, Volume 188, Issue 4, pp 1105–1119 | Cite as

From the predictable to the unexpected: kelp forest and benthic invertebrate community dynamics following decades of sea otter expansion

  • Andrew O. SheltonEmail author
  • Chris J. Harvey
  • Jameal F. Samhouri
  • Kelly S. Andrews
  • Blake E. Feist
  • Kinsey E. Frick
  • Nick Tolimieri
  • Gregory D. Williams
  • Liam D. Antrim
  • Helen D. Berry
Community ecology – original research


The recovery of predators has the potential to restore ecosystems and fundamentally alter the services they provide. One iconic example of this is keystone predation by sea otters in the Northeast Pacific. Here, we combine spatial time series of sea otter abundance, canopy kelp area, and benthic invertebrate abundance from Washington State, USA, to examine the shifting consequences of sea otter reintroduction for kelp and kelp forest communities. We leverage the spatial variation in sea otter recovery to understand connections between sea otters and the kelp forest community. Sea otter increases created a pronounced decline in sea otter prey—particularly kelp-grazing sea urchins—and led to an expansion of canopy kelps from the late 1980s until roughly 2000. However, while sea otter and kelp population growth rates were positively correlated prior to 2002, this association disappeared over the last two decades. This disconnect occurred despite surveys showing that sea otter prey have continued to decline. Kelp area trends are decoupled from both sea otter and benthic invertebrate abundance at current densities. Variability in kelp abundance has declined in the most recent 15 years, as it has the synchrony in kelp abundance among sites. Together, these findings suggest that initial nearshore community responses to sea otter population expansion follow predictably from trophic cascade theory, but now, other factors may be as or more important in influencing community dynamics. Thus, the utility of sea otter predation in ecosystem restoration must be considered within the context of complex and shifting environmental conditions.


Sea otters Sea urchins Kelp forests Top–down control Trophic cascades Predator–prey interactions Keystone predator Community ecology Spatial ecology Marine ecosystems Enhydra lutris Macrocystis pyrifera Nereocystis luetkeana 



We thank H Jackson and G Galasso for piloting the research vessels during field work, and the United States Coast Guard station at Neah Bay for providing docking space. We thank Washington Department of Fish and Wildlife for their excellent sea otter surveys. C. Pfister provided thoughtful discussions, field assistance, and comments on the manuscript. J. Hale, K. Laidre, and two anonymous reviewers provided comments that improved the manuscript. Order of authorship was determined in part by efficiency of SCUBA-based navigation of Tatoosh Island while dodging menacing Steller sea lions. This study was supported by funding from the National Marine Fisheries Service, the Office of National Marine Sanctuaries, and the NOAA Integrated Ecosystem Assessment program.

Author contribution statement

AOS, CJH, JFS, KSA, BEF, KEF, NT, and GDW designed the surveys and performed field work. AOS, CJH, and JFS analyzed the data. AOS, CJH, and JFS wrote the manuscript; other authors provided editorial advice. BEF created Fig. 1.

Supplementary material

442_2018_4263_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1334 kb)


  1. Anderson MJ, Ellingsen KE, McArdle BH (2006) Multivariate dispersion as a measure of beta diversity. Ecol Lett 9:683–693CrossRefGoogle Scholar
  2. Arkema KK, Reed DC, Schroeter SC (2009) Direct and indirect effects of giant kelp determine benthic community structure and dynamics. Ecology 90:3126–3137CrossRefGoogle Scholar
  3. Bakun, A. 1973. Coastal upwelling indices, west coast of North America, 1946–71. U.S. Department of Commerce, NOAA Technical Report NMFS–SSRF–671. Accessed at on July 5, 2018
  4. Bell TW, Cavanaugh KC, Reed DC, Siegel DA (2015) Geographical variability in the controls of giant kelp biomass dynamics. J Biogeogr 42:2010–2021CrossRefGoogle Scholar
  5. Bellwood DR, Hughes TP, Hoey AS (2006) Sleeping functional group drives coral-reef recovery. Curr Biol 16:2434–2439CrossRefGoogle Scholar
  6. Carter SK, VanBlaricom GR, Allen BL (2007) Testing the generality of the trophic cascade paradigm for sea otters: a case study with kelp forests in northern Washington, USA. Hydrobiologia 579:233–249CrossRefGoogle Scholar
  7. Duggins DO (1988) The effects of kelp forests on nearshore environments biomass, detritus and altered flow. In: Van Blaricom G, Estes J (eds) The community ecology of sea otters. Springer, BerlinGoogle Scholar
  8. Ebeling A, Laur D (1988) Fish populations in kelp forests without sea otters: effects of severe storm damage and destructive urchin grazing. In: VanBlaricom G, Estes J (eds) The community ecology of sea otters. Springer, Berlin, pp 169–191CrossRefGoogle Scholar
  9. Eisenlord ME, Groner ML, Yoshioka RM, Elliott J, Maynard J, Fradkin S, Turner M, Pyne K, Rivlin N, van Hooidonk R, Harvell CD (2016) Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Philos Trans R Soc B 371:20150212CrossRefGoogle Scholar
  10. Estes JA, Duggins DO (1995) Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecol Monogr 65:75–100CrossRefGoogle Scholar
  11. Estes JA, Palmisano JF (1974) Sea otters: their role in structuring nearshore communities. Science 185:1058–1060CrossRefGoogle Scholar
  12. Estes JA, Riedman ML, Staedler MM, Tinker MT, Lyon BE (2003) Individual variation in prey selection by sea otters: patterns, causes and implications. J Anim Ecol 72(1):144–155. CrossRefGoogle Scholar
  13. Filbee-Dexter K, Scheibling RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25CrossRefGoogle Scholar
  14. Foster MS (1990) Organization of macroalgal assemblages in the Northeast Pacific—the assumption of homogeneity and the illusion of generality. Hydrobiologia 192:21–33CrossRefGoogle Scholar
  15. Gouhier TC, Guichard F (2014) Synchrony: quantifying variability in space and time. Methods Ecol Evol 5:524–533CrossRefGoogle Scholar
  16. Grothe PR, Taylor LA, Eakins BW, Carignan KS, Warnken RR, Lim E, Caldwell RJ (2010) Digital elevation model of Taholah, Washington: procedures, data sources and analysis. NOAA Tech, BoulderGoogle Scholar
  17. Hughes BB, Eby R, Van Dyke E, Tinker MT, Marks CI, Johnson KS, Wasson K (2013) Recovery of a top predator mediates negative eutrophic effects on seagrass. Proc Natl Acad Sci USA 110:15313–15318CrossRefGoogle Scholar
  18. Jameson RJ (1993) Survey of a translocated sea otter population. IUCN Otter Special Group Bull 8:2–4Google Scholar
  19. Jameson RJ, Jeffries S (1999) Results of the 1999 survey of the reintroduced sea otter population in Washington State. IUCN Otter Special Group Bull 16:79–85Google Scholar
  20. Jameson RJ, Kenyon KW, Johnson AM, Wight HW (1982) History and status of translocated sea otter populations in North America. Wildlife Soc B 10:100–107Google Scholar
  21. Jeffries S, Jameson R (2014) Results of the 2013 survey of the reintroduced sea otter population in Washington State. Washington Department of Fish and WildlifeGoogle Scholar
  22. Kenner MC, Estes JA, Tinker MT, Bodkin JL, Cowen RK, Harrold C, Hatfield BB, Novak M, Rassweiler A, Reed DC (2013) A multi-decade time series of kelp forest community structure at San Nicolas Island, California (USA). Ecol Lett 94:2654–2655CrossRefGoogle Scholar
  23. Knowlton N (2004) Multiple “stable” states and the conservation of marine ecosystems. Prog Oceanogr 60:387–396CrossRefGoogle Scholar
  24. Kvitek RG, Shull D, Canestro D, Bowlby EC, Troutman BL (1989) Sea otters and benthic prey communities in Washington State. Mar Mammal Sci 5:266–280CrossRefGoogle Scholar
  25. Kvitek RG, Iampietro PJ, Thomas K (1998) Sea otters and benthic prey communities: a direct test of the sea otter as keystone predator in Washington state. Mar Mammal Sci 14:895–902CrossRefGoogle Scholar
  26. Kvitek RG, Iampietro PJ, Thomas K (2000) Quantitative assessment of sea otter benthic prey communities within the Olympic Coast National Marine Sanctuary: 1999 re-survey of 1995 and 1985 monitoring stations. Final report to the Olympic Coast National Marine SanctuaryGoogle Scholar
  27. Lafferty KD (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl 14:1566–1573CrossRefGoogle Scholar
  28. Laidre KL, Jameson RJ (2006) Foraging patterns and prey selection in an increasing and expanding sea otter population. J Mammal 87:799–807CrossRefGoogle Scholar
  29. Laidre KL, Jameson RJ, Demaster DP (2001) An estimation of carrying capacity for sea otters along the California coast. Mar Mammal Sci 17:294–309CrossRefGoogle Scholar
  30. Laidre KL, Jameson RJ, Jeffries SJ, Hobbs RC, Bowlby CE, VanBlaricom GR (2002) Estimates of carrying capacity for sea otters in Washington state. Wildlife Soc B 30:1172–1181Google Scholar
  31. Laidre KL, Jameson RJ, Gurarie E, Jeffries SJ, Allen H (2009) Spatial habitat use patterns of sea otters in coastal Washington. J Mammal 90:906–917CrossRefGoogle Scholar
  32. Lance MM, Richardson SA, Allen HL (2004) Washington state recovery plan for the sea otter. Washington Department of Fish and Wildlife, OlympiaGoogle Scholar
  33. Legendre P, Borcard D, Peres-Neto PR (2005) analyzing beta diversity: partitioning the spatial variation of community composition data. Ecol Monogr 75:435–450CrossRefGoogle Scholar
  34. Ling SD, Scheibling E, Rassweiler A, Johnson CR, Shears N, Connell SD, Salomon AK, Norderhaug KM, Perez-Matus A, Hernandez JC, Clemente S, Blamey LK, Hereu B, Ballesteros E, Sala E, Garrabou J, Cebrian E, Zabala M, Fujita D, Johnson LE (2015) Global regime shift dynamics of catastrophic sea urchin overgrazing. Phil Trans R Soc B 370:20130269. CrossRefGoogle Scholar
  35. Loreau M, de Mazancourt C (2008) Species synchrony and its drivers: neutral and nonneutral community dynamics in fluctuating environments. Am Nat 172:E48–E66CrossRefGoogle Scholar
  36. Mann KH (1973) Seaweeds: their productivity and strategy for growth: The role of large marine algae in coastal productivity is far more important than has been suspected. Science 182:975–981CrossRefGoogle Scholar
  37. Mantua NJ, Hare SR (2002) The Pacific decadal oscillation. J Oceanogr 58:35–44CrossRefGoogle Scholar
  38. Mantua N, Hare S, Zhang Y, Wallace J, Francis R (1997) A Pacific interdecadal climate oscillation with impacts on salmon production. Bull Am Meteorol Soc 78:1069–1079CrossRefGoogle Scholar
  39. Markel RW, Shurin JB (2015) Indirect effects of sea otters on rockfish (Sebastes spp.) in giant kelp forests. Ecology 96:2877–2890CrossRefGoogle Scholar
  40. National Park Service (2008) Final general management plan and environmental impact statement. Olympic National Park, Washington, D.C.Google Scholar
  41. Office of National Marine Sanctuaries (2008) Olympic Coast National Marine Sanctuary condition report 2008. US Department of Commerce, National Oceanic and Atmospheric Administration, Office of National Marine Sanctuaries, Silver SpringGoogle Scholar
  42. Paine RT (1969) A note on trophic complexity and community stability. Am Nat 103:91–93CrossRefGoogle Scholar
  43. Petraitis PS, Methratta ET, Rhile EC, Vidargas NA, Dudgeon SR (2009) Experimental confirmation of multiple community states in a marine ecosystem. Oecologia 161:139–148CrossRefGoogle Scholar
  44. Pfister CA, Berry HD, Mumford T (2018) The dynamics of kelp forests in the Northeast Pacific Ocean and the relationship with environmental drivers. J Ecol. CrossRefGoogle Scholar
  45. Pinsky ML, Fogarty M (2012) Lagged social-ecological responses to climate and range shifts in fisheries. Clim Change 115:883–891CrossRefGoogle Scholar
  46. Pinsky ML, Guannel G, Arkema KK (2013) Quantifying wave attenuation to inform coastal habitat conservation. Ecosphere 4(8):95. CrossRefGoogle Scholar
  47. Power ME, Tilman D, Estes JA, Menge BA, Bond WJ, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT (1996) Challenges in the quest for keystones. Bioscience 46:609–620CrossRefGoogle Scholar
  48. R Core Team (2017). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
  49. Reed DC, Rassweiler A, Carr MH, Cavanaugh KC, Malone DP, Siegel DA (2011) Wave disturbance overwhelms top-down and bottom-up control of primary production in California kelp forests. Ecology 92:2108–2116CrossRefGoogle Scholar
  50. Reisewitz SE, Estes JA, Simenstad CA (2006) Indirect food web interactions: sea otters and kelp forest fishes in the Aleutian archipelago. Oecologia 146:623–631CrossRefGoogle Scholar
  51. Sergio F, Schmitz OJ, Krebs CJ, Holt RD, Heithaus MR, Wirsing AJ, Ripple WJ, Ritchie E, Ainley D, Oro D, Jhala Y, Hiraldo F, Korpimäki E (2014) Towards a cohesive, holistic view of top predation: a definition, synthesis and perspective. Oikos 123:1234–1243CrossRefGoogle Scholar
  52. Shelton AO, Francis T, Feist BE, Williams GE, Lindquist A, Levin P (2017) Forty years of seagrass population stability and resilience in an urbanizing estuary. J Ecol 105:458–470CrossRefGoogle Scholar
  53. Sherman K, Duda AM (1999) An ecosystem approach to global assessment and management of coastal waters. Mar Ecol Prog Ser 190:271–287CrossRefGoogle Scholar
  54. Steneck R, Graham M, Bourque B, Corbett D, Erlandson J, Estes J, Tegner M (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459CrossRefGoogle Scholar
  55. Stier AC, Samhouri JF, Novak M, Marshall KN, Ward EJ, Holt RD, Levin PS (2016) Ecosystem context and historical contingency in apex predator recoveries. Sci Adv 2:e1501769CrossRefGoogle Scholar
  56. Taylor LA, Eakins BW, Carignan KS, Warnken RR, Sazonova T, Schoolcraft DC (2008) Digital Elevation Model of La Push, Washington: procedures, data sources and analysis. NOAA Tech, BoulderGoogle Scholar
  57. Tinker MT, Bentall G, Estes JA (2008) Food limitation leads to behavioral diversification and dietary specialization in sea otters. Proc Nat Acad Sci 105(2):560–565. CrossRefPubMedGoogle Scholar
  58. Van Wagenen RF (2015) Washington Coastal kelp resources—port townsend to the Columbia River, summer 2014. Washington Department of Natural Resources, OlympiaGoogle Scholar
  59. WADNR (2017) “Kelp monitoring—Olympic Peninsula” Washington State Department of Natural Resources, Olympia, WA. Accessed: 1 Sept 2017
  60. Walker KA, Davis JW, Duffield DA (2008) Activity budgets and prey consumption of Sea Otters (Enhydra lutris kenyoni) in Washington. Aquatic Mammals 34:393–401CrossRefGoogle Scholar
  61. Watson J, Estes JA (2011) Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island, Canada. Ecol Monogr 81:215–239CrossRefGoogle Scholar
  62. Wilmers CC, Estes JA, Edwards M, Laidre KL, Konar B (2012) Do trophic cascades affect the storage and flux of atmospheric carbon? An analysis of sea otters and kelp forests. Front Ecol Environ 10:409–415CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2018

Authors and Affiliations

  • Andrew O. Shelton
    • 1
    Email author
  • Chris J. Harvey
    • 1
  • Jameal F. Samhouri
    • 1
  • Kelly S. Andrews
    • 1
  • Blake E. Feist
    • 1
  • Kinsey E. Frick
    • 2
  • Nick Tolimieri
    • 1
  • Gregory D. Williams
    • 3
  • Liam D. Antrim
    • 4
  • Helen D. Berry
    • 5
  1. 1.Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationSeattleUSA
  2. 2.Fisheries Ecology Division, Northwest Fisheries Science Center, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationSeattleUSA
  3. 3.Pacific States Marine Fisheries Commission, Under Contract to Northwest Fisheries Science Center, National Marine Fisheries ServiceNational Oceanic and Atmospheric AdministrationSeattleUSA
  4. 4.Olympic Coast National Marine Sanctuary, National Ocean ServiceNational Oceanic and Atmospheric AdministrationPort AngelesUSA
  5. 5.Washington State Department of Natural ResourcesOlympiaUSA

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