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Ecological niche segregation among five toothed whale species off the NW Iberian Peninsula using ecological tracers as multi-approach

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Abstract

This study aims to assess niche segregation among the five main toothed whales that frequent the NW Iberian Peninsula waters: the common dolphin, the harbour porpoise, the bottlenose dolphin, the striped dolphin and the long-finned pilot whale. We used cadmium (Cd) and stable isotope ratios (δ13C and δ15N) as ecological tracers to assess degree of segregation in diet/trophic level and in foraging habitat, over various time-scales. δ13C values highlighted different habitats, while Cd concentrations highlighted feeding differences between oceanic and neritic species. Moreover, δ15N values suggest different trophic levels of prey targeted within oceanic and neritic species. Hence, results revealed long-term ecological segregation among five toothed whales that coexist in the NWIP and demonstrated the ability of ecological tracers to discriminate ecological niches among closely related species.

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References

  • Aguilar A (1997) Inventario de los cetáceos de las aguas atlánticas peninsulares: aplicación de la directiva 92/43/CEE. Memoria Final del Departamento de Biología Animal, University of Barcelona, Barcelona

  • Aguilar A, Borrell A, Pastor T (1999) Biological factors affecting variability of persistent pollutant levels in cetaceans [special issue]. J Cetac Res Manage 1:83–116

    Google Scholar 

  • Akaike H (1981) Likelihood of a model and information criteria. J Econom 16:3–14

    Article  Google Scholar 

  • Ballance LT (2002) Cetacean ecology. In: Perrin WF, Wiirsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 196–201

    Google Scholar 

  • Bryan GW (1976) Heavy metal contamination in the sea. In: Johnston R (ed) Marine pollution, ch 3. Academic Press, London, pp 185–302

    Google Scholar 

  • Bustamante P, Caurant F, Fowler SW, Miramand P (1998a) Cephalopods as a vector for the transfer of cadmium to top marine predators in the north-east Atlantic Ocean. Sci Total Environ 220:71–80

    Article  CAS  Google Scholar 

  • Bustamante P, Cherel Y, Caurant F, Miramand P (1998b) Cadmium, copper and zinc in octopuses from Kerguelen Islands, Southern Indian Ocean. Pol Biol 19:264–271

    Article  Google Scholar 

  • Bustamante P, Teyssié JL, Fowler SW, Cotret O, Danis B, Miramand P, Warnau M (2002a) Biokinetics of zinc and cadmium accumulation and depuration at different stages in the life cycle of the cuttlefish Sepia officinalis. Mar Ecol Progr Ser 231:167–177

    Article  CAS  Google Scholar 

  • Bustamante P, Cosson RP, Gallien I, Caurant F, Miramand P (2002b) Cadmium detoxification processes in the digestive gland of cephalopods in relation to accumulated cadmium concentrations. Mar Environ Res 53:227–241

    Article  CAS  Google Scholar 

  • Bustamante P, Morales CF, Mikkelsen B, Dam M, Caurant F (2004) Trace element bioaccumulation in grey seals Halichoerus grypus from the Faroe Islands. Mar Ecol Progr Ser 267:291–301

    Article  CAS  Google Scholar 

  • Cabana G, Rasmussen JB (1996) Comparison of aquatic food chains using nitrogen isotopes. Proc Nat Acad Sci USA 93:10844–10847

    Article  CAS  Google Scholar 

  • Caurant F, Amiard JC, Amiard-Triquet C, Sauriau PG (1994) Ecological and biological factors controlling the concentrations of trace elements (As, Cd, Cu, Hg, Se, Zn) in delphinids Globicephala melas from the North Atlantic Ocean. Mar Ecol Progr Ser 103:207–219

    Article  CAS  Google Scholar 

  • Caurant F, Chouvelon T, Lahaye V, Méndez-Fernandez P, Rogan E, Spitz J, Ridoux V (2009) The use of ecological tracers for discriminating populations: the case of the short-beaked common dolphin Delphinus delphis in the European Atlantic waters. RIWC Madeira

  • Cendrero O (1993) Nota sobre los hallazgos de cetáceos en el norte de España. Bol Inst Esp Oceanogr 9:251–255

    Google Scholar 

  • Cherel Y, Le Corre M, Jaquemet S, Ménard F, Richard P, Weimerskirch H (2008) Resource partitioning within a tropical seabird community: new information from stable isotopes. Mar Ecol Prog Ser 366:281–291

    Article  CAS  Google Scholar 

  • Chouvelon T, Spitz J, Caurant F, Mèndez-Fernandez P, Chappuis A, Laugier F, Le Goff E, Bustamante P (2012) Revisiting the use of δ15N in meso-scale studies of marine food webs by considering spatio-temporal variations in stable isotopic signatures—the case of an open ecosystem: the Bay of Biscay (North-East Atlantic). Progr Oceanogr 101:92–105

    Article  Google Scholar 

  • Christopher SJ, Pugh RS, Ellisor MB, Mackey EA, Spatz RO, Porter BJ, Bealer KJ, Kucklick JR, Rowles TK, Becker PR (2007) Description and results of the NIST/NOAA 2005 interlaboratory comparison exercise for trace elements in marine mammals. Accred Qual Assur 12:175–187

    Article  CAS  Google Scholar 

  • Das K, Lepoint G, Loizeau V, Debacker V, Dauby P, Bouquegneau J-M (2000) Tuna and dolphin associations in the North-east Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Mar Poll Bull 40:102–109

    Article  CAS  Google Scholar 

  • Das K, Debacker V, Pillet S, Bouquegneau J-M (2003a) Heavy metals in marine mammals. In: Vos JG, Bossart GD, Fournier M, O’shea TJ (eds) Toxicology of marine mammals, volume 3 systems. Taylor & Francis Inc, New York, pp 135–167

    Google Scholar 

  • Das K, Lepoint G, Leroy Y, Bouquegneau J-M (2003b) Marine mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Mar Ecol Progr Ser 263:287–298

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506

    Article  CAS  Google Scholar 

  • Evans WE (1994) Common dolphin, white-bellied porpoise Delphinus delphis Linnaeus, 1758. In: Ridgway S, Harrison R (eds) Handbook of marine mammals, vol 5. Academic Press, London, pp 191–224

    Google Scholar 

  • Fernández R, García-Tiscar S, Santos MB, López A, Martínez-Cedeira JA, Newton J, Pierce GJ (2011a) Stable isotope analysis in two sympatric populations of bottlenose dolphins Tursiops truncatus: evidence of resource partitioning? Mar Biol 158:1043–1055

    Article  Google Scholar 

  • Fernández R, Santos MB, Pierce GJ, Llavona A, López A, Silva MA, Ferreira M, Carrillo M, Cermeño P, Lens S, Piertney SB (2011b) Fine-scale genetic structure of bottlenose dolphins, Tursiops truncatus, in Atlantic coastal waters of the Iberian Peninsula. Hydrobiologia 670:111–125

    Article  Google Scholar 

  • Fraga F (1981) Upwelling off the Galician Coast, Northwest Spain. In: Richards FA (ed) Coastal upwelling. American Geophysical Union, Washington, pp 176–182

    Chapter  Google Scholar 

  • Fry B (2006) Stable isotope ecology. Springer, New York

    Book  Google Scholar 

  • González N, González JJ, García C, Cabanas JM (1979) Dinámica de nutrientes en las Rías de Arosa y Muros. Bol Inst Esp Oceanogr 1:51–81

    Google Scholar 

  • González AF, López A, Guerra A, Barreiro A (1994) Diets of marine mammals stranded on the northwestern Spanish Atlantic coast with special reference to Cephalopoda. Fish Res 21:179–191

    Article  Google Scholar 

  • Hansson S, Hobbie JE, Elmgren R, Larsson U, Fry B, Johansson S (1997) The stable nitrogen isotope ratio as a marker of food-web interactions and fish migration. Ecology 78:2249–2257

    Article  Google Scholar 

  • Hastie TJ, Tibshirani RJ (1990) Generalized additive models. Chapman & Hall, New-York

    Google Scholar 

  • Herman DP, Burrows DG, Wade PR, Durban JW, Matkin CO, LeDuc RG, Barrett-Lennard LG, Krahn MM (2005) Feeding ecology of eastern North Pacific killer whales Orcinus orca from fatty acid, stable isotope, and organochlorine analyses of blubber biopsies. Mar Ecol Progr Ser 302:275–291

    Article  Google Scholar 

  • Hobson KA (1999) Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia 120:314–326

    Article  Google Scholar 

  • Hobson KA, Clark RG (1992) Assessing avian diets using stable isotopes: I. Turnover of carbon-13. Condor 94:181–188

    Article  Google Scholar 

  • Hobson KA, Sease JL (1998) Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using steller sea lions. Mar Mam Sci 14:116–129

    Article  Google Scholar 

  • Hobson KA, Sease JL, Merrick RL, Piatt JF (1997) Investigating trophic relationships of pinnipeds in Alaska and Washington using stable isotope ratios of nitrogen and carbon. Mar Mam Sci 13:114–132

    Article  Google Scholar 

  • Hohn AA, Lockyer C (1995) Protocol for obtaining age estimates from harbour porpoise teeth. Appendix 3, Report of the harbour porpoise age determination workshop. In: Bjørge A, Donovan GP (eds) Biology of phocoenids. RIWC Cambridge

  • Honda K, Tatsukawa R, Itano K (1983) Heavy metal concentrations in muscle, liver and kidney tissue of striped dolphin, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agric Biol Chem 47:1219–1228

    Article  CAS  Google Scholar 

  • Huisman J, Weissing FJ (2001) Biological conditions for oscillations generated by multispecies oscillations. Ecology 82:2682–2695

    Article  Google Scholar 

  • Hutchinson GE (1957) A treatise on limnology. Wiley, New York

    Google Scholar 

  • Jardine TD, Kidd KA, Fisk AT (2006) Applications, considerations, and sources of uncertainty when using stable isotope analysis in ecotoxicology. Env Sci Technol 40:7501–7511

    Article  CAS  Google Scholar 

  • Kiszka J, Simon-Bouhet B, Martίnez L, Pusineri C, Richard P, Ridoux V (2011) Ecological niche segregation within a community of sympatric dolphins around a tropical island. Mar Ecol Progr Ser 433:273–288

    Article  Google Scholar 

  • Knoff A, Hohn A, Macko S (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mam Sci 24:128–137

    Article  Google Scholar 

  • Krahn MM, Hanson MB, Baird RW, Boyer RH, Burrows DG, Emmons CK, Ford JKB, Jones LL, Noren DP, Ross PS, Schorr GS, Collier TK (2007) Persistent organic pollutants and stable isotopes in biopsy samples (2004/2006) from Southern Resident killer whales. Mar Pollut Bull 54:1903–1911

    Article  CAS  Google Scholar 

  • Kuiken T, Garcia Hartmann M (1991) Proceedings of the first European Cetacean Society workshop on ‘Cetacean pathology: dissection techniques and tissue sampling’. ECS Newslett 17:1–39

    Google Scholar 

  • Lahaye V, Bustamante P, Spitz J, Dabin W, Das K, Pierce GJ, Caurant F (2005) Long-term dietary segregation of common dolphins Delphinus delphis in the Bay of Biscay, determined using cadmium as an ecological tracer. Mar Ecol Progr Ser 305:275–285

    Article  CAS  Google Scholar 

  • Lahaye V, Bustamante P, Dabin W, Van Canneyt O, Dhermain F, Cesarini C, Pierce GJ, Caurant F (2006) New insights from age determination on toxic element accumulation in striped and bottlenose dolphins from Atlantic and Mediterranean waters. Mar Pollut Bull 52:1219–1230

    Article  CAS  Google Scholar 

  • Leibold MA (1995) The niche concept revisited: mechanistic models and community context. Ecology 76:1371–1382

    Article  Google Scholar 

  • Lockyer C (1993) A report on patterns of deposition of dentine and cement in teeth of pilot whales, genus Globicephala. RIWC Special Issue 14:138–161

    Google Scholar 

  • López A (2003) Estatus dos Pequenos cetaceos da Plataforma de Galicia. Dissertation, University of Santiago de compostela, Santiago de compostela

  • López A, Santos MB, Pierce GJ, González AF, Valeiras X, Guerra A (2002) Trends in strandings of cetaceans on the Galician coast, NW Spain, during the 1990s. J Mar Biol Assoc UK 82:513–521

    Article  Google Scholar 

  • López A, Pierce GJ, Valeiras X, Santos MB, Guerra A (2004) Distribution patterns of small cetaceans in Galician waters. J Mar Biol Assoc UK 84:283–294

    Article  Google Scholar 

  • Mahe K, Amara R, Bryckaert T, Kacher M, Brylinski JM (2007) Ontogenetic and spatial variation in the diet of hake (Merluccius merluccius) in the Bay of Biscay and the Celtic Sea. ICES J Mar Sci 64:1210–1219

    Google Scholar 

  • McCullagh P, Nelder JA (1989) Generalized linear models. Chapman & Hall, London

    Google Scholar 

  • Meissner AM, MacLeod CD, Richard P, Ridoux V, Pierce G (2011) Feeding ecology of striped dolphins, Stenella coeruleoalba, in the north-western Mediterranean Sea based on stable isotope analyses. J Mar Biol Assoc UK 92(8):1677–1687

    Google Scholar 

  • Ménard F, Lorrain A, Potier M, Marsac F (2007) Isotopic evidence of distinct feeding ecologies and movement patterns in two migratory predators (yellowfin tuna and swordfish) of the western Indian Ocean. Mar Biol 153:141–152

    Article  Google Scholar 

  • Mèndez-Fernandez P, Bustamante P, Bode A, Chouvelon T, Ferreira M, López A, Pierce GJ, Santos MB, Spitz J, Vingada JV, Caurant F (2012) Foraging ecology of five toothed whale species in the Northwest Iberian Peninsula, inferred using δ13C and δ15N isotopic signatures. J Exp Mar Biol Ecol 413:150–158

    Article  Google Scholar 

  • Miramand P, Bentley D (1992) Concentration and distribution of heavy metals in tissues of two cephalopods, Eledone cirrhosa and Sepia officinalis, from the French coast of the English Channel. Mar Biol 114:407–414

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Newsome SD, Martίnez del Rio C, Bearhop S, Phillips DL (2007) A niche for isotopic ecology. Front Ecol Environ 5:429–436

    Google Scholar 

  • Nordstrom CA, Wilson LJ, Sara IJ, Tollit DJ (2008) Evaluating quantitative fatty acid signature analysis (QFASA) using harbour seals Phoca vitulina richardsi in captive feeding studies. Mar Ecol Prog Ser 360:245–263

    Article  Google Scholar 

  • Pianka ER (1974) Niche overlap and diffuse competition. Proc Nat Acad Sci USA 71:2141–2145

    Article  CAS  Google Scholar 

  • Pierce GJ, Santos MB, Ross HM, Reid RJ, Patterson AIP, López A, Cedeira J (2007) Diets of teuthophagous small cetaceans from the Scottish and Galician coasts. Poster, European Cetacean Society, San Sebastian

    Google Scholar 

  • Pierce GJ, Caldas M, Cedeira J, Santos MB, Llavona Á, Covelo P, Martίnez G, Torres J, Sacau M, López A (2010) Trends in cetacean sightings along the Galician coast, north-west Spain, 2003–2007, and inferences about cetacean habitat preferences. J Mar Biol Assoc UK 90:1547–1560

    Article  Google Scholar 

  • R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, http://www.R-project.org

  • Rogan E, Murphy S, Learmonth JA, González A, Dabin W (2004) Age determination in small cetaceans from the NE Atlantic. Appendix 4. In: Pierce GJ, Santos MB, Learmonth JA, Smeenk, C and others (eds) Bioaccumulation of persistent organic pollutants in small cetaceans in European waters: transport pathways and impact on reproduction. Final Report to the European Commission’s Directorate General for Research on Project EVK3-2000-00027, Aberdeen

  • Ruiz-Cooley RI, Engelhaupt DT, Ortega-Ortiz JG (2012) Contrasting C and N isotope ratios from sperm whale skin and squid between the Gulf of Mexico and Gulf of California: effect of habitat. Mar Biol 159:151–164

    Article  CAS  Google Scholar 

  • Santos MB, Clarke MR, Pierce DGJ (2001) Assessing the importance of cephalopods in the diets of marine mammals and other top predators: problems and solutions. Fish Res 52:121–139

    Article  Google Scholar 

  • Santos MB, Pierce GJ, Learmonth JA, Reid RJ, Ross HM, Patterson IAP, Reid DG, Beare D (2004) Variability in the Diet of Harbor porpoises (Phocoena phocoena) in scottish waters 1992–2003. Mar Mam Sci 20:1–27

    Article  Google Scholar 

  • Santos MB, Fernández R, López A, Martίnez JA, Pierce GJ (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

    Article  Google Scholar 

  • Santos MB, Pierce GJ, Ross HM, Reid RJ, Patterson AIP, López A, Cedeira J (2007b) Diets of piscivorous small cetaceans from the Scottish and Galician coasts. Poster, European Cetacean Society, San Sebastian

    Google Scholar 

  • Santos MB, Monteiro SS, Vingada, JV, Ferreira M, López A, Cedeira JAM, Reid RJ, Brownlow A, Pierce GJ (in press) Patterns and trends in diet of long-finned pilot whales (Globicephala melas) based on the analysis of stomachs contents of animals stranded on Northeast Atlantic coasts. Mar Mam Sci

  • Santos MB, Pierce GJ, López A, Martínez JA, Fernández MT, Ieno E, Mente E, Porteiro C, Carrera P, Meixide M (in press) Variability in the diet of common dolphins (Delphinus delphis) in Galician waters 1991–2003 and relationship with prey abundance. Mar Ecol Progr Ser

  • Sherwood GD, Rose GA (2005) Stable isotope analysis of some representative fish and invertebrates of the Newfoundland and Labrador continental shelf food web. Estuar Coast Shelf Sci 63:537–549

    Article  CAS  Google Scholar 

  • Spitz J, Rousseau Y, Ridoux V (2006) Diet overlap between harbour porpoise and bottlenose dolphin: an argument in favour of interference competition for food? Estuar Coast Shelf Sci 70:259–270

    Article  Google Scholar 

  • Spitz J, Cherel Y, Bertin S, Kiszka J, Dewez A, Ridoux V (2011) Prey preferences among the community of deep-diving odontocetes from the Bay of Biscay, Northeast Atlantic. Deep-Sea Res Pt I 58:273–282

    Article  Google Scholar 

  • Spyrakos E, Santos-Diniz TC, Martίnez-Iglesias G, Torres-Palenzuela JM, Pierce GJ (2011) Spatiotemporal patterns of marine mammal distribution in coastal waters of Galicia, NW Spain. Hydrobiologia 670:87–109

    Article  CAS  Google Scholar 

  • Tenore KR, Alonso-Noval M, Álvarez-Ossorio M, Atkinson LP, Cabanas JM, Cal RM, Campos HJ, Castillejo F, Chesney EJ, González N, Hanson RB, Mcclain CR, Miranda A, Roman MR, Sanchez J, Santiago G, Valdes L, Varela M, Yoder J (1995) Fisheries and oceanography off Galicia, NW Spain: mesoscale spatial and temporal changes in physical processes and resultant patterns of biological productivity. J Geophys Res 100:10943–10966

    Article  Google Scholar 

  • Whittingham MJ, Stephens PA, Bradburry RB, Freckleton RP (2006) Why do we still use stepwise modelling in ecology and behavior? J Anim Ecol 75:1182–1189

    Article  Google Scholar 

  • Wood S, Augustin N (2002) GAMs with integrated model selection using penalized regression splines and applications to environmental modelling. Ecol Model 157:157–177

    Article  Google Scholar 

  • Zhao L, Castellini MA, Mau TL, Trumble SJ (2004) Trophic interactions of Antarctic seals as determined by stable isotope signatures. Polar Biol 27:368–373

    Article  Google Scholar 

  • Zuur AF, Ieno EN, Smith GM (2007) Analysing ecological data. Springer, New York

    Google Scholar 

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Acknowledgments

The authors gratefully acknowledge the assistance of volunteers from the Galician (CEMMA) and Portuguese (SPVS) stranding networks. They also thank P. Richard and G. Guillou (UMR LIENSs) for running stable isotope measurements, C. Churlaud and M. Kalombo from the Centre Commun d’Analyses (Fédération de Recherche en Environnement pour le Développement Durable FR 3097 CNRS-IFREMER-Université de La Rochelle) for running part of the metal analyses, and P. Brunello from the Cellule Géomatique (UMR LIENSs) for providing the map of the study area. We also wish to thank B. Simon-Bouhet and Géraldine Lassale (UMR LIENSs) for useful comments during statistical analysis and T. Berthuin for her assistance during laboratory work. This work was supported through the PhD grant to P. Méndez-Fernandez from the Portuguese Foundation for Science and Technology of the Government of Portugal (SFRH/BD/36766/2007). G.J. Pierce acknowledges support from the EU under the ANIMATE project (MEXC-CT-2006-042337). M.B. Santos acknowledges support from the LOTOFPEL project (Plan Nacional de I + D + I, CTM 2010-16053) and from the Spanish Ministry of Education, Programa Nacional de Movilidad de Recursos Humanos de Investigación (PR-2010-0518). Two anonymous reviewers and the associate editor C. Harrod are thanked for helpful suggestions and comments on an earlier form of this manuscript.

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Méndez-Fernandez, P., Pierce, G.J., Bustamante, P. et al. Ecological niche segregation among five toothed whale species off the NW Iberian Peninsula using ecological tracers as multi-approach. Mar Biol 160, 2825–2840 (2013). https://doi.org/10.1007/s00227-013-2274-9

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