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

Nature Ecology & Evolution volume 8, pages 1285–1297 (2024)Cite this article

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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.

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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.

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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).

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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

  1. Department of Integrative Biology, Oregon State University, Corvallis, OR, USA

    Zechariah D. Meunier, Sally D. Hacker & Bruce A. Menge

Authors
  1. Zechariah D. Meunier
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  2. Sally D. Hacker
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  3. Bruce A. Menge
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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.

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Correspondence to Zechariah D. Meunier.

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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.

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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
Full size table
Extended Data Table 2 Results of hidden Markov models with 2 or 3 hidden states
Full size table
Extended Data Table 3 Results of one-sided paired t-tests for Bray-Curtis similarities per plot
Full size table

Supplementary information

Supplementary Information

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

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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

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