An Acad Bras Cienc (2021) 93(2): e20190549 DOI 10.

1590/0001-3765202120190549
Anais da Academia Brasileira de Ciências | Annals of the Brazilian Academy of Sciences
Printed ISSN 0001-3765 I Online ISSN 1678-2690
www.scielo.br/aabc | www.fb.com/aabcjournal

ECOSYSTEMS

Diet of arthropodophagous bats (Mammalia,

Chiroptera) from Northwestern Argentina

SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ

Abstract: The diet of arthropodophagous bats can be influenced by several factors.

Furthermore, its study is critical for understanding their role in the ecosystem as
regulators of arthropod abundance. The aim of this study was to analyze the diet of 12
species beloging to two families of arthropodophagous bats from the Yungas Forests,
Northwestern Argentina. We also evaluated differences in diet between well-preserved
and disturbed sites, sexes, and seasons. The specimens were collected with mist nets
in eight different localities, four well-preserved and four disturbed sites of the Yungas
Forests. Through the analysis of feces, arthropod remains were identified until the
lowest possible taxonomic level. Volume and frequency of occurrence percentages for
each food item and the niche breadth for the species were estimated. A total of 475
samples from 12 species were analyzed and their diet contained arthropods from eight
orders and seven families; the highest number of consumed arthropod orders were
registered for Eptesicus diminutus. A low niche breadth was recorded in general for all
species. The diet was significantly influenced by season and site characteristics only in
E. diminutus and E. furinalis, respectively. This showed that bats could modify its diet
according to the different habitats and seasons.
Key words: feeding habits, Molossidae, Vespertilionidae, Yungas Forests.

INTRODUCTION At present, there are more than 1,400

recognized species of bats worldwide (Fenton
The structure of an assemblage is affected by & Simmons 2014), and about 75% of them
several ecological parameters, being the diet feed on arthropods (Hutson et al. 2001).
one of the most important (Vitt & Zani 1998). Arthropodophagous bats are voracious
Food is a key dimension of the niche (Krebs predators of nocturnal arthropods, including
1999), and the studies about feeding habits are many crop and forest pests, providing substantial
crucial in our understanding of the ecological ecosystem services (Boyles et al. 2011). The food
relationships between species and their habitat habits of these bats can be influenced by several
(Belver & Avila 2002). Additionally, this basic factors, including the time of emergence (Lee &
information can be useful in the evaluation of McCracken 2001), seasons changes and nutrient
the conservation status of some poorly known demands (Kunz et al. 1995, Lee & McCracken
species (Reca et al. 1994). Species at the highest 2002), temporal and spatial distribution of their
trophic levels are more affected by the human prey (Whitaker et al. 1996, Henry et al. 2002),
activities, as well as specialist species with and weather conditions (Lee & McCracken
narrow trophic niches (Bunnel 1978, Reca et al. 2005). Dietary studies of arthropodophagous
1994). bats are critical for understanding their role in

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

the ecosystem and as regulators of arthropod ecology of arthropodophagous bats is that the
abundance (Debelica et al. 2006). arthropods consumed often vary seasonally
Although most species of bats are and in different habitats (Whitaker et al. 2009).
arthropodophagous (Shiel et al. 1997), in tropical Moreover, previous studies on diet of other
environments they are usually not the dominant arthropodophagous bat species from the same
guild, whereas at higher latitudes its importance study area found differences in foraging activity
in the structure of bat communities increases in different types of land use and between
(Gamboa Alurralde et al. 2017). In Argentina, the seasons, but no significant differences between
arthropodophagous species are dominant and sexes (Gamboa Alurralde & Díaz 2018, 2019).
represent 74 % of the 67 species of bats (Barquez Therefore, we expect to observe differences
& Diaz 2020, Díaz et al. 2016, Urquizo et al. 2017, in the diet of these arthropodophagous bat
Sánchez et al. 2019). Three of the five families of species among types of sites and seasons but
bats registered in the country, Emballonuridae, not between males and females.
Molossidae, and Vespertilionidae are entirely
arthropodophagous. In the other two families,
Noctilionidae and Phyllostomidae, three species MATERIALS AND METHODS
belong to this guild (Díaz et al. 2016). Study area
In Argentina, the first studies of feeding The area belongs to the Yungas Forests
habits of bats were focused on frugivorous ecoregion (Burkart et al. 1999), and it is
species (Iudica 1995, Iudica & Bonaccorso represented by typical vegetation dominated
1997, Giannini 1999, Sánchez et al. 2012a, b), by tall trees such as Cedrela lilloi (cedar),
whereas data on the arthropodophagous bat Enterolobium contortisiliquum (earpod tree),
diet were scarce and anecdotal (Bracamonte and Cinnamomum porphyrium (laurel). There
& Lutz 2013, N. Regueiro, unpublished data); are also smaller trees that do not exceed 20 m
because these bats are difficult to capture on as Allophyllus edulis (chalchal), Celtis boliviensis
mist nets because they avoid them (Carrol et (tala), among others. Bushes as Urera baccifera,
al. 2002). However, in the last two years, new Piper tucumanum and Solanum sp. are present,
studies about arthropodopagous feeding as well as herbs which range from smaller forms
habits were conducted. Additionaly, these to taller than two meters (Cabrera 1976); epiphytes
were the first studies which analyzed the bat are abundant, and lichens, ferns, bromeliads,
diet in relation to habitat alteration, sex, and and mosses are dominant (Brown et al. 2001).
season on molossids and vespertilionids bats The climate in the area is warm and humid; the
in Argentina (Gamboa Alurralde & Díaz 2018, annual precipitation varies between 900 and
2019). In the present study, we describe the 1000 mm, with a wet season from October to
diet of 12 species of the families Molossidae March and the rainfalls are concentrated mainly
and Vespertilionidae from the Yungas Forests in summer (Burkart et al. 1999).
in the Northwestern Argentina, and evaluate
differences in diet between well-preserved Sampling
and disturbed sites, sexes, and seasons. In The specimens were collected in eight different
Argentina, there is no previous information for localities (Figure 1), four well-preserved and
the diet of the bat species here analyzed. An four disturbed sites of the Yungas Forests (see
important aspect of the study of the trophic Appendix I), during 10 field surveys of three

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

Figure 1. Collection
localities in the Yungas
Forests ecoregion (gray
region), Northwestern
Argentina. These
included four well-
preserved sites (white
dots) and four disturbed
sites (white squares).
Localities: 1. Las Capillas
(Jujuy); 2. Finca Las
Capillas (Jujuy); 3. Río
Las Conchas (Salta);
4. Metán (Salta); 5.
Reserva Aguas Chiquitas
(Tucumán); 6. El Cadillal
(Tucumán); 7. Villa de
Batiruana (Tucumán);
8. Villa de Escaba
(Catamarca). For details
see Appendix I.

nights each, between September 2012 and of six hours. External measurements, age, sex,
October 2015. The sites were selected from and reproductive condition were recorded from
pairs at different latitudes, and the separation all captured specimens following Díaz et al.
distance between each pair ranged from three (1998). To collect the fecal samples, each bat was
to 18 km. In well-preserved sites, the vegetation placed in a separate, clean, cotton cloth bag for
was typical of the montane forest district, where at least three hours (Lee & McCracken 2005). The
all vegetation strata were recorded; whereas in collection of specimens was authorized through
disturbed sites the structure of the vegetation permits (No. 213-13) issued by the Dirección
was modified and some strata were missing, de Flora, Fauna y Suelos, Tucuman Province.
usually bushes and small trees. In the study All animals were handled consistent with the
sites, deforestation for cattle raising and animal care and use guidelines of the American
selective cutting are the main causes of habitat Society of Mammalogists (Sikes et al. 2016).
alteration. Additionally, we used ArcGIS 10.1
(ESRI 2011) to calculate the proportion of native Dietary analysis
forest in the landscape as a measure of forest From each specimen, up to 10 of the largest,
loss (Rodríguez-San Pedro & Simonetti 2015). intact, fecal pellets were examined; according to
Forest amount ranged from 98 to 100% in well- Whitaker et al. (1996) five pellets are sufficient
preserved sites and from 79 to 88% in disturbed to give reliable estimate of the diet of one
sites. The source of data used in the GIS individual. Each pellet, considered a sample,
analysis was the Instituto Geográfico Nacional of was soaked and softened in a Petri dish with
Argentina. The bats were captured using six 12-m 70% ethyl alcohol and then examined with a
mist nets, set after sunset inside the forest and dissecting microscope (Lee & McCracken 2005).
over streams or rivers, and kept open for periods Arthropod remains were sorted and identified

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

to the lowest possible taxonomic level (usually arthropod taxa as the response variable, and
family) following Whitaker (1988), Shiel et the disturbance level of capture site (well-
al. (1997), and Whitaker et al. (2009). Average preserved/disturbed), sex of bats (male/
percentage volume and percent frequency of female), and season (wet/dry) as explanatory
occurrence of each food item were estimated variables. For each run we used the Bray-
(Whitaker et al. 2009). The percent volume is the Curtis similarity index for 10,000 permutations.
average percentage by volume of each food type The analyses were conducted using the free
in the total sample of an individual and provides software PAST 3.11 (Hammer et al. 2001). When
an index of the proportional contribution of significant differences were observed in diet
arthropod taxa to the diet of bats sampled. of the species, we performed General Linear
The percent frequency of occurrence is the Models (Crawley 2007) to determine which
percentage of bats eating each food type and arthropod taxa contribute to the differences
provides a standardized measure of the most among the variables. To ensure that bat diet
common food type in the diet of bat species was not spatially autocorrelated across the sites,
(McAney et al. 1991, Lee & McCracken 2005). we used Moran’s I test for species captured in
more than two sites. According to this test, bat
Statistical analysis diet was not significantly autocorrelated for any
The Levins’ measure of niche breadth, B = 1/Σpi2 of the species (Moran’s I from -0.64 to -0.002, p >
, and its standardized version Ba = B-1/B-n, were 0.05). These analyses were conducted using the
also estimated to assess dietary heterogeneity free software R (R Core Team 2013).
(Krebs 1999, Lee & McCracken 2005), where pi
is the proportion of individuals consuming a
particular prey item i and n is the number of RESULTS
possible resource states. B is maximal when the We analyzed 475 samples from 81 specimens,
species does not discriminate among resources belonging to 12 species of arthropodophagous
and has the broadest possible niche. Levins’ bats in the Yungas Forests from Northwestern
B is minimal when all the individuals occur in Argentina. Their diet contained arthropods from
only one resource state, showing maximum eight orders, four suborders, seven families,
specialization. The range of B is from 1 to n, and one undetermined taxon (see Tables I and
whereas Ba is expressed on a scale from 0 to 1 II). Regarding molossids bats, we registered
(Krebs 1999). 21 individuals from four species: Eumops
The differences in the diet were evaluated bonariensis, Eumops glaucinus, Molossus
separately for each bat species. The species molossus, and Promops nasutus (Table I).
with less than three captured individuals Among them, E. bonariensis (Figure 2) showed
were excluded of these analysis. For each of a higher number of consumed prey orders,
the other species, differences between sites, being Coleoptera which contributed the highest
sexes, and seasons, were separately evaluated. volume proportion in its diet, with a total fecal
To test for significant differences in diet volume of 49%. This order was also the most
composition, we performed for each factor a commonly consumed, observed in 100% of total
Nonparametric Multivariate Analysis of Variance analyzed individuals (Table I). The other species
(NPMANOVA — Anderson 2001). We determined of Eumops, E. glaucinus showed a diet dominated
the average volume of consumed prey for each

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

Table I. Orders, suborders and/or families of arthropods found in the diet of species of Molossidae from
Northwestern Argentina. In brackets is indicated the number of individuals analyzed for each species. Average
percent volume and frequency of occurrence of each item are indicated, as well as the Levins’ measure of niche
breadth and its standardized version.

Eumops Eumops Molossus Promops nasutus

   
bonariensis (7) glaucinus (9) molossus (4) (1)
Freq Freq Freq Freq
Order SubO/Family Vol (%) Vol (%) Vol (%) Vol (%)
(%) (%) (%) (%)

Araneae Undetermined - - - - - - - -

Coleoptera Carabidae 47.14 85.71 - - - - - -

  Chrysomelidae - - 5.56 11.11 0.75 25 - -

  Curculionidae - - - - - - - -

  Scarabeidae 2.15 42.86 11.44 44.44 20.37 100 - -

  Undetermined - - 0.25 11.11 - - - -

Total
  49.29 100 17.25 55.55 21.12 100 - -
Coleoptera

Diptera Brachycera - - - - - - - -

  Nematocera - - 0.17 11.11 - - - -

  Culicidae 0.28 14.29 - - - - - -

  Total Diptera 0.28 14.29 0.17 11.11 - - - -

Hemiptera Undetermined 16.71 85.71 2.61 44.44 20.5 50 - -

Homoptera Cicadomorpha - - - - - - - -

  Fulgoromorpha 1.29 28.57 - - - - - -

  Delphacidae - - 0.11 11.11 - - - -

Total
  1.29 28.57 0.11 11.11 - - - -
Homoptera

Hymenoptera Formicidae - - - - 58.13 100 - -

Lepidoptera Undetermined 30.29 85.71 79.86 100 - - 100 100

Neuroptera Crisopidae 2.14 14.29 - - - - - -

Undetermined Undetermined - - - - 0.25 25 - -

Levins’ Index B 2.75 1.5 2.35 1

Std Levins’
Ba 0.219 0.062 0.169 0
Index

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

by Lepidoptera. These insects represented 80% all of the analyzed individuals. Regarding the
of the total volume and they were registered restant species, in all of them we observed a diet
in all of the evaluated individuals. Regarding dominated by Lepidoptera, which represented
M. molossus, Hymenoptera contributed to the 63-98% of the total volume and it was registered
highest volume proportion of its diet, with a total in 100% of individuals analized for each species
fecal volume of 58%; this order was registered (Table II). Except for Eptesicus diminutus, the
in 100% of the analyzed individuals (Table I). analyzed species of bats showed low values of
In one individual of M. molossus arthropods niche breadth (B = 1.04-2.66, Ba = 0.005-0.207; see
of the subclass Acari were observed, however Tables I and II), indicating a low diversity diet.
they were not taken in account for the analysis We evaluated the diet composition of 12
because its consumption was considered related species of bats according to three different
to grooming habit. Finally, we captured only one variables: site, sex, and season (see Appendix
individual of P. nasutus (Figure 2) and its diet II). We only observed differences in the diet of
only contained insects of the order Lepidoptera. Eptesicus diminutus and E. furinalis, between
With respect to vespertilionids bats, we seasons and sites, respectively. For E. diminutus,
analyzed 60 individuals from eight species (Table the registered variations were significantly
II). The species of Eptesicus, E. diminutus and E. different according to the NPMANOVA (p = 0.049),
furinalis (Figure 2), showed the highest number being Hymenoptera the order that was mostly
of consumed prey orders. In E. diminutus, contributing to the dissimilarities according
Hymenoptera contributed to the highest volume to the GLM (p < 0.0001). Hymenopterans were
proportion of its diet, with a total fecal volume mostly consumed by E. diminutus in dry season
of 23%. However, the most commonly consumed (Figure 3). Regarding E. furinalis, the registered
order by this species was Lepidoptera, registered variations by sites were significantly different
in 100% of the analyzed individuals (Table II). On according to the NPMANOVA (p = 0.006), being
the other hand, we observed in E. furinalis a diet Coleoptera (p = 0.002), Hemiptera (p = 0.023),
dominated by Coleoptera, which represented the and Homoptera (p = 0.018) the arthropod
58% of the total fecal volume. This was also the orders most contributing to the dissimilarities
most commonly consumed order, registered in according to the GLM. Coleoptera was mostly

Figure 2. Adult individuals of Eumops

bonariensis (a), Promops nasutus
(b), Eptesicus diminutus (c) and
Eptesicus furinalis (d) captured in
the study area. Photos by Santiago
Gamboa Alurralde.

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

Table II. Orders, suborders and/or families of arthropods found in the diet of species of Vespertilionidae from
Northwestern Argentina. In brackets is indicated the number of individuals analyzed for each species. Average
percent volume and frequency of occurrence of each item are indicated, as well as the Levins’ measure of niche
breadth and its standardized version.

Dasypterus ega Eptesicus Eptesicus Histiotus

   
(3) diminutus (7) furinalis (25) laephotis (1)

Vol Freq Vol Freq Vol Freq Vol Freq

Order SubO/Family
(%) (%) (%) (%) (%) (%) (%) (%)

Araneae Undetermined - - 1.43 28.57 0.04 4 - -

Coleoptera Carabidae 26.83 33.33 7.43 57.14 7.62 36 - -

Chrysomelidae - - 4.57 42.86 7.26 48 - -

Curculionidae - - - - 3.6 20 - -

Scarabeidae 7.17 66.67 6.57 28.57 36.95 68 4 100

Undetermined - - - - 2.16 8 - -

Total Coleoptera 34 66.67 18.57 71.43 57.63 100 4 100

Diptera Brachycera 1.83 66.67 0.29 14.29 0.24 8 - -

Nematocera - - 0.43 14.29 0.4 20 - -

Culicidae - - 3.71 14.29 - - - -

Total Diptera 1.83 66.67 4.43 28.57 0.64 24 - -

Hemiptera Undetermined - - 20 100 7.06 52 - -

Homoptera Cicadomorpha - - 1.43 28.57 1.64 36 - -

Fulgoromorpha - - 4.43 57.14 7.36 36 - -

Delphacidae - - 5 28.57 4.48 16 - -

Total Homoptera - - 10.86 57.14 13.48 44 - -

Hymenoptera Formicidae - - 22.57 57.14 7.85 36 - -

Lepidoptera Undetermined 62.83 100 20.43 100 12.14 52 96 100

Neuroptera Crisopidae 1.34 33.33 1.71 28.57 0.96 12 - -

Undetermined Undetermined - - - - 0.2 4 - -

Levins’ Index B 1.96 5.51 2.66 1.08

Std Levins’
Ba 0.12 0.564 0.207 0.01
Index

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

Table II. Continuation.

Histiotus Histiotus Lasiurus Lasiurus

   
macrotus (6) velatus (1) blossevillii (15) villosissimus (2)
Vol Freq Vol Freq Vol Freq Vol Freq
Order SubO/Family
(%) (%) (%) (%) (%) (%) (%) (%)
Araneae Undetermined - - - - - - - -

Coleoptera Carabidae - - - - - - - -

  Chrysomelidae 2.67 33.33 - - - - - -

  Curculionidae - - - - - - - -

  Scarabeidae - - 16 100 - - - -

  Undetermined - - - - - - - -

  Total Coleoptera 2.67 33.33 16 100 - - - -

Diptera Brachycera - - - - - - - -

  Nematocera 1.19 16.67 - - - - - -

  Culicidae - - - - - - - -

  Total Diptera 1.19 16.67 - - - - - -

Hemiptera Undetermined 0.95 16.67 - - - - 0.5 50

Homoptera Cicadomorpha - - - - - - - -

  Fulgoromorpha - - - - 0.2 6.67 7 50

  Delphacidae - - - - - - - -

  Total Homoptera - - - - 0.2 6.67 7 50

Hymenoptera Formicidae - - - - - - - -

Lepidoptera Undetermined 95.19 100 84 100 98 100 92.5 100

Neuroptera Crisopidae - - - - 1.8 40 - -

Undetermined Undetermined - - - - - - - -

Levins’ Index B 1.1 1.37 1.04 1.16

Std Levins’
Ba 0.012 0.046 0.005 0.02
Index

consumed by E. furinalis in disturbed sites,

DISCUSSION
whereas Hemiptera and Homoptera were mainly
consumed in well-preserved ones (Figure 4). For This study analyzed the diet of
this species, the observed variations between arthropodophagous bats from the families
sexes were not significantly different according Molossidae and Vespertilionidae in Argentina,
to the NPMANOVA (p = 0.736) adding important information in the southward
part of the distribution of these species. Except
for Eptesicus diminutus, we registered for all
species a low diversity diet. This was reflected

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

Figure 3. Percent volume and

Standard Error of each prey order
identified in the diet of Eptesicus
diminutus compared between sites
(a), and seasons (b). The arthropod
orders that showed significant
differences between treatments
are marked with *. Abbreviations
for arthropod orders: Ara, Araneae;
Col, Coleoptera; Dip, Diptera; Hem,
Hemiptera; Hom, Homoptera; Hym,
Hymenoptera; Lep, Lepidoptera; and
Neu, Neuroptera.

in the niche breadth, according to the values of 4.17, Ba = 0.40), which is known to have a great
both measures. The low diversity was a result, diverse diet (Gamboa Alurralde & Díaz 2018).
in general, of the elevated consumption of Regarding the molossids species here
moths by the different species. These results analyzed, little is known of its biology in
were similar to those obtained in another study Argentina (Barquez et al. 1999). The diet of
conducted on diet of four species of Myotis Eumops bonariensis was described by Bowles et
(Vespertilionidae) in the same study area (see al. (1990) in Mexico, however posterior studies
Gamboa Alurralde & Díaz 2019), where low values showed that the species studied by these authors
of both niche breadth measures were registered corresponds to E. delticus (Eger 2008). Thus, the
(B = 1.43-2.93, Ba = 0.05-0.24). Eptesicus diminutus information here reported for E. bonariensis
was the exception to this general pattern with (see Table I) represented unpublished data.
a diet that included eight orders and seven For E. glaucinus, several arthropod orders had
families of arthropods. These heterogeneity been registered in its diet (Belwood 1981, Best
was also reflected in the Levins’ measures of et al. 1997, Aguirre et al. 2003). In this study,
niche breadth. These values were higher than we registered similar results and added the
obtained for another arthropodophagous bat in order Homoptera to the diet of this species. A
the same study area, Tadarida brasiliensis (B = great number of arthropod orders had been

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

registered in the diet of Molossus molossus

(Willig et al. 1993, Ramírez-Chaves et al. 2008,
A. Rodales, unpublished data), and our results
were consistent with these studies. In addition,
we observed in this species many individuals
of the subclass Acari, but they were considered
as ingested during self-grooming (see Gamboa
Alurralde & Díaz 2019, L. Damián, unpublished
data). With regards to the diet of Promops
nasutus, no data were found in previous
researches, thus the results here obtained are
inedit for the species.
In vespertilionids species, a few arthropod
orders had been registered in the diet of
Dasypterus ega (Ross 1967, Kurta & Lehr
1995); here we added the orders Diptera and
Neuroptera. The biology, in general, and the diet
in particular are almost unknown for Eptesicus
diminutus (Barquez et al. 1999, Davis & Gardner
2008). Except for Coleoptera, all arthropod
orders registered in this study represented
inedit data for this species. For the other
species of Eptesicus analyzed, E. furinalis, several
arthropod orders had been registered in its diet
(Aguiar & Antonini 2008, Bracamonte 2013, A.
Rodales, unpublished data); we added here the
order Araneae. The consumption of spiders had
been already registered for arthropodophagous
bats (Aguirre et al. 2003, Kaupas & Barclay 2018,
Shively et al. 2018), including other species in
the same study area (Gamboa Alurralde &
Figure 4. Percent volume and Standard Error of each Díaz 2018, 2019). Shively et al. (2018) registered
prey order identified in the diet of Eptesicus furinalis
for Myotis lucifugus that the majority of the
compared between sites (a), sexes (b), and seasons
(c). The arthropod orders that showed significant spiders were orbweavers (Araneidae), which
differences between treatments are marked with *. supports the hypothesis that little brown bats
Abbreviations for arthropod orders: Ara, Araneae;
are likely gleaning spiders from webs. We could
Col, Coleoptera; Dip, Diptera; Hem, Hemiptera; Hom,
Homoptera; Hym, Hymenoptera; Lep, Lepidoptera; Neu, not identify in this study the kind of spiders
Neuroptera; and Und, Undetermined. consumed by the species of bats, therefore the
hypothesis of the extraction from the web is one
possibility. Another possibility is an accidental
ingestion during self-grooming on the roost (see
Gamboa Alurralde & Díaz 2019). We analyzed

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the diet of three species of Histiotus and two conserved sites, but further studies are needed
of Lasiurus with similar results in each genus. to confirm this.
The diet information obtained for both genera Coleopterans, lepidopterans, homopterans,
was similar to the reported in previous studies and hemipterans are among the major pests in
(Rolseth et al. 1994, Fenton et al. 1999, Zanon farms (Oliveira 2005), and we observed these
& dos Reis 2007, Valdez & Cryan 2009, Giménez orders in the diet of the 12 analyzed species. Thus,
2010, Bracamonte 2013, dos Reis et al. 2013). the obtained results would be consistent with
their role as natural pest controllers. However,
For H. laephotis and H. velatus the results are
the proportion of crop pest remains in the bats
preliminary because only one individual of each
diet is unclear due to the difficulty of identifying
species were captured.
highly masticated arthropod fragments in the
In contrast with our expectations, when feces to species. DNA metabarcoding analyses
we evaluated the diet composition of the 12 to document predation by arthropodophagous
species of arthropodophagous bats according species are necessary in order to confirm their
to three different variables, we only registered role as pest controllers in Argentina.
significant differences in the diet of both This study provides baseline research in
species of Eptesicus. The amount of forest Argentina and adds new information about the
cover was high even in the disturbed sites, this diet of some species of arthropodophagous
might be responsible for the lack of between- bats, as Eumops bonariensis and Promops
site differences observed. On the other hand, nasutus. However, is difficult to identify
the lower sample size of several species may masticated arthropod fragments in the feces
have influenced the obtained results. In E. to species, therefore for identifyng the lowest
taxonomic levels of arthropods we recommend
diminutus, we found significant differences
DNA metabarcoding analyses. But the study
in the diet between seasons, with a higher
of bat diet is still incipient, actually we added
consumption of Hymenoptera (Formicidae) in
new arthropod orders for several of the other
the dry season. It is important to mention that species here analyzed. This study includes the
in Northwestern Argentina, many ant species evaluation of the effects of different variables
conduct their nuptial flights at night and on the diet of molossid and vespertilionid
during the dry season (Kusnezov 1962). Similar bats in Argentina. Moreover, we registered
results were obteined for Tadarida brasiliensis differences in the diet of two species between
in the same study area (Gamboa Alurralde & well-preserved and disturbed sites and between
Díaz 2018). Regarding E. furinalis, we found wet and dry seasons, showing that bats can
significant differences in the diet between sites modify their diet according to habitat quality
with a higher consumption of Coleoptera in and season of the year. In contrast, for the rest
disturbed sites, whereas in conserved ones it of the analyzed species we found no differences
showed a higher consumption of Hemiptera and on bat diet in response to these variables. The
high abundance of arthropods in the study area,
Homoptera. The former results were consistent
independently of the site or season, could be
with the great abundance of coleopterans in
the reason of these results. Further studies of
highly fragmented habitats (Bustamante et
bat diet that include more analyzed individuals
al. 2006, de la Vega & Grez 2008), whereas the of bats and also the arthropod composition and
latter results coul be an indication of a higher abundance of the study sites are necessary to
abundance of hemipterans and homopterans in test this hypothesis.

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

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their norhtern range limit: a multimethod approach. Can
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AMERICAN SOCIETY OF MAMMALOGISTS. 2016. 2016 Guidelines
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of the American Society of Mammalogists for the use of blossevillii (1), Lasiurus villosissimus (1).
wild mammals in research and education. J Mammal 97: 2 - Finca Las Capillas, 3 km al E del cruce
663-688. entre río Las Capillas y ruta provincial n° 20
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Argentina. Mastozool Neotrop 24: 257-261. 65°09’07.86’’ W, 1141 m. Eptesicus furinalis (2),
Lasiurus blossevillii (3), Lasiurus villosissimus
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Lasiurus blossevillii (4).
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for the study of bats, Washington, D. C.: Smithsonian 25°29’34.76’’ S, 65°00’29.95’’ W, 1019 m. No
Institution Press, USA, p. 171-189. individuals of these species were captured here.
WHITAKER JO JR, MCCRACKEN GF & SIEMERS BM. 2009. Food 5 - Reserva Provincial Aguas Chiquitas,
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Parsons S (Eds) Ecological and behavioral methods
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for the study of bats, Baltimore: The Johns Hopkins 26°36’32.40’’ S, 65°10’36.60’’ W, 605 m. Eumops
University Press, p. 567-592. bonariensis (7), Dasypterus ega (1), Eptesicus
WHITAKER JO JR, NEEFUS C & KUNZ TH. 1996. Dietary variation diminutus (1), Eptesicus furinalis (9), Lasiurus
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mexicana). J Mammal 77: 716-724.
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WILLIG MR, CAMILO GR & NOBLE SJ. 1993. Dietary overlap in
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habitats of Brazil. J Mammal 74: 117-128.

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SANTIAGO GAMBOA ALURRALDE & MÓNICA DÍAZ DIET OF ARTHROPODOPHAGOUS BATS FROM ARGENTINA

APPENDIX II
Total samples evaluated for each species of bats and for each statistical analysis considering site characteristics,
sexes, and seasons.

Site Sex Season

Species Total Well-preserved Disturbed Male Female Wet Dry

Molossidae

Eumops bonariensis 33 33 - 8 25 28 5

Eumops glaucinus 79 79 - 19 60 - 79

Molossus molossus 40 40 - - 40 - 40

Vespertilionidae

Dasypterus ega 25 15 10 5 20 15 10

Eptesicus diminutus 30 5 25 - 30 24 6

Eptesicus furinalis 121 75 46 32 89 84 37

Histiotus macrotus 48 48 - - 48 - 48

Lasiurus blossevillii 72 49 23 55 17 34 38

Promops nasutus (1), Eptesicus diminutus (6), MÓNICA DÍAZ1,2,3

https://orcid.org/0000-0001-9519-6461
Eptesicus furinalis (7), Lasiurus blossevillii (1).
7 - Villa de Batiruana (La Cocha, Tucumán).
1
Programa de Investigaciones de Biodiversidad
Argentina (PIDBA), Programa de Conservación de los
27°38’11.61’’ S, 65°44’40.29’’ W, 515 m. Dasypterus
Murciélagos de Argentina (PCMA), Facultad de Ciencias
ega (1), Eptesicus furinalis (1), Lasiurus blossevillii Naturales e IML, Universidad Nacional de Tucumán.
(1). Miguel Lillo 205, 4000 Tucumán, Argentina
8 - Villa de Escaba, 22 km al SE, sobre ruta 2
Consejo Nacional de Investigaciones Científicas y Técnicas
provincial n° 9 (Paclín, Catamarca). 27°47’48.48’’ (CONICET), Crisóstomo Álvarez 722, 4000 Tucumán, Argentina

S, 65°46’56.70’’ W, 538 m. Eptesicus furinalis (3),

3
Fundación Miguel Lillo, Miguel Lillo, 251, 4000 Tucumán,
Argentina
Histiotus laephotis (1), Histiotus macrotus (6),
Lasiurus blossevillii (3).
Correspondence to: Santiago G. Alurralde
E-mail: [email protected]
How to cite
GAMBOA ALURRALDE S & DÍAZ M. 2021. Diet of arthropodophagous bats
(Mammalia, Chiroptera) from Northwestern Argentina. An Acad Bras Author contributions
Cienc 93: e20190549. DOI 10.1590/0001-3765202120190549. SGA and MMD collected the specimens in the field and wrote
the text; SGA analyzed the samples and drew the map.
Manuscript received on May 10, 2019
accepted for publication on September 10, 2019

SANTIAGO GAMBOA ALURRALDE1,2

https://orcid.org/0000-0002-6824-8665

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