50
Views
0
CrossRef citations to date
0
Altmetric
Ecology

Comparison of carbon, nitrogen, and oxygen stable isotope ratios and mercury concentrations in muscle tissues of five beaked whale species and sperm whales stranded in Hokkaido, Japan

, , , , &
Pages 251-271 | Received 26 Dec 2023, Accepted 10 Apr 2024, Published online: 04 Jun 2024

References

  • Brownell Jr RI, Kasuya T. Sato’s beaked whale: A new cetacean species discovered around Japan. Mar Mamm Sci. 2021;37:768–771. doi: 10.1111/mms.12810
  • MacLeod CD, Santos MB, Pierce GP. Review of data on diets of beaked whales: evidence of niche separation and geographic segregation. J Mar Biol Assoc UK. 2003;83:651–665. doi: 10.1017/S0025315403007616h
  • Ruiz-Cooley RI, Gendron D, Aguiniga S, et al. Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Mar Ecol Prog Ser. 2004;277:275–283. doi: 10.3354/meps277275
  • MacLeod CD. Beaked whales, overview. In: Würsig B, Thewissen JGM, Kovacs KM, editors. Encyclopedia of marine mammals. 3rd ed. London: Academic Press; 2017. p. 80–82.
  • Ellis R, Mead JG. Beaked whales. A complete guide to their biology and conservation. Baltomore, ML: Johns Hopkins University Press; 2017.
  • Cherel Y, Ridoux V, Spitz J, et al. Stable isotopes document the trophic structure of a deep-sea cephalopod assemblage including giant octopod and giant squid. Biol Lett. 2009;5:364–367. doi: 10.1098/rsbl.2009.0024
  • Whitehead H. Sperm whale. In: Würsig B, Thewissen JGM, Kovacs KM, editors. Encyclopedia of marine mammals. 3rd ed. London: Academic Press; 2017. p. 919–925.
  • Ciner B, Wang Y, Parker W. Oxygen isotopic variations in modern cetacean teeth and bones: implications for ecological, paleoecological, and paleoclimatic studies. Sci Bull. 2016;61:92–104. doi: 10.1007/s11434-015-0921-x
  • Endo T, Matsuishi T, Fujii Y, et al. Marine environment and contaminations of radiocesium and organohalogens in cetaceans and pacific cod inhabiting the coastal waters around Hokkaido, Northern Japan. In: Charles L, editor. Marine environments: Diversity, threats and conservation. Hauppauge, NY: Nova Science Publishers; 2020. p. 199–255.
  • Nakamura T, Kimura O, Matsuda A, et al. Radiocesium contamination of cetaceans stranded along the coast of Hokkaido, Japan, and an estimation of their travel routes. Mar Ecol Prog Ser. 2015;535:1–9. doi: 10.3354/meps11432
  • Fujii Y, Kato Y, Sakamoto K, et al. Tissue-specific bioaccumulation of long-chain perfluorinated carboxylicacids and halogenated methylbipyrroles in Dall’s porpoises (Phocoenoides dalli) and harbor porpoises (Phocoena phocoena) stranded in northern Japan. Sci Total Environ. 2018;616–617:554–563. doi: 10.1016/j.scitotenv.2017.10.033
  • Nakagun S, Watanabe K, Matsuishi T, et al. Surveillance of amyloidosis in stranded and bycaught cetaceans off Hokkaido, Japan. J Vet Med Sci. 2019;81:897–902. doi: 10.1292/jvms.18-0706
  • Yamada TK, Kitamura S, Abe S, et al. Description of a new species of beaked whale (Berardius) found in the North Pacific. Sci Rep. 2019;9:12723. doi: 10.1038/s41598-019-46703-w
  • Culik BM. Review of small cetaceans: Distribution, behaviour, migration and threats. Bonn, Germany: UNEP/CMS Secretariat, Germany; 2004. (Regional Seas REPORTS and STudies; No. 177). https://wedocs.unep.org/20.500.11822/8393
  • MacLeod CD, Perrin WF, Pitman R, et al. Known and inferred distributions of beaked whale species (Cetacea: Ziphiidae). J Cetacean Res Manage. 2005;7:271–286. doi: 10.47536/jcrm.v7i3.737
  • Nishikawa M, Oguro N. Catch of the Cuvier’s beaked whales of Japan in recent years. Sci Rep Whales Res Inst. 1972;24:35–41.
  • Ohizumi H, Isoda T, Kishiro T, et al. Feeding habits of Baird’s beaked whale Berardius bairdii, in the western North Pacific and Sea of Okhotsk off Japan. Fish Sci. 2003;69:11–20. doi: 10.1046/j.1444-2906.2003.00582.x
  • Endo T, Hisamichi Y, Kimura O, et al. Stable isotope ratios of carbon and nitrogen and mercury concentrations in 13 toothed whale species taken from the western Pacific Ocean off Japan. Environ Sci Technol. 2010;44:2675–2681. doi: 10.1021/es903534r
  • Morin PA, Baker CS, Brewer RS, et al. Genetic structure of the beaked whale genus Berardius in the North Pacific, with genetic evidence for a new species. Mar Mamm Sci. 2017;33:96–111. doi: 10.1111/mms.12345
  • Kelly JF. Stable isotopes of carbon and nitrogen in the study of avian and mammalian trophic ecology. Can J Zool. 2000;78:1–27. doi: 10.1139/z99-165
  • O’Brien DM. Stable isotope ratios as biomarkers of diet for health research. Ann Rev Nutr. 2015;35:565–594. doi: 10.1146/annurev-nutr-071714-034511
  • Cherel Y, Hobson KA. Geographical variation in carbon stable isotope signatures of marine predators: a tool to investigate their foraging areas in the Southern Ocean. Mar Ecol Prog Ser. 2007;329:281–287. doi: 10.3354/meps329281
  • Baylis AMM, Orben RA, Arnould JPY, et al. Diving deeper into individual foraging specializations of a large marine predator, the southern sea lion. Oecologia. 2015;179:1053–1065. doi: 10.1007/s00442-015-3421-4
  • Chouvelon T, Spitz J, Caurant F, et al. Enhanced bioaccumulation of mercury in deep-sea fauna from the Bay of Biscay (north-east Atlantic) in relation to trophic positions identified by analysis of carbon and nitrogen stable isotopes. Deep-Sea Res Part I. 2012;65:113–124. doi: 10.1016/j.dsr.2012.02.010
  • Kalish JM. 13C and 18O isotopic disequilibria in fish otoliths: metabolic and kinetic effects. Mar Ecol Prog Ser. 1991;75:191–203. doi: 10.3354/meps075191
  • Lukeneder A, Harzhauser M, Müllegger S, et al. Stable isotopes (δ18O and δ13C) in Spirula spirula shells from three major oceans indicate developmental changes paralleling depth distributions. Mar Boil. 2008;154:175–182. doi: 10.1007/s00227-008-0911-5
  • Lin HY, Shiao JC, Chen YG, et al. Ontogenetic vertical migration of grenadiers revealed by otolith microstructures and stable isotopic composition. Deep-Sea Res Part I. 2012;61:123–130. doi: 10.1016/j.dsr.2011.12.005
  • Méndez-Fernandez P, Pierce GJ, 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. 2013;160:2825–2840.
  • Yoshida N, Miyazaki N. Oxygen isotope correlation of cetacean bone phosphate with environmental water. J Geophys Res. 1991;96:815–820. doi: 10.1029/90JC01580
  • Clementz MT, Koch PL. Differentiating aquatic mammal habitat and foraging ecology with stable isotopes in tooth enamel. Oecologia. 2001;129:461–472. doi: 10.1007/s004420100745
  • Matthews CJD, Longstaffe FJ, Ferguson SH. Dentine oxygen isotopes (δ18O) as a proxy for odontocete distributions and movements. Ecol Evol. 2016;6:4643–4653. doi: 10.1002/ece3.2238
  • Endo T, Terasaki M, Kimura O. Stable isotope ratios of carbon, nitrogen, oxygen, and mercury concentrations in North Pacific baleen whales and the comparison of their calves with toothed whale calves. J Vet Sci Med. 2022;10:10. doi: 10.13188/2325-4645.1000059
  • Endo T, Kimura O, Terasaki M, et al. Carbon, nitrogen, and oxygen stable isotope ratios of striped dolphins and short-finned pilot whales stranded in Hokkaido, northern Japan, compared with those of other cetaceans stranded and hunted in Japan. Isot Environ Health Stud. 2023;59:230–247. doi: 10.1080/10256016.2023.2234590
  • Atwell L, Hobson KA, Welch HE. Biomagnification and bioaccumulation of mercury in an Arctic marine food web: insights from stable nitrogen isotope analysis. Can J Fish Aquat Sci. 1998;55:1114–1121. doi: 10.1139/f98-001
  • Power M, Klein GM, Guiguer KRRA, et al. Mercury accumulation in the fish community of a sub-Arctic lake in relation to trophic position and carbon sources. J App Ecol. 2002;39:819–830. doi: 10.1046/j.1365-2664.2002.00758.x
  • Chouvelon T, Caurant F, Cherel Y, et al. Species- and size-related patterns in stable isotopes and mercury concentrations in fish help refine marine ecosystem indicators and provide evidence for distinct management units for hake in the Northeast Atlantic. ICES Mar Sci. 2014;71:1073–1087. doi: 10.1093/icesjms/fst199
  • Pethybridge H, Butler ECV, Cossa D, et al. Trophic structure and biomagnification of mercury in an assemblage of deepwater chondrichthyans from southeastern Australia. Mar Ecol Prog Ser. 2012;451:163–174.
  • Honda K, Tatsukawa R, Itano K, et al. Heavy metal concentrations in muscle, liver and kidney tissue of striped dolphin, Stenella coeruleoalba, and their variations with body length, weight, age and sex. Agr Biol Chem. 1983;47:1219–1228.
  • Endo T, Kimura O, Hisamichi Y, et al. Age-dependent accumulation of heavy metals in a pod of killer whales (Orcinus orca) stranded in the northern area of Japan. Chemosphere. 2007;67:51–59. doi: 10.1016/j.chemosphere.2006.09.086
  • Endo T, Hisamichi Y, Kimura O, et al. Contamination levels of mercury and cadmium in melon-headed whales (Peponocephala electra) from a mass stranding on the Japanese coast. Sci Total Environ. 2008;401:73–80. doi: 10.1016/j.scitotenv.2008.04.006
  • Choy CA, Popp BN, Kaneko JJ, et al. The influence of depth on mercury levels in pelagic fishes and their prey. PNAS. 2009;106:13865–13869. doi: 10.1073/pnas.0900711106
  • Logan JM, Lutcavage ME. Assessment of trophic dynamics of cephalopods and large pelagic fishes in the central North Atlantic Ocean using stable isotope analysis. Deep-Sea Res. Part II. 2013;95:63–73. doi: 10.1016/j.dsr2.2012.07.013
  • Peterson SH, Ackerman JT, Costa DP. Marine foraging ecology influences mercury bioaccumulation in deep-driving northern elephant seals. Proc Biol Sci. 2015;282:20150710.
  • Lehnherr I. Methylmercury biogeochemistry: a review with special reference to Arctic aquatic ecosystems. Environ Rev. 2014;22:229–243. doi: 10.1139/er-2013-0059
  • Huang SI, Chou LS, Ni IH. Comparable length at weaning in cetaceans. Mar Mamm Sci. 2009;25:875–887. doi: 10.1111/j.1748-7692.2009.00288.x
  • Carwardine, M. Whales, dolphins and porpoises. London/New York: Dorling Kindersley; 1995. (Eyewitness handbooks).
  • Leatherwood S, Reeves RR. The sierra club handbook of whales and dolphins. San Francisco, CA: Sierra Club Books; 1983.
  • Kasuya T. Baird’s beaked whale. In: Perrin W, editor. Small cetaceans of Japan: Exploitation and biology. Boca Raton (FL): CRC Press; 2017. p. 395–434. doi: https://doi.org/10.1201/b21801
  • Endo T, Kimura O, Terasaki M, et al. Body length, stable carbon, and nitrogen isotope ratios and mercury levels in common minke whales stranded along the coast of Hokkaido, Japan. Aquat Mamm. 2021;47:86–95. doi: 10.1578/AM.47.1.2021.86
  • Logan JM, Lutcavage ME. A comparison of carbon and nitrogen stable isotope ratios of fish tissues following lipid extractions with non-polar and traditional chloroform/methanol solvent systems. Rapid Commun Mass Spectrom. 2008;22:1081–1086. doi: 10.1002/rcm.3471
  • Ogasawara H, Hayasaka M, Maemoto A, et al. Stable isotope ratios of carbon, nitrogen and selenium concentration in the scalp hair of Crohn's disease patients who ingested the elemental diet Elental®. Rapid Commun Mass Spectrom. 2019;33:41–48. doi: 10.1002/rcm.8296
  • Endo T, Kimura O, Sato R, et al. Stable isotope ratios of carbon, nitrogen and oxygen in killer whales (Orcinus orca) stranded on the coast of Hokkaido, Japan. Mar Pollut Bull. 2014;86:238–243. doi: 10.1016/j.marpolbul.2014.07.012
  • Brand WA, Coplen TB, Aerts-Bijam AT, et al. Comprehensive inter-laboratory calibration of reference materials for δ18O versus VSMOW using various on-line high-temperature conversion techniques. Rapid Commun Mass Spectrom. 2009;23:999–1019. doi: 10.1002/rcm.3958
  • Endo T, Hotta Y, Hisamichi Y, et al. Stable isotope ratios and mercury levels in red meat products from baleen whales sold in Japanese markets. Ecotoxicol Environ Saf. 2012;79:35–41. doi: 10.1016/j.ecoenv.2012.01.020
  • Riccialdelli L, Viola MNP, Paranello HO, et al. Evaluating the isotopic niche of beaked whales from the southwestern South Atlantic and Southern Oceans. Mar Ecol Prog Ser. 2017;581:183–198. doi: 10.3354/meps12296
  • Meissner AM, Macleod CD, Richard P, et al. Feeding ecology of striped dolphins, Stenella coeruleoalba, in the north-western Mediterranean Sea based on stable isotope analyses. J Mar Biol Assoc. 2012;92:1677–1687. doi: 10.1017/S0025315411001457
  • Matsuda A, Yamada TK, Tajima Y, et al. Diet of mass-stranded striped dolphins (Stenella coeruleoalba) in southern Japan (east China Sea). Mamm Study. 2021;46:17–24. doi: 10.3106/ms2020-0005
  • Newsome SD, Clementz MT, Koch PL. Using stable isotope biogeochemistry to study marine mammal ecology. Mar Mamm Sci. 2010;26:509–572.
  • Borrell A, Gómez-Campos E, Aguilar A. Influence of reproduction on stable-isotope ratios: Nitrogen and carbon isotope discrimination between mothers, fetuses, and milk in the fin whale, a capital breeder. Physiol Biochem Zool. 2016;89:41–50. doi: 10.1086/684632
  • Capelli R, Das K, de Pellegrini R, et al. Distribution of trace elements in organs of six species of cetaceans from the Ligurian Sea (Mediterranean), and the relationship with stable carbon and nitrogen ratios. Sci Total Environ. 2008;390:569–578. doi: 10.1016/j.scitotenv.2007.10.036
  • Chouvelon T, Spitz J, Caurant F, et al. 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). Prog Oceanogr. 2012;101:92–105. doi: 10.1016/j.pocean.2012.01.004
  • Pinzone M, Damseaux F, Michel LN, et al. Stable isotope ratios of carbon, nitrogen and sulphur and mercury concentrations as descriptors of trophic ecology and contamination sources of Mediterranean whales. Chemosphere. 2019;237:124448. doi: 10.1016/j.chemosphere.2019.124448
  • Storelli MM, Zizzo N, Marcotrigiano GO. Heavy metals and methylmercury in tissues of Risso's dolphin (Grampus griseus) and Cuvier's beaked whale (Ziphius cavirostris) stranded in Italy (South Adriatic Sea). Bull Environ Contam Toxicol. 1999;63:703–710. doi: 10.1007/s001289901037
  • Frodello JP, Viale D, Marchand B. Metal levels in a Cuvier's beaked whale (Ziphius cavirostris) found stranded on a Mediterranean coast, Corsica. Bull Environ Contam Toxicol. 2002;69:662–666. doi: 10.1007/s00128-002-0112-8
  • Shoham-Frider E, Kerem D, Roditi-Elasar M, et al. Trace elements in tissues of cetacean species rarely stranded along the Israeli Mediterranean coast. Mar Pollut Bull. 2014;83:376–382. doi: 10.1016/j.marpolbul.2014.03.017
  • Bilandžić N, Sedak M, Dokić M, et al. Concentration of mercury and selenium in tissues of five cetacean species from Croatian coastal waters. Arch Biol Sci. 2015;67:1377–1389. doi: 10.2298/ABS140215116B
  • Borrell1 A, Vacca1 AV, Pinela AM, et al. Stable isotopes provide insight into population structure and segregation in eastern North Atlantic sperm whales. PLoS One. 2013;8(12):e82398. doi: 10.1371/journal.pone.0082398
  • Yasunaga G, Fujise Y. A note on POPs and Hg accumulation in sperm whale based on JARPN II samples collected during 2001–2013. Paper SC/F16/JR34 presented to the Scientific Commitee of International Whaling Commission; 2016. https://www.icrwhale.org/pdf/SC-F16-JR34.pdf
  • Mazzariol S, Guardo GD, Petrella A, et al. Sometimes sperm whales (Physeter macrocephalus) cannot find their way back to the high seas: A multidisciplinary study on a mass stranding. PLoS One. 2011;6(5):e19417. doi: 10.1371/journal.pone.0019417
  • Nakamura T, Tanaka T, Kimura O, et al. Comparison of radiocesium and stable isotope ratios of carbon and nitrogen among three stocks of Pacific cod (Gadus macrocephalus) around Hokkaido, Japan. Mar Pollut Bull. 2018;127:39–44. doi: 10.1016/j.marpolbul.2017.11.029
  • Payo-Paya A, Ruiz B, Cardona L, et al. Effect of tissue decomposition on stable isotope signatures of striped dolphins Stenella coeruleoalba and loggerhead sea turtles Caretta caretta. Aquat Biol. 2013;18:141–147. doi: 10.3354/ab00497

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.