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Growth and Metabolic Responses of the Giant Clam- Zooxanthellae Symbiosis in a Reef-Fertilisation Experiment

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Growth and Metabolic Responses of the Giant Clam- Zooxanthellae Symbiosis in a Reef-Fertilisation Experiment MARINE ECOLOGY PROGRESS SERIES Vol. 170: 131-141, 1998 Published September 3 Mar Ecol Prog Ser Growth and metabolic responses of the giant clam- zooxanthellae symbiosis in a reef-fertilisation experiment 'Department of Biochemistry and Molecular Biology and 'Department of Zoology, James Cook University of North Queensland, Townsville, Queensland 4811, Australia ABSTRACT: To evaluate the impact of elevated nutrients on reef organisms symbiotic with zooxan- thellae, giant clams Tridacna maxima were exposed daily to increased ammonia and phosphate (N, P, N+P) in their natural reef environment for 3 to 6 mo. The results strongly corroborate the major responses of the syn~bioticassociation to nutrient enr~chlnentpreviously observed (wlth T gigas) under controlled outdoor conditions. Exposure of the clams to elevated N (10 pM) increased zooxanthellae density, reduced zooxanthellae size, down-regulated N uptake by zooxanthellae freshly isolated from their hosts, and reduced glutamate in the clam haernolymph, with increased pools of some free amino acids (methionine, tyrosine) In the zooxanthellae These results confirm that the zooxanthellae in giant clams are N limited jn situ and have free access to inorganic N from the sea water. There is also cor- roborating evidence that the zooxanthellae are P limited jn situ as well, possibly due to host interfer- ence While the N-Pratios of the animal host reflected ambient N and P concentrations in the sea water, those of the zooxanthellae d~dnot. Regardless of P exposure (2 FM P) of the clams, zooxanthellae N:P ratios were cons~stent'lyhigh (>30:1) and phosphate concentrations in the clam haemolymph bathing the zooxanthellae tube system consistently low (<0.1 PM). These field findings, consistent with previ- ous laboratory observations, confirm the Limiting roles of both N and P in the giant clam-zooxanthellae symbiosis. That significant changes occurred earlier and at lower nutrient loading compared to some reef organisms investigated within the same experimental framework further demonstrates organism- level responses of a potential bio-indicator of the early onset of eutrophication in reef waters. KEY WORDS: Giant clam . Zooxanthellae . Symb~os~sNutrient limitat~on. Bio-indicators . Eutrophi- cation INTRODUCTION tropical waters (Hawkins & Klumpp 1995). Adapted to such an impoverished environment, the giant clams' Like many marine invertebrates symbiotic with pho- growth and physiology can be strongly influenced by el- tosynthetic dinoflagellates (Symbiodinium sp.) called evated nutrient concentrations from natural or anthro- zooxanthellae, tndacnid clams are able to thrive in the pogenic events. For instance, it has previously been nutrient-poor tropical waters of the Indo-Pacific region. demonstrated that a major effect of chronically elevated The tridacnids' efficient utilisation of particulate organic nutrients (mainly N) on giant clams is enhancement of matter through filter-feeding (Klumpp et al. 1992), and soft-tissue production (Hastie et al. 1992, Belda et al. the algal symbionts' capability to recycle scarce nutrients 1993b, Fitt et al. 1993),with a simultaneous weakening are characteristics that are advantageous in oligotrophic of the shell structure (5 to 10 pM N, 2 to 10 pM P) (Belda P et al. 1993a).While the former effect is appealing to on- shore ventures in the commercial mariculture of these bi- 'Present address: Manne Science Institute. University of the Philippines, Diliman, Quezon City 1101, The Philippines valves, the effect on calcification has adverse implica- "Addressee for correspondence. tions for calcifying organisms in reef waters with E-mail: [email protected] elevated nutrient concentrations. 0 Inter-Research 1998 Resale of full article not permitted 132 Mar Ecol Prog Ser It is notable that such gross changes in clam tissue sponses in situ or confound the effects of nutrients. In production with N-enrichment are accompanied by the case of sewage outfall in Kaneohe Bay (Kinsey more subtle effects on a range of metabolic parameters 1988), there was a pronounced shift in community including: C:N:P ratios of the animal tissue; ammo- structure. The resulting enhancement of phytoplank- nia/ammonium concentration in the clarn haernolymph ton growth favoured the dominance of particle feeders, (Fitt et al. 1995); and densrty. chlorophyll a content, loss of available substratum, reduction in light penetra- and ammonium uptake rates of the zooxanthellae tion, and decline in benthic primary production. In an (Belda et al. 1993b). While these responses to elevated early experiment of Kinsey & Domm (1974), however, nutrients (along with a lack of change in other proper- where nitrogen (mainly urea) and phosphorus were ties) provide useful information on the metabolic rela- added daily to a patch reef over 8 mo, a striking 50% tionship between the clam and its algal symbionts, reduction in calcification of the reef system was evi- they are also indicative of the nutrient regimen In dent (Kinsey & Davies 1979), along with a 25% en- which the symbiotic partners are growing. As such, hancement in primary productivity due to increased these parameters may represent powerful environ- benthic algae. Clearly, experimental manipulations in mental tools for evaluating current and perhaps recent the field are necessary to better understand the impact nutrient exposure of reef organisms. Identification of of eutrophication on reef organisms. bio-indicators of the early onset of eutrophication on The Enrichment of Nutrients on a Coral Reef Experi- coral reefs should prove extremely useful. ment or ENCORE is the latest initiative and the first Studies elucidating the effects of inorganic nutrients fully replicated and controlled field experiment on the on coral reef organisms have been few until recently. long-term effect of elevated nutrients on reef commu- One of the first collaborative programs to address the nities. This large-scale manipulative reef-fertilisation issue of nutrient effects on reef-building corals was the experiment was carried out on Australia's Great Bar- 1991 US-Israel workshop at the Hawaii Institute of rier Reef (GBR) by the Great Barrier Reef Marine Park Marine Biology in Kaneohe Bay, Hawaii, USA (Jokiel Authority from 1993 to 1996 in response to a global et al. 1994). Exposure of 2 species of Hawaiian corals, concern about the effect of eutrophication on coral Pocillopora darnicornis and Montipora verrucosa, in reefs. This interdisciplinary undertaking, consisting of tanks containing elevated N (20 and 50 pM N as acclimation, nutrient enrichment, and recovery (NH,),SO,) significantly affected a broad spectrum of phases, was designed to: (1) provide quantitative evi- growth and metabolic parameters of the symbiotic dence on the relative impacts of elevated N and P on partners. N enrichment increased area1 concentrations various reef organisms, and the processes that regulate of zooxanthellae and chlorophyll, host protein and these responses; and (2) test the usefulness of parame- zooxanthellae N, but did not affect host C:N:P ratio ters proposed as sub-lethal indicators of eutrophication (Muller-Parker et al. 1994a, b); increased zooxanthel- (Larkum & Steven 1994). The present study on giant lae mitotic index and growth rate, and disrupted the clams was part of this initiative. cell division phase (Hoegh-Guldberg 1994);decreased In this paper, the results of an in sifu experiment on a glutamine synthetase (GS) activity of the host as well natural population of Tridacna maxima are presented. as the GS activity and ammonium uptake capacity of The major aim of this study was to test if clams (T max- freshly isolated zooxanthellae (Yellowlees et al. 1994); ima) periodically exposed to increased nutrients in and increased g1n:glu (g1utamine:glutamic acid) and their natural environment would behave in a manner pool sizes of most free amino acids in the zooxanthellae similar to clams (7.gigas) similarly investigated in an (McAuley 1994). essentially artificial environment (Belda et al. 1993a, b; It should be noted that the above studies were con- Belda & Yellowlees 1995). Indeed, the present field ducted under carefully controlled conditions in an arti- findings are, in most cases, consistent with previous ficial environment and in the absence of other major laboratory observations, and together constitute valu- organisms. They do not guarantee that parallel studies able information that 1s useful in reaching definitive in situ would yield similar results. Although such labo- conclusions regarding the impact of nutrlent enrich- ratory studies are quite useful and necessary in isolat- ment on reef organisms such as giant clams and their ing the effects of a complex range of environmental zooxanthellae. factors on reef organisms, they are necessarily limited by the handling sensitivity of the experimental organ- isms and the inadequate simulation of conditions in the MATERIALS AND METHODS field, which is usually an extremely complex and heterogeneous environment. The presence of other or- Experimental design and maintenance. Thls study ganisms competing for available nutrients, for in- constituted a part of ENCORE, a large-scale, manipu- stance, could conceivably decrease the clam's re- lative reef-fertilisation experiment undertaken on the Belda-Ba~ll~eel al.. In situ nutrient effects on reef clams 133 GBR to document the responses of coral reefs to nutri- shell, the mantle was excised from the rest of the soft ent enrichment. This multi-agency project
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