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New Geographical Records of Bat Flies (Diptera: Streblidae) Associated With

Phyllostomid Bats (Chiroptera: Phyllostomidae) in the West Highlands of
Mexico

Article  in  Journal of Medical Entomology · September 2018

DOI: 10.1093/jme/tjy166

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 Journal of Medical Entomology, XX(X), 2018, 1–11
doi: 10.1093/jme/tjy166
Arthropod/Host Interaction, Immunity Research

New Geographical Records of Bat Flies (Diptera:

Streblidae) Associated With Phyllostomid Bats (Chiroptera:

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Phyllostomidae) in the West Highlands of Mexico
L. Trujillo-Pahua and S. Ibáñez-Bernal1,

Instituto de Ecología A. C. (INECOL), Red de Ambiente y Sustentabilidad, Carretera antigua a Coatepec 351, Col. El Haya Xalapa,
91070 Veracruz, Mexico and 1Corresponding author, e-mail: sergio.ibanez@inecol.mx

Subject Editor: Richard Wilkerson

Received 5 July 2018; Editorial decision 20 August 2018

Abstract
Streblidae are ectoparasites exclusive to bats and feed only on their blood. Studies on ectoparasite fauna have
increased our ecological knowledge of the parasitic relationship between streblids and their bat hosts. We
evaluate assemblages of phyllostomid bats and their ectoparasitic flies in three scenarios with different types of
anthropogenic use: pine–oak forest, avocado orchards, and an urban park during an annual cycle in the highlands of
Michoacan, Mexico. We recorded a total of 325 bats belonging to nine species in three subfamilies: Glossophaginae,
Desmodontinae, and Stenodermatinae, and obtained 225 bat flies belonging to seven species. The nectivorous bat
Anoura geoffroyi Gray, 1838, had the highest prevalence of infestation and the hematophagous bat Desmodus
rotundus (É. Geoffroy, 1810) was the host with the highest mean parasite abundance and mean intensity. Aspidoptera
delatorrei Wenzel, 1966, Megistopoda proxima (Séguy, 1926), Paratrichobius longicrus (Miranda Ribeiro, 1907),
Trichobius brennani Wenzel, 1966, and T.  parasiticus Gervais, 1844, are new records for the state of Michoacan
reported in this study.

Key words: bat ectoparasite, Phyllostomidae, Uruapan, Michoacan

Family Streblidae is a small group of Diptera Hippoboscoidea
ectoparasites of bats, specialized to live on the skin and fur of their
hosts and that feed on their blood, with the exception of females
of the genus Ascodipteron (Wenzel et  al. 1966). Because they are
exclusive to bats, their geographic distribution follows that of
their hosts. Currently, there are 239 described species (Borkent
et  al. 2018). Streblidae include five subfamilies worldwide, with
Nycterophiliinae, Streblinae, and Trichobiinae present in the New
World and predominating in tropical areas where they are found
mainly on bats of the family Phyllostomidae (Jobling 1936, Wenzel
et al. 1966, Wenzel 1976).
The relationship between bats and streblids reflects their strong
co-evolutionary relationship over the past 15–20 million years,
according to the oldest fossil record (Poinar and Brown 2012). The
phylogenetic relationships of bats and streblids have been studied to
understand the association between them (Graciolli and de Carvalho
2012); however, the scarcity of streblid information at the regional
level makes it difficult to identify some streblids. Sample contamin-
ation can also limit phylogenetic analysis, and studies of their coevo-
lution and ecological interactions.
From the taxonomic point of view, there are still difficulties
with species recognition, because intraspecific variability has not
been documented, and there are some species groups for which the
characters used for differentiation are subtle. This is the case with
Trichobius for which the 68 recognized species are grouped into
seven species groups (Wenzel et al. 1966). Even with molecular anal-
ysis it is difficult to define whether Trichobius is monophyletic or
paraphyletic (Graciolli and de Carvalho 2012, Dittmar et al. 2006).
Another example is the taxonomic difficulty in distinguishing the
species of Aspidoptera as they only can be told apart by the male
genitalia, making it difficult to identify females unless they are found
with males (Wenzel et al. 1966, Wenzel 1976).
Considering that the most complete works on the taxonomy
of Neotropical streblids are those Wenzel et al. (1966) and Wenzel
(1976), Guerrero (1993, 1994a,b, 1995a,b, 1996, 1997), based on
the description of specimens collected in Panama and Venezuela,
it is possible that there is variation in some of the species distrib-
uted in other parts of the Neotropical realm. Knowledge of species
in the Neotropics is without a doubt incomplete, as demonstrated
by the recent description of new species (e.g., Anatrichobius pas-
sosi Graciolli 2003 in southern Brazil, Metalasmus wenzeli Graciolli
and Dick 2004, from southern Brazil and eastern Paraguay and
Synthesiostrebla cisandina (Graciolli and Azevedo 2011, from
Brazil). Additionally, new geographic records have been reported in

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2 Journal of Medical Entomology, 2018, Vol. XX, No. XX
recent years (e.g., Dick 2013), reflecting the scarcity of information
on the geographical distribution, host association and morphologi-
cal variation of some streblid species.
The main goal of this study was to record the streblid assem-
blage and the parasitic relationship between phyllostomid bats and
streblid flies in the highlands of central Michoacan. Although our
approach is taxonomic, some parasitological parameters and host
preference is given, and additional information about the geograph-
ical distribution of species in a not previously studied region of
Mexico is also provided.
Materials and Methods
Study Area
The municipality of Uruapan in the state of Michoacan, Mexico
(Fig.  1), is located between parallels 19° 17′ and 19° 45′ North
Latitude, and meridian 101° 50′ and 102° 14′ West Longitude, at
an elevation of 1,611 m a.s.l., and with an area of 948.05 km2.
In this region, six types of plant communities have been identified:
1)  Cloud forest, 2)  Gallery Forest (heterogeneous trees grouped
mainly along rivers), 3) Pine Forest, 4) Pine–oak forest, 5) Tropical
dry Forest, and 6) Grassland (Rzedowski 2006, Chávez-León and
Ramos-Rivera 2017).
In Uruapan, we selected three sample sites with an average area
of 20 ha, each with different types of vegetation: Forest that is mainly
composed of pine–oak forest, with some elements of cloud forest
located at 19° 29′28.66″ N, 101° 59′30.35″ W; Orchard (Avocado
and macadamia nut crops under conventional agricultural manage-
ment) at 19° 28′ 43.26″N 102° 00′14.14″ W; and an Urban park
that includes some elements of pine–oak and cloud forest, but highly
disturbed owing to the presence of exotic plant species, located at
19° 25′11.28″ N 102° 07′40.04″ W.
Field Work
To capture the bats, we used 10 mist nests hung three nights per
season (warm, rainy and cold) at each site in 2016. The nets were
opened at sunset (between 1900 and 2000 h) and were closed in the
Fig. 1.  Study area. Municipality of Uruapan, in the state of Michoacan, Mexico.
early morning (0300–0400  h). For the taxonomic identification of
the bats, we used the work of Medellín et al. (2008). All bats were
processed when captured to record general measurements (body and
forearm length), sex, reproductive condition, and age. The ectopara-
sites were collected with soft forceps and placed in Eppendorf tubes
with 96% ethanol. Each bat was marked with nail polish before
being released to avoid re-captures. Streblids were studied under
a stereoscopic microscope Nikon SMZ 800N and identified using
mainly the keys of Wenzel et  al. (1966). The material collected is
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deposited in the Insect Collection of Instituto de Ecología, A.  C.
(IEXA) Xalapa, Veracruz, Mexico.
Data Analysis
We calculated the percentage of host individuals that were infested
with streblids of the total number of host bats captured (prevalence),
the mean number of parasites present on a host individual (mean
abundance) and the average number of infected individuals by a
parasite species (mean intensity). We used Fisher’s exact test and the
Bootstrap t-test run in the program Quantitative Parasitology 3.0
(Rózsa et al. 2000).
Taxonomical Descriptions
In order to contribute to the identifications of the streblid species,
we made diagnoses based in the original descriptions of Wenzel et al.
(1966) and Wenzel (1976), adding missing information for some
structures. Also, we complete the diagnoses with draws of the main
taxonomical characters for each species.
Results
Sampling effort was a total of 2,880 net hours in the field over the
course of a year (2016). We captured 325 phyllostomid bats belong-
ing to three subfamilies: Glossophaginae: Anoura geoffroyi, Gray,
1838, Desmodontinae: Desmodus rotundus (Geoffroy, 1810), and
Stenodermatinae: Artibeus hirsutus, Andersen, 1906, A.  jamaicen-
sis, Leach, 1821, A.  lituratus (Olfers, 1818), Dermanura azteca,
K. Andersen, 1906, D. phaeotis (Miller, 1902), D. tolteca (Saussure,
Journal of Medical Entomology, 2018, Vol. XX, No. XX 3

1860), Sturnira hondurensis, Goodwin, 1940. The yellow-shouldered
bat S. hondurensis was the most abundant phyllostomid throughout
the year.
Over the year, from all the captured bats a total of 225 streblids
were recorded for the three sites. Megistopoda proxima was the
most abundant, followed by Trichobius parasiticus, Paratrichobius
longicrus, Anastrebla modestini, Exastinion clovisi, Trichobius bren-
nani, and Aspidoptera delatorrei. Prevalence, mean abundance, and
mean intensity of streblid parasitism on bats are presented by species
tibiae with short setae but lacking macrosetae dorsally; abdomen
connexivum without setae dorsally (Wenzel et al. 1966).
Comments
Currently, five species of Anastrebla are recognized (A.  nycteridis
Wenzel, A.  modestini Wenzel, A.  mattadeni Wenzel, A.  spurrelli
Wenzel; A.  caudiferae Wenzel), all apparently restricted to bats of
the subfamily Glossophaginae (Wenzel et  al. 1966; Wenzel 1976).
Three species have been recorded in Central America (Dick and

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in Table 1.
The nectarivorous bat A.  geoffroyi had the highest number
of individuals parasitized by streblids, followed by the frugivor-
ous yellow-shouldered bat S.  hondurensis and the hematophagous
D.  rotundus. The highest mean abundance of parasites infecting a
single host was recorded for the common vampire bat Desmodus
rotundus, which had the highest number of streblids per individual,
and also the highest mean intensity with around eight ectoparasites
per individual host. Bat sex proportion was higher for males (182
individuals) than females (143 individuals). More streblid males were
recorded (127 specimens) than females (98 specimens). The propor-
tion of bats captured per site was Forest (27%), Orchard (24%) and
Urban park (49%), while the inverse pattern was observed for the
streblids: Forest (50%), Orchard (26%), and Urban park (24%).
List of the Streblidae species recorded, with commentary.
Genus Anastrebla Wenzel, 1966
Anastrebla Wenzel, In: Wenzel et  al. 1966: 627. Type species:
Anastrebla modestini Wenzel, 1966.
Diagnosis
Body dorsoventrally compressed. Head with ctenidium, extending
around sides to dorsolateral parts of head. Postgenae with a laterally
directed remiform scale behind ctenidium (Fig. 2a). Prescutum with
the median longitudinal suture incomplete, and with a second trans-
verse suture (Fig. 2b). Wings fully developed. Legs elongated, hind
Miller 2010), but only A.  modestini is known in Mexico (Wenzel
et al. 1966, Guerrero and Morales-Malacara 1996, Martínez et al.
2016, Cuxim-Koyoc et  al. 2016, Hernández-Arciga et  al. 2016,
Rivera-García et al. 2017).
Anastrebla modestini Wenzel, 1966
Anastrebla modestini Wenzel, In: Wenzel et  al. 1966: 629. Type
locality: Panama, Chiriqui, Cerro Punta, Casa Lewis, ex. Anoura
geoffroyi lasiopyga (= Anoura geoffroyi) (Fig. 2a–e).
Materials Examined
9♂♂, 3♀♀. MEXICO, MICHOACAN, URUAPAN: Uruapan, 1♂ ex.
Anoura geoffroyi, 4.VII.2016; 3♂♂ ex. Anoura geoffroyi, 5.VII.2016
and Toreo el Alto, 1♂ ex. Anoura geoffroyi, 8.VII.2016; 1♂, 1♀
ex. Anoura geoffroyi, 14.VII.2016; 3♂♂, 1♀ ex. Anoura geoffroyi,
9.XI.2016; 1♀ ex. Anoura geoffroyi, 22.III.2017.
Diagnosis
Head: Postvertex and occiput each with five pairs of heavy sub-
equal spine-like setae with point apex, setae of postvertex slightly
longer than occipitals; eyes with seven to nine externally distinct fac-
ets; postgena with a long macroseta anterior to the remiform scale
(Fig. 2a). Thorax: Prescutum sparsely setose, the median setose area
usually not extending beyond the anterior suture. Epaulets with four
setae. Antescutellar row of 10–12 setae, the middle ones shorter than
the outer ones (Fig. 2b). Wing: Veins R1 and Rs with setae, except

Table 1.  Bat and streblid species recorded in Uruapan, Michoacán, with prevalence, mean abundance, and mean intensity parasitological
parameters

Bat species N Streblid species n Prevalence %* Mean abundance* Mean intensity*

Anoura geoffroyi 15 Anastrebla modestini 13 66.7% 1.2 1.8

Aspidoptera delatorrei 1 (0.39–0.85) (0.67–1.67) (1.4–2.1)
Exastinion clovisi 5
Artibeus hirsutus 9 Paratrichobius longicrus 8 44.4% 0.89 2
(0.16–0.74) (0.22–2.22) (1–3)
Artibeus jamaicensis 38 Paratrichobius longicrus 5 13.2% 0.16 1.2
Megistopoda proxima 1 (0.05–0.27) (0.05–0.32) (1–1.4)
Artibeus lituratus 22 Paratrichobius longicrus 2 9.1% 1.09 12
(0.01–0.29) (0–2.73) †
Dermanura azteca 3 — — 0 0 0
Dermanura phaeotis 93 Paratrichobius longicrus 1 2.2% 0.02 1
Megistopoda proxima 1 (0–0.07) (0–0.05) †
Dermanura tolteca 35 Paratrichobius longicrus 4 8.6% 0.14 1.67
Megistopoda proxima 1 (0.02–0.22) (0.03–0.43) (1–2.33)
Desmodus rotundus 4 Trichobius parasiticus 30 50% 7.5 2
Megistopoda proxima 1 (0.09–0.90) † †
Sturnira hondurensis 106 Aspidoptera delatorrei 2 54.7% 1.26 2.31
Megistopoda proxima 128 (0.44–0.64) (0.95–1.70) (1.88–3.02)
Trichobius brennani 4

N = total number of bats; n = total number of streblids.

*Confidence interval of 95%.
†
Insufficient data to calculate the confidence intervals.
4 Journal of Medical Entomology, 2018, Vol. XX, No. XX
on the base (Fig.  2c). Abdomen: Dorsal connexivum of abdomen
bare. Median setose area of sternum I narrow and extending anteri-
orly beyond middle. Apical margin of sternum I with about 15 setae,
including 2 macrosetae. Females: Tergum VII with a pair of long
macrosetae, medial and posterior to these a pair of very short setae;
supra-anal plate with four apical macrosetae and just anterior to
them a pair of very short widely separated setae (Fig.  2d). Male:
Postgonites strongly tapered, and rather strongly curved apically;
macroseta inserted at about basal fourth, very long, extending to
apex; accessory seta well developed (Fig. 2e) (Wenzel et al. 1966).
Comments
Anastrebla modestini is the only species of the genus reported in
Mexico with previous collections in the states of Sinaloa (Wenzel
et  al. 1966), Estado de Mexico (Guerrero and Morales-Malacara
1996), Veracruz (Hernández-Arciga et  al. 2016, Cuxim-Koyoc
et  al. 2016), Michoacan (Rivera-García et  al. 2017), and Jalisco
(Martínez et al. 2016). A. modestini seems to have high host specific-
ity with Anoura geoffroyi, though there are records of this species
on Leptonycteris yerbabuenae (Rivera-García et  al. 2017). In this
study, all specimens were collected exclusively from 13 individuals
of A. geoffroyi.
Genus Aspidoptera Coquillett, 1899
Aspidoptera Coquillett, 1899: 334. Type species: Aspidoptera
busckii Coquillett, 1899, by subsequent designation of Coquillett,
1910: 511.
Fig. 2.  Anastrebla modestini. a) Head dorsal view, b) thorax dorsal view, c)
right wing, d) female terminalia dorsal view, and e) male right postgonites
lateral view.
Syn. Lepopteryx Speiser, 1900: 42, 53. Type species: Lipoptena
phyllostomatis Perty.
Diagnosis
Body small (1.65–2.36 mm) dorsoventrally compressed. Head with-
out ctenidium; laterovertices and occipital plates well differentiated;
the occipital plates rounded posteriorly without a posterior lobe or
flap (Fig. 3a), palpi nearly vertical. Thorax with a complete median
suture united with the transverse suture forming an inverse “T” on
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mesonotum (Fig. 3b); sternopleura not strongly produced anteriorly,
sides oblique. Wings brachypterous with complete venation. Legs all
about the same size. Abdomen, covered with short setae in dorsal
view (Wenzel et al. 1966).
Comments
There are three described species: A. phyllostomatis (Perty), A. dela-
torrei Wenzel, and A.  falcata Wenzel. All the species of this genus
are easily recognized by their small size, short legs, and short oval
wings with complete venation. All have been collected from bats of
family Phyllostomidae, specifically species of Artibeus and Sturnira,
but only A. phyllostomatis and A. delatorrei have been recorded in
Mexico (Guerrero and Morales-Malacara, 1996, Morse et al. 2012).
Aspidoptera delatorrei Wenzel, 1966
Aspidoptera delatorrei Wenzel, In: Wenzel et  al. 1966: 557. Type
locality: Panama, Los Santos, Guánico, ex. Sturnira lilium parvidens
(Fig. 3a–e).
Fig. 3.  Aspidoptera delatorrei. a) Head dorsal view, b) thorax dorsal view, c)
mesepisternum lateral view, d) female terminalia dorsal view, and e) male
left postgonite lateral view.
Journal of Medical Entomology, 2018, Vol. XX, No. XX 5

Material Examined
1♂, 1♀. MEXICO, MICHOACAN, URUAPAN: Toreo el Alto: 1♂,
1♀ ex. Sturnira hondurensis, 23.III.2017.

Diagnosis
Body pigmented and setose. Head in dorsal view as in Fig. 3a; gena
and postgena with bristles along dorsal and oral margins, respect-
ively; palpi with the ventral surface covered in short setae that nearly
reach the apex. Thorax: Dorsally covered with setae of the same size

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(Fig. 3b), the dorsal surface of mesepisternum with three to four lon-
gitudinal rows of long subequal bristles (Fig. 3c). Abdomen: Tergum
I+II with about 24 bristles of different sizes arrange in irregular rows.
Females: Supra-anal plate with six apical macrosetae, and anter-
ior to these a transverse row of four to six shorter setae (Fig. 3d).
Male: Postgonites bent but not falciform, the ventral margin at apex
nearly straight, the apical dorsal bristle is inserted near apex (Fig. 3e)
(Wenzel et al. 1966, Wenzel 1976).

Comments
Aspidoptera delatorrei and A. falcata are very similar species that
can only be recognized by the shape of the male gonapophyses.
Females cannot be separated and are assigned to species only by
association with the males (Wenzel 1976). The principal hosts
of this species are bats of the genus Sturnira. Nevertheless, spe-
cies of Aspidoptera have been also reported on bats of the genus
Artibeus, Carollia, Chiroderma, and Vampyressa (Wenzel et  al.
1966). Mexican records of Aspidoptera delatorrei include the states
of Yucatán (Cuxim-Koyoc et  al. 2015), Jalisco (Zarazúa-Carbajal
et  al. 2016, Martínez et  al. 2016), Veracruz (Cuxim-Koyoc et  al.
2016), Oaxaca (Guerrero and Morales-Malacara, 1996), and
Chiapas (Colín-Martínez et al. 2018), so the present record is the
first for the state of Michoacan.
Genus Exastinion Wenzel, 1966
Exastinion Wenzel, In: Wenzel et  al. 1966: 558. Type species:
Aspidoptera clovisi Pessôa and Guimarães, 1936.
Diagnosis
Body small (1.2–1.8 mm). Head flattened with two oblique flap-like
occipital lobes and with setae on the festooned posterior margin;
without ctenidium (Fig. 4a); palpi nearly oval. Thorax with median
suture on prescutum, bifurcated anteriorly and posteriorly united
with the transverse suture (Fig.  4b); wings reduced (Wenzel et  al.
1966, Dick and Miller 2010).
Comments
There are three described species [E. clovisi (Pessôa and Guimarães),
E.  oculatum Wenzel, and E.  deceptivum Wenzel] associated with
bats of the genus Anoura (subfamily Glossophaginae) (Wenzel et al.
1966). Only E. clovisi has been reported in Mexico.
Exastinion clovisi (Pessôa and Guimarães, 1936)
Aspidoptera clovisi Pessôa and Guimarães, 1936: 262. Type locality:
Brazil, São Paulo, Ipiranga, ex. Anoura geoffroyi (Fig. 4a–e).
Materials Examined
4♂♂, 2♀♀. MEXICO, MICHOACAN, URUAPAN: Toreo el Alto:
1♂, 1♀ ex. Anoura geoffroyi, 8.VII.2016; 2♂♂, ex. Anoura geof-
froyi, 15.VII.2016; 1♀ ex. Anoura geoffroyi, 9.XI.2016; 1♂, ex.
Anoura geoffroyi, 21.III.2017.
Fig. 4.  Exstinion clovisi. a) Head dorsal view, b) thorax dorsal view, c) thorax ventral
view, d) female terminalia dorsal view, and e) male left postgonite lateral view.
Diagnosis
Body length: 1.2–1.8  mm. Head (Fig.  4a): palpi usually setose ven-
trally on less than basal half; eyes with four to seven bad defined facets.
Thorax: Scutum with about eight setae (Fig.  4b); median pleurotro-
chantinal lobe well developed, longer than broad (Fig. 4c). Abdomen:
Lateral lobes of tergum I+II with about 15 long setae and about 18
short setae; sternum II with setose area extending from anterior margin
to near or slightly beyond the middle. Female: Connexivum dorsolat-
eral with about five long setae, compare with the next shortest setae
on the apical region of connexivum; sternite VII with 17–18 setae; of
which about 12 are long and the others short (Fig. 4d). Male: Sternum
VII+VIII with about 10 setae on each side, the ventral area with mac-
rosetae except for three setae that are shorter; tergum IX with less than
16 setae, mostly macrosetae, that become shorter to the sides ventrally
(Wenzel et al. 1966; Wenzel 1976). Postgonites slightly curved, with a
short seta followed by a long seta near the middle (Fig. 4e).
Comments
Exastinion clovisi can be easily distinguish from species of the genus
Aspidoptera by the head flaps and the thorax structure. In Mexico, this
species has been reported in the states of Michoacan (Rivera-García
et  al. 2017), Estado de México (Guerrero and Morales-Malacara
1996), Jalisco (Martínez et  al. 2016), Veracruz (Hernández-Arciga
et al. 2016), and Chiapas (Colín-Martínez et al. 2018). It is a parasite
of Glossophaginae bats, as it has been reported on Anoura geoffroyi,
Leptonycteris yerbabuenae, and Choeroniscus godmani (Guerrero and
Morales-Malacara 1996, Martínez et al. 2016).
Genus Megistopoda Macquart, 1852
Megistopoda Macquart, 1852: 332. Type species: Megistopoda
pilatei Macquart, by original designation.
6 Journal of Medical Entomology, 2018, Vol. XX, No. XX
Syn. Pterellipsis Coquillett, 1899: 333. Type species: Pterellipsis ara-
nea Coquillett, 1899, by original designation.
Diagnosis
Body large (1.7–2.48 mm), somewhat compressed laterally but never
flea like. Head lacking ctenidium (Fig.  5a). Thorax with mesepis-
ternum not divided by a membranous cleft; scutum sclerotized, the
suture between it and the scutellum rigid (Fig.  5b); sterna shield-
like with anterior and posterior margins broadly rounded. Wings
reduced but represented by an inconspicuous flap (Fig.  5c). Front
legs with femur lacking stout spines on inner face. Hind legs long,
about twice the length of front legs (Wenzel et al. 1966).
Comments
Wenzel et al. (1966) considered M. aranea, M. proxima, and M. the-
odori, as valid species of this genus. Later, Wenzel (1976) observed
that M. theodori might be a synonym of M. proxima, but more mate-
rial needed to be examined in order to correctly divide the M. prox-
ima complex. Authors like Wenzel (1976) and Guerrero (1994b)
considered Megistopoda theodori to be a synonym of M. proxima.
In contrast, other authors such as Dick (2006) and Martínez (2016),
thought M.  theodori to be a valid species. All these authors agree
that a revision of the genus is needed, so other species associated
with Sturnira (other than S. lilium and S. ludovici) can appropriately
be included. It is important to mention that Megistopoda specimens
from different Sturnira ludovici populations have been recog-
nized as different species. We agree that new redescriptions of the
Fig.  5.  Megistopoda proxima. a) Head dorsal view, b) thorax dorsal view,
c) right wing, d) female terminalia lateral view, and e) male left postgonite
lateral view.
M. proxima complex are needed to be sure of the species collected in
Mexico, the specimens collected in this study have the characteristics
described by Wenzel (1966), so we agree to identify as M. proxima.
All Megistopoda species are parasites on Phyllostomidae bats of the
genera Artibeus and Sturnira and have been recorded in Mexico.
Megistopoda proxima (Séguy, 1926)
Pterellipsis proxima Séguy, 1926: 194. Type locality: Argentina,
Misiones, environs de San Ignacio, Villa Lutecia, ex. not determined
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(Fig. 5a–e).
Materials Examined
82♂♂, 50♀♀. MEXICO, MICHOACAN, URUAPAN: Uruapan:
2♂♂, 1♀ ex. Sturnira hondurensis, 3.VII.2016; 4♂♂, 1♀ ex.
Sturnira hondurensis, 4.VII.2016; 1♂, 2♀♀ ex. Sturnira honduren-
sis, 5.VII.2016; 1♂, 1♀ ex. Sturnira hondurensis, 13.XI.2016; 7♂♂,
2♀♀ ex. Sturnira hondurensis, 15.XI.2016; 1♀ ex. Sturnira hondu-
rensis, 16.XI.2016; 3♀♀ ex. Sturnira hondurensis, 29.III.2017; 1♀
ex. Sturnira hondurensis, 1.IV.2017; 1♂ ex. Sturnira hondurensis,
1♂ ex. Dermanura tolteca, 30.III.2017 and Toreo el Alto: 18♂♂, 1♀
ex. Sturnira hondurensis 8.VII.2016; 1♂, 1♀ ex. Sturnira honduren-
sis 10.VII.2016; 3♂♂, 5♀♀ ex. Sturnira hondurensis, 11.VII.2016;
2♂♂, 1♀ ex. Sturnira hondurensis, 13.VII.2016; 13♂♂, 4♀♀ ex.
Sturnira hondurensis, 4.XI.2016; 4♂♂, 6♀♀ ex. Sturnira honduren-
sis, 6.XI.2016; 5♂♂, 4♀♀ ex. Sturnira hondurensis, 8.XI.2016; 2♂♂
ex. Sturnira hondurensis, 9.XI.2016; 5♂♂, 6♀♀ ex. Sturnira hondu-
rensis, 21.III.2017; 1♂, 3♀♀ ex. Sturnira hondurensis, 22.III.2017;
2♂♂, 1♀ ex. Sturnira hondurensis, 23.III.2017; 5♂♂ ex. Sturnira
hondurensis, 25.III.2017; 1♀ ex. Sturnira hondurensis, 25.III.2017;
1♀ ex. Dermanura phaeotis, 25.III.2017; 1♀ ex. Artibeus jamaicen-
sis, 25.III.2017; 1♂ ex. Sturnira hondurensis, 27.III.2017; 1♂ ex.
Desmodus rotundus, 27.III.2017; 1♀ ex. Sturnira hondurensis,
27.III.2917; 2♂♂, 2♀♀ ex. Sturnira hondurensis, 28.III.2017.
Diagnosis
Body length: 1.98–2.47  mm. Head: Occipital lobes with two long
and about five short setae; eyes with about 14 facets and the later-
overtices with five setae (Fig. 5a). Thorax: Prescutum with about 22
bristles at disk; scutum with about 14 bristles, those on the anterior-
median area shorter than the rest (Fig. 5b). Wings with six longitu-
dinal veins, the veins 3, 4, and 5 forming a W (Fig. 5c). Legs short
in relation to the length of the body, hind femora between 0.99 and
1.43  mm. Abdomen: Connexivum full covered with heavy bristles
and with subapical macrosetae that are longest on the latero-ven-
tral part; the tergum I+II with about 20 bristles, the posterior ones
thicker than the others. Female: Supra-anal plate and tergum VII
united at the middle, each with a conspicuous pair of macrosetae and
between them one to two pair of short setae (Fig. 5d); sternite VII
with about 15 setae, some of them large. Male: Hypopygium with
two to three macrosetae on the dorsolateral part; postgonites curved
in lateral view with the ventral margin almost straight, with a long
macroseta singular inserted near basal area and with about eight
small setae, almost translucent along the ventral margin (Fig.  5e)
(Wenzel et al. 1966).
Comments
This species is recorded for first time in the state of Michoacan,
as it was previously known only in Veracruz (Cuxim-Koyoc et al.
2016), Yucatán (Bolívar-Cimé et  al. 2018), Jalisco (Zarazúa-
Carbajal et  al. 2016, Martínez et  al. 2016), and Chiapas (Colín-
Martínez et al. 2018). Additionally, the list of host bats is increased
Journal of Medical Entomology, 2018, Vol. XX, No. XX 7

for Mexico to M.  proxima, whose registered hosts were, Carollia

sowelli (Cuxim-Koyoc et  al. 2016), Sturnira hondurensis, Natalus
mexicanus (Martínez et al. 2016), and Sturnira parvidens (Cuxim-
Koyoc et al. 2015); here we add Artibeus jamaicensis, Dermanura
phaeotis, D. tolteca, and Desmodus rotundus. It is remarkable that
this was the most abundant species in our study, accounting for a
higher proportion of the total than any of the other streblids, which
may indicate that it is the most common species, at least for the
study region.

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Genus Paratrichobius Costa Lima, 1921
Paratrichobius Costa Lima, 1921: 20. Type species: Trichobius longi-
crus, Miranda Ribeiro, 1907.

Diagnosis
Body dorsoventrally compressed. Head without ctenidium. Large
multifaceted eyes. Thorax shield-like ventrally with the posterior
margin rounded (Fig. 6a). Wing fully developed. Anterior legs with
the inner face of front femora presenting a diagonal row of heavy
spines (except P. lowei, Wenzel, which has only two or three strong
setae). Hind legs elongated, longer than the body, with tibiae often
curved with numerous minute unsclerotized cracks. Females with a
postgenital sclerite and with a fusion between the cerci and the ven-
tral arc. Males with the paired setae of postgonites inserted at the
distal region (Wenzel et al. 1966, Dick and Miller 2010).

Comments
The genus comprises six described species [P. dunni (Curran), P. sal-
vini, Wenzel P. longicrus (M. Ribeiro), P. sanchezi, Wenzel, P. ameri-
canus, Peterson and Ross, and P.  lowei, Wenzel), but authors like
Wenzel et  al. (1966) and Wenzel (1976) indicated that there are Fig.  6.  Paratrichobius longicrus. a) Thorax dorsal view, b) anterior femora,
some undescribed species and agree that there is a complex that inner face, c) female terminalia dorsal view, and d) male left postgonite
includes P. longicrus and P. salvini, and so have suggested that there lateral view.

be a review of this genus based on data from a larger number of

specimens.
Paratrichobius longicrus (Miranda Ribeiro, 1907)
Trichobius longicrus, Miranda Ribeiro, 1907: 236. Type locality:
Brazil, Rio de Janeiro, Quinta da Boa Vista, probably ex. Artibeus
jamaicensis (Fig. 6a–d).
Materials Examined
8♂♂, 12♀♀. MEXICO, MICHOACAN, URUAPAN: Uruapan: 1♀
ex. Artibeus jamaicensis, 4.VII.2016; 1♂ ex. Artibeus jamaicen-
sis, 5.VII.2016; 2♂♂ ex. Dermanura tolteca, 5.VII.2016; 2♀♀
ex. Artibeus jamaicensis, 5.VII.2016; 1♀ ex. Dermanura tolteca,
5.VII.2016; 1♂ ex. Artibeus lituratus, 13.XI.2016; 3♂♂ ex. Artibeus
hirsutus, 15.XI.2016; 1♀ ex. Artibeus lituratus, 15.XI.2016; 5♀♀
ex. Artibeus hirsutus, 15.XI.2016; 1♀ ex. Dermanura phaeotis,
16.XI.2016; 1♀ ex. Artibeus jamaicensis, 1.IV.2017; and Toreo el
Alto: 1♂ ex. Dermanura tolteca, 9.XI.2016.
Diagnosis
Thorax: Anterior margin of sterna nearly straight between the front
coxae. Prescutum with anterior area clothed with scattered setae
(Fig. 6a). Legs: Inner face of front femora with a complete row of
six stout spines, which is medial and parallel to the oblique row of
small setae (Fig.  6b), hind femora long with about 1.32–1.77  mm
(Wenzel et al. 1966). Female: Tergum I+II with two groups of short
and compact setae near the anterior margin and 8–10 setae on the
middle part, 5 fine setae on the postero-dorsal margin, 3 pairs of
heavy setae on lateral margin, 5 setae on the postero-lateral lobe
and 3 setae on the ventral margin. Tergum VII undefined with two
to three setae, the anterior ones long. Supra-anal plate with a pair
of short setae on the lateral and basal region, and with four long
setae of the same size on the posterior margin and one seta at mid-
dle anterior to the four long setae (Fig. 6c). Cercus with four short
setae. Connexivum bare on dorsal region but near midline setae are
present as follows: third segment with 2 + 1 setae, fourth segment
with 1 + 2 setae, fifth and sixth segment with 1 + 1 setae. Sternite VII
with 12 setae at each side. Males: Tergum I+II with four fine dorsal
setae, two rows of four heavy setae on the latero-posterior angle, five
spine-like short setae on the postero-ventral margin, and two spine-
like short setae on ventral margin. Tergum VII with a pair of long
setae and external to these a pair of short setae around a third of
the longitude of inner setae. Tergum IX with 16 long and fine setae.
Postgonites evenly tapered with apical third slightly curved, with a
pair of setae inserted in the apical fifth, the basal seta strong and the
apical one slender (Fig. 6d).
Comments
This is the first record of P. longicrus for the state of Michoacan, as it
was previously known for Veracruz (Hernández-Arciga et al. 2016,
Cuxim-Koyoc et al. 2016), Jalisco (Martínez et al. 2016, Zarazúa-
Carbajal et  al. 2016), Tlaxcala (Guerrero and Morales-Malacara
1996), and Chiapas (Colín-Martínez et  al. 2018). P.  longicrus has
been found parasitizing bats of the genus Artibeus, but evidently
8 Journal of Medical Entomology, 2018, Vol. XX, No. XX

there are other undescribed species of the longicrus complex col-

lected on Dermanura. In Mexico, there are records of Paratrichobius
lowei and P.  salvini in Jalisco (Zarazúa-Carbajal et  al. 2016) and
P.  lowei and P.  sanchezi in Chiapas (Colín-Martínez et  al. 2018).
However, the main taxonomic characteristics indicate that our mate-
rial corresponds to P. longicrus.

Genus Trichobius Gervais, 1844

Trichobius Gervais, 1844: 14. Type species: Trichobius parasiticus

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Gervais, 1844, by original designation.
Syn. Kolenatia Rondani, 1878: 169. Type species: Strebla wiedeman-
nii Kolenati, 1863, not Kolenati 1856).
Syn. Kesselia Curran, 1934: 522. Type species: Kesselia pallida
Curran, by original designation.

Diagnosis
Body dorsoventrally depressed. Head without ctenidium; palpi with
setae along margin and on ventral surface (Fig.  7a). Thorax with
the anterior margin of prescutum straight or sinuous, sternum with
the anterior margin never rounded, the posterior margin roughly as
broad as the anterior margin (Fig.  7b). Wings fully developed and
functional; the costal vein and R1 lacking macrosetae; vein 5 con-
tinuing beyond the transversal vein 2, ending near or at apex of the
wing; R1 connected to the costal vein at a point beyond that level
with transversal vein 3. Hind legs not twice the length of forelegs, if
elongated, then the fore and middle legs are also long, and the pos-
terior legs are as long or somewhat less than the body length; tibiae
with setae of small size in some species but can be long without being
macrosetae (Wenzel et al. 1966, Dick and Miller 2010).

Comments
This is the richest genus of family Streblidae with 68 species, dis-
tributed in seven groups. In Mexico 24 species have been recorded,
representing the 35% of all Trichobius species registered (Ryckman
1956, Morales-Malacara 1990, Guerrero and Morales-Malacara
1996, Guzmán-Cornejo 2003, Villegas-Guzán 2005, Dittmar et al.
2006, Morse et al. 2012, Cuxim-Koyoc et al. 2015, Lira-Olguin et al.
2015, Tlapaya-Romero et al. 2015, Cuxim-Koyoc 2016, Hernández-
Arciga 2016, Martínez et  al. 2016, Zarazúa-Carvajal et  al. 2016,
Rivera-García et al. 2017, Salinas-Ramos et al. 2017, Colín-Martínez
et al. 2018, Bolívar-Cimé et al. 2018).
Trichobius brennani Wenzel, 1966
Trichobius brennani Wenzel, In: Wenzel et al. 1966: 497. Type local-
ity: Panama, Chiriquí, near Cerro Punta, casa Tilley, ex. Sturnira
ludovici (Fig. 7a–e).
Materials Examined
1♂, 3♀♀. MEXICO, MICHOACAN, URUAPAN: Uruapan: 1♀
ex. Sturnira hondurensis, 3.VII.2016; 1♀ ex. Sturnira hondurensis,
5.VII.2016; 1♂ ex. Sturnira hondurensis, 13.XI.2016; and Toreo el
Alto: 1♀ ex. Sturnira hondurensis, 4.XI.2016.
Diagnosis
Head: Occipital lobes with about 12–14 thick setae, laterovertices
with 6 setae, both sclerites well differentiated; eye with 19 facets
(Fig. 7a). Thorax: Scutum slightly broad than long, with the anterior
margin projected anteriorly at midline; prescutum with long setae
on the anterior portion and short setae on disc; scutellum with four
Fig.  7.  Trichobius brennani. a) Head dorsal view, b) thorax dorsal view, c)
thorax ventral view, d) female terminalia dorsal view, and e) male left
postgonite lateral view.
long setae (Fig. 7b); sternopleura strong projected wide and truncate
emarginate (Fig. 7c). Wing: Rs short, its length less than the distance
between cross-vein r-m and fork. Legs: Hind legs longer than the
anterior ones; femora and tibiae with short setae regularly scattered.
Abdomen: Dorsal connexivum bare at midline except for four pairs
of short setae, the rest of the connexivum with small setae. Tergum
I+II with about 19 long setae and 5 short setae along the inferior
margin; sternum I+II broad than the pleurotrochantines, with the
posterior margin presenting long setae, other setae distributed in a
triangle area. Female: Tergum VII almost as wide as the supra-anal
plate with one long seta on each side of the lateral margin and two
short setae posterior to it. Sternite VII small and with about 18 setae
of different length (Fig. 7d). Male: Postgonites thin and remarkable
curved at apex (Fig. 7e); sternum V with 12 long setae along poster-
ior margin. Sternum VI absent (Wenzel et al. 1966).
Comments
Trichobius brennani is recorded for first time in the state of
Michoacan, so it is known geographical distribution extends to the
western region of Mexico. This species belongs to the phyllostomae
species complex that seems to be exclusive to the bats of subfamily
Stenodermatinae. It can be separated from other species in the com-
plex by anterior margin of sternum strongly projected and truncate,
with the lateral margins almost parallel on the anterior portion.
Journal of Medical Entomology, 2018, Vol. XX, No. XX
Trichobius parasiticus Gervais, 1844
Trichobius parasiticus Gervais, 1844: 14. Type locality: Guiane, ex.
Desmodus rufus (=Desmodus rotundus) (Fig. 8a–e).
Syn. Trichobius kesseli Guimarães, 1938: 660. Nomen novo for par-
asiticus Gervais of Kessel, 1925, error.
Materials Examined
15♂♂, 15♀♀, and 18 additional specimens from a recaptured bat,
8♂♂, 10♀♀. MEXICO, MICHOACAN, URUAPAN: Toreo el Alto:
11♂♂, 9♀♀ ex. Desmodus rotundus, 1.XI.2016; 4♂♂, 6♀♀ ex.
Desmodus rotundus, 27.III.2017.
Diagnosis
Head: Laterovertices and occipital lobes well differentiated, eyes
with about eight facets; palpi short and oval shaped, with setae only
on the basal portion and on margin (Fig.  8a). Thorax: Prescutum
and scutum with nude appearance, and with long setae laterally
on the humeral region and on the anterior margin of prescutum;
a transverse row of small setae previous to the transversal suture
(Fig. 8b); sternum with the anterior margin not extended anteriorly
and lacking pleurotrochantinal lobe (Fig. 8c). Wing: Rs shorter than
the distance between the fork and vein r-m. Abdomen: Connexivum
without setae dorsally; tergum I+II with an oblique row of three
strong seta anteriorly, group of four seta in the dorsal posterior zone
and a row of five shortest setae along the ventro-posterior margin.
Female: Tergum VII longer than broad, with a long seta at each lat-
eral margin and inner shorter and small setae; sternite VII with 15
Fig.  8.  Trichobius parasiticus. a) Head dorsal view, b) thorax dorsal view,
c) thorax ventral view, d) female terminalia dorsal view, and e) male left
postgonite lateral view.
9
setae, the apical ones long; supra-anal plate with an anterior row of
four short setae and a posterior row of four longer setae; subanal
plate with six setae (Fig. 8d) (Wenzel et al. 1966). Male: Postgonites
in lateral view, tapered with the ventral margin straight and the dor-
sal margin gibbous at middle, each with one long seta preceded by a
shorter one and numerous short setae near them (Fig. 8e); sternum V
with large setae at the apical margin that are longer than the discal
seta; sternum VI not sclerotized.
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Comments
Trichobius parasiticus is recorded for the first time in the state
of Michoacan. This species has been recorded associated with
Desmodus rotundus in Yucatán (Dittmar et al. 2006, Cuxin-Koyoc
et al. 2015, Bolívar-Cimé et al. 2018), Tabasco (Ryckman 1956), and
Jalisco (Martínez et al. 2016, Zarazúa-Carbajal et al. 2016). Wenzel
et al. (1966) mentioned D. rotundus is the primary host of this spe-
cies, but Zarazúa-Carbajal et  al. (2016) report T.  parasiticus on
Artibeus jamaicensis. The other Mexican records were on Desmodus
rotundus, as is the case with our findings.
Discussion
This study contributes to our knowledge of the streblid fauna on
an understudied region and reveals the need to reinforce taxonomic
characteristics for the correct identification of these species in future
studies. Even though interest in the study of streblids has grown in
recent years, many studies have yet to be conducted in a wide range
of regions across the country. Additionally, many authors agree
that the taxonomic keys of Wenzel et  al. (1966), Wenzel (1976),
and Guerrero (1993, 1994a,b, 1995a,b, 1996, 1997) are not clear
enough. Some characters need to be researched and there is a lack
of other characters in the description of some species or one of the
sexes. It is vital for all this new information that is being generated in
the country, contribute to clarify the background of the species, not
only with respect to their geographical distribution or their associ-
ation with their bat hosts, but also considering intraspecific variation
in characteristics.
As regards our study, it is noteworthy that we recorded higher
bats species richness than streblid richness; the opposite to almost
all of the other studies done in Mexico, in which the number of
streblids has always been greater than the number of bats species.
Only one study in Chiapas had the same result (Tlapaya-Romero
et  al. 2015). The main faunistic lists that have been drawn up for
the western region of the country near our study zone are two arti-
cles written for the state of Jalisco and both reported 24 species of
streblids (Martínez et  al. 2016, Zarazúa-Carbajal et  al. 2016). In
Michoacan only one article has been published (Rivera-García et al.
2017) with five species of bats and five species of streblids, and there
is also one unpublished thesis by Montañez-García, who reported 12
bats species and 5 streblid genera.
Regarding the species we report, it is noteworthy that they were
found on new bat host species such as Paratrichobius longicrus
on bats of the genus Dermanura sp. This streblid species has been
reported to be almost exclusive to the genus Artibeus sp., according
to Wenzel et al. (1966), although other studies in Mexico report this
same species for Dermanura sp. (Guerrero and Morales-Malacara
1996, Zarazúa-Carbajal et  al. 2016), Choeronycteris mexicana
(Hernández-Arciga et  al. 2016), and Enchistenes hartii (Colín-
Martínez et al. 2018). Wenzel mentions that there are another three
undescribed species from the longicrus complex that are undescribed
and were found on Dermanura species, which seems to suggest that
the Mexican material should be reviewed to ensure the correct
10
taxonomic identification of the specimens. Our material presents the
distinct characteristic of the row of six spines on the inner face of the
prefemora, which only corresponds to P. longicrus. For the descrip-
tion of many species we noticed an impractical reference system
by some authors (e.g., Wenzel, Guerrero), in which they compare
species of the same genus; however, it is rarely possible to have the
whole set of species to use as a reference. We suggest that new taxo-
nomic and phylogenetic analyses are needed for the material from
Mexico to clarify the species complex that remains unsolved.
With respect to the ecological and parasitological aspects that
we observed during this study, the case of the common vampire bat
Desmodus rotundus—only parasitized by Trichobius parasiticus—
was significant. The only female marked had a parasitic load of 20 bat
flies the first day of capture and was recaptured the next day infested
with another 18 of this streblid species. We suggest that this re-infes-
tation with a high number of streblids might be caused by the type
of roost or the social behavior of these animals (Wilkinson 1986).
They usually live in groups and even feed each other (Denault and
McFarlane 1995), increasing contact between individuals and facili-
tating the transfer of ectoparasites. Also, the roosting preferences of
bats can influence the density of ectoparasites they carry for bat flies
that pupate on the roosts (Jobling 1949, Ter Hofstede and Fenton
2005), thus increasing the possibility of infesting different host species.
Acknowledgments
We thank J. C. Pérez Magaña, C. E. Almazán Marín, and E. Trujillo Hernández
(Thank you dad) for their invaluable assistance with the field work. We are
grateful to Rafael García Soriano for the permit to work in the “Barrancas del
Cupatitzio” National Park, and to Fernando Villaseñor Gómez for facilitating
our field work at the “Vasco de Quiroga” biological station. The first author
was supported by a scholarship from the Mexican Council of Science and
Technology (CONACyT, No. 263854). The present work was supported by
the project INECOL-10816 granted to SIB. This study was conducted under
collection permit SEMARNAT-FAUT-0204.
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