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Disease epidemic and a marine heat wave are associated with the continental-scale collapse of a pivotal predator ( Pycnopodia helianthoides )

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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 persistence and may have large ecosystem-level consequences.
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Disease epidemic and a marine heat wave are
associated with the continental-scale collapse of a
pivotal predator (Pycnopodia helianthoides)
C. D. Harvell
1
*
, D. Montecino-Latorre
2
*, J. M. Caldwell
3
, J. M. Burt
4,5
, K. Bosley
6
, A. Keller
7
,
S. F. Heron
8,9,10
, A. K. Salomon
4,5
, L. Lee
4,5
, O. Pontier
5
, C. Pattengill-Semmens
11
, J. K. Gaydos
12
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; 20062017) from California to Alaska and deep offshore
(55 to 1280 m) trawl surveys from California to Washington (n= 8968; 20042016) 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 theorypredicts 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)isdriving
declines in the wild populations (6). These pathogen-associated im-
pacts are further exacerbated in a changing climate (79).
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 (20132015) 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 (1015). 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 lesions (13,14),
arms detach from the central disc, gonads spilled from fully reproduc-
tive stars and individuals die, often leaving white piles of ossicles and
disconnected limbs (fig. S1). Sea star mortalities during the first years
of the Northeast Pacific SSWD event (20132015) were linked to a sea
starassociated densovirus (SSaDV; family Parvoviridae), based on me-
tagenomic analysis of bacteria and viruses in field samples, the experi-
mental generation of disease in sea stars challenged with nonheated
viral-sized material, the correlation between SSWD progression and
SSaDV loads, and higher SSaDV prevalence in symptomatic stars
(13). Further support for densovirus involvement in the Northeast
Pacific SSWD event includes experimental infection and morbidity
in Pycnopodia helianthoides (17), the relationship between asteroid
densovirus load and SSWD in P. helianthoides,andexperimental
transmission of SSWD disease to asymptomatic individuals through
exposure to a viral-sized agent (0.22 mm) from SSWD symptomatic
stars (17,18).
While the Northeast Pacific SSWD event caused severe reduc-
tions of the keystone intertidal ochre sea star across its entire west-
coast range (14,15,1921), the impacts on subtidal species are less
wellknown.Becauseitwasthemostabundantsubtidalstarand
also the most susceptible in early reports, initial studies quantified
devastating declines of P. helianthoides,inWashingtonandBritish
Columbia, linked with high prevalence of wasting disease (22,23),
but these observations are limited to the initial years, specific regions,
and shallow depths accessible to divers. Hence, the current status of
P. helianthoides in the Northeast Pacific and at all depths is un-
known. This species is an important predator of sea urchins, and ur-
chin populations released from top-down predatory control can
expand and threaten kelp forests and biodiversity (24,25). In many
locations, P. helianthoides is the apex subtidal predator when other
urchin predators are absent (22,26). In these locations, its decline has
triggered a trophic cascade, causing urchin populations to explode and
kelp to rapidly diminish (22). If P. helianthoides reductions occur
throughout its range at the magnitude reported in local surveys, and
at greater depths, this disease could not only threaten the long-term
persistence of this species but also have wide-ranging cascading eco-
system effects.
1
Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY
14853, USA.
2
One Health Institute, School of Veterinary Medicine, University of
California, Davis, CA 95616, USA.
3
Department of Biology, Stanford University,
Stanford, CA 94040, USA.
4
School of Resource and Environmental Management,
Simon Fraser University, Burnaby, BC V5A 1S6, Canada.
5
Hakai Institute, Heriot
Bay, BC V0P 1H0, Canada.
6
Fishery Resource Analysis and Monitoring Division,
Northwest Fisheries Science Center, National Marine Fisheries Service, National
Oceanic and Atmospheric Administration (NOAA), 2032 SE OSU Drive, Newport,
OR 97365, USA.
7
Fishery Resource Analysis and Monitoring Division, Northwest
Fisheries Sc ience Center, National Ma rine Fisheries Service, N OAA, 2725 Montlake
Boulevard East, Seattle, WA 98112, USA.
8
NOAA Coral Reef Watch, College Park,
MD 20740, USA.
9
ReefSense Pty Ltd., Townsville, Queensland, Australia.
10
Marine
Geophysical Laboratory, Physics, College of Science and Technology, James Cook
University, Townsville, Queensland, Australia.
11
Reef Environmental Education
Foundation (REEF), Key Largo, FL 33037, USA.
12
The SeaDoc Society, Karen C.
Drayer Wildlife Health CenterOrcas 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: cdh5@cornell.edu
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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. Potential ecosystem 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 20112012 and an
unprecedented decline after the onset of the Northeast Pacific SSWD
event. In California and Oregon, the average biomass decreased 100%
during 20132015 (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 m
2
) along the coast of central British Columbia
using annual subtidal belt transect surveys conducted between 3 and
18 m depth in 20102011 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 m
2
in 20102014, pre-Northeast Pacific SSWD event) to virtually zero
(0.01 to 0.07 kg/10 m
2
) in 20152017. The abundance score from the
shallow nearshore waters surveys revealed fluctuating but regionally
constant P. helianthoides abundance during 20062013 and a con-
sistent continental-wide decline after the onset of the Northeast Pa-
cific SSWD event (Fig. 2).
To assess the relationship between P. helianthoides declines at shal-
low nearshore waters and SST, we modeled the ACs reported for this
species in the roving-diver surveys as a function of a satellite-derived
SST anomaly metric and days since the SST metric was observed. Be-
tween 2013 and 2015, SST anomalies (departures from the climatolo-
gically expected temperature calculated from 1985 to 2012) were
warm at all locations, but their magnitude and duration varied with
latitude (Fig. 3). In California, 2014 was anomalously warm, increas-
ing to extreme warming throughout 2015 with a peak anomaly of C.
In Washington, 2013 was anomalously warm during July to October
but otherwise followed the seasonal climatology. In July 2014, a pro-
longed warm anomaly began, increasing to an extreme 2.5°C anomaly
through 2015, coinciding with the long residence of the heat wave in
the northeast Pacific Ocean (29). Central British Columbia followed a
similar pattern seen in Washington, with the arrival of the anomalous-
ly warm waters in the fall of 2015 (30). Oregon was more variable than
other locations, likely because of periodic cold upwelling events.
On the basis of ordinal regression models of P. helianthoides abun-
dance and biologically relevant SST anomaly metrics, we provide
evidence that P. helianthoides declines in shallow nearshore waters
were associated with the maximum temperature anomaly exposure
from within 60 days before each survey (tables S1 and S2). Our
selected model indicates that with every 1°C increase in the maxi-
mum temperature anomaly, we would expect a 6% increase in the
log odds of observing a low AC compared with all higher ACs (AC 0
versus 1 to 4, AC 1 versus 2 to 4, etc.), when all other variables are
held constant (table S2). We evaluated the goodness of fit between
the model and data using NagelkerkespseudoR
2
(31)andesti-
mated that our model explained 68.5% of the variance in sea star
ACs compared to a null model. To investigate the role of the max-
imum temperature anomaly exposure from within 60 days before
the survey, we also calculated a pseudo R
2
for a model that included
all covariates other than this variable. This model explained 30.5%
ofthevarianceinP. helianthoides ACs, suggesting that this SST
anomaly metric alone explains ~38% of the variance.
DISCUSSION
Using longitudinal data from complementary survey methods, we show
(i) consistent or slightly increasing populations of P. helianthoides
across most of its natural range in the decade before the Northeast
Pacific SSWD event in shallow nearshore waters; (ii) consistent popu-
lations of P. helianthoides across most of its natural range in the dec-
ade before the Northeast Pacific SSWD event in deep offshore waters;
(iii) a continental-scale collapse of this major ocean predator in these
habitats associated temporally and spatially to the Northeast Pacific
SSWD event and, therefore, to the multihost SSaDV; and (iv) an as-
sociation between P. helianthoides declines in shallow nearshore
waters and period of anomalously warm nearshore waters.
Our statistical analysis provides evidence for anomalous tem-
perature as a key facilitator of the disease-related declines in the shal-
low nearshore waters, explaining more than a third of the variance by
itself. These results align with field and experimental evidence of the
interacting roles of temperature and SSWD in P. ochraceus morbid-
ity and mortality, where infected stars exposed to warmer tempera-
tures died at a faster rate (10,14,15,27). Previous studies suggest that
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high water temperatures are associated with lower coelomic fluid vo-
lumes, higher metabolic demands, and metabolic stress in asteroids
(10,3234), 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 explanation
forthiscollapse.Thisspecieswasidentifiedasthemostsusceptibleto
SSWD (13,14), the observed widespread declines occurred right after
the onset of this event, and they followed the timing and spatial pat-
tern of the declines observed in nearshore P. helianthoides popula-
tions and intertidal P. ochraceus populations (15). Moreover,
necrotic stars with autotomizing arms were observed by one of the
coauthors (K. Bosley) in the trawls at the initiation of the Northeast
Pacific SSWD event. The limitations of deep offshore water tempera-
ture data prevented an analysis of the role of water temperature in
exacerbating P. helianthoides declines at deep offshore waters, as this
Fig. 1. Continental collapse of a pivotal predator: Deep offshoresurveys. Mean biomass of sunflower star in 8968 deep offshore trawls (55 to 1280 m) from (A) Washington,
(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 initiation across regions.
Yellow circles depict the 20132016 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. (Ato 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, annual mean 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 m
2
) in belt transect surveys in central British Columbia, with 95% confidence
interval in light blue. Yellow circles depict the 20132017 locations. The red rectangle depicts the area where the belt transect surveys were conducted. The surveys per
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 show
that anomalous warm temperatures associated with recent marine
heat waves were broadly detected at about 140 m depth in the North-
east Pacific beginning in mid-2014 (36), which may have contributed
to SSWD morbidity at these depths.
The abrupt decline of P. helianthoides after the onset of the North-
east Pacific SSWD event occurred in shallow and deep waters regard-
less of the abundance before the collapse. Similarly, Miner et al.(15)
did not detect a relationship between the degree of population decline
and pre-outbreak intertidal P. ochraceus density. The current popula-
tion status of P. helianthoides raises important questions about the
potential for recovery and persistence of this species. With SSWD,
reservoir species could be a continuous source of SSaDV to remaining
P. helianthoides given that asymptomatic star species within the range
of P. helianthoides have tested positive for SSaDV genetic material
(17). In its current status and with new bouts of mortality recorded
by divers in August 2018, continuous infection from reservoir popula-
tions or small stochastic disturbances could cause the restricted rem-
nant populations of P. helianthoides to vanish (1,2,37,38).
Cascading effects of the P. helianthoides loss are expected across
its range and will likely change the shallow water seascape in some
locations and threaten biodiversity through the indirect loss of kelp
(22,25,26,39). P. helianthoides was the highest biomass subtidal as-
teroid across most of its range before the Northeast Pacific SSWD
event (39). Loss or absence of this major predator has already been
associated with elevated densities of green (Strongylocentrotus
droebachiensis), red (Mesocentrotus franciscanus), and purple urch-
ins (Strongylocentrotus purpuratus) across their range (22,23,26,39),
even in regions with multiple urchin predators (40). Associated kelp re-
ductions have been reported following the outbreak (22,39). Examples
from other widespread marine diseasesthe near extirpation of the in-
tertidal sea star Heliaster kubiniji from Gulf of California (40), the mass
mortality of the urchin Diadema antillarum from Caribbean reefs (41),
and the withering syndromeinfluenced endangerment of multiple
California abalone species (42)demonstratehowthelossofkeyspecies
can drive community effects that influence marine ecosystem processes.
SSWD, the anomalously warm water, P. helianthoides declines, and
subsequent urchin explosions (fig. S2) have been described as the per-
fect storm.This stormcould result not only in trophic cascades and
reduced kelp beds (22) but also in abalone and urchin starvation (43).
We encourage scientific review of P. helianthoides recovery, assessment
of the probability for endangerment, and, more generally, expanded
surveillance ofthe consequences stemming from complex interactions
that emerging infectious diseases and warming ocean temperatures can
have in shaping ecosystems, even in the deep ocean.
MATERIALS AND METHODS
Study area
This study includes data from across the northeast Pacific, encom-
passing most of the natural range of the endemic sunflower sea star
P. helianthoides. We analyzed data from shallow nearshore roving-
diver surveys collected in California, Oregon, and Washington (USA)
and British Columbia (Canada), in addition to deep offshore trawl
surveys conducted from California to Washington.
Deep offshore surveys
The National Marine Fisheries Service [National Oceanic and Atmo-
spheric Administration (NOAA)] conducted 8968 individual bottom
Fig. 3. Ocean temperature anomaly averaged over the roving-diver survey
locations for the three initial years 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 20132017, 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 m
2
.P. helianthoides biomass for the central coast region
(range from 51°24.612N to 52°4.242N) 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 0.0 (~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 pixel near the coastal boundary. SST anomalies describe
the variation in temperature from expected values at a given time
of year and location and were determined using the Coral Reef
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). Jurisdictional SST 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 hierarchical ordinal regression model with a probit link
function
PðYijÞ¼qjb1ðSSTmetriciÞb2ðDays:SSTmetriciÞ
b313ðYear20072017iÞmðLatitudeiÞ
gðMonthiÞ
mðLatitudeiÞeNð0;s2
mÞ
gðMonthiÞeNð0;s2
gÞ
i=1,, I surveys,
j=1,,j1 abundance categories,
where the cumulative probability of the ith survey falling in the jth AC
or below is modeled as a function of the following: q
j
threshold pa-
rameters across ACs, which provide a separate intercept for each
category j, an SST anomaly metric (SSTmetric
i
), days since the SST
anomaly metric was observed (Days.SSTmetric
i
), year (Year
20072017
),
month (Month
i
), and latitude (Latitude
i
).Yearwasincludedasafixed
effect to determine the year when sea star abundances collapsed (years
that were statistically significantly different from the 2006 baseline).
Month and latitude were included as random effects to account for ad-
ditional variation over time and space. s
2m
and s
2g
corresponded to the
variance of the distribution of month and latitude random effects, re-
spectively. Our data met all model assumptions: (i) the response variable
was measured on an ordinal scale; (ii) the predictor variables were con-
tinuous or categorical; (iii) there was no multicollinearity among predic-
tor variables, which we assessed with correlation tests for correlations
between two predictors and visually for correlations among three pre-
dictors; and (iv) there were proportional odds between each AC as in-
dicated by nearly identical effects among generalized logistic regression
models comparing each AC split individually (slopes < 2). We fit 10
candidate models that included the year, latitude, and month covariates
and one of the following SST metrics: the maximum SST in the 30, 60,
90, 180, or 360 days prior to each roving diver survey; or the maximum
anomalous SST in the 30, 60, 90, 180, or 360 days prior to each roving-
diver survey. We compared the AIC value of the candidate models with
and without the covariate days since the SST metric was observed,and
then selected the model with the lowest AIC value (tables S1 and S2). We
assessed convergence of models by inspecting the maximum absolute gra-
dient of the log-likelihood function and the magnitude of the Hessian.
Each model was empirically identifiable by ensuring that the condition
number of the Hessian measure was no larger than 10
4
(47). We evalu-
ated variance explained by the final model using NagelkerkespseudoR
2
(31). NagelkerkespseudoR
2
is a commonly used statistic to measure
goodness of fit that is calculated by comparing likelihood ratios between
a full model and an intercept model. We conducted this analysis in R
statistical software v3.4.3 (48)usingtheclmmfunctionoftheordinal
package (47) for the ordinal regression model and the nagelkerke function
in the rcompanionpackage to calculate pseudo R
2
values (49).
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/
content/full/5/1/eaau7042/DC1
Table S1. Summary of results of the candidate hierarchical ordinal regression 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. Annual SST 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 Sensingprogram.
British Columbia monitoring was funded by an NSERC Discovery, Canadian Foundation
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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. Salomo n, L. Lee, O. Pontier, C. Pattengill-Semmens, J. K. Gaydos, Disease
epidemic and a marine heat wave are associated with the conti nental-scale collapse of a
pivotal predator (Pycnopodia helianthoides). Sci. Adv. 5, eaau7042 (2019).
SCIENCE ADVANCES |RESEARCH ARTICLE
Harvell et al., Sci. Adv. 2019; 5: eaau7042 30 January 2019 8of8
on January 31, 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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The sea star Pisaster ochraceus and sea otters ( Enhydra lutris ) are two predators capable of shaping rocky intertidal and kelp forest community structure and functioning. In 2013, a sea star wasting event decimated populations of Pisaster along the west coast of North America. The collapse of this species in the rocky intertidal revealed an unexpected relationship between two keystone predators. In this study, we show how the loss of Pisaster along the Monterey Peninsula, CA, USA led to an increase in mussel ( Mytilus californianus ) size and expansion into lower tidal zones. Before the sea star wasting event, the local sea otter population fluctuated around a near equilibrium. However, in the absence of Pisaster , sea otters increased their dietary intake on mussels, which contributed in part to a local population-level rise. These results demonstrate how the loss of a keystone predator in one ecosystem may impart population-level changes to another.
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Disease outbreaks as a driver of wildlife mass mortality events have increased in magnitude and frequency since the 1940s. Remnant populations, composed of individuals that survived mass mortality events, could provide insight into disease dynamics and species recovery. The sea star wasting disease (SSWD) epidemic led to the rapid >90% decline of the sunflower star Pycnopodia helianthoides. We surveyed the biomass density of P. helianthoides on the central British Columbia coast before, during and after the arrival of SSWD by conducting expert diver surveys in shallow subtidal habitats from 2013 to 2023. We found a rapid decline in biomass density following the onset of SSWD in 2015. Despite consistent recruitment post-outbreak to sites associated with outer islands, we found repeated loss of large adult individuals over multiple years. Within nearby fjord habitats, we found remnant populations composed of large adult P. helianthoides. The interaction of temperature and salinity with the biomass density of P. helianthoides varied by location, with high biomass density associated with higher temperatures in the outer islands and with lower temperatures and higher salinity in the fjords. These patterns suggest that fjords provide refuge from consequences of SSWD and protecting these populations could be imperative for the species.
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While satellite data indicate that the surface expression of the North Pacific marine heatwave, nicknamed “The Blob”, disappeared in late 2016, Argo float and ship‐based CTD data show that warm conditions persisted below the surface mixed layer through at least March 2018. We trace this anomalously warm subsurface water from the open ocean through Queen Charlotte Sound to Rivers Inlet, on British Columbia's central coast. In Rivers Inlet, deep water below the sill depth continues to be 0.3° to 0.6°C warmer than the monthly average, suggesting that impacts of this marine heatwave have persisted in coastal waters at least 4 years after its onset, with potentially substantial effects on coastal ecosystems.
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While changes in the abundance of keystone predators can have cascading effects resulting in regime shifts, the role of mesopredators in these processes remains underexplored. We conducted annual surveys of rocky reef communities that varied in the recovery of a keystone predator (sea otter, Enhydra lutris) and the mass mortality of a mesopredator (sunflower sea star, Pycnopodia helianthoides) due to an infectious wasting disease. By fitting a population model to empirical data, we show that sea otters had the greatest impact on the mortality of large sea urchins, but that Pycnopodia decline corresponded to a 311% increase in medium urchins and a 30% decline in kelp densities. Our results reveal that predator complementarity in size-selective prey consumption strengthens top-down control on urchins, affecting the resilience of alternative reef states by reinforcing the resilience of kelp forests and eroding the resilience of urchin barrens. We reveal previously underappreciated species interactions within a 'classic' trophic cascade and regime shift, highlighting the critical role of middle-level predators in mediating rocky reef state transitions.
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Significance Opportunities to study microevolution in wild populations are rare and challenging. Annual monitoring allowed us to capture both the prelude to and aftermath of one of the largest marine mass mortality events on record in a keystone marine species. Median mortality of 81% across populations was recorded along with significant allele frequency shifts at multiple loci in the adult population. Shifts were consistent across locations and also occurred in new recruits, with few exceptions. These results indicate a long-term species-wide change in allele frequencies will persist through future generations. Population genomic monitoring, at a time when marine diseases and mass mortalities are on the rise, will be essential for documenting rapid genetic shifts in response to chronic and extreme events.
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Disturbances such as disease can reshape communities through interruption of ecological interactions. Changes to population demographics alter how effectively a species performs its ecological role. While a population may recover in density, this may not translate to recovery of ecological function. In 2013, a sea star wasting syndrome outbreak caused mass mortality of the keystone predator Pisaster ochraceus on the North American Pacific coast. We analyzed sea star counts, biomass, size distributions, and recruitment from long‐term intertidal monitoring sites from San Diego to Alaska to assess regional trends in sea star recovery following the outbreak. Recruitment, an indicator of population recovery, has been spatially patchy and varied within and among regions of the coast. Despite sea star counts approaching predisease numbers, sea star biomass, a measure of predation potential on the mussel Mytilus californianus, has remained low. This indicates that post‐outbreak populations have not regained their full predation pressure. The regional variability in percent of recovering sites suggested differences in factors promoting sea star recovery between regions but did not show consistent patterns in postoutbreak recruitment on a coast‐wide scale. These results shape predictions of where changes in community composition are likely to occur in years following the disease outbreak and provide insight into how populations of keystone species resume their ecological roles following mortality‐inducing disturbances.
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Disease outbreaks can have substantial impacts on wild populations, but the often patchy or anecdotal evidence of these impacts impedes our ability to understand outbreak dynamics. Recently however, a severe disease outbreak occurred in a group of very well-studied organisms–sea stars along the west coast of North America. We analyzed nearly two decades of data from a coordinated monitoring effort at 88 sites ranging from southern British Columbia to San Diego, California along with 2 sites near Sitka, Alaska to better understand the effects of sea star wasting disease (SSWD) on the keystone intertidal predator, Pisaster ochraceus. Quantitative surveys revealed unprecedented declines of P. ochraceus in 2014 and 2015 across nearly the entire geographic range of the species. The intensity of the impact of SSWD was not uniform across the affected area, with proportionally greater population declines in the southern regions relative to the north. The degree of population decline was unrelated to pre-outbreak P. ochraceus density, although these factors have been linked in other well-documented disease events. While elevated seawater temperatures were not broadly linked to the initial emergence of SSWD, anomalously high seawater temperatures in 2014 and 2015 might have exacerbated the disease’s impact. Both before and after the onset of the SSWD outbreak, we documented higher recruitment of P. ochraceus in the north than in the south, and while some juveniles are surviving (as evidenced by transition of recruitment pulses to larger size classes), post-SSWD survivorship is lower than during pre-SSWD periods. In hindsight, our data suggest that the SSWD event defied prediction based on two factors found to be important in other marine disease events, sea water temperature and population density, and illustrate the importance of surveillance of natural populations as one element of an integrated approach to marine disease ecology. Low levels of SSWD-symptomatic sea stars are still present throughout the impacted range, thus the outlook for population recovery is uncertain.
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Sea Star Wasting Disease (SSWD) describes a suite of disease signs that affected >20 species of asteroid since 2013 along a broad geographic range from the Alaska Peninsula to Baja California. Previous work identified the Sea Star associated Densovirus (SSaDV) as the best candidate pathogen for SSWD in three species of common asteroid (Pycnopodia helianthoides, Pisaster ochraceus, and Evasterias troscheli), and virus-sized material (<0.22 μm) elicited SSWD signs in P. helianthoides. However, the ability of virus-sized material to elicit SSWD in other species of asteroids was not known. Discordance between detection of SSaDV by qPCR and by viral metagenomics inspired the redesign of qPCR primers to encompass SSaDV and two densoviral genotypes detected in wasting asteroids. Analysis of asteroid samples collected during SSWD emergence in 2013–2014 showed an association between wasting asteroid-associated densoviruses (WAaDs) and SSWD in only one species (P. helianthoides). WAaDs were found in association with asymptomatic asteroids in contemporary (2016 and later) populations, suggesting that they may form subclinical infections at the times they were sampled. WAaDs were found in SSWD-affected P. helianthoides after being absent in asymptomatic individuals a year earlier at one location (Kodiak). Direct challenge of P. ochraceus, Pisaster brevispinus, and E. troscheli with virus-sized material from SSWD-affected individuals did not elicit SSWD in any trial. RNA viral genomes discovered in viral metagenomes and host transcriptomes had viral loads and metagenome fragment recruitment patterns that were inconsistent with SSWD. Analysis of water temperature and precipitation patterns on a regional scale suggests that SSWD occurred following dry conditions at several locations, but mostly was inconsistently associated with either parameter. Semi-continuous monitoring of SSWD subtidally at two sites in the Salish Sea from 2013 to 2017 indicated that SSWD in E. troscheli and P. ochraceus was associated with elevated water temperatures, but wasting in P. helianthoides occurred irrespective of environmental conditions. Our data therefore do not support that widespread SSWD is associated with potential viral pathogens in species other than P. helianthoides. Rather, we speculate that SSWD may represent a syndrome of heterogeneous etiologies between geographic locations, between species, or even within a species between locations.
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As keystone species, sea stars serve to maintain biodiversity and species distribution through trophic level interactions in marine ecosystems. Recently, Sea Star Wasting Disease (SSWD) has caused widespread mass mortality in several sea star species from the Pacific Coast of the United States of America (USA) and Asterias forbesi on the Atlantic Coast. A densovirus, named Sea Star associated Densovirus (SSaDV), has been associated with the wasting disease in Pacific Coast sea stars, and limited samples of A. forbesi. The goal of this research is to examine the pathogenesis of SSWD in A. forbesi on the Atlantic Coast of the USA and to determine if SSaDV is associated with the wasting disease in this species. Histological examination of A. forbesi tissues affected with SSWD showed cuticle loss, vacuolation and necrosis of epidermal cells, and oedema of the dermis, but no consistent evidence indicating the cause of the lesions. Challenge experiments by cohabitation and immersion in infected water suggest that the cause of SSWD is viral in nature, as filtration (0.22 μm) of water from tanks with sea stars exhibiting SSWD did not prevent the transmission and progression of the disease. Death of challenged sea stars occurred 7–10 d after exposure to infected water or sea stars, and the infectivity crossed species (A. forbesi and Pateria miniata) with equal penetrance. Of the 48 stars tested by quantitative real time PCR, 29 (60%) were positive for the SSaDV VP1 gene. These stars represent field-collected sea stars from all geographical regions (South Carolina to Maine) in 2012–2015, as well as stars exposed to infected stars or water from affected tanks. However, a clear association between the presence of SSaDV and SSWD signs in experimental and field-collected A. forbesi was not found in this study.
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Managing for simultaneous recovery of interacting species, particularly top predators and their prey, is a longstanding challenge in applied ecology and conservation. The effects of sea otters (Enhydra lutris kenyoni) on abalone (Haliotis spp.) is a salient example along North America's west coast where sea otters are recovering from 18th- and 19th-century fur trade while efforts are being made to recover abalone from more recent overfishing. To understand the direct and indirect effects of sea otters on northern abalone (H. kamtschatkana) and the relative influence of biotic and abiotic conditions, we surveyed subtidal rocky reef sites varying in otter occupation time in three regions of British Columbia, Canada. Sites occupied by sea otters for over 30 years had 16 times lower densities of exposed abalone than sites where otters have yet to recover (0.46 ± 0.08/20 m² vs. 7.56 ± 0.98/20 m²), but they also had higher densities of cryptic abalone (2.17 ± 1.31/20 m² vs. 1.31 ± 0.20/20 m²). Abalone densities were greater in deeper vs. shallower habitats at sites with sea otters compared to sites without otters. Sea otter effects on exposed abalone density were three times greater in magnitude than those of any other factor, whereas substrate and wave exposure effects on cryptic abalone were six times greater than those of sea otters. While higher substrate complexity may benefit abalone by providing refugia from sea otter predation, laboratory experiments revealed that it may also lead to higher capture efficiency by sunflower stars (Pycnopodia helianthoides), a ubiquitous mesopredator, compared to habitat with lower complexity. Sea otter recovery indirectly benefitted abalone by decreasing biomass of predatory sunflower stars and competitive grazing sea urchins, while increasing stipe density and depth of kelp that provides food and protective habitat. Importantly, abalone persisted in the face of sea otter recovery, albeit at lower densities of smaller and more cryptic individuals. We provide empirical evidence of how complex ecological interactions influence the effects of recovering predators on their recovering prey. This ecosystem-based understanding can inform conservation trade-offs when balancing multifaceted ecological, cultural, and socio-economic objectives for species at risk.
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We determined prevalence and altitudinal distribution of forest birds infected with avian pox at 16 locations on Hawaii, from sea level to tree line in mesic and xeric habitats, during 1977–1980. Isolates from lesions were cultured in the laboratory for positive identification of Poxvirus avium. Infected birds from the wild were brought into the laboratory to assess differences in the course of infection in native versus introduced species. We also documented distributions and activity cycles of potential avian pox vectors.>Native forest birds were (1) more susceptible to avian pox infection than were introduced species, (2) most likely to be infected during the wet season, and (3) found to have a higher prevalence in mesic when compared to xeric forests. Avian pox occurred in forest birds at all elevations, but highest levels were in the mid-elevational ranges (∼1,200 m) where vectors and native birds had the greatest overlap. Temporal and elevational differences in prevalence were apparent throughout the annual cycle. Avian pox probably did not reach epizootic proportions on Hawaii until after introduction of the mosquito and domestic birds in the early 1800s, and since then has had a negative effect on the population dynamics of native forest birds. Today, this introduced disease is an important factor that should be considered in future conservation efforts that are directed at the recovery of native forest birds in Hawaii.
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Population declines in wild and cultured abalones (Haliotis spp.) due to a bacterial disease called withering syndrome (WS) have been documented along the northeastern Pacific Ocean. However, observed differences in species susceptibility to the disease are not well understood. Here, we examined the susceptibility of three temperate abalone species, the cool water (4-14°C) pinto or northern abalone (Haliotis kamtschatkana), the intermediate water (8-18°C) red abalone (H. rufescens), and the warm water (12-23°C) pink abalone (H. corrugata), to experimental WS infection at temperatures facilitating disease proliferation. Mortality data paired with histological and molecular detection of the WS pathogen confirmed that these abalone species exhibit different levels of susceptibility to infection and resistance to WS development ranging from high susceptibility and low resistance in pinto abalone to moderate/low susceptibility and resistance in red and pink abalones. The temperature associated with WS induced mortalities also varied among species: pinto abalone died at the lowest experimental temperature (17.32 ± 0.09°C), while red abalone died at an intermediate temperature (17.96 ± 0.16°C), and pink abalone required the highest temperature (18.84 ± 0.16°C). When data from the current and previous studies were examined, susceptibility to WS was inversely related to phylogenetic distance from white abalone (H. sorenseni), which had the highest susceptibility and lowest resistance of all abalone species tested prior to the current study. These results provide further evidence that an abalone's thermal optima and phylogenetic relationship can determine its susceptibility to WS; species with cool water evolutionary histories are most susceptible to WS and the most susceptible species appear to be closely related. Differences among the thermal ranges of abalone species have broad implications for WS disease dynamics and highlight the importance of understanding the mechanisms governing the abalone-WS relationship in order to properly manage declining abalone populations.