STABLE ISOTOPES ANALYSIS ON BALEEN WHALES (SUBORDER: MYSTICETI): A REVIEW UNTIL 2017
DOI:
https://doi.org/10.18764/1981-6421e2020.10Keywords:
Baleen whales, Mysticeti, Stable Isotopes Analysis, Conservation EcologyAbstract
ABSTRACT
Stable Isotope Analysis (SIA) has provided information on ocean productivity, and ecological aspects related to whales’ habitat use and feeding ecology, stock structure, physiology, and evolution. We reviewed published studies using SIA on whales worldwide from November 1979 to June 2017. Gaps in geographical areas and heterogeneity amongst species studied using this methodology were
assessed. We also investigated which tissue was most frequently analysed, sources of variation in stable isotope values, how this methodology has been combined with other techniques, and how it can be useful for the conservation of the taxon and marine ecosystems. A total of 63 publications were found, and it was possible to detect a general increase in the number of publications along time, as 49% of the studies were from the last 7.5 years of the period analyzed. Almost 55% of studies focused on foraging ecology and habitat use. The baleen plate was the main tissue analyzed. Studies were related to 14 species, the most common being the fi n whale, Balaenoptera physalus (N=19) and the bowhead whale, Balaena mysticetus (N=18). Telemetry and SIA methodologies combined were helpful to understand geographical variations in stable isotope values. The methodology can also be valuable under the current scenario of climate change, for example providing information on feeding plasticity and changes in niche amplitude of diff erent species. Despite uncertainties related with stable isotopes distribution in the ocean, and with its incorporation rates for whales, for example, SIA provides primordial ecological information for effi cient management and conservation of this group.
RESUMO
A análise de isótopos estáveis (AIE) fornece informações sobre a produtividade do oceano e aspectos ecológicos de baleias relacionados ao uso do habitat e ecologia alimentar, estrutura de estoque, fi siologia e evolução. Foram revisados estudos publicados usando a AIE em baleias em todo o mundo entre novembro de 1979 e junho de 2017. Foram avaliadas lacunas nas áreas geográfi cas e
heterogeneidade entre as espécies estudadas usando essa metodologia. Também investigamos quais tecidos foram mais utilizados para análise, as fontes de variação em valores de isótopos estáveis, a combinação desta metodologia com outras técnicas e como pode ser útil para a conservação deste táxon e dos ecossistemas marinhos. Um total de 63 publicações foi encontrado e foi possível detectar aumento no número de publicações, uma vez que 49% dos estudos foram realizados nos últimos 7 anos e meio do período analisado. Quase 55% dos estudos concentraram-se na ecologia de forrageio e no uso do habitat. As cerdas bucais foram o principal tecido analisado. Os estudos investigaram
14 espécies, sendo mais comuns aqueles relacionados a baleia-fi n, Balaenoptera physalus (N=19) e a baleia-da-Groenlândia, Balaena mysticetus (N=18). As metodologias de telemetria e AIE combinadas foram úteis para entender as variações geográfi cas em valores de isótopos estáveis. A
metodologia pode também ter valor no cenário de mudanças climáticas fornecendo informações sobre plasticidade alimentar e amplitude de nicho de diferentes espécies, por exemplo. Apesar das incertezas relacionadas à distribuição dos valores de isótopos estáveis no mar e às taxas de
incorporação em baleias, por exemplo, a AIE fornece informações ecológicas primordiais para o manejo e conservação desse grupo.
Palavras-chave: Balaenopteridae; Balaenidae; Análise de isótopos estáveis; Ecologia da conservação.
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References
Aguilar, A., Giménez, J., Gómez-Campos, E., Cardona, L. & Borrell, A. 2014. δ15N value does not reflect fasting in Mysticetes. PLoS ONE, 9(3): 1-7.
Bentaleb, I., Martin, C., Vrac, M., Mate, B., Mayzaud, P., Siret, D., … & Guinet, C. 2011. Foraging ecology of Mediterranean fin whales in a changing environment elucidated by satellite tracking and baleen plate stable isotopes. Mar. Ecol. Prog. Ser., 438: 285-302.
Best, P.B. & Schell, D.M. 1996. Stable Isotopes in southern right whale (Eubalaena australis) baleen as indicators of seasonal movements, feeding and growth. Mar. Biol., 124: 483-494.
Boecklen, W.J., Christopher, T.Y., Cook, B.A. & James, A.C. 2011. On the use of stable isotopes in trophic ecology. Annual Review of Ecology, Evolution and Systematics, 42: 411-440.
Borrell, A., Abad-Oliva, N., Gomez-Campos, E., Giménez, J. & Aguilar, A. 2012. Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans. Rapid. Commun. Mass. Sp., 26: 1596-1602.
Born, E.W., Outrige, P., Riget, F.F., Hobsons, K.A., Dietz, R., Øie, N. & Haug, T. 2003. Population substructure of North Atlantic minke whales (Balaenoptera acutorostrata) inferred from regional variation of elemental and stable isotopic signatures in tissues. J. Marine. Syst., 43: 1-17.
Borobia, M., Gearing, P.J., Simard, Y., Gearing, J.N. & Béland, P. 1995. Blubber fatty acids of finback and humpback whales from the gulf of St. Lawrence. Mar. Biol., 122: 341-353
Boyd, I.L., Bowen, W.D. & Iverson, S.J. 2010. Marine Mammal Ecology and Conservation, A handbook of techniques. Oxford University Press, New York. 450 p.
Budge, S.M., Wooler, M.J., Springer, A.M., Iverson, S.J., McRoy, C.P. & Divoky, G.J. 2008. Tracing carbon flow in an arctic marine food web using fatty acid-stable isotope analysis. Oecologia, 157: 117-129.
Busquets-Vass, G., Newsome, S.D., Calambokidis, J., Serra-Valente, G., Jacobsen, J.K., Aguíñiga-García, S. & Gendron, D. 2017. Estimating blue whale skin isotopic incorporation rates and baleen growth rates: Implications for assessing diet and movement patterns in mysticetes. PLoS ONE, 12(5): 1-25.
Caraveo-Patiño, J. & Soto, L.A. 2005. Stable carbon isotope ratios of the gray whale (Eschrichtius robustus) in the breeding grounds of Baja California Sur, Mexico. Hydrobiologia, 539: 99-107.
Caraveo-Patiño, J., Hobson, K.A. & Soto, L.A. 2007. Feeding ecology of gray whales inferred from stable-carbon and nitrogen isotopic analysis of baleen plates. Hydrobiologia, 586: 17-25.
Clark, C.T., Fleming, A.H., Calambokidis, J., Kellar, N.M., Allen, C.D., Catelani, K.N., … & Harvey, J.T. 2016. Heavy with child? Pregnancy status and stable isotope ratios as determined from biopsies of humpback whales. Conservation Physiology, 4(1): 1-13.
Clementz, M.T., Fordyce, R.E., Peek, S.L. & Fox, D.L. 2014. Ancient marine isoscapes and isotopic evidence of bulk-feeding by Oligocene cetaceans. Palaeogeography, Palaeoclimatology, Palaeoecology, 400: 28-40.
Committee on Taxonomy. 2014. List of marine mammal species and subspecies. Society for Marine Mammalogy. www.marinemammalscience.org, consulted on November 4th, 2017.
Crawford, K., McDonald, R.A. & Bearhop, S. 2008. Applications of stable isotope techniques to the ecology of mammals. Mammal Review, 38(1): 87-107.
Croll, D.A., Tershy, B.R. & Newton, K.M. 2009. Filter Feeding. In: Encyclopedia of Marine Mammals (Eds. Perrin WF, Würsig B, Thewissen JGM) Elsevier ink. 2nd edition. 429-433.
Das, K., Lepoint, G., Leroy, Y. & Bouquegneau, J.M. 2003. Marine Mammals from the southern North Sea: feeding ecology data from δ13C and δ15N measurements. Mar. Ecol. Prog. Ser., 263: 287-298.
Das, K., Holleville, O., Ryan, C., Berrow, S., Gilles, A., Ody, D. & Michel, L.N. 2017. Isotopic niches of fin whales from the Mediterranean Sea and the Celtic Sea (North Atlantic). Mar. Environ. Res., 127: 75-83.
Davenport, S.R. & Bax, N.J. 2002. A trophic study of a marine ecosystem off southeastern Australia using stable isotopes of carbon and nitrogen. Can. J. Fish. Aquat. Sci., 59: 514-530.
Dehn, L.A., Follmann, E.H., Rosa, C., Duffy, L.K., Thomas, D.L., Bratton, G.R., Taylor, R.J., O´Hara, T.M. 2006. Stable isotope and trace element status of subsistence-hunted bowhead and beluga whales in Alaska and gray whales in Chukotka. Marine Pollution Bulletin, 52: 301-309.
Eisenmann, P., Fry, B., Holyoake, C., Coughran, D., Nicol, S. & Nash, S.B. 2016. Isotopic evidence of a wide spectrum of feeding strategies in Southern hemisphere humpback whale baleen records. PLoS ONE, 11(5): 1-20.
Eisenmann, P., Fry, B., Mazumder, D., Jacobsen, G., Holyoake, C.S., Coughran, D. & Nash, S.B. 2017. Radiocarbon as a Novel Tracer of Extra-Antarctic Feeding in Southern Hemisphere Humpback Whales. Scientific Reports, 7: (4366).
Filatova, O.A., Witteveen, B.H., Goncharov, A.A., Tiunov, A.V., Goncharova, M.I., Burdin, A.M. & Hoyt, E. 2013. The diets of humpback whales (Megaptera novaeangliae) on the shelf and oceanic feeding grounds in the western North Pacific inferred from stable isotope analysis. Mar. Mammal. Sci., 29(3): 253-265.
Fleming, A.H., Clark, C.T., Calambokidis, J. & Barlow, J. 2016. Humpback whale diets respond to variance in ocean climate and ecosystem conditions in the California Current. Global Change. Biol., 22(3): 1214-1224.
Fry, B. 2006. Stable Isotope Ecology. Springer Science + Business Media. 308 p.
Gavrilchuk, K., Lesage, V., Ramp, C., Sears, R., Bérubé, M., Bearhop, S. & Beauplet, G. 2014. Trophic niche partitioning among sympatric baleen whale species following the collapse of groundfish stocks in the Northwest Atlantic. Mar. Ecol. Prog. Ser., 497: 285-301.
Gendron, D., Aguíñiga, S. & Carriquiry, J.D. 2001. δ15N and δ13C in skin biopsy samples: a note on their applicability for examining the relative trophic level in three rorqual species. Journal of Cetacean Research Management, 3: 41-44.
Giménez, J., Gómez-Campos, E., Borrel, A., Cardona, L. & Aguiar, A. 2013. Isotopic evidence of limited exchange between Mediterranean and eastern North Atlantic fin whales. Rapid Commun. Mass. Sp., 27: 1801-1806.
Graham, B.S., Koch, P.L., Newsome, S.D., McMahon, K.W. & Aurioles, D. 2010. Using Isoscapes to Trace the Movements and Foraging Behavior of Top Predators in Oceanic Ecosystems. In: West JB et al. (Eds) Isoscapes: Understanding Movement, Pattern, and Process on Earth Through Isotope Mapping. Springer Science + Business Media B.V. 299-318.
Hobson, K., Alisauskas, R. & Clark, R. 1993. Stable-Nitrogen Isotope Enrichment in Avian Tissues Due to Fasting and Nutritional Stress: Implications for Isotopic Analyses of Diet. The Condor, 95: 388-394.
Hobson, K.A. 1999. Tracing origins and migration of wildlife using stable isotopes: a review. Oecologia, 120: 314-326.
Hobson, K.A., Fisk, A., Karnovsky, N., Holst, M., Gagnon, J. & Fortier, M. 2002. A stable isotope (δ13C, δ15N) model for the North Water food web: implications for evaluating trophodynamincs and the flow of energy and contaminants. Deep Sea Res, 49: 5131-5150.
Hobson, K.A., Riget, F.F., Outridge, P.M., Dietz, R. & Born, E. 2004. Baleen as biomonitor of mercury content and dietary history of North Atlantic Minke Whales (Balaenoptera acutorostrata) combining elemental and stable isotope approaches. Sci. Total Environ., 331: 69-82.
Hoekstra, P.F., Dehn, L.A., George, J.C., Solomon, K.R., Muir, D.C.G. & O'hara, T.M. 2002. Trophic ecology of bowhead whales (Balaena mysticetus) compared with that of other arctic marine biota as interpreted from carbon-, nitrogen-, and sulfur-isotope signatures. Can. J. Zool., 80: 223-231.
Horstmann-Dehn, L., Follmann, E.H., Rosa, C., Zelensky, G. & George, C. 2012. Stable carbon and nitrogen isotope ratios in muscle and epidermis of arctic whales. Mar. Mammal Sci., 28(2): 173-190.
Hunt, K.E., Lysiak, N.S., Moore, M.J. & Rolland, R.M. 2016. Longitudinal progesterone profiles in baleen from female North Atlantic right whales (Eubalaena glacialis) match known calving history. Conservation Physiology, 4: 1-9.
Jardine, T.D., Kidd, K.A. & Fisk, A.T. 2006. Applications, Considerations and Sources of Uncertainty When Using Stable Isotope Analysis in Ecotoxicology. Environ. Sci. Technol., 40: 7501-7511.
Killingley, J.S. 1979. Migrations of California Gray Whales Tracked by Oxygen-18 Variations in their epizoic Barnacles. Science, 207: 759-760
Lee, S.H., Schell, D.M., McDonald, T.L. & Richardson, W.J. 2005. Regional and seasonal feeding by bowhead whales Balaena mysticetus as indicated by stable isotope ratios. Mar. Ecol. Prog. Ser., 285: 271-287.
Lesage, V., Morin, Y., Rioux, E., Pomerleau, C., Ferguson, S.H. & Pelletier, E. 2010. Stable isotopes and trace elements as indicators on diet and habitat use in cetaceans: predicting errors related to preservation, lipid extraction, and lipid normalization. Mar. Ecol. Prog. Ser., 419: 249-265.
Matthews, C.J.D. & Ferguson, S.H. 2015. Seasonal foraging behavior of eastern Canada-West Greenland bowhead whales: An assessment of isotopic cycles along baleen. Mar. Ecol. Prog. Ser., 522: 269-286.
McMahon, K.W., Hamady, L.L. & Thorrold, S.R. 2013a. Review of ecogeochemistry approaches to estimating movements of marine mammal. Limnol. Oceanograph. 58: 697-714.
McMahon, K.W., Hamady, L.L. & Thorrold, S.R. 2013b. Ocean Ecogeochemistry: a review. Oceanography and Marine Biology. edited by Hughes RN, Hughes DJ, Smith IP. In: Oceanography and marine biology an annual review 51:327-374.
Milmann, L., Machado, R., Sucunza, F., Oliveira, L.R., Santos, R.A., Di Beneditto, A.P.M., Rezende, C.E., Baumgarten, J. & Ott, P.H. 2018. New trophic link and potential feeding area of dwarf minke whale (Balaenoptera acutorostrata subsp.) in mid latitude waters of the southwestern Atlantic Ocean. Mammalia, 4 p.
Mitani, Y., Bando, T., Takai, N. & Sakamoto, W. 2006. Patterns of stable carbon and nitrogen isotopes in baleen of common minke whale Balaenoptera acutorostrata from the western North Pacific. Fisheries Science, 72: 69-75.
Morais, O.B.I., Danilewicz, D., Zerbini, A.M., Edmundson, W. & Bortolotto, G.A. 2016. From the southern right whale hinting decline to the humpback whaling expansion: a reviw of whale catch records in the tropical western South Atlantic Ocean. Mamm. Rev., 13 p.
Newsome, S.D., Clementz, M.T. & Koch, P.L. 2010. Using stable isotope biogeochemistry to study marine mammal ecology. Mar. Mammal. Sci., 26: 509-572.
Niño-Torres, A.C., Urbán, J. & Olavarrieta, T. 2013. Dietary preferences of Bryde’s whales (Balaenoptera edeni) from the gulf of California: A δ13C, δ15N analysis. Mar. Mammal. Sci., 30: 1140-1148.
Ostrom, P.H. & Fry, B. 1993. Sources and Cycling of Organic Matter within Modern and Prehistoric Food Webs. In: Topics in Geobiology eds: M. H. Engel and S. A. Macko. Chapter 37:786-798. Springer Science-Business Media New York
Ostrom, P.H., Lien, J. & Macko, S.A. 1993. Evaluation of the diet of Sowerby´s beaked whale, Mesoplodon bidens based on isotopic comparisons among northwestern Atlantic cetaceans. Can. J. Zool., 71: 858-861.
Pomerleau, C., Lesage, V., Ferguson, S.H., Winkler, G., Petersen, S.D. & Higdon, J.W. 2012. Prey assemblage isotopic variability as a tool for assessing diet and the spatial distribution of bowhead whale Balaena mysticetus foraging in the Canadian eastern Arctic. Mar. Ecol. Prog. Ser. Series, 469: 161-174.
Pomerleau, C., Lesage, V., Winkler, G., Rosenberg, B. & Ferguson, S.H. 2014. Contemporary diet of bowhead whales (Balaena mysticetus) from the eastern Canadian arctic inferred from fatty acid biomarkers. Arctic, 67: 84-92.
Pomerleau, C., Heide-Jørgensen, M.P., Ferguson, S.H., Stern, H.L., Høyer, J.L. & Stern, G.A. 2017. Reconstructing variability in West Greenland ocean biogeochemistry and bowhead whale (Balaena mysticetus) food web structure using amino acid isotope ratios. Polar. Biol., 40: 2225-2238.
Ramos, R.A. & González-Solís, J. 2012. Trace me if you can: the use of intrinsic biogeochemical markers in marine top predators. Front. Ecol. Envirn., 10: 258-266.
Rau, G.H., Sweeney, R.E. & Kaplant, I.R. 1982. Plankton 13C:12C ratio changes with latitude: differences between northern and southern oceans. Deep-Sea Research, 29: 1035-1039.
Rau, G.H., Mearns, A.J., Young, D.R., Olson, R.J., Schafer, H.A. & Kaplan, I.R. 1983. Animal C13/C12 correlates with trophic level in pelagic food webs. Ecology, 64: 1314-1318.
Roubira, P., Bosch, D. & Bentaleb, I. 2015. Pb isotopic compositions of fin whale baleen plates - A clue to unravel individual migrations between the Atlantic Ocean and the Mediterranean Sea? Procedia Earth and Planetary Science, 13: 173-176.
Rowntree, V., Payne, R. & Schell, D. 2001. Changing patterns of habitat use by southern right whales (Eubalaena australis) on their nursery ground at Península Valdés, Argentina, and in their long-range movements. J. Cetacean Res. Manage. Special Issue, 2:133-143.
Rowntree, V.J., Valenzuela, L.O., Fraguas, P.F. & Seger, J. 2007. Foraging behavior of southern right whales (Eubalaena australis) inferred from variation of carbon stable isotope ratios in their baleen. J. Cetacean. Res. Manage., SC/60/BRG23. 10 p.
Rubestein, R. & Hobson, K.A. 2004. From birds to butteflies: animal movement patterns and stable isotopes. Trends in Ecology & Evolution, 19: 256-264.
Rugh, D.J. & Shelden, K.E.W. 2008. "Bowhead Whale". In Perrin WF., Würsig B, Thewissen JGM. Encyclopedia of Marine Mammals (Second ed.). Academic Press. p. 131.
Ryan, C., McHugh, B., Trueman, C.N., Harrod, C., Berrow, S.D. & O'Connor, I. 2012. Accounting for the effects of lipids in stable isotope (δ13C and δ15N values) analysis of skin and blubber of Balaenopteridae whales. Rapid Commun. Mass. Spectrom. 26: 2745-2754.
Ryan, C., McHugh, B., Trueman, C.N., Sabin, R., Deaville, R., Harrod, C., Berrow, S.D. & O'Connor, I. 2013. Stable isotope analysis of baleen reveals resource portioning among sympatric rorquals and population structure in fin whales. Mar. Ecol. Prog. Ser., 479: 251-261.
Ryan, C., Berrow, S.D., Mchugh, B., O’Donnell, C., Trueman, C.N. & O’Connor, I. 2014. Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models. Mar. Mammal. Sci. 30: 242-258.
Seyboth, E., Botta, S. & Secchi, E. 2017. Using chemical elements to the study of trophic and spatial ecology in marine mammals of the southwestern Atlantic Ocean. Advances in Marine Vertebrate Research in Latin America, 22: 221-248.
Seyboth, E., Botta, S., Mendes, C.R.B., Negrete, J., Dalla Rosa, L. & Secchi, E.R. 2018. Isotopic evidence of the effect of warming on the northern Antarctic Peninsula ecosystem. Deep Sea Research Part II: Topical Studies in Oceanography, 149: 218-228.
Schell, D.M., Saupe, S.M. & Haubenstock, N. 1989a. Bowhead whale (Balaena mysticetus) growth and feeding as estimated by D13C techniques. Mar. Biol., 103: 433-443.
Schell, D.M., Saupe, S.M. & Haubenstock, N. 1989b. Natural Isotope abundances in Bowhead Whale (Balaena mysticetus) baleen: markers of aging and habitat usage. In: Stable Isotopes in Ecological Research (eds) Rundel PW, Ehleringer JR, Nagy KA. p. 260-269.
Schell, D.M. 2001a. Carbon isotope ration variations in Bering Sea biota: The role of anthropogenic carbon dioxide. Limnol. Oceanogr., 46: 999-1000.
Schell, D.M. 2001b. Declining carrying capacity in the Bering Sea: Isotopic evidence from whale baleen. Limnol. Oceanogr., 45: 459-462.
Shoeninger, M.J. & DeNiro, M.J. 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta, 48: 625-639.
Thomas, P.O., Reeves, R.R. & Brownell Jr., R.L. 2015. Status of the world’s baleen whales. Mar. Mamm. Sci., 32: 683-734.
Todd, S., Ostrom, P., Lien, J. & Abrajano, J. 1997. Use of biopsy samples of Humpback whale (Megaptera novaengliae) skin for stable isotope (13C) determination. J. Northw. Atl. Fish. Sci., 22: 71-76.
Torres, L.G., Rayment, W., Olavarri C., Graham, B., Baker, C.S., Patenaude, N., …, Carroll, E.L. 2016. Demography and ecology of southern right whales Eubalaena australis wintering at sub-Antarctic Campbell Island, New Zealand. Polar Biol., 40: 95-106.
Valenzuela, L.O., Sironi, M., Rowntree, V.J. & Seger, J. 2009. Isotopic and genetic evidence for culturally inherited site fidelity to feeding grounds in southern right whales (Eubalaena australis). Molecular Ecology, 18(5): 782-791.
Van de Vijver, K.I., Hoff, P.T., Das, K., Dongen, W.V., Esmans, E.L., Jauniax, T., Bouquegneau, J.M., Blust, R. & De Coen, W. 2003. Perfluorinated Chemicals Infiltrate Ocean Waters: Link between Exposure Levels and Stabe Isotope Ratios In Marine Mammals. Envirn. Sci. Technol., 37: 5545-5550.
Vighi, M., Borrel, A., Crespo, E.A., Oliveira, L.R., Simões-Lopes, P.C., Flores, P.A.C., García, N.A. & Aguilar, A. 2014. Stable isotopes indicate population structuring in the Southwest Atlantic Population of Right Whales (Eubalaena australis). Plos One, 9(3).
Vighi, M., Borrell, A. & Aguilar, A. 2016. Stable isotope analysis and fin whale subpopulation structure in the eastern North Atlantic. Mar. Mammal Sci., 32: 535-551.
Witteveen, B.H., Anthony, G., Worthy, J., Worthy, G.A.J. & Roth, J.D. 2009a. Tracing migratory movements of breeding North Pacific humpback whales using stable isotope analysis Tracing migratory movements of breeding North Pacific humpback whales using stable isotope analysis. Mar. Ecol. Prog. Ser., 393: 173-183.
Witteveen, B., Worthy, G., Wynne, K. & Roth, J. 2009b. Population structure of North Pacific humpback whales on their feeding grounds revealed by stable carbon and nitrogen isotope ratios. Mar. Ecol. Prog. Ser., 379: 299-310.
Witteveen, B.H., Worthy, G.A.J., Wynne, K.M., Hirons, A.C., Andrews, A.G. & Markel, R.W. 2011. Trophic Levels of North Pacific Humpback Whales (Megaptera novaeangliae) Through Analysis of Stable Isotopes: Implications on Prey and Resource Quality. Aquatic Mammals, 37(2): 101-110.
Witteveen, B.H., Worthy, G.A.J., Foy, R.J. & Wynne, K.M. 2012. Modeling the diet of humpback whales: An approach using stable carbon and nitrogen isotopes in a Bayesian mixing model. Mar. Mammal Sci., 28: 1-18.
Witteveen, B.H. & Wyinne, K.M. 2016. Trophic niche partitioning and diet composition of sympatric fin (Balaenoptera physalus) and humpback whales (Megaptera novaeangliae) in the Gulf of Alaska revealed through stable isotope analysis. Mar. Mammal Sci., 32: 1319-1339.
Wood, S.N. 2006. Generalized additive models: an introduction. R. Chapman and Hall. 1st edn. CRC Press. Boca Raton, FL.
Wright, D.L., Witteveen, B., Wynne, K. & Horstmann-Dehn, L. 2015. Evidence of two sub aggregations of humpback whales on the Kodiak, Alaska, feeding ground revealed from stable isotope analysis. Mar. Mammal Sci., 31(4): 1378-1400.