Ecology News: Sea Star Collapse Linked to Disease and Heat Wave

This essay examines the continental-scale collapse of the sunflower sea star (Pycnopodia helianthoides) due to sea star wasting disease (SSWD) and its association with a marine heat wave in the Northeast Pacific. The study uses data from deep offshore trawl surveys and shallow nearshore diver surveys to demonstrate a significant decline in sea star populations across a vast geographic range. The research identifies a correlation between the timing of peak declines and anomalously warm sea surface temperatures, suggesting that increased temperatures exacerbate the effects of SSWD. The collapse of this keystone predator has triggered trophic cascades, leading to urchin population explosions and kelp forest degradation, highlighting the far-reaching ecological consequences of this marine epidemic. Desklib offers a variety of study tools and resources, including similar essays and solved assignments for students.

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Disease epidemic and a marine heat wave are
associated with the continental-scale collapse of a
pivotalpredator (Pycnopodia helianthoides)
C. D. Harvell1*†, D. Montecino-Latorre2*, J. M. Caldwell3, J. M. Burt4,5
, K. Bosley6, A. Keller7,
S. F. Heron8,9,10
, A. K. Salomon4,5
, L. Lee4,5
, O. Pontier5, C. Pattengill-Semmens11, J. K. Gaydos12
Multihost infectious disease outbreaks have endangered wildlife, causing extinction of frogs and endemic birds,
and widespread declines of bats, corals, and abalone. Since 2013, a sea star wasting disease has affected >20 sea
star species from Mexico to Alaska. The common, predatory sunflower star (Pycnopodia helianthoides), shown to
be highly susceptible to sea star wasting disease,has been extirpated across most of its range.Diver surveys
conducted in shallow nearshore waters (n = 10,956;2006–2017) from California to Alaska and deep offshore
(55 to 1280 m) trawl surveys from California to Washington (n = 8968;2004–2016) reveal 80 to 100% declines
across a ~3000-km range. Furthermore, timing of peak declines in nearshore waters coincided with anomalously
warm sea surface temperatures. The rapid, widespread decline of this pivotal subtidal predator threatens its per-
sistence and may have large ecosystem-level consequences.
INTRODUCTION
Host-pathogen theory predicts that multihost pathogens can cause ex-
treme population impacts, including extinction of susceptible species
if they are continuously infected from reservoir species (1, 2). For ex-
ample,introduced multihost pathogens such as avian malaria and
avian pox have driven multiple native Hawaiian bird species to extinc-
tion (3). Similarly, the Batrachochytrium dendrobatidis pandemic may
have caused hundreds of species extinctions worldwide and decimated
more than 38 amphibian species in Central America (4, 5). In another
example, spillover of shared pathogens from domesticated bees to wild
bumblebees (e.g., deformed wing virus and Nosema ceranae) is driving
declines in the wild populations (6).These pathogen-associated im-
pacts are further exacerbated in a changing climate (7–9).
Since 2013,sea star wasting disease (SSWD) has caused massive,
ongoing mortality from Mexico to Alaska (known as the Northeast
Pacific SSWD event). In particular, the epidemic phase of the North-
east Pacific SSWD event (2013–2015) was notably different from pre-
vious events elsewhere in terms of its geographic extent,persistence,
involvement of multiple species, symptoms in reproductive stars, and
the extremely rapid progression of disease to death (10–15). More than
20 asteroid species have been affected in what is currently the largest
documented epizootic of a noncommercial marine taxon (13, 14, 16).
Diseased sea stars develop progressively worse dermal lesion
arms detach from the central disc, gonads spilled from fully re
tive stars and individuals die, often leaving white piles of ossi
disconnected limbs (fig. S1). Sea star mortalities during the fi
of the Northeast Pacific SSWD event (2013–2015) were linked
star–associated densovirus (SSaDV; family Parvoviridae), base
tagenomic analysis of bacteria and viruses in field samples, th
mental generation of disease in sea stars challenged with non
viral-sized material,the correlation between SSWD progression an
SSaDV loads,and higher SSaDV prevalence in symptomatic star
(13).Further support for densovirus involvement in the Northe
Pacific SSWD event includes experimental infection and morb
in Pycnopodia helianthoides (17), the relationship between as
densovirus load and SSWD in P.helianthoides,and experimental
transmission of SSWD disease to asymptomatic individuals th
exposure to a viral-sized agent (0.22 mm) from SSWD sympto
stars (17, 18).
While the Northeast Pacific SSWD event caused severe red
tions of the keystone intertidal ochre sea star across its entire
coast range (14, 15, 19–21), the impacts on subtidal species a
well known.Because it was the most abundant subtidalstar and
also the most susceptible in early reports, initial studies quan
devastating declines of P. helianthoides, in Washington and B
Columbia, linked with high prevalence of wasting disease (22
but these observations are limited to the initial years, specific
and shallow depths accessible to divers. Hence, the current st
P. helianthoides in the Northeast Pacific and at alldepths is un-
known. This species is an important predator of sea urchins, a
chin populations released from top-down predatory controlcan
expand and threaten kelp forests and biodiversity (24, 25). In
locations, P. helianthoides is the apex subtidal predator when
urchin predators are absent (22, 26). In these locations, its de
triggered a trophic cascade, causing urchin populations to exp
kelp to rapidly diminish (22).If P. helianthoides reductions occur
throughout its range at the magnitude reported in local surve
at greater depths, this disease could not only threaten the lon
persistence of this species but also have wide-ranging cascad
system effects.
1Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY
14853,USA.2One Health Institute,School of Veterinary Medicine,University of
California,Davis,CA 95616,USA. 3Department of Biology,Stanford University,
Stanford,CA 94040,USA.4School of Resource and Environmental Management,
Simon Fraser University,Burnaby,BC V5A 1S6,Canada.5HakaiInstitute,Heriot
Bay,BC V0P 1H0,Canada.6Fishery Resource Analysis and Monitoring Division,
Northwest Fisheries Science Center,NationalMarine Fisheries Service,National
Oceanic and Atmospheric Administration (NOAA),2032 SE OSU Drive,Newport,
OR 97365,USA.7Fishery Resource Analysis and Monitoring Division,Northwest
Fisheries Science Center, National Marine Fisheries Service, NOAA, 2725 Montlake
Boulevard East,Seattle,WA 98112,USA.8NOAA CoralReef Watch,College Park,
MD 20740,USA.9ReefSense Pty Ltd.,Townsville,Queensland,Australia.10
Marine
Geophysical Laboratory, Physics, College of Science and Technology, James Cook
University,Townsville,Queensland,Australia.11Reef EnvironmentalEducation
Foundation (REEF),Key Largo,FL 33037,USA.12The SeaDoc Society,Karen C.
Drayer Wildlife Health Center–Orcas Island Office,University of California,Davis,
942 Deer Harbor Road,Eastsound,WA 98245,USA.
*These authors contributed equally to the work and supervision of the project.
†Corresponding author.Email:[e-mail]
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Increasingly warm or anomalous temperatures are being shown
to influence the prevalence and severity of marine infectious diseases
[e.g., (8)]. Experimental and field studies support a role for tempera-
ture in SSWD morbidity. Current evidence suggests that at warmer
temperatures, Pisaster ochraceus have a higher risk of infection and
progression to mortality (10, 14, 15, 27). If this relationship applies to
other sea star species, then we expect that declines of P. helianthoides
populations will be associated with warmer temperature exposure.
Here, we investigated the current status of P. helianthoides in both
shallow nearshore and deep offshore waters, from California to British
Columbia (~3000 km), using data from over a decade of complemen-
tary survey methods that cover from pre- to post-outbreak periods
of the Northeast Pacific SSWD event. We report the rapid collapse of
P. helianthoides populations along most of its range after the onset of
the Northeast Pacific SSWD event, and at all depths, confirming the
lack of a deep-water refuge for this species. Furthermore, to explore
the hypothesis that warmer waters may be linked to the decline, we
assessed the relationship between P.helianthoides abundance in
shallow nearshore waters and sea surface temperature (SST). We de-
tected a negative association between P.helianthoides abundance
and anomalously warm SST.Potentialecosystem impacts of this
decimation are discussed.
RESULTS
To assess P.helianthoides decline in deep offshore waters,we esti-
mated the average yearly biomass (kg/10 ha) collected in 8968 bottom
trawls (55 to 1280 m depth) conducted from California to Washington
between 2004 and 2016. Deep-water trawl surveys showed fluctuat-
ing but constant P.helianthoides biomass up to 2011–2012 and an
unprecedented decline after the onset of the Northeast Pacific SSWD
event. In California and Oregon, the average biomass decreased 100%
during 2013–2015 (from 2.78 and 1.73 kg/10 ha,respectively).In
Washington, average biomass declined 99.2% (from 3.11 to 0.02 kg/10 ha)
during this period. In 2016, no P. helianthoides were collected across
the 1264-ha area covered by 692 trawl surveys. The collapse in biomass
collection occurred 1 year earlier in California compared with other
regions (2014; Fig. 1).
To quantify the impact of the Northeast Pacific SSWD event on
P. helianthoides in shallow nearshore waters,we analyzed changes
in abundance reported in 10,956 roving-diver surveys conducted be-
tween 2006 and 2017 from California to Alaska (sparse survey cov-
erage for Alaska not plotted).Abundance categories (ACs;0 to 4
corresponding to 0,1,2 to 10,11 to 100,and >100 individuals,re-
spectively) were analyzed within regional jurisdictions as an annual
abundance score (28). Furthermore, we report nearshore biomass of
P. helianthoides (kg/10 m2
) along the coast of central British Columbia
using annual subtidal belt transect surveys conducted between 3 and
18 m depth in 2010–2011 and again between 2013 and 2017.
In the years before the Northeast Pacific SSWD event onset, ACs
2 (2 to 10 stars) and 3 (11 to 100 stars) were the most commonly
reported (64 to 80% of the reports),but since 2014 (after the epi-
demic onset), at least 60% of surveys across the study area and up to
100% in California and Oregon report declines to ACs 0 and 1 (Fig. 2).
Belt transect surveys in central British Columbia also showed that
P. helianthoides biomass declined by ~96% (from 0.57 to 0.93 kg/10 m2
in 2010–2014,pre-Northeast Pacific SSWD event) to virtually zero
(0.01 to 0.07 kg/10 m2) in 2015–2017. The abundance score from the
shallow nearshore waters surveys revealed fluctuating but regionally
constant P.helianthoides abundance during 2006–2013 and a c
sistent continental-wide decline after the onset of the Northea
cific SSWD event (Fig. 2).
To assess the relationship between P. helianthoides decline
low nearshore waters and SST, we modeled the ACs reported
species in the roving-diver surveys as a function of a satellite
SST anomaly metric and days since the SST metric was obser
tween 2013 and 2015, SST anomalies (departures from the cl
gically expected temperature calculated from 1985 to 2012) w
warm at all locations,but their magnitude and duration varied wit
latitude (Fig. 3). In California, 2014 was anomalously warm, in
ing to extreme warming throughout 2015 with a peak anomal
In Washington, 2013 was anomalously warm during July to Oc
but otherwise followed the seasonal climatology. In July 2014,
longed warm anomaly began, increasing to an extreme 2.5°C
through 2015, coinciding with the long residence of the heat w
the northeast Pacific Ocean (29). Central British Columbia foll
similar pattern seen in Washington, with the arrival of the ano
ly warm waters in the fall of 2015 (30). Oregon was more vari
other locations, likely because of periodic cold upwelling even
On the basis of ordinal regression models of P. helianthoide
dance and biologically relevant SST anomaly metrics,we provide
evidence that P. helianthoides declines in shallow nearshore w
were associated with the maximum temperature anomaly exp
from within 60 days before each survey (tables S1 and S2).Our
selected model indicates that with every 1°C increase in the m
mum temperature anomaly,we would expect a 6% increase in the
log odds of observing a low AC compared with all higher ACs (
versus 1 to 4, AC 1 versus 2 to 4, etc.), when all other variable
held constant (table S2). We evaluated the goodness of fit be
the modeland data using Nagelkerke’s pseudo R2 (31) and esti-
mated that our model explained 68.5% of the variance in sea
ACs compared to a null model. To investigate the role of the m
imum temperature anomaly exposure from within 60 days be
the survey, we also calculated a pseudo R2 for a model that included
all covariates other than this variable. This model explained 3
of the variance in P.helianthoides ACs,suggesting that this SST
anomaly metric alone explains ~38% of the variance.
DISCUSSION
Using longitudinal data from complementary survey methods
(i) consistent or slightly increasing populations of P.helianthoides
across most of its natural range in the decade before the Nort
Pacific SSWD event in shallow nearshore waters; (ii) consisten
lations of P. helianthoides across most of its natural range in t
ade before the Northeast Pacific SSWD event in deep offshore
(iii) a continental-scale collapse of this major ocean predator i
habitats associated temporally and spatially to the Northeast
SSWD event and, therefore, to the multihost SSaDV; and (iv)
sociation between P.helianthoides declines in shallow nearshore
waters and period of anomalously warm nearshore waters.
Our statistical analysis provides evidence for anomalous te
perature as a key facilitator of the disease-related declines in
low nearshore waters, explaining more than a third of the var
itself. These results align with field and experimental evidenc
interacting roles of temperature and SSWD in P. ochraceus m
ity and mortality, where infected stars exposed to warmer tem
tures died at a faster rate (10, 14, 15, 27). Previous studies su
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high water temperatures are associated with lower coelomic fluid vo-
lumes, higher metabolic demands, and metabolic stress in asteroids
(10,32–34),making the case for how a viral epidemic could be ex-
acerbated in an invertebrate with a limited immune response capabil-
ity (35). Although warming waters likely accelerated and increased the
scale of disease-induced morbidity,P. helianthoides mortality still
occurred at high levels in colder temperatures of British Columbia.
This finding supports a facilitating role of anomalously warm tem-
perature for disease morbidity as previously reported in intertidal
P. ochraceus during the Northeast Pacific SSWD event (15).
Our data document the widespread decline of P. helianthoides at
depths beyond shallow nearshore waters,confirming the lack of a
deep-water refuge for this species.Available data support that the
Northeast Pacific SSWD event is the most parsimonious expla
for this collapse. This species was identified as the most susce
SSWD (13, 14), the observed widespread declines occurred ri
the onset of this event, and they followed the timing and spat
tern of the declines observed in nearshore P. helianthoides po
tions and intertidalP. ochraceus populations (15).Moreover,
necrotic stars with autotomizing arms were observed by one o
coauthors (K. Bosley) in the trawls at the initiation of the Nort
Pacific SSWD event. The limitations of deep offshore water te
ture data prevented an analysis of the role of water temperat
exacerbating P. helianthoides declines at deep offshore water
Fig. 1.Continental collapse of a pivotal predator: Deep offshore surveys. Mean biomass of sunflower star in 8968 deep offshore trawls (55 to 1280
(B) Oregon, and (C) California from 2004 to 2016 with 95% confidence interval in light blue. Gray line marks the year 2013 for comparison of SSWD
Yellow circles depict the 2013–2016 trawl locations.The trawls per jurisdiction per year are shown in the top of each plot.
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Fig. 2. Continental collapse of a pivotal predator:Shallow nearshore surveys.(A to D) Percentage of shallow nearshore ACs of sunflower star (P.helianthoides)
reported in roving-diver surveys from southern California to southern British Columbia,Canada,from 2006 to 2017 (blue scale bars,right axis).Black line,annual
abundance score (left axis);red line,annualmean of the maximum temperature anomaly 60 days before each survey (whiskers,95% confidence interval;left axis).
(A) British Columbia.(B) Washington.(C) Oregon.(D) California.(E) Mean biomass (kg/10 m2) in belt transect surveys in central British Columbia,with 95% confidence
interval in light blue. Yellow circles depict the 2013–2017 locations. The red rectangle depicts the area where the belt transect surveys were condu
jurisdiction per year are shown in the top of each plot.For other details,see Fig.1.
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information is collected once annually. However, new findings
that anomalous warm temperatures associated with recent m
heat waves were broadly detected at about 140 m depth in th
east Pacific beginning in mid-2014 (36), which may have cont
to SSWD morbidity at these depths.
The abrupt decline of P. helianthoides after the onset of the
east Pacific SSWD event occurred in shallow and deep waters
less of the abundance before the collapse. Similarly, Miner et
did not detect a relationship between the degree of populatio
and pre-outbreak intertidal P. ochraceus density. The current
tion status of P.helianthoides raises important questions about t
potential for recovery and persistence of this species.With SSWD,
reservoir species could be a continuous source of SSaDV to re
P. helianthoides given that asymptomatic star species within
of P.helianthoides have tested positive for SSaDV genetic mat
(17).In its current status and with new bouts of mortality recor
by divers in August 2018, continuous infection from reservoir
tions or small stochastic disturbances could cause the restrict
nant populations of P. helianthoides to vanish (1, 2, 37, 38).
Cascading effects of the P. helianthoides loss are expected
its range and will likely change the shallow water seascape in
locations and threaten biodiversity through the indirect loss o
(22, 25, 26, 39). P. helianthoides was the highest biomass sub
teroid across most of its range before the Northeast Pacific SS
event (39). Loss or absence of this major predator has already
associated with elevated densities of green (Strongylocentrot
droebachiensis), red (Mesocentrotus franciscanus), and purple
ins (Strongylocentrotus purpuratus) across their range (22, 23
even in regions with multiple urchin predators (40). Associate
ductions have been reported following the outbreak (22, 39).
from other widespread marine diseases—the near extirpation
tertidal sea star Heliaster kubiniji from Gulf of California (40),
mortality of the urchin Diadema antillarum from Caribbean re
and the withering syndrome–influenced endangerment of mu
California abalone species (42)—demonstrate how the loss of
can drive community effects that influence marine ecosystem
SSWD, the anomalously warm water, P. helianthoides decli
subsequent urchin explosions (fig. S2) have been described a
fect storm.” This “storm” could result not only in trophic casca
reduced kelp beds (22) but also in abalone and urchin starvat
We encourage scientific review of P. helianthoides recovery, a
of the probability for endangerment,and,more generally,expanded
surveillance of the consequences stemming from complex int
that emerging infectious diseases and warming ocean temper
have in shaping ecosystems, even in the deep ocean.
MATERIALS AND METHODS
Study area
This study includes data from across the northeast Pacific, en
passing most of the natural range of the endemic sunflower s
P. helianthoides. We analyzed data from shallow nearshore ro
diver surveys collected in California, Oregon, and Washington
and British Columbia (Canada), in addition to deep offshore tr
surveys conducted from California to Washington.
Deep offshore surveys
The National Marine Fisheries Service [National Oceanic and A
spheric Administration (NOAA)] conducted 8968 individual bo
Fig. 3. Ocean temperature anomaly averaged over the roving-diver survey
locations for the three initialyears of the epidemic.Blue,2013;green,2014;
red,2015.BC,British Columbia;WA,Washington;OR,Oregon;CA,California.
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trawls along the coasts of California,Oregon,and Washington be-
tween 2004 and 2016.These bottom trawls quantify the biomass of
P. helianthoides (kg) as well as the total area swept by the trawl (ha).
We estimated the mean kg/10 ha per state per year using bottom
trawls conducted between 55 and 1280 m depth. The 95% confidence
intervals of the yearly means were calculated.
Shallow nearshore surveys
Trained and tested recreational scuba divers searching for P. helianthoides
on the coast of Washington, Oregon, and California (USA) and north-
ern British Columbia (Canada) conducted 10,956 roving-diver surveys
between 2006 and 2017. After the surveys were completed, the abun-
dance of P. helianthoides was ranked between 1 and 4 corresponding
to estimated ACs of 1, 2 to 10, 11 to 100, or >100 individuals sighted,
respectively. This information was submitted to the Reef Environmental
Education Foundation (REEF) Volunteer Fish Survey Project Database
(28). With this information, we calculated P. helianthoides abundance
score as previously explained (23,44) per state and per year.Those
surveys that did not report P. helianthoides presence were assigned 0
abundance (category 0). Furthermore, we calculated the proportion that
each AC, including the category 0, was reported per state and per year. The
surveys were conducted in kelp forest, rock/shale reefs, open ocean, sea
grass beds (Phyllospadix and Zostera spp.),pinnacles,bull kelp beds
(Nereocystis sp.), cobblestone/boulder fields, and walls over 10 feet high.
The abundance and size of P. helianthoides were recorded on an-
nual scuba surveys using belt transects at 11 rocky reef sites located
on the central coast of British Columbia between 2010 and 2017 (3 to
15 m depth).Belt transects (30 m × 2 m,n = 6 per site) were con-
ducted at all 11 sites in 2013–2017, whereas 8 and 4 sites were sur-
veyed in 2011 and 2010, respectively (belt transects, 10 m × 2 m; n = 3
to 9 per site). P. helianthoides biomass was calculated using a length-
to-biomass regression (45) and summed across transects at a site to
yield kg/10 m2. P. helianthoides biomass for the central coast region
(range from 51°24.612′N to 52°4.242′N) was calculated as the mean
across all site-year combinations.The 95% confidence intervals of
these yearly means were calculated.
Sea surface temperature
Satellite SST data were obtained at 0.05° (~5 km) daily resolution
from the CoralTemp product by NOAA Coral Reef Watch (NOAA
Coral Reef Watch 2018).Time series of SST were acquired at each
location of the roving-diver surveys or at the nearest neighboring
satellite pixelnear the coastalboundary.SST anomalies describe
the variation in temperature from expected values at a given time
of year and location and were determined using the CoralReef
Watch approach based on monthly climatologies (46).Where SST
is warmer (cooler) than expected, the SST anomaly is positive (neg-
ative).For each survey,maximum values of SST and SST anomaly
from several periods immediately prior were extracted (30,60,90,
180,and 360 days) for comparison with survey data.Jurisdictional
(California, Oregon, Washington, and British Columbia) SST anom-
aly summaries for each year were calculated by spatially averaging
60-day-prior maximum values from survey locations for that year
(Fig.2).JurisdictionalSST and SST anomaly time series (Fig.3
and fig. S3) were averaged across all survey locations.
Statistical analysis
We estimated the relationship between sea star abundance re-
ported in the shallow nearshore roving-diver surveys and SST by
fitting a hierarchicalordinalregression modelwith a probit link
function
PðYi ≤ jÞ ¼ qj b 1ðSSTmetriciÞ b 2ðDays:SSTmetriciÞ
b 313 ðYear20072017iÞ mðLatitudeiÞ
gðMonthiÞ
mðLatitudeiÞe Nð0; s2
mÞ
gðMonthiÞe Nð0; s2
gÞ
i = 1,…,I surveys,
j = 1,…,j−1 abundance categories,
where the cumulative probability of the ith survey falling in th
or below is modeled as a function of the following:qj threshold pa-
rameters across ACs,which provide a separate intercept for each
category j,an SST anomaly metric (SSTmetrici), days since the SST
anomaly metric was observed (Days.SSTmetrici), year (Year2007–2017),
month (Monthi), and latitude (Latitudei). Year was included as a fixed
effect to determine the year when sea star abundances collap
that were statistically significantly different from the 2006 ba
Month and latitude were included as random effects to accoun
ditional variation over time and space. s2mand s2g corresponded to the
variance of the distribution of month and latitude random effe
spectively. Our data met all model assumptions: (i) the respo
was measured on an ordinal scale; (ii) the predictor variables
tinuous or categorical; (iii) there was no multicollinearity amo
tor variables, which we assessed with correlation tests for cor
between two predictors and visually for correlations among th
dictors; and (iv) there were proportional odds between each A
dicated by nearly identical effects among generalized logistic
models comparing each AC split individually (slopes < 2).We fit 10
candidate models that included the year, latitude, and month
and one of the following SST metrics: the maximum SST in th
90, 180, or 360 days prior to each roving diver survey; or the
anomalous SST in the 30, 60, 90, 180, or 360 days prior to ea
diver survey. We compared the AIC value of the candidate mo
and without the covariate “days since the SST metric was obs
then selected the model with the lowest AIC value (tables S1
assessed convergence of models by inspecting the maximum
dient of the log-likelihood function and the magnitude of the H
Each model was empirically identifiable by ensuring that the c
number of the Hessian measure was no larger than 104 (47). We evalu-
ated variance explained by the final model using Nagelkerke’2
(31).Nagelkerke’s pseudo R2 is a commonly used statistic to measur
goodness of fit that is calculated by comparing likelihood ratio
a full model and an intercept model. We conducted this analy
statistical software v3.4.3 (48) using the clmm function of the
package (47) for the ordinal regression model and the nagelk
in the “rcompanion” package to calculate pseudo R2 values (49).
SUPPLEMENTARY MATERIALS
Supplementary materialfor this article is available at http://advances.sciencemag.org/cgi/
content/full/5/1/eaau7042/DC1
Table S1.Summary of results of the candidate hierarchicalordinalregression models.
Table S2.Parameter estimates,SEs,and 95% confidence interval of the selected ordinal model
linking the reporting of ACs 0 to 4 in the shallow nearshore roving-diver surveys and
maximum temperature anomalies from within 60 days before each survey.
Fig.S1.Massive decline of P.helianthoides over 20 days between 9 and 29 October 2013.
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Fig.S2.AnnualSST records during 2013,2014,and 2015 by jurisdiction for British Columbia,
Washington,Oregon,and California.
Fig.S3.Sackinaw Rock before and after development of green urchin barrens following
decimation of P.helianthoides.
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Acknowledgments:We thank REEF surveyors for contributing data.Funding: This work
was supported by the SeaDoc Society,private donors,Seattle Aquarium,NSF RCN
OCE 1215977, NOAA Coral Reef Conservation Program, and Ocean Remote Sensing program.
British Columbia monitoring was funded by an NSERC Discovery,Canadian Foundation
for Innovation,and Tula Foundation grant to A.K.S.as well as NSERC postgraduate and
Hakai fellowships to J.M.B. and L.L. The scientific results and conclusions, as well as any views
or opinions expressed herein,are those of the author(s) and do not necessarily reflect
the views of NOAA or the Department of Commerce.Author contributions: C.D.H., D.M.-L.,
and J.K.G.conceived and planned the paper,with contributions from J.M.C.,S.F.H.,J.M.B.,
A.K.S.,A.K.,and K.B.J.M.C.,S.F.H.,and D.M.-L.conducted statistical analyses with input
from J.M.B.,A.K.S.,and C.D.H.C.D.H.,J.K.G.,D.M.-L.,J.M.C.,S.F.H.,J.M.B.,A.K.S.,A.K.,and K.B.
contributed to writing the paper.J.M.B.,L.L.,O.P.,K.B.,A.K.S.,and C.P.-S.collected data.
Competing interests: The authors declare that they have no competing interests.Data
and materials availability: Supplementary material is available for this paper and includes
a summary of the candidate hierarchical ordinal regression models,a summary of the
final model,and supplementary figures.All data needed to assess the main results in the
paper are in the Figshare repository (DOI:10.6084/m9.figshare.7300409),while the script
to conduct the ordinal regression is located in https://github.com/jms5151/SSWD.
Additional data related to this paper may be requested from the authors.
Submitted 7 July 2018
Accepted 17 December 2018
Published 30 January 2019
10.1126/sciadv.aau7042
Citation:C. D. Harvell,D. Montecino-Latorre,J. M. Caldwell,J. M. Burt,K. Bosley,A. Keller,
S. F. Heron,A. K. Salomon,L. Lee,O. Pontier,C. Pattengill-Semmens,J. K. Gaydos,Disease
epidemic and a marine heat wave are associated with the continental-scale collapse ofa
pivotalpredator (Pycnopodia helianthoides).Sci.Adv.5, eaau7042 (2019).
S C I E N C E A D V A N C E S| R E S E A R C H A R T I C L E
Harvellet al.,Sci.Adv.2019; 5 : eaau704230 January 2019 8 of 8
on February 8, 2019http://advances.sciencemag.org/Downloaded from

)Pycnopodia helianthoidesof a pivotal predator (
Disease epidemic and a marine heat wave are associated with the continental-scale collapse
Pontier, C. Pattengill-Semmens and J. K. Gaydos
C. D. Harvell, D. Montecino-Latorre, J. M. Caldwell, J. M. Burt, K. Bosley, A. Keller, S. F. Heron, A. K. Salomon, L. Lee, O.
DOI: 10.1126/sciadv.aau7042
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