Abstract
Short-beaked common dolphins (Delphinus delphis) and Atlantic spotted dolphins (Stenella frontalis) are the two most abundant cetacean species in the oceanic waters of Madeira and the Azores. They are of similar size, occur in similar habitats and are regularly observed in mixed-species groups to forage together. Genetic analyses suggested that, within each species, dolphins ranging around both archipelagos belong to the same panmictic population. We tested the hypotheses that (1) within each species, individuals from the two archipelagos belong to a single ecological stock; (2) between species, common and spotted dolphins have distinct trophic niches; using fatty acid (FA) and stable isotope (SI) analyses. Fatty acids and stable isotopes were analysed from 86 blubber and 150 skin samples of free-ranging dolphins, respectively. Sex-related differences were not significant, except for common dolphin FA profiles. In S. frontalis, FA and SI differences between archipelagos suggested that individuals belonged to different ecological stocks, despite the existence of gene flow between the two archipelagos. In D. delphis, differences were more pronounced, but it was not possible to distinguish between stock structure and a seasonal effect, due to differential sampling periods in the Azores and Madeira. Inter-specific comparisons were restricted to the Azores where all samples were collected during summer. Differences in FA proportions, noticeably for FA of dietary origin, as well as in nitrogen SI profiles, confirmed that both species feed on distinct resources. This study emphasizes the need for an integrated approach including both genetic and biochemical analyses for stock assessment, especially in wide-ranging marine top predators.
Similar content being viewed by others
References
Abend AG, Smith TD (1997) Differences in stable isotope ratios of carbon and nitrogen between long-finned pilot whales (Globicephala melas) and their primary prey in the western north Atlantic. ICES J Mar Sci 54:500–503
Aguilar A, Borrell A (1990) Patterns of lipid content and stratification in the blubber of fin whales (Balaenoptera physalus). J Mammal 71:544–554
Arnould JPY, Nelson MM, Nichols PD, Oosthuizen WH (2005) Variation in the fatty acid composition of blubber in Cape fur seals (Arctocephalus pusillus pusillus) and the implications for dietary interpretation. J Comp Physiol B 175:285–295
Bandarra NM, Batista I, Nunes ML, Empis JM, Christie WW (1997) Seasonal changes in lipid composition of sardine (Sardina pilchardus). J Food Sci 62(1):40–42
Borobia M, Gearing PJ, Simard Y, Gearing JN, Beland P (1995) Blubber fatty acids of finback and humpback whales from the Gulf of St. Lawrence. Mar Biol 122:341–353
Borrell A, Aguilar A, Tornero V, Sequeira M, Fernandez G, Ahs S (2006) Organochlorine compounds and stable isotopes indicate bottlenose dolphin subpopulation structure around the Iberian Peninsula. Environ Int 32:516–523
Brown DJ, Boyd IL, Cripps GC, Butler PJ (1999) Fatty acid signature analysis from the milk of Antarctic fur seals and Southern elephant seals from South Georgia: implications for diet determination. Mar Ecol Prog Ser 187:251–263
Budge SM, Iverson SJ, Koopman HN (2006) Studying trophic ecology in marine ecosystems using fatty acids: a primer on analysis and interpretation. Mar Mamm Sci 22:759–801
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 49:2053–2073
Chou L, Bright AM, Yeh S (1995) Stomach content of dolphins from North Pacific ocean. Zool Stud 34:206–210
Clua E, Grosvalet F (2001) Mixed-species feeding aggregation of dolphins, large tunas and seabirds in the Azores. Aquat Living Res 14:11–18
Dahl TM, Lydersen C, Kovacs KM, Falk-Petersen S, Sargent J, Gjertz I, Gulliksen B (2000) Fatty acid composition of the blubber in white whales (Delphinapterus leucas). Polar Biol 23:401–409
Das K, Lepoint G, Loizeau V, Debacker V, Dauby P, Bouquegneau JM (2000) Tuna and dolphin associations in the north-east Atlantic: evidence of different ecological niches from stable isotope and heavy metal measurements. Mar Pollut Bull 40:102–109
Das K, Lepoint G, Leroy Y, Bouquegneau JM (2003) Marine mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Mar Ecol Prog Ser 263:287–298
De Niro ML, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
Dinis A, Cascão I, Alves F, Freitas L, Quérouil S et al (2008) Comparing the epipelagic diet between short-beaked common dolphin and Atlantic spotted dolphin in two Atlantic oceanic archipelagos 22nd Conference of the European Cetacean Society, Egmond aan Zee, The Netherlands
Evans WE (1994) Common dolphin, white-bellied purpose Delphinus delphis Linnaeus 1758. In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol 5: the first book of dolphins. Academic Press, London, pp 191–224
Falk-Petersen S, Haug T, Nilssen KT, Wold A, Dahl TM (2004) Lipids and trophic linkages in harp seal (Phoca groenlandica) from the eastern Barents Sea. Polar Res 23:43–50
Freitas L, Alves F, Dinis A, Nóbrega F et al (2004) Relatório dos resultados científicos. Projecto para a conservação dos cetáceos no Arquipélago da Madeira (Project report)
Gloutney ML, Hobson KA (1998) Field preservation techniques for the analysis of stable-carbon and nitrogen isotope ratios in eggs. J Field Ornithol 69(2):223–227
Gonçalves JM, Barreiros JP, Azevedo JN, Norberto R (1996) Cetaceans stranded in the Azores during 1992–96. Arquipelago 14A:57–65
Grinnell J (1924) Geography and evolution. Ecology V-3:225–229
Guitart R, Silvestre AM, Guerrero X, Mateo R (1999) Comparative study of the fatty acid composition of two marine vertebrates: striped dolphins and loggerhead turtles. Comp Biochem Physiol 124 B:439–443
Heithaus MR, Dill LM (2002) Food availability and tiger shark predation influence dolphin habitat use. Ecology 83:480–491
Hicks BD, St Aubin DJ, Geraci JR, Brown WR (1985) Epidermal growth in the bottlenose dolphin, Tursiops truncatus. J Invest Dermatol 85:60–63
Hobson KA, Welch HE (1992) Determination of trophic relationships within a high Arctic marine food web using delta-13C and delta-15N analysis. Mar Ecol Prog Ser 84:9–18
Hobson KA, Gloutney ML, Gibbs HL (1997) Preservation of blood and tissue samples for stable-carbon and stable-nitrogen isotope analysis. Rev Can Zool 75(10):1720–1723
Hooker SK, Iverson SJ, Ostrom P, Smith SC (2001) Diet of northern bottlenose whales inferred from fatty-acid and stable-isotope analyses of biopsy samples. Can J Zool 79:1442–1454
Iverson SJ, Arnould JPY, Boyd IL (1997a) Milk fatty acid signatures indicate both major and minor shifts in the diet of lactating Antarctic fur seals. Can J Zool 75:188–197
Iverson SJ, Frost KJ, Lowry LF (1997b) Fatty acid signatures reveal fine scale structure of foraging distribution of harbor seals and their prey in Prince William Sound, Alaska. Mar Ecol Prog Ser 151:255–271
Iverson SJ, Field C, Bowen WD, Blanchard W (2004) Quantitative fatty acid signature analysis: a new method of estimating predator diets. Ecol Monogr 74:211–235
Kaehler S, Pakhomov EA (2001) Effects of storage and preservation on the δ13C and δ15N signatures of selected marine organisms. Mar Ecol Prog Ser 219:299–304
Kirsch PE, Iverson SJ, Bowen WD, Kerr SR, Ackman RG (1998) Dietary effects on the fatty acid signature of whole Atlantic cod (Gadus morhua). Can J Fish Aquat Sci 55:1378–1386
Kirsch PE, Iverson SJ, Bowen WD (2000) Effect of a low-fat diet on body composition and blubber fatty acids of captive juvenile harp seals (Phoca groenlandica). Physiol Biochem Zool 73:45–59
Kiszka J, Orémus M, Richard P, Poole MM, Ridoux V (2010a) The use of stable isotope analyses from skin biopsy samples to assess trophic relationships of sympatric delphinids off Moorea (French Polynesia). J Exp Mar Biol Ecol 395:48–54
Kiszka J, Simon-Bouhet B, Charlier F, Pusineri C, Ridoux V (2010b) Individual and group behavioural reactions of small delphinids to remote biopsy sampling. Anim Welf 19:411–417
Kiszka J, Simon-Bouhet B, Martinez L, Pusineri C, Richard P, Ridoux V (2011) Ecological niche segregation within a community of sympatric dolphins around a tropical island. Mar Ecol Prog Ser 433:273–288
Kleivane L, Espeland O, Ugland KI, Skaare JU (1995) Seasonal variation of organochlorine concentrations in harp seal (Phoca groenlandica). In: Blix AS, Walløe L, Ulltang Ø (eds) Whales, seals, fish and man. Elsevier Science B.V, Amsterdam, pp 599–605
Koopman HN, Iverson SJ, Gaskin DE (1996) Stratification and age-related differences in blubber fatty acids of the male harbour porpoise (Phocoena phocoena). J Comp Physiol B 165:628–639
Koopman HN, Iverson SJ, Read AJ (2003) High concentrations of isovaleric acid in the fats of odontocetes: stability in the melon vs. variation and patterns of accumulation in blubber. J Comp Physiol B 173:247–261
Kramer JK, Blackadar CB, Zhou J (2002) Evaluation of two GC columns (60 m Supelcowax 10 and 100 m CP Sil 88) for analysis of milkfat with emphasis on CLA, 18:1, 18:2 and 18:3 isomers, and short and long-chain fatty acids. Lipids 37:823–835
Le Duc RG, Perrin WF, Dizon AE (1999) Phylogenetic relationships among the delphinid cetaceans based on full cytochrome b sequences. Mar Mamm Sci 15:619–648
Lesage V, Hammill MO, Kovacs KM (2001) Marine mammals and the community structure of the Estuary and Gulf of St Lawrence, Canada: evidence from stable isotope analysis. Mar Ecol Prog Ser 210:203–221
Lopes XM, de Oliveira Santos MC, da Silva E, Bassoi M, Aguiar dos Santos R (2012) Feeding habits of the Atlantic spotted dolphin, Stenella frontalis, in southeastern Brazil. Braz J Oceanogr 60:189–198
Mathews EA, Keller S, Weiner DB (1988) A method to collect and process skin biopsies for cell culture from the free-ranging gray whales (Eschrichtius robustus). Mar Mamm Sci 4:1–12
Meynier L, Pusineri C, Spitz J, Santos MB, Pierce GJ, Ridoux V (2008) Intraspecific dietary variation in the short-beaked common dolphin Delphinus delphis in the Bay of Biscay: importance of fat fish. Mar Ecol Prog Ser 354:277–287
Nakamura MT, Nara TY (2003) Essential fatty acid synthesis and its regulation in mammals. Prostaglandins Leukot Essent Fatty Acids 68:145–150
Newland C, Field IC, Nichols PD, Bradshaw CJA, Hindell MA (2009) Blubber fatty acid profiles indicate dietary resource partitioning between adult and juvenile southern elephant seals. Mar Ecol Prog Ser 384:303–312
Olsen E, Grahl-Nielsen O (2003) Blubber fatty acids of minke whales: stratification, population identification and relation to diet. Mar Biol 142:13–24
Özyurt G, Duysak Ö, Akamca E, Tureli C (2006) Seasonal changes of fatty acids of cuttlefish Sepia officinalis L. (Mollusca: Cephalopoda) in the north eastern Mediterranean sea. Food Chem 95:382–385
Park Y, Albright KJ, Cai ZY, Pariza MW (2001) Comparison of methylation procedures for conjugated linoleic acid and artefact formation by commercial (trimethylsilyl) diazomethane. J Agric Food Chem 49:1158–1164
Pauly D, Trites AW, Capuli E, Christensen V (1998) Diet composition and trophic levels of marine mammals. ICES J Mar Sci 55:467–481
Perrin WF, Caldwell DK, Caldwell MC (1994) Atlantic spotted dolphin Stenella frontalis (G. Cuvier, 1829). In: Ridgway SH, Harrison R (eds) Handbook of marine mammals, vol 5: the first book of dolphins. Academic Press, London, pp 173–190
Phillips KL, Nichols PD, Jackson GD (2002) Lipid and fatty acid composition of the mantle and digestive gland of four Southern Ocean squid species: implications for food-web studies. Antarct Sci 14:212–220
Pianka ER (1974) Niche overlap and diffuse competition. Proc Natl Acad Sci USA 71:2141–2145
Praca E, Gannier A (2008) Ecological niches of three teuthophageous odontocetes in the northwestern Mediterranean Sea. Ocean Sci 4:49–59
Praca E, Laran S, Lepoint G, Thomé J-P, Quetglas A, Belcari P, Sartor P, Dhermain F, Ody D, Tapie N, Budzinski H, Das K (2011) Toothed whales in the northwestern Mediterranean: insight into their feeding ecology using chemical tracers. Mar Pollut Bull 62:1058–1065
Pusineri C, Magnin V, Meynier L, Spitz J, Hassani S, Ridoux V (2007) Food and feeding ecology of the common dolphin (Delphinus delphis) in the oceanic Northeast Atlantic and comparison with its diet in neritic areas. Mar Mamm Sci 23:30–47
Quérouil S, Silva MA, Cascão I, Magalhães S, Seabra MI, Machete MA, Santos RS (2008) Why do dolphins form mixed-species associations in the Azores? Ethology 114:1183–1194
Quérouil S, Freitas L, Cascão I, Alves F, Dinis A, Almeida JR, Prieto R, Borràs S, Matos JA, Mendonça D, Santos RS (2010a) Molecular insight on the population structure of common and spotted dolphins inhabiting the pelagic waters of the Northeast Atlantic. Mar Biol 157:2567–2580
Quérouil S, Freitas L, Dinis A, Alves F, Cascão I, Prieto R, Silva MA, Magalhães S, Matos JA, Santos RS (2010b) Sex bias in biopsy samples collected from free-ranging dolphins. Eur J Wildl Res 56:151–158
Roughgarden J (1976) Resource partitioning among competing species: a coevolutionary approach. Theor Popul Biol 9:388–424
Saito H, Murata M (1998) Origin of the monoene fats in the lipid of midwater fishes: relationship between the lipids of myctophids and those of their prey. Mar Ecol Prog Ser 168:21–33
Samuel AM, Worthy GAJ (2004) Variability in fatty acid composition of bottlenose dolphin (Tursiops truncatus) blubber as a function of body site, season, and reproductive state. Can J Zool 82:1933–1942
Santos-Reis M, Mathias ML (1996) The historical and recent distribution and status of mammals in Portugal. Hystrix 8:75–89
Silva MA (1999) Diet of common dolphins, Delphinus delphis, off the Portuguese continental coast. J Mar Biol Assoc UK 79:531–540
Silva MA, Prieto R, Magalhães S, Cabecinhas R, Cruz A, Gonçalves JM, Santos RS (2003) Occurrence and distribution of cetaceans in the waters around the Azores (Portugal), Summer and Autumn 1999–2000. Aquat Mammal 29:77–83
Smith HR, Worthy GAJ (2006) Stratification and intra- and inter-specific differences in fatty acid composition of common dolphin (Delphinus sp.) blubber: implications for dietary analysis. Comp Biochem Physiol B 143:486–499
Smith RJ, Hobson KA, Koopman HN, Lavigne DM (1996) Distinguishing between populations of fresh- and salt-water harbour seals (Phoca vitulina) using stable-isotope ratios and fatty acid probes. Can J Fish Aquat Sci 53:272–279
St Aubin DJ, Smith TG, Geraci JR (1990) Seasonal epidermal molt in beluga whales, Delphinapterus leucas. Revue canadienne de zoologie 8:359–367
Steiner L, Silva MA, Zereba J, Leal MJ et al (2008) Bryde’s Whales, Balaenoptera edeni, observed in the Azores: a new species record for the region. J Mar Biol Assoc UK. Biodiversity Records, p 6
Strandberg U, Käkelä A, Lydersen C, Kovacs KM, Grahl-Nielsen O, Hyvärinen H, Käkelä R (2008) Stratification, composition, and function of marine mammal blubber: the ecology of fatty acids in marine mammals. Physiol Biochem Zool 81:473–485
Syväranta J, Vesala S, Rask M, Ruuhijärvi J, Jones RI (2008) Evaluating the utility of stable isotope analyses of archived freshwater sample materials. Hydrobiologia 1:121–130
Thiemann GW, Iverson SJ, Stirling I (2008) Variation in blubber fatty acid composition among marine mammals in the Canadian Arctic. Mar Mamm Sci 24:91–111
Tieszen LL, BouttonTW, Tesdahl KG, Slade NA (1983) Fractionation and turnover of stable carbon isotopes in animal tissues: Implications for δ13C analysis of diet. Oecologia 57:32-37
Wade PR, Angliss R (1997) Guidelines for assessing marine mammal stocks: report of the GAMMS Workshop, April 3–5, 1996, Seattle, Washington. Office of Protected Resources, National Marine Fisheries Service, Silver Spring, Maryland
Walton M, Pomeroy P (2003) Using blubber fatty acid profiles to detect inter-annual variations in the diet of grey seals Halichoerus grypus. Mar Ecol Prog Ser 248:257–266
Walton MJ, Silva MA, Magalhães SM, Prieto R, Santos RS (2007) Using blubber biopsies to provide ecological information about bottlenose dolphins (Tursiops truncatus) around the Azores. J Mar Biol Assoc UK 87:223–230
Wang C, Harris WS, Chung M, Lichtenstein AH, Balk EM, Kupelnick B, Jordan HS, Lau J (2006) n-3 Fatty acids from fish or fish-oil supplements, but not α-linolenic acid, benefit cardiovascular disease outcomes in primary- and secondary-prevention studies: a systematic review. Am J Clin Nutr 84:5–17
Wheatley KE, Nichols PD, Hindell MA, Harcourt RG, Bradshaw CJA (2007) Temporal variation in the vertical stratification of blubber fatty acids alters diet predictions for lactating Weddell seals. J Exp Mar Biol Ecol 352:103–113
Williams G, Crawford MA, Perrin WF (1987) Comparison of the fatty acid component in structural lipids from dolphins, zebra and giraffe: possible evolutionary implications. J Zool 213:673–684
Young DD, Cockcroft VG (1994) Diet of common dolphins (Delphinus delphis) off the south-east coast of southern Africa: opportunism or specialization? J Zool 234:41–53
Acknowledgments
Authors are very grateful to the Portuguese Foundation for Science and Technology (FCT) and the FEDER programme for funding the GOLFINICHO project (POCI/BIA-BDE/61009/2004), S.Q.’s postdoctoral grants (IMAR/FCT-PDOC-006/2001-MoleGen and SFRH/BPD/19680/2004), A.R.C and I.C.’s investigation assistant grants (IMAR/FCT/GOLFINICHO/001/2005, 003/2006 and 004/2006) and I.C.’s doctoral grant (SFRH/BD/41192/2007). They also acknowledge FCT for its pluri-annual funding to Research Unit #531. They wish to thank two anonymous referees who commented on an earlier version of the manuscript, as well as S. Borràs, J. Wiszniewski and all the persons who contributed to this project, with special thanks to the skippers (P. Martins, V. Rosa, R. Bettencourt, N. Serpa, H. Vieira and J. Viveiros), whose dexterity greatly helped sample collection. Sample collection and analysis complied with the current Portuguese laws. Samples were obtained under sampling permits 06/CN/2002, 11/CN/2003, 3/CN/2004 and 7/CN/2005 of the Environment Directorate of the Regional Government of the Azores, and Of. 668/04 Inf 711/04 DAC/DSCN, Credential no. 103-107/2006/CAPT from the Instituto de Conservação da Natureza.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by U. Siebert.
Rights and permissions
About this article
Cite this article
Quérouil, S., Kiszka, J., Cordeiro, A.R. et al. Investigating stock structure and trophic relationships among island-associated dolphins in the oceanic waters of the North Atlantic using fatty acid and stable isotope analyses. Mar Biol 160, 1325–1337 (2013). https://doi.org/10.1007/s00227-013-2184-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00227-013-2184-x