Skip to main content
Log in

In situ observations of three deep-sea cephalopods in the central Mediterranean Sea

  • Original paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The development of in situ observational tools has significantly contributed to the study of deep-sea cephalopods and exploration of their habitat in the last decades. In this paper, we report in situ observations of rarely observed deep-sea Mediterranean cephalopods (Chiroteuthis veranyi, Chtenopteryx sicula, and Octopoteuthis sicula). These cephalopods were encountered during a scientific expedition, aimed at characterizing the biodiversity of a deep-sea area in the northern Ionian Sea. Images and video were collected by a remotely operated vehicle (ROV) between 537 and 1248 m. Chromatic, postural, locomotor, and bioluminescent behavioral components were reported for each species. This was the first time that O. sicula was filmed in its habitat and all individuals showed hovering and an arm spread posture with the arm tips exposed, producing an intermittent bioluminescence. Furthermore, our observations on six living specimens of C. sicula represent exceptional events, since this species was only observed once in the eastern Mediterranean in 2012. Overall, five females and a mature male of C. sicula were observed; the male had a large dorsal light organ. Finally, an individual of C. veranyi was observed consuming a large lanternfish (Myctophidae). In the near future, in situ explorations in the Mediterranean should be implemented to shed light on deep-sea cephalopods inhabiting this basin and fill information gaps on the biology, ecology, and behavior of elusive species.

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

Similar content being viewed by others

Data availability

The datasets analysed during the current study are not publicly available but are available from the corresponding author on reasonable request.

References

  • Battaglia P, Pedà C, Sinopoli M, Romeo T, Andaloro F (2013) Cephalopods in the diet of young-of-the- year bluefin tuna (Thunnus thynnus L. 1758, Pisces: Scombridae) from the southern Tyrrhenian Sea (central Mediterranean Sea). It J Zool 80:560–565. https://doi.org/10.1080/11250003.2013.837105

    Article  Google Scholar 

  • Battaglia P, Pedà C, Malara D, Milisenda G, MacKenzie BR, Esposito V, Consoli P, Vicchio TM, Stipa MG, Pagano L, Longo F, Romeo T (2022) Importance of the lunar cycle on mesopelagic foraging by Atlantic bluefin tuna in the upwelling area of the Strait of Messina (Central Mediterranean Sea). Animals 12(17):2261. https://doi.org/10.3390/ani12172261

    Article  PubMed  PubMed Central  Google Scholar 

  • Bello G (1991) Role of cephalopods in the diet of the swordfish, Xiphias gladius, from the eastern Mediterranen sea. Bull Mar Sci 49(1–2):312–324

    Google Scholar 

  • Bello G (1996) Teuthophagous predators as collectors of oceanic cephalopods: the case of the Adriatic Sea. Boll Malacol 32:71–78

    Google Scholar 

  • Bello G (1999) Cephalopods in the diet of albacore, Thunnus alalunga, from the Adriatic Sea. J Molluscan Stud 65:233–240. https://doi.org/10.1093/mollus/65.2.233

    Article  Google Scholar 

  • Bello G, Andaloro F, Battaglia P (2020) Non-indigenous cephalopods in the Mediterranean Sea: a review. Acta Adriat 61(2):113–134. https://doi.org/10.32582/aa.61.2.1

    Article  Google Scholar 

  • Boyle PR, Rodhouse P (2005) Cephalopods: ecology and fisheries. Blackwell Science, Oxford

    Book  Google Scholar 

  • Budelmann BU (1996) Active marine predators: the sensory world of cephalopods. Mar Freshw Behav Physiol 27(2–3):59–75. https://doi.org/10.1080/10236249609378955

    Article  Google Scholar 

  • Burford BP, Robison BH (2020) Bioluminescent backlighting illuminates the complex visual signals of a social squid in the deep sea. Proc Natl Acad Sci 117(15):8524–8531. https://doi.org/10.1073/pnas.1920875117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burford BP, Robison BH, Sherlock RE (2015) Behaviour and mimicry in the juvenile and subadult life stages of the mesopelagic squid Chiroteuthis calyx. J Mar Biol Assoc UK 95(6):1221–1235. https://doi.org/10.1017/S0025315414001763

    Article  Google Scholar 

  • Bush SL (2012) Economy of arm autotomy in the mesopelagic squid Octopoteuthis deletron. Mar Ecol Progr Ser 458:133–140. https://doi.org/10.3354/meps09714

    Article  Google Scholar 

  • Bush SL, Robison BH, Caldwell RL (2009) Behaving in the dark: locomotor, chromatic, postural, and bioluminescent behaviors of the deep-sea squid Octopoteuthis deletron Young 1972. Biol Bull 216(1):7–22. https://doi.org/10.1086/BBLv216n1p7

    Article  PubMed  Google Scholar 

  • Choy CA, Haddock SH, Robison BH (2017) Deep pelagic food web structure as revealed by in situ feeding observations. Proc R Soc B 284(1868):20172116. https://doi.org/10.1098/rspb.2017.2116

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke MR (1977) Beaks, nets and numbers. Proc Zool Soc Lond 38:89–126

    Google Scholar 

  • Clarke MR (1986) A handbook for the identification of cephalopods beaks. Clarendon Press, Oxford

    Google Scholar 

  • Clarke MR (1996a) The role of cephalopods in the world’s oceans: an introduction. Philos Trans R Soc B 351:979–983

    Article  Google Scholar 

  • Clarke MR (1996) Cephalopods as prey. III. Cetaceans. Philos Trans R Soc B 351(1343):1053–1065

    Article  Google Scholar 

  • Cuccu D, Mereu M, Masala P, Cau A, Jereb P (2009) Chiroteuthis veranii and Ommastrephes bartramii (Cephalopoda: Teuthidae) in the Sardinian waters. Biol Mar Medit 16(1):334–335

    Google Scholar 

  • Cuccu D, Cannas R, Mereu M, Follesa MC, Jereb P, Cau A (2013) On the first record of the genus Octopoteuthis (Cephalopoda, Octopoteuthidae) in the Sardinian Channel (central western Mediterranean Sea). Molluscan Res 33(2):135–142. https://doi.org/10.1080/13235818.2013.782795

    Article  Google Scholar 

  • D’Onghia G, Maiorano P, Panetta P (1995) Octopoteuthis sicula (Rüppell, 1844) and Brachioteuthis. Boll Malacol 31(5–8):137–142

    Google Scholar 

  • D’Onghia G, Maiorano P, Panza M, Panetta P (1998) Rinvenimento di Chtenopteryx sicula (Verany, 1851)(Mollusca, Cephalopoda) nel Mar Ionio settentrionale. Biol Mar Medit 5:690–693

    Google Scholar 

  • Escánez A, Roura Á, Riera R, González ÁF, Guerra Á (2018) New data on the systematics of comb-fin squids Chtenopteryx spp. (Cephalopoda: Chtenopterygidae) from the Canary Islands. Zool Stud 57:40. https://doi.org/10.6620/ZS.2018.57-40

    Article  Google Scholar 

  • Férussac AEJPJF d’Audebard de (1835) Note sur deux genres de Céphalopodes encore peu connus, les genres Calmaret et Cranchie, et sur une nouvelle espèce fort remarquable de chacun de ces deux genres. Magasin De Zoologie, Classe V, pp 65–66

  • Foskolos I, Koutouzi N, Polychronidis L, Alexiadou P, Frantzis A (2020) A taste for squid: the diet of sperm whales stranded in Greece, Eastern Mediterranean. Deep Sea Res Part I 155:103164. https://doi.org/10.1016/j.dsr.2019.103164

    Article  Google Scholar 

  • Garibaldi F, Podestà M (2014) Stomach contents of a sperm whale (Physeter macrocephalus) stranded in Italy (Ligurian Sea, north-western Mediterranean). J Mar Biolog Assoc UK 94(6):1087–1091. https://doi.org/10.1017/S0025315413000428

    Article  Google Scholar 

  • Golikov AV, Stauffer JB, Schindler SV, Taylor J, Boehringer L, Purser A, Sabirov RM, Hoving H-J (2023) Miles down for lunch: deep-sea in situ observations of Arctic finned octopods Cirroteuthis muelleri suggest pelagic–benthic feeding migration. Proc R Soc B 290:20230640. https://doi.org/10.1098/rspb.2023.0640

    Article  PubMed  PubMed Central  Google Scholar 

  • Guerra Á (1992) Mollusca, Cephalopoda. In: Ramos MA et al (eds) Fauna Ibérica, vol 1. Museo Nacional de Ciencias Naturales. CSIC, Madrid

    Google Scholar 

  • Hanlon R, Vecchione M, Allcock AL (2018) Octopus, squid and cuttlefish. A visual scientific guide to the oceans’ most advanced invertebrates. University of Chicago Press, Chicago, p 224

    Chapter  Google Scholar 

  • Herring P (2002) The biology of the deep ocean. Oxford University Press, New York

    Google Scholar 

  • Hoving HJ, Robison BH (2012) Vampire squid: detritivores in the oxygen minimum zone. Proc Royal Soc B 279(1747):4559–4567. https://doi.org/10.1098/rspb.2012.1357

    Article  Google Scholar 

  • Hoving HJT, Lipiński MR, Videler JJ (2008) Reproductive system and the spermatophoric reaction of the mesopelagic squid Octopoteuthis sicula (Rüppell 1844) (Cephalopoda: Octopoteuthidae) from southern African waters. Afr J Mar Sci 30(3):603–612. https://doi.org/10.2989/AJMS.2008.30.3.13.647

    Article  Google Scholar 

  • Hoving HJ, Bush SL, Robison BH (2012) A shot in the dark: same-sex sexual behaviour in a deep-sea squid. Biol Lett 8(2):287–290. https://doi.org/10.1098/rsbl.2011.0680

    Article  PubMed  Google Scholar 

  • Hoving HJ, Zeidberg LD, Benfield MC, Bush SL, Robison BH, Vecchione M (2013) First in situ observations of the deep-sea squid Grimalditeuthis bonplandi reveal unique use of tentacles. Proc Royal Soc B 280(1769):20131463. https://doi.org/10.1098/rspb.2013.1463

    Article  Google Scholar 

  • Hoving HJT, Perez JAA, Bolstad KS, Braid HE, Evans AB, Fuchs D, Judkins H, Kelly JT, Marian JEAR, Nakajima R, Piatkowski U, Reid A, Vecchione M, Xavier JCC (2014) The study of deep-sea cephalopods. Adv Mar Biol 67:235–359

    Article  Google Scholar 

  • Hoving HJT, Christiansen S, Fabrizius E, Hauss H, Kiko R, Linke P, Neitzel P, Piatkowski U, Körtzinger A (2019) The pelagic in situ observation system (PELAGIOS) to reveal biodiversity, behavior, and ecology of elusive oceanic fauna. Ocean Sci 15:1327–1340. https://doi.org/10.5194/os-15-1327-2019

    Article  CAS  Google Scholar 

  • Jamieson AJ, Vecchione M (2022) Hadal cephalopods: first squid observation (Oegopsida, Magnapinnidae, Magnapinna sp.) and new records of finned octopods (Cirrata) at depths> 6000 m in the Philippine trench. Mar Biol 169(1):1–5. https://doi.org/10.1007/s00227-021-03993-x

    Article  Google Scholar 

  • Jereb P, Roper CFE (2010) Cephalopods of the world. an annotated and illustrated catalogue of cephalopod species known to date. Volume 2. Myopsid and Oegopsid Squids. FAO Species Catalogue for Fishery Purposes 4., FAO. 630 pp

  • Jereb P, Cannas R, Maiorano P, Bello G, Garibaldi F, Mereu M, Ancona FG, Ammendolia G, Battaglia P, Duysak Ö, Hoving HJT, Lefkaditou E, Lipinski MR, Melis R, Peristeraki PN, Ragonese S, Romeo T, Salman A, Santos MB, Villari A, Cuccu D (2016) The deep-water squid Octopoteuthis sicula Rüppell, 1844 (Cephalopoda: Octopoteuthidae) as the single species of the genus occurring in the Mediterranean Sea. Mar Biol 163(9):192. https://doi.org/10.1007/s00227-016-2965-0

    Article  Google Scholar 

  • Joubin L (1900) Cephalopodes provenant des campagnes de la Princesse-Alice (1891–1897). Resultats Des Campagnes Scientifiques Accomplies Sur Son Yacht Par Albert Ier Prince Souverain De Monaco 17:1–135

    Google Scholar 

  • Karakulak FS, Salman A, Oray IK (2009) Diet composition of bluefin tuna (Thunnus thynnus L. 1758) in the Eastern Mediterranean Sea, Turkey. J Appl Ichthyol 25:757–761

  • Krstulović Šifner S, Petrić M, Isajlović I, Vrgoč N, Ikica Z, Piccinetti C (2014) Insight in some aspects of the reproductive biology, morphometry and age of Chtenopteryx sicula (Cephalopoda: Chtenopterygidae) in the Adriatic Sea. Acta Adriat 55(1):31–42

    Google Scholar 

  • Kubodera T, Mori K (2005) First-ever observations of a live giant squid in the wild. Proc R Soc B 272(1581):2583–2586. https://doi.org/10.1098/rspb.2005.3158

    Article  PubMed  PubMed Central  Google Scholar 

  • Kubodera T, Koyama Y, Mori K (2007) Observations of wild hunting behaviour and bioluminescence of a large deep-sea, eight-armed squid, Taningia danae. Proc R Soc B 274(1613):1029–1034. https://doi.org/10.1098/rspb.2005.3158

    Article  PubMed  PubMed Central  Google Scholar 

  • Lorance P, Trenkel VM (2006) Variability in natural behaviour, and observed reactions to an ROV, by mid-slope fish species. J Exp Mar Biol Ecol 332(1):106–119. https://doi.org/10.1016/j.jembe.2005.11.007

    Article  Google Scholar 

  • Mastrototaro F, D’Onghia G, Corriero G, Matarrese A, Maiorano P, Panetta P, Gherardi M, Longo C, Rosso A, Sciuto F, Sanfilippo R, Gravili C, Boero F, Taviani M, Tursi A (2010) Biodiversity of the white coral bank off Cape Santa Maria di Leuca (Mediterranean Sea): an update. Deep-Sea Res II 57(5–6):412–430. https://doi.org/10.1016/j.dsr2.2009.08.021

    Article  Google Scholar 

  • Mooney TA, Hanlon RT, Christensen-Dalsgaard J, Madsen PT, Ketten DR, Nachtigall PE (2010) Sound detection by the longfin squid (Loligo pealeii) studied with auditory evoked potentials: sensitivity to low-frequency particle motion and not pressure. J Exp Biol 213(21):3748–3759. https://doi.org/10.1242/jeb.048348

    Article  PubMed  Google Scholar 

  • Naef A (1923) Die Cephalopoden. Fauna e Flora de Golfo di Napoli. Bardi G. (Ed.), monograph 35, 863 pp

  • Nesis KN (1987) Cephalopods of the world (English edition). Neptune City, NJ and London. Nesis KN. 1982. Kratky opredelitel´ golovonogikh molluskov Mirovogo okeana (Trans: Levitov BS.), Moscow

  • Orsi Relini L, Garibaldi F (2005) Diversità dei cefalopodi mesopelagici del Santuario dei cetacei in base a campionamenti diretti e osservazioni sull’alimentazione dello Zifio. Ziphius Cavirostris Biol Mar Medit 12(1):106–115

    Google Scholar 

  • Osterhage D, MacIntosh H, Althaus F, Ross A (2020) Multiple observations of bigfin squid (Magnapinna sp) in the Great Australian Bight reveal distribution patterns, morphological characteristics, and rarely seen behaviour. PLoS One 15(11):e0241066. https://doi.org/10.1371/journal.pone.0241066

    Article  CAS  PubMed Central  Google Scholar 

  • Pedà C, Battaglia P, Scuderi A, Voliani A, Mancusi C, Andaloro F, Romeo T (2015) Cephalopod prey in the stomach contents of odontocete cetaceans stranded in the western Mediterranean Sea. Mar Biol Res 11(6):593–602. https://doi.org/10.1080/17451000.2014.966724

    Article  Google Scholar 

  • Pedà C, Battaglia P, Romeo T, Stipa MG, Longo F, Malara D, Consoli P, Andaloro F (2022) Photographic atlas of cephalopod beaks from the Mediterranean Sea. Eta Beta ed., pp. 109, ISBN: 9791259686381

  • Pfeffer G (1912) Die Cephalopoden der Plankton-expedition. Ergebnisse Der Plankton-Expedition Der Humboldt-Stiftung 2:1–815

    Google Scholar 

  • Robinson NJ, Johnsen S, Brooks A, Frey L, Judkins H, Vecchione M, Widder E (2021) Studying the swift, smart, and shy: unobtrusive camera-platforms for observing large deep-sea squid. Deep Sea Res Part I 172:103538. https://doi.org/10.1016/j.dsr.2021.103538

    Article  Google Scholar 

  • Robison BH (2004) Deep pelagic biology. J Exp Mar Biol Ecol 300:253–272. https://doi.org/10.1016/j.jembe.2004.01.012

    Article  Google Scholar 

  • Robison BH, Reisenbichler KR, Sherlock RE (2017) The coevolution of midwater research and ROV technology at MBARI. Oceanography 30(4):26–37. https://doi.org/10.5670/oceanog.2017.421

    Article  Google Scholar 

  • Romeo T, Battaglia P, Pedà C, Perzia P, Consoli P, Esposito V, Andaloro F (2012) Pelagic cephalopods of the central Mediterranean Sea determined by the analysis of the stomach content of large fish predators. Helgol Mar Res 66:295–306. https://doi.org/10.1007/s10152-011-0270-3

    Article  Google Scholar 

  • Roper CFE (1977) Comparative captures of pelagic cephalopods by midwater trawls. Proc Zool Soc Lond 38:61–87

    Google Scholar 

  • Roper CF, Vecchione M (1996) In situ observations on Brachioteuthis beanii Verrill: paired behavior, probably mating (Cephalopoda, Oegopsida). Am Malacol Bull 13(1/2):55–60

    Google Scholar 

  • Roper CF, Young RE (1975) Vertical distribution of pelagic cephalopods. Smith Contrib Zool 209:1–51

  • Rosas-Luis R, Loor-Andrade P, Carrera-Fernández M, Pincay-Espinoza JE, Vinces-Ortega C, Chompoy-Salazar L (2016) Cephalopod species in the diet of large pelagic fish (sharks and billfishes) in Ecuadorian waters. Fish Res 173:159–168. https://doi.org/10.1016/j.fishres.2015.07.002

    Article  Google Scholar 

  • Rüppell E (1844) Intorno ad alcuni cefalopodi del mare di Messina. Lettera del Dr. Eduardo Rüppell di Frankfurt sul Meno al Prof. Anastasio Cocco. Giornale Del Gabinetto Letterario Di Messina 5:129–135

    Google Scholar 

  • Smale MJ, Cliff G (1998) Cephalopods in the diets of four shark species (Galeocerdo cuvier, Sphyrna lewini, S. zygaena and S mokarran) from Kwazulu-Natal South Africa. Afr J Mar Sci 20(1):241–253. https://doi.org/10.2989/025776198784126610

    Article  Google Scholar 

  • Spartà A (1933) Osservazioni compiute nello Stretto di Messina sul comportamento dei pesci e cefalopodi all’azione di sorgenti luminose. C Ferrari Mem R Com Talassogr 206:206–220

    Google Scholar 

  • Stenvers VI, Sherlock RE, Reisenbichler KR, Robison BH (2022) ROV observations reveal infection dynamics of gill parasites in midwater cephalopods. Sci Rep 12(1):1–12. https://doi.org/10.1038/s41598-022-11844-y

    Article  CAS  Google Scholar 

  • Torchio M (1966) Euribatia di Teutacei spiaggamenti ed apporto di acque di origine continentale. Atti Soc Ital Sc Nat Mus Civ Storia Nat 105:317–342

    Google Scholar 

  • Vecchione M (2019) ROV observations on reproduction by deep-sea cephalopods in the central Pacific Ocean. Front Mar Sci 6:403. https://doi.org/10.3389/fmars.2019.00403

    Article  Google Scholar 

  • Vecchione M, Roper CF (1991) Cephalopods observed from submersibles in the western North Atlantic. Bull Mar Sci 49(1–2):433–445

    Google Scholar 

  • Vecchione M, Roper CFE, Widder EA, Frank TM (2002) In-situ observations on three species of large-finned deep-sea squids. Bull Mar Sci 71(2):893–901

    Google Scholar 

  • Vérany GB (1851) Mollusques méditeranéens observés, décrits, figurés et chromolitographiés d’après le vivant. Part 1. Céphalopodes de la Méditerranée. Imprimerie des Sourds-Muets, Gênes

    Book  Google Scholar 

  • Villari A, Ammendolia G (2009) On a beached specimen of Octopoteuthis sicula (Cephalopoda: Octopoteuthidae) in the Strait of Messina. Boll Malacol 45:9–11

    Google Scholar 

  • Widder E (2013) The Kraken revealed: the technology behind the first video recordings of live giant squid. Sea Technol 54:47–54

    Google Scholar 

  • Wormuth JH, Roper CFE (1983) Quantitative sampling of oceanic cephalopods by nets: problems and recommendations. Biol Oceanogr 2(2–4):357–377. https://doi.org/10.1080/01965581.1983.10749466

    Article  Google Scholar 

  • Young RE (1978) Cephalopods from Hawaiian waters. Fish Bull 76(3):583–615

    Google Scholar 

  • Young RE, Vecchione M (2016). Chtenopteryx sicula (Verany 1851). Version 16 November 2016 (under construction). http://tolweb.org/Chtenopteryx_sicula/19441/2016.11.16 in The Tree of Life Web Project, http://tolweb.org/. Accessed 1 Mar 2023

  • Young RE, Vecchione M, Mangold KM (1922–2003) (2019) Cephalopoda Cuvier 1797. Octopods, squids, nautiluses, etc.. Version 26 March 2019 (under construction). http://tolweb.org/Cephalopoda/19386/2019.03.26 in The Tree of Life Web Project, http://tolweb.org/. Accessed 1 Mar 2023

  • Zylinski S, Johnsen S (2011) Mesopelagic cephalopods switch between transparency and pigmentation to optimize camouflage in the deep. Curr Biol 21(22):1937–1941. https://doi.org/10.1016/j.cub.2011.10.014

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are grateful to Dr Teresa Romeo, Dr Daniela Pica, Dr Frine Cardone, Dr Valentina Costa, Dr Antonio Giova, Dr Valeria Palummo, Dr Gennaro Ucciero, Dr Martina Genovese, Dr Francesco Stenico.

Funding

This study was funded by Renantis—Falck Renewables.

Author information

Authors and Affiliations

Authors

Contributions

PB and SC contributed to the study conception. SC, ES and SG contributed to the sampling design. SC and SE supervised the ROV survey at sea. PB performed the video and data analysis, writing also the first draft. All authors reviewed and revised the first draft and gave final approval for submission.

Corresponding author

Correspondence to Pietro Battaglia.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Ethical approval

Surveys were conducted by ROV and no cephalopod samples were collected during the study. Activities were cpnducted with all applicable permits in place.

Additional information

Responsible Editor: Henk-Jan Hoving.

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 Video_1 Octopoteuthis sicula in its habitat showing an arm spread posture with the arm tips exposed, producing an intermittent bioluminescence (MOV 118414 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Battaglia, P., Canese, S., Salvati, E. et al. In situ observations of three deep-sea cephalopods in the central Mediterranean Sea. Mar Biol 170, 151 (2023). https://doi.org/10.1007/s00227-023-04264-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00227-023-04264-7

Keywords

Navigation