Skip to main content

Advertisement

SpringerLink
Log in

Trace elements in subantarctic false killer whale (Pseudorca crassidens) tissues, including the skin as an offshore bioindicator

Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

On a global scale, cetaceans are recognized well indicators of marine ecosystem health. Trace elements accumulate in their bodies and potentially constitute a toxicological threat. Here, the concentrations of essential Se; unknown physiological elements Br, Rb, Cs, Ni, and Sr; and pollutants arsenic, Cd, Hg, and Ag were assessed in the skin of false killer whales (Pseudorca crassidens) stranded at Estrecho de Magallanes, South America, and next, tissue comparisons and relationships between elemental concentrations in the skin and internal tissues (liver, kidney, spleen, lung, skeletal muscle, and testis) were assessed. Results showed elemental concentration variations among tissues. Selenium concentration was found to be higher in the liver 398 (75) μg g−1 dry weight (DW) (standard deviation in parenthesis), followed by skin. Rubidium and Br concentrations were higher in testis 7.92 (0.42) and 99.1 (5.4) μg g−1 DW, respectively, and Cs in muscle 0.36 (0.12) μg g−1 DW, while Ni concentrations range (<0.05–0.91 μg g−1 DW) did not show differences among tissues. Cadmium and arsenic were found to be higher in kidneys, 71.2 (17.6) and 2.54 (1.77) μg g−1 DW, respectively, while Hg was highest in the liver 1068 (234) μg g−1 DW. Concerning inter-tissue relationships, a positive skin-to-kidney and skin-to-muscle correlations were observed for Cs concentrations, and also Hg showed positive skin-to-spleen, skin-to-kidney, and skin-to-testis correlations, which support its use as potential offshore marine biomonitor.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (Finland)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Data Availability

Not applicable.

References

  • Agency for Toxic Substances and Disease Registry (ATSDR) (2007) CERCLA priority list of hazardous substances. Department of Health and Human Services, Washington, DC

  • Aubail A, Méndez-Fernandez P, Bustamante P, Churlaud C, Ferreira M, Vingada JV, Caurant F (2013) Use of skin and blubber tissues of small cetaceans to assess the trace element content of internal organs. Mar Pollut Bull 76:158–169

    Article  CAS  Google Scholar 

  • Baird RW (2018) Pseudorca crassidens (errata version published in 2019). The IUCN red list of threatened species 2018: e.T18596A145357488. https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T18596A145357488.en

  • Borrell A, Clusa M, Aguilar A, Drago M (2015) Use of epidermis for the monitoring of tissular trace elements in Mediterranean striped dolphins (Stenella coeruleoalba). Chemosphere 122:288–294

    Article  CAS  Google Scholar 

  • Bryan CE, Christopher SJ, Balmer BC, Wells RS (2007) Establishing baseline levels of trace elements in blood and skin of bottlenose dolphins in Sarasota Bay, Florida: implications for non-invasive monitoring. Sci Total Environ 388:325–342

    Article  CAS  Google Scholar 

  • Bustamante P, Caurant F, Fowler SW, Miramand P (1998) 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 

  • Cáceres-Saez I, Ribeiro Guevara S, Dellabianca N, Goodall RNP, Cappozzo HL (2013) Heavy metals and essential elements in Commerson’s dolphins (Cephalorhynchus c. commmersonii) from the Southwestern South Atlantic Ocean. Environ Monit Assess 185:5375–5386

    Article  Google Scholar 

  • Cáceres-Saez I, Goodall RNP, Dellabianca N, Cappozzo HL, Ribeiro Guevara S (2015) The Commerson’s dolphins (Cephalorhynchus commersonii) skin as a biomonitor of mercury and selenium in subantarctic waters. Chemosphere 138:735–743

    Article  Google Scholar 

  • Cáceres-Saez I, Ribeiro Guevara S, Goodall RNP, Dellabianca NA, Cappozzo HL (2017) Elemental concentrations in skin and internal tissues of Commerson’s dolphins (Cephalorhynchus commersonii) from subantarctic waters. Polar Biol 40(2):351–364

    Article  Google Scholar 

  • Cáceres-Saez I, Haro D, Blank O, Aguayo-Lobo A, Dougnac C, Arredondo C, Cappozzo HL, Ribeiro Guevara S (2018) High status of mercury and selenium in false killer whales (Pseudorca crassidens, Owen 1846) stranded on southern South America: a possible toxicological concern? Chemosphere 199:637–646

    Article  Google Scholar 

  • Cáceres-Saez I, Haro D, Blank O, Aguayo-Lobo A, Dougnac C, Arredondo C, Cappozzo HL, Guevara Riberio S (2019) Stranded false killer whales, Pseudorca crassidens, in Southern South America reveal potentially dangerous silver concentrations. Mar Pollut Bull 145:325–333

    Article  Google Scholar 

  • Carvalho ML, Pereira RA, Brito J (2002) Heavy metals in soft tissues of Tursiops truncatus and Delphinus delphis from West Atlantic Ocean by X-ray spectrometry. Sci Total Environ 292(3):247–254

    Article  CAS  Google Scholar 

  • Caurant E, Amiard-Triquet C (1995) Cadmium contamination in pilot whales Globicephala melas: source and potential hazard to the species. Mar Pollut Bull 30(3):207–210

    Article  CAS  Google Scholar 

  • Chen M-H, Zhuang M-F, Chou L-S, Liu J-Y, Shih C-C, Chen C-Y (2017) Tissue concentrations of four Taiwanese toothed cetaceans indicating the silver and cadmium pollution in the western Pacific Ocean. Mar Poll Bull 124(2):993–1000

  • Cuvin-Aralar ML, Furness RW (1991) Mercury and selenium interaction: a review. Ecotoxicol Environ Saf 21(3):348–364

    Article  CAS  Google Scholar 

  • Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity and carcinogenicity. Crit Rev Oncol Hematol 42:35–56

    Article  CAS  Google Scholar 

  • Desforges J-PW, Sonne C, Levin M, Siebert U, De Guise S, Dietz R (2016) Immunotoxic effects of environmental pollutants in marine mammals. Environ Int 86:126–139

    Article  CAS  Google Scholar 

  • Eisler R (1988) Arsenic hazards to fish, wildlife, and invertebrates: a synoptic review. Patuxent Wildlife Research Center, U.S. Fish and Wildlife Service. Biological Reports 85(1.12), Contaminant Hazard Reviews, Report No. 12, pp. 65.

  • EU Commission Regulation as regards heavy metals. Directive 2001/22/EC, No. 466/ 2001 EEC as amended by regulation 221/2002/EC.

  • Fujise Y, Honda K, Tatsukawa R, Mishima S (1988) Tissue distribution of heavy metals in Dall’s porpoise in the northwestern Pacific. Mar Pollut Bull 19:226–230

    Article  CAS  Google Scholar 

  • Genchi G, Carocci A, Lauria G, Sinicropi MS, Catalano A (2020) Nickel: human health and environmental toxicology. Int J Environ Res Public Health 17(3):679

    Article  CAS  Google Scholar 

  • Haro D, Aguayo-Lobo A, Blank O, Cifuentes C, Dougnac C, Arredondo C, Pardo C, Cáceres-Saez I (2015) Nuevo varamiento masivo de orca falsa, Pseudorca crassidens, en el Estrecho de Magallanes, Chile. Rev Biol Mar Oceanogr 50:149–155

    Article  Google Scholar 

  • Honda K, Tatsukawa R, Fujiyama T (1982) Distribution characteristics of heavy metals in the organs and tissues of striped dolphin, Stenella coeruleoalba. Agric Biol Chem 46(12):3011–3021

    CAS  Google Scholar 

  • Hopkins BJ, Tuttle LW, Pories WJ, Strain WH (1963) Strontium-90 in hair. Science 139:1064–1065

    Article  CAS  Google Scholar 

  • Ikemoto T, Kunito T, Watanabe I, Yasunaga G, Baba N, Miyazaki N, Petrov EA, Tanabe S (2004) Comparison of trace element accumulation in Baikal seals (Pusa sibirica), Caspian seals (Pusa caspica) and northern fur seals (Callorhinus ursinus). Environ Pollut 127:83–97

    Article  CAS  Google Scholar 

  • Jarup L, Akesson A (2009) Current status of cadmium as an environmental health problem. Toxicol Appl Pharmacol 238(3):201–208

    Article  Google Scholar 

  • Koen Alonso M, Pedraza SN, Schiavini ACM, Goodall RNP, Crespo EA (1999) Stomach contents of false killer whales (Pseudorca crassidens) stranded on the coasts of the Strait of Magellan, Tierra del Fuego. Mar Mamm Sci 15:712–724

    Article  Google Scholar 

  • Kohrle J, Jakob F, Contempre B, Dumont JE (2005) Selenium, the thyroid, and the endocrine system. Endocr Rev 26:944–984

    Article  CAS  Google Scholar 

  • Kunito T, Watanabe I, Yasunaga G, Fujise Y, Tanabe S (2002) Using trace elements in skin to discriminate the populations of minke whales in southern hemisphere. Mar Environ Res 53:175–197

    Article  CAS  Google Scholar 

  • Kunito T, Nakamura S, Ikemoto T, Anan Y, Kubota R, Tanabe S, Rosas FCW, Fillman G, Readman JW (2004) Concentration and subcellular distribution of trace elements in liver of small cetaceans incidentally caught along the Brazilian coast. Mar Pollut Bull 49:574–578

    Article  CAS  Google Scholar 

  • Kunito T, Kubota R, Fujihara J, Aqusa T, Tanabe S (2008) Arsenic in marine mammals, seabirds, and sea turtles. Rev Environ Contam Toxicol 195:31–69

    CAS  Google Scholar 

  • Law RJ, Stringer RL, Allchin CR, Jones BR (1996) Metals and organochlorines in sperm whales (Physeter macrocephalus) stranded around the North Sea during the 1994/1995 winter. Mar Pollut Bull 32:72–77

    Article  CAS  Google Scholar 

  • Mackey EA, Demiralp R, Becker PR, Greenberg RR, Koster BJ, Wise SA (1995) Trace element concentrations in cetacean liver tissues archived in the National Marine Mammal Tissue Bank. Sci Total Environ 175(1):25–41

    Article  CAS  Google Scholar 

  • McCall AS, Cummings CF, Bhave G, Vanacore R, Page-McCaw A, Hudson BG. 2014. Bromine is an essential trace element for assembly of collagen IV scaffolds in tissue development and architecture. Cell 157(6):1380–1392

  • Méndez-Fernandez P, Webster L, Chouvelon T, Bustamante P, Ferreira M, González AF, López A, Moffat F, Pierce GJ, Read FL, Russell M, Santos MB, Spitz J, Vingada JV, Caurant F (2014) An assessment of contaminant concentrations in toothed whale species of the NW Iberian Peninsula: Part II. Trace element concentrations. Sci Total Environ 484:206–217

    Article  Google Scholar 

  • Miller PJO, Shapiro AD, Deecke VB (2010) The diving behavior of mammal-eating killer whales (Orcinus orca): variation with ecological not physiological factors. Can J Zool 88:1103–1112

    Article  Google Scholar 

  • Monaci F, Borrell A, Leonzio C, Marsili L, Calzada N (1998) Trace elements in striped dolphins (Stenella coeruleoalba) from the western Mediterranean. Environ Pollut 99:61–68

    Article  CAS  Google Scholar 

  • Mouton M, Botha A, Thornton M, Mesjasz-Przybyłowicz J, Przybyłowicz WJ (2015) Elemental distribution patterns in the skins of false killer whales (Pseudorca crassidens) from a mass stranding in South Africa, analyzed using micro-PIXE. Nucl Inst Methods Phys Res B 363:70–74

    Article  CAS  Google Scholar 

  • O’Hara TM, Hanns C, Wöshner VM, Zeh J, Bratton G, Taylor R (2008) Essential and non-essential elements in the bowhead whale: epidermis-based predictions of blubber, kidney, liver and muscle tissue concentrations. J Cetacean Res Manag 10:107–117

    Google Scholar 

  • Owen RA (1846) A history of British fossil mammals and birds. London, pp 560

  • Paludan-Müller P, Agger CT, Dietz R, Kinze CC (1993) Mercury, cadmium, zinc, copper and selenium in harbour porpoise (Phocoena phocoena) from west Greenland. Polar Biol 13:311–320

    Article  Google Scholar 

  • Rosenthal HL, Cochban OA, Eves MM (1972) Strontium content of mammalian bone, diet and excretal. Environ Res 5:182–191

    Article  CAS  Google Scholar 

  • Santra A, Gupta JD, De BK, Ray B, Mazumder DNG (1999) Hepatic manifestation in chronic arsenic toxicity. Indian Soc Gastroenerology 18:152–155

    CAS  Google Scholar 

  • Savery LC, Evers DC, Wise SS, Falank C, Wise J, Gianios C Jr, Kerr I, Payne R, Thompson WD, Perkins C, Zheng T, Zhu C, Benedict L, Wise JP (2013) Global mercury and selenium concentrations in skin from free-ranging sperm whales (Physeter macrocephalus). Sci Total Environ 450-451:59–71

    Article  CAS  Google Scholar 

  • Savery LC, Wise J, Wise S, Falank C, Gianios C Jr, Thompson WD, Perkins C, Zheng T, Zhu C, Pierce Wise J (2014) Global assessment of arsenic pollution using sperm whales (Physeter macrocephalus) as an emerging aquatic model organism. Comp Biochem Physiol Part C 163:55–63

    CAS  Google Scholar 

  • Savery LC, Li Chen T, Wise JTF, Wise SS, Gianios C Jr, Buonagurio J, Perkins C, Falank C, Zheng T, Zhu C, Wise JP Sr (2015) Global assessment of cadmium concentrations in the skin of free-ranging sperm whales (Physeter macrocephalus). Comp Biochem Physiol Part C 178:136–144

    CAS  Google Scholar 

  • Sengupta A, Lichti UF, Carlson BA, Ryscavage AO, Gladyshev VN, Yuspa SH, Hatfield DL (2010) Selenoproteins are essential for proper keratinocyte function and skin development. PLoS One 5(8):e12249

    Article  Google Scholar 

  • Sørmo EG, Ciesielski TM, Øverjordet IB, Lierhagen S, Eggen GS, Berg T, Jenssen BM (2011) Selenium moderates mercury toxicity in free-ranging freshwater fish. Environ Sci Technol 45:6561–6566

    Article  Google Scholar 

  • Stavros HW, Bossart GD, Hulsey TC, Fair PA (2007) Trace element concentrations in skin of free-ranging bottlenose dolphins (Tursiops truncatus) from the southeast Atlantic coast. Sci Total Environ 388:300–315

    Article  CAS  Google Scholar 

  • Stavros HCW, Stolen M, Durden WN, McFee W, Bossart GD, Fair PA (2011) Correlation and toxicological inference of trace elements in tissues from stranded and free-ranging bottlenose dolphins (Tursiops truncatus). Chemosphere 82:1649–1661

    Article  CAS  Google Scholar 

  • Stacey PJ, Leatherwood S, Baird RW (1994) Pseudorca crassidens. Mamm Species 456:1–6

    Article  Google Scholar 

  • Storelli MM, Giacominelli R, Storelli A, Marcotrigiano GO (2005) Accumulation of mercury, cadmium, lead and arsenic in swordfish and bluefin tuna from the Mediterranean Sea: A comparative study. Mar Poll Bull 44:281–288

  • Sun X, Yu RQ, Zhang M, Zhang XY, Chen X, Xiao YS, Ding YL, Wu YP (2017) Correlation of trace element concentrations between epidermis and internal organ tissues in Indo-Pacific humpback dolphins (Sousa chinensis). Sci Total Environ 605:238–245

    Article  Google Scholar 

  • Theron AJ, Tintinger GR, Anderson R (2013) Harmful interactions of nonessential heavy metals with cells of the innate immune system. J Clin Toxic S3:005

    Google Scholar 

  • Thompson DR (1990) Metal levels in marine vertebrates. In: Furness RW, Rainbow PS (eds) Heavy metals in the marine environment. CRC Press, pp 143–182

  • Tu NPC, Agusa T, Ha NN, Tuyen BC, Tanabe S, Takeuchi I (2011) Stable isotope-guided analysis of biomagnification profiles of arsenic species in a tropical mangrove ecosystem. Mar Poll Bull 63(5–12):124–134

  • Ueno S, Nakashima K, Sakamoto Y, Wada S (2015) Synthesis of silver-strontium titanate hybrid nanoparticles by sol-gel-hydrothermal method. Nanomaterials 5:386–397

    Article  CAS  Google Scholar 

  • Wagemann R, Muir D (1984) Concentrations of heavy metals and organochlorines in marine mammals of Northern waters: overview and evaluation. Can Tech Rep Fish Aquat Sci 1279:1–97

    Google Scholar 

  • Wagemann R, Innes S, Richard PR (1996) Overview and regional and temporal differences of heavy metals in Arctic whales and ringed seals in the Canadian Arctic. Sci Total Environ 186:41–66

    Article  CAS  Google Scholar 

  • Wagemann R, Kozlowska H (2005) Mercury distribution in the skin of beluga (Delphinapterus leucas) and narwhal (Monodon monoceros) from the Canadian Arctic and mercury burdens and excretion by moulting. Sci Total Environ 351-352:333–343

    Article  CAS  Google Scholar 

  • Wang J, Houk RS, Dreessen D, Wiederin DR (1998) Identification of inorganic elements in proteins in human serum and in DNA fragments by size exclusion chromatography and inductively coupled plasma mass spectrometry with a magnetic sector mass spectrometer. J Am Chem Soc 120:5793–5799

    Article  CAS  Google Scholar 

  • Wise JP Sr, Thompson WD, Wise SS, LaCerte C, Wise J, Gianios C Jr, Perkins C, Zheng T, Benedict L, Mason MD, Payne R, Kerr I (2011) A global assessment of gold, titanium, strontium and barium pollution using sperm whales (Physeter Macrocephalus) as an indicator species. J Ecosys Ecograph 1:1

    Google Scholar 

  • Wise JP Jr, Wise JTF, Wise CF, Wise SS, Gianios C Jr, Xie H, Walter R, Boswell M, Zhu C, Zheng T, Perkins C, Wise P Sr (2018) A three year study of metal levels in skin biopsies of whales in the Gulf of Mexico after the Deepwater Horizon oil crisis. Comp Biochem Physiol C Toxicol Pharmacol 205:15–25

    Article  CAS  Google Scholar 

  • Wise JP Jr, Wise JTF, Wise CF, Wise SS, Zhu C, Browning CL, Zheng T, Perkins C, Gianios Jr. C. Xie H, Wise Sr. JP (2019a) Metal levels in whales from the Gulf of Maine: a one environmental health approach. Chemosphere 216:653–660

  • Wise JP Jr, Croom-Perez TJ, Meaza I, Aboueissa AE-M, López Montalvo CA, Martin-Bras M, Speer RM, Bonilla-Garzón A, Urbán JR, Perkins C, Wise JP Sr (2019b) A whale of a tale: a one environmental health approach to study metal pollution in the Sea of Cortez. Toxicol Appl Pharmacol 376:58–69

    Article  CAS  Google Scholar 

  • Wöshner VW, O’Hara TM, Bratton GR, Suydam RS, Beasley VR (2001) Concentrations and interactions of selected essential and non-essential elements in bowhead and beluga whales of Arctic Alaska. J Wildl Dis 37:693–710

    Article  Google Scholar 

  • Wöshner V, Knott K, Wells R, Willetto C, Swor R, O’Hara T (2008) Mercury and selenium in blood and epidermis of bottlenose dolphins (Tursiops truncatus) from Sarasota Bay, FL: interaction and relevance to life history and hematologic parameters. EcoHealth 5:360–370

    Article  Google Scholar 

  • Xiong X, Qian Z, Mei Z, Wu J, Hao Y, Wang K, Wu C, Wang D (2019) Trace elements accumulation in the Yangtze finless porpoise (Neophocaena asiaeorientalis asiaeorientalis) – a threat to the endangered freshwater cetacean. Sci Total Environ 686:797–804

    Article  CAS  Google Scholar 

  • Yang J, Kunito T, Tanabe S, Amano M, Miyazaki N (2002) Trace elements in skin of Dall’s porpoises (Phocoenoides dalli) from the northern waters of Japan: an evaluation for utilization as non-lethal tracers. Mar Pollut Bull 45:230–236

    Article  CAS  Google Scholar 

  • Zhang X, Lin W, Yu R-Q, Sun X, Ding Y, Chen H, Chen X, Wu Y (2017) Tissue partition and risk assessments of trace elements in Indo-Pacific Finless Porpoises (Neophocaena phocaenoides) from the Pearl River Estuary coast, China. Chemosphere 185:1197–1207

    Article  CAS  Google Scholar 

  • Zeisler R, Demiralp R, Koster BJ, Becker PR, Burow M, Ostapczuk P, Wise S (1993) Determination of inorganic constituents in marine mammal tissues. Sci Total Environ 139-140:365–386

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to volunteers who allowed necropsies and field support. We sincerely appreciate the officers of Armada de Chile. This study is a part of a binational research program between Chile and Argentina, approved by the Secretaría de Gobierno de Ambiente y Desarrollo Sustentable de la Nación, Argentina (license N° 2680428/16). All the samples were imported from Punta Arenas, Chile, to Buenos Aries, Argentina, under CITES N° 16CL000003WS.

Author information

Authors and Affiliations

  1. Consejo Nacional de Investigaciones Científicas y Técnicas, Museo Argentino de Ciencias Naturales Bernardino Rivadavia, Avenida Ángel Gallardo 470 (C1405DJR), Buenos Aires, Argentina

    Iris Cáceres-Saez & H. Luis Cappozzo

  2. Centro Bahía Lomas, Facultad de Ciencias, Universidad Santo Tomas, Avenida Costanera, 01834, Punta Arenas, Chile

    Daniela Haro

  3. Clínica Veterinaria Timaukel y Centro de Rehabilitación de Aves Leñadura (CRAL), José Pithon, 01316, Punta Arenas, Chile

    Olivia Blank

  4. Instituto Antártico Chileno (INACH), Plaza Muñoz Gamero, 1055, Punta Arenas, Chile

    Anelio Aguayo-Lobo

  5. Wildlife Conservation Society, Balmaceda, 586, Punta Arenas, Chile

    Catherine Dougnac & Cristóbal Arredondo

  6. Tarukari, Non-government Organization (no number), Santiago, Chile

    Cristóbal Arredondo

  7. Laboratorio de Análisis por Activación Neutrónica, Centro Atómico Bariloche, Av. Bustillo, 8500, Bariloche, Argentina

    Sergio Ribeiro Guevara

Authors
  1. Iris Cáceres-Saez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniela Haro
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Olivia Blank
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anelio Aguayo-Lobo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Catherine Dougnac
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Cristóbal Arredondo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. H. Luis Cappozzo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sergio Ribeiro Guevara
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

ICS and SRG: investigation and study design. ICS, DHD, OB, CD, and CA: methodology in the field. SRG, OB, and AGL: logistical resources. ICS and DHD: sample conditioning and processing in laboratory. SRG: analytical methods. ICS and SRG: data processing and writing original draft. ICS, DHD, OB, CD, CA, AAL, HLC, and SRG: writing-review and editing the manuscript.

Corresponding author

Correspondence to Iris Cáceres-Saez.

Ethics declarations

Ethics approval

Not applicable.

Consent to participate

No conflicts.

Consent for publication

No conflicts.

Competing interests

The authors declare no competing interests.

Additional information

Responsible Editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 32 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Cáceres-Saez, I., Haro, D., Blank, O. et al. Trace elements in subantarctic false killer whale (Pseudorca crassidens) tissues, including the skin as an offshore bioindicator. Environ Sci Pollut Res 28, 31746–31757 (2021). https://doi.org/10.1007/s11356-021-12890-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-12890-1

Keywords

Search

Navigation