Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens

Abstract

Extreme climatic events have recently impacted marine ecosystems around the world, including foundation species such as corals and kelps. Here, we describe the rapid climate-driven catastrophic shift in 2014 from a previously robust kelp forest to unproductive large scale urchin barrens in northern California. Bull kelp canopy was reduced by >90% along more than 350 km of coastline. Twenty years of kelp ecosystem surveys reveal the timing and magnitude of events, including mass mortalities of sea stars (2013-), intense ocean warming (2014–2017), and sea urchin barrens (2015-). Multiple stressors led to the unprecedented and long-lasting decline of the kelp forest. Kelp deforestation triggered mass (80%) abalone mortality (2017) resulting in the closure in 2018 of the recreational abalone fishery worth an estimated 44Mandthecollapseofthenorthcoastcommercialredseaurchinfishery(2015−)worth44 M and the collapse of the north coast commercial red sea urchin fishery (2015-) worth 3 M. Key questions remain such as the relative roles of ocean warming and sea star disease in the massive purple sea urchin population increase. Science and policy will need to partner to better understand drivers, build climate-resilient fisheries and kelp forest recovery strategies in order to restore essential kelp forest ecosystem services.

Full text

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Marine heat wave and multiple
stressors tip bull kelp forest to sea
urchin barrens
L. Rogers-Bennett* & C. A. Catton
Extreme climatic events have recently impacted marine ecosystems around the world, including
foundation species such as corals and kelps. Here, we describe the rapid climate-driven catastrophic
shift in 2014 from a previously robust kelp forest to unproductive large scale urchin barrens in northern
California. Bull kelp canopy was reduced by >90% along more than 350 km of coastline. Twenty years
of kelp ecosystem surveys reveal the timing and magnitude of events, including mass mortalities of sea
stars (2013-), intense ocean warming (2014–2017), and sea urchin barrens (2015-). Multiple stressors
led to the unprecedented and long-lasting decline of the kelp forest. Kelp deforestation triggered
mass (80%) abalone mortality (2017) resulting in the closure in 2018 of the recreational abalone shery
worth an estimated $44 M and the collapse of the north coast commercial red sea urchin shery (2015-)
worth $3 M. Key questions remain such as the relative roles of ocean warming and sea star disease in
the massive purple sea urchin population increase. Science and policy will need to partner to better
understand drivers, build climate-resilient sheries and kelp forest recovery strategies in order to
restore essential kelp forest ecosystem services.
Rapid environmental changes are threatening critical marine ecosystems around the world1, leading to large-scale
catastrophic ecosystem shis and loss of ecosystem services2. Severe declines in key habitat-forming species, or
ecosystem engineers, such as corals3,4, seagrass5 and kelps6 will be particularly devastating to biodiversity and
productivity. Kelp species are the primary structuring component of highly-productive temperate nearshore
rocky reefs7,8 growing up to 60 cm per day, but are vulnerable to climate change stressors9,10 and may be at risk
worldwide11,12. Historically, kelp forests have occupied 25% of the world’s coastlines13, providing a wide range of
ecosystem services, including both habitat structure and food resources14,15 as well as modifying light levels and
sedimentation16, water ow17, nutrient dynamics18, carbon sequestration19 and physical disturbance20. Dense kelp
beds are biodiversity hot spots, with many kelp-forest obligate species21 as well as species utilizing kelp forests as
critical nursery habitats22, including many economically-important shed species. Kelp forests are resilient to
short-term warming events23, but multiple severe ecological and climatic stressors could tip kelp ecosystems into
an urchin-dominated ecosystem. Sea urchin barrens have multiple feedback loops which could maintain barrens
as an alternative stable state2,24,25. e dynamics of productive, species-rich, macroalgal-dominated kelp forests
are nonlinear and can rapidly transform into unproductive, species-poor urchin-dominated barrens known as a
state or phase shi26–28.
Starting in 2013, the Northeast Pacic Ocean experienced a record-breaking Marine Heat Wave (MHW) that
resulted in well-documented declines of many oshore marine populations and ecosystems, from Baja California
to Alaska. Nutrient-poor, warm water conditions associated with the MHW (2013–2015)29,30 originated in the
Bering Sea, Alaska in 2013 and expanded to the California coast in 2014. Sea surface temperatures 2.5 °C warmer
than normal persisted for 226 days, making this MHW the longest duration ever recorded31. e MHW led to
an unprecedented coast-wide harmful algal bloom which increased concentrations of the neurotoxin domoic
acid, resulting in marine mammal strandings and prolonged shery closures32. Further, unusual mass mortality
and starvation events were observed in oshore birds and mammals (e.g. Tued pun33). Overlapping with the
MHW, the “Godzilla” El Niño (2015–2016) shied geographic distributions of warm-water species poleward34,35,
with unknown impacts to long-term ecosystem community structure and productivity.
Coastal Marine Science Institute, Karen C. Drayer Wildlife Health Center, University of California, Davis, and
California Department of Fish and Wildlife, Bodega Marine Laboratory 2099 Westside Rd., Bodega Bay, CA, 94923-
0247, USA. *email: rogersbennett@ucdavis.edu
OPEN
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Temperate kelp forests in northern California (Fig.1) were particularly vulnerable to the MHW and other
concurrent ecological stressors. is region, which was historically very productive, supported robust sheries
including the recreational red abalone, Haliotis rufescens, shery (valued at $44 M yr−1 36) as well as the commer-
cial red sea urchin, Mesocentrotus franciscanus, shery (valued at $3 M yr−1). e bull kelp forests in this region
(>350 km) were the rst along the west coast of North America to show severe impacts to kelp productivity. e
long-term kelp forest monitoring program was critical for tracking and understanding the biological responses
to these multiple climate-related stressors and resulting degradation of sheries and other ecosystem services37.
Similar impacts seem to be developing in kelp forests from Baja California to Alaska (personal communications),
so that the dynamics described from this northern California case study will be critical for tracking and under-
standing the biological responses to these multiple climate-related stressors and resulting degradation of sheries
and other ecosystem services37.
Here, we document the catastrophic declines in northern California kelp forests during the MHW, and the
subsequent rapid shi of historically persistent kelp ecosystems to wide-spread urchin barrens. We describe the
timing and magnitude of events aecting this critical nearshore region based on long-term monitoring data of
kelp canopy area (1999–2016), subtidal temperature (2006–2018), and extensive scuba-based ecosystem surveys
(1999–2018). We discuss the vulnerability of ecosystem services aecting economic outcomes for the region (e.g.
sheries collapse, loss of tourism), and explore opportunities to enhance resilience38 against climate changes
which are predicted to increase in the future.
Results
e region north of San Francisco to the Oregon border (Fig.1) historically supported extensive, nearly pristine,
productive, and persistent bull kelp, Nereocystis luetkeana, forests39. Human population densities and develop-
ment are low in the region, so no abrupt anthropogenic impacts to ocean conditions and ecosystem health were
anticipated. A series of perturbations40 including a loss of sea star predators of urchins41, prolonged warm-water
conditions, and a population explosion of purple sea urchins occurred prior to and concurrently with an abrupt
shi from bull kelp forest to persistent urchin barrens (Fig.2).
Bull kelp. Bull kelp canopy area declined dramatically in 2014 (Fig.3) throughout the historically-persistent
region of bull kelp forest (>350 km of coastline) in northern California. Maximum historic extent of kelp canopy
(available data: 1999, 2002, 2003, 2004 and 2008) in the region exceeded 50 km2, with a range of 2.4 to 14.9 km2
observed in any given year. Nearly 95% of the historic kelp canopy area was observed in Sonoma and Mendocino
counties, a 250 km region of coastline dominated by contiguous rocky reef habitat. Bull kelp forests continued to
be productive in 2009–2013, growing extensive thick beds throughout Sonoma and Mendocino counties (Fig.2a;
personal observation). In 2014–2016, the kelp canopy area declined to <2 km2, with no appreciable recovery
observed in the core region of the kelp forest in 2017–2019 (personal observation).
Figure 1. Map of study region in northern California. Extent of aerial survey of kelp canopy represented by the
thick black coastline (inset map). Subtidal survey sites in Sonoma and Mendocino counties (main map). Maps
were made using ArcGIS Version 10.6 soware by Esri (http://desktop.arcgis.com).
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Water temperature. e bull kelp decline in 2014 coincided with the onset of the persistent warm water
conditions associated with the MHW30 in northern California (Fig.4a Temperature Time Series). Nutrient-poor
conditions associated with warmer ocean temperatures (>12 °C)42,43 typically appear in fall (September/October),
aer the primary growing season for bull kelp (June - August). In the summer of 2014 through winter of 2015,
daily maximum subtidal nearshore temperatures exceeded 12 °C the majority of days, starting in August (74%)
until February 2015 (93%), reaching a record breaking peak temperature of 17.4 °C on September 24, 2014.
Cooler temperatures prevailed during the spring upwelling season of 2015, until temperatures exceeding 12 °C
again when warm days dominated cool days from July 2015 (65%) to March 2016 (77%). Warmer conditions
developed early again in August 2017 and 2018, but were more variable, and on average cooler, than the 2014–
2016 time period.
Sea stars. Prior to the MHW impacts to the kelp forest in northern California, a mass mortality event of
twenty seastar species, Sea Star Wasting Syndrome (SSWS)41,44,45 decimated local seastar populations from San
Mateo to Mendocino counties, beginning in the summer of 2013. Particularly impacted were populations of the
Sunower star, Pycnopodia helianthoides, an important urchin predator in kelp forest ecosystems. Prior to 2013,
Sunower stars were commonly observed on transect surveys (average population densities 0.01–0.12 stars m2)
(Fig.4b). Within one year of detecting SSWS in the populations, Sunower stars were functionally extinct (only
1 observed in 2014 and 2015). No Sunower stars have been observed at any sites 2016–2019, strongly suggesting
that this species is now locally extinct.
Sea urchin. Purple sea urchin, Strongylocentrotus purpuratus, were historically very low densityin the sub-
tidal (0.0–1.7 urchins m−2) prior to 2014, primarily distributed in small dense patches in the shallows. Populations
of purple urchins began to moderately increase in the fall of 2014, dramatically increasing 60 fold in 2015 (range:
8.2–12.9 urchins m−2) (Fig.4c). Starting in 2015, the purple sea urchins shied to a more aggressive feeding
behavior associated with food limited urchin barren conditions, grazing down stipes of subcanopy kelps and
eshy algae (Fig.2e), then grazing through the calcied crustose coralline algal cover (Fig.2f). Since 2015, purple
urchin densities have continued to increase at most of the sites (2018 range: 9.2–24.1 urchins m−2).
Figure 2. Ecosystem shis observed for kelp forest canopy (top), subcanopy (middle), and benthose (bottom),
pre-impact (a–c) and post-impact (d–f). Photo credit: CDFW (K. Joe (a,c,e); L. Rogers-Bennett (b); C. Catton
(d,f)).
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Abalone. Red abalone populations were historically abundant (range: 0.24–1.01 abalone m−2) and produc-
tive prior to the severe ecosystem shis in 2014 supporting an economically and culturally important shery.
While food-limited conditions progressively worsened aer 2014, red abalone populations started to succumb
to prolonged starvation, and a mass mortality event initiated in 2017 (Fig.4d). Piles of shells were observed in
the subtidal and severely weakened and shrunken abalone were common. Strong winter storms washed abalone
ashore in large numbers, adding to the mass mortality. Population densities decreased at monitoring sites by
48–82% between 2016 and 2017, with additional 43–96% declines observed between 2017 and 2018 (2018 range:
0.01–0.21 abalone m−2).
Discussion
A combination of large-scale environmental and ecological stressors led to dramatically reduced bull kelp canopy
in northern California, starting in 2014. Climate-driven impacts of warm-water, including thermal stress and
nutrient limitation, associated with the MHW suppressed bull kelp growth (and spore production) during the
summer of 2014. ese climate-driven impacts persisted for multiple years, and were exacerbated by a strong
ecological impact of moderate sea urchin herbivory starting in 2014 and becoming intense in 2015-present. From
eld observations during subtidal monitoring work, we know that kelp was abundant prior to the impacts in
2014. e continued low bull kelp abundance aer 2014 is likely due to the combination of unfavorable environ-
mental conditions (warm water and low nutrients), intensive urchin grazing pressure, and limited spore availabil-
ity due to multiple years of low production of this annual species.
Starting in 2014, sea urchin populations began to increase to higher densities than previously observed in the
region. Populations increased at many sites to more than 30 times historic numbers by 2015, and have continued
to increase. Despite widespread starvation conditions, spawning adults of purple urchins have been observed
even at sites devoid of macroalgae, and young of the year (<20 mm) are abundant throughout the region. It is
unknown if there was a primary driver of the urchin population increase, or if both top-down (sea star predation)
and bottom-up recruitment of purple sea urchin processes were responsible. Similarly, the driver(s) of SSWS
which led to the local extinction of the Sunower star is unknown. e rst observations of SSWS in the region
were recorded during cold-water conditions in the summer of 2013, suggesting that this mass mortality was not
initially driven by changes in ocean climate, however warm-water conditions may have later exacerbated the
mortalities44.
Figure 3. Surface kelp canopy area pre- and post-impact from sites in Sonoma and Mendocino counties,
northern California from aerial surveys (2008, 2014–2016). Maps were made using ArcGIS Version 10.6
soware by Esri (http://desktop.arcgis.com).
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e large-scale ecosystem stressors leading to urchin barrens in northern California illustrates the vulnera-
bility of our ecosystems and communities to climate-driven collapses. Many kelp forest ecosystem services have
collapsed on a large scale throughout the region, with particularly severe economic impacts due to collapsed sh-
eries, kelp harvest, tourism opportunities, and loss of cultural resources. e northern California recreational red
abalone shery was the largest in the world, with 35,000 shers landing 245,000 abalone (292 mt) yr−1 36, however
the California and Oregon sheries were closed in 2018 due to abalone mass mortalities. Widespread abalone
starvation and mortality was observed in the wild (Fig.4d). From previous laboratory experiments, we showed
that starvation conditions alone will impact red abalone health and reproduction, which will be exacerbated with
warm water46. Similarly, the commercial red sea urchin shery has collapsed due to starvation conditions leading
to poor gonad production and unmarketable sea urchins. Small remnant kelp patches (<5%) observed since 2014
are not as capable of promoting kelp recruitment as intact kelp forests47. Further, this ecosystem shi to urchin
barrens may persist as sea urchins can thrive in low food conditions on dissolved organics as both larvae48 and
adults49 suggesting urchins barrens could be an alternative stable state.
Even if kelps recover from these multiple stressors, it may take decades before the complex biological com-
munities, associates, and the ecosystem services provided by macroalgal forests (Table1) rebound as has been
Figure 4. Time series of ecosystem stressors and species abundances (2003–2018). (a) Benthic (10 m depth)
temperature in Mendocino County; (b–d):Average population densities observed across four equal depth strata
(0–20 m depth) of Sunower Stars (b), Purple Urchin (c), and Red Abalone (d). Error bars are s.e.m. across the
four depth strata. Image credit: UCSC Ocean Sciences (a); CDFW (A. Maguire (b), K. Sowul (c), K. Joe (d)).
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observed in other parts of the world50–52. While the red sea urchin shery may take only a few months to rebound
aer kelp recovery, red abalone populations have declined so low that population recovery will likely take decades
aer kelp populations recover. A host of economically important non-consumptive recreational opportunities,
including scuba diving, kayaking, and nature photography, may also impact tourism as the broader nearshore
kelp associated community slowly recovers (Table1).
e documented severe loss of kelp in northern California, starting in 2014, is remarkable because of the scale
(>300 km), magnitude (>90%), and speed (within one year) of the impact in an area of historically persistent
kelp forests. e severity of on-going ecological and economic consequences underscores the need to investigate
the climate impacts and interactions of multiple stressors inuencing the vulnerability of ecosystems, even in
regions that are relatively pristine (minimal anthropogenic impacts). Identifying the relative impact of individual
stressors on a natural system is frequently not possible with observational data alone, particularly when multiple
stressors co-occurred or occurred in a rapid sequence. Here, we draw on the long time series of monitoring work
and experience with the system, ecological knowledge and theory for kelp forest ecosystems to elucidate the tim-
ing of the strongest known stressors in the system.
Given the loss of ecosystem services associated with the shi to an unproductive alternative state, it is impor-
tant to understand the perturbations that disrupted the marine ecosystem53 and its ability to rebound from
perturbations (resilience to phase shis)4,54. Identifying the relative importance of factors inuencing climate
vulnerability is the focus of ongoing research and will be critical for informing recovery potential. A plan for bull
kelp recovery in northern California, developed in 2018–2019 with broad scientist and stakeholder input, iden-
ties actionable recovery strategies aimed at enhancing ecological understanding of the drivers that will inform
climate ready restoration actions and build resilience for the future55.
Science-based management action plans must be initiated to bolster resilience in vulnerable and impacted
ecosystems51 as all indications are the urchin barrens will persist. In the future, MHW are predicted to continue56
increasing in frequency and intensity globally31 with the NE Pacic a regional hot-spot34. is threat provides
strong motivation for developing climate-ready action plans to increase ecosystem resilience to major climate
stressors and identify recovery bright spots57,58. Such plans should focus on tracking resilience such as within
favorable microclimates59, enhancing recovery of ecosystem engineers and keystone species, as well as identifying
opportunities for economic incentives to support climate resiliency. For kelp forests in California, solutions may
include developing economic opportunities to reduce urchin grazing pressure by supporting emerging purple
sea urchin restorative sheries and shiing away from sheries being the sole support for ecosystem monitoring.
Climate-ready resource management will require garnering support and building broad partnerships between
science, industry and nonprots, to develop new monitoring and restoration approaches that enhance resilience
of foundational species and their ecosystem services into the future.
Methods
Northern california region. We present monitoring data from the nearshore kelp forest ecosystem at sites
in rocky subtidal habitats in northern California (San Francisco to the Oregon border), with particular focus on
Sonoma and Mendocino counties, from 2003–2018 (Fig.1). Kelp communities in this region are on rocky reefs
dominated by bull kelp, Nereocystis luetkeana (Fig.2a). e understory is comprised of short eshy red and crus-
tose coralline algae as well as subcanopy kelps, such as Pterygophora and Laminaria (Fig.2b). ese subtidal rocky
reefs in northern California support a diverse assemblage of macroalgae and marine invertebrates.
Kelp canopy cover. Total kelp surface canopy area was assessed in 2008, 2014–2016 by aerial surveys from
San Francisco to the Oregon border. Kelp canopy was quantied using low-ying aircra to photographically
survey the nearshore coastline. Cameras were mounted on the aircra to capture the images. Image frames were
auto-georeferenced using customized soware, and manually shied as needed. ERDAS IMAGINE soware was
used to mosaic the frames and run them through classication in ERDAS IMAGINE. Maximum extent of the
Ecosystem Services Goods and Services References
Biodiversity
Enhanced Resilience 11
Feeding Habitat 61
Community Structure 62
Enhanced Microorganisms 63
Fisheries and Aquaculture Finsh, Shellsh, Algae 61,64
Recreational Non-Consumptive Activities Scuba Diving, Kayaking, Photography 65
Economic Source 66
Provisioning
Kelp 67
Dri Kelp Subsidies 68,69
Dissolved Organics 70
Coastal Protection Storm Buer 17
Carbon Sequestration
Oxygen Production 19
Water Quality 71
Fossil Fuel Source 72
Table 1. Ecosystem services provided by kelp forests to nearshore subtidal marine communities.
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kelp forest was determined by overlaying shapeles from all available survey years which include 1999, 2002–
2005, and 2008. Using ArcGIS Version 10.6 soware by Esri, the total area representing kelp on the composite
shape le was quantied in km2. is procedure shows the potential for kelp canopy cover throughout the area as
compared with the extent of canopy cover in a given year. No comparable large-scale kelp aerial survey data exist
for this region from 2009–2013.
Subtidal temperature. Underwater temperature loggers were placed by scuba divers at Van Damme State
Park at 10 m depth inside the kelp forest to monitor subsurface sea water temperatures from August 2003–August
2018. Tidbit temperature loggers made by Onset HOBO recorded temperature once per hour and were retrieved
once a year by divers in August. Note: ere is a gap in August 2004 to October 2005 due to failure of the logger.
ese data are used to detect the magnitude of the temperature and the frequency and duration of exceedance
above 12 °C, an important metric for bull kelp growth as NO3 concentrations are low at this temperature and
warmer42.
Subtidal scuba surveys. e nearshore kelp forest ecosystem monitoring program60 conducts scuba surveys
at sites in rocky subtidal habitats along Sonoma and Mendocino counties in northern California. ese surveys
of the nearshore rocky reefs were initiated in 1999 and allowed for photographic documentation of communi-
ties before and aer multiple stressors impacted the region. Subtidal surveys were conducted by the California
Department of Fish and Wildlife (CDFW) by motor boat at twelve sites along the Sonoma and Mendocino county
coasts. e sites ranged in coastal length from 2.4 to 3.2 km. e sites in Sonoma County from south to north
include: Fort Ross, Timber Cove, Ocean Cove, Salt Point, and Sea Ranch. In Mendocino County the sites from
south to north include: Point Arena, Albion, Van Damme, Russian Gulch, Point Cabrillo (State Marine Reserve),
Caspar Cove and Todd’s Point (Fig.1). e surveys are conducted along band transects 30 × 2 m, located ran-
domly within four depth strata (random stratied) from 1 to 20 m depths. e density estimation for each species
is determined by averaging the densities within each of the four depth strata and then calculating the average
of the four densities from each depth. e error bars represent standard error of the mean densities across four
depth strata. e sites are surveyed to enumerate abalone, sea urchins, sea stars, macro-invertebrate densities as
well as percent cover of algae and substrate type. All size classes observed are recorded. At each site 15–55 tran-
sects were surveyed. Transects were located in areas with >50% rocky reef.
Permissions for protected areas. Underwater surveys were conducted inside two marine protected areas.
Van Damme State Park (State Marine Conservation Area) and Point Cabrillo (State Marine Reserve) with the per-
mission of the California Department of Fish and Wildlife who is the managing authority for Marine Protected
Areas in California.
Data availability
e data that support the ndings of this study are available from the corresponding author upon request.
Received: 11 July 2019; Accepted: 23 September 2019;
Published: xx xx xxxx
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Acknowledgements
We thank the Kelp Forest Ecosystem monitoring team from the California Department of Fish and Wildlife
(CDFW) and the University of California, Davis for their work collecting this time series of ecosystem data.
We thank the CDFW and UCD volunteer divers who contributed to the dive surveys over the past 20 years
especially S. Kawana. We thank CDFW Captains R. Puccinelli, A. Roberts and B. Bailie and their crew for their
support at sea. We thank the kelp mapping and GIS team at CDFW including M. Fredle. We thank T. Ebert and
R. Strathmann for discussions about sea urchin population explosions. e data used in this paper were from a
20 year time series of northern California kelp forest monitoring conducted by the California Department of Fish
and Wildlife for sheries management in collaboration with the University of California, Davis.
Author contributions
Both authors L.R.-B. and C.C. wrote the paper, contributed to data collection and performed the analyses.
Competing interests
e authors declare no competing interests.
Additional information
Correspondence and requests for materials should be addressed to L.R.-B.
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