Skip to main content

Advertisement

SpringerLink
Log in

Sponges associated with stylasterid thanatocoenosis (Cnidaria, Hydrozoa) from the deep Ross Sea (Southern Ocean)

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

In the Antarctic seas, where hard substrates are scarce, the presence of secondary bio-substrates formed by calcareous organisms is an essential condition to increase the epibiosis and therefore the diversity of sessile benthic fauna. The aggregations of stylasterid hydrozoa, with their branched carbonate structures, are an example of a secondary habitat defined as a ‘deep marine animal forest’. The three-dimensional habitat made by these corals supports a high biodiversity of associated organisms, usually invertebrates. Recently, deep remotely operated vehicle (ROV) exploration of the Iselin Bank and the Hallett Ridge (Ross Sea, Antarctica) documented wide areas characterised by large thanatocoenosis of stylasterid skeletons lying on flat muddy substrates, with scattered living colonies generally made of few short branches. In our study, sponges associated with 54 dead colonies of two stylasterid species recorded in these areas were investigated. The analysis led to the discovery of a remarkable number of specimens (127) ascribed to 38 sponge species (31 encrusting and 7 massive). Two of these sponges, Asbestopluma (Asbetopluma) sinuosa and Lissodendoryx (Ectyodoryx) inferiolabiatae, are new. In light of the present data, we can assume that, in Antarctica, stylasterid skeletal remains, due to their three-dimensional structure, play an important role in maintaining sponge biodiversity. This is also due to the ability of sponge specie to produce miniaturised specimens able to colonise these peculiar substrata.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

Data availability

All data generated or analysed during this study are included in this manuscript.

References

  • Anderson MJ (2005) Permutational multivariate analysis of variance. University of Auckland, Auckland, Department of Statistics

    Google Scholar 

  • Bavestrello G, Calcinai B, Cerrano C, Sarà M (1998) Alectona species from north-western Pacific (Demospongiae: Clionidae). J Mar Biolog Assoc UK 78(1):59–73. https://doi.org/10.1017/S0025315400039965

    Article  Google Scholar 

  • Bax NN, Cairns SD (2014) Stylasteridae (Cnidaria; Hydrozoa). In: Danis AP, David B, Grant S, Gutt J, Held C, Hosie G, Huettman F, Post A, Ropert-Coudert Y (eds) De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem d’Acoz, C d’ Van de Putte. Biogeographic Atlas of the Southern Ocean. Scientific Committee on Antarctic Research, Cambridge, pp 107–112

    Google Scholar 

  • Bell JJ (2008) The functional roles of marine sponges. Estuar Coast Shelf Sci 79:341–353. https://doi.org/10.1016/j.ecss.2008.05.002

    Article  Google Scholar 

  • Bertolino M, Ricci S, Canese S, Cau A, Bavestrello G, Pansini M, Bo M (2019) Diversity of the sponge fauna associated with white coral banks from two Sardinian canyons (Mediterranean Sea). J Mar Biol Assoc UK 99(8):1735–1751. https://doi.org/10.1017/S0025315419000948

    Article  CAS  Google Scholar 

  • Buhl-Mortensen L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, Buhl-Mortensen P, Gheerardyn H, King NJ, Raes M (2010) Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Mar Ecol 31(1):21–50. https://doi.org/10.1111/j.1439-0485.2010.00359.x

    Article  Google Scholar 

  • Burton M (1932) Sponges. Discov Rep 6:237–392

    Article  Google Scholar 

  • Cairns SD (1983) Antarctic and sub-Antarctic Stylasterina (Coelenterata: Hydrozoa). Antarct Res Ser 38:61–164

    Article  Google Scholar 

  • Cairns SD (2011) Global diversity of the stylasteridae (Cnidaria: Hydrozoa: Athecatae). PLoS One 6(7):e21670. https://doi.org/10.1371/journal.pone.0021670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cárdenas P, Pérez T, Boury-Esnault N (2012) Sponge Systematics Facing New Challenges. In: Becerro MA, Uriz MJ, Maldonado M, Turon X (ed). Advances in Sponge Science: Phylogeny, Systematics, Ecology. Adv Mar Biol 61:79–209

  • Carter HJ (1875) Notes introductory to the study and classification of the Spongida. Part II. Proposed classification of the Spongida. Ann Mag Nat Hist 4(16):126–145

  • Carter HJ (1879) Contributions to our knowledge of the Spongida. Ann Mag Nat Hist 3(5):284–304

    Article  Google Scholar 

  • Cerrano C, Calcinai B, Bertolino M, Valisano L, Bavestrello G (2006) Epibionts of the scallop Adamussium colbecki (Smith, 1902) in the Ross Sea. Antarctica Chem Ecol 22(sup1):S235–S244. https://doi.org/10.1080/02757540600688101

    Article  Google Scholar 

  • Cerrano C, Calcinai B, Di Camillo CG, Valisano L, Bavestrello G (2007) How and why do sponges incorporate foreign material? Strategies in Porifera. In: Custódio MR, Hajdu E, Lôbo-Hajdu G, Muricy G (eds) Porifera research: biodiversity, innovation and sustainability. Museum Nacional, Rio de Janeiro, pp 239–246

    Google Scholar 

  • Cerrano C, Bertolino M, Valisano L, Bavestrello G, Calcinai B (2009) Epibiotic demosponges on the Antarctic scallop Adamussium colbecki (Smith, 1902) and the cidaroid urchins Ctenocidaris perrieri Koehler, 1912 in the nearshore habitats of the Victoria Land, Ross Sea. Antarctica Polar Biol 32(7):1067–1076. https://doi.org/10.1007/s00300-009-0606-5

    Article  Google Scholar 

  • Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Austral Ecol 18(1):117–143. https://doi.org/10.1111/j.1442-9993.1993.tb00438.x

    Article  Google Scholar 

  • Dendy A (1924) Porifera. Part I. Non-Antarctic sponges. Natural History Report. British Antarctic (Terra Nova) Expedition, 1910 (Zoology). 6 (3):269–392

  • Di Camillo CG, Bavestrello G, Cerrano C, Gravili C, Piraino S, Puce S, Boero F (2017) Hydroids (Cnidaria, Hydrozoa): a neglected component of animal forests. Mar Anim Forest 20:397–427. https://doi.org/10.1007/978-3-319-21012-4_11

    Article  Google Scholar 

  • Etnoyer P, Morgan LE (2006) Habitat-forming deep-sea corals in the Northeast Pacific Ocean. In: Freiwald A, Roberts JM (eds) Cold-water corals and ecosystems. Springer, Berlin, Heidelberg, pp 331–343

    Google Scholar 

  • Garcia TM, Matthews-Cascon H, Franklin-Junior W (2009) Millepora alcicornis (Cnidaria: Hydrozoa) as substrate for benthic fauna. Braz J Oceanogr 57(2):153–155. https://doi.org/10.1590/S1679-87592009000200009

    Article  Google Scholar 

  • Gili JM, Abellò P, Villanueva R, (1993) Epibionts and intermolt duration in the crab Bathynectes piperitus. Mar Ecol Prog Ser 98:107–113

    Article  Google Scholar 

  • Goodwin CE, Berman J, Downey RV, Hendry KR (2017) Carnivorous sponges (Porifera : Demospongiae : Poecilosclerida : Cladorhizidae) from the Drake Passage (Southern Ocean) with a description of eight new species and a review of the family Cladorhizidae in the Southern Ocean. Inverteb Syst 31(1):37–64

  • Gutt J, Cummings V, Dayton P, Isla E, Jentsch A, Schiaparelli S (2017) Antarctic Marine Animal Forests: Three-Dimensional Communities in Southern Ocean Ecosystems. In: Rossi S, Bramanti L, Gori A, Orejas Saco del Valle C (ed). Marine Animal Forests: The Ecology of Benthic Biodiversity Hotspots, Springer International Publishing, Switzerland, pp 30

  • Gutt J, Schickan T (1998) Epibiotic relationship in the Antarctic benthos. Antarct Sci 10:398–405. https://doi.org/10.1017/S0954102098000480

    Article  Google Scholar 

  • Häussermann V, Försterra G (2007) Extraordinary abundance of hydrocorals (Cnidaria, Hydrozoa, Stylasteridae) in shallow water of the Patagonian fjord region. Polar Biol 30(4):487–492. https://doi.org/10.1007/s00300-006-0207-5

    Article  Google Scholar 

  • Heifetz J (2002) Coral in Alaska: distribution, abundance, and species associations. Hydrobiologia 471:19–28. https://doi.org/10.1023/A:1016528631593

    Article  Google Scholar 

  • Heip C, Hummel H, van Avesaath P, Appeltans W, Arvanitidis C, Aspden R, Austen M, Boero F, Bouma TJ, Boxshall G, Buchholz F, Crowe T, Delaney A, Deprez T, Emblow C, Feral JP, Gasol JM, Gooday A, Harder J, Ianora A, Kraberg A, Mackenzie B, Ojaveer H, Paterson D, Rumohr H, Schiedek D, Sokolowski A, Somerfield P, Sousa Pinto I, Vincx M, Weslawski J, Nash R (2009) Marine biodiversity and ecosystem functioning. Printbase, Dublin

  • Hentschel E (1914) Monaxone Kieselschwämme und Hornschwämme der Deutschen Südpolar-Expedition 1901–1903. Deutsche Südpolar-Expedition 15(1):35–141

    Google Scholar 

  • Hughes TP, Bellwood DR, Connolly SR (2002) Biodiversity hotspots, centres of endemicity, and the conservation of coral reefs. Ecol Lett 5(6):775–784. https://doi.org/10.1046/j.1461-0248.2002.00383.x

    Article  Google Scholar 

  • Jensen A, Frederiksen R (1992) The fauna associated with the bank-forming deepwater coral Lophelia pertusa (Scleractinaria) on the Faroe shelf. Sarsia 77(1):53–69. https://doi.org/10.1080/00364827.1992.10413492

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386. https://doi.org/10.1007/978-1-4612-4018-1_14

    Article  Google Scholar 

  • Kirkpatrick R (1907) Preliminary report on the monaxonellida of the national antarctic expedition. Ann Mag Nat Hist 7(20):271–291

    Article  Google Scholar 

  • Kirkpatrick R (1908) Porifera (Sponges). II. Tetraxonida, Dendy. National Antarctic Expedition, 1901–1904 Natural History. (4)Zool: 1–56

  • Koltun VM (1964) Sponges of the Antarctic. 1 Tetraxonida and Cornacuspongida. In: Pavlovskii EP, Andriyashev AP, Ushakov PV (ed) Biological Reports of the Soviet Antarctic Expedition (1955–1958). pp 6–133, 443–448.

  • Lendenfeld RV (1907) Tetraxonia der Deutschen Südpolar-Expedition 1901–1903. In: Drygalski EV (ed) Deutsche Südpolar-Expedition 1901–1903. Zool 1:303–342.

  • Linley TD, Lavaleye M, Maiorano P, Bergman M, Capezzuto F, Cousins NJ, D’Onghia G, Duineveld G, Shields MA, Sion L, Tursi A, Priede IG (2017) Effects of cold-water corals on fish diversity and density (European continental margin: arctic, NE Atlantic and Mediterranean Sea): Data from three baited lander systems. Deep Sea Res II: Top Stud Oceanogr 145:8–21. https://doi.org/10.1016/j.dsr2.2015.12.003

    Article  Google Scholar 

  • Lopes DA, Bravo A, Hajdu E (2011) New carnivorous sponges (Cladorhizidae: Poecilosclerida: Demospongiae) from Diego Ramirez Archipelago (south Chile), with comments on taxonomy and biogeography of the family. Invertebr Syst 25:407–443. https://doi.org/10.1071/IS11015

    Article  Google Scholar 

  • Melis R, Capotondi L, Torricella F, Ferretti P, Geniram A, Hong JK, Kuhn G, Khim B-k, Kim S, Malinverno E, Yoo KC, Colizza E (2021) Last glacial maximum to holocene paleoceanography of the northwestern ross sea inferred from sediment core geochemistry and micropaleontology at Hallett Ridge. J Micropalaeontol 40(1):15–35. https://doi.org/10.5194/jm-40-15-2021

    Article  Google Scholar 

  • Messmer V, Jones GP, Munday PL, Holbrook SJ, Schmitt RJ, Brooks AJ (2011) Habitat biodiversity as a determinant of fish community structure on coral reefs. Ecol 92(12):2285–2298. https://doi.org/10.1890/11-0037.1

    Article  Google Scholar 

  • Miller J, Mundy K, Lindsay CN, Chadderton W (2004) Ecological and genetic evidence of the vulnerability of shallow-water populations of the stylasterid hydrocoral Errina novaezelandiae in New Zealand’s fiords. Aquat Conserv 14(1):75–94. https://doi.org/10.1002/aqc.597

    Article  Google Scholar 

  • Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool 12(1):7. https://doi.org/10.1186/s12983-015-0099-8

    Article  PubMed  PubMed Central  Google Scholar 

  • Moseley HN (1879) On the structure of the Stylasteridae, a family of the hydroid stony corals. Philos Trans R Soc Lond 169(2):425–503

  • Pham CK, Murillo FJ, Lirette C, Maldonado M, Colaço A, Ottaviani D, Kenchington E (2019) Removal of deep-sea sponges by bottom trawling in the Flemish Cap area: conservation, ecology and economic assessment. Sci Rep 9(1):1–13. https://doi.org/10.1038/s41598-019-52250-1

    Article  CAS  Google Scholar 

  • Pica D, Bertolino M, Calcinai B, Puce S, Bavestrello G (2012) Boring and cryptic sponges in stylasterids (Cnidaria: Hydrozoa). It J Zool 79(2):266–272. https://doi.org/10.1080/11250003.2011.632384

    Article  Google Scholar 

  • Pica D, Bavestrello G, Puce S (2018) First record of Lepidopora (Hydrozoa: Stylasteridae) from the North Pacific Ocean with description of a new species. Pac Sci 72(2):245–250. https://doi.org/10.2984/72.2.6

    Article  Google Scholar 

  • Pica D, Cairns SD, Puce S, Newman WA (2015) Southern hemisphere deep-water stylasterid corals including a new species, Errina labrosa sp. n. (Cnidaria, Hydrozoa, Stylasteridae), with notes on some symbiotic scalpellids (Cirripedia, Thoracica, Scalpellidae). ZooKeys (472):1. https://doi.org/10.3897/zookeys.472.8547

  • Plaisance L, Knowlton N, Paulay G, Meyer C (2009) Reef-associated crustacean fauna: biodiversity estimates using semi-quantitative sampling and DNA barcoding. Coral Reefs 28(4):977–986. https://doi.org/10.1007/s00338-009-0543-3

    Article  Google Scholar 

  • Post AL, O’Brien PE, Beaman RJ, Riddle MJ, De Santis L (2010) Physical controls on deep water coral communities on the George V Land slope. East Antarctica Antarct Sci 22(4):371–378. https://doi.org/10.1017/S0954102010000180

    Article  Google Scholar 

  • Ridley SO, Dendy A (1886) Preliminary report on the monaxonida collected by H.M.S. challenger. Part i Ann Mag Nat Hist 18:325–351

    Article  Google Scholar 

  • Rimondino C, Torre L, Sahade R, Tatian M (2015) Sessile macro-epibiotic community of solitary ascidians, ecosystem engineers in soft substrates of Potter Cove. Antarctica Polar Res 34(1):24338. https://doi.org/10.3402/polar.v34.24338

    Article  Google Scholar 

  • Roberts CM, McClean CJ, Veron JE, Hawkins JP, Allen GR, McAllister DE, Mittermeier CG, Schueler FW, Spalding M, Wells F, Vynne C, Werner TB (2002) Marine biodiversity hotspots and conservation priorities for tropical reefs. Science 295(5558):1280–1284. https://doi.org/10.1126/science.1067728

    Article  CAS  PubMed  Google Scholar 

  • Rützler K (1978) Sponges in coral reefs. In: Stoddart DR, Johannes RE (ed) Coral Reefs: Research Methods: 299–313. Monographs on Oceanographic Methodology 5, Unesco, Paris.

  • Salvati E, Angiolillo M, Bo M, Bavestrello G, Giusti M, Cardinali A, Puce S, Spaggiari C, Greco S, Canese S (2010) The population of Errina aspera (Hydrozoa: Stylasteridae) of the Messina Strait (Mediterranean Sea). J Mar Biol Ass UK 90(1331):1336. https://doi.org/10.1017/S0025315410000950

    Article  Google Scholar 

  • Sarà M, Corriero G, Bavestrello G (1993) Tethya (Porifera, Demosponglae) species coexisting in a maldivian coral reef lagoon: taxonomical, genetic and ecological data. Mar Ecol 14(4):341–355. https://doi.org/10.1111/j.1439-0485.1993.tb00005.x

    Article  Google Scholar 

  • Schejter L, Genzano G, Gaitán E, Pérez CD, Bremec CS (2020) Benthic communities in the Southwest Atlantic Ocean: conservation value of animal forests at the Burdwood Bank slope. Aquat Conserv 30:426–439. https://doi.org/10.1002/aqc.3265

    Article  Google Scholar 

  • Schmidt O (1862) Die Spongien des adriatischen Meeres. Wilhelm Engelmann (ed). Leipzig

  • Schulze FE (1880) Untersuchungen über den Bau und die Entwicklung der Spongien. Neunte Mittheilung. Die Plakiniden. Zeitschrift für wissenschaftliche Zoologie 34(2):407–451

  • Van Soest RW, Hooper JN, Butler PJ (2020) Every sponge its own name: removing Porifera homonyms. Zoot 4745(1):1–93. https://doi.org/10.11646/ZOOTAXA.4745.1.1

  • Sollas WJ (1885) A classification of the sponges. Ann Mag Nat Hist 16(95)

  • Solórzano MR (1990) Poriferos del litoral gallego: estudio faunístico, distribución e inventariado. Dissertation, Universidade de Santiago de Compostela

  • Thiele J (1905) Die Kiesel-und Hornschwämme der Sammlung Plate. Zoologische Jahrbücher Supplement 6 (Fauna Chilensis III). 407–496.

  • Topsent E (1901) Spongiaires. Résultats du voyage du S.Y. ‘Belgica’en 1897–99 sous le commandement de A. de Gerlache de Gomery. Expédition Antarctique Belge Zool 4:1–54

    Google Scholar 

  • Topsent E (1907) Poecilosclérides nouvelles recueillies par le Français dans l’Antarctique. Bulletin Du Muséum National D’histoire Naturelle, Paris 13:69–76

    Google Scholar 

  • Topsent E (1908) Spongiaires. Expédition antarctique française (1903–1905) commandée par le Dr Jean Charcot (Paris). 4:1–37.

  • Topsent E (1916) Diagnoses d’éponges recueillies dans l’Antarctique par le Pourquoi-Pas?. Bull Mus Natl Hist Nat(1). 22(3): 163–172.

  • de Voogd NJ, Alvarez B, Boury-Esnault N, Carballo JL, Cárdenas P, Díaz MC, Dohrmann M, Downey R, Hajdu E, Hooper JNA, Kelly M, Klautau M, Manconi R, Morrow CC, Pisera AB, Ríos P, Rützler K, Schönberg C, Vacelet J, van Soest RWM (2021) World Porifera Database. At http://www.marinespecies.org/porifera on 2021–12. Accessed May 2021

  • Wisshak M, Correa ML, Zibrowius H, Jakobsen J, Freiwald A (2009) Skeletal reorganisation affects geochemical signals, exemplified in the stylasterid hydrocoral Errina dabneyi (Azores Archipelago). Mar Ecol Prog Ser 397:197–208. https://doi.org/10.3354/meps08165

    Article  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Tim McNelis for correcting the English language. The authors are grateful to the three reviewers for their criticisms, corrections and advice, and we are very grateful to the non-anonymous reviewer Dr. Dorte Janussen for the compliments on our manuscript.

Funding

The project PNRA-GRACEFUL (Grant No. PNRA16_00069) contributed to the study providing the stylasterid samples, video footage and still photographs of the seafloor of the Ross Sea.

Author information

Authors and Affiliations

  1. Department of Earth, Environment and Life Sciences (DISTAV), University of Genoa, Genoa, Italy

    Gabriele Costa, Giorgio Bavestrello, Martina Canessa, Stefano Schiaparelli & Marco Bertolino

  2. Stazione Zoologica Anton Dohrn, Naples, Italy

    Simonepietro Canese

  3. Department of Geosciences, University of Padova, Padova, Italy

    Claudio Mazzoli

  4. Institute of Polar Sciences (ISP-CNR), Bologna, Italy

    Paolo Montagna

  5. Department of Life and Environmental Sciences (DiSVA), Polytechnic University of Marche, Ancona, Italy

    Stefania Puce

  6. Italian National Antarctic Museum (MNA, Section of Genoa), University of Genoa, Genoa, Italy

    Stefano Schiaparelli

Authors
  1. Gabriele Costa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Giorgio Bavestrello
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Simonepietro Canese
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Martina Canessa
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Claudio Mazzoli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Paolo Montagna
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Stefania Puce
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Stefano Schiaparelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marco Bertolino
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

G.C. and M.B. identified the sponge samples and wrote the first draft of the manuscript. M.C. analysed the data at a statistical level. S.C. and C.M. collected samples during Antarctic expedition. S.P. identified the stylasterid samples. G.B., M.C., P.M. and S.S. contributed to improve the final version of the manuscript. All authors contributed to manuscript corrections and improved the final version.

Corresponding author

Correspondence to Gabriele Costa.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and institutional guidelines for animal testing, animal care, and use of animals were followed by the authors.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities and are mentioned in the text.

Additional information

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 (DOCX 33 kb)

Supplementary file2 (DOCX 34 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Costa, G., Bavestrello, G., Canese, S. et al. Sponges associated with stylasterid thanatocoenosis (Cnidaria, Hydrozoa) from the deep Ross Sea (Southern Ocean). Polar Biol 45, 703–718 (2022). https://doi.org/10.1007/s00300-022-03023-6

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-022-03023-6

Keywords

Search

Navigation