Seasonal variation and host sex affect bat–bat fly interaction networks in the Amazonian savannahs

Abstract

Bats are the second-most diverse group of mammals in the world, and bat flies are their main parasites. However, significant knowledge gaps remain regarding these antagonistic interactions, especially since diverse factors such as seasonality and host sex can affect their network structures. Here, we explore the influence of such factors by comparing species richness and composition of bat flies on host bats, as well as specialization and modularity of bat–bat fly interaction networks between seasons and adult host sexes. We captured bats and collected their ectoparasitic flies at 10 sampling sites in the savannahs of Amapá State, northeastern region of the Brazilian Amazon. Despite female bats being more parasitized and recording greater bat fly species richness in the wet season, neither relationship was statistically significant. The pooled network could be divided into 15 compartments with 54 links, and all subnetworks comprised >12 compartments. The total number of links ranged from 27 to 48 (for the dry and wet seasons, respectively), and female and male subnetworks had 44 and 41 links, respectively. Connectance values were very low for the pooled network and for all subnetworks. Our results revealed higher bat fly species richness and abundance in the wet season, whereas specialization and modularity were higher in the dry season. Moreover, the subnetwork for female bats displayed higher specialization and modularity than the male subnetwork. Therefore, both seasonality and host sex contribute in different ways to bat–bat fly network structure. Future studies should consider these factors when evaluating bat–bat fly interaction networks.

Keywords

Amapá / Amazon biome / bat flies / bats / interaction networks

References

[1] Aguirre LF, Lens L, Matthysen E (2003). Patterns of roost use by bats in a neotropical savanna: Implications for conservation. Biological Conservation 111, 435–43.

[2] Almeida-Neto M, Ulrich W (2011). A straightforward computational approach for measuring nestedness using quantitative matrices. Enviromental Modeling & Software 26, 173–8.

[3] Anthony ELP (1988). Age determination in bats. In: Kunz TH, ed. Ecological and Behavioral Methods for the Study of Bats. Smithsonian Institute Press, Washington DC, pp. 47–58.

[4] Barbier E, Bernard E (2017). 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. Parasitology Research 116, 3043–55.

[5] Barbier E, Graciolli G, Bernard E (2019). Structure and composition of Nycteribiidae and Strelidae flies on bats along an enviromental gradient in Northeastern Brazil. Canadian Journal of Zoology 97, 409–18.

[6] Beckett SJ (2015). Nestedness and Modularity in Bipartite Networks. University of Exeter, Exeter, UK.

[7] Beckett SJ (2016). Improved community detection in weighted bipartite networks. Royal Society Open Science 3, 140536.

[8] Bernard E, Fenton MB (2003). Bat mobility and roosts in a fragmented landscape in Central Amazonia, Brazil. Biotropica 35, 262–77.

[9] Bezerra RHS, Bocchiglieri A (2018). Association of ectoparasites (Diptera and Acari) on bats (Mammalia) in a resting habitat in northeastern Brazil, Parasitology Research 117, 3413–20.

[10] Blüthgen N, Klein A-M (2011). Functional complementarity and specialisation: The role of biodiversity in plant – pollinator interactions. Basic and Applied Ecology 12, 282–91.

[11] Blüthgen N, Menzel F, Hovestadt T, Fiala B, Blüthgen N (2007). Specialization, constraints, and conflicting interests in mutualistic networks. Current Biology 17, 341–6.

[12] Carvalho WD, Mustin K, Farneda FZ et al. (2021). Taxonomic, functional and phylogenetic bat diversity decrease from more to less complex natural habitats in the Amazon. Oecologia 197, 223–39.

[13] Carvalho WD, Rosalino LM, Da Silva Xavier B et al. (2023). The relative importance of forest cover and patch-level drivers for phyllostomid bat communities in the Amazonian savannas. Landscape Ecology 38, 117–30.

[14] Carvalho WD, Gomes LAC, de Castro IJ, Martins AC, Esbérard CEL, Mustin K (2018). Beyond the Amazon forest: Richness, abundance and flight height of bats in the understory of savannahs, campiranas and terra firme forest. Acta Chiropterologica 20, 407–19.

[15] Chao A, Chiu C-H (2016). Nonparametric estimation and comparison of species richness. In: Nonparametric Estimation and Comparison of Species Richness. John Wiley & Sons, Chichester, pp. 1–11.

[16] Chao A, Gotelli NJ, Hsieh TC et al. (2014). Rarefaction and extrapolation with Hill numbers: A framework for sampling and estimation in species diversity studies. Ecologycal Monographs 84, 45–67.

[17] Christe P, Glaizot O, Evanno G et al. (2007). Host sex and ectoparasites choice: Preference for, and higher survival on female hosts. Journal of Animal Ecology 76, 703–10.

[18] Clarke KR (1993). Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–43.

[19] Costa-Neto SV (2017). Flora das savanas do estado do Amapá. In: Bastos A, Miranda-Júnior J, Silva R, eds. Conhecimento e Manejo Sustentável da Biodiversidade Amapaense. Blucher, Sao Paulo, pp. 65–94.

[20] Cumming G, Finch S (2005). Inference by eye: confidence intervals and how to read pictures of data. American Phychologist 60, 170–80.

[21] De Carvalho WD, Martins MA, Dias D, Saldaña-Vázquez RA, Palmeirim JM, Esbérard CEL (2019). Reproductive constraints in frugivorous phyllostomid bats: Seasonal and elevational variation in reproductive rates in the Brazilian Atlantic Forest. Journal of Mammalogy 100, 487–99.

[22] De Carvalho WD, Mustin K (2017). The highly threatened and little known Amazonian savannahs. Nature Ecology and Evolution 1, 0100.

[23] Dias PA, Santos CLCD, Rodrigues FS, Rosa LC, Lobato KS, Rebêlo JMM (2009). Especies de moscas ectoparasitas (Diptera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera) no estado do Maranhão. Revista Brasileira de Entomologia 53, 128–33.

[24] Dick CW (2007). High host specificity of obligate ectoparasites. Ecological Entomology 32, 446–50.

[25] Dick CW, Dick SC (2006). Effects of prior infestation on host choice of bat flies (Diptera: Streblidae). Journal of Medical Entomology 43, 433–6.

[26] Dick CW, Esbérard CEL, Graciolli G, Bergallo HG, Gettinger D (2009). Assessing host specificity of obligate ectoparasites in the absence of dispersal barriers. Parasitology Research 105, 1345–9.

[27] Dick CW, Patterson BD (2007). Against all odds: Explaining high host specificity in dispersal-prone parasites. International Journal for Parasitology 37, 871–6.

[28] Dick CW, Patterson BD (2006). Bat flies: Obligate ectoparasites of bats. In: Poulin R, ed. Micromammals and Macroparasites: From Evolutionary Ecology to Management. Springer-Verlag, Tokyo, pp. 179–94.

[29] Dittmar K, Dick CW, Patterson BD, Whiting MF, Gruwell ME (2009). Pupal deposition and ecology of bat flies (Diptera: Streblidae): Trichobius sp. (Caecus Group) in a Mexican cave habitat. Journal of Parasitology 95, 308–14.

[30] Dormann CF, Fründ J, Gruber B (2019). Package ‘bipartite’. R package. Available from URL:

[31] Dormann CF, Gruber B, Fründ J (2008). Introducing the bipartite package: Analysing ecological networks. Rnews 8, 8–11.

[32] Dormann CF, Fründ J, Blüthgen N, Gruber B (2009). Indices, graphs and null models: Analyzing bipartite ecological networks. The Open Ecology Journal 2, 7–24.

[33] Dormann CF, Strauss R (2014). A method for detecting modules in quantitative bipartite networks. Methods in Ecology and Evolution 5, 90–8.

[34] Esbérard CEL (2006). Efeito da coleta de morcegos por noites seguidas no mesmo local. Revista Brasileira de Zoologia 23, 1093–6.

[35] Esbérard CEl, Martins-Hatano F, Bittencourt EB et al. (2005). A method for testing the host specificity of ectoparasites: Give them the opportunity to choose. Memorias do Instituto Oswaldo Cruz 100, 761–4.

[36] Fagundes R, Antonini Y, Aguiar LMS (2017). Overlap in cave usage and period of activity as factors structuring the interactions between bats and ectoparasites. Zoological Studies 56, e22.

[37] Garbino GST, Gregorin R, Lima IP et 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).

[38] Garbino GST, Tavares VDaC (2018). Roosting ecology of Stenodermatinae bats (Phyllostomidae): Evolution of foliage roosting and correlated phenotypes. Mammal Review 48, 75–89.

[39] Gardner Alfred L (2008). Mammals of South America, Volume 1: Marsupials, Xenarthrans, Shrews, and Bats, 1st edn. University of Chicago Press, Chicago, IL.

[40] Graciolli G, Bernard E (2002). Novos registros de moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) em morcegos (Mammalia, Chiroptera) do Amazonas e Pará, Brasil. Revista Brasileira de Zoologia 19, 77–86.

[41] Graciolli G, Linardi PM (2002). Some Streblidae and Nycteribiidae (Diptera: Hippoboscoidea) from Maracá Island, Roraima, Brazil. Memorias do Instituto Oswaldo Cruz 97, 139–41.

[42] Graciolli G, Zortéa M, Carvalho LFADaC (2010). Bat flies (Diptera, Streblidae and Nycteribiidae) in a Cerrado area of Goiás State, Brazil. Revista Brasileira de Entomologia 54, 5151–4.

[43] Guerrero R (1993). Catalogo de los Streblidae (Diptera: Pupipara) parásitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. I. Clave para los géneros y Nycterophiliinae. Acta Biologica Venezuelica 14, 61–75.

[44] Guerrero R (1994a). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. II. Los grupos: Pallidus, Caecus, Major, Uniformis y Longipes del género Trichobius Gervais, 1844. Acta Biologica Venezuelica 15, 1–18.

[45] Guerrero R (1994b). Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo Mundo. IV. Trichobiinae con alas desarrolladas. Boletin de Entomologia Venezolana 9, 161–92.

[46] Guerrero R (1995a). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de los murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. III. Los grupos: Dugesii, Dunni y Phyllostomae del género Trichobius Gervais, 1844. Acta Biologica Venezuelica 15, 1–27.

[47] Guerrero R (1995b). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. V. Trichobiinae con alas reducidas o ausentes y miscelaneos. Boletin de Entomologia Venezolana 10, 135–60.

[48] Guerrero R (1996). Catálogo de los Streblidae (Diptera: Pupipara) parasitos de murciélagos (Mammalia: Chiroptera) del nuevo mundo. VI. Streblinae. Acta Biologica Venezuelica 16, 1–25.

[49] Hernández-Martínez J, Morales-Malacara JB, Alvarez-Añorve MY, Amador-Hernández S, Oyama K, Avila-Cabadilla LD (2019). Drivers potentially influencing host-bat fly interactions in anthropogenic neotropical landscapes at different spatial scales. Parasitology 146, 74–88.

[50] Hiller T, Vollstädt MGR, Brändel SD, Page RA, Tschapka M (2021). Bat–bat fly interactions in Central Panama: Host traits relate to modularity in a highly specialised network. Insect Conservation and Diversity 14, 686–99.

[51] Hrycyna G, Martins ACM, Graciolli G (2019). Infracommunities of bat flies (Diptera: Streblidae and Nycteribiidae) of bats (Mammalia: Chiroptera) in three conservation units in the State of Amapá, Brazil. Biota Neotropica 19, e20180715.

[52] Hsieh TC, Ma KH, Chao A (2014). iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Ecological Monographs 7, 45–67.

[53] Janzen DH, Schoener TW (1967). Differences in insect abundance and diversity between wetter and drier sites during a tropical dry season. Ecology 49, 96–110.

[54] Júnior LDeF, De Araújo WS, Falcão LAD (2020). Structure of the interaction networks between bats (Mammalia: Chiroptera) and ectoparasite flies (Diptera: Streblidae, Nycteribiidae) on a latitudinal gradient. Acta Chiropterologica 22, 187–96.

[55] Kerth G (2008). Causes and consequences of sociality in bats. Bioscience 58, 737–46.

[56] Klingbeil BT, Willig MR (2010). Seasonal differences in population-, ensemble- and community-level responses of bats to landscape structure in Amazonia. Oikos 119, 1654–64.

[57] Komeno CA, Linhares AX (1999). Batflies parasitic on some phyllostomid bats in Southeastern Brazil: Parasitism rates and host-parasite relationships. Memorias do Instituto Oswaldo Cruz 94, 151–6.

[58] Kunz TH (1982). Roosting ecology of bats. In: Kunz TH, ed. Ecology of Bats. Plenum Publishing Corporation, New York, pp. 1–46.

[59] Kunz TH, Hood WR (2000). Parental care and postnatal growth in the Chiroptera. In: Crichton EG, Krutzsch PH, eds. Reproductive Biology of Bats. Academic Press, London, pp. 415–68.

[60] Kunz TH, Mccracken GF (1996). Tents and harems: Apparent defence of foliage roosts by tent-making bats. Journal of Tropical Ecology 12, 121–37.

[61] Lewis SE (1995). Roost fidelity of bats: A review. Journal of Mammalogy 76, 481–96.

[62] Lim BK, Engstrom MD (2001). Species diversity of bats (Mammalia: Chiroptera) in Iwokrama Forest, Guyana, and the Guianan subregion: Implications for conservation. Biodiversity and Conservation 10, 613–57.

[63] López-Baucells A, Rocha R, Bobrowiec P, Bernard E, Palmeirim JM, Meyer CFJ (2018). Field Guide to the Bats of the Amazon. Pelagic Publishing, Exeter, UK.

[64] 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. Parasitology Research 115, 4379–88.

[65] Luna P, Corro EJ, Ahuatzin-Flores DA et al. (2017). The risk of use small matrices to measure specialization in host – parasite interaction networks: A comment to Rivera-García (2016). Parasitology 144, 1102–6.

[66] Luz HR, Muñoz-Leal S, De Carvalho WD et al. (2019). Detection of “Candidatus Rickettsia wissemanii” in ticks parasitizing bats (Mammalia: Chiroptera) in the northern Brazilian Amazon. Parasitology Research 118, 3185–9.

[67] Macgregor-Fors I, Payton ME (2013). Contrasting diversity values: Statistical inferences based on overlapping confidence intervals. PLoS ONE 8, e56794.

[68] Marques JT, Ramos Pereira MJ, Marques TA et al. (2013). Optimizing sampling design to deal with mist-net avoidance in Amazonian birds and bats. PLoS ONE 8, e74505.

[69] Marshall AC (1982). Ecology of insect ectoparasites of bats. In: Kunz TH, ed. Ecology of Bats. Plenum Publishing Corporation, New York, pp. 369–97.

[70] McCracken GF, Wilkinson GS (2000). Reproductive Biology of Bats. Academic Press, Cambridge, MA, pp. 321–62.

[71] Mckee CD, Krawczyk AI, Sándor AD et al. (2019). Host phylogeny, geographic overlap, and roost sharing shape parasite communities in European bats. Frontiers in Ecology and Evolution 7, 1–21.

[72] Mello MAR, Schittini GM, Selig P, Bergallo HG (2004). A test of the effects of climate and fruiting of Piper species (Piperaceae) on reproductive patterns of the bat Carollia perspicillata (Phyllostomidae). Acta Chiropterologica 6, 309–18.

[73] Meyer CFJ, Aguiar LMS, Aguirre LF et al. (2015). Species undersampling in tropical bat surveys: Effects on emerging biodiversity patterns. Journal of Animal Ecology 84, 113–23.

[74] Morrison DW (1979). Apparent male defense of tree hollows in the fruit bat, Artibeus jamaicensis. Journal of Mammalogy 60, 11–5.

[75] Morrison DW, Handley CO (1991). Roosting behavior. In: Handley CO, Wilson DE, Gardner AL, eds. Demography and Natural History of the Common Fruit Bat, Artibeus jamaicensis, on Barro Colorado Island, Panama. Smithsonian Institute Press, Washington DC, pp. 131–6.

[76] Mustin K, Carvalho WD, Hilário RR et al. (2017). Biodiversity, threats and conservation challenges in the ‘Cerrado of Amapá’, an Amazonian savanna. Nature Conservation 22, 107–27.

[77] Ocampo-Gonzáles P, López-Wilchis R, Espinoza-Medinilla EE, Rioja-Paradela TM (2021). A review of the breeding biology of Chiroptera. Mammal Review 51, 338–52.

[78] Oksanen J, Simpson G, Blanchet F et al. (2022). vegan: Community Ecology Package. R package version 2.6-4,

[79] Overal WL (1980). Host-relations of the batfly Megistopoda aranea (Diptera: Streblidae) in Panama. The University of Kansas Science Bulletin 52, 1–19.

[80] Palheta LR, Urbieta GL, Brasil LS et al. (2020). The effect of urbanization on bats and communities of bat flies (Diptera: Nycteribiidae and Streblidae) in the Amazon, Northern Brazil. Acta Chiropterologica 22, 403–16.

[81] Patterson BD, Dick CW, Dittmar K (2007). Roosting habits of bats affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology 23, 177–89.

[82] Pilosof S, Dick CW, Korine C, Patterson BD, Krasnov BR (2012). Effects of anthropogenic disturbance and climate on patterns of bat fly parasitism. PLoS ONE 7, e41487.

[83] Pinheiro F, Diniz IR, Coelho D, Bandeira MPS (2002). Seasonal pattern of insect abundance in the Brazilian cerrado. Austral Ecology 27, 132–6.

[84] Presley SJ, Willig MR (2008). Intraspecific patterns of ectoparasite abundances on Paraguayan bats: Effects of host sex and body size. Journal of Tropical Ecology 24, 75–83.

[85] R Core Team (2021). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.

[86] Racey PA (1982). Ecology of bat reproduction. In: Kunz TH, ed. Ecology of Bats. Plenum Publishing Corporation, New York, pp. 57–93.

[87] Racey PA, Entwistle AC (2000). Life-history and reproductive strategies of bats. In: Crichton EG, Krutzsch PH, eds. Reproductive Biology of Bats. Academic Press, Cambridge, MA.

[88] Ramos Pereira MJ, Marques JT, Palmeirim JM (2010). Ecological responses of frugivorous bats to seasonal fluctuation in fruit availability in Amazonian forests. Biotropica 42, 680–7.

[89] Reis NR, Peracchi AL, Batista CB, Lima IP (2017). História Natural dos Morcegos Brasileiros: Chave de Identificação de Espécies. Technical Books Livraria LTDA, Rio de Janeiro.

[90] Rifkin JL, Nunn CL, Garamszegi LZ (2012). Do animals living in larger groups experience greater parasitism? A meta-analysis. The American Naturalist 180, 70–82.

[91] Rivera-García KD, Sandoval-Ruiz CA, Saldaña-Vázquez RA, Schondube JE (2017). The effects of seasonality on host–bat fly ecological networks in a temperate mountain cave. Parasitology 144, 692–7.

[92] Roswell M, Dushoff J, Winfree R (2021). A conceptual guide to measuring species diversity. Oikos 130, 321–38.

[93] Rui AM, Graciolli G (2005). Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: Associações hospedeiros-parasitos e taxas de infestação. Revista Brasileira de Zoologia 22, 438–45.

[94] Saldaña-Vázquez RA, Sandoval-Ruiz CA, Veloz-Maldonado OS, Durán AA, Ramírez-Martínez MM (2019). Host ecology moderates the specialization of Neotropical bat-fly interaction networks. Parasitology Research 118, 2919–24.

[95] Salinas-Ramos VB, Zaldívar-Riverón A, Rebollo-Hernández A, Herrera-M LG (2018). Seasonal variation of bat-flies (Diptera: Streblidae) in four bat species from a tropical dry forest. Mammalia 82, 133–43.

[96] Santos C, Pereira A, Bastos V, Graciolli G, Rebêlo J (2013). Parasitism of ectoparasitic flies on bats in the northern Brazilian cerrado. Acta Parasitologica 58, 207–14.

[97] Santos CLC, Dias PA, Rodrigues FS et al. (2009). Moscas ectoparasitas (Diptera: Streblidae) de Morcegos (Mammalia: Chiroptera) do Município de São Luís, MA: Taxas de Infestação e Associações Parasito-Hospedeiro. Neotropical Entomology 38, 595–601.

[98] Schenker N, Gentleman JF (2001). On judging the significance of differences by examining the overlap between confidence intervals. The American Statistician 55, 37–41.

[99] Sikes RS, Animal Care and Use Commitee of the American Society of Mammalogists (2016). 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. Journal of Mammalogy 97, 663–88.

[100] Stephen Dobson F (1982). Competition for mates and predominant juvenile male dispersal in mammals. Animal Behaviour 30, 1183–92.

[101] Straube FC, Bianconi GV (2002). Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes de neblina. Chiroptera Neotropical 8, 150–2.

[102] Tavares JPN (2014). Características da climatologia de Macapá-AP. Caminhos de Geografía 15, 138–51.

[103] Ter Hofstede HM, Fenton MB (2005). Relationships between roost preferences, ectoparasite density, and grooming behaviour of neotropical bats. Journal of the Zoological Society of London 266, 333–40.

[104] Theodor O, Peterson BV (1964). On some new species of Nycteribiidae (Diptera: Puppipara). The Great Basin Naturalist 24, 107–15.

[105] Urbieta GL, Graciolli G, Da Cunha Tavares V (2022). Review of studies about bat-fly interactions inside roosts, with observations on partnership patterns for publications. Parasitology Research 121, 3051–61

[106] Urbieta GL, Graciolli G, Vizentin-Bugoni J (2021). Modularity and specialization in bat–fly interaction networks are remarkably consistent across patches within urbanized landscapes and spatial scales. Current Zoology 67, 403–10.

[107] Webber QMR, Brigham RM, Park AD, Gillam EH, O'shea TJ, Willis CKR (2016). Social characteristics and predicted pathogen transmission in summer colonies of female big brown bats (Eptesicus fuscus). Behavioral Ecology and Sociobiology 70, 701–12.

[108] Wenzel RL (1976). The Streblid Bat Flies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Biological Series, Utah, USA.

[109] Wilkinson GS (1986). Social grooming in the common vampire bat, Desmodus rotundus. Animal Behaviour 34, 1880–9.

[110] 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. Parasitology Research 115, 4037–44.

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