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Parasitism of Bat Flies (Nycteribiidae and Streblidae) on Bats in Urban

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Acta Chiropterologica, 20(2): 511–518, 2018
PL ISSN 1508-1109 © Museum and Institute of Zoology PAS
doi: 10.3161/15081109ACC2018.20.2.021

Parasitism of bat flies (Nycteribiidae and Streblidae) on bats in urban environments:

lower prevalence, infracommunities, and specificity

GUSTAVO L. URBIETA1, 4, JAIRE M. TORRES2, ELAINE A. CARVALHO DOS ANJOS3,

CRISTIANO M. ESPÍNOLA CARVALHO2, and GUSTAVO GRACIOLLI1
1Programa de Pós-Graduação em Biologia Animal, Laboratório de Sistemática, Ecologia e Evolução (LSEE), Instituto
de Biociências (INBIO), Universidade Federal de Mato Grosso do Sul (UFMS), 79090-900, Campo Grande, MS, Brazil
2
Programa de Pós-Graduação em Biotecnologia, Universidade Católica Dom Bosco (UCDB), Campo Grande, MS, Brazil
3
Bolsista CAPES - Proc. Number 1218-13-1, University of Manitoba, Biological Sciences Building, Winnipeg,
MB R3T 2N2, Canada
4Corresponding author: E-mail: gustavo.cx@hotmail.com

Studies involving parasitism between ectoparasitic flies and bats are scarce for urban environments, which makes it difficult to find
association patterns in these altered environments. Herein, we describe the bat flies community, and estimate the prevalence, mean
intensity of infestation, infracommunities, and specificity of bat fliesassociations in urban remnants of Cerrado. We collected 371
bat flies of 14 species and 944 bats of 17 species. The most abundant species of bats were Artibeus planirostris (n = 312), Artibeus
lituratus (n = 197), Carollia perspicillata (n = 124) and Platyrrhinus lineatus (n = 110). Regarding bat flies, Megistopoda aranea
(n = 148) and Trichobius joblingi (n = 118) were the most abundant. The prevalence of bat flies ranged from 0.3 to 43.5% and the
mean infestation intensity from 1 to 12 (mean general of 2.04). We found 16 bat flies infracommunities on the most representative
hosts (n > 30). Concerning specificity, 71% of bat flies were associated with a single host species (monoxenic). Our results indicate
that bats were most parasitized by a single bat flies species, and prevalence and specificity between bat flies and bats were lower in
these urban environments.

Key words: fragmentation, Phyllostomidae, Cerrado, ectoparasite

INTRODUCTION Bats and parasitic bat flies are an excellent model

The process of urbanization causes constant
change in natural environments (Buczkowski and
Richmond, 2012) by reducing local diversity (Orte-
ga-Álvarez and MacGregor-Fors, 2009), excluding
sensitive species, and favoring species that are more
adapted to altered environments (Dar and Reshi,
2014). Many studies have shown that urbanization
affects wildlife populations by influencing habitat
selection and space use (McKinney, 2002; Hansen et
al., 2005; Riley et al., 2010). Furthermore, one of
the most evident effects of urbanization on the land-
scape is habitat fragmentation, as it generates a mo-
saic of native vegetation arranged between different
man-made (constructed) areas (MacGregor-Fors,
2011). Such landscape changes have been studied to
understand how human actions interfere with coevo-
lutionary relationships, including parasite dynamics
in wild populations (Salkeld et al., 2013).
of coevolution for studying such environmental frag-
mentation since bats are one of the most diverse
mammals within these urban environments (Jung
and Kalko, 2011), while bat flies are limited to cer-
tain hosts and have high specificity (Marshall, 1982).
Currently, nine families, 68 genera, and 184 bat spe-
cies have been registered in Brazil (Nogueira et al.,
2014; Feijó et al., 2015; Moratelli and Dias, 2015;
Gregorin et al., 2016; Rocha et al., 2016; Pavan
et al., 2018). Such high species richness results in
a high richness of bat flies species (see Dick and Get-
tinger, 2005). In Brazil, 177 species of bat flies are
known, with 81 species (23 genera) of Streblidae
(Graciolli, 2017; Barbier et al., 2018) and 26 species
(two genera) of Nycteribiidae (Graciolli et al., 2007).
These flies are obligatory ectoparasites of bats and
exhibit adenotrophic viviparity (larvae develop in the
mother’s body), and larvae are deposited into bat
host shelters (Marshall, 1982; Dittmar et al., 2015).
512 G. L. Urbieta, J. M. Torres, E. A. Carvalho dos Anjos, C. M. Espínola Carvalho, and G. Graciolli
Recently, different effects of urbanization and
fragmentation have been recorded for bat flies-bat
relationships. For example, Frank et al. (2016) re-
ported effects on parasitism of bats caused by an-
thropogenic impacts and fragmentation in Costa
Rica. Effects of fragmentation have also been re-
ported for Streblidae (see Bolívar-Cimé et al.,
2018). Anthropic disturbance (human population
density) and climate (precipitation, temperature, and
elevation) have also affected parasitism between bat
flies and bats (Pilosof et al., 2012). In addition, habi-
tat degradation may increase parasitism rates, as it
increases host stress and concentration, which facil-
itates parasite transmission (Mbora and Mcpeek,
2009). Furthermore, the characteristics of bat shel-
ters in these environments may directly influence
the reproduction and survival rates of ectoparasites
(Patterson et al., 2007).
However, in general, interactions between bat
flies and bats in urban environments have been
poorly explored. Thus far, only Urbieta et al. (2014)
have effectively studied bat flies parasitism of urban
bats in Brazil using parasitological index. In these
urban and fragmented environments, we propose
that all these previously mentioned factors (i.e., ur-
banization, fragmentation, anthropic disturbance)
can directly influence the specific parasitism rates
(e.g., prevalence, infracommunities, and speci-
ficity). Prevalence, for example, tends be higher in
fragmented environments since bats tend to concen-
trate in available shelters due to limited mobility in
urban environments (Hofstede and Fenton, 2005;
Bolívar-Cimé et al., 2018). Like prevalence, the
amount of infracommunities tends to be higher in
urban environments due to the high fidelity of bats
and their ectoparasites to shelters (Hofstede and
Fenton, 2005; Bolívar-Cimé et al., 2018). Converse-
ly, specificity tends to be lower in urban areas since
bat flies-bat associations are exposed to the climate
of the urban and fragmented environment, which
could affect the specificity of associations (Pilosof
et al., 2012). Herein, we describe the community
and infracommunities of bat flies (Nycteribiidae and
Streblidae) and their hosts in urban remnants of
Cerrado. We characterize the degree and intensity of
associations using prevalence values, mean intensity
of infestation, and specificity index.
MATERIALS AND METHODS
Study Area
Our study was carried out in three Cerrado remnants in
Campo Grande, the capital city of Mato Grosso do Sul (MS)
State, Central-Western Brazil: Instituto de Pesquisa Săo Vicente
(IPS) (20°23’08.5”S, 054°36’28.8”W — total area 191 ha),
Área de Preservação do Córrego Bandeira (APABAND)
(20°29’31”S, 54°34’45”W — total area 14 ha), and Centro de
Educação Ambiental do Imbirussu (CEAIMB) (20°26’53”S,
54°41’38”W — total area 17 ha). These areas are located in the
urban perimeter of Campo Grande and are priority areas for
urban afforestation, playing an important role in maintaining
forested areas within the municipality (Planurb, 2016). Al-
though the IPS area is georeferenced as periurban (Planurb,
2016), we considered this area urban due to the evident popula-
tion growth (e.g., paved streets, residential neighborhoods, com-
merce). The phytophysiognomies within the study areas were:
cerrado sensu stricto, cerradăo, and riparian forest (Planurb,
2016). In this region, the climate is tropical (Aw) according to
Köppen classification (Peel et al., 2007), with dry winters and
humid summers and average annual rainfall of 1,745 mm and
average annual temperature of 24° C (Planurb, 2016).
Data Collection
We captured bats during two periods: between February
2014 to May 2015 (total of 29 nights) and between November
2016 to April 2017 (total of 45 nights). The sampling effort was
estimated according to Straube and Bianconi (2002) (sampling
effort = mist nets total area x exposure time x number of repeti-
tions x total number of mist nets). Since IPS was the largest
remnant in this study, the sampling effort was 20,088 h.m2
(31 nights), followed by APABAND with 14,256 h.m2
(22 nights) and CEAIMB with 13,608 h.m2 (21 nights). We used
six mist nets (6.0 m × 3.0 m) placed 0.5 m above the ground
(maximum height of 3.5 m) on trails, in clearings, and at the
edges and interior of remnants. Nets were left open for 6 hours
and checked every 15 min. Bat captures were authorized
through licenses 42.457 issued by the Biodiversity Authori-
zation and Information System (SISBIO) and 10.566 issued by
the Environmental Institute (IBAMA).
In the field, we identified bats following Gregorin and
Taddei (2002), Reis et al. (2007), Gardner (2008), Aguirre et al.
(2009), and Barquez and Díaz (2009). We never examined the
same bat twice because we marked all bats with marking bands
during the first capture period and marked their forearms with a
non-toxic permanent pen during the second capture period. We
collected the bat flies using fine-tipped tweezers and alcohol-
moistened brushes and placed them in microtubules with 70%
ethanol. Afterwards, we identified the bat flies in the Laboratory
of Systematics, Ecology, and Evolution (LSEE) at the Federal
University of Mato Grosso do Sul (UFMS) using dichotomous
keys by Guerrero (1994a, 1994b, 1995, 1996, 1997) and Gra-
ciolli (2004). The flies were deposited in the Zoological Refer-
ence Collection of the Federal University of Mato Grosso do Sul
(ZUFMS) in Campo Grande.
Data Analysis
To describe association patterns between bat flies and their
hosts, we used the following indices: prevalence (P) (number of
hosts parasitized/number of hosts examined × 100) and mean
intensity of infestation (MI) (number of ectoparasites/number of
parasitized hosts) (Bush et al., 1997). We estimated the confi-
dence intervals for these two parameters through randomization
analysis using 2,000 replications (Ròzsa et al., 2000). These val-
ues were calculated using Quantitative Parasitology 3.0 (Ròzsa
 Parasitism on bats in urban environments
et al., 2000). We also calculated the relative frequency of infra-
communities for each bat species with more than 30 individuals
captured. The term infracommunity refers to the set of ectopar-
asites found on a determinate host species (sensu Bush et al.,
1997). The relative frequency was based on the number of times
infracommunities were found on the host/the total number of
hosts parasitized by the same species × 100.
Finally, we used the specificity index (STD*) (Poulin and
Mouillot, 2005), which assigns a single value for each bat flies
in the host community. This index considers the average taxo-
nomic and phylogenetic distance between host species used by
a parasite, with a weight for each taxonomic level ranging from
0 to 5. When this index is equal to 0, the parasite is monoxenic,
i.e., parasites a single species only. If the value is 1, the parasite
is oligoxenic (i.e., parasites congeneric individuals). If the value
is greater than 1, the parasite is considered non-specific. The
value can reach up to 5 when found in hosts of different classes.
The analyzes to obtain STD were done in the program Taxo-
Biodiv 1.2 (http://www.otago.ac.nz/parasitegroup/downloads.
html). To calculate the specificity, accidental associations were
excluded according to Graciolli et al. (2008). To infer the taxo-
nomic distances of bats we used the taxonomy published by
Reis et al. (2007).
RESULTS
We captured and examined 944 bats from the
families Phyllostomidae (n = 828), Vespertilionidae
(n = 110), and Molossidae (n = 6) (Table 1). The
most abundant species of bats were Artibeus
planirostris (n = 312), Artibeus lituratus (n = 197),
Carollia perspicillata (n = 124) and Platyrrhinus
lineatus (n = 110). Only Phyllostomidae and
Vespertilionidae were parasitized by Streblidae
and Nycteribiidae bat flies, respectively. Streblidae
(n = 371) presented higher species richness with
12 species. Among them, Megistopoda aranea
(n = 148) and Trichobius joblingi (n = 118) were the
most abundant. We only found two species from
Nycteribiidae: Basilia ortizi (n = 9) and Basilia car-
teri (n = 7). We found the highest prevalence for the
association between T. joblingi on C. perspicillata
(43.5%) and the highest mean intensity of infesta-
tion for T. costalimai parasitizing Phyllostomus dis-
color (12).
We found 16 infracommunities on five bat
species, with three accidental associations. The rich-
ness of infracommunities ranged from one to five
bat flies per host species. The highest frequencies
were recorded for T. joblingi on C. perspicillata
(96%) followed by M. aranea on A. planirostris
(85%) and T. angulatus on P. lineatus (80%) (Table
2). Regarding specificity, approximately 71% of the
bat flies presented a STD* value equal to zero, con-
sidered monoxenic. Megistopoda aranea and
Aspidoptera phyllostomatis were the only oligo-
xenic bat flies species found in the present study
513
(both with STD* = 1) and parasitized the congeners
A. planirostris and A. lituratus. Approximately
28.5% of the bat flies species found presented STD*
values above 1, indicating parasitism on more than
one non-congeneric bat species (Table 1).
DISCUSSION
Prevalence and Mean Intensity of Infestation
With the exception of Urbieta et al. (2014), we
compared our results to studies performed in non-
urban areas and found our results presented lower
prevalence values than such studies. Even though
mean infestation values were lower in some cir-
cumstances, these values varied slightly within an
expected range compared to other studies. For
example, we recorded the highest prevalence value
of parasitism for T. joblingi on C. perspicillata
(43.5%). However, this value was lower than other
studies (e.g., Komeno and Linhares, 1999; Bertola et
al., 2005; Dornelles and Graciolli, 2017; Dornelles
et al., 2017) and drastically different from Barbier
and Graciolli (2016), who registered a prevalence of
80.0%. The mean intensity of infestation (2.19) fell
within the expected range (see Barbier and Gra-
ciolli, 2016) and was not higher than 4.8, which was
found by Santos et al. (2009) in the Cerrado of
northern Brazil.
Furthermore, we highlight that the second high-
est prevalence was recorded for M. aranea on
A. planirostris (27.2%), which was also lower than
other studies (e.g., Eriksson et al., 2011; Santos et
al., 2013; Lourenço et al., 2014; Barbier and
Graciolli, 2016; Vasconcelos et al., 2016; Dornelles
et al., 2017). However, the mean infestation inten-
sity (1.74) was within the values recorded by these
studies (not higher than 2.09). Curiously, the preva-
lence and mean infestation intensity values were
similar to those of Urbieta et al. (2014; 29.5% and
1.71), who studied this association in urban Cerrado
remnants.
Regarding lower prevalence, we highlight Para-
trichobius longicrus on A. lituratus (5.1%), as the
prevalence value was much lower than the values
found by Dornelles et al. (2017) (20.9%) and by
Dornelles and Graciolli (2017) (32.8%). Additional-
ly, our mean infestation intensity (1.30) was lower
than the values recorded in both studies: 1.56 and
1.84, respectively. We also highlight that T. angula-
tus on P. lineatus (7.3%) had a lower prevalence
value than in Eriksson et al. (2011) (22.6%) and
Barbier and Graciolli (2016) (12.7%). While the
514 G. L. Urbieta, J. M. Torres, E. A. Carvalho dos Anjos, C. M. Espínola Carvalho, and G. Graciolli

TABLE 1. Bat flies (Diptera: Streblidae and Nycteribiidae) collected on their hosts from February 2014 to May 2015 and from
November 2016 to April 2017 in urban remnants of Cerrado, Campo Grande, Mato Grosso do Sul, Brazil: HI — Hosts parasitized,
P — prevalence (%), MI — mean intensity of infestation, CI — confidence intervals, STD* — specificity index; a — Insufficient data
to calculate confidence intervals, b — Accidental association

Host (n) and bat flies (n) HI P (CI 95%) MI (CI 95%) STD*
Family Phyllostomidae
Artibeus planirostris (Spix, 1823) (312) 92 29.5 (0.24–0.34) 1.87 (1.62–2.13)
Megistopoda aranea (Coquillet, 1899) (148) 85 27.2 (0.22–0.32) 1.74 (1.49–2.02) 1
Aspidoptera phyllostomatis (Perty, 1833) (18) 13 4.2 (0.02–0.07) 1.38 (1.08–1.54) 1
Trichobius angulatus Wenzel 1976 (1)b 1 0.3 (0.00–0.01) 1a –
Aspidoptera falcata Wenzel 1976 (1)b 1 0.3 (0.00–0.01) 1a –
Artibeus lituratus (Olfers, 1818) (197) 19 9.6 (0.05–0.14) 1.37 (1.05–1.84)
Paratrichobius longicrus (Miranda Ribeiro, 1907) (13) 10 5.1 (0.02–0.09) 1.30 (1.00–1.90) 2
Megistopoda aranea (Coquillet, 1899) (11) 7 3.6 (0.01–0.07) 1.57 (1.00–2.14) 1
Aspidoptera phyllostomatis (Perty, 1833) (1) 1 0.5 (0.00–0.02) 1a 1
Trichobius angulatus Wenzel 1976 (1)b 1 0.5 (0.00–0.02) 1a –
Carollia perspicillata (Linnaeus, 1758) (124) 55 44.4 (0.35–0.53) 2.18 (1.80–2.64)
Trichobius joblingi Wenzel 1966 (118) 54 43.5 (0.34–0.52) 2.19 (1.80–2.65) 0
Strebla guajiro (García & Casal, 1965) (2) 2 1.6 (0.00–0.05) 1a 0
Platyrrhinus lineatus (E. Geoffroy, 1810) (110) 10 9.1 (0.04–0.16) 1.60 (1.00–2.60)
Trichobius angulatus Wenzel 1976 (14) 8 7.3 (0.03–0.13) 1.75 (1.00–3.00) 0
Paratrichobius longicrus (Miranda Ribeiro, 1907) (1) 1 0.9 (0.00–0.04) 1a 2
Aspidoptera phyllostomatis (Perty, 1833) (1)b 1 0.9 (0.00–0.04) 1a –
Glossophaga soricina (Pallas, 1766) (42) 4 9.5 (0.02–0.22) 1a
Trichobius dugesii Townsend 1891 (3) 3 7.1 (0.01–0.19) 1a 0
Trichobius joblingi Wenzel 1966 (1)b 1 2.4 (0.00–0.12) 1a –
Sturnira lilium (E, Geoffroy, 1810) (16) 6 37.5 (0.15–0.64) 1.50 (1.00–1.67)
Megistopoda proxima (Séguy, 1926) (7) 5 31.3 (0.11–0.58) 1.40 (1.00–1.60) 0
Aspidoptera falcata Wenzel 1976 (6) 3 18.8 (0.04–0.45) 2b 0
Trichobius joblingi Wenzel 1966 (1)b 1 6.3 (0.00–0.30) 1a –
Phyllostomus discolor Wagner, 1843 (6) 3 50.0 (0.11–0.88) 7.67 (5.00–10.0)
Trichobius costalimai Guimarães 1937 (12) 1 16.7 (0.00–0.64) 12a 0
Trichobius longipes (Rudow, 1871) (6) 2 33.3 (0.04–0.77) 3.00 (1.00–3.00) 0
Trichobioides perspicillatus Pessôa & Guimarães 1938 (5) 1 16.7 (0.00–0.64) 5a 0
Platyrrhinus cf. helleri (Thomas, 1912) (17) – – – –
Chiroderma villosum Peters, 1860 (2) – – – –
Phyllostomus hastatus (Pallas, 1767) (1) – – – –
Diaemus youngi (Jentink 1893) (1) – – – –
Family Vespertilionidae
Eptesicus furinalis (d’Orbigny & Gervais 1847) (12) 3 25 (0.05–0.57) 1.67 (1.00–2.33)
Basilia ortizi Machada-Allison, 1963 (5) 3 25 (0.05–0.57) 1.67 (1.00–2.33) 2
Myotis nigricans (Schinz, 1821) (95) 10 10.5 (0.05–0.18) 1.10 (1.00–1.30)
Basilia ortizi Machado-Allison, 1963 (4) 4 4.2 (0.01–0.10) 1a 2
Basilia carteri Scott, 1936 (7) 6 6.3 (0.02–0.13) 1.17 (1.00–1.33) 0
Eptesicus brasiliensis (Desmarest, 1819) (1) – – – –
Lasiurus ega (Gervais, 1856) (2) – – – –
Family Molossidae
Molossops temminckii (Burmeister, 1854) (3) – – – –
Molossus molossus (Pallas, 1766) (3) – – – –
Total: 944 bats and 387 flies

mean intensity (1.75) fell within the intensities
found in both studies (2.0) and (1.29), respectively.
Contrary to our expectations, we noted lower
values of prevalence and mean intensity of infesta-
tion, which can be explained by environmental
disturbance and shelter quality. Barbier and
Graciolli (2016) related the high prevalence and
mean intensity of T. joblingi infestation on C. per-
spicillata (80.0%; 3.5) to environmental heterogene-
ity and the presence of undisturbed areas in Hill
(Paxixi). In addition, the prevalence of some Stre-
blidae species is affected by habitat fragmentation
on bats sheltering in caves and foliage (Bolívar-
Cimé et al., 2018). Thus, we support that the poor
 Parasitism on bats in urban environments
TABLE 2. Infracommunities of bat flies and relative frequency
on bats captured from February 2014 to May 2015 and from
November 2016 to April 2017 in urban remnants of Cerrado,
Campo Grande, Mato Grosso do Sul, Brazil; a — Infra-
communities with accidental parasite
Frequency
Host (n) Infracommunity
Artibeus planirostris, 92 Megistopoda aranea
Aspidoptera phyllostomatis
Megistopoda aranea+
Aspidoptera phyllostomatis
Megistopoda aranea +
Trichobius angulatusa
Aspidoptera falcataa
Artibeus lituratus, 19 Paratrichobius longicrus
Megistopoda aranea
Aspidoptera phyllostomatis
Trichobius angulatusa
Carollia perspicillata, 55 Trichobius joblingi
Trichobius joblingi+
Strebla guajiro
Platyrrhinus lineatus, 10 Trichobius angulatus
Paratrichobius longicrus
Aspidoptera phyllostomatisa
Glossophaga soricina, 4 Trichobius dugesii
Trichobius joblingia
quality of disturbed areas (i.e., high habitat fragmen-
tation, lower environmental heterogeneity, and
urban climate) affects the quality of available shel-
ters by decreasing host fidelity to such shelters
(Barbier and Graciolli, 2016; Pilosof et al., 2012).
Furthermore, the lack of bat recaptures during this
study supports such idea of high mobility and infi-
delity of bats in these remnants. The infidelity of
bats to shelters directly interferes with parasitism,
since more loyal bats tend to be more easily infested
by emerging bat flies (Barbier and Graciolli, 2016).
Infracommunities
We recorded few infracommunities (16) com-
pared to other studies performed in non-urban areas,
like Santos et al. (2013) who found 18, Aguiar and
Antonini (2016) who found 28, and Dornelles and
Graciolli (2017) who found 31. All the infracommu-
nities found herein have been recorded in other stud-
ies (e.g., Santos et al., 2013; Aguiar and Antonini,
2016; Barbier and Graciolli, 2016; Dornelles and
Graciolli, 2017) and showed dominance of a single
flies species (between 53% and 96%). This pattern
was also found by Barbier and Graciolli (2016) (be-
tween 58% and 96%) and by Dornelles and Graciolli
(2017) (between 62% and 88%). Infracommunities
composed of two bat flies species parasitizing the
515
same bat at the same time were less frequent (18%).
Likewise, our percentage of infracommunities was
low when compared to other studies performed in
non-urban areas, as Santos et al. (2013) (100%),
Aguiar and Antonini (2016) (100%) and Dornelles
%
and Graciolli (2017) (55%).
85
Contrary to our expectations, we found few in-
7 fracommunities and our results suggested infidelity
of bats to their shelters in these remnants. The low
6 number of infracommunities can be explained by bat
richness, since the richness of bat flies tends to in-
1
1 crease with bat species richness (Dick and Gettinger,
53 2005) due to host specificity (Wenzel et al., 1966).
37 However, the dominance of a single bat flies species
5 in the infracommunities suggests low fidelity by
5 hosts to their shelters (see Barbier and Graciolli,
96
2016). Factors related to these shelters may also ex-
4 plain the variation in the frequencies of infracom-
80 munities (e.g., type of shelter or level of aggregation
10 within their colonies) (Santos et al., 2013). That is,
10
if hosts are faithful to these shelters (i.e., high fi-
75
25 delity), the co-occurrence of bat flies species would
be favored (Presley, 2011), which explains the low
frequency of infracommunities with two bat flies
species parasitizing the same bat at the same time.
The presence of such infracommunities can be ex-
plained by the strength of the resulting similarity,
which tends to decrease competition and favor the
association of infracommunities with unrelated
species (Ingram and Shurin, 2009; Krasnov et al.,
2014). This seems to be the case for infracommuni-
ties composed of morphologically distinct bat flies:
M. aranea + A. phyllostomatis on A. planirostris and
M. aranea + T. angulatus on A. planirostris. More-
over, the presence of these bat flies on the same host
is favored because they parasitize different regions
of the bat (Presley, 2011).
Parasitic Specificity
The specificity recorded herein (71% monoxenic
bat flies) was low when compared to Dick and
Gettinger (2005) (87%), Dick (2007) (99.2%),
Santos et al. (2013) (88%) and Vasconcelos et al.
(2016) (76%). In Brazil, the only researchers to use
the STD* index to study bat flies were Vasconcelos et
al. (2016) in Brazilian dry forests. Such studies were
concerned with discriminating and/or excluding
non-primary associations (accidental) and presented
monoxenic bat flies species. Similarly, we excluded
non-primary associations and recommend such ex-
clusion when calculating indices, such as prevalence
and specificity, to avoid false interpretations (see
516 G. L. Urbieta, J. M. Torres, E. A. Carvalho dos Anjos, C. M. Espínola Carvalho, and G. Graciolli
Dick and Gettinger, 2005; Barbier and Bernard,
2017). These highly specific bat flies aretransferred
by contamination to other host species, resulting in
associations that do not spontaneously occur in na-
ture (Marshall, 1981).
As expected, we found low specificity in these
urban and fragmented environments. Even though
we found such result, high parasitic specificity is ex-
pected due to the low survival rate of bat flies on bat
species that are not their usual hosts (Fritz, 1983).
This high specificity can be explained by the previ-
ously discussed factors (i.e., environmental quality,
shelter availability, shelter bat infidelity), as well as
other factors, as immunological incompatibility.
Immunological incompatibility between unusual bat
flies and bats is the main factor linked to high speci-
ficity, since bat flies can mimic their host’s molecu-
lar signals and avoid an immune response by bats
(Dick and Patterson, 2007).
The other 28.5% of bat flies found herein were
oligoxenic or polyxenic. We believe that this low
specificity results from the breakdown of dispersion
barriers (e.g., encounter, compatibility, and repro-
ductive filter) which interfere with specificity and
prevent the parasite from colonizing new hosts
(Combes, 1991; Dick and Patterson, 2007; Vascon-
celos et al., 2016). The breakdown of these barriers
results in the colonization of new hosts and a de-
crease in specificity (Vasconcelos et al., 2016),
which may be influenced by colony size, host biol-
ogy, or absence of primary host (Morand and Poulin,
1998; Hofstede and Fenton, 2005; Bordes et al.,
2008; Dick et al., 2009). Bat flies mobility is an-
other key factor in breaking down barriers and, con-
sequently, specificity (Marshall, 1981). This is evi-
denced by the results of P. longicrus (low specificity
here), which has developed wings (sensu Graciolli
and Carvalho, 2001) facilitating dispersion to other
hosts. However, P. longicrus is a species complex
(Wenzel, 1966), suggesting the specificity of these
bat flies may not be as low as found in this study. On
the other hand, B. ortizi does not have specific hosts
and presents individuals without wings. Therefore,
dispersion occurs by sharing shelter with their hosts,
usually Molossidae and Vespertilionidae bats (Gra-
ciolli and Carvalho, 2001).
Overall, our results suggest a logical order for the
parasitism of bat flies and bats in these environments.
The lower prevalence values (in relation to non-
urban areas) seem to be related to the shelter quality
and environmental disturbances in the remnants and
surrounding areas. Thus, shelter quality and envi-
ronmental disturbances decrease bat fidelity and the
presence of bat flies in the shelters, which generated
the low number of infracommunities recorded here.
Therefore, the low specificity seems to be caused by
the factors reported above and the lower bat richness
in these environments. Herein, we show that even
when we exclude accidental associations, the speci-
ficity remains lower in urban areas. Finally, all of
these results suggest that the characteristics of the
urban environment both directly and indirectly af-
fect parasitism between bat flies and bats.
ACKNOWLEDGEMENTS
We thank the Universidade Católica Dom Bosco (UCDB),
the Parque Linear do Imbirussu and the Área de Preservação do
Córrego Bandeira for providing support and allowing captures
during this study. We are grateful for the valuable contribu-
tions of the anonymous reviewers. We also thank Alessandro
Shinohara and Luciano Brasil Martins de Almeida for assisting
with identification of some of the flies collected. We are grateful
for the team that has intensely assisted with field work, espe-
cially: Allan Corral, Klysman Fernandes, Rafael Oliveira, Tha-
wane Siqueira, Daniela Lopes, Francine Dorneles, Lincoln Hen-
rique, Cláudia Liz and Guilherme Torres. CAPES (case number
1591062), CNPq (case number 304616 / 2015-0) and Fundect
for the grant awarded.
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Received 27 November 2017, accepted 10 July 2018
Associate Editor: M. Corrie Schoeman