Document Type : Original Research Paper

Authors

1 Department of Earth Sciences, Faculty of Sciences, University of Kurdistan, Sanandaj, Iran

2 Geological Survey of Iran, West Territory, Sanandaj, Iran

Abstract

Kraftu cave, 67 km northwest of Divandareh in Kurdistan province, includes four floors. The bottom of the second floor, in the bat hall, is covered by thick guano deposits. SEM–EDX analyses of the guano deposits showed secondary sulfate (gypsum, cesanite), phosphate (phosphammite, brushite, taranakite, francoanellite, whitlockite, leucophosphite, spheniscidite, pyrocoproite), and nitrate (urea, niter) minerals, along with microorganisms and chitin. Occurrence of these minerals is due to changes in the pH (from acidic to alkaline) and moisture (wet and dry conditions) in the presence of microorganisms. Bat guano has accumulated in Karaftu cave during three different paleoclimate conditions, from base to top, including dry, wet, and dry conditions. A comparison between distributions of secondary minerals and Ce-anomalies along the profile represents that taranakite only forms in wet conditions, but whitlockite, urea, and cesanite only occur in dry ones. Therefore, they are significant indicators of climate in the geologic record, but other minerals, because they can be in both conditions, don't be so.Various reactions between the solutions derived from guano with substrate have resulted in phosphatization and dolomitization of bedrock. The abundance of chitin in the Karaftu cave guano deposits indicates that they are feces of insectivorous bats.

Keywords

Main Subjects

Addesso, R., Gonzalez-Pimentel, J.L., D'Angeli, I.M., De Waele, J., Saiz-Jimenez, C., Jurado, V., Miller, A.Z., Cubero, B., Vigliotta, G., and Baldantoni, D., 2021. Microbial Community Characterizing Vermiculations from Karst Caves and Its Role in Their Formation. Microbial Ecology, 81:884–896.  DOI: 10.1007/s00248-020-01623-5.
Adetutu, E.M., and Ball, A.S., 2014. Microbial diversity and activity in caves. Microbiology Australia, 35(4): 192-194. DOI: 10.1071/MA14062. 
Albuquerque, A.R.L., Angélica, R.S., Gonçalves, D.F., and Paz, S.P.A., 2018. Phosphate speleothems in caves developed in iron ores and laterites of the Carajás Mineral Province (Brazil) and a new occurrence of spheniscidite. International Journal of Speleology, 47: 53-67. DOI:10.5038/1827-806X.47.1. 2135.
Armstrong, P., Beard, J., Bonilla, L., Arboleda, N., Lindsley, M., Chae, S., Castillo, D., Nuñez, R., Chiller, T., De Perio, M., Pimentel, R., and Vallabhaneni, S., 2018. Outbreak of severe histoplasmosis amongtunnel workers Dominican Republic, 2015. Clin Infect Dis, 66: 1550- 1557. DOI: 10.1093/cid/cix1067.
Audra, P., Bosák, P., Gázquez, F., Cailhol, D., Skála, R., Lisá, L., Jonášová, Š., Frumkin, A., Knez, M., Slabe, T., Zupan Hajna, N., and Al-Farraj, A., 2017. Bat urea-derived minerals in arid environment. First identification of allantoin, C4H6N4O3, in Kahf Kharrat Najem Cave, United Arab Emirates. International Journal of Speleology, 46: 81-92. DOI: 10.5038/1827-806X.46.1.2001. 
Audra, P., De Waele, J., Bentaleb, I., Chroňáková, A., Krištůfek, V., D’Angeli, I.M., Carbone, C., Madonia, G., Vattano, M., Scopelliti, G., Cailhol, D., Vanara, N., Temovski, M., Bigot, J.-Y., Nobécourt, J.-C., Galli, E., Rull, F., and Sanz-Arranz, A., 2019. Guano-related phosphate-rich minerals in European caves. International Journal of Speleology, 48: 75-105. DOI: 10.5038/1827-806X.48.1.2252.
Audra, P., Heresanu, V., Barriquand, L., Boutchich, M.E.K., Jaillet, S., Pons-Branchu, E., Bosák, P., Cheng, H., Edwards, R.L., and Renda, M., 2021. Bat guano minerals and mineralization processes in chameau cave, Eastern Morocco. International Journal of Speleology, 50: 91-109. DOI: 10.5038/1827-806X.50.1.2374.
Back, M.E., and Mandarino, J.A., 2008. Fleischer’s glossary of mineral species. Tucson. The Mineralogical Record, 344 p. ISSN: 1062-3531.
Batina, M.C., and Reese, C.A., 2011. A Holocene pollen record recovered from a guano deposit: Round Spring Cavern, Missouri, USA. Boreas, 40: 332-341. DOI: 10.1111/j.1502-3885.2010.00186.x.
Bau, M., and Dulski, P., 1996. Distribution of yttrium and rare-earth elements in the Penge and Kuruman iron-formations, Transvaal Supergroup, South Africa. Precambrian Research, 79: 37-55.
Benda, P., Faizolâhi, K. Andreas, M., Obuch, J., Reiter, A., Ševčík, M., Uhrin, M., Vallo, P., and Ashrafi, S., 2012. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 10. Bat fauna of Iran. Acta Societatis Zoologicae Bohemicae, 76: 163–582. ISSN: 1211-376X.
Bogdan, P., Onac, B.P., and Forti, P., 2011. Minerogenetic mechanisms occurring in the cave environment: an overview. International Journal of Speleology, 40: 79-98. DOI: 10.5038/1827-806X.40.2.1.
Bottrell, S., 2003. Microbial processes incaves. In: J. Gunn (ed.), Encyclopedia of caves and karst science. Fitzroy Dearborn, New York, 69: 505-506. ISBN: 978-0-12-814124-3.
Bozorgnia, F., 1965. Qom Formation stratigraphy of the Central Basin of Iran and its intercontinental position. Bulletin of the Iranian Petroleum Institute, 24: 69–75.
Bridge, P.J., 1973. Urea, a new mineral, and neotype phosphammite from Western Australia. Mineralogical Magazine, 39: 346–348. DOI: 10.1180/minmag.1973.039.303.11.
Cuffey, K.M., and Clow, G.D., 1997. Clow temperature accumulation and ice sheet elevation in central Greenland through the last deglacial transition. Journal of Geophysical Research, 102: 26383- 26396. DOI: 10.1029/96JC03981.
D’Angeli, I.M., Carbone, C., Nagostinis, M., Parise, M., Vattano, M., Madonia, G., and De Waele, J., 2018. New insights on secondary minerals from Italian sulfuric acid caves. International Journal of Speleology, 47: 271-291. DOI: 10.5038/1827-806X.47.3.2175.
Dana, E.S., 1997. Dana’s system of mineralogy. 8th ed., New York, Wiley, 807 p. ISBN: 0471193100.
De Waele, J., Audra, P., Madonia, G., Vattano, M., Plan, L., D’Angeli, I.M., Bigot, J.-Y., and Nobécourt, J.C., 2016. Sulfuric acid speleogenesis (SAS) close to the water table: Examples from southern France, Austria, and Sicily. Geomorphology, 253: 452-467. DOI: 10.1016/j.geomorph.2015.10.019.
Dimkić, I., Fira, D., Janakiev, T., Kabić, J., Stupar, M., Nenadić, M., Unković, N., and Grbić, M.L., 2021. The microbiome of bat guano: for what is this knowledge important? Applied microbiology and biotechnology, 105: 1407–1419. DOI: 10.1007/s00253-021-11143-y.
Dove, S., Ortiz, J.C., Enriquez, S., Fine, M., Fisher, P., Iglesias-Prieto, R., Thornhill, D., and Hoegh-Guldberg, O., 2006. Response of holosymbiont pigments from the scleractinian coral Montipora monasteriata to short-term heat stress. Limnology and Oceanography, 51: 1149–1158. DOI: 10.4319/lo.2006.51.2.1149.
Dumitraş, D.G., Hatert, F., Bilal, E., and Marincea, Ş., 2004. Gypsum and bassanite in the bat guano deposit from the "dry" Cioclovina cave (Sureanu Mts., Romania). Romanian Journal of Mineral Deposits, 81: 84-87.
Dumitraş, D., and Marincea, Ş., 2008. Apatite-(CaOH) in the fossil bat guano deposit from the “Dry” Cioclovina Cave, Şureanu Mountains, Romania. Canadian Mineralogist, 46: 431–445. DOI: 10.3749/canmin.46.2.431.
Dumitraş, D., and Marincea, Ş., 2021. Sequential dehydration of the phosphate–sulfate association from Gura Dobrogei Cave, Dobrogea, Romania. European Journal Mineralogy, 33: 329–340. DOI: 10.5194/ejm-33-329-2021.
Falasco, E., Ector, L., Isaia, M., Wetzel, C.E., Hoffmann, L., and Bona, F., 2014. Diatom flora in subterranean ecosystems: a review. International Journal of Speleology, 43: 231-251. DOI: 10.5038/1827-806X.43.3.1.
Figueira, R.L., Coimbra Horbe, A.M., Herrera Aragón, F.F., and Gonçalves, D.F., 2019. Exotic sulphate and phosphate speleothems in caves from eastern Amazonia (Carajás, Brazil): Crystallographic and chemical insights. Journal of South American Earth Sciences, 90: 412- 422. DOI: 10.1016/j.jsames.2018.12.007.
Forbes, M.S., and Bestland, E.A., 2006. Guano-derived deposits within the sandy cave fills of Naracoorte, South Australia. Journal of Palaeontology, 30:129-146. DOI: 10.1080/03115510609506859.
Forray, F.L., Onac, B.P., Tanţău, I., Wynn, J.G., Tămaş, T., Coroiu, I., and Giurgiu, A.M., 2015. A Late Holocene environmental history of a bat guano deposit from Romania: an isotopic, pollen and microcharcoal study. Quaternary Science Reviews, 127: 141-154. DOI: 10.1016/j.quascirev.2015.05.022.
Forti, P., 2001. Biogenic speleothems: an overview. International Journal of Speleology, 30: 39-56. DOI: 10.5038/1827-806X.30.1.4.
Forti, P., 2010. Genesis and evolution of the caves in the Naica Mine (Chihuahua, Mexico). Zeitschrift für Geomorphologie, Supplementary Issues, 54: 115-135. DOI: 10.1127/0372-8854/2010/0054S2-0007.
Forti, P., Galli, E., Rossi, A., Pint, J., and Pint, S., 2004. Ghar Al Hibashi Lava Tube: The Richest Site in Saudi Arabia for Cave Minerals. Acta Carsologica, 33: 189- 205. DOI: 10.3986/ac.v33i2.299.
Frost, R., and Palmer, S.J., 2011. Thermal stability of the ‘cave’ mineral brushite CaHPO4•2H2O – Mechanism of formation and decomposition. Thermochimica Acta, 521: 14-17. DOI: 10.1016/j.tca.2011.03.035.
Frost, R.L., Xi, Y., and Palmer, S.J., 2011. Are the ‘cave’ minerals archerite (K,NH4)H2PO4 and biphosphammite (K,NH4)H2PO4 Identical? A molecular structural study. Journal of Molecular Structure, 1001: 49-55. DOI: 10.1016/j.molstruc.2011.06.015.
Frost, R.L., Xi, Y., Scholz, R., Belotti, F.M., and Filho, M.C., 2013. Infrared and Raman Spectroscopic Characterization of the Phosphate Mineral Leucophosphite K(Fe3+)2(PO4)2(OH).2(H2O). Spectroscopy Letters, An International Journal for Rapid Communication, 46: 415-420, DOI: 10.1080/00387010.2012.733478.
García-Ruiz, J.M., Villasuso, R., Ayopa, C., Canals, A., and Otálora, F., 2007. The formation of natural gypsum megacrystals in Naica, Mexico. Geology, 35: 327-330. DOI: 10.1130/G23393A.1.
Giurgiu, A., and Tămaş, T., 2013. Mineralogical data on bat guano deposits from three Romanian caves. Studia UBB Geologia, 58: 13-18. DOI: 10.5038/1937-8602.58.2.2.
Giurgiu, A.M., Onac, B.P., Tămaş, T., and Fornós. J.J., 2013. Evolution of guano under different environmental conditions. A Mineralogical Approach. School of Geosciences Faculty and Staff Publications, ICS Proceedings, 483-485.
Hess, W.H., 1990. The Origin of Nitrates in Cavern Earths. The Journal of Geology, 8: 129- 134. URL:https://www.jstor.org/stable/30055739.
Hill, C.A., 1981. Origin of Cave Saltpeter. The Journal of Geology, 89: 252-259.
Hill, C.A., and Forti, P., 1997. Cave minerals of the world. 2nd ed., Huntsville, National Speleological Society, 464 p. ISBN: 1-879961-07-5.
Hosono, T., Uchida, E., Suda, C., Ueno, A., and Nakagawa, T., 2006. Salt weathering of sandstone at the Angkor monuments, Cambodia: identification of the origins of salts using sulfur and strontium isotopes. Journal of Archaeological Science, 33: 1541–1551. DOI: 10.1016/j.jas.2006.01.018.
Johnston, V.E., McDermott, F., and Tămaş, T., 2010. A radiocarbon dated bat guano deposit from NW Romania: Implications for the timing of the Little Ice Age and Medieval Climate Anomaly. Palaeogeography, Palaeoclimatology, Palaeoecology, 291: 217-227. DOI: 10.1016/j.palaeo.2010.02.031.
Kaya, M., Seyyar, O., Baran, T., and Turkes, T., 2014. Bat guano as new and attractive chitin and chitosan source. Frontiers in Zoology, 11: 59-66. DOI: 10.1186/s12983-014-0059-8.
Kong, D.-Y., Lee, S.-J., Jun, C.-P., and Kim, Y.-K., 2012. Mineralogy of guano distributed in the limestone cave in Korea (Gossi Cave, Baekrong Cave, and Sungryu Cave). Journal of the Mineralogical Society of Korea, 25: 131- 141. DOI: 10.9727/jmsk.2012.25.3.131.
Kumaresan, D., Hillebrand-Voiculescu, A.M., Wischer, D., Stephenson, J., Chen, Y., and Murrell, J.C., 2015. Microbial life in unusual cave ecosystems sustained by chemosynthetic primary production. In: A.S. Engel (ed.), Microbial Life of Cave Systems. Hubert & Co. GmbH & Co. KG, Göttingen, 215- 230 pp. DOI: 10.1515/9783110339888.
Lavoie, K.H., 2015. A grand, gloomy, and peculiar place: microbiology in the Mammoth Cave region. In: A.S. Engel (ed.), Life in extreme environments: microbial life of cave systems. DeGruyter, Berlin, 47- 78 pp.
Lundberg, J., and McFarlane, D.A., 2021. The impact of burning on the structure and mineral composition of bat guano. International Journal of Speleology, 50: 189-202. DOI: 10.5038/1827-806X.50.2.2387.
Maher, Jr,L., 2006. Environmental information from guano palynology of insectivorous bats of the central part of the United States of America. Palaeogeography, Palaeoclimatology, Palaeoecology, 237: 19–31. DOI: 10.1016/j.palaeo. 2005.11.026.
Marincea, S., Dumitraş, D.-G., Dianocu, G., and Bilal, E., 2004. Hydroxylapatite, brushite and ardealite in the bat guano deposit form Pestera Mare de la Meresti, Persani Mountains, Romania. Neues Jahrbuch für Mineralogie- Monatshefte, 10: 464–488.
Miscoe, L.H., Johansen, J., Vaccarino, M., Pietrasiak, N., and Sherwood, A., 2016a. Novel cyanobacteria from caves on Kauai, Hawaii. Bibliotheca Phycologica, 120: 75- 152. ISBN: 978-3-443-60047-1.
Miscoe, L.H., Johansen, J., Kociolek, J., Lowe, R., Vaccarino, M.A., Pietrasiak, N., and Sherwood, A., 2016b. The diatom flora and cyanobacteria from caves on Kauai, Hawaii. Bibliotheca Phycologica, 120: 3-74. ISBN: 978-3-443-60047-1.
Najafi, N., Sharifi, M., and Akmali, V., 2018. A review of Rhinolophus mehelyi in Iran with new distributional records.Iranian Journal of Animal Biosystematics (IJAB), 14: 43- 54. DOI: 10.22067/ijab.v14i1.73876.
Newman, M.M., Kloepper, L.N., Duncan, M., McInroy, J.A., and Kloepper, J.W., 2018. Variation in Bat Guano Bacterial Community Composition With Depth. Frontiers in Microbiology, 9 (Article 914): 1-9. DOI:10.3389/fmicb.2018.00914.
Northup, D.E., and Lavoie, K.H., 2001. Geomicrobiology of caves: a review. Geomicrobiology Journal, 18: 199–222. DOI: 10.1080/01490450152467750.
Northup, D.E., Lavoie, K., and Mallory, L., 1997. Microbes in Caves. NSS News, 506-509 pp.
Onac, B.P., 2012. Minerals. In: D.C. Culver and W.B. White (eds.), Encyclopedia of Caves. Academic Press, 5: 22-41. DOI:10.5242/iamg.2011.0074.
Onac B.P., 2019. Cave discovered by mining activities and mined caves. In: G.M.L. Ponta and B.P. Onac (eds.), Cave and karst systems of Romania. Springer International, Cham, 475-483 pp. DOI: 10.1007/978-3-319-90747-5_54.
Onac, B.P., and Forti, P., 2011. Minerogenetic mechanisms occurring in the cave environment: an overview. International Journal of Speleology, 40: 79-98. DOI: 10.5038/1827-806X.40.2.1.
Onac, B.P., and Vereş, D.Ş., 2003. Sequence of secondary phosphates deposition in a karst environment: evidence from Măgurici Cave (Romania). European Journal of Mineralogy, 15: 741-745. DOI: 10.1127/0935-1221/2003/0015-0741.
Onac, B.P., and White, W.B., 2003. First reported sedimentary occurrence of berlinite (AlPO4) in phosphate-bearing sediments from Cioclovina Cave, Romania. American Mineralogist, 88: 1395-1397. DOI: 10.2138/am-2003-8-925.
Onac, B.P., Mylroie, J.E., and White, W.B., 2001. Mineralogy of cave deposits on San Salvador Island, Bahamas. Carbonates and Evaporites, 16: 8-16. 
Onac, B.P., Effenberger, H.S., and Breban, R.C., 2007. High-temperature and “exotic” minerals from the Cioclovina Cave, Romania: a review. Studia UBB, Geologia, 52: 1-7. DOI: 10.5038/1937-8602.52.2.1.
Ortiz, M., Legatzki, A., Neilson, J.W., Fryslie, B., Nelson, W.M., Wing, R.A., Soderlund, C.A., Pryor, B.M., and Maier, R.M., 2014. Making a living while starving in the dark: metagenomic insights into the energy dynamics of a carbonate cave. The ISME Journal, 8: 478−491. DOI: 10.1038/ismej.2013.159.
Pohlman, J.W., Iliffe, T.M., and Cifuentes, L.A., 1997. A stable isotope study of organic cycling and the ecology of an anchialine cave ecosystem. Marine Ecology Progress Series, 155:17–27.
Puşcaş, C.M., Kristaly, F., Stremţan, C.C., Onac, B.P., and Effenberger, H.S., 2014. Stability of cave phosphates: Case study from Liliecilor Cave (Trascău Mountains, Romania): Neues Jahrbuch Mineralogie-Abhandlungen. Journal of Mineralogy and Geochemistry, 191: 157–168. DOI: 10.1127/0077-7757/2014/0254.
Queffelec, A., Bertran, P., Bos, T., and Lemée, L., 2018. Mineralogical and organic study of bat and chough guano: implications for guano identification in ancient context. Journal of Cave and Karst Studies, 80: 1-17. DOI: 10.4311/2017ES0102.
Raabe, D., Romano, P., Sachs, C., Fabritius, H., Sawalmih, A., Yi, S.-B., Servos, G., and Hartwig, H.G., 2006. Microstructure and crystallographic texture of the chitin–protein network in the biological composite material of the exoskeleton of the lobster Homarus americanus. Materials Science and Engineering A, 421: 143–153. DOI: 10.1016/j.msea.2005.09.115.
Romero, A., 2009. Cave biology: Life in darkness. 1st ed., New York, Cambridge University Press, 306 p. ISBN-13: 978-0521535533. 
Sakoui, S., Derdak, R., Boutaina, A., Serrano, A., Soukri, A., and El Khalfi, B., 2020. The Life hidden inside caves.Ecological and economic importance of bat guano. International Journal of Ecology, 7 p. DOI: 10.1155/2020/9872532.
Schnug, E., Jacobs, F., and Stöven, K., 2018. Guano: the white gold of the seabirds. Intech Open, 81- 100 pp. DOI: 10.5772/intechopen.79501.
Schulz, H.N., and Schulz, H.D., 2005. Large sulfur bacteria and the formation of phosphorite. Science, 307: 416–418. DOI: 10.1126/science.1103096.
Snow, M.R., Pring, A., and Allen, N., 2014. Minerals of the Wooltana Cave, Flinders Ranges, South Australia. Transactions of the Royal Society of South Australia, 138: 214-230. DOI: 10.1080/03721426.2014.11649009.
Stöcklin, J., 1968. Structural history and tectonics of Iran: a review. American Association of Petroleum Geologists Bulletin, 52: 1229–1258. DOI: 10.1306/5D25C4A5-16C1-11D7-8645000102C1865D.
Tiessen, H., Lo Monaco, S., Ramirez, A. Santos, M.C.D., and Shang, C., 1996. Phosphate minerals in a lateritic crust from Venezuela. Biogeochemistry, 34: 1-17. DOI: 10.1007/BF02182952.
Vergouwen, L., 1981. Eugsterite, a new salt mineral. American Mineralogist, 66: 632–633.
Wurster, C. M., Bird, M., Bull, I., Bryant, C., and Ascough, P., 2009. A protocol for radiocarbon dating tropical subfossil cave guano. By the Arizona Board of Regents on behalf of the University of Arizona, 51: 977-986. ISSN: 0033-8222. 
Wurster, C.M., McFarlane, D.A., Bird, M.I., Ascough, P., and Athfield, N.B., 2010. Stable isotopes of subfossil bat guano as a long-term environmental archive: insights from a Grand Canyon cave deposit. Journal of Cave and Karst Studies, 72: 111–121. DOI: 10.4311/jcks2009es0109
Wurster, C.M., Munksgaard, N., Zwart, C., and Bird, M.I., 2015. The biogeochemistry of insectivorous cave guano: a case study from insular Southeast Asia. Springer International Publishing Switzerland, 124:1-13. DOI: 10.1007/s10533-015-0089-0.
Wurster, C.M., Rifai, H., Haig, J., Titin, J., Jacobsen, G., and Bird, M., 2017. Stable isotope composition of cave guano from eastern Borneo reveals tropical environments over the past 15,000 cal yr BP. Palaeogeography, Palaeoclimatology, Palaeoecology, 473: 73-81. DOI: 10.1016/j.palaeo.2017.02.029.