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

Effect of Elevated Temperature on the Metabolic Activity of theCoral Reef Asteroid Acanthaster planci (L.) I

MASASHI YAMAGUCHI2

ABSTRACT: Standard rate of oxygen uptake in the coral reef asteroid Acanthasterplanci(L.) was determined for the temperature range of 25° to 33° C and a metabolicrate-temperature (M-T) curve was drawn. Acanthaster planci is a metabolic con­former. The rate of oxygen uptake increased with increase of temperature to 31 ° C.The rate decreased at 33° C, which is slightly above the ambient temperature forthe laboratory-reared Acanthasterplanci tested. The decrease indicates a disturbancein the metabolic activity due to the elevated temperature. The incipient thermaldeath point for the asteroid was estimated to be near 33° C, at which temperaturethe animals did not maintain a normal behavior in feeding and resting cycles.Increasing modification in thermal conditions by human activity would pose ahazard to the maintenance of coral reef communities if Acanthaster planci representsmetabolic conformer invertebrates with narrow tolerance to elevated temperature.

MATERIALS AND METHODS

Acanthaster planci (L.), a coral-predatorasteroid, is an excellent laboratory animal. It iseasily maintained under laboratory conditionsand can readily be subjected to experimentationunder well-defined nutritive and behavioralconditions. Furthermore, it is a widely distri­buted and relatively common reef asteroid withpopulations recorded from the Red Sea andthroughout the entire tropical Indo-Pacificregion including Hawaii (see review by Vine1972). Thus, it may well represent an importanttest animal for experimentation on the effectsof altered thermal conditions on tropical reeforganisms. This report considers the effect ofwater temperature on the" standard metabolicactivity" of the starfish, measured in thelaboratory as the rate of oxygen uptake whenthe test animals are at rest.

Three laboratory-grown Acanthaster about15 months old and from the same batch offertilized eggs were used for the present experi­ment. They were about 120 mm in total dia­meter at the beginning of this series of observa­tions and each individual specimen was weigh­ed throughout the experimental period from19 November to 9 December 1972 (Fig. 1). The

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ALTHOUGH much research has been done onthe effects of elevated temperature on temper­ate marine animals (see reviews by Kinne 1970,McWhinnie 1967, Vernberg and Vernberg1970), knowledge of thermal stress on coralreef animals is limited. Mayer (1914) conductedthermal experiments on reef-building coralsand other invertebrates in Samoa. Cary (1931)studied the effects of temperature on theSamoan Alcyonaria. Edmondson (1928, 1946)recorded behavior of both adults and larvae ofHawaiian corals under conditions of thermalstress. The above papers indicate that manycoral reef invertebrates have narrow uppertolerance range of temperature for their survi­val and well-being. Thermal environments ofcoral reefs are subjected to increasing modifica­tions by human activities, mostly by dischargesofheated effluent from power generating plants.Since temperature has a direct effect on themetabolism, it is important to know how ther­mal conditions modify the metabolic activityand behavior of coral reef animals.

I This study was supported in part by an Environ­mental Protection Agency grant to R. S. Jones, and by aGovernment of Guam Acanthaster research appropria­tion. Contribution no. 48, University of Guam MarineLaboratory. Manuscript received 21 September 1973.

2 The Marine Laboratory, University of Guam, BoxEK, Agana, Guam 96910.

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FIG. 1. Growth of Acanthaster planci during the experiment, from 19 November to 9 December 1972. Underwaterweight, measured in seawater of about 1.024 in specific gravity, for the three experimental animals is plotted onordinate.

Effect of Elevated Temperature on Acanthaster planci-YAMAGUCHI 141

animals were weighed in seawater by means ofa specific-gravity type balance (Ohaus Dial-O­Gram Balance). Wet weight of asteroids deter­mined in the air is highly variable due topermeability of the body to fluids, whereasweight in seawater gives more consistent results.The underwater weight of Acanthaster isapproximately one-half its dry weight.

Each experimental animal was kept individ­ually in a 40-liter rectangular plastic holdingaquarium with a sand-filter bed on the bottom.Seawater in the aquarium was circulated by anair lift. The chlorinity of seawater in the aquariawas maintained at 19.1 ±0.1 %0 by adding dis­tilled water to compensate for evaporation.Chlorinity was determined by silver nitratetitration. Water temperature of each aquariumwas controlled by an immersion heater con­nected to a bimetal thermostat and was keptwithin ± 0.5° C fluctuation at most.

Each animal was kept in a holding aquarium,the temperature of which was maintained atthe next experimental level, for at least 12 hoursprior to transfer into the respiration chamber.

The three young Acanthaster were fed ex­clusively Acropora spp. during the experimentalperiod, as this genus of coral is consistentlygrazed by the asteroid in the laboratory. Theasteroid showed cyclic feeding activities, feed­ing on coral at night and remaining quiescentin the day. The animals showed locomotiveactivities when disturbed during weighing andtransfer from holding aquaria to respirationchambers. They became quiescent again withinan hour inside the chamber and remained soduring the observation period for up to 7 hourseach day. It was possible to take advantage oftheir cyclic activities to determine the at-restcondition of experimental animals for measure­ment of standard metabolism in the growingyoung. The need to use well-fed animals wasindicated by preliminary research that showed amarked reduction in rate of oxygen uptake instarved animals.

Rate of oxygen uptake was determined forthe temperature range of 25° to 33° C at inter­vals of 2 degrees. Prior to the experiment, theexperimental animals were raised through mostof their coral-eating juvenile life in outdoor

aquaria, where their thermal environmentfluctuated between 25° and 31 ° C.

Two respiration chambers were placed insidean aquarium of otherwise the same setting asthe holding aquaria. Each consisted of 4.5-literpolycarbonate cylinder (ca. 16 cm in diameter x23 cm in height) and a Plexiglas cover fastenedon top of the cylinder by means of rubbertubing. Three holes were drilled through thecover. One was drilled in the center to accom­modate the glass shaft of an agitating plasticpropeller (5 cm in diameter) that was connectedto a 100-rpm motor. Two other holes werelocated near the edge of the lid for tubingthrough which seawater could be circulatedthrough the chamber at the rate of about 1 literper minute by a vibrating pump. The circula­tion of seawater through the respiration cham­ber was maintained from the time each starfishwas placed inside the chamber until the end ofeach run except during the periods of uptakedetermination. The animals were thus condi­tioned in the chamber with circulating andagitated seawater. Temperature of the aquariumwith the two respiration chambers was con­trolled at each experimental level within± 0.05° C by means of vigorous water circula­tion from two air lifts and a mercury thermo­regulator.

Each determination of the rate of oxygenuptake was made by stopping circulation for30 minutes and then sampling. Seawater sam­ples were taken into 50-ml Winkler bottlesthrough the outgoing circulation tube after ithad been disconnected from the pump. Thereduction in oxygen concentration inside therespiration chamber was computed as the rateof oxygen consumed in ml per hour per gramunderwater weight of Acanthaster. Three repli­cate samples were titrated at the beginning andat the end of each determination period; theWinkler method was used. The means from thethree determinations gave results with a relativeerror of less than 0.5 percent. Blank testsindicated a negligible rate of oxygen uptake inchambers without starfish. The bias due tosources of oxygen uptake other than the starfishwas less than that due to titration error.

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FIG. 2. Metabolic rate and temperature (M-T) curve of Acanthaster. Arrhenius plot of the rate of oxygen uptake ofAcanthaster against the water temperature. Ordinate indicates the logarithm of the rate as ml oxygen consumed perhour, per gram of underwater weight. Abscissa indicates the reciprocal of the water teffi.perature in degrees absolute,with an indication ofcentigrade scale on the top which corresponds to absolute temperature. Mean rate of uptake and1 S.D. to either side is shown. The ligures on the slopes indicate Qro value for each slope.

RESULTS AND DISCUSSIONS

Each of three Acanthaster was exposed toeach of the experimental temperatures: 25°,27°,29°,31°, and 33° C. Six replicates of rate ofoxygen uptake for each combination of tem­perature and animal were determined. Themean oxygen uptake, expressed as ml oxygenconsumed per hour per gram underwaterweight, for three animals and each temperature

level is shown in Fig. 2. An Arrhenius plot isused with the logarithm (base: 10) of the rate ofoxygen uptake on the ordinate versus the recip­rocal of absolute temperature on the abscissa.

Questions may be raised regarding the validityof using an Arrhenius plot for analysis ofmetabolic rate and temperature relationships inthese organisms. Living systems have complexmetabolic networks involving many differentchemical reactions that affect metabolic rate in

Effect of Elevated Temperature on Acanthaster planci-YAMAGUCHI 143

many different ways. On the other hand, theeffect of temperature on the rate of chemicalreactions, in general, gives a straight line slopeon the Arrhenius plot that is characteristic ofthe particular reaction. (See Farrell and Rose1967 about problems on this point.) If we canassume that metabolism and growth oforganismis an overall chemical reaction (as a blackbox),we might at least understand changes in thelevel of chemical reactions through the devia­tion of the metabolic rate and temperature curve(M-T curve) from a straight line slope on theArrhenius plot. However, it would be difficultto explain what particular process would beaffected in relation to the environmentaltemperature.

The results showed steady increase of thestandard metabolic rate, determined as the rateof oxygen uptake in a quiescent condition inAcanthaster planci, between 25° and 31° C anda sharp decrease from 31° to 33° C. The greatmajority of researchers on the effects of tem­perature express their results by analyzing thetemperature coefficient: QlO value, instead of JLvalue from the Arrhenius's equation. Indeed,the QlO value indicates the slope of the M-Tcurve on the Arrhenius plot as a close approxi­mation within the narrow range of temperaturethat allows normal biological processes. There­fore, the Ql0 values for each temperature stepare indicated on the curve in Fig. 2. The slope ofthe M-T curve of Acanthaster gave QlO valuesof about two up to 31° C, which means that theextrapolated rate of increase would be twofoldwith a 10° increase in temperature. However,the value between 31° and 33° C shows a nega­tive figure, indicating a decrease in rate with anincrease in temperature. A similar trend in theM-T curve was observed in the growth ofmicroorganisms (QlO value turned negative)above the optimum temperature by Farrell andRose (1967). On the other hand, various tem­perate littoral invertebrates showed little changein their standard rates of oxygen uptake over awide range of temperature. However, theiractive rates showed a decrease above ambienttemperature (Newell 1970) similar to thedecrease for standard rates in Acanthaster.

There seemed to be no significant differencein the behavior of the animals at temperaturesup to 31° C. At 33° C the starfish showed signs

of stress that interfered with their normal cyclicfeeding activity. When they tried to feed oncoral pieces, which were placed in the holdingaquaria on the first or second night, stomacheversion was incomplete and the feeding processwas shorter than that under normal conditions.Moreover, the starfish ceased feeding activityaltogether after 2 full days at 33° C in the hold­ing aquaria. At this time all the body surfaceswere swollen and the ambulacral grooves thatare usually half-closed when the starfish is ina quiescent condition at normal temperaturewere wide open. When the starfish were keptat a higher temperature (35° C), the body be­came extremely swollen and tube feet showed arestless expansion and contraction from thegaping ambulacral grooves. Therefore, stan­dard metabolic rate with temperatures above33° C could not be determined.

It is well known that the rate of oxygen up­take in asteroids is determined not only bytemperature but also by a number of endogen­ous and environmental conditions such as thebody size, activity of the animal, nutrition,salinity, pH, and concentration of dissolvedoxygen (Farmanfarmaian 1966). An attempt wasmade to account for the above factors in thepresent study either by controlling them or bymonitoring the range of fluctuation. Feedingand activity of the experimental animals werefairly constant except at 33° C when the animalstopped feeding. Body size increased consider­ably during the observation period (Fig. 1), butthe weight increment during this period seemedto have little effect on the rate of oxygen uptake.Duplicate determinations at the same tempera­ture on the same animal at different sizes pro­duced nearly identical results. The weightincreased about 25 to 30 percent but the incre­ment of diameter was less than 20 percentduring the period. Salinity of seawater in theexperimental aquarium was controlled at34.50±0.10 %0 (chlorinity 19.10±0.05 %0) andpH varied between 8.0 and 8.1, with a tendencytoward inverse correlation with temperature.It is doubtful that either salinity or pH affectedthe results significantly.

Because the solubility of oxygen in seawaterdecreases with increase in water temperature,the level of dissolved oxygen in the experimen­tal aquarium and respiration chambers varied

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concentration in the respiration chambers de­creased in a similar manner. The saturation levelremained at about 90 percent in the chamberwithout the animal and about 80 to 85 percentwith the animal. The reduction in the latter wasdue to the limited water circulation between the

FIG. 3. Relationship of water temperature and concentration of dissolved oxygen inside the respiration chamberswith animals (mean and 1 S.D. from initial determinations when the circulation of water stopped) and withoutanimals (blank tests). A theoretical concentration of oxygen saturated in the seawater of19.1 %0 in chlorinity (afterGreen 1965) is also shown.

significantly with the changes in water tempera­ture as a matter ofcourse. The dissolved oxygenin the respiration chambers and that of theoreti­cal concentration at full saturation are shown inFig. 3. As the theoretical concentration de­creased with increase of temperature, the oxygen

Effect of Elevated Temperature on Aeanthaster planei-YAMAGUCHI 145

aquarium and the chamber. Aeanthaster wouldpresumably be similar to other asteroids in thatthe rate of oxygen uptake is related to the con­centration of oxygen (Farmanfarmaian 1966).The slope of M-T curve in Fig. 2 might bemuch steeper than that observed if the deter­mination of oxygen uptake was carried out at aconstant level of environmental oxygen con­centration of each temperature.

The elevated temperature results in a reducedoxygen concentration. The increased require­ment for oxygen in poikilothermic animals withaccelerated metabolism at higher temperatureis obviously not favored by this reduction ofoxygen tension. The response of Aeanthaster tohigh temperature in the form of swollen bodyand gaping ambulacral grooves might be anaid in the exchange of dissolved gases. The mainrespiratory surface of asteroids is believed tobe the podia (tube feet), which are enclosedinside the ambulacral grooves (Farmanfarmaian1966). However, the actual rate of oxygenuptake dropped at 33° C, compared with thatat 31° C.

Thermal death in Aeanthaster planei wasobserved in three field specimens and two lab­oratory-grown ones. Those starfish, rangingfrom 5 cm to 18 cm in total diameter, were keptin aquaria under the same culture conditionsdescribed in the present experiments. Watertemperature was held between 33° and 34° Cfor these animals and their behavior and appear­ence were noted. There seemed no significantdifferences between the responses of the fiveanimals. The general pattern of their thermaldeath was as follows:

1. Cease feeding within 1 or 2 days.2. Dorsal spines depressed, body wall swollen,

and ambulacral grooves wide open within 3to 4 days.

3. Spines located near arm tips are shed fromthe body surface, locomotion ceases, anddegeneration of whole body commences aday later.

The period required for the complete death ofthe animals was about 1 week at temperaturesbetween 33° and 34° C.

CONCLUSION

Aeanthaster planei represents a typical meta­bolic conformer in that its rate of oxygen up­take is controlled by environmental temperatureand other factors. The range of temperature inwhich the starfish could behave normally andmaintain normal metabolism seems to belimited to 31° C. At 33° C, the starfish showedabnormal behavior, ceased feeding, and itsmetabolic activity seemed to be disturbed asthe slope of M-T curve turned negative. Theasteroid has no specialized respiratory organand is not organized to regulate a constantmetabolic level over any range of temperature.These characteristics, which may be commonamong many invertebrates, will prove detri­mental to their population maintenance if thethermal environment is modified above acertain level. Information on this point is veryimportant in evaluating the effects of thermaldischarge over coral reefs by the power plantswhich use seawater as a coolant.

The incipient thermal death point is near33° C for Aeanthaster, although this pointmight be shifted slightly beyond this range byacclimation. Water temperature around Guamfluctuates between 27° and 30° C outside thereef(oceanic water), but may be several degreeswarmer inside the reef margin. Tide pools andsmall lagoons on the reef-flat often show largefluctuations in environmental conditions. Thetemperature range that may stress Aeanthasteris found commonly in such areas when springtides are low in the mid and late afternoon.Aeanthaster is uncommon on the reef-flat andmay avoid these areas because of stress includ­ing high temperature. There is, however, atleast one conspicuous reef asteroid, Linekialaevigata, which does inhabit the reef-flat habitatavoided by Aeanthaster. It would be interestingto make a comparative study of the relationshipbetween metabolic activity and temperature forLinekia, since resistance to thermal stress in thisspecies may be different from that of Aeanthaster.

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LITERATURE CITED

CARY, L. R. 1931. Studies on the coral reefs ofTutuila, American Samoa, with specialreference to the Alcyonaria. PubIs. CarnegieInstn. no. 413: 53-98.

EDMONDSON, C. H. 1928. The ecology of anHawaiian coral reef. Bull. Bishop Mus.,Honolulu 45. 64 pp.

---. 1946. Behavior of coral planulae underaltered saline and thermal conditions. Occ.Pap. Bishop Mus. 18 (19): 283-304.

FARMANFARMAIAN, A. 1966. The respiratoryphysiology of echinoderms. Pages 245-265 inR. A. Boolootian, ed. Physiology of Echino­dermata. John Wiley & Sons, Interscience,New York. 822 pp.

FARRELL, J., and A. H. ROSE. 1967. Tempera­ture effects on microorganisms. Pages 147­218 in A. H. Rose, ed. Thermobiology.Academic Press, New York. 653 pp.

PACIFIC SCIENCE, Volume 28, April 1974

GREEN, E. J. 1965. Solubility of oxygen in sea­water. Page 198 in R. A. Horne (1969).Marine chemistry. John Wiley & Sons,Interscience, New York.

KINNE, 0., ed. 1970. Marine ecology. Vol. 1,Part 1. Environmental factors. John Wiley &Sons, Interscience, New York. 681 pp.

MAYER, A. G. 1914. The effects of temperatureupon tropical marine animals. PubIs. Car­negie Instn. no. 183: 3-21.

McWHINNIE, M. A. 1967. The heat responsesof invertebrates (exclusive of insects). Pages353-374 in A. H. Rose, ed. Thermobiology.Academic Press, New York. 653 pp.

NEWELL, R. C. 1970. Biology of intertidalanimals. American Elsevier, New York.555 pp.

VERNBERG, F. J., and W. B. VERNBERG. 1970.The animal and the environment. Holt,Rinehart & Winston, New York. 398 pp.

VINE, P. J. 1972. Recent research on the crown­of thorns starfish. Underwat. J. 4: 64-73.