Resource Partitioning by Reef Corals As Determined from Stable Isotope Composition II

Resource Partitioning by Reef Corals as Determined from Stable Isotope Composition II. ~l5N of Zooxanthellae and Animal Tissue versus Depth l

L. MUSCATINE2 AND I. R. KAPLAN3

ABSTRACT: The pattern of resource partitioning versus depth for corals col lected in February, 1983, from Jamaica was investigated by analyzing their stable nitrogen isotope composition. Observations were made on isolated zoo xanthellae and corresponding algae-free animal tissue from nine species of sym biotic corals at four depths over a 50-m bathymetric range, and from a nonsym biotic coral at 1 m. /5 15N values versus depth ranged from +3.54 to -2.15 %0 for zooxanthellae and from +4.71 to +0.23 %0 for animal tissue. In those species that occurred over a 30- to 50-m depth range, both animal tissue and zooxanthellae tended to be depleted in 15N as depth increased to 30 m. In a few species animal tissue was enriched in 15N from 30 to 50 m. Depletion of 15N in zooxanthellae with increasing depth may be the result of depth-dependent dif ferences in their nitrogen-specific growth rates. Animal tissue was consistently more depleted in 15N than for the nonsymbiotic coral Tubastrea coccinea (Ellis) at the same depth, but it was still slightly more enriched in 15N than corre sponding zooxanthellae in 16 of 25 paired samples. The latter trend was not 13 15 correlated with depth. A comparison of /5 C and /5 N for zooxanthellae and animal tissue over 50 m revealed a tendency toward depletion ofheavy isotopes as depth increases. Increased carbon fixation appears to be accompanied by decreased nitrogen fractionation.

RESOURCE UTILIZATION by scleractinian reef Wafar et al. 1985, Summons et al. 1986, An corals is profoundly affected by endosymbio derson and Burris 1987, Rahav et al. 1989) tic dinoflagellates (zooxanthellae). Although from the environment and from host catabo coral polyps feed on particulate organic car lism. Organic carbon and nitrogen is translo bon and nitrogen (Lewis and Price 1975, cated from algae to host (Muscatine 1980b, Lewis 1976, 1977, Clayton and Lasker 1982), Falkowski et al. 1984) and possibly from host their phototrophic endosymbionts take up to algae (e.g., see Cook 1983, Steen 1986). and assimilate inorganic carbon (Muscatine The symbiotic algae also enable the retention and Cernichiari 1969, Schmitz and Kremer and recycling of carbon and nitrogen atoms 1977, Crossland et al. 1980, Black and Burris within the coral. These features confer an ap 1983) and nitrogen (Franzisket 1974, Cross parent selective advantage on coral animals land and Barnes 1977, D'Elia and Webb in oligotrophic environments. There is little 1977, Muscatine and D'Elia 1978, Webb and information, however, on how depth and Wiebe 1978, Muscatine et al. 1979, Musca light attenuation might influence these poten tine 1980a, Burris 1983, D'Elia et al. 1983, tial fluxes and consequently the selective ad vantage of the symbiosis to the partners.

I Research was supported by grants from the Na In previous studies, Davies (1984), Mc tional Science Foundation (OCE-85105l8) to L.M. and Closkey and Muscatine (1984), and Musca the Department of Energy (EY-763-03-0034) to I.R.K. tine et al. (1984) noted that photosynthetic Manuscript accepted 15 August 1993. rates by zooxanthellae in shallow-water cor 2 Department of Biology, University of California, Los Angeles, California 90024. als are high and that carbon translocated 3 Institute ofGeophysics and Planetary Physics, Uni from algae could meet the daily carbon versity of California, Los Angeles, California 90024. demand of the animal for respiration and 304

'-=Mtlltli.WMqi§l¥.li#.¥##%itI:t#jl!T#itlf#§t:ii#i¥f.Wt.i#M## iAii ¢¥.iij Ut4/i ¥MIMf¥NMI d& Resource Partioning by Reef Corals-MusCATINE AND KAPLAN 305 growth. In contrast, in deep-water corals, fractionation during assimilation (Wada and photosynthetic rates are low and much less Hattori 1978, Minegawa and Wada 1980, photosynthetically fixed and translocated Wada 1980, Macko et al. 1986, 1987). D15N carbon is available for animal respiration and values are also useful as indicators of trophic growth. McCloskey and Muscatine (1984) level (Van Dover and Fry 1989). predicted that in deep water, reduced input of The data presented here show that both photosynthetically fixed and translocated the zooxanthellae and the animal tissues in carbon may be supplemented by input ofcar Jamaican scleractinian corals tend to be de bon from allochthonous sources. Muscatine pleted in 15N, particularly as depth increases. et al. (1989) attempted to evaluate this pre Depth-dependent variables that may contrib diction by analyzing the stable carbon iso ute to 15N depletion are discussed. topes of coral animal tissue and zooxan thellae as a function of depth. Their data revealed that D13C of zooxanthellae was rel MATERIALS AND METHODS atively high in shallow water. These high values were interpreted as the result of Methods for sampling corals, separation diffusion-depletion of internal CO2 at high of zooxanthellae and animal tissue, and ana rates ofphotosynthesis and consequent mini lytical techniques were described by Musca mal stable isotope discrimination (see also tine et al. (1989). Briefly, 10 species of corals Goreau 1977). Zooxanthellae D13C became (nine symbiotic, one nonsymbiotic) were col lower as depth increased and as light for pho lected from 1 and 10m depth from the back tosynthesis diminished. Animal tissue D13C reef and from 10, 30, and 50 m depth from was slightly lower than zooxanthellae D13C in the fore-reef at Discovery Bay, Jamaica, in shallow water, probably as a result of trans February 1983. Tissue was removed from location of photosynthetically fixed carbon whole colonies or from large pieces of mas from zooxanthellae to animal. As depth in sive corals to minimize sample heterogeneity creased, the animal tissue exhibited a dis within colonies. Algae and animal tissues proportionately lower D13C, suggesting that were separated by a series of careful centrifu more particulate organic carbon (POC) is gations and washings. Algae were recovered taken up in deep water or that at the lower as pellets, and animal tissue was deposited on rates of photosynthesis CO2 was no longer precombusted glass fiber filters (Reeve An limiting. gel). Both fractions were dried at 50°C. Sam To gain further insight into resource utili ples were combusted as described by Mine zation by reef corals, we examined the D15N gawa et al. (1984). Mass spectrometry was of zooxanthellae and animal tissue versus performed on a Varian MAT 250 instrument. depth in the same coral samples as those ana The 15N/14N of the samples is reported as lyzed by Muscatine et al. (1989). D15N values D15N, in units per mil (%0), where: for marine organisms generally range from 15 about - 3 %0 to about + 20 0/00 (Owens 1987), D N (0/00) = [(Rsample/Rstandard) - 1] x 1000 but some organisms from hydrothermal and vents or hydrocarbon seeps, or possessing en R = 15N/14N dosymbiotic bacteria, exhibit values as low as - 12.9 0/00 (Rau 1981, Paull et al. 1985, Atmospheric nitrogen was the standard. The Brooks et al. 1987, Conway et al. 1989). D15N analytical precision of these measurements values reflect the nature of the source nitro was 0.2 %0. gen, which may undergo only minimal frac tionation when it is limiting (Wada and Hat tori 1976, Owens 1987) or when atmospheric RESULTS nitrogen is fixed by marine cyanobacteria (see references in Macko et al. 1984). Alterna The values of D15N for each species versus tively, source nitrogen may undergo maximal depth ranged from +3.54 to -2.15 %0 for 306 PACIFIC SCIENCE, Volume 48, July 1994

TABLE I "ISN FOR ALGAE AND ANIMAL TISSUE FROM JAMAICAN CORALS OVER A 50-m BATHYMETRIC RANGE

DEPTH

CORALS 1m 10m 30m 50m

Symbiotic corals Madracis mirabilis (Duchassaing & Michelotti) Algae +3.54 +3.26 +2.64 • Animal +3.90 +3.05 + 1.84 • Acropora cervicornis (Lamarck) Algae + 1.76 + 1.68 +0.16 • Animal +4.11 + 1.86 + 1.56 • Agaricia agaricities (Linnaeus) Algae + 1.64 + 1.85 +1.86 +0.30 Animal +3.02 •• + 1.48 + 1.54 Acropora pa/mata (Lamarck) Algae + 1.76 +1048 • • Animal •• +2.13 • • Porites astreoides Lamarck Algae +2.99 +2.30 +1.74 • Animal +2.79 +2.10 +2.04 • Montastrea annu/aris (Ellis & Solander) Algae +3.00 + 1.83 +2.21 -0.16 Animal +3.32 +2.41 +0.23 + 1.87 Montastrea cavernosa (Linnaeus) Algae +0.95 +0.35 -2.15 -1.73 Animal +2.96 + 1.11 +1.16 +3.43 Eusmiliafastigiata (Pallas) Algae +3.45 +2.18 +0.94 • Animal +3.45 +2.52 +2.76 • Dendrogyra cy/indrus Ehrenberg Algae • +2.43 •• Animal • +2.23 •• Nonsymbiotic coral Tubastrea coccinea (Ellis) +4.74 •• •

., not found at depth; ••, samples lost. algae and from + 4.11 to + 0.23 0/00 for ani The b15N value for Tubastrea coccinea mal tissue (Table I). In those species that oc (Ellis) is +4.740/00 and is taken as representa curred over a 30- to 50-m depth range, both tive of coral animal tissue at I m that has zooxanthellae and animal tissue tended to be acquired particulate and/or dissolved organic depleted in 15N as depth increased, although nitrogen in the absence of a photosynthetic in Montastrea annularis (Ellis & Solander) endosymbiont. and M. cavernosa (Linnaeus) at 50 m, animal tissue was again enriched in 15N. There were differences between b15Nanimal DISCUSSION and b15Naigae in each species. Animal tissue was more enriched in 15N than algae in 16 of b15N ofZooxanthellae the 25 paired samples (mean ± SD = 1.51 ± 1.3 0/00; range, 0.30-5.16 0/00). In the remaining b15N values for zooxanthellae in Jamaican nine, the b15N animal values were equal to corals range from -2.15 to +3.540/00. The or lower than those of corresponding algae data cluster at the low end of the range of (mean ± SD = 0.46 ± 0.61 0/00; range, 0.18 values representative of marine organisms. 1.98 0/00). Interpretation of the absolute values of t5 15N

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for the algae and animal must await data corals and other symbiotic cnidarians may on the <5 15N values of the source nitrogen, be nitrogen-limited (Cook and D'Elia 1987, which, at present, are unknown. The most Cook et al. 1988, Dubinsky et al. 1989, important sources of dissolved inorganic ni H0egh-Guldberg and Smith 1989, Muscatine trogen (DIN) for symbiotic dinoflagellates et al. 1989). N-limited cells in shallow water seem to be nitrate and ammonium from sea might assimilate most of the available DIN water and ammonium from coral animal ca and consequently might exhibit minimal sta tabolism (D'Elia 1988, Rahav et al. 1989). ble isotope fractionation (Wada and Hattori Other potential sources include nitrate and 1976). In contrast, zooxanthellae in light-lim ammonium from local sources such as ited deep-water corals may grow more slowly groundwater (D'Elia et al. 1981), nitrification and consequently exhibit greater isotope dis associated with bacteria in sponges (Corre crimination. Wilkerson et al. (1988) esti dor et al. 1988) and coral skeletons (Szmant mated generation times for zooxanthellae Froelich and Pilson 1977, Wafar et al. 1985), from the same set of corals as analyzed in coral head porewater (Risk and Muller this study. When our <5 15N data are plotted 1983), and migrating fishes (see, for example, against their growth rate data (as generation Meyer and Schultz 1985a,b). times) for zooxanthellae from all species at An interpretation of the trend in depletion all depths, no significant correlation emerges ofzooxanthellae 15N with depth is suggested (<5 15N = 1.38 + 0.02 (generation time) (n = by observations of Wada and Hattori (1978; 26; r = 0.01). This appears to argue against see also Minegawa and Wada 1980) on cul a "growth rate fractionation" hypothesis. tured marine diatoms. They demonstrated However, generation time is derived from that isotope fractionation of nitrate and am zooxanthellae mitotic index and is a function monium was negligible during uptake, but ofthe standing stock ofcells. It does not take substantial during assimilation, and that into account the translocated nitrogen that fractionation was inversely proportional to does not appear in the standing stock of growth rate. The highest fractionation oc cell nitrogen. Consequently, the parameter of curred when growth was light-limited and N interest is the nitrogen-specific growth rate sufficient. Because the specific growth rate of (UN), manifested by the uptake and assimila zooxanthellae in at least one coral species tion of DIN by zooxanthellae and the trans tends to be higher in high-light habitats than location ofdissolved organic nitrogen (DON) in shade (Muscatine et al. 1989), the depth to the host. That is, in symbiotic algae, and profile for zooxanthellae <5 15N could be perhaps even in some free-living algae (see interpreted on the basis of relative specific Zehr et al. 1988), nutrient uptake and assimi growth rates of light-sufficient, nutrient lation is uncoupled from cell growth at the limited zooxanthellae in shallow water and low specific growth rates exhibited by zoo light-limited, nutrient-sufficient zooxanthel xanthellae in hospice. For example, from data lae in deep water. A few observations support on uptake rates of 15N (as ammonium) by this scenario. the shallow-water Red Sea coral Stylophora Zooxanthellae in corals are very effective pistil/ata Esper, Muscatine et al. (1984) esti scavengers ofnitrogen, often taking up ambi mated that UN was 0.31 day-l for light ent DIN at or below concentrations of 1 JLM adapted cells and 0.25 day-l for shade and effectively retaining host catabolic am adapted cells, a 20% decrease. This trend is monium so that, under normal conditions, consistent with our conjecture that UN for little host catabolic ammonium is released coral zooxailthellae may decrease with de to the environment (Muscatine and D'Elia creasing irradiance at greater depths, so that 1978, Cook and D'Elia 1987, Cook et al. rates of uptake, assimilation, and transloca 1988, Rahav et al. 1989, Stambleret al. 1991). tion are lower and the scope for fractionation However, there is a growing body ofevidence is higher. that suggests that growth rate or biomass Alternatively, the lower <5 15N values increase of zooxanthellae in shallow-water ( < 1.00 0/00), especially as depth increases, are 308 PACIFIC SCIENCE, Volume 48, July 1994 close to the generally accepted value of 0.00 that may be acquired by the host (Markell %0 for dissolved nitrogen in seawater (Owens and Trench 1993). Animal tissue could also 1987) and so could be derived from acquisi be enriched in 15N relative to zooxanthellae tion of DIN from fixed nitrogen sources. The as a result of protein catabolism and excre lower values could also result from assimila tion of isotopically light ammonium. More tion of local sources of 15N-depleted ammo than 90% of the ammonium excreted by nium, such as host catabolism, zooplankton Stylophora pistil/ata is taken up by resident excretion (Checkley and Entzeroth 1985), or zooxanthellae (Rahav et al. 1989). Retention from greater discrimination by the algae of of such host excretory ammonium by zoo locally elevated concentrations of ammo xanthellae may be a general phenomenon nium and nitrate. among corals (Muscatine and D'Elia 1978) and would exacerbate the tendency of zoo xanthellae to be depleted in 15N relative to b15N ofAnimal Tissue animal tissue. b15N of animal tissue ranged from +4.71 to + 0.23 %0. Corals living at I m depth had Comparison with Other Endosymbioses consistently lower animal tissue b15N values (mean ± SD = 3.36 ± 0.49 0/00; range, 2.79 Relatively low (i.e., negative) b15N values 4.11 %0) than the nonsymbiotic coral Tu have been reported for some, though not all, bastrea coccinea (+4.74 0/00), living at the endosymbioses involving bacteria in worms same depth. The reasons for these differences and clams from communities associated with are still obscure, but are undoubtedly related hydrothermal vents and deep seeps (Rau to the fact that the diet of T. coccinea is solely 1981, Paull et al. 1985, Brooks et al. 1987, allochthonous particulate and DON enriched Van Dover and Fry 1989, Rau et al. 1990a). in 15N (e.g., zooplankton), whereas the diet The low b15N values are attributed to either of the symbiotic corals also includes sub assimilation of isotopically depleted nitrogen strates acquired from the zooxanthellae. Al sources, fractionation, or nitrogen fixation lochthonous substrates may also account for (Rau 1985). Bacteria and host tissues in the increase in animal tissue b15N in M. annu protobranch bivalves (Solemya reidi) from laris and M. cavernosa at 50 m depth. This shallow-water reducing sediments have simi interpretation is consistent with the previous lar b15N values. The similarity is attributed interpretation that b13C of animal tissue to assimilation by bacteria of a nonlimiting versus depth is influenced by allochthonous DIN source, such as porewater ammonium, POC (Muscatine et al. 1989). and translocation of DON to the host (Con Although the b15N values for animal tis way et al. 1989). However, like endosymbi sue are low relative to those for T. coccinea, otic algae, although the cell-specific growth in the majority of coral species they are still rate of endosymbiotic chemoautotrophic slightly higher than those of their corre bacteria in S. reidi is relatively low (see Cava sponding zooxanthellae. The difference, al naugh 1985), the nitrogen-specific growth though not correlated with depth, is consis rate could be relatively high and as such tent with the general observation that, in could be a factor that influences b15N values. most cases, the b15N of marine invertebrates and vertebrates is greater than their dietary b13C and b15N versus Depth b15N by an average of 2.6 ± 2.1 %0 (Owens 1987). Coral animal cells could acquire 15N_ The analysis of multiple stable isotopes enriched substrates by translocation from has been used to provide insight into the diet zooxanthellae. Coral zooxanthellae release ofa variety of organisms and their trophody alanine in vitro (Muscatine and Cernichiari namics (see Owens 1987, Rau et al. 1990a,b, 1969) and may do so in situ (Lewis and 1991). Figure I provides a first glimpse of Smith 1971). In addition, some zooxanthellae variation in b13C and b15N versus depth for secrete nitrogen-containing macromolecules animal tissue and zooxanthellae in Jamaican

MA Resource Partioning by Reef Corals-MusCATINE AND KAPLAN 309

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