Arthropoda fauna of Zindan Cave (Isparta, Turkey) with notes on new records and some ecological characteristics

Year 2021, Volume: 45 Issue: 2, 229 - 243, 01.06.2021

Cemal Çağrı Çetin , Ergin Turantepe Mehmet Gürbüz

https://doi.org/10.16970/entoted.889779

Abstract

The aims of the study were to investigate the Arthropoda fauna of Zindan Cave (Aksu, Isparta Province, Turkey) and to consider some ecological characteristics of the collected species such as feeding habits, cave-dwelling categories, and zone distributions in caves. Twenty-seven species of Arthropoda were determined between May 2015 and December 2016, from Zindan Cave. The species found belong to the following orders: nine to Collembola, six to Coleoptera, five to Araneae, two to Diplopoda and one to Orthoptera, Trichoptera, Diptera, Trombidiformes and Isopoda. Nine species are endemic of Turkey. Traegaardhia distosolenidia Zacharda, 2010 (Acari: Rhagidiidae) and Folsomia asiatica Martynova, 1971 (Collembola: Isotomidae) are newly recorded for the fauna of Turkey. The presence of Heteromurus sexoculatus Brown, 1926 (Collembola: Entomobryidae) in Turkey is confirmed. Twenty-four of the 27 species were from the dark zone and half of the collected species (6 troglobites and 8 troglophiles) are ecologically adapted to cave ecosystems. Species can be divided into three groups according to trophic preferences: 15 scavengers, 10 predators and two omnivores. Food habits, cave-dwelling categories, and zone distributions of collected species are discussed.

Keywords

Arthropoda, biospeleology, cave-dwelling categories, habitat, Zindan Cave

Supporting Institution

This study was supported by Süleyman Demirel University, Scientific Research Unit, Isparta, Turkey.

Project Number

Grant Project No: 4272-YL1-15

Thanks

We thank Dr. Gökhan Aydın (Isparta University of Applied Science, Turkey) and all of the members of the Biospeleology Society (BAT, Turkey). We are appreciative our colleagues who identify the species: Dr. Kadir Boğaç Kunt (Eskişehir Technical University, Turkey), Arachnida; Dr. Hasan Koç (Muğla Sıtkı Koçman University, Turkey), Diptera; Dr. Stefano Taiti (Institute of Ecosystem Studies, CNR, Italy), Isopoda; Dr. Igor Kaprus (The National Museum of Natural History at the National Academy of Sciences of Ukraine), Collembola; Dr. Michel Perreau (Paris Diderot University, France), Leiodidae; Dr. Mustafa Darılmaz (Aksaray University, Turkey), Dytiscidae; Dr. Dragan Antic (Belgrad University, Serbia) and Dr. Henrik Enghof (Natural History Museum of Denmark), Diplopoda; Dr. Miloslav Zacharda (Institute of Systems Biology and Ecology, Czech Republic), Rhagidiidae; Dr. Füsun Sipahiler (Hacettepe University, Turkey), Trichoptera; Dr. Mehmet Sait Taylan (Hakkari University, Turkey), Orthoptera; and Dr. Sinan Anlaş (Celal Bayar University, Alaşehir Vocational School, Turkey), Staphylinidae. Also, we thank Dr. İsmail Şen (Isparta University of Applied Science, Turkey) for his contributions during the preparation of the article. This study was undertaken by the first author as a master's thesis and was supported by the Unit of Scientific Research Projects of Süleyman Demirel University (BAP 4272-YL1-15).

Zindan Mağarası (Isparta, Türkiye) Arthropoda faunası, yeni kayıtlar ve bazı ekolojik özellikler üzerine notlar

Abstract

Çalışmanın amacı, Zindan Mağarası (Aksu, Isparta, Türkiye) Arthropoda faunasını belirlemek ve toplanan türlerin beslenme alışkanlıkları, ekolojik sınıflandırılması ve zon dağılımları gibi bazı ekolojik özelliklerini ortaya koymaktır. Zindan Mağarası'ndan Mayıs 2015 ile Aralık 2016 arasında 27 Arthropoda türü belirlenmiştir. Bu türlerden dokuzu Collembola, altısı Coleoptera, beşi Araneae, ikisi Diplopoda takımlarına ait iken, Orthoptera, Trichoptera, Diptera, Trombidiformes ve Isopoda takımlarına aittir. Bu türlerden dokuzu Türkiye için endemiktir. Traegaardhia distosolenidia Zacharda, 2010 (Acari: Rhagidiidae) ve Folsomia asiatica Martynova, 1971 (Collembola: Isotomidae) türleri, Türkiye faunası için yeni kayıtlardır. Aynı zamanda Türkiye için Heteromurus sexoculatus Brown, 1926 (Collembola: Entomobryidae) varlığı doğrulanmıştır. Toplanan 27 türden yirmi dördü karanlık zondan ve türlerin yarısının (6 troglobit ve 8 troglofil) ekolojik olarak mağara ekosistemine adapte olduğunu ortaya konmuştur. Ayrıca türlerin trofik tercihlerine göre: 15 çöpcül, 10 predatör ve iki omnivor olmak üzere üç gruba ayrıldığı belirlenmiştir. Sonuç olarak, toplanan türlerin beslenme alışkanlıkları, ekolojik sınıflandırılması ve zon dağılımları tartışılmıştır.

Keywords

Arthropoda, biyospeleoloji, ekolojik sınıflandırılma, habitat, Zindan Mağarası

Project Number

Grant Project No: 4272-YL1-15

References

• Alp, A. O., 2013. Aksu - Zindan Mağarası ΜHTHP ΘΕΩΝ ΟΥΕΓΕΙΝΟΣ Kutsal Alanının Restitüsyonu. Adalya, 16: 119-140 (in Turkish with abstract in English).
• Antić, D., C. Ç. Çetin, E. Turantepe & M. F. Gürbüz, 2016. A new cave-dwelling species of the genus Mesoiulus Berlese, 1886 (Diplopoda, Julida, Julidae) from Turkey. Zootaxa, 4196 (2): 296-300.
• Argano, R. & C. Manicastri, 1988. Il genere Trichonethes Strouhal, 1953 di Turchia (Isopoda, Oniscidea, Trichoniscidae). Fragmenta Entomologica, 21 (1): 9-16.
• Armas, L. F. De & G. Alayón Garcia, 1984. Sinopsis de los aracnidos cavernicolas de Cuba (excepto acaros). Zoologie, 276: 1-25.
• Aydın, G. & İ. Şen, 2020. Determination of arthropod biodiversity and some ecological parameters of Erdal Şekeroğlu (Isparta, Turkey) and Kadıini (Antalya, Turkey) cave ecosystems with evaluation of usability of insects in cave mapping. Turkish Journal of Entomology, 44 (4): 539-557.
• Barnes, J. K., M. E. Slay & S. J. Taylor, 2009. Adult Diptera from Ozark Caves. Proceedings of the Entomological Society of Washington, 111 (2): 335-353.
• Barr, T. C., 1968. “Cave Ecology and the Evolution of Troglobites, 35-102”. In: Evolutionary Biology, Vol. 2 (Eds. T. Dobzhansky, M. K. Hecht & W. C. Steere) Springer, Boston, MA, USA, 452 pp.
• Bilgin, S., O. Özgül & H. Koç, 2015. Türkiye için beş yeni kayıt ile Sündiken Dağları (Eskişehir) Limoniidae (Diptera) faunasına katkılar. Türkiye Entomoloji Bülteni, 5 (1): 3-9 (in Turkish with abstract in English).
• Bordoni, A., 2010. Catalogue of the Staphylinidae of Cyprus and Asia Minor (Coleoptera). Fragmenta Entomologica, 42 (1): 35-348.
• Bozcu, A., 2007. Zindan mağarası ve çevresinin jeolojik -arkeolojik özellikleri. Fen Bilimleri Enstitüsü Dergisi, 11 (1): 54-63 (in Turkish with abstract in English).
• Brignoli, P. M., 1972. Terzo contributo alla conoscenza dei ragni cavernicola di Turchia (Araneae). Fragmenta Entomologica, 8 (3): 161-190.
• Brignoli, P. M., 1978. Ragni di Turchia V. Specie nuove o interessanti, cavernicole ed epigee, di varie famiglie (Araneae). Revue Suisse de Zoologie, 85 (3): 461-541.
• Cooper, S., J. Bradbury, K. M. Saint, R. Leys, A. D. Austin & W. F. Humphreys, 2007. Subterranean archipelago in the Australian arid zone: mitochondrial DNA phylogeography of amphipods from central Western Australia. Molecular Ecology, 16 (7): 1533-1544.
• Corallini, C. & O. Marchetti, 2016. Parasitic infestation in a female of Micropterna nycterobia McLachlan 1875 (Trichoptera, Limnephilidae) found in Monte Cucco cave (Central Italy). Zoosymposia, 10 (1): 165-171.
• Čuchta, P., D. Miklisová & Ľ. Kováč, 2019. The succession of soil Collembola communities in spruce forests of the High Tatra Mountains five years after a windthrow and clear-cut logging. Forest Ecology and Management, 433: 504-513.
• Dániel, W. & T. G. Nándor, 2012. Eco-faunistic study on the Collembola fauna in the Vasvár-Nagymákfa area (Őrség, Western Hungary). Natura Somogyiensis, 22: 39-52.
• Dányi, L. & G. Traser, 2008. An annotated checklist of the springtail fauna of Hungary (Hexapoda: Collembola). Opuscula Zoologica Instituti Zoosystematici et Oecologici Universitatis Budapestinensis, 38: 3-82.
• Darılmaz, M. & S. Kıyak, 2006. A contribution to the knowledge of the Turkish water beetles fauna (Coleoptera). Munis Entomology & Zoology, 1 (1): 129-144.
• Deltshev, C., 2008. Faunistic diversity and zoogeography of cave-dwelling spiders on the Balkan Peninsula. Advances in Arachnology and Developmental Biology, 12: 327-348.
• Di Russo, C., M. Rampini & I. Landeck, 2007. The cave crickets of northeast Turkey and trans Caucasian regions, with descriptions of two new species of the genera Dolichopoda and Troglophilus (Orthoptera, Rhaphidophoridae). Journal of Orthoptera Research, 16 (1): 67-76.
• Driauach, O. & B. Belqat, 2016. Additions to the Limoniidae and Pediciidae Fauna of Morocco, with an updated checklist (Diptera, Tipuloidea). ZooKeys, 563: 129-146.
• Ellis, W. N., 1974. The spring fauna of Collembola (Insecta) from Rhodos, with descriptions of some new taxa. Beaufortia, 292 (22): 105-152.
• Enghoff, H., 2006. The millipedes of Turkey (Diplopoda). Steenstrupia, 29 (2): 175-198.
• Erguvanlı, K., 1975. Türkiye’de Miralay Dr. Abdullah Bey’in jeoloji öğretiminde ve araştırmalarında öncülüğü. Türk Mikrobiyoloji Cemiyeti Dergisi, 5: 19-28 (in Turkish with abstract in English).
• Fidan, E. C., Ş. Ümit & H. Çalışkan, 2014. Second record of rare cave-dwelling beetle, Choleva (Cholevopsis) bertiae Giachino & Vailati, 2000 (Coleoptera: Leiodidae), from Tütüncüini and Sarikaya caves in Eskişehir. Hacettepe Journal of Biology and Chemistry, 42 (4): 473-477.
• Folsom, J. W., 1932. Hawaiian Collembola. Proceeding of Society of Hawaiian Entomology, 8 (1): 51-92. Gasparo, F., 2007. Note su Tegenaria percuriosa Brignoli, 1972, con descrizione del maschio (Araneae, Agelenidae). Atti e Memorie della Commissione Grotte “E. Boegan”, 41: 95-103.
• Gibert, J. & L. Deharveng, 2002. Subterranean Ecosystems: A Truncated Functional Biodiversity. BioScience, 52 (6): 473-481.
• Hüppop, K., 2012. "Adaptation to Low Food, 1-9" In: Encyclopedia of Caves. 2nd Edition (Eds. W. B. White & D. C. Culver). Elsevier, 966 pp.
• Ibrahimi, H., A. Gashi & L. Grapci-Kotori, 2013. First records of the genus Micropterna Stein, 1873 (Insecta: Trichoptera) in Kosovo with distributional and ecological notes. Natura Croatica, 22 (1): 147-155.
• Juan, C., M. T. Guzik, D. Jaume & S. J. Cooper, 2010. Evolution in caves: Darwin’s ‘wrecks of ancient life in the molecular era. Molecular Ecology, 19 (18): 3865-3880.
• Juberthie, C. & V. Decu, 1994. Encyclopaedia Biospeologica. Société de Biospéologie, France, 834 pp. Karadem, A., 2011. Cr-39 dedektörleri ile mağaralarda radon konsantrasyonu ölçümleri. Süleyman Demirel Üniversitesi, (Unpublished) Yüksek Lisans Tezi, Isparta, 65 s (in Turkish with abstract in English).
• Karaman, B., 2007. Trabzon İli Sucul Coleoptera (Insecta) Faunası. Gazi Üniversitesi, (Unpublished) Yüksek Lisans Tezi, Ankara, 72 s.
• Kaya, D. & S. Mitchell, 1985. The Sanctuary of the God Eurymedon at Tymbriada in Pisidia. Anatolian Studies, 35: 39-55.
• Kaya, R., K. Kunt, Y. Marusik & İ. Uğurtaş, 2010. A new species of Tegenaria Latreille, 1804 (Araneae, Agelenidae) from Turkey. ZooKeys, 51: 1-16.
• Kaya, R. S. & İ. H. Uğurtaş, 2007. A faunistic study on spiders (Araneae) of Terzioğlu Island (Uluabat Lake, Bursa). Journal of Biological and Environmental Sciences, 1 (1): 31-36.
• Kıyak, S., M. C. Darilmaz, A. Salur & S. Canbulat, 2007. Diving beetles (Coleoptera: Dytiscidae, Noteridae) of the southwestern Anatolian region of Turkey. Munis Entomology & Zoology, 2 (1): 103-114.
• Komonen, A. & S. Kataja-Aho, 2017. Springtails (Collembola) in meadows, pastures and road verges in Central Finland. Entomologica Fennica, 28 (3): 157-163.
• Kopar, İ., 2009. Aladağlar’da [Orta Toroslar (Yahyalı-Kayseri)] iki fosil mağara: Zindan-i Köşk-1 ve Zindan-i Köşk - 2 mağaraları. Türk Coğrafya Dergisi, 53: 69-83 (in Turkish with abstract in English).
• Kováč, Ľ., A. Mock, P. Ľuptáčik, V. Košel, P. Fenďa, J. Svatoň & P. Mašán, 2005b. “Terrestrial Arthropods of the Domica Cave System and the Ardovská Cave (Slovak Karst) - Principal Microhabitats and Diversity, 61-70”. In: Contributions to Soil Zoology in Central Europe I (Eds. K. Tajovský, J. Schlaghamerský & V. Pižl). České Budějovice, Czech Republic, 221 pp.
• Kováč, L., N. Kostúrová & D. Miklisová, 2005a. Comparison of collembolan assemblages (Hexapoda, Collembola) of thermophilous oak woods and Pinus nigra plantations in the Slovak Karst (Slovakia). Pedobiologia, 49 (1): 29-40.
• Kunt, K. B., M. Elverici, E. A. Yağmur, & R. S. Özkütük, 2019. Kut gen. nov., a new troglomorphic spider genus from Turkey (Araneae, Dysderidae). Subterranean Biology, 32: 95-109.
• Kunt, B. K., A. E. Yağmur, S. Özkütük & S. Anlaş, 2010. Checklist of the cave dwelling invertebrates (Animalia) of Turkey. Biological Diversity and Conservation, 3 (2): 26-41.
• Malicky, H. & G. Winkler, 1974. Untersuchungen über die Höhlenimmigration von Micropterna nycterobia (Trichoptera, Limnephilidae). Oecologia, 15 (4): 375-382.
• Mammola, S., P. Cardoso, C. Ribera, M. Pavlek & M. Isaia, 2018. A synthesis on cave-dwelling spiders in Europe. Journal of Zoological Systematics and Evolutionary Research, 56 (3): 301-316.
• Manenti, R., E. Lunghi & G. F. Ficetola, 2015. The distribution of cave twilight-zone spiders depends on microclimatic features and trophic supply. Invertebrate Biology, 134 (3): 242-251.
• Marusik, Y., R. Özkütük & K. B. Kunt, 2012. Spiders (Araneae) new to the fauna of Turkey. 10. Two new species records of Tetragnathidae. Life Sciences and Biotechnology, 2 (2): 69-73.
• Moretti, G. & F. Gianotti, 1964. Considerazioni biogeografiche sul popolamento cavernicolo dei Tricotteri. Archivio botanico e biogeografico italiano, (IV serie), 9 (4): 341-348.
• Nazik, L. & S. Bayarı, 2018. Mağara zengini ülke: Türkiye. Mavi Gezegen, 24: 7-19 (in Turkish with abstract in English). Nazik, L., K. Törk, K. Tuncer, E. Özel, H. İnan & F. Savaş, 2005. “Türkiye mağaraları, 31-46”. Ulusal Mağara Günleri Sempozyumu Bildiriler Kitabı (24-26 Haziran 2005, Beyşehir, Konya), Türkiye Tabiat Koruma Derneği, 46 s (in Turkish).
• Özata, M. A., H. Sevgili & I. J. Kaprus, 2017. New records of springtail fauna (Hexapoda: Collembola: Entomobryomorpha) from Ordu Province in Turkey. Turkish Journal of Zoology, 41 (1): 24-32.
• Özgenç, F., 2011. Çorum İli Dytiscidae (Coleoptera) Familyası Türlerinin Erkek Genitalinin Araştırılması. Gazi Üniversitesi, (Unpublished) Yüksek Lisans Tezi, Ankara, 71 s (in Turkish with abstract in English).
• Özgül, O., H. Koç, M. Barlas & A. Tonguç, 2009. Güneybatı Anadolu Bölgesi Limoniidae (Diptera, Nematocera) faunası. Selçuk Üniversitesi Fen Fakültesi Fen Dergisi, 2 (33): 61-66 (in Turkish with abstract in English).
• Page, T. J., W. F. Humphreys, & J. M. Hughes, 2008. Shrimps down under: evolutionary relationships of subterranean crustaceans from Western Australia (Decapoda: Atyidae: Stygiocaris). Plos One, 3 (2): e1618.
• Palmer, M. W., 1991. Estimating species richness: the second-order jackknife reconsidered. Ecology, 72 (4): 1512-1513. Parimuchová, A., L. P. Dušátková, L. Kováč, T. Macháčková, O. Slabý & S. Pekár, 2021. The food web in a subterranean ecosystem is driven by intraguild predation. Scientific Reports, 11 (1): 1-11.
• Peck, S. B., A. E. Ruiz-Baliú & G. F. Garcés González, 1998. The cave-inhabiting beetles of Cuba (Insecta: Coleoptera): Diversity, distribution and ecology. Journal of Cave and Karst Studies, 60 (3): 156-166.
• Popa, I., 2012. Two new records of springtails (Hexapoda: Collembola) for the Romanian fauna - Maramureş county. Travaux de l’Institut de Speologie “Emile Racovitza”, 51: 73-79.
• Popa, I. & V. Šustr, 2017. First record of Lipothrix italica (Cassagnau, 1968) (Hexapoda : Collembola) in Romania. Travaux de l’Institut de Speologie “Emile Racovitza”, 56: 51-55.
• Porco, D., M. Potapov, A. Bedos, G. Busmachiu, W. M. Weiner, S. Hamra-Kroua & L. Deharveng, 2012. Cryptic diversity in the ubiquist species Parisotoma notabilis (Collembola, Isotomidae): A Long-Used Chimeric Species? Plos One, 7 (9): e46056.
• Potapov, M., 2001. Synopses on Palaearctic Collembola Pt 3: lsotomidae. Staatliches Museum für Naturkunde, Görlitz, 603 pp.
• Poulson, T. L. & W. B. White, 1969. The cave environment. Science, 165 (3897): 971-981.
• Prokopenko, E. V., 2019. The first record of Lepthyphantes centromeroides Kulczyński, 1914 (Aranei: Linyphiidae) from the Ukrainian Carpathians. Kavkazskij Entomologiceskij Bulleten, 15 (1): 23-24.
• Rad, A. A. & K. Morteza, 2015. The first study of Isotomidae fauna (Collembola: Apterygota) in Lorestan Province, Western Iran, with new records for Iranian fauna. Journal of Biodiversity and Environmental Sciences (JBES), 7 (1): 128-133.
• Rampini, M. & C. Di Russo, 2003. Una nuova specie di Troglophilus di Turchia (Orthoptera, Rhaphidophoridae). Fragmenta Entomologica, 34 (2): 235-247.
• Raschmanová, N., M. Žurovcová, Ľ. Kováč, L. Paučulová, V. Šustr, A. Jarošová & D. Chundelová, 2017. The cold-adapted population of Folsomia manolachei (Hexapoda, Collembola) from a glaciated karst doline of Central Europe: evidence for a cryptic species? Journal of Zoological Systematics and Evolutionary Research, 55 (1): 19-28.
• Rendoš, M., N. Raschmanová, Ľ. Kováč, D. Miklisová, A. Mock & P. Ľuptáčik, 2016. Organic carbon content and temperature as substantial factors affecting diversity and vertical distribution of Collembola on forested scree slopes. European Journal of Soil Biology, 75: 180-187.
• Romero, A., 2009. Cave Biology: Life in Darkness Cave Biology. Cambridge University Press, Cambridge. 306 pp.
• Ruffo, S., 1957. Le attuali conoscenze sulla fauna cavernicola della Regione Pugliese. MemBiogeogr Adriat, 3:1-43.
• Scheers, K. & S. Thant, 2017. Agabus didymus (Olivier, 1795) and A. dilatatus (Brullé, 1832), two species new to the fauna of Croatia with notes on the ecology and distribution of both species (Coleoptera: Dytiscidae). Bulletin de la Société royale belge d’Entomologie/Bulletin van de Koninklijke Belgische Vereniging voor Entomologie, 153 (1): 54-58.
• Sevgili, H. & M. A. Özata, 2014. Checklist of the springtails (Hexapoda: Collembola) of Turkey. Zoology in the Middle East, 60 (2): 162-168.
• Shayanmehr, M., E. Yahyapour, M. Kahrarian & E. Y. Lafooraki, 2013. An introduction to Iranian Collembola (Hexapoda): an update to the species list. ZooKeys, 335: 69-83.
• Sket, B., 2008. Can we agree on an ecological classification of subterranean animals? Journal of Natural History, 42 (21-22): 1549-1563.
• Taylan, M. S., 2011. Türkiye Mağara Çekirgeleri (Orthoptera, Rhaphidophoridae): Morfolojik ve Moleküler Veriler Işığında Taksonomi, Filogeni ve Biyocoğrafyaları. Akdeniz Üniversitesi, (Unpublished) Doktora Tezi, Antalya, 203 s (in Turkish with abstract in English).
• Trajano, E., 2012. "Ecological Classification of Subterranean Organisms, 275-277". In: Encyclopedia of Caves (Eds. W. B. White & D. C. Culver). Elsevier, Amsterdam, 945 pp.
• Vafaei, R., M.C. Darilmaz, E. Nazari, U. Incekara & N. Piazak, 2009. Contributions to the knowledge of Iranian aquatic coleoptera fauna (Dytiscidae, Gyrinidae, Helophoridae and Hydrophilidae) with new records and notes on the rare species Coleostoma Transcaspicum Reitter, 1906. Acta Entomologica Serbica, 14 (1): 101-107.
• Von Saltzwedel, H., S. Scheu & I. Schaefer, 2017. Genetic structure and distribution of Parisotoma notabilis (Collembola) in Europe: Cryptic diversity, split of lineages and colonization patterns. Plos One, 12 (2): e0170909.
• Vrenozi, B. & P. Jäger, 2012. A faunistic study on ground-dwelling spiders (Araneae) in the Tirana district, Albania. Arachnologische Mitteilungen, 44 (7): 81-87.
• Yamaç, A., É. Gilli, E. Tok & K. Törk, 2021. Caves and Karst of Turkey-Vol. 1: History, Archaeology and Caves. Springer, Switzerland AG, 108 pp.
• Zacharda, M., D. Fong, H. H. Hobbs III, E. Piva, M. E. Slay & S. J. Taylor, 2010. A review of the genus Traegaardhia (Acari, Prostigmata, Rhagidiidae) with descriptions of new species and a key to species. Zootaxa, 2474 (1): 1-64.