A keystone avian predator faces elevated energy expenditure in a warming Arctic.
activity budgets
climate change
daily energy expenditure
dovekie
ecotoxicology
mercury
plasticity
sea surface temperature
Journal
Ecology
ISSN: 1939-9170
Titre abrégé: Ecology
Pays: United States
ID NLM: 0043541
Informations de publication
Date de publication:
05 2023
05 2023
Historique:
revised:
28
02
2023
received:
23
11
2022
accepted:
09
03
2023
medline:
2
5
2023
pubmed:
21
3
2023
entrez:
20
3
2023
Statut:
ppublish
Résumé
Climate change is transforming bioenergetic landscapes, challenging behavioral and physiological coping mechanisms. A critical question involves whether animals can adjust behavioral patterns and energy expenditure to stabilize fitness given reconfiguration of resource bases, or whether limits to plasticity ultimately compromise energy balance. In the Arctic, rapidly warming temperatures are transforming food webs, making Arctic organisms strong models for understanding biological implications of climate change-related environmental variability. We examined plasticity in the daily energy expenditure (DEE) of an Arctic seabird, the little auk (Alle alle) in response to variability in climate change-sensitive drivers of resource availability, sea surface temperature (SST) and sea ice coverage (SIC), and tested the hypothesis that energetic ceilings and exposure to mercury, an important neurotoxin and endocrine disrupter in marine ecosystems, may limit scope for plasticity. To estimate DEE, we used accelerometer data obtained across years from two colonies exposed to distinct environmental conditions (Ukaleqarteq [UK], East Greenland; Hornsund [HS], Svalbard). We proceeded to model future changes in SST to predict energetic impacts. At UK, high flight costs linked to low SIC and high SST drove DEE from below to above 4 × basal metabolic rate (BMR), a proposed energetic threshold for breeding birds. However, DEE remained below 7 × BMR, an alternative threshold, and did not plateau. Birds at HS experienced higher, relatively invariable SST, and operated above 4 × BMR. Mercury exposure was unrelated to DEE, and fitness remained stable. Thus, plasticity in DEE currently buffers fitness, providing resiliency against climate change. Nevertheless, modeling suggests that continued warming of SST may promote accelerating increases in DEE, which may become unsustainable.
Substances chimiques
Mercury
FXS1BY2PGL
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e4034Informations de copyright
© 2023 The Authors. Ecology published by Wiley Periodicals LLC on behalf of The Ecological Society of America.
Références
Ackerman, J. T., C. A. Eagles-Smith, M. P. Herzog, C. A. Hartman, S. H. Peterson, D. C. Evers, A. K. Jackson, J. E. Elliott, S. S. Vander Pol, and C. E. Bryan. 2016. “Avian Mercury Exposure and Toxicological Risk across Western North America: A Synthesis.” Science of the Total Environment 568: 749-69.
AMAP. 2021. “2021 AMAP Mercury Assessment.” In Summary for Policy-makers 16. Tromsø: Arctic Monitoring and Assessment Programme (AMAP).
Amélineau, F., D. Grémillet, D. Bonnet, T. Le Bot, and J. Fort. 2016. “Where to Forage in the Absence of Sea Ice? Bathymetry As a Key Factor for an Arctic Seabird.” PLoS One 11: e0157764.
Amélineau, F., D. Grémillet, A. Harding, W. Walkusz, R. Choquet, and J. Fort. 2019. “Arctic Climate Change and Pollution Impact Little Auk Foraging and Fitness across a Decade.” Scientific Reports 9: 1014.
Bartley, T. J., K. S. McCann, C. Bieg, K. Cazelles, M. Granados, M. M. Guzzo, A. S. MacDougall, T. D. Tunney, and B. C. McMeans. 2019. “Food Web Rewiring in a Changing World.” Nature Ecology & Evolution 3: 345-54.
Bates, D., M. Mächler, B. Bolker, and S. Walker. 2015. “Fitting Linear Mixed-Effects Models Using lme4.” Journal of Statistical Software 1406: v067.i01.
Bustamante, P., V. Lahaye, C. Durnez, C. Churlaud, and F. Caurant. 2006. “Total and Organic Hg Concentrations in Cephalopods from the North Eastern Atlantic Waters: Influence of Geographical Origin and Feeding Ecology.” Science of the Total Environment 368: 585-96.
Carstensen, J., A. Weydmann, A. Olszewska, and S. Kwasniewski. 2012. “Effects of Environmental Conditions on the Biomass of Calanus Spp. in the Nordic Seas.” Journal of Plankton Research 34: 951-66.
Chastel, O., J. Fort, J. T. Ackerman, C. Albert, F. Angelier, N. Basu, P. Blévin, et al. 2022. “Mercury Contamination and Potential Health Risks to Arctic Seabirds and Shorebirds.” Science of the Total Environment 844: 156944.
Cottier, F., V. Tverberg, M. Inall, H. Svendsen, F. Nilsen, and C. Griffiths. 2005. “Water Mass Modification in an Arctic Fjord through Cross-Shelf Exchange: The Seasonal Hydrography of Kongsfjorden, Svalbard.” Journal of Geophysical. Research 110: C12005.
Descamps, S., K. Wojczulanis-Jakubas, D. Jakubas, M. Vihtakari, H. Steen, N. Karnovsky, J. Welcker, et al. 2022. “Consequences of Atlantification on a Zooplanktivorous Arctic Seabird.” Frontiers in Marine Science 20: 933.
Drent, R. H., and S. Daan. 1980. “The Prudent Parent: Energetic Adjustments in Avian Breeding.” Ardea 55: 225-52.
Eamer, J., G. Donaldson, T. Gaston, K. Kosobokova, K. Lárusson, I. Melnikov, J. D. Reist, et al. 2013. Life Linked to Ice: A Guide to Sea-Ice Associated Biodiversity in this Time of Rapid Change. CAFF Assessment Series, Vol 10 115. Akureyri, Iceland: CAFF International Secretariat.
Elliott, K. H., G. K. Davoren, and A. J. Gaston. 2007. “The Influence of Buoyancy, and Drag on the Dive Behaviour of an Arctic Seabird, the Thick-Billed Murre.” Canadian Journal of Zoology 85: 352-61.
Elliott, K. H., M. Le Vaillant, A. Kato, A. J. Gaston, Y. Ropert-Coudert, J. F. Hare, J. R. Speakman, and D. Croll. 2014. “Age-Related Variation in Energy Expenditure in a Long-Lived Bird within the Envelope of an Energy Ceiling.” Journal of Animal Ecology 83: 136-46.
Fossette, S., G. Schofield, M. Lilley, A. Gleiss, and G. Hays. 2012. “Acceleration Data Reveal the Energy Management Strategy of a Marine Ectotherm during Reproduction: Accelerometry Reveals Turtle Energy Management Strategy.” Functional Ecology 26: 324-33.
Fox, J., and S. Weisberg. 2019. An R Companion to Applied Regression, 3rd ed. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/.
Gabrielsen, G. W., J. Taylor, M. Konarzewski, and F. Mehlum. 1991. “Field and Laboratory Metabolism and Thermoregulation in Dovekies (Alle alle).” The Auk 108: 71-8.
Gerson, A. R., D. A. Cristol, and C. L. Seewagen. 2019. “Environmentally Relevant Methylmercury Exposure Reduces the Metabolic Scope of a Model Songbird.” Environmental Pollution 246: 790-6.
Gilg, O., K. M. Kovacs, J. Aars, J. Fort, G. Gauthier, D. Grémillet, R. A. Ims, et al. 2012. “Climate Change and the Ecology and Evolution of Arctic Vertebrates: Climate Change Impacts on Arctic Vertebrates.” Annals of the New York Academy of Sciences 1249: 166-90.
Gilmour, M. E., J. L. Lavers, C. Lamborg, O. Chastel, S. A. Kania, and S. A. Shaffer. 2019. “Mercury as an Indicator of Foraging Ecology but Not the Breeding Hormone Prolactin in Seabirds.” Ecological Indicators 103: 248-59.
González-Bergonzoni, I., K. L. Johansen, A. Mosbech, F. Landkildehus, E. Jeppesen, and T. A. Davidson. 2017. “Small Birds, Big Effects: The Little Auk (Alle Alle) Transforms High Arctic Ecosystems.” Proceedings of the Royal Society of London B 284: 20162572.
Grémillet, D., J. Welcker, N. Karnovsky, W. Walkusz, M. Hall, J. Fort, Z. W. Brown, J. R. Speakman, and A. M. A. Harding. 2012. “Little Auks Buffer the Impact of Current Arctic Climate Change.” Marine Ecology Progress Series 454: 197-206.
Grunst, A. S., M. L. Grunst, D. Grémillet, A. Kato, C. Albert, É. Brisson-Curadeau, M. Clairbaux, et al. 2023. “Mercury Contamination Challenges the Behavioral Response of a Keystone Species to Arctic Climate Change.” Environmental Science and Technology 57: 2054-63.
Grunst, M. L., A. S. Grunst, D. Grémillet, A. Kato, P. Bustamante, C. Albert, C. Brisson-Curadeau, et al. 2022. “DATASETS FOR: A Keystone Avian Predator Faces Elevated Energy Expenditure in a Warming Arctic.” Zenodo. Data Set. https://doi.org/10.5281/zenodo.7334556.
Halsey, L. G., J. A. Green, S. D. Twiss, W. Arnold, S. J. Burthe, P. J. Butler, S. J. Cooke, et al. 2019. “Flexibility, Variability and Constraint in Energy Management Patterns across Vertebrate Taxa Revealed by Long-Term Heart Rate Measurements.” Functional Ecology 33: 260-72.
Hammond, K. A., and J. Diamond. 1997. “Maximal Sustained Energy Budgets in Humans and Animals.” Nature 386: 457-62.
Harding, A., A. Kitaysky, M. Hall, J. Welcker, N. Karnovsky, S. Talbot, K. C. Hamer, and D. Grémillet. 2009. “Flexibility in the Parental Effort of an Arctic-Breeding Seabird.” Functional Ecology 23: 348-58.
Harding, A., J. Piatt, J. Schmutz, M. Shultz, T. Pelt, A. Kettle, and S. G. Speckman. 2007. “Prey Density and the Behavioral Flexibility of a Marine Predator: The Common Murre (Uria aalge).” Ecology 88: 2024-33.
Harrell, F. E., Jr., and C. Dupont. 2019. “Hmisc: Harrell Miscellaneous.” R Package Version 4.3-0. https://CRAN.R-project.org/package=Hmisc.
Hovinen, J. E. H., J. Welcker, S. Descamps, H. Strøm, K. Jerstad, J. Berge, and H. Steen. 2014. “Climate Warming Decreases the Survival of the Little Auk (Alle alle), a High Arctic Avian Predator.” Ecology and Evolution 4: 3127-38.
IPCC. 2021. In Climate Change 2021: The Physical Science Basis. Contribution of Working Group I to the Sixth Assessment Report of the Intergovernmental Panel on Climate Change, edited by V. Masson-Delmotte, P. Zhai, A. Pirani, S. L. Connors, C. Péan, S. Berger, et al. Cambridge: Cambridge University Press.
Jakubas, D., K. Wojczulanis-Jakubas, R. Boehnke, D. Kidawa, K. Błachowiak-Samołyk, and L. Stempniewicz. 2016. “Intra-Seasonal Variation in Zooplankton Availability, Chick Diet and Breeding Performance of a High Arctic Planktivorous Seabird.” Polar Biology 39: 1547-61.
Jakubas, D., K. Wojczulanis-Jakubas, L. Iliszko, D. Kidawa, R. Boehnke, K. Błachowiak-Samołyk, and L. Stempniewicz. 2020. “Flexibility of Little Auks Foraging in Various Oceanographic Features in a Changing Arctic.” Scientific Reports 10: 8283.
Jakubas, D., K. Wojczulanis-Jakubas, L. Iliszko, H. Strøm, and L. Stempniewicz. 2017. “Habitat Foraging Niche of a High Arctic Zooplanktivorous Seabird in a Changing Environment.” Scientific Reports 7: 16203.
Jakubas, D., K. Wojczulanis-Jakubas, and A. Petersen. 2022. “A Quiet Extirpation of the Breeding Little Auk Alle Alle Population in Iceland in the Shadow of the Famous Cousin Extermination.” Science of the Total Environment 808: 152167.
Jenssen, B. M. 2006. “Endocrine-Disrupting Chemicals and Climate Change: A Worst-Case Combination for Arctic Marine Mammals and Seabirds?” Environmental Health Perspectives 114: 76-80.
Jodice, P., D. Roby, R. Suryan, D. Irons, K. Turco, E. Brown, J. F. Thedinga, and G. H. Visser. 2006. “Increased Energy Expenditure by a Seabird in Response to Higher Food Abundance.” Marine Ecology Progress Series 306: 283-93.
John, R. S. 1998. “The History and Theory of the Doubly Labeled Water Technique.” The American Journal of Clinical Nutrition 68: 932S-8S.
Jonsson, S., M. Mastromonaco, F. Wang, A. Bravo, W. Cairns, J. Chételat, T. A. Douglas, et al. 2022. “Arctic Methylmercury Cycling.” Science of the Total Environment 850: 157445.
Kampp, K., H. Meltofte, and C. E. Mortensen. 1987. “Population Size of the Little Auk (Alle Alle).” Journal of the Danish Ornithological Society 81: 129-36.
Karnovsky, N., A. Harding, W. Walkusz, S. Kwasniewski, I. Goszczko, J. Wiktor, H. Rutti, et al. 2010. “Foraging Distributions of Little Auks Alle Alle across the Greenland Sea: Implications of Present and Future Arctic Climate Change.” Marine Ecology Progress Series 415: 283-93.
Karnovsky, N., S. Kwasniewski, J. Weslawski, W. Walkusz, and A. Beszczynska-Möller. 2003. “Foraging Behavior of Little Auks in a Heterogeneous Environment.” Marine Ecology Progress Series 253: 289-303.
Keslinka, L. K., K. Wojczulanis-Jakubas, D. Jakubas, and G. Neubauer. 2019. “Determinants of the Little Auk (Alle Alle) Breeding Colony Location and Size in W and NW Coast of Spitsbergen.” PLoS One 14: e0212668.
Krabbenhoft, D. P., and E. M. Sunderland. 2013. “Global Change and Mercury.” Science 341: 1457-8.
Kuznetsova, A., P. Brockhoff, and R. Christensen. 2017. “lmerTest Package: Tests in Linear Mixed Effects Models.” Journal of Statistical Software 82: 1-26.
Kwasniewski, S., M. Gluchowska, D. Jakubas, K. Wojczulanis-Jakubas, W. Walkusz, N. Karnovsky, K. Blachowiak-Samolyk, M. Cisek, and L. Stempniewicz. 2010. “The Impact of Different Hydrographic Conditions and Zooplankton Communities on Provisioning Little Auks along the West Coast of Spitsbergen.” Progress in Oceanography 87: 72-82.
Lenth, R. 2019. “emmeans: Estimated Marginal Means, aka Least-Squares Means.” R Package Version 1.4.3.01. https://CRAN.R-project.org/package=emmeans.
Lifson, N., and R. McClintock. 1966. “Theory of Use of the Turnover Rates of Body Water for Measuring Energy and Material Balance.” Journal of Theoretical Biology 12: 46-74.
Loeng, H. 1991. “Features of the Physical Oceanographic Conditions of the Barents Sea.” Polar Research 10: 5-18.
Moe, B., L. Stempniewicz, D. Jakubas, F. Angelier, O. Chastel, F. Dinessen, G. W. Gabrielsen, et al. 2009. “Climate Change and Phenological Responses of Two Seabird Species Breeding in the High-Arctic.” Marine Ecology Progress Series 393: 235-46.
Mueller, P., and J. Diamond. 2001. “Metabolic Rate and Environmental Productivity: Well-Provisioned Animals Evolved to Run and Idle Fast.” Proceedings of the National Academy of Science U.S.A. 98: 12550-4.
Peig, J., and A. J. Green. 2009. “New Perspectives for Estimating Body Condition from Mass/Length Data: The Scaled Mass Index as an Alternative Method.” Oikos 118: 1883-91.
Pinaud, D., Y. Cherel, and H. Weimerskirch. 2005. “Effect of Environmental Variability on Habitat Selection, Diet, Provisioning Behaviour and Chick Growth in Yellow-Nosed Albatrosses.” Marine Ecology Progress Series 298: 295-304.
Post, E., U. Bhatt, C. Bitz, J. Brodie, T. Fulton, M. Hebblewhite, J. Kerby, S. J. Kutz, I. Stirling, and D. A. Walker. 2013. “Ecological Consequences of Sea-Ice Decline.” Science 341: 519-24.
R Core Team. 2021. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. https://www.R-project.org/.
Regular, P. M., A. Hedd, W. Montevecchi, G. Robertson, A. Storey, and C. Walsh. 2014. “Why Timing Is Everything: Energetic Costs and Reproductive Consequences of Resource Mismatch for a Chick-Rearing Seabird.” Ecosphere 5: art155.
Sakamoto, K. Q., K. Sato, M. Ishizuka, Y. Watanuki, A. Takahashi, F. Daunt, and S. Wanless. 2009. “Can Ethograms Be Automatically Generated Using Body Acceleration Data from Free-Ranging Birds?” PLoS One 4: e5379.
Schielzeth, H. 2010. “Simple Means to Improve the Interpretability of Regression Coefficients.” Methods in Ecology and Evolution 1: 103-13.
Shankar, A., C. Graham, J. Canepa, S. Wethington, and D. Powers. 2019. “Hummingbirds Budget Energy Flexibly in Response to Changing Resources.” Functional Ecology 33: 1904-16.
Sherwood, S. C., and M. Huber. 2010. “An Adaptability Limit to Climate Change Due to Heat Stress.” Proceedings of the National Academy of Sciences of the United States of America 107: 9552-5.
Speakman, J. R., T. Ergon, R. Cavanagh, K. Reid, D. Scantlebury, and X. Lambin. 2003. “Resting and Daily Energy Expenditures of Free-Living Field Voles Are Positively Correlated but Reflect Extrinsic Rather than Intrinsic Effects.” Proceedings of the National Academy of Sciences of the United States of America 100: 14057-62.
Ste-Marie, E., D. Grémillet, J. Fort, A. Patterson, É. Brisson-Curadeau, M. Clairbaux, S. Perret, J. R. Speakman, and K. H. Elliott. 2022. “Accelerating Animal Energetics: High Dive Costs in a Small Seabird Disrupt the Dynamic Body Acceleration-Energy Expenditure Relationship.” Journal of Experimental Biology 225: jeb243252.
Stempniewicz, L., K. Błachowiak-Samołyk, and J. Węsławski. 2007. “Impact of Climate Change on Zooplankton Communities, Seabird Populations and Arctic Terrestrial Ecosystem-A Scenario.” Deep Sea Research Part II: Topical Studies in Oceanography 54: 2934-294.
Stern, G., R. Macdonald, P. Outridge, S. Wilson, J. Chételat, A. Cole, H. Hintelmann, et al. 2012. “How Does Climate Change Influence Arctic Mercury?” Science of the Total Environment 414: 22-42.
Strzelewicz, A., A. Przyborska, and W. Walczowski. 2022. “Increased Presence of Atlantic Water on the Shelf South-West of Spitsbergen with Implications for the Arctic Fjord Hornsund.” Progress in Oceanography 200: 102714.
Suryan, R., D. Irons, M. Kaufman, J. Benson, P. Jodice, D. Roby, and E. D. Brown. 2002. “Short-Term Fluctuations in Forage Fish Availability and the Effect on Prey Selection and Brood-Rearing in the Black-Legged Kittiwake.” Marine Ecology Progress Series 236: 273-87.
Tinbergen, J. M., and S. Verhulst. 2000. “A Fixed Energetic Ceiling to Parental Effort in the Great Tit?” Journal of Animal Ecology 69: 323-34.
Tremblay, F., S. Whelan, E. Choy, S. Hatch, and K. Elliott. 2022. “Resting Costs Too: The Relative Importance of Active and Resting Energy Expenditure in a Sub-Arctic Seabird.” Journal of Experimental Biology 225: jeb243548.
Von Bank, J, M. Weegman, P. Link, S. Cunningham, K. Kraai, D. Collins, and B. M. Ballard. 2021. “Winter Fidelity, Movements, and Energy Expenditure of Midcontinent Greater White-Fronted Geese.” Movement Ecology 9: 2.
Welcker, J., A. Harding, A. Kitaysky, J. Speakman, and G. Gabrielsen. 2009. “Daily Energy Expenditure Increases in Response to Low Nutritional Stress in an Arctic-Breeding Seabird with no Effect on Mortality.” Functional Ecology 23: 1081-90.
Wojczulanis-Jakubas, K. 2021. “Being the Winner Is Being the Loser when Playing a Parental Tug-of-War - A New Framework on Stability of Biparental Care.” Frontiers in Ecology & Evolution 9: 763075.
Wojczulanis-Jakubas, K., D. Jakubas, J. Welcker, A. Harding, N. Karnovsky, D. Kidawa, H. Steen, L. Stempniewicz, and C. J. Camphuysen. 2011. “Body Size Variation of a High-Arctic Seabird: The Dovekie (Alle alle).” Polar Biology 34: 847-54.
Wood, S. N. 2017. Generalized Additive Models: An Introduction with R, 2nd ed. Boca Raton: Chapman and Hall/CRC.
Zamora-Vilchis, I., S. Williams, and C. Johnson. 2012. “Environmental Temperature Affects Prevalence of Blood Parasites of Birds on an Elevation Gradient: Implications for Disease in a Warming Climate.” PLoS One 7: e39208.
Zuur, A. F., E. Ieno, and C. Elphick. 2010. “A Protocol for Data Exploration to Avoid Common Statistical Problems.” Methods in Ecology and Evolution 1: 3-14.