Metabolic response to temperature change in red lionfish

(Pterois volitans) at Hoga Island, Indonesia

E.C. Oakley

School of Marine Science and Technology, Newcastle University, Newcastle upon Tyne, Tyne
and Wear, NE1 7RU, United Kingdom

e.c.oakley@newcastle.ac.uk

Journal format: Journal of Thermal Biology

1
Abstract

Increasing sea temperature is predicted to impact species living in equatorial regions as they are
poorly adapted to a wide temperature range. The standard metabolic rate (SMR) of Pterois
volitans was measured after laboratory acclimation at 25C (group A) and 30C (group B) and in
one group of field acclimatised fish (group C) using stop flow respirometry. SMR was measured
again after acute thermal transfer between temperatures to calculate the temperature quotient
(Q10), and a day after transfer to study the change in oxygen consumption (VO2). Groups A, B
and C had a mean Q10 of 4.54, 2.41 and 2.88 respectively, however, there were no significant
differences in the Q10 values. Groups B and C had significantly different SMRs after thermal
transfer. No significant difference in oxygen consumption for group A was observed after transfer
to 30C. Group C had a much lower SMR at both temperatures than those acclimated in the
laboratory. The results suggest P. volitans has limited scope for acclimation facing the projected
increases in sea surface temperature. An increased SMR may result in trade-offs affecting growth
and reproduction. P. volitans populations may persist if the rate of temperature change does not
exceed their thermal tolerance.

Keywords: Pterois volitans; Hoga Island; Stop flow respirometry; VO2; Q10; Standard metabolic
rate.

1. Introduction

Fish are poikilotherms and are highly affected by temperature change. Increases in standard
metabolic rate (SMR) of fish have been attributed to rises in temperature. Increased SMR is a
consequence of greater kinetic energy of cellular components, resulting in a higher ATP
requirement and subsequently increasing the consumption of oxygen (Clarke and Fraser, 2004).
Vant Hoffs Rule demonstrates that the response to temperature of fish can be quantified through
use of temperature quotients (Q10). Fish normally show a Q10 of 2.0 when temperature is
increased by 10C, resulting in the doubling of SMR and other biological processes (Eme and
Bennett, 2009a). Prolonged exposure to temperature leads to acclimation as a result of
physiological and biochemical adaptations (Nilsson et al., 2010). However, acclimation is not a
permanent change in the tolerance of organisms, and is quickly lost when fish are returned to
more optimal temperatures (Beitinger and Bennett, 2000).

Acclimation is becoming an essential feature of fish populations in order to allow persistence in

their native range, attributable to the increasing sea surface temperatures impacting SMR

2
(Donelson et al., 2011; Eme and Bennett, 2009b; Hiddink and Ter Hofstede, 2008). The results
of the current study were evaluated in the context of the projected sea temperature increases,
linked to climate change in the western Pacific region. The current mean temperature in the reef
zone surrounding Hoga Island, Indonesia, is 27C with temperature fluctuations between 25C
and 30C (Eme and Bennett, 2009a). Increases of up to 3C in sea surface temperature are
predicted by 2100 (Donelson et al., 2011; IPCC, 2007). In addition, it is believed species living in
relatively temperature stable latitudes have a reduced capacity for thermal acclimatisation
(Rummer et al., 2014; Sunday et al., 2011). Therefore, many species could be living in sub-
optimum conditions at the extent of their thermal limit, resulting in an increased SMR (Clarke and
Fraser, 2004; Donelson et al., 2011; Munday et al., 2008). An increased SMR could cause
tradeoffs in the life cycle of the fish, through allocation of resources to growth and reproduction.
It is important to research the SMR of tropical fish in order to determine potential effects of climate
change, linked to determining future conservation and management strategies (Gardiner et al.,
2010; Rummer et al., 2014). Furthermore, deleterious impacts on species living in coral reef areas
could be further increased as Indonesia has one of the most threatened reef systems in the world,
with a decline in size of 2% a year between 1997 and 2003 (Bruno and Selig, 2007; Reytar et al.,
2011). These negative effects are linked to climate change and anthropogenic impacts such as
the number of fishery dependent populations, destructive fishing practices and pollution (Hughes
et al., 2003; Reytar et al., 2011).

The red lionfish (Pterois volitans), a native to the Indo-Pacific region, was the focus of the current
study, as this is a key predatory species in the dynamics of coral reefs and has a huge role in
controlling many reef fish populations (Albins and Hixon, 2008; Morris et al., 2011; Morris and
Akins, 2009). Lionfish are also abundant in the Indo-Pacific, allowing ease to acquire a large
sample size (Fishelson, 1997; Green and Ct, 2009). Little is known about the species thermal
biology, and it is therefore important to study the effects of temperature, e.g. on metabolism, to
predict the effects of change on lionfish. In addition, the red lionfish is currently invading areas of
the Atlantic coast off mainland USA and spreading into the Gulf of Mexico (Albins and Hixon,
2008; Green and Ct, 2009; Morris et al., 2011; Schofield, 2009), making it even more vital to
understand the physiology and biology of lionfish in an attempt to limit the spread.

The objectives of the current study were to measure the SMR of lionfish in three groups; 25C
acclimated (group A), 30C acclimated (group B) and field acclimatised (group C) using stop flow
respirometry. SMR will be measured before and after acute temperature transferal. The Q10
values of fish from each group will be determined to study metabolic compensation. The results

3
will be interpreted in the context of the predicted sea surface temperature increase, with an overall
aim of examining the impacts of climate change on lionfish.

2. Material and Methods

2.1. Location

Hoga Island is in the Wakatobi Marine National Park, Banda Sea, Sulawesi, the Republic of
Indonesia (0527.53S, 12346.33E) (Figure 1). The data were collected during a six week period
on Hoga Island from June to July 2014.

Figure 1: Study site of Hoga Island, Wakatobi Marine National Park, Banda Sea, Sulawesi, the
Republic of Indonesia. Adapted from Eme and Bennett (2009a).

2.2. Source of experimental fish

A total of 31 lionfish with mean lengths of 10.80 cm 1.30 S.D. and mean weights of 46.44 g
16.82 S.D. were collected by fishermen using dip nets and transported to the laboratory in
containers holding seawater from the capture site. On arrival, the fish were put into 150 L tanks
of aerated seawater at room temperature. Ammonia accumulation was prevented through
changing 20 % of the water in the tanks three times a day. The dissolved oxygen and water
temperature of the tanks were measured three times a day. Fish were fed live food from the
intertidal sea grass area every two days until satiated, including small fish and crustaceans. Fish

4
were fasted for 24 hours before tests were run, resulting in fish being in a post-absorptive state
during trials.

2.3. Acclimation

The laboratory acclimated fish, groups A and B, were kept at a constant temperature, 25C or
30C respectively. These temperatures corresponded well with the average temperature range
around Hoga Island (Eme and Bennett, 2009a). Fish were acclimated for 12 days, a sufficient
period to allow for physiological and biochemical adaptations (Barrionuevo and Fernandes, 1998;
Gardiner et al., 2010; Nilsson et al., 2009; Nilsson et al., 2010). The temperature was maintained
in the 25C tank using a flow through system with ice buckets that were changed every four hours.
The 30C tank was controlled by a Finnex, 300W submersible heater and a RANCO temperature
controller. Field acclimatised fish, group C, were kept at room temperature for 24 hours before
respirometry trials. After the 12 day acclimation period the SMR of groups A and B (n=3), with
four trials for each fish, was measured using stop flow respirometry (day 0). The fish were then
acutely transferred between temperatures, plunging group A into 30C and vice versa for group
B. The SMR was measured again after one day at the new temperature. In addition, the SMR of
fish from groups A (n=4), B (n=3) and C (n=12), with eight trials for each fish, were recorded
before acute thermal transfer in the respirometer and were then recorded again after transfer to
allow comparisons. Group C were transferred from 25C to 30C to study the effects of
temperature fluctuations found in the field.

2.4. Stop flow respirometry

Oxygen consumption was determined using stop flow respirometry (Figure 2). The system
consisted of a respirometry chamber in a tank with water flow from a submersible pump. Water
used was filtered with a 0.83 m plankton net to reduce the impacts of background respiration.
The temperature in the system was maintained using ice at 25C and a RANCO temperature
controller at 30C. The mean temperatures during stop flow respirometry were maintained during
experiments with a mean of 25.03 C 0.07 S.D and 29.97 C 0.11 S.D. A constant flow rate
through the system was maintained with the pressure created by the head box. Water was
pumped within the respirometry chamber with a peristaltic pump to constantly mix water within
the chamber. The water flow into the respirometry chamber was cut off using a plastic needle
valve. The original dissolved oxygen level (mg) and water temperature (C) were recorded using
a YSI Modle 55A oxygen probe, which was sealed into the top of the respirometry chamber. The
box remained closed until 30 minutes had passed or ~20% of the oxygen had depleted to prevent

5
hypoxia affecting the SMR (Clark et al., 2013; Rummer et al., 2014). The time taken (minutes),
final dissolved oxygen concentration and temperature were recorded. The system was re-opened
and allowed to flush until the oxygen in the chamber had reached original levels. The fish standard
length (cm), volume (ml) and mass (g) were recorded to allow a mass adjusted comparison.

A control was undertaken where the respirometry chamber was run for 4 hours at 25C and 30C,
with the tap closed to measure the bacterial respiration in the system. The control showed that
1.025x10-6 mgO2ml-1min-1 and 1.275x10-6 mgO2ml-1min-1 of oxygen were consumed at 25C and
30C, respectively. The results of the trials were not adjusted for the control, as background
respiration was negligible.

The method used in the current study combined the closed tank and flow through respirometry
techniques. The closed tank technique is often based on too few repeats as the chamber remains
closed for a long period of time. This long time period can also result in accumulation of waste
products and oxygen depletion (Barrionuevo and Fernandes, 1998; Steffensen, 1989). The
method in the current study allows the water to be flushed through use of a plastic needle valve
to prevent a buildup of waste products such as ammonia, as well as allowing the chamber to be
opened and closed continually. In addition, stop flow respirometry uses only one oxygen probe to
avoid error, unlike the flow through method. The methodology follows the guidelines of Clark et
al. (2013) who has created recommendations on how to undertake respirometry.

6
Figure 2: Schematic of stop flow respirometry experimental set up. A: submersible pump, B: head
box, C: temperature probe, D and E are the inflow and the outflow of the peristaltic pump
respectively, F: plastic needle valve and G: YSI Modle 55A oxygen probe.

2.5. Calculation of VO2 and Q10

The oxygen consumption (VO2) is measured on days 0 and one day after the acute temperature
to allow comparison of oxygen consumption. VO2 is calculated using the following equation:

(COI COF ) (Vresp Vfish )

VO2 =
Time

With COI being the initial oxygen concentration (mg), COF the final oxygen concentration, Vresp the
volume of the respirometer and Vfish the volume of the fish.

The data were mass adjusted to allow comparison between fish of different weights, using the
following equation:
V02
Normalised V02 =
weight 0.75
A factor of 0.75 was used, following Kleibers law, as metabolic rate does not follow a linear
relationship with weight. 0.75 is widely accepted as the metabolic scaling rate for teleosts and
corrects this allometric relationship (Brown et al., 2004; Clarke, 2006; Clarke and Johnston, 1999;
Gillooly et al., 2001; Moran and Wells, 2007; West et al., 1997).

7
The temperature quotient (Q10) response was calculated for fish that were acutely transferred
whilst in the respirometer. The Q10 response was calculated with the following equation:

R2 10
Q10 = ( ) (T2 T1 )
R1

With R2 and R1 being the VO2 at temperatures T2 (30C) and T1 (26C) respectively. Mean oxygen
consumption values of each fish were used to calculate the mean Q10 value.

2.6. Statistical Analysis

All data conformed to a normal distribution (Kolmogorov-Smirnov, P>0.05), excluding the Q10
values which were log10 transformed to normalise, hence parametric tests were used.
Homogenous variances were tested before undertaking t-tests and one-way analysis of variance
(ANOVA), confirming that for each statistical test there was no significant difference (Levenes
test of homogeneity of variances, P>0.05). T-tests were used on the VO2 data as different fish
were studied before and after thermal transfer. Paired t-tests were used on the Q10 data to
compare within groups, as the same fish were used to determine the acute response. ANOVA
was completed on the oxygen consumptions from the Q10 data to compare between groups within
temperatures. In addition, ANOVA was undertaken on the transformed Q10 values. If ANOVA
revealed statistically significant results post-hoc Tukey pairwise comparison tests were
undertaken. Statistical decisions were based on = 0.05. All statistical analysis was carried out
using Minitab 17 Statistical Software.

3. Results

At day 0 there was a statistically significant difference in mean VO2 in group A (mean = 0.90
0.29 S.D.) and group B (mean = 1.30 0.19 S.D.) (t-test, t = -2.85, df = 11, P<0.05), suggesting
that an increase in temperature results in an increase in SMR.

3.1. VO2 results

Group B showed a statistically significant difference between the VO2 of fish at day 0 (mean =
1.32 mgO2kg-1min-1 0.25 S.D.) and 1 (mean = 0.78 mgO2kg-1min-1 0.11 S.D.) (t-test, t = 3.52,
df = 4, P<0.05). However, group A had no significant difference between the VO2 of fish at day 0
(mean = 1.14 mgO2kg-1min-1 0.30 S.D) and day 1 (mean = 1.25 mgO2kg-1min-1 0.24 S.D.) (t-
test, t = -0.49, df = 4, P>0.05).

8
3.2. Q10 results

3.2.1. Within group comparisons

The mean VO2 within each group was compared before and after acute thermal transfer (Figure
3). There was a statistically significant difference for fish in group B before (mean = 1.28 mgO2kg-
1
min-1 0.18 S.D.), and after (mean = 0.84 mgO2kg-1min-1 0.19 S.D.) (paired t-test, t = 9.63, df
= 2, P<0.05). Group B showed a decrease in SMR of 0.44 mgO2kg-1min-1 when thermally
transferred to 25C. Likewise, there was a statistically significant difference in group C fish before
(mean = 0.29 mgO2kg-1min-1 0.22 S.D) and after (mean = 0.48 mgO2kg-1min-1 0.38 S.D) the
fish were transferred to 30C (paired t-test, t = -3.41, df = 11, P<0.05). Group C showed an
increase of 0.19 mgO2kg-1min-1 in SMR after transfer. There was no statistically significant
difference in mean VO2 for fish in group A before transfer (mean = 0.73 mgO2kg-1min-1 0.13
S.D.) and after transfer (mean = 1.37 mgO2kg-1min-1 0.72 S.D.) (paired t-test, t = -1.8, df = 3,
P>0.05).

3.2.2. Between group comparisons

Comparisons were also undertaken within temperatures, comparing groups A, B and C. At 25C
there was a statistically significant difference in VO2 between groups (ANOVA, F = 13.58, df =
2,16, P<0.05). Post-hoc Tukey pairwise comparison (P=0.05) showed there was no significant
difference in VO2 between the groups A and B, but the VO2 in group C was significantly lower.
There was a statistically significant difference in VO2 at 30C between groups (ANOVA, F =
8.06, df = 2,16, P<0.05). Post-hoc Tukey pairwise comparison (P=0.05) showed there was no
significant difference in VO2 between groups A and B but the VO2 in group C was significantly
lower. Groups A and B show statistically similar SMRs at both 25C and 30C (Figure 3). The
SMR of field acclimatised fish (group C) is demonstrated to be much lower than laboratory
acclimated fish.

3.2.3. Q10 values

In addition, the Q10 values were calculated, revealing that there was no significant difference
between group A (mean = 4.54 5.14 S.D.), group B (mean = 2.41 0.45 S.D.) and group C
(mean = 2.88 1.63 S.D.) (ANOVA, F = 0.2, df = 2, 16, P>0.05)

9
 2.5

Mean VO2 (S.D.) (mgO2kg-1min-1)

2

1.5

1 25 degrees
30 degrees

0.5

0
A1 A2 B1 B2 C1 C2

Acclimation Group

Figure 3: Mean oxygen consumption (S.D.) (mgO2kg-1min-1) of red lionfish in groups A, B and C,
during thermal transfer (1: Before) (2: After) between 25C and 30C.

4. Discussion

The response of lionfish to temperature change conveys important information relating to

population persistence in the context of the predicted increase in sea surface temperature. This
study aimed to quantify this relationship in Indo-Pacific lionfish, using the dual approach of
examining VO2 and Q10 data, successfully presenting the first Q10 values for lionfish.

After the acclimation period there was a significant difference discerned in the oxygen
consumption of groups A and B. The SMR of group B was significantly higher, revealing that fish
metabolically compensated for the higher temperature of 30C, following the general relationship
observed in poikilotherms (Eme and Bennett, 2009b). An increase in SMR related to a higher
temperature leads to a higher kinetic energy of cellular components, resulting in an increased
ATP requirement and consequently increasing consumption of oxygen (Clarke and Fraser, 2004).
Furthermore, proteins are often temperature sensitive, necessitating faster protein synthesis.

For group B there was a statistically significant difference in SMR after thermal transfer in the VO2
and Q10 data. Likewise, group C demonstrated a significantly higher oxygen consumption at 30C
than 25C. Acute transferral of group B fish from 30C to the lower temperature of 25C reduced

10
thermal stress, as lionfish have been shown to have a high tolerance to lower temperatures
(Kimball et al., 2004). However, the latter study extrapolates results from Indonesian lionfish,
transported to the USA, to study the effect of temperatures observed in US waters which lacks
ecological relevance. The study also makes no differentiation between P. volitans and Pterois
miles, making the results somewhat unreliable. Group C had a statistically similar Q10 to group B,
this could be a result of group C experiencing a wide range of temperature fluctuations in the field
and the lack of acclimation to one temperature, reducing the thermal stress of temperature change
(Eme and Bennett 2009a). The Q10 of the field acclimatised lionfish allows us to study the effects
of rapid climate change.

However, there was no significant difference in mean SMR for group A that were transferred to
30C, both acutely and after one day. This was an unexpected result, as it was hypothesised that
30C would be a thermally stressful environment, as it is at the extreme limit of what lionfish
experience in Indo-Pacific waters (Eme and Bennett, 2009b). Whilst this may demonstrate that
lionfish are relatively thermally tolerant, there is a large standard deviation in the Q10 data,
necessitating the P value to be used with caution (Figure 3). In addition, group A had the highest
Q10 value (mean Q10 = 4.54 5.14 S.D.). The high Q10 implies that fish acclimated at lower
temperatures have the most stressful response to an increase in temperature. This could be
related to a decrease in upper and lower temperature tolerance limits (Beitinger and Bennett,
2000). However, the Q10 was not statistically significant from those of groups B and C, showing
there may be limited effects of temperature change.

Overall, the Q10 values from the current study are the first presented for lionfish. Whilst Vant
Hoffs rule predicts animals to have a Q10 of 2.0, it is normally observed that a Q10 would be
between 2.0 and 3.0 (Eme and Bennett, 2009a). Lionfish live in somewhat stable reef habitats,
with less frequent temperature fluctuations compared to other environments such as tide pools,
allowing them to survive with a higher Q10. With the predicted sea temperature increases, lionfish
may be at a disadvantage as they may have to rapidly increase their SMR. Lionfish will be able
to survive climate change if the temperature change does not exceed their temperature tolerance
(Eme and Bennett, 2009b). The Eme and Bennett study (2009b), regarding temperature quotients
in other fish in the Hoga Island region, found that fish that often experience temperature
fluctuations in their environment, for example tidal creeks, had lower Q10 values. This study
included fish such as the common goby (Bathygobius fuscus) and the blackspot sergeant
(Abudefduf sordidus), potentially making these species more likely to survive climate change. All
fish in the Eme and Bennett study (2009b), excluding the white-tail humbug (Dascyllus aruanus),

11
had lower Q10 values than those found in lionfish. This could result in changes in the species
assemblage, as some species are more predisposed to cope with the impacts of increased
temperature. However, temperature quotients are somewhat limited as they only look at the acute
effect of temperature change. Future studies should include a time course experiment on
metabolism, as climate change is occurring over a long period of time.

The effects of laboratory acclimation were revealed in both Figure 3 and the ANOVA test
completed on the Q10 results, discerning the similarities in VO2 at the same temperature. It
appears that acclimation did not affect the metabolic response to temperature. At 25C fish in
group A were shown to have a statistically similar SMR as group B when they were transferred to
25C. The same result was observed at 30C. It was hypothesised that group B would gain high
temperature tolerance, and would begin to metabolically compensate for the temperature change,
with fish that were transferred to 30C from 25C having a much higher SMR as they are under
thermal stress. This could demonstrate that lionfish have a limited scope for acclimation.
Nevertheless, group C were revealed to have much lower SMRs at both temperatures, providing
evidence that there is some impact of acclimation on lionfish. Laboratory acclimated lionfish may
potentially experience stress as a result of removal from their natural habitat though the period of
acclimation in the current study aimed to negate this, allowing fish to metabolically compensate
and adapt to their environment.

An increased SMR at 30C could lead to an increased food demand. The Fishelson (1997) study
on food consumption in P. volitans indicated that currently the juveniles consumed 5.5 - 13.5 gday-
1
and adults consumed 14.6 gday-1. The day 0 data of the current study reveals that P. volitans
may have to increase its food consumption by up to 44.40% per unit time (applicable for the mean
weight of lionfish used in the current study). This would provide enough energy to maintain the
increase in SMR. Ct and Green (2012) also used the Fishelson data set and predicted that in
the Bahamas, with an increase of 1C in temperature, a 150 g lionfish would need to increase
prey consumption by 17%. These predictions seem relatively consistent with those of the current
study. An increase in mean food consumption could hugely impact the reef community, as
increased numbers of smaller fish would be consumed. However, the Fishelson (1997) study was
based on invasive lionfish and hence may not be applicable to the native species, as a result of
the differing environmental factors. The reef communities are also currently being impacted by
the effects of climate change. Climate change is likely to have an effect on the plankton
communities, leading to trophic cascade effects in the number of reef fish species available as
prey for lionfish (Donelson et al., 2010). In addition, Nilsson et al. (2009) studied aerobic capacity

12
of cardinal fish and damselfish, concluding that cardinal fish had reduced aerobic capacity.
Gardiner et al. (2010) indicates that this could influence species composition of the reef
communities. Despite this potential change in prey species abundance, it is likely that P. volitans
will continue to be a successful predator as they are opportunistic generalist feeders (Albins and
Hixon, 2008; Morris and Akins, 2009; Sloan and Turingan, 2014).

All functions are affected by temperature, but temperature for optimal metabolic scope coincides
with the temperature for optimal growth (Donelson et al., 2011). An increased food demand linked
with the negative effects of an increased temperature on growth could result in trade-offs within
the species. Less energy may be invested into reproduction, affecting egg size, embryo
development and gonad maturation (Donelson et al., 2010). These trade-offs could have
deleterious effects such as reduced species persistence and population sustainability (Donelson
et al., 2011; Mora and Ospina, 2001).

Increased temperature has many other potential effects on P. volitans populations. Rummer et
al. (2014) reveals the capacity to perform aerobically is vital in determining the response of
animals to climate change. Overall, the maximum rate of oxygen uptake is determined by cardiac
output, respiratory surface area, oxygen carrying capacity of blood and the degree of downloading
of blood to tissues (Gardiner et al., 2010). However, the current study has revealed, through the
Q10 values, that to maintain function at an increased temperature, lionfish need to raise their SMR
and in turn oxygen demand, limiting aerobic function. If lionfish are unable to develop phenotypic
plasticity it is likely that reduced aerobic performance will cause extinction or relocation to cooler
waters (Hiddink and Ter Hofstede, 2008; Nilsson et al., 2009; Nilsson et al., 2010; Prtner and
Knust, 2007; Ter Hofstede et al., 2010). In addition, the reduced oxygen concentration in warmer
water requires an increase in SMR to continue to extract a sufficient quantity of oxygen (Prtner
and Knust, 2007).

In conclusion, if climate change is consistent with the predicted values of temperature increase,
then it is likely there will be deleterious effects on P. volitans populations in the Indo-Pacific. The
Q10 values presented in the current study reveal that to survive a temperature increase, lionfish
may have to double if not triple their SMR to compensate. An increased SMR could result in
increased food demands and trade-offs affecting growth and reproduction. The population will be
able to persist in their current native range if the rate of temperature change does not exceed that
of their temperature tolerance and if they are able to develop phenotypic plasticity.

Acknowledgements

13
The author would like to thank Operation Wallacea. Dr. Wayne Bennett and Theresa Dabruzzi for
overseas supervision. Dr. Per Berggren for supervision throughout the project.

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