Abstract
This study aimed to investigate the presence of ectoparasites and the occurrence of natural infection by Rickettsia spp. and Trypanosoma spp. in bats from Rio Grande do Sul (RS), Brazil. The evaluated animals were obtained from the Instituto de Pesquisas Veterinárias Desidério Finamor, sent by the Centro Estadual de Vigilância Sanitária, to carry out rabies diagnostic tests, during the period from 2016 to 2021. The bats came from 34 municipalities in RS. Of the 109 animals surveyed, 35.8% (39/109) had 385 ectoparasites, with an average of 9.9 parasites per animal. Of these bats, all had insectivorous feeding habits, with 35.9% (14/39) females and 64.1% (25/39) males. The co-parasitism of Chirnyssoides sp., Ewingana inaequalis, and Chiroptonyssus robustipes on Molossus currentium (Mammalia, Chiroptera) was recorded for the first time. All bats surveyed were negative for infection by the protozoan and bacteria. Thus, the expansion of the occurrence of these ectoparasites in insectivorous bats in RS was observed. Furthermore, this study corresponds to the first recorded interspecific associations for the species.
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Bedin C, Mello F, Wilhelms TS, Torres MA, Estima C, Ferreira CF, Sehn L (2009) Vigilância ambiental: doença de Chagas no Rio Grande do Sul. Bol Epiodemiol 11:1–8
Bedin C, Wilhelms T, Villela MM, Silva GC, Riffel AP, Sackis P, Mello F (2021) Residual foci of Triatoma infestans infestation: surveillance and control in Rio Grande do Sul, Brazil, 2001-2018. Rev Soc Bras Med Trop 54:e0530-2020. https://doi.org/10.1590/0037-8682-0530-2020
Bianchi TF, Jeske S, Sartori A, Grala AP, Villela MM (2021) Validation of a documentar on Chagas disease by a population living in an endemic area. Braz J Biol 81(3). https://doi.org/10.1590/1519-6984.228876
Brook CE, Dobson AP (2015) Bats as “special” reservoirs for emerging zoonotic pathogens. Trends Microbiol 23(3):172–180. https://doi.org/10.1016/j.tim.2014.12.004
Camandaroba ELP, Lima CMP, Andrade SG (2002) Oral transmission of Chagas Disease: Importance of Trypanosoma cruzi biodeme in the intragastric experimental infection. Rev Inst Med Trop São Paulo 44(2)97–103. https://doi.org/10.1590/S0036-46652002000200008
Camargo ME, Silva GR, Castilho EA, Silveira AC (1984) Inquérito sorológico de prevalência da infecção chagásica no Brasil, 1975/1980. Rev Inst Med Trop Sao Paulo 26(4):192–204. https://doi.org/10.1590/S0036-46651984000400003
Cicuttin GL, Salvo MN, Rosa IL, Dohmen FG (2017) Neorickettsia risticii, Rickettsia sp. and Bartonella sp.in Tadarida brasiliensis bats from Buenos Aires, Argentina. Comp Immunol Microbiol Infect Dis 52:1–5. https://doi.org/10.1016/j.cimid.2017.04.004
D’Auria SRN, Camargo MCG, Pacheco RC, Savani ESMM, Dias MAG, Rosa AR, Almeida MF, Labruna MB (2010) Serologic survey for rickettsiosis in bats from São Paulo city, Brazil. Vector Borne Zoonotic Dis 10(5):459–463. https://doi.org/10.1089/vbz.2009.0070
Dario MA, Lisboa CV, Costa LM, Moratelli R, Nascimento MP, Costa LP, Leite YLR, Llewellyn MS, Xavier SCC, Roque ALR, Jansen AM (2017) High Trypanosoma spp. diversity is maintained by bats and triatomines in Espírito Santo state, Brazil. PLoS One 12(11):e0188412. https://doi.org/10.1371/journal.pone.0188412
Desquesnes M, McLaughlin G, Zoungrana A, Dávila AM (2001) Detection and identification of Trypanosoma of African livestock through a single PCR based on internal transcribed spacer 1 of rDNA. Int J Parasitol 31(5–6):610–4. https://doi.org/10.1016/s0020-7519(01)00161-8
Díaz MM, Solari S, Aguirre LF, Aguiar L, Barquez RM (2016) Clave de identificación de losmurciélagos de Sudamérica – Chave de identificação dos morcegos da América do Sul. 1ed. bilíngue – Argentina:Yerba Buena, 160 p.
Dick CW, Patterson BD (2006) Bat flies: Obligate ectoparasites of bats. In: Micromammals and Macroparasites: from Evolutionary Ecology to Management. Springer-Verlag Publishing. 647
Dietrich M, Tjale MA, Weyer J, Kearney T, Seamark ECJ, Nel LH, Monadjem A, Markotter W (2016) Diversity of Bartonella and Rickettsia spp. in bats and their blood-feeding ectoparasites from South Africa and Swaziland. PLoS One 11(3):e0152077. https://doi.org/10.1371/journal.pone.0152077
Durden LA, Best TL, Wilson N, Hilton CD (1992) Ectoparasites mites (Acari) of sympatric brazilian free-tailed bats and big brown bats in Alabama. J Med Entomol 29(2):507–511. https://doi.org/10.1093/jmedent/29.3.507
Dusbábek F (1968) Los acaros cubanos de la familia Spinturnicidae (Acarina), com notas sobre su especificidad de hospedeiros. Poeyana Serie A 57:1–31
Fain A (1959) Les acariens psoriques parasites des chauves-souris. X. Le genre Chirnyssoides g.n. chez les chauves-souris sud-américaines (Sarcoptiformes: Sarcoptidae). Bulletin de l'Institut Royal des Sciences Naturelles de Belgique Entomologie. 35(31): 1–19
Fain A (1994) Adaptation, specificity and host-parasite coevolution in mites (ACARI). Int J Parasitol 24(8):1273–1283. https://doi.org/10.1016/0020-7519(94)90194-5
Fain A, Lukoschus FS (1971) Parasitic mites of Surinam. XVIII. Mites of the genera Notoedres and Chirnyssoides from bats (Sarcoptiformes: Sarcoptidae). Bull Ann Soc Roy Entomol Belgique 107:298–313
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
Fonseca F (1948) A monograph ofthe genera and species of Macronyssidae oudemans, 1936 (Synom Liponissidae Vitzthum, 1931) (Acari). Proc Zool Soc Lond 118:249–334
Furman DP (1966) The spinturnicid mites of Panama. In: Wenzel, R.L., Tipton, V.J. Ectoparasites of Panama Editado; Chicago: Field Museum of Natural History. 125–166
Galvão C, Carcavalho R, Rocha DS, Jurberg J (2003) A checklist of the current valid species of the subfamily Triatominae Jeannel, 1919 (Hemiptera, Reduviidae) and their geographical distribution, with nomenclatural and taxonomic notes. Zootaxa 202:1–36. https://doi.org/10.11646/zootaxa.202.1.1
Garbino GST, Gregorin R, Lima IP, Loureiro L, Moras L, Moratelli R, Nogueira MR, Pavan AC, Tavares VC, Nascimento MC, Novaes RLM, Peracchi AL (2020) Updated checklist of Brazilian bats: versão 2020. Comitê da Lista de Morcegos do Brasil—CLMB. Sociedade Brasileira para o Estudo de Quirópteros (Sbeq)
Gardner RA, Molyneux DH (1987) Babesia vesperuginis: natural and experimental infections in British bats (Microchiroptera). Parasitology 95:461–469. https://doi.org/10.1017/s0031182000057887
Graciolli G, Rui AM (2001) Streblidae (Diptera, Hippoboscoidea) em morcegos (Chiroptera, Phyllostomidae) no nordeste do Rio Grande do Sul, Brasil. Iheringia, Sér. Zool. Porto Alegre 90:85–92. https://doi.org/10.1590/S0073-47212001000100009
Guzman-Cornejo C, García-Prieto L, León GP, Juan B, Morales-Malacara JB (2003) Parasites of Tadarida brasiliensis mexicana (Chiroptera: Molossidae) from Arid Regions of Mexico. Comp Parasitol 70(1):11–25. https://doi.org/10.1654/1525-2647(2003)070[0011:POTBMC]2.0.CO;2
Hamilton PB, Teixeira MMG, Stevens JR (2012) The evolution of Trypanosoma cruzi: The “bat seeding” hypothesis. Trends Parasitol. https://doi.org/10.1016/j.pt.2012.01.006
Herrera-Mares A, Guzmán-Cornejo C, Morales-Malacara JB (2021) The myobiid mites (Acariformes, Eleutherengona, Myobiidae) from Mexico: hosts, distribution and identification key for the genera and species. Syst Appl Acarol 26(4):724–748. https://doi.org/10.11158/saa.26.4.6
IBGE (2022) Instituto brasileiro de geografia e estatística: censo demográfico. Available in: <https://www.ibge.gov.br/cidades-e-estado>. Accessed in: 10 jan 2023
IBGE (2024) Instituto brasileiro de geografia e estatística: censo demográfico. Available in: <https://www.ibge.gov.br/cidades-e-estado>. Accessed in: 17 jan 2024
Jansen AM, Roque ALR (2010) Domestic and wild mammalian reservoir. In: Telleria J, Tibayrenc M (eds) American trypanosomiasis Chagas Disease—one hundred years of research. Elsevier, London, pp 249–276
Klompen JSH (1992) Phylogenetic relationships in the mite family Sarcoptidae (Acari: Astigmata). Museum of Zoology, University of Michigan, Michigan, p 154
Labruna MB (2009) Ecology of Rikettsia in South America. Ann N Y Acad Sci 1166:156–166. https://doi.org/10.1111/j.1749-6632.2009.04516.x
Labruna MB, Whitworth T, Horta MC, Bouyer DH, McBride JW, Pinter A, Popov V, Gennari SM, Walker DH (2004) Rickettsia species infecting Amblyomma cooperi ticks from an area in the state of São Paulo, Brazil, where Brazilian spotted fever is endemic. J Clin Microbiol 42(1):90–98. https://doi.org/10.1128/JCM.42.1.90-98.2004
Lavoipierre MMJ, Beck AJ (1967) Feeding mechanism of Chiroptonyssus robustipes on the transiluminated bat wing. Exp Parasitol 20:312–320. https://doi.org/10.1016/0014-4894(67)90054-9
Lavoipierre MMJ, Beck AJ (1970) Host-parasite relationships of acarine parasites and their vertebrate hosts. II. Lesions produced by myobiid mites in the skin of their hosts. Acta Trop 27(2):146–64
Lourenço EC, Pinheiro MC, Faccini JLH, Famadas KM (2013) New record, host and localities of bat mite of genus Chirnyssoides (Acari, Sarcoptiformes, Sarcoptidae). Rev Bras Parasitol Vet 22(2):260–264. https://doi.org/10.1590/S1984-29612013000200045
Marinkelle CJ (1982) Developmental stages of Trypanosoma cruzi-like flagellates in Carvenicola pilosa. Rev Biol Trop 30:107–111
Matei IA, Corduneanu A, Sándor AD, Ionică AM, Panait L, Kalmár Z, Ivan T, Papuc I, Bouari C, Fit N, Mihalca AD (2021) Rickettsia spp. in bats of Romania: high prevalence of Rickettsia monacensis in two insectivorous bat species. Parasit Vectors 14(1):107. https://doi.org/10.1186/s13071-021-04592-x
Ministério da Saúde (2021) Doenças tropicais negligenciadas. Boletim Epidemiológico - Secretaria de Vigilância em Saúde. Número Especial. Mar
Monteiro SG, Hermann GP, Luchese FC, Mottin VD (2005) Primeiro registro de Rhynchopsylluspulex (Siphonaptera: Tungidae) em Nyctinomops laticaudatus (Chiroptera: Molossidae) no Brasil. Ciência Rural 35:956–957. https://doi.org/10.1590/S0103-84782005000400037
Monteiro SG (2017) Parasitologia na Medicina Veterinária. 2 ed- Rio de Janeiro, Roca. 370
Novakova M, Costa FB, Krause F, Literak I, Labruna MB (2016) Rickettsia vini n. sp. (Rickettsiaceae) infecting the tick Ixodes arboricola (Acari:Ixodidae). Parasit Vectors 9:469. https://doi.org/10.1186/s13071-016-1742-8
Pacheco SM (2013) Chiroptera, p. 175–176, 244, 254. In: Weber MM, Roman C, Cáceres NC (Org.). Mamíferos do Rio Grande do Sul. Santa Maria, Editora da UFSM, 554
Pesenti TC, Gomes SN, Rui AM, Müller G (2014) Geographic variation in ectoparasitic mites diversity in Tadarida brasiliensis (Chiroptera, Molossidae) Iheringia. Série Zoologia 104(4):451–456. https://doi.org/10.1590/1678-476620141044451456
Priotto MC, Santos CV, Mello F, Ferraz ML, Villela MM (2014) Aspectos da vigilância entomológica da doença de Chagas no sul do Rio Grande do Sul, Brasil. Rev Patol Trop 43:228–238. https://doi.org/10.5216/rpt.v43i2.31113
Radovsky FJ (1967) The Macronyssidae and Laelapidae (Acarina: Mesostigmata) parasitic on bats. Univ Calif Publ Entomol 46:1–288
Radovsky FJ (2010) Revision of genera of the parasitic mite family Macronyssidae (Mesostigmata: Dermanyssoidea) of the world. Michigan, West Bloomfield, Indira Publishing House, USA, p 170
Reeves WK, Streicker DG, Loftis AD, Dasch GA (2006) Serologic survey of Eptesicus fuscus from Georgia, USA for Rickettsia and Borrelia and laboratory transmission of a Rickettsia by bat ticks. J Vector Ecol 31(2):386–389. https://doi.org/10.3376/1081-1710(2006)31[386:ssoeff]2.0.co;2
Reeves WK, Beck J, Orlova MV, Daly JL, Pippin K, Revan F, Loftis AD (2016) Ecology of bats, their ectoparasites, and associated pathogens on Saint Kitts Island. J Med Entomol 53:1218–1225. https://doi.org/10.1093/jme/tjw078
Ribeiro AR, Mendonça VJ, Alves RT, Martinez I, Araújo RF, Mello F, Rosa JA (2014) Trypanosoma cruzi strains from triatomine collected in Bahia and Rio Grande do Sul, Brazil. Rev Saude Publica 48(2):295–302. https://doi.org/10.1590/S0034-8910.2014048004719
Ribeiro RD, Garcia TAR, Bonomo WC (1987) Contribuição para o estudo dos mecanismos de transmissão do agente etiológico da Doença de Chagas. Rev. Saúde Pública, São Paulo, v. 21, n. 1, p. 51–54, feb. https://doi.org/10.1590/S0034-89101987000100008
Rui AM, Graciolli G (2005) Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasitas e taxas de infestação. Rev Bras Zool 22(2):438–445. https://doi.org/10.1590/S0101-81752005000200021
Sangster CR, Gordon AN, Hayes D (2012) Systemic toxoplasmosis in captive flying-foxes. Aust Vet J 90:140–142. https://doi.org/10.1111/j.1751-0813.2011.00868.x
Santos FGA, Calouro AM, Souza SF, Lague BM, Marciente R, Faustino CL, Santos GJL, Cunha AO (2012) Ectoparasitismo em uma assembléia de morcegos em um fragmento florestal no estado do Acre, Brasil. Acta Vet Bras 6(3):211–218. https://doi.org/10.21708/avb.2012.6.3.2778
Schroeder CLC, Narra HP, Rojas M, Sahni A, Patel J, Khanipov K, Wood TG, Fofanov Y, Sahni SK (2015) Bacterial small RNAs in the Genus Rickettsia. BMC Genom 16(1075). https://doi.org/10.1186/s12864-015-2293-7
Secretaria da Saúde (SES) and Secretaria de Agricultura (SEAPI) do Rio Grande do Sul (2023) Febre Maculosa: situação do Rio Grande do Sul em 2023. Nota conjunta sobre Febre Maculosa. https://saude.rs.gov.br/upload/arquivos/202306/15185007-nota-febre-maculosa-2023.pdf
Silva IG, Silva HHG (1993) Suscetibilidade de 11 espécies de Triatomíneos (Hemiptera, Reduviidae) à cepa ‘Y’ de Trypanosoma cruzi (Kinetoplastida, Trypanosomatidae). Rev Bras Entomol 37:459–63
Silva CL, Graciolli G, Rui AM (2009) Novos registros de ácaros ectoparasitos (Acari, Spinturnicidae) de morcegos (Chiroptera, Phyllostomidae) no Rio Grande do Sul, Brasil. Chiroptera Neotropical 15(2):469–471
Silva CL, Valim MP, Graciolli G (2017) Ácaros ectoparasitos de morcegos no estado de Mato Grosso do Sul, Brasil. Iheringia, Série Zoologia, 107(supl.): e2017111. https://doi.org/10.1590/1678-4766e2017111
Silva AB, Sato TP, Carvalho PVS, Oliveira ML, Freitas EJP (2019) Panorama Epidemiológico de Rickettsia spp. no Brasil: Uma breve revisão. Acta Tecnologica FAVALE,1. v.01, n.01
Silva D, Ratzlaff FR, Osmari V, Fernandes FD, Lourenço EC, Famadas KM, Campos A, Witt AA, Pacheco SM, Vogel FSF, Botton SA, Sanigioni LA (2023) Rhipicephalus microplus larvae: first report in bats, Molossus rufus. Vet Res Commun. https://doi.org/10.1007/s11259-022-10050-5
Socolovschi C, Kernif T, Raoult D, Parola P (2012) Borrelia, Rickettsia, and Ehrlichia Species in Bat Ticks, France, 2010. Emerg Infect Dis 18(12):1966–1975. https://doi.org/10.3201/eid1812.111237
Spears RE, Durden LA, Hagan DV (1999) Ectoparasiites of Brazilian free-tailed bats with emphasis on anatomical site preferences for Chiroptonyssus robustipes (Acari: Macronyssidae). J Med Entomol 36(4):481–485. https://doi.org/10.1093/jmedent/36.4.481
Szentiványi T, Haelewaters D, Pfliegler WP, Clément L, Christe P, Glaizot O (2018) Laboulbeniales (Fungi: Ascomycota) infection of bat flies (Diptera: Nycteribiidae) from Miniopterus schreibersii across Europe. Parasit Vectors 11(1):395. https://doi.org/10.1186/s13071-018-2921-6
Ter Hofstede HM, Fenton MB, Whitaker JO Jr (2004) Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Can J Zool 82:616–626. https://doi.org/10.1139/Z04-030
Uieda W, Bred A (2016) Morcegos: agentes negligenciados da sustentabilidade. Sustentabilidade em Debate – Brasília. 7(1):186–209
Vargas M (2006) Clave para los géneros más comunes de larvas de Ixodida. (Acari:Ixodidae) Agron Costarricense. 30(1):101–105
Whitaker JO Jr, Ritzi CM, Dick CW (1988) Collecting and preserving bat ectoparasites for ecological study. In: Kunz TH (ed) Ecological and Behavioral Methods for the Study of Bats. Smithsonian Institution Press, Washington, D.C., pp 459–474
Yoshida N (2009) Molecular mechanisms of Trypanosoma cruzi infection by oral route. Mem Inst Oswaldo Cruz, Rio de Janeiro 104, (Suppl I):101–107. https://doi.org/10.1590/S0074-02762009000900015
Zhao S, Yang M, Liu G, Hornok S, Zhao S, Sang C, Tan W, Wang Y (2020) Rickettsiae in the common pipistrelle Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) and the bat soft tick Argas vespertilionis (Ixodida: Argasidae). Parasit Vectors 9;13(1):10. https://doi.org/10.1186/s13071-020-3885-x
Zhou P, Yang XL, Wang XG, Hu B, Zhang L, Zhang W, Si HR, Zhu Y, Li B, Huang CL, Chen HD, Chen J, Luo Y, Guo H, Jiang RD, Liu MQ, Chen Y, Shen XR, Wang X, Zheng XS, Zhao K, Chen QJ, Deng F, Liu LL, Yan B, Zhan FX, Wang YY, Xiao GF, Shi ZL (2020) A pneumonia outbreak associated with a new coronavirus of probable bat origin. Nature 579(7798):270–273. https://doi.org/10.1038/s41586-020-2012-7. (Erratum.In:Nature.2020Dec;588(7836):E6)
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da Silva, D., Ratzlaff, F.R., Osmari, V. et al. Detection of ectoparasites and investigation of infection by Rickettsia spp. and Trypanosoma spp. in bats from Rio Grande do Sul, Brazil. Parasitol Res 123, 177 (2024). https://doi.org/10.1007/s00436-024-08198-x
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DOI: https://doi.org/10.1007/s00436-024-08198-x