ENCOUNTER RATE AND RELATIVE ABUNDANCE OF BOTTLENOSE DOLPHINS AND DISTRIBUTION MODELLING OF MAIN CETACEAN SPECIES IN THE NORTH AEGEAN SEA (GREECE)

Encounter rate and relative abundance of bottlenose dolphins and distribution modelling of main cetacean species in the North Aegean Sea (Greece)

Cristina B. Milani, Adriana Vella, Pavlos Vidoris, Aristidis Christidis, Emmanouil Koutrakis, Georgos Sylaios, Argyris Kallianiotis

Conservation Biology Research Group, University of Malta, Msida MSD 2080 MALTA
Fisheries Research Institute of Kavala, 64007 Nea Peramos, Kavala, GREECE
Department of Environmental Engineering, Democritus University of Thrace, Xanthi, GREECE

Abstract

The encounter rate, relative abundance and distribution of bottlenose dolphins were investigated as part of a first detailed study on cetacean populations in the Greek North Aegean Sea. Sighting data were recorded between 2005 and 2013 through dedicated scientific marine surveys, covering 14,701 km. The line-transect sampling method was used to estimate relative abundance, using Distance software 6.0. Bottlenose dolphins presented an overall encounter rate of 0.46 groups/100km (2.5 dolphin/100km) and a mean group size of 3.45 (SE=0.38). The yearly relative abundance in the area was estimated after post-stratification at 377 individuals (95% C.I.=289–465; CV=18.37). Environmental modeling has been proposed for the main species of the study area using GAM and PCA; dolphin sightings were then correlated to eight environmental variables (distance from the coast, depth, slope, gradient of salinity, median salinity, gradient of temperature, median temperature and mean current). Bottlenose dolphin sightings were significantly correlated to depth and median temperature. This research presents the first data on encounter rate, relative abundance for the species and species distribution in relation to environmental variables in study area which are essential for effective conservation and management considerations.

Keywords: DISTANCE sampling analysis, Generalized Additive Modelling (GAM), Marine Protected Areas, North Aegean Sea, Principal Component Analysis (PCA), Tursiops truncatus

References

ACCOBAMS (2004) Report of the Second Meeting of the Parties to ACCOBAMS. Palma de Maillorca, Spain 9-12 November 2004. 180 pp.

ACCOBAMS (2007) Report of the Third Meeting of the Contracting Parties to ACCOBAMS, Dubrovnik, Croatia 22-25 October 2007. 350 pp.

ACCOBAMS (2010) Rapport de la quatrieme reunion des parties contractantes a l’ACCOBAMS. Monaco, 9-12 Novembre 2010. 399 pp.

Agardy, T. (1997) Marine Protected Areas and Ocean Conservation. Academic Press and R.G. Landes Company, Austin. 244 pp.

ASCOBANS (2008) Small Cetaceans in the European Atlantic and North Sea (SCANS-II). Final Report, 15th ASCOBANS Advisory Committee Meeting Document AC15/Doc.21(S). UN Campus, Bonn, Germany, 31 March-3 April
2008. 54 pp.

Baş, A. A., Erdogan, M. A., Morris, N. R. C., Yeoman, K., Humphrey, O., Gaggioli, E., Roland, C. (2016) Seasonal encounter rates and residency patterns of an unstudied population of bottlenose dolphin (Tursiops truncatus) in the
northwestern Levantine Sea, Turkey. Hyla 2016(1): 1-13.

Bassos-Hull, K., Perrtree, R., Shepard, C., Schilling, S., Barleycorn, A., Allen, J., Balmer, B., Pine, W., Wells, R. (2013) Long-term site fidelity and seasonal abundance estimates of common Bottlenose dolphins (Tursiops truncatus) along
the southwest coast of Florida and responses to natural perturbations. Journal of Cetacean Research and Management 13: 19-30.

Bearzi, G., Notarbartolo di Sciara, G., Politi, E. (1997) Social ecology of bottlenose dolphins in the Kvarneric (Northern Adriatic Sea). Marine Mammal Science 4: 650-668.

Bearzi, G., Politi, E., Agazzi, S., Bruno, S., Costa, M., Bonizzoni, S. (2005) Occurrence and present status of coastal dolphins (Delphinus delphis and Tursiops truncatus) in the eastern Ionian Sea. Aquatic Conservation: Marine and
Freshwater Ecosystems 15: 243-257.

Bearzi, G., Agazzi, S., Bonizzoni, S., Costa, M., Azzellino, A. (2008) Dolphins in a bottle: abundance, residency patterns and conservation of bottlenose dolphins Tursiops truncatus in the semi-closed eutrophic Amvrakikos Gulf, Greece. Aquatic Conservation: Marine and Freshwater Ecosystem 18: 130-146.

Bonizzoni, S., Santostasi, N.L., Würsig, B., Bearzi, G. (2014) Bottlenose dolphin abundance in the Northern Evoikos Gulf, Greece. In: Abstracts of the 28th Annual Conference of the European Cetacean Society 2014, 5-9 April 2014, Liege Belgium, p.104.

Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., Borchers, D.L., Thomas, L. (2001) Introduction to Distance Sampling: Estimating Abundance of Biological Populations. Oxford University Press, Oxford, UK. 432 pp.

Buckland, S.T., Anderson, D.R., Burnham, K.P., Laake, J.L., Borchers, D.L., Thomas, L. (2004) Advanced Distance Sampling. Oxford University Press, Oxford, UK. 416 pp.

Buckland, S.T., Laake, J.L., Borchers, D.L. (2010) Double-observer line transect methods: levels of independence. Biometrics 66: 169-177.

Cañadas, A. (2006) Towards conservation of dolphins in the Alboran Sea. PhD Thesis – European Doctorate. Universidad Autonoma de Madrid. 329 pp.

Cañadas, A., Burt, M. L., Macleod, K., Rogan, E., Santos, B., Vázquez, J. A. Hammond, P. S. (2010) CODA Cetacean Offshore Distribution and Abundance. Appendix II. Model-based estimates of cetacean abundance in offshore European Atlantic waters. Final report. 46 pp.

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

Cañadas, A., Sagarminaga, R., De Stephanis, R., Urquiola, E., Hammond, P. (2005) Habitat preference modelling as a conservation tool: proposals for marine protected areas for cetaceans in southern Spanish waters. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 495-521.

Casale, M., Milani, C., Kallianiotis, A. (1999) Preliminary survey on the interactions between local populations of Delphinus delphis and Tursiops truncatus and coastal fishery in north-eastern Aegean Sea (Greece). European
Research on Cetaceans 13: 100.

CIESM (2004) Investigating the roles of cetaceans in marine ecosystems. CIESM Workshop. Monograph n°25. Monaco, 144 pp.

CIESM (2010) Marine Peace Parks in the Mediterranean – a CIESM proposal. Workshop Monographs, n°41. Siracusa (Italy) 18 – 20 November 2010, 128 pp.

Clarke, K. R., Gorley, R. N. (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth.

Clarke, K. R., Warwick, R. M. (2001) Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd edition. PRIMER-E Plymouth, UK. 172 pp.

Coll, M., Pirrodi, C., Steenbeek, J., Kaschner, K., Lasram, F. B. R., Aguzzi, J., Ballestreros, E., Bianchi, C. N., Corbera, J., Dailianis, T., Danovaro, R. (2010) The biodiversity of the Mediterranean Sea: estimates, patterns, and threats. Plos
One 5(8): e11842.

Dawson, S., Slooten, E., Du Fresne, S., Wade, P., Clement, D. (2004) Small boat surveys for coastal dolphins: line-transect surveys for Hector’s dolphins (Cephalorhynchus hectori). Fisheries Bulletin 102(3): 441-451.

Dawson, S., Wade, P., Slotten, E., Barlow, J. (2008) Design and field methods for sighting surveys of cetaceans in coastal and riverine habitats. Mammal Reviews 38(1): 19-49.

Dick, D. M., Hines, E. M. (2011) Using distance sampling techniques to estimate Bottlenose dolphin (Tursiops truncatus) abundance at Turneffe Atoll, Belize. Marine Mammal Science 27(3): 606-621.

Fayos, J.A., Cañadas, A., Sagarminaga, R. (2000) A comparative approach of the movement patterns and orientation of common dolphins (Delphinus delphis) and bottlenose dolphins (Tursiops truncatus) in the north-eastern Alboran Sea. In: Proceedings of the 14th Annual Conference of the European Cetacean Society, Ireland, 2-5 April, Cork, pp. 130-133.

Fayos, J.A., Cañadas, A., Sagarminaga, R. (2001) Habitat use and general behaviour analysis as a tool for the designation of marine protected areas. In: Proceedings of the 15th Annual Conference of the European Cetacean Society, Rome, Italy, 6-10 May 2001, pp. 223-224.

Forcada, J., Gazo, M., Aguilar, A., Gonzalvo, J., Fernández-Contreras, M. (2004) Bottlenose dolphin abundance in the NW Mediterranean: addressing heterogeneity in distribution. Marine Ecology Progress Series 275: 275-287.

Forcada, J., Hammond, P. S. (1998) Geographical variation in density and numbers of striped and common dolphins of the western Mediterranean. Journal of Sea Research 39(3-4): 31-325.

Frantzis, A. 2009. Cetaceans in Greece: Present Status of Knowledge. Initiative for the Conservation of Cetaceans in Greece, Athens, Greece. 94 pp.

Frantzis, A., Alexiadou, P., Paximadis, G., Politi, E., Gannier, A., Corsini-Foka, M. (2003) Current knowledge of the cetacean fauna of the Greek Seas. Journal of Cetacean Research and Management 5(3): 219-232.

Gnone, G., Bellingeri, M., Dhermain, F., Dupraz, F., Nuti, S., Bedocchi, D., Moulins, A., Rosso, M., Alessi, J., Mac Crea, R. S., Azzellino, A., Airoldi, S., Portunato, N., Laran, S., David, L., Di Meglio, N., Bonelli, P., Montesi, G.,
Trucchi, R., Fossa, F., Wurtz, M. (2011) Distribution, abundance, and movements of the bottlenose dolphin (Tursiops truncatus) in the Pelagos Sanctuary MPA (north‐west Mediterranean Sea). Aquatic Conservation: Marine and Freshwater Ecosystems 21: 372-388.

Hammond, P. S., Macleod, K., Berggren, P., Borchers, D. L., Burt, L., Cañadas, A., Desportes, G., Donovan, G. P., Gilles, A., Gillespie, D., Gordon, J., Hiby, L., Kuklik, I., Leaper, R., Lehnert, K., Leopold, M., Lovell, P., Øienm, N., Paxton. C. G. M., Ridoux, V., Rogan, E., Samarra, F., Scheidat, M., Sequeira, M., Siebert, U., Skov, H., Swift, R., Tasker, M. L., Teilmann, J., Van Canneyt, O., Vázquez, J. A. (2013) Cetacean abundance and distribution in European Atlantic shelf water to inform conservation and management. Biological Conservation 164: 107-122.

Hastie, T.J., Tibshirani, R.J. (1990) Generalized Additive Models. Chapman & Hall/CRC Monographs on Statistics & Applied Probability. 339 pp.

Holt, R. D. (2003) On the evolutionary ecology of species’ ranges. Evolutionary Ecology Research 5: 159-178.

Hoyt, E. (2011) Marine Protected Areas for Whales, Dolphins and Porpoises. A World Handbook for Cetacean Habitat Conservation and Planning. 2nd edition. Earthscan, London. 464 pp.

Kallianiotis, A., Vidoris, P., Sylaios, G. (2004) Species assemblages and fishing geographical sub areas in North Aegean Sea, Greece. Fisheries Research 68: 171-187.

Kotzageorgis, G., Mantzavelas, A., Hadjicharalambous, E., Defingou, M., Gioutlakis, M., Papagrigoriou, S., Alexandridou, E. (Eds.) (2015) Deliverable C7: New Natura 2000 areas or Natura 2000 sites proposal with digital or printed maps, filled in Standard Data Forms and new updated Natura 2000 database (Access 2003) with data from the new proposed areas. YΡEN, Athens, Joint venture of Enveco S.A., Omikron S.A., Karolidis Theodoros, Fyselias Spyridon, Consultant EKVY. 124 pp.

MacLeod, K., Burt, M.L., Cañadas, A., Rogan, E., Santos, B., Uriarte, A., Van Canneyt, O., Vázquez, J.A., Hammond, P.S. (2010) CODA Cetacean Offshore Distribution and Abundance. Appendix I. Design-based estimates of cetacean
abundance in offshore European Atlantic waters. Final report. 16 pp.

MacLeod, C. D., Weir, C. R., Pierpoint, C., Harland, E. J. (2007) The habitat preferences of marine mammals west of Scotland (UK). Journal of the Marine Biological Association of the U.K. 87: 157-164.

Milani, C. (2015) Cetaceans and their interactions with coastal fisheries in the Gulf of Kavala, Eastern Mediterranean Sea. PhD Dissertation at the University of Malta, Department of Biology, Research group of Conservation Biology. 384 pp.

Milani, C., Vella, A., Vidoris, P., Christidis, A., Kallianiotis, A. (2011) Diet of five cetacean species in the North Aegean Sea (Greece) In: Abstracts of the 25th Conference of the European Cetacean Society, Cadiz (Spain), 21-23 March 2011, p. 247.

Milani, C., Vella, A., Vidoris, P., Christidis, A., Kallianiotis, A. (2012) Dolphin species’ diet, fisheries association and net damage in coastal fisheries of the north Aegean Sea (Greece). In: Abstracts of the 26th Conference of the European
Cetacean Society. Galway (Ireland), 26-28 March 2012. p. 299.

Milani, C., Vella, A., Vidoris, P., Christidis, A., Koutrakis, E. (2013) Cetacean distribution in the Thracian Sea (Greece) related with fishing activities. Abstracts of the 27th Annual Conference on the European Cetacean Society, Setubal
(Portugal), 8-10 April 2013, p. 170.

Milani, C., Vella, A., Vidoris, P., Christidis, A., Koutrakis, E., Kallianiotis, A. (2017) Cetacean strandings and diet analyses in the North Aegean Sea (Greece).Journal of the Marine Biological Association of the UK: 1-18. doi:10.1017/S0025315417000339.

Milani, C., Vella, A., Vidoris, P., Christidis, A., Koutrakis, E., Kallianiotis, A. (Submitted). Abundance and distribution of the Common dolphin, Delphinus delphis, in the North Aegean Sea (Greece). Aquatic Conservation: Marine and
Freshwater Ecosystems. Special Issue Common dolphins.

Mitra, S., Koutrakis, E., Milani, C. (2001) Cetacean interaction with small-scale coastal fisheries: implications for conservation and damage limitation. In: Proceedings of the 15th Conference of the European Cetacean Society, Rome
(Italy) 1, p.39.

Mitra, S., Koutrakis, E., Clark, T., Milani, C. (2004) Cetacean interaction with small scale coastal fisheries: implications for conservation and damage limitation in the Northern Aegean, Greece. European Research on Cetacean 15: 172-176.

Oedekoven, C. S., Mackenzie, M. L., Scott-Hayward, L. A. S., Rexstad, E. (2014) Statistical Modelling of Seabird and Cetacean data: Literature Review. Marine Scotland Science, Report 05/14, 31 pp.

OCEANA. (2014) MPAs in the Mediterranean Sea. Addressing opportunities to face the protection gap. First working group on MPAs, SAC, SCMEE. Bar, Montenegro, 3rd February 2014, 39 pp.

Panigada, S., Zanardelli, M., MacKenzie, M., Donovan, C., Mélin, F., Hammond, P. S. (2008) Modelling habitat preferences for fin whales and striped dolphins in the Pelagos Sanctuary (Western Mediterranean Sea) with physiographic and remote sensing variables. Remote Sensing of Environment 112: 3400-3412.

Petroselli, A. (2006) Habitat use and distribution of short-beaked common dolphins Delphinus delphis around the island of Kalamos, Greece (eastern Ionian Sea). MPhill Thesis, University of Wales, Bangor, UK, 108 pp.

Pinn, E. H. (2010). Healthy and Biologically Diverse Seas Evidence Group Technical Report Series: Evaluation and gap analysis of current and potential indicators for Cetaceans. Joint Nature Conservation Committee. Peterborough
2010. 69 pp.

Pirrotta, E., Matthiopoulos, J., MacKenzie, M., Scott-Hayward, L., Rendell, L. (2011) Modelling sperm whale habitat preference: a novel approach combining transect and follow data. Marine Ecology Progress Series 436: 257-272.

Poulos, S. E., Drakopoulos, P. G., Collins, M. B. (1997) Seasonal variability in sea surface oceanographic conditions in the Aegean Sea (Eastern Mediterranean): an overview. Journal of Marine Systems 13(1-4): 225-244.

Ryan, C., Boisseau, O., Cucknell, A.C., Romagosa, M., Moscrop, A., McLanagan, R. (2014) Comparison of cetacean distribution in the Aegean and Levantine Seas with ambient noise and shipping density. In Abstracts of the 28th
Annual Conference of the European Cetacean Society, Liege, Belgium, 5-9 April 2014, p. 222.

Scheinin, A.P. (2010) The population of bottlenose dolphins (Tursiops truncatus), bottom trawl catch trends and the interaction between the two along the Mediterranean continental shelf of Israel. PhD Thesis. University of Haifa,
Israel. 142 pp.

Schimek, M. G. (2000) Estimation and inference in partially linear models with smoothing splines. JSPI 91: 525-540.

Shane, S.H. (1990) Behavior and Ecology of the Bottlenose Dolphin at Sanibel Island, Florida. In: The Bottlenose Dolphin (eds., S. Leatherwood, R. R. Reeves), San Diego Academic Press Inc., pp. 245-266.

Silva, M.A., Prieto, R., Cascão, I., Seabra, M. I., Machete M., Baumgartner M. F. and Santos R. S. (2014). Spatial and temporal distribution of cetaceans in the mid-Atlantic waters around the Azores. Marine Biology Research 10(2): 123-
137.

Somarakis, S., Isari, S., Machias, A. (2011) Larval fish assemblages in coastal waters of central Greece: reflections of topographic and oceanographic heterogeneity. Scientia Marina 75(3): 605-618.

Stockin, K.A., Weir, C.R.. Pierce, G.J. (2006) Examining the importance of Aberdeenshire (UK) coastal waters for North Sea bottlenose dolphins (Tursiops truncatus). Journal of the Marine Biological Association of the U.K. 87: 327-338.
120

Sylaios, G., Stamatis, N., Kallianiotis, A., Vidoris, P. (2005) Monitoring water quality and assessment of land-based nutrient loadings and cycling in Kavala Gulf. Water Resources Management 19(6): 713-735.

Thomas, L., Buckland, S.T., Rexstad, E.A., Laake, J.L., Strindberg, S., Hedley, S.L., Bishop, J.R.B., Marques, T.A., Burnham, K.P. (2010) Distance software: design and analysis of distance sampling surveys for estimating population size. Review in Journal of Applied Ecology 47: 5-14.

UNEP-MAP.-RAC/SPA. (2008) Procedure for the Revision of the Areas Included in the SPAMI List. Tunis, 18 pp.

UNEP-MAP-RAC/SPA. (2010) Specially Protected Areas in the Mediterranean Assessment and Perspectives. (eds., Ben Haj, S., Ben Nakhla, L., Ouerghi, A., Rais, C.), Tunis, pp. 1-36.

Vella, A. (1999) Cetacean research and conservation around the Maltese islands. European Research on Cetaceans 13: 274.

Vella, A. (2005) Common dolphins (Delphinus delphis) status in the central and southern Mediterranean around the Maltese Islands. In: Common dolphins: Current Research, threats and issues. (eds., K. Stockin, A.Vella, P. Evans). ECS newsletter no. 45 – special issue July 2005, pp. 8-16.

Vella, A. (2009) Sustainable Fisheries in the Mediterranean. Study and Publication commissioned by the Regional Activity Centre for Cleaner Production (CP/RAC), Barcelona, Spain (available from: http://www.cprac.org/en/downloads/documents/sector-studies).

Vella, A. (2016) Resolving Bottlenose dolphin – fisheries association problems in Maltese waters, Central Mediterranean. Rapp. Comm. int. Mer Medit. 41:499.

Viale, D. (1994) Cetaceans as indicators of a progressive degradation of Mediterranean water quality. International Journal of Environmental Studies 45 (3-4): 183-198.

Viddi, F. A., Hucke-Gaete, R., Torrses-Florez, J. P., Ribeiro, S. (2010) Spatial and seasonal variability in cetacean distribution in the fjords of northern Patagonia, Chile. ICES Journal of Marine Science 67: 959-970.

Wilson, B., Reid, R. J., Grellier, K., Thompson, P. M., Hammond, P. S. (2004) Considering the temporal when managing the spatial: a population range expansion impacts protected areas-based management for bottlenose dolphins.
Animal Conservation 7: 331-338.