Abstract
The Commerson’s dolphin (Cephalorhynchus c. commersonii, Lacépède, 1804) is the most common endemic dolphin of the coastal waters of Tierra del Fuego incidentally caught in artisanal coastal gill nets. A better understanding of its trophic ecology is essential to facilitate the effective management and conservation of its population. The aim of this study was to analyze possible shifts in diet among age and sex classes by analyzing bone collagen δ13C and δ15N values collected from 220 individuals along the coast of Tierra del Fuego. Additional analysis of potential prey allowed us to use a stable isotope mixing model to quantify resource use. Isotopic comparisons suggest that all age classes share the same foraging areas. We found, however, a significant dietary shift: juveniles consume a higher mean (±SD) proportion (60 ± 7 %) of pelagic Sprattus fuegensis than adults (36 ± 10 %), and the consumption of benthopelagic species such as Illex argentinus and Loligo gahi is higher in adults (33 ± 12 %) than juveniles (20 ± 7 %). This may result from an improvement in foraging skills and expansion of habitats in adulthood. While males move greater distances in search of mates and resources, a lack of isotopic differences between the sexes suggests little evidence for sex-related resource partitioning. A significant decrease in δ15N values between calves and juveniles indicates a weaning period between 0.5 and 1 year as was shown in previous captive studies on this species. Our results also suggest that artisanal fisheries, despite being a major source of mortality, do not affect the long-term food habits of Commerson’s dolphin since they showed a weak trophic overlap.
Similar content being viewed by others
References
Ambrose SH (1990) Preparation and characterization of bone and tooth collagen for isotopic analysis. J Archaeol Sci 17:431–451
Bastida R, Lichtschein V, Goodall RNP (1988) Food habits of Cephalorhynchus commersonii off Tierra del Fuego. Rep Int Whal Comm (Spec Issue) 9:143–160
Berón Vera B, Pedraza SN, Raga JA, Gil de Pertierra A, Crespo EA, Koen Alonso M, Goodall RNP (2001) Gastrointestinal helminthes of Commerson’s dolphins Cephalorhynchus commersonii from central Patagonia and Tierra del Fuego. Dis Aquat Org 47:201–208
Cerling TE, Harris JM (1999) Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implication for ecological and paleontological studies. Oecologia 120:347–363
Cipriano F, Hevia M, Iñíguez M (2011) Genetic divergence over small geographic scales and conservation implications for Commerson’s dolphins (Cephalorhynchus commersonii) in southern Argentina. Mar Mamm Sci 27:701–718. doi:10.1111/j.1748-7692.2010.00434.x
Clarke M, Goodall RNP (1994) Cephalopods in the diets of three odontocete cetacean species stranded at Tierra del Fuego, Globicephala melaena (Traill, 1809), Hyperoodon planifrons Flower, 1882 and Cephalorhynchus commersonii (Lacépède, 1804). Antarct Sci 6:149–154
Clementz MT, Koch PL (2001) Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia 129:461–472
Collet A, Robineau D (1988) Data on the genital tract and reproduction in Commerson’s dolphin, Cephalorhynchus commersonii (Lacépède, 1804) from the Kerguelen Islands. Rep Int Whal Comm (Spec Issue) 9:119–141
Coscarella MA (2005) Ecología, comportamiento y evaluación del impacto de embarcaciones sobre manadas de tonina overa Cephalorhynchus commersonii en Bahía Engaño, Chubut. PhD Dissertation, Universidad de Buenos Aires, Argentina (in Spanish)
Coscarella MA, Pedraza SN, Crespo EA (2010) Behaviour and seasonal variation in the relative abundance of Commerson’s dolphin (Cephalorhynchus commersonii) in northern Patagonia, Argentina. J Ethol 28:463–470. doi:10.1007/s10164-010-0206-4
Dellabianca NA, Hohn AA, Goodall RNP (2012) Age estimation and growth layer patterns in teeth of Commerson’s dolphins (Cephalorhynhcus c. commersonii) in subantarctic waters. Mar Mamm Sci 28:378–388. doi:10.1111/j.1748-7692.2011.00475.x
DeNiro MJ, Epstein S (1978) Influence of diet on the distribution of carbon isotopes in animals. Geochim Cosmochim Acta 42:495–506
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim Acta 45:341–351
Dolar MLL, Suarez P, Ponganis PJ, Kooyman GL (1999) Myoglobin in pelagic small cetaceans. J Exp Biol 202:227–236
Drago M, Cardona L, Crespo EA, García N, Ameghino S, Aguilar A (2010) Change in the foraging strategy of female South American sea lions (Carnívora: Pinnipedia) after parturition. Sci Mar 74:589–598. doi:10.3989/scimar.2010.74n3589
Eichelberger L, Fetcher ES Jr, Geiling EMK, Vos BJ Jr (1940) The composition of dolphin milk. J Biol Chem 134:171–176
Fogel ML, Tuross N, Owsley DW (1989) Nitrogen isotope tracers of human lactation in modern and archaeological populations. In: Geophysical Laboratory, Carnegie Institution of Washington (publisher). Annual report of the director of the Geophysical Laboratory, Carnegie Institution of Washington, 1988–1989. Washington, DC, pp 111–117
Francey RK, Allison CE, Etheridge DM, Trudinger CM, Enting IG et al (1999) A 1,000 year record of δ13C in atmospheric CO2. Tellus B 51:170–193
Garaffo GV, Dans SL, Pedraza SN, Degrati M, Schiavini A, Gonázlez R, Crespo EA (2011) Modeling habitat use for dusky dolphin and Commerson’s dolphin in Patagonia. Mar Ecol Prog Ser 421:217–277. doi:10.3354/meps08912
Goodall RNP (1994) Commerson’s dolphin Cephalorhynchus commersonii (Lacépède 1804). In: Ridgway SH, Harrison SR (eds) Handbook of marine mammals, vol 5., The first book of dolphinsAcademic Press, London, pp 241–267
Goodall RNP, Galeazzi AR, Lichter AA (1988) Exploitation of small cetaceans off Argentina 1979–1986. Rep Int Whal Comm 38:407–410
Goodall RNP, Schiavini ACM, Fermani C (1994) Net fisheries and net mortality of small cetaceans off Tierra del Fuego, Argentina. Rep Int Whal Commn (Spec Issue) 15:295–304
Goodall RNP, Benegas LG, Boy CC, Dellabianca N, Pimper L, Riccialdelli L (2008) Review of small cetaceans stranded or incidentally captured on the coast of Tierra del Fuego, Argentina, over 33 years. Paper SC/60/SM21 presented to the Scientific Committee, International Whaling Commission, June 2008, pp 14 (unpublished). Available from www.iwcoffice.org
Graham BS, Koch PL, Newsome SD, McMahon KW, Aurioles D (2010) Using isoscapes to trace the movements and foraging behavior of top predators in oceanic ecosystems. In: West J (ed) Isoscapes: understanding movement, pattern, and process on earth through isotope mapping. Springer Science + Business Media BV, New York, pp 299–318
Hare PE, Fogel ML, Stafford TW Jr, Mitchell AD, Hoering TC (1991) The isotopic composition of carbon and nitrogen in individual amino acids isolated from modern and fossil proteins. J Archaeol Sci 18:277–292
Hedges REM, Stevens RE, Koch PL (2005) Isotopes in bones and teeth. In: Leng MJ (ed) Isotopes in palaeoenvironmental research. Springer, Netherlands, pp 117–145
Hobson KA, Sease JL (1998) Stable isotope analyses of tooth annuli reveal temporal dietary records: an example using Steller sea lion. Mar Mamm Sci 14:116–129
Idermühle A, Stocker T, Joos F, Fisher H, Smith H, Wahlen M, Deck B, Mastroianni D, Tschumi J, Blunier T, Meyer R, Stauffer B (1999) Holoce carbon-cycle dynamics based in CO2 trapped in ice at Taylor Dome, Antarctica. Nature 398:121–126
Iñíguez MA, Tossenberger VP (2007) Commerson’s dolphins (Cephalorhynchus commersonii) off Ría Deseado, Patagonia, Argentina. Aquat Mamm 33:276–285
Iñíguez MA, Hevia M, Gasparrou C, Tomsin AL, Secchi ER (2003) Preliminary estimate of incidental mortality of Commerson’s dolphins (Cephalorhynchus commersonii) in an artisanal setnet fishery in La Angelina beach and Ría Gallegos, Santa Cruz, Argentina. LAJAM 2:87–94. doi:10.5597/lajam00036
Jenkins SG, Partridge ST, Stephenson TR, Farley SD, Robbins CT (2001) Nitrogen and carbon isotope fractionation between mothers, neonates and nursing offspring. Oecologia 129:336–341
Joseph BE, Antrim JE, Cornell LH (1987) Commerson’s dolphin (Cephalorhynchus commersonii): a discussion of the first live birth within a marine zoological park. Zoo Biol 6:69–77
Kastelein RA, McBain J, Neurohr B (1993a) Information on the biology of Commerson’s dolphins (Cephalorhynchus commersonii). Aquat Mamm 19:13–19
Kastelein RA, McBain J, Neurohr B, Mohri M, Saijo S, Wakabayashi I, Wiepkema PR (1993b) The food consumption of Commerson’s dolphins (Cephalorhynchus commersonii). Aquat Mamm 19:99–121
Knoff A, Hohn A, Macko SA (2008) Ontogenetic diet changes in bottlenose dolphins (Tursiops truncatus) reflected through stable isotopes. Mar Mamm Sci 24:128–137. doi:10.1111/j.1748-7692.2007.00174.x
Lauriano G, Caramanna L, Scarno M, Andaloro F (2009) An overview of dolphin depredation in Italian artisanal fisheries. J Mar Biol Assoc UK 89:921–929. doi:10.1111/j.1748-7692.2007.00174.x
Lescrauwaet AC, Gibbons J, Guzman L, Schiavini ACM (2000) Abundance estimation of Commerson’s dolphin in the eastern area of the strait of Magellan—Chile. Rev Chil Hist Nat 73:473–478
Lockyer C, Smellie GG, Goodall RNP, Cameron IS (1981) Examination of teeth of Commerson’s dolphin, Cephalorhynchus commersonii, for age determination. J Zool Soc Lond 195:123–131
Lockyer C, Goodall RNP, Galeazzi AR (1988) Age and body length characteristics of Cephalorhynchus commersonii from incidentally-caught specimens off Tierra del Fuego. Rep Int Whal Comm (Spec Issue) 9:103–118
Martínez del Rio C, Wolf N, Carleton SA, Gannes LZ (2009) Isotopic ecology ten years after a call for more laboratory experiments. Biol Rev 84:91–111. doi:10.1111/j.1469-185X.2008.00064.x
Matthiopoulos J, Smout S, Winshio AJ, Thompson D, Boyd IL, Harwood J (2008) Getting beneath the surface of marine mammal—fisheries competition. Mammal Rev 38:167–188
Mendes S, Newton J, Reid RJ, Frantzis A, Pierce GJ (2007) Stable isotope profiles in sperm whale teeth: variations between areas and sexes. J Mar Biol Ass UK 87:621–627. doi:10.1017/S0025315407056019
Minagawa M, Wada E (1984) Stepwise enrichment of 15N along food chains: further evidence and the relation between δ15N and animal age. Geochim Cosmochim Acta 48:1135–1140
Newsome SD, Koch PL, Etnier MA, Aurioles-Gamboa D (2006) Using carbon and nitrogen isotope values to investigate maternal strategies in Northeast Pacific otariids. Mar Mamm Sci 22:556–572. doi:10.1111/j.1748-7692.2006.00043.x
Newsome SD, Etnier MA, Monson DH, Fogel ML (2009a) Retrospective characterization of ontogenetic shifts in killer whale diets via δ13C and δ15N analysis of teeth. Mar Ecol Prog Ser 374:229–242. doi:10.3354/meps07747
Newsome SD, Tinker MT, Monson DH, Oftedal OT, Ralls K, Staedler MM, Fogel ML, Estes JA (2009b) Using stable isotopes to investigate individual diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90:961–974
Newsome SD, Clementz MT, Koch PL (2010) Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci 26:509–572. doi:10.1111/j.1748-7692.2009.00354.x
Noren SR, Williams TM, Pabst DA, McLellan WA, Dearolf JL (2001) The development of diving in marine endotherms: the skeletal muscles of dolphins, penguins, and seals for activity during submergence. J Comp Physiol B 171:127–134. doi:10.1007/s003600000161
Noren SR, Lacave G, Wells RS, Williams TM (2002) The development of blood oxygen stores in bottlenose dolphins (Tursiops truncatus): implications for diving capacity. J Zool Lond 258:105–113. doi:10.1017/S0952836902001243
Noren SR, Iverson SJ, Boness SJ (2005) Development of the blood and muscle oxygen stores in gray seals (Halichoerus grypus): implications for juvenile diving capacity and the necessity of a terrestrial postweaning fast. Physiol Biochem Zool 78:482–490
Norris K (1961) Standardized methods for measuring and recording data on the smaller cetaceans. J Mammal 42:471–476
Northridge SP (1985) Estudio mundial de las interacciones entre los mamíferos marinos y la pesca. FAO Documento Técnico de Pesca 251 FIRM/T251 (in Spanish)
Oftedal OT (1997) Lactation in whales and dolphins: evidence of divergence between baleen- and toothed-species. J Mammary Gland Biol Neoplasia 2:205–230
Parnell AC, Inger R, Bearhop S, Jackson AL (2010) Source partitioning using stable isotopes: coping with too much variation. PLoS One 5:e9672
Pedraza SN (2008) Ecología de la tonina overa (Cephalorhynhcus commersonii) en el litoral patagónico. PhD Dissertation, Universidad de Buenos Aires, Argentina (in Spanish)
Perrin WF, Myrick AC (eds) (1980) Age determination of toothed whales and sirenians. Rep Int Whal Comm (Spec Issue) 3, pp 229
Pimper LE (2010) Estructura poblacional y conservación de la tonina overa, Cephalorhynchus commersonii, en Tierra del Fuego y zonas aledañas. PhD Dissertation, Universidad de Buenos Aires, Argentina (in Spanish)
Pimper LE, Remis MI, Goodall RNP, Baker SC (2009) Teeth and bones as sources of DNA for genetic diversity and sex identification of Commerson’s dolphins (Cephalorhynchus commersonii) from Tierra del Fuego, Argentina. Aquat Mamm 35:330–333. doi:10.1578/AM.35.3.2009.330
Pimper LE, Baker CS, Goodall RNP, Olavarría C, Remis MI (2010) Mitochondrial DNA variation and population structure of Commerson’s dolphins (Cephalorhynchus commersonii) in their southernmost distribution. Conservat Genet 11:2157–2168. doi:10.1007/s10592-010-0102-z
Reeves RR, Smith BD, Crespo EA, Notarbartolo di Sciara G (compilers) (2003) Dolphins, whales and porpoises: 2002–2010 conservation action plan for the world’s cetaceans. IUCN/SSC Cetacean Specialist Group. IUCN, Gland, Switzerland and Cambridge, UK, pp 139
Riccialdelli L, Newsome SD, Fogel ML, Goodall RNP (2010) Isotopic assessment of prey and habitat preferences of a cetacean community in the southwestern South Atlantic Ocean. Mar Ecol Prog Ser 418:235–248. doi:10.1578/AM.35.3.2009.330
Richards MP, Mays S, Fuller BT (2002) Stable carbon and nitrogen isotope values of bone and teeth reflect weaning age at the medieval Wharram Percy site, Yorkshire, UK. Am J Phys Anthropol 119:205–210
Richmond JP, Burns JM, Rea LD (2006) Ontogeny of total body oxygen stores and aerobic dive potential in Steller sea lions (Eumetopias jubatus). J Comp Physiol B 176:535–545. doi:10.1007/s00360-006-0076-9
Rosero Caicedo DM (2005) Dieta de la tonina overa, Cephalorhynchus commersonii (Lacépède, 1804) en Tierra del Fuego, Argentina. Bs. Dissertation, Pontificia Universidad Javeriana, Bogota DC, Colombia (in Spanish)
Tuross N, Fogel ML, Hare PE (1988) Variability in the preservation of the isotopic composition of collagen from fossil bone. Geoquim Comsoquim Acta 52:929–935
Valenzuela LO, Sironi M, Rowntree VJ (2010) Interannual variation in the stable isotope differences between mothers and their calves in southern right whales (Eubalaena australis). Aquat Mamm 36:138–147. doi:10.1578/AM.36.2.2010.138
Young BG, Loseto LL, Ferguson SH (2010) Diet differences among age classes of Arctic seals: evidence from stable isotope and mercury biomarkers. Polar Biol 33:153–162. doi:10.1007/s00300-009-0693-3
Acknowledgments
We thank Santiago Favoretti for his assistance during different steps of the study. The Centro Austral de Investigaciones Científicas and Museo Acatushún de Aves y Mamíferos Marinos Australes also provided logistical support. We also thank the Carnegie Institution of Washington and W. M. Keck Foundation for financial support and Will Würzel, Mónica Torres and María Natalia Paso Viola for technical assistance. We also thank Lida Pimper for genetic data and especially appreciate the hard work of volunteers who located strandings, obtained vital data and cleaned specimens. The Committee for Research and Exploration (CRE) of the National Geographic Society has supported the work of RNP. LR has been supported under a PhD and a postdoctoral fellowship from the Consejo Nacional de Investigaciones Científicas y Técnicas of Argentina (CONICET) and funded by grants from Cetacean Society International, Sigma-Xi Committee on Grants-in-Aid of Research, and Conservation and Research and Education Opportunities (CREO). Bone samples were exported under CITES permits 029884 and 029885 granted by the Ministerio de Salud y Ambiente, Secretaría de Ambiente y Desarrollo Sustentable, Buenos Aires, Argentina.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Riccialdelli, L., Newsome, S.D., Dellabianca, N.A. et al. Ontogenetic diet shift in Commerson’s dolphin (Cephalorhynchus commersonii commersonii) off Tierra del Fuego. Polar Biol 36, 617–627 (2013). https://doi.org/10.1007/s00300-013-1289-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-013-1289-5