Symbiotic Sea Anemone Research Articles

Calorimetric Studies of Behavior, Metabolism and Energetics of Sessile Intertidal Animals

Synopsis. Behaviors to conserve water during intertidal exposure at the same time impair respiratory gas exchange, so that observed responses to emersion may reflect compromises between these incompatible needs. Behavioral isolation of the tissues from air results in the complete or partial reliance on anoxic energy metabolism, which is most reliably measured directly as heat dissipation. Combined direct calorimetry and indirect calorimetry (respirometry) enable the partitioning of total metabolic heat dissipation into its aerobic and anoxic components, which may vary according to physical and biological factors. The mussel Mytilus edulis is tolerant of anoxia and saves water and energy during aerial exposure in its rocky intertidal habitat by closing its shell valves and becoming largely anoxic. Like most suspension feeders in this habitat, its compensation for reduced feeding time involves energy conservation; there is little evidence for energy supplementation such as increases in feeding rate or absorption efficiency. Ammonia production continues during aerial exposure and is involved in acid-base balance in the hemolymph and mantle cavity fluid. Infaunal cockles (Cardium edule) and mussels (Geukensia demissa) gape their shell valves, remain largely aerobic and have high rates of heat dissipation during intertidal exposure, a response which appears related to the lower desiccation potential and exploitation of richer trophic resources in their soft-sediment habitats. The variable expansion of the symbiotic sea anemone Anthopleura elegantissima reflects inter? action among the responses to desiccation, irradiance and continued photosynthesis by its zooxanthellae during exposure to air. One could safely predict that all phys? iological processes correspondingly might be shown to be influenced by the tide, could we but read delicately enough

Seasonal variation in light-shade adaptation of natural populations of the symbiotic sea anemone Aiptasiapulchella (Carlgren, 1943) in Hawaii

The productivity and biomass parameters of the symbiotic anemone Aiptasia pulchella (Carlgren, 1943) from a shaded mangrove lagoon (maximum summer irradiance of 100 μE m −2 · s −1) and a sunlit reef flat (maximum summer irradiance of 1400 μE · m −2 · s −1) were examined in Hawaii. Light-shade adaptation was evident in the summer populations (1981) but not observed during the fall (1982). In the summer, zooxanthellae from the lagoon A. pulchella (shade anemones) contained 2.97 pg Chl a cell −1 and those from the reef flat (sun anemones) contained 1.70 pg Chl a · cell −1; but Chl a : c 2 ratios were 2.5 in zooxanthellae from both shade and sun anemones. During the fall, there were no significant differences in Chl a and c 2 of zooxanthellae (2.25 pg Chl a · cell −1) in shade and sun anemones, but Chl a : c 2 ratios averaged 3.9. During both seasons, shade anemones were larger and contained higher densities of zooxanthellae than sun anemones. In addition to differences between shade and sun habitats, there was localized photoadaptation of zooxanthellae within individual anemones due to microhabitat variations in ambient irradiance. Growth rates of zooxanthellae in A. pulchella differed in shade and sun anemones. Specific growth rates for zooxanthellae in situ were the same for shade populations in both summer and fall (0.016 day −1). However, zooxanthellae in sun anemones grew four times faster in the fall (0.033 day −1) than during the summer (0.008 day −1). These results suggest that growth of zooxanthellae in these anemones was independent of ambient irradiance. Photosynthesis-irradiance ( P- I) responses of shade and sun anemones during the summer showed that shade anemones had greater photosynthetic efficiencies (α) but lower photosynthetic capacities ( P max) than sun anemones. Dark-respiration rates of sun anemones were twice those obtained with shade anemones. In the fall, these populations of anemones did not exhibit P- I responses characteristic of light-shade adaptation. Both α and P max of shade and sun anemones were higher in the fall, indicating that zooxanthellae in A. pulchella adapted to seasonal reduction in irradiance.

Glycerol translocation in Condylactis gigantea

Sodium cyanide (NaCN) was used to partially uncouple respiration and photosynthesis in the symbiotic sea anemone Condylactis gigantea. NaCN significantly increased the ratio of gross photosynthesis to respiration in both intact tentacles and isolated zooxanthellae (Symbiodinium microadriaticum), increased carbon translocation from 17.7±3.5% of total fixed in controls to 43.5±5.8%, and doubled the amount of photosynthetically fixed carbon accumulating in the coelenterate host over that in controls. Only 2% of the non-particulate radioactivity recovered in the host tissue was 14C-glycerol when uninhibited symbiotic tentacles were incubated in 14C-bicarbonate for 1 h. At 10-5M NaCN, approximately 25% of the host nonparticulate radioactivity was recovered as 14C-glycerol, the absolute concentration of glycerol in the host tissue was three times higher than in controls, and 14C-glycerol was found in the medium. While glycerol has been proposed to play a major role in the translocation of photosynthetically fixed carbon from zooxanthellae to their coelenterate hosts, its concentration has never been measured in the animal and algal components of the symbiosis. The isolated zooxanthellae contained 3.62±0.33 mM glycerol, 26x the 0.141±0.02 mM found in the anemone. Aposymbiotic anemone tissue contained 0.169±0.06 mM glycerol. The rate of glycerol mineralization was not saturated even when exogenous glycerol levels were 70x internal concentrations. These data show that respiration and photosynthesis in symbiotic associations may be partially uncoupled by NaCN, and that this uncoupling allows the verification of the translocation and rapid catabolism of glycerol within the host.

Impact of symbiotic algae on sea anemone metabolism: analysis by in vivo 31P nuclear magnetic resonance spectroscopy.

High-field pulsed Fourier-transform nuclear magnetic resonance spectroscopy (NMR) was used to quantify the adenylate levels of sea anemones (Aiptasia pulchella) with and without symbiotic dinoflagellates (Symbiodinium sp.). Animals were fed to repletion, then starved in darkness for up to six days before collection of in vivo NMR spectra. The host adenylate ratio of ATP: (ATP + ADP) declined significantly with increasing periods of starvation in both symbiotic and aposymbiotic hosts (P less than 0.05). However, the decline in the animal adenylate ratio was significantly more rapid in animals bearing symbiotic algae (P less than 0.05). This suggests that symbiotic algae in darkness cause more rapid depletion of host energy reserves, possibly by drawing on host pools of organic substrates. In vivo NMR spectroscopy was also used to evaluate the effect on A. pulchella of photosynthesis by zooxanthellae. Symbiotic anemones were fed to repletion, then starved under high irradiance (300 to 320 mu Ein m-2 s-1) or low irradiance (70 to 80 mu Ein m-2 s-1) conditions for up to five days. The host adenylate ratio declined significantly (P less than 0.01) with starvation under both treatments, but no significant difference was detected between treatments (P greater than 0.35). Blotted wet weight of anemones under high and low irradiance declined by 50% over eight days of starvation, but there was no significant difference in the rate of weight loss by anemones in the two treatments. There results suggest that translocation of photosynthate from symbiotic zooxanthellae does not significantly affect host adenylate ratio or have a sparing effect on host biomass during starvation in this symbiotic sea anemone.

Why do anemonefishes inhabit only some host actinians?

The 25 species ofAmphiprion and one ofPremnas (family Pomacentridae) are obligate symbionts of 10 species of facultatively symbiotic sea anemones. Throughout the tropical Indo-West Pacific range of the relationship, a fish species inhabits only certain of the hosts potentially available to it. This specificity is due to the fishes. Five fishes occupy six sea anemone species at Lizard Island, Great Barrier Reef, Australia.Entacmaea quadricolor harborsP. biaculeatus, A. melanopus andA. akindynos. Adults ofPremnas occur deeper than about 3 m in large, primarily solitary actinians; juveniles may occupy peripheral members ofEntacmaea clones in shallow water. Specimens ofA. melanopus live exclusively in clonal anemones, which are found no deeper than 3 m. Most individuals ofA. akindynos inEntacmaea are juveniles, occurring shallow and deep, in solitary anemones or at the margins of clones. Interspecific as well as intraspecific social control of growth may be responsible for keeping fish small at clone fringes. Conspicuous specimens ofE. quadricolor depend upon their anemonefish to survive. Actinians cleared of symbionts disappeared within 24 h, probably having been eaten by reef fishes.Entacmaea, the most abundant and widespread host actinian at Lizard Island and throughout the range of the association, is also arguably the most attractive to anemonefishes. I believe its vulnerability to predation was a factor in its evolving whatever makes it desirable to fishes. Experimental transfers pitted fish of one species against those of another, controlling for ecophenotype of host, and sex, size and number of fish. Competitive superiority was in the same order as abundance and over-all host specificity:P. biaculeatus, A. melanopus, A. akindynos. At least three factors are necessary to explain patterns of species specificity - innate or learned host preference, competition, and stochastic processes.

Effect of feeding regime and irradiance on the photophysiology of the symbiotic sea anemone Aiptasia pulchella

To determine how the animal and algal components of the symbiotic sea anemone Aiptasia pulchella respond to changes in food availability and culture irradiance, sea anemones from a single clone were maintained at four irradiance levels (320, 185, 115, and 45 μE m-2 s-1) and either starved or fed for 5 wk. Changes in protein biomass of sea anemones maintained under these conditions were not related to the productivity of zooxanthellae, since the protein biomass of fed A. pulchella decreased with increase in irradiance and there was no difference in protein biomass among starved sea anemones at the four irradiance levels. Except for the starved high-light sea anemones, the density of symbiotic zooxanthellae was independent of culture irradiance within both starved and fed. A. pulchella. Starved sea anemones contained over twice the density of zooxanthellae as fed sea anemones. Within both starved and fed individuals, chlorophyll per zooxanthella increased with decreasing culture irradiance while algal size remained constant (in fed sea anemones) at about 8.80 μm diameter. Chlorophyll a: c2 ratios of zooxanthellae increased with decreasing culture irradiance in zooxanthellae from starved sea anemones but remained constant in zooxanthellae from fed sea anemones. As estimated from mitotic index data, the in situ growth rates of zooxanthellae averaged 0.007 d-1 and did not vary with irradiance or feeding regime. Photosynthesis-irradiance (P-I) responses of fed A. pulchella indicated an increase in photosynthetic efficiency with decreasing culture irradiance. But there was no consistent pattern in photosynthetic capacity with culture irradiance. Respiration rates of fed sea anemones also did not vary in relation to culture irradiance. The parameter I k , defined as the irradiance at which light-saturated rates of photosynthesis are first attained, was the only parameter from the P-I curves which increased linearly with increasing culture irradiance. The daily ratio of net photosynthesis to respiration for A. pulchella ranged from 1.6 to 2.8 for sea anemones maintained at the three higher irradiances, but was negative for those maintained at 45 μE m-2 s-1. Since the final protein biomass was greatest for sea anemones maintained at the lowest irradiance, these results indicate that sea anemone growth cannot be directly related to productivity of zooxanthellae in this symbiotic association.

The energetics of asexual reproduction: Pedal laceration in the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943)

Asexual reproduction of the symbiotic sea anemone Aiptasia pulchella (Carlgren, 1943) was studied in the context of energy budgets determined under a variety of light and feeding conditions. Continuous darkness significantly increased rates of pedal laceration (the method of asexual reproduction), while different feeding rates had no significant effect. Digestive assimilation efficiency averaged 63% for whole brine shrimp, and conversion efficiencies (assimilated energy into biomass) averaged 31%. There were no significant differences between the conversion efficiencies of energy obtained from light or food. The index of reproductive effort (RE) for pedal laceration was very low, ranging from 0.004 to 0.044. This low RE associated with a substantial rate of asexual reproduction may, in part, explain the widespread success of certain sea anemones.

DISPERSAL OF ZOOXANTHELLAE ON CORAL REEFS BY PREDATORS ON CNIDARIANS

Fish and nudibranchs prey on cnidarians that contain high densities of symbiotic dinoflagellates (zooxanthellae). Several fish (Arothron meleagris, Chaetodon auriga, and Chaetodon unimaculatus) and one nudibranch (Berghia major) feed on the Hawaiian symbiotic sea anemone Aiptasia pulchella. Fecal material of these predators consisted primarily of zooxanthellae, which were shown to be photosynthetically active and capable of re-establishing symbioses with aposymbiotic A. pulchella.

Uptake and assimilation of dissolved inorganic nitrogen by a symbiotic sea anemone

The tropical sea anemone,Aiptasia pulchella, harbours symbiotic dinoflagellates (zooxanthellae). Animals in their natural habitat in Hawaii and those maintained in the laboratory in Los Angeles took up ammonium from nutrient enriched seawater. That the uptake experiment was done in the dark did not influence uptake although prolonged (19 h) dark treatment caused the animals to release ammonium. Aposymbiotic anemones (lacking zooxanthellae) typically excreted ammonium in the light. Freshly isolated zooxanthellae were also able to deplete enriched seawater of ammonium, indicating that the capacity for uptake by the symbiosis is due to the zooxanthellae. Uptake rates of freshly isolated zooxanthellae exceeded those of zooxanthellae in symbiosis. There was evidence that uptake of ammonium follows diffusion kinetics rather than the Michaelis-Menten model, since there was no saturation component. Neither symbioticA.pulchellanor their isolated algae were able to remove nitrate from enriched seawater, even when pretreated for 24 h or one month with 5 or 10 µm nitrate. Symbiotic anemones that were not fed zooplankton for a month, to reduce the internal pools of excretory ammonium, showed a slight ability to deplete the medium of nitrate. Enzymes involved in assimilation of dissolved inorganic nitrogen were assayed in cell-free zooxanthellae extracts. Neither nitrate reductase nor glutamate synthase activity was found. There was glutamate dehydrogenase activity, with aKmfor ammonium of 4—5 mm;Kmfor α-ketoglutarate of 5-7 mm. The zooxanthellae also showed glutamine synthetase activity with aKmfor glutamate of 12.5 µM but exhibiting negative cooperativity with ammonium.

Gastropod shells: A dynamic resource that helps shape benthic community structure

Empty gastropod shells are an important resource for many animals in shallow benthic marine communities. Shells provide shelter for hermit crabs, octopuses, and fishes, provide attachment substratum for hermit crab symbionts, and directly or indirectly modify hermit crab predation. Creation of an empty shell due to predation of one gastropod on another and acquisition of that shell by a hermit crab are two key events in the subsequent use of that shell. Shells of different gastropod species and the species of hermit crab acquiring them affect the symbiont complement that attaches to the shell, which in turn may affect future shell use by other symbionts. Certain shell types worn by the hermit crab, Pagurus pollicaris Say, are positively associated with the symbiotic sea anemone, Calliactis tricolor (Lesueur), which protects the hermit crab from predation by the crab, Calappa flammea (Herbst), and possibly from the octopus, Octopus joubini Robson. Shells of other species of gastropods are resistant to being crushed by the spiny lobster, Panulirus argus (Latreille). The inter-and intraspecific interactions centered on the gastropod shell are termed a “habitat web.” The potential of the shell to limit the size and distribution of animal populations demonstrates how this resource helps shape community structure.

Lipid droplets, medium of energy exchange in the symbiotic anemone Condylactis gigantea: a model coral polyp

The symbiotic sea anemone Condylactis gigantea does not make a CaCO3 skeleton, yet its lipid metabolism appears to be very similar to that of reef-building corals. Like hermatypic corals, it is roughly 1/3 lipid on a dry weight basis, its lipid is composed primarily of saturated wax ester and triglyceride, and in the light, its symbiotic algae (zooxanthellae) are the major sites of lipid synthesis in the intact association. Lipid droplets isolated from host tentacle tissue, where the majority of zooxanthellae also occur, contained primarily wax ester and triglyceride in an apparently supercooled liquid state. The diameter of the extra-algal droplets, 3.4±0.7 μm, was similar to that of droplets observed to protrude from isolated zooxanthellae. When anemones were allowed to assimilate acetate-1-14C in the light, only the zooxanthellae and tentacle lipid droplets incorporated significant radioactivity. In the corresponding dark incubations the lipid droplets showed the highest specific activity (5.0 pmol acetate-1-14C/mg lipid). With photic exposure, extra-algal droplet specific activity increased 60% and the zooxanthellae specific activity increased from a dark value of 1.0 to 20.0 pmol acetate-1-14C/mg lipid in the light. A scheme is presented to suggest how carbon may be fixed into lipids by the algae. In C. gigantea, 97% of the total lipid is stored in the polyp column, which is connected to the tentacles by the gastrovascular cavity. In the tentacle tissue, lipid droplets were often found to be inside vesicles; however, upon tentacle contraction free droplets accumulated in the tentacle lumen. Thus, lipid synthesized in the tentacle may be transported to coelenterate tissues via the circulating internal fluid in the form of lipid droplets.

Photosynthesis, respiration, and contribution to community productivity of the symbiotic sea anemone Anthopleura elegantissimA (Brandt, 1835)

The photosynthetic and respiratory physiology of the sea anemone Anthopleura elegantissima (Brandt, 1835), living in association with the endosymbiotic dinoflagellate Symbiodinium (= Gymnodinium) microadriaticum Freudenthal, was investigated in anemones that were fed and starved for 2 wk under laboratory conditions or newly collected from the intertidal zone. The photosynthetic performances of this association were similar to those of marine phytoplankton and intertidal seaweeds. Light saturation for Anthopleura elegantissima occurred between 125–350μE · m −2 · s −1 and inhibition was not observed at intensities up to 1550 μE · m −2 · s −1. Weight-specific gross photosynthetic rates decreased with increasing anemone size and were similar for fed, starved, and newly collected anemones. Gross photosynthetic rates were positively correlated with chlorophyll a content and number of zooxanthellae. Weight-specific respiration rates also decreased with increasing anemone size. Fed anemones respired at rates about twice those of starved anemones and A. elegantissima measured within 10 h of collection had respiration rates similar to starved anemones. Gross photosynthesis to respiration (P : R) ratios were a function of the nutritional state of the anemones, typically ranging from 2.0 to 3.0 for starved anemones, but seldom over 1.0 for fed anemones. Estimates of the relative contribution of carbon from the zooxanthellae to the host (animal) respiratory carbon depended on host nutritional state, averaging ≈ 13% for fed anemones and 45% for starved or newly collected anemones. Photosynthetic rates were similar to temperate intertidal seaweeds having low surface to volume ratios. Calculations of the contributions of anemones to intertidal gross primary production (48–151 gC · m −2 · yr −1) fall within the range of temperate intertidal seaweed populations.

Amphiprion clarkii juvenile: Innate protection against and chemical attraction by symbiotic sea anemones.

Amphiprion clarkii juvenile: Innate protection against and chemical attraction by symbiotic sea anemones.

The nature of the adhesion of tentacles to shells during shell-climbing in the sea anemone Calliactis parasitica (Couch)

Phase contrast microscopy and scanning electron microscopy show that during the response of the symbiotic sea anemone Calliactis parasitica (Couch) to shells of Buccinum undatum (L.) three times as many spirocysts as nematocysts are discharged. Observations indicate that spirocysts are responsible for the adhesion of tentacles to shells. Discharge levels are not significantly influenced by the nature of the substratum to which the anemones are attached. The reported observation that fewer tentacles adhere to shells when anemones are settled on shells than when they are fixed on a different substratum is re-interpreted in terms of a new model for the control of spirocyst discharge.

The nature of the adhesion to shells of the symbiotic sea anemone calliactis tricolor (Leseur)

The mechanism of tentacular adhesion to gastropod shells has been demonstrated for a symbiotic sea anemone, Calliactis tricolor (Leseur) by means of scanning electron microscopy. Both basitrichous isorhiza nematocysts and spirocysts are involved with the former being much more abundant on the shells. Contrary to its classical characterization, the thread of the basitrichous isorhiza nematocyst possesses, in addition to the large spines at its base, minute spines along its length. C. tricolor whose pedal discs were attached to gastropod shells showed no difference in the number of nematocysts discharged than did those anemones whose pedal discs were attached to glass.