diversity
Article
Diversity and Conservation of Cave-Dwelling Bats
in the Brunca Region of Costa Rica
Stanimira Deleva * ID and Gloriana Chaverri ID
Recinto de Golfito, Universidad de Costa Rica, 4000 Alamedas, Golfito 60701, Costa Rica;
gchaverri@upacificosur.org
* Correspondence: stanimira.deleva@ucr.ac.cr; Tel.: +359-883-490-378




Received: 10 April 2018; Accepted: 30 May 2018; Published: 2 June 2018 

Abstract: The Brunca region in Costa Rica contains the largest number of caves in the country, yet the
diversity and distribution of bat species within those caves is currently unknown. Without this
information, it is not possible to assess changes in populations and assemblages that may indicate
severe damages to these critical roosting habitats, and to take evidence-based conservation actions.
We present the first study to describe the diversity of cave-dwelling bat species in the Brunca region of
Costa Rica in a large number of caves. We collected data of bat species diversity by direct observation
and capturing bats inside roosts. Bats were observed in 38 of the 44 surveyed caves, representing
20 species from 4 families, with colony sizes ranging from a few individuals to >7500. In addition,
we collected information about the human activities carried out in and around the roosts to assess
potential threats that these sites face. Data indicate that caves suffer mostly from unregulated tourist
visitation and that one of the most visited caves is also the one with the most species-rich bat
assemblages. Our study determined the most important and vulnerable bat roosts in the region and
shows the need for urgent conservation actions to protect them.
Keywords: bats; Brunca region; caves; conservation; Costa Rica; diversity
1. Introduction
Caves are broadly defined as natural openings in solid rock [1], and as such, they serve as the
“windows” in which we glance into the underground. Caves have been attracting people’s interest from
prehistoric times by serving as shelters, sacred places, or sources of artistic expression [2], but present
a significant challenge for scientific research because they are largely hidden from view and hardly
accessible for exploration. Most caves do not appear on topographic maps or satellite images and
are neglected by mainstream scientists, making cave research a priority for only a small number
of highly dedicated individuals [3]. Their unique features, the complete absence of light, almost
constant temperature, and high air humidity make caves a suitable habitat for a large variety of highly
specialized organisms such as cave crickets [1,4], and some vertebrates including the blind salamander
and angel fish [1,5]. These organisms are so well adapted to the specific conditions in caves that they
would not survive in a surface habitat.
Caves are dependent on energy sources brought by several organisms that forage at the surface
and which use caves as shelter, such as oilbirds, swiftlets, and bats [1,2,6]. Bats, in fact, are so tightly
associated with caves and are often so abundant that they can significantly modify these ecosystems
by altering their microclimatic conditions and providing significant amounts of guano, the essential
food source and base of the food chain in most caves [2,7]. In turn, caves provide bats a refuge from
predators and inclement weather, and a critical venue for social interactions [8–10]. Caves are so
important for bats worldwide that the majority of species, including many that are vulnerable and rare,
are either specialized cave-dwellers or use caves temporarily [11]. Also, the largest aggregations of
Diversity 2018, 10, 43; doi:10.3390/d10020043 www.mdpi.com/journal/diversity
Diversity 2018, 10, 43 2 of 15
bats are found in caves, with numbers reaching several millions of individuals [12–14], which makes
them critical roosts for species that form such large colonies.
Costa Rica is a bat diversity hotspot with 114 species, most of which are well represented in the
southwestern Brunca region [15,16]. The Brunca region has the largest karst region (185 km2) and the
largest number of caves (n = 156) in the country [17]. While many of the species that inhabit the region
are known to roost in caves in other parts of their range [15,18,19], there is still no baseline information
about the populations of cave-dwelling bats in this region. Cave-dwelling bats are extremely important
for the local ecosystems, playing the role of pollinators, seed-dispersers, and pest-suppressors [20].
Cave-related tourism activities are also becoming popular in the Brunca region [17], which makes
the caves potential sources of local income, but also endangers cave-dwelling bats, which are often
vulnerable to disturbance. Other threats that bats are facing include habitat loss and direct killing at
their roosts. To the best of our knowledge, there is no information on distribution and the ecology of
cave-dwelling bats in this region, nor information about which roosts contain large colonies or rare
species of bats that need to be considered a conservation priority [18], or even the types of threats these
roosts are facing. This study is the first to assess the diversity and distribution of cave-dwelling bats
species in a large number of the caves in the country. Our study provides valuable information about
underground roosts of conservation importance.
Monitoring cave roosts is a highly accurate method for estimating colony size, species composition,
and seasonal changes in the populations of cave-dwelling bats [21,22], and in the temperate zones, it
is a widely distributed activity with well-established traditions [23–25]. The regular monitoring of
bat roosts is of particular importance to assess population decline in vulnerable species and for the
identification of potential threats (e.g., disturbance or dangerous diseases) [26,27]. Roost monitoring is,
however, uncommon in Costa Rica, where most of the research on bat diversity and distribution is
conducted around research stations and with the method of mist-netting [28–30], and most recently
also with acoustic monitoring at feeding or commuting sites. Our efforts are aimed at establishing
roosts of national monitoring priority, which will help us assess population trends and serve as a base
for conservation activities in the future.
Cave-dwelling bats are facing threats worldwide such as habitat loss, pollution, disturbance,
quarrying and mining, guano extraction, and vandalism [31–33]. Bats that roost in caves are particularly
vulnerable to human activities due to their tendency to aggregate in large colonies in a single roost,
as a single disturbance event could lead to the eradication of an entire colony [10]. In the Neotropics,
cave-dwelling bats face additional threats due to direct killing, as local residents attempt to eradicate
species that are considered pests, specifically vampire bats (Desmodus rotundus) [34]. These bats are
chased by cattle farmers and killed inside the caves where they roost, leading to the decline of other
species as well [35]. The efforts against vampire bats threaten all of the cave-roosting bats, as people
aiming to kill vampire bats do not distinguish the different species and often destroy all bats in a single
roost [36]. It is crucial to obtain information about the distribution of cave-dwelling bats in Costa Rica,
so we can take conservation actions before important bat colonies are lost.
2. Materials and Methods
2.1. Study Region
We investigated caves and artificial tunnels in the Southwestern (Brunca) region of Costa Rica
(N 9.23643, W 82.84233) at sites ranging in altitude from 0 to 520 masl. The Brunca region contains the
largest karst area of the country, with 185 km2 of karst surface and 156 caves [17]. The region has an
average annual temperature of 26.2 ◦C and an average annual rainfall of 4398 mm [37]. The dominant
habitat of the region is evergreen moist lowland forest, including large areas of well-preserved
rainforests in the Corcovado and Amistad national parks [38]. For a better visual portrayal of the field
sites, we roughly divided them into 5 areas (Figure 1): area A—Ballena, area B—Boruca, area C—Osa,
area D—Rio Claro, and area E—Corredores. We do not provide the exact locations of the field sites to
Diversity 2018, 10, 43 3 of 15
Diversity 2018, 10, x FOR PEER REVIEW  3 of 17 
protect them from further disturbance; however, these data are available upon request from the digital
rreeppoossitiotorryy FigshaFreig(shtatpres ://figsh(harttep.cso:/m/fi/gpshroajreec.ctso/mD/pivreorjseicttys_/Danivde_rcsoitnys_earnvda_ticoonn_soefr_vcaativoen-_dowf_ecllaivneg-_
dbwatesl_liing__thbea_tsB_riun_ntchae__rBegruionnc_ao_fr_eCgiosnt_ao_Rf_iCcao/st3a4_4R1i5c)a./34415). 
 
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depending on the complexity of the roost and the presence of bats during our first visit (Appendix 
A, Table A1, column D). If we observed only a few (<30) bats and low species richness (1 or 2 species), 
we visited the roost only once. When a large number of individuals or indirect traces of presence 
 
Diversity 2018, 10, 43 4 of 15
Table A1, column D). If we observed only a few (<30) bats and low species richness (1 or 2 species),
we visited the roost only once. When a large number of individuals or indirect traces of presence
(e.g., guano, food remains) was observed during our first visit, we performed additional monitoring
and tried to obtain data in both the rainy and dry seasons if possible. Due to high water levels and
technical difficulties, some caves were inaccessible during the rainy season, so we visited them in the
intermediate period between seasons (December–January and May–June).
In addition to the field surveys, we interviewed local people about the activities conducted
in caves. We included questions about visitation, hunting, other uses of the caves, and awareness
about bat populations. We focused on farmers and landowners living near the locations of the caves.
We also used direct observations in and around roosts to assess additional anthropogenic activities.
For example, we recorded evidence of graffiti, waste, broken speleothems, footprints, entrance blocking
or traces of resource extraction inside the roosts. In proximity to the roosts (radius of 1 km), we recorded
the land use activities (agriculture, deforestation, quarrying). Depending on the dimension of the
activities, we evaluated them on a scale from 1 to 4, 1 being the highest and 4 the lowest disturbance.
2.3. Bat Surveys
We used flashlights and binoculars to search visually for roosting bats or indirect traces of their
presence (i.e., skulls, guano or food remains) [43]. Small clusters of bats (up to 50 individuals) were
counted directly at the cave. We photographed larger groups of bats using a digital DSLR camera
(D3200, Nikon, Tokyo, Japan) and used ImageJ software [44] to estimate the number of individuals.
We determined the species of observed bats using the available literature [15,16,45] as a reference.
To confirm species identification and obtain biometric data, we used a custom-made hand-held 2 m
mist net to capture a few individuals within the roost. We measured forearm length, sex, age, and
reproductive status of the captured bats [21]. In one vertical cave, we used a harp trap at the entrance
to capture bats during their evening emerge. After taking biometric data, we released all individuals
without further disturbance. No voucher specimens were collected during this study. We operated
under the research permit INV-ACOSA-018-16.
2.4. Assessing Conservation Priority
We evaluated the conservation priority of each cave using the Bat Cave Vulnerability Index (BCVI),
based on the bat species diversity and presence of human-induced threats in the caves [46]. The index
is a novel approach for conservation prioritization of bat caves and it was developed with a focus on
tropical regions. It contains two components: Biotic Potential Index (BP) and Biotic Vulnerability Index
(BV). The Biotic Potential Index includes several species diversity and rarity measurements, including
species richness, abundance, relative abundance, endemism, conservation status [47], and rarity index.
The BP index has a value between 1 and 4, with level 1 being the highest and 4 the lowest biotic
potential. The Biotic Vulnerability Index includes information on cave accessibility, morphology,
visitation, and land use in adjacent areas. The BV index has a value of A, B, C, and D, with A being
the highest vulnerability to disturbance and D no disturbance. We classified all roosts based on the
combined values of BP and BV. The roosts with indicated values of 1A and 1B were considered of
highest conservation priority. The roosts with values between 1C and 3D were considered as medium
conservation priority, and the roosts in category 4 of low priority.
3. Results
In the study period we visited 44 underground roosts, including 40 caves, 2 artificial tunnels, and
2 abandoned gold mines. From the researched caves, 30 were described for the first time during this
study and included in the National Cave Database, and named after geographical or morphological
features in their respective locations (Appendix A, Table A1). From all caves, 22 were horizontal and
22 were vertical (Appendix A, Figure A1). We observed bats in 38 of the 44 roosts. We identified
20 species of bats from the families Phyllostomidae, Emballonuridae, Natalidae and Mormoopidae
Diversity 2018, 10, 43 5 of 15
(Table 1, Figure 2). The most frequently observed species was Carollia perspicillata, which occurred in
25 roosts. Other common species were Peropteryx kappleri (found in 18 roosts) and Saccopteryx bilineata
(14 roosts). We observed relatively large (n > 100 ind.) colonies of bats (Anoura sp., Artibeus jamaicensis,
C. perspicillata, Desmodus rotundus, Natalus mexicanus, Pteronotus gymnonotus, Pteronotus parnellii, and
Pteronotus personatus) in 11 caves and very large (>500 ind.) (C. perspicillata, P. gymnonotus, P. parnellii,
and P. personatus) in 6 caves (Appendix A, Table A1). The largest colony of bats was observed in
the Campanario cave, estimated at around 7600 individuals, and included three species of the genus
Pteronotus (Appendix A, Table A1). Other large colonies are those found in the Laguna Perdida
(ca. 2000 individuals) and Corredores (ca. 1500 individuals) caves. The roost with the greater species
richness was Corredores, with 8 species, followed by Emus and Laguna Perdida with 7 species
(Appendix A, Table A1). Three caves were inhabited by mixed colonies of Pteronotus spp.: Tortuga,
Campanario, and Corredores; the first two are considered maternity colonies since we observed
hundreds of pups. Both Tortuga and Campanario are very similar littoral caves, which have a single
entrance, leading to a simple chamber, and are partially filled with sea water during high tides. In the
Campanario cave, we observed a third species of Pteronotus, P. personatus, which is so far the only
known location of the species during this study. A single bat species occurred in 14 caves, specifically
the greater dog-like bat (Peropteryx kappleri) and Seba’s short-tailed bat (C. perspicillata), observed in
6 roosts each.
Table 1. Observed species of bats and their respective locations.
Family Species Roosts
Anoura sp. Laguna Perdida, Piedras Blancas 2
Artibeus jamaicensis Arelis, Carma, Corredores, Gran Galería, Túnel ICE 2, San Pedrillo
Afrodiziaco Pozo, Alma, Árbol Caido, Bananal, Bombasa, Buena
Cueva, Caballo Muerto, Cinco Millones, Corredores, Dos Brazos,
Carollia perspicillata Emús, Final 7 Pozo, Gran Galería, Gran Madre, Túnel ICE 1,
Túnel ICE 2, San Josecito, Laguna Perdida, Los Sueños,
Miramar Pozo, San Pedrillo, Sapo Gordo Pozo, Titi Mono, Tortuga
Carollia sowelli Miramar
Phyllostomidae Chrotopterus auritus Corredores
Desmodus rotundus Alma, Bombasa, Buena Cueva, Cinco Millones, Emús, Gran Madre,Túnel ICE 2, San Josecito, Laguna Perdida, Los Sueños, Miramar
Glossophaga soricina Alma, Bombasa, Corredores, Dos Brazos
Lonchophylla concava San Josecito, Miramar Pozo, San Pedrillo
Lonchophylla robusta Bombasa, Laguna Perdida
Lonchorhina aurita Gran Madre, Miramar
Phyllostomus discolor Arelis
Phyllostomus hastatus Laguna Perdida
Trachops cirrhosus Bombasa, San Pedrillo
Alma, Arbol Caido, Arelis, Bamboo Pozo, Banano Quemado,
Peropteryx kappleri Caballo Muerto, Castillo Real, Cinco Millones, Cueva 1 No Name,Cueva Cerca Cor, Emús, Gran Galería, Gran Madre, La Troja,
Metros 12, Monteadores, Rectángulo, Serpiente Dormida
Emballonuridae Peropteryx macrotis Emús, Gran Galería
Alma, Arelis, Bamboo Pozo, Cinco Millones, Corredores, Emús,
Saccopteryx bilineata Gran Galería, Gran Madre, Túnel ICE 2, Laguna Perdida,
Los Sueños, Monteadores, Rectángulo, San Pedrillo
Natalidae Natalus mexicanus Corredores, Emus
Pteronotus gymnonotus Campanario, Corredores, Tortuga
Mormoopidae Pteronotus parnellii Bombasa, Campanario, Corredores, Emus, Túnel ICE 2,Laguna Perdida, Los Sueños, Tortuga
Pteronotus personatus Campanario
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Diversity 2018, 10, x FOR PEER REVIEW  6 of 17 
 
Figure 2. Some of the species, observed during our study: (A) Common vampire bat (D. rotundus), (B) 
Figure 2. Some of the species, observed during our study: (A) Common vampire bat (D. rotundus),
Big naked-backed bat (P. gymnonotus), (C) Parnell’s mustached bat (P. parnellii), and (D) Greater sac-
(B) Big naked-backed bat (P. gymnonotus), (C) Parnell’s mustached bat (P. parnellii), and (D) Greater
winged bat (S. bilineata) (photos: S. Deleva). 
sac-winged bat (S. bilineata) (photos: S. Deleva).
We interviewed 10 groups of people, mainly farmers and landowners around the locations of 
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w2,iwthi trhelraetliavteivlye llyarlgaerg beabt aptoppoupluatliaotinosn, sa,nadn dthtrheree ecacvaevse swwereer eclcalsassisfiifieded aas slelevveel l33, ,wwiitthh ffeeww ssppeecciieess,, 
maaiinnllyy ccoommoonn,, wwiiddeesspprreeaadd,, aanndd ssmaallll ppooppuullaattiioonnss ooff bbaattss.. TThhee ootthheerr 2299 ccaavveess wweerree ccllaassssiiffiieedd aass 
lleevveell 44,, aass tthheeyy sshhoowweedd vveerryy llooww ssppeecciieess rriicchhnneessss,, rreepprreesseenntteedd bbyy oonnllyy aa ffeeww iinnddiivviidduuaallss ((TTaabbllee2 2)).. 
Wee ccoombbiinneedd tthhee twtwoo ininddexeexse stot odedteertemrminein teheth reoorsotos swtsitwh itthhe thhieghheisgth ceosntsceornvsaetirovna tpiorinorpitryio (rBitayt 
(CBaavteC VauvleneVrualbnielirtayb IinlidtyexI)n. dOeuxr) .reOsuulrtsr eshsuolwtsedsh tohwate ndinthe actavneins ehacvave ethseh haivgehtehset choingsheersvtactioonns eprrvioartiitoyn. 
The Tortuga cave received the highest BCVI (1A) due to the large bat colony and vulnerability. In 
addition, eight other caves (i.e., Arelis, Bombasa, Corredores, Dos Brazos, Emus, Túnel Ice 2, Laguna 
 
Diversity 2018, 10, 43 7 of 15
priority. The Tortuga cave received the highest BCVI (1A) due to the large bat colony and vulnerability.
In addition, eight other caves (i.e., Arelis, Bombasa, Corredores, Dos Brazos, Emus, Túnel Ice 2,
Laguna Perdida, and San Pedrillo) had a BCVI result of 1B—highest species diversity and very high
vulnerability. Medium conservation priority caves were evaluated with BCVI values between 1C
(High diversity and low vulnerability) and 3B (low diversity and high disturbance). The roosts with
category 4A, 4B, and 4C were evaluated as low conservation priority due to their low bat diversity
(Table 2).
Table 2. Bat Cave Vulnerability Index (BCVI) as the combination of the Biotic Potential Index (BP) and
the Biotic Vulnerability Index (BV), description of each observed category and the roosts.
BCVI
Priority Description * Roosts
BP BV
1 A High Large population, highest site accessibility,highly prone to disturbance. Tortuga
Large population, high species diversity,
1 B High high site accessibility, highly prone to Arelis, Bombasa, Corredores, Dos Brazos, Emus,
disturbance. Túnel Ice 2, Laguna Perdida, San Pedrillo
Large population, high species diversity,
1 C Medium low site accessibility and less prone to Campanario, Miramar
disturbance.
Relatively high population, low species
2 C Medium diversity, low site accessibility and less Carma
prone to disturbance.
Small populations, relatively high species
3 B Medium diversity, high site accessibility, highly Alma, Gran Galeria
prone to disturbance.
Relatively large population, low species
3 D Medium diversity, rare species present, low site Piedras Blancas 2
accessibility, not prone to disturbance.
4 A Low No bats present, highest site accessibility,highly prone to disturbance. Arco, Ventana
4 B Low Small populations, relatively high speciesdiversity, high site accessibility. San Jocesito Cataratas, Los Sueños, Gran Madre
Afrodiziaco, Aprendizaje, Arbol Caido, Bamboo,
Bananal, Banano Quemado, Buena Cueva,
Very small population, low species Caballo Muerto, Castillo Real, Cinco millones,
4 C Low diversity, lower site accessibility and less Cueva 1, Cueva 3, Cueva 5, Cueva cerca
prone to disturbance. Corredores., Final 7, Túnel ICE 2, La Troja,
Lagrima, Metros 12, Monteadores, Rectangulo,
Sapo Gordo, Serpiente Dormida, Titi Mono.
* Based on Tanalgo et al. 2018 [46].
4. Discussion
This study represents the first significant effort to characterize bat diversity in a large number of
caves in Costa Rica. We provide new data on some additional roosting resources that are available
to many bat species in the region, and our study will serve as a baseline for further research on the
cave-dwelling bats in the Brunca region and in the country (Appendix A, Table A1). With our results,
we have identified caves with a large number of species that potentially may require strong initiatives
to protect, such as the Corredores and Laguna Perdida caves [46]. We have also identified colonies of a
few species that are extremely rare and were only found in one or two caves, including Corredores
and Emus (N. mexicanus in both, C. auritus in the former, and Peropteryx macrotis in the latter), Miramar
(L. aurita), and Campanario (P. personatus), which points to the need for establishing strict visitation
controls for all visitors (including speleologists) to secure the persistence of these colonies, as some
of these species may be considered of high extinction risk [48]. These caves were not categorized as
high-priority by the BCVI given that they do not suffer, yet, from human disturbance, as the caves
are fairly inaccessible. Furthermore, we have also identified two maternity colonies that harbor large
Diversity 2018, 10, 43 8 of 15
numbers of individuals from three species of the genus Pteronotus, primarily in the Campanario cave,
but also in Tortuga (Figure 3). To secure the long-term persistence of these populations, visitation of
Diversity 2018, 10, x FOR PEER REVIEW  8 of 17 
these sites should never be allowed during lactation (February—May) as during this period, a single
edvuernitngo fthdiiss ptuerrbioadn,c ae scionugllde elevaednt toof tdhiestudrebtaacnhcme ceonutladn ldeafda ltlo (tahned dpetoascshibmlyendt eaantdh )faolfl (haunndd proedsssibolfy 
pduepasth[)2 5o]f. hundreds of pups [25].  
FFrroomm tthhee 4444 sstutuddieiedd ccaavveess,, 3388 ((8866.3.366%%)) wweerree ooccccuuppiieedd bbyy bbaattss,, wwhhiicchh rreepprreesseennttss aa hhiigghheerr 
ooccccuuppaattiioonn rraattee tthhaann ssiimmiillaarr ssttuuddiieess rreeppoorrtteedd inin ooththeer rcocuountnrtireise sini nLaLtainti nAmAmeriecraic. aIn.  IPnuePrutoe rRtoicRo,i cfoo,r 
feoxraemxapmlep, loen, olyn l3y13%1 %of otfhteh ceacvaevse isni nthteh eNNataitoionnaal lSSppeeleleoolologgyy ddaattaabbaassee aarree uusseedd aass rroooossttss [[4499]].. AA ssiimmiillaarr 
ssttuuddyy iinn BBrraazziill sshhoowwss tthhaatt oonnllyy aabboouutt hhaallff ooff tthhee oobbsseerrvveedd ccaavvees shhaadd bbatast s[5[05]0.] W. We ealaslos ofofuonudn dthtaht aitn 
icnocmobminbaintiaotnio, na,lla cllavcaevs ehsahrbaorbr oar taottaolt oalf o2f0 2s0pescpieecsi.e Hs.oHwoewveerv, ewr,ew kenokwno twhatth aatt laetaslet a4s6t s4p6escpieesc iiens tihne 
tBhreuBnrcuan rceagrioegni oonf CofoCstoa sRtaicRai caarea creoncsoindseirdeedr ecdavcea-vdew-dewlleerllse [r1s5[]1, 5a]n, adn tdhethreefroerfeo,r ew, ownodnedr ewr hwyh nyonnoen oef 
otfhethsee soethoethr esrpescpieecsi ewsewree rreecroercdoerdd eind oinuro sutur dstyu (dAyp(pAepnpdeixn dAi,x TAab, lTea Abl2e).A O2n).e Oponsesipboilsistyib iisli tthyaits otthhaetr 
ortohoesrtirnogo srteinsgourercseosu racrees maroerme orreeadreilayd ialyvaaivlaabillaeb tloe tboabtsa ttshtahta atraer ennoot tccaavvee--ssppeecciiaalliissttss,, ssuucchh aass sseevveerraall 
ssppeeccieiessw witihtihninth tehter ibtreibMe icMroicnryocnteyrcitneir(ien.ig .(,eM.gi.c, rMoniyccrtoenryiscmtericisr omtisicarnodtisL aamndpr oLnaymctperroisnybrcatecrhiyso btirsa)c, hwyhoticish), 
mwahyicohf tmenayro oofsttenin rhooosllto iwn htroelelosw[5 1tr]e, easn d[51A]r, taibnedu sAlrittuibreautsu sli,twurhaitcuhs, iws thyipchic aisl ltyyfpoiucanldlyr fooousntidn grouonsdtienrg 
fuonlidagere [f5o2li]a. gAel t[e5r2n]a. tAivletelyr,nmatoivreelvyu, lmneorraeb vleualnnedrarbarlee sapnedc ireasr,es uscphecaisesth, esucachrn aivso trhoeu scabrantiVvoamropuysr ubmat 
sVpeacmtrpuymruamn dspMectarcuromp haynldlu Mmamcraocprohpyhllyulmlu mma[5cr3o–p5h5y]l,lmuma y[5h3a–v5e5]a, lmreaayd yhadvisea aplpreeaadreyd dfirsoampptehaereadre farowmh etrhee 
tahreeam wajhoerritey thoef mstuajdoyritcya voef sstwuderye claovceast ewde,raes losucarrteodu,n adsi snugrrnoautunrdailngh anbaittuartsalf ahcaebisteavtse rfaecleo ssesvaenrde /loosrs 
saignndi/fiocra snitgdniefgicraandta tdioengr[a3d8a].tiHono w[3e8v]e. rH, wowe hevoepre, twhaet hsoompee tohfatth essoemoet hoefr tshpeescei eostwheirll sbpeerceiceos rdweidll abse 
wreecocordnetidn uase wtoe mcoonntiitnouret htoe msaomnietoarn tdhea dsadmiteio annadl  caadvdeitriooonsatls cwavieth roaocsotsm wbiitnha ati oconmobf iontahteiornr eosfe oatrhcehr 
treecshenairqcuhe tse,cihnncliuqduiensg, icnacplutudrinesg actatphteurceasv aete tnhter acnacvee aenndtrathneceu asendo fthuelt ruasseo oufn udltdraetseocutonrds d[5e6te].ctors [56].  
 
Figure 3. A nursery colony of Pteronotus spp. in the Tortuga cave (photo: S. Deleva). 
Figure 3. A nursery colony of Pteronotus spp. in the Tortuga cave (photo: S. Deleva).
From the 44 caves we visited, only two (i.e., Laguna Perdida and Piedras Blancas 2) are under 
someF rloemvelt hoef 4p4roctaevcetisown,e avs isthiteeyd ,aoren llyoctawteod( ii.ne. ,thLea gPuiendarPase rBdliadnacaasn dNPatiieodnraals PBalrakn.c Tashe2r)ea irse nuon dlaewr  
spormoteecletivnegl ocfavperos teinc tiCoons,taas Rthiceay, aarnedl omcaotsetd ainret hloecPatieedd raosn Bplarinvcaatse NparotipoenratliePsa, rwk.hTichhe rmeaiskenso tlhaewir 
pprrootetecctitniognc aav desecinisiCoons toaf Rthicea ,laannddomwonset rasr.e Florocamte tdhoen 1p14ri vsapteecpierso poef rbtiaetss, winh Cicohsmtaa Rkiecsat,h aeti rleparsott e4c8t ioarne 
acadveec-isdiwonelolefrtsh eanladn ddoewpennedrs .oFnr ocmavtehse a1s1 4rosopsetcsi eisno of nbea tsdiengrCeoes toar Raincao,thaterle a[1s5t ,4587]a. reThcaisv em-dawkeesll etrhse 
apnrdotdeectpioennd ofo ncacvaevse asnads orothoesrt suinndoenrgerdoeugnrde erooorsatsn osuthcehr a[s1 5a,r5t7if]i.cTiahl itsumnnaekles satnhde gporlodt emctiinoens oaf mcaavtteesr 
aonfd tohteh ehriguhnedsetr gprroiuonridtyr.o oTshtes smucohsta sefafretcifiticviea l wtuanyn etlos apnrdesgeorvlde mthinee scaavmesa titse rtoof pthreophoigshe estht ep rriooroistyts.  
Tchaetemgoorsitzeefdfe catsi voefw haigyhto cpornesseerrvvaettihoen cparvieosriitsyt oaps riompopsoerttahnetr osoitsetss cfoatre gthoer izceodnsaesrovfahtiiognh coof nbsaetrsv a(Stiiotino 
pIrmioproitrytaansteim ppaorrat alna tCsiotnessefrovratchieónco dnes elrovsa tMiounrociféblaagtsos(S),i tbioasIemdp oornt atnhtee dpoacraumlaeCnotantsioernv aocfi óthned Lealotisn 
MAumrecriéiclaagno Bsa),t bCaosnedseorvnatthioend Noceutwmoernkt a[5ti8o]n. Towf oth oef Lthatei ncaAvmese wriictahn thBea thCigohnesset rcvoantisoenrvNateiotwn oprrkio[r5i8ty]., 
TCwoorroefdothreesc aavneds Ewmituhst, haereh igahlseos tthcoen mseorvsta thioenavpilryio raiftfye,cCteodr rbeyd oarnestharnodpoEgmenuics , aacrteivailtsieost, hseumcho sats 
huenacvoilnytraoflfleecdte dvibsyitaatniothnr oapnodg evnaicnadcatliivsimtie, s,asnudc hbaosthu nacroen trreoalldeidlyv iascitcaetsiosinblaen. dDvuaen dtaol istmhe,  afnrdeqbuoetnht 
disturbance, the bat colonies in these caves are facing a dire future unless conservation groups, tour 
guides, and landowners join forces to set limits to visitation rates and enforce proper visitation 
guidelines [59].  
Тhe Bat Cave Vulnerability Index (BCVI) has further allowed us to identify roosts with high 
species diversity that are currently subject to anthropogenic pressure, thus urgent actions are needed 
 
Diversity 2018, 10, 43 9 of 15
are readily accessible. Due to the frequent disturbance, the bat colonies in these caves are facing a dire
future unless conservation groups, tour guides, and landowners join forces to set limits to visitation
rates and enforce proper visitation guidelines [59].
The Bat Cave Vulnerability Index (BCVI) has further allowed us to identify roosts with high
species diversity that are currently subject to anthropogenic pressure, thus urgent actions are needed
to prevent further disturbance. Some roosts with high bat diversity are excluded from the list due
to their difficult approach, which makes them less vulnerable to anthropogenic pressure. Others,
which are highly vulnerable or already affected by anthropogenic activities, were excluded from the
list due to low species diversity. We propose that if limited resources are available, we should focus
our conservation efforts on the roosts of category 1A and 1B, but the other categories need further
monitoring, as new visits can detect new bat species or new threats that could be prevented before
extensive damage is caused to the colonies [46].
5. Conclusions
With this study, we now have the tools to develop conservation strategies to protect the most
important and vulnerable roosts and baseline information to start long-term monitoring programs
of the bat colonies that inhabit these caves. Previous data of cave-dwelling bats in the Brunca region
are available from a few expedition reports made in 1993, conducted mainly by non-specialists,
that present general information about the presence of just a few bat species without information on
their abundance [40]. As such, this report does not provide reliable baseline data to gauge changes in
bat colony size and species assemblages that might allow us to determine if caves are suffering from
human activities conducted in them, most notably uncontrolled visitation.
Our data confirm that caves in the Brunca region of Costa Rica are inhabited by a rich bat fauna
and we must take urgent conservation efforts to protect them. Many of the bats in Costa Rica are of
the lowest conservation priority (least concern) because of their wide distribution, but some species
may be locally rare or declining. We propose cave surveys be included in the national priorities for bat
research and an annual monitoring scheme for roosts to be set up. In this way, we will be able to trace
the change in populations and to take actions if certain species are declining.
Author Contributions: Conceptualization, S.D. and G.C.; Methodology, S.D. and G.C.; Formal Analysis, S.D. and
G.C.; Investigation, S.D. and G.C.; Resources, S.D. and G.C.; Data Curation, S.D.; Writing-Original Draft
Preparation, S.D.; Writing-Review & Editing, S.D. and G.C.; Visualization, S.D.; Supervision, G.C.; Funding
Acquisition, S.D. and G.C.
Acknowledgments: This study was funded by a Rufford Small Grant (No 16923-1), the University of Costa Rica
(Grant No B6033), and partially by the Alvaro Ugalde Grant of Osa Conservation. We also received a grant
from Idea Wild. We thank Carlos Goicoechea and Gustavo Quesada for providing cave location data and the
invaluable help for organizing field expeditions. We would like to express our gratitude to Angel Ivanov for his
support during all stages of this research. We are also very grateful to all the cavers and researchers who provided
an invaluable assistance in the field work: Cristian Castillo Salazar, Karen Miranda Gamboa, Scott Trescott,
Richard Solano Quesada, Michael Martinez Bonilla, Inazio Garin, Jose Alfaro, Joxerra Aihartza, Leonard Baile,
Amanda Vicente-Santos, Gustavo Alfaro Jimenez, Luis Ramirez Castro, Miranda Mitchell, Victor Hugo Carvajal
Rivera, Félix Eduardo, Monica Lerici, Paula Iturralde-Polit, Wilson Hernández Cabrera, Esteban Zárate Brizuela.
Conflicts of Interest: The authors declare no conflict of interest.
Diversity 2018, 10, 43 10 of 15
Appendix A
Table A1. All field sites in the Brunca region, their location (see Figure 1), visit dates, the Bat Cave Vulnerability Index (BCVI), and the Number of individuals of
each species.
Cave Area Visits/mm/yy BCVI No ofSpecies A sp. **
A C C C D G L L L N P P P P P P P S T
jam per sow aur rot sor con rob aur mex kap mac dis has gym par per bil cir
AFRODIZIACO POZO * D 03/16 4 C 1 0 0 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
ALMA E 02/16, 05/16, 02/17. 12/17 3 B 5 0 0 10 0 0 6 3 0 0 0 0 59 0 0 0 0 0 0 15 0
APRENDIZAJE POZO * D 03/16 4 C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
ARBOL CAIDO * D 03/16 4 C 2 0 0 14 0 0 0 0 0 0 0 0 11 0 0 0 0 0 0 0 0
ARCO * A 02/16, 05/16 4 A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
ARELIS * D 01/16; 04/16 1 B 4 0 22 0 0 0 0 0 0 0 0 0 45 0 36 0 0 0 0 55 0
BAMBOO POZO * D 03/17 4 C 2 0 0 0 0 0 0 0 0 0 0 0 12 0 0 0 0 0 0 14 0
BANANAL E 01/17 4 C 1 0 0 9 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
BANANO QUEMADO E 03/16 4 C 2 0 0 0 3 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0
BOMBASA * C 02/18 1 B 6 0 0 350 0 0 1 40 0 20 0 0 0 0 0 0 0 100 0 0 1
BUENA CUEVA * D 03/16 4 C 2 0 0 74 0 0 2 0 0 0 0 0 0 0 0 0 0 0 0 0 0
CABALLO MUERTO * D 01/16, 03/16 4 C 2 0 0 3 0 0 0 0 0 0 0 0 4 0 0 0 0 0 0 0 0
CAMPANARIO * C 05/17, 02/18 1 C 3 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 2000 5000 600 0 0
CARMA E 02/16 2 C 1 0 179 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
CASTILLO REAL E 04/16 4 C 1 0 0 0 0 0 0 0 0 0 0 0 7 0 0 0 0 0 0 0 0
CINCO MILLIONES * D 03/16 4 C 4 0 0 15 0 0 4 0 0 0 0 0 26 0 0 0 0 0 0 20 0
CORREDORES E 01/16, 03.16, 02/16, 12/17 1 B 8 0 14 49 0 1 0 1 0 0 0 235 0 0 0 0 500 700 0 8 0
CUEVA 1 NO NAME * D 01/16 4 C 1 0 0 0 0 0 0 0 0 0 0 0 12 0 0 0 0 0 0 0 0
CUEVA 3 NO NAME * D 01/16 4 C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
CUEVA 5 NO NAME * D 01/16 4 C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
CUEVA CERCA COR E 02/16 4 C 1 0 0 0 0 0 0 0 0 0 0 0 22 0 0 0 0 0 0 0 0
DOS BRAZOS * C 03/17, 02/18 1 B 2 0 0 663 0 0 0 90 0 0 0 0 0 0 0 0 0 0 0 0 0
EMUS D 01/16, 04/16, 12/17 1 B 7 0 0 813 0 0 44 0 0 0 0 10 9 2 0 0 0 200 0 26 0
FINAL 7 POZO * D 03/16 4 C 1 0 0 15 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
GRAN GALERIA E 03/16, 10/16, 12/17 3 B 5 0 49 60 0 0 0 0 0 0 0 0 15 1 0 0 0 0 0 24 0
GRAN MADRE * D 03/16, 03/16 4 C 5 0 0 16 0 0 4 0 0 0 1 0 62 0 0 0 0 0 0 31 0
ICE 1 TUNNEL B 02/17 4 C 1 0 0 200 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
ICE 2 TUNNEL B 02/17, 12/17 1 B 5 0 320 70 0 0 39 0 0 0 0 0 0 0 0 0 0 150 0 12 0
LA TROJA E 04/16 4 C 1 0 0 0 0 0 0 0 0 0 0 0 7 0 0 0 0 0 0 0 0
LAGRIMA POZO * D 03/16 4 C 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
LAGUNA PERDIDA * D 10/16, 10/16, 12/17 1 B 7 100 0 1239 0 0 176 0 0 118 0 0 0 0 0 57 0 350 0 1 0
LOS SUEÑOS * D 11/16, 02/18 4 B 4 0 0 250 0 0 25 0 0 0 0 0 0 0 0 0 0 4 0 65 0
METROS 12 NO NAME * D 01/16 4 C 1 0 0 0 0 0 0 0 0 0 0 0 6 0 0 0 0 0 0 0 0
MIRAMAR POZO * E 12/15, 01/16 1 C 5 0 0 134 1 0 1 0 11 0 108 0 0 0 0 0 0 0 0 0 0
MONTEADORES * E 01/16 4 C 2 0 0 0 0 0 0 0 0 0 0 0 8 0 0 0 0 0 0 2 0
PIEDRAS BLANCAS 2 * D 10/17 3 D 1 80 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
RECTANGULO E 04/16 4 C 2 0 0 0 0 0 0 0 0 0 0 0 13 0 0 0 0 0 0 4 0
SAN JOSECITO * C 05/17, 02/18 4 B 3 0 0 35 0 0 19 0 4 0 0 0 0 0 0 0 0 0 0 0 0
SAN PEDRILLO * C 05/17 1 B 5 0 34 5 0 0 0 0 50 0 0 0 0 0 0 0 0 0 0 1 1
SAPO GORDO POZO * D 03/16 4 C 1 0 0 10 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
SERPIENTE DORMIDA E 03/17 4 C 1 0 0 0 0 0 0 0 0 0 0 0 28 0 0 0 0 0 0 0 0
TITI MONO * D 03/16 4 C 1 0 0 4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
TORTUGA * A 05/16, 10/16, 02/17 1 A 3 0 0 6 0 0 0 0 0 0 0 0 0 0 0 0 427 400 0 0 0
VENTANA * A 05/16 4 A 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
* New caves, according to the National Cave database. ** Species abbreviations: Anoura sp., Artibeus jamaicensis, Carollia perspicillata, Carollia sowelli, Chrotopterus auritus, Desmodus rotundus,
Glossophaga soricina, Lonchophylla concava, Lonchophylla robusta, Lonchorhina aurita, Natalus mexicanus, Peropteryx kappleri, Peropteryx macrotis, Phyllostomus discolor, Phyllostomus hastatus,
Pteronotus gymnonotus, Pteronotus parnellii, Pteronotus personatus, Saccopteryx bilineata, Trachops cirrhosus.
Diversity 2018, 10, 43 11 of 15
Table A2. Bat species in the Brunca region, their conservation status, population trend [51], presence in caves, and cave dependence [11,15,51].
Common Name Latin Name IUCN Status Population Trend Cave-Dwelling Cave-Dependent
Handley’s tailless bat Anoura cultrata LC decreasing Yes No
Geoffroy’s tailless bat Anoura geoffroyi LC stable Yes No
Jamaican fruit bat Artibeus jamaicensis LC stable Yes No
Great fruit-eating bat Artibeus lituratus LC stable Yes No
Chestnut short-tailed bat Carollia castanea LC stable Yes No
Seba’s short-tailed bat Carollia perspicillata LC stable Yes No
Sowell’s short-tailed bat Carollia sowelli LC stable Yes No
Shaggy bat Centronycteris centralis LC unknown No No
Wrinkle-faced bat Centurio senex LC stable No No
Salvin’s big-eyed bat Chiroderma salvini LC stable No data No
Hairy big-eyed bat Chiroderma villosum LC stable No No
Godman’s long-tailed bat Choeroniscus godmani LC unknown No data No data
Big-eared wooly bat Chrotopterus auritus LC stable Yes No
Wagner’s sac-winged bat Cormura brevirostris LC unknown No No
Aztec fruit-eating bat Dermanura azteca LC unknown Yes No
Toltec fruit-eating bat Dermanura tolteca LC unknown Yes No
Thomas’ fruit eating bat Dermanura watsoni LC stable No No
Common vampire bat Desmodus rotundus LC stable Yes No
White-winged vampire bat Diaemus youngi LC unknown Yes No
Northern ghost bat Diclidurus albus LC unknown No No
Hairy-legged vampire bat Diphylla ecaudata LC stable Yes No
Velvety fruit-eating bat Enchisthenes hartii LC unknown No data No data
Brazilian brown bat Eptesicus brasiliensis LC unknown No No
Chirqui brown bat Eptesicus chiriquinus LC unknown No No
Argentine brown bat Eptesicus furinalis LC unknown Yes No
Big brown bat Eptesicus fuscus LC increasing Yes No
Black bonneted bat Eumops auripendulus LC unknown No No
Sanborn’s bonneted bat Eumops hansae LC unknown No data No data
Commissaris’s long-tongued bat Glossophaga commissarisi LC stable Yes No
Pallas’s long-tongued bat Glossophaga soricina LC stable Yes No
Underwood’s long-tongued bat Hylonycteris underwoodi LC stable Yes Yes
Yellow-throated big-eared bat Lampronycteris brachyotis LC stable Yes No
Desert red bat Lasiurus blossevillii LC unknown No No
Southern yellow bat Lasiurus ega LC unknown No No
Dark long-tongued bat Lichonycteris obscura LC unknown No data No data
Goldman’s nectar bat Lonchophylla concava LC unknown Yes No data
Orange nectar bat Lonchophylla robusta LC unknown Yes Yes
Tomes’s sword-nosed bat Lonchorhina aurita LC stable Yes Yes
Pygmy round-eared bat Lophostoma brasiliense LC stable No No
White-throated round-eared bat Lophostoma silvicolum LC unknown No No
Long-legged bat Macrophyllum macrophyllum LC unknown Yes No data
Hairy big-eared bat Micronycteris hirsuta LC unknown No No
Diversity 2018, 10, 43 12 of 15
Table A2. Cont.
Common Name Latin Name IUCN Status Population Trend Cave-Dwelling Cave-Dependent
Common big-eared bat Micronycteris microtis LC stable Yes No
White-bellied big-eared bat Micronycteris minuta LC unknown Yes No
Schmidts’s big-eared bat Micronycteris schmidtorum LC stable No No
Striped hairy-nosed bat Mimon crenulatum LC stable No No
Coiban Mastiff Bat Molossus coibensis LC unknown No No
Velvety free-tailed bat Molossus molossus LC unknown No No
Miller’s mastiff bat Molossus pretiosus LC unknown Yes No data
Black mastiff bat Molossus rufus LC stable No No
Sinaloan mastiff bat Molossus sinaloae LC stable Yes No
Silver-tipped myotis Myotis albescens LC stable Yes No
Hairy-legged myotis Myotis keaysi LC unknown Yes No
Black myotis Myotis nigricans LC stable Yes No
Montane myotis Myotis oxyotus LC unknown No data No data
Riparian myotis Myotis riparius LC stable No data No data
Mexican funnel-eared bat Natalus mexicanus LC unknown Yes Yes
Lesser bulldog bat Noctilio albiventris LC stable No No
Greater bulldog bat Noctilio leporinus LC unknown Yes No
Greater dog-like bat Peropteryx kappleri LC unknown Yes No
Lesser doglike bat Peropteryx macrotis LC stable Yes No
Pale spear-nosed bat Phyllostomus discolor LC stable Yes No
Greater spear-nosed bat Phyllostomus hastatus LC stable Yes No
Heller’s broad-nosed bat Platyrrhinus helleri LC stable Yes No
Greater broad-nosed bat Platyrrhinus vittatus LC unknown Yes No data
Naked-backed bat Pteronotus davyi LC stable Yes Yes
Big naked-backed bat Pteronotus gymnonotus LC stable Yes Yes
Parnell’s mustached bat Pteronotus mesoamericanus LC unknown Yes Yes
Wagner’s mustached bat Pteronotus personatus LC stable Yes Yes
Thomas’ yellow bat Rhogeessa io LC unknown No No
Proboscis bat Rhynchonycteris naso LC unknown No No
Greater sac-winged bat Saccopteryx bilineata LC unknown Yes No
Lesser sac-winged bat Saccopteryx leptura LC unknown No No
Talamancan yellow-shouldered bat Sturnira mordax NT stable No data No data
Mexican free-tailed bat Tadarida brasiliensis LC stable Yes No
Spix’s disk-winged bat Thyroptera tricolor LC unknown No No
Stripe-headed round-eared bat Tonatia saurophila LC stable No No
Fringe-lipped bat Trachops cirrhosus LC stable Yes No
Niceforo’s big-eared bat Trinycteris nicefori LC unknown No No
Tent-making bat Uroderma bilobatum LC stable No No
Striped yellow-eared bat Vampyriscus nymphaea LC unknown No No
Northern little yellow-eared bat Vampyressa thyone LC unknown No No
Great stripe-faced bat Vampyrodes major LC unknown No No
Spectral bat Vampyrum spectrum NT decreasing Yes No
DiversityD2iv0e1r8si,ty1 02,01483, 10, x FOR PEER REVIEW  14 of 171 3 of 15
 
Figure A1. Some of the field work sites, mentioned in this study: (A) San Pedrillo cave, photo: S. 
FigureDAe1le.vSao; m(Be) oEfmthuse ficaevlde, wphoortkos: iSte. sT,rmesecnottti;o (nCe)d Bianmthboiso sctuavdey, :p(hAo)toS:a Cn. PCeadsrtiilllloo cSaalvaez,apr;h (oDto) :GSr.aDn eleva;
(B) EmMuasdcraev cea,vpe,h pohtoot:oS: S. .T Dreeslecvoat.t ; (C) Bamboo cave, photo: C. Castillo Salazar; (D) Gran Madre cave,
photo: S. Deleva.
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