Heat stress does not induce wasting
symptoms in the giant California sea
cucumber (Apostichopus californicus)
Declan Dawson Taylor1 ,2 ,* , Jonathan J. Farr2 ,3 ,* , Em G. Lim4 , Jenna L. Fleet2 ,5 ,
Sara J. Smith Wuitchik2 ,6 ,7 ,8 and Daniel M. Wuitchik2 ,6
1

Earth, Ocean and Atmospheric Sciences, University of British Columbia, Vancouver, British Columbia, Canada
Bamfield Marine Sciences Center, Bamfield, British Columbia, Canada
3
Biological Sciences, University of Alberta, Edmonton, Alberta, Canada
4
Biological Sciences, Simon Fraser University, Vancouver, British Columbia, Canada
5
Biological Sciences, University of Winnipeg, Winnipeg, MB, Canada
6
Biological Sciences, Boston University, Boston, MA, United States of America
7
Informatics Group, Harvard University, Cambridge, MA, United States of America
8
Biology, Mount Royal University, Calgary, Alberta, Canada
*
These authors contributed equally to this work.
2

ABSTRACT

Submitted 10 June 2022
Accepted 20 November 2022
Published 7 February 2023
Corresponding authors
Sara J. Smith Wuitchik,
sara.wuitchik@gmail.com,
ssmith6@mtroyal.ca
Daniel M. Wuitchik,
wuitchik@bu.edu
Academic editor
Eric Ward
Additional Information and
Declarations can be found on
page 11

Oceanic heatwaves have significant impacts on disease dynamics in marine ecosystems.
Following an extreme heatwave in Nanoose Bay, British Columbia, Canada, a severe sea
cucumber wasting event occurred that resulted in the mass mortality of Apostichopus
californicus. Here, we sought to determine if heat stress in isolation could trigger
wasting symptoms in A. californicus. We exposed sea cucumbers to (i) a simulated
marine heatwave (22 ◦ C), (ii) an elevated temperature treatment (17 ◦ C), or (iii)
control conditions (12 ◦ C). We measured the presence of skin lesions, mortality,
posture maintenance, antipredator defences, spawning, and organ evisceration during
the 79-hour thermal exposure, as well as 7-days post-exposure. Both the 22 ◦ C and
17 ◦ C treatments elicited stress responses where individuals exhibited a reduced ability
to maintain posture and an increase in stress spawning. The 22 ◦ C heatwave was
particularly stressful, as it was the only treatment where mortality was observed.
However, none of the treatments induced wasting symptoms as observed in the
Nanoose Bay event. This study provides evidence that sea cucumber wasting may not
be triggered by heat stress in isolation, leaving the cause of the mass mortality event
observed in Nanoose unknown.
Subjects Ecology, Marine Biology, Zoology
Keywords Wasting disease, Skin ulceration syndrome, Sea cucumber, Thermal stress, Echino-

derm

DOI 10.7717/peerj.14548

INTRODUCTION

Copyright
2022 Dawson Taylor et al.

Climate change is increasing the intensity, duration, range, and frequency of marine
heatwaves across the globe with potentially catastrophic effects on organism fitness,
ecosystems, and human economies (Frölicher, Fischer & Gruber, 2018; Allan et al., 2021).
In marine ecosystems these extreme climatic events often cause immediate and mass
mortality at all trophic levels from thermal stress, starvation, toxicity, and hypoxia (Cavole

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How to cite this article Dawson Taylor D, Farr JJ, Lim EG, Fleet JL, Smith Wuitchik SJ, Wuitchik DM. 2022. Heat stress does not induce
wasting symptoms in the giant California sea cucumber (Apostichopus californicus). PeerJ 11:e14548 http://doi.org/10.7717/peerj.14548

et al., 2016; Di Lorenzo & Mantua, 2016; von Biela et al., 2019; Suryan et al., 2021). Marine
heatwaves may exacerbate disease because thermal stress can compromise the immune
response, and warmer temperatures can increase the virulence of pathogens (Harvell et
al., 1999; Marcogliese, 2008; Branco et al., 2012; Matozzo et al., 2012; Oliver et al., 2017).
This temperature-associated increase in virulence and infectivity has been associated with
stimulating and intensifying sea star wasting disease to devastating effects (Harvell et
al., 1999; Bates, Hilton & Harley, 2009; Eisenlord et al., 2016; Hewson et al., 2018; Aquino
et al., 2021). A notorious example of the impacts of a wasting disease outbreak was the
2013-current sea star wasting epidemic, which has affected more than 20 sea star species
in the Northeast Pacific Ocean over the last decade (Hewson et al., 2018). Sea star wasting
disease encompasses a broad set of symptoms including twisted arms, lesions, deflation/loss
of turgor, loss of arms, lack of grip strength in tube feet, and liquefaction (Bates, Hilton &
Harley, 2009; Menge et al., 2016; Hewson et al., 2018). In most sea star species, the driving
cause of wasting disease remains largely uncertain. It has often been assumed that wasting
in echinoderms is driven by infectious agents (Hewson et al., 2014; Bucci et al., 2017; Miner
et al., 2018; Hewson, Johnson & Tibbetts, 2020). Warm temperatures have also been linked
to several mass mortality events (Bates, Hilton & Harley, 2009; Eisenlord et al., 2016; Harvell
et al., 2019). Because of the population-level impacts on ecologically important species,
understanding the pathogenic and environmental drivers of sea star wasting remains an
area of active research (Aalto et al., 2020; Aquino et al., 2021; Hewson, 2021).
Wasting is not limited to sea stars and is an emerging concern across closely related
taxa. For example, sea urchins have faced a variety of disease-linked mass mortality events
and epizootics (Feehan & Scheibling, 2014). Several of these bacterial and amoebic diseases
have been linked to warm water anomalies, from climate events or storms (Sweet, 2020).
Red sea urchins (Mesocentrotus franciscanus) and purple sea urchins (Strongylocentrotus
purpuratus) have suffered from ‘‘bald sea urchin disease’’ and ‘‘sea urchin wasting disease’’
along the Pacific coast of British Columbia (B.C.). Pathology of these diseases includes
lesions to the body wall and a shortening or loss of spines, and both have been associated
with mass mortality events (Feehan & Scheibling, 2014; Sweet, 2020). While these diseases
are believed to have bacterial origins, a single bacterial strain has not been identified as
the cause (Sweet, 2020). Disease-mediated mass mortality events in urchins and sea stars
have caused trophic cascades and dramatic ecosystem shifts, highlighting the importance
of understanding these ecological phenomena (Schultz, Cloutier & Côté, 2016; Suryan et
al., 2021; Traiger et al., 2022). Recent evidence has emerged that wasting may occur in sea
cucumbers as well, promoting further concerns about the impacts of marine diseases in
shallow, near-shore ecosystems.
Since 2014, there have been reports of giant California sea cucumbers (Apostichopus
californicus) with wasting symptoms similar to those of sea stars throughout their range
in the northeast Pacific Ocean (Hewson, Johnson & Tibbetts, 2020). Sea cucumber wasting
disease is poorly defined, with symptoms typically including non-focal lesions and fissures
across the body wall, epidermal tissue sloughing, and rapid liquefaction (Hewson, Johnson
& Tibbetts, 2020; Fig. 1C). Much like in sea stars, there are numerous potential causal
agents that could elicit this suite of symptoms. Heat stress may be particularly relevant

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A

D

N

Heatwave (22oC)

Average Temperature (ºC)

20
Warm (17oC)

15

B

C

Control (12oC)

10

5

January

April

July

October

January

Figure 1 Temperature anomalies and sea cucumber wasting. (A) Map of western North America with
(B) an inset of Vancouver Island showing the data collection locations of Bamfield Inlet (green), Nanoose
Bay (purple). (C) A. californicus in Nanoose Bay exhibiting wasting symptoms. (D) Eight-day rolling average seasonal sea surface temperatures in Nanoose Bay from 2010 to 2020 (black line with grey SE ribbon)
and 2021 (colour gradient line), with experimental temperature treatments highlighted.
Full-size DOI: 10.7717/peerj.14548/fig-1

given that after a series of heatwaves from June 25 to July 07, 2021 (Environment and
Climate Change Canada, 2021; Ocean Networks Canada) a wasting event with very high
mortality occurred in the Strait of Georgia near Nanoose, B.C., from late August to
October 2021 (Fig. 1D; E Lim, pers. comm., 2021). At its peak, up to 94% of observed
A. californicus at a single site showed evidence of wasting. On average, across all affected
sites (n = 7), 50% of observed A. californicus exhibited wasting symptoms. The six to ten
week delay between peak near-surface sea temperatures and widespread mortality may be
indicative of a potential link between thermal stress and wasting in A. californicus, perhaps
mediated by the progression of disease symptoms and immune failure. Temperature is
an especially compelling mechanism considering that healthy individuals were abundant
below depths of 19 metres where the water was cooler (E Lim, pers. comm., 2021). The
effect of temperature-related stressors on wasting in sea cucumbers has yet to be tested.
Here, we assess whether acute heat stress rapidly induces wasting in A. californicus.
We also evaluate behavioural stress response signatures through stiffening, spawning,
and evisceration to explore how they are affected by extreme elevated temperature. Sea
cucumbers are important benthic detritivores that play an important role in organic
matter decomposition and sediment aeration (Purcell, Conand & Byrne, 2016). Evidence
of a connection between temperature and mass wasting events in sea stars (Bates, Hilton &
Harley, 2009; Eisenlord et al., 2016; Harvell et al., 2019) necessitates a proactive assessment
of whether heat stress can induce similar symptoms in sea cucumbers.

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MATERIALS & METHODS
Collection and acclimation
We collected Apostichopus californicus via SCUBA from a depth of 7–12 m in July 2021
from Scott’s Bay and Bamfield Inlet in Barkley Sound, British Columbia (48◦ 500 0200 N,
125◦ 080 4500 W). The sea cucumbers were initially collected and used in an unrelated short
term tagging experiment comparing T-bar and coded wire tags at the end of July 2021,
after which they were all tagged with coded wire tags. Tagging had no measurable impact
on sea cucumber behaviour or physiology in the short or long term (Leedham et al.,
unpublished data; Cieciel, Pyper & Eckert, 2009). After this experiment sea cucumbers were
then maintained in an open flow-through system at the Bamfield Marine Sciences Centre,
with inflow from Bamfield Inlet for four months prior to the start of the thermal stress
experiment.

Experimental design
To determine an average wet weight of each individual, sea cucumbers were weighed
twice at the beginning of the experiment. Individuals (N = 56) were randomly divided
into one of three temperature treatments: control (12 ◦ C, n = 19), warm (17 ◦ C, n =
19), or heatwave (22 ◦ C, n = 18). Our experimental temperatures reflect average summer
temperatures and those recorded in the Strait of Georgia when wasting of A. californicus
was observed (Fig. 1D). Specifically, the average temperature across July and August 2020
and 2021 was 17.5 ◦ C at 5 m depth and 11.9 ◦ C at 20 m depth (Fig. S1). In the summer 2021
heatwave, a maximum temperature at 5 m depth of 21.6 ◦ C was reached on August 04,
2021 (Pawlowicz, 2017; Xuereb et al., 2018; Chen et al., 2021; Ocean Networks Canada Data
Archive, 2022). Our control temperature (12 ◦ C) was that of the Bamfield Inlet at the time
of the temperature experiment and was the temperature the cucumbers were acclimated
to.
We separated the sea cucumbers into 27 isolated experimental containers (61×41×22.2
cm) with two individuals per container, aside from two smaller containers (33 ×45.7
×11.4 cm) that housed one individual each. A plastic mesh divider was used to separate
sea cucumbers within each container to allow for tracking individuals throughout the
experiment. The containers were randomly placed into sea tables which acted as water
baths. The target water bath temperatures were achieved by having a constant flow of cooler
inlet sea water to act as the control (12 ◦ C), allowed to reach ambient room temperature
for the warm treatment (17 ◦ C), or heated using two 800 W aquarium heaters for the
heatwave treatment (22 ◦ C). The 22 ◦ C treatment temperature was gradually increased
over a 24-hour period in the sea table water baths (day 1; Fig. S2). During the temperature
treatment period, there was no seawater flow to the experimental containers in which sea
cucumbers were housed for any of the temperature treatments. To prevent stagnation and
maintain high oxygen levels, all containers were constantly aerated with airstones. The
water remained at target temperatures for 79 h, after which they were lowered back to the
control temperature of 12 ◦ C over 9-hours. Days five through 12 were a recovery period
where all sea cucumber holding containers were maintained on the flow through system.
Throughout the experiment, the sea cucumbers were closely monitored. To avoid water

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fouling, water changes were completed in individual containers as needed to maintain
nitrate and ammonium levels below 0.5 ppm, and fresh sea water was heated to the
appropriate treatment temperature prior to water changes. Water quality was measured
using API R saltwater ammonium and nitrate kits, and food was withheld during the
thermal stress window. We monitored if sea cucumbers were defecating three times each
day throughout the experiment, based on the presence of fecal pellets, as cessation of
defecation is considered to be indicative of a loss or atrophy of digestive organs (Swan,
1961; Fankboner & Cameron, 1985).

Phenotyping sea cucumber stress
We assessed sea cucumbers for wasting symptoms throughout the experiment and counted
skin lesions on days 5, 6, 7, and 12. Epidermal damage was classified as either minor lesions
or major ulcers based on their size and appearance. We defined minor lesions as regions of
epidermal damage at the spine tips without signs of considerable discoloration, where the
dermis was not damaged across its full thickness (Fig. 2B). We classified major ulcers as
epidermal ulceration exposing underlying white mutable connective tissues beneath (Fig.
2D).
We assessed body stiffness using a 3-point ordinal scale to measure heat-stress induced
deviations from normal behaviour. To do so, first we removed each individual from their
bin and gently palpated them for 10 s to encourage them to stiffen. Then we placed them
on an elevated platform to measure their ability to maintain their posture over 5 s. The
stiffness testing platform was constructed by cutting a piece of plastic pipe into an eight cm
long, eight cm in diameter, and four cm tall section, which we glued onto an eight cm tall
block. We assigned a score of 0 if the organism failed to stiffen at all (full droop), a score
of 1 if it did not remain stiff for the full 5 s when placed on the platform (partial droop),
and a score of 2 if it maintained its posture for the entire 5 s (no droop). Stiffness was
measured on days 1–5 of the experiment (as a baseline and throughout the treatment), on
day 7 (48 h after experimental endpoint) and day 12 (7 days after experimental endpoint).
Frequency of handling individuals occurred equally across treatments.
As some sea cucumbers spawned, we recorded whether there was any evidence of
spawning every 12 h. Spawning was assigned to each container rather than individual,
since some individuals were co-housed (Nbin = 30). We also evaluated whether specimens
had eviscerated based on the presence or absence of ejected internal organs during these
routine checks.

Statistical analyses
All statistical analyses were conducted in R (v4.0.3, R Core Team, 2020). We tested the
distribution of the number of lesions using the fitDist function (Rigby & Stasinopoulos,
2005) and determined that minor lesion count best fit a geometric distribution. We
modelled the maximum number of minor lesions as a function of treatment, weight,
evisceration (binary), and defecation status (binary). We included the sea table and bin
as random effects. We then used backwards selection with the stepGAIC function from
GAMLSS (Rigby & Stasinopoulos, 2005) to determine the most parsimonious combination
of variables that best explained the maximum number of lesions.

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Total Lesions / Indiv.

12

A

B

8

4

0
Control

Major Lesions / Indiv.

12

Warm

Heat Wave

C

D

8

4

0
Control

Warm

Heat Wave

Figure 2 Skin ulcers observed in Apostichopus californicus across treatments. (A) Minor ulcer count,
defined as small lesions on the ends of spines (B). (C) Major ulcer count, defined as open wounds that expose white subdermal tissue (D).
Full-size DOI: 10.7717/peerj.14548/fig-2

We examined the covariates that affected the likelihood of mortality with a logistic
regression model. Sea cucumber mortality was a binary measure, with treatment,
evisceration, defecation status, initial droop score, and initial weight as explanatory
variables. Terms for the final model were selected via backwards model selection using
stepGAIC (Rigby & Stasinopoulos, 2005) to produce the most parsimonious model of
variation in sea cucumber mortality.
To assess changes in stiffness, we constructed full ordinal regression models using the
clmm function (Christensen, 2019) with temperature treatment, date, and the interaction
between treatment and date as explanatory variables. We restricted stiffness measurements
to those taken before the heat treatment began (day 1), during the treatment (days 2–4)

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and immediately after the heat treatment (day 5). We included individual identity as a
random effect to account for repeated measures on the same individuals over time. We also
included bin and sea table as random effects to account for the paired (co-housing) and
blocked (five bins per sea table) experimental design. We used backwards model selection
to determine the most parsimonious models using dredge (Bartoń, 2020).
To assess the drivers of evisceration, we constructed a logistic regression model with
treatment, weight, and defecation status as explanatory variables, along with sea table as a
random effect. We determined the most parsimonious model through backwards selection.
To compare the incidence of stress spawning across temperature treatments, we conducted
a Dunn’s Kruskal-Wallace (K-W) test using the dunnTest function from the FSA package
(Ogle et al., 2022).
All data and annotated code for the analyses described above are publicly available at
https://github.com/declan-taylor/sea_cucumber_wasting (DOI: 10.5281/zenodo.7259325).

RESULTS
The temperature treatments varied slightly from the target temperatures during the
experimental heatwaves. During the 79 h treatment, the mean temperature of the control
treatment was 12.4 ◦ C and varied from 10.8 - 14.0 ◦ C; the mean of the warm treatment
was 16.6 ◦ C and ranged from 14.8 ◦ C to 17.9 ◦ C; the mean of the heatwave treatment was
21.7 ◦ C and varied from 19.6 ◦ C to 23.3 ◦ C. Temperature treatments were significantly
different from each other (K-W χ2 = 463.32, df = 2, p < 2.2e−16).
Minor skin lesions occurred during the experiment and were not statistically different
between treatments (ncontrol = 17, nwarm = 15, nheatwave = 10; Fig. 2). Major ulcers were
only observed in the warm (n = 1) and heatwave treatments (n = 2). These major ulcers
appeared to heal throughout the recovery period and were re-classified as minor lesions
on day 12. The maximum number of minor lesions per individual was not significantly
explained by treatment, weight, evisceration, or defecation status.
Mortality was only observed in the 22 ◦ C heatwave treatment (Fig. 3; n = 5), while
there were no mortalities observed in the control or warm treatments. Based on backwards
model selection, mortality was driven by treatment and weight (Table S1). Body stiffness
was lower in the warm and heatwave treatments compared to the control treatment (Fig.
3). Backwards-selected models indicated that temperature treatment and day affected
stiffness (Table S2). Sea cucumbers were significantly less likely to have high stiffness scores
relative to the control treatment in the warm (p = 1.99e−7) and heatwave (p = 2.44e−11)
treatments. Structural stiffness values were significantly likely to be lower than day 1 on
day 3 (p = 1.37e−5), day 4 (p = 2.50e−5) and day 5 (p = 8.66e−5), but not on day 2
(p = 0.0627; Table S2).
Stress spawning was observed during the temperature treatment (n = 11 bins), with
spawning occurring in the 17 ◦ C warm (n = 5 bins) and the 22 ◦ C heatwave (n = 4 bins)
treatments. However, there was no significant difference in spawning between temperature
treatments (K-W χ 2 = 1.94, df = 2, p = 0.379).
Evisceration was observed across all treatments (ncontrol = 2, nwarm = 5, nheatwave =
5). Treatment temperature did not explain a significant amount of the variance in the

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Ramp

Temperature Stress

Recovery
Full Droop

15

Heat Wave

10

5

Number of Sea Cucumbers

0

Partial Droop

15

Warm

10

5

0

No Droop
15

Control

10

5

0

1

2

3

4

Experiment Day

5

6

7

Mortality

Figure 3 Stiffness and mortality of Apostichopus californicus. Heat ramp (day 1), during temperature
stress (days 2–4), and recovery (days 5–7) from the temperature treatment.
Full-size DOI: 10.7717/peerj.14548/fig-3

occurrence of evisceration (Table S3), however, weight (p = 0.0383) and defecation status
(p = 0.0163) were significant drivers increasing likelihood of evisceration (Table S3). Along
with evisceration of internal organs, we also observed the expulsion of the respiratory tree
in two individuals. Both individuals were in the 22 ◦ C heatwave treatment and mortality
shortly followed the expulsion of the respiratory tree.

DISCUSSION
The objective of our study was to determine if heat stress can induce wasting symptoms
in Apostichopus californicus. While we saw minor skin lesions at all treatment levels, and
major ulcers in the warm and heatwave treatments, these were not characteristic of wasting
symptoms observed previously (Hewson, Johnson & Tibbetts, 2020; Fig. 1). Neither the
minor lesions nor major ulcers that we observed matched the wasting symptoms reported
in A. californicus in Nanoose Bay, B.C. (E Lim, pers. comm., 2021), or the isolated wasting
events reported along the Pacific coast (Hewson, Johnson & Tibbetts, 2020). We also did
not see any sloughing of body tissues or liquefaction, as has been anecdotally reported
in previous wasting events (Schroeder, 2017; Hewson, Johnson & Tibbetts, 2020). Despite

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the major ulcers sharing some resemblance in colour, texture, and location to wasting
disease symptoms, the sea cucumbers did not exhibit the full suite of symptoms that are
typical from a wasting cucumber, and, within the treatment period, these lesions did
not develop into fissures covering the dorsal body wall as seen in the wild (Fig. 1C). In
Nanoose, wasting symptoms developed into a mass outbreak and mortality event over
several months. However, unlike in reports of widespread wasting-driven mortality in
wild A. californicus, the major ulcers in our specimens healed within the 7-day recovery
period, and there was no evidence of these symptoms persisting or spreading to co-housed
individuals. As such, we could not conclude that the sea cucumbers in our experiment were
afflicted by the fatal wasting disease that has been previously reported (Schroeder, 2017;
Hewson, Johnson & Tibbetts, 2020). Future experiments could address the multi-week delay
between the heat dome and maximum die-off through prolonged exposure to elevated
temperatures and utilise histopathology to further investigate the etiology of epidermal
ulceration.
While we are uncertain of the ultimate cause of the lesions that we observed, they were
likely associated with handling while assessing their posture maintenance, which increased
the frequency of potential abrasions on the epidermal surface tissue. Major ulcers may
have begun as minor lesions that were then exacerbated by the high physiological stress
caused by the 22 ◦ C treatment. White skin ulcerations, like the major ulcers we observed,
are a recognized condition in other Holothuroidea, described as a Skin Ulceration Disease
or Skin Ulceration Syndrome (SUS; Delroisse et al., 2020). SUS has been documented
in commercially farmed Apostichopus japonicus and Holothuria scabra, and has been
characterized by white ulcers on both sides of the body wall (Wang et al., 2007; Deng et al.,
2009; Li et al., 2012; Zhang et al., 2018). Minor SUS symptoms in commercially farmed A.
japonicus and the major ulcers in our A. californicus specimens are visually similar (Deng
et al., 2009; Zhang et al., 2018). Unlike the SUS symptoms reported in A. japonicus, we did
not see any indication of swelling or discolouration of the peristomes, and we did not
see an initial abundance of ulcers around the mouth or cloaca (Becker et al., 2004; Wang
et al., 2007; Delroisse et al., 2020). Extreme cases of SUS in farmed A. japonicus also bear
resemblance to the wasting symptoms in wild A. californicus, raising further questions
about the causes of skin ulceration in Holothuroidea (Delroisse et al., 2020).
Despite not seeing evidence of wasting, we observed compelling evidence of stress
symptoms in response to thermal stress. We observed five mortality events in the 22 ◦ C
heatwave treatment. None of these mortalities were co-housed together, suggesting that it
is unlikely a fatal disease spread between cohoused individuals. Therefore, we suggest that
the heatwave treatment is close to the upper critical thermal tolerance of A. californicus,
but the warm treatment temperature does not cause sufficient stress for mortality to occur.
Our findings align with previous work on larval life stages, where Ren, Liu & Pearce (2018)
found that at 22 ◦ C, larval A. californicus experienced reduced survival which was not
observed at 16 ◦ C or 18 ◦ C.
Beyond lethal effects, we observed reduced stiffening behaviour associated with both
the 22 ◦ C heatwave and 17 ◦ C warm water treatment. A temperature-induced loss in
stiffness may have implications for sea cucumber fitness under warming sea temperatures,

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as a limited ability to stiffen may inhibit their ability to avoid predation or maintain
posture while feeding and spawning. Thermal stress may have reduced stiffness by causing
muscular fatigue and relaxation (Dowd & Somero, 2013) in the circular and longitudinalambulacral muscles (Gao & Yang, 2015). Stiffening is also caused by protein-mediated
changes in mutable collagenous tissue within the dermis of sea cucumbers (Takehana et al.,
2014). Therefore, heat stress may have reduced stiffening by denaturing or decreasing the
production of tensilin, a stiffening protein, or increasing the production of the de-stiffening
protein softenin (Yamada et al., 2010; Takehana et al., 2014; Tamori et al., 2016).
Unlike stiffening behaviour, we did not observe any significant trends in spawning
behaviour or evisceration. Of the 11 spawning events, nine occurred in elevatedtemperature treatments (warm or heatwave) and this trend, although statistically
insignificant, was expected as stress spawning has been previously reported in other
sea cucumber species (Battaglene et al., 2002; Rakaj et al., 2018; Schagerström et al., 2021).
We were unable to associate spawning with individual phenotypes due to the co-housing
experimental design. Evisceration appeared random across treatments, potentially because
A. californicus in all treatments may have been reacting to handling stimulation and stress
during the experiment (Ding et al., 2019). However, we found evidence that biological
mechanisms, weight and defecation status, partially explain the non-treatment related
variation in evisceration (Table S1). Defecation status in particular showed that A.
californicus that were not defecating were more likely to eviscerate. This may have occurred
because the energetic cost of eviscerating digestive organs would be lower for A. californicus
that had already ceased using their organs, either because they were preparing to eviscerate
(Swan, 1961) or undergoing viscera atrophy (Fankboner & Cameron, 1985). As such, when
stressed by handling, A. californicus that had already begun seasonal reductions in digestive
function may have been more likely to eviscerate from stress and overstimulation. Unlike
digestive tract evisceration, we do not believe that the expulsion of the respiratory tree
in the 22 ◦ C heatwave treatment was linked to seasonal senescence. For both individuals,
respiratory evisceration was followed by mortality, suggesting that this is an indication of
extreme physiological distress from thermal exposure.
Since we observed skin lesions under thermal stress that were likely unassociated with
wasting, other factors are likely causing recent wasting outbreaks in A. californicus. Like
wasting, severe cases of SUS are highly transmissible and result in mortality (Delroisse et al.,
2020); bacterial and viral pathogenic causal agents have been previously linked to SUS and
wasting-like symptoms, both in other sea cucumbers (Deng et al., 2008; Deng et al., 2009;
Liu et al., 2010; Zhang et al., 2018; Delroisse et al., 2020) and sea stars (Hewson et al., 2014;
Hewson et al., 2018; Work et al., 2021). A study examining a single wasting A. californicus
specimen found a high viral load but was unable to identify a specific pathogen causing
wasting symptoms (Hewson, Johnson & Tibbetts, 2020). Avenues for future research on
wasting diseases in A. californicus could address the potential for shared etiology with SUS,
given the symptomatic similarities, as well as the possibility of pathogenic origins. Such
investigations would benefit from histopathological examinations of potentially diseased
tissue to reveal more about the symptom’s pathogenesis. Infectious factors (viral, bacterial)
and non-infectious factors (chemical pollution, hypoxia, eutrophication) should both be

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investigated because widespread environmental degradation and anthropogenic climate
change are shifting pathogenic dynamics globally (Marcogliese, 2008; Allan et al., 2021).
These investigations would add valuable insight to the field of wasting diseases, given the
scarcity of published information on these events in echinoderms.
In this study, we exposed A. californicus to extreme thermal stress as measured by
mortality, degraded stiffening behaviour, and the development of skin lesions. Despite this,
we found no evidence that wasting is induced by temperature stress alone. Therefore, the
August 2021 mass wasting event in Nanoose, British Columbia, was likely not triggered
solely by the anomalous heatwave. Determining the factors that cause and exacerbate
wasting in A. californicus is essential for predicting and managing mass mortality events.
Sea cucumbers are ecologically important benthic detritivores, which break down organic
matter, recycle nutrients, and maintain sediment health (Wheeling, Verde & Nestler, 2007;
Purcell, Conand & Byrne, 2016). Efforts to protect, manage, and sustainably harvest A.
californicus in the face of global environmental change will require a comprehensive
understanding of their stress responses, disease dynamics, and the novel threat of sea
cucumber wasting.

ACKNOWLEDGEMENTS
The species collections and experiments took place on the traditional territories of the
Huu-ay-aht First Nations, a Nuu-chah-nulth Nation and signatory to the Maa-nulth First
Nations Final Agreement, and we are grateful for the opportunity to conduct research in
protected and sacred areas. We would like to thank Chloe Curry, Arya Horon, and Juliane
Jones for providing lab assistance; Payton Arthur, Mike Chung, Gabrielle Languedoc,
Sammie Foley, Juliane Jones, and Carter Burtlake for feedback on early versions of this
manuscript.

ADDITIONAL INFORMATION AND DECLARATIONS
Funding
Funding was provided by Bamfield Marine Sciences Centre to the Fall Program and by
Mount Royal University to Sara J Smith Wuitchik. The funders had no role in study design,
data collection and analysis, decision to publish, or preparation of the manuscript.

Grant Disclosures
The following grant information was disclosed by the authors:
Bamfield Marine Sciences Centre to the Fall Program.
Mount Royal University.

Competing Interests
The authors declare there are no competing interests.

Dawson Taylor et al. (2022), PeerJ, DOI 10.7717/peerj.14548

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Author Contributions
• Declan Dawson Taylor conceived and designed the experiments, performed the
experiments, analyzed the data, prepared figures and/or tables, authored or reviewed
drafts of the article, and approved the final draft.
• Jonathan J. Farr conceived and designed the experiments, performed the experiments,
analyzed the data, prepared figures and/or tables, authored or reviewed drafts of the
article, and approved the final draft.
• Em G. Lim conceived and designed the experiments, prepared figures and/or tables, and
approved the final draft.
• Jenna L. Fleet conceived and designed the experiments, prepared figures and/or tables,
and approved the final draft.
• Sara J. Smith Wuitchik conceived and designed the experiments, analyzed the data,
prepared figures and/or tables, authored or reviewed drafts of the article, and approved
the final draft.
• Daniel M. Wuitchik conceived and designed the experiments, analyzed the data, prepared
figures and/or tables, authored or reviewed drafts of the article, and approved the final
draft.

Data Availability
The following information was supplied regarding data availability:
The data and code is available at GitHub: https://github.com/declan-taylor/sea_
cucumber_wasting.

Supplemental Information
Supplemental information for this article can be found online at http://dx.doi.org/10.7717/
peerj.14548#supplemental-information.

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