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Research Article

Phenological synchronization disrupts trophic interactions between Kodiak brown bears and salmon

William W. Deacy, Jonathan B. Armstrong, William B. Leacock, Charles T. Robbins, David D. Gustine, Eric J. Ward, Joy A. Erlenbach, and Jack A. Stanford
PNAS first published August 21, 2017; https://doi.org/10.1073/pnas.1705248114
William W. Deacy
aDepartment of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331;
bFlathead Lake Biological Station, University of Montana, Missoula, MT 59860;
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  • For correspondence: will.deacy@gmail.com
Jonathan B. Armstrong
aDepartment of Fisheries and Wildlife, Oregon State University, Corvallis, OR 97331;
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William B. Leacock
cKodiak National Wildlife Refuge, US Fish and Wildlife Service, Kodiak, AK 99615;
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Charles T. Robbins
dSchool of Biological Sciences, Washington State University, Pullman, WA 99164;
eSchool of the Environment, Washington State University, Pullman, WA 99164;
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David D. Gustine
fGrand Teton National Park, National Park Service, Moose, WY 83012;
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Eric J. Ward
gConservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, Seattle, WA 98112
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Joy A. Erlenbach
eSchool of the Environment, Washington State University, Pullman, WA 99164;
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Jack A. Stanford
bFlathead Lake Biological Station, University of Montana, Missoula, MT 59860;
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  1. Edited by James A. Estes, University of California, Santa Cruz, CA, and approved July 18, 2017 (received for review March 30, 2017)

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  • Climate change disrupts bear–salmon interaction
    - Sep 18, 2017
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Significance

Climate change is altering the seasonal timing of biological events, effectively rescheduling the potential interactions among species. We know specialist consumers suffer when they fail to synchronize with their prey; however, little is known about how generalist consumers respond to phenological shifts across multiple food resources. This reshuffling may create novel temporal overlap between foods that were once separated in time. We examined how a generalist consumer, the Kodiak brown bear, responded when two key foods, red elderberry and sockeye salmon, became synchronized. Bears switched from eating salmon to elderberries, disrupting an ecological link that typically fertilizes terrestrial ecosystems and generates high mortality rates for salmon. These results demonstrate an underappreciated mechanism by which climate-altered phenologies can alter food webs.

Abstract

Climate change is altering the seasonal timing of life cycle events in organisms across the planet, but the magnitude of change often varies among taxa [Thackeray SJ, et al. (2016) Nature 535:241–245]. This can cause the temporal relationships among species to change, altering the strength of interaction. A large body of work has explored what happens when coevolved species shift out of sync, but virtually no studies have documented the effects of climate-induced synchronization, which could remove temporal barriers between species and create novel interactions. We explored how a predator, the Kodiak brown bear (Ursus arctos middendorffi), responded to asymmetric phenological shifts between its primary trophic resources, sockeye salmon (Oncorhynchus nerka) and red elderberry (Sambucus racemosa). In years with anomalously high spring air temperatures, elderberry fruited several weeks earlier and became available during the period when salmon spawned in tributary streams. Bears departed salmon spawning streams, where they typically kill 25–75% of the salmon [Quinn TP, Cunningham CJ, Wirsing AJ (2016) Oecologia 183:415–429], to forage on berries on adjacent hillsides. This prey switching behavior attenuated an iconic predator–prey interaction and likely altered the many ecological functions that result from bears foraging on salmon [Helfield JM, Naiman RJ (2006) Ecosystems 9:167–180]. We document how climate-induced shifts in resource phenology can alter food webs through a mechanism other than trophic mismatch. The current emphasis on singular consumer-resource interactions fails to capture how climate-altered phenologies reschedule resource availability and alter how energy flows through ecosystems.

  • climate change
  • mismatch
  • grizzly bear
  • phenology
  • prey switch

Footnotes

  • ↵1To whom correspondence should be addressed. Email: will.deacy{at}gmail.com.
  • Author contributions: W.W.D., J.B.A., W.B.L., and J.A.S. designed research; W.W.D., J.B.A., and W.B.L. performed research; C.T.R. and J.A.E. contributed analytic tools; W.W.D., D.D.G., and E.J.W. analyzed data; C.T.R. and J.A.E. performed elderberry digestibility and composition analyses; D.D.G. modeled elderberry phenology; and W.W.D. and J.B.A. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1705248114/-/DCSupplemental.

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Resource synchronization disrupts predation
William W. Deacy, Jonathan B. Armstrong, William B. Leacock, Charles T. Robbins, David D. Gustine, Eric J. Ward, Joy A. Erlenbach, Jack A. Stanford
Proceedings of the National Academy of Sciences Aug 2017, 201705248; DOI: 10.1073/pnas.1705248114

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Resource synchronization disrupts predation
William W. Deacy, Jonathan B. Armstrong, William B. Leacock, Charles T. Robbins, David D. Gustine, Eric J. Ward, Joy A. Erlenbach, Jack A. Stanford
Proceedings of the National Academy of Sciences Aug 2017, 201705248; DOI: 10.1073/pnas.1705248114
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