Abstract and Figures

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 28 • C to 36 • C. Gnathiids from both locations showed rapid mortality when held in temperatures 2 • C to 3 • 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.
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Article
Eect 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, *
1
Institute of Environmental and Marine Sciences, Silliman University, 6200 Dumaguete City, Negros Oriental,
Philippines; mary.shodipo@gmail.com
2School of Biological Sciences, The University of Queensland, St Lucia QLD 4072, Australia;
berilin.duong@uq.net.au (B.D.); a.grutter@uq.edu.au (A.S.G.)
3ARC Centre of Excellence for Coral Reef Studies, James Cook University, Townsville QLD 4811, Australia;
alexia.grabalandry@my.jcu.edu.au
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
*Correspondence: paul.sikkel@gmail.com
Received: 17 July 2020; Accepted: 27 September 2020; Published: 4 October 2020


Abstract:
Extreme warming events that contribute to mass coral bleaching are occurring with
increasing regularity, raising questions about their eect on coral reef ecological interactions. However,
the eects 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 eects 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
28
C to 36
C. Gnathiids from both locations showed rapid mortality when held in temperatures 2
C
to 3
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.
Keywords:
Gnathiidae; Isopoda; coral reefs; climate change; ocean warming; coral bleaching;
Great Barrier Reef; Coral Triangle
1. Introduction
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 [
1
]. 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 [
1
], and as such, warming may
have an indirect eect 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
Oceans 2020,1216
a thermal optimum after which it rapidly declines (Thermal Performance Curve: [
2
]). Hence, the
eect of increasing temperature on marine ectotherms may be more direct, aecting physiology
and metabolism [
3
7
], which may have implications for growth, motor function, development,
reproduction and behaviour [
6
15
], which in turn may impact species’ abundance and distribution [
16
].
Therefore, increasing temperatures may be the most pervasive climate change factor influencing marine
organisms [
7
,
17
,
18
]. Warming can subsequently impact entire ecological communities and ecosystems
by dierentially impacting individuals and functional traits [1921].
Coral reefs are one of the most biodiverse ecosystems in the world [
22
,
23
]. Even though the
rate of increase in sea surface temperature (SST) is 30% less in tropical oceans than the global
average [
24
], coral reefs are also among the most sensitive ecosystems to changes in environmental
conditions [
22
,
25
,
26
], 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 [
27
,
28
]. As SSTs rise, corals and coral reef
associated organisms are being subjected to higher temperatures (29–31
C) for increasing periods
of time [
24
]. As a consequence many tropical organisms are thought to be living at or close to their
thermal limits [
29
]. SSTs are predicted to continue to rise over the coming years [
1
] and extreme
warming events, resulting in global scale coral bleaching, are occurring with increasing regularity and
severity [3034], causing degradation of coral reef habitats [22,30,31,35,36].
In addition to the corals themselves, research on the eects of marine heatwaves has also
focused heavily on fishes [
37
48
], which are also typically included in coral reef monitoring eorts.
However, studies have almost completely ignored the myriad of small, cryptic, species, which make
up a disproportionate amount of coral reef biodiversity [
49
51
]. One such group are parasites,
which make up the largest consumer strategy globally [
52
] and comprise an estimated 40% of
global biodiversity [
53
56
]. 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 [
55
,
57
60
]. Parasites are particularly
diverse on coral reefs [
61
] with an estimate of over 20,000 species on the Great Barrier Reef (GBR)
alone [
62
]. However even with such a large presence in coral reef communities, they are significantly
underrepresented in ecological studies [
10
,
55
,
63
]. Coral reef parasites are also ectothermic, and as
such, may be aected by changes to their environmental temperature [
10
,
11
,
64
67
]. 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 aected through changes
in community structure due to temperature impacts on hosts [
68
] 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 [69].
Gnathiid isopods are one of the most common ectoparasites in coral reef habitats [
70
72
]. They are
small crustaceans, typically 1–3 mm long, that do not permanently live on their fish hosts [
73
,
74
].
In fact, with few exceptions, they associate only long enough to extract a blood meal and may therefore
also be referred to as “micropredators” [
75
,
76
]. After feeding on tissue and blood from their fish host
they return to the benthos to molt and progress to the next developmental stage [
73
,
74
]. 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 [
66
]. Direct eects include influencing
behavior [
77
83
], physiology [
84
], and mortality [
85
]. Indeed, as few as one gnathiid can kill a young
juvenile fish [
83
,
86
90
]. Indirect eects include transmission of blood-borne parasites [
91
] and wounds
that can facilitate infection [
92
]. Gnathiids are also the most common items in the diet of many cleaner
fishes, including Labroides dimidiatus [
93
,
94
], a species with far-reaching ecosystem eects [
95
97
].
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 [
48
]. However,
the processes leading to this decline remain unknown.
Oceans 2020,1217
A long-term monitoring study of gnathiid isopods oLizard 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 [
65
]. However, the cause
of this decline was unclear. Sikkel et al. (2019) [
65
] hypothesized that the direct eects 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 eect 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 [
31
,
32
,
98
], and Philippines [
99
101
], 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 [
102
]. 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 [102].
Gnathiids for the Philippines study were collected from the shallow fringing coral reefs (<10 m)
of Cangmating reef (9
21
0
18.38” N, 123
17
0
58.91” E) and Agan-an reef (9
20
0
2.6” N, 123
18
0
41.5” E) in
Sibulan and from Bantayan reef (9
19
0
49.22” N, 123
18
0
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
sites [
103
,
104
]. Gnathiids were collected using light traps, adapted from Artim et al. (2015) [
89
] and
Artim and Sikkel (2016) [
105
]. 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
µ
m plankton
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 diculty with
species identification of the juvenile stages [
73
], 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
×
25
×
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 [
102
].
Oceans 2020,1218
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
×
17
×
10 cm), one for each treatment and replicate (n=9 baskets). Baskets had four
mesh (1 mm
2
) 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 dierent temperature treatment and held 10 aquaria
(previously used for another experiment, see Graba-Landry et al. 2020 [
106
]). Three aquaria were
randomly selected per bench and allocated to replicates.
We estimated the predicted ambient seawater temperature (29.25
C
±
0.013 SE) based on the
Australian Institute of Marine Science long-term average water temperature for February [
107
] (Figure
S1). Actual average daily seawater temperature during the experiment was 29.0
C
±
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 [108].
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
1
pumps (Eheim
®
) at a rate of approximately 1 L minute
1
. Tanks were
wrapped in Insulbreak
®
insulation to stabilize water temperatures. Temperature (
±
0.1
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, 28
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:
29
C: 29.5
C
±
0.07 SE, 31
C: 31.4
C
±
0.02 SE, and 32
C: 32.6
C
±
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.
2.3.2. Philippines
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.
Oceans 2020,1219
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 eect 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
µ
m) secured on the top, and the containers were submerged in one of
five 27 L aerated aquaria, each with a dierent set temperature. Each container was labelled with the
size class, treatment, trial and replicate. The first trial consisted of 5 temperature treatments, ambient
(28
C), 30
C, 32
C, 34
C and 36
C. A second trial was also conducted to obtain a finer resolution of the
temperature eect, with treatments of 30
C, 32
C, 33
C, 34
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
thermometer (Doutop
®
) 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 eects 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. [109].
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 dierent 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) [
77
]. Due to the large dierence 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 diered among temperature treatments, we used a
proportional hazards Cox mixed-eects model with temperature treatment and gnathiid juvenile stage
as categorical fixed eects, 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” [
110
,
111
] and function “Anova” in
the package “car” [
112
]. 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).
Oceans 2020,1220
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
2.4.2. Philippines
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 diered 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 eect, and size class, life stage (male, female, or juvenile) and container (which the gnathiids
were kept in) were treated as random eects. 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
spline plots).
2.5. Ethics
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. Results
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, 31
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 eect of temperature
on gnathiid survival (p<0.0001, Table 1, Figure 1), due to a significantly lower survival at 32
C
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).
Oceans 2020,1221
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, 31
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 diered according to an interaction between
temperature and juvenile stage (p=0.0085, Table 2); when further explored separately by stage
(Figure 2), the eect of temperature was significant for stage two (p<0.0001), and three (p=0.0009,
Figure 2b,c, Table S10b,c), with the strongest eect of temperature being that between the baseline
(29
C) and the 32
C treatments for stage three (Table S10c, Figure 2c). Survival diered according
to an interaction between temperature and headwidth (p=0.0480, Table 2); when further explored
separately by temperature treatment, the eect of headwidth was largely due to non-significant weakly
positive relationships between survival and headwidth at 29
C (p=0.0758) and 32
C (p=0.0718,
Table S11a,c).
0.00
0.25
0.50
0.75
1.00
0 5 10 15 20
Days
Survival probability
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 2020,1222
Oceans 2020, 1, FOR PEER REVIEW 8
(a)
(b)
Figure 2. Cont.
Oceans 2020,1223
Oceans 2020, 1, FOR PEER REVIEW 9
(c)
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. Philippines
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
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 7.50 ×107***
Headwidth 1 1.9549 0.16206
Stage 2 21.3179 2.35 ×105***
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. Philippines
3.2.1. Trial 1
There was a significant eect 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).
Oceans 2020,1224
+
+
+
+
0.00
0.25
0.50
0.75
1.00
0 5 10 15 20
Days
Survival probability
+++++
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 eect 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).
Oceans 2020,1225
+
+
+
+
+
+
+
0.00
0.25
0.50
0.75
1.00
0 5 10 15 20
Days
Survival probability
+++++
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.
4. Discussion
With ocean temperatures predicted to rise 3
C by the end of the century [
113
], the eects 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 [
67
]. In the only long-term monitoring study of any marine parasitic crustacean,
Sikkel et al. (2019) [
65
] 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 eect of temperature on gnathiid mortality. Such an eect
of temperature on the larvae of a tropical ectoparasite has been shown for monogeneans on farmed
tropical fish [69].
The present study is the first to examine eects 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 eect
which was consistent across all three juvenile stages. For fed gnathiids on the GBR, the eect of
temperature was significant for juvenile stages two and three, with the strongest eect 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
Oceans 2020,1226
from both regions. These results indicate not only that an acute change of temperature to just 32
C
decreases the survival of gnathiids, but that the eect of increased temperature is greater on the larger
juvenile stages.
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
C.
Gnathiid length is correlated with headwidth [
95
,
105
] 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 dierence in the thermal response related to size may be due to the increased metabolic
demand caused by the increase in temperature, an eect 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 [114]. 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 dier 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 dierential energetic requirements for development may also explain the
variation in the thermal response among juvenile stages in our study. Therefore, understanding the
eect of increasing temperature on individual metabolism and survival also requires an understanding
of food resources and availability [114].
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 dierences 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 dierent 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 [
115
]) have been predicted to become more frequent, longer and more severe [
116
,
117
].
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 [
4
,
118
]). 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
Oceans 2020,1227
species [
118
,
119
]. Tropical species of bivalves have also been shown to have a smaller thermal tolerance
window than temperate species [
118
]. 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
conditions [
27
]. Other studies on marine invertebrates have also shown increased mortality with high
SST [
120
,
121
], 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 [
123
125
]. Temperature
was consistently observed to have a significant eect on the survival times of trematodes in their
free-living juvenile stage, with survival rates decreasing as temperature increased (e.g., [
126
133
]).
Similarly, temperature has been reported to have an eect on parasitic barnacles (rhizocephalans),
with their prevalence decreasing at higher temperatures [68].
In one of the few other studies on ectoparasites, Conley and Curtis (1993) [
134
] 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 [
135
,
136
] and one study of monogeneans in a tropical region [
69
]. In all
three studies, temperature treatments of 30
C and above had the lowest survival rates [
69
,
135
,
136
].
Similar results were also observed with trematode cercariae from sub-tropical regions [
137
139
].
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 eects of temperature on mortality, increased temperature can also
have sub-lethal eects on marine organisms, impacting their ability to perform essential tasks [
140
142
].
Based on a review of the literature, Lough (2012) [
24
] suggested that temperatures between 30–32
C
may reflect a potential temperature threshold where a proportion of reef organisms’ physiological
processes are negatively impacted. Higher temperatures may also aect 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
temperature [
134
]. For newly emerged cercariae, swimming speed increased in higher temperatures
(19–36
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 [
143
].
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
C [
137
]. This could be attributable to greater
cercariae swimming activity [
137
]. Although, we did not quantify the eects 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 eects 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 eects 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
eradication [
68
]. 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
to 34–40
C,
[3,15,37,47]
. However, they can still experience sub-lethal eects with smaller increases in
temperatures [3,6,12,14,15,142,144146], 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 [
39
,
40
,
43
46
,
147
], depriving gnathiids and other
similar ectoparasites, like natatory-stage cymothoid isopods of hosts [
148
]. The potentially impaired
Oceans 2020,1228
physiological and swimming ability of the parasite, combined with direct eects on mortality and host
availability, could result in a decline in parasite populations. However, the ability of some gnathiids
to feed on invertebrate hosts [
149
,
150
], 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 [
48
]. This could have also contributed significantly to the crash
in gnathiid populations observed by Sikkel et al. (2019) [
65
]. 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 [
73
].
The gnathiids may, thereby, be transferred to dierent locations [
151
,
152
]. 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 eect of increased SST may be eects 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 [
153
,
154
], and thus high coral mortality associated with warm-water events,
combined with the loss of cleaner fish [
48
], which prey on ectoparasites [
93
], 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 [
65
]. While, oceans are also
experiencing increased acidification [
1
,
155
], Paula et al. (2020) [
156
] found no eect 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 [
157
159
]. Therefore, while the diversity of coral reef
parasites and their hosts makes it dicult 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 eects of warming [
67
]. Future studies on gnathiids examining sublethal thermal
eects on molting, physiology, locomotion, host-detecting mechanisms and reproductive performance
will provide a more comprehensive understanding of eects of temperature on host-parasite interactions
in coral reef systems.
Supplementary Materials:
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 dierent
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;
Oceans 2020,1229
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.
Author Contributions:
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.
Funding:
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).
Acknowledgments:
We thank the many volunteers and the Lizard Island Research Station (GBR) stawho helped
maintain the gnathiid culture and provided equipment and facilities. We also thank Jessica Vorse, who conducted
an earlier pilot study on the eects 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 staof
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
constructive comments.
Conflicts of Interest: The authors declare no conflict of interest.
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(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
... Gnathiids prefer or occur more often in dead and degraded coral microhabitat compared to live coral (Artim and Sikkel 2013;Santos and Sikkel 2017;Paula et al. 2021) likely due to risk of predation from live corals (Artim and Sikkel 2013;Paula et al. 2021). Paradoxically, decreases in gnathiid abundance in the benthos have been associated with bleaching events in the GBR (Sikkel et al. 2019), possibly due in part to an acute effect of increased temperature on gnathiid survival rate (Shodipo et al. 2020). However, in the subsequent cooler months post-bleaching, the abundance of gnathiids was higher and comparable to non-bleaching months, suggesting that, in the long term, the loss of coral cover was favourable to gnathiid recovery (Sikkel et al. 2019). ...
... Few studies have experimentally evaluated the effects of environmental changes that lead to habitat degradation on marine fish ectoparasites. These have included the effects of thermal stress (Shodipo et al. 2020) and ocean acidification (Paula et al. 2020) on gnathiid survival rates. Our study, however, is the first to integrate the effect of the chemistry dynamics of corals on gnathiid infection rates. ...
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Widespread coral mortality is leading to coral reef degradation worldwide. Many juvenile reef fishes settle on live coral, and their predator-avoidance behaviour is disrupted in seawater exposed to dead corals, ultimately increasing predation risk. Gnathiid isopods are micropredatory fish ectoparasites that occur in higher abundances in dead coral. However, the effect of seawater associated with dead coral on the susceptibility of fish to micropredators has never been investigated. We tested whether the infection rate of cultured gnathiid ectoparasites on individual damselfish, Pomacentrus amboinensis Bleeker 1868, from two different ontogenetic stages (juveniles and adults) was influenced by seawater exposed to three different treatments: dead coral, live coral, or no coral. Seawater treatments were presumed to contain different chemical properties and are meant to represent environmental changes associated with habitat degradation on coral reefs. Gnathiid infection of juvenile fish in seawater exposed to dead coral was twice as high as that of fish in live coral or no coral. Infection rates did not significantly differ between live coral and no coral treatments. In contrast to juveniles, the susceptibility of adults to gnathiids was not affected by seawater treatment. During experiments, juvenile fish mortality was relatively low, but was higher for infected fish (9.7%), compared to fish held without exposure to gnathiids (1.7%). No mortality occurred in adult fish that became infected with gnathiids. Our results suggest that chemical cues released from dead corals and/or dead coral colonisers affect the ability of juvenile, but not adult fish to avoid parasite infection. Considering increased habitat degradation on coral reefs and that gnathiids are more abundant in dead coral substrate, it is possible that wild juvenile fish may experience increased susceptibility to parasitic infection and reduced survival rate. This highlights the importance of including parasitism in ecological studies of global environmental change.
... Yet, to date, only four unidentified species of gnathiid isopods have been mentioned in literature (Santos and Sikkel, 2017) and no Philippine gnathiids have been described or named. Thus, especially given the high biodiversity of the region, research on coral reef gnathiids in the Philippines lags far behind other regions, with only five gnathiid studies to our knowledge being conducted to date: one study in the Luzon region the North of the Philippines (Cruz-Lacierda and Nagasawa, 2017) and the other four in the Visayas region in the central Philippines (Sikkel et al., 2014;Santos and Sikkel, 2017;Shodipo et al., 2019Shodipo et al., , 2020. ...
... While the work in the Visayas region over the past decade has resulted in extensive sampling of gnathiids (Sikkel et al., 2014;Santos and Sikkel, 2017;Shodipo et al. 2019Shodipo et al. , 2020, until now, none of the species captured have been identified. Our descriptions here thus represent the first gnathiid species identified from the Philippines. ...
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Due to their unusual life cycle that includes parasitic larval and free living adult stages, gnathiid isopods are typically overlooked in biodiversity surveys, even those that focus on parasites. While the Philippines sits within the region of highest marine biodiversity in the world, the coral triangle, no gnathiid species have been identified or described from that region. Here we present the first records of two gnathiid species collected from the Visayas, central Philippines: Gnathia malaysiensis Müller, 1993, previously described from Malaysia, and G. camuripenis Tanka, 2004, previously described from southern Japan. This paper provides detailed morphological redescriptions, drawings and scanning electron microscope images as well as the first molecular characterisation of both species, Furthermore, a summary of the Central-Indo Pacific Gnathia species is provided.
... But while it quickly recovered after the first extreme event (possibly due to lower coral cover, see Paula et al., 2021), it did not do so in 2017 and remained low postbleaching (in 2018) (Sikkel et al., 2019). This overall decrease in gnathiids may have been caused by an interaction between the short-term negative impacts of thermal stress on gnathiids, as shown in laboratory studies (Shodipo et al., 2020), and a decline in host availability, causing gnathiid abundance to drop (Sikkel et al., 2019;Triki and Bshary, 2019). Since heatwave intensity and frequency is increasing (Oliver et al., 2018), client fish (e.g., P. amboinensis) population attempts of adaptation to either ocean acidification or parasite infection can quickly be erased following such extreme events, if, for example, individuals that develop tolerance to either parasite infection or OA die during such extreme events. ...
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Cleaning symbioses are key mutualistic interactions where cleaners remove ectoparasites and tissues from client fishes. Such interactions elicit beneficial effects on clients’ ecophysiology, with cascading effects on fish diversity and abundance. Ocean acidification (OA), resulting from increasing CO 2 concentrations, can affect the behavior of cleaner fishes making them less motivated to inspect their clients. This is especially important as gnathiid fish ectoparasites are tolerant to ocean acidification. Here, we investigated how access to cleaning services, performed by the cleaner wrasse Labroides dimidiatus , affect individual client’s (damselfish, Pomacentrus amboinensis ) aerobic metabolism in response to both experimental parasite infection and OA. Access to cleaning services was modulated using a long-term removal experiment where cleaner wrasses were consistently removed from patch reefs around Lizard Island (Australia) for 17 years or left undisturbed. Only damselfish with access to cleaning stations had a negative metabolic response to parasite infection (maximum metabolic rate— Ṁ O 2Max ; and both factorial and absolute aerobic scope). Moreover, after an acclimation period of 10 days to high CO 2 (∼1,000 µatm CO 2 ), the fish showed a decrease in factorial aerobic scope, being the lowest in fish without the access to cleaners. We propose that stronger positive selection for parasite tolerance might be present in reef fishes without the access to cleaners, but this might come at a cost, as readiness to deal with parasites can impact their response to other stressors, such as OA.
... These authors suggested that at high temperatures, A. foliaceus has fewer opportunities for infection. In another example, Shodipo et al. (2020) determined that isopods (Gnathia aureamaculosa) experienced rapid mortality when exposed to temperatures 2 • C to 3 • C above average SST (32 • C). The evidence suggests that the short larval duration and increased energetic demands imposed by anomalously high temperatures result in a reduction in the number of parasitic copepods on fish. ...
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The prevalence and median intensity of infection of Pacific sierra (Scomberomorus sierra) by parasitic copepods (Caligus fajerae, Caligus omissus, and Cybicola buccatus), and monogeneans (Thoracocotylidae) were examined over a six-year period (2015 to 2021) in the southeastern Gulf of California. This period included sea surface temperatures that were warmer and colder than average (SST anomalies). A regression model indicated that the prevalence of parasitic species was higher when conditions were warmer than average, although some of the relationships were non-significant. Prolonged periods of high temperature and heat pulses >2 °C above the average temperature negatively affected the prevalence of parasites. A moderate or high prevalence of parasites was observed during colder than average conditions. These results are in accordance with those of previous studies showing that fish ectoparasites are able to develop under a wide range of thermal conditions.
... The first study reported that, in the wild, gnathiid isopods were lower in abundance during a marine heatwave that generated widespread coral bleaching in the Great Barrier Reef compared to cooler months . The authors suggested a mechanism whereby altered developmental rates would mediate an apparent low tolerance of gnathiids to temperature fluctuations Shodipo et al. 2020). In a different study, gnathiids demonstrated a clear preference for dead coral rubble compared to live corals (Santos and Sikkel 2017), suggesting that physiological impacts from climate change could be offset, to some extent, by larger availability of desirable microhabitats. ...
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For the last seven decades, cleaning sym-biosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intimate association and high frequency of interactions between cleaners and clients potentially facilitates pathogen transmission and disease spread. In this review, we identify knowledge gaps and develop novel hypotheses on the interrelationship between parasites, hosts and the environment (disease triangle concept), with a particular emphasis on the potential role of cleaner organisms as hosts and/or transmitters of parasites. Despite evidence supporting the positive effects of cleaner organisms, we propose the cleaners as transmitters hypothesis; that some parasites may benefit from facilitated transmission to cleaners during cleaning interactions, or may use cleaner organisms as transmitters to infect a wider diversity and number of hosts. This cost of cleaning interactions has not been previously accounted for in cleaning theory. We also propose the parasite hotspot hypothesis; that parasite infection pressure may be higher around cleaning stations, thus presenting a conundrum for the infected client with respect to cleaning frequency and duration. The impact of a changing environment, particularly climate stressors on cleaners' performance and clients' cleaning demand are only beginning to be explored. It can be expected that cleaners, hosts/cli-ents, and parasites will be impacted in different ways by anthropogenic changes which may disrupt the long-term stability of cleaning symbiosis.
... More recently, Pagán et al. (2020) showed that tropical cyclones are also capable of having direct effects on gnathiid populations by transporting large numbers of gnathiids, and over hundreds of kilometres, sufficient to alter the population-genetic structure. Alongside, Shodipo et al. (2020) showed that gnathiid survival rates in the laboratory decrease in warmer water. Moreover, Paula et al. (2020) showed that gnathiids are resilient to other environmental stressors, such as ocean acidification. ...
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Gnathiid isopods, common fish ectoparasites, can affect fish physiology, behaviour and survival. Gnathiid juveniles emerge from the benthos to feed on fish blood. In the Caribbean, gnathiids are positively associated with dead coral and negatively associated with live coral, due to coral predation on gnathiids. However, such interactions were unstudied in the Great Barrier Reef (GBR). Due to recent extreme weather events (two cyclones and one mass warm-water coral bleaching event, 2014–2016), it is now urgent to understand the role of corals on the abundance of these ectoparasites. Here, to understand parasite–coral dynamics at the micro-habitat level, we examined substrate associations of gnathiid isopods on Lizard Island (GBR) using demersal plankton emergence traps. Additionally, we determined whether two abundant hard coral species, Goniopora lobata and Pocillopora damicornis, predate on gnathiids in a laboratory experiment using containers with gnathiids and fragments from each coral species or dead coral as controls. The abundance of gnathiids over natural substrates was higher for dead compared to live hard coral and sand, but not live soft coral. Moreover, we found that free-swimming gnathiids decreased in containers with live coral compared to dead coral controls. This was attributed to predation as we also directly observed a coral ingesting a gnathiid. Our results suggest that dead coral is a suitable microhabitat for gnathiids, but that live coral is not since live corals can predate on gnathiids. We propose that following extreme events, such as cyclones and heat waves, gnathiids might benefit from more dead coral substrate and a decrease in predation by the reduction in coral cover on the reef. We advocate that an increase in the frequency of extreme events may have cascading effects for the fish population through changes in the population of benthos-dependent ectoparasites.
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The current trend in marine parasitology research, particularly in South Africa, is to focus on a specific parasite taxon and not on the total parasite community of a specific fish host. However, these records do not always reveal the ecological role of parasites in ecosystems. Thus, the present study aimed to determine which factors influence the parasite community composition of the endemic southern African intertidal klipfish, Clinus superciliosus (n = 75). Metazoan parasites were sampled from four localities (two commercial harbours - west coast; and two relatively pristine localities - southeast coast) along the South African coast. A total of 75 klipfish were examined for parasites, where 30 distinct taxa, representing seven taxonomic groups were found: Acanthocephala (4 taxa), Cestoda (2 taxa), Crustacea (5 taxa), Digenea (11 taxa), Hirudinea (2 taxa), Monogenea (1 taxon) and Nematoda (5 taxa). Results indicated that the main driver of diversity was locality, with the highest diversity on the southeast coast, most likely due to higher water temperatures and upwelling compared to the west coast. The parasite community composition of the klipfish was significantly influenced by water temperature and parasite life cycle. These results emphasise the importance of parasitological surveys including all parasite taxa in hosts from multiple localities and seasons, to better comprehend their ecological role.
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Organisms with a parasitic lifestyle comprise a high proportion of biodiversity in aquatic and terrestrial environments. However, there is considerable variation in the ways in which they acquire nutrients. Hematophagy is a common consumption strategy utilized by some terrestrial, aquatic, and marine organisms whereby the parasite removes and digests blood from a host. Gnathiid isopods are marine hematophagous parasites that live in benthic substrates from the intertidal to the abyss. Although ecologically similar to ticks and mosquitoes, they feed only during each of 3 juvenile stages and adults do not feed. They have long been considered as generalist fish parasites and to date, there have been no reports of their successfully feeding on invertebrates. Based on observations of gnathiids attached to soft-bodied invertebrates collected from light traps, we conducted a laboratory experiment in which we collected and individually housed various common Caribbean invertebrates and placed them in containers with gnathiids to see if the gnathiids would feed on them. All fed gnathiids were subsequently removed from containers and given the opportunity to metamorphose to the next developmental stage. In total, 10 out of the 260 gnathiids that were presented with 1 of 4 species of potential invertebrate hosts had fed by the next morning. Specifically, 9 of a possible 120 gnathiids fed on lettuce sea slugs (Elysia crispata), and 1 of a possible 20 fed on a bearded fireworm (Hermodice carunculata). Eight of these 10 fed gnathiids metamorphosed to the next stage (5 to adult male, 2 to adult female, and 1 to third-stage juvenile). Even though feeding rates on invertebrates were considerably lower than observed for laboratory studies on fishes, this study provides the first documented case of gnathiids’ feeding on and metamorphosing from invertebrate meals. These findings suggest that when fish hosts are not readily available, gnathiids could switch to soft-bodied invertebrates. They further provide insights into the evolution of feeding on fluids from live hosts in members of this family.
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The reliance of parasites on their hosts makes host-parasite interactions ideal models for exploring ecological and evolutionary processes. By providing a consistent supply of parasites, in vivo monocultures offer the opportunity to conduct experiments on a scale that is generally not otherwise possible. Gnathiid isopods are common ectoparasites of marine fish, and are becoming an increasing focus of research attention due to their experimental amenability and ecological importance as ubiquitous harmful blood-feeding “mosquito-like” organisms. They feed on hosts once during each of their three juvenile stages, and after each feeding event they return to the benthos to digest and moult to the next stage. Adults do not feed and remain in the benthos, where they reproduce and give birth. Here, we provide methods of culturing gnathiids, and highlight ways in which gnathiids can be used to examine parasite-host-environment interactions. Captive-raised gnathiid juveniles are increasingly being used in parasitological research; however, the methodology for establishing gnathiid monocultures is still not widely known. Information to obtain in vivo monocultures on teleost fish is detailed for a Great Barrier Reef, (Australia) and a Caribbean Sea (US Virgin Islands) gnathiid species, and gnathiid information gained over two decades of successfully maintaining continuous cultures is summarised. Providing a suitable benthic habitat for the predominantly benthic free-living stage of this parasite is paramount. Maintenance comprises provision of adequate benthic shelter, managing parasite populations, and sustaining host health. For the first time, we also measured gnathiids’ apparent attack speed (maximum 24.5 cm sec⁻¹; 6.9, 4.9/17.0, median, 25th/75th quantiles) and illustrate how to collect such fast moving ectoparasites in captivity for experiments. In addition to providing details pertaining to culture maintenance, we review research using gnathiid cultures that have enabled detailed scientific understanding of host and parasite biology, behaviour and ecology on coral reefs.
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Infectious disease outbreaks emerged across the globe during the recent 2015–2016 El Niño event, re-igniting research interest in how climate events influence disease dynamics. While the relationship between long-term warming and the transmission of disease-causing parasites has received substantial attention, we do not yet know how pulse heat events – common phenomena in a warming world – will alter parasite transmission. The effects of pulse warming on ecological and evolutionary processes are complex and context dependent, motivating research to understand how climate oscillations drive host health and disease. Here, we develop a framework for evaluating and predicting the effects of pulse warming on parasitic infection. Specifically, we synthesize how pulse heat stress affects hosts, parasites, and the ecological interactions between them.
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Territorial and roving grazing fishes farm, and feed on, algae, sediment, or detritus, thus exerting different influences on benthic community structure, and are common clients of cleaner fish. Whether cleaners affect grazing-fish diversity and abundance, and indirectly the benthos, was tested using reefs maintained free of the bluestreak cleaner wrasse Labroides dimidiatus for 8.5 yr (removals) compared with controls. We quantified fish abundance per grazing functional group, foraging rates of roving grazers, cleaning rates of roving grazers by L. dimidiatus , reef benthos composition, and fouling material on settlement tiles. Abundances of ‘intensive’ and ‘extensive’ territorial farmers, non-farmers, parrotfishes and Acanthurus spp. were lower on removal than control reefs, but this was not the case for ‘indeterminate’ farmers and Ctenochaetus striatus . Foraging rates of Acanthurus spp. and C. striatus were unaffected by cleaner presence or cleaning duration. This suggests some robustness of the grazers’ foraging behaviour to loss of cleaners. Acanthurus spp. foraged predominantly on sediment and detritus, whereas C. striatus and parrotfishes grazed over algal turfs. Nevertheless, benthic community structure and amount of organic and inorganic material that accumulated over 3.5 mo on tiles were not affected by cleaner presence. Thus, despite greater abundances of many roving grazers, and consequently higher grazing rates being linked to the presence of cleaners, the benthos was not detectably affected by cleaners. This reveals that the positive effect of cleaners on fish abundance is not associated with a subsequent change in the benthos as predicted. Rather, it suggests a resilience of benthic community structure to cleaner-fish loss, possibly related to multiple antagonistic effects of different grazer functional groups. However, losing cleaners remains a problem for reefs, as the lack of cleaning has adverse consequences for fish physiology and populations.
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Human activities have caused an increase in atmospheric CO2 over the last 250 years, leading to unprecedented rates of change in seawater pH and temperature. These global scale processes are now commonly referred to as ocean acidification and warming (OAW), and have the potential to substantially alter the physiological performance of many marine organisms. It is vital that the effects of OAW on marine organisms are explored so that we can predict how marine communities may change in future. In particular, the effect of OAW on host-parasite dynamics is poorly understood, despite the ecological importance of these relationships. Here, we explore the response of one himasthlid trematode, Himasthla sp., an abundant and broadly distributed species of marine parasite, to combinations of elevated temperature and pCO2 that represent physiological extremes, pre-industrial conditions, and end of century predictions. Specifically, we quantified the life span of the free-living cercarial stage under elevated temperature and pCO2, focussing our research on functional life span (the time cercariae spend actively swimming) and absolute life span (the period before death). We found that the effects of temperature and pCO2 were complex and interactive. Overall, increased temperature negatively affected functional and absolute life span, e.g. across all pCO2 treatments the average time to 50% cessation of active swimming was approximately 8 h at 5°C, 6 h at 15°C, 4 h at 25°C, and 2 h at 40°C. The effect of pCO2, which significantly affected absolute life span, was highly variable across temperature treatments. These results strongly suggest that OAW may alter the transmission success of trematode cercariae, and potentially reduce the input of cercariae to marine zooplankton. Either outcome could substantially alter the community structure of coastal marine systems.