Eﬀect of Acute Seawater Temperature Increase on the
Survival of a Fish Ectoparasite
Mary O. Shodipo 1, Berilin Duong 2, Alexia Graba-Landry 3, Alexandra S. Grutter 2and
Paul C. Sikkel 4, 5, *
Institute of Environmental and Marine Sciences, Silliman University, 6200 Dumaguete City, Negros Oriental,
2School of Biological Sciences, The University of Queensland, St Lucia QLD 4072, Australia;
email@example.com (B.D.); firstname.lastname@example.org (A.S.G.)
3ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville QLD 4811, Australia;
4Department of Biological Sciences and Environmental Sciences Program, Arkansas State University,
Jonesboro, AR 72467, USA
5Water Research Group, Unit for Environmental Science and Management, North-West University,
Potchefstroom 2520, South Africa
Received: 17 July 2020; Accepted: 27 September 2020; Published: 4 October 2020
Extreme warming events that contribute to mass coral bleaching are occurring with
increasing regularity, raising questions about their eﬀect on coral reef ecological interactions. However,
the eﬀects of such events on parasite-host interactions are largely ignored. Gnathiid isopods are
common, highly mobile, external parasites of coral reef ﬁshes, that feed on blood during the juvenile
stage. They have direct and indirect impacts on their ﬁsh hosts, and are the major food source for
cleaner ﬁshes. However, how these interactions might be impacted by increased temperatures is
unknown. We examined the eﬀects of acute temperature increases, similar to those observed during
mass bleaching events, on survivorship of gnathiid isopod juveniles. Laboratory experiments were
conducted using individuals from one species (Gnathia aureamaculosa) from the Great Barrier Reef
(GBR), and multiple unknown species from the central Philippines. Fed and unfed GBR gnathiids
were held in temperature treatments of 29
C to 32
C and fed Philippines gnathiids were held at
C to 36
C. Gnathiids from both locations showed rapid mortality when held in temperatures 2
C above average seasonal sea surface temperature (32
C). This suggests environmental changes
in temperature can inﬂuence gnathiid survival, which could have signiﬁcant ecological consequences
for host-parasite-cleaner ﬁsh interactions during increased temperature events.
Gnathiidae; Isopoda; coral reefs; climate change; ocean warming; coral bleaching;
Great Barrier Reef; Coral Triangle
Among the myriad anthropogenic impacts on the world’s oceans, perhaps the most signiﬁcant
is the increase in temperature associated with production of greenhouse gases [
]. This warming
is responsible for large-scale changes in circulation and storm activity through melting of glaciers,
warming of air masses, and increased evaporation and salinity [
], and as such, warming may
have an indirect eﬀect on marine organisms. However, the majority of marine organisms are
ectothermic, and are therefore dependent on environmental temperature to gain adequate energy
for their own biological functions. The relationship between the performance of an ectotherm and
temperature is non-linear, where performance gradually increases with temperature until it reaches
Oceans 2020,1, 215–236; doi:10.3390/oceans1040016 www.mdpi.com/journal/oceans
a thermal optimum after which it rapidly declines (Thermal Performance Curve: [
]). Hence, the
eﬀect of increasing temperature on marine ectotherms may be more direct, aﬀecting physiology
and metabolism [
], which may have implications for growth, motor function, development,
reproduction and behaviour [
], which in turn may impact species’ abundance and distribution [
Therefore, increasing temperatures may be the most pervasive climate change factor inﬂuencing marine
]. Warming can subsequently impact entire ecological communities and ecosystems
by diﬀerentially impacting individuals and functional traits [19–21].
Coral reefs are one of the most biodiverse ecosystems in the world [
]. Even though the
rate of increase in sea surface temperature (SST) is 30% less in tropical oceans than the global
], coral reefs are also among the most sensitive ecosystems to changes in environmental
], and thus, are particularly at risk of thermal stress. Tropical ectotherms have a
narrow thermal tolerance range, and their thermal optimum is close to their thermal maximum, as
they have evolved under relatively stable thermal conditions [
]. As SSTs rise, corals and coral reef
associated organisms are being subjected to higher temperatures (29–31
C) for increasing periods
of time [
]. As a consequence many tropical organisms are thought to be living at or close to their
thermal limits [
]. SSTs are predicted to continue to rise over the coming years [
] and extreme
warming events, resulting in global scale coral bleaching, are occurring with increasing regularity and
severity [30–34], causing degradation of coral reef habitats [22,30,31,35,36].
In addition to the corals themselves, research on the eﬀects of marine heatwaves has also
focused heavily on ﬁshes [
], which are also typically included in coral reef monitoring eﬀorts.
However, studies have almost completely ignored the myriad of small, cryptic, species, which make
up a disproportionate amount of coral reef biodiversity [
]. One such group are parasites,
which make up the largest consumer strategy globally [
] and comprise an estimated 40% of
global biodiversity [
]. In addition to host behavior, physiology, and population dynamics,
parasitic organisms have been shown to have impacts on interspeciﬁc interactions, energy ﬂow,
and the structure, ecology, and biodiversity of communities [
]. Parasites are particularly
diverse on coral reefs [
] with an estimate of over 20,000 species on the Great Barrier Reef (GBR)
]. However even with such a large presence in coral reef communities, they are signiﬁcantly
underrepresented in ecological studies [
]. Coral reef parasites are also ectothermic, and as
such, may be aﬀected by changes to their environmental temperature [
]. Some parasites are
ectoparasitic and would be highly vulnerable to increased temperatures. Ectoparasites are also likely to
be directly impacted by the temperature itself, in addition to being indirectly aﬀected through changes
in community structure due to temperature impacts on hosts [
] and other organisms. For example,
the life cycle of a monogenean ectoparasite (Neobenedinia) was faster and the life span of their larvae
(oncomiracidia) decreased as temperatures increased from 22 ◦C to 34 ◦C .
Gnathiid isopods are one of the most common ectoparasites in coral reef habitats [
]. They are
small crustaceans, typically 1–3 mm long, that do not permanently live on their ﬁsh hosts [
In fact, with few exceptions, they associate only long enough to extract a blood meal and may therefore
also be referred to as “micropredators” [
]. After feeding on tissue and blood from their ﬁsh host
they return to the benthos to molt and progress to the next developmental stage [
]. They are
only parasitic during their three juvenile stages, and no longer feed once they metamorphose into an
adult. Gnathiids can have signiﬁcant impacts on their hosts [
]. Direct eﬀects include inﬂuencing
], physiology [
], and mortality [
]. Indeed, as few as one gnathiid can kill a young
juvenile ﬁsh [
]. Indirect eﬀects include transmission of blood-borne parasites [
] and wounds
that can facilitate infection [
]. Gnathiids are also the most common items in the diet of many cleaner
ﬁshes, including Labroides dimidiatus [
], a species with far-reaching ecosystem eﬀects [
Indeed, environmental perturbations, including a coral bleaching event with water temperatures
reaching up to 30
C, resulted in an 80% decline in L. dimidiatus at Lizard Island, GBR [
the processes leading to this decline remain unknown.
A long-term monitoring study of gnathiid isopods oﬀLizard Island, GBR, revealed a signiﬁcant
decrease in gnathiid abundance during extreme warm-water periods associated with bleaching events,
compared with cooler periods in the same year or during non-bleaching years [
]. However, the cause
of this decline was unclear. Sikkel et al. (2019) [
] hypothesized that the direct eﬀects of temperature
on gnathiid mortality may have partly contributed to the decline in gnathiid abundance. The aim of
this study therefore, was to assess the direct eﬀect of a rapid increase in seawater temperatures on
mortality of shallow-reef gnathiid isopods. By conducting laboratory experiments on gnathiids in two
coral reef regions subject to bleaching, GBR, Australia [
], and Philippines [
], we show
that a rapid increase in temperature causes signiﬁcant increases in mortality.
2. Materials and Methods
2.1. Study Sites
This study was conducted between January and February 2018 at the Lizard Island Research
Station (LIRS), northern GBR and between July and October 2017 at the Silliman University–Institute of
Environmental and Marine Sciences (SU-IEMS), Dumaguete City, Negros Oriental, Visayas, Philippines.
2.2. Gnathiid Collection
For the GBR study, gnathiids were obtained from a culture maintained at LIRS since 2001, which
uses the continual availability of wrasse Hemigymnus melapterus (Labridae) as hosts [
]. The culture
is outdoors and uses a ﬂow-through seawater system that obtains water directly from the nearby
reefs. The previous exposures of the experimental (and previous generations) of gnathiids would have,
therefore, reﬂected similar temperatures to the ocean and land ones .
Gnathiids for the Philippines study were collected from the shallow fringing coral reefs (<10 m)
of Cangmating reef (9
18.38” N, 123
58.91” E) and Agan-an reef (9
2.6” N, 123
41.5” E) in
Sibulan and from Bantayan reef (9
49.22” N, 123
43.43” E) in Dumaguete City, all within Negros
Oriental Province. The Bantayan reef has small patch reefs with inshore seagrass beds. Cangmating
and Agan-an have larger patch reefs and inshore seagrass beds. Gnathiids are common at all three
]. Gnathiids were collected using light traps, adapted from Artim et al. (2015) [
Artim and Sikkel (2016) [
]. The traps were set at dusk and retrieved the following morning and
then transported by boat to the SU-IEMS laboratory where they were emptied into individual 10 L
plastic buckets with aerators. The contents of each trap were ﬁltered with a funnel and 55
mesh. The gnathiids were then sorted using a stereoscope and placed in an aquarium (27 L) with fresh,
ﬁltered, aerated seawater. The species of gnathiids collected were unknown due to diﬃculty with
species identiﬁcation of the juvenile stages [
], and the fact that no species have yet been formally
described from our Philippines study region.
2.3. Experimental Protocol
At both locations, gnathiid mortality was deﬁned as the absence of detectable movement, even after
disturbance (e.g., by moving the vial it was held in while viewing it under the microscope).
2.3.1. Great Barrier Reef
Gnathiids, all belonging to the species Gnathia aureamaculosa, were collected from the culture in
the morning and afternoon, and placed together into 75 mL holding containers ﬁlled with seawater.
They were collected by moving a black tray (35
5 cm) up the side of the gnathiid culture
tank and were removed using a pipette. From the holding containers, gnathiids were individually
transferred into 5 mL vials that were half-ﬁlled with seawater. These vials were then individually
labelled. Collecting and processing took approximately 2 to 4 h, depending on the catch size of the
day (ranging from 9 to 226 gnathiids). The daily number varied as a result of ﬂuctuations in the
number that were active, most likely due to normal high variation in their population dynamics [
A mixture of fed and unfed gnathiids was used, and it was not known how much time elapsed since
the last feeding. Gnathiids were not fed for practical reasons. After processing the gnathiids, the vials
were randomly allocated, in a balanced way (approximate equal number), to a temperature treatment
and aquarium replicate combination; there were three aquarium replicates per temperature treatment.
Vials were labelled with a unique number across all replicates. Only the lids of the vials were labelled,
reducing any potential bias when viewing them under the microscope. It also made it easier to monitor
and return them to their respective treatment and aquarium daily. Vials were held underwater in
plastic baskets (17
10 cm), one for each treatment and replicate (n=9 baskets). Baskets had four
mesh (1 mm
) windows (12
5 cm) on the sides and one on the lid (12
12 cm) to allow for ﬂow of
water. A dive weight was used to submerge the baskets. Aquaria were supplied with ﬂow-through
seawater, with seawater that was either chilled or heated in a sump under the aquarium benches and
pumped up to the aquaria. Each bench had a diﬀerent temperature treatment and held 10 aquaria
(previously used for another experiment, see Graba-Landry et al. 2020 [
]). Three aquaria were
randomly selected per bench and allocated to replicates.
We estimated the predicted ambient seawater temperature (29.25
0.013 SE) based on the
Australian Institute of Marine Science long-term average water temperature for February [
S1). Actual average daily seawater temperature during the experiment was 29.0
0.67 SE (February
1 to 23, 2018 available only). The temperature of the water that gnathiids had been maintained in
throughout their lifetimes was not available. However, the temperature of incoming water from the
station’s holding tanks was on average 1.4
C warmer than the ocean, when sampled at two sources at
three times of the day (09:00, 15:00 and 21:00 h from 15 to 20 October, 2018) relative to the same period
in the ocean .
Temperature was manipulated in an outdoor seawater ﬂow-through system at LIRS using purpose
built 1KW steel bar heaters and chillers (Teco
) in a header or sump tank. Each sump, one per
temperature treatment, fed replicate 40 L tanks with the appropriate experimental ﬂow-through
seawater using 1000 L hr
) at a rate of approximately 1 L minute
. Tanks were
wrapped in Insulbreak
insulation to stabilize water temperatures. Temperature (
C) was also
measured at 12:00 h daily from each of the nine tanks housing the gnathid cultures/vials using a
portable temperature probe (Comark
) calibrated to 26
C and 30
C (National Association of
Testing Authorities certiﬁed) to ensure temperature remained stable across treatments. Experimental
temperatures at 12:00 h per treatment, averaged across the means of the three replicate aquaria, were:
0.07 SE, 31
0.02 SE, and 32
0.02 SE. Temperatures were very
similar among replicates within a treatment, (Figure S2). One calibrated temperature logger (HOBO
Pendant temperature/light logger, UA-002-08) per treatment also recorded the temperature every 2 h
throughout the course of the study to account for diurnal ﬂuctuations in temperature [mean (SE) per
treatment: 29 ◦C: 28.9(0.042); 31 ◦C: 31.2(0.035): 32 ◦C: 31.9(0.06); Figure S3].
Each day, one random basket from each treatment was removed (to reduce time exposed to air
temperature). The vials from each basket were rinsed in freshwater and placed in a large tub (all
treatments were examined together to avoid bias). Each vial was then examined under a dissection
microscope to check for gnathiid mortality. Vials with alive gnathiids were sorted back into their
respective treatments/replicates and placed back into the aquaria. This was repeated for each of the
remaining baskets from each treatment-replicate combination. Gnathiids were monitored until all had
died (except for four survivors, see Results for details). Vials with dead gnathiids were preserved for
later to undertake headwidth measurements, by adding a few drops of formalin into the seawater.
Unfed juvenile gnathiids were given one day to acclimatize in an aquarium after collection,
before host ﬁsh, Dascyllus trimaculatus (Pomacentridae) and various species of Labridae, were placed
in the aquarium overnight to allow them to feed. The gnathiids did not feed again for the duration
of the experiment. The following day, fed, mobile and healthy-looking individuals were selected.
However, as the gnathiids’ species and therefore the consequent size range for each stage was not
known, they could not be separated by juvenile stage as in the GBR study. Instead they were sorted
into two size classes (<2 mm and >2 mm, to account for any eﬀect of size of the gnathiid on its molting
rate and survival.
Gnathiids were then placed in 270 mL plastic containers, 5–10 gnathiids per container,
with plankton mesh (55
m) secured on the top, and the containers were submerged in one of
ﬁve 27 L aerated aquaria, each with a diﬀerent set temperature. Each container was labelled with the
size class, treatment, trial and replicate. The ﬁrst trial consisted of 5 temperature treatments, ambient
C and 36
C. A second trial was also conducted to obtain a ﬁner resolution of the
temperature eﬀect, with treatments of 30
C and 35
C. Aquaria were individually
heated gradually with 100W and 200W aquarium electric heaters (Venusaaqua
) over a 10 h period to
their desired temperature. Temperature readings were taken daily with an aquarium-mounted digital
) to ensure the desired water temperatures were maintained and to calculate
the average temperature for each treatment per trial (Table S1a,b). Containers from each treatment
were inspected daily for evidence of changes in gnathiid development and mortality. Dead gnathiids
were removed from the containers and molted adult males were preserved in ethanol for future species
identiﬁcation. The experiment was concluded for each treatment when all gnathiids were dead or
when 20 d had passed. One third of the water in each aquarium was removed daily and replaced with
ambient temperature, ﬁltered, fresh seawater. Over the 20 d duration of each replicate the aquaria
used for each temperature treatment was alternated every week (once per replicate) to ensure there
were no confounding eﬀects associated with individual aquaria. Three replicates of each temperature
treatment were run for each trial. Trials 1 (n=369 gnathiids) and 2 (n=318 gnathiids) had a range of
60–76 and 59–68 gnathiids per temperature treatment respectively (Table S2a,b).
The baseline ambient temperatures for Trials 1 (28
C) and 2 (30
C) were similar to the SST in the
Bohol Sea, Philippines, which ﬂuctuated by about 3 ◦C (about 27–30 ◦C) during 2017; the SST during
the experiment (July–October 2017) averaged at 30 ◦C±0.04 SE. .
2.4. Statistical Analyses
2.4.1. Great Barrier Reef
One live unfed gnathiid (stage three, 15 d), two adult males (alive, 15 d; dead, 29 d) and three
adult females (alive, 15 and 24 d; dead, 16 d) were excluded from the data. These gnathiids were
excluded because they were adults and thus their longevity would be diﬀerent to that of the juveniles.
The single juvenile that was still alive when we terminated the experiment was omitted for simplicity
and consistency. We categorized the three juvenile stages based on their headwidth (stage one: 0.14–0.2,
stage two: 0.21–0.24, stage three: 0.25–0.32 mm) [
]. Due to the large diﬀerence in sample size per
unfed/fed status (based on the presence of an engorged gut), we conducted separate analyses for unfed
(n=1133) and fed gnathiids (n=87).
To test whether survival of gnathiids diﬀered among temperature treatments, we used a
proportional hazards Cox mixed-eﬀects model with temperature treatment and gnathiid juvenile stage
as categorical ﬁxed eﬀects, aquarium as a random factor, and gnathiid headwidth as a covariate (Table 1
and Table S3). We used ambient temperature (29
C) and juvenile stage one as the baselines for the
analyses. We used the function “coxme” in the package “coxme” [
] and function “Anova” in
the package “car” [
]. We tested the Cox model assumption of proportionality using the Global
test statistic in the function “coxph” and “cox.zph” in the package “coxme” and graphically using a
smoothed spline plot of the Shoenfeld residuals relative to time (see Tables S3 and S4 for results and
Figures S4 and S5 for spline plots).
Table 1. Great Barrier Reef;
Analysis of deviance table (Type II tests) for unfed gnathiid survival
among temperature treatments and juvenile stages for Cox model. Bolded values are ones mentioned
in main text. *** p<0.001.
Df Chisq Pr(>Chisq)
Temperature 2 183.76 <0.0001 ***
Headwidth 1 1.87 0.1719
Stage 2 26.93 <0.0001 ***
Temperature ×Headwidth 2 0.07 0.9639
Temperature ×Stage 4 3.06 0.5471
Headwidth ×Stage 2 23.85 <0.0001 ***
Temperature ×Headwidth ×Stage 4 6.51 0.1642
In the size class <2 mm (n=168 gnathiids) for Trial 1, ﬁve (3%) gnathiids molted into adult
females and nine (5%) into males. In the size class <2 mm (n=153) for Trial 2, no gnathiids molted
into adults. In contrast, for the larger size class >2 mm for Trial 1 (n=201), 20 (10%) gnathiids molted
into females and 85 (42%) into males. In the size class >2 mm (n=165) for Trial 2, 37 (22%) gnathiids
molted into females and 68 (41%) into males. In this study, newly metamorphosed males were ﬁrst
observed after day 1 in Trial 2 and day 2 in Trial 1, and no additional males appeared after day 5 in
Trial 2 and day 7 in Trial 1. The mean number of days juvenile gnathiids molted into males for all
treatments was 3.39 ±0.75 and 3.23 ±0.16 for Trials 1, and 2, respectively.
To test whether survival of gnathiids diﬀered among temperature treatments, we used the same
statistical methods as for the GBR data, with some modiﬁcations to the model. Temperature treatment
was a ﬁxed eﬀect, and size class, life stage (male, female, or juvenile) and container (which the gnathiids
were kept in) were treated as random eﬀects. The ambient temperature of 28
C was used as the
baseline for analysis for Trial 1 and 30
C for Trial 2. Assumptions of proportionality were met for
both analyses (both Global tests: p>0.05, see Tables S5 and S6 for results and Figures S6 and S7 for
All applicable international, national, and/or institutional guidelines for the care and use of animals
were followed. All procedures performed in studies involving animals were in accordance with the
ethical standards of Silliman University, Arkansas State University, The University of Queensland,
and the Government of Australia and the Philippines.
3.1. Great Barrier Reef
3.1.1. Unfed Gnathiids
From the 1220 gnathiids whose survival was followed over time, 93% were unfed individuals.
For unfed individuals, the numbers of gnathiids per stage and per temperature was relatively even
within each of the 29
C, and 32
C temperature treatments (stage one: 186, 198, 210; stage two:
73, 66, 71; stage three: 113, 113, 103, respectively). There was a signiﬁcant eﬀect of temperature
on gnathiid survival (p<0.0001, Table 1, Figure 1), due to a signiﬁcantly lower survival at 32
compared with the 29
C baseline temperature (p=0.016, Table S7). The interaction between gnathiid
headwidth and juvenile stage was signiﬁcant (p<0.0001, Table 1); when further explored separately by
stage, the association was largely due to a weakly positive relationship between gnathiid survival and
gnathiid headwidth in stage one (p<0.0001, Table S9a).
3.1.2. Fed Gnathiids
For fed individuals, the numbers of gnathiids per juvenile stage and per temperature were
also relatively even between the 29
C, and 32
C temperature treatments (stage one: 8, 6, 6;
stage two: 17, 15, 13; stage three: 8, 7, 7, respectively). Three (3.4%) contained more blood than clear
material (i.e., plasma) in their gut, the remainder had a clear gut. Of the 87 individuals followed, 60%
had molted during the course of the study. Survival diﬀered according to an interaction between
temperature and juvenile stage (p=0.0085, Table 2); when further explored separately by stage
(Figure 2), the eﬀect of temperature was signiﬁcant for stage two (p<0.0001), and three (p=0.0009,
Figure 2b,c, Table S10b,c), with the strongest eﬀect of temperature being that between the baseline
C) and the 32
C treatments for stage three (Table S10c, Figure 2c). Survival diﬀered according
to an interaction between temperature and headwidth (p=0.0480, Table 2); when further explored
separately by temperature treatment, the eﬀect of headwidth was largely due to non-signiﬁcant weakly
positive relationships between survival and headwidth at 29
C (p=0.0758) and 32
0 5 10 15 20
Temperature=29C Temperature=31C Temperature=32C
Figure 1. Lizard Island Research Station
; Kaplan-Meier survival curves for unfed gnathiids per
temperature treatment. Shaded areas are 95% conﬁdence intervals.
Oceans 2020, 1, FOR PEER REVIEW 8
Figure 2. Cont.
Oceans 2020, 1, FOR PEER REVIEW 9
Figure 2. Great Barrier Reef; Kaplan-Meier survival curves for fed gnathiids per temperature
treatment for (a) stage one, (b) stage two, and (c) stage three juveniles. For ease of interpretation, 95%
confidence intervals are not included.
Table 2. Great Barrier Reef; Analysis of deviance table (Type II tests) for fed gnathiid survival among
temperature treatments and juvenile stages for Cox model. Bolded values are ones mentioned in main
text. ** P < 0.01, *** P < 0.001.
Df Chisq Pr(>Chisq)
Temperature 2 28.2063 7.50E-07 ***
Headwidth 1 1.9549 0.16206
Stage 2 21.3179 2.35E-05 ***
Temperature × Headwidth 2 6.0753 0.04795 *
Temperature × Stage 4 13.6392 0.00854 **
Headwidth × Stage 2 3.0686 0.21561
Temperature × Headwidth × Stage 4 3.3548 0.5003
3.2.1. Trial 1
There was a significant effect of temperature on gnathiid survival (p < 0.0001) in Trial 1, driven
by lower survival curves for the 36 °C (p < 0.0001) and 32 °C (p = 0.024) treatments, compared with
the 28 °C baseline temperature treatment (Tables 3 and S12, Figure 3).
Figure 2. Great Barrier Reef;
Kaplan-Meier survival curves for fed gnathiids per temperature treatment
) stage one, (
) stage two, and (
) stage three juveniles. For ease of interpretation, 95% conﬁdence
intervals are not included.
Table 2. Great Barrier Reef;
Analysis of deviance table (Type II tests) for fed gnathiid survival among
temperature treatments and juvenile stages for Cox model. Bolded values are ones mentioned in main
text. ** p<0.01, *** p<0.001.
Df Chisq Pr(>Chisq)
Temperature 2 28.2063 7.50 ×10−7***
Headwidth 1 1.9549 0.16206
Stage 2 21.3179 2.35 ×10−5***
Temperature ×Headwidth 2 6.0753 0.04795 *
Temperature ×Stage 4 13.6392 0.00854 **
Headwidth ×Stage 2 3.0686 0.21561
Temperature ×Headwidth ×Stage 4 3.3548 0.5003
3.2.1. Trial 1
There was a signiﬁcant eﬀect of temperature on gnathiid survival (p<0.0001) in Trial 1, driven by
lower survival curves for the 36
C (p<0.0001) and 32
C (p=0.024) treatments, compared with the
28 ◦C baseline temperature treatment (Table 3and Table S12, Figure 3).
0 5 10 15 20
Temperature=28C Temperature=30C Temperature=32C Temperature=34C Temperature=36C
Figure 3. Philippines;
Trial 1, Kaplan-Meier survival curves for gnathiids per temperature treatment.
Shaded areas are 95% conﬁdence intervals.
Table 3. Philippines;
Analysis of deviance table (Type II tests) for Trial 1 and 2 gnathiid survival for
Cox model. Bolded values are ones mentioned in main text.
Trial Df Chisq Pr(>Chisq)
1 Temperature 4 24.927 <0.0001
2 Temperature 4 8.4374 0.07681
3.2.2. Trial 2
Overall, the eﬀect of temperature on gnathiid survival was not quite statistically signiﬁcant
p=0.0768, Table 3
). Nevertheless, the 35
C treatment had a much steeper survival curve than that
for the 30 ◦C baseline (Figure 4) (p=0.0057, Table S13).
0 5 10 15 20
Temperature=30C Temperature=32C Temperature=33C Temperature=34C Temperature=35C
Figure 4. Philippines;
Trial 2, Kaplan-Meier survival curves for gnathiids per temperature treatment.
Shaded areas are 95% conﬁdence intervals.
With ocean temperatures predicted to rise 3
C by the end of the century [
], the eﬀects of
ocean warming on coral reef organisms have received an increasing amount of attention. However,
such studies largely ignore the cryptofauna that comprises most of coral reef’s biodiversity and biomass,
including parasites [
]. In the only long-term monitoring study of any marine parasitic crustacean,
Sikkel et al. (2019) [
] reported that during extreme warm-water events in the GBR parasitic gnathiid
isopod populations crashed. The ﬁndings reported here are consistent with their hypothesis that this
may be attributable, in part, to a direct eﬀect of temperature on gnathiid mortality. Such an eﬀect
of temperature on the larvae of a tropical ectoparasite has been shown for monogeneans on farmed
tropical ﬁsh .
The present study is the ﬁrst to examine eﬀects of acute temperature increases on this common reef
ﬁsh ectoparasite. In our study, gnathiids from both the GBR in Australia and Negros Oriental in the
Philippines demonstrated rapid mortality in temperatures raised to above average SST, suggesting that
environmental changes in temperature can inﬂuence gnathiid survival. In the Philippines, temperatures
as little as 2
C (i.e., 32
C) above average seasonal SST (30
C) caused signiﬁcantly lower survival,
with increasingly steep survival curves at 35
C, with the steepest at 36
C, where no gnathiids survived
past ﬁve days. Unfed gnathiids on the GBR had lower survival at 32
C compared with 29
C, an eﬀect
which was consistent across all three juvenile stages. For fed gnathiids on the GBR, the eﬀect of
temperature was signiﬁcant for juvenile stages two and three, with the strongest eﬀect of temperature
on stage three, also between the 32
C and 29
C treatments. It is, therefore, likely that gnathiids
from both the Philippines and Australia may be living near their thermal limit, as small increases
in temperature from the annual seasonal mean have resulted in increased mortality in organisms
from both regions. These results indicate not only that an acute change of temperature to just 32
decreases the survival of gnathiids, but that the eﬀect of increased temperature is greater on the larger
In the GBR we found evidence that greater gnathiid headwidth, not just juvenile stage,
increased gnathiid survival. For unfed gnathiids, there was a weakly positive relationship between
gnathiid survival and gnathiid headwidth, but only in juvenile stage one. For fed gnathiids, there was
also a weakly positive relationship between survival and headwidth, but only at 29
C and 32
Gnathiid length is correlated with headwidth [
] and thus likely with mass also. Both results
suggest that even small increases in gnathiid size within a juvenile stage can increase gnathiid
survival; these ﬁndings also supported our decision to include both headwidth and stage in the
statistical model as being important factors to consider when modelling gnathiid juvenile survival.
Such a diﬀerence in the thermal response related to size may be due to the increased metabolic
demand caused by the increase in temperature, an eﬀect which may lead to an energetic deﬁcit for
smaller individuals if enough food cannot be obtained, therefore, creating a metabolic mismatch
between energy obtained versus energy required . Alternatively, there may possibly be a higher
baseline metabolism or higher growth rate at smaller sizes, which then slows down as they reach the
maximum size for that stage, resulting in smaller sizes using up their reserves faster than larger sizes.
Furthermore, the energetic demands of development may also diﬀer among juvenile life-history stages.
Thus increased metabolic demand for basal processes (such as cell maintenance) as a result of increases
in temperature, coupled with diﬀerential energetic requirements for development may also explain the
variation in the thermal response among juvenile stages in our study. Therefore, understanding the
eﬀect of increasing temperature on individual metabolism and survival also requires an understanding
of food resources and availability .
Overall, these results suggest that even with a small increase of 2–3
C above the normal ambient
mean, raised temperature can ultimately lead to increased gnathiid mortality. However, there were
some key diﬀerences in the experimental protocol between the GBR and Philippines studies that should
be considered. First, only one species of gnathiid was used in the GBR experiment, compared to at
least three (all undescribed, M.O.S. personal observation) species present in the pool of gnathiids used
for the Philippines experiment. Second, because these species were unknown, we were unable to
conﬁdently separate juvenile gnathiids into their diﬀerent stages, and so used size class as a proxy.
Therefore, we cannot discount the possibility of some among-species and life-stage variation in thermal
tolerance. Finally, in contrast to the Philippines, in the GBR study the time the gnathiids were last
fed was unknown. This would account for much of the unexplained variation in survivorship in the
analysis of the GBR data, as the variation in resources available to the gnathiid, in the form of a blood
meal, would decrease over time since their last feeding event. In addition, it should be noted that,
in both studies, the gnathiids were not fed for the duration of the experiment, and thus starvation
may have been a contributing cause of mortality. While starvation may have inﬂuenced mortality
of gnathiids among the treatments (as suggested by increased mortality over time in the ambient
temperatures), the rates of mortality at higher temperatures were greater, with rapid mortality taking
place very early on in the experiments (e.g., one to ﬁve days in the Phillipines). This supports the
interpretation that increased temperatures inﬂuence gnathiid survival directly. It is of relevance that
marine “heatwaves” (which are categorised as periods of abnormally high SST lasting for longer
than ﬁve days [
]) have been predicted to become more frequent, longer and more severe [
Our observations of rapid gnathiid mortality even after just one day suggests there may be a decline in
gnathiid survival from early on in a heatwave, so that gnathiid populations may be heavily impacted
if there are more frequent and severe heatwaves in the future.
Our ﬁndings appear consistent with data for other tropical marine invertebrates, which have an
upper thermal tolerance that is not far above normal sea temperature (reviewed in [
]). For example,
in a meta-analysis on bivalves, and a study on porcelain crabs, tropical species were found to have
upper thermal limits that were closer to the maximum temperature of their habitat than temperate
]. Tropical species of bivalves have also been shown to have a smaller thermal tolerance
window than temperate species [
]. This is thought to be due to tropical marine organisms being
more sensitive to changes in temperature as they have evolved under relatively invariable thermal
]. Other studies on marine invertebrates have also shown increased mortality with high
], with hermatypic corals being particularly sensitive to increases, with SSTs needing to
rise only a few degrees for bleaching to occur [25,26,31,122].
There are a number of studies investigating the potential impact of temperature increase associated
with climate change on parasite communities and aquatic parasite-host interactions. The majority of
these studies have been on endoparasitic trematodes from temperate regions [
was consistently observed to have a signiﬁcant eﬀect on the survival times of trematodes in their
free-living juvenile stage, with survival rates decreasing as temperature increased (e.g., [
Similarly, temperature has been reported to have an eﬀect on parasitic barnacles (rhizocephalans),
with their prevalence decreasing at higher temperatures .
In one of the few other studies on ectoparasites, Conley and Curtis (1993) [
] found that,
in temperatures of 8–20
C, survival of copepodids was also inversely proportional to temperature.
This same trend was observed in the survival rates of monogeneans, and isopods (Cymothoidae) in two
studies in sub-tropical regions [
] and one study of monogeneans in a tropical region [
]. In all
three studies, temperature treatments of 30
C and above had the lowest survival rates [
Similar results were also observed with trematode cercariae from sub-tropical regions [
Summer temperatures for these lower latitudes parasites are in the range of 30–31
C, which suggests
that like gnathiids in the warmer months they are living close to their thermal limits.
Although, this study focused on eﬀects of temperature on mortality, increased temperature can also
have sub-lethal eﬀects on marine organisms, impacting their ability to perform essential tasks [
Based on a review of the literature, Lough (2012) [
] suggested that temperatures between 30–32
may reﬂect a potential temperature threshold where a proportion of reef organisms’ physiological
processes are negatively impacted. Higher temperatures may also aﬀect the ability of parasites with
mobile life history stages (such as gnathiids) to successfully detect and associate with a host. To our
knowledge there are no studies that speciﬁcally examine this. However, the ability to physically reach
a host by swimming does appear to be inﬂuenced by temperature. For temperate parasitic copepods
in their free-living stage, the duration of swimming activity was found to be inversely related to water
]. For newly emerged cercariae, swimming speed increased in higher temperatures
C). However, the speed declined over time, with rate of decline increasing with temperature.
This resulted in higher swimming speeds, but for shorter durations in water of 30
C and above [
In a sub-tropical study, cercariae infectivity also increased with temperature with maximum infectivity
occurring at 30
C before declining at 36
C and 40
]. This could be attributable to greater
cercariae swimming activity [
]. Although, we did not quantify the eﬀects of temperature on
movement, in the Philippines study it was apparent that gnathiids moved more slowly and less
frequently at temperatures of 32
C and above, with movement decreasing further as temperature
increased, and also with apparent eﬀects greater for the larger size class (
M.O.S. personal observation
Elevated temperatures may also impact host physiology, behavior and survival in ways that
impact the balance between parasite and host. For parasitic barnacles (rhizocephalans), the eﬀects of
temperature on infected host mortality (and consequent transmission) could threaten their survival,
with models showing that just an increase of 2
C in ambient temperature could cause local parasite
]. In contrast, reef ﬁshes can live further away from their thermal limits than
gnathiids were observed to do in this study and in some cases can tolerate temperatures of up
. However, they can still experience sub-lethal eﬀects with smaller increases in
temperatures [3,6,12,14,15,142,144–146], which could also impact host-parasite interactions.
Large hosts, like many reef ﬁshes, can also leave areas of warm water for cooler water, or leave
habitat impacted by coral bleaching for other habitats [
], depriving gnathiids and other
similar ectoparasites, like natatory-stage cymothoid isopods of hosts [
]. The potentially impaired
physiological and swimming ability of the parasite, combined with direct eﬀects on mortality and host
availability, could result in a decline in parasite populations. However, the ability of some gnathiids
to feed on invertebrate hosts [
], combined with weakened immune response for the smaller,
less mobile, ﬁsh species could leave ﬁsh more susceptible to ectoparasites, and thus, compensate for
the loss of larger hosts. Indeed, during the 2016–2017 mass bleaching event on the GBR, there was
a signiﬁcant decrease in the numbers of larger, more mobile host ﬁshes in shallow areas, with only
smaller, site-attached species remaining [
]. This could have also contributed signiﬁcantly to the crash
in gnathiid populations observed by Sikkel et al. (2019) [
]. However, it should also be noted that
as gnathiids are mostly free-living and have a temporary association with their hosts, they too can
potentially avoid higher water temperatures. This might happen passively by the gnathiid “hitching a
ride” whilst feeding on their host, a process which can last from a few minutes up to a few hours [
The gnathiids may, thereby, be transferred to diﬀerent locations [
]. However, as knowledge
of the dispersal mechanisms of gnathiids, the infection rates of host ﬁsh, and ﬁsh movements after
disturbances is limited, the proportion of the gnathiid populations that could transfer location with
their hosts remains unknown.
Another indirect eﬀect of increased SST may be eﬀects of warming on predators of gnathiids
and other ectoparasites’ free-living stages. In particular, coral polyps are a major source of predation
on juvenile gnathiids [
], and thus high coral mortality associated with warm-water events,
combined with the loss of cleaner ﬁsh [
], which prey on ectoparasites [
], might increase living
space and decrease predation on gnathiids. Indeed, once water cools following a bleaching event
and most corals are dead, gnathiid populations appear to recover rapidly [
]. While, oceans are also
experiencing increased acidiﬁcation [
], Paula et al. (2020) [
] found no eﬀect of acidiﬁcation on
the mortality of the same GBR gnathiid isopod as that studied here.
As parasites have a signiﬁcant role in ecosystem function, changes in parasite abundance may
pose consequences for ecological communities [
]. Therefore, while the diversity of coral reef
parasites and their hosts makes it diﬃcult to draw general conclusions on how warming events will
impact parasite-host interactions, it remains important to further investigate parasite responces to both
the direct and indirect eﬀects of warming [
]. Future studies on gnathiids examining sublethal thermal
eﬀects on molting, physiology, locomotion, host-detecting mechanisms and reproductive performance
will provide a more comprehensive understanding of eﬀects of temperature on host-parasite interactions
in coral reef systems.
The following are available online at http://www.mdpi.com/2673-1924/1/4/16/s1.
Table S1: Philippines; Average water temperature of aquaria for ﬁve treatments over three aquarium replicates,
Table S2: Philippines; Sample size of larval gnathiid isopods <2 mm and >2 mm in length in ﬁve diﬀerent
temperature treatments over three aquarium replicates, Table S3: Great Barrier Reef; Tests of proportionality,
using function “cox.zph” in library “coxme” in R 3.2.5, for full model for unfed gnathiid survival among
temperature treatments and juvenile stages, Table S4: Great Barrier Reef; Tests of proportionality, using function
“cox.zph” in library “coxme”, for full model of fed gnathiid survival among temperature treatments and juvenile
stages, TableS5: Philippines; Tests of proportionality, using function “cox.zph” in library “coxme” in R 3.2.5, for full
model for Trial 1 gnathiid survival among temperature treatments, Table S6: Philippines; Tests of proportionality,
using function “cox.zph” in library “coxme” in R 3.2.5, for full model for Trial 2 gnathiid survival among
temperature treatments, Table S7: Great Barrier Reef; Summary output for full model for unfed gnathiid survival
among temperature treatments and juvenile stages for Cox model, Table S8: Great Barrier Reef; Summary output
for full model for fed gnathiid survival among temperature treatments and juvenile stages for Cox model, Table S9:
Great Barrier Reef; Analysis of deviance tables (Type II tests) and summary outputs for unfed gnathiid survival
for separate Cox models for each juvenile stage, Table S10: Great Barrier Reef; Analysis of deviance tables (Type II
tests) and summary outputs for fed gnathiid survival for separate Cox models for each juvenile stage, Table S11:
Great Barrier Reef; Analysis of deviance tables (Type II tests) and summary outputs for fed gnathiid survival for
separate Cox models for each temperature treatment, Table S12: Philippines; Summary output for full model for
Trial 1gnathiid survival among temperature treatments for Cox model, Table S13: Philippines; Summary output
for full model for Trial 2 gnathiid survival among temperature treatments for Cox model. Bolded values are ones
mentioned in main text, Figure S1: Seawater temperature for Great Barrier Reef data, Figure S2: Great Barrier
Reef; Temperatures, measured using a handheld device at 12:00 h, for three replicate aquaria per temperature
treatment, Figure S3: Great Barrier Reef; Water temperatures in an aquarium over duration of study for each of
the temperature treatments between February 1 and March 2 2018, Figure S4: Great Barrier Reef; Scaled Shoenfeld
residual plot for full model testing unfed gnathiid survival relative to time (days), Figure S5: Great Barrier Reef;
Scaled Shoenfeld residual plot for full model testing fed gnathiid survival relative to time (days), Figure S6:
Philippines; Scaled Shoenfeld residual plot for full model testing gnathiid survival relative to time (days) for Trial
1, Figure S7: Philippines; Scaled Shoenfeld residual plot for full model testing gnathiid survival relative to time
(days), for Trial 2.
Conceptualization, P.C.S. and A.S.G.; methodology, P.C.S., A.S.G., M.O.S. and B.D.;
validation, A.S.G. and P.C.S.; formal analysis, A.S.G., M.O.S. and A.G.-L.; investigation, M.O.S. and B.D.; resources,
P.C.S., A.S.G., M.O.S. and A.G.-L.; data curation, M.O.S. and B.D.; writing—original draft preparation, M.O.S.,
B.D., P.C.S. and A.S.G.; writing—review and editing, M.O.S., A.G.-L. and P.C.S.; visualization, A.S.G. and M.O.S.;
supervision, P.C.S. and A.S.G.; project administration, A.S.G., P.C.S. and M.O.S.; funding acquisition, A.S.G.,
A.G.-L. and P.C.S. All authors have read and agreed to the published version of the manuscript.
This research was funded by the Australian Research Council (A00105175, A19937078, ARCFEL010G,
DP0557058, DP120102415), Sea World Research and Rescue Foundation Australia (SWR/2/2012), and the US
National Science Foundation (OCE-1536794, PC Sikkel, PI).
We thank the many volunteers and the Lizard Island Research Station (GBR) staﬀwho helped
maintain the gnathiid culture and provided equipment and facilities. We also thank Jessica Vorse, who conducted
an earlier pilot study on the eﬀects of temperature on gnathiid survival on the Great Barrier Reef; this was
invaluable in the development of the ﬁnal methodology implemented in the present study. We thank the
municipality of Sibulan, and Dumaguete City, Negros Oriental, Philippines, for permission to conduct this study
(0154-18 DA-BFAR). We also thank Hilconida P. Calumpong, Janet S. Estacion, Rene A. Abesamis, and the staﬀof
the Silliman University Institute for Environmental and Marine Sciences for logistic support, equipment and use
of facilities. We thank Jeremiah Gepaya and Lucille Jean Raterta for their ﬁeld assistance and Dioscoro Inocencio
for ﬁsh collections and ﬁeld support. The Authors are also grateful to the three anonymous reviewers for their
Conﬂicts of Interest: The authors declare no conﬂict of interest.
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