Parasitism of ectoparasitic flies on bats in the

Transcrição

DOI: 10.2478/s11686-013-0135-9
© W. Stefański Institute of Parasitology, PAS
Acta Parasitologica, 2013, 58(2), 207–214; ISSN 1230-2821
Parasitism of ectoparasitic flies on bats
in the northern Brazilian cerrado
Ciro Líbio Caldas dos Santos1*, Agostinho Cardoso Nascimento Pereira²,
Vagner de Jesus Carneiro Bastos², Gustavo Graciolli3 and José Manuel Macário Rebêlo²
¹Programa de Pós-graduação em Ecologia e Conservação, Centro de Ciências Biológicas e da Saúde,
Universidade Federal de Mato Grosso do Sul, Campo Grande, CEP 79070-900, Brasil; ²Departamento de Biologia,
Centro de Ciências Biológicas e da Saúde, Universidade Federal do Maranhão, São Luís, CEP 65000-000, Brasil;
³Departamento de Biologia, Universidade Federal de Mato Grosso do Sul, Campo Grande, CEP 79070-900, Brasil
Abstract
In this work we record the highest number of bat flies species among those already performed in the Brazilian cerrado and discuss the associations and patterns of parasitism of these species and their hosts. A total of 1,390 ectoparasitic flies were collected, belonging to 24 species of Streblidae and one of Nycteribiidae, parasitizing 227 bats of 15 species. Among the species
found, the presence of Trichobius sp. on Lonchophylla mordax and the first occurrence of Hershkovitzia sp. on Thyroptera devivoi are highlighted. Lophostoma species presented the highest proportion of individuals with infracommunities and the highest values of parasitological indexes. The high number of bat fly species and hosts, as well as the high values for rates of
parasitism and infracommunities, suggests that this area of cerrado has good shelter conditions for these species. The abundance
of species and high rates of parasitism detracts from the hypothesis that a higher mean intensity of ectoparasites results from
lower competition among flies for hosts in areas with lower ectoparasite species richness. Biogeographical and historical factors of host populations, besides the number of host species and individuals sampled, may contribute to species number and intensity of parasitism.
Keywords
Diptera, Streblidae, Nycteribiidae, Phyllostomidae, savannah, host-parasite associations
Introduction
Among the causes of variation in patterns of parasitism are
characteristics both intrinsic to the host and to the parasite. By
being associated with their hosts for most of their life cycles,
their geographic distribution, behavior, body size, immune defenses and type of shelter are determinants in abundance and
diversity of parasites in a region (Marshall 1982, ter Hofstede
and Fenton 2005, Patterson et al. 2007). Moreover, the rate of
reproduction, the reproductive behavior and sex ratio of ectoparasites (Reckardt and Kerth 2006, Dittmar et al. 2011), as
well as the interspecific relationships in the same host (Patterson et al. 2009; Presley 2011) also contribute to their occurrence.
The dipteran ectoparasites of bats, belonging to the families Streblidae and Nycteribiidae, are obligatorily hemato-
phagous with great morphological variation and high specificity to their hosts (Marshall 1982, Wenzel et al. 1966, Dick
2007). In the neotropics, these families are distributed across
various ecoregions (Prevedello et al. 2005), with more records
in the Amazon region (Wenzel et al. 1966, Wenzel 1976, Guerrero 1997) and in deciduous forests of the south-central portion of the continent (Dick and Gettinger 2005, Bertola et al.
2005, Autino et al. 2009, Camilotti et al. 2010).
In Brazil, the cerrado is characterized by diverse physiognomies and patterns of flora distribution throughout its extent
(Oliveira-Filho and Ratter 2002). Therefore, this biome is of
great importance for understanding the patterns of host-parasite associations in their remaining areas. In Brazil, studies on
bats’ ectoparasitic flies in cerrado region have mainly comprised of faunal inventories (Graciolli and Coelho 2001; Graciolli and Aguiar 2002; Graciolli et al. 2006a, 2010). The few
*Corresponding author: [email protected]
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Ciro Líbio Caldas dos Santos et al.
studies that have addressed quantitative aspects of this system
in this biome are concentrated in areas of west-central Brazil
(Coimbra et al. 1984, Komeno and Linhares 1999, Eriksson et
al. 2011, Aguiar and Antonini 2011).
In this paper we document the highest number of bat fly
species relative to those previously reported from the Brazilian cerrado and describe quantitatively the associations between streblid and nycteribiid flies and their hosts. From the
results discussed here, we intended to contribute to the knowledge of parasitism patterns of these Diptera in the cerrado and
to encourage further research in other areas and cerrado physiognomies that have not yet inventoried.
rainy season in the first six months of the year and drought in
the other months (IMESC 2011). The predominant vegetation
type is cerrado (sensu stricto), also showing formations of
campo cerrado, cerradão, veredas and riparian forest, according to the classification of Oliveira-Filho and Ratter (2002).
Bats were captured at 12 localities in cerrado (sensu
stricto), each more than 3 km apart, and located approximately
200 m from roads. Between January and May 2011, five
nights of capture were performed at each location (18h to 24h)
during periods of waning and new moon. To capture the bats,
we used 12 mist nets (2.5 m x 12 m) arranged in pairs, more
than 20 m distant from each other. The total capture effort was
129,600 m².h according to standards proposed by Straube and
Bianconi (2002).
Materials and methods
The study area is located in the municipality of Barreirinhas
(3º0´S, 43º6´W), state of Maranhão, and represents the northern
limit of cerrado in Brazil (Fig. 1). The climate is semi-arid hot
tropical (Aw type according to Köppen’s classification – Peel
et al. 2007), with mean annual temperature exceeding 27ºC. The
annual rainfall varies between 1,200 mm and 1,600 mm, with
For collection of ectoparasite flies, the bats’ body surface was
searched and flies were collected with forceps and preserved
in 70% alcohol. In order to identify the recaptures, all bats
were marked, by cutting part of the dorsal fur, before being
released. Bat species were identified according to the classification given by Gardner (2007). The ectoparasitic flies were
identified using keys of Wenzel (1976), Wenzel et al. (1966)
Fig. 1. Location of the study area (arrow) at the northern edge of the Brazilian cerrado (gray area). Figure source: Oliveira-Filho and Ratter
(2002)
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Parasitism on bats in the northern cerrado boundary
and Guerrero (1994a, 1994b, 1995, 1996). The voucher specimens of each species of bats and ectoparasites are deposited
in the Zoological Reference Collection of the Federal University of Mato Grosso do Sul (ZUFMS) and in the Zoological Collection of the Laboratory of Entomology and Vectors,
Federal University of Maranhão.
We adopted the definitions proposed by Bush et al. (1997)
for the component community (set of ectoparasite species
found on one host species), infracommunity (community of
ectoparasite populations on a single host), prevalence (number
of infested hosts/number of captured hosts) and mean intensity
of infestation (mean of parasites per infested host). The percentage of the total abundance of a single ectoparasite species
found on each host species is presented in the specificity
index, according to Dick and Gettinger (2005). To calculate
the confidence intervals for the prevalence and mean intensity
of infestation we used the software Quantitative Parasitology
3.0 (Rózsa et al. 2000). Infestations in non-primary hosts occurred on nights when the main host was captured were considered accidental, according to Dick (2007).
Results
We captured 487 bats belonging to 27 species and four families (Molossidae, Phyllostomidae, Vespertilionidae and Thyropteridae). The phyllostomid species totaled 85.2% of the
captures, the most abundant being Artibeus cinereus Gervais,
Table I. Prevalence and mean intensity values of streblid and nycteribiid species on their respective host bat species
Host (n)
Artibeus planirostris (39)
Carollia perspicillata (106)
Desmodus rotundus (15)
Glossophaga soricina (9)
Lonchophylla mordax (25)
Lonchophylla thomasi (3)
Lophostoma brasiliense (7)
Lophostoma carrikeri (48)
Lophostoma silvicolum (28)
Mimon crenulatum (15)
Phyllostomus discolor (13)
Phyllostomus hastatus (8)
Sturnira lilium (6)
Thyroptera devivoi (2)
Tonatia bidens (9)
Ectoparasite (n)
Aspidoptera phyllostomatis(14)
Megistopoda aranea (24)
Speiseria ambigua (17)
Strebla guajiro (13)
Trichobius joblingi (135)
Trichobius parasiticus (17)
Trichobius dugesii (1)
Trichobius sp. (17) a
Trichobius sp. (1) a
Mastoptera minuta (59)
Strebla hoogstraali (16)
Trichobius silvicolae (8)
Pseudostrebla sparsisetis (90)
Stizostrebla longirostris (175)
Trichobius joblingi (1) b
Pseudostrebla greenwelli (2)
Pseudostrebla riberoi (9)
Stizostrebla longirostris (1) b
Strebla tonatiae (9)
Trichobius silvicolae (1)
Basilia mimoni (10)
Strebla hertigi (2)
Trichobioides perspicillatus (9)
Trichobius costalimai (42)
Trichobius longipes (13)
Aspidoptera falcata (18)
Megistopoda proxima (5)
Hershkovitzia sp. (1) a
Strebla galindoi (4)
P (95% CI)
MI (95% CI)
25.6 (13.0–42.1)
33.3 (19.1–50.2)
12.3 (6.7–20.1)
10.4 (5.3–17.9)
54.7 (44.7–64.4)
53.3 (26.6–78.7)
11.1c
28 (12.1–49.4)
33.3 c
85.7 (42.1–99.6)
57.1 (18.4–90.1)
42.9 (9.9–81.6)
97.9 (88.9–99.9)
52.1 (37.2–66.7)
83.3 (69.8–92.5)
2.1 c
78.6 (59.0–91.7)
3.6 c
21.4 (8.3–41.0)
3.6 c
7.1 (0.9–23.5)
3.6 c
33.3 (11.8–61.6)
15.4 (1.9–45.4)
38.5 (13.8–68.4)
92.3 (64.0–99.8)
25 (3.2–65.1)
62.5 (24.5–91.5)
66.7 (22.3–95.7)
33.3 (4.3–77.7)
50 c
22.2 (2.8–60.0)
1.4 (1.0–1.8)
1.8 (1.3–2.8)
1.3 (1.1–1.7)
1.2 (1.0–1.4)
2.3 (2–2.8)
2.1 (1.5–2.7)
1c
2.3 (1.3–4.4)
1c
9.8 (4.3–20.3)
4 (1.0–5.5)
2.7 (2.0–3)
11.3 (9.3–14)
3.6 (2.4–5.8)
4.4 (3.4–5.6)
1c
5.9 (3.7–11.5)
2c
1.5 (1.0–2.2)
1c
4.5 (1.0–4.5)
1c
2 (1.0–3.6)
1c
1.8 (1.0–2.4)
3.5 (2.0–5.2)
1c
2.6 (1.2–4)
4.5 (1.7–6.5)
1.5 (1.0–2.0)
1c
2 (1.0–3.0)
SI
100
100
100
100
99.3
100
100
100
100
8.1
100
88.9
73.6
100
99.4
0.7
17.9
100
100
0.5
100
11.1
100
100
100
100
0.3
100
100
100
100
100
P – prevalence (%), MI – mean intensity of infestation, CI – confidence interval; SI – specificity index (%); a – new records of parasitism in
the host b – accidental associations; c – insufficient data to calculate the CI.
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1856 (24.1%), Carollia perspicillata (Linnaeus, 1758)
(21.8%) and Lophostoma carrikeri (JA Allen, 1910) (9.9%).
227 bats (15 species) had ectoparasites (Table I), no parasitism
was verified for A. cinereus – 117 individuals captured, A. lituratus (Olfers, 1818) – 7, A. obscurus (Schinz, 1821) – 10, Carollia brevicauda (Schinz, 1821) – 1, Micronycteris microtis
Miller, 1898 – 3, Phylloderma stenops Peters, 1865 – 1,
Platyrrhinus lineatus (E. Geoffroy, 1810) – 9, Trinycteris nicefori Sanborn, 1949 – 1, Uroderma bilobatum Peters, 1866 – 2
(Phyllostomidae), Cynomops planirostris (Peters, 1865) – 1
(Molossidae), Eptesicus furinalis (d’Orbigny, 1847) – 1 and
Myotis riparius Handley, 1960 – 1 (Vespertilionidae).
We collected 1,390 ectoparasitic flies, representing 24
species (10 genera) of Streblidae and one of Nycteribiidae;
N
%
4
19
among them, 22 (88%) were monoxenous (associated with a
single host species), two oligoxenous (present in congeneric
host species) and one polyxenous (associated with non-congeneric host species). Four bats with ectoparasites were recaptured: three individuals of the species C. perspicillata –
infested by 12 flies of the species Trichobius joblingi Wenzel,
1966, one of Speiseria ambigua Kessel, 1925 and one of Strebla guajiro (García et Casal, 1965); and one individual of Lonchophylla mordax Thomas, 1903 parasitized by the streblid
Trichobius sp. The streblids on hosts that were recaptured
were not considered for analyzing the patterns of parasitism,
since they do not represent an independent sample of the population.
Most host-parasite species associations were exclusive
(68.7%), with specificity index equal to 100% (Table I), and
with one streblid species (59.5% of infested hosts). The
species with the highest number of infracommunities of ectoparasites was L. carrikeri, with 44.7% of associations with
three streblid species and 48.9% with two (Table II). Regarding the ectoparasites, the species with highest number of nonaccidental associations was Mastoptera minuta (Costa Lima,
1921), found in four host species.
Speiseria ambigua + Trichobius joblingi
7
10.4
Discussion
Strebla guajiro + Trichobius joblingi
7
10.4
S. ambigua + S. guajiro + T. joblingi
3
4.5
2
28.6
2
28.6
M. minuta + Pseudostrebla sparsisetis
4
8.5
M. minuta + Stizostrebla longirostris
19
38.3
M. minuta + P. sparsisetis + S. longirostris
21
44.7
1
2.1
M. minuta + Pseudostrebla riberoi
5
20.8
M. minuta + Pseudostrebla greenwelli
+ Strebla tonatiae
M. minuta + S. tonatiae + T. silvicolae
1
4.2
1
4.2
4
30.7
1
7.7
1
7.7
2
33.3
3
75
Table II. Number of hosts infested by infracommunities of ectoparasitic flies (N) and percentage of total parasitized bats in cerrado area
studied
Hosts (n)/Ectoparasite
Artibeus planirostris (21)
Aspidoptera phyllostomatis
+ Megistopoda aranea
Carollia perspicillata (67)
Lophostoma brasiliense (7)
Mastoptera minuta + Strebla hoogstraali
M. minuta + S.hoogstraali
+ Trichobius silvicolae
Lophostoma carrikeri (47)
M. minuta + S. longirostris + T. joblingi
Lophostoma silvicolum (24)
Phyllostomus discolor (13)
Trichobioides perspicillatus
+ Trichobius costalimai
Strebla hertigi + T. perspicillatus
+ T. costalimai
S. hertigi + T. costalimai
Phyllostomus hastatus (6)
M. minuta + Trichobius longipes
Sturnira lilium (4)
Aspidoptera falcata
+ Megistopoda proxima
The number of ectoparasitic fly species recorded in this study
(25) was higher than in most studies already performed in
South America, being lower only than inventories carried out
in various locations in Paraguay (Dick and Gettinger 2005, 31
species) and South Brazil (Prevedello et al. 2005, 32). In cerrado areas, other studies have recorded fewer species, including Graciolli et al. (2010, 21 species), Eriksson et al. (2011,
17) and Komeno and Linhares (1999, 12).
Among factors that may attribute to the highest number of
bat fly species found in the cerrado, we propose: 1) the study
area’s location near the Amazon eastern transition zone (Ab
‘Saber 1977), which includes the distributional limit of various host species (Simmons 2005) that can support different
component communities; 2) factors external to the host that
can affect the abundance of ectoparasites and their hosts, such
as the type of climate, vegetation (Prevedello et al. 2005) or
host shelter (Wenzel et al. 1966, Patterson et al. 2007); 3) the
highest number of individuals and host species than those reported in other studies with less rich and abundant fauna, such
as those conducted in deciduous forest (Camilotti et al. 2010)
and caatinga (Rios et al. 2008), a result that could favor the
sample of host species with different component communities
as well as the finding of bat fly species that occur in low prevalence in their host species; 4) the major sampling effort that
may contribute to the finding of more host species and individuals, which is comparable just to the realized in Atlantic
forest by Bertola et al. (2005, with 84% of our sampling effort
and 22 bat fly species) and is greater than the others already
carried out in cerrado (Graciolli et al. 2010, Eriksson et al.
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2011) – that had, at most, the half of the sampling effort of
this study.
Changes in component communities of ectoparasitic flies
in host species can be attributed to the regional differences in
species composition of bats, to the biogeographic history of
the area or to the lack of specificity of ectoparasites (Rui and
Graciolli 2005). In addition to the new records of associations
(Table I), we found the following variations in the component
communities: the absence of Paraeuctenodes similis Wenzel,
1976 on C. perspicillata, association observed in regions of
Atlantic forest (Bertola et al. in 2005, Prevedello et al. 2005)
and Amazon forest (Guerrero 1996); the absence of Metelasmus pseudopterus Coquillet, 1907, which is found parasitizing
species of Artibeus from the south-central Brazil (Eriksson et
al. 2011, Bertola et al. 2005); the lower number of ectoparasitic species on Desmodus rotundus (E. Geoffroy, 1810), that
in other areas of cerrado is also parasitised by Trichobius furmani Wenzel, 1966 and Strebla wiedemanni Kolenati, 1856
(Eriksson et al. in 2011, Aguiar and Antonini 2011); the absence of Trichobius uniformis Curran, 1935 and Strebla curvata Wenzel, 1976 on Glossophaga soricina (Pallas, 1766),
found on this species in cerrado areas (Eriksson et al. 2011,
Graciolli et al. 2010), in addition to the parasitism by Paraeuctenodes longipes Pessoa et Guimaraes, 1937 recorded in the
southern Brazil (Graciolli and Rui 2001). It is also highlighted
the absence of parasitism on A. cinereus, a species with register of parasitism by ectoparasitic flies of the genus Neotrichobius Wenzel and Aitken, 1966 in the Amazon region
(Guerrero 1994a).
Only two accidental associations were recorded, T. joblingi
on L. carrikeri and Stizostrebla longirostris Jobling, 1939 on
Lophostoma silvicolum Tomes, 1863. Excluding these associations, we found a proportion of monoxenous species (88%)
similar to the study performed by Dick and Gettinger (2005,
87.1%), who also prioritized methods that reduced the number
of accidental associations. The only polyxenous species found
(M. minuta) is currently grouped into a complex, by having
little morphological variation among individuals from different host species (Wenzel 1976). However, its greater specificity recorded in Lophostoma (99.6%) in this study corroborates its high abundance on bats of this genus (Guerrero
1995, Wenzel 1976).
The prevalence and mean intensity of infestation of T.
joblingi on C. perspicillata (54.7% and 2.3, respectively) had
a value intermediate to those found in other regions of cerrado
by Komeno and Linhares (1999, 66%, 2.1) and Eriksson et al.
(2011, 40.5%, 2.8). We observed this difference in prevalence
also in the associations between: Trichobius parasiticus Gervais, 1844 and D. rotundus (53.3%), higher than those
recorded in Paraguay (Dick and Gettinger 2005, 31.4%) and
in caves from the central-western Brazil (Aguiar and Antonini
2011, 29.5%); Aspidoptera falcata Wenzel, 1976 and Sturnira
lilium (E. Geoffroy, 1810) (66.7%), with higher values than
those observed in cerrado (Eriksson et al. in 2011, 21.3%), Atlantic forest (Graciolli et al. 2006b, 10%) and Araucaria for-
est (Graciolli and Bianconi 2007, 13.5%). Although most studies do not show the confidence interval of ectoparasite prevalence, this variation among values observed in studies from
different regions supports the hypothesis that the streblid distribution in the different host populations is highly variable
(Graciolli and Bianconi 2007).
The protection and durability of host’ shelters are factors
that favor the increase of infestation of flies on bats, since they
favor the development of ectoparasite pupae in these shelters
(ter Hofstede and Fenton 2005) and favor the likelihood of
bats to colonize upon eclosion (Patterson et al. 2007). Among
the parasitized species found, there was a higher proportion
of phyllostomines (46.7%) and nectarivorous (20%) bats than
in other studies in the Neotropics with similar capture effort,
in which represented less than 40% of species infested
(Bertola et al. 2005, Eriksson et al. 2011, Komeno and Linhares 1999). The species of these groups have more durable
shelters, mainly inhabiting hollow trees, caves and nests of
termites (Fenton et al. 2001, Bernard and Fenton 2003). This
major occurrence of phyllostomines and nectarivorous species
possibly have contributed to the greatest number of bat flies
species recorded, since their roosting habits could favor them
to harbor parasites (Patterson et al. 2007). Likewise, the lower
frequency of parasitism on stenodermatines, the most abundant group found, may be related to their lower fidelity and
durability of their shelters, since these bats refuge mainly in
foliage and may change shelter more frequently (Fenton et al.
2001).
The associations of Pseudostrebla greenwelli Wenzel,
1966, Strebla tonatiae (Kessel, 1924) and Trichobius silvicolae Wenzel, 1976 with L. silvicolum, in spite of having low
prevalence, were considered natural, since their primary hosts
were not captured on the same night. Pseudostrebla greenwelli and S. tonatiae are found mainly in Lophostoma brasiliense (Peters, 1866) (Guerrero 1994a, Dias et al. 2009, Graciolli and Bernard 2002), the first having only six specimens
in collections (Guerrero 1996, Graciolli and Bernard 2002).
However, the species T. silvicolae, although appearing with
greater prevalence in L. brasiliense, parasitizes mainly L. silvicolum (Wenzel 1976, Graciolli and Bernard 2002).
The species of Lophostoma primarily use termite nests as
shelter (Bernard and Fenton 2003, Kalko et al. 1999), which
in cerrado areas play a key role as refuges resistant to seasonal
burning (Redford 1984). Since L. silvicolum had been found
in three of the four capture points where L. brasiliense was
present, the inverse prevalence of ectoparasitic flies between
these hosts species may be related to shelter sharing by individuals of Lophostoma. The low availability of termite nests
in the study area for the abundance of Lophostoma observed
may be the reason for this probable sharing, as well as for the
highest values of the parasitological indexes in these species
(Table I).
In the neotropics, bat species harboring more than one
fly species has been observed also in areas of tropical forest
(Teixeira and Ferreira 2010, Bertola et al. 2005), cerrado
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(Aguiar and Antonini 2011), Venezuela (Wenzel 1976) and
eastern Amazon forest (Santos et al. 2009). In this study, the
highest proportion of hosts with infracommunities of ectoparasitic flies (40.5%) was found mainly in Lophostoma
species (Table II). We note also the occurrence in all infracommunities of the same host species the presence of the
most abundant fly species (M. minuta, T. costalimai and T.
joblingi), co-occurrence pattern also observed in other studies in the parasitism of M. proxima on S. lilium (Bertola et al.
2005), T. joblingi on C. perspicillata and T. costalimai on P.
discolor (Santos et al. 2009). With the exception of species
of Lophostoma, all infracommunities of other host species
had been recorded in other studies (Bertola et al. 2005, Santos et al. 2009).
Regarding the number of individuals with infracommunities, we found a value higher than that reported by Bertola et
al. (2005) and Santos et al. (2009) for S. lilium, even with less
number of infestations (four) in this species. In C. perspicillata, we observed lower proportion of individuals infected
with infracommunities (25.4%) than in these studies, which
have captured less infested individuals (30 and 12, respectively). The variation in the frequency of infracommunities of
flies may suggest the existence of ecological factors of the bats
(e.g., type of shelter or level of aggregation within their
colonies) which should facilitate finding hosts by parasites,
which in turn would favor the co-occurrence of fly species
(Presley 2011). This relationship may be responsible for
higher incidence of infracommunities of flies on hosts with
more durable shelters, as the species of Lophostoma herein
recorded.
The high number of bat fly species and hosts, as well as the
high values of parasitism rates and infracommunities, shows
that the northern cerrado area has good shelter conditions for
these species. This abundance of both species and ectoparasites per host is opposed to the hypothesis that a higher mean
intensity of ectoparasites would be a result of less competition for hosts by flies in areas with lower richness of ectoparasite species (Camilotti et al. 2010). Probably, biogeographical and historical factors of host populations in each area,
besides the number of species and individuals sampled, should
also have their contribution in species number and intensity
of infestation of ectoparasites. However, further efforts are
needed to understand the processes influencing patterns of parasitism over the distribution of ectoparasite fly species, in
order to relate them to different types of climate, vegetation
and host populations in the Neotropics.
Acknowledgement. We thank the Fundação de Amparo à Pesquisa
e ao Desenvolvimento Científico e Tecnológico do Maranhão (FAPEMA) and the Conselho Nacional de Desenvolvimento Científico
e Tecnológico (CNPq) by grants related to this work, besides the
scholarship to C.L.C. Santos granted by the latter institution. We also
thank Gustavo A. Brito, Jorge L.P. Moraes, Joudellys A. Silva, Leandro S. Moraes and Marco A.M. Ferreira for support in field work,
as well as Marcelo A. Bordignon for taxonomic confirmation of host
species.
References
Ab’Saber A.N. 1977. Os domínios morfoclimáticos na América do
Sul. Geomorfologia, 52, 1–21.
Aguiar L.M.Z., Antonini Y. 2011. Descriptive ecology of bat flies
(Diptera: Hippoboscoidea) associated with vampire bats (Chiroptera: Phyllostomidae) in the cerrado of Central Brazil.
Memórias do Instituto Oswaldo Cruz, 106, 170–176. DOI:
10.1590/S0074-02762011000200009.
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, 165–177. DOI: 10.1590/S1519-566X2009000200002.
Bernard E., Fenton M.B. 2003. Bat mobility and roosts in a fragmented landscape in Central Amazonia, Brazil. Biotropica,
35, 262–277. DOI: 10.1646/02156.
Bertola P.B., Aires C.C., Favorito S.E., Graciolli G., Amaku M., Pintoda-Rocha R. 2005. Bat flies (Diptera: Streblidae, Nycteribiidae) parasitic on bats (Mammalia: Chiroptera) at Parque
Estadual da Cantareira, São Paulo, Brasil: parasitism rates and
host-parasite associations. Memórias do Instituto Oswaldo
Cruz, 100, 25–32. DOI: 10.1590/S0074-02762005000100005.
Bush A.O., Lafferty J.M., Lotz J.M., Shostak A.W. 1997. Parasitology
meets ecology in its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583. DOI: 10.2307/3284227.
Camilotti V.L., Graciolli G., Weber M.M., Arruda J.L.S., Cáceres N.C.
2010. Bat flies from the deciduous Atlantic Forest in southern
Brazil: host-parasite relationships and parasitism rates. Acta Parasitologica, 55, 194–200. DOI: 10.2478/s11686-010-0026-2.
Coimbra C.E.A., Guimarães L.R., Mello D.A. 1984. Ocorrência de
Streblidae (Diptera: Pupipara) em morcegos capturados em
regiões de cerrado do Brasil central. Revista Brasileira de Entomologia, 28, 547–550.
Dias P.A., Santos C.L.C., Rodrigues F.S., Rosa L.C., Lobato K.S.,
Rebêlo J.M.M. 2009. Espécies de moscas ectoparasitas (Diptera, Hippoboscoidea) de morcegos (Mammalia, Chiroptera)
no estado do Maranhão. Revista Brasileira de Entomologia,
53, 128–133. DOI: 10.1590/S1519-566X2009000500006.
Dick C.W. 2007. High host specificity of obligate ectoparasites. Ecological Entomology, 32, 446–450. DOI: 10.1111/j.1365-2311.
2006.00836.x.
Dick C.W., Gettinger D. 2005. A faunal survey of streblid flies
(Diptera: Streblidae) associated with bats in Paraguay. Journal
of Parasitology, 91, 1015–1024. DOI: 10.1645/GE-536R.1.
Dittmar K., Morse S., Gruwell M., Mayberry J., DiBlasi E. 2011.
Spatial and temporal complexities of reproductive behavior
and sex ratios: a case from parasitic insects. PLoS ONE, 6, 1–
9. DOI: 10.1371/journal.pone.0019438.
Eriksson A., Graciolli G., Fischer E. 2011. Bat flies on phyllostomid
hosts in the Cerrado region: component community, prevalence and intensity of parasitism. Memórias do Instituto Oswaldo Cruz, 106, 274–278. DOI: 10.1590/S0074-02762011
000300004.
Fenton M.B., Bernard E., Bouchard S., Hollis L., Johnston D.S.,
Lausen C.L., Ratcliffe J.M., Riskin D.K., Taylor J.S., Zigouris
J. 2001. The bat fauna of Lamanai, Belize: roosts and trophic
roles. Journal of Tropical Ecology, 17, 511–524. DOI: 10.1017/
S0266467401001389.
Gardner A.L. (Ed.). 2007. Mammals of South America: Volume 1,
marsupials, xenarthrans, shrews and bats. The University of
Chicago Press, Chicago, 690 pp.
Graciolli G., Aguiar L.S. 2002. Ocorrência de moscas ectoparasitas
(Diptera, Streblidae e Nycteribiidae) de morcegos (Mammalia, Chiroptera) no Cerrado de Brasília, Distrito Federal, Brasil. Revista Brasileira de Zoologia, 19, 177–181. DOI: 10.1590/
S0101-81752002000500012.
Authenticated
213
Graciolli G., Bernard E. 2002. Novos registros de moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae) em morcegos
(Mammalia, Chiroptera) do Amazonas e Pará, Brasil. Revista
Brasileira de Zoologia, 19, 77–86. DOI: 10.1590/S010181752002000500003.
Graciolli G., Bianconi G.V. 2007. Moscas ectoparasitas (Diptera,
Streblidae e Nycteribiidae) em morcegos (Mammalia, Chiroptera) em área de Floresta com Araucária no Estado do Paraná, sul do Brasil. Revista Brasileira de Zoologia, 24,
246–249. DOI: 10.1590/S0101-81752007000100033.
Graciolli G., Coelho D.C. 2001. Streblidae (Diptera, Hippoboscoidea) sobre morcegos filostomídeos (Chiroptera, Phyllostomidae) em cavernas do Distrito Federal. Revista Brasileira de
Zoologia, 18, 965–970. DOI: 10.1590/S0101-8175200100030
0028.
Graciolli G., Cáceres N.C., Bornschein M.R. 2006a. Novos registros
de moscas ectoparasitas (Diptera, Streblidae e Nycteribiidae)
de morcegos (Mammalia, Chiroptera) em áreas de transição
cerrado-floresta estacional no Mato Grosso do Sul, Brasil.
Biota Neotropica, 6, 1–4.
Graciolli G., Passos F.C., Pedro W.A., Lim B.K. 2006b. Moscas ectoparasitas (Diptera, Streblidae) de morcegos filostomídeos
(Mammalia, Chiroptera) na Estação Ecológica de Caetetus,
São Paulo, Brasil. Revista Brasileira de Zoologia, 23, 298–
299. DOI: 10.1590/S0101-81752006000100025.
Graciolli G., Rui A.M. 2001. Streblidae (Diptera, Hippoboscoidea)
em morcegos (Chiroptera, Phyllostomidae) no nordeste do
Rio Grande do Sul, Brasil. Iheringia, 90, 85–92. DOI:
10.1590/S0073-47212001000100009.
Graciolli G., Zórtea M., Carvalho L.F.A.C. 2010. Bat flies (Diptera,
Streblidae and Nycteribiidae) in a Cerrado area of Goiás State,
Brazil. Revista Brasileira de Entomologia, 54, 511–514. DOI:
10.1590/S0085-56262010000300025.
Guerrero R. 1994a. Catalogo de los Streblidae (Diptera: Pupipara)
parasitos de murciélagos (Mammalia: Chiroptera) del Nuevo
Mundo. IV. Trichobiinae com alas desarrolladas. Boletin Entomologia Venezolana, 9, 161–192.
Guerrero R. 1994b. Catalogo de los Streblidae (Diptera: Pupipara)
parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo
Mundo. II. Los grupos: pallidus, caecus, major, uniformis y
longipes del gênero Trichobius Gervais, 1844. Acta Biologica
Venezuelica, 15, 1–18.
Guerrero R. 1995. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del Nuevo
Mundo. V. Trichobiinae com alas reducidas o ausentes y miscelaneos. Boletin Entomologia Venezolana, 10, 135–160.
Guerrero R. 1996. Catalogo de los Streblidae (Diptera: Pupipara)
parasitos de murciélagos (Mammalia, Chiroptera) del Nuevo
Mundo. VI. Streblinae. Acta Biologica Venezuelica, 16,
1–26.
Guerrero R. 1997. Catalogo de los Streblidae (Diptera: Pupipara) parasitos de murcielagos (Mammalia: Chiroptera) del novo
mundo. VII. Lista de especies, hospedadores y países. Acta
Biologica Venezuelica, 17, 9–24.
IMESC – Instuto Maranhense de Estudos Socioeconômicos e cartográficos (2011) Mapas cartográficos do Maranhão. Available
in: http://www.imesc.ma.gov.br (accessed March, 2012).
Kalko E.K.V., Friemel D., Handley Jr., C.O., Schnitzler H. 1999.
Roosting and foraging behavior of two neotropical gleaning
bats, Tonatia silvicola and Trachops cirrhosus (Phyllostomidae). Biotropica, 31, 344–353. DOI: 10.1111/j.1744-7429.
1999.tb00146.x.
Komeno C.A., Linhares A.X. 1999. Bat flies parasitic on some Phyllostomidae bats in southeastern Brazil: Parasitism rates and
host-parasite relationships. Memórias do Instituto Oswaldo
Cruz, 94, 151–156.
Marshall A.G. 1982. Ecology of insects ectoparasitic on bats. In: (Ed.
T.H. Kunz) Ecology of Bats. Plenum Press, New York, USA,
69–401.
Oliveira-Filho A.T., Ratter J.A. 2002. Vegetation physiognomies and
woody flora of the cerrado biome. In: (Eds. P.S. Oliveira and
R.J. Marquis) The cerrados of Brazil. Ecology and natural
history of a Neotropical savanna. Columbia University Press,
New York, 91–120.
Patterson B.D., Dick K.W., Dittmar K. 2007. Roosting habits of bats
affect their parasitism by bat flies (Diptera: Streblidae). Journal of Tropical Ecology, 23, 177–189. DOI: 10.1017/S0266
467406003816.
Patterson B.D., Dick K.W., Dittmar K. 2009. Nested distributions of
bat flies (Diptera: Streblidae) on Neotropical bats: artifact and
specificity in host-parasite studies. Ecography, 32, 1–7. DOI:
10.1111/j.1600-0587.2008.05727.x.
Peel M.C., Finlayson B.L., McMahon T.A. 2007. Updated world map
of the Köppen-Geiger climate classification. Hydrology and
Earth System Science, 11, 1633–1644. DOI: 10.5194/hess-111633-2007.
Presley S.J. 2011. Interspecific aggregation of ectoparasites on bats:
importance of hosts as habitats supersedes interspecific interactions. Oikos, 120, 832–841. DOI: 10.1111/j.1600-0706.
2010.19199.x.
Prevedello J.A., Graciolli G., Carvalho C.J.B. 2005. A fauna de dípteros (Streblidae e Nycteribiidae) ectoparasitas de morcegos
(Chiroptera) do estado do Paraná, Brasil: Composição, distribuição e áreas prioritárias para novos estudos. Biociências,
13, 193–209.
Reckardt K., Kerth G. 2006. The reproductive success of the parasitic
bat fly Basilia nana (Diptera: Nycteribiidae) is affected by the
low roost fidelity of its host, the Bechstein’s bat (Myotis bechsteinii). Parasitology Research, 98, 237–243. DOI: 10.1007/
s00436-005-0051-5.
Redford K.H. 1984. The termitaria of Cornitermes cumulans
(Isoptera, Termitidae) and their role in determining a potential keystone species. Biotropica, 16, 112–119.
Rios G.F.P., Sá-Neto R.J., Graciolli G. 2008. Fauna de dípteros parasitos de morcegos em uma área de caatinga do nordeste do
Brasil. Chiroptera Neotropical, 14, 339–345.
Rózsa L., Reiczigel J., Majoros G. 2000. Quantifying parasites in
samples of hosts. Journal of Parasitology, 86, 228–232. DOI:
10.2307/3284760.
Rui A.M., Graciolli G. 2005. Moscas ectoparasitas (Diptera, Streblidae) de morcegos (Chiroptera, Phyllostomidae) no sul do Brasil: associações hospedeiros-parasitos e taxas de infestação.
Revista Brasileira de Zoologia, 22, 438–445. DOI: 10.1590/
S0101-81752005000200021.
Santos C.L.C., Dias P.A., Rodrigues F.S., Lobato K.S., Rosa L.C.,
Oliveira T.G., Rebêlo J.M.M. 2009. Moscas ectoparasitas
(Diptera: Streblidae) de morcegos (Mammalia: Chiroptera)
do município de São Luís, MA: taxas de infestação e associações parasito-hospedeiro. Neotropical Entomology, 38,
595–601. DOI: 10.1590/S1519-566X2009000500006.
Simmons N.B. 2005. Order Chiroptera. In: (Eds. D.E. Wilson, D.M.
Reeder) Mammal species of the world: a taxonomic and geographic reference. Johns Hopkins University Press, Baltimore, 312–529.
Straube F.C., Bianconi G.V. 2002. Sobre a grandeza e a unidade utilizada para estimar o esforço de captura com utilização de redes-de-neblina. Chiroptera Neotropical, 8, 150–
152.
Teixeira A.L.M., Ferreira R.L. 2010. Fauna de dípteros parasitas
(Diptera: Streblidae) e taxas de infestação em morcegos presentes em cavidades artificiais em Minas Gerais. Chiroptera
Neotropical, 16, 748–754.
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214
ter Hofstede H.M., Fenton M.B. 2005. Relationships between roost
preferences, ectoparasite density and grooming behaviour of
neotropical bats. Journal of Zoology, 266, 333–340. DOI:
10.1017/S095283690500693X.
Wenzel R.L. 1976. The streblid batflies of Venezuela (Diptera: Streblidae). Brigham Young University, Science Bulletin, Biological Series, 20, 1–177.
Wenzel R.L., Tipton V.J., Kiewlicz A. 1966. The streblid bat flies of
Panama (Diptera: Calyptera: Streblidae). In: (Eds. R.L. Wenzel and V.J. Tipton) Ectoparasites of Panama. Field Museum
of Natural History, Chicago, Illinois, USA, 405–675.
(Accepted February 28, 2013)
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