Scientia Marina, Vol 81, No 2 (2017)

Habitat preferences among three top predators inhabiting a degraded ecosystem, the Black Sea

Alicia Sánchez-Cabanes
Marine Wildlife Department , United Kingdom

Maja Nimak-Wood
Marine Wildlife Department , United Kingdom

Nicola Harris
Marine Wildlife Department , United Kingdom

Renaud de Stephanis
GEMA, Grupo de Ecología Marina Aplicada, Estación Biológica de Doñana, CSIC - CIRCE , Spain


This study investigated whether there is evidence of widespread niche partitioning based on environmental factors in the Black Sea and tested the hypothesis that physiographic factors may be employed as predictors. It addresses poorly researched areas with good habitat potential for the only three cetacean subspecies living in this area: the Black Sea short-beaked common dolphin (Delphinus delphis spp. ponticus), the Black Sea bottlenose dolphin (Tursiops truncatus spp. ponticus) and the Black Sea harbour porpoise (Phocoena phocoena spp. relicta). Generalized additive models (GAMs) were used to analyse data collected from multiple sources. In total, 745 sightings of the three species between 1998 and 2010 throughout the Black Sea were included. The analysis found depth and sea surface temperature to be the most important variables for separating the occurrence of the three species. Common dolphins occurred mainly in deep waters and in areas where the sea surface temperature was low, bottlenose dolphins were distributed primarily in shallower and warmer waters than common dolphins, and harbour porpoises were distributed in shallower waters with lower sea surface temperature than bottlenose dolphins. This study suggests strong niche segregation among the three cetacean species. The study is also the first contribution to the basic information of cetacean species distribution and habitat preferences in the Black Sea as a whole. Knowledge of the distribution of the three dolphin species in the study area is essential to establish conservation measures for these populations.


Black Sea; bottlenose dolphin; common dolphin; GAM; habitat preferences; harbour porpoise; niche segregation; spatial modelling

Full Text:



Abel O. 1905. Eine Stammtype der Delphiniden aus dem Miocän der Halbinsel Taman. Jahrbuch der Kaiserlich-Königlichen Geologischen Reichsanstalt. Jahrb. der Kais. Geol. Reichsanstalt. 55: 375-392.

Agirbas E., Seyhan K., Kasapoglu N. et al. 2010. Recent changes of the Turkish anchovy fishery in the Black Sea with special reference to climate change. J. Environ. Prot. Ecol. 11: 1495-1503.

Amante C., Eakins B. 2009. ETOPO1 1 Arc-minute global relief model: procedures, data sources and analysis.

Anton E., Nicolaev S., Radu G., et al. 2010. Fisheries impact on dolphin populations in the Black Sea Romanian sector. Cercet Mar. Rech. Mar. 39: 281-292.

Au D.W.K., Perryman W.L. 1985. Dolphin habitats in the eastern tropical Pacific. Fish. Bull. 83: 623-643.

Balkas T., Decev G., Mihnea R., et al. 1990. State of the Marine Environment in the Black Sea Region. UNEP, Regional Seas Reports and Studies, No:124. UNEP, Nairobi, 40 pp.

Barabash I.I. 1935. Delphinus delphis ponticus subsp. Bull Mosk Obs Ispyt Prir (Bulletin Moscow Soc Nat New Ser 44: 246-249 (In Russian with English summary).

Barabash-Nikiforov I.I. 1940. Cetacean fauna of the Black Sea. Its composition and origin. Voronezh University Publ., Voronezh, 86 pp. (in Russian).

Bat L., ?ahin F., Satılmı? H.H., et al. 2007. The changed ecosystem of the Black Sea and its impact on anchovy fisheries. J. FishSci. com 1: 191-226.

Bearzi G., Reeves R.R., Notarbartolo-Di-Sciara G., et al. 2003. Ecology, status and conservation of short-beaked common dolphins Delphinus delphis in the Mediterranean Sea. Mamm. Rev. 33: 224-252.

Bearzi G., Politi E., Agazzi S. et al. 2005. Occurrence and present status of coastal dolphins (Delphinus delphis and Tursiops truncatus) in the eastern Ionian Sea. Aquat. Conserv. Mar. Freshw. Ecosyst. 15: 243-257.

Birkun A.J. 2002. The current status of bottlenose dolphins in the Black Sea. ACCOBAMS. AC18 Inf. 2, Monaco, 28 pp. PMid:12034546

Birkun A.J. 2008. Delphinus delphis ssp. ponticus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Downloaded on 19 April 2014.

Birkun A.J. 2012. Tursiops truncatus ssp. ponticus. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Downloaded on 21 April 2014.

Birkun A.J., Frantzis A. 2008. Phocoena phocoena ssp. relicta. In: IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. Downloaded on 21 April 2014.

Birkun A.J., Kuiken T., Krivokhizhin S., et al. 1999. Epizootic of morbilliviral disease in common dolphins (Delphinus delphis ponticus) from the Black Sea. Vet. Res. 144: 85-92.

Birkun A.J., Krivokhizhin S.V., Glazov D.M., et al. 2004. Abundance estimates of cetaceans in coastal waters of the northern Black Sea: results of boat surveys in August-October 2003. In: Belkovich V.M. (ed.) Marine Mammals of the Holartic, Collection of Scientific Papers. KMK Scientific Press, Moscow, pp. 64-71.

Birkun A.J., Ca-adas A., Donovan G., et al. 2006. Conservation Plan for Black Sea Cetaceans. ACCOBAMS, 50 pp.

Blanco C., Salomon O., Raga J.A. 2001. Diet of the bottlenose dolphin (Tursiops truncatus) in the western Mediterranean Sea. J. Mar. Biol. Assoc. UK 81: 1053-1058.

Bologa A.S., Sava D. 2012. Present state and evolution trends of biodiversity in the Black Sea: decline and restoration. J. Black Sea/Mediterranean Environ. 18: 144-154.

BSC. 2008. State of the Environment of the Black Sea (2001 - 2006/7). In O?uz T. (ed.). Publications of the Commission on the Protection of the Black Sea Against Pollution (BSC) 2008- 3, Istambul, Turkey.

Buckland S.T., Smith T.D., Cattanach K.L. 1992. Status of small cetacean populations in the Black Sea: Review of current information and suggestions for future research. In: Report Of The International Whaling Commission. The International Whaling Commission, pp. 513-516.

Bushuev S.G. 2002. Principal results of the aerial observations of the Black Sea dolphins in 1970s-80s. In: Belkovich V.M. (ed.) Marine Mammals of the Holartic. Second International Conference. KMK, Baikal, Russia, pp. 60-61.

Cañadas A., Hammond P.S. 2008. Abundance and habitat preferences of the short-beaked common dolphin (Delphinus delphis) in the South-western Mediterranean: implications for conservation. Endangered Species Res. 4: 309-331.

Cañadas A., Vázquez J.A. 2014. Conserving Cuvier's beaked whales in the Alboran Sea (SW Mediterranean): Identification of high density areas to be avoided by intense man-made sound. Biol. Conserv. 178: 155-162.

Cañadas A., Sagarminaga R., García-Tiscar S. 2002. Cetacean distribution related with depth and slope in the Mediterranean waters off southern Spain. Deep Sea Res. I, 49: 2053-2073.

Cañadas A., Sagarminaga R., De Stephanis R., et al. 2005. Habitat selection modelling as a conservation tool: proposals for marine protected areas for cetaceans in southern Spanish waters. Aquat. Conserv. 15: 495-521.

Carder K., Chen F., Lee Z., et al. 2003. MODIS Ocean Science Team Algorithm Theoretical Basis Document.

Carretta J.V., Taylor B.L., Chivers S.J. 2001. Abundance and depth distribution of harbour porpoise (Phocoena phocoena) in northern California determined from a 1995 ship survey. Fish. Bull. 99:29-39.

Chashchin A.K. 1996. The Black Sea populations of anchovy. Sci. Mar. 60: 219-225.

D'Amico A., Bergamasco A., Zanasca P., et al. 2003. Qualitative correlation of marine mammals with physical and biological parameters in the Ligurian Sea. IEEE J. Ocean. Eng. 28: 29-43

Daskalov G.M. 2003. Long-term changes in fish abundance and environmental indices in the Black Sea. Mar. Ecol. Prog. Ser. 255: 259-270.

Daskalov G.M., Grishin A.N., Rodionov S., et al. 2007. Trophic cascades triggered by overfishing reveal possible mechanisms of ecosystem regime shifts. Proc. Natl. Acad. Sci. USA 104: 10518-10523. PMid:17548831 PMCid:PMC1965545

De Stephanis R., Cornulier T., Verborgh P., et al. 2008. Summer spatial distribution of cetaceans in the Strait of Gibraltar in relation to the oceanographic context. Mar. Ecol. Prog. Ser. 353: 275-288.

Dede A., Tonay A.M. 2010. Cetacean sightings in the Western Black Sea in autumn 2007. J. Environ. Prot. Ecol. 11: 1491-1494.

Embling C.B., Gillibrand P.A., Gordon J., et al. 2010. Using habitat models to identify suitable sites for marine protected areas for harbour porpoises (Phocoena phocoena). Biol. Conserv. 143: 267-279.

Eremeev V.N., Zuyev G.V. 2007. Commercial Fishery Impact on the Modern Black Sea Ecosystem: A Review. Turkish J. Fish. Aquat. Sci. 82: 75-82.

Esteban R., Verborgh P., Gauffier P., et al. 2013. Identifying key habitat and seasonal patterns of a critically endangered population of killer whales. J. Mar. Biol. Assoc. UK 94: 1-9.

Evans P.G.H. 1980. Cetaceans in British waters. Mamm. Rev. 10: 1-52.

Evans P.G.H. 1987. The Natural History of Whales and Dolphins. Christopher Helm, London, UK, pp. 343.

Ferrero R.C., Walker W.A. 1995. Growth and reproduction of the common dolphin, Delphinus delphis Lineaus, in the offshore waters of the North Pacific Ocean. Fish. Bull. (Wash DC) 93: 483-494.

Fiedler P.C., Reilly S.B. 1994. Interannual variability of dolphin habitats in the eastern tropical Pacific. I. Research vessel surveys, 1986-1990. Fish. Bull. 92: 434-450.

Fontaine M.C., Snirc A., Frantzis A., et al. 2012. History of expansion and anthropogenic collapse in a top marine predator of the Black Sea estimated from genetic data. Proc. Natl. Acad. Sci. USA 109: E2569-2576. PMid:22949646 PMCid:PMC3458354

Forcada J., Aguilar A., Evans P.G.H., et al. 1990. Distribution of common and striped dolphins in the temperate waters of the eastern North Atlantic. European Research on Cetaceans, 4: 64-66.

Forney K.A. 2000. Environmental Models of Cetacean Abundance: Reducing Uncertainty in Population Trends. Conserv. Biol. 14: 1271-1286.

Frantzis A., Gordon J., Hassidis G., et al. 2001. The enigma of harbour porpoise presence in the Mediterranean Sea. Mar. Mammal Sci. 17: 937-943.

Gaskin D.E. 1982. The Ecology of Whales and Dolphins. Heinemann Educational Books Inc, London, 459 pp. PMCid:PMC370992

Gladilina E., Gol'din P.E. 2014. New Prey Fishes in Diet of Black Sea Bottlenose Dolphins "Tursiops truncatus" (Mammalia, Cetacea). Vestn. Zool. 48: 83-92.

Gol'din E.B., Gol'din P.E. 2004. Observations of cetaceans in the Calamita Gulf (Black Sea) and the adjoining sea area. In: Db V.M. (ed) Marine Mammals of the Holartic. Collection of Scientific Papers. KMK Scientific Press, Moscow, pp. 163-167.

Hamazaki T. 2002. Spatiotemporal prediction models of cetacean habitats in the mid-western north Atlantic Ocean (from Cape Hatteras, North Carolina, U.S.A. to Nova Scotia, Canada). Mar. Mammal Sci. 18: 920-939.

Hammond P. S., Macleod K., Berggren P., et al. 2013. Cetacean abundance and distribution in European Atlantic shelf waters to inform conservation and management. Biol. Conserv. 164: 107-122.

Hastie T., Tibshirani R. 1990. Generalized additive models. Monogr. Stat. Appl. Probab., 43 pp.

Hastie G.D., Wilson B., Wilson L.J., et al. 2004. Functional mechanisms underlying cetacean distribution patterns: hotspots for bottlenose dolphins are linked to foraging. Mar. Biol. 144: 397-403.

Ingram S.N., Rogan E. 2002. Identifying critical areas and habitat preferences of bottlenose dolphins Tursiops truncatus. Mar. Ecol. Prog. Ser. 244: 247-255.

Isojunno S., Matthiopoulos J., Evans P.G.H. 2012. Harbour porpoise habitat preferences: robust spatio-temporal inferences from opportunistic data. Mar. Ecol. Prog. Ser. 448: 155-170.

Jefferson T.A., Webber M.A., Pitman R.L. 2008. Marine Mammals of the World. A Comprehensive Guide to their Identification. Academic Press, London, 616 pp.

Jefferson T.A., Fertl D., Bola-os-Jiménez J., et al. 2009. Distribution of common dolphins (Delphinus spp.) in the western Atlantic Ocean: A critical re-examination. Mar. Biol. 156: 1109-1124.

Kaschner K., Quick N.J., Jewell R., et al. 2012. Global coverage of cetacean line-transect surveys: status quo, data gaps and future challenges. PLoS One 7: e44075. PMid:22984461 PMCid:PMC3440399

Kenney R.D., Scott G.P., Thompson T.J., et al. 1995. Estimates of prey consumption and trophic impacts of cetaceans in the USA northeast continental shelf ecosystem. J. Northwest Atl. Fish. Sci. 22: 155-171.

Kideys A.E. 2002. Fall and Rise of the Black Sea Ecosystem. Science 297: 1482-1484. PMid:12202806

Kleinenberg K.E. 1956. Mammals of the Black and Azov Seas: Research Experience for Biology and Hunting. USSR Acad. Science Publ. House, Moscow, 288 pp. (In Russian).

Klinowska M. 1991. Dolphins, Porpoises and Whales of the World. The IUCN Red Data Book. IUCN, Gland and Cambridge, 429 pp.

Krivokhizhin S., Birkun A.J. 2006. Offshore gathering of harbour porpoises in the central Black Sea: is it a norm or exception? FINS (the Newsl. ACCOBAMS) 2:2(2): 14-17.

Kuznetsov V.B. 2004. Fluctuations of dolphins' abundance in northern and north-eastern parts of the Black Sea according to polling data (1995-2003). In: Db V.M. (ed) Marine Mammals of the Holartic, Collection of Scientific Papers. KMK Scientific Press, Moscow, pp. 308-310.

Leatherwood S., Reeves R.R. 1990. The Bottlenose Dolphin. Academic Press, San Diego, 653 pp. PMid:2405489

Mikhalev Y.A. 2004. The Black Sea bottlenose dolphin (Tursiops truncatus, Montagu, 1821) distribution pattern according to aerial survey data. In: Belkovich V.M. (ed.) Marine Mammals of the Holartic. Collection of Scientific Papers. KMK Scientific Press, Moscow, pp. 397-402.

Mikhalev Y.A., Savusin V.P., Bushuev S.G. 2004. Associated connection between the accumulations of fishes and dolphins in the Black Sea according to the data of aerial surveys. In: Belkovich V.M. (ed) Marine Mammals of the Holartic, Collection of Scientific Papers. KMK Scientific Press, Moscow, pp. 393-397.

Miokovic D., Kovacic D., Pribanic S. 1999. Stomach content analysis of one bottlenose dophin (Tursiops truncatus, Montagu 1821) from the Adriatic Sea. Natura Croatica 8: 61-65.

Moura A.E., Sillero N., Rodrigues A. 2012. Common dolphin (Delphinus delphis) habitat preferences using data from two platforms of opportunity. Acta Oecol. 38: 24-32.

Notarbartolo di Sciara G., Venturino M.C., Zanardelli M., et al. 1993. Cetaceans in the central Mediterranean Sea: distribution and sighting frequencies. Boll. Zool. 60: 131-138.

Notarbartolo di Sciara G., Lauriano G., Pierantonio N., et al. 2015. The Devil We Don't Know: Investigating Habitat and Abundance of Endangered Giant Devil Rays in the North-Western Mediterranean Sea. PLoS ONE 10: e0141189. PMid:26580814 PMCid:PMC4651356

Nøttestad L., Sivle L.D., Krafft B.A., et al. 2014. Prey selection of offshore killer whales Orcinus orca in the Northeast Atlantic in late summer: Spatial associations with mackerel. Mar. Ecol. Prog. Ser. 499: 275-283.

O?uz T, Öztürk B. 2011. Mechanisms impeding natural Mediterranization process of Black Sea fauna. J. Black Sea/Mediterranean Environ. 17: 234-253.

O?uz T., Malanotte-Rizzoli P., Aubrey D. 1995. Wind and thermohaline circulation of the Black Sea driven by yearly mean climatological forcing. J. Geophys. Res. Ocean. 100: 6845-6863.

Ozsoy E., Unluata U. 1997. Oceanography of the Black Sea: a review of some recent results. Earth-Sci. Rev. 42: 231-272.

Öztürk B. 2013. Some remarks of Illegal , Unreported and Unregulated (IUU) fishing in Turkish part of the Black Sea. J. Black Sea/Mediterranean Environ. 19: 256-267.

Öztürk B., Öztürk A.A. 2002. Status of the cetaceans in the Turkish Black Sea and the Turkish straits system (the Istanbul Strait, Marmara Sea and Canakkale Strait). Report of the International Whaling Commission SC/55/SM2.

Öztürk B., Unsal N., Altug G. 2006. Final Report of Feedback Monitoring Program on the Cyclic Fish Migration through Bosphorus within the Frame of Marine Works to be Carried out in the Marmora Project. Istanbul, Turkey.

Radu G., Anton E., Golumbeanu M., et al. 2011. State of the Main Black Sea Commercial Fish Species Correlated with the Ecological Conditions and Fishing Effort. J. Environ. Prot. Ecol. 12: 549-557.

Radu G., Anton E., Nenciu M., et al. 2013. Distribution and Abundance of Cetacean in the Romanian Marine Area. Cercet. Mar. 43: 320-341.

Raum-Suryan K.L., Harvey J.T. 1998. Distribution and abundance of and habitat use by harbour porpoise, Phocoena phocoena, off the northern San Jaun Islands, Washington. Fish. Bull. (Wash DC). 96: 808-822.

Raykov V.S., Panayotova M. 2012. Cetacean Sightings of the Bulgarian Black Sea Coast over the Period 2006-2010. J. Environ. Prot. Ecol. 13: 1824-1835.

Read A.J., Westgate A.J. 1997. Monitoring the movements of harbour porpoises (Phocoena phocoena) with satellite telemetry. Mar. Biol. 130: 315-322.

Reid J.B., Evans P.G.H., Northridge S.P. 2003. Atlas of cetacean distribution in north-west European waters. JNCC, Peterborough, 76 pp.

Redfern J.V., Ferguson M.C., Becker E.A., et al. 2006. Techniques for cetacean-habitat modeling. Mar. Ecol. Prog. Ser. 310: 271-295.

Reilly S.B. 1990. Seasonal changes in distribution and habitat differences among dolphins in the eastern tropical Pacific. Mar. Ecol. Prog. Ser. 66: 1-11.

Santos M.B., Pierce G.J., López Barreiro A., et al. 1996. Diets of small cetaceans stranded NW Spain. ICES, C.M. 1994/N:11.

Santos M.B., Fernandez R., López A., et al. 2007a. Variability in the diet of bottlenose dolphin, Tursiops truncatus, in Galician waters, north-western Spain, 1990-2005. J. Mar. Biol. Assoc. UK 87: 231-241.

Santos M. E., Coniglione C., Louro S. 2007b. Feeding behaviour of the bottlenose dolphin, Tursiops truncatus (Montagu, 1821) in the Sado estuary, Portugal, and a review of its prey species. Rev. Bras. Zoo. 9: 31-39.

Sahin C., Hacimurtazao?lu N. 2013. Abundance and distribution of eggs and larvae of anchovy (Engraulis encrasicolus, Linnaeus, 1758) and horse mackerel (Trachurus mediterraneus, Steindachner, 1868) on the coasts of the eastern Black Sea, Turkish J. Zool. 37: 773-781.

Satilmis H.H., Gordina A.D., Bat L., et al. 2003. Seasonal distribution of fish eggs and larvae off sinop (the southern Black Sea) in 1999-2000. Acta Oecol. 24: S275-S280.

Shapiro G.I., Aleynik D.L., Mee L.D. 2010. Long term trends in the sea surface temperature of the Black Sea. Ocean Sci., 6: 491-501.

Smith T.D. 1982. Current understanding of the status of small cetacean populations in the Black Sea. In: Mammals in the sea. FAO Fisheries Series, pp. 121-130.

Stockwell D. 1999. The GARP modelling system: problems and solutions to automated spatial prediction. Int. J. Geogrf. Inf. Sci. 13: 143-158.

Tonay A., Öztürk B. 2003. Cetacean bycatches in turbot fishery on the western coast of the Turkish Black Sea. In: Int. Symp. Fish. Zool., Istanbul, Istanbul University, Faculty of Fisheries, 8 pp.

Tonay A., Öztürk A.A. 2012. Historical records of cetacean fishery in the Turkish seas. J. Black Sea/Mediterranean Environ. 18: 388-399.

Tonay A., Dede A., Öztürk A.A., et al. 2007. Stomach content of harbour porpoises (Phocoena phocoena) from the Turkish Western Black Sea in spring and early summer. Rapp. Comm. Int. Mer Mediterranée 38.

Torres L.G., Read A.J., Halpin P. 2008. Fine-scale habitat modeling of a top marine predator: do prey data improve predictive capacity? Ecol. Appl. 18: 1702-1717. PMid:18839765

UNEP 1996. State of the marine and coastal environment in the Mediterranean region. MAP Technical Report Series No. 100. Athens: UNEP.

Van der Wal J., Shoo L., Januchowski S. 2010. SDMTools: Species Distribution Modelling Tools: tools for processing data associated with species distribution modelling exercises. R Packag version 1.

Watts P., Gaskin D. 1985. Habitat index analysis of the harbour porpoise (Phocoena phocoena) in the southern Bay of Fundy, Canada. J. Mammal 66: 733-744.

Wood S.N. 2001. mgcv: GAMs and Generalized Ridge Regression for R. News 1: 20-25.

Wood S.N. 2006. On confidence intervals for generalized additive models based on penalized regression splines. Australian and New Zealand. J. Statistics 48: 445-464.

Young D.D., Cockcroft V.G. 1994. Diet of common dolphins (Delphinus delphis) off the south-east coast of southern Africa: opportunism or specialization? J. Zool. 234: 41-53.

Zaitsev Y., Mamaev V. 1997. Biological diversity in the Black Sea: A study of change and decline. United Nations Publishers, New York, 208 pp. PMCid:PMC20740

Zemsky V. 1994. History of the Russian fishery of dolphins in the Black Sea. In: Proceedings of the First International Symposium on the Marine Mammals of the Black Sea (Istanbul, Turkey, 27-30 Jun 1994). ACAR Matbaacilik AS, Istanbul, Turkey, pp. 46-48.

Zuur A.F., Ieno E.N., Elphick C.S. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1: 3-14.

Copyright (c) 2017 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

Contact us

Technical support