Маматкалыков Пиримкул Маматкалыкович

Underground habitats as a unit for bat conservation in Southwestern Kyrgyzstan

Heliana Dundarova1*, Kursantbek Altybaev2 ,Pirimkul Mamatkalykov2, BegaiymSultanbek kyzy2, Abdurashit Nizamiev2, Guliza Momosheva2and Dmitry Milko3

1. Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria

2. OshStateUniversity, 331 Lenin str., 723500 Osh, Kyrgyzstan

3. Institute for Biology and Pedology at the NationalAcademy of Sciences, 265 Chuy str., 720021 Bishkek, Kyrgyzstan

* Corresponding author: heliana.dundarova@iber.bas.bg

Abstract

The study was conducted in Southwestern Kyrgyzstan which is a transboundary territory in Central Asia. The presence of limestone rocks from the Carboniferous and Devonian age determines the occurence of many underground sites. Thesecharacteristics make the area an important place for cave-dwelling bat species.

Assessment of bat abundance, species richness, and conservation priority of each cave was estimated using the Bat Cave Vulnerability Index (BCVI) for first time out of the tropics. The method revealed that two underground sites are the most threatened and in need of protection. These caves are easily accessible and under constant anthropogenetic pressure.

We confirm significant maternity colonies ofRhinolophus ferrumequinum, Rh. lepidus, Myotis blythiiand M. emarginatusin five caves,where the most abundant summer colonies are found for M.blythiiin two of them. We report for first time a maternity colony of Rh. lepidus in Kyrgyzstan due to its long-term erroneous definition as Rh. hipposideros. The results show that the conservation status of Rh. hipposideros must be reviewed and changed to Near Threatened or Vulnerable for the Central Asia region.

The study will be used as a baseline for future conservation research on cave-dwelling bats and underground habitats in the region.

Keywords: Central Asia, Chiroptera, caves,protection

Introduction

Underground habitats, or caves senso lato, present natural openings mainly in limestone rocks and rarely in lava tubes. Considered as azonal habitats - unevenly distributed around the Earth with similar environment (total darkness except in the entrance zone, relatively constant temperature and humidity) across all latitudes (Furey&Racey 2016, Moldovan et al. 2018), they are suitable roosts for many bat species, protecting them against inclement weather and reducing the loss of body water (Kunz 1982; Gunn 2003, Avila-Flores & Medellin 2004). Caves are regularly used by bats as maternity colonies in the summer, hibernacula in the winter and swarming sites in the autumn and spring (Dietz et al. 2009, Nagy &Postawa 2010, Dundarova 2018).

Considering that bats are extremely sensitive to habitat loss, pollution, disturbance, quarrying, mining and vandalism (Baker et al. 1998, Hudson & Mickleburgh 2001), regular monitoring of their colonies in underground sites is a widely used method for assessment of their species richness, age structure, seasonal changes, population trends and anthropogenic threats (Petrov 2008, Kunz et al. 2009, EUROBATS 2010). The main treaties that are of particular relevance to bats includethe Ramsar Convention, World Heritage Convention, CITES, Bonn Convention, Bern Convention, The EEC Habitats and Species Directive, and EUROBATS. However, national legal protection given to bats is varied. In some countries, bats receive no protection at all. According to Hudson & Mickleburgh (2001) in Central Asia, and the former SovietRepublics little information on the status and distribution of bat species is available.

In Kyrgyzstan studies directed on the bat fauna included the Soviet and the post-Soviet periods of XXth century. Most of them contain sporadic data and were focused on Uzbekistan, Kazakhstan, Tajikistan and Turkmenistan (Bobrinski1929, Kuzyakin 1950, Bogdanov 1953, Bobrinski et al. 1964, Strelkov1978, 1980, 1983, 1987, Strelkov &Shajmardanov 1983, Khabilov 1980, 1992). The first thematic study aimed to assess bat diversity in Kyrgyzstan is provided by Rybin et al. (1987), where 16 species are described. Benda et al. (2011) provided a review of bats from Transcaucasia and West Turkestan and clarified some of the questionable taxa previously discussed by Rybin et al. (1987) in Kyrgyzstan. Finally, Khabilov et al. (2018) discussed the distribution of Blyth′s horseshoe bat in Central Asia and its sympatry with the Lesser horseshoe bat.

Due to the absence of thematic research in Kyrgyzstan focused on the cave-dwelling bat specific sites, recent mining and quarry activities have been started without preceding impact assessment. Since the importance of bat colonies in caves is largely unknown, need for detailed impact assessments in big infrastructure and exploitation planning can only be raised by providing basic data for the existence of the affected species groups. Further, Kyrgyzstan became a popular tourist destination during the last few years and most of the tour operators conducted illegal excursions to the caves close the villages. The influence of such anthropogenic factors has a negative impact on the species composition and abundance of bats.

This is a pilot study for the region of Central Asia and aims to: 1) assess the main threats for bat summer colonies in Southwestern Kyrgyzstan 2) use underground habitats as a unit for bat conservation 3) start regular monitoring of cave-dwelling bat colonies in Southwestern Kyrgyzstan.

The results are relevant to ecological and environmental issues linked to habitat lost, climate change and bat conservation decision-making.

Material and methods

Study region

The investigation was conducted in Southwestern Kyrgyzstan, located within the Tien Shan and Pamir – Alay mountain systems in Central Asia. The total area is 79,682 km2 and includes three administrative regions:Batken (N 39.833333, E 71.5), Osh (N 40.536944, E72.798889) and Jalal-Abad (N 40.933333, E 73). Climate varies from continental in Tien Shan to semi-arid in the FerganaValley (Beck et al. 2018). This part has a transboundary character, situated between Uzbekistan and Tajikistan. The territory can be divided into two main zones: arid with agricultural areas in the valleys, and mountainous, covered by sparse meadows or not covered by vegetation.

Cave survey

Fieldwork was conducted during two periods: June – September 2018, and February 2019 – April 2019 (table 1). Information about the caves and their accessibility was gathered from Dudashvili (2012), and Ogudin (2013). According to them more than 60 underground habitats of Carboniferous and Devonian age were present in the study region.

The final decision for the valuable underground sites was made using Rybin et al. (1987), Benda et al. (2011) and preliminary exploration in 2017 (fig. 1). Data were collected from each site, which was visited at least twice (once in the bat’s active summer period, and once in their hibernation period). The location and elevation of each cave was determined using a GPS unit. We also described the number of entrances, cave length, and the presence of water.

Bat surveys

Bat species were identified based on their morphological characteristics. Specimens were captured

using mist-nets with different lengths. Every bat was placed in а separate cloth bag. Determination of the gender, age and reproductive status was provided for every individual. Calipers were used to take measurements of the length of the forearm (FA), and for some species groups, additional measurements like, fifth finger (D5), third finger (D3), and the upper teeth row length (CM3) (Kunz et al. 2009). All captured bats were released as soon as possible after being measured.

Population sizes were estimated for each species. In small clusters of bats for example, around 30 individuals were counted directly in the cave. For larger colonies of bats, a photographic method of counting inside the site was used (Eurobats 2008).

No voucher specimens were collected during this study. Capture and handling with the bats were carried out under the research permits № 000025ЖО from 2018 and № 000036ЖО from 2019, State Agency for Environmental Protection and Forestry under the Government of the Kyrgyz Republic.

Assessment of the Conservation Priority of the caves

The conservation priority of each cave was estimated using the Bat Cave Vulnerability Index (BCVI), based on the bat species diversity and the presence of human-induced threats in the caves (Tanalgo et al. 2018). The index is tailored to rapidly evaluate cave biotic potential and vulnerability based on bat species diversity and the presence of human-induced threats using two components. The first one is Biotic Potential Index (BP) which contains species richness, abundance, relative abundance, endemism, conservation status (IUCN 2018), and rarity index. The BP index values varies between 1 and 4, where level 1is the highest and 4 the lowest.

The second component is Biotic Vulnerability Index (BV) which gives information on cave accessibility, morphology, visitation, and land use in adjacent areas. The BV index values are A, B, C, and D, where A represents the highest vulnerability to disturbance and D no disturbance.

Underground roosts in the study area were classified using the combined values of BP and BV. Caves which were classified under 1A,1B and 2A values have the highest conservation priority. Caves under 1C and 3D have moderate conservation priority, and the rest under category 4 have low conservation priority.

Results

Cave and Bat Survey

Overall, 13 underground sites (natural and artificial), 9 in Osh region, 3 in Batken region and 1 in the Jalal-Abad region were studied (fig. 1). The average elevation was 1260 m a.s.l., where the minimal altitude was 659 m a.s.l. (Sasyk-Unkur cave) in Osh and maximal 1865 m a.s.l. (Sulunkur cave) in Batken region. The length of the caves varied from 10 m in Sulaiman-Too cave to more than 2000 m in Kan-i-Gut cave, with average cave length of 472 m. Most of the caves were with 1 entrance. Water was present only in 3 of them (Mine of Fersman, Chil-Ustun, and Kara-Unkur), see table 1. Technical equipment was required for the vertical passage of Fersman mine and for rock climbing to the entrance of Chil-Ustun cave.

During the cave survey 11 bat species from 3 families Rhinolophidae ( Rhinolophus ferrumequinum, Rh. hipposideros, Rh. lepidus), Vespertilionidae(Myotis blythii, M. emarginatus, Eptesicus ognevi, Hypsigosavii, Pipistrellus pipistrellus, Barbastella capsica, Plecotusstrelkovi ) and Molossidae (Tadaridateniotis) were identified. Significant bat abundance was found in 4 caves, significant bat richness in 3 caves, and both parameters only in 1 cave (table 2). The prevalent species were M. blythii (n > 10000), Rh. lepidus (n > 1700), and Rh. ferrumequinum (n > 500), followed by M. emarginatus (n > 20) andP. pipistrellus (n > 10) and less frequent species were Rh. hipposideros,E. ognevi,H. savii, B.capsica, P. strelkovi and T. teniotis.

Most of the bat species are categorized by IUCN (2019) as Least Concern, for Rh. ferrumequinum, Rh. hipposideros, M. blythii with Decreasing population trends; Not evaluated and with Unknown population trends for E. ognevi, B. capsica, P. strelkovi, and Least Concern with Unknown population trends for Rh. lepidus (table 2).

Evaluation of cave vulnerability and conservation priority

Assessment using the BCVI showed different vulnerability and conservation priority levels for each cave (table 3). The BP index scored Mine of Fersman and Baritova cave as the most vulnerable (BP= 1), since the first one comprises the highest abundance and species richness, and both comprise cave-dwelling bat species with decreasing and unknown population trends. Other caves were less vulnerable (BP = 3 and 4), because of the relatively low species richness, mosly present by one common species and the absence of endemic species. Surprisingly, Azhidar-Unkur and Ashkana caves were evaluated with BP index 4, probably due to the high abundance of one common species in the first one and high species richness butless frequent species in the second one.

The BV index identified 6 caves as vulnerable (BV = A), due to their easy accessibility and signs of local exploitation and illegal tourism. Six caves had BV index status B, indicating their accessibility for local people. There was one cave - Ashkana with BV index status of C, which indicates that is in a less accessible area and with lesser signs of exploitation.

Both BP and BV indices revealed the Mine of Fersman and Baritova caves as high priority underground sites for conservation (BCVI = 1A), 2 caves were assessed as medium priority for conservation and 9 caves were assessed as low priority for conservation. Azhidar-Unkur and Ashkana caves were assessed as low priority caves (BCVI = 4B and 4C), due to the fact that both are less accessible for the local people and not popular for tourism. Duvahan-Unkur/Jarganat-Unkur were categorized with a high level of vulnerability (BV=A) but at the same time with low species richness (BP =4) due to the large population of one species.

Discussion

Bat abundance and diversity

The most abundant cave-dwelling species wereRhinolophus ferrumequinum, Rh. lepidus,Myotis blythii and M. emarginatus in the Mine of Fersman, Baritova, Azhidar-Unkur, Duvahan-Unkur/Jarganat-Unkur, and Chil-Ustun caves. Comparing our results with the available literature (Bogdanov 1953, Rybin et al. 1987, Khabilov 1992, Benda 2011, Tadzibaeva2018) these sites included one of the biggest maternity aggregations for Rh. lepidus and M. blythiiin Central Asia, see table 2. Due to the fact, that for a long time Rh. lepidus was mis-identifiedas Rh. hipposideros (Benda et al. 2016), we confirm nursery colonies of Rh. lepidus(fig. 2 ) for first time in Kyrgyzstan within the Mine of Fersman and Chil-Ustun cave. During the research we found only 4 individuals from the species Rh. hipposideros, one in a mist-net in front of Ashkana cave in the summer and three hibernated individuals in Uluu-Too cave. This observation and the wrongly assigned colonies of Rh. lepidusin previous studies confirm that Rh. hipposideros is a rare element in the Central Asian fauna.

According to Bobrinski (1929), Kuzyakin (1950), Bogdanov (1953), Bobrinski et al. (1964), Strelkov (1978, 1980, 1983, 1987), Strelkov &Shajmardanov (1983), Khabilov (1980, 1992), Rybin et al. (1987), Benda et al. (2011), Rhinolophus bocharicus is a typical representative of the Central Asian cave-dwelling bat fauna. The species was reported in the Mine of Fersman,Duvahan-Unkur/Jarganat-Unkur and Kan-i-Gut caves (Rybin et al. 1987, Benda et al. 2011, Tadzibaeva 2018) in Kyrgyzstan. However,Rh.ferrumequinumand Rh. bocharicus are sibling species and the photographic method is not a useful tool for assessment in mix bat aggregations. Based on the morphometric characters, we failed to find Rh. bocharicus, and all specimens were definite as Rh.ferrumequinum.

We observedmixed maternity colony of Rh.ferrumequinum,M. blythii and M. emarginatus in Baritova cave, where up to 30 individuals of M. emarginatus were directly counted. The biggest nursery sites belonged to M. blythii, exceeding 6000 and 10000 individuals in Azhidar-Unkur, and Duvahan-Unkur/Jarganat-Unkur (appendix A, fig. A1). However, during the winter period neither M. blythii norM. emarginatus were detected. Small colonies of M. blythii were found in the beginning of the spring (April) in both caves.

Pipistrellus pipistrelluss. l . is one of the most common species in the Palearctic region (Wilson&Mittermeier2019). Due to this fact it was not been surprise to find summer colonies in Ashkana and Sulaiman-Too caves.

In addition, we captured single representative of Eptesicus ognevi, Hypsugosavii, Barbastella capsica, Plecotusstrelkovi and Tadaridateniotis in front of the Mine of Fersman, Baritova, Sasyk-Unkur, Ashkana, Aktur-Pak, Kan-i-Gut caves in the summer, and only B. caspicaand P. strelkoviin the Mine of Fersman and Baritova cave in the winter. These results corresponded well with the published data (Benda et al. 2011) to be rarely established species, except T. teniotis,a common bat in Southern Kyrgyzstan (Rybin 1987, Benda 2011) and B. caspica frequently reported from Northern Tajikistan (Tadzibaeva 2018).

Underground habitats as a unit for bat conservation

Generally, underground habitats in Southwestern Kyrgyzstan are drier due to the lower humidity result from the semi-arid climate zone (Beck et al 2018), compared with those in the Palearctic region (Zukal et al. 2017, Barlas&Yamaç 2019). Water bodies were rarely present within the studied caves (table 1), except in Kara-Unkur cave in the Jalal-Abad region and the Mine of Fersman and Chil-Ustun cave in the Osh region. Kara-Unkur cave is located in Jalpak – Tash, which is a hilly gypsum karstic terrain with thick loess cover. Bat guano and an individual of M. blythii was found inside during our visit in the late autumn. This cave is a potential significant roost for the bats inhabitingJalpak – Tash, regarding the large area of the plateau and the absence of other suitable shelters. In the Osh region we found both extremes for water bodies within the underground sites (appendix A1, fig. A2), sinter lakes in a typical limestone cave (Chil-Ustun) and hydrothermal karst with thermal water in the Mine of Fersman (Dudashvili 2012). Both caves are significant for the Horseshoe bat species. The altitude of this study does not exceed 2000 m with maximum bat diversity around 1000 m. The highest cave which we surveyed was Sulunkur in the Batken region. However, the weather was cold and snowy in the early spring and only one bat from the species Rh.ferrumequinum was observed. Both underground sites Kara-Unkur and Sulunkur were visited only once.

Standardized assessment using BCVI revealed two underground sites (Mine of Fersman and Baritova cave) that were the most threatened and in need of protection. They are home to relatively diverse and abundant cave-dwelling bats and present important maternity sites for 4 bat species (Rh.ferrumequinum, Rh. lepidus,M. blythii and M. emarginatus) in Central Asia. These caves are in easily accessible locations and subjected to illegal tourism pressures. Unregulated tourism causes a variety of negative impacts, especially to the cave-dwelling bats, which might result in roost abandonment and/or decline in the population (Furey et al 2016). Four additional caves (Sasyk-Unkur, Duvahan-Unkur/Jarganat-Unkur, Sulaiman-Too, Aktur-Pak) are vulnerable, as these sites are prone to disturbance, insome of them signs of recent mining and vandalism were found. Two caves (Azhidar-Unkur and Ashkana) seemed to be naturally protected from the anthropogenetic pressure due to their inaccessibility regarding illegal tourism.

A pressing concern from the present study is that most of the species areclassified as Least Concern (IUCN 2019).Contrary to this statement, our study displayedthe rarity of Rh. hipposiderosin the region. The species is also presented in the Red Data Book of Kyrgyzstan and we suggest it to be categorized as Near Threatened or Vulnerable for the Central Asia area. In addition, three species (E. ognevi, B. capsica and P. strelkovi) are still not evaluated by IUCN due to the absence of sufficient and comparable information.

Conclusion

This study is a key step for the development of conservation strategies for protection of the most important and vulnerable to anthropogenic pressure underground sites in Southwestern Kyrgyzstan. Since within the territory more than 60 caves are reported, this research contributes with baseline information for future long-term monitoring programs of the bat colonies that inhabit these caves. Previous studies were focused on bat taxonomy and diversity (Rybin eta al. 1987, Benda et al. 2011) without information of the cave-dwelling species abundance and the conservation status of the maternity colonies. Our research confirms that underground sites in Southwestern Kyrgyzstan are important roosts for the cave-dwelling bats, playing an irreplaceable role as nursery sites and are inhabited by a rich bat fauna, regarding the bat diversity in the arid and semi-arid climate zone.

The majority of the bats in Kyrgyzstan are of the lowest conservation priority (least concern) because of their wide distribution in the Palearctic region, but some species are locally rare or declining, as is the case with Rh. hipposideros. Therefore, capacity building programs for bat researchers must be included in the national priorities and monitoring programs to be taken. In this way, we will be able to trace the change in populations and to take conservation actions if certain species are declining.

Acknowledgments

The study was funded by a Rufford Small Grant (No 24890-1). We are sincerely grateful to Dr. Christian Dietz and prof. Ivan Horáček for giving us the strength, knowledge, ability and opportunity to undertake this research study and to persevere and complete it satisfactorily.

We would like to express our gratitude to the Foundation for the Preservation and Exploration of Caves represented by of the director Alexey Dudashvili for providing cave location data and ZheenbekKulenbekov from the American University of Central Asia for the project popularization. We are very grateful to Sergey Dudashvili for his administrative and accommodation help. We are sincerely grateful to DaniarImlokov and his family for their cordial support and providing their home as a basecamp during the fieldwork implementation. We would like to thank to Lee Knight, Anton Brancelj, Josiane and Bernard Lips, which provided invaluable assistance in the first stage of the project.

Special thanks to the students which were a part of the fieldworks and capacity building workshops. They are the future of bat research in Kyrgyzstan!

Author Contributions

HD conceived the project, and designed the study. HD, AN, GM, KA, PM, BS and DMorganized fieldwork and performed the field studies. HD analyzed the data and wrote the paper with input from all authors.

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Figure 1. Map of Kyrgyzstan with particular focus on the studied underground sited in the Southwestern part of the country. 1 – Kara-Unkur, 2 – Sulaiman-Too, 3 – Baritova, 4 – MineofFersman, 5 – Azhidar, 6 – Uluu-Too, 7 ­– Duvahan/Jarganat – Unkur, 8 – Sasyk-Unkur, 9 – Ashkana, 10 – Chil-Ustun, 11 – Aktur-Pak, 12 –Sulunkur cave, 13 – Kan-i-Gut.


Figure 2. Maternity colony of Rhinolophus lepidus in the Mine of Fersman.


Table 1. Physical characteristics, location and visit time of 15 underground sites in Southwestern Kyrgyzstan; Summer (June – early August); Autumn (end of August - September); Winter (February – March); Spring (April), where” +” means visit and “–“not visit.

Cave

Coordinates

alt/m

Cave length/m

# entrances

Water

2018

2019

N

E

Summer

Autumn

Winter

Spring

MineofFersman

40,3534

72,6095

1106

990

2

present

+

+

+

+

Baritova

40,3538

72,5938

1217

110

2

absent

+

+

+

+

Azhidar-Unkur

40,3533

72,5976

1226

120

1

absent

+

+

+

+

Uluu-Too

40,3868

72,3549

1475

1

absent

Duvahan-Unkur/Jarganat-Unkur

40,5433

72,4975

937

110

1

absent

+

-

+

+

Chil-Ustun

40,5341

72,5319

1250

380

1

present

+

-

+

-

Ashkana niche

40,5349

72,5315

1220

30

1

absent

-

+

-

-

Sasyk-Unkur

40,5479

72,4931

659

115

1

absent

+

-

-

+

Sulaiman-Too

40,5299

72,7859

1123

10

passable

absent

-

+

-

-

Kan-i-Gut

40,0133

70,3462

1588

more than 2000

2

absent

+

-

-

-

Aktur-Pak

40,1764

71,0625

880

50

1

+

-

-

-

Sulunkur

39,9533

71,3254

1865

30

1

absent

-

-

-

+

Kara-Unkur

40,5769

73,5213

1812

100

1

present

-

+

-

-

Table 2. Bat conservation status and population trend in the studied caves, where * indicates the highest abundance and species diversity sites, indicates sites with significant abundance, and ⁂ sites with significant species richness (diversity).

Species

IUCN status

Populationtrends

Cave sites

Fersman *,

Baritova

Azhidar

Uluu

Duvahan

Chil

Sasyk

Ashkana

Sulaiman

Kan

Aktur

Sulunkur

Kara

Rh . ferrumequinum

LC

Decreasing

143

578

4

10

109

1

1

Rh. hipposideros

LC

Decreasing

3

1

Rh . lepidus

LC

Unknown

1786

580

1

1

M.blythii

LC

Decreasing

71

860

6600

88

10390

2

1

M . emarginatus

LC

Stable

28

1

1

1

E. ognevi

Notevaluated

Unknown

1

H. savii

LC

Stable

2

1

1

P. pipistrellus

LC

Stable

10

10

B . caspica

Notevaluated

Unknown

5

1

4

2

P . strelkovi

Notevaluated

Unknown

3

T. teniotis

LC

Unknown

3

2

Abundance (А)

Species richness ( S)

2010

1467

6600

96

10390

590

117

16

11

4

3

1

1

6

3

1

4

1

2

6

6

2

1

2

1

1

Table 3. Assessing cave disturbance in Southwestern Kyrgyzstan using BCVI. This index is a combination between Biotic Potential Index (BP) and Biotic Vulnerability Index (BV) derived from assessing status of cave-dwelling bats and caves. Based on Tanalgoetal.(2018).

BCVI

Priority

Description

Underground sites

BP index

BV index

1

A

High

Largest population abundance and species richness, easy accessibility and highly prone to disturbance

Mine of Fersman, Baritova

3

A

Medium

Relatively large population abundance of common species, low species richness, easy accessibility and highly prone to disturbance

Sasyk-Unkur

3

B

Medium

Relatively large population abundance of common species, low species richness, lesser accessibility, but prone to disturbance

Chil-Ustun

4

A

Low

Large population abundance, one species, easy accessibility and highly prone to disturbance

Duvahan-Unkur/Jarganat-Unkur, Sulaiman-Too, Aktur-Pak

4

B

Low

Relatively large population abundance, one species, lesser accessibility, and prone to disturbance

Azhidar-Unkur, Uluu-Too, Kan-i-Gut, Sulunkur, Kara-Unkur

4

C

Low

Small population abundance, relatively high species richness, lesser accessibility, and less prone to disturbance

Ashkana


Appendix A

Figure A1. Maternity colony of Myotis blythiiincluding 10 390 individualsin Duvahan-Unkur/Jarganat-Unkur.

Figure A2. Water bodies within the underground sites. (A) Mine of Fersman and (B) Chil-Ustun cave.

(A) (B)