Abstract
Better knowledge of the geographical distribution of parasites and their hosts can contribute to clarifying aspects of host specificity, as well as on the interactions among hosts, parasites, and the environment in which both exist. Ectoparasitic flies of the Nycteribiidae and Streblidae families are highly specialized hematophagous parasites of bats, whose distributional patterns, species richness, and associations with hosts remain underexplored and poorly known in Brazil. Here, we used information available in the literature and unpublished data to verify if the occurrence of bat hosts in a given environment influences the occurrence and distribution of nycteribiid and streblid flies in different ecoregions in the northeastern Brazil. We evaluate species richness and similarity between ecoregions and tested correlations between species richness and the number of studies in each ecoregion and federative unit. We recorded 50 species and 15 genera of bat ectoparasitic flies on 36 species and 27 genera of bat hosts. The Atlantic Forest had the highest fly species richness (n = 31; 62%), followed by Caatinga (n = 27; 54%). We detected the formation of distinct groups, with low species overlap between ecoregions for both flies and bats. Fly species richness was correlated with host species richness and with the number of studies in each federative unit, but not with the number of studies by ecoregion. Due to the formation of distinct groups with low species overlap for both groups, host availability is likely to be one of the factors that most influence the occurrence of highly specific flies. We also discuss host specificity for some species, produced an updated list of species and distribution for both nycteribiid and streblid flies with information on interaction networks, and conclude by presenting recommendations for more effective inventories of bat ectoparasites in the future.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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 51:176–187. https://doi.org/10.1080/01650521.2016.1215042
Barbier E, Prado-Neto JG, Bernard E (2016) Records of bat flies (Diptera: Nycteribiidae and Streblidae) in the semi-arid Caatinga in the state of Paraíba, northeastern Brazil. Neotrop Entomol 45:740–745. https://doi.org/10.1007/s13744-016-0432-8
Barbier E, Souza AQS, Bezerra JPB, Santos JOF, Telino WR Jr (2017) New record, new host, and geographic distribution of Basilia hughscotti Guimarães, 1946 (Diptera: Nycteribiidae). Entomol News 126:394–399. https://doi.org/10.3157/021.126.0507
Bezerra RHS, Vasconcelos PF, Bocchiglieri A (2016) Ectoparasites of bats (Mammalia: Chiroptera) in Atlantic forest fragments in northeastern Brazil. Parasitol Res 10:3759–3765. https://doi.org/10.1007/s00436-016-5137-8
Bordes F, Morand S, Guerrero R (2008) Bat fly species richness in Neotropical bats: correlations with host ecology and host brain. Oecologia 158:109–116. https://doi.org/10.1007/s00442-008-1115-x
Brasil (1982) Decreto n° 87.222 de 31 de maio de 1982. Diário Oficial da União, Brasília
Brasil (1983) Reserva biológica de saltinho. Decreto de criação n° 88.744. http://www.icmbio.gov.br/portal/images/stories/imgs-unidades-coservacao/rebio_saltinho.pdf. Accessed 9 November 2015
Brasil (1997) Decreto de 4 de agosto de 1997. Diário Oficial da União, Brasília http://www.planalto.gov.br/ccivil_03/DNN/Anterior%20a%202000/1997/Dnn5587.htm. Accessed 19 September 2016
Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x
Cordero-Schmidt E, Barbier E, Vargas-Mena JC, Oliveira PP, Santos FAR, Medellín RA, Herrera BR, Vinticinque EM (2017) Natural history of the Caatinga endemic Vieira's flower bat, Xeronycteris vieirai. Acta Chiropterol
Delgado-Jaramillo M, Barbier E, Bernard E (2017) New records, potential distribution, and conservation of the near threatened cave bat Natalus macrourus in Brazil. Oryx https://doi.org/10.1017/S0030605316001186
Dias PA, Santos CLC, Rodrigues FS, Rosa LC, Lobato KS, Rebêlo JMM (2009) Espécies de moscas ectoparasitas (Diptera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera) no estado do Maranhão. Rev Bras Entomol 53:128–133. https://doi.org/10.1590/S0085-56262009000100027
Dick CW (2007) High host specificity of obligate ectoparasites. Ecol Entomol 32:446–450. https://doi.org/10.1111/j.1365-2311.2006.00836.x
Dick CW (2013) Review of the bat flies of Honduras, central America (Diptera: Streblidae). J Parasitol Res 2013:437696. https://doi.org/10.1155/2013/437696
Dick CW, Dittmar K (2014) Parasitic bat flies (Diptera: Streblidae and Nycteribiidae): host specificity and potential as vectors. In: Klimple S, Mehlhorn H (eds) Bats (Chiroptera) as vectors of diseases and parasites. Springer, Heidelberg, pp 131–155. https://doi.org/10.1007/978-3-642-39333-4_6
Dick CW, Gettinger D (2005) A faunal survey of streblid bat flies (Diptera: Streblidae) associated with bats in Paraguay. J Parasitol 91:1015–1024. https://doi.org/10.1645/GE-536R.1
Dick CW, Graciolli G (2008) Checklist of world Streblidae. Hippoboscoidea, Diptera http://fm1.fieldmuseum.org/aa/Files/cdick/Streblidae_Checklist_1jul08.pdf. Accessed 29 November 2009
Dick CW, Patterson BD (2006) Bat flies: obligate ectoparasites of bats. In: Morand S, Krasnov BR, Poulin R (eds) Micromammals and macroparasites: from evolutionary ecology to management. Springer-Verlag, Tokyo, pp 179–194. https://doi.org/10.1007/978-4-431-36025-4_11
Dick CW, Patterson BD (2007) Against all odds: explaining high host specificity in dispersal-prone parasites. Int J Parasitol 37:871–876. https://doi.org/10.1016/j.ijpara.2007.02.004
Dittmar K, Morse SF, Dick CW, Patterson BD (2015) Bat flies evolution from the Eocene to the present (Hippoboscoidea, Streblidae and Nycteribiidae). In: Morand S, Krasnov BR, Littlewood DTJ (eds) Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Cambridge University Press, Cambridge, pp 246–264
Eriksson A, Graciolli G, Fischer E (2011) Bat flies on phyllostomid hosts in the Cerrado region: component community, prevalence and intensity of parasitism. Mem I Oswaldo Cruz 106:274–278. https://doi.org/10.1590/S0074-02762011000300004
Esbérard CEL, Astúa D, Geise L, Costa LM, Pereira LG (2012) Do young Carollia perspicillata (Chiroptera: Phyllostomidae) present higher infestation rates of Streblidae (Diptera)? Braz J Biol 72:617–621. https://doi.org/10.1590/S1519-69842012000300027
Ferraz EMN (2002) Panorama da Floresta Atlântica no estado de Pernambuco. In: Araújo EL, Moura AN, Sampaio EVSB, Gestinari LMS, Carneiro JMT (eds) Biodiversidade, conservação e uso sustentável da flora do Brasil. Imprensa Universitária UFRPE, Recife, pp 23–26
Ferreira CGT, Oliveira RC, Vall JFM, Loiola MIB (2009) Poaceae da Estação Ecológica do Seridó, Rio Grande do Norte, Brasil. Hoehnea 36:679–707. https://doi.org/10.1590/S2236-89062009000400008
Figueiredo D, Graciolli G, Aguiar LMS (2015) New records of bat flies (Diptera, Streblidae and Nycteribiidae) in Cerrado of Central Brazil. Check List 11:1761. https://doi.org/10.15560/11.5.1761
Gandon S, Ebert D, Oliviere I, Michalakis Y (1998) Differential adaptation in spatially heterogeneous environments and host-parasite coevolution. In: Mopper S, Strauss S (eds) Genetic structure and local adaptation in natural insect populations. Springer, New York, pp 325–340. https://doi.org/10.1007/978-1-4757-0902-5_13
Giorgi MS, Arlettaz R, Guillaume F, Nusslé S, Ossola C, Vogel P, Christe P (2004) Causal mechanisms underlying host specificity in bat ectoparasites. Oecologia 138:648–654. https://doi.org/10.1007/s00442-003-1475-1
Graciolli G, Dick CW (2008) Checklist of world Nycteribiidae. Hippoboscoidea, Diptera https://web.archive.org/web/20120213212308/http://fm1.fieldmuseum.org/aa/Files/cdick/Nycteribiidae_Checklist_22oct08.pdf. Accessed 29 November 2009
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
Graciolli G, Zortéa M, Carvalho LFAC (2010) Bat flies (Diptera, Streblidae and Nycteribiidae) in a Cerrado area of state of Goiás, Brazil. Rev Bras Entomol 54:511–514. https://doi.org/10.1590/S0085-56262010000300025
Guerrero R (1994) Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. IV. Trichobiinae con alas desarrolladas. Bol Entomol Venezol 9:161–192
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
Guimarães LR (1937) Sobre as espécies sul americanas do gênero Trichobius (Diptera, Streblidae). Rev Mus Paul 23:653–666
Guimarães LR (1938) Sobre uma nova espécie de Nycteribiidae (Diptera, Pupipara). In: Lent H, Freitas JFT (eds) Livro Jubilar Professor Lauro Travassos. Ex-Libris, Rio de Janeiro, pp 183–184
Guimarães LR (1941) Notas sobre Streblidae I – Sobre a verdadeira identidade de Trichobius dugesii Towns, 1891. Pap Avulsos Zool 1:213–222
Guimarães LR (1944) Sobre os primeiros estágios de alguns dípteros pupíparos. Pap Avulsos Zool 6:181–182
Guimarães LR (1946) Revisão das espécies Sul-Americanas do gênero Basilia (Diptera, Nycteribiidae). Arq Zool 5:1–87
Guimarães LR, D'Andretta MAV (1956) Sinopse dos Nycteribiidae (Diptera) do Novo Mundo. Arq Zool 10:1–84
Hammer O (2016) PAST: paleontological statistics version 3.14 – Reference manual. http://folk.uio.no/ohammer/past/past3manual.pdf. Accessed 7 November 2016
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Handley CO (1967) Bats of the canopy of an Amazonian Forest. Atlas do Simpósio Sobre a Biota Amazônica 5:211–215
Hawlena H, Abramsky Z, Krasnov BR (2005) Age-biased parasitism and density-dependent distribution of fleas (Siphonaptera) on a desert rodent. Oecologia 146:200–208. https://doi.org/10.1007/s00442-005-0187-0
Hintze F, Barbier E, Bernard E (2016) Emballonuridae Gervais, 1855 (Chiroptera) of Reserva Biológica de Saltinho (Atlantic Forest), in Brazil, revealed by echolocation. Check List 12:1925. https://doi.org/10.15560/12.4.1925
ter Hofstede HM, Fenton MB (2005) Relationships between roost preferences, ectoparasite density and grooming behaviour of Neotropical bats. J Zool 266:333–340. https://doi.org/10.1017/S095283690500693X
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
Hurtado N, Pacheco V (2014) Análisis filogenético del género Mimon Gray, 1847 (Mammalia, Chiroptera, Phyllostomidae) con la descripción de un nuevo género. Therya 5:751–791. https://doi.org/10.12933/therya-14-230
IBGE (2016) Instituto brasileiro de geografia e estatistica – resolução n° 2, de 21 de junho de 2016 http://pesquisa.in.gov.br/imprensa/jsp/visualiza/index.jsp?jornal=1&pagina=87&data=22/06/2016. Accessed 16 December 2016
ICMBio (2015) Instituto chico mendes de conservação da biodiversidade – reserva biológica de saltinho http://www.icmbio.gov.br/portalbiodiversidade/unidades-de-conservacao/biomas-brasileiros/mata-atlantica/unidades-de-conservacaomata-atlantica/2156-rebio-de-saltinho.html. Accessed 10 November 2015
ICMBio (2016) Instituto Chico Mendes de Conservação da Biodiversidade – Área de Preservação Ambiental da Chapada do Araripe http://www.icmbio.gov.br/portal/unidadesdeconservacao/biomas-brasileiros/caatinga/unidades-de-conservacao-caatinga/2110-apa-da-chapada-do-araripe. Accessed 19 September 2016
Jobling B (1939) On some American genera of the Streblidae and their species, with the description of a new species of Trichobius (Diptera, Acalypterae). Parasitology 31:486–497
Kessel QC (1925) A synopsis of the Streblidae of the world. J N Y Entomol Soc 33:11–33
Komeno CA, Linhares AX (1999) Batflies parasitic on some phyllostomid bats in southeastern Brazil: parasitism rates and host-parasite relationships. Mem I Oswaldo Cruz 94:151–156. https://doi.org/10.1590/S0074-02761999000200004
Krasnov BR, Sarfati M, Arakelyan MS, Khokhlova IS, Burdelova NV, Degen AA (2003) Host specificity and foraging efficiency in blood-sucking parasite: feeding patterns of a flea Parapulex chephrenis on two species of desert rodents. Parasitol Res 90:393–399. https://doi.org/10.1007/s00436-003-0873-y
Krasnov BR, Poulin R, Shenbrot GI, Mouillot D, Khokhlova IS (2005) Host specificity and geographic range in haematophagous ectoparasites. Oikos 108:449–456. https://doi.org/10.1111/j.0030-1299.2005.13551.x
Krasnov BR, Mouillot D, Shenbrot GI, Khokhlova IS, Poulin R (2011) Beta-specificity: the turnover of host species in space and another way to measure host specificity. Int J Parasitol 41:33–41. https://doi.org/10.1016/j.ijpara.2010.06.001
Lourenço EC, Almeida JC, Famadas KM (2016) Richness of ectoparasitic flies (Diptera: Streblidae) of bats (Chiroptera) – a systematic review and meta-analysis of studies in Brazil. Parasitol Res 115:4379–4388. https://doi.org/10.1007/s00436-016-5223-y
Marshall AG (1981) The ecology of ectoparasitic insects. Academic Press, New York
Marshall AG (1982) Ecology of insects parasitic on bats. In: Kunz TH (ed) Ecology of bats. Plenum Press, New York, pp 69–401
MMA (2002) Ministério do meio ambiente – biodiversidade brasileira: avaliação e identificação de áreas e ações prioritárias para a conservação, utilização sustentável e repartição dos benefícios da biodiversidade nos biomas brasileiros. Brasília
MMA (2004) Ministério do meio ambiente – plano de manejo da estação ecológica do seridó. Brasília
MMA (2008) Ministério do meio ambiente – plano de manejo da reserva biológica de saltinho, pernambuco. Brasília
MMA (2014) Ministério do Meio Ambiente – Portaria n° 444 de dezembro de 2014. Diário Oficial da União, Brasília
Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727. https://doi.org/10.1023/A:1006537600093
Nogueira MR, Lima IP, Moratelli R, Tavares VC, Gregorin R, Peracchi AL (2014) Checklist of Brazilian bats, with comments on original records. Check List 10:808–821. https://doi.org/10.15560/10.4.808
Nooy W, Mrvar A, Batagelj V (2011) Exploratory social network analysis with Pajek, 2nd edn. Cambridge University Press, Cambridge
Paes MLN, Dias IFO (2008) Plano de Manejo – Estação Ecológica Raso da Catarina. IBAMA, Brasília
Perlman SJ, Jaenike J (2003) Infection success in novel hosts: an experimental and phylogenetic study of drosophila-parasitic nematodes. Evolution 57:544–557. https://doi.org/10.1554/0014-3820(2003)057[0544:ISINHA]2.0.CO;2
Pessôa SB, Galvão AL (1937) Descripção de uma nova espécie do gênero Trichobius. Fol Clin Biol 9:1–14
Poinar G, Brown A (2012) The first fossil streblid batfly, Enischnomyi astegosoma n. G., n. Sp. (Diptera: Hippoboscoidea: Streblidae). Syst Parasitol 81:79–86. https://doi.org/10.1007/s11230-011-9339-2
Poulin R (2007) Evolutionary ecology of parasite, 2nd edn. Princeton University Press, Princeton
Poulin R, Krasnov BR, Mouillot D (2011) Host specificity in phylogenetic and geographic space. Trends Parasitol 27:355–361. https://doi.org/10.1016/j.pt.2011.05.003
Price PW (1990) Host populations as resource defining parasite community organization. In: Esch GW, Bush AO, Aho JM (eds) Parasite communities: patterns and processes. Springer, Dordrecht, pp 21–40. https://doi.org/10.1007/978-94-009-0837-6_2
Rios GFP, Sá-Neto RJ, Graciolli G (2008) Fauna de dípteros parasitas de morcegos em uma área de Caatinga do nordeste do Brasil. Chirop Neotrop 14:339–345
Rodal MJN, Andrade KVSA, Sales MF, Gomes APS (1998) Fitossociologia do componente lenhoso de um refúgio vegetacional no município de Buíque, Pernambuco. Rev Bras Biol 58:517–526. https://doi.org/10.1590/S0034-71081998000300017
Santos CLC, Dias PA, Rodrigues FS, Lobato KS, Rosa LC, Oliveira TG, Rebêlo JMM (2009) Moscas ectoparasitas (Diptera: Streblidae) de morcegos (Mammalia: Chiroptera) do município de São Luis, MA: taxas de infestação e associações parasito-hospedeiro. Neotrop Entomol 38:595–601. https://doi.org/10.1590/S1519-566X2009000500006
Santos CLC, Pereira ACN, Bastos VJC, Graciolli G, Rebêlo JMM (2013) Parasitism of ectoparasitic flies on bats in the northern Brazilian Cerrado. Acta Parasitol 58:207–214. https://doi.org/10.2478/s11686-013-0135-9
Shapiro JT, Barbier E, Monadjem A (2016) First record of Streblidae, Raymondia alulata Speiser, 1908 (Diptera: Streblidae), in Swaziland and a review of the genus Raymondia and their hosts in Africa. Acta Chiropterol 18:249–268. https://doi.org/10.3161/15081109ACC2016.18.1.015
Sikes RS, Gannon WL, The Animal Care and Use Committee of the American Society of Mammalogists (2011) Guidelines of the American Society of Mammalogists for the use of wild mammals in research. J Mammal 92:235–253. https://doi.org/10.1644/10-MAMM-F-355.1
Soares FAM, Graciolli G, Alcântara DMC, Ribeiro AEBP, Valença GC, Ferrari SF (2013) Bat flies (Diptera: Streblidae) ectoparasites of bats at an Atlantic rainforest site in northeastern Brazil. Biota Neotrop 13:242–246. https://doi.org/10.1590/S1676-06032013000200024
Soares FAM, Graciolli G, Ribeiro AEBP, Bandeira RS, Moreno JAT, Ferrari SF (2016) Bat (Mammalia: Chiroptera) diversity in an area of mangrove forest in southern Pernambuco, Brazil, with a new species record and notes on ectoparasites (Diptera: Streblidae). Pap Avulsos Zool 56:63–68. https://doi.org/10.11606/0031–1049.2016.56.06
Sosa VJ, Hernández-Salazar E, Hernández-Conrique D, Castro-Luna AA (2008) Murciélagos. In: Manson RH, Hernández-Ortiz V, Gallina S, Mehltreter K (eds) Agroecosistemas cafetaleros de Veracruz: biodiversidad, manejo y conservación. Instituto de Ecología A.C (INECOL) / Instituto Nacional de Ecología (INE-SEMAR-NAT), Mexico, pp 181–192
Straube FC, Bianconi GV (2002) Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de-neblina. Chirop Neotrop 8:150–152
SUDENE (1990) Superintendência do Desenvolvimento do Nordeste – Dados pluviométricos mensais do Nordeste. Estado de Pernambuco. Série Pluviometria 6. Recife
Vasconcelos PF, Falcão LAD, Graciolli G, Borges MAZ (2016) Parasite-host interactions of bat flies (Diptera: Hippoboscoidea) in Brazilian tropical dry forests. Parasitol Res 115:367–377. https://doi.org/10.1007/s00436-015-4757-8
Velloso AL, Sampaio EVSB, Pareyn FGC (2002) Ecorregiões propostas para o bioma Caatinga. Associação Plantas do Nordeste & Instituto de Conservação Ambiental The Nature Conservancy do Brasil, Recife
Wenzel RL (1976) The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young Univ Sci Bull 20:1–177
Wenzel RL, Tipton VJ, Kiewlicz A (1966) The streblid batflies of Panama (Diptera: Calyptera: Streblidae). In: Wenzel RL, Tipton VJ (eds) Ectoparasites of Panama. Field Museum of Natural History, Chicago, pp 405–675
Zarazúa-Carbajal M, Saldaña-Vázquez RA, Sandoval-Ruiz CA, Stoner KE, Benitez-Malvido J (2016) The specificity of host-bat fly interaction networks across vegetation and seasonal variation. Parasitol Res 115:4037–4044. https://doi.org/10.1007/s00436-016-5176-1
Acknowledgements
We thank all the staff of the Laboratório de Ciência Aplicada à Conservação da Biodiversidade, especially A. Jardelino, É. Figueiredo, F. Hintze, Í. Azevedo, and J. Torres for support during fieldwork. Thanks to M. Delgado-Jaramillo for help with Fig. 1, M. Barros for donating fly specimens, and P. Vasconcelos for providing information on the study areas and flies collected in the north of Minas Gerais. We also thank PELD Catimbau for logistical support. M. Mello provided tutorials on interaction networks, available in the Ecological Synthesis Lab (www.marcomello.org). This manuscript is based on E. Barbier’s Thesis to receive his Doctorate in “Biologia Animal” (Zoology) at PPGBA/CB/UFPE. We are grateful to A. Maia, L. Iannuzzi, S. Vasconcelos, and two anonymous reviewers for their constructive comments in an earlier version of the manuscript. We also thank Coordenação de Aperfeiçoamento de Pessoal de Nível Superior–CAPES and Conselho Nacional de Desenvolvimento Científico e Tecnológico–CNPq for the grants to the first and second authors, respectively.
Funding
This study was funded by Grupo Boticário de Proteção à Natureza (grant number 0983-20132) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (grant number 552006/2011-4, CNPq/ICMBio 13/2011–Project “Rede de pesquisas e conservação de pequenos mamíferos em áreas protegidas da Caatinga”).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Fieldwork was authorized by MMA/IBAMA/ICMBio (permits #33353-1, #33353-2, #43816-1, and #43816-2) and Ethics Committee on Animal Care-UFPE (permit #23076.027916/2015-13).
Additional information
Section Editor: Boris R. Krasnov
Rights and permissions
About this article
Cite this article
Barbier, E., Bernard, E. From the Atlantic Forest to the borders of Amazonia: species richness, distribution, and host association of ectoparasitic flies (Diptera: Nycteribiidae and Streblidae) in northeastern Brazil. Parasitol Res 116, 3043–3055 (2017). https://doi.org/10.1007/s00436-017-5615-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-017-5615-7