379

Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(2): 379-390, April-june 2021 (Published 11 Feb. 2021)

Bat (Mammalia: Chiroptera) biodiversity in a subtropical

inselberg ecosystem of Northeastern Argentina

María A. Argoitia

Rodrigo Cajade

Alejandra B. Hernando

Pablo Teta

1. Laboratorio de Investigación en Diversidad, Ecología y Conservación de Vertebrados, Facultad de Ciencias Exactas

y Naturales y Agrimensura, Universidad Nacional del Nordeste, Av. Libertad 5470 (3400), Corrientes, Argentina;

anto.a_25@hotmail.com, rodrigocajade@hotmail.com, alejahernando@gmail.com; *Correspondence.

2. División Mastozoología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Consejo Nacional

de Investigaciones Científicas y Técnicas, Ángel Gallardo 470, C1405DJR Ciudad Autónoma de Buenos Aires,

Argentina; antheca@yahoo.com.ar

Received 07-VII-2020. Corrected 27-XI-2020. Accepted 13-I-2021.

ABSTRACT

Introduction: Rocky outcrops influence both micro and macro habitat for plants and animals by increasing

the availability and predictability of food, providing shelter, and unique microclimatic conditions. Objective:

We describe the bat assemblage in three isolated rocky outcrops and their surrounding pediments, adding new

data about trophic guilds and roosts. Methods: We surveyed the bat fauna of Paraje Tres Cerros, Corrientes

Province, Argentina, exploring 13 sites during 26 field trips, using mist nets and search of roosts. We made an

accumulation species curve and calculate inventory completeness. The similarity and composition of different

habitats was compared by a Non-Metric Multidimensional Scaling (NMDS) and an ANOSIM test. Results:

We reported 13 species, with a completeness inventory of the 80 % (Jacknife1), corresponding to the families

Vespertilionidae, Molossidae and Phyllostomidae. The insectivorous bats were the best represented guild. We

found nine types of roost for eight species in different sites. The analysis expressed low differences in the species

composition between both types of habitats in the area. Conclusions: The rocky outcrops and their pediments

are important ecosystems for the conservation and diversity of the bats in the region, since their assemblages

are regionally unique.

Key words: assemblages; roosts; trophic guilds; rocky microhabitat.

Inselbergs are defined as isolated rocky

outcrops forming small and discrete ecosys-

tems scattered worldwide. Besides its cul-

tural and economic importance, this kind of

habitat is characterized by their singular biotas

(Porembski & Barthloltt, 2012; Fitzsimons

& Michael, 2017). Overall, the importance

of these ecosystems for the conservation of

biodiversity has been attributed to their unique

microclimatic conditions regarding to their sur-

rounding areas, higher habitat heterogeneity,

and relative isolation, which locally increase

the diversity of unaltered land cover (Poremb-

ski & Barthlott, 2012; Burke, 2003; Speziale &

Argoitia, M.A., Cajade, R., Hernando, A.B., & Teta, P. (2021). Bat

(Mammalia: Chiroptera) biodiversity in a subtropical inselberg

ecosystem of Northeastern Argentina. Revista de Biología

Tropical, 69(2), 379-390. DOI 10.15517/rbt.v69i2.42815

DOI 10.15517/rbt.v69i2.42815

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Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(2): 379-390, April-june 2021 (Published 11 Feb. 2021)

Ezcurra, 2015; Fitzsimons & Michael, 2017).

In the case of bats, inselbergs increase avail-

ability and predictability of food (especially

insects) and provide variety of roosts, being

important sites for their conservation (Fred-

ericksen, Fredericksen, Flores, Mcdonald, &

Rumiz, 2003).

Bat diversity in Argentina comprises 67

species (Barquez, Díaz, Montani, & Pérez,

2020), with most species (~49) being distrib-

uted in the Northern portions of the country

(Barquez, Díaz, & Ojeda, 2006). Accordingly,

most of the available knowledge about these

mammals is restricted to the forested areas of

Northern Argentina, including the Yungas and

the Paranense forests (Sánchez, 2016). How-

ever, more in general, our regional knowledge

about bats is mostly historical and based on

punctual records, with few studies focusing

on entire assemblages (Sandoval, Sánchez, &

Barquez, 2010; Barquez, Sánchez, & Sandoval,

2011; Sánchez, Carrizo, Giannini, & Barquez,

2012a; Sánchez, Giannini, & Barquez, 2012b;

Idoeta, 2018).

The Paraje Tres Cerros (PTC), Corrientes

Province, Argentina, is characterized by the

presence of isolated rocky outcrops surrounded

by a plain matrix of grasslands and wetlands.

Several studies have pointed out their impor-

tance for the biodiversity conservation, high-

lighting the presence of species with different

biogeographic affinities and some endemisms

(Meregalli, 1998; Ravenna, 2003; Ravenna,

2009; Cajade et al., 2013a; Cajade, Etchepare,

Falcione, Barrasso, & Álvarez, 2013b; Ger-

vazoni, 2017; Fandiño, Fernandez, Thoman,

Cajade, & Hernando, 2017; Ojanguren-Afilas-

tro et al., 2017; Nadal, Achitte-Schmutzler,

Zanone, Gonzalez, & Avalos, 2018). Previ-

ous contributions to the knowledge of the

bat fauna of PTC include the first record of

Eumops bonariensis for Corrientes Province

and the mention of an unidentified species of

Myotis that roosts under rocks (Idoeta, Cajade,

Piñeiro, Acosta, & Pautasso, 2015; Cajade et

al., 2013a). Based on these and other unpub-

lished studies (Argoitia, 2016), this area was

recognized as an AICOM (Spanish acronym for

“Important area for the conservation of bats”)

in March of 2016 (RELCOM, 2020).

In this study, we report and summarize

new natural history data of the bat fauna of

PTC. We discuss the importance of inselbergs

and the surrounding matrix for conservation of

tropical bat diversity at a regional level. In this

way, we studied the richness of bats associ-

ated to different habitats (rocky outcrops vs.

pediments) in relation to their trophic guilds

and roosts. Finally, we highlight the need to

conduct additional ecological studies on these

poorly known habitats, with special focus on

their conservation.

MATERIALS AND METHODS

Study area: The studied inselbergs are in

PTC, San Martín Department, Corrientes Prov-

ince, Central-Eastern Argentinian Mesopota-

mia. Mean annual temperatures are between

21.5 and 19.5 °C, varying from 16-13 °C in

the coldest month (July) and 27-26 °C during

the warmest (January). Accumulated annual

precipitations varies between 1 500 and 1 000

mm (Carnevali, 1994). The relief in this area

consists of three small hills of quartz sandstone

of dune geo-morphology and trunked summits,

oriented SE-NW along 10 km of extension

(Herbst & Santa Cruz, 1999). Individual hills

are locally known as “Cerro Nazareno” (179

m.a.s.l., 83 ha, 29º06’78” S & 56º55’19” W),

“Cerro Chico” (148 m.a.s.l., 34 ha, 29º06’89”

S & 56º55’87” W) and “Cerro Capará” (158

m.a.s.l., 79 ha, 29º09’55” S & 56º51’43” W)

(Fig. 1). A geological interface of pediments of

low slope is placed between the rocky outcrops

and the flat matrix with a typical vegetation of

the “Campos y Malezales” ecoregion (Burkart,

Bárbaro, Sánchez, & Gómez, 1999). The rocky

outcrops are characterized by hydrophilic for-

ests at the Southern flanks and grasslands on

the summits and the Northern sides, and they

lack waterbodies. The pediments contain some

small artificial ponds, and are principally cov-

ered by grasslands, with some small patches

of hydrophilic forest (Parodi, 1943; Cajade et

al., 2013a).

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Bat sampling: We did field trips in 2012

(one time in August and September and two

times in November), 2013 (two times in Febru-

ary and one time in April), 2014 (two times in

February, and one in March and July), 2015

(February to May, September and October),

2016 (February to May, July and September to

December) at 13 sites distributed in two types

of habitats: (i) the rocky outcrops (including

three sites in grasslands and three in forest

patches), and (ii) the pediment (including five

forest patches and two cutwaters) (Fig. 1). Each

site was explored twice (26 in total), during

two consecutive nights, using five mist nets

(four of 6 x 3 m and one of 12 x 3 m, with

a size mesh of 12 x 12 mm), placed 40-50 m

apart from each other. The total sampling effort

was of 52 nights with 130 nets for the entire

area and 104 hours of roosts search. Only days

with occurrence of bats (= 30) were considered

for the analyzes. Nets were activated in time

bands between 18:00 and 01:00 h depending

on seasons and revised for ~5 hours at intervals

of 20 minutes. The placement of nets was car-

ried out during the daylight hours, considering

potential flight paths (e.g., edges and clear-

ings of forests, rocky cliffs) or food resources

(e.g., near to plants known to be consumed

by bats; Kunz & Parsons, 2009). Surveys

were conducted in each site during the night,

except when there was a full moon (due to the

lunar phobia of bats), rains or strong winds, to

avoid biases in the capture of bats (Morrison,

1978). Captured bats were photographed and

taxonomically identified in situ using specific

keys (Barquez, Mares, & Braun 1999; Díaz,

Solari, Aguirre, Aguiar, & Barquez 2016). Each

captured specimen was placed in a cloth bag,

then we took the following data: sex, relative

age, reproductive condition, total length, tail

length, hind foot length, ear length and forearm

length (Díaz, Flores, & Barquez, 1998), and

then they were released. All measurements

were taken with a digital caliper to the nearest

0.5 mm. Animals were trapped, manipulated,

and a sample was euthanized to confirm spe-

cies identification, following the guidelines

of the American Society of Mammalogists

(Sikes, Gannon, & The Animal Care and Use

Committee of the American Society of Mam-

malogists, 2011). Voucher specimens were

deposited at the Museo Argentino de Ciencias

Naturales “Bernardino Rivadavia” (MACN,

Buenos Aires, Argentina), and the Colección

Fig. 1. A. Location of the isolated rocky outcrops of Paraje Tres Cerros (black star), Corrientes Province, Argentina. B and

C: general satelital imagens of the hilly system, depicting the Cerros Nazareno (Nz) and Chico (Ch) in B and Capará (Cp)

in C. References for symbols: ■ Rocky grasslands, ● Rocky forest patches, ▲ Pediment forest patches and ♦ Cutwaters.

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de Mastozoología de la Facultad de Ciencias

Exactas, Naturales y Agrimensura de la Uni-

versidad Nacional del Nordeste (CM-FaCENA,

Corrientes, Argentina) (Digital Appendix 1).

Species richness: We inventoried and

described the bat species richness (S) of PTC,

including both the rocky outcrops and their

pediments. A species accumulation curve was

made to evaluate the representativeness of the

inventory. The sampling effort was considered

as the total number of days with occurrence

data for pediments and rocky environments.

We built a matrix of presence/absence (Digital

Appendix 2), calculating the completeness of

the inventory through a non-parametric estima-

tor (Jacknife 1; first-order Jackknife richness)

for incidence data. This estimator uses the num-

ber of species occurring in once sample, and is

efficient with low sampling efforts (Moreno,

2001). Samples were randomized 1 000 times

to eliminate the influence of the order in which

the data was taken (Colwell & Coddington,

1994). The degree of completeness of the

inventory was obtained as the percentage of

species observed in relation to the number of

species predicted by the richness estimator.

Bat assemblages were characterized using the

relative frequency (F), as the occurrence of

each species in the area regarding to the total

number of captures expressed as percentage.

The similarity in the composition of species

between two types of habitats (rocky outcrops

vs. pediments) was compared by a Non-Metric

Multidimensional Scaling (NMDS), using Jac-

card index as a measure of similarity, based

on incidence data matrix. The distortion of the

resolution of the two-dimensional arrangement

is represented by a stress value. The difference

between the richness values for the studied

habitats was tested with an ANOSIM test. In all

analyses, the significance level was of α = 0.05.

All analyses were made using the R Version

3.6.2, packages: BiodivesityR, ggplot2, vegan

(R Development Core Team, 2019).

Bat ecology: Trophic guilds were assigned

following the criterion proposed by Sánchez

et al., (2012a) and Sánchez (2016), based on

the species diet, foraging habitat and type of

flight of each taxon. The conservation status

of each species was taken from the assessment

of extinction risk of Mammals from Argentina

(SAyDS-SAREM, 2019). Roost searches were

carried out randomly at each site during the

day, lasting two hours before to the place-

ment of nets. We reviewed all those possible

places in which bats usually rest, such as trees,

crevices between or under rocks, and human

constructions. Roosts in trees were identified

and classified according to the keys proposed

by Andrews (2013). Individuals in each roost

were taxonomically identified and counted

whenever possible. In the case of Myotis sp.,

given the large number of found specimens, we

also recorded the seasonal patterns of the use

of the refuges between or under rocks through

walks in each rocky outcrops of two hours on

each field trip (N = 8), from August 2013 to

August 2014. We marked each checked rock

with paper tape to avoid recounting.

RESULTS

Species richness: Thirteen species were

recorded, including three families (Molossi-

dae, Phyllostomidae, and Vespertilionidae) and

seven genera (Eptesicus, Eumops, Lasiurus,

Molossops, Molossus, Myotis, and Sturnira).

The relative frequency (F) for most species in

the area varied between 2.3 to 14.8 % (N = 10);

the highest F corresponded to Eptesicus furi-

nalis, while Lasiurus blossevillii and Molossus

rufus were recorded only once (Table 1). All

specimens were determined to species level,

except for a sample of individuals of a distinc-

tive morphotype of Myotis that were identified

to the genus level, which is currently under

study. According to the estimator Jacknife 1,

inventory completeness reached high levels of

80 % (Obs = 13/Exp =17, with a 1.4 of standard

deviation). An accumulation curve of softened

species for our entire dataset (i.e., clustering

all sites) seemed to asymptote, indicating that

a large percentage of the regional bat richness

was sampled (Fig. 2).

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Regarding the composition of bat assem-

blages based in two NMDS axes, the arrange-

ment of species in the bi-dimensional space

shows a difference in relation to compared

habitats (pediments vs. rocky outcrops). Low

values of stress (0.5) and R

(0.9) show a high

adjustment to the explained proportion of the

variation (Fig. 3). The ANOSIM analysis did

not express significant differences between the

composition of both habitats (R = 0.2; P = 0.06).

Fig. 2. Bat species accumulation curve for Paraje Tres Cerros, Corrientes Province, Argentina. The gray area corresponds

to the standard deviation.

TABLE 1

Species and trophic guilds of the bats of the Paraje Tres Cerros, Corrientes province, Argentina

Code Taxa

Nazareno Chico Capará Pediment

F Trophic guild

RG RFP RG RFP RG RFP FP C

Phyllostomidae

Sli

Sturnira lilium

+ + + + 14.8 FHCGU

Vespertilionidae

Mal

Myotis albescens

+ + + + 5.7 IBCT

Msp

Myotis sp.

+ + + + + + 12.5 IBCA

Mri

Myotis riparius

+ + + + 13.6 IHCA

Mrb

Myotis ruber

+ + 4.5 IHCA

Leg

Lasiurus ega

+ 2.3 IBUnA

Lbl

Lasiurus blossevillii

+ 1.1 IBUnA

Efu

Eptesicus furinalis

+ + + + + 17 IHCA

Molossidae

Ebo

Eumops bonariensis

+ + 4.5 IBUnA

Epa

Eumops patagonicus

+ + + 5.7 IBUnA

Mte

Molossops temminckii

+ + 12.5 IBCA

Mmo

Molossus molossus

+ + 4.5 IBUnA

Mru

Molossus rufus

+ 1.1 IBUnA

Reference: RG, rocky grassland; RFP, rocky forest patches; FP, forest patches; C, cutwaters; FHCGU, highly cluttered

space/gleaning/understory frugivore; IBCT, background-cluttered space/trawling insectivore; IBCA, background-cluttered

space/aerial insectivore; IBUnA, uncluttered space/aerial insectivore; IHCA, highly cluttered space/aerial insectivore and F,

relative frequency. + = presence.

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Bat ecology: We registered five trophic

guilds represented differently in each environ-

ment. Insectivorous bats were represented by

one background-cluttered space/trawling species

(IBCT), two background-cluttered space/aerial

species (IBCA), three highly cluttered space/

aerial species (IHCA) and six uncluttered space/

aerial species (IBUnA), while the only frugivore

Fig. 3. Composition of the Non-Metric Dimensional Scaling (NMDS) species from the bat assemblage of the Paraje Tres

Cerros, Corrientes Province, Argentina. The plot represents two habitats, rocky outcrops, and pediment, in eight sites of the

study area. References are as follow: (1) gray light labels are the sites names; NzRFP, Nazareno rocky forest patches; ChRFP,

Chico rocky forest patches; CpRFP, Capará rocky forest patches; NzRG, Nazareno rocky grasslands; ChRG, Chico rocky

grasslands; CpRG, Capará rocky grasslands; PPF, Pediment forest patches (5); C, Cutwaters; (2) black labels correspond to

the species (see code on Table 1). Ellipses represent 70% confidence intervals of centroids for rocky outcrops and pediments.

Fig. 4. Guild structure assemblage for the bats from Paraje Tres Cerros, Corrientes Province, Argentina. Relative frequency

of each guild per site are depicted. Reference: IBCA, background-cluttered space/aerial insectivore; IBCT, background-

cluttered space/trawling insectivore; IBUnA, uncluttered space/aerial insectivore; IHCA, highly cluttered space/aerial

insectivore; FHCGU, highly cluttered space/gleaning/understory frugivore.

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was represented by a highly cluttered space/

gleaning/understory (FHCGU) species (Fig. 4).

We registered nine types of refuges, five

of them in trees trunks (3 in pediment and 2

in rocky outcrops), one on palm leaf (in pedi-

ment), two on rocks (in rocky outcrops) and

one in a human construction (rocky forest

patches) for eight species (Table 2).

Two types of roosts were alternatively

used by Myotis sp. in rocky microhabitats: (i)

within horizontal and vertical crevices between

larger rocks, and (ii) under rocks. In this case,

each rock provides refuge by presence of small

spaces formed between them and large rock

blocks (rock terraces) near to cliffs or towards

flanks of the rocky outcrops. In some cases (not

counted), Myotis sp. shared these roosts with

arachnids, blatids and lizards. We recorded 17

occurrences for 168 revised rocks and a total

of 49 individuals (6 in Cerro Nazareno, 24 in

Cerro Capará, and 16 in Cerro Chico). During

the cold seasons, the occurrence of individuals

between or under rocks was higher, with groups

varying between 3 to 18 specimens. Contrarily,

only solitary individuals were recorded during

the warm seasons (Fig. 5).

DISCUSSION

The Northern portion of Argentina consti-

tutes the Southernmost limit for several species

of tropical to subtropical distribution (Gardner,

2007). At least 37 species were documented

for the ecoregion of “Campos y Malezales,”

belonging to four families (Noctilionidae,

Phyllostomidae, Vespertilionidae and Molos-

sidae) (Idoeta, 2018). In this study, 13 species

were recorded, representing 35 % of regional

chiropterofauna. Other localities sampled in

this ecoregion have less than 7-6 species in

bat assemblages (59; Idoeta, 2018); only three

localities placed in an ecotonal area with the

Interior Atlantic Forests, Misiones Province,

reach a richness of 15 species. Overall, the

“Campos y Malezales” ecoregion is dominated

by phyllostomids bats -with Artibeus lituratus

and Sturnira lilium as most abundant species-,

followed by molossids and vespertilionids

(Idoeta, 2018), while in PTC molossids and

TABLE 2

Identified roosts for bats of Paraje Tres Cerros, Corrientes Province, Argentina

Roosts Taxa N Sites Observations

Tree trunks

Sturnira lilium

8 CpRFP Adults in knot-hole and tear-out of

Ocotea puberula

5 Adults in trunks of unidentified Myrtaceae

Tree trunks

Myotis riparius

6 PFP

Juveniles and adults between aerial roots

of Ficus luschnathiana

Tree trunks Molossops temminckii UN PFP In desiccation-fissures unidentified dead tree

Tree trunks

Molossus molossus

UN PFP Tear-out unidentified tree

Palm leaf

Lasiurus ega

4 PFP

Adults in Washingtonia sp.

Rock crevices

Myotis sp.

4 NzRG Northern slope vertical and horizontal ~150 m

of height

Molossops temminckii

1 ChRG Northern slope vertical ~130 m of height

Lasiurus blossevillii

Under rock

Myotis sp.

* NzRG, ChRG

and CpRG

Adults solitary and in group

Human

construction

Eumops patagonicus

Myotis sp.

~20

ChRFP Adults in a mix colony

References: NzRFP, Nazareno rocky forest patches; ChRFP, Chico rocky forest patches; CpRFP, Capará rocky forest

patches; NzRG, Nazareno rocky grasslands; ChRG, Chico rocky grasslands; CpRG, Capará rocky grasslands; PPF, Pediment

forest patches; C, Cutwaters. *See figure 5 for specific information.

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vespertilionids are better represented than phyl-

lostomids, being Eptesicus furinalis the most

frequent species. Further studies, including

the use of acoustic monitoring could increase

the number of recorded species, especially

for those taxa that avoid traditional samplings

(i.e., mist nets).

The PTC bat fauna includes species from

different trophic guilds, but with a dominance

of insectivorous species (i.e., Vespertilionidae

and Molossidae). This could be explained

by the microclimatic conditions of the rocky

outcrop ecosystems that favors the availabil-

ity of arthropods (Fredericksen et al., 2003).

According to Fredericksen et al. (2003), rocks

capture heat during day, releasing it gradu-

ally during the night, and attracting numerous

flying insects.

Therefore, both molossids and vesper-

tilionids bats roost preferably near or in rock

crevices (Kunz, 1982). Background-cluttered

species (i.e., Myotis riparius, Myotis ruber,

Eptesicus furinalis) were frequent in edge for-

est patches, while highly cluttered species (i.e.,

Myotis sp., Molossops temminckii) were most

commonly caught in closed vegetation. Finally,

uncluttered species (i.e., Lasiurus ega, Lasi-

urus blossevillii, Eumops bonariensis, Eumops

patagonicus, Molossus molossus, Molossus

rufus) were mostly found in open rocky grass-

lands. Myotis albescens, a background-clut-

tered space/trawling insectivorous, was mostly

captured in cutwater, but also in forest patches.

The only frugivore understory bat species,

Sturnira lilium, was caught in a wide variety of

sites within PTC.

The rocky outcrops of PTC provide a wide

array of refuges, both in rocky and pediment

environments for at least eight species (i.e.,

Eumops patagonicus, Lasiurus blossevillii,

Lasiurus ega, Molossops temminckii, Molossus

molossus, Myotis riparius, Myotis sp., Sturnira

lilium). Overall, the recording roost sites are

in accordance with the available data in the

literature (Barquez, et al., 2020). The use of

rock roosts (mostly by Myotis sp.), specially at

Cerro Capará, is perhaps related to the avail-

ability of more suitable rocks at this place

(i.e., quadrangular in outline and with rounded

edges, with a mean surface of 107.5 cm

and

the entrances orientated to sunset direction).

However, we do not rule out the possibility that

other factors may influence the use of rocks at

Cerro Capará, such as the absence of predators,

or the availability of food resources. Although

no specific studies of the microclimatic condi-

tions of these refuges have been carried out

so far, we think that the conglomeration of

Fig. 5. Use of the roosts under rocks by individuals of Myotis sp. in Paraje Tres Cerros, Corrientes Province, Argentina. A.

Solitary form and B. Group form.

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individuals of Myotis sp. in the colder seasons

would be a behavior to deal with low tempera-

tures, as was documented for other bat species

that inhabits in temperate to cold areas (Ran-

some, 1968; Raesly & Gates, 1987; Herreid,

1967; Lewis, 1996). This and other aspects of

the social behavior of this species should be

studied in depth to explain the observed pat-

terns in the use of roosts.

Both Lasiurus blossevilli and Lasiurus ega

were documented only by individuals found in

their roosts. This fact shows the importance of

adding this kind of sampling to produce com-

plete bat inventories.

The isolated condition of most inselbergs

has a fundamental role as an evolutionary force

over their biota, reflected in the presence of

endemisms, microhabitat specialized species,

or the evolution of singular social behav-

iors (Mares, 1997; Speziale & Ezcurra, 2012;

Cajade et al., 2013b; Fitzsimons & Michael,

2017). For example, Myotis sp. developed the

ability to take flight from the ground rocks

instead from a free fall, using sometimes a

quadruped locomotion to reach their shelters

(Cajade et al., 2013a). Similar behaviors were

developed by other rocky dwelling bats, such

as Molossops mattogrossensis, Myotis vivesi

and Platymops setiger (Blood & Clark, 1998;

Happold, 2013).

At a local and regional level, rocky out-

crops lead to an increase of mammal diversity

compared to the surrounding non-rocky habitat

(Mares, 1997). The richness of the assemblage

and their different ecological aspects observed,

seen among the bats of PTC is an indicator of

the importance of inselbergs for the regional

conservation of these mammals. Although the

NMDS shows differences in the composition

of the bat sets in both environments, the ANO-

SIM test indicates that these differences are not

significant; this highlights the importance of

both rocky outcrops and surrounding landscape

on the pediments for the bat assemblage in the

area. This situation is due that some species

are exclusively found in one of the environ-

ments, Lasiurus ega and Molossus rufus in

pediments and Lasiurus blossevillii in rocky

outcrops. Also, the importance of the forest

patches is that they offer shelter to the only spe-

cies considered as threatened within the area

(i.e., Myotis ruber, a little-known bat in this

region, categorized as Near Threatened (NT) in

Argentina) (Lutz, Díaz, Giménez, Sánchez, &

Sandoval, 2019).

Overall, our findings highlight the impor-

tance and need to continue protecting insel-

bergs ecosystems, avoiding those anthropic

activities of great impact (e.g., large-scale agri-

cultural activities, intensive tourism) (Kunz,

1982; Turner, 1996). The conservation of iso-

lated rocky outcrops will not only maintain

a high regional richness of bat species, but

also their functional importance for the main-

tenance of ecological processes (Kunz, de

Torrez, Bauer, Lobova, & Fleming, 2011). We

observe that both the rocky outcrops and the

surrounding matrix are important for the local

chiropterofauna, as both provide foraging areas

and roost sites.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank to Giordani, Couthinio, and

Pacheco families for their kind hospitality dur-

ing field works. Pedro Cuaranta, Luz Thomann,

Juan Manuel Fernandez, Azul Courtis and José

Miguel Piñeiro supplied technical and logisti-

cal assistance. “Fundación Amado Bonpland”

enable field work at the “Reserva Natural

Privada Paraje Tres Cerros”. We are grateful

to Universidad Nacional del Nordeste (UNNE)

and Consejo Nacional de Investigaciones

Científicas y Técnicas (CONICET) for finan-

cial support. Dirección de Recursos Naturales,

388

Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(2): 379-390, April-june 2021 (Published 11 Feb. 2021)

Ministerio de Turismo, Corrientes Province

authorized specimens collections.

RESUMEN

Biodiversidad de murciélagos (Mammalia: Chi-

roptera) en un ecosistema inselberg subtropical del

Noreste de Argentina. Introducción: Los afloramientos

rocosos influyen tanto en el micro como en el macro hábi-

tat de plantas y animales al incrementar la disponibilidad

de alimentos, proporcionar refugios y brindar condiciones

microclimáticas únicas. Objetivo: Describir el ensamble

de murciélagos en tres afloramientos rocosos aislados y

sus pendientes circundantes, incorporando nuevos datos

sobre gremios tróficos y refugios. Métodos: Muestreamos

la fauna de murciélagos del Paraje Tres Cerros, provincia

de Corrientes, Argentina, exploramos 13 sitios durante

26 viajes de campo, usando redes de niebla y búsqueda

de refugios. Realizamos una curva de acumulación de

especies y calculamos la completitud del inventario. La

similitud y composición de diferentes hábitats se com-

paró mediante un escalado multidimensional no métrico

(NMDS) y una prueba ANOSIM. Resultados: Reportamos

13 especies, con una completitud del 80 % del inventario

(Jacknife1), correspondientes a las familias Vespertilio-

nidae, Molossidae y Phyllostomidae. Los gremios mejor

representados fueron los insectívoros. Encontramos nueve

tipos de refugios para ocho especies en diferentes sitios.

Los análisis expresaron bajas diferencias en la composi-

ción de especies entre ambos tipos de hábitats en el área.

Conclusión: Los afloramientos rocosos y pendientes son

ecosistemas importantes para la conservación y diversidad

de los murciélagos en la región, ya que sus comunidades

son regionalmente únicas.

Palabras clave: ensambles; refugios; gremios tróficos;

microhabitat rocoso.

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