Pacific Science (1994), vol. 48, no. 3: 313-324 © 1994 by University of Hawaii Press. All rights reserved

Ratio of Energy and Nutrient Fluxes Regulates between Zooxanthellae and Corals1

Z. DUBINSKy2 AND P. L. JOKIEL3

ABSTRACT: Ambient irradiance levels determine the rate ofcarbon influx into zooxanthellae at any given time, and thereby the energy available for the whole coral symbiotic association. Long-term photoacclimation of zooxanthellae to the time-averaged light regime at which the host coral grows results in optimiza­ tion of light harvesting and utilization. Under high irradiance light harvesting is reduced, thereby avoiding photodynamic damage, whereas under low light, photon capture and quantum yield are maximized. Most of the photosynthate produced by the is respired. However, the capability of the zooxanthellae and the coral to retain carbon beyond that required to meet their respiratory needs depends on the availability of the commonly limiting nutrients, nitrogen and phosphorus. Therefore, the ratio of the flux of these nutrients into the colony to that of the photosynthetically driven carbon flux will regulate the growth ofthe zooxanthellae and ofthe . Nutrients acquired by predation of the coral on are available first to the animal, whereas those absorbed by the zooxanthellae from seawater as inorganic compounds lead first to growth of the algae.

IT HAS BEEN an accepted dogma in coral biol­ to the photosynthetic production of high­ ogy that the extensive spatial and long-term energy compounds, mainly carbohydrates. temporal success of coral reefs in the oligo­ These are produced in great excess of that trophic littoral of tropical seas stems from needed to support the basic metabolic needs the symbiotic association between endocellu­ ofthe zooxanthellae. However, because these lar microalgae (the zooxanthellae) and the compounds have a very high C: N ratio, they host hermatype. It is this association that cannot by themselves support multiplication allows corals and coral reef communities to ofthe algae. The excess photosynthate, which thrive in spite of the low concentrations of may reach as much as 95% of the total, is nitrogen and phosphorus in the oligotrophic "translocated" to the host animal, a process ambient waters (Muscatine and Porter 1977). stimulated by "host factors" that dramati­ It is this oligotrophy that also causes the cally increase the excretion of assimilated striking paucity of phyto- and zooplankton carbon compounds by the algae (Muscatine in these "blue deserts," limiting the availabil­ 1967, Sutton and Heegh-Guldberg 1990). ity ofparticulate food as an alternate nutrient The translocated carbon compounds are source. more than enough to provide for the respira­ In this mutualistic symbiosis the algae tory needs ofthe host (Muscatine et al. 1984), contribute their capability to harness sunlight although, as is also the case for the zooxan­ thellae, they cannot support growth of ani­ mal tissue. These energy-rich, nitrogen-poor I This study was supported by grant no. 89 00444 products of photosynthesis were termed from the U.S.-Israel Binational Science Foundation. "junk food" because of their insufficiency as Manuscript accepted 15 August 1993. food for growth (Falkowski et al. 1984). 2 Department of Life Sciences, Bar-Ilan University, Ramat Gan 52900, Israel. In return for fixed carbon, the zooxanthel­ 3 Hawaii Institute of Marine Biology, University of lae gain access to the high nitrogen and phos­ Hawaii, P.O. Box 1346, Kaneohe, Hawaii 96744. phorus metabolic waste products of their 313 314 PACIFIC SCIENCE, Volume 48, July 1994 host. Thereby the colony retains and recycles zooxanthellae of S. pistillata is by change in these precious substances, which in the ab­ size, not in the number, of photosynthetic sence of the algae would have been excreted units (Falkowski and Dubinsky 1981), al­ into the sea and lost to the system. In addi­ though this may not be true for all zooxan­ tion to photosynthetic capability, the two thellae (Chang and Tr:ench 1982). It was also partners in the coral symbiosis also differ in found that the HL zooxanthellae had higher that the animal is an avid and efficient preda­ dark respiration and light-saturated photo­ tor on zooplankton, an important source of synthetic rates and lower quantum yields nitrogen, while the zooxanthellae are capable than their LL counterparts (Falkowski and of assimilating inorganic nitrogen and phos­ Dubinsky 1981, Dubinsky et al. 1984, Porter phorus compounds inaccessible to the ani­ et al. 1984). The animal responses to the dif­ mal. However, it is important to bear in mind ferent light regimes included higher respira­ that under normal reef conditions both of tion and calcification in the HL corals (Du­ these sources are very limited. Therefore, al­ binsky et al. 1983, Porter et al. 1984). In those though the very efficient uptake by the zoo­ studies it was also concluded that in S. pis­ xanthellae of nutrients produced by the host tillata, under high light, photosynthesis is animal assures recycling of these resources sufficient to provide substrata for both ani­ and prevents their loss from the association mal and algal respiration, which is not the (Rahav et al. 1989), this cannot account for case in LL colonies, which have to supple­ growth or "new production." ment algal photosynthesis by animal preda­ The effects ofthe modulation ofthe flux of tion (Falkowski et al. 1984). carbon into zooxanthellate corals in response In a subsequent series of studies the effect to different light intensities, as those encoun­ ofadded nutrients and of feeding on Artemia tered at different depths, has been examined salina (Linnaeus) nauplii on S. pistillata was in some detail, mostly in a series ofstudies of examined (Muscatine et al. 1989, Dubinsky the common coral Stylophora pis­ et al. 1990, Falkowski et al. 1993). Although tillata Esper (Falkowski and Dubinsky 1981, nutrient-enriched colonies changed within 3 Muscatine et al. 1983, 1984, Dubinsky et al. weeks to nearly black, whereas the controls 1984, Falkowski et al. 1984, Porter et al. remained ivory colored, making them look 1984). It has been found that the zooxanthel­ like LL and HL colonies, this change resulted lae photoacclimate within a week to a new not from change in the pigment content in irradiance level and that the host also re­ the zooxanthellae as was the case in photo­ sponds to this change. Among the reported acclimation, but from an up to five-fold in­ differences between high (HL)- and low-light crease in algal population. Nutrient enrich­ (LL) corals were differences in areal chloro­ ment brought about additional changes in phyll a. These were a result ofup to four-fold the interrelation between the zooxanthellae increases in the concentration ofthis pigment and the coral. Division rate of the zooxan­ in the LL zooxanthellae. This difference was thellae increased (H0egh-Guldberg 1994), clearly mirrored on the ultrastructural level, but their photosynthetic rates on a per-cell as a corresponding difference in thylakoid basis decreased, probably resulting from area (Dubinsky et al. 1984, Berner et al. carbon limitation in the dense algal popula­ 1987). tion (Dubinsky et al. 1990). The fraction of In most cases, photoacclimation was re­ photosynthate translocated to the host also ported to occur primarily on the cellular level decreased. of the zooxanthellae, and their densities re­ In studies on the effect of nutrient enrich­ mained around 106 cells cm-2 (but see also ment done in Hawaii with Pocillopora dami­ Dustan 1979 and Titlyanov 1991). However, cornis (Linnaeus), it was also found that under extremely low irradiance the algae are nutrient enrichment resulted in increased confined to the side of the colony facing the algal density (Stambler et al. 1991). In those light (Figures I and 2). studies nutrient enrichment also led to signifi­ The strategy of photoacclimation in the cantly reduced calcification rates (Stimson

Uli Energy and Nutrient Ratios Regulate Symbiosis-DuBINSKY AND JOKIEL 315 ..

FIGURE I. Stylophora pistil/ata colony from a deep, shaded crevice. The dark side is the one facing the light; the side facing the rear wall, reflected in the mirror, is nearly white.

1992). Nitrogen enrichment was also re­ teractions between the underwater light and ported to weaken the skeletal architecture of nutrient fields surrounding corals. The effects corals (Yamashiro 1992) and slow down its oflight and ofnutrients were hitherto studied growth (Stambler et al. 1991). separately, and we shall attempt to integrate In this study we examine the possible in- the concepts that emerged from these studies. 316 PACIFIC SCIENCE, Volume 48, July 1994

FIGURE 2. Stylophora pistillata at 66 m in the Gulf of Elat, northern Red Sea. Zooxanthellae are found only on the up-facing, dark surface; none are on the down-facing side (shown).

Light and Nutrient Flux under low light most corals remain with their tentacles extended continuously (Figure 3). When corals exposed to various light in­ Second, why should HL corals, which have tensities are compared, two interesting ques­ more photosynthate produced than that tions emerge. First, in LL corals, photosyn­ needed to support respiration (Figure 4a and thesis alone cannot account for all of the b), still have to hunt for zooplankton. Al­ colony respiration; therefore such colonies though such HL colonies usually extend their have to supplement zooxanthellae autotro­ tentacles only after sundown, why should phy with heterotrophic animal predation on they extend them at all? Yonge (1930:54) zooplankton (Falkowski et al. 1984). Indeed, wrote "Corals as a general rule, expand only

IX " Energy and Nutrient Ratios Regulate Symbiosis-DuBINSKY AND JOKIEL 317

FIGURE 3. Stylophora pistillata colony growing under low light. Polyps remain constantly extended. at night when, as the results of the investiga­ nitrogen-limited and, assuming that respira­ tions on plankton will make abundantly tion preferentially uses high C: N com­ clear, their food is most abundant." There is pounds, may in fact not be nitrogen-limited no doubt that these corals are hunting quite at all, HL corals have to be severely nitrogen­ efficiently the zooplankton that rises at night limited, although both grow in the same from deeper waters. water. In an analysis of the products of Because the nutrient concentration to photosynthesis in corals growing at different which LL and HL corals are exposed does depths, it was indeed found that in deep­ not differ, we would assume that they do not water corals a much higher fraction ofphoto­ differ in their nutrient status. However, this synthetically assimilated 14C was incorpo­ seems not to be the case. To grow, both zoo­ rated into amino acids than in shallow-water xanthellae and coral have to acquire carbon (HL) corals (Bil' et al. 1992). and nitrogen at the same ratios found in their We suggest that, unlike LL colonies, HL biomass, but assuming that inorganic nitro­ corals do not hunt zooplankton for their car­ gen intake by the zooxanthellae is controlled bon but rather for their nitrogen (Atkinson by its concentration in the water, that ofcar­ 1992). Of course, the nutrient requirement of bon is governed by photosynthesis and, the zooxanthellae population also depends thereby, by irradiance. Therefore, although on algal numbers. Indeed, under reduced LL colonies acquire carbon and nitrogen at densities of zooxanthellae, like those oc­ the C:N ratio of 9.97, HL colonies acquire curring in partially bleached coral colonies, them at a 30.15 ratio (Falkowski et al. 1984, the algae are nutrient sufficient (Cook et al. Muscatine et al. 1984). From this follows that 1992). while at low light corals may be only slightly Although it is easy to see why LL corals

-..:.-:.:-...... -.:_.~.~-,...:>."'----...... -_._----~---_ ...._.-----_._._- 318 PACIFIC SCIENCE, Volume 48, July 1994

a

f:t. POO:~ ~.. )TRN

PREDATION...... SKELETON

b RESPIRATION

MUCUS, PLANULAE, PHOT~S~Es;::)· )TRANSlOCATIO~ ~ ZOOX

PREDATION...... SKELETON

FIGURE 4. Carbon budget for 24 hr in HL (a) and LL (b) colonies of Stylophora pistillata (redrawn after Falkowski and Dubinsky 1981). would extend their tentacles continuously, to such as Goniopora lobata Edwards & Haime. capture as much ofthe scarce zooplankton as However, this may not be a universal phe­ possible, we do not have an explanation of nomenon (Lasker 1979) and is not the case in the daylight retraction of tentacles by most Hawaiian reefs. An analogous situation was (not all) shallow-water corals, as may be seen described when S. pistil/ata colonies from dif­ in Figures 5-7 (Abe 1939). In the Red Sea ferent depths and irradiance levels were com­ and in the Caribbean (Porter 1974), this is pared for their prey hunting and killing effi­ indeed the rule, with very few exceptions, ciency (E. A. Titlyanov, V. A. Leletkin, and FIGURE 5. The Red Sea coral Pleurogyra sinuosa (Dana): (a) during daytime, with polyps contracted, vesicles extended; (b) at night with polyps fully extended, nematocyte batteries visible, vesicles collapsed. FIGURE 6. The Red Sea coral Platygyra lamellina (Ehrenberg): (a) during daytime, with polyps contracted; (b) at night, with polyps fully extended.

!Q == FIGURE 7. The Red Sea coral Favitesjiexuosa (Dana): a and b as in Figure 6. 322 PACIFIC SCIENCE, Volume 48, July 1994

Z.D., unpublished data). In all cases HL col­ ratios in the algae decrease (Muscatine et al. onies showed lower prey-hunting efficiency 1989, Muller-Parker et al. 1992), and the al­ than the deep-water, LL colonies. gae are able to use photosynthetically pro­ duced carbon skeletons for the synthesis of nitrogen-containing molecules required for The Effects ofNutrient Enrichment and cell multiplication, such as amino acids and Feeding on Carbon Flux nucleotides. The algal population increases If we examine the energy and nutrient re­ two- to five-fold in numbers, with their respi­ lationships from the nutrient end, we may ratory needs being satisfied before those of find some additional interesting interactions. the coral. As a result of this growth in algal Because to increase in numbers zooxanthel­ population, the increased algal population lae have to acquire on the order of one atom becomes carbon-limited, producing less pho­ of nitrogen for every seven carbon atoms, it tosynthate per cell (Dubinsky et al. 1990); follows that any carbon in excess ofthis ratio of the total produced, more is respired, and will be either respired or translocated to the more is retained, ending up as new zooxan­ host. In corals exposed to elevated nutrient thellae cells. levels, the zooxanthellae, instead of acting It also was shown that if the coral is fed like a carbon-moving conveyer belt translo­ zooplankton, not only will the coral tissue be eating "junk food" to the coral host, retain able to grow, as is shown in an increase in seven carbon atoms for every nitrogen atom animal protein (Muscatine et al. 1989), but as absorbed from the water. This results in two a result of enhanced metabolism (Rahav et changes in the symbiotic association. Less al. 1989) and digestion the zooxanthellae will carbon is translocated to the host, the C:N be provided with nitrogen by "reverse trans-

, .­ , , / '" / I

00 SKELETON EXPULSION 0

FIGURE 8. Interactions between nitrogen and carbon fluxes in zooxanthellate corals. Light and dissolved inor­ ganic nitrogen control the allocation ofcarbon to either proliferation ofalgae or translocation to host. Translocation affects the importance and intensity of feeding. Solid arrows represent carbon fluxes, dashed lines fluxes of nitrogen. I and 2 are the main external forcing functions; 3 is an internal feedback loop. Shaded areas represent biomass growth.

4 B Ii pin: I IE dfi¥DI Qli§ilt%PJl4& tZU,' _ Energy and Nutrient Ratios Regulate Symbiosis-DuBINSKY AND JOKIEL 323

location." Feeding on zooplankton, by in­ levels of zooxanthellae in the soft coral creasing nitrogen supply, will reduce the up­ arboreum (, Al­ take of ammonium from the water by the cyonacea). Symbiosis 3: 23-40. zooxanthellae, as was shown using 14C me­ BIL', K. Y., P. V. KOLMAKOV, and L. MUSCA­ thylamine, a nonmetabolizable ammonuim TINE. 1992. Photosynthetic products of analogue (D'Elia and Cook 1988). Al­ zooxanthellae of the reef-building corals Moghraby et al. (1992) recently reported that Stylophora pistillata and Seriatopora co­ feeding Galaxeafascicularis (Linnaeus) polyps liendrum from different depths of the Sey­ reduced their uptake of free amino acids chelles Islands. Atoll Res. Bull. 377: 1-8. from the water. CHANG, S. S., and R. K. TRENCH. 1982. Peridinin-chlorophyll a proteins from Conclusions the symbiotic ( = Gymnodinium) microadriaticum, Freu­ Figure 8 summarizes the main interactions denthal. Proc. R. Soc. Lond. B BioI. Sci. and feedback mechanisms connecting light 215: 191-210. intensity, nutrient level, and feeding in zoo­ COOK, C. B., G. MULLER-PARKER, and C. F. xanthellate corals: (1) Under constant D'ELIA. 1992. Factors affecting nutrient nutrient concentration, light intensity deter­ sufficiency for symbiotic zooxanthellae. mines the onset ofnutrient limitation; as light Page 19 in Proc. 7th Int. Coral Reef increases, C:N ratios exceed Redfield ratios. Symp., Guam (abstract). (2) The availability ofother nutrients, mainly D'ELIA, C. F., and C. B. COOK. 1988. nitrogen, determines the fate of photoassimi­ Methylamine uptake by zooxanthellae­ lated carbon. Under high C: N ratios, most invertebrate symbioses: Insights into host carbon goes into respiration, calcification, ammonium environment and nutrition. and excreted mucus, whereas low C:N ratios Limnol. Oceanogr. 33: 1153-1165. favor increases in zooxanthellae density, re­ DUBINSKY, Z., P. G. FALKOWSKI, J. PORTER, duce translocation, and slow down calcifica­ and L. MUSCATINE. 1984. The absorption tion. (3) Feeding on zooplankton by the coral and utilization of radiant energy by light under low light provides carbon for metab­ and shade-adapted colonies of the herma­ olism. Under high light it supplies both algae typic coral, Stylophora pistillata. Proc. R. and animal with nitrogen. Soc. Lond. B BioI. Sci. 222:203-214. DUBINSKY, Z., P. FALKOWSKI, and D. SCHARF. 1983. Aspects of the adaptation LITERATURE CITED of hermatypic corals and their endosym­ ABE, N. 1939. On the expansion and contrac­ biotic zooxanthellae to light. In Proceed­ tion of the polyp of a reef coral, Caula­ ings of the International Conference on strea furcata Dana. Palao Trop. BioI. Stn. Marine Science in the Red Sea. Bull. Inst. Stud. 1:651-669. Oceanogr. Fish. 9: 124-134. AL-MoGHRABY, S., D. ALLEMAND, and J. DUBINSKY, Z., N. STAMBLER, M. BEN-ZION, lAUBERT. 1992. Neutral amino acid uptake L. MCCLOSKEY, P. G. FALKOWSKI, and L. by the symbiotic coral Galaxea fascicu­ MUSCATINE. 1990. The effects of external laris: Effect of light and feeding. Page 2 in nutrient resources on the optical proper­ Proc. 7th Int. Coral Reef Symp., Guam ties and photosynthetic efficiency of Stylo­ (abstract). phora pistillata. Proc. R. Soc. Lond. B ATKINSON, M. J. 1992. Toward a kinetic un­ BioI. Sci. 239: 231-246. derstanding of coral reef metabolism. In DUSTAN, P. 1979. Distribution ofzooxanthe1­ Proc. 7th Int. Coral Reef Symp., Guam lae and photosynthetic chloroplast pig­ (abstract 5q. ments of the reef-building coral Mon­ BERNER, T., Y. ACHITUV, Z. DUBINSKY, and tastrea annularis Ellis and Solander in re­ Y. BENAYAHU. 1987. Pattern of distribu­ lation to depth on a West Indian coral tion and adaptation to different irradiance reef. Bull. Mar. Sci. 29: 79-95. 324 PACIFIC SCIENCE, Volume 48, July 1994

FALKOWSKI, P. G., and Z. DUBINSKY. 1981. MUSCATINE, L., P. G. FALKOWSKI, J. PORTER, Light-shade adaptation of Stylophora pis­ and Z. DUBINSKY. 1984. Fate ofphotosyn­ til/ata, a hermatypic coral from the Gulfof thetically fixed carbon in light and shade­ Eilat. Nature (Lond.) 289: 172-174. adapted corals. Proc. R. Soc. Lond. B FALKOWSKI, P. G., Z. DUBINSKY, L. MUSCA­ BioI. Sci. 222: 181-202. TINE, and L. MCCLOSKEY. 1993. Popula­ PORTER, J. W. 1974. Zooplankton feeding by tion control in symbiotic corals. Bio­ the Caribbean reef-building coral Monta­ Science 43 (9): 606-611. strea cavernosa. Pages 111-125 in Proc. FALKOWSKI, P. G., Z. DUBINSKY, L. MUSCA­ 2nd Int. Coral Reef Symp., Brisbane. TINE, and J. PORTER. 1984. Light and the PORTER, J., L. MUSCATINE, Z. DUBINSKY, and bioenergetics of a symbiotic coral. Bio­ P. G. FALKOWSKI. 1984. Reef coral ener­ Science 34: 705-709. getics: Primary production and photo­ H0EGH-GULDBERG, O. 1994. Population dy­ adaptation. Proc. R. Soc. Lond. B BioI. namics of symbiotic zooxanthellae in the Sci. 222: 161-180. coral Pocil/opora damicornis exposed to RAHAV, 0., Z. DUBINSKY, Y. ACHITuv, and elevated ammonium [(NH4)2S04] con­ P. G. FALKOWSKI. 1989. Ammonium centrations. Pac. Sci. 48: 263-272. metabolism in the zooxanthellate coral LASKER, H. R. 1979. Light dependent activity Stylophora pistil/ata. Proc. R. Soc. Lond. patterns among reef corals: Montastraea B BioI. Sci. 236: 325-337. cavernosa. BioI. Bull. (Woods Hole) 156: STAMBLER, N., N. POPPER, Z. DUBINSKY, and 196-211. J. STIMSON. 1991. Effects of nutrient en­ MULLER-PARKER, G., C. F. D'EuA, and C. B. richment and water motion on the coral COOK. 1992. Elemental composition of Pocil/opora damicornis. Pac. Sci. 45: 299­ corals exposed to elevated seawater NH4. 307. Page 73 in Proc. 7th Int. Coral Reef Symp., STIMSON, J. 1992. The effect of ammonium Guam (abstract). addition on coral growth rate. Page 99 in MUSCATINE, L. 1967. Glycerol excretion by Proc. 7th Int. Coral Reef Symp., Guam symbiotic algae from corals and Tridacna, (abstract). and its control by the host. Science (Wash­ SUTTON, D. C., and O. H0EGH-GULDBERG. ington, D.C.) 156: 516-519. 1990. Host-zooxanthella interactions in MUSCATINE, L., and J. PORTER. 1977. Reef four marine invertebrate symbioses: As­ corals: Mutualistic symbioses adapted to sessment of host extract on symbionts. nutrient-poor environments. BioScience BioI. Bull. (Woods Hole) 178: 175-186. 27: 454-460. TITLYANOV, E. A. 1991. Light adaptation and MUSCATINE, L., P. G. FALKOWSKI, and Z. production characteristics of branches DUBINSKY. 1983. Carbon budgets in sym­ differing by age and illumination of the biotic associations. Endocytobiosis 2: hermatypic coral Pocil/opora verrucosa. 649-658. Symbiosis 10: 249-260. MUSCATINE, L., P. G. FALKOWSKI, Z. Du­ YAMASHIRO, H. 1992. Skeleton dissolution in BINSKY, P. COOK, and L. MCCLOSKEY. scleractinian corals. Page 110 in Proc. 7th 1989. The effect of external nutrient re­ Int. Coral Reef Symp., Guam (abstract). sources on the population dynamics of YONGE, C. M. 1930. Studies on the physiol­ zooxanthellae in a reef-building coral. ogy of corals. 1. Feeding mechanisms and Proc. R. Soc. Lond. B BioI. Sci. 236: 311­ food. Great Barrier Reef Expedition 1928­ 324. 29 Sci. Rep. 1(2): 13-57.

§i8.