Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Regime shifts in rocky intertidal communities associated with a marine heatwave and disease outbreak

Abstract

Long-term, large-scale experimental studies provide critical information about how global change influences communities. When environmental changes are severe, they can trigger abrupt transitions from one community type to another leading to a regime shift. From 2014 to 2016, rocky intertidal habitats in the northeast Pacific Ocean experienced extreme temperatures during a multi-year marine heatwave (MHW) and sharp population declines of the keystone predator Pisaster ochraceus due to sea star wasting disease (SSWD). Here we measured the community structure before, during and after the MHW onset and SSWD outbreak in a 15-year succession experiment conducted in a rocky intertidal meta-ecosystem spanning 13 sites on four capes in Oregon and northern California, United States. Kelp abundance declined during the MHW due to extreme temperatures, while gooseneck barnacle and mussel abundances increased due to reduced predation pressure after the loss of Pisaster from SSWD. Using several methods, we detected regime shifts from substrate- or algae-dominated to invertebrate-dominated alternative states at two capes. After water temperatures cooled and Pisaster population densities recovered, community structure differed from pre-disturbance conditions, suggesting low resilience. Consequently, thermal stress and predator loss can result in regime shifts that fundamentally alter community structure even after restoration of baseline conditions.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Intertidal water temperatures measured at rocky intertidal capes during the NE Pacific MHW.
Fig. 2: Per cent cover (mean ± s.e.m.) of rocky intertidal functional groups in experimental plots from 2006 to 2020.
Fig. 3: Relative abundance of rocky intertidal community states from 2006 to 2020 in the capes (rows) and experimental treatments (columns).
Fig. 4: Transitions between alternative states in rocky intertidal communities.
Fig. 5: Rocky intertidal community similarity (mean and 99% confidence intervals) per treatment and cape before, during and after SSWD and the MHW.
Fig. 6: Relationships between mussel length and Pisaster ochraceus diameter, and between kelp canopy cover and intertidal water temperature anomaly measured at rocky intertidal capes.

Similar content being viewed by others

Data availability

Community structure data are available on the Environmental Data Initiative Data Portal (https://doi.org/10.6073/pasta/1589a0ed9412db430a5555bc968a18a0). Temperature data (for example, https://doi.org/10.6085/AA/YBHX00_XXXITV2XMMR03_20200919.50.1) and sea star population data (https://doi.org/10.6085/AA/LTREB_Data.1.1) are published on DataONE. Source data are provided with this paper.

Code availability

Code supporting the findings of this study is publicly available on GitHub (https://github.com/zechmeunier/intertidal-regime-shifts).

References

  1. Oliver, E. C. J. et al. Longer and more frequent marine heatwaves over the past century. Nat. Commun. 9, 1324 (2018).

    PubMed  PubMed Central  Google Scholar 

  2. McCabe, R. M. et al. An unprecedented coastwide toxic algal bloom linked to anomalous ocean conditions. Geophys. Res. Lett. 43, 10,366–10,376 (2016).

    Google Scholar 

  3. Chan, F., Barth, J., Kroeker, K., Lubchenco, J. & Menge, B. The dynamics and impact of ocean acidification and hypoxia: insights from sustained investigations in the northern California current large marine ecosystem. Oceanography 32, 62–71 (2019).

    Google Scholar 

  4. Hughes, T. P. & Connell, J. H. Multiple stressors on coral reefs: a long-term perspective. Limnol. Oceanogr. 44, 932–940 (1999).

    Google Scholar 

  5. McCauley, D. J. et al. Marine defaunation: animal loss in the global ocean. Science 347, 1255641 (2015).

    PubMed  Google Scholar 

  6. Scheffer, M. et al. Early-warning signals for critical transitions. Nature 461, 53–59 (2009).

    CAS  PubMed  Google Scholar 

  7. Conversi, A. et al. A holistic view of marine regime shifts. Philos. Trans. R. Soc. B 370, 20130279 (2015).

    Google Scholar 

  8. Rogers-Bennett, L. & Catton, C. A. Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens. Sci. Rep. 9, 15050 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Ling, S. D. et al. Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos. Trans. R. Soc. B 370, 20130269 (2015).

    Google Scholar 

  10. Estes, J. A. & Palmisano, J. F. Sea otters: their role in structuring nearshore communities. Science 185, 1058–1060 (1974).

    CAS  PubMed  Google Scholar 

  11. Watson, J. & Estes, J. A. Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island. Can. Ecol. Monogr. 81, 215–239 (2011).

    Google Scholar 

  12. Schultz, J. A., Cloutier, R. N. & Côté, I. M. Evidence for a trophic cascade on rocky reefs following sea star mass mortality in British Columbia. PeerJ 4, e1980 (2016).

    PubMed  PubMed Central  Google Scholar 

  13. Burt, J. M. et al. Sudden collapse of a mesopredator reveals its complementary role in mediating rocky reef regime shifts. Proc. R. Soc. B. 285, 20180553 (2018).

    PubMed  PubMed Central  Google Scholar 

  14. Harvell, C. D. et al. Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator (Pycnopodia helianthoides). Sci. Adv. 5, eaau7042 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Bond, N. A., Cronin, M. F., Freeland, H. & Mantua, N. Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophys. Res. Lett. 42, 3414–3420 (2015).

    Google Scholar 

  16. Gentemann, C. L., Fewings, M. R. & García‐Reyes, M. Satellite sea surface temperatures along the West Coast of the United States during the 2014–2016 northeast Pacific marine heat wave. Geophys. Res. Lett. 44, 312–319 (2017).

    Google Scholar 

  17. Hobday, A. et al. Categorizing and naming marine heatwaves. Oceanography 31, 162–173 (2018).

    Google Scholar 

  18. Weitzman, B. et al. Changes in rocky intertidal community structure during a marine heatwave in the Northern Gulf of Alaska. Front. Mar. Sci. 8, 556820 (2021).

    Google Scholar 

  19. Suryan, R. M. et al. Ecosystem response persists after a prolonged marine heatwave. Sci. Rep. 11, 6235 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Magel, C. L., Chan, F., Hessing-Lewis, M. & Hacker, S. D. Differential responses of eelgrass and macroalgae in Pacific Northwest estuaries following an unprecedented NE Pacific Ocean marine heatwave. Front. Mar. Sci. 9, 16 (2022).

    Google Scholar 

  21. Spiecker, B. J. & Menge, B. A. El Niño and marine heatwaves: ecological impacts on Oregon rocky intertidal kelp communities at local to regional scales. Ecol. Monogr. 92, e1504 (2022).

  22. Whalen, M. A., Starko, S., Lindstrom, S. C. & Martone, P. T. Heatwave restructures marine intertidal communities across a stress gradient. Ecology 104, e4027 (2023).

    PubMed  Google Scholar 

  23. Cavole, L. et al. Biological Impacts of the 2013–2015 warm-water anomaly in the Northeast Pacific: winners, losers, and the future. Oceanography 29, 273–285 (2016).

    Google Scholar 

  24. Miner, C. M. et al. Large-scale impacts of sea star wasting disease (SSWD) on intertidal sea stars and implications for recovery. PLoS ONE 13, e0192870 (2018).

    PubMed  PubMed Central  Google Scholar 

  25. Menge, B. A. et al. Sea star wasting disease in the keystone predator Pisaster ochraceus in Oregon: insights into differential population impacts, recovery, predation rate, and temperature effects from long-term research. PLoS ONE 11, e0153994 (2016).

    PubMed  PubMed Central  Google Scholar 

  26. Konar, B. et al. Wasting disease and static environmental variables drive sea star assemblages in the Northern Gulf of Alaska. J. Exp. Mar. Biol. Ecol. 520, 151209 (2019).

    Google Scholar 

  27. Paine, R. T. Food web complexity and species diversity. Am. Nat. 100, 65–75 (1966).

    Google Scholar 

  28. Menge, B. A. et al. Keystone predation: trait‐based or driven by extrinsic processes? Assessment using a comparative-experimental approach. Ecol. Monogr. 91, e01436 (2021).

    Google Scholar 

  29. Paine, R. T. Size-limited predation: an observational and experimental approach with the MytilusPisaster interaction. Ecology 57, 858–873 (1976).

    Google Scholar 

  30. Moritsch, M. M. Expansion of intertidal mussel beds following disease-driven reduction of a keystone predator. Mar. Environ. Res. 169, 105363 (2021).

    CAS  PubMed  Google Scholar 

  31. Hacker, S. D., Menge, B. A., Nielsen, K. J., Chan, F. & Gouhier, T. C. Regional processes are stronger determinants of rocky intertidal community dynamics than local biotic interactions. Ecology 100, e02763 (2019).

    PubMed  Google Scholar 

  32. Eisenlord, M. E. et al. Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Philos. Trans. R. Soc. B 371, 20150212 (2016).

    Google Scholar 

  33. Menge, B. A. et al. Stasis or kinesis? Hidden dynamics of a rocky intertidal macrophyte mosaic revealed by a spatially explicit approach. J. Exp. Mar. Biol. Ecol. 314, 3–39 (2005).

    Google Scholar 

  34. Menge, B. A., Gouhier, T. C., Hacker, S. D., Chan, F. & Nielsen, K. J. Are meta-ecosystems organized hierarchically? A model and test in rocky intertidal habitats. Ecol. Monogr. 85, 213–233 (2015).

    Google Scholar 

  35. Traiger, S. B. et al. Evidence of increased mussel abundance related to the Pacific marine heatwave and sea star wasting. Mar. Ecol. 43, e12715 (2022).

    CAS  Google Scholar 

  36. Menge, B. A., Gravem, S. A., Johnson, A., Robinson, J. W. & Poirson, B. N. Increasing instability of a rocky intertidal meta-ecosystem. Proc. Natl Acad. Sci. USA 119, e2114257119 (2022).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Sanford, E. D. & Menge, B. A. Reproductive output and consistency of source populations in the sea star Pisaster ochraceus. Mar. Ecol. Prog. Ser. 349, 1–12 (2007).

    Google Scholar 

  38. Lüning, K. & Freshwater, W. Temperature tolerance of Northeast Pacific marine algae. J. Phycol. 24, 310–315 (1988).

    Google Scholar 

  39. Barner, A. K., Hacker, S. D., Menge, B. A. & Nielsen, K. J. The complex net effect of reciprocal interactions and recruitment facilitation maintains an intertidal kelp community. J. Ecol. 104, 33–43 (2016).

    Google Scholar 

  40. Paine, R. T. & Trimble, A. C. Abrupt community change on a rocky shore—biological mechanisms contributing to the potential formation of an alternative state. Ecol. Lett. 7, 441–445 (2004).

    Google Scholar 

  41. Beisner, B., Haydon, D. & Cuddington, K. Alternative stable states in ecology. Front. Ecol. Environ. 1, 376–382 (2003).

    Google Scholar 

  42. Benedetti-Cecchi, L., Tamburello, L., Maggi, E. & Bulleri, F. Experimental perturbations modify the performance of early warning indicators of regime shift. Curr. Biol. 25, 1867–1872 (2015).

    CAS  PubMed  Google Scholar 

  43. Estes, J. A. et al. Trophic downgrading of Planet Earth. Science 333, 301–306 (2011).

    CAS  PubMed  Google Scholar 

  44. Hobbs, R. J., Higgs, E. & Harris, J. A. Novel ecosystems: implications for conservation and restoration. Trends Ecol. Evol. 24, 599–605 (2009).

    PubMed  Google Scholar 

  45. Menge, B. A. & Menge, D. N. L. Dynamics of coastal meta-ecosystems: the intermittent upwelling hypothesis and a test in rocky intertidal regions. Ecol. Monogr. 83, 283–310 (2013).

    Google Scholar 

  46. Jacox, M. G., Edwards, C. A., Hazen, E. L. & Bograd, S. J. Coastal upwelling revisited: Ekman, Bakun, and improved upwelling indices for the U.S. West Coast. J. Geophys. Res. Oceans 123, 7332–7350 (2018).

    Google Scholar 

  47. Schlegel R. W. & Smit A. J. heatwaveR: a central algorithm for the detection of heatwaves and cold-spells. R package version 0.4.6 (R Project, 2018).

  48. Hobday, A. J. et al. A hierarchical approach to defining marine heatwaves. Prog. Oceanogr. 141, 227–238 (2016).

    Google Scholar 

  49. Thomsen, M. S. et al. Local extinction of bull kelp (Durvillaea spp.) due to a marine heatwave. Front. Mar. Sci. 6, 84 (2019).

    Google Scholar 

  50. Filbee-Dexter, K. et al. Marine heatwaves and the collapse of marginal North Atlantic kelp forests. Sci. Rep. 10, 13388 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Oksanen et al. vegan: community ecology package. R package version 2.6-2 (R Project, 2022).

  52. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M. & Hornik, K. cluster: cluster analysis basics and extensions. R package version 2.1.4 (R Project, 2022).

  53. De Caceres, M. & Legendre, P. indicspecies: relationship between species and groups of sites. R package version 1.7.12 (R Project, 2022).

  54. Smith, R. J. Solutions for loss of information in high-beta-diversity community data. Methods Ecol. Evol. 8, 68–74 (2017).

    Google Scholar 

  55. Arribas, L. P., Donnarumma, L., Palomo, M. G. & Scrosati, R. A. Intertidal mussels as ecosystem engineers: their associated invertebrate biodiversity under contrasting wave exposures. Mar. Biodiv. 44, 203–211 (2014).

    Google Scholar 

  56. Elsberry, L. & Bracken, M. Functional redundancy buffers mobile invertebrates against the loss of foundation species on rocky shores. Mar. Ecol. Prog. Ser. 673, 43–54 (2021).

    Google Scholar 

  57. Legendre, P. in Encyclopedia of Biodiversity 264–268 (Elsevier, 2013).

  58. McCune, B. & Grace, J. B. Analysis of Ecological Communities (MjM Software, 2002).

  59. Holling, C. S. Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4, 1–23 (1973).

    Google Scholar 

  60. Aarts E. mHMMbayes: multilevel hidden Markov models using Bayesian estimation. R package version 0.2.0 (R Project, 2022).

  61. Zucchini, W., MacDonald, I. L. & Langrock, R. Hidden Markov Models for Time Series: An Introduction Using R. (CRC Press, 2016).

  62. McClintock, B. T. et al. Uncovering ecological state dynamics with hidden Markov models. Ecol. Lett. 23, 1878–1903 (2020).

    PubMed  PubMed Central  Google Scholar 

  63. Glennie, R. et al. Hidden Markov models: pitfalls and opportunities in ecology. Methods Ecol. Evol. 14, 43–56 (2023).

    Google Scholar 

  64. Gal, G. & Anderson, W. A novel approach to detecting a regime shift in a lake ecosystem. Methods Ecol. Evol. 1, 45–52 (2010).

    Google Scholar 

  65. Gennaretti, F., Arseneault, D., Nicault, A., Perreault, L. & Bégin, Y. Volcano-induced regime shifts in millennial tree-ring chronologies from northeastern North America. Proc. Natl Acad. Sci. USA 111, 10077–10082 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank J. Aerni, R. Askerooth, A. Barner, D. Chabot, A. Chiachi, M. Feezell, L. Field, H. Fulton-Bennett, S. Gerrity, T. Kruss, K. Matthews, B. Meunier, L. Miksell, S. Ngo, K. Nielsen, J. Robinson and E. Van Belle for field assistance. The raw temperature data were processed by M. Frenock and R. Gaddam. Most California measurements of Pisaster ochraceus size were provided by the Multi-Agency Rocky Intertidal Network (MARINe), a long-term ecological consortium funded and supported by many groups. This work was supported by National Science Foundation grants to B.A.M., S.D.H. and colleagues. Z.D.M. received fellowship and grant support from the National Science Foundation, Oregon State University and the Phycological Society of America. This is contribution number 535 from PISCO (http://www.piscoweb.org/).

Author information

Authors and Affiliations

Authors

Contributions

S.D.H. and B.A.M. designed the study. All authors conducted the field experiment. Z.D.M. performed quality assurance on the datasets, analysed the data, created figures and tables and drafted the initial paper. All authors interpreted the results and revised the paper.

Corresponding author

Correspondence to Zechariah D. Meunier.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Ecology & Evolution thanks Luca Rindi, J. Wootton and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

Extended Data Fig. 1 Experimental plots and locations of rocky intertidal sites on the coasts of Oregon and northern California.

Permanent plots (n = 260) were established in the low intertidal zone and assigned to control, recovery, macrophyte-only or invertebrate-only treatments in five replicate blocks per site. a, Replicate block showing control treatment (blue outline) and the recovery, macrophyte-only and invertebrate-only treatments (cleared areas) during experimental set up at the northernmost site in May 2006. Control treatments were never manipulated, recovery treatments recolonized naturally following initial organism removal, macrophyte-only treatments had annual removals of sessile invertebrates, and invertebrate-only treatments had annual removals of macroalgae and surfgrasses. b, Map of 13 rocky intertidal sites grouped into regions on four capes. c-f, Examples of kelp-dominated and mussel-dominated alternative states observed in one representative recovery treatment plot at the southernmost site in July 2009 (c), July 2014 (d), June 2018 (e) and June 2022 (f). As in f, mussels in every plot dominated by mussels in 2022 were measured and then marked with red pastel to avoid repeat measurement.

Extended Data Fig. 2 Intertidal water temperature anomalies (mean ± s.e.m.) from 2006 to 2020.

Daily anomalies were calculated as the difference between the daily temperature per cape (n = 5,375 d for Cape Foulweather, 5,376 d for Cape Perpetua, 5,392 d for Cape Blanco and 4,936 d for Cape Mendocino) and the long-term climatology per cape. Daily anomalies were then averaged within year and cape. Positive anomalies indicate warmer than average temperatures, while negative anomalies indicate colder than average temperatures.

Source data

Extended Data Fig. 3 Indicators of Pisaster ochraceus populations from 2006 to 2020.

Data were collected in annual or semiannual surveys during spring (earlier point) or summer (later point) per year. a, Sea star wasting disease (SSWD) prevalence (mean ± s.e.m.) was calculated as the per cent of diseased or recovering individuals in the population (n = 44,586 Pisaster). b, Density (mean ± s.e.m.) was calculated as the number of individuals that occurred within belt transects of known area (n = 42,306 Pisaster). c, Diameter (mean ± s.e.m.) was calculated from center length or madreporite length (n = 43,696 Pisaster).

Source data

Extended Data Fig. 4 Posterior distributions for the community state emission probabilities on Cape Foulweather.

Group-level posterior densities for alternative states 1 and 2 in the control (a,b), recovery (c,d), macrophyte-only (e,f) and invertebrate-only (g,h) treatments. Group-level densities are the means of 15 experimental plot densities.

Source data

Extended Data Fig. 5 Posterior distributions for the community state emission probabilities on Cape Perpetua.

Group-level posterior densities for alternative states 1 and 2 in the control (a,b), recovery (c,d), macrophyte-only (e,f) and invertebrate-only (g,h) treatments. Group-level densities are the means of 15 experimental plot densities.

Source data

Extended Data Fig. 6 Posterior distributions for the community state emission probabilities on Cape Blanco.

Group-level posterior densities for alternative states 1 and 2 in the control (a,b), recovery (c,d), macrophyte-only (e,f) and invertebrate-only (g,h) treatments. Group-level densities are the means of 20 experimental plot densities.

Source data

Extended Data Fig. 7 Posterior distributions for the community state emission probabilities on Cape Mendocino.

Group-level posterior densities for alternative states 1 and 2 in the control (a,b), recovery (c,d), macrophyte-only (e,f) and invertebrate-only (g,h) treatments. Group-level densities are the means of 15 experimental plot densities.

Source data

Extended Data Table 1 Results of indicator species analysis showing the functional groups that are strongly associated with the community states
Extended Data Table 2 Results of hidden Markov models with 2 or 3 hidden states
Extended Data Table 3 Results of one-sided paired t-tests for Bray-Curtis similarities per plot

Supplementary information

Supplementary Information

Supplementary Tables 1–8 and Figs. 1–21.

Reporting Summary

Peer Review File

Source data

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Meunier, Z.D., Hacker, S.D. & Menge, B.A. Regime shifts in rocky intertidal communities associated with a marine heatwave and disease outbreak. Nat Ecol Evol 8, 1285–1297 (2024). https://doi.org/10.1038/s41559-024-02425-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-024-02425-5

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing