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Response to heat stress of brittlestar [Ophiocoma erinaceus (Müller & Troschel, 1842)]:

Behaviour and respiration


,
Tri Dewi Kusumaningrum Pribadi , Riani Rostami, Melanie, and Yudi Nurul Ihsan

Citation: 1744, 020058 (2016); doi: 10.1063/1.4953532


View online: http://dx.doi.org/10.1063/1.4953532
View Table of Contents: http://aip.scitation.org/toc/apc/1744/1
Published by the American Institute of Physics
Response to Heat Stress of Brittlestar
[Ophiocoma erinaceus (Müller & Troschel, 1842)]:
Behaviour and Respiration

Tri Dewi Kusumaningrum Pribadi1, a), Riani Rostami1, Melanie1 and


Yudi Nurul Ihsan2
1
Department of Biology, Universitas Padjadjaran, Jl. Raya Bandung-Sumedang km.21, Jatinangor, West Java
45363, Indonesia
2
Department of Marine Science, Universitas Padjadjaran, Jl. Raya Bandung-Sumedang km.21, Jatinangor,
West Java 45363, Indonesia

a)Corresponding email: tridewi.pribadi@unpad.ac.id

Abstract. Tide pools are considered as a harsh ecosystem in which many natural threats to living organisms are
living, including extreme temperatures. As the water temperature rises due to global warming, tide pool
temperature will also increase and therefore force the organisms living inside to adapt to alteration. Brittlestar
(Ophiocoma erinaceus) is one type of the species that lives in tide pools and plays an important role in the food
chain. A study of temperature treatment to O. erinaceus was conducted to investigate the behaviour and
respiration as the response to adapt to heat stress. The experiments were conducted in 144 h. Temperatures
used were 27 °C, 30 °C, 33 °C and ambient water as the control, with three replicas each. Behaviour and
respiration were observed and measured after reaching 48 h, 96 h and 144 h each respectively. The results
showed that the activities decreased at 33 °C, with burrowing as the most often response. Individuals in
temperature of 33 °C respired at a lower rate after 48 h of the experimental period.

Keywords: Behaviour, heat, Ophiocoma erinaceus (Müller & Troschel, 1842), respiration.

INTRODUCTION
Stress can be biotic such as lack of food, or abiotic due to temperature or salinity. Measuring production
and response at different levels of environmental variables should indicate if the factor is stress [1]. The
temperature rise caused by global warming can also affect the survival ability of water organisms,
particularly the ones which live in shallow water such as tide pools, interfering the metabolism and activity of
animals and plants, which can cause death in extreme condition.
Tide pools are characteristic of a rocky beach that has an uneven place to hold water during low tide
[2, 3]. Although organisms found in tide pools remain submerged in the whole tidal cycle, considerable
temperature changes can be found in subtidal zones. Its temperature may vary every day with a range up to
15 °C, depending on the height of tide pools, exposure to sunlight, shades and volume level of tide pools
[4].
Karang Papak, one of the rocky intertidal coasts in Southern Java, Indonesia was formed from rocky
shore with tide pools as characteristic of the beach [5]. This special characteristic of tide pools is often seen
as an attractive habitat for marine organisms, notedly animals due to its limited space of habitat known for
high density and diversity of organisms living in, such as brittle stars, sea urchins, coral fish, shrimp,

Towards the sustainable use of biodiversity in a changing environment: From basic to applied research
AIP Conf. Proc. 1744, 020058-1–020058-8; doi: 10.1063/1.4953532
Published by AIP Publishing. 978-0-7354-1401-3/$30.00

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macroalgae and seagrass [2]. One of so many species in Karang Papak is a brittle star (Ophiuroidea).
Despite being unknown for its economic value, the presence of this class in intertidal zone plays an
important role in the food chain [6]. Brittlestar (Ophiuroidea) is the source of food for various species of
reef fish [7, 8]. It has been recorded that 33 species of reef fish have brittle stars as their source of food and
henceforth perform a shelter along with macroalgae together [9].
Due to global warming, high-temperature fluctuations in tide pools will affect the community structure
along the coast, particularly in the tide pools and therefore, a study is required on the response and
physiological behaviour of organisms which live in such places to investigate the future adaptation to heat
stress. Furthermore, they will be able to provide information about understanding ecological changes due to
climate change.

MATERIAL AND METHODS

Acclimatisation
Species used in this study were species with high population in the tide pools, Ophiocoma erinaceus
(Müller & Troschel, 1842). Individuals were collected from the rocky intertidal area of Karang Papak
(S 07°38.490'; E 107°40.977') during low tide, with 10 g weight in average. They were held in the
laboratory for two day acclimatisation in an artificial tide pool of a 120 cm × 120 cm × 40 cm mesocosm
with aeration, sand and rocks in the bottom, under natural light exposure and at room temperature.

Preliminary Observation
This study was conducted during February to March 2015. Observation of physical parameters was
conducted at several tide pools in intertidal zone which have passed 50 m line parallel transect to the
coastline in order to determine ambient physical parameters of tide pools, such as temperature, pH, salinity,
depth and diameter. Behavioural observation of O. erinaceus was done after acclimatisation in the mesocosm
under natural light and at room temperature to investigate the natural types of behaviours. The observation
was conducted for 48 h. Individuals used in this preliminary study will then consecutively be used for heat
stress experiments.

Experiments
After acclimatisation, O. erinaceus was placed in a glass jar of 1 200 mL. The jar was filled with filtered
seawater (0.2 μm) and sand with 5cm depth. The jar was then covered with gauze in order to prevent the
objects come out ofthe jar and allow sufficient water circulation. Each of the three jars was placed in aquaria of
100 cm × 60 cm × 40 cm filled with filtered seawater that had already been set up to different temperatures
using thermostat at the level of 27 °C, 30 °C, 33 °C and maintained constant during the experimental
period. This constant temperature treatment was performed to investigate the maximum tolerance of these
species to constant exposure to higher temperature levels. The temperature levels were selected at 27 °C, 33
°C and maximum ambient temperature at 30 °C. Objects with ambient temperature treatment were used as the
control. Each aquarium was equipped with digital thermometers to record and control any changes of
seawater temperature [1]. The aquaria were placed under natural daylight. Objects are fed in the form of fish
food once a day.
The behavioural observation was conducted during the 144 h experimental period using scan sampling
method [10] where object activities in each jar were recorded in 60 min intervals for 5 min. Types of
activities of O. erinaceus were observed in this study and also modified as per Boos et al. [11] which were
described as burrowing (digging), moving the arms, actively moving (migrate) and remain still (passive). O.
erinaceus behaviour was recorded in a worksheet.
Respiration rate was observed using the same individuals after 48 h, 96 h and 144 h exposure time. Objects
were then taken out of the jars and placed into dark jars to avoid light stress. The dark jars were placed
in the same aquaria to maintain the same temperature level. Objects then were allowed to stand for an hour,
so that they could adapt to the new environment. Once the jars were airtight sealed up, they were then left
for 4 h to measure the respiration rate. Then, the water was released using a small tube into the bottle

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winkler to measure the dissolved oxygen [1]. Dissolved oxygen and respiration rate were measured using
the formula of Pavlovskii [12].

RESULTS
The ambient physical parameter of tide pools in Karang Papak is showed in range (Table 1). Water
and air temperatures fluctuated slightly, ranging from 29 °C to 30 °C and from 29 °C to 31 °C, where the pH
also fluctuated in the range of pH 7.15 to pH 7.43. Salinity remained the same at several tide pools which
had been observed previously. DO was measured in the morning at the lowest and the highest sun positions.
The depth of the tide pools varied, ranging from 15 cm to 38 cm, with the widest diameter of one tide pool
measuring 2.45 m.
TABLE 1. Ambient physical parameters of tide pools in Karang Papak are showed in range during February–March 2015
Parameters Measurement
Water (29 to 30) °C
Air temperature (29 to 31) °C
DO temperature (6.2 to 7.1) mg · L–1
Salinity 34 mg · L–1
pH 7.15 to 7.43
Depth (15 to 38) cm

During preliminary behavioural observation in the mesocosm, the objects have shown four types of
behaviour which are described in Table 2. In general, the results showed that activities would decrease at 33
°C, with burrowing as the most often responsive one. During the first 48 h (Fig. 1a), individuals
showed various trends of behaviours in each temperature treatment. The high performance of active
behaviour was spotted only in individuals with ambient temperature during high performance of passive
behaviour with 33 °C treatment. The active behaviour decreased with increasing of temperature levels.
Moving the arms behaviour was showed by individuals in all temperature treatments.
TABLE 2. Types of the behaviour of O. erinaceus during a two-day acclimatisation in mesocosm (lab scale)
Activities Descriptions
Migrate Activities of moving from one place to another
Moving the arms Activities of moving limbs extremities, as the
whole arm or only one part of extremities
Passive Activities of not doing any activity. The object’s
position was at the bottom of the water column and
on top of the sand substrate
Burrowing Activities of positioning the whole or part of the
body under the sand with the arm positions are
still above the sediment surface [13, 14]

In the interval of 49 h to 96 h (Fig. 1b), burrowing and passive behaviour increased with increasing
temperature levels, where the frequency reached 58 %. The high performance of active behaviour showed
only in individuals under 27 °C and ambient temperature exposure, which in contrast to other individuals,
was exposed to the other temperature levels.
At the end of the experimental period (Fig. 1c), burrowing and passive behaviour of individuals showed
less frequency compared to the previous period in all temperature levels. The active behaviour of O.
erinacieus showed very low performance in individuals under 33 °C temperature exposure.

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(a)

(b)

(c)

FIGURE 1. The frequency of behaviour under different temperature levels during experimental period of 144 h;
(a) interval of 0 h to 48 h, (b) interval of 48 h to 96 h, (c) interval of 96 h to 144 h. Bars were SE.

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Physiological response as respiration was also measured in this study. Respiration is indicated as
Dissolved Oxygen (DO) in water samples, oxygen consumption and respiration rate. Dissolved Oxygen in
water samples decreased with increasing duration and temperature levels (Fig. 2). The lowest DO was
showed in water samples with individuals exposed to 33 °C.

FIGURE 2. Effect of temperature levels exposure to Dissolved Oxygen (mg · L 1) in water samples of Ophiocoma

erinaceus during 144 h experimental period. Bars were SE.

Generally, oxygen consumption increased along with increasing exposure time (Fig. 3). Oxygen
consumption of each individual under 33 °C exposure showed obvious rising curve which was higher than
any other individuals with lower temperature exposure. The demand of oxygen consumption was shown in
the first 48 h of exposure to all temperature levels. After 48 h, only individuals under 33 °C temperature
exposure remained high in oxygen consumption.

FIGURE 3. Effect of exposure to different temperature levels on oxygen consumption (mg · L 1) of Ophiocoma erinaceus

during 144 h experimental period. Bars were SE

Respiration rate fluctuated slightly at all temperature levels (Fig. 4). Obvious decrease in respiration rate is
only shown in the first 48 hours for individuals with 33 °C exposure. In the last 48 hours, individuals
with no temperature exposure showed only slight decrease in respiration rate.

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FIGURE 4. Effect of exposure to different temperature levels on respiration rate (mgO2 · g 1 · L 1) of Ophiocoma erinaceus
– –

during144 h experimental period. Bars were SE.

DISCUSSION
During the experiments, only individuals with no temperature exposure showed active migratory in
high frequency. The remaining individuals with temperature exposure showed diminishing activities along
with increasing temperature levels. On the contrary, burrowing behaviour showed an increasing activity
along with increasing temperature levels during the experiments. Burrowing behaviour showed more
activities at the end of the experimental period, notedly for individuals under 33 °C temperature exposure,
which indicated a potential response to stress [11]. This tendency of several behaviours indicated that
increasing temperature levels had an impact on O. erinaceus.
Increasing temperature levels can lead to hypoxia. Low oxygen concentration, in this study, was shown by
DO, in water column can reduce the activities of water organisms [15]. In this study, O. erinaceus
exposed by high-temperature levels showed passive behaviour at the bottom of water column due to depletion
of oxygen. This result of the recent study parallel with Ophiomastix annulosa was exposed at 32.3 °C [16].
Temperature affects metabolism process which means physiological process [17]. At the range of 10 °C to 30
°C, brittle stars were in their top condition to normally do metabolism. Temperature exposure under 10 °C
or above 35 °C will make brittle stars insensible. Temperature exposure above 40 °C can cause
coma condition while above 50 °C death. Activities still occur between insensible and comma condition,
but the metabolism will decline. They stay alive but with very low metabolism activities, henceforth when it
continues to happen, it will lead to death [18].
Increasing oxygen consumption for individuals exposed to 33 °C indicates the rise of water temperature
level, which can cause oxygen depletion, which then forces organisms to escalate their respiration
organ to maximise their oxygen exploitation to allow normal or increasing metabolism [19]. This finding
is also parallel to Brown’s [2] who reported that an increasing temperature of 1 °C will raise oxygen
consumption of 10 % on average. Respiratory organs work more quickly than normally due to enzyme
acceleration, which results in higher activation energy than usual [21]. Body enzyme plays a significant role in
controlling chemical reaction as an energy resource to form glucose, lipid and protein. When temperature rises,
the metabolic rate will raise as well. On the other hand, when the temperature exceeds the threshold,
enzyme denaturates and reduces the metabolic rate [19]. This condition presumably occurs with individuals
below 33 °C.
Brittlestar is a poikilothermic animal whose body temperature varies with the fluctuation of ambient
temperature [22]. Poikilothermal aquatic animals have difficulty avoiding temperature changes and as the
result, they will do gas exchange in the respiratory surface. They produce heat which will then disappear
quickly on the respiratory surface for the absorption of O2 and CO2 expenditure or expenditure of other
products such as ammonia. Respiration rate in poikilothermal animals is very much affected by ambient
temperature changes. When water temperature increases, water molecules will be denser and more

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difficult to flow to the respiratory organs. Organisms must expend more energy to take up oxygen for
the respiratory organs to work more quickly than usual [17]. At normal temperatures, organisms move
quite actively because dissolved oxygen levels are still high, leading to normal rate of respiration. At higher
temperature exposure, the behaviour of individuals will decrease due to the increasingly low value of
dissolved oxygen. The depletion of oxygen occurs due to increasingly rapid respiration rate of the test animals
which make them difficult to get oxygen.

CONCLUSION
Ophiocoma erinaceus performed varied frequent responses to different temperature levels and duration of
heat exposure. Active behaviour decreased with increasing temperature levels and duration of heat
exposure, with burrowing as the most responsive one. Individuals at 33 °C respired at a lower rate after
48 h of the experimental period. Exposure to 33 °C after 48 h showed to be the critical point of insensible
condition of O. erinaceus.

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