MARINE ECOLOGY PROGRESS SERIES Vol. 157: 53-59.1997 Published October 16 Mar Ecol Prog Ser

Effects of reduced salinity on the rates of photosyn- thesis and respiration in the hermatypic and damicornis

'Dept of Systems Ecology. Stockholm University, S-106 91 Stockholm, Sweden 'Dept of Marine Science, Faculty of Science, Chulalongkorn University, Bangkok 103 30. Thailand

ABSTRACT. This paper deals with sublethal salinity stress on reef building corals in the Inner Gulf of Thailand. Maximum photosynthetic and respiratory rates were measured in Porites lutea and Pocillo- pora damicornis as changes in dissolved oxygen levels per hour and the gross production to respiration ratio (Pg:R)calculated. Pg:Rratios were significantly lowered in both when exposed to sudden salinity drops from ambient 3OnR>to 20 and 10%, but P lutea was less affected. Photosynthetic rates were lowered in proportion to the salinity reductions in both species, whereas respiration rates were either slightly decreased or unaltered. When calculating the Pg:R ratios on a 24 h basis both species dis- played values below 1, even at amblent salin~ty[P. lutea 0 71 k 0.04 and P dan1icornis0.89 * 0.02), thus ind~catingthat they do not solely depend on internal primary production for their maintenance. In an experiment on the capacity of hctcrotrophic feeding with Arten~iasahna, P. damicornis showed a clear- ance rate 4 times higher than P. lutea, indicating that P. darnicornis may be more capable of compen- sating for a low Pg:Rratio by heterotrophic feeding.

KEYWORDS: . Porites lutea . Pocillopora danlicornis. Salinlty . Photosynthesis . Respirat~on

INTRODUCTION ity of the surface water decreases dramatically (Menas- veta & Hongskul 1988) and, according to our own field Reef corals were earlier considered to be dependent observations, shallow coral reefs can be exposed to on a very narrow range of environmental conditions salinities as low as 10%0for short periods of time during (Johannes 1975, Endean 1976, Loya 1976, Loya & low tide. Rinkevich 1980). More recent results, however, suggest Despite the importance of salinity to physiological that corals are more adapted to physical stresses than functions necessary for reef coral survival, relatively was previously believed (Muthiga & Szmant 1987, Har- few studies have been made. Most of the literature is land & Brown 1989, Grigg & Dollar 1990, Coles 1992, over 50 yr old, deals with field observations of lethal Coles & Jokiel 1992, Brown 1997b). Nonetheless, there effects following rainstorms or groundwater intrusions, is considerable variation in environmental tolerances and suggests that most species of reef corals are killed among species which can have a major influence on the if salinity is reduced to 15-20% for 24 h or more community structure within sites (Brown 1997a). (Edmondson 1928, Coles & Jokiel 1992, Jokiel et al. Since 4 of Thailand's 5 major rivers discharge into 1993). Only a few authors have studied the effects of the Inner Gulf of Thailand the area receives an exten- sublethal salinity changes (Muthiga & Szmant 1987, sive freshwater load (253 X 108 m3 yr-l; Menasveta et Coles 1992). Corals, like most coelenterates, have few al. 1986).Therefore, during the rainy season the salin- or no mechanisms for osmoregulation (Muthiga & Szmant 1987),and thus a deviation from amb~entsalin- 'E-mail: [email protected] ity will affect their overall metabolism, In the long "Order of these 2 authors was determined by flipping a coin term, this stressed condition will imply decreased

O Inter-Research 1997 Resale of full article not permitted 54 Mar Ecol Prog Se

potential for growth, reproduction, and survival (Coles grown under similar light conditions) were placed in & Jokiel 1992) 5.35 1 transparent cylindrical plastic experimental The objective of the present study was to determine chambers equipped with submersible pumps (Whalee, the physiological responses of corals when exposed to supersub 881). The enclosures were placed in a cool- lowered salinity. Coral photosynthesis and respiration ing bath of continuously running seawater to minimise were measured and changes in the gross production to temperature fluctuations. A short-term experimental respiration ratio (Pg:Rratio) were used to determine set-up was employed since salinity changes mostly the effects of salinity stress on coral metabolism occur rapidly in the study area (Nakano et al. in press) (e.g McCloskey et al. 1978, Kinsey 1983, Edmunds & and because incubation in enclosures for more than a Davies 1986, Muthiga & Szmant 1987). couple of hours without flushing may affect the corals If the net input from the photosynthesis of the coral's severely and make interpretation of data unreliable symbiotic zooxanthellae is reduced (i.e. Pg:Rratio below (McCloskey et al. 1978, Sorokin 1993). 1) this must be compensated for by increased ingestion Physiological measurements. The net effect of the of organic carbon from heterotrophic feeding (Falkowski salinity change on coral metabolism was studied by et al. 1990). The role of heterotrophic nutrition has been calculating the gross production to respiration ratio investigated by several authors, e.g Porter (1976), Ed- (Pg:R).This ratio is a dimensionless estimate of the munds & Davies (1986), Bythell (1988) and Sorokin autotrophic capability of a community or an organism, (1993), and the prevalent conclusion drawn from these and a ratio equal to or above 1 on a 24 h basis indicates studies is that the majority of hermatypic coral species self-maintenance (e.g. Odum & Odum 1.955, Mc- are largely autotrophic. However, we hypothesise that Closkey et al. 1978, Kinsey 1.983). It can be used in a heterotrophic feeding will be relatively more important short-term test to evaluate the effects of changes in in areas like the Inner Gulf of Thailand, where photo- physical parameters on the net metabolism of a photo- synthesis might be reduced due to turbidity and salinity synthetic organism (Johannes 1975, Lindblad et al. stress. Accordingly, in order to estimate the relative ca- 1989, Coles & Jokiel 1992, Sorokin 1993). pability of the corals to compensate for a low Pg:Rratio Net primary production and respiration were mea- by heterotrophic nutrition, the clearance rate was stud- sured as changes in dissolved oxygen levels over 1 h ied. The coral species investigated here were chosen for under both light and dark conditions at 10, 20 and 30'Yx, their dominance in the study area and because Pocillo- salinity. The corals were acclimated in aerated flow- pora damicornis has been shown to be a superior com- through tanks at a specific salinity for 1.5 h before petitor in the area under unstressed conditions com- measurements were started (using filtered natural sea- pared to Porites lutea (Sakai et al. 1989). water diluted with pre-analysed filtered freshwater for the lower salinities). Readings were made every half hour with a polarographic oxygen electrode (Oximeter MATERIALS AND METHODS OX1 196).Oxygen saturation levels were maintained at 75% or above throughout the experiment. The pumps Study site. The present study was conducted in were run during measurements and also for 10 S every November 1994 at Angsila Marine Biological Research 15 min to avoid the build up of oxygen gradients in the Station using coral specimens from the Khang Khao enclosures and to create adequate water movement for Island (13" 09' N, 100" 48' E), in the Sichang Islands. exchange of materials at the tissue-water interface. Inner Gulf of Thailand. The massive coral Porites lutea All oxygen production experiments were run out- is overwhelmingly dominant in the coral community, doors under clear weather conditions between 10:OO which is otherwise poorly developed with low diversity and 14:00 h. Light intensities were recorded continu- (Sakai et al. 1989). ously with a Li Cor quantum sensor, placed adjacent to Collection of corals. Corals were collected along the the experimental chambers, measuring photosyntheti- eastern coast of Khang Khao Island at 4 m depth (tidal cally active radiation. The relationship between the ir- range 53 m; Menasveta et al. 1986). Colonies of Porites radiance at the sensor and the irradiance in the cham- lutea and Pocillopora darnicornis were transported un- bers was determined after the experiments, and the der reduced light and continuous aeration to the field continuously measured insolation actually experienced station where they were placed in continuous-flow by the corals was calculated according to this relation- tanks. No significant temperature increase occurred ship. Light intensities in the study were between 870 during the transport. Corals used in the expenments and 1060 pE m-' S-', which is approximately the same were in good condition, and epiphytes and boring ani- as in the study site at 4 m depth on a clear day (pers. mals were absent or had been carefully removed. obs.). Since these light intensities were above the light Experimental design. Pieces of corals (a total of 27 saturation level (approximately 500 pEm-' S-'; Chalker replicates of each species, of approximately equal size, et al. 1983) the production measured should be consid- Moberg et al.:Salinity effects in herrnatypic corals 55

ered as maximum net photosynthesis. To obtain the taken and also every 20 min for a period of 10 S to maximum gross production (Pg), respiration (R) was ensure that the nauplii were evenly distributed. The added to the net production (Pn), assuming that con- nauplii were counted by visual inspection and the bio- stant respiration over the whole diurnal cycle, and the mass specific clearance rate (CR) was calculated photosynthetic quotient (PQ) and respiratory quotient according to the formula: (RQ)are at approximate unity (McCloskey et al. 1978). CR = lnC,,- lnCl X V X Corr. X B-' X t-' The Pg:R ratios were then extrapolated on a 24 h basis using the light factor method (Kautsky 1995): where CO= initial concentration of A. salina; C, = final concentration of A. salina; V = water volume (enclo- Pg,,, I24 sure volume - coral volume); Corr. = correction factor Pg:'t24' = R,, X 24 X I,, (in percent) for A. salina adsorbed to the coral skeleton where Pg,, = gross production during the 1 h measure- or the wall of the enclosure; B = coral biomass in grams ment (pg O2 1.' h-'); RA,= respiration during the 1 h ash-free dry weight; t = time between the readings. measurement (~igO2 1-! h-'); IL\( = insolation during the Statistical analysis. Statistical comparisons between incubation; and = the daily insolation. means of the Pg:R, Pg:B and R:B ratios for the 3 salini- Biomass determination. The use of Pg:R ratios ties were done using l-factor analysis of variance eliminates the need for biomass determinations. (ANOVA). All data were tested for homogeneity of However, in order to compare the Pg and R values of variance using Cochran's test. When the variances the 2 coral species these data were normalised by were unequal, log-transformations were done and the means of a biomass determination. Such estimations success of each transformation was tested before run- are difficult in corals since the active living biomass is ning the ANOVA. The data was somewhat unbal- distributed in various amounts of calcium carbonate anced, but, as Shaw & Mitchell-Olds (1993) concluded, (McCloskey et al. 1978). Thus, several methods have the effect of unbalanced data on single factor ANOVA been used in the literature, e.g. decalcification, is negligible. Where the l-factor ANOVA showed sig- chlorophyll extraction and ash-free dry weight mea- nificant differences, a multiple comparison of means surement. In the present study the corals were dried was conducted using the Student-Newman-Keuls test. at 70°C for 12 h and combusted at 430°C for 4 h. The coral pieces were purposely selected, for same ap- pearance, size and shape, and ash-free dry weight RESULTS determination was therefore considered to give suffi- ciently accurate values. Pg:Rratio Heterotrophic feeding experiment. The hetero- trophic feeding capacity was studied in a particle Physiological measurements showed that Pg:R ratios retention experiment, conducted at 30%"salinity, using were lowered in both Porites lutea and Pocillopora newly hatched nauplii (0.7 to 1.0 mm) of the commer- damicornis when salinity was reduced (Fig. 1, Tables 1 cial brine shrimp Artemia salina. Dead coral colonies of & 2),indicating that both species were stressed by the equal size to the replicates (all <500 cm3) were used as sudden salinity drop. The Pg:R ratio in P. damicornis controls in order to estimate how many A. salina decreased more rapidly than in P. lutea, implying that attached to the coral structure itself. The initial con- P. darnicornis is more sensitive to decreased salinity centration averaged 7000 A. salina per liter. For each (the slopes of the regression lines in Fig. 1 were signif- replicate 3 samples of 10 m1 were taken initially and icantly different, fi2- fi, = 0.0153 + 0.0037Zooo5,p < after 3 h. The pumps were run while the samples were 0.01).

Table 1. Porites lutea and Pocillopora darnicornis. Data from th,e physiological measurements.Gross production (Pg),respiration (R)and biomass (B)in corals calculated g-' ash-free dry weight (AFDW).SE of means within parentheses

Species Salinity (2,)

Porites lutea 30 20 10 Pocillopora darnjcornjs 30 20 5 6 Mar Ecol Prog Ser 157: 53-59. 1997

R:B ratio lutea displayed a significant decrease in R:B ratio when salinity was reduced from 30 to 10% and from 20 to 10%. However, no significant change was measured between 30 and 20%. Pocillopora damicor- nis, on the other hand, lowered its R:B ratio signifi- cantly between salinity changes from 30 to 10Ym as well as from 30 to 20%0,whereas a decrease from 20 to 10'%0was not significant (Fig. 3, Tables 1 & 2).

01 30 20 10 Salinity (L)

Fig. 1 Por~teslutea and Poc~llopora damicornis. Regression l~nesshowing the correlation between Pg:R ratios per hour and salinity. Pg:R ratios decreased in both species when salin- ity was reduced. The slopes of the 2 lines were significantly different,p2 - 0, = 0.0153 * 0.0037&,,us (p < 0.01). Coefficients of determination for. P. lutea r2 = 0.691 (t= 7.47, df = 25, p << 0.001); P. damicornis rZ = 0.896 (t = 14.68, df = 25, p c< 0.001). For further statistical comparison see Table 2. Numbers of replicates: P. lutea n(30YL) = 11, n(20%) = 8, n(1O0&) = 8; P. darnicornisn(30%0]= 12. n(20Yi) = 8, n(l0%0)= 7

Salinity Pg:B ratio Fig. 3. Porites lutea and Pocillopora darnjcornis. Respiration to The gross production per unit biomass decreased biomass ratios (R:B ratios) + SE per hour at 3 different salini- significantly in proportion to the salinity reductions for ties. In P. lutea respiration was lowered with salinity between both Porites lutea and Pocillopora damicornis. How- 30 and 10L, although the decrease between 30 and 20% was not significant (Student-Newman-Keuls, crit. diff. = 0.217 and ever, P. damicornis showed a larger relative decrease dlff. = 0.136, p > 0.05). Respirat~onIn P. darnicornls was low- when salinity was reduced (Fig. 2, Tables 1 & 2). ered between 30 and 20Ym but not between 20 and loo& (Student-Newman-Keuls, p >> 0.05). For further statistical comparison see Table 2. Numbers of replicates are the same as in Fig 1 Pocillopora Porites Heterotrophic feeding

The heterotrophic feeding experiment, conducted at 30% salinity, indicates that Pocillopora damicornis is more efficient than Porites lulea in consuming zoo- within the size range used here. The clear- ance rate for P damicornis was more than 4 times larger than for P. lutea (0.24 * 0.086 1 h-' g-' biomass compared to 0.05 +. 0.019 1 h-' g-l) (Fig. 4).

30 Fv, 20 Yw Salinity DISCUSSION

Flg. 2. Porites lutea and Pocillopora darnicornis. Gross pro- duction to biomass ratios (Pg:B ratios) + SE per hour at 3 dif- The present study did intend separate the ferent salinities. Pg:B ratio decreased for both species when responses of the coral polyps and their symbiotic zoo- salinity was reduced. For statistical comparison see Table 2. xanthellae, but rather to investigate the combined Numbers of rephcates are the same as in Fig. 1 physiological response of both the and algae. Mobery et al.: Salin~tyeffects in hermatyp~ccol-als 5 7

Table 2. Porites lutea and Pocjllopora darnicornis. Signlfl- species should be regarded as more sensitive to a sud- cance levels of the statistical analysis of means for the 3 phys- den drop in salinity. This conforms with several other ~ologicalratios at 30, 20 and 10% salinity. Comparisons done studies indicating that P. damicornis is more stenoha- withln each species. One-factorANOVA, log transformed val- ues when needed, and multiple comparisons of means con- line than most other corals and Porites is among the ducted using the Student-Newman-Keuls test, ns:not signifl- least sensitive to salinity changes (Edmondson 1928, cant. 'p < 0.05, "p < 0.01 Coles 1992, Coles & Jokiel 1992, Jokiel et al. 1993, Nakano et al. in press).

Species Salinity (%D) Photosynthetic rates (Pg:Bratios) were diminished in 20 30 both coral species when salinity was reduced below ambient levels, but Pocillopora damicornis was slightly Porites lutea Pg:R 10 .. .. 20 - .. more affected. However, reduced photosynthesis was Pg:B 10 .. .. also accompanied by a decreased respiratory rate for 20 - both species. Similar physiological responses to sud- R:B 10 .. den salinity drops were observed by Muthiga & 20 - ns Szmant (1987) in Siderastrea siderea, and, according Pocillopora damicornis Pg:R 10 .. .. to Vernberg & Vernberg (1972), a reduction in respira- 20 - .. tory rate is a typical adaptive response to salinity Pg:B 10 .. .. stress. Lowering of the respiration rate entails de- - .. 20 .. creased metabolic costs for maintenance, which has R:B 10 ns .. been described as an important function in the cellular 20 - response to stress, that increases the capability of the organism to resist changes in the environment (Koehn & Bayne 1989). Compared to P. damicornis, Porites lutea had a significantly greater ability to reduce respi- ratory costs when salinity dropped to 10%o.The respi- ration rate of P. damicornis was reduced when exposed to 20%, whereas no further reduction was seen at 10?L0,implying that P. damicornis is not able to adapt its metabolism to the same extent as P. lutea. A possible reason for both the reduction in photosyn- thesis and respiration could be that corals contract their polyps in order to minimise contact with the low salinity water (Muthiga & Szmant 1987). Contraction was actually observed in both species. This leads to reduced gas exchange and thus lowered respiration. 0.0 Moreover, contraction also entails diminished photo- Porites Pocillopora synthesis as a consequence of reduced exposure of the zooxanthellae to light. Other possible detrimental Fig. 4. Clearance rate+ SE for Porites lutea (0.05 * 0.019 1 h-' effects of the osmoregulatory stress are: cell disruption g-' AFDW) and Pocillopora damicornis (0.24 2 0.086 1 h-' g-'1 at 30% salinity on Artemia salina nauplii due to swelling (Muthiga & Szmant 1987) and a de- crease in chlorophyll per algal cell or zooxanthellae loss (bleaching) (e.g. Coles & Jokiel 1992, Fang et al. Such an approach implies that the metabolic activity of 1995). Moreover, corals display enhanced mucus consumers, such as heterotrophic bacteria in the release under stressed conditions, which is a metaboli- secreted mucus of corals (Segel & Ducklow 1982), is cally important carbon sink (Riegl & Branch 1995). The included in the Pg:R ratio measurements. overall stress in terms of energy loss could thus be con- Since salinity reductions often occur very rapidly, siderably greater at 20 and 10%0than what is indicated generally a few hours during low tide and extreme by the decrease in Pg:R ratios. rainfall, we argue that a short-term stress study was There may be several explanations for the domi- appropriate. The sudden salinity reductions from nance of Porites lutea and the impoverishment of other ambient to 20 and 10%0resulted in a significant decline coral species at the study area. These include interspe- in Py:R ratios in both studied species, but Pocillopora cific variation in sediment tolerance (cf. Stafford-Smith darnlcornis showed a more marked response than 1993), selective grazing by the Diadema setosum ur- Porites lutea when considering a range of salinities chin on juvenile corals and bioerosion inducing frag- between 30 and 10%o.Thus, we believe that the former mentation-propagation of large P, lutea corals (Sakai et 58 Mar Ecol Prog Ser

al. 1989) Moreover, as shown in this study, different Acknowledgenients We thank Professor Plamsak Mena- susceptibility to sublethal salinity stress may play an s~t-td, Dlrcctor of Aquatic Resources Research Institute, and equally significant role. Professors Manuwadi Hungspreugs and Suraphol Sudara, Department of Marine Science. ChulalongkornUnivers~ty, for Although extrapolation of short-term metabolic makinq th~sstudy possible. Ure are especially grateful to Dr studies to a daily basis may produce artefacts (cf Mc- Ron Johnstone, Departmentof Zoology, Stockholm University Closkey et al. 1978, Jokiel & Morrissey 1986), we also for helpful comments on an earlier version of the manuscript. calculated our values over 24 h for purposes of com- Finally, we would like to express our gratitude for the finan- clal support given by SiVEDMAR (SwedishCentre for Coastal parison with previously published data. Even at the Development and Management of Aquatic Resources) and ambient salinity Pg:R ratios were below 1 on a 24 h SIDA (Swedish International Development Cooperation basis for both species; 0.7 for Pontes lutea and 0.9 for Authority). Pocillopora damicornis. ~VcCloskey et al. (1978) and Sorokin (1993) suggest normal ranges in the Pg:R ratio LITERATURE CITED between 0.8 and 3.5 for Pocillopora and 0.3 and 3.6 for Porites. Even though our results are within these Abdel-Salam HA, Porter JW (1988) Physiological effects of ranges they are still too low for autotrophic mainte- sediment rejection on photosynthesis and respiration In nance of the corals. To some extent the low values three Caribbean reef corals. Proc 6th Int Symp 2:285-291 could be due to stress, related to the handling of the Brown BE (1997a) Disturbances to reefs In recent times. In: specimens. Such an effect is, however, considered to Birkeland C (ed)Life and death of coral reefs. Chapman & be low as an experiment conducted in situ gave the Hall, New York, p 354-378 same results (Nystrom et al. 1997). Brown BE (1997b)Adaptations of reef corals to physical envi- A more likely explanation of the low Pg:R ratios is ronmental stress Adv Mar B101 31:221-299 Bythell JC (1988) A total nitrogen and carbon budget for the that the present study site is subjected to siltation com- elkhorn coral Acropora palrnata (Lamarck). Proc 6th Int bined with eutrophication (Lemay & Hale 1991), lead- Coral Reef Symp 2:535-540 ing to increased respiration due to sedimentation stress Chalker BE, Dunlap WC, Ol~verJK (1983) Bathymetric adap- (Abdel-Salam & Porter 1988) and decreased net pro- tation of reef-building corals at Davies Reef, Great Barrier Reef, Australia. 11.Light saturation curvesfor photosynthe- duction as a consequence of reduced light penetration. sis and respiration. J Exp Mar Biol Ecol73:37-56 Although corals are able to photoadapt, it seems that Coles SL (1992) Experimental companson of salinlty toler- shade ad.apted corals might excrete more organic car- ances of reef corals from the Arabian Gulf and Hawaii. bon and therefore need to supplement autotrophic fix- Evidence for hyperhaline adaptation. Proc 7th Int Coral ation by ingesting organic carbon from heterotrophic Reef Symp 1:223-234 Coles SL, Joklel PL (1992)Effects of sallnity on coral reefs. In: feedlng (Falkowski et al. 1990). Thus, reduced light Connell DW, Hawker DW (eds) Pollution In tropical penetration may in the long run favour species relying aquatic systems. CRC Press Inc, London, p 147-166 more upon heterotrophic feeding. Edmondson CH (1928)The ecology of a Hawaiian coral reef. The present study implies that Pocillopora damicor- Bull Bernice P Bishop Mus 45:l Edmunds PJ, Davies PS (1986)An energy budget for Pontes nis, when compared to Porites lutea, is 4 times more pontes. Mar Biol92:339-347 efficient in heterotrophic feeding on newly hatched Endean R (1976) Destruction and recovery of coral reef com- Artemia salina. This result is only an estimation of the munities. In: Jones OA, Endean R (eds) Biology and geol- clearance rate and the feeding rates obtained may ogy of coral reefs, Vol 3. Bjology 2. Academ~cPress, New therefore not equate to the efficiency at different food York, p 215-255 Falkowski PG, Jokiel PL, Kinzle RA (1990) Irradiance and availabilities and qualities or different size classes of corals In: Dubinsky Z (ed) Ecosystems of the world, Vol food particles. Thus, the results must be critically eval- 25. Elsevier, New York. p 89-107 uated before being related to the situation in nature. Fang LS. Liao CW. Liu MC (1995) Pigment compositionin dif- Nonetheless, the relative difference in the feeding ferent-colored sclcractinian corals before and during the bleach~ngprocess. Zool Stud 34:lO-17 rates of the 2 species conforms with sim~larstudies by Gngg RMI, Dollar SJ (1990)Natural and anthropogenic distur- Sorokin (1993) showing an assimilation rate approxi- bance on coral reefs. In: Dubinsky Z (ed) Ecosystems of mately 4 times higher for l? damicornis than Pontes the world, V01 25 Elsevier, New York, p 439-452 annae. On the other hand, P lutea may be better Harland AD, Brown BE (1989)Metal tolerance in the sclerac- adapted to feeding on bacterioplankton and dissolved tinian coral Porites lutea. Mar Pollut Bull 20(7):353-357 Johannes RE (1975) Pollution and degradation of coral reef organic matter than P damicornis, which has been communities. In: Ferguson Wood EJ, Johannes RE (eds) observed in other corals of the genus Porites (P,annae) Tropical marine pollution. Elsevier Scientific Publishing, (Sorokin 1993). Hence, degree of physiological toler- Amsterdam, p 13-50 ance to salinity fluctuations and capacity to feed on Jok~elPL, Hunter CL, Taguchi S, Watarai L (1993)Ecological Impact of a fresh-water 'reef kill' in Kaneohe Bay, Oahu, dissolved and particulate organlc matter may be very Hawal~.Coral Reefs 12:177-184 important structuring factors for the coral community Jokiel PL. Morrissey JI (1986) Influence of size on primary in the innermost part of the Gulf of Thailand. production in the reef coral PociUopora danlicornis and the Moberg et al.. Salinity effects In hermatypic corals 5 9

macroalga Acanthophora spicifera. Mar Biol91:15-26 ence to the Sichang Islands. Galaxea 5:?-13 Kautsky U (1995) Ecosystem processes in coastal areas of the Muthiga NA, Szmant AM (1987) The effects of salinity stress Baltic sea. PhD thesis, Department of Zoology, Stockholm on the rates of aerobic respiration and photosynthesis in University the hermatypic coral Siderastrea siderea. Biol Bull (Woods Kinsey DW (1983) Standards and performance in coral reef Hole) 173:539-551 primary production and carbon turnover. In Barnes DJ Nakano Y, Tsuchiya M, Rungsupa S, Yamazato K (in press) (ed) Perspectives on coral reefs. Australian Institute of Influences of severe freshwater floodlng dunng the rainy Marine Science Contribution Number 200, Brian Clouston season on the coral community around Khang Khao Island Publisher, Manuka, p 209-220 in the Inner Gulf of Thailand. Tha~J Aquat Sci Koehn RK, Bayne BL (1989) Towards a physiological and Kystrom M, Moberg F, Tedengren M (1997) Natural and genetical understanding of the energetics of the stress anthropogenic disturbance on reef corals in the Inner Gulf response. Biol J Linn Soc 37:157-171 of Thailand; physiological effects of reduced salinity, cop- Lemay M, Hale LZ (1991) A national coral reef strategy for per and siltation. Proc 8th Int Coral Reef Symp Thailand. Vol 1, Statement of need, Thailand Coastal Odum HT, Odum EP (1955) Trophic structure and productiv- Resources Management Project, Offlce of the National ity of a \vlnd\vard coral reef community on Eniwetok Atoll. Environment Board, University of Rhode Island, and US Ecol Monogr 25:291-320 Agency for International Development Porter (1976)Autotrophy, heterotrophy and resource partition- Lindblad C, Kautsky U, Andre C, Kautsky N, Tedengren M lng in Canbbean reef-building corals. Am Nat 110:731-742 (1989) Functional response of Fucus veslculosus commu- Riegl B, Branch GM (1995) Effects of sediment on the energy nities to tributyltin measured in an in s~tucontlnuos flow- budgets of four scleractinian (Bourne 1900) and five alcy- through system. Hydroblologia 188/189:277-283 onacean (Lamourox 1816) corals. J Exp Mar Biol Ecol 186: Loya Y (1976) Recolonisation of Red Sea corals affected by 259-275 natural catastrophes and man-made perturbations. Ecol- Sakai K. Snidvongs A. Nishihira M (1989) A mapping of a ogy 57:278-289 coral-based, non-reefal community at Khang Khao Island, Loya Y, Rinkevich B (1980) Effects of oil pollution on coral reef inner part of the Gulf of Thailand: interspecific competi- communities. Mar Ecol Prog Ser 3:167-180 tion and community structure. Galaxea 8:185-216 McCloskey LR,Wethey DS, Porter JW (1978) Measurement Segel LA, Ducklow HW (1982) A theoretical investigation into and interpretation of photosynthesis and respiration the ~nfluenceof sublethal stresses on coral-bacterial eco- in reef corals In: Stoddart DR, Johannes RE (eds) Coral system dynamics. Bull Mar Sci 32(4):919-935 reefs: research methods. Monographs on oceanographic Shaw RG, M~tchell-OldsT (1993) ANOVA for unbalanced methodology, VolS.UNESC0, Paris, p 379-396 data: an overview. Ecology 74(6):1638-1645 Menasveta D, Hongskul V (1988) The Gulf of Thailand. In: Sorokin Y1 (1993) Coral reef ecology. Ecological stud~es,Vol Postma H, Zijlstra JJ (eds) Ecosystems of the world. Vol27, 102. Springer Verlag, Berlin Continental shelves (Ecosystem Analyses). Elsevier. Ams- Stafford-Smith MG (1993) Sediment-rejection of 22 species of terdam, p 363-383 Australian scleractinian corals. Mar Biol 115:229-243 Menasveta P, Navanarasest M, Rungsupa S (19861 Env~ron- Vernberg FJ, Vernberg WB (1972) Environmental physiology mental setting of the Gulf of Thailand with special refer- of marine . Springer Verlag, New York

Editorial resp~n~iblllty~Otto Kinne, Submitted: January 20, 1997; Accepted. July 14, 1997 OldendorfILuhe, Germany Proofs received from author(s): September 22, 1997