Individual and population dietary specialization decline in fin whales during a period of ecosystem shift.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
25 08 2021
25 08 2021
Historique:
received:
23
03
2021
accepted:
28
07
2021
entrez:
26
8
2021
pubmed:
27
8
2021
medline:
5
11
2021
Statut:
epublish
Résumé
This study sought to estimate the effect of an anthropogenic and climate-driven change in prey availability on the degree of individual and population specialization of a large marine predator, the fin whale (Balaenoptera physalus). We examined skin biopsies from 99 fin whales sampled in the St. Lawrence Estuary (Canada) over a nine year period (1998-2006) during which environmental change was documented. We analyzed stable isotope ratios in skin and fatty acid signatures in blubber samples of whales, as well as in seven potential prey species, and diet was quantitatively assessed using Bayesian isotopic models. An abrupt change in fin whale dietary niche coincided with a decrease in biomass of their predominant prey, Arctic krill (Thysanoessa spp.). This dietary niche widening toward generalist diets occurred in nearly 60% of sampled individuals. The fin whale population, typically composed of specialists of either krill or lipid-rich pelagic fishes, shifted toward one composed either of krill specialists or true generalists feeding on various zooplankton and fish prey. This change likely reduced intraspecific competition. In the context of the current "Atlantification" of northern water masses, our findings emphasize the importance of considering individual-specific foraging tactics and not only population or group average responses when assessing population resilience or when implementing conservation measures.
Identifiants
pubmed: 34433851
doi: 10.1038/s41598-021-96283-x
pii: 10.1038/s41598-021-96283-x
pmc: PMC8387503
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
17181Informations de copyright
© 2021. The Author(s).
Références
Hutchinson, G. E. Concluding remarks. Cold Spring Harb. Symp. Quant. Biol. 22, 415–427 (1957).
doi: 10.1101/SQB.1957.022.01.039
Bolnick, D. I. et al. The ecology of individuals: Incidence and implications of individual specialization. Am. Nat. 161, 1–28 (2003).
pubmed: 12650459
doi: 10.1086/343878
Araújo, M. S., Bolnick, D. I. & Layman, C. A. The ecological causes of individual specialisation. Ecology 14, 948–958 (2011).
Kassen, R. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15, 173–190 (2002).
doi: 10.1046/j.1420-9101.2002.00377.x
Clavel, J., Julliard, R. & Devictor, V. Worldwide decline of specialist species: Toward a global functional homogenization?. Front. Ecol. Environ. 9, 222–228 (2011).
doi: 10.1890/080216
Svanbäck, R. & Bolnick, D. I. Intraspecific competition drives increased resource use diversity within a natural population. Proc. R. Soc. B Biol. Sci. 274, 839–844 (2007).
doi: 10.1098/rspb.2006.0198
Tinker, M. et al. Structure and mechanism of diet specialization: Testing models of individual variation in resource use with sea otters. Ecology 15, 475–483 (2012).
Newsome, S. D. et al. The interaction of intraspecific competition and habitat on individual diet specialization: A near range-wide examination of sea otters. Oecologia 178, 45–59 (2015).
pubmed: 25645269
doi: 10.1007/s00442-015-3223-8
Layman, C. A., Newsome, S. D. & Crawford, T. G. Individual-level niche specialization within populations: Emerging areas of study. Oecologia 178, 1–4 (2015).
pubmed: 25690712
doi: 10.1007/s00442-014-3209-y
Moore, S. E., Haug, T., Víkingsson, G. A. & Stenson, G. B. Baleen whale ecology in arctic and subarctic seas in an era of rapid habitat alteration. Prog. Oceanogr. 176, 102–118 (2019).
doi: 10.1016/j.pocean.2019.05.010
Møller, E. F. & Nielsen, T. G. Borealization of Arctic zooplankton - Smaller and less fat zooplankton species in Disko Bay, Western Greenland. Limnol. Oceanogr. 65, 1175–1188 (2020).
doi: 10.1002/lno.11380
COSEWIC. COSEWIC Assessment and Status Report on the Fin Whale Balaenoptera physalus, Atlantic Population and Pacific Population, in Canada. xv + 72 (COSEWIC, 2019).
Kawamura, A. A review of food of balaenopterid whales. Sci. Rep. Whales Res. Inst. 32, 155–197 (1980).
Baumgartner, M. F. & Mate, B. R. Summertime foraging ecology of North Atlantic right whales. Mar. Ecol. Prog. Ser. 264, 123–135 (2003).
doi: 10.3354/meps264123
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, e76507. https://doi.org/10.1371/journal.pone.0076507 (2013).
doi: 10.1371/journal.pone.0076507
pubmed: 24116112
pmcid: 3792998
Gavrilchuk, K. et al. 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 (2014).
doi: 10.3354/meps10578
Aguilar, A. & García-Vernet, R. Fin whale. in Encyclopedia of Marine Mammals (eds. Würsig, B., Thewissen, J. G. M., Kovacs, K. M.) 368–371 (Elsevier, 2018).
Silva, M. A. et al. A stable isotopes reveal winter feeding in different habitats in blue, fin and sei whales migrating through the Azores. R. Soc. Open Sci. 6, 181800. https://doi.org/10.1098/rsos.181800 (2019).
doi: 10.1098/rsos.181800
pubmed: 31598219
pmcid: 6731742
Savenkoff, C. et al. Changes in the northern Gulf of St Lawrence ecosystem estimated by inverse modelling: Evidence of a fishery-induced regime shift?. Est. Coast. Shelf Sci. 73, 711–724 (2007).
doi: 10.1016/j.ecss.2007.03.011
Galbraith, P. S. et al. Physical oceanographic conditions in the gulf of St. Lawrence during 2019. Can. Sci. Adv. Sec. Res. Doc. 2020/043, iv + 9 (2020).
Myers, R. A. & Worm, B. Extinction, survival or recovery of large predatory fishes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 13–20 (2005).
pubmed: 15713586
pmcid: 1636106
doi: 10.1098/rstb.2004.1573
Plourde, S. et al. Ecosystem perspective on changes and anomalies in the Gulf of St. Lawrence: A context in support of the management of the St. Lawrence beluga whale population. Can. Sci. Adv. Sec. Res. Doc. 2013/129, v + 29 (2014).
Hammill, M. O., Stenson, G. B., Doniol-Valcroze, T. & Mosnier, A. Conservation of northwest Atlantic harp seals: Past success, future uncertainty?. Biol. Conserv. 192, 181–191 (2015).
doi: 10.1016/j.biocon.2015.09.016
Stenson, G. B., Haug, T. & Hammill, M. O. Harp seals: Monitors of change in differing ecosystems. Front. Mar. Sci. 7, 738. https://doi.org/10.3389/fmars.2020.569258 (2020).
doi: 10.3389/fmars.2020.569258
Comtois, S., Savenkoff, C., Bourassa, M. N., Brêthes, J. C. & Sears, R. Regional distribution and abundance of blue and humpback whales in the Gulf of St. Lawrence. Can. Tech. Rep. Fish. Aquat. Sci. 2877, viii+8 (2010).
Phillips, D. L. et al. Best practices for use of stable isotope mixing models in food-web studies. Can. J. Zool. 835, 823–835 (2014).
doi: 10.1139/cjz-2014-0127
Iverson, S. J., Field, C., Don Bowen, W. & Blanchard, W. Quantitative fatty acid signature analysis: A new method of estimating predator diets. Ecol. Monogr. 74, 211–235 (2004).
doi: 10.1890/02-4105
Arregui, M., Borrell, A., Víkingsson, G., Ólafsdóttir, D. & Aguilar, A. Stable isotope analysis of fecal material provides insight into the diet of fin whales. Mar. Mamm. Sci. 34, 1059–1069 (2018).
doi: 10.1111/mms.12504
Bourdages, H. et al. Preliminary results from the ecosystemic survey in August 2019 in the Estuary and northern Gulf of St. Lawrence. Can. Sci. Adv. Sec. Res. Doc. 2020/009, iv+93 (2020).
Lesage, V., Lair, S., Turgeon, S. & Béland, P. Diet of St. Lawrence Estuary Beluga (Delphinapterus leucas) in a changing ecosystem. Can. Field Nat. 134, 21–35 (2020).
doi: 10.22621/cfn.v134i1.2421
Aubin, D. S., Smith, T. G. & Geraci, J. R. Seasonal epidermal molt in beluga whales, Delphinapterus leucas. Can. J. Zool. 68, 359–367 (1990).
doi: 10.1139/z90-051
Busquets-Vass, G. et al. Estimating blue whale skin isotopic incorporation rates and baleen growth rates: Implications for assessing diet and movement patterns in mysticetes. PLoS ONE 12, e0177880. https://doi.org/10.1371/journal.pone.0177880 (2017).
doi: 10.1371/journal.pone.0177880
pubmed: 28562625
pmcid: 5451050
Vighi, M., Borrell, A. & Aguilar, A. Stable isotope analysis and fin whale subpopulation structure in the eastern North Atlantic. Mar. Mam. Sci. 32, 535–551 (2016).
doi: 10.1111/mms.12283
Ramp, C., Delarue, J., Bérubé, M., Hammond, P. S. & Sears, R. Fin whale survival and abundance in the Gulf of St. Lawrence, Canada. Endanger. Species Res. 23, 125–132 (2014).
doi: 10.3354/esr00571
Lesage, V., Hammill, M. O. & Kovacs, K. M. Marine mammals and the community structure of the Estuary and Gulf of St. Lawrence, Canada: Evidence from stable isotope analysis. Mar. Ecol. Prog. Ser. 210, 203–221. https://doi.org/10.3354/meps210203 (2001).
doi: 10.3354/meps210203
Ryan, C. et al. Prey preferences of sympatric fin (Balaenoptera physalus) and humpback (Megaptera novaeangliae) whales revealed by stable isotope mixing models. Mar. Mamm. Sci. 30, 242–258 (2014).
doi: 10.1111/mms.12034
Flinn, R. D., Trites, A. W., Gregr, E. J. & Perry, R. I. Diets of fin, sei, and sperm whales in British Columbia: An analysis of commercial whaling records, 1963–1967. Mar. Mamm. Sci. 18, 663–679 (2002).
doi: 10.1111/j.1748-7692.2002.tb01065.x
Bentaleb, I. et al. 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 (2011).
doi: 10.3354/meps09269
Bolnick, D. I. & Fitzpatrick, B. M. Sympatric speciation: Models and empirical evidence. Annu. Rev. Ecol. Evol. Syst. 38, 459–487 (2007).
doi: 10.1146/annurev.ecolsys.38.091206.095804
Goldbogen, J. A. et al. Underwater acrobatics by the world’s largest predator: 360 rolling manoeuvres by lunge-feeding blue whales. Biol. Lett. 9, 20120986. https://doi.org/10.1098/rsbl.2012.0986 (2013).
doi: 10.1098/rsbl.2012.0986
pubmed: 23193050
pmcid: 3565519
Abrahms, B. et al. Memory and resource tracking drive blue whale migrations. Proc. Natl. Acad. Sci. 116, 5582–5587 (2019).
pubmed: 30804188
pmcid: 6431148
doi: 10.1073/pnas.1819031116
Lesmerises, F., Johnson, C. J. & St-Laurent, M. H. Landscape knowledge is an important driver of the fission dynamics of an alpine ungulate. Anim. Behav. 140, 39–47 (2018).
doi: 10.1016/j.anbehav.2018.03.014
Serres, A. & Delfour, F. Social behaviors modulate bottlenose dolphins (Tursiops truncatus) breathing rate. Anim. Cogn. 6, 127–140 (2019).
doi: 10.26451/abc.06.02.04.2019
Goldbogen, J. A. et al. Kinematics of foraging dives and lunge-feeding in fin whales. J. Exp. Biol. 209, 1231–1244 (2006).
pubmed: 16547295
doi: 10.1242/jeb.02135
Potvin, J., Goldbogen, J. A. & Shadwick, R. E. Metabolic expenditures of lunge feeding rorquals across scale: Implications for the evolution of filter feeding and the limits to maximum body size. PLoS ONE 7, e44854. https://doi.org/10.1371/journal.pone.0044854 (2012).
doi: 10.1371/journal.pone.0044854
pubmed: 23024769
pmcid: 3443106
Sexton, J. P., McIntyre, P. J., Angert, A. L. & Rice, K. J. Evolution and ecology of species range limits. Ann. Rev. Ecol. Evol. Syst. 40, 415–436 (2009).
doi: 10.1146/annurev.ecolsys.110308.120317
Schleimer, A. et al. Decline in abundance and apparent survival rates of fin whales (Balaenoptera physalus) in the northern Gulf of St. Lawrence. Ecol. Evol. 9, 4231–4244 (2019).
pubmed: 31016001
pmcid: 6468087
doi: 10.1002/ece3.5055
Lesage, V. et al. 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, 249–265 (2010).
doi: 10.3354/meps08825
Plourde, S., Winkler, G., Joly, P., St-Pierre, J. F. & Starr, M. Long-term seasonal and interannual variations of krill spawning in the lower St. Lawrence estuary, Canada, 1979–2009. J. Plankton Res. 33, 703–714 (2011).
doi: 10.1093/plankt/fbq144
Plourde, S. et al. Daytime depth and thermal habitat of two sympatric krill species in response to surface salinity variability in the Gulf of St Lawrence, eastern Canada. ICES J. Mar. Sci. 71, 272–281 (2014).
doi: 10.1093/icesjms/fst023
Cabrol, J. et al. Seasonal and large-scale spatial variability of the energy reserves and the feeding selectivity of Meganyctiphanes norvegica and Thysanoessa inermis in a Subarctic environment. Prog. Oceanogr. 179, 102203 (2019).
doi: 10.1016/j.pocean.2019.102203
Cabrol, J. et al. Functional feeding response of Nordic and Arctic krill on natural phytoplankton and zooplankton. J. Plankton Res. 42, 239–252 (2020).
doi: 10.1093/plankt/fbaa012
Cabrol, J. et al. Trophic niche partitioning of dominant North-Atlantic krill species, Meganyctiphanes norvegica, Thysanoessa inermis, and T. raschii. Limnol. Oceanogr. 64, 165–181 (2019).
doi: 10.1002/lno.11027
Guilpin, M. et al. Repeated vessel interactions and climate-or fishery-driven changes in prey density limit energy acquisition by foraging blue whales. Front. Mar. Sci. 7, 626. https://doi.org/10.3389/fmars.2020.00626 (2020).
doi: 10.3389/fmars.2020.00626
Guilpin, M. Étude des interactions bioénergétiques entre le rorqual bleu Balaenoptera musculus et le krill dans l’estuaire et le golfe du Saint-Laurent. Doctoral Thesis. (Université du Québec à Rimouski, 2020).
MacArthur, R. H. & Pianka, E. R. On optimal use of a patchy environment. Am. Nat. 100, 603–609 (1966).
doi: 10.1086/282454
Schleimer, A. et al. Spatio-temporal patterns in fin whale Balaenoptera physalus habitat use in the northern Gulf of St. Lawrence. Mar. Ecol. Prog. Ser. 623, 221–234 (2019).
doi: 10.3354/meps13020
Bernier-Graveline, A. et al. Lipid metabolites as indicators of body condition in highly contaminant-exposed belugas from the endangered St. Lawrence Estuary population (Canada). Environ. Res. 192, 110272. https://doi.org/10.1016/j.envres.2020.110272 (2020).
doi: 10.1016/j.envres.2020.110272
pubmed: 33038366
Kershaw, J. L. et al. Declining reproductive success in the Gulf of St Lawrence’s humpback whales (Megaptera novaeangliae) reflects ecosystem shifts on their feeding grounds. Glob. Change Biol. 10, 1–15. https://doi.org/10.1111/gcb.15466 (2020).
doi: 10.1111/gcb.15466
Mosnier, A. & Gosselin, J.-F. Seasonal distribution and concentration of four baleen whale species in the St. Lawrence Estuary based on 22 years of DFO observation data. Can. Sci. Adv. Sec. Res. Doc. 2020/053, iv+119 (2020).
Gowans, S., Simard, P., Giard, J., Vashro, C. & Sears, R. Photographic identification of fin whales (Balaenoptera physalus) off the Atlantic coast of Nova Scotia, Canada. Mar. Mamm. Sci. 21, 323–326 (2005).
doi: 10.1111/j.1748-7692.2005.tb01232.x
Bérubé, M. & Palsbøll, P. Identification of sex in cetaceans by multiplexing with three ZFX and ZFY specific primers. Mol. Ecol. 5, 283–287 (1996).
pubmed: 8673273
doi: 10.1111/j.1365-294X.1996.tb00315.x
Williams, R. et al. Evidence for density-dependent changes in body condition and pregnancy rate of North Atlantic fin whales over four decades of varying environmental conditions. ICES J. Mar. Sci. 70, 1273–1280 (2013).
doi: 10.1093/icesjms/fst059
Lockyer, C. Body fat condition in Northeast Atlantic fin whales, Balaenoptera physalus, and its relationship with reproduction and food resource. Can. J. Fish Aquat. Sci. 43, 142–147 (1986).
doi: 10.1139/f86-015
Ryan, C. et al. Accounting for the effects of lipids in stable isotope (δ
pubmed: 23124665
doi: 10.1002/rcm.6394
Elliott, K. H., Roth, J. D. & Crook, K. Lipid extraction techniques for stable isotope analysis and ecological assays. Method Mol. Biol. 1609, 9–24 (2017).
doi: 10.1007/978-1-4939-6996-8_2
Newsome, S. D., Chivers, S. J. & Berman Kowalewski, M. The influence of lipid-extraction and long-term DMSO preservation on carbon (δ13C) and nitrogen (δ15N) isotope values in cetacean skin. Mar. Mamm. Sci. 34, 277–293 (2018).
doi: 10.1111/mms.12454
Budge, S. M., Iverson, S. J. & Koopman, H. N. Studying trophic ecology in marine ecosystems using fatty acids: A primer on analysis and interpretation. Mar. Mamm. Sci. 22, 759–801 (2006).
doi: 10.1111/j.1748-7692.2006.00079.x
Iverson, S. J., Frost, K. J. & Lang, S. Fat content and fatty acid composition of forage fish and invertebrates in Prince William Sound, Alaska: Factors contributing to among and within species variability. Mar. Ecol. Prog. Ser. 241, 161–181 (2002).
doi: 10.3354/meps241161
Lesage, V. Trends in the trophic ecology of St. Lawrence beluga (Delphinapterus leucas) over the period 1988–2012, based on stable isotope analysis. Can. Sci. Adv. Sec. Res. Doc. 2013/126, iv+26 (2014).
Anderson, M. J. & Walsh, D. C. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing?. Ecol. Monogr. 83, 557–574 (2013).
doi: 10.1890/12-2010.1
Clarke, K. R. & Gorley, R. N. PRIMER v7: User Manual/Tutorial 3rd edn. (Primer-E Ltd, 2015).
Bates, D. M., Mäechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Soft. 67, 1–48 (2015).
doi: 10.18637/jss.v067.i01
Wood, S. Mixed GAM computation vehicle with GCV/AIC/REML smoothness estimation and GAMMs by REML/PQL. in R Package Version 1–8 (2018).
R Core Team. R: A Language and Environment for Statistical Computing. https://www.R-project.org (R Foundation for Statistical Computing, 2021).
Stock, B. C. et al. Analyzing mixing systems using a new generation of Bayesian tracer mixing models. PeerJ 6, e5096. https://doi.org/10.7287/peerj.preprints.26884v1 (2018).
doi: 10.7287/peerj.preprints.26884v1
pubmed: 29942712
pmcid: 6015753
Parnell, A., Inger, R., Bearhop, S. & Jackson, A. Source partitioning using stable isotopes: coping with too much variation. PLoS Biol. 5, e9672. https://doi.org/10.1371/journal.pone.0009672 (2010).
doi: 10.1371/journal.pone.0009672
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, 1596–1602 (2012).
pubmed: 22693115
doi: 10.1002/rcm.6267
Gendron, D., Aguíñiga, S. & Carriquiry, J. D. d15N and d13C in skin biopsy samples: A note on their applicability for examining the relative trophic level in three rorqual species. J. Cetacean Res. Manag. 3, 41–44 (2001).
Giménez, J., Ramírez, F., Almunia, J., Forero, M. G. & 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, 54–61 (2016).
doi: 10.1016/j.jembe.2015.11.001
Caut, S., Angulo, E. & Courchamp, F. Discrimination factors (Δ
doi: 10.1111/j.1365-2435.2007.01360.x
Stock, B. C. & Semmens, B. X. Unifying error structures in commonly used biotracer mixing models. Ecology 97, 2562–2569 (2016).
pubmed: 27859126
doi: 10.1002/ecy.1517
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, 329–341 (2012).
doi: 10.1644/11-MAMM-S-187.1
Nifong, J. C., Layman, C. A. & Silliman, B. R. Size, sex and individual-level behavior drive intrapopulation variation in cross-ecosystem foraging of a top-predator. J. Anim. Ecol. 84, 35–48 (2015).
pubmed: 25327480
doi: 10.1111/1365-2656.12306
Devries, M. S., Stock, B. C., Christy, J. H., Goldsmith, G. R. & Dawson, T. E. Specialized morphology corresponds to a generalist diet: Linking form and function in smashing mantis shrimp crustaceans. Oecologia 182, 429–442 (2016).
pubmed: 27312263
doi: 10.1007/s00442-016-3667-5