Skip to main content

Advertisement

Log in

Cryptic serpulid-microbialite bioconstructions in the Kakoskali submarine cave (Cyprus, Eastern Mediterranean)

  • Original Paper
  • Published:
Facies Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Abdelahad N (1989) On four Myxosarcina-like species (Cyanophyta) living in the Inferniglio cave (Italy). Algol Stud 54:3–13

    Google Scholar 

  • Antonioli F, Silenzi S, Frisia S (2001) Tyrrhenian Holocene palaeoclimate trends from spelean serpulids. Quat Sci Rev 20:1661–1670

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Chafetz HS (1986) Marine peloids: a product of bacterially induced precipitation of calcite. J Sediment Petrol 56:812–817

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Coma R, Carola M, Riera T, Zabala M (1997) Horizontal transfer of matter by a cave-dwelling mysid. Mar Ecol PSZNI 18:211–226

    Article  Google Scholar 

  • Cubbon BD (1976) Cave flora. In: Ford TD, Cullingford CHD (eds) Science of speleology. Academic Press, London, pp 423–433

    Google Scholar 

  • Culver DC (1985) Trophic relationships in aquatic cave environments. Stygologia 1:43–53

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Dravies JJ, Yurewicz DA (1985) Enhanced carbonate petrography using fluorescence microscopy. J Sediment Petrol 55:795–804

    Google Scholar 

  • Dupraz C, Strasser A (1999) Microbialites and micro-encrusters in shallow coral bioherms (Middle-Late Oxfordian, Swiss Jura Mountains). Facies 40:101–130

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fichez R (1990a) Decrease in allochthonous organic inputs in dark submarine caves, connection with lowering in benthic community richness. Hydrobiologia 207:61–69

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Forti P (2001) Biogenic speleothems: an overview. Int J Speleol 30:39–56

    Article  Google Scholar 

  • Friebe JG (1994) Serpulid-bryozoan-foraminiferal biostromes controlled by temperate climate and salinity: Middle Miocene of the Styrian Basin, Austria. Facies 30:51–62

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gerovasileiou V, Voultsiadou E (2016) Sponge diversity gradients in marine caves of the eastern Mediterranean. J Mar Biol Assoc UK 96:407–416

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Harmelin JG (1969) Bryozoaires des grottes sous-marines obscures de la re´gion marseillaise, faunistique et écologie. Téthys 1:793–806

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Harmelin J-G (1986) Patterns in the distribution of bryozoans in the Mediterranean marine caves. Stygologia 2:10–25

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • Kennard JM, James NP (1986) Thrombolites and stromatolites: two distinct types of microbial structures. Palaios 1:492–503

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Paerl HW, Steppe TF, Reid RP (2001) Bacterially mediated precipitation in marine stromatolites. Environ Microbiol 3:123–130

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Reitner J (1993) Modern cryptic microbialite/metazoan facies from Lizard Island (Great Barrier Reef, Australia): formation and concepts. Facies 29:3–40

    Article  Google Scholar 

  • Reolid M, Molina JM (2010) Serpulid-Frutexites assemblages from shadow-cryptic environments in Jurassic marine caves, Betic Cordillera, southern Spain. Palaios 25:468–474

    Article  Google Scholar 

  • Riding R (2000) Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47:179–214

    Article  Google Scholar 

  • Riding R (2002) Biofilm architecture of Phanerozoic cryptic carbonate marine veneers. Geology 30:31–34

    Article  Google Scholar 

  • Riding R (2008) Abiogenic, microbial and hybrid authigenic carbonate crusts: components of Precambrian stromatolites. Geologia Croatica 61:73–103

    Google Scholar 

  • Riedl R (1966) Biologie der Meereshöhlen. Paul Parey, Hamburg

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Sarbu SM, Kane TC, Kinkle BK (1996) A chemoautotrophically based cave ecosystem. Science 272:1953–1955

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Taylor PD, Palmer TJ (1994a) Submarine palaeocaves. Geol Today 10:169–170

    Article  Google Scholar 

  • Taylor PD, Palmer TJ (1994b) Submarine caves in a Jurassic reef (La Rochelle, France) and the evolution of cave biotas. Naturwissenschaften 81:357–360

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

Download references

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.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Adriano Guido.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

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

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10347-017-0502-3

Keywords

Navigation