Humpback whales (Megaptera novaeangliae) breeding off Mozambique and Ecuador show geographic variation of persistent organic pollutants and isotopic niches
[en] Humpback whales (Megaptera novaeangliae) from the Southern Hemisphere carry information on persistent organic pollutants (POPs) from their feeding zones in Antarctica to their breeding grounds, making this species a sentinel of contaminants accumulation in the Southern Ocean. This study aimed to evaluate driving factors, namely feeding areas, trophic level, and sex, affecting POP concentrations in the blubber of humpback whales breeding off Mozambique and off Ecuador. Biopsies of free-ranging humpback whales including blubber and skin were collected in 2014 and 2015 from Ecuador (n = 59) and in 2017 from Mozambique (n = 89). In both populations, HCB was the major contaminant followed by DDTs > CHLs > PCBs > HCHs > PBDEs. POP concentrations were significantly higher in males compared to females. HCB, DDTs, HCHs and PBDEs were significantly different between whales from the Mozambique population and the Ecuador population. Sex and feeding habits were important driving factors accounting for POP concentrations in Ecuador whales. The whales from our study had some of the lowest POP concentrations measured for humpback whales in the world. These whales fed predominantly on krill as reflected from the low δ13C and δ15N values measured in the skin. However, the isotopic niches of whales from Mozambique and Ecuador did not overlap indicating that the two populations are feeding in different areas of the Southern Ocean.
Research center :
FOCUS - Freshwater and OCeanic science Unit of reSearch - ULiège
Pinzone, Marianna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
Castro, Cristina
Jauniaux, Thierry ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Département de morphologie et pathologie (DMP)
Garigliany, Mutien-Marie ; Université de Liège - ULiège > Département de morphologie et pathologie (DMP) > Pathologie générale et autopsies
Malarvannan, Govindan
Covaci, Adrian
Das, Krishna ; Université de Liège - ULiège > Département de Biologie, Ecologie et Evolution > Océanographie biologique
✱ These authors have contributed equally to this work.
Language :
English
Title :
Humpback whales (Megaptera novaeangliae) breeding off Mozambique and Ecuador show geographic variation of persistent organic pollutants and isotopic niches
Publication date :
December 2020
Journal title :
Environmental Pollution
ISSN :
0269-7491
eISSN :
1873-6424
Publisher :
Elsevier, United Kingdom
Volume :
267
Pages :
115575
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
EXPOSURE OF HUMPBACK WHALES FROM THE SOUTHERN HEMISPHERE TO PERSISTENT ORGANIC POLLUTANTS: INFLUENCE OF THEIR ISOTOPIC NICHE, SEX AND AGE DETERMINED BY EPIGENETICS
Funders :
F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]
Acevedo, J., Rasmussen, K., Félix, F., Castro, C., Llano, M., Secchi, E., Saborío, M.T., Aguayo-Lobo, A., Haase, B., Scheidat, M., Dalla-Rosa, L., Olavarría, C., Forestell, P., Acuña, P., Kaufman, G., Pastene, L.A., Migratory destinations of humpback whales from the Magellan Strait feeding ground, southeast Pacific. Mar. Mamm. Sci. 23 (2007), 453–463, 10.1111/j.1748-7692.2007.00116.x.
Bachman, M.J., Keller, J.M., West, K.L., Jensen, B.A., Persistent organic pollutant concentrations in blubber of 16 species of cetaceans stranded in the Pacific Islands from 1997 through 2011. Sci. Total Environ. 488–489 (2014), 115–123, 10.1016/j.scitotenv.2014.04.073.
Baker, C.S., Perry, A., Bannister, J.L., Weinrich, M.T., Abernethy, R.B., Calambokidis, J., Lien, J., Lambertsen, R.H., Ramírez, J.U., Vasquez, O., Abundant mitochondrial DNA variation and world-wide population structure in humpback whales. Proc. Natl. Acad. Sci. Unit. States Am. 90 (1993), 8239–8243, 10.1073/pnas.90.17.8239.
Bengtson Nash, S.M., Castrillon, J., Eisenmann, P., Fry, B., Shuker, J.D., Cropp, R.A., Dawson, A., Bignert, A., Bohlin-Nizzetto, P., Waugh, C.A., Polkinghorne, B.J., Dalle Luche, G., McLagan, D., Signals from the South; Humpback whales carry messages of Antarctic sea-ice ecosystem variability. Global Change Biol. 24 (2018), 1500–1510, 10.1111/gcb.14035.
Bengtson Nash, S.M., Poulsen, A.H., Kawaguchi, S., Vetter, W., Schlabach, M., Persistent organohalogen contaminant burdens in Antarctic krill (Euphausia superba) from the eastern Antarctic sector: a baseline study. Sci. Total Environ. 407 (2008), 304–314, 10.1016/j.scitotenv.2008.08.034.
Bengtson Nash, S.M., Waugh, C.A., Schlabach, M., Metabolic concentration of lipid soluble organochlorine burdens in the blubber of Southern Hemisphere humpback whales through migration and fasting. Environ. Sci. Technol. 47 (2013), 9404–9413, 10.1021/es401441n.
Best, P.B., Findlay, K.P., Sekiguchi, K., Peddemors, V.M., Rakotonirina, B., Rossouw, A., Gove, D., Winter distribution and possible migration routes of humpback whales Megaptera novaeangliae in the southwest Indian Ocean. Mar. Ecol. Prog. Ser. 162 (1998), 287–299, 10.3354/meps162287.
Borrell, A., Abad-Oliva, N., Gómez-Campos, E., Giménez, J., Aguilar, A., Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans. Rapid Commun. Mass Spectrom. 26:14 (2012), 1596–1602.
Branch, T.A., Humpback whale abundance south of 60°S from three completed sets of IDCR/SOWER circumpolar surveys. J. Cetacean Res. Manag. Special is, 2011, 53–69.
Breivik, K., Sweetman, A., Pacyna, J.M., Jones, K.C., Towards a global historical emission inventory for selected PCB congeners — a mass balance approach: 3. An update. Sci. Total Environ. 377 (2007), 296–307, 10.1016/j.scitotenv.2007.02.026.
Busquets-Vass, G., Newsome, S.D., Calambokidis, J., Serra-Valente, G., Jacobsen, J.K., Aguíñiga-García, S., Gendron, D., Estimating blue whale skin isotopic incorporation rates and baleen growth rates: implications for assessing diet and movement patterns in mysticetes. PloS One, 2017, 10.1371/journal.pone.0177880.
Castro, C., Aguayo-Lobo, A., Allen, J., Dalla Rosa, L., Kaufman, G., Forestell, P., Scheidat, M., Secchi, R., Santos, M.C., Humpback Whale Identification off Ecuador and Their Migratory Connections to Antartica (Area I and II). SC/64/SH23 Presented to the 66th Scientific Committee of the International Whaling Commission. 2013.
Castro, C., Engel, M.H., Martin, A., Kaufman, G., Comparison of humpback whale identification catalogues between Ecuador, and Southern Georgia and Sandwich Islands: evidence of increased feeding area I boundary or overlap between feeding areas I and II? SC/66/SH. 2015.
Cerchio, S., Trudelle, L., Zerbini, A., Geyer, Y., Mayer, F.X., Charrassin, J., Jung, J., Adam, O., Rosenbaum, H., Satellite tagging of humpback whales off Madagascar reveals long range movements of individuals in the Southwest Indian Ocean during the breeding season. Pap. Present. To Sci. Comm. Int. Whal. Comm. 01/2013; SC/65a/SH22 1–19, 2013, 1–19.
Chikaraishi, Y., Ogawa, N.O., Kashiyama, Y., Takano, Y., Suga, H., Tomitani, A., Miyashita, H., Kitazato, H., Ohkouchi, N., Determination of aquatic food-web structure based on compound-specific nitrogen isotopic composition of amino acids. Limnol Oceanogr. Methods 7 (2009), 740–750, 10.4319/lom.2009.7.740.
Constantine, R., Jackson, J.A., Steel, D., Baker, C.S., Brooks, L.O., Burns, D., Clapham, P., Hauser, N., Madon, B., Mattila, D., Oremus, M., Poole, M., Robbins, J., Thompson, K.F., Garrigue, C., Abundance of humpback whales in Oceania using photo-identification and microsatellite genotyping. Mar. Ecol. Prog. Ser. 453 (2012), 249–261.
Corsolini, S., Covaci, A., Ademollo, N., Focardi, S., Schepens, P., Occurrence of organochlorine pesticides (OCPs) and their enantiomeric signatures, and concentrations of polybrominated diphenyl ethers (PBDEs) in the Adelie penguin food web, Antarctica. Environ. Pollut. 140 (2006), 371–382, 10.1016/j.envpol.2005.04.039.
Dale, J.J., Wallsgrove, N.J., Popp, B.N., Holland, K.N., Nursery habitat use and foraging ecology of the brown stingray Dasyatis lata determined from stomach contents, bulk and amino acid stable isotopes. Mar. Ecol. Prog. Ser. 433 (2011), 221–236, 10.3354/meps09171.
Das, K., Malarvannan, G., Dirtu, A., Dulau, V., Dumont, M., Lepoint, G., Mongin, P., Covaci, A., Linking pollutant exposure of humpback whales breeding in the Indian Ocean to their feeding habits and feeding areas off Antarctica. Environ. Pollut. 220 (2017), 1090–1099, 10.1016/j.envpol.2016.11.032.
DeNiro, M.J., Epstein, S., Influence of diet on the distribution of carbon isotopes in animals. Geochem. Cosmochim. Acta 42 (1978), 495–506.
Desforges, Jean-Pierre, W., Sonne, Christian, Milton Levin, Siebert, Ursula, Sylvain De Guise, Rune, Dietz., Immunotoxic effects of environmental pollutants in marine mammals. Environ. Int., 86, 2016, 10.1016/j.envint.2015.10.007 126–39.
Dorneles, P.R., Lailson-Brito, J., Secchi, E.R., Dirtu, A.C., Weijs, L., Dalla Rosa, L., Bassoi, M., Cunha, H.A., Azevedo, A.F., Covaci, A., Levels and profiles of chlorinated and brominated contaminants in Southern Hemisphere humpback whales, Megaptera novaeangliae. Environ. Res. 138 (2015), 49–57, 10.1016/j.envres.2015.02.007.
Dulau-Drouot, V., Fayan, J., Mouysset, L., Boucaud, V., Occurrence and residency patterns of humpback whales off Réunion Island during 2004-10. J. Cetacean Res. Manag. 12 (2012), 255–263.
Dunton, K.H., δ15N and δ13C measurements of Antarctic Peninsula fauna: trophic relationships and assimilation of benthic seaweeds. Am. Zool. 41 (2001), 99–112, 10.1093/icb/41.1.99.
Eisenmann, P., Fry, B., Holyoake, C., Coughran, D., Nicol, S., Bengtson Nash, S., Isotopic evidence of a wide spectrum of feeding strategies in Southern Hemisphere humpback whale baleen records. PloS One, 11, 2016, e0156698, 10.1371/journal.pone.0156698.
Elfes, C.T., Vanblaricom, G.R., Boyd, D., Calambokidis, J., Clapham, P.J., Pearce, R.W., Robbins, J., Salinas, J.C., Straley, J.M., Wade, P.R., Krahn, M.M., Geographic variation of persistent organic pollutant levels in humpback whale (Megaptera novaeangliae) feeding areas of the North Pacific and North Atlantic. Environ. Toxicol. Chem. 29 (2010), 824–834, 10.1002/etc.110.
Ersts, P.J., Kiszka, J., Vély, M., Rosenbaum, H.C., Density, group composition and encounter rates of humpback whales (Megaptera novaeangliae) in the eastern Comoros archipelago (C2). J. Cetacean Res. Manag., 2011, 175–182.
Espinasse, B., Pakhomov, E., Hunt, B.P.V., Bury, S.J., Latitudinal gradient consistency in carbon and nitrogen stable isotopes of particulate organic matter in the Southern Ocean. Mar. Ecol. Prog. Ser. 631 (2019), 19–30.
Findlay, K.P., Seakamela, S.M., Meÿer, M.A., Kirkman, S.P., Barendse, J., Cade, D.E., Hurwitz, D., Kennedy, A.S., Kotze, P.G.H., McCue, S.A., Thornton, M., Vargas-Fonseca, O.A., Wilke, C.G., Humpback whale “super-groups” - a novel low-latitude feeding behaviour of Southern Hemisphere humpback whales (Megaptera novaeangliae) in the Benguela Upwelling System. PloS One, 12, 2017, 10.1371/journal.pone.0172002 e0172002–e0172002.
Fleming, A., Jackson, J., Global review of humpback whales (Megaptera novaeangliae). NOAA Technical Memorandum NMFS. NOAA-TM-NMFS-SWFSC-474. 2011, NOAA Technical Memorandum NMFS Type a message.
Flores, H., Atkinson, A., Kawaguchi, S., Krafft, B.A., Milinevsky, G., Nicol, S., Reiss, C., Tarling, G., Werner, R., Bravo Rebolledo, E.L., Cirelli, V., Cuzin-Roudy, J., Fielding, S., Van Franeker, J.A., Groeneveld, J.J., Haraldsson, M., Lombana, A., Marschoff, E., Meyer, B., Pakhomov, E., Van de Putte, A.P., Rombolá, E., Schmidt, K., Siegel, V., Teschke, M., Tonkes, H., Toullec, J.-Y., Trathan, P.N., Tremblay, N., Werner, T., Impact of climate change on Antarctic krill. Mar. Ecol. Prog. Ser. 458 (2012), 1–19.
Fossette, S., Heide-Jørgensen, M.-P., Jensen, M.V., Kiszka, J., Bérubé, M., Bertrand, N., Vély, M., Humpback whale (Megaptera novaeangliae) post breeding dispersal and southward migration in the western Indian Ocean. J. Exp. Mar. Biol. Ecol. 450 (2014), 6–14, 10.1016/j.jembe.2013.10.014.
Francois, R., Altabet, M.A., Goericke, R., McCorkle, D.C., Brunet, C., Poisson, A., Changes in the δ 13 C of surface water particulate organic matter across the subtropical convergence in the SW Indian Ocean. Global Biogeochem. Cycles 7 (1993), 627–644, 10.1029/93GB01277.
Frazer, T.K., Stable isotope composition (δ13C and δ15N) of larval krill, Euphausia superba, and two of its potential food sources in winter. J. Plankton Res. 18 (1996), 1413–1426, 10.1093/plankt/18.8.1413.
Gauthier, J.M., Metcalfe, C.D., Sears, R., Chlorinated organic contaminants in blubber biopsies from northwestern Atlantic balaenopterid whales summering in the Gulf of St Lawrence. Mar. Environ. Res. 44 (1997), 201–223.
Giménez, J., Ramírez, F., Almunia, J., G Forero, M., de Stephanis, R., From the pool to the sea: applicable isotope turnover rates and diet to skin discrimination factors for bottlenose dolphins (Tursiops truncatus). J. Exp. Mar. Biol. Ecol. 475 (2016), 54–61, 10.1016/j.jembe.2015.11.001.
Griffin, M.P.A., d15N isotope studies of life history and trophic position of Fundulus heteroclitus and Menidia menidia. Mar. Ecol. Prog. Ser. 214 (2001), 299–305.
Hageman, K.J., Bogdal, C., Scheringer, M., Chapter 11 - long-range and regional atmospheric transport of POPs and implications for global cycling. Zeng, E.Y., (eds.) Persistent Organic Pollutants (POPs): Analytical Techniques, Environmental Fate and Biological Effects, 2015, Elsevier, 363–387, 10.1016/B978-0-444-63299-9.00011-9.
Hodum, P.J., Hobson, K.A., Trophic relationships among Antarctic fulmarine petrels: insights into dietary overlap and chick provisioning strategies inferred from stable-isotope (δ15N and δ13C) analyses. Mar. Ecol. Prog. Ser. 198 (2000), 273–281, 10.3354/meps198273.
International Whaling Commission. Report of the Sub-Committee on Comprehensive Assessment of Southern Hemisphere Humpback Whales. Report of the Scientific 184 Committee. Annex G. Rep. int. Whal. Commn, 48, 1998.
Jackson, A.L., Inger, R., Parnell, A.C., Bearhop, S., Comparing isotopic niche widths among and within communities: SIBER–Stable Isotope Bayesian Ellipses in R. J. Animal Ecol. 80:3 (2011), 595–602.
Jackson, J.A., Steel, D.J., Beerli, P., Congdon, B.C., Olavarría, C., Leslie, M.S., Pomilla, C., Rosenbaum, H., Baker, C.S., Global diversity and oceanic divergence of humpback whale (Megaptera novaeangliae). Proc. R. Soc. Biol. Sci., 281, 2014, 20133222, 10.1098/rspb.2013.3222.
Jeong, Y., Lee, S., Kim, S., Park, J., Kim, H.-J., Choi, G., Choi, S., Kim, S., Kim, S.Y., Kim, S., Choi, K., Moon, H.-B., Placental transfer of persistent organic pollutants and feasibility using the placenta as a non-invasive biomonitoring matrix. Sci. Total Environ. 612 (2018), 1498–1505, 10.1016/j.scitotenv.2017.07.054.
Kajiwara, N., Kamikawa, S., Amano, M., Hayano, A., Yamada, T.K., Miyazaki, N., Tanabe, S., Polybrominated diphenyl ethers (PBDEs) and organochlorines in melon-headed whales, Peponocephala electra, mass stranded along the Japanese coasts: maternal transfer and temporal trend. Environ. Pollut. 156 (2008), 106–114, 10.1016/j.envpol.2007.12.034.
Kang, J.-H., Son, M.-H., Hur, S.-D., Hong, S., Motoyama, H., Fukui, K., Chang, Y.-S., Deposition of organochlorine pesticides into the surface snow of East Antarctica. Sci. Total Environ. 433 (2012), 290–295, 10.1016/j.scitotenv.2012.06.037.
Kannan, K., Blankenship, A.L., Jones, P.D., Giesy, J.P., Toxicity reference values for toxic effects of polychlorinated biphenyls to aquatic mammals. Hum. Ecol. Risk Assess. 6 (2000), 181–201.
Lesage, V., Morin, Y., Rioux, È., Pomerleau, C., Ferguson, S., Pelletier, E., Stable isotopes and trace elements as indicators of diet and habitat use in cetaceans: predicting errors related to preservation, lipid extraction, and lipid normalization. Mar. Ecol. Prog. Ser. 419 (2010), 249–265.
Li, Y., Lohmann, R., Zou, X., Wang, C., Zhang, L., Air-water exchange and distribution pattern of organochlorine pesticides in the atmosphere and surface water of the open Pacific ocean. Environ. Pollut., 265, 2020, 114956, 10.1016/j.envpol.2020.114956.
Lorrain, A., Graham, B., Ménard, F., Popp, B., Bouillon, S., Van Breugel, P., Cherel, Y., Nitrogen and carbon isotope values of individual amino acids: a tool to study foraging ecology of penguins in the Southern Ocean. Mar. Ecol. Prog. Ser. 391 (2009), 293–306, 10.3354/meps08215.
Macé, M., Crouau-Roy, B., A highly polymorphic insertion in the Y-chromosome amelogenin gene can be used for evolutionary biology, population genetics and sexing in Cetacea and Artiodactyla. BMC Genet. 9 (2008), 1–9, 10.1186/1471-2156-9-64.
McClelland, J.W., Valiela, I., Michener, R.H., Nitrogen-stable isotope signatures in estuarine food webs: a record of increasing urbanization in coastal watersheds. Limnol. Oceanogr. 42 (1997), 930–937, 10.4319/lo.1997.42.5.0930.
McMahon, K.W., Hamady, L.L., Thorrold, S.R., Ocean ecogeochemistry: a review. Oceanogr. Mar. Biol. Annu. Rev., 2013, 327–374.
Metcalfe, C., Koenig, B., Metcalfe, T., Paterson, G., Sears, R., Intra- and inter-species differences in persistent organic contaminants in the blubber of blue whales and humpback whales from the Gulf of St. Lawrence, Canada. Mar. Environ. Res. 57 (2004), 245–260.
Nash, S.B., Persistent organic pollutants in Antarctica: current and future research priorities. J. Environ. Monit. 13:3 (2011), 497–504.
Newsome, S.D., Yeakel, J.D., Wheatley, P.V., Tinker, M.T., Tools for quantifying isotopic niche space and dietary variation at the individual and population level. J. Mammal. 93 (2012), 329–341, 10.1644/11-MAMM-S-187.1.
Newsome, S.D., Clementz, M.T., Koch, P.L., Using stable isotope biogeochemistry to study marine mammal ecology. Mar. Mamm. Sci. 26 (2010), 509–572.
Pacheco, A., Silva, S., Alcorta, B., Winter distribution and group composition of humpback whales (Megaptera novaeangliae) off northern Peru. Lat. Am. J. Aquatic Mamm. 7 (2009), 33–38 Lat. Am. J. Aquat. Mamm. 7(1- 2): 33-38.
Pinzone, M., Budzinski, H., Tasciotti, A., Ody, D., Lepoint, G., Schnitzler, J., Scholl, G., Thomé, J.-P., Tapie, N., Eppe, G., Das, K., POPs in free-ranging pilot whales, sperm whales and fin whales from the Mediterranean Sea: influence of biological and ecological factors. Environ. Res. 142 (2015), 185–196, 10.1016/j.envres.2015.06.021.
Pinzone, M., Damseaux, F., Michel, L.N., Das, K., Stable isotope ratios of carbon, nitrogen and sulphur and mercury concentrations as descriptors of trophic ecology and contamination sources of Mediterranean whales. Chemosphere, 237, 2019, 124448, 10.1016/j.chemosphere.2019.124448.
Polanowski, Andrea, Robbins, Jooke, Chandler, David, Jarman, Simon, Epigenetic estimation of age in humpback whales. Mol. Ecol. Resour., 2014, 976–987, 10.1111/1755-0998.12247.
Polito, M.J., Reiss, C.S., Trivelpiece, W.Z., Patterson, W.P., Emslie, S.D., Stable isotopes identify an ontogenetic niche expansion in Antarctic krill (Euphausia superba) from the South Shetland Islands, Antarctica. Mar. Biol. 160 (2013), 1311–1323, 10.1007/s00227-013-2182-z.
Post, D.M., Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83 (2002), 703–718, 10.1890/0012-9658(2002)083[0703:USITET]2.0.CO;2.
Poulsen, A.H., Kawaguchi, S., Kukkonen, J.V.K., Leppänen, M.T., Bengtson Nash, S.M., Aqueous uptake and sublethal toxicity of p,p’-DDE in non-feeding larval stages of Antarctic krill (Euphausia superba). Environ. Pollut. 160 (2012), 185–191, 10.1016/j.envpol.2011.09.022.
Quezada-Romegialli, C., Jackson, A.L., Hayden, B., Kahilainen, K.K., Lopes, C., Harrod, C., tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios. Methods Ecol. Evol. 9 (2018), 1592–1599, 10.1111/2041-210X.13009.
Rasmussen, K., Palacios, D.M., Calambokidis, J., Saborío, M.T., Dalla Rosa, L., Secchi, E.R., Steiger, G.H., Allen, J.M., Stone, G.S., Southern Hemisphere humpback whales wintering off Central America: insights from water temperature into the longest mammalian migration. Biol. Lett. 3 (2007), 302–305, 10.1098/rsbl.2007.0067.
Risebrough, R.W., De Lappe, B.W., Younghans-Haug, C., PCB and PCT contamination in winter quarters bay, Antarctica. Mar. Pollut. Bull., 1990, 10.1016/0025-326X(90)90300-W.
Rosenbaum, H.C., Kershaw, F., Mendez, M., Pomilla, C., Leslie, M.S., Findlay, K.P., Best, P.B., Collins, T., Vely, M., Engel, M.H., Baldwin, R., Minton, G., Meÿer, M., Flórez-González, L., Poole, M.M., Hauser, N., Garrigue, C., Brasseur, M., Bannister, J., Anderson, M., Olavarría, C., Baker, C.S., First circumglobal assessment of Southern Hemisphere humpback whale mitochondrial genetic variation and implications for management. Endanger. Species Res. 32 (2017), 551–567, 10.3354/ESR00822.
Rosenbaum, H.C., Pomilla, C., Mendez, M., Leslie, M.S., Best, P.B., Findlay, K.P., Minton, G., Ersts, P.J., Collins, T., Engel, M.H., Bonatto, S.L., Kotze, D.P.G.H., Meÿer, M., Barendse, J., Thornton, M., Razafindrakoto, Y., Ngouessono, S., Vely, M., Kiszka, J., Population structure of humpback whales from their breeding grounds in the South Atlantic and Indian Oceans. PloS One, 4, 2009, e7318, 10.1371/journal.pone.0007318.
Ross, P.S., Ellis, G.M., Ikonomou, M.G., Barrett-Lennard, L.G., Addison, R.F., High PCB concentrations in free-ranging Pacific killer whales, Orcinus orca: effects of age, sex and dietary preference. Mar. Pollut. Bull. 40:6 (2000), 504–515.Chicago.
Ryan, C., Berrow, S.D., McHugh, B., O'Donnell, C., Trueman, C.N., O'Connor, I., Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models. Mar. Mamm. Sci. 30 (2014), 242–258, 10.1111/mms.12034.
Ryan, C., McHugh, B., Trueman, C.N., Harrod, C., Berrow, S.D., O'Connor, I., Accounting for the effects of lipids in stable isotope (δ13C and δ15N values) analysis of skin and blubber of balaenopterid whales. Rapid Commun. Mass Spectrom. 26 (2012), 2745–2754, 10.1002/rcm.6394.
Scheidat, M., Castro, C.C., Denkinger, J., González, J., Adelung, D., A breeding area for humpback whales (Megaptera novaeangliae) off Ecuador. J. Cetacean Res. Manag. 2 (2000), 165–172.
Schmidt, K., Atkinson, A., Stübing, D., JamesMcClelland, W., JosephMontoya, P., Maren, V., Trophic relationships among Southern Ocean Copepods and Krill: Some uses and limitations of a stable isotope approach. Limnol. Oceanogr., 48((1 I):277–89.), 2003, 10.4319/lo.2003.48.1.0277.
Schmidt, K., Atkinson, A., Stübing, D., McClelland, J.W., Montoya, J.P., Voss, M., Trophic relationships among Southern Ocean copepods and krill: some uses and limitations of a stable isotope approach. Limnol. Oceanogr. 48 (2003), 277–289, 10.4319/lo.2003.48.1.0277.
Silva, M.A., Prieto, R., Jonsen, I., Baumgartner, M.F., Santos, R.S., North Atlantic blue and fin whales suspend their spring migration to forage in middle latitudes: building up energy reserves for the journey?. PloS One, 8, 2013, 10.1371/journal.pone.0076507.
Stevick, P.T., Neves, M.C., Johansen, F., Engel, M.H., Allen, J., Marcondes, M.C.C., Carlson, C., A quarter of a world away: female humpback whale moves 10,000 km between breeding areas. Biol. Lett. 7 (2011), 299–302, 10.1098/rsbl.2010.0717.
Stowasser, G., Atkinson, A., McGill, R.A.R., Phillips, R.A., Collins, M.A., Pond, D.W., Food web dynamics in the Scotia Sea in summer: a stable isotope study. Deep Sea Res. Part II Top. Stud. Oceanogr. 59–60 (2012), 208–221, 10.1016/j.dsr2.2011.08.004.
Sweeting, C.J., Polunin, N.V.C., Jennings, S., Effects of chemical lipid extraction and arithmetic lipid correction on stable isotope ratios of fish tissues. Rapid Commun. Mass Spectrom. 20 (2006), 595–601, 10.1002/rcm.2347.
Todd, C.R., Ostrom, P., Lien, J., Abrajano, J., Use of biopsy samples of humpback whale (Megaptera novaeangliae) skin for stable isotope (d 13C) determination. J. Northwest Atl. Fish. Sci. 22 (1997), 71–76.
Van Den Berg, H., Global status of DDT and its alternatives for use in vector control to prevent disease. Environ. Health Perspect., 2009, 10.1289/ehp.0900785.
Wang, P., Li, Y., Zhang, Q., Yang, Q., Zhang, L., Liu, F., Fu, J., Meng, W., Wang, D., Sun, H., Zheng, S., Hao, Y., Liang, Y., Jiang, G., Three-year monitoring of atmospheric PCBs and PBDEs at the Chinese Great Wall Station, West Antarctica: levels, chiral signature, environmental behaviors and source implication. Atmos. Environ. 150 (2017), 407–416, 10.1016/j.atmosenv.2016.11.036.
Wania, F., Mackay, D., Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions. Ambio 22 (1993), 10–18.
Witteveen, B.H., Worthy, G., Roth, J., Tracing migratory movements of breeding North Pacific humpback whales using stable isotope analysis. Mar. Ecol. Prog. Ser. 393 (2009), 173–183, 10.3354/meps08231.
Witteveen, B.H., Worthy, G., Wynne, K., Roth, J., Population structure of North Pacific humpback whales on their feeding grounds revealed by stable carbon and nitrogen isotope ratios. Mar. Ecol. Prog. Ser. 379 (2009), 299–310, 10.3354/meps07900.
Wright, D.L., Variability in foraging by humpback whales (Megaptera novaeangliae) on the Kodiak, AK, feeding ground. 2014, University of Alaska Fairbanks, Fairbanks, AK, 153.
Zhang, Ye, Li, C., Yang, G., Wang, Y., Tao, Z., Zhang, Yongshan, Wang, A., Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: a stable isotope analysis. Acta Oceanol. Sin. 36 (2017), 67–78, 10.1007/s13131-017-1049-4.
Zhang, Y.E., Li, C., Yang, G., Wang, Y., Tao, Z., Zhang, Y., Wang, A., Ontogenetic diet shift in Antarctic krill (Euphausia superba) in the Prydz Bay: A stable isotope analysis. Acta Oceanologica Sinica 36:12 (2017), 67–78.Chicago.
