Abstract
The biostalactites from the Kakoskali cave in Cyprus represent a new example of the complex biotic relationships between skeletal organisms and microbial communities in building bioconstructions of cryptic marine environments. Biostalactites are mainly constituted of polychaetes of the family Serpulidae and, to a lesser degree, foraminifers and bryozoans. Within the skeletal framework of these organisms, two types of microcrystalline calcite (micrite) have been recognized: autochthonous and detrital micrite. The autochthonous fraction is syndepositionally lithified and occurs as clotted peloidal and, subordinately, aphanitic (structureless) textures, suggesting the presence of heterotrophic microbial activities thriving on decaying metazoan organic matter. This fraction is limited to the protected portions of the bioconstructions, especially in the inner and lower parts. The presence of iron and manganesiferous oxidizing bacteria is suggested by the deposition of ferromanganesiferous crusts and Frutexites-like structures. These microbial-induced biomineralizations are the main evidence of carbonatogenetic and Fe–Mn, autotrophic and chemoheterotrophic, bacterial activities. The Kakoskali cave is frequently visited by divers who, during their immersions, resuspend the fine bottom sediment, which later covers the surface of the bioconstructions, disturbing the delicate equilibrium of the biotic association. This perturbation, which is also caused by strong waves and currents, during winter months, reflects on the bioconstruction morphologies, community composition, and colonization pattern. Bioconstructions exhibit an upper smooth surface, produced by few taxa (e.g., polychaetes, foraminifers), hosting a low number of living individuals, and a lower comparably rough surface, colonized by a more abundant community showing a higher species richness. The ratio surface roughness/smoothness is related to micrite sediment type: the upper part is mainly characterized by loose detrital micrite while the internal and lower parts by syndepositional cemented autochthonous micrite.
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References
Abdelahad N (1989) On four Myxosarcina-like species (Cyanophyta) living in the Inferniglio cave (Italy). Algol Stud 54:3–13
Antonioli F, Silenzi S, Frisia S (2001) Tyrrhenian Holocene palaeoclimate trends from spelean serpulids. Quat Sci Rev 20:1661–1670
Belmonte G, Ingrosso G, Poto M, Quarta G, D’Elia M, Onorato O, Calcagnile L (2009) Biogenic stalactites in submarine caves at the Cape of Otranto (SE Italy): dating and hypothesis on their formation. Mar Ecol 30:376–382
Bertling M, Insalaco E (1998) Late Jurassic coral/microbial reefs from the northern Paris Basin facies, palaeoecology and palaeobiogeography. Palaeogeogr Palaeoclim Palaeoecol 139:139–175
Bianchi CN, Morri C (1994) Studio biologico comparativo di alcune grotte marine sommerse: definizione di una scala di confinamento. Memorie Istituto Italiano di Speleologia 6:107–123
Bianchi CN, Sanfilippo R (2003) Policheti serpuloidei. In: Cicogna F, Bianchi CN, Ferrari G, Forti P (eds) Grotte Marine: Cinquant’anni di Ricerca in Italia CLEM-ONLUS, Ministero dell’Ambiente e della Tutela del Territorio. Officine Grafiche Canessa, Rapallo, pp 175–185
Bianchi CN, Cattaneo-Vietti R, Cinelli F, Morri C, Pansini M (1996) Lo studio biologico delle grotte sottomarine del Mediterraneo: conoscenze attuali e prospettive. Boll Mus Ist Biol Univ Genova 60–61:41–69
Bibiloni MA, Gili JM, Ros J (1984) Les coves submarines de les illes Medes. In: Ros J, Olivella I, Gili JM (eds) Els sistemes naturals de les illes Medes. Institut d’Estudis Catalans, Barcelona, pp 707–737
Bussotti S, Terlizzi A, Fraschetti S, Belmonte G, Boero F (2006) Spatial and temporal variability of sessile benthos in shallow Mediterranean marine caves. Mar Ecol Prog Ser 325:109–119
Carola M, Coma R, Riera T, Cabala M (1993) Fecal pellets collection as a method for assessing egesta of the marine cave-dwelling mysid Hemimysis speluncola. Scientia Marina 57:51–63
Chafetz HS (1986) Marine peloids: a product of bacterially induced precipitation of calcite. J Sediment Petrol 56:812–817
Cirilli S, Iannace A, Jadoul F, Zamparelli V (1999) Microbial serpulids buildups in Norian–Rhaetian of the Western Mediterranean area: ecological response of marginal communities to stressed environments. Terra Nova 11:195–202
Coma R, Carola M, Riera T, Zabala M (1997) Horizontal transfer of matter by a cave-dwelling mysid. Mar Ecol PSZNI 18:211–226
Cubbon BD (1976) Cave flora. In: Ford TD, Cullingford CHD (eds) Science of speleology. Academic Press, London, pp 423–433
Culver DC (1985) Trophic relationships in aquatic cave environments. Stygologia 1:43–53
D’Elia M, Quarta G, Calcagnile L, Belmonte G (2007) Study of the formation of biogenic speleothems found in submarine caves at the cape of Otranto, Italy, by 14C AMS. Nucl Instrum Methods B 259:395–397
Dravies JJ, Yurewicz DA (1985) Enhanced carbonate petrography using fluorescence microscopy. J Sediment Petrol 55:795–804
Dupraz C, Strasser A (1999) Microbialites and micro-encrusters in shallow coral bioherms (Middle-Late Oxfordian, Swiss Jura Mountains). Facies 40:101–130
Dupraz C, Reid PR, Braissant O, Decho AW, Norman RS, Visscher PT (2009) Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev 96:141–162
Fichez R (1990a) Decrease in allochthonous organic inputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia 207:61–69
Fichez R (1990b) Absence of redox potential discontinuity in dark submarine cave sediments as evidence of oligotrophic conditions. Estuar Coast Shelf S 31:875–881
Fornós JJ, Forteza V, Martinez-Taberner A (1997) Modern polychaete reefs in Western Mediterranean lagoons: Ficopomatus enigmaticus (Fauvel) in the Albufera of Menorca, Balearic Islands. Palaeogeogr Palaeoclimatol Palaeoecol 128:175–186
Forti P (2001) Biogenic speleothems: an overview. Int J Speleol 30:39–56
Friebe JG (1994) Serpulid-bryozoan-foraminiferal biostromes controlled by temperate climate and salinity: Middle Miocene of the Styrian Basin, Austria. Facies 30:51–62
Garrabou J, Flos J (1995) A simple diffusion-sedimentation model to explain planktonic gradients within a NW Mediterranean submarine cave. Mar Ecol Prog Ser 123:273–280
Gerovasileiou V, Voultsiadou E (2016) Sponge diversity gradients in marine caves of the eastern Mediterranean. J Mar Biol Assoc UK 96:407–416
Gerovasileiou V, Koutsoubas D, Voultsiadou E (2014) Spatial heterogeneity of benthic communities in a marine cave off Lesvos Island (Aegean Sea). In: Langar H, Bouafif C, Ouerghi A (eds) Proceedings of the 1st Mediterranean symposium on the conservation of dark habitats, Portorož, Slovenia, 27–31 October 2014. RAC/SPA, Tunis, pp 69–70
Gischler E, Heindel K, Birgel D, Brunner B, Reitner J, Peckmann J (2017) Cryptic biostalactites in a submerged karst cave of the Belize Barrier Reef revisited: pendant bioconstructions cemented by microbial micrite. Palaeogeogr Palaeoclim Palaeoecol 468:34–51
Gücü AC, Ok M, Sakinan S (2009) A survey of the critically endangered Mediterranean monk seal, Monachus monachus (Hermann, 1779) along the coast of northern Cyprus. Isr J Ecol Evol 55:77–82
Guido A, Mastandrea A, Rosso A, Sanfilippo R, Russo F (2012) Micrite precipitation induced by sulphate reducing bacteria in serpulid bioconstructions from submarine caves (Syracuse, Sicily). Rend Online Soc Geol It 21:933–934
Guido A, Heindel K, Birgel D, Rosso A, Mastandrea A, Sanfilippo R, Russo F, Peckmann J (2013) Pendant bioconstructions cemented by microbial carbonate in submerged marine caves (Holocene, SE Sicily). Palaeogeogr Palaeoclim Palaeoecol 388:166–180
Guido A, Mastandrea A, Rosso A, Sanfilippo R, Tosti F, Riding R, Russo F (2014) Commensal symbiosis between agglutinated polychaetes and sulfate-reducing bacteria. Geobiology 12:265–275
Guido A, Rosso A, Sanfilippo R, Russo F, Mastandrea A (2016a) Frutexites from microbial/metazoan bioconstructions of Recent and Pleistocene marine caves (Sicily, Italy). Palaeogeogr Palaeoclim Palaeoecol 453:127–138
Guido A, Mastandrea A, Stefani M, Russo F (2016b) Role of autochthonous versus detrital micrite in depositional geometries of Middle Triassic carbonate platform systems. Geol Soc Am Bull 128:989–999
Guido A, Rosso A, Sanfilippo R, Russo F, Mastandrea A (2017) Microbial biomineralization in biotic crusts from a Pleistocene marine cave (NW Sicily, Italy). Geomicrobiol J. doi:10.1080/01490451.2017.1284283
Harmelin JG (1969) Bryozoaires des grottes sous-marines obscures de la re´gion marseillaise, faunistique et écologie. Téthys 1:793–806
Harmelin J-G (1980) Etablissement des communautés de substrats durs en milieu obscur. Résultats préliminaires d’une expérience à long terme en Méditerranée. Mem Biol Mar Ocean 10:29–52
Harmelin J-G (1985) Bryozoan dominated assemblages in Mediterranean cryptic environments. In: Nielsen C, Larwood GP (eds) Bryozoan: Ordovician to Recent. Olsen & Olsen, Fredensborg, pp 135–143
Harmelin J-G (1986) Patterns in the distribution of bryozoans in the Mediterranean marine caves. Stygologia 2:10–25
Harmelin J-G (1997) Diversity of bryozoans in a Mediterranean sublittoral cave with bathyal-like conditions: role of dispersal processes and local factors. Mar Ecol Prog Ser 153:139–152
Harmelin J-G (2000) Ecology of cave and cavity dwelling bryozoans. In: Herrera Cubilla A, Jackson JBC (eds) Proceedings of the 11th international Bryozoology Association conference. Smithsonian Tropical Research Institute, Panama, pp 38–55
Harrison RW, Tsiolakis E, Stone BD, Lord A, McGeehin JP, Mahan SA, Chirico P (2013) Late Pleistocene and Holocene uplift history of Cyprus: implications for active tectonics along the southern margin of the Anatolian microplate. In: Robertson AHF, Parlak O, Ünlügenc UC (eds) Geological development of Anatolia and the Easternmost Mediterranean Region, vol 372. Geological Society, Special Publications, London, pp 561–584
Jimenez C, Hadjioannou L, Petrou A, Andreou V, Georgiou A (2017) Fouling Communities of two accidental artificial reefs (Modern Shipwrecks) in Cyprus (Levantine Sea). Water 9:1–11
Jones B (1995) Processes associated with microbial biofilms in the twilight zone of caves: examples from the Cayman Islands. J Sediment Res 65:552–560
Kennard JM, James NP (1986) Thrombolites and stromatolites: two distinct types of microbial structures. Palaios 1:492–503
Machel HG, Mason RA, Mariano AN, Mucci A (1991) Causes and emission of luminescence in calcite and dolomite. In: Baker CE, Kopp OC (eds) Luminescence microscopy and spectroscopy: qualitative and quantitative applications, vol 25. Society of Economic PA, short course, pp 495–510
Macintyre IG, Videtich PE (1979) Pseudostalactites from a submarine cave near Columbus Cay, Belize barrier-reef complex: evidence of extensive submarine lithification. Tulsa, Oklahoma. Program AAPG-SEPM Annual Convention, American Association Petroleum Geologists, Houston, TX
Martí R, Uriz MJ, Ballesteros E, Turon X (2004) Benthic assemblages in two Mediterranean caves: species diversity and coverage as a function of abiotic parameters and geographic distance. J Mar Biol Assoc UK 84:557–572
Mattison R, Abbiati M, Dando P, Fitzsimons M, Pratt S, Southward A, Southward E (1998) Chemoautotrophic microbial mats in submarine caves with hydrothermal sulphidic springs at Cape Palinuro, Italy. Microbial Ecol 35:58–71
Monty CLV(1976) The origin and development of cryptalgal fabrics. In: Walter MR (ed) Stromatolites. Dev Sedimentol 20:193–249
Moscatello S, Belmonte G (2007) The plankton of a shallow submarine cave (‘Grotta di Ciolo’ Salento Peninsula, SE Italy). Mar Ecol 28:27–59
Muricy G, Boury-Esnault N, Bezac C, Vacelet J (1998) Taxonomic revision of the Mediterranean Plakina Schulze (Porifera, Demospongiae, Homoscleromorpha). Zool J Linn Soc 124:169–203
Neuweiler F, Reitner J (1995) Epifluorescence-microscopy of selected automicrites from lower Carnian Cipit-boulders of the Cassian formation (Seeland Alpe, Dolomites). In: Reitner J, Neuweiler F (eds) Mud mounds: a polygenetic spectrum of fine-grained carbonate buildups. Facies 32:26–28
Olivier N (2004) Microbialites dans les bioconstructions du Jurassique: morphologies, rôles édificateurs et significations paléoenvironnementales: Ph.D. thesis, Université Claude-Bernard Lyon 1, Lyon, France
Olivier NC, Colombié B, Pittet B, Lathuiliére B (2001) Microbial carbonates and corals on the marginal French Jura platform (Late Oxfordian, Molinges section). Facies 57:469–492
Olivier N, Hantzpergue P, Gaillard C, Pittet B, Leinfelder RR, Schmid DU, Werne W (2003) Microbialite morphology, structure and growth: a model of the Upper Jurassic reefs of the Chay Peninsula (western France). Palaeogeogr Palaeoclim Palaeoecol 193:383–404
Onorato R, Forti P, Belmonte G, Costantini A, Poto M (2003) La grotta sottomarina lu Lampiùne: novità esplorative e prime indagini ecologiche. Thalassia Salentina 26:55–64
Paerl HW, Steppe TF, Reid RP (2001) Bacterially mediated precipitation in marine stromatolites. Environ Microbiol 3:123–130
Palau M, Cornet C, Riera T, Zabala M (1991) Planktonic gradients along a Mediterranean Sea cave. In: Ros JD, Prat N (eds) Homage to R. Margalef or Why there is such pleasure in studying nature. Oecol Aquat 10:299–316
Palma RM, Angeleri MP (1992) Early Cretaceous serpulid limestones: Chachao Formation, Neuquen Basin, Argentina. Facies 27:175–178
Quarta G, D’Elia M, Calcagnile L, Belmonte G, Ingrosso G (2010) Reconstructing the formation mechanism of submarine biogenic stalactites: the contribution of AMS. Nucl Instrum Methods B 268:1244–1247
Reitner J (1993) Modern cryptic microbialite/metazoan facies from Lizard Island (Great Barrier Reef, Australia): formation and concepts. Facies 29:3–40
Reolid M, Molina JM (2010) Serpulid-Frutexites assemblages from shadow-cryptic environments in Jurassic marine caves, Betic Cordillera, southern Spain. Palaios 25:468–474
Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47:179–214
Riding R (2002) Biofilm architecture of Phanerozoic cryptic carbonate marine veneers. Geology 30:31–34
Riding R (2008) Abiogenic, microbial and hybrid authigenic carbonate crusts: components of Precambrian stromatolites. Geologia Croatica 61:73–103
Riedl R (1966) Biologie der Meereshöhlen. Paul Parey, Hamburg
Riera T, Vives F, Gili J (1991) Stephos margalefi sp. nov. (Copepoda: Calanoida) from a submarine cave of Majorca Island (western Mediterranean). Oecol Aquatica 10:317–323
Rosso A, Di Martino E, Sanfilippo R, Di Martino V (2013a) Bryozoan communities and thanatocoenoses from submarine caves in the Plemmirio Marine Protected Area (SE Sicily). In: Ernst A, Schäfer P, Scholz J (eds) Bryozoan Studies 2010. Proceedings of the 15th IBA conference, Kiel, Germany. Lecture Notes in Earth System Science, vol 143, pp 251–269
Rosso A, Sanfilippo R, Taddei Ruggiero E, Di Martino E (2013b) Faunas and ecological groups of Serpuloidea, Bryozoa and Brachiopoda from submarine caves in Sicily (Mediterranean Sea). Boll Soc Paleont It 52:167–176
Rosso A, Sanfilippo R, Mastrototaro F (2014) Bryozoan and serpuloidean distribution pattern on a deep-water slab (Bari Canyon, Adriatic Sea). In: Proceedings of the 1st Mediterranean symposium on the conservation of the dark habitats, Portoroz, Slovenia, 31 October 2014, pp 79–80. doi:10.13140/2.1.4798.3042
Russo F, Neri C, Mastandrea A, Baracca A (1997) The mud mound nature of the Cassian Platform Margins of the Dolomites A case history: the Cipit boulders from Punta Grohmann (Sasso Piatto Massif, northern Italy). Facies 36:25–36
Sanfilippo R, Rosso A, Guido A, Mastandrea A, Russo F, Riding R, Ruggiero ET (2015) Metazoan/microbial biostalactites from present-day submarine caves in the Mediterranean Sea. Mar Ecol 36:1277–1293
Sanfilippo R, Rosso A, Guido A, Gerovasileiou V (2017) Serpulid communities from two marine caves in the Aegean Sea, Eastern Mediterranean. J Mar Biol Ass UK. doi:10.1017/S0025315417000297
Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955
Scicchitano G, Monaco C (2006) Grotte carsiche e linee di costa sommerse tra Capo Santa Panagia e Ognina (Siracusa, Sicilia sud-orientale). Il Quaternario 19(2):187–194
Taylor PD, Palmer TJ (1994a) Submarine palaeocaves. Geol Today 10:169–170
Taylor PD, Palmer TJ (1994b) Submarine caves in a Jurassic reef (La Rochelle, France) and the evolution of cave biotas. Naturwissenschaften 81:357–360
Ten Hove HA, Van den Hurk P (1993) A review of recent and fossil serpulid “reefs”; actuopalaeontology and the “Upper Malm” serpulid limestones in NW Germany. Geol Mijnbouw 72:23–67
Toscano F, Raspini A (2005) Epilithozoan fauna associated with ferromanganese crustgrounds on the continental slope segment between Capri and Li Galli Islands Bay of Salerno, Northern Tyrrhenian Sea, Italy. Facies 503:427–441
Zabala M, Rieira T, Gili JM, Barange M, Lobo A, Peñuelas J (1989) Water flow, trophic depletion, and benthic macrofauna impoverishment in a submarine cave from the western Mediterranean. Mar Ecol PSZNI 10:271–287
Acknowledgements
The authors wish to express their gratitude to Matthias López Correa and another anonymous reviewer for their constructive comments and suggestions. This research was financially supported by grants MIUR (ex 60% 2016 A. Mastandrea, University of Calabria), grants to AR and RS by the University of Catania, AP Marine Environmental Consultancy Ltd. (Cyprus), Mr. Nick Galea (ENALIA Research Program, Cyprus), and Mr. Angelos Tsirides. The authors also thank Prof. Dr. Helmut Zibrowius for his advice since the beginning of the Kakoskali project. Catania Paleoecological Research Group: contribution n. 430.
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Guido, A., Jimenez, C., Achilleos, K. et al. Cryptic serpulid-microbialite bioconstructions in the Kakoskali submarine cave (Cyprus, Eastern Mediterranean). Facies 63, 21 (2017). https://doi.org/10.1007/s10347-017-0502-3
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DOI: https://doi.org/10.1007/s10347-017-0502-3