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Marine Biodiversity

, Volume 49, Issue 5, pp 2369–2380 | Cite as

Distribution and swimming ability of the deep-sea holothuroid Penilpidia ludwigi (Holothuroidea: Elasipodida: Elpidiidae)

  • G. ChimientiEmail author
  • R. Aguilar
  • A. V. Gebruk
  • F. Mastrototaro
Original Paper

Abstract

The deep-sea elpidiid holothuroid, Penilpidia ludwigi, was recorded using a Remotely Operated Vehicle in the Western, Central, and Eastern Mediterranean Sea. This species, endemic to the basin, was previously captured above the seabed in sediment traps and based on these records its swimming ability was assumed. The present study reports the first in situ observations of swimming P. ludwigi and provides an update on the geographic and bathymetric distribution of this species. A large aggregation of thousands of specimens was observed in the Levantine Sea with a maximum local density 300 ind. m−2. The ROV surveys allowed observation of the behavior of the species and description of its mode of swimming. Active swimming using strokes of the tentacle crown is combined with drifting benefiting of the current, the former used for fast escape the latter mainly for energy-saving displacement. Swimming behavior allows P. ludwigi to exploit various deep-sea habitats including seamounts, canyons, and ridges inaccessible to non-swimming deposit feeders.

Keywords

Elpidiid Sea cucumber Behavior Biogeography ROV Mediterranean Sea 

Notes

Acknowledgements

This study was funded by the MAVA Fondation pour la Nature, IF International Foundation, Smile-Wave Fund, Pictet Charitable Foundation, Adessium Foundation, Robertson Foundation, the Foundation for the Third Millennium, Fundación Biodiversidad, Spanish Ministerio de Agricultura, Alimentación y Medio Ambiente, and National Geographic (Grant EC-176R-18).

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interest.

Ethical approval

No animal testing was performed during this study.

Sampling and field studies

All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities. The study is compliant with CBD and Nagoya protocols.

Data availability

The datasets generated during and/or analyzed for the current study are available from the corresponding author upon request.

References

  1. Acosta J, Munõz A, Herranz P, Palomo C, Ballesteros M, Vaquero M, Uchupi E (2001a) Geodynamics of the Emile Baudot escarpment and the Balearic Promontory, western Mediterranean. Mar Pet Geol 18:349–369.  https://doi.org/10.1016/S0264-8172(01)00003-4 CrossRefGoogle Scholar
  2. Acosta J, Munõz A, Herranz P, Palomo C, Ballesteros M, Vaquero M, Uchupi E (2001b) Pockmarks in the Ibiza Channel and western end of the Balearic Promontory (western Mediterranean) revealed by multibeam mapping. Geo-Mar Lett 21:123–130.  https://doi.org/10.1007/s003670100074 CrossRefGoogle Scholar
  3. Acosta J, Canals M, Carbó A, Muñoz A, Urgeles R, Muñoz-Martı́n A, Uchupi E (2004) Sea floor morphology and Plio-Quaternary sedimentary cover of the Mallorca Channel, Balearic Islands, western Mediterranean. Mar Geol 206:165–179.  https://doi.org/10.1016/j.margeo.2004.02.008 CrossRefGoogle Scholar
  4. Aguilar R, López Correa M, Calcinai B, Pastor X, De la Torriente A, Garcia S (2011) First records of Asbestopluma hypogea Vacelet and Boury-Esnault, 1996 (Porifera, Demospongiae Cladorhizidae) on seamounts and in bathyal settings of the Mediterranean Sea. Zootaxa 2925:33–40CrossRefGoogle Scholar
  5. Andrès A (1880) Prodromus neapolitanae actiniarum faunae, addio generalis actiniarum bibliographiae catalogo. Mittheil Zool Stat Neapel 2:305–371Google Scholar
  6. Angeletti L, Taviani M, Canese S, Foglini F, Mastrototaro F, Argnani A, Trincardi F, Bakran-Petricioli T, Ceregato A, Chimienti G, Mačić V, Poliseno A (2014) New deep-water cnidarian sites in the southern Adriatic Sea. Mediterr Mar Sci 15(2):263–273.  https://doi.org/10.12681/mms.558 CrossRefGoogle Scholar
  7. Barnes AT, Quetin LB, Childress JJ, Pawson DL (1976) Deep-sea macroplanktonic sea cucumbers: suspended sediment feeders captured from deep submergence vehicle. Science 194:1083–1085.  https://doi.org/10.1126/science.194.4269.1083 CrossRefPubMedGoogle Scholar
  8. Bett BJ, Malzone G, Narayanaswamy EB, Wigham BD (2001) Temporal variability in phytodetritus and megabenthic activity at the seabed in the deep Northeast Atlantic. Prog Oceanogr 50:349–368.  https://doi.org/10.1016/S0079-6611(01)00066-0 CrossRefGoogle Scholar
  9. Billett DSM (1991) Deep-sea holothurians. Oceanogr Mar Biol Annu Rev 29:259–317Google Scholar
  10. Billett DSM, Hansen B (1982) Abyssal aggregations of Kolga hyalina Danielssen and Koren (Echinodermata: Holothurioidea) in the Northeast Atlantic Ocean, a preliminary report. Deep Sea Res A 29:799–818.  https://doi.org/10.1016/0198-0149(82)90047-4 CrossRefGoogle Scholar
  11. Billett DSM, Lampitt RS, Rice AL, Mantoura RFC (1983) Seasonal sedimentation of phytoplankton to the deep-sea benthos. Nature 302:520–522.  https://doi.org/10.1038/302520a0 CrossRefGoogle Scholar
  12. Chimienti G, Angeletti L, Mastrototaro F (2018a) Withdrawal behaviour of the red sea pen Pennatula rubra (Cnidaria: Pennatulacea). Eur Zool J 85(1):64–70.  https://doi.org/10.1080/24750263.2018.1438530 CrossRefGoogle Scholar
  13. Chimienti G, Angeletti L, Rizzo L, Tursi A, Mastrototaro F (2018b) ROV vs trawling approaches in the study of benthic communities: the case of Pennatula rubra (Cnidaria: Pennatulacea). J Mar Biol Assoc UK 98(8):1859–1869.  https://doi.org/10.1017/S0025315418000851 CrossRefGoogle Scholar
  14. Chimienti G, Bo M, Mastrototaro F (2018c) Know the distribution to assess the changes: Mediterranean cold-water coral bioconstructions. Rend Lincei Sci Fis Nat 29:583–588.  https://doi.org/10.1007/s12210-018-0718-3 CrossRefGoogle Scholar
  15. Chimienti G, Bo M, Taviani M, Mastrototaro F (2019) Occurrence and biogeography of Mediterranean cold-water corals. In: Orejas C, Jiménez C (eds) Mediterranean cold-water corals: past, present and future, Coral Reefs of the World 9, 213–243. Springer International Publishing.  https://doi.org/10.1007/978-3-319-91608-8_19 CrossRefGoogle Scholar
  16. Danielssen D, Koren J (1879) Fra den norske Nordhavsexpedition. Echinodermer 3. Nyt Mag Naturvid 25:83–140Google Scholar
  17. El Hourany R, Fadel A, Gemayel E, Abboud-Abi Saab M, Faour G (2017) Spatio-temporal variability of the phytoplankton biomass in the Levantine basin between 2002 and 2015 using MODIS products. Oceanologia 59:153–165.  https://doi.org/10.1016/j.oceano.2016.12.002 CrossRefGoogle Scholar
  18. Esper EJC (1788) Die Pflanzenthiere in Abbildungen nach der Natur : mit Farben erleuchtet nebst Beschreibungen. Nürnberg: Raspische Buchhandlung 1(1–2):1–96Google Scholar
  19. Fabricius JC (1775) Systema Entomologiae, sistens Insectorum classes, Ordines, genera, species, adiectis Synonymis, Locis, Descriptionibus, Observationibus. Flensbvrgi et Lipsiae. In: Officina Libraria Kortii, 832Google Scholar
  20. Fiege D, Liao Y (1996) Penilpidia ludwigi (Marenzeller, 1893) (Holothuroidea. Elpidiidae) rediscovered from the eastern Mediterranean Sea. In: Uiblein F, Ott J, Stachowitsch M (eds) Deep-sea and extreme shallow-water habitats: affinities and adaptations. Österreichische Akademie der Wissenschaften, Vienna. Biosystematics and Ecology Series 11:61–66Google Scholar
  21. Gebruk AV (1988) New taxa of abyssal sea cucumbers of the family Elpidiidae (Elasipoda). Zool Zhurnal 67(6):914–922Google Scholar
  22. Gebruk AV (1990) Deep-sea holothurians of the family Elpidiidae. Nauka, Moscow, p 160Google Scholar
  23. Gebruk AV (1994) Two main stages in the evolution of the deep-sea fauna of elasipodid holothurians. In: Guille D, Roux F (eds) Echinoderm through time. Balkema, Rotterdam, pp 507–513Google Scholar
  24. Gebruk AV (2008) Holothurians (Holothuroidea, Echinodermata) of the northern Mid-Atlantic Ridge collected by the G.O. Sars MAR-ECO expedition with descriptions of four new species. Mar Biol Res 4:48–60CrossRefGoogle Scholar
  25. Gebruk AV, Rogacheva AV, Pawson DL, Hamel JF, Macisaac KG, Mercier A (2013) Penilpidia desbarresi sp. nov. (Echinodermata: Holothuroidea: Elasipodida) from the upper slope of Newfoundland and re-description of P. ludwigi (von Marenzeller, 1893). Mar Biol Res 9:1029–1036.  https://doi.org/10.1080/17451000.2013.793810 CrossRefGoogle Scholar
  26. Haedrich RL, Maunder JE (1985) The echinoderm fauna of the Newfoundland continental slope. In: Keegan BF, O’Connor BDS (eds) Echinodermata. Proceedings of the Fifth International Echinoderm Conference, Galway, 24–29 September 1984. Balkema, Rotterdam, pp 37–46Google Scholar
  27. Hamel JF, Sun J, Gianasi BL, Montgomery EM, Kenchington EL, Burel B, Rowe S, Winger PD, Mercier A (2019) Active buoyancy adjustment increases dispersal potential in benthic marine animals. J Anim Ecol 88:820–832.  https://doi.org/10.1111/1365-2656.12943 CrossRefGoogle Scholar
  28. Hansen B (1975) Systematics and biology of the deep-sea holothurians. Part. 1. Elasipoda. Scientific results of the Danish Deep-Sea Expedition Round the World 1950–52, Galathea Report 13:1–262Google Scholar
  29. IEO (Instituto Español de Oceanografía) (2005) Mar Balear: Mapa topobatimétrico del Mar Balear y Golfo de Valencia. Ministerio de Educación y Ciencia, Instituto Español de Oceanografía. 1:500.000; Proyec. UTM Huso. Instituto Español de Oceanografía, Madrid, p 31NGoogle Scholar
  30. Knittweis L, Evans J, Aguilar R, Álvarez H, Borg JA, García S, Schembri PJ (2019) Recent discoveries of extensive cold-water coral assemblages in Maltese waters. In: Orejas C, Jiménez C (eds) Mediterranean cold-water corals: past, present and future, Coral Reefs of the World. Springer International Publishing. 22:253–256Google Scholar
  31. Lastras G, Canals M, Ballesteros E, Gili J-M, Sanchez-Vidal A (2016) Cold-water corals and anthropogenic impacts in La Fonera submarine canyon head, northwestern Mediterranean Sea. PLoS One 11(5):e0155729.  https://doi.org/10.1371/journal.pone.0155729 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Madsen FJ, Hansen B (1994) Echinodermata, Holothurioidea. Marine invertebrates of Scandinavia 9. Scandinavian University Press, Copenhagen, p 143Google Scholar
  33. Marenzeller E von (1893) Berichte der Commission für Erforschung des östlichen Mittelmeeres. Zoologische Ergebnisse, 1. Echinodermen gesammelt 1890, 1891 und 1892. Denkschriften Kaiserlichen Akademie Wissenschaften, WienGoogle Scholar
  34. Mastrototaro F, Aguilar R, Chimienti G, Gravili C, Boero F (2016) The rediscovery of Rosalinda incrustans (Cnidaria: Hydrozoa) in the Mediterranean Sea. Ital J Zool 83(2):244–247.  https://doi.org/10.1080/11250003.2016.1181800 CrossRefGoogle Scholar
  35. Mastrototaro F, Chimienti G, Acosta J, Blanco J, Garcia S, Rivera J, Aguilar R (2017) Isidella elongata (Cnidaria: Alcyonacea) facies in the western Mediterranean Sea: visual surveys and descriptions of its ecological role. Eur Zool J 84(1):209–225CrossRefGoogle Scholar
  36. Mecho A, Billett DSM, Ramírez-Llodra E, Aguzzi J, Tyler PA, Company JB (2014) First records, rediscovery and compilation of deep-sea echinoderms in the middle and lower continental slope of the Mediterranean Sea. Sci Mar 78(2):281–302.  https://doi.org/10.3989/scimar.03983.30C CrossRefGoogle Scholar
  37. Miller JE, Pawson DL (1990) Swimming sea cucumbers (Echinodermata: Holothuroidea): a survey, with analysis of swimming behavior in four bathyal species. Smithson Contrib Mar Sci (35):1–16.  https://doi.org/10.5479/si.01960768.35.1
  38. Ohta S (1985) Photographic observations of the swimming behavior of the deep-sea pelagothuriid holothurian Enypniastes (Elasipoda, Holothurioidea). J Oceanogr Soc Jpn 41:121–133.  https://doi.org/10.1007/BF02109182 CrossRefGoogle Scholar
  39. Pagès F, Martín J, Palanques A, Puíg P, Gílí J-M (2007) High occurrence of the elasipodid holothurian Penilpidia ludwigi (von Marenzeller, 1893) in bathyal sediment traps moored in a western Mediterranean submarine canyon. Deep-Sea Res Pt I 54:2170–2180.  https://doi.org/10.1016/j.dsr.2007.09.002 CrossRefGoogle Scholar
  40. Pawson DL, Foell EJ (1986) Peniagone leander new species, an abyssal benthopelagic sea cucumber (Echinodermata: Holothuroidea) from the eastern Central Pacific Ocean. Bull Mar Sci 38(2):293–299Google Scholar
  41. Perrier E (1886) Les explorations sous-marines. Librairie Hachette et Cie, Paris, p 352Google Scholar
  42. Rafinesque CS (1810) Caratteri di alcuni nuovi generi e nuove specie di animali e piante della sicilia, con varie osservazioni sopra i medisimi. Per le stampe di Sanfilippo, Palermo, Italy, p 105CrossRefGoogle Scholar
  43. Roberts D, Gebruk A, Levin V, Manship B (2000) Feeding and digestive strategies in deposit-feeding holothurians. Oceanogr Mar Biol 38:257–310Google Scholar
  44. Rogacheva A, Gebruk A, Alt CHS (2012) Swimming deep-sea holothurians (Echinodermata: Holothuroiudea) on the northern Mid-Atlantic Ridge. Zoosymposia 7:213–224CrossRefGoogle Scholar
  45. Rogacheva A, Gebruk A, Alt CHS (2013) Holothuroidea of the Charlie Gibbs Fracture Zone area, northern Mid-Atlantic Ridge. Mar Biol Res 9(5–6):587–623.  https://doi.org/10.1080/17451000.2012.750428 CrossRefGoogle Scholar
  46. Romagnoli C, Casalbore D, Bortoluzzi G, Bosman A, Chiocci FL, D’Oriano F, Gamberi F, Ligi M, Marani M (2013) Bathy-morphological setting of the Aeolian Islands. In: Lucchi F, Peccerillo A, Keller J, Tranne CA, Rossi PL (eds) The Aeolian Islands volcanoes. Geol Soc Lond Mem, 37:27–36.  https://doi.org/10.1144/M37.4 CrossRefGoogle Scholar
  47. Rowe GT (1971) Observations on bottom currents and epibenthic populations in Hatteras submarine canyon. Deep-Sea Res Oceanogr Abstr 18(6):569–581.  https://doi.org/10.1016/0011-7471(71)90123-9 CrossRefGoogle Scholar
  48. Sars M (1867) Om nogle Echinodermer og Coelenterater fra Lofoten. Oversigt over det Kongelige Danske Videnskabernes Selskabs Forhandlingar Christiana:1–7Google Scholar
  49. Sars M (1868) Om Afbildninger af nogle af hans son I forrige Aar ved Lofoten fundne Echinodermer og Coelenterater. Forhandlinger Videnskabs Selskabet, Christiana 19–23Google Scholar
  50. Shirayama Y, Ohta S, Horikoshi M (1985) Some results on the ecology of deep-sea benthos obtained using “SHINKAI 2000”. Technical Reports JAMSTEC Special Issue, pp 119–121Google Scholar
  51. Théel H (1882) Report on the Holothuroidea dredged by H.M.S. ‘Challenger’ during the years 1873-76. Part i. Report on the scientific results of the voyage of H.M.S. Challenger during the years 1873–1876. Zoology 4(13):1–176Google Scholar
  52. Tyler PA, Rice AL, Young CM, Gebruk A (1996) A walk on the deep side: animals in the deep sea. In: Summerhayes CP, Thorpe SA (eds) Oceanography: an illustrated guide. John Wiley, New York, pp 195–211Google Scholar
  53. Wigham BD, Tyler PA, Billett DSM (2003) Reproductive biology of the abyssal holothurian Amperima rosea: an opportunistic response to variable flux of surface derived organic matter? J Mar Biol Assoc UK 83:175–188.  https://doi.org/10.1017/S0025315403006957h CrossRefGoogle Scholar

Copyright information

© Senckenberg Gesellschaft für Naturforschung 2019

Authors and Affiliations

  1. 1.Department of Biology University of Bari Aldo MoroBariItaly
  2. 2.CoNISMaRomeItaly
  3. 3.OceanaMadridSpain
  4. 4.Shirshov Institute of OceanologyRussian Academy of SciencesMoscowRussia

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