Reconstructing the diet, trophic level and migration pattern of mysticete whales based on baleen isotopic composition

Baleen from mysticete whales is a well-preserved proteinaceous material that can be used to identify migrations and feeding habits for species whose migration pathways are unknown. Analysis of δ13C and δ15N from bulk baleen has been used to infer migration patterns for individuals. However, this approach has fallen short of identifying migrations between regions as it is difficult to determine variations in isotopic shifts without temporal sampling of prey items. Here we apply analysis of δ15N values of amino acids to five baleen plates belonging to three species, revealing novel insights on trophic position, metabolic state, and migration between regions. Humpback and minke whales had higher reconstructed trophic levels than fin whales (3.4-3.5 versus 2.7-2.9, respectively) as expected due to different feeding specialization. Isotopic niche areas between baleen minima and maxima were well separated, indicating regional resource use for individuals during migration that aligned with isotopic gradients in Atlantic Ocean particulate organic matter. δ15N values from phenylalanine confirmed regional separation between the niche areas for two fin whales as migrations occurred and elevated glycine and threonine δ15N values revealed physiological changes due to fasting. Simultaneous resolution of trophic level and physiological changes allow for identification of regional migrations in mysticetes.

[1]  E. Olsen,et al.  A note on common minke whale (Balaenoptera acutorostrata) diets in the Norwegian Sea and the North Sea , 2023, J. Cetacean Res. Manage..

[2]  P. D. de Bruyn,et al.  Fasting affects amino acid nitrogen isotope values: a new tool for identifying nitrogen balance of free-ranging mammals , 2020, Oecologia.

[3]  S. Schouten,et al.  Practical considerations for improved reliability and precision during determination of δ15 N values in amino acids using a single combined oxidation-reduction reactor. , 2020, Rapid communications in mass spectrometry : RCM.

[4]  D. Baker,et al.  Trophic strategy and bleaching resistance in reef-building corals , 2020, Science Advances.

[5]  S. Ferguson,et al.  Amino acid δ15N underestimation of cetacean trophic positions highlights limited understanding of isotopic fractionation in higher marine consumers , 2020, Ecology and evolution.

[6]  Natalie Cooper,et al.  Combining simulation modeling and stable isotope analyses to reconstruct the last known movements of one of Nature’s giants , 2019, PeerJ.

[7]  M. Silva,et al.  Stable isotopes reveal winter feeding in different habitats in blue, fin and sei whales migrating through the Azores , 2019, Royal Society Open Science.

[8]  K. Hobson,et al.  Temporal and intra-population patterns in polar bear foraging ecology in western Hudson Bay , 2019, Marine Ecology Progress Series.

[9]  Stefan Schouten,et al.  Practical considerations for improved reliability and precision during compound specific analysis of δ15N in amino acids using a single combined oxidation-reduction reactor , 2019, bioRxiv.

[10]  R. Reisinger,et al.  Sensitivity of δ13C values of seabird tissues to combined spatial, temporal and ecological drivers: A simulation approach , 2019, Journal of Experimental Marine Biology and Ecology.

[11]  A. Jackson,et al.  tRophicPosition, an r package for the Bayesian estimation of trophic position from consumer stable isotope ratios , 2018 .

[12]  P. I. Miller,et al.  A matter of timing: how temporal scale selection influences cetacean ecological niche modelling , 2018 .

[13]  T. Larsen,et al.  Advances in the application of amino acid nitrogen isotopic analysis in ecological and biogeochemical studies , 2017 .

[14]  A. Zerbini,et al.  Satellite tagging of Mediterranean fin whales: working towards the identification of critical habitats and the focussing of mitigation measures , 2017, Scientific Reports.

[15]  T. O’Connell.  ‘Trophic’ and ‘source’ amino acids in trophic estimation: a likely metabolic explanation , 2017, Oecologia.

[16]  J. Calambokidis,et al.  Estimating blue whale skin isotopic incorporation rates and baleen growth rates: Implications for assessing diet and movement patterns in mysticetes , 2017, PloS one.

[17]  Michael B. Wunder,et al.  Using ocean models to predict spatial and temporal variation in marine carbon isotopes , 2017 .

[18]  B. T. Fuller,et al.  The dietary protein paradox and threonine 15 N-depletion: Pyridoxal-5'-phosphate enzyme activity as a mechanism for the δ15 N trophic level effect. , 2017, Rapid communications in mass spectrometry : RCM.

[19]  M. Leopold,et al.  Unorthodox sampling of a fin Whale's (Balaenoptera physalus) diet yields several new mesopelagic prey species , 2016 .

[20]  K. McMahon,et al.  Embracing variability in amino acid δ15N fractionation: mechanisms, implications, and applications for trophic ecology , 2016 .

[21]  B. Fry,et al.  Isotopic Evidence of a Wide Spectrum of Feeding Strategies in Southern Hemisphere Humpback Whale Baleen Records , 2016, PloS one.

[22]  A. Aguilar,et al.  Stable isotope analysis and fin whale subpopulation structure in the eastern North Atlantic , 2016 .

[23]  A. Aguilar,et al.  Influence of Reproduction on Stable-Isotope Ratios: Nitrogen and Carbon Isotope Discrimination between Mothers, Fetuses, and Milk in the Fin Whale, a Capital Breeder , 2016, Physiological and Biochemical Zoology.

[24]  T. Crowther,et al.  Predicting rates of isotopic turnover across the animal kingdom: a synthesis of existing data. , 2015, The Journal of animal ecology.

[25]  A. Berta,et al.  Vascularization of the Gray Whale Palate (Cetacea, Mysticeti, Eschrichtius robustus): Soft Tissue Evidence for an Alveolar Source of Blood to Baleen , 2015, Anatomical record.

[26]  S. Ferguson,et al.  Seasonal foraging behaviour of Eastern Canada-West Greenland bowhead whales: an assessment of isotopic cycles along baleen , 2015 .

[27]  Peter J. Dugan,et al.  Seasonal migrations of North Atlantic minke whales: novel insights from large-scale passive acoustic monitoring networks , 2014, Movement ecology.

[28]  M. Fogel,et al.  Amino acid δ13C analysis shows flexibility in the routing of dietary protein and lipids to the tissue of an omnivore. , 2014, Integrative and comparative biology.

[29]  Richard Inger,et al.  Best practices for use of stable isotope mixing models in food-web studies , 2014 .

[30]  A. Aguilar,et al.  δ15N Value Does Not Reflect Fasting in Mysticetes , 2014, PloS one.

[31]  I. Jonsen,et al.  North Atlantic Blue and Fin Whales Suspend Their Spring Migration to Forage in Middle Latitudes: Building up Energy Reserves for the Journey? , 2013, PloS one.

[32]  E. M. Robinson,et al.  Blue whale earplug reveals lifetime contaminant exposure and hormone profiles , 2013, Proceedings of the National Academy of Sciences.

[33]  J. Harvey,et al.  Nitrogen isotope fractionation in amino acids from harbor seals: implications for compound-specific trophic position calculations , 2013 .

[34]  R. Deaville,et al.  Stable isotope analysis of baleen reveals resource partitioning among sympatric rorquals and population structure in fin whales , 2013 .

[35]  A. Quigg,et al.  Isotope baseline shifts in pelagic food webs of the Gulf of Mexico , 2012 .

[36]  A. Aguilar,et al.  Discrimination of stable isotopes in fin whale tissues and application to diet assessment in cetaceans. , 2012, Rapid communications in mass spectrometry : RCM.

[37]  C. Guinet,et al.  Foraging ecology of Mediterranean fin whales in a changing environment elucidated by satellite tracking and baleen plate stable isotopes , 2011 .

[38]  S. Mazumdar,et al.  Generalized linear mixed models in time series studies of air pollution , 2011 .

[39]  Andrew L Jackson,et al.  Comparing isotopic niche widths among and within communities: SIBER - Stable Isotope Bayesian Ellipses in R. , 2011, The Journal of animal ecology.

[40]  I. Stirling,et al.  Quantifying dietary pathways of proteins and lipids to tissues of a marine predator , 2011 .

[41]  Trevor J. Krabbenhoft,et al.  A general hypothesis-testing framework for stable isotope ratios in ecological studies. , 2010, Ecology.

[42]  Paul L. Koch,et al.  Using stable isotope biogeochemistry to study marine mammal ecology , 2010 .

[43]  L. Felicetti,et al.  The impact of protein quality on stable nitrogen isotope ratio discrimination and assimilated diet estimation , 2010, Oecologia.

[44]  Y. Takano,et al.  Determination of aquatic food‐web structure based on compound‐specific nitrogen isotopic composition of amino acids , 2009 .

[45]  R. Foy,et al.  Investigation of foraging habits and prey selection by humpback whales (Megaptera novaeangliae) using acoustic tags and concurrent fish surveys , 2008 .

[46]  A. Zerbini,et al.  Movements of satellite-monitored humpback whales on their feeding ground along the Antarctic Peninsula , 2008, Polar Biology.

[47]  H. Kitazato,et al.  Metabolic control of nitrogen isotope composition of amino acids in macroalgae and gastropods: implications for aquatic food web studies , 2007 .

[48]  C. Deutsch,et al.  New developments in the marine nitrogen cycle. , 2007, Chemical reviews.

[49]  Y. Mitani,et al.  Patterns of stable carbon and nitrogen isotopes in the baleen of common minke whale Balaenoptera acutorostrata from the western North Pacific , 2006, Fisheries Science.

[50]  C. Kendall,et al.  Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur , 2003 .

[51]  S. Palumbi,et al.  Whales Before Whaling in the North Atlantic , 2003, Science.

[52]  J. Pinnegar,et al.  Isotope trophic-step fractionation: a dynamic equilibrium model. , 2003, The Journal of animal ecology.

[53]  D. Post.  USING STABLE ISOTOPES TO ESTIMATE TROPHIC POSITION: MODELS, METHODS, AND ASSUMPTIONS , 2002 .

[54]  M. Clarke,et al.  Assessing the importance of cephalopods in the diets of marine mammals and other top predators: problems and solutions , 2001 .

[55]  F. Chavez,et al.  The nitrogen isotope biogeochemistry of sinking particles from the margin of the Eastern North Pacific , 1999 .

[56]  H. Gjøsæter,et al.  Do Minke Whales (Balaenoptera acutorostrata) Exhibit Particular Prey Preferences , 1997 .

[57]  K. Hobson,et al.  Stable carbon and nitrogen isotopic fractionation between diet and tissues of captive seals: implications for dietary reconstructions involving marine mammals , 1996 .

[58]  R. Bowman,et al.  FEEDING BEHAVIOR OF A HUMPBACK WHALE IN LOW‐LATITUDE WATERS , 1991 .

[59]  D. Schell,et al.  Bowhead whale (Balaena mysticetus) growth and feeding as estimated by δ13C techniques , 1989 .

[60]  B. Fry.  Food web structure on Georges Bank from stable C, N, and S isotopic compositions , 1988 .

[61]  M. Minagawa,et al.  Stepwise enrichment of 15N along food chains: Further evidence and the relation between δ15N and animal age , 1984 .

[62]  H. Krebs.  The Croonian Lecture, 1963 Gluconeogenesis , 1964, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[63]  William Hyde Wollaston,et al.  I. The Croonian Lecture , 1810, Philosophical Transactions of the Royal Society of London.

[64]  William Hyde Woollaston.  Croonian Lecture , 1810, The Medical and physical journal.

[65]  C. Trueman,et al.  Isotopic Tracking of Marine Animal Movement , 2019, Tracking Animal Migration with Stable Isotopes.

[66]  A. Kawamura.  A REVIEW OF FOOD OF BALAENOPTERID WHALES , 2017 .

[67]  Adamo,et al.  Local and migratory movements of humpback whales (Megaptera novaeangliae) satellite-tracked in the North Atlantic Ocean , 2014 .

[68]  C. Trueman,et al.  Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models , 2014 .

[69]  R. Suydam,et al.  Themed Issue Article: Stress in Vertebrates Baleen hormones: a novel tool for retrospective assessment of stress and reproduction in bowhead whales (Balaena mysticetus) , 2014 .

[70]  T. Patterson,et al.  Deep Sea Research Part II: Topical Studies in Oceanography , 2013 .

[71]  Daniel P. Costa,et al.  THE SECRET LIFE OF MARINE MAMMALS , 2007 .

[72]  B. Fry.  Stable Isotope Ecology , 2006 .

[73]  M. Altabet.  Isotopic Tracers of the Marine Nitrogen Cycle: Present and Past , 2005 .

[74]  M. Altabet,et al.  Nitrogen isotope biogeochemistry of the Antarctic Polar Frontal Zone at 170°W , 2001 .

[75]  J. Sigurjónsson.  On the life history and autecology of North Atlantic rorquals , 1995 .

[76]  Daniel P. Costa,et al.  THE SECRET LIFE OF MARINE MAMMALS NOVEL TOOLS FOR STUDYING THEIR BEHAVIOR AND BIOLOGY AT SEA , 1993 .