Dietrich Schlichter

FACTORS CONTROLLING HOLOCENE REEF GROWTH - AN INTERDISCIPLINARY APPROACH

SummaryThis interim report deals with investigations on key factors controlling reef growth by zoophysiologists, ecologists, paleontologists and geologists. The different levels of emphasis are the coral animal and the reef community. The main study area is the Red Sea which reaches over 20°C latitude up to the northernmost margin of the global coral reef belt. Supplementary results on microborer ecology are provided from the Bahamas.The desert enclosed Red Sea, not influenced by land runoff and only minimally by anthropogenic (urban and touristic) nutrient inputs, is predestined for a study on the principal influence of light on calcification within bathymetrical and latitudinal gradients. Hence, on the level of the zooxanthellate scleractinian animal phototrophic and heterotrophic energy supply and its bearing on calcification are being measured in different coral species—in particular inPorites sp., one of the most important reef builders.The growth of 15 zooxanthellate scleractinians in the Gulf of Aqaba correlates with the annual light cycle. This correlation is observable down to 40 m depth. Other growth promoting factors seem to have less influence on coral extension. The availability of organically enriched sediments in shallow water probably yields nutritional value, in particular for filter feeding species, thus restricting their distribution to those areas. Zooxanthellae, when isolated fromMycedium elephantotus, are different in their dependence on depth in maximum rates of photosynthesis and photosynthetic efficiency (-slope). Increasing concentrations of pigments as a function of depth could be determined. Maximum rates of photosynthesis of zooxanthellae in vivo, collected at corresponding depth, have been 4 times higher. Structural and physiological adaptations improving heterotrophic and phototrophic energy intake are highlighted. Porites sp. was the subject of annual growth studies at locations extending from Aqaba in the North over the northern and southern Egyptian coast and islands, Sanganeb Atoll and Wingate reef offshore Sudan to the Gulf of Tadjoura in the Gulf of Aden (Djibouti). Mean growth rates in the shallow water zone increase with decreasing latitude and are highest at the southernmost studied reefs in the Gulf of Tadjoura. However, the observed latitutdinal growth reduction is restricted to the upper ca. 15 m of the water column. The upper limit of growth potential decreases with depth parallel to the decrease of light availability. Highest growth rates are recorded in shallow depth (10–2.9 mm yr−1). This zone reaches at Aqaba (29°30′N) to a depth of ca. 10 m. At the southern Egyptian reefs (24°30′N) this zone extends to ca. 15 m water depth. This effect is probably a result of the stronger reduction of winter light levels and water temperature in the northern regions. Compared to other oceans the decrease of growth with increasing latitude of Red SeaPorites corals is far less, and growth rates at Aqaba are the highest observed at these latttudes.On the level of the community of reef inhabitants four principal topics are addressed:The first one is the dynamics of the proportions of hermatypic and ahermatypic organisms and open space. The occurrence of stony and soft corals and the sharing of empty space in different reef sections at Aqaba and on Sanganeb Atoll were quantified. Soft corals, mainlySinularia- and xeniid species, occupy decreasing shares with depth. Among theXenia species a bathymetrical zonation pattern was detected.The next issue is the growth impeding role of soft corals and gastropod parasites and predators on scleractinians. Experimental and field observations showed xeniid soft corals to be opportunistic i.e. occupying rapidly open space rather than to attacking and outcompeting stony corals. An increasingly specialized behaviour was detected among corallivorous gastropods of the family Coralliophilidae to exploit their coral hosts. Whereas these snails are more or less sessile and depend for a long time on the surrounding host polyps the mobileDrupella cornus (Thaididae) forms feeding aggregations which denude mainly branching corals on shallow reef parts.Furthermore, the role counteracting reef growth of macro- and microbioeroders is investigated.Diadema setosum is a major destructive agent on reefs at Aqaba (not in the central Red Sea). The grazing sea urchins do not only keep potential colonization area free but also erode carbonate material (e. g. 1468 g/m2/year, 10 m depth). Demographic and bathymetric patterns in the sea urchin population are analyzed including their bearing on bioerosion of the reef. Investigations on microboring organisms in carbonate material have started in the Red Sea; initial results, however, are only available from similar studies near Lee Stocking Island, Bahamas.Three major environments have been identified based on the distribution of the different microborers. These are1)the intertidal environment dominated by boring cyanobacteria.,2)reef sites from 2 to 30 m water depth dominated by a diverse assemblage of boring cyanobacteria and chlorophytes, and3)the deep reef slope from 100 to 300 m dominated by boring green algae and heterotrophs. The boring chlorophyte genusPhaeophila appears rapidly and dominates at sites from 2 to 30 m, but it leaves vacated borings and is replaced byOstreobium quekettii after 1 year. Different substrate types show very different rates of colonization by microborers. The greatest excavation rates (100 g/m2/3 months) occur in fine-grained limestone, while the slowest rates (0.5 g/m2/3 months) occur in calcite crystals. Molluscan shell material shows intermediate rates of excavation. Light conditions appear very important in determining the growth rate and distribution of different microborers between the sites, however, the interaction of light with other factors, such as substrate, time period of exposure, and water quality conditions may be involved.

Improvement of photosynthesis in zooxanthellate corals by autofluorescent chromatophores

Autofluorescent chromatophores were detected in 17 out of 71 zooxanthellate coral species studied. Chromatophores are localized either in the oral gastrodermic (endoderm) or oral epidermis (ectoderm). The pigment granules within the chromatophores (0.5–1.0 μm in diameter) show a brilliant light-blue/turquoise autofluorescence (emission between 430 and 500 nm) after excitation with light of 365–410 nm. All species where the autofluorescent gastrodermal chromatophores form a compact layer, embedding the zooxanthellae, belong to the family Agariciidae. In contrast, some species of the Faviidae (2), Pectiniidae (1) and Mussidae (1) were found to have distinct, autofluorescent chromatophores in the oral epidermis. Autofluorescent pigments of the host may enhance photosynthesis of the symbionts as in Leptoseris fragilis. Short wavelength irradiance, less suitable for photosynthesis, is transformed by host pigments into longer wavelengths which are photosynthetically more effective. Thus, host species possessing autofluorescent chromatophores might have selective advantage over non-fluorescent species, and have the potential to survive in light-limited habitats. Furthermore, the daily period of photosynthesis is extended, thus increasing the energy supply and enhancing the deposition of skeletal carbonate. The absence or presence of chromatophores may have value in taxonomy and could putatively be of plalaeontological and palaeoecological interest.

Macromolecular Mimicry: Substances Released by Sea Anemones and Their Role in the Protection of Anemone Fishes

To provide a background for the investigations dealt with in this paper, it is necessary to summarize some fundamental experiments on the protection of anemone fishes.

Influence of light on algal symbionts of the deep water coral Leptoseris fragilis

Photoadaptations of zooxanthellae living within the deep water coral Leptoseris fragilis taken from the Gulf of Aqaba (Red Sea) were studied. Specimens-collected in summer 1988 between 110 and 120 m depth —were transplanted to 70 and 160 m. At each depth individuals were exposed in their natural growth position (oral side facing the surface) or in a reverse growth position (oral side facing the bottom). After 1 yr of exposure the corals were collected and the zooxanthellae were isolated. As a function of the availability of light with depth and growth position several algal parameters showed changes which are related to photoadaptations. The relatively low density of zooxanthellae of 0.15x106 cellsxcm-2 at a natural growth depth of 116 m decreased to 0.0034x106 cellsxcm-2 (Δ2%) at 160 m in specimens growing with a natural orientation. In corals with a downward-facing oral surface at the same depth (160 m) only degenerated algae could be observed. With respect to depth dependence the volume of the algae decreased from 728 μm3 at 116 m to 406 μm3 at a depth of 160 m and the content of pigments increased. The augmentation of peridinin per cell was low (two times at 160 m compared to 116 m). Chlorophyll a and in particular chlorophyll c2 concentrations per cell were enhanced. Compared to natural amounts at 116 m, chl a was five times and chl c2 eight times higher at 160 m. At all depths the chl c2 content per cell was higher than for chl a. The formation of chl a/chl c2 complexes as light harvestor is discussed. Light harvesting, with chl c2 prevailing may be explained as a special type of chromatic adaptation of L. fragilis in a double sense: (1) in the habitat light short wavelengths predominate. This light can be directly absorbed with pigments such as chl a and chl c2. (2) Host pigments absorb visible violet light and transform these wavelengths, less suitable for photosynthesis, into longer ones by means of autofluorescence. The emitted longer wavelengths fit the absorption maxima of the algal pigments. Thus the host supports photosynthesis of his symbionts. Corals exposed at 160 m depth with a downward facing oral surface were alive after 1 yr and the host wavelength transforming pigment system was still present, but zooxanthellae were absent or degenerated. The light field at 160 m seems therefore to be critical: the combined photoadaptations of host and symbionts, allowing photosynthesis under barren light conditions, seem to be exhausted. In L. fragilis the photoadaptive strategies of host and symbionts cooperate harmoniously. In addition, the adaptations are interlocked with the particular light situation of the habitat with respect to light quantity and quality. The cooperation of physical and organismic parameters examplifies how evolution and, in particular, coevolution has led to optimal fitness.

A perforated gastrovascular cavity in the symbiotic deep-water coral Leptoseris fragilis: a new strategy to optimize heterotrophic nutrition

The organization of the zooxanthellate scleractinian coralLeptoseris fragilis was studied. The architecture of the corallite and the histology of the polyparium were analysed for adaptations that enable efficient capture and retention of suspended particles which would increase energy supply. The data indicate that the gastrovascular system ofL. fragilis is not a blind but a flowthrough system. Water entering the coelenteron through the mouth leaves the body not only through the mouth but also through microscopic pores (≂ 1–2 μm) which are located near the crests of the sclerosepta in the oral epithelia. Irrigation is achieved by flagellar and probably also by muscular activity. This type of filtration enablesL. fragilis, which lacks tentacles, to utilize suspended organic material including bacteria. The supposed suspension feeding in combination with effective photoadaptations (presented in former communications) seems to be the basis for the survival ofL. fragilis in an extreme habitat (between-95 and-145 m) and for its, successful competion with other scleractinian species provided with larger catching surfaces, and with other invertebrates depending on filter feeding.

Epidermal nutrition of the alcyonarian Heteroxenia fuscescens (Ehrb.): absorption of dissolved organic material and lost endogenous photosynthates

SummaryThe trophic strategies were studied of Heteroxenia fuscescens living in shallow tropical waters. Structural and physiological adaptations show that particulate food is of less nutritional importance than the uptake of organic material dissolved in the sea, the utilization of assimilates of cytosymbiotic algae (zooxanthellae) and even the symbionts themselves. The external and internal surfaces of the tentacles are enlarged by featherlike pinnules, on the one hand facilitating the epidermal uptake of dissolved organic compounds and on the other offering wellilluminated spaces in which large numbers of zooxanthellae can be ‘cultivated’.Zooxanthellae expelled from gastrodermal cells may be taken up by the mesenteric filaments of the dorsal mesenteries, where they are often decomposed and utilized. The transport of photo-assimilates from the gastrodermis to the epidermis through the mesogloea takes place at a low rate. Most of the released assimilates of the symbionts appear in the coelenteron. One fraction of these assimilates is distributed within the gastric channel system and can be taken up by developing stages living there; another fraction reaches the epidermis extracorporally via the pharynx and the sea. Thus both the pharynx and the epidermis absorb these photo-assimilates. The epidermal uptake capacity serves two main purposes: (1) active uptake and incorporation of external organic material dissolved in the sea; (2) reabsorption of internal, self-produced organic material, i.e. reduction of the loss of endogenous compounds escaping from the gastric cavity necessarily due to the polyfunctionality of the coelenteron.

Ernährungsphysiologische und ökologische aspekte der Aufnahme in Meerwasser gelöster Aminosäuren durch Anemonia sulcata (Coelenterata, Anthozoa)

SummaryAnemonia sulcata resorbs and accumulates tritiated l-amino acids dissolved in sea water in their natural concentrations (70–700 nmol/l).Resorption takes place mainly through the apical membrane of the ectoderm. Even after quite long periods of exposure autoradiography reveals that the amino acids resorbed are located in the ectoderm; this is attributable to its cytological structure. Electronmicrographs show that only the ectoderm bears microvilli.The rate uptake (2–10 μg/g wet weight/h) depends on the type of the amino acid and its concentration.The concentration below which only a very slight degree of uptake is detected ranges from 10–100 nmol/l for the different amino acids.Certain amino acids (phe, lys, leu, his, pro) are used mainly in metabolic synthesis. Others (gly, ser) are also used in oxidative processes, as indicated by the presence of tritium water which results from the oxidation of 3H-amino acids.The concentration of free amino acids in tentacle tissue has been analyzed. The concentration of glycine, for example, is greater by a factor of 107 in tissue than in the medium in which resorption takes place, showing that uptake is an active process.Calculation reveals that the actinians satisfy a substantial proportion of their metabolic requirements by resorbing organic material from the environment.ZusammenfassungAnemonia sulcata resorbierte und akkumulierte tritiummarkierte l-Aminosäuren aus Meerwasser, welche diesem in natürlicher Konzentration zugesetzt worden waren (70–700 nMol/l).Die Aufnahme erfolgte nahezu ausschließlich ektodermal; der überwiegende Teil der aufgenommenen und dann eingebauten Aminosäuren befand sich auch nach längerer Inkubation im Ektoderm. Diese Tatsache ist auf unterschiedliche cytologische Differenzierungen von Ento- und Ektoderm zurückzuführen. Elektronenmikroskopische Aufnahmen zeigen, daß nur das Ektoderm resorbierende Strukturen (Mikrovilli) besitzt.Die Aufnahmeraten waren (von natürlichen Konzentrationen ausgehend) für die untersuchten Aminosäuren verschieden hoch (2–10 μg/g Frischgewicht/h). Die aufgenommene Menge war von der Außenkonzentration abhängig. Die Konzentrationen, unterhalb denen nur noch eine sehr geringe Aufnahme registriert werden konnte, schwankten für die einzelnen Aminosäuren zwischen 10 und 100 nMol/l.Eine Gruppe von Aminosäuren (Phe, Lys, Leu, His, Pro) wurde vorwiegend in den Synthesestoffwechsel eingeschleust, eine andere (Gly und Ser) wurde überwiegend oxydativen Prozessen zugeführt.Der Gehalt an freien Aminosäuren von Tentakelgewebe wurde bestimmt. Die Konzentration von Glycin z.B. ist im Gewebe 107mal höher als im Medium, aus dem noch resorbiert wird. Die Aufnahme erfolgt daher mit größter Wahrscheinlichkeit aktiv.Formale Berechnungen zeigen, daß den Tieren durch die Aufnahme gelöster organischer Verbindungen ein Energiegewinn erwächst; dieser liegt über dem Energieverbrauch, der dem Sauerstoffverbrauch äquivalent ist.Anemonia sulcata resorbs and accumulates tritiated L-amino acids dissolved in sea water in their natural concentrations (70-700 nmol/l).Resorption takes place mainly through the apical membrane of the ectoderm. Even after quite long periods of exposure autoradiography reveals that the amino acids resorbed are located in the ectoderm; this is attributable to its cytological structure. Electronmicrographs show that only the ectoderm bears microvilli.The rate uptake (2-10 μg/g wet weight/h) depends on the type of the amino acid and its concentration.The concentration below which only a very slight degree of uptake is detected ranges from 10-100 nmol/l for the different amino acids.Certain amino acids (phe, lys, leu, his, pro) are used mainly in metabolic synthesis. Others (gly, ser) are also used in oxidative processes, as indicated by the presence of tritium water which results from the oxidation of 3H-amino acids.The concentration of free amino acids in tentacle tissue has been analyzed. The concentration of glycine, for example, is greater by a factor of 107 in tissue than in the medium in which resorption takes place, showing that uptake is an active process.Calculation reveals that the actinians satisfy a substantial proportion of their metabolic requirements by resorbing organic material from the environment.

Plasticity of the scleractinian body plan: Functional morphology and trophic specialization ofMycedium elephantotus (Pallas, 1766)

SummaryMorphological, histological and behavioral features indicate thatMycedium elephantotus, a zooxanthellate scleractinian species without tentacles, is well adapted for utilizing suspended organic matter for nutrition. The colonies are composed of vertically growing fan-like plates and can reach diameters of more than 1 m in depths below 20 m. The external body surface is coated with a mucus layer (cuticle) which enables the acquisition and accumulation of suspended organic material. The mucus-entangled particles pass to the mouth openings by gravitational transport assisted by water movement.In experiments the corals were able to discriminate between suspended food and mineral particles. Both types of particles were rapidly entangled in fine mucus nets or filaments. Mineral particles were never ingested and instead tumbled down the inclined skeletal plates. In contrast, food particles were actively incorporated when the mucus filaments accidentally touched the stomodaea during the downward gliding.The food-enriched mucus filaments were either transported by ciliary activity into the coelenteron or were sucked into the body cavities by decreasing pressure in the coelenteron caused by contraction of longitudinal, mesenterial muscles. The discriminative reactions to mineral or food particles are probably based on the release of different types of mucus.Nematocysts are infrequent in the oral epidermis, indicating that the capture of living prey plays a subordinate role in nutrition. The mesenterial filaments, in contrast, are densely packed with large nematocysts. Storage products were piled up within the tissues of gastral pockets.The adaptations ofMycedium elephantotus for using suspended food particles may explain the particularly high abundance of this species between ca. 20 and 40 m depth on a steeply inclined fore-reef slope in the Gulf of Aqaba (Red Sea).The evidence indicating the importance of heterotrophic fueling toM. elephantotus is supported by carbonate production rates which are, in contrast to that of many other zooxanthellate scleractinian species, almost constant at depths between 5 and 40 m and which are uneffected by varying light regimes over the year, suggesting that the reduced phototrophic contribution by the zooxanthellae is compensated by mucus suspension feeding.

Compatible intracellular ion composition of the host improves carbon assimilation by Zooxanthellae in mutualistic symbioses

Abstract. Cytosymbiotic algae within the hosts plasma are exposed to completely different ionic conditions than microalgae living in the sea. The altered ionic gradients, in particular, could be the reason for higher in hospite carbon assimilation levels. To study the effect of varying extracellular ionic conditions on isolated zooxanthellae, their photosynthetic capacity in pure seawater was compared to that in a test medium in which the concentrations of the major inorganic ions, the pH and the osmolality were adjusted to the conditions measured in the host cytoplasm. In this test medium the ratio between oxygen evolution and carbon fixation was 1.2:1.0; in contrast, zooxanthellae in the hyperionic seawater medium showed a comparatively higher oxygen production (2.6:1.0). These results are attributed to a higher energy demand for ion regulation of the isolated algae in the hyperionic medium. Isolated cytosymbionts in seawater need more energy both for the readjustment to the original intracellular ion concentration within the host cell and also for the maintenance of a much steeper gradient during incubation under hyperionic conditions outside the host. The particular intracellular ion concentration of the host cells could have been a decisive evolutionary factor for the very successful establishment of the mutualistic symbioses between anthozoans and dinoflagellates more than 200 million years ago.

THE EXTRACTION OF SPECIFIC PROTEINS FOR THE SIMULTANEOUS ECTODERMAL ABSORPTION OF CHARGED AND NEUTRAL AMINO ACIDS BY ANEMONIA SULCATA (COELENTERATA, ANTHOZOA)

Anemones posses distinct uptake systems for the absorption of neutral, acidic and basic amino acids. The uptake systems for acidic and basic amino acids seem to be highly specific. Neutral amino acids are absorbed either by a single system with broad specificity or by several systems with overlapping specificity. It was possible to separate by means of gel filtration and electrophoresis those proteins which specifically bind amino acids. The molecular weights of these proteins are larger than 30 000. Although the systems for the uptake of charged and neutral amino acids are different as far as their specificity is concerned, the isoelectrical points of the extracted proteins are similar.