Preliminary findings on Cuvier’s beaked whale mass stranding in Northern Cyprus

Arda M. Tonay, Işıl Aytemiz Danyer, İlayda Taşkaya, Erdem Danyer, Neslihan Öznur, Ayhan Dede, Ahmet Gülçubuk, Gülay Yüzbaşıoğlu Öztürk, Sabri Hacıoğlu, Tayfun Çanakcı, Ayaka Amaha Öztürk

ORCID IDs: A.M.T. 0000-0003-2718-9328; I.A.D. 0000-0003-4658-1819; İ.T. 0009-0008-3180-6054; E.D. 0000-0002-7922-7384; N.Ö. 0009-0003-0229-1091; A.D. 0000-0002-7712-615X A.G. 0000-0002-9722-8831; G.Y.Ö. 0000-0002-1761-0409;
S.H. 0000-0002-5493-0807; T.Ç. 0000-0002-6551-6820; A.A.Ö. 0000-0003-2281-7372

Faculty of Aquatic Sciences, Istanbul University, Fatih, Istanbul, TÜRKİYE
Turkish Marine Research Foundation (TUDAV), Beykoz, Istanbul, TÜRKİYE
Cyprus Wildlife Research Institute, Taşkent Doğa Parkı, Taşkent, Kyrenia, CYPRUS
Veterinary Control Central Research Institute, 06020, Etlik, Ankara, TÜRKİYE
TRNC Ministry of Agriculture and Natural Resources, Veterinary Department Directorate, Lefkoşa, Nicosia, CYPRUS
Department of Pathology, Faculty of Veterinary Medicine, Istanbul University-Cerrahpaşa, Büyükçekmece, Istanbul, TÜRKİYE

Abstract

Cuvier’s beaked whales, Ziphius cavirostris, one of the regular cetacean species of the Mediterranean Sea, are affected by underwater noise, mainly shipping, naval exercise and seismic operations worldwide. Between 9 February – 6 March 2023 but mostly in 9-10 February, at least 13 beaked whales stranded in the northwest and west of the Cyprus Island in the eastern Mediterranean Sea. This study presents the preliminary findings of necropsy, histopathology and virology of six individuals and compiles information on the present human threats in the region at the time of the incident. Histopathological findings did not provide a clear result. However, intense congestion was seen in both macroscopic and histopathological examinations. The presence of undigested fresh squid in the stomach is an indicator of sudden death. Besides, intravascular gas bubbles in macroscopic examination were in line with the general findings in previous studies on beaked whale strandings after they had died due to military exercises. As a precautionary approach, activities generating impulsive underwater noise need to follow the ACCOBAMS Mitigation Guideline and if not they should halt particularly in areas where cetaceans presence is known. In a further note, all the Parties of ACCOBAMS are expected to refrain from conducting naval exercises involving sonar or underwater bursts near “Areas of Particular Concern for Beaked Whales”, taking into account the ACCOBAMS resolution 5.13 of 2013 and urges the implementation of underwater noise mitigation strategies in the fragile habitats of the eastern Mediterranean Sea.

Keywords: Ziphius cavirostris, eastern Mediterranean Sea, military exercise, impulsive underwater noise, mitigation, ACCOBAMS

References

ACCOBAMS (2010) Guidelines to address the impact of anthropogenic noise on cetaceans in the ACCOBAMS area. Available at: https://accobams.org/wp-content/uploads/2020/05/GL_Impact_anthropogenic_noise.pdf (accessed 20 July 2023).

ACCOBAMS (2013) Resolution 5.13: Conservation of Cuvier’s beaked whales in the Mediterranean. Available at: https://www.accobams.org/wp-content/uploads/2016/06/ ACCOBAMS_MOP5_Res.5.13.pdf (accessed 20 August 2023).

ACCOBAMS (2019) Resolution 7.13 Anthropogenic Noise. Available at: ACCOBAMS-MOP7/2019/Doc38/Annex15/Res.7.13 (accessed 20 July 2023).

ACCOBAMS (2022) Methodological Guide v3.1: Guidance on underwater noise mitigation measures. ACCOBAMS-MOP8/2022/Inf44 Available at: https://accobams.org/wp-content/uploads/2019/04/MOP7.Doc31Rev1_Methodological-Guide-Noise.pdf (accessed 20 September 2023).

Akkaya Baş, A., Lagoa, J.C., Atchoi, E. (2016) New records of Cuvier’s beaked whales (Ziphius cavirostris) from the Turkish Levantine Sea. Turkish Journal of Zoology 40(3): 454-460.

Amaha Öztürk, A., Tonay, A.M., Dede, A., Danyer, E., Danyer Aytemiz, I., Aydinel, A., Deval, C. (2018) Stranding records of Cuvier’s beaked whale, Ziphius cavirostris on the coast of Turkey and Northern Cyprus, 2016-2017. 32. Conference of European Cetacean Society, 6-10 April 2018, La Spezia, Italy. pp.122.

Awbery, T., Akkaya, A., Lyne, P., Rudd, L., Hoogenstrijd, G., Nedelcu, M., Kniha, D., Erdoğan, M.A., Persad, C., Amaha Öztürk, A., Öztürk, B. (2022) Spatial distribution and encounter rates of delphinids and deep diving cetaceans in the eastern Mediterranean Sea of Turkey and the extent of overlap with areas of dense marine traffic. Frontiers in Marine Science 9: 860242.

Balcomb, III, K.C., Claridge, D.E. (2001) A mass stranding of cetaceans caused by naval sonar in the Bahamas. Bahamas Journal of Science 2: 2-12.

Boisseau, O., Lacey, C., Lewis, T., Moscrop, A., Danbolt, M., McLanaghan, R. (2010) Encounter rates of cetaceans in the Mediterranean Sea and contiguous Atlantic area. Journal of the Marine Biological Association of the United Kingdom 90(8): 1589.

Bora, D.P., Venkatesan, G., Bhanuprakash, V., Balamurugan, V., Prabhu, M., Sankar, M.S., Yogisharadhya, R. (2011) TaqMan real-time PCR assay based on DNA polymerase gene for rapid detection of Orf infection. Journal of Virological Methods 178(1-2): 249-252.

Bowden, T.R, Babiuk, S.L, Parkyn, G.R., Copps, J.S., Boyle, D.B. (2008) Capripox virus tissue tropism and shedding: A quantitative study in experimentally infected sheep and goats. Virology 371: 380-393.

Cañadas, A., Aguilar de Soto, N., Aissi, M., Arcangeli, A., Azzolin, M., B-Nagy, A., Bearzi, G., Campana, I., Chicote, C., Cotte, C., Crosti, R., David, L., Di Natale, A., Fortuna, C., Frantzis, A., Garcia, P., Gazo, M., Gutierrez-Xarxa, R., Holčer, D., Laran, S., et al. (2018) The challenge of habitat modelling for threatened low density species using heterogeneous data: the case of Cuvier’s beaked whales in the Mediterranean. Ecological Indicators 85: 128-136.

Cañadas, A., Notarbartolo di Sciara, G. (2018) Ziphius cavirostris (Mediterranean subpopulation) (errata version published in 2021). The IUCN Red List of Threatened Species 2018: e.T16381144A199549199. https://dx.doi.org/10.2305/IUCN.UK.2018-2.RLTS.T16381144A199549199.en (accessed 20 September 2023).

Charlou, J.L., Donval, J.P., Zitter, T., Roy, N., Jean-Baptiste, P., Foucher, J.P., Woodside, J., Party, M.S. (2003) Evidence of methane venting and geochemistry of brines on mud volcanoes of the eastern Mediterranean Sea. Deep Sea Research Part I: Oceanographic Research Papers 50(8): 941-958.

Chu, D.K.W., Poon, L.L.M., Guan, Y., Peiris, J.S.M. (2008) Novel astroviruses in insectivorous bats. Journal of Virology 82(18): 9107-9114.

CWRI (2023) Cuvier’s Beaked Whale Mass Stranding Event Preliminary Report. Cyprus Wildlife Research Institute, Available at: https://simplebooklet.com/gagalbalinatoplukarayavurmaolaynrapor?fbclid=IwAR39JCJrlj29D-gJ-WmHBHQJS4TKQrdjuXuDku27W6Iv3qDUL8Pm0RAt7 I#page=1 (accessed 20 March 2023)

Dalebout, M., Robertson, K.M., Frantzis, A., Engelhaupt, D., Mignucci-Giannoni, A.A., Rosario-Delestre, R.J., Baker, C.S. (2005) Worldwide structure of mtDNA diversity among Cuvier’s beaked whales (Ziphius cavirostris): implications for threatened populations. Molecular Ecology 14: 3353-3371.

D’Amico, A., Gisiner, R.C., Ketten, D.R., Hammock, J.A., Johnson, C., Tyack, P.L., Mead, J. (2009) Beaked whale strandings and naval exercises. Aquatic Mammals 35(4): 452-472.

Decaro, N., Elia, G., Martella, V., Desario, C., Campolo, M., Di Trani, L., Buonavoglia, C. (2005) A real-time PCR assay for rapid detection and quantitation of canine parvovirus type 2 in the feces of dogs. Veterinary Microbiology 105(1): 19-28.

Dede, A., Amaha Öztürk, A., Tonay, A.M., Özsandıkçı, U., Gönülal, O., Öztürk, B. (2022) Cetacean sightings in the Finike Seamounts area and adjacent waters during the surveys in 2021. Journal of the Black Sea Mediterranean Environment 28(2): 221-239.

Delyamure, S.L. (1968) The Helminth Fauna of Marine Mammals (Ecology and Phylogeny), (ed., Skrjabin, K.I.), Israel Program for Scientific Translations, Jerusalem.

DHA (2023) Available at: https://www.haberturk.com/kiyiya-vuran-yunus-depremzede-aile-sayesinde-kurtarildi-3565950?page=2 (accessed 20 July 2023)

Díaz-Delgado, J., Fernández, A., Xuriach, A., Sierra, E., Bernaldo de Quirós, Y., Mompeo, B., Pérez, L., Andrada, M., Marigo J., Catão-Dias, J.L., Groch, K.R., Edwards, J.F., Arbelo, M. (2016) Verminous arteritis due to Crassicauda sp. in Cuvier’s beaked whales (Ziphius cavirostris). Veterinary Pathology 53(6): 1233-1240.

Eiden, M., Vina-Rodriguez, A., Hoffmann, B., Ziegler, U. Groschup, M.H. (2010) Two new real-time quantitative reverse transcription polymerase chain reaction assays with unique target sites for the specific and sensitive detection of lineages and West Nile virus strains. Journal of Veterinary Diagnostic Investigation 22: 748-753.

Evans, D.L., England, G.R., (eds.) (2001) Joint Interim Report Bahamas Marine Mammal Stranding Event of 14–16 March 2000, US Department of Commerce (NOAA)/US Navy, p. 61.

Fernández, A., Edwards, J.F., Rodríguez, F., Espinosa De Los Monteros, A., Herráez, P., Castro, P., Jaber, J.R., Martin, V., Arbelo, M. (2005) “Gas and fat embolic syndrome” involving a mass stranding of beaked whales (Family Ziphiidae) exposed to anthropogenic sonar signals. Veterinary Pathoogy 42(4): 446-57.

Fernández, A., Sierra, E., Martín, V., Méndez, M., Sacchini, S., Bernaldo de Quirós, Y., Andrada, M., Rivero, M., Quesada O., Tejedor, M., Arbelo, M. (2012) Last “Atypical” beaked whales mass stranding in the Canary Islands (July, 2004). Journal of Marine Science: Research and Development 2: 107. doi:10.4172/2155-9910.1000107.

Frantzis, A. (1998) Does acoustic testing strand whales? Nature 329: 29.

Gordon, J., Gillespie, D., Potter, J., Frantzis, A., Simmonds, M. P., Swift, R., Thompson, D. (2003) A review of the effects of seismic surveys on marine mammals. Marine Technology Society Journal 37(4): 16-34.

Heyning, J.E., Mead, J.G. (2009) Cuvier’s Beaked Whale Ziphius cavirostris. In: Encyclopedia of Marine Mammals, Second Edition, (eds., Perrin, W.F., Würsig, B., Thewissen, G.M.), Academic Press, pp. 294-295.

Hoffmann, B., Depner, K., Schirrmeier, H., Beer, M. (2006) A universal heterologous internal control system for duplex real-time RT-PCR assays used in a detection system for pestiviruses. Journal of Virological Methods 136: 200-209.

Hooker, S. K., De Soto, N. A., Baird, R. W., Carroll, E. L., Claridge, D., Feyrer, L., Miller, P.J., Onoufriou, A., Schorr, G., Siegal, E., Whitehead, H. (2019) Future directions in research on beaked whales. Frontiers in Marine Science 5: 514.

IJsseldijk, L.L., Brownlow, A.C., Mazzariol, S. (eds.) (2019) Best Practice on Cetacean Post Mortem Investigation and Tissue Sampling. Bonn/Monaco: ASCOBANS/ACCOBAMS, 73 pp. doi: 10.31219/osf.io/zh4ra

IUCN-MMPATF (2017) Hellenic Trench IMMA. Full Accounts of Mediterranean IMMA Factsheet. IUCN Joint SSC/WCPA Marine Mammal Protected Areas Task Force, 2017. Available at: www.marinemammalhabitat.

org/portfolio-item/hellenic-trench/ (accessed 1 Sep 2023)

Jefferson, T.A., Webber, M.A., Pitman, R.L. (2015) Marine Mammals of the World: A Comprehensive Guide to Their Identification, Second Edition. Academic Press, Elsevier.

JRCC (2023) Republic of Cyprus, Joint Rescue Coordination Center. ZCZC MA92 Available at: https://www.mod.gov.cy/mod/cjrcc.nsf/page44_en/page44_en?OpenDocument (accessed 22 Sep 2023)

MMPATF (2022) Three stranded Cuvier’s beaked whales raise the red flag stop that noise. Marine Mammal Protected Areas Task Force. Available at: https://www.marinemammalhabitat.org/three-stranded-cuviers-beaked-whales-raise-the-red-flag-stop-that-noise/ (accessed 20 Aug 2023).

Notarbartolo di Sciara, G., Tonay, A.M. (2021) Conserving Whales, Dolphins and Porpoises in the Mediterranean Sea, Black Sea and Adjacent Areas: an ACCOBAMS Status Report. ACCOBAMS, Monaco.

ONHO (2023) Weekly Notices to Mariners Bulletin, Week: 06, NtMs 025-029.

Onoufriou, A.B., Gaggiotti, O.E., de Soto, N.A., McCarthy, M.L., Morin, P.A., Rosso, M., Dalebout, M., Davison, N., Baird, R.W., Baker, C.S., Berrow, S., Brownlow, A., Burns, D., Caurant, F., Claridge, D., Constantine, R., Demaret, F., Dreyer, S., Duras, M., Durban, J.W., et al. (2022) Biogeography in the deep: Hierarchical population genomic structure of two beaked whale species. Global Ecology and Conservation 40: e02308.

Öztürk, B. (2022) Editor’s Note to the issue dedicated to the Finike Seamounts (Anaximander) Special Environmental Protection Area, the eastern Mediterranean Sea. Journal of the Black Sea/Mediterranean Environment 28 (2): 127-138.

Podestà, M., Azzellino, A., Cañadas, A., Frantzis, A., Moulins, A., Rosso, M., Tepsich, P., Lanfredi, C. (2016) Cuvier’s beaked whale, Ziphius cavirostris, distribution and occurrence in the Mediterranean Sea: high-use areas and conservation threats. Advances in Marine Biology 75: 103-140.

Podesta, M., D’Amico, A., Pavan, G., Drougas, A., Komnenou, A., Portunato, N. (2006) A review of Cuvier’s beaked whale strandings in the Mediterranean Sea. The Journal of Cetacean Research and Management 7(3): 251-261.

Rowles, T.K., Van Dolah, F.M, Hohn, A.A. (2001) Gross Necropsy and Specimen Collection Protocols. In: CRC Handbook of Marine Mammal Medicine, 2nd edition, (eds., Dierauf L.A., Gulland F.M.D.), CRC Press, New York, pp. 449-470.

Siebert, U., Stürznickel, J., Schaffeld, T., Oheim, R., Rolvien, T., Prenger-Berninghoff, E., Wohlsein, P., Lakemeyer, J., Rohner, S., Aroha Schick, L., Gross, S., Nachtsheim, D., Ewers, C., Becher, P., Amling, M., Morell, M. (2022) Blast injury on harbour porpoises (Phocoena phocoena) from the Baltic Sea after explosions of deposits of World War II ammunition. Environment International 159: 107014.

Simmonds, M.P., Lopez-Jurado, L.F. (1991) Whales and the military. Nature 51: 448.

Tonay, A.M., Karaman, K., Dede, A., Danyer, E., Aytemiz Danyer, I., Uzun, B., Meray, Y., Deval, C., Amaha Ozturk, A., Bilgin, R. (2024) Genetic investigation on Cuvier’s beaked whale, Ziphius cavirostris on the coast of Türkiye and Northern Cyprus, based on mtDNA sequences. Journal of the Marine Biological Association of the United Kingdom 104: e14, doi: 10.1017/S0025315424000079.

Van Bree, P.J.H., Kristensen, I. (1974) On the intriguing stranding of four Cuvier’s beaked whales, Ziphius cavirostris G. Cuvier, 1823, on the Lesser Antillean Islands of St. Martin and Curacao. Lutra 15: 6-8.

Verna, F., Giorda, F., Miceli, I., Rizzo, G., Pautasso, A., Romano, A., Goria, M. (2017) Detection of morbillivirus infection by RT-PCR RFLP analysis in cetaceans and carnivores. Journal of Virological Methods 247: 22-27.

Vonk, R., Martin-Martel, V. (1989) Goose-beaked whales Ziphius cavirotris mass stranding in the Canary Islands. Proceedings of 3rd Annual Conference of European Cetacean Society, pp. 73-77, La Rochelle (France), 24-26 February 1989.

Wernike, K., Beer, M., Freuling, C.M., Klupp, B., Mettenleiter, T.C., Müller, T., Hoffmann, B. (2014) Molecular double-check strategy for the identification and characterization of Suid herpesvirus. Journal of Virological Methods 209: 110-115.

Zeng, S.Q., Halkosalo, A., Salminen, M., Szakal, E.D., Puustinen, L., Vesikari, T. (2008) One-step quantitative RT-PCR for the detection of rotavirus in acute gastroenteritis. Journal of Virological Methods 153(2): 238-240.