Mammalia æquatorialis 2023(5): 49–73

The Ecuadorian Journal of Mammalogy

ISSN 2697-3286

DOI: https://doi.org/10.59763/mam.aeq.v5i.67

Submitted: 2023-06-20 Accepted: 2023-10-24 Published: 2023-12-01

ORIGINAL article

Ectoparasites (Diptera: Streblidae and Nycteribiidae)
of bats from some localities of the Coast of Ecuador

Ectoparásitos (Diptera: Streblidae y Nycteribiidae) de murciélagos
en algunas localidades de la Costa del Ecuador

Katherine Portilla, Ana Lucía Pilatasig,
and M. Alejandra Camacho

Sección de Mastozoología, Museo de Zoología, Facultad de Ciencias Exactas
y Naturales, Pontificia Universidad Católica del Ecuador,
Av. 12 de octubre y Roca, Quito, Ecuador.

Corresponding author: [email protected] (M. Alejandra Camacho)

ABSTRACT

In Ecuador, studies of parasitic bat flies are scarce and biased towards the family Streblidae: reports indicate the existence of 50 species, five of them on the western lowlands. In this study, in addition to Streblidae, we include information of the family Nycteribiidae that has not been studied in Ecuador. Both families are associated with bats in several localities of the western lowlands of the country. We used samples from the associated collection of parasites of the Mammalogy Section of the Museo de Zoología at Pontificia Universidad Católica del Ecuador (QCAZ-M), as well as the database of the collection that allowed obtaining information on the host taxa. Thus, 145 individuals of bats of 22 species of the families Phyllostomidae and Vespertilionidae and 424 individuals of 29 species of parasitic flies are reported. Of these, five species are new in Ecuador, 19 are confirmed records in the west and the geographic distribution was extended for species previously reported in this region. Trichobius joblingi was the most abundant parasitic fly species and together with Speiseria ambigua were associated with the greatest number of bat species. Species of the genus Carollia were the most abundant and harbored the greatest diversity of flies. The study constitutes the first extensive review of Diptera (Streblidae and Nycteribiidae) in the area and, therefore, contributes to expanding the knowledge of the diversity of ectoparasites of bats in Ecuador.

Keywords: bats, ectoparasites, host, parasitic flies, Ecuadorian coast.

RESUMEN

En Ecuador, los estudios de moscas parásitas de murciélagos son escasos y sesgados hacia la familia Streblidae: los reportes indican la existencia de 50 especies, cinco de ellas en las tierras bajas del occidente. En este estudio, además de Streblidae, incluimos información de la familia Nycteribiidae que no ha sido estudiada en Ecuador. Las dos familias están asociadas a murciélagos de varias localidades del occidente. Utilizamos muestras de la colección asociada de parásitos de la sección de Mamíferos del Museo de Zoología de la Pontificia Universidad Católica del Ecuador (QCAZ-M), así como de la base de datos de la colección para obtener información de los taxones hospederos. Reportamos 145 individuos de murciélagos de 22 especies de las familias Phyllostomidae y Vespertilionidae y 424 individuos y 29 especies de las moscas parásitas. De ellas, cinco especies son nuevos registros para Ecuador, 19 son registros confirmados en el Litoral y ampliamos la distribución geográfica para especies previamente reportadas en esta región. Trichobius joblingi fue la especie de mosca parásita más abundante y, en conjunto con, Speiseria ambigua, se asociaron con el mayor número de especies de murciélagos. Las especies de murciélagos del género Carollia fueron las más abundantes y albergaron la mayor diversidad de moscas. El estudio constituye la primera revisión extensa de dípteros (Streblidae y Nycteribiidae) de la zona y, por consiguiente, contribuye a mejorar el conocimiento de la diversidad de ectoparásitos de murciélagos en Ecuador.

Palabras claves: ectoparásitos, hospedero, murciélagos, moscas parásitas, Costa ecuatoriana.

INTRODUCTION

Ectoparasites are organisms that can adhere and introduce themselves to the skin or its excretions for variable periods (Hopla et al., 1994). They are mainly part of the phylum Arthropoda and are made up of different taxonomic groups, such as fleas (Siphonaptera), lice (Phthiraptera), flies (Diptera), bedbugs (Hemiptera), ticks (Ixodida), and mites (Mesostigmata) (Sánchez et al., 2020).

A characteristic of ectoparasites is the ability to establish associations in the host to protect themselves from the external environment and changes in temperature and humidity, factors that determine their life cycle (Amat-Valero et al., 2013). They use the host as a means of transport to new and suitable habitats, increasing their dispersal capacity (Baumann, 2018).

Around 6000 species of insects have been reported worldwide as external parasites of warm-blooded vertebrates; of these, 742 parasitize bats (Haelewaters et al., 2018; Marshall, 1982). In accordance with the most recent catalogues, Central and South America are inhabited by a comprehensive array of 273 ectoparasite species associated with bats, comprising 187 species of flies (141 belonging to the family Streblidae and 46 within Nycteribiidae), eight flea species, four bedbug species, and 74 mites and tick species (Frank et al., 2014).

It is noteworthy that the families Streblidae and Nycteribiidae have been the primary focus of research in the Neotropical region. As evidenced by various publications, 68 species have been documented in Peru (Minaya et al., 2021), 82 in Colombia (Dick et al., 2016; Graciolli et al., 2016; Pastrana-Montiel et al., 2019), 130 in Venezuela (Guerrero, 2019; Guimarães, 1972; Wenzel, 1976), and 119 in Brazil (Graciolli & Hrycyna, 2023; Hrycyna et al., 2019).

In Ecuador, 59 species of bat ectoparasites have been reported; among these, 54 correspond to the order Diptera (families Streblidae and Nycteribiidae), two belong to the order Prostigmata (Trombiculidae and Myobiidae), two conform the order Mesostigmata (Macronyssidae and Spinturnicidae), and one is member of the order Siphonaptera (Ischnopsyllidae) (Camacho et al., 2014; Correa et al., 2019; Espinoza, 2020; Guerrero, 1997; Guimarães & D’Andretta, 1956; Liu et al., 2020; Salgado, 2019; Stamper, 2012; Tello, 2005). Of these species, five are located on the Ecuadorian Coast and belong to the family Streblidae (Correa et al., 2019; Liu et al., 2020; Tello, 2005).

Of the studies, only Salgado (2019), Stamper (2012), and Tello (2005) focused directly on the study of ectoparasites and bats in Ecuador. It is important to note that research on this topic, and even more so those focused on the Coast, are scattered in time, very scarce, primarily focused on dipterous of the family Streblidae and, therefore, exclude information on other families and orders presents in the country and their association with different species of bats. This is due to two essential aspects: the findings of Streblidae in bats are better documented and this is the ectoparasite family with the highest species richness and most abundant in the Western Hemisphere (Calonge-Camargo & Pérez-Torres, 2018; Reeves et al., 2016; Santos et al., 2016).

The present study consists of an extensive and detailed review covering a larger number of bat species, their parasitic bat flies, and several coastal areas duly associated with the host collection site. In this sense, the objective is to identify the diversity of ectoparasites of the families Streblidae and Nycteribiidae associated with bats in some localities on the Coast of Ecuador.

MATERIALS AND METHODS

Sample

The study sample came from the associated collection of ectoparasites of the Mammalogy Section of the Museo de Zoología at Pontificia Universidad Católica del Ecuador (QCAZ-M) and, specifically, those that registered collection sites on the Ecuadorian Coast. The sample, being conformed by a collection of ectoparasites of bats, contained specimens of different species, so it was necessary to carry out a first revision to isolate the parasitic bat flies of the families Streblidae and Nycteribiidae from the rest of the ectoparasites.

We obtained most of the samples from the project “Caracterización de la Diversidad Biológica y Genética de los Mamíferos del Ecuador” carried out in 2017; a smaller proportion came from the project “Prevalencia y Diversidad Genética de Coronavirus en Murciélagos del Ecuador” carried out in 2021, and only one specimen came from a different project.

Taxonomic identification

We used a stereo microscope to identify specimens to the genus level, and an optical microscope to observe in detail the specific structures required for species identification. In this process, we used several morphological keys (Graciolli, 2004; Guerrero, 1994a, 1994b, 1995a, 1995b, 1996, 1998, 2019; Guimarães & D’Andretta, 1956; Jobling, 1936; Peterson, 1959; Theodor, 1967; Wenzel, 1976; and Wenzel et al., 1966).

We took microscopic photographs based on distinctive taxonomic characters to compare more than two species of the same genus. For species in Streblidae, we photographed the thorax, head, and wings, in addition to capturing images of the entire body for genera with only one species. For species of Nycteribiidae, we focused on taking pictures of the abdomen.

Host information, including identification to species level and site of capture, was obtained from the QCAZ-M database (https://bioweb.bio/faunaweb/mammaliaweb/). We needed to identify some bat specimens that were only available at the genus level. For this, we used the taxonomic key of Diaz et al. (2021).

The annotated list of bat fly species is presented as family, subfamily, genus, and species. The details of each species are divided into three sections: the first includes information about the number of specimens reviewed, locality, collection date, sex of bat flies, and host species; the second corresponds to diagnostic characters, which can be reviewed in detail in the publications of Guerrero (2019), Guimarães & D’Andretta (1956), Wenzel (1976) and Wenzel at al. (1966). The third section provides information on host-parasite interactions according to bibliographic records, as well as relevant findings.

We have maintained the phylogenetic order proposed by Guerrero (2019) in one of his most current works on the family Streblidae. The species of the family Nycteribiidae are organized alphabetically.

The nomenclature for bat host species follows Tirira et al. (2022). The species of bat flies belonging to the families Streblidae and Nycteribiidae, aligns with the nomenclature of Guerrero (2019) and Guimarães & D’Andretta (1956), respectively.

Appendix 1 presents a toponymic index, with all the localities referred to in the text, as well as the species of bat flies and their geographic distribution reported in this study.

RESULTS

Diversity

We recorded 424 parasitic bat flies belonging to nine genera and 26 species of the family Streblidae, and one genus and three species of the family Nycteribiidae. The most abundant bat fly species were Trichobius joblingi (24%) and Basilia ferrisi (21%) (Table 1).

In terms of bat hosts, we obtained information from 145 individuals of two families, 13 genera and 22 species (Phyllostomidae, n = 18; Vespertilionidae, n = 4). Carollia brevicauda (15%), C. perspicillata (14%), and C. castanea (12%) were the most abundant species (Table 1; Figure 1).

In the context of host-parasite interactions, Trichobius joblingi and Speiseria ambigua were associated with the highest number of host species: five each (Table 1). Similarly, Carollia brevicauda, C. castanea, and Glossophaga soricina harbored five species of parasitic flies (Figure 1).

New records

Of the 29 species analyzed, five (17%) are new records for Ecuador, 19 (66%) are confirmed records from the Ecuadorian Coast, and three (10%) correspond to previous report in other regions of Ecuador (Sierra and Amazonia). In addition, we were not able to determine the species for two morphotypes from Trichobius (Streblidae) and Basilia (Nycteribiidae) (Table 1).

We report the presence of Streblidae and Nycteribiidae species in nine localities distributed in Esmeraldas, Manabí, Santo Domingo de los Tsáchilas, Los Ríos, and El Oro, provinces (Figure 2). Records in Manabí and Los Ríos correspond to new distribution data for Strebla altmani, Speiseria ambigua, and Trichobius joblingi.

Annotated list of
ectoparasite species

Family Streblidae Kolenati, 1863

Subfamily Trichobiinae Jobling, 1936

Genus Trichobius Gervais, 1844

Trichobius uniformis Curran, 1935

Figure 3A

Material examined [6]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 23.XI.2021, 1♂, 1♀ ex Glossophaga soricina; 25.XI.2021, 1♂, 1♀ ex Glossophaga soricina; 26.XI.2021, 1♂ ex Lonchophylla concava • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 1♂ ex Glossophaga soricina.

Identification: The species was identified from the presence of setae on the basal angle of vein 6 of the wing. In addition, vein R1 is straight, and each occipital lobe has a tubercle on the posterior edge (Guerrero, 1994a).

Remarks: Trichobius uniformis is a characteristic species of the genus Glossophaga, particularly associated with Glossophaga soricina (Cuxim-Koyoc et al., 2018; Wenzel, 1976), which is the same host reported from Ecuador (Stamper, 2012). In this study, we found this species in association with Lonchophylla concava.

Trichobius longipes (Rudow, 1871)

Figure 3B

Material examined [1]: Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 25.VII.2017, 1♂ ex Phyllostomus hastatus.

Identification: This species is distinguished by short setae along the anterior margin of the prescutum and long ones along the midline. Also, those found in the lateral rows are longer compared to those found in the center (Guerrero, 1994a, 2019).

Remarks: Although Phyllostomus hastatus is the characteristic host of Trichobius longipes (Wenzel, 1976), several species of the family Phyllostomidae have been reported as hosts in Ecuador (Stamper, 2012).

Trichobius costalimai Guimarães, 1938

Figure 3C

Material examined [11]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 27.XI.2021, 2♂, 2♀ ex Phyllostomus discolor • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 21.VII.2017, 7♂ ex Phyllostomus discolor.

Identification: It is possible to differentiate between 10 to 12 setae in the anterolateral region of the prescutum and short setae between the transverse and median sutures of the mesonotum. These characteristics are exclusive to this species (Guerrero, 1994a).

Remarks: Phyllostomus discolor is the main host of Trichobius costalimai (Wenzel, 1976), also occurring in Ecuador (Stamper, 2012).

Trichobius dugesii Townsend, 1891

Figure 3D

Material examined [5]: Esmeraldas: Eloy Alfaro, La Tola, Finca Cocadilla; 21.VIII.2017, 1♂, 2♀ ex Glossophaga soricina • Eloy Alfaro, La Tola, Centro de Interpretación Majagual; 19.VIII.2017, 1♀ ex Glossophaga soricina; 22.VIII.2017, 1♀ ex Glossophaga soricina.

Identification: The antescutellar setae of Trichobius dugesii are shorter, and the setae of the prescutum are gradually reduced towards the discal area. Also, behind the lateral lobe of tergum 1+2, no long setae are evident in females, but in males, sternum 6 is present (Guerrero, 1995a).

Remarks: Glossophaga soricina is considered the main host of Trichobius dugesii (Dick & Gettinger, 2005). However, in Ecuador, it is also found on Artibeus lituratus and Carollia brevicauda (Stamper, 2012).

Trichobius joblingi Wenzel, 1966

Figure 3E

Material examined [100]: Esmeraldas: Eloy Alfaro, La Tola, Finca Cocadilla; 21.VIII.2017, 2♂ ex Carollia perspicillata • Eloy Alfaro, La Tola, Centro de Interpretación Majagual; 21.VIII.2017, 1♂ ex Glossophaga soricina, 1♂ ex Carollia perspicillata • Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 25.VIII.2017, 1♂, 3♀ ex Carollia perspicillata • Quinindé, Rosa Zárate, Jaboncillo, Finca La Esperanza; 09.IX.2021, 4♂, 5♀ ex Carollia brevicauda, 1♂ ex Carollia castanea, 3♂, 1♀ ex Carollia perspicillata • Manabí: El Carmen, El Carmen, comunidad El Zapote; 20.XI.2021, 2♂, 1♀ ex Carollia brevicauda; 25.XI.2021, 3♂, 2♀ ex Carollia brevicauda; 26.XI.2021, 4♂ ex Carollia brevicauda; 20.XI.2021, 1♀ ex Carollia castanea; 24.XI.2021, 3♂ ex Carollia castanea; 25.XI.2021, 1♂ ex Carollia castanea; 26.XI.2021, 1♂, 2♀ ex Carollia castanea; 19.XI.2021, 1♂, 1♀ ex Carollia perspicillata; 23.XI.2021, 3♂, 5♀ ex Carollia perspicillata; 24.XI.2021, 1♂, 1♀ ex Carollia perspicillata; 26.XI.2021, 1♂, 2♀ ex Carollia perspicillata; 19.XI.2021, 1♂ ex Myotis riparius • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 6♂, 6♀ ex Carollia brevicauda; 23.VII.2017, 1♂, 2♀ ex Carollia brevicauda; 25.VII.2017, 4♂, 2♀ ex Carollia brevicauda; 21.VII.2017, 2♂, 1♀ ex Carollia castanea; 24.VII.2017, 3♂, 3♀ ex Carollia castanea; 22.VII.2017, 2♂, 5♀ ex Carollia perspicillata; 23.VII.2017, 1♂ ex Carollia perspicillata; 25.VII.2017, 3♂ ex Carollia perspicillata.

Identification: It is possible to differentiate Trichobius joblingi by the combination of short and long setae on the antescutellar row and prescutellar setae that gradually shorten to the discal area. Behind the lateral lobe of tergum 1+2 there are two to five long setae in females, while sternum 6 is observed in the males (Guerrero, 1995a).

Remarks: According to Wenzel (1976), Carollia perspicillata is the characteristic host of Trichobius joblingi, although in Ecuador it is also reported in 10 species of the families Phyllostomidae and Vespertilionidae (Stamper, 2012; Tello, 2005). In this study, we report Trichobius joblingi associated with Glossophaga soricina and Myotis riparius; for the first species, there are no previous mentions of this type of association.

Trichobius parasiticus Gervais, 1844

Figure 3F

Material examined [2]: El Oro: Zaruma, Zaruma, Cerro Zaruma Urcu; 2♂ ex Platyrrhinus sp.

Identification: The mesonotum of Trichobius parasiticus has distinctive characteristics that make it easy to recognize, such as long setae on the anterolateral angles of the prescutum, short setae arranged in a row anterior to the transverse suture and the antescutellar row (Guerrero, 1995a).

Remarks: According to Wenzel (1976), the primary host of Trichobius parasiticus is Desmodus rotundus, but it has also been documented in Glossophaga soricina in Ecuador (Stamper, 2012).

Trichobius dugesioides Wenzel, 1966

Figure 3G

Material examined [25]: Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 21.VII.2017, 2♂, 2♀ ex Trachops cirrhosus; 25.VII.2017, 1♂, 1♀ ex Carollia brevicauda, 2♂ ex Lonchorhina aurita; 26.VII.2017, 9♂, 8♀ ex Trachops cirrhosus.

Identification: Trichobius dugesioides can be identified by the row of antescutellar setae slightly longer than those preceding it. In addition, sternite 7 has 13 to 14 setae in females, and tergite 9 has 17 to 18 setae in males (Guerrero, 1998).

Remarks: Trachops cirrhosus is the main host species of this parasite (Wenzel, 1976). However, in Ecuador, it was also associated with Phyllostomus elongatus (Stamper, 2012). In this study, we found this species in association with Lonchorhina aurita and Carollia brevicauda.

Trichobius flagellatus Wenzel, 1976

Figure 3H

Material examined [14]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 19.XI.2021, 3♂, 7♀ ex Lonchorhina aurita • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 25.VII.2017, 2♂, 2♀ ex Lonchorhina aurita.

Identification: In this species, the setae of the antescutellar row are the same size as those preceding them. Also, very small setae are found behind the lateral lobes of tergum 1+2 of females and males have 22 to 25 setae on tergum 9 (Guerrero, 1995a).

Remarks: Lonchorhina aurita is the main host of Trichobius flagellatus (Wenzel, 1976).

Trichobius anducei Guerrero, 1998

Figure 3I

Material examined [14]: Esmeraldas: Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 25.VIII.2017, 1♂ ex Carollia perspicillata • Manabí: El Carmen, El Carmen, comunidad El Zapote; 20.XI.2021, 1♀ ex Carollia brevicauda; 23.XI.2021, 1♀ ex Carollia perspicillata; 24.XI.2021, 1♂, 1♀ ex Carollia brevicauda, 1♀ ex Carollia castanea; 26.XI.2021, 1♂ ex Carollia perspicillata • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 1♂ ex Carollia brevicauda; 23.VII.2017, 1♀ ex Carollia brevicauda; 25.VII.2017, 1♂, 1♀ ex Carollia castanea, 3♂ ex Carollia perspicillata.

Identification: Females of Trichobius anducei differ in having a more extended band of setae on the lateral margin of the abdomen, as well as 9 to 11 setae on sternite 7. In contrast, the tergite 9 of males has 11 to 12 setae (Guerrero, 1998).

Remarks: Trichobius anducei parasitizes mainly Carollia perspicillata (Guerrero, 2019; Hiller et al., 2021); however, in Ecuador, it was also associated with Carollia brevicauda (Stamper, 2012). Furthermore, in this study, we document that Trichobius anducei parasitizes Carollia castanea.

Trichobius sp. (complex dugesii)

Figure 3J

Material examined [1]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 19.XI.2021, 1♂ ex Platyrrhinus umbratus.

Remarks: We were unable to identify this species; however, it has specific characteristics close to Trichobius angulatus such as the angled transverse suture, prescutellar setae shortening towards the center and setae of the antescutellar row longer than the predecessors (Guerrero, 1995a).

Genus Trichobioides Wenzel, 1966

Trichobioides perspicillatus (Pessôa & Galvao, 1937)

Figure 4

Material examined [15]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 23.XI.2021, 5♂, 2♀ ex Phyllostomus discolor; 26.XI.2021, 1♂ ex Carollia castanea; 27.XI.2021, 2♂, 2♀ ex Phyllostomus discolor • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 21.VII.2017, 2♂, 1♀ ex Phyllostomus discolor.

Identification: There is only one species in the genus Trichobioides. Although it is very similar to Trichobius, the difference lies in the median suture that extends to the transverse suture but does not unite. Also, a row of short and long antescutellar setae is present (Guerrero, 1994b).

Remarks: According to Wenzel (1976), Trichobioides perspicillatus is the parasite commonly associated with Phyllostomus discolor, a situation also evidenced by Stamper (2012) in Ecuador. In this study, we found an association with Carollia castanea that has not previously documented.

Genus Speiseria Kessel, 1925

Speiseria ambigua Kessel, 1925

Figure 5

Material examined [23]: Esmeraldas: Eloy Alfaro, La Tola, Finca Cocadilla; 21.VIII.2017, 1♂, 1♀ ex Glossophaga soricina, 1♀ ex Carollia perspicillata • Eloy Alfaro, La Tola, Centro de Interpretación Majagual; 21.VIII.2017, 1♂ ex Carollia perspicillata • Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 25.VIII.2017, 1♀ ex Carollia castanea, 1♂, 1♀ ex Carollia perspicillata • Manabí: El Carmen, El Carmen, comunidad El Zapote; 19.XI.2021, 1♂ ex Lonchorhina aurita; 20.XI.2021, 1♂, 1♀ ex Carollia castanea; 23.XI.2021, 1♂ ex Carollia castanea; 24.XI.2021, 1♂ ex Carollia brevicauda, 1♀ ex Carollia castanea, 1♂ ex Carollia perspicillata; 25.XI.2021, 1♂ ex Carollia castanea • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 3♂, 2♀ ex Carollia brevicauda, 1♀ ex Carollia castanea; 25.VII.2017, 1♂, 1♀ ex Carollia perspicillata.

Identification: In this species, females are distinguished by having tergum 7 longer than the supra-anal plate and with parallel sides. In contrast, males exhibit strongly curved postgonites and tergum 9 between nine and ten setae (Guerrero, 1994b).

Remarks: According to Wenzel (1976), Speiseria ambigua infests mainly Carollia perspicillata; but in Ecuador, it was also associated with several species of the family Phyllostomidae and with greater incidence in bats of the genus Carollia (Stamper, 2012; Tello, 2005). Additionally, during the research, we documented a new association with Glossophaga soricina.

Genus Paratrichobius Costa Lima, 1921

Paratrichobius longicrus (Miranda-Ribeiro, 1907)

Figure 6A

Material examined [2]: Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 25.VII.2017, 1♂, 1♀ ex Artibeus lituratus.

Identification: The relevant characteristics of this species are the rounded anterior angles on the pronotum and the internal face of the profemurs covered only by small setae accompanied by a row of six thick spines (Guerrero, 1994b).

Remarks: Artibeus lituratus is the characteristic host of Paratrichobius longicrus (Dick & Gettinger, 2005; Wenzel,1976), and the same host has been reported in Ecuador (Stamper, 2012).

Paratrichobius dunni (Curran, 1935)

Figure 6B

Material examined [4]: Manabí: Manta, San Lorenzo, Refugio de Vida Silvestre Marino Costera Pacoche; 09.IX.2017, 1♂, 3♀ ex Uroderma convexum.

Identification: Paratrichobius dunni was identified by the straight anterior angles of the pronotum and its profemurs, with two to three short spines extending parallel to a line of six thick spines on the inner side (Guerrero, 1994b).

Remarks: It is mainly found in species of the genus Uroderma, especially in Uroderma bilobatum (Guerrero, 2019; Hiller et al., 2021).

Genus Megistopoda Macquart, 1852

Megistopoda aranea (Coquillet, 1899)

Figure 7A

Material examined [8]: Manabí: Manta, San Lorenzo, Refugio de Vida Silvestre Marino Costera Pacoche; 09.IX.2017, 1♂, 1♀ ex Artibeus fraterculus • El Carmen, El Carmen, comunidad El Zapote; 19.XI.2021, 3♂, 1♀ ex Platyrrhinus umbratus • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 1♂, 1♀ ex Artibeus lituratus.

Identification: This species has narrow wings with four longitudinal veins, long hind legs, and a scutellum with two macrosetae (Guerrero, 1994b).

Remarks: Dick & Gettinger (2005) state that Artibeus fimbriatus and A. jamaicensis are the primary hosts of Megistopoda aranea. However, Stamper (2012) indicates that in Ecuador, it has been reported in association with several species of the family Phyllostomidae. In addition, in the study, we document the association with Platyrrhinus umbratus.

Megistopoda proxima (Seguy, 1926)

Figure 7B

Material examined [9]: Esmeraldas: Quinindé, Rosa Zárate, Jaboncillo, Finca La Esperanza; 09.IX.2021, 1♂ ex Sturnira bakeri • Manabí: El Carmen, El Carmen, comunidad El Zapote; 25.XI.2021, 3♀ ex Sturnira bakeri; 26.XI.2021, 1♀ ex Sturnira bakeri; 26.XI.2021, 1♀ ex Sturnira ludovici • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 1♂ ex Sturnira bakeri; 25.VII.2017, 1♀ ex Sturnira bakeri; 27.VII.2017, 1♀ ex Sturnira bakeri.

Identification: Megistopoda proxima is distinguished by its broad wings with six longitudinal veins and the scutellum with four macrosetae (Guerrero, 1994b).

Remarks: Dick and Gettinger (2005) mention that Sturnira lilium is the main host of Megistopoda proxima. However, in Ecuador, it is also found in different species of the genus Sturnira (Stamper, 2012).

Genus Aspidoptera Coquillett, 1899

Aspidoptera phyllostomatis (Perty, 1833)

Figure 8A

Material examined [5]: Manabí: Manta, San Lorenzo, Refugio de Vida Silvestre Marino Costera Pacoche; 09.IX.2017, 2♂, 2♀ ex Artibeus fraterculus; 11.IX.2017, 1♀ ex Artibeus fraterculus.

Identification: Unlike Aspidoptera falcata, the mesepisternum of this species exhibits long setae on the dorsal side and shorter on the periphery. Likewise, the supra-anal plate of females has a short seta; in males, the postgonites are slightly curved (Guerrero, 1995b).

Remarks: Aspidoptera phyllostomatis is mainly found in Artibeus jamaicensis (Wenzel, 1976). However, in Ecuador, we reported in other species of the genus Artibeus (Stamper, 2012).

Aspidoptera falcata Wenzel, 1976

Figure 8B

Material examined [2]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 26.XI.2021, 1♂, 1♀ ex Sturnira ludovici.

Identification: In contrast to Aspidoptera phyllostomatis, this species has a more setose appearance and the setae on the dorsal surface of the mesepisternum are long. In addition, in females, the supra-anal plate includes six apical macrosetae and a short seta on each side of the anterior ones; on the other hand, males have very curved postgonites (Wenzel et al., 1966; Wenzel,1976).

Remarks: Although Sturnira lilium is the primary host of Aspidoptera falcata (Dick & Gettinger, 2005), most of the parasitized species in Ecuador belong to the genus Sturnira (Stamper, 2012).

Genus Exastinion Wenzel, 1966

Exastinion clovisi (Pessôa & Guimarães, 1936)

Figure 9

Material examined [1]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 19.XI.2021, 1♀ ex Carollia castanea.

Identification: This species is characterized by the presence of eight setae on the scutum, and a very setose area on sternum 2 that extends anteriorly to the middle. In addition, females have a group of five setae on the abdominal connexivum that are longer than the following ones (Wenzel, 1976).

Remarks: In this study, we document that Exastinion clovisi parasitizes Carollia castanea; Stamper (2012) also evidenced its association with Glossophaga soricina in Ecuador. The characteristic host is Anoura geoffroyi (Guerrero, 2019).

Subfamily Streblinae Jobling, 1936

Genus Strebla Wiedemann, 1824

Strebla mirabilis (Waterhouse, 1879)

Figure 10A

Material examined [21]: Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 21.VII.2017, 1♂ ex Trachops cirrhosus; 26.VII.2017, 8♂, 12♀ ex Trachops cirrhosus.

Identification: Unlike other species, Strebla mirabilis has eyes with several facets, a pointed anterior end of the postvertex that forms an angle close to 90 degrees and, finally, all setae are strong. In addition, the metatibia has two to three macrosetae; and on the mesonotum, between the transverse and pigmented suture, three rows of setae are located (Guerrero, 2019; Wenzel et al., 1966).

Remarks: Although Strebla mirabilis is commonly associated with Trachops cirrhosus (Wenzel, 1976), hosts in Ecuador include several species of the family Phyllostomidae (Stamper, 2012).

Strebla guajiro (García & Casal, 1965)

Figure 10B

Material examined [16]: Esmeraldas: Quinindé, Rosa Zárate, Jaboncillo, Finca La Esperanza; 09.IX.2021, 1♂ ex Carollia brevicauda • Eloy Alfaro, La Tola, Finca Cocadilla; 21.VIII.2017, 1♂ ex Carollia perspicillata • Eloy Alfaro, La Tola, Centro de Interpretación Majagual; 21.VIII.2017, 1♀ ex Carollia perspicillata • Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 25.VIII.2017, 1♀ ex Carollia perspicillata • Manabí: El Carmen, El Carmen, comunidad El Zapote; 25.XI.2021, 1♂, 1♀ ex Carollia brevicauda; 26.XI.2021, 1♀ ex Carollia perspicillata • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 22.VII.2017, 5♂, 4♀ ex Carollia brevicauda.

Identification: The anterior end of the postvertex of Strebla guajiro is more rounded than in other species and forms an angle of fewer than 90 degrees. All its setae are strong, and two to three rows are found between the transverse and pigmented suture, as well as two or three macrosetae on the metatibia (Guerrero, 1996; Wenzel et al., 1966).

Remarks: Strebla guajiro is mainly associated with Carollia perspicillata (Dick & Gettinger, 2005; Wenzel, 1976). In the case of Ecuador, it usually also parasitizes several species of the family Phyllostomidae, especially bats of the genus Carollia (Stamper, 2012; Tello, 2005).

Strebla hertigi Wenzel, 1966

Figure 10C

Material examined [2]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 23.XI.2021, 1♀ ex Phyllostomus hastatus; 27.XI.2021, 1♂ ex Phyllostomus discolor.

Identification: Strebla hertigi has a distinctive subquadrate postvertex, the anterior end of which forms an angle greater than 120 degrees; in addition, the internal setae of the occipital plates are short; there are three rows of setae located between the transverse and pigmented sutures on the mesonotum; finally, the metatibia has two to three macrosetae (Guerrero, 1996; Wenzel et al., 1966).

Remarks: Strebla hertigi is a characteristic parasite of Phyllostomus discolor (Wenzel, 1976). According to Stamper (2012), this species is associated with Phyllostomus discolor and Phyllostomus hastatus in Ecuador.

Strebla galindoi Wenzel, 1966

Figure 10D

Material examined [32]: Esmeraldas: Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 25.VIII.2017, 19♂, 13♀ ex Tonatia bakeri.

Identification: It is possible to recognize this species by several characteristics: it has eight facets on the eyes; the anterior end of the postvertex forms an angle greater than 120 degrees; its setae are thin and elongated; before the pigmented suture on the mesonotum, a row of longer setae stands out; finally, it has three large setae on the metatibia (Guerrero, 1996).

Remarks: Tonatia bidens is the characteristic host of Strebla galindoi (Wenzel, 1976). In Ecuador, this species parasitizes those of the genus Tonatia (Stamper, 2012).

Strebla machadoi Wenzel, 1966

Figure 10E

Material examined [2]: Santo Domingo de los Tsáchilas: Santo Domingo de los Colorados, Alluriquín, La Unión del Toachi; 09.IX.2017, 2♂ ex Micronycteris simmonsae.

Identification: Strebla machadoi has eyes with a single facet, a postvertex with a pointed anterior end forming an angle of fewer than 45 degrees, and two dorsal rows containing six to eight setae longer than the rest on the metatibia (Guerrero, 1996; Wenzel et al., 1966).

Remarks: Strebla machadoi parasitizes some species of Micronycteris (Guerrero, 2019).

Strebla altmani Wenzel, 1966

Figure 10F

Material examined [5]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 19.IX.2021, 2♂, 1♀ ex Lonchorhina aurita • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 25.VII.2017, 1♂, 1♀ ex Lonchorhina aurita.

Identification: This species is distinguished by the following characteristics: six facets are identified on the eyes; the anterior end of the postvertex is pointed and forms an angle close to 90 degrees; the internal setae of the occipital plates are very short and thin; between the transverse and pigmented suture of the mesonotum there are two to three rows of setae; finally, two of the setae of the metatibia are noticeably longer (Guerrero, 1996).

Remarks: Lonchorhina aurita is the characteristic host of Strebla altmani (Guerrero, 2019).

Genus Metelasmus Coquillett, 1907

Metelasmus pseudopterus Coquillett, 1907

Figure 11

Material examined [1]: Manabí: El Carmen, El Carmen, comunidad El Zapote; 23.IX.2021, 1♀ ex Artibeus lituratus.

Identification: According to Guerrero (2019), only one species of the genus Metelasmus has been determined so far. Its characteristics include the following: well-developed frontoclypeus; large postvertex, with triangular anterior margin and flattened posterior margin and two strong setae; it also has a hook-shaped postgena with a remiform seta; complete ctenidium; small wings with reduced venation; posterior tibiae with very small setae and, finally, setae that completely covering the dorsal connexivum (Guerrero, 2019; Jobling, 1936).

Remarks: Metelasmus pseudopterus was reported by Wenzel (1976) as a characteristic parasite of Artibeus jamaicensis. In Ecuador, it also parasitizes some species of Artibeus (Stamper, 2012).

Family Nycteribiidae Samouelle, 1819

Subfamily Nycteribiinae Samouelle, 1819

Genus Basilia Miranda-Ribeiro, 1903

Basilia carteri Scott, 1936

Figure 12A

Material examined [7]: Esmeraldas: Quinindé, Rosa Zárate, Jaboncillo, Finca La Esperanza; 09.IX.2021, 1♂, 1♀ ex Myotis nigricans • Manabí: El Carmen, El Carmen, comunidad El Zapote; 24.XI.2021, 2♂, 3♀ ex Myotis albescens.

Identification: Females of Basilia carteri are differentiated by tergite 1 having eight to nine long setae on the posterior margin, while tergite 2 has a subcodiform shape with very few disc-like setae. Conversely, males exhibit a sternite V with two asymmetrical rows of setae (Graciolli, 2004).

Remarks: Basilia carteri has been documented in association with Myotis albescens, M. levis, M. nigricans, and M. riparius; also, with Tadarida brasiliensis (Autino et al., 2009).

Basilia ferrisi Schuurmans Stekhoven, 1931

Figure 12B

Material examined [88]: Esmeraldas: Eloy Alfaro, La Tola, Finca Cocadilla; 20.XII.2017, 1♂ ex Glossophaga soricina • Eloy Alfaro, La Tola, Centro de Interpretación Majagual; 23.VIII.2017, 1♀ ex Myotis nigricans • Eloy Alfaro, Luis Vargas Torres, Playa de Oro; 23. VIII.2017, 1♀ ex Myotis riparius; 25.VIII.2017, 8♂, 26♀ ex Myotis riparius • Manabí: El Carmen, El Carmen, comunidad El Zapote; 26.XI.2021, 2♂, 1♀ ex Myotis riparius • Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 20.VII.2017, 6♂, 15♀ ex Myotis diminutus; 24.VII.2017, 5♂, 6♀ ex Myotis diminutus; 27.VII.2017, 1♂, 7♀ ex Myotis diminutus; 27.VII.2017, 3♂, 5♀ ex Myotis nigricans.

Identification: Tergite 1 of females is very long in this species and has six to nine bristles on the posterior margin. In contrast, the sternite V of males is slightly rounded and with a small notch in the middle (Guimarães & D’Andretta, 1956; Peterson, 1959).

Remarks: Basilia ferrisi is associated with Carollia brevicauda, Histiotus montanus, Myotis nigricans, and M. keaysi (Raigosa et al., 2020); however, in Ecuador, it was also associated with bats of the genus Myotis and Platyrrhinus matapalensis (Stamper, 2012). In addition, we report the association with Myotis diminutus and Glossophaga soricina.

Basilia sp. (group ferruginea)

Figure 12C

Material examined [2]: Los Ríos: Buena Fe, Patricia Pilar, Centro Científico Río Palenque; 21.VII.2017, 2♀ ex Myotis riparius.

Remarks: We were unable to identify this species; however, the bilobed tergite 2 is a characteristic of the ferruginea group (Theodor, 1967).

DISCUSSION

Ecuador, known for its remarkable biodiversity (Mittermeier et al., 2011), lacks comprehensive information about specific taxonomic groups such as the parasitic bat flies from the families Streblidae and Nycteribiidae. Most of the known records come from localities in Amazonia, and only five species have been documented in the few studies conducted on the Coast (Camacho et al., 2014; Correa et al., 2019; Guerrero, 1997; Guimarães & D’Andretta, 1956; Liu et al., 2020; Stamper, 2012; Tello, 2005). This study aims to address this knowledge gap by providing valuable insights. Our findings contribute to the knowledge of bat flies of the families Streblidae and Nycteribiidae, as we have documented new records for Ecuador (Trichobius flagellatus, Paratrichobius dunni, Strebla machadoi, S. altmani, and Basilia carteri), bringing the species richness to 61. In addition, their geographic range has expanded, as they had previously only been documented in countries such as Argentina, Panama, Mexico, and Venezuela (Cuxim-Koyoc et al., 2018; Guerrero, 2019; Hiller et al., 2021; Oscherov et al., 2012). Notably, in the coastal region, the species count has shown a substantial increase from 5 to 31.

Stamper (2012), documented 42 species of bat flies in Ecuador, 19 of which we report in this study. However, Stamper’s study provided only general locality descriptions without additional information that could establish a direct association between each specimen and its collection site. This lack of specific data has raised concerns regarding the accurate distribution patterns of these species. Our research considers these findings as confirmed records specifically within the Ecuadorian coastal region, offering more precise insights into their distribution. Trichobius joblingi, Speiseria ambigua, and Strebla guajiro had already been documented in Morona Santiago, Orellana, Pastaza, Cotopaxi, Pichincha, Esmeraldas, and Santo Domingo de los Tsáchilas (Tello, 2005). This study extends the records to Manabí and Los Ríos.

The most abundant fly parasite was Trichobius joblingi, and some of the factors influencing these results are probably due to the fact that it is a generalist species (Barbier & Bernard, 2017; Tlapaya-Romero et al., 2015), which has been reported parasitizing several bat species (de Groot et al., 2020; Santos et al., 2016; Soares et al., 2017). Additionally, previous research mentions that parasite abundance is related to host abundance (Ascuntar-Osnas et al., 2020; Cuxim-Koyoc et al., 2015). Carollia perspicillata is the main host (Wenzel, 1976), and in the present investigation, it is documented among the most abundant bat species, along with Carollia brevicauda and C. castanea, all widely distributed on the Ecuadorian Coast (Tirira, 2017).

Bat flies are highly host-specific, that is, they parasitize a single bat species (Dick & Gettinger, 2005; Wenzel et al., 1966; Wenzel, 1976;). However, we report some novel interactions, such as the association of one bat fly species with multiple host species, as well as the presence of several bat fly species on the same host, which have also been documented in previous research (Barbier & Graciolli, 2016; da Silva et al., 2023; Durán et al., 2017; França et al., 2013; Lira-Olguin et al., 2020; Menezes et al., 2021). Factors such as sample contamination, transfers due to disturbance at the time of capture (Dick, 2007; Fritz, 1983), and accidental transfers when bat hosts share roosts with other species (Aguiar & Antonini, 2016; Barbier & Bernard, 2017; Hernández-Martínez et al., 2019; ter Hofstede et al., 2004), could explain these findings. It is important to clarify that the aim of the present study did not include at any time to assess specificity or factors influencing host-parasite associations. Therefore, these aspects were not explored to avoid misinterpretations, but relevant association findings that may be the subject of future research were documented.

It is important to point out that during the taxonomic identification process there were certain limitations since it was not possible to determine the species level in three individuals, due to taxonomical publications with ambiguous descriptions and outdated illustrations. The taxonomic keys used for the family Streblidae are the result of very complete works that include the description of a large number of species. On the other hand, the information on the family Nycteribiidae is scattered; in fact, most of the available works describe mainly females and relegate the identification of males to the background. Several of these problems coincide with those described by Lira-Olguin et al. (2020) and Trujillo-Pahua & Ibáñez-Bernal (2019, 2020), demonstrating the need for further research on this taxon.

According to studies by Barbier & Bernard (2017) and Dick & Gettinger (2005), the great variety of bat fly species is correlated with host diversity. Under this premise, we consider that the current species richness of the families Streblidae and Nycteribiidae is still underestimated, since 179 species of bats have been reported in Ecuador (Tirira et al., 2022), 120 of them in the Coast (Brito et al., 2023; Carrera et al., 2010). Along the same lines, in countries of the region with a similar number of bat species, there are even twice as many records of flies that parasitize them, in contrast to those documented at the national level. A notable example is Brazil, which has 181 species of bats (Garbino et al., 2022) and 119 species of the family Streblidae and Nycteribiidae (Graciolli & Hrycyna, 2023; Hrycyna et al., 2019); it also ranks among the nations with the highest number of publications on the taxonomic group under discussion (Urbieta et al., 2022). This shows that there are several species to be identified and, therefore, it is relevant to propose more studies such as the one carried out throughout this research.

The natural history collections reflect the planet’s biota over time (Bradley et al., 2014). Therefore, the results of this research, obtained based on museum specimens and associated data, provide valuable information on this taxonomic group in the country, which evidences the importance of the collections and the need to continue collecting more specimens as possible.

Future research should include the analysis of specimens in other regions and from different families, as well as the use of molecular techniques that facilitate species identification and validate the findings of host-parasite interaction reported in this study. Undoubtedly, works such as this one contributes to expanding the knowledge of the diversity of parasitic bat flies in the country and consolidate the basis for future research to address ecological and evolutionary questions due to the close relationship of bat flies with their hosts (Brown et al., 2022; Hiller et al., 2020). They are also important in the public health area since bat flies are reservoirs of viruses and bacteria and could act as vectors of zoonotic pathogens (Lee et al., 2021; Morse et al., 2012; Ramirez-Martinez et al., 2021).

CONCLUSION

The study contributed to increasing the knowledge of the diversity of parasitic bat flies as well as broadening their distribution. The document also consolidates baseline information on host-parasite associations and establishes the first collection with the largest number of identified bat fly species of the families Streblidae and Nycteribiidae in the Ecuadorian coastal region.

Acknowledgements: Special thanks to Santiago F. Burneo, curator of the Mammalogy Section of the Museo de Zoología of the Pontificia Universidad Católica del Ecuador (QCAZ-M), for authorizing the use of the ectoparasite collection and for his comments on the manuscript. Also, to Carlos Carrión-Bonilla, who through his research contributed to this collection. Also, to the Centro de Investigación para la Salud en América Latina (CISeAL) and the Invertebrate Section of the Museo de Zoología of the Pontificia Universidad Católica del Ecuador (QCAZ-I) for facilitating the use of their microscopy equipment. Finally, to Fernando Anaguano for his recommendations in the elaboration of the map, to Gustavo Graciolli for sharing bibliographic material, to Jessica Revelo, Kevin Lievano, Fabián Sáenz, Marcela Lareschi, and two anonymous reviewer who provided valuable comments to the manuscript.

Conflict of Interest Statement: The authors declare that they have no conflicts of interest.

Author contributions: KP: design of the research plan, analysis of the information, taking photographs, and drafting of the manuscript. KP and ALP: elaboration of the database, peer review. and identification of bat fly species and bat species. MAC: design of the research plan, logistical support, and manuscript review.

Orcid:

KP https://orcid.org/0009-0004-9438-4603

APC https://orcid.org/0000-0002-6956-570X

MAC https://orcid.org/0000-0001-7965-184X

REFERENCES

Aguiar, L. M. S., & Antonini, Y. (2016). Prevalence and intensity of Streblidae in bats from a Neotropical savanna region in Brazil. Folia Parasitologica, 63, 1–8. https://doi.org/10.14411/fp.2016.024

Amat-Valero, M., Calero-Torralbo, M. A., & Valera, F. (2013). Temperature during the free-living phase of an ectoparasite influences the emergence pattern of the infective phase. Parasitology, 140(11), 1357–1367. https://doi.org/10.1017/S0031182013000929

Ascuntar-Osnas, O., Montoya-Bustamante, S., & González-Chávez, B. (2020). Records of Streblidae (Diptera: Hippoboscoidea) in a tropical dry forest fragment in Colombia. Biota Colombiana, 21(1), 16–27. https://doi.org/10.21068/c2020.v21n01a02

Autino, A. G., Claps, G. L., Sánchez, M. S., & Barquez, R. M. (2009). New records of bat ectoparasites (Diptera, Hemiptera and Siphonaptera) from northern Argentina. Neotropical Entomology, 38(2), 165–177. https://doi.org/10.1590/s1519-566x2009000200002

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. Studies on Neotropical Fauna and Environment, 51(3), 176–187. https://doi.org/10.1080/01650521.2016.1215042

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(11), 3043–3055. https://doi.org/10.1007/s00436-017-5615-7

Baumann, J. (2018). Tiny mites on a great journey-a review on scutacarid mites as phoronts and inquilines (Heterostigmatina, Pygmephoroidea, Scutacaridae). Acarologia, 58(1), 192–251. https://doi.org/10.24349/acarologia/20184238

Bradley, R. D., Bradley, L. C., Garner, H. J., & Baker, R. J. (2014). Assessing the value of Natural History collections and addressing issues regarding long-term growth and care. BioScience, 64(12), 1150–1158. https://doi.org/10.1093/biosci/biu166

Brito, J., Camacho, M. A., Romero, V., & Vallejo, A. F. 2023. Mamíferos del Ecuador. Versión 2023.0. Museo de Zoología, Pontificia Universidad Católica del Ecuador. https://bioweb.bio/faunaweb/mammaliaweb/

Brown, A. M., Speer, K. A., Teixeira, T., Clare, E., Simmons, N. B., Balbuena, J. A., Dick, C. W., Dittmar, K., & Perkins, S. (2022). Phylogenetic and ecological trends in specialization: Disentangling the drivers of ectoparasite host specificity. BioRxiv, https://doi.org/10.1101/2022.04.06.487338

Calonge-Camargo, B., & Pérez-Torres, J. (2018). Ectoparasites (Polyctenidae, Streblidae, Nycteribiidae) of bats (Mammalia: Chiroptera) from the Caribbean region of Colombia. Therya, 9(2), 171–178. https://doi.org/10.12933/therya-18-492

Camacho, M. A., Tirira, D. G., Dick, C. W., & Burneo, S. F. (2014). Lophostoma carrikeri (Allen, 1910) (Chiroptera: Phyllostomidae): first confirmed records in Ecuador. Check List, 10(1), 217–220. https://doi.org/10.15560/10.1.217

Carrera, J. P., Solari, S., Larsen, P. A., Alvarado, D.F., Brown, A.D., Carrión, C., Tello, S., & Baker, R. J. (2010). Bats of the tropical lowlands of western Ecuador. Special Publications of the Museum of Texas Tech University, 57, 1–37. https://www.depts.ttu.edu/nsrl/publications/downloads/SP57.pdf

Correa, D. M., Graciolli, G., & Nihei, S. S. (2019). Revision of Noctiliostrebla (Diptera: Streblidae), parasites of bulldog bats (Chiroptera: Noctilionidae: Noctilio). Zootaxa, 4560(3), 483–521. https://doi.org/10.11646/zootaxa.4560.3.4

Cuxim-Koyoc, A., Reyes-Novelo, E., Morales-Malacara, J. B., Bolívar-Cimé, B., & Laborde, J. (2015). Streblidae (Diptera: Hippoboscoidea) from Yucatan and updated species list for Mexico. Journal of Medical Entomology, 52(5), 947–961. https://doi.org/10.1093/jme/tjv117

Cuxim-Koyoc, A., Reyes-Novelo, E., MacSwiney, M. C., & Pech-Canché, J. M. (2018). Moscas ectoparásitas de murciélagos (Diptera: Streblidae y Nycteribiidae) del valle de Uxpanapa, Veracruz, México. Revista Mexicana de Biodiversidad, 89(4), 1074–1088. https://doi.org/10.22201/ib.20078706e.2018.4.2686

Da Silva, S. G., Ferreira, F. F., Hrycyna, G., Eriksson, A., Graciolli, G., & Canale, G. R. (2023). Determinants of the composition of ectoparasitic flies of bats (Diptera: Streblidae, Nycteribiidae) in the Amazon and Cerrado landscape scales and ecotonal areas. Parasitology Research, 122(8), 1851–1861. https://doi.org/10.1007/s00436-023-07886-4

De Groot, M. D., Dumolein, I., Hiller, T., Sándor, A. D., Szentiványi, T., Schilthuizen, M., Aime, M. C., Verbeken, A., & Haelewaters, D. (2020). On the fly: Tritrophic associations of bats, bat flies, and fungi. Journal of Fungi, 6, 1–13. https://doi.org/10.3390/jof6040361

Díaz, M. M., Solari, S., Gregorin, R., Aguirre, L. F., & Barquez, R. M. (2021). Clave de identificación de los murciélagos / Chave de identificação dos morcegos neotropicais. Publicación Especial N° 4 PCMA (Programa de Conservación de los Murciélagos de Argentina).

Dick, C. W. (2007). High host specificity of obligate ectoparasites. Ecological Entomology, 32(5), 446–450. https://doi.org/10.1111/j.1365-2311.2007.00836.x

Dick, C. W., & Gettinger, D. (2005). A faunal survey of Streblid flies (Diptera: Streblidae) associated with bats in Paraguay. Journal of Parasitology, 91(5), 1015–1024. https://doi.org/10.1645/GE-536R.1

Dick, C. W., Graciolli, G., & Guerrero, R. (2016). Family Streblidae. Zootaxa, 4122(1), 784–802. https://doi.org/10.11646/zootaxa.4122.1.67

Durán, A. A., Álvarez García, D. M., & Graciolli, G. (2017). Ectoparasitic flies (Diptera, Streblidae) on bats (Mammalia, Chiroptera) in a dry tropical forest in the northern Colombia. Papéis Avulsos de Zoologia, 57(8), 105–111. https://doi.org/10.11606/0031-1049.2017.57.08

Espinoza, M. J. (2020). Ectoparásitos (Insecta: Diptera) de murciélagos en Ecuador [Biology Bachelor’s Degree Thesis, Universidad San Francisco de Quito]. https://repositorio.usfq.edu.ec/bitstream/23000/9646/1/139854.pdf

França, D. S., Pereira, S. N., Maas, A., Martins, M. A., Bolzan, D. P., Lima, I. P., & Peracchi, A. L. (2013). Ectoparasitic flies (Diptera, Streblidae) of bats (Chiroptera, Phyllostomidae) in an Atlantic Forest area, south‐eastern Brazil. Brazilian Journal of Biology, 73(4), 847–854. https://doi.org/10.1590/S1519-69842013000400022

Frank, R., Münster, J., Schulze, J., Liston, A., & Klimpel, S. (2014). Macroparasites of Microchiroptera: Bat ectoparasites of Central and South America. In Klimpel, S., & Mehlhron, H. (Eds.), Bats (Chiroptera) as vectors of diseases and parasites. Volume 5 (pp. 87–130). Springer. https://doi.org/10.1007/978-3-642-39333-4

Fritz, G. N. (1983). Biology and ecology of bat flies (Diptera: Streblidae) on bats in the genus Carollia. Journal of Medical Entomology, 20(1), 1–10. https://doi.org/10.1093/jmedent/20.1.1

Garbino, G. S. T., Gregorin R., Lima I. P., Loureiro, L., Moras, L., Moratelli, R., Nogueira, M. R., Pavan, A. C., Tavares, V. C., Nascimento, M. C., Novaes, R. L. M., & Peracchi A. L. (2022). Updated checklist of Brazilian bats. Version 2020. Sociedade Brasileira para o Estudo de Quirópteros. https://www.sbeq.net/lista-de-especies

Graciolli, G. (2004). Nycteribiidae (Diptera, Hippoboscoidea) in the Southern Region of Brazil. Revista Brasileira de Zoologia, 21(4), 971–985. https://doi.org/10.1590/S0101-81752004000400035

Graciolli, G., & Hrycyna, G. (2023). Nycteribiidae in Catálogo taxonômico da fauna do Brasil. Programa de las Naciones Unidas para el Desarrollo. http://fauna.jbrj.gov.br/fauna/faunadobrasil/1145

Graciolli, G., Dick, C. W., & Guerrero, R. (2016). Family Nycteribiidae. Zootaxa, 4122(1), 780–783. https://doi.org/10.11646/zootaxa.4122.1.66

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 Biológica Venezuelica, 15(1), 1–18.

Guerrero, R. (1994b). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. IV. Trichobinae con alas desarrolladas. Boletín de Entomología Venezolana, 9(2), 161–192.

Guerrero, R. (1995a). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. III. Los grupos: dugesii, dunni y phyllostomae del género Trichobius Gervais. 1844. Acta Biológica Venezuelica, 15(3–4), 1–27.

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 misceláneos. Boletín de Entomología Venezolana, 10(2), 135–160.

Guerrero, R. (1996). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. VI. Streblinae. Acta Biológica Venezuelica, 16(2), 1–5.

Guerrero, R. (1997). Catálogo de los Streblidae (Diptera: Pupipara) parásitos de murciélagos (Mammalia: Chiroptera) del Nuevo Mundo. VII. Lista de especies, hospedadores y países. Acta Biológica Venezuelica, 17(1), 9–24.

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 Parasitológica, 43(2), 86–93.

Guerrero, R. (2019). Streblidae (Diptera: Pupipara) de Venezuela: sistemática, ecología y evolución. Editorial Académica Española.

Guimarães, L. R. (1972). Venezuelan Nycteribiid batflies (Diptera: Nycteribiidae). Brigham Young University Science Bulletin, Biological Series, 17(1), 1–11. https://scholarsarchive.byu.edu/byuscib/vol17/iss1/1

Guimarães, L. R., & D’Andretta, M. A. (1956). Sinopse dos Nycteribiidae (Diptera) do Novo Mundo. Arquivos de Zoologia, 10, 1–184. https://www.revistas.usp.br/azmz/article/view/207752

Haelewaters, D., Hiller, T., & Dick, C. W. (2018). Bats, bat flies, and fungi: A case of Hyperparasitism. Trends in Parasitology, 34(9), 784–799. https://doi.org/10.1016/j.pt.2018.06.006

Hernández-Martínez, J., Morales-Malacara, J. B., Alvarez-Anõrve, M. Y., Amador-Hernández, S., Oyama, K., & Avila-Cabadilla, L. D. (2019). Drivers potentially influencing host-bat fly interactions in anthropogenic neotropical landscapes at different spatial scales. Parasitology, 146(1), 74–88. https://doi.org/10.1017/S0031182018000732

Hiller, T., Brändel, S. D., Honner, B., Page, R. A., & Tschapka, M. (2020). Parasitization of bats by bat flies (Streblidae) in fragmented habitats. Biotropica, 52(3), 488–501. https://doi.org/10.1111/btp.12757

Hiller, T., Vollstädt, M. G. R., Brändel, S. D., Page, R. A., & Tschapka, M. (2021). Bat-bat fly interactions in Central Panama: host traits relate to modularity in a highly specialized network. Insect Conservation and Diversity, 14(5), 686–699. https://doi.org/10.1111/icad.12508

Hopla, C. E., Durden, L. A., & Keirans, J. E. (1994). Ectoparasites and classification. Revue Scientifique et Technique (International Office of Epizootics), 13(4), 985–1017. https://doi.org/10.20506/rst.13.4.815

Hrycyna, G., Moreira, A. C., & 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(4). https://doi.org/10.1590/1676-0611-BN-2018-0715

Jobling, B. (1936). A revision of the subfamilies of the Streblidae and the genera of the subfamily Streblinae (Diptera Acalypterae) including a redescription of Metelasmus pseudopterus Coquillett and a description of two new species from Africa. Parasitology, 28(3), 355–380. https://doi.org/10.1017/S0031182000022538

Lee, H., Seo, M. G., Lee, S. H., Oem, J. K., Kim, S. H., Jeong, H., Kim, Y., Jheong, W. H., Kwon, O. D., & Kwak, D. (2021). Relationship among bats, parasitic bat flies, and associated pathogens in Korea. Parasites and Vectors, 14, 1–11. https://doi.org/10.1186/s13071-021-05016-6

Lira-Olguin, A. Z., Guzmán-Cornejo, C., & León-Paniagua, L. (2020). Bat flies (Diptera: Streblidae) associated with Phyllostomid bats (Chiroptera: Phyllostomidae) in caves in Mexico. Studies on Neotropical Fauna and Environment, 56(3), 1–13. https://doi.org/10.1080/01650521.2020.1783478

Liu, J., Haelewaters, D., Pfliegler, W. P., Page, R. A., Dick, C. W., & Aime, M. C. (2020). A new species of Gloeandromyces from Ecuador and Panama revealed by morphology and phylogenetic reconstruction, with a discussion of secondary barcodes in Laboulbeniomycetes taxonomy. Mycologia, 112(6), 1192–1202. https://doi.org/10.1080/00275514.2020.1781496

Marshall, A. (1982). Ecology of insects ectoparasitic on bats. In Kunz, T. H. (Ed.), Ecology of bats: Volume 1 (pp. 369–401). Springer.

Menezes Júnior, L. F., Santos, D. M. C., Menezes, A. C. D. P., & Peracchi, A. L. (2021). Ectoparasitic flies (Diptera: Streblidae) on bats (Mammalia: Chiroptera) from a Private Natural Heritage Reserve in southeastern Brazil. Papéis Avulsos de Zoologia, 61, e20216102. https://doi.org/10.11606/1807-0205/2021.61.02

Minaya, D., Mendoza, J., & Iannacone, J. (2021). Ectoparasitic fauna on the common vampire bat Desmodus rotundus (Geoffroy, 1810) (Chiroptera: Phyllostomidae) from Huarochiri, Lima, and a checklist of ectoparasites in bats of Peru. Graellsia, 77(1), 1–15. https://doi.org/10.3989/graellsia.2021.v77.293

Mittermeier, R. A., Turner, W. R., Larsen, F. W., Brooks, T. M., & Gascon, C. (2011). Global Biodiversity Conservation: The critical role of hotspots. In Zachos, F., & Habel, J. (Eds.), Biodiversity hotspots (pp. 3–22). https://doi.org/10.1007/978-3-642-20992-5_1

Morse, S. F., Olival, K. J., Kosoy, M., Billeter, S., Patterson, B. D., Dick, C. W., & Dittmar, K. (2012). Global distribution and genetic diversity of Bartonella in bat flies (Hippoboscoidea, Streblidae, Nycteribiidae). Infection, genetics and evolution. Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases, 12(8), 1717–1723. https://doi.org/10.1016/j.meegid.2012.06.009

Oscherov, E. B., Idoeta, F. M., & Milano. A. (2012). Nuevos registros de ectoparásitos (Insecta: Diptera) de murciélagos (Chiroptera) del nordeste argentino. FACENA, Revista de la Facultad de Ciencias Exactas y Naturales y Agrimensura, 28, 63–68. http://dx.doi.org/10.30972/fac.280902

Pastrana-Montiel, M. R., Ballesteros-Correa, J., & Chacón-Pacheco, J. (2019). First record of the parasite bat fly Basilia mimoni Theodor & Peterson, 1964 (Diptera: Nycteribiidae) in Colombia. Oecologia Australis, 23(3), 685–689. https://doi.org/10.4257/oeco.2019.2303.27

Peterson, B. V. (1959). New distribution and host records for bat flies, and a key to the North American species of Basilia Ribeiro (Diptera: Nycteribiidae). Proceedings of the Entomological Society of Ontario, 90, 30–37.

Raigosa, J., García, C., Autino, A., & Gomes, L. (2020). First records of ectoparasitic insects (Diptera: Hippoboscoidea) of bats in the department of Caldas, Colombia. Papéis Avulsos de Zoologia, 60, 1–9. https://doi.org/10.11606/1807-0205/2020.60.18

Ramírez-Martínez, M. M., Bennett, A. J., Dunn, C. D., Yuill, T. M., & Goldberg, T. L. (2021). Bat flies of the family Streblidae (Diptera: Hippoboscoidea) host relatives of medically and agriculturally important “bat-associated” viruses. Viruses, 13(5), 1–15. https://doi.org/10.3390/v13050860

Reeves, W. K., Beck, J., Orlova, M. V., Daly, J. L., Pippin, K., Revan, F., & Loftis, A. D. (2016). Ecology of bats, their ectoparasites, and associated pathogens on Saint Kitts Island. Journal of Medical Entomology, 53(5), 1218–1225. https://doi.org/10.1093/jme/tjw078

Salgado, P. E. (2019). Prevalencia y abundancia de ectoparásitos asociados a la quiropterofauna de la cueva de la gruta de la Paz (Carchi-Ecuador) [Bachelor’s thesis in Biological and Environmental Sciences, Universidad Central del Ecuador]. http://www.dspace.uce.edu.ec/handle/25000/17908

Sánchez, J. P., Leonardi, M. S., Debarbora, V. N., Di Benedetto, I. M. D., Ezquizaga, M. C., Gozzi, A. C., López, F., Moreno, L., & Silva de la Fuente, M. C. (2020). Aportes en taxonomía, ecología e importancia sanitaria de los ectoparásitos de herpetozoos y mamíferos silvestres de la Argentina y Chile en la última década. Revista Argentina de Parasitología, 9(1), 7–26. http://hdl.handle.net/11336/139806

Santos, R. H., Fonseca de Vasconcelos, P., & Bocchiglieri, A. (2016). Ectoparasites of bats (Mammalia: Chiroptera) in Atlantic forest fragments in north-eastern Brazil. Parasitology Research, 115(10), 3759–3765. https://doi.org/10.1007/S00436-016-5137-8

Soares, F. A. M., da Rocha, P. A., Mikalauskas, J. S., Graciolli, G., & Ferrari, S. F. (2017). Ectoparasitic bat flies (Diptera, Streblidae) of bats (Chiroptera, Mammalia) from Mata do Junco Wildlife Refuge, Sergipe, northeastern Brazil. Oecologia Australis, 21(4), 385–395. https://doi.org/10.4257/oeco.2017.2104.03

Stamper, E. (2012). Host specificity of Ecuadorian bat flies (Diptera: Streblidae) [Bachelor of Science’s thesis, Western Kentucky University]. http://digitalcommons.wku.edu/stu_hon_theses/358

Tello, J. S. (2005). Relaciones ecológicas entre murciélagos del género Carollia (Chiroptera: Phyllostomidae) y sus dípteros ectoparásitos (Diptera: Streblidae) [Biological Sciences Bachelor’s thesis, Pontificia Universidad Católica del Ecuador].

Ter Hofstede, H. M., Fenton, M. B. & Whitaker, J. (2004). Host and host-site specificity of bat flies (Diptera: Streblidae and Nycteribiidae) on Neotropical bats (Chiroptera). Canadian Journal of Zoology, 82(4), 616–626. https://doi.org/10.1139/z04-030

Theodor, O. (1967). An illustrated catalogue of the Rothschild collection of Nycteribiidae (Diptera) in the British Museum (Natural History) with keys and short descriptions for the identification of subfamilies, genera, species and subspecies. The British Museum (Natural History).

Tirira, D. G. (2017). A field guide to the mammals of Ecuador (1st English Ed.). Asociación Ecuatoriana de Mastozoología & Editorial Murciélago Blanco. Publicación Especial sobre los Mamíferos del Ecuador 10.

Tirira, D. G., Brito, J., Burneo, S. F., Pinto, C. M., Salas, J. A., & Comisión de Diversidad de la AEM. (2022). Mamíferos del Ecuador: lista oficial actualizada de especies/ Mammals of Ecuador: official updated species checklist. Version 2022.2. Asociación Ecuatoriana de Mastozoología. http://aem.mamiferosdelecuador.com

Tlapaya-Romero, L., Horváth, A., Gallina-Tessaro, S., Naranjo, E. J., & Gómez, B. (2015). Prevalencia y abundancia de moscas parásitas asociadas a una comunidad de murciélagos cavernícolas en La Trinitaria, Chiapas, México. Revista mexicana de biodiversidad, 86(2), 377–385. https://doi.org/10.1016/j.rmb.2015.04.012

Trujillo-Pahua, L., & Ibáñez-Bernal, S. (2019). New geographical records of bat flies (Diptera: Streblidae) associated with Phyllostomid bats (Chiroptera: Phyllostomidae) in the west highlands of Mexico. Journal of Medical Entomology, 56(1), 18–28. https://doi.org/10.1093/jme/tjy166

Trujillo-Pahua, L., & Ibáñez-Bernal, S. (2020). Bat flies (Diptera: Streblidae) of Phyllostomid bats (Chiroptera: Phyllostomidae) from the mountainous central region of Veracruz, Mexico. Systematic Parasitology, 97(6), 743–777. https://doi.org/10.1007/s11230-020-09951-3

Urbieta, G. L., 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(11), 3051–3061. https://doi.org/10.1007/S00436-022-07635-z

Wenzel, R. L. (1976). The Streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University Science Bulletin, Biological Series, 20(4), 1–177. https://scholarsarchive.byu.edu/byuscib/vol20/iss4/1

Wenzel, R. L., Tipton, V. J., & Kiewlicz, A. (1966). The Streblid bat flies of Panama (Diptera: Calypterae: Streblidae). In Wenzel, R. L., & Tipton, V. J. (Eds.), Ectoparasites of Panama (pp. 405–675). Field Museum of Natural History.

Appendix 1

Toponymic index

El Oro

Zaruma Urcu, Cerro (03°41’01.6” S, 79°37’21.4” W; 1126 m a.s.l.). Trichobius parasiticus.

Esmeraldas

Cocadilla, Finca (01°11’29.2” N, 79°03’07.7” W; 5 m a.s.l.). Trichobius dugesii, T. joblingi, Speiseria ambigua, Strebla guajiro, Basilia ferrisi.

La Esperanza, Finca (00°12’54.3” N, 79°35’54.9” W; 100 m a.s.l.). Trichobius joblingi, Strebla guajiro, Megistopoda proxima, Basilia carteri.

Majagual, Centro de Interpretación (01°10’23.0” N, 79°04’45.8” W; 11 m a.s.l.). Trichobius dugesii, T. joblingi, Speiseria ambigua, Strebla guajiro, Basilia ferrisi.

Playa de Oro (00°52’33.0” N, 78°47’40.7” W; 113 m a.s.l.). Trichobius joblingi, T. anducei, Speiseria ambigua, Strebla guajiro, S. galindoi, Basilia ferrisi.

Los Ríos

Río Palenque, Centro Científico (00°35’19.8” S, 79°21’39.8” W; 150 m a.s.l.). Trichobius uniformis, T. longipes, T. costalimai, T. joblingi, T. dugesioides, T. flagellatus, T. anducei, Trichobioides perspicillatus, Speiseria ambigua, Paratrichobius longicrus, Megistopoda aranea, M. proxima, Strebla mirabilis, S. guajiro, S. altmani, Basilia ferrisi, Basilia sp.

Manabí

El Zapote, comunidad (00°22’31.4” S, 79°36’ 16.3” W; 200 m a.s.l.). Trichobius uniformis, T. costalimai, T. joblingi, T. flagellatus, T. anducei, Trichobius sp., Trichobioides perspicillatus, Speiseria ambigua, Megistopoda aranea, M. proxima, Aspidoptera falcata, Exastinion clovisi, Strebla guajiro, S. hertigi, S. altmani, Metelasmus pseudopterus, Basilia carteri, B. ferrisi.

Pacoche, Refugio de Vida Silvestre Marino Costera (01°04’00.91” S, 80°53’20.00” W; 118 m a.s.l.) Paratrichobius dunni, Megistopoda aranea, Aspidoptera phyllostomatis.

Santo Domingo de los Tsáchilas

La Unión del Toachi (00°19’14.2” S, 78°57’08.8” W; 811 m a.s.l.). Strebla machadoi.

Citation:

Portilla, K., Pilatasig, A. L., & Camacho, M. A. (2023). Ectoparasites (Diptera: Streblidae and Nycteribiidae) of bats from some localities of the Coast of Ecuador. Mammalia aequatorialis, 5, 49–73. https://doi.org/10.59763/mam.aeq.v5i.67