Effect of Elevated Temperature on the Metabolic Activity of the Coral Reef

Pacific Science (1974), Vol. 28, No.2, p. 139-146 Printed in Great Britain

Effect of Elevated Temperature on the Metabolic Activity of the

Coral Reef Asteroid Acanthaster planci (L.) I

MASASHI YAMAGUCHI2

ABSTRACT: Standard rate ofoxygen uptake in the coral reefasteroid Acanthaster planci(L.) was determined for the temperature range of25° to 33° C and a metabolic rate-temperature (M-T) curve was drawn. Acanthaster planci is a metabolic con­ former. The rate ofoxygen uptake increased with increase oftemperature to 31 ° C. The rate decreased at 33° C, which is slightly above the ambient temperature for the laboratory-reared Acanthasterplanci tested. The decrease indicates a disturbance in the metabolic activity due to the elevated temperature. The incipient thermal death point for the asteroid was estimated to be near 33° C, at which temperature the animals did not maintain a normal behavior in feeding and resting cycles. Increasing modification in thermal conditions by human activity would pose a hazard to the maintenance of coral reef communities if Acanthasterplanci represents metabolic conformer invertebrates with narrow tolerance to elevated temperature.

ALTHOUGH much research has been done on Acanthaster planci (L.), a coral-predator the effects of elevated temperature on temper­ asteroid, is an excellent laboratory animal. It is ate marine animals (see reviews by Kinne 1970, easily maintained under laboratory conditions McWhinnie 1967, Vernberg and Vernberg and can readily be subjected to experimentation 1970), knowledge of thermal stress on coral under well-defined nutritive and behavioral reef animals is limited. Mayer (1914) conducted conditions. Furthermore, it is a widely distri­ thermal experiments on reef-building corals buted and relatively common reefasteroid with and other invertebrates in Samoa. Cary (1931) populations recorded from the Red Sea and studied the effects of temperature on the throughout the entire tropical Indo-Pacific Samoan Alcyonaria. Edmondson (1928, 1946) region including Hawaii (see review by Vine recorded behavior of both adults and larvae of 1972). Thus, it may well represent an important Hawaiian corals under conditions of thermal test animal for experimentation on the effects stress. The above papers indicate that many of altered thermal conditions on tropical reef coral reef invertebrates have narrow upper organisms. This report considers the effect of tolerance range of temperature for their survi­ water temperature on the"standard metabolic val and well-being. Thermal environments of activity" of the starfish, measured in the coral reefs are subjected to increasing modifica­ laboratory as the rate of oxygen uptake when tions by human activities, mostly by discharges the test animals are at rest. ofheated effluent from power generating plants. Since temperature has a direct effect on the metabolism, it is important to know how ther­ MATERIALS AND METHODS mal conditions modify the metabolic activity and behavior of coral reef animals. Three laboratory-grown Acanthaster about 15 months old and from the same batch of

I This study was supported in part by an Environ­ fertilized eggs were used for the present experi­ mental Protection Agency grant to R. S. Jones, and by a ment. They were about 120 mm in total dia­ Government of Guam Acanthaster research appropria­ meter at the beginning ofthis series of observa­ tion. Contribution no. 48, University of Guam Marine tions and each individual specimen was weigh­ Laboratory. Manuscript received 21 September 1973. ed throughout the experimental period from 2 The Marine Laboratory, University of Guam, Box EK, Agana, Guam 96910. 19 November to 9 December 1972 (Fig. 1). The 139 140 PACIFIC SCIENCE, Volume 28, April 1974 7·5

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FIG. 1. Growth ofAcanthaster planci during the experiment, from 19 November to 9 December 1972. Underwater weight, measured in seawater of about 1.024 in specific gravity, for the three experimental animals is plotted on ordinate. Effect of Elevated Temperature on Acanthaster planci-YAMAGUCHI 141 animals were weighed in seawater by means of aquaria, where their thermal environment a specific-gravity type balance (Ohaus Dial-O­ fluctuated between 25° and 31 ° C. Gram Balance). Wet weight of asteroids deter­ Two respiration chambers were placed inside mined in the air is highly variable due to an aquarium of otherwise the same setting as permeability of the body to fluids, whereas the holding aquaria. Each consisted of 4.5-liter weight in seawatergives moreconsistent results. polycarbonate cylinder (ca. 16 cm in diameter x The underwater weight of Acanthaster is 23 cm in height) and a Plexiglas cover fastened approximately one-half its dry weight. on top of the cylinder by means of rubber Each experimental animal was kept individ­ tubing. Three holes were drilled through the ually in a 40-liter rectangular plastic holding cover. One was drilled in the center to accom­ aquarium with a sand-filter bed on the bottom. modate the glass shaft of an agitating plastic Seawater in the aquarium was circulated by an propeller (5 cm in diameter) that was connected air lift. The chlorinity ofseawater in the aquaria to a 100-rpm motor. Two other holes were was maintained at 19.1 ±0.1 %0 by adding dis­ located near the edge of the lid for tubing tilled water to compensate for evaporation. through which seawater could be circulated Chlorinity was determined by silver nitrate through the chamber at the rate ofabout 1 liter titration. Water temperature of each aquarium per minute by a vibrating pump. The circula­ was controlled by an immersion heater con­ tion of seawater through the respiration cham­ nected to a bimetal thermostat and was kept ber was maintained from the time each starfish within ± 0.5° C fluctuation at most. was placed inside the chamber until the end of Each animal was kept in a holding aquarium, each run except during the periods of uptake the temperature of which was maintained at determination. The animals were thus condi­ the next experimental level, for at least 12 hours tioned in the chamber with circulating and prior to transfer into the respiration chamber. agitated seawater. Temperature ofthe aquarium The three young Acanthaster were fed ex­ with the two respiration chambers was con­ clusively Acropora spp. during the experimental trolled at each experimental level within period, as this genus of coral is consistently ± 0.05° C by means of vigorous water circula­ grazed by the asteroid in the laboratory. The tion from two air lifts and a mercury thermo­ asteroid showed cyclic feeding activities, feed­ regulator. ing on coral at night and remaining quiescent Each determination of the rate of oxygen in the day. The animals showed locomotive uptake was made by stopping circulation for activities when disturbed during weighing and 30 minutes and then sampling. Seawater sam­ transfer from holding aquaria to respiration ples were taken into 50-ml Winkler bottles chambers. They became quiescent again within through the outgoing circulation tube after it an hour inside the chamber and remained so had been disconnected from the pump. The during the observation period for up to 7 hours reduction in oxygen concentration inside the each day. It was possible to take advantage of respiration chamber was computed as the rate their cyclic activities to determine the at-rest of oxygen consumed in ml per hour per gram condition ofexperimental animals for measure­ underwater weight of Acanthaster. Three repli­ ment of standard metabolism in the growing cate samples were titrated at the beginning and young. The need to use well-fed animals was at the end of each determination period; the indicated by preliminary research that showed a Winkler method was used. The means from the marked reduction in rate of oxygen uptake in three determinations gave results with a relative starved animals. error of less than 0.5 percent. Blank tests Rate of oxygen uptake was determined for indicated a negligible rate of oxygen uptake in the temperature range of 25° to 33° C at inter­ chambers without starfish. The bias due to vals of 2 degrees. Prior to the experiment, the sources ofoxygen uptake other than the starfish experimental animals were raised through most was less than that due to titration error. of their coral-eating juvenile life in outdoor 142 PACIFIC SCIENCE, Volume 28, April 1974 33 31 29 27 25

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3·25 3·30 3·35 ( 1/ T) X 1000· FIG. 2. Metabolic rate and temperature (M-T) curve ofAcanthaster. Arrhenius plot ofthe rate ofoxygen uptake of Acanthaster against the water temperature. Ordinate indicates the logarithm of the rate as ml oxygen consumed per hour, per gram ofunderwater weight. Abscissa indicates the reciprocal ofthe water teffi.perature in degrees absolute, with an indication ofcentigrade scale on the top which corresponds to absolute temperature. Mean rate ofuptake and 1 S.D. to either side is shown. The ligures on the slopes indicate Qro value for each slope.

level is shown in Fig. 2. An Arrhenius plot is RESULTS AND DISCUSSIONS used with the logarithm (base: 10) of the rate of Each of three Acanthaster was exposed to oxygen uptake on the ordinate versus the recip­ each of the experimental temperatures: 25°, rocal of absolute temperature on the abscissa. 27°,29°,31°, and 33° C. Six replicates of rate of Questions may be raised regarding the validity oxygen uptake for each combination of tem­ of using an Arrhenius plot for analysis of perature and animal were determined. The metabolic rate and temperature relationships in mean oxygen uptake, expressed as ml oxygen these organisms. Living systems have complex consumed per hour per gram underwater metabolic networks involving many different weight, for three animals and each temperature chemical reactions that affect metabolic rate in Effect of Elevated Temperature on Acanthaster planci-YAMAGUCHI 143 many different ways. On the other hand, the ofstress that interfered with their normal cyclic effect of temperature on the rate of chemical feeding activity. When they tried to feed on reactions, in general, gives a straight line slope coral pieces, which were placed in the holding on the Arrhenius plot that is characteristic of aquaria on the first or second night, stomach the particular reaction. (See Farrell and Rose eversion was incomplete and thefeeding process 1967 about problems on this point.) If we can was shorter than that under normal conditions. assume that metabolismand growth oforganism Moreover, the starfish ceased feeding activity is an overall chemical reaction (as a blackbox), altogether after 2 full days at 33° C in the hold­ we might at least understand changes in the ing aquaria. At this time all the body surfaces level of chemical reactions through the devia­ were swollen and the ambulacral grooves that tion ofthe metabolic rate and temperature curve are usually half-closed when the starfish is in (M-T curve) from a straight line slope on the a quiescent condition at normal temperature Arrhenius plot. However, it would be difficult were wide open. When the starfish were kept to explain what particular process would be at a higher temperature (35° C), the body be­ affected in relation to the environmental came extremely swollen and tube feet showed a temperature. restless expansion and contraction from the The results showed steady increase of the gaping ambulacral grooves. Therefore, stan­ standard metabolic rate, determined as the rate dard metabolic rate with temperatures above of oxygen uptake in a quiescent condition in 33° C could not be determined. Acanthaster planci, between 25° and 31 ° C and It is well known that the rate of oxygen up­ a sharp decrease from 31 ° to 33° C. The great take in asteroids is determined not only by majority of researchers on the effects of tem­ temperature but also by a number of endogen­ perature express their results by analyzing the ous and environmental conditions such as the temperature coefficient: QlO value, instead of JL body size, activity of the animal, nutrition, value from the Arrhenius's equation. Indeed, salinity, pH, and concentration of dissolved the QlO value indicates the slope of the M-T oxygen(Farmanfarmaian 1966). An attempt was curve on the Arrhenius plot as a close approxi­ made to account for the above factors in the mation within the narrow range oftemperature present study either by controlling them or by that allows normal biological processes. There­ monitoring the range of fluctuation. Feeding fore, the Ql0 values for each temperature step and activity of the experimental animals were are indicated on the curve in Fig. 2. The slope of fairly constant except at 33° C when the animal the M-T curve of Acanthaster gave QlO values stopped feeding. Body size increased consider­ ofabout two up to 31 ° C, which means that the ably during the observation period (Fig. 1), but extrapolated rate of increase would be twofold the weight increment during this period seemed with a 10° increase in temperature. However, to have little effect on the rate ofoxygen uptake. the value between 31 ° and 33° C shows a nega­ Duplicate determinations at the same tempera­ tive figure, indicating a decrease in rate with an ture on the same animal at different sizes pro­ increase in temperature. A similar trend in the duced nearly identical results. The weight M-T curve was observed in the growth of increased about 25 to 30 percent but the incre­ microorganisms (QlO value turned negative) ment of diameter was less than 20 percent above the optimum temperature by Farrell and during the period. Salinity of seawater in the Rose (1967). On the other hand, various tem­ experimental aquarium was controlled at perate littoral invertebrates showed little change 34.50±0.10 %0 (chlorinity 19.10±0.05 %0) and in their standard rates of oxygen uptake over a pH varied between 8.0 and 8.1, with a tendency wide range of temperature. However, their toward inverse correlation with temperature. active rates showed a decrease above ambient It is doubtful that either salinity orpH affected temperature (Newell 1970) similar to the the results significantly. decrease for standard rates in Acanthaster. Because the solubility of oxygen in seawater There seemed to be no significant difference decreases with increase in water temperature, in the behavior of the animals at temperatures the level of dissolved oxygen in the experimen­ up to 31 ° C. At 33° C the starfish showed signs tal aquarium and respiration chambers varied 144 PACIFIC SCIENCE, Volume 28, April 1974 5·0

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25 27 29 31 33 WATER TEMPERATURE FIG. 3. Relationship of water temperature and concentration of dissolved oxygen inside the respiration chambers with animals (mean and 1 S.D. from initial determinations when the circulation of water stopped) and without animals (blank tests). A theoretical concentration of oxygen saturated in the seawater of19.1 %0 in chlorinity (after Green 1965) is also shown. significantly with the changes in water tempera­ concentration in the respiration chambers de­ ture as a matter ofcourse. The dissolved oxygen creased in a similar manner. The saturation level in the respiration chambers and that of theoreti­ remained at about 90 percent in the chamber cal concentration at full saturation are shown in without the animal and about 80 to 85 percent Fig. 3. As the theoretical concentration de­ with the animal. The reduction in the latter was creased with increase oftemperature, the oxygen due to the limited water circulation between the Effect of Elevated Temperature on Aeanthaster planei-YAMAGUCHI 145 aquarium and the chamber. Aeanthaster would presumably be similar to other asteroids in that CONCLUSION the rate of oxygen uptake is related to the con­ Aeanthaster planei represents a typical meta­ centration of oxygen (Farmanfarmaian 1966). bolic conformer in that its rate of oxygen up­ The slope of M-T curve in Fig. 2 might be take is controlled by environmental temperature much steeper than that observed if the deter­ and other factors. The range of temperature in mination of oxygen uptake was carried out at a which the starfish could behave normally and constant level of environmental oxygen con­ maintain normal metabolism seems to be centration of each temperature. limited to 31 ° C. At 33° C, the starfish showed The elevated temperature results in a reduced abnormal behavior, ceased feeding, and its oxygen concentration. The increased require­ metabolic activity seemed to be disturbed as ment for oxygen in poikilothermic animals with the slope of M-T curve turned negative. The accelerated metabolism at higher temperature asteroid has no specialized respiratory organ is obviously not favored by this reduction of and is not organized to regulate a constant oxygen tension. The response of Aeanthaster to metabolic level over any range of temperature. high temperature in the form of swollen body These characteristics, which may be common and gaping ambulacral grooves might be an among many invertebrates, will prove detri­ aid in the exchange ofdissolved gases. The main mental to their population maintenance if the respiratory surface of asteroids is believed to thermal environment is modified above a be the podia (tube feet), which are enclosed certain level. Information on this point is very inside the ambulacral grooves (Farmanfarmaian important in evaluating the effects of thermal 1966). However, the actual rate of oxygen discharge over coral reefs by the power plants uptake dropped at 33° C, compared with that which use seawater as a coolant. at 31 ° C. The incipient thermal death point is near Thermal death in Aeanthaster planei was 33° C for Aeanthaster, although this point observed in three field specimens and two lab­ might be shifted slightly beyond this range by oratory-grown ones. Those starfish, ranging acclimation. Water temperature around Guam from 5 cm to 18 cm in total diameter, were kept fluctuates between 27° and 30° C outside the in aquaria under the same culture conditions reef(oceanic water), but may be several degrees described in the present experiments. Water warmer inside the reef margin. Tide pools and temperature was held between 33° and 34° C small lagoons on the reef-flat often show large for these animals and their behavior and appear­ fluctuations in environmental conditions. The ence were noted. There seemed no significant temperature range that may stress Aeanthaster differences between the responses of the five is found commonly in such areas when spring animals. The general pattern of their thermal tides are low in the mid and late afternoon. death was as follows: Aeanthaster is uncommon on the reef-flat and 1. Cease feeding within 1 or 2 days. may avoid these areas because of stress includ­ 2. Dorsal spines depressed, body wall swollen, ing high temperature. There is, however, at and ambulacral grooves wide open within 3 least one conspicuous reef asteroid, Linekia to 4 days. laevigata, which does inhabit the reef-flat habitat 3. Spines located near arm tips are shed from avoided by Aeanthaster. It would be interesting the body surface, locomotion ceases, and to make a comparative study of the relationship degeneration of whole body commences a between metabolic activity and temperature for day later. Linekia, since resistance to thermal stress in this species may be different from that of Aeanthaster. The period required for the complete death of the animals was about 1 week at temperatures between 33° and 34° C. 146 PACIFIC SCIENCE, Volume 28, April 1974

GREEN, E. J. 1965. Solubility of oxygen in sea­ LITERATURE CITED water. Page 198 in R. A. Horne (1969). CARY, L. R. 1931. Studies on the coral reefs of Marine chemistry. John Wiley & Sons, Tutuila, American Samoa, with special Interscience, New York. reference to the Alcyonaria. PubIs. Carnegie KINNE, 0., ed. 1970. Marine ecology. Vol. 1, Instn. no. 413: 53-98. Part 1. Environmental factors. John Wiley & EDMONDSON, C. H. 1928. The ecology of an Sons, Interscience, New York. 681 pp. Hawaiian coral reef. Bull. Bishop Mus., MAYER, A. G. 1914. The effects of temperature Honolulu 45. 64 pp. upon tropical marine animals. PubIs. Car­ ---. 1946. Behavior of coral planulae under negie Instn. no. 183: 3-21. altered saline and thermal conditions. Occ. McWHINNIE, M. A. 1967. The heat responses Pap. Bishop Mus. 18 (19): 283-304. of invertebrates (exclusive of insects). Pages FARMANFARMAIAN, A. 1966. The respiratory 353-374 in A. H. Rose, ed. Thermobiology. physiology ofechinoderms. Pages 245-265 in Academic Press, New York. 653 pp. R. A. Boolootian, ed. Physiology of Echino­ NEWELL, R. C. 1970. Biology of intertidal dermata. John Wiley & Sons, Interscience, animals. American Elsevier, New York. New York. 822 pp. 555 pp. FARRELL, J., and A. H. ROSE. 1967. Tempera­ VERNBERG, F. J., and W. B. VERNBERG. 1970. ture effects on microorganisms. Pages 147­ The animal and the environment. Holt, 218 in A. H. Rose, ed. Thermobiology. Rinehart & Winston, New York. 398 pp. Academic Press, New York. 653 pp. VINE, P. J. 1972. Recent research on the crown­ of thorns starfish. Underwat. J. 4: 64-73.