LITERATUREResearch
TROPHIC STRATEGIES OF ANTHOZOANS
The polytrophic nature of anthozoans enable the utilization of up to four independent
possibilities to suffice their energy supply: 1) They use living and/or dead
particulate organic material either as macrophages or microphages.
2) They absorb dissolved organic material through the epidermal tissue (ectoderm).
3) Zooxanthellate species profit from their endocytosymbiotic algae (zooxanthellae
= unicellular algae of the genus Symbiodinium).
4) Finally, the skeletons of a multitude of scleractinian corals are colonized
by endolithic red and green algae (e.g. Ostreobium quekettii), whose
photoassimilates like those of the zooxanthellae, are used by the corals.
Depending on the availability of trophic resources in the different habitats,
different species compensate the shortage of one resource e.g. mesozooplankton
by specializing on using another e.g. picoplankton or microplankton. The versaltility
of such a specialized species enables them to settle in "trophic niches" far
out of reach for the less adaptable species. These species-specific qualities
especially of the scleractinian corals in relation to environmental conditions
have been a topic of discussion for decades.
HETEROTROPHY
On reefs sessile suspension feeders are in mutual competition for food resources
with each other and also with mobile filter feeders and predators. Species may,
however, reduce trophic competition by turning to less attractive foodstuffs
e.g. phytoplankton, protozooplankton, bacterioplankton, organic debris. To be
able to utilize those resources the species require adaptations to accumulate
and digest the microparticulate trophic components.
During our studies at the reefs in the Gulf of Aqaba, Red Sea; (Marine Science
Station Aqaba, Jordan) we were able to prove that such adaptations exist, enabling
the collection and retention of microscopic particles based on two different
strategies
Leptoseris fragilis, a deep-water stony coral lives in depths between
90 and 145 m. This zooxanthellate species, lacking tentacles, posesses a perforated
coelenteron which greatly enhances it`s supply of micro-POM. The corals grow
with the oral surface facing upwards, functioning as a sediment trap.
Suspended particles transported by ciliary activity along the surface and through
the mouth into the coelenteron are retained in the highly ramified gastrovascular
system (working like a sieve) while the "cleaned" water - now bare of particles
- flows out of the coelenteron through perforations in the oral body wall
(Fig.1).This species has become an active suspension
feeder, creating a water flow through the body, greatly increasing the particle
supply in a low flow velocity deep water environment. The body plan of L.
fragilis is unique.
Mycedium elephantotus a zooxanthellate scleractinian species without
tentacles, has its highest abundance at 20 m depth (Gulf of Aqaba, Red Sea).
The colonies are composed of vertically growing fan-like plates. The external
body surface, free of cilia, is coated with a thick mucus layer enabling the
acquisition and accumulation of suspended organic material. The food particles
trapped in the mucus slide down the vertically orientated skeleton plates due
to gravitational transport and weak water movement, only. In contrast to mineral
grains, food particles are actively incorporated when the food-enriched mucus
threads accidently touches the mouth openings (Fig.2)
. Due to this strategy particles with a diameter of less than 1 µm can
be trapped and metabolically used. Proven with 14C-labelled zoodetritus.
The composition of anemone and coral mucus was studied biochemically and histochemically.
Predators and suspension feeders were analyzed comparatively. The analyses show
that the constituents of the mucus from the different "feeding types" differ
both qualitatively and quantitatively.
The acquisition and retention of food particles are prerequisites to utilized
abundant microscopic particles, which are, however, low in nutritional value.
The capability to digest the retained particles is decisive for the utilization
of living or dead organic material. The equipment with digestive enzymes of
hexacorallia and octocorallia from low and high latitudes are currently investigated.
The zooxanthellate and azooxanthellate species were chosen according to features
which characterize the species as predators or suspension feeders. Key enzymes
for the digestion of food sources of plant or animal origin are also presently
being analysed. We are studying for sea anemones, soft corals and scleractinians
the activity of cellulase, laminarinase, chitinase, lysozyme, protease, lipase
and wax ester hydrolase.
Herbivory of soft corals
The use of living or dead algae by cnidarians is controversly discussed. In the azooxanthellate soft coral Dendronephthya sp. histological autoradiographs and biochemical analyses show that 14C-labelled microalgae (diatoms, chlorophytes and dinoflagellates) are used as a recource of food. Digestion of the algae takes place at the point of exit of the pharynx into the coeleron (Fig.3). Ingestion of labelled algae depends on incubation time, cell density, and to a lesser extend on species-specificity. The 14C-labelling patterns of the four classes of substances (polysaccharides, proteins, lipids and compounds of low molecular weight) vary depending on incubation time and cell density. 14C incorporation is highest into lipids and proteins. Dissolved labelled algal metabolites, relesased during incubation into the medium, contributed between 4% and 25% to the total 14C activity incorporated. The incorporated microalgae contribute a maximum of 26% (average of four species studied) to the daily organic carbon demand, as calculated from assimilation rates at natural eucaryotic phytoplankton densities (6000 cells per ml) and a 1 h incubation period (Tab.1). The calculated contribution to the daily organic carbon demand decreased after prolonged incubation periods to about 5% after 3 h and to 1-3% after 9 h. Thus the main energetic demand of Dendronephthya sp. has to be complemented by other components of the seston.
2. Epidermal Absorption of Dissolved Organic Material = D O M
The carrier mediated uphill transport and the metabolic use of dissolved organic
material is ubiquous (universal) for cnidarians. Cytological, physiological
and biochemical aspects of the exploitation of this trophic resource were studied
intensely in the past. Estimates indicate that through this way of nutrition
a substantial amount of energy becomes available.
The transport of amino acids is sodium sensitive, indicated by investigations
with membrane vesicles prepared from epidermal tissue. This was the background
to study the absorption of amino acids by the brackish hydrozoon Cordylophora
caspia, which lives in both sea and fresh water, displaying an optimal growth
rate at 16 °/oo salinity (Fig.4). The absorption
of amino acids has it`s maximum at the same salinity. The ability of C. caspia
to absorb DOM may be particularly important for mouthless redifferentiated polyps
are unable to use POM.
The exploitation of DOM requires an active transoport mode, as the intracellular
concentration of amino acids is much higher than that of the environment, so
that uptake of e. g. amino acids must proceed against concentration gradients
of up to 1:105. Speculatively speaking, the epidermal mucus layer
of anthozoans may be involved in an first adsorptive step in DOM absorption,
thus lowering the high concentration gradients across the epidermal membranes.
Experiments were carried out with mucus in vivo and in vitro. The properties
of the mucus of the sea anemone Anemonia sulcata was changed by inducing
alterations of: the pH, presence/absence of Ca2+ and Mg2+
(influencing the charge of the glycoproteins), temperature and salinity. At
low concentrations (5-30 nM) the adsorption of amino acids on the mucus was
saturable (Fig.5). Adsorption of charged amino
acids was less compared to the adsorption of neutral apolar or neutral polar
ones; implying that the adsorption is due to hydrophobic interactions. The adsorptive
accumulation of amino acids to the mucus reduces the gradient and thus the energetic
costs for the energy dependent transport. In addition the epidermal mucus layer
may also reduce the loss of intracellular low molecular compounds into the sea.
3. Photoecology of Zooxanthellae
In former studies the metabolic interactions between the coral host (Heteroxenia
fuscescens) and the endocytosymbiontic algae (zooxanthellae) have been investigated.
Presently the photosynthetic properties of zooxanthellae are under investigation
to obtain an idea on whether or not the zooxanthellae living within the various
coral species belong to one taxon.
Isolated zooxanthellae of different origin (prepared from various species and
from individuals collected at different depth levels) showed photoadaptations
toward light limitation (quantitative and qualitative alterations of chla and
accessory pigments). These detected different photosynthetic features (a-
slope, IC) point towards a phenotypic plasticity and not towards
a genetic heterogenety of the zooxanthellae (enzyme electrophoresis)
(Fig.6).
Zooxanthellae posses adaptations to low light condition as mentioned above.
In the zooxanthellate, agariciide coral Leptoseris fragilis (living between
90 and 145m) an autofluorescent chromatophore system was detected which improve
the photosynthesis of the symbiotic algae; i. e. the host provides the symbionts
with light. In follow up investigations of all other agariciide species in the
Red Sea, even for those living in shallow waters, a similar "light supplying
mechanisms" was detectable. The pigment granules of the chromatophores in the
gastrodermis of the host underlie and partially cover the zooxanthellae (Fig.8).
The functions of the chromatophores are: 1. The layer of pigment granules serves
as a reflector. 2. The light is scattered by the granules. Both these mechanisms
increase photon absorption of the algal pigments. 3. Light of short wavelengths
is absorbed by the host pigments located within the granules of the chromatophores
transforming the short wavelengths into longer ones
(Fig.7). The emitted light is far more suitable
for photosynthesis. This mechanism enables the utilization of "light energy",
otherwise unavailable for photosynthesis prior to transformation by the host.
Action spectra measurements of photosynthesis confirmed the improvement of photosynthesis
by the autofluorescent chromatophores. Monochromatic light of 387 nm (outside
the main absorption maxima of the algal pigments) was as effective as polychromatic
light of 415-490 nm, correlating with the absorption maxima of the zooxanthellae.
The presence of such light supplying chromatophore systems in certain zooxanthellate
scleractinian species and the availability of solar energy in reefs is of general
ecological interest. Species posessing autofluorescent chromatophores are able
to settle in dim-light habitats, extending their bathymetric distribution (e.g.
L. fragilis). The host's light supply in part compensates shadowing due
to self-shading (colony shape) or overgrowing. The daily photosynthetic active
period may thus be extended and intensified, leading to faster growth and carbonate
production.
The Agariciidae consits of predominantly deep water or cryptic living species,
including a few very successful pioneer species.
The impact of the intracellular ion composition on photosynthesis
Cytosymbiotic algae within the hostīs plasma are -in general- 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) (Fig.9). These results are attributed to a higher energy demand for ion regulation of the isolated algae in the hyperionic medium. Isolated cytosymbionts in sea-water 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.
A broad variety of organisms including filamentous green algae (Ostreobium
quekettii) live within carbonate substrates, in particular in the skeletons
of corals (Fig.10) (Fig.11).
The objectives of our studies are threefold: 1) to study the trophic potential
of the endolithic algae in terms of biomass and productivity; 2) to determine
the impact of radiation on pigmentation of endolithic algae and 3) to analyse
trophic interactions between the endolithic algae and the overlying coral tissues.
The biomass of O. quekettii represents ca. 7% of the protein content
of the zooxanthellae-containing coral tissue (on surface basis). Oxygen production
of the endoliths averaged ca. 6 % of that of the zooxanthellae. Algae within
the skeletons receive ca. 4 - 6% of the ambient irradiance. Increasing depth
(decreasing radiation) correlated with an increase of the Chlb to Chla ratio,
indicating an improvement on light harvesting under low light conditions.
Zooxanthellate species are not ideal for studying metabolic interactions between
endolithic algae and coral tissue as in 14C-tracer experiments the much higher
photosynthetic activity of the zooxanthellae masks the much lower photosynthetic
rate of the endolithic algae. The experiments were therefore carried out with
the non-zooxanthellate species Tubastraea micranthus.
The time course of 14C light fixation into the endolithic algae and the transfer
of photoassimilates to the coral tissue is slow. After 9 h, 60% of the 14C activity
recovered in the organic material was in the organic components of the skeleton
- predominantly in the endolithic algae - and 40% in the coral tissue; dark
fixation averaged 15% of light fixation. The different components of the coral
tissue were fractionated showing the highest 14C incorporation in the lipid
fraction, emphasizing the well-known fact that lipids play a central role in
the metabolism of corals.
The trophic role of endolithic algae is twofold: firstly, endoliths are consumed
by grazers, in particular by urchins and parrot fish. Though the actual productivity
is low, compared to epibenthic algae, the endolithic biomass is of importance
in reefal food webs. Secondly, endolithic photoassimilates are utilized by the
metabolisms of the corals themselves, i.e. endolithic algae are involved in
recycling processes within scleractinian colonies reducing the loss of mineral
nutrients into the open sea and thus contributing to the high productivity of
photic, subtropical/tropical reefs.
CONTROL OF CARBONATE PRODUCTION
5. Calcification Dependent on Energy Supply
Growth rates of entire coral colonies in the Gulf of Aqaba are species-specific
and depend upon the water depth level. Water depth is an environmental
factor comprising several subfactors, such as: gradients in radiation, temperature,
salinity and pressure. Incorporating water movement, substrate properties, substrate
inclination and the availability of POM. Each of the above listed subfactors
can potentially influence the carbonate production.
In our field studies we are particularly interested in energy delivering processes
involved in calcification.
In zooxanthellate, hermatypic coral species growth and carbonate production
depends on metabolic energy, which may originate from all of the four nutritional
pathways mentioned above. We tried to quantify the availability of POM and irradiance
with carbonate production in bathymetric dependence and in an annual cycle.
Species-specific differences in colonial carbonate production exist the whole
year round independent of growing depths and exhibit a maximum during the summer
months (Fig.12). The absolute increment of carbonate
decreases in all species as a function of depth. At different depth levels studied
(2,10,20,40 m) the carbonate production of the different species appears similar
when related to the surface of the skeletogenic tissue. The annual availability
of POM (we determined the amount of organic carbon in the sediment and the seston)
does not correlate with carbonate production. The annual skeletal mass increment
correlates best with seasonal changes of irradiance, a fact which supports the
importance of the zooxanthellae in calcification.
Supported by the DFG. Date: Juli 2002