A tripartite survey of hyperparasitic fungi associated with ectoparasitic flies on bats (Mammalia: Chiroptera) in a neotropical cloud forest in Panama

Abstract

The Darién province in eastern Panama is one of the most unexplored and biodiverse regions in the world. The Chucantí Nature Reserve, in Serranía de Majé, consists of a diverse tropical cloud forest ecosystem. The aim of this research was to explore and study host associations of a tripartite system of bats, ectoparasitic flies on bats (Diptera, Streblidae), and ectoparasitic fungi (Ascomycota, Laboulbeniales) that use bat flies as hosts. We captured bats at Chucantí, screened each bat for presence of bat flies, and screened collected bat flies for presence of Laboulbeniales. We mistnetted for 68 mistnet hours and captured 227 bats representing 17 species. We captured Micronycteris schmidtorum, a species previously unreported in Darién. In addition, we encountered the rarely collected Platyrrhinus dorsalis, representing the westernmost report for this species. Of all captured bats, 148 carried bat flies (65%). The number of sampled bat flies was 437, representing 16 species. One species represents a new country record (Trichobius anducei) and five species represent first reports for Darién (Basilia anceps, Anatrichobius scorzai, Nycterophilia parnelli, T. johnsonae, T. parasiticus). All 74 bat fly species currently reported in Panama are presented in tabulated form. Of all screened bat flies, 30 bore Laboulbeniales fungi (7%). Based on both morphology and large ribosomal subunit (LSU) sequence data, we delimited 7 species of Laboulbeniales: Gloeandromyces nycteribiidarum (newly reported for Panama), G. pageanus, G. streblae, Nycteromyces streblidinus, and 3 undescribed species. Of the 30 infected flies, 21 were Trichobius joblingi. This species was the only host on which we observed double infections of Laboulbeniales.

Laboulbeniales hyperparasites (Fungi, Ascomycota) of bat flies: Independent origins and host associations

“…sp. nov. 3 ( sensu Walker et al., ) are sister taxa and have high support. Gloeandromyces streblae falls apart into two clades A and B, each lacking ML BS support but with moderate to high pp support.…”

“…Gloeandromyces sp. nov. 2 ( sensu Walker et al., ) falls in Clade B, among isolates of G. streblae . Clade C includes isolates of the recently described G. pageanus .…”

“…Included in this study were bat flies from Latin America [Costa Rica (T. Hiller, unpublished data), Ecuador, Mexico, Nicaragua (C.W. Dick, unpublished data), Honduras (Dick, ), Panama (Walker et al., ) and Trinidad (J.J. Camacho, unpublished data)] and Europe [Croatia, Hungary, Portugal, Slovakia, and Spain in Europe (Haelewaters et al., ; Szentiványi et al., )].…”

“…To assess phylogenetic diversity within the genus Gloeandromyces , the LSU rDNA dataset was used. This region was put forward by previous studies to replace ITS as barcode for species delimitation in Laboulbeniomycetes (D. Haelewaters et al., unpublished data; Walker et al., ). Maximum likelihood (ML) analysis was run using the PAUP on XSEDE 4.0b tool (Swofford, ).…”

“…Some of his publications presented species descriptions and new records for Arthrorhynchus , a genus apparently restricted to Old World bat flies (Thaxter, , , , , ), and two genera that thus far have only been reported on neotropical bat flies, Gloeandromyces and Nycteromyces (Thaxter, , , ). Until we initiated our studies on bat fly‐associated Laboulbeniales, five species were known from the type collections only (Haelewaters et al., 2017a, ; Walker et al., ). This illustrates how underexplored these hyperparasites are.…”