793. https://doi.org/10.15560/11.6.1793
Lourenço EC, Pinheiro MC, Famadas KM, Faccini JLH (2013) New record, host and localities of bat mite of genus Chirnyssoides (Acari, Sarcoptiformes, Sarcoptidae). Rev Bras Parasitol Vet 22:260–264. https://doi.org/10.1590/S1984-29612013000200045
Lourenço EC, Patrício PMP, Famadas KM (2016) Community components of spinturnicid mites (Acari: Mesostigmata) parasitizing bats (Chiroptera) in the Tinguá Biological Reserve of Atlantic Forest of Brazil. Int J Acarol 42(2):63–69. https://doi.org/10.1080/01647954.2015.1117525
Dantas-Torres F, Soares FM, Ribeiro CEBP, Daher MRM, Valença GC, Valim MP (2009) Mites (Mesostigmata: Spinturnicidae and Spelaeorhynchidae) associated with bats in northeast Brazil. J Med Entomol 46(3):712–715. https://doi.org/10.1603/033.046.0340
Silva CDL, Graciolli G (2013) Prevalence, mean intensity of infestation and host specificity of Spinturnicidae mites (Acari: Mesostigmata) on bats (Mammalia: Chiroptera) in the Pantanal. Brazil Acta Parasitol 58(2):174–179. https://doi.org/10.2478/s11686-013-0134-x
Patterson BD, Dick CW, Dittmar K (2007) Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). J Trop Ecol 23(02):177–189. https://doi.org/10.1017/S0266467406003816
Presley SJ (2011) Interspecific aggregation of ectoparasites on bats: Importance of hosts as habitats supersedes interspecific interactions. Oikos 120(6):832–841. https://doi.org/10.1111/j.1600-0706.2010.19199.x
Schooler ML (2017) Co-occurrence patterns of bat flies on Neotropical Chiroptera. University Kentucky, Lexington
Patrício PMP, Lourenço EC, Freitas AQ, Famadas KM (2016) Host morphophysiological conditions and environment abiotic factors correlate with bat flies (Streblidae) prevalence and intensity in Artibeus Leach, 1821 (Phyllostomidae). Ciênc Rural 46(4):648–653
Webber QMR, Willis CKR (2015) Sociality, parasites, and pathogens in bats. In: Ortega J (ed) Sociality in bats. Springer International Publishing, Berlin, pp 105–139
Dornelles GDP, Graciolli G (2017) Streblid bat flies on Phyllostomid bats from an Island off the coast of São Paulo Brazil. Pap Avulsos Zool 57(4):31–36. https://doi.org/10.11606/0031-1049.2017.57.04
Esbérard C, Astúa D, Geise L, Costa L, Pereira L (2012) Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)? Braz J Biol 72(3):617–621. https://doi.org/10.1590/S1519-69842012000300027
Dick CW, Dick SC (2006) Effects of prior infestation on host choice of bat flies (Diptera: Streblidae). J Med Entomol 43(2):433–436. https://doi.org/10.1603/0022-2585(2006)043[0433:EOPIOH]2.0.CO;2
Ingram T, Shurin JB (2009) Trait-based assembly and phylogenetic structure in northeast Pacific rockfish assemblages. Ecology 90(9):2444–2453. https://doi.org/10.1890/08-1841.1
Krasnov BR, Pilosof S, Stanko M, Morand S, Korallo-Vinarskaya NP, Vinarski MV, Poulin R (2014) Co-occurrence and phylogenetic distance in communities of mammalian ectoparasites: Limiting similarity versus environmental filtering. Oikos 123(1):63–70. https://doi.org/10.1111/j.1600-0706.2013.00646.x
Acknowledgements
We are grateful to Sisbio/ICMBio for allowing the bat caches (license number: 30412-2), Paracambi Secretary of the Environment and Sustainable Development for allowing this research in the park (authorization number: 027/2011), Entidade Ambientalista Onda Verde for logistic support, and many colleagues for helping in the field and the Artrópodes Parasitas Lab. Lourenço E.C. thanks the Rio de Janeiro Post-Doctoral Research Support Program (FAPERJ/CAPES—E-26/202.158/2015) for the stipends conceded. Gomes L.C.A. thanks CAPES for the Masters and PhD scholarships. Viana A.O. thanks FAPESP for the Masters scholarships.
Funding
Not applicable.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of Interest
The authors declare there are no conflicts of interest.
Ethical Approval
This study followed: Sikes, R.S., & Gannon, W. L. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92(1), 235–253 and the Brazilian Council of Veterinary Medicine (Resolution Nº 1000, 11 May 2012, Resolution Nº 879, 15 February 2008). The entire procedure was authorized by the Ethics Committee for the Care and Use of experimental animals of Rural Federal University of Rio de Janeiro (number 23083009482/2012).
Rights and permissions
About this article
Cite this article
Lourenço, E.C., Gomes, L.A.C., Viana, A.d. et al. Co-occurrence of Ectoparasites (Insecta and Arachnida) on Bats (Chiroptera) in an Atlantic Forest Remnant, Southeastern Brazil. Acta Parasit. 65, 750–759 (2020). https://doi.org/10.2478/s11686-020-00224-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11686-020-00224-z