Skip to main content

Advertisement

Log in

Unexpected high molluscan diversity in a submarine cave in the Eastern Mediterranean

  • Original Paper
  • Published:
Marine Biodiversity Aims and scope Submit manuscript

Abstract

Marine caves are abundant throughout the Mediterranean Sea, but most studies have focused on those occurring in its western part so far. However, the few studies covering the Eastern Mediterranean showed that its caves are characterized by high diversity. We here describe the molluscan assemblage of the Kakoskali submarine cave in northwestern Cyprus, a shallow water cave characterized by the occurrence of large biostalactites. To avoid any destructive sampling in such a delicate environment, we used death assemblages from cave sediments (that can faithfully represent the composition of nearby living assemblages) sampled across a gradient from the inner chamber to nearby Posidonia patches outside the cave. Inside the cave, we found 217 species, 38% of the molluscan fauna currently known from Cyprus; sampling saturation was 0.99 and the estimated diversity at perfect coverage was 258 (+ 17%) species. One species has never been reported from Cyprus previously (Austronucula perminima) and another one is a first record for the entire Eastern Mediterranean (Hyalogyra zibrowii). We also report an unidentified Pyramidellidae which has eluded all identification efforts. In the cave, we found only five (2%) non-indigenous species represented by 50 individuals (1%). The Posidonia patches outside the cave hosted 143 species with a coverage of 0.98 and an estimated 180 (+ 26%) species at perfect coverage. The high diversity here recorded highlights the important role played by caves as biodiversity reservoirs. Additionally, this diversity is higher than the one described from Western Mediterranean caves inspected with comparable methods, contributing to questioning the magnitude of the west to east decreasing diversity gradient in the Mediterranean Sea.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdulla A, Gomei M, Maison E, Piante C (2008) Status of marine protected areas in the Mediterranean Sea. IUCN, Malaga and WWF, France

    Google Scholar 

  • Achilleos K, Jimenez C, Berning B, Petrou A (2020) Bryozoan diversity of Cyprus (eastern Mediterranean Sea): first results from census surveys (2011–2018). Mediterr Mar Sci 21:228–237. https://doi.org/10.12681/mms.21201

  • Albano PG, Sabelli B (2011) Comparison between death and living molluscs assemblages in a Mediterranean infralittoral off-shore reef. Palaeogeogr Palaeoclimatol Palaeoecol 310:206–215. https://doi.org/10.1016/j.palaeo.2011.07.012

    Article  Google Scholar 

  • Albano PG, Sabelli B (2012) The molluscan assemblages inhabiting the leaves and rhizomes of a deep water Posidonia oceanica settlement in the central Tyrrhenian Sea. Sci Mar 76:721–732. https://doi.org/10.3989/scimar.03396.02C

    Article  Google Scholar 

  • Albano PG, Stockinger M (2019) The rhizome layer of Posidonia oceanica: an important habitat for Mediterranean brachiopods. Mar Biodiv 49:2467–2472. https://doi.org/10.1007/s12526-019-00968-6

    Article  Google Scholar 

  • Albano PG, Azzarone M, Amati B et al (2020) Low diversity or poorly explored? Mesophotic molluscs highlight undersampling in the Eastern Mediterranean. Biodivers Conserv 29:4059–4072. https://doi.org/10.1007/s10531-020-02063-w

    Article  PubMed  PubMed Central  Google Scholar 

  • Albano PG, Steger J, Bakker PAJ et al (2021a) Numerous new records of tropical non-indigenous species in the Eastern Mediterranean highlight the challenges of their recognition and identification. ZooKeys 1010:1–95. https://doi.org/10.3897/zookeys.1010.58759

    Article  PubMed  PubMed Central  Google Scholar 

  • Albano PG, Steger J, Bošnjak M et al (2021b) Native biodiversity collapse in the eastern Mediterranean. Proc Biol Sci 288:20202469. https://doi.org/10.1098/rspb.2020.2469

    Article  PubMed  Google Scholar 

  • Bergamin L, Ruggiero ET, Pierfranceschi G, et al (2020) Benthic foraminifera and brachiopods from a marine cave in Spain: environmental significance. Mediterr Mar Sci 21:506–518. https://doi.org/10.12681/mms.23482

  • Bouchet P, Rocroi J-P, Bieler R et al (2010) Nomenclator of bivalve families with a classification of bivalve families. Malacologia 52:1–184. https://doi.org/10.4002/040.052.0201

    Article  Google Scholar 

  • Bouchet P, Rocroi J-P, Hausdorf B et al (2017) Revised classification, nomenclator and typification of gastropod and monoplacophoran families. Malacologia 61:1–526. https://doi.org/10.4002/040.061.0201

    Article  Google Scholar 

  • Cantone G, Fassari G, Brigandì S (1979) Ricerche sui Policheti e Molluschi di una grotta semisommersa del litorale catanese. Animalia, Catania 6:127–141

    Google Scholar 

  • Castelló J, Bitar G, Zibrowius H (2020) Isopoda (Crustacea) from the Levantine sea with comments on the biogeography of Mediterranean isopods. Mediterr Mar Sci 21:308–339. https://doi.org/10.12681/mms.20329

  • Cattaneo-Vietti R, Bo M, Cannas R et al (2016) An overexploited Italian treasure: past and present distribution and exploitation of the precious red coral Corallium rubrum (L., 1758) (Cnidaria: Anthozoa). Ital J Zool 83:443–455. https://doi.org/10.1080/11250003.2016.1255788

    Article  CAS  Google Scholar 

  • Cattaneo-Vietti R, Russo GF (1987) Molluscs from submarine caves of the Sorrentine Peninsula (southern Tyrrhenian Sea). Stygologia 3:138–148

    Google Scholar 

  • Cattaneo-Vietti R (1981) Molluscs fauna of some marine caves of the Sorrentina Peninsula (Naples). Rapp Comm Int Mer Médit 27:169–170

    Google Scholar 

  • Cattaneo-Vietti R (1982) The benthic populations of the submarine reserve of Monaco: 3. Opisthobranch molluscs. In: Journée d’études sur les aspects scientifiques concernant les récifs artificiels et la mariculture suspendue, 87–88

  • Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. https://doi.org/10.2307/41739612

    Article  PubMed  Google Scholar 

  • Coll M, Piroddi C, Steenbeek J, et al (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. PLoS ONE 5:e11842. https://doi.org/10.1371/journal.pone.0011842

  • Crocetta F, Bitar G, Zibrowius H, Oliverio M (2020) Increase in knowledge of the marine gastropod fauna of Lebanon since the 19th century. Bull Mar Sci 96:22. https://doi.org/10.5343/bms.2019.0012

  • Davis D, Tisdell C (1995) Recreational SCUBA-diving and carrying capacity in marine protected areas. Ocean Coast Manag 26:19–40. https://doi.org/10.1016/0964-5691(95)00004-L

    Article  Google Scholar 

  • Di Geronimo I, Allegri L, Improta S, La Perna R, Rosso A, Sanfilippo R (1997) Spatial and temporal aspects of benthic thanatocoenoses in a Mediterranean infralittoral cave. Riv Ital Paleontol Stratigr 103:15–28. https://doi.org/10.13130/2039-4942/5277

  • Di Geronimo I, La Perna R, Rosso A, Sanfilippo R (1993) Popolamento e tanatocenosi bentonica della Grotta dell’Accademia (Ustica, Mar Tirreno meridionale). Nat Sicil 17:4–17

    Google Scholar 

  • Dimarchopoulou D, Gerovasileiou V, Voultsiadou E (2018) Spatial variability of sessile benthos in a semi-submerged marine cave of a remote Aegean Island (eastern Mediterranean Sea). Reg Stud Mar Sci 17:102–111. https://doi.org/10.1016/j.rsma.2017.11.015

    Article  Google Scholar 

  • Faresi L, Bettoso N, Aleffi F, Orel G (2006) Benthic macrofauna of a submarine cave on the Istrian peninsula (Croatia). Ann Ser Hist Nat 16:9–16

    Google Scholar 

  • Gerovasileiou V, Bianchi C (2021) Mediterranean marine caves: a synthesis of current knowledge. Ocean Mar Biol 59:1–88

  • Gerovasileiou V, Chintiroglou C, Vafidis D, et al (2015) Census of biodiversity in marine caves of the eastern Mediterranean Sea. Mediterr Mar Sci 16:245. https://doi.org/10.12681/mms.1069

  • Gerovasileiou V, Drosos Koutsoubas, Voultsiadou E (2014) Spatial heterogeneity of benthic communities in a marine cave off Lesvos Island (Aegean Sea). In: Symposium on the conservation of dark habitats. https://doi.org/10.13140/2.1.4292.7049

  • Gerovasileiou V, Voultsiadou E (2012) Marine caves of the Mediterranean Sea: a sponge biodiversity reservoir within a biodiversity hotspot. PLoS ONE 7:e39873. https://doi.org/10.1371/journal.pone.0039873

  • Gerovasileiou V, Voultsiadou E, Issaris Y, Zenetos A (2016) Alien biodiversity in Mediterranean marine caves. Mar Ecol 37:239–256. https://doi.org/10.1111/maec.12268

    Article  Google Scholar 

  • Gerovasileiou V, Trygonis V, Sini M, Koutsoubas D, Voultsiadou E (2013) Three-dimensional mapping of marine caves using a handheld echosounder. Mar Ecol Prog Ser 486:13–22. https://doi.org/10.3354/meps10374

    Article  Google Scholar 

  • Giakoumi S, Sini M, Gerovasileiou V, et al (2013) Ecoregion-based conservation planning in the Mediterranean: dealing with large-scale heterogeneity. PLoS ONE 8:e76449. https://doi.org/10.1371/journal.pone.0076449

  • Gili J-M, Riera T, Zabala M (1986) Physical and Biological gradients in submarine cave on the Western Mediterranean coast (NE Spain). Mar Biol 90:291–297. https://doi.org/10.1007/BF00569141

    Article  Google Scholar 

  • Gofas S, Moreno D, Salas Casanova C (2011) Moluscos marinos de Andalucía Volumen II - Clase Gastropoda (Heterobranchia), clase Bivalvia, clase Scaphopoda, clase Cephalopoda, glosario e índices. Universidad de Málaga, Málaga

    Google Scholar 

  • Guarnieri G, Terlizzi A, Bevilacqua S, Fraschetti S (2012) Increasing heterogeneity of sensitive assemblages as a consequence of human impact in submarine caves. Mar Biol 159:1155–1164. https://doi.org/10.1007/s00227-012-1895-8

    Article  Google Scholar 

  • Guido A, Jimenez C, Achilleos K, Rosso A, Sanfilippo R, Hadjioannou L, Petrou A, Russo F, Mastandrea A (2017) Cryptic serpulid-microbialite bioconstructions in the Kakoskali submarine cave (Cyprus, Eastern Mediterranean). Facies 63:21. https://doi.org/10.1007/s10347-017-0502-3

    Article  Google Scholar 

  • Harmelin JG, Vacelet J, Vasseur P (1985) Les grottes sous-marines obscures: un milieu extrême et un remarquable biotope refuge. Tethys 1:214–229

    Google Scholar 

  • Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613

    Article  Google Scholar 

  • Idan T, Shefer S, Feldstein T, et al (2018) Shedding light on an East-Mediterranean mesophotic sponge ground community and the regional sponge fauna. Mediterr Mar Sci 19:84–106. https://doi.org/10.12681/mms.13853

  • Idato E, Cinelli F, Fresi E, Mazzella L, Scipione MB (1983) Distribuzione dei popolamenti bentonici di substrato duro lungo un gradiente di luce in una grotta marina superficiale dell’isola di Ischia: molluschi. Arch Oceanogr e Limnol 20:113–129

    Google Scholar 

  • Janssen A, Chevaldonné P, Martínez Arbizu P (2013) Meiobenthic copepod fauna of a marine cave (NW Mediterranean) closely resembles that of deep-sea communities. Mar Ecol Prog Ser 479:99–113. https://doi.org/10.3354/meps10207

    Article  Google Scholar 

  • Jimenez C, Achilleos K, Petrou A, et al (2019) A dream within a dream: Kakoskali Cave, a unique marine ecosystem in Cyprus (Levantine Sea). In: Öztürk B (ed) Marine Caves of the Eastern Mediterranean Sea. Biodiversity, Threats and Conservation. Beykoz, Istanbul, pp 91–110

  • Kidwell S (2013) Time-averaging and fidelity of modern death assemblages: building a taphonomic foundation for conservation palaeobiology. Palaeontology 56:487–522. https://doi.org/10.1111/pala.12042

    Article  Google Scholar 

  • Kidwell SM, Tomašových A (2013) Implications of time-averaged death assemblages for ecology and conservation biology. Annu Rev Ecol Evol Syst 44:539–563. https://doi.org/10.1146/annurev-ecolsys-110512-135838

    Article  Google Scholar 

  • Kowalewski C, Casazza L et al (2003) Quantitative fidelity of brachiopod-mollusk assemblages from modern subtidal environments of San Juan Islands, USA. J Taph 1:43–65

    Google Scholar 

  • Lloret J, Marín A, Marín-Guirao L, Carreño MF (2006) An alternative approach for managing scuba diving in small marine protected areas. Aquatic Conservation: Aquat Conservat Mar Freshwat Ecosyst 16:579–591. https://doi.org/10.1002/aqc.734

    Article  Google Scholar 

  • Lucrezi S, Milanese M, Markantonatou V et al (2017) Scuba diving tourism systems and sustainability: Perceptions by the scuba diving industry in two Marine Protected Areas. Tour Manag 59:385–403. https://doi.org/10.1016/j.tourman.2016.09.004

    Article  Google Scholar 

  • Montefalcone M, De Falco G, Nepote E et al (2018) Thirty year ecosystem trajectories in a submerged marine cave under changing pressure regime. Mar Environ Res 137:98–110. https://doi.org/10.1016/j.marenvres.2018.02.022

    Article  CAS  PubMed  Google Scholar 

  • Morri C, Puce S, Bianchi CN et al (2009) Hydroids (Cnidaria: Hydrozoa) from the Levant Sea (mainly Lebanon), with emphasis on alien species. J Mar Biol Ass 89:49–62. https://doi.org/10.1017/S0025315408002749

    Article  Google Scholar 

  • Oliver J, Templado J, Kersting D (2012) Gasterópodos marinos de las Islas Columbretes (Mediterráneo occidental). Iberus 30:49–87. https://doi.org/10.5281/zenodo.4558169

    Article  Google Scholar 

  • Ouerghi A, Gerovasileiou V, Bianchi C (2019) Mediterranean marine caves: a synthesis of current knowledge and the Mediterranean Action Plan for the conservation of “dark habitats”. In: Öztürk B (ed) Marine Caves of the Eastern Mediterranean Sea. Biodiversity, Threats and Conservation. Beykoz, Istanbul, p 1–13

  • Öztürk B, Buzzurro G, Benli HA (2004) Marine molluscs from Cyprus: new data and checklist. Boll Malacol 39:49–78

    Google Scholar 

  • Öztürk B (2019) Marine Caves of the Eastern Mediterranean Sea. Biodiversity, Threats and Conservation. Beykoz, Istanbul

  • Palazzi S, Villari A (2001) Molluschi e brachiopodi delle grotte sottomarine del Taorminese. Evolver

  • Pino de la Torre L, Navarro-Barranco C, Gofas S (2020) Malacofauna from soft bottoms in the Cerro Gordo marine cave (Alboran Sea): biodiversity and spatial distribution. Mediterr Mar Sci 21: 684–704. https://doi.org/10.12681/mms.22920

  • Ponder WF, Lindberg DR, Ponder JM (2019) Biology and Evolution of the Mollusca. CRC Press, Boca Raton, Florida. https://doi.org/10.1201/9781351115667

    Book  Google Scholar 

  • R Development Core Team (2019) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

  • Roditi-Elasar M, Kerem D, Lazar M, Barneah O, Almogi-Labin A, Angel DL (2019) Benthic macro-faunal abundance and diversity and sediment distribution in Akhziv submarine canyon and the adjacent slope (eastern Levant Basin, Mediterranean Sea). Mediterr Mar Sci, 20:521–531. https://doi.org/10.12681/mms.19430

  • Romani L, Raveggi A, Scaperrotta M, Bartolini S (2017) Nota sui micromolluschi marini conchiferi rinvenuti nei dintorni di Paleokastritsa (Corfù [Kerkyra] Grecia, Mar Ionio Nord-Orientale). Alleryana 35:24–46

    Google Scholar 

  • Romani L, Sbrana C (2016) A new Mediterranean species of the Cornirostridae (Gastropoda, Heterobranchia), with notes on the genus Tomura. Iberus 34:55–61. https://doi.org/10.5281/zenodo.4603235

    Article  Google Scholar 

  • Sigwart JD, Stoeger I, Knebelsberger T, Schwabe E (2013) Chiton phylogeny (Mollusca : Polyplacophora) and the placement of the enigmatic species Choriplax grayi (H. Adams & Angas). Invertebr Syst 27:603–621. https://doi.org/10.1071/IS13013

  • Smith SDA (2008) Interpreting molluscan death assemblages on rocky shores: are they representative of the regional fauna? J Exp Mar Biol Ecol 366:151–159. https://doi.org/10.1016/j.jembe.2008.07.019

    Article  Google Scholar 

  • Starmühlner F (1968) Investigations about the mollusc fauna in submarine caves. Proc Symp Mollusca 1:136–163

    Google Scholar 

  • Steiner G, Kabat A (2001) Catalogue of supraspecific taxa of Scaphopoda (Mollusca). Zoosystema 23:433–460

    Google Scholar 

  • Tomašových A, Kidwell S (2009) Fidelity of variation in species composition and diversity partitioning by death assemblages: time-averaging transfers diversity from beta to alpha levels. Paleobiology 35:94–118. https://doi.org/10.1666/08024.1

    Article  Google Scholar 

  • Tortonese E (1951) I caratteri biologici del Mediterraneo orientale e i problemi relativi. Attualità Zoologiche 7:207–251

    Google Scholar 

  • Tunesi L, Diviacco G (1993) Environmental and socio-economic criteria for establishment of marine coastal parks. Int J Environ Stud 43:253–259. https://doi.org/10.1080/00207239308710832

    Article  Google Scholar 

  • UNEP-MAP-RAC/SPA (2008) Action plan for the conservation of the coralligenous and other calcareous bio-concretions in the Mediterranean Sea. RAC/SPA, Tunis, 21.

  • UNEP-MAP-RAC/SPA (2015) Action plan for the conservation of habitats and species associated with seamounts, underwater caves and canyons, aphotic hard beds and chemo-synthetic phenomena in the Mediterranean Sea. Dark Habitats Action Plan. RAC/SPA, Tunis, 17

  • Vacelet J, Boury-Esnault N, Harmelin J-G (1994) Hexactinellid cave, a unique deep-sea habitat in the scuba zone. Deep Sea Res Part I Oceanogr Res Pap 41:965–973. https://doi.org/10.1016/0967-0637(94)90013-2

    Article  Google Scholar 

  • Warén A, Carozza F, Rocchini R (1997) Description of two new species of Hyalogyrinidae (Gastropoda, Heterobranchia) from the Mediterranean. Boll Malacol 32:57–66

    Google Scholar 

  • Warwick RM, Light J (2002) Death assemblages of molluscs on St Martin’s Flats, Isles of Scilly: a surrogate for regional biodiversity? Biodiv Conserv 11:99–112. https://doi.org/10.1023/A:1014094829984

    Article  Google Scholar 

  • Zakai D, Chadwick-Furman NE (2002) Impacts of intensive recreational diving on reef corals at Eilat, northern Red Sea. Biol Conserv 105:179–187. https://doi.org/10.1016/S0006-3207(01)00181-1

    Article  Google Scholar 

  • Zenetos A, Katsanevakis S, Poursanidis D, et al (2011) Marine alien species in Greek Seas: Additions and amendments by 2010. Mediterr Mar Sci 12:95–120 https://doi.org/10.12681/mms.55

Download references

Acknowledgements

Our gratitude goes in particular to Louis Hadjioannou and Antonis Petrou from ENALIA for their participation in the field work and encouragement to study Kakoskali’s singular ecology. We thank Martin Zuschin and Christian Baal for their support and assistance at the University of Vienna. We express our gratitude to the Reviewers of the Journal Marine Biodiversity for their constructive comments during the revision process. These helped us to improve the quality of our manuscript.

Funding

The study was performed in the framework of the project “Historical ecology of Lessepsian migration” funded by the Austrian Science Fund (FWF) P28983-B29 (PI: P.G. Albano). DDF was supported by the Erasmus + Traineeship Programme and CJ by ENALIA’s research program.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Davide Di Franco.

Ethics declarations

Conflict of interest

The author declares no competing interests.

Ethics approval

No animal testing was performed during this study.

Sampling and field studies

Fieldwork in the cave was conducted according to all applicable local and international laws.

Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Author contribution

PGA, DDF, and CJ conceived and designed the study. CJ conducted fieldwork. DDF sorted the samples and identified the species. DDF and PGA analyzed the data. DDF wrote the first draft of the manuscript which was contributed by all co-authors.

Additional information

Communicated by C. Chen

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (XLSX 26.4 KB)

Supplementary file2 (XLSX 10 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Di Franco, D., Jimenez, C. & Albano, P.G. Unexpected high molluscan diversity in a submarine cave in the Eastern Mediterranean. Mar. Biodivers. 51, 85 (2021). https://doi.org/10.1007/s12526-021-01219-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12526-021-01219-3

Keywords

Navigation