Research by marine biologists from Wageningen University has shown that feeding on zooplankton by scleractinian corals has been greatly underestimated.
|Zooxanthellae uptake by coral larvae|
|Written by Tim Wijgerde|
A large number of marine organisms is known to live in symbiosis with other species, of which mutualism is the most common one. The dominant symbiotic interaction is the association between invertebrates and zooxanthellae. Recent studies have revealed how this beautiful partnership is established during early life.
Mutualism is very common in ocean ecosystems, and the reason for it is that it increases chances of survival for both parties involved. For example, crabs protect corals from being eaten by crown-of-thorns sea stars, cleaner gobies remove parasites from the skins of surgeon fish and pistol shrimp help many gobies dig their burrows while they are on a stake-out for predators and prey.
A very well known example of mutualism is the partnership between marine species and algae; foraminifera, radiolaria, nudibranches, jellyfish, anemones, Tridacna clams (fig.1) and of course corals have established partnerships with symbiotic algae from the genus Symbiodinium (zooxanthellae). The algae provide the animals with carbohydrates, which generates up to 95% of their daily required energy1,2,3. The algae, in turn, receive ammonium and other nutrients from their host, as well as a safer place to live.
Figure 1, above right: A large number of marine species has formed a symbiotic relationship. A nice example are Tridacna clams, harboring zooxanthellae in their outer mantles. Photograph: Tim Wijgerde.
Several years ago, scientists began understanding how the unique partnership between corals and algae was established at the start of each generation. It was discovered that corals either take up algae from the environment during their larval stage, called horizontal transmission, or that they receive them from their parent colony, called vertical transmission; a nice example is Xenia macrospiculata8. This last mode of transfer is now regularly found in brooding coral species, and about 15% of all coral species is estimated to make use of this strategy.
Both modes of symbiont transfer have their (dis)advantages; vertical transmission ensures that coral larvae are already equipped with these useful algae, whereas horizontal transfer allows the larvae to take up superior algae which may be adapted to the specific environment. Some corals, such as Montastrea faveolata/annularis, even harbour two species of zooxanthellae at one time4,5.
Several ways exist by which corals start teaming up with zooxanthellae. First, zooxanthellae may be taken up by the developing egg or embryo; this process probably takes place during offspring development of brooding coral species. Second, zooxanthellae may be taken up by the coral ectoderm, after which they migrate into the endoderm. Both of these mechanisms occur in the jellyfish Linuche unguiculata; both embryos and young, non-feeding larvae are capable of becoming infected by manually adding zooxanthellae. Third, zooxanthellae may be taken up directly by endodermal cells. This has been found in scyphistomae of Cassiopeia xamachana. In this mode of infection, symbionts enter through the mouth of the host and are taken up by endodermal cells lining the polyp gut.
This last mode of infection was also found in Fungia scutaria, a Fungiid or mushroom coral which inhabits the Indo-Pacific waters. For this study, 75 adult specimens of Fungia scutaria were maintained in running seawater tables at the Hawaii Institute of Marine Biology on Coconut Island, Kaneohe Bay, Hawaii. This species usually spawns between 5 and 7 p.m., about 2-4 days after the full moon during June and August. Eggs were kept in small glass bowls, and were fertilized by adding sperm cells from male colonies. Over the next days, the larvae were kept alive by regularly changing the water. They also isolated zooxanthellae from the tissue of adult corals, which were then used to infect the larvae. They stimulated feeding behaviour by adding an extract of Artemia nauplii. Next, they used microscopes to visualize larvae development and zooxanthellae uptake.
12 hours after fertilization, larvae started to appear. They were covered in cilia which allowed them to slowly move. After 24 hours, they were actively swimming, and at day 3 they had developed a mouth. When the larvae were exposed to the Artemia extract, they stopped swimming and dropped to the tank bottom. They started to feed on everything, including zooxanthellae (fig.2). Some larvae started swimming again while producing mucus, which trapped even more zooxanthellae (fig.2b). After 4 days they changed shape, turning into a ball and started to creep over the tank bottom. At day 5, they metamorphosed into a volcano-shaped polyp without tentacles. Day 6 marked the start of tentacle development (fig.2c and 3).
The larvae were also given zooxanthellae from different animals; Aiptasia pallida (glass anemone, clade B zooxanthellae) and Cassiopeia xamachana (clade D zooxanthellae). Interestingly, they had no problem with ingesting and retaining them. Settlement of larvae which did not ingest zooxanthellae was gravely affected, although they still underwent normal metamorphosis (fig.3).
Figure 2: Several stages of F. scutaria development. Top: 2 day old planula larva, before development of a mouth. Middle: 3 day old feeding larva with mucous production and food particles attached to it (m= mouth, mf= mucous strand with food particles, z = zooxanthella. Bottom: polyp with tentacles, 6 days after settling. Zooxanthellae are visible as golden spheres. Larvae length and polyp diameter are 100 µm (modified from Schwarz et al, Biol. Bull, 1999).
The azooxanthellate larvae which did not take up any symbiotic algae, usually died at the 'ball' stage just before settling. This is however affected by temperature, as the scientists observed one year later. When temperatures were normal, even larvae with zooxanthellae settled in low rates. It seems that when temperatures reached the bleaching threshold (about 30-32 °C, 86-90°F), larvae with zooxanthellae had a survival advantage.
They also determined the effect of larval feeding strength on zooxanthellae uptake. After adding Artemia suspension, 96.8% of the larvae became infected with zooxanthellae, compared to only 25% without this extra treatment. It seems that a high load of protein/amino acids (in this case from the Artemia suspension) stimulates the larvae to feed. In nature, these larvae are immersed in a pool full of diverse types of plankton, which may stimulate them to take up symbionts. It is also known that Cnidarians such as anemones produce mucus which are rich in zooxanthellae, especially when they are spawning6,7. This might help the larvae to take up the algae from the water column.
Figure 3: A: Major developmental stages of Fungia larvae. B: Left: Percentages of F. scutaria larvae at several stages of development in relation to time. Right: The effect of zooxanthellae uptake in relation to larval settlement. Without an algal symbiont, F. scutaria larvae do not settle properly (modified from Schwarz et al, Biol. Bull, 1999).
As soon as F. scutaria had developed a mouth, they were able to get infected by zooxanthellae at all later stages, including after settlement. Other broadcasting species produce non-feeding larvae which lack mouths, and only accept zooxanthellae after metamorphosis into a primary polyp such as some soft corals. Azooxanthellate corals such as Dendronephthya gigantea also brood larvae which do not develop a mouth until they have metamorphosed into a primary polyp (see our article about Dendronephthya reproduction). This last species exists without zooxanthellae throughout life, whereas many other corals rely on their symbiotic algae.
Merging corals and algae
The next question was how these larvae actually merged their tissues with the zooxanthellae. The scientists already observed larvae eating the zooxanthellae (figure 4), by moving small hairs, called cilia, creating small water currents that sucked the algae into their mouths. But what was the next step? How did these larvae retain their algal partners?
They found that a common mechanism called endocytosis was responsible for this. After having passed through the mouth of the larva, the algae were engulfed by the endodermal cytoplasm (fig.5). Both endodermal and ectodermal cells took up zooxanthellae within 1 h after larvae were exposed to them. After the uptake, the zooxanthellae resided inside a vacuole, small compartments reserved exclusively for the algae. Here, they produced sugars by photosynthesis, which probably started to benefit the larvae even before settlement.
Figure 4: Pictures of F. scutaria larvae, taken with an electron microscope. The larvae were exposed to zooxanthellae and Artemia suspension for 1 hour. Top: feeding 3-day old larva with zooxanthellae attached to its mucous strand (m=mouth, z=zooxanthella). Bottom: feeding larvae with several zooxanthellae entering the mouth. Bars: 10 µm.
Diverse feeding; it's all about staying alive
The fact that F. scutaria larvae are able to benefit from zooxanthellae before settlement, may have allowed them to spread through the Indo-Pacific waters, according to the scientists. Not only do they receive sugars from these algae, they are also supplied with yolk from the egg until day 6 of development (which is when they start settling). Their mouths will probably also allow them to ingest plankton, as they will do as well once they have transformed into primary polyps. A fourth mechanism by which these corals could feed might be the uptake of inorganic nutrients from the water, such as amino acids. Adult coral colonies, such as Stylophora pistillata, are known to efficiently take up free amino acids from the water even at very low concentrations (see our article about amino acids ).
Coral reproduction is diverse (see coral science archive, reproduction section and Dana Riddle, Advanced Aquarist Volume VII, issue X), and so too is coral larva development. The development of a mouth prior to settlement may be of great benefit to the worldwide dispersion of coral species.
The results from the above experiments may be important for future efforts of coral sexual reproduction, as optimizing symbiont acquirement and larval settling are key in this process. This research also helps us to understand how selective coral larvae are for taking up various zooxanthellae strains, which might determine which coral species will survive bleaching during the next centuries of global warming. This is because zooxanthellae type, or clade, determines how resistant corals are against bleaching caused by elevated temperatures (see coral science archive, section Climate change & Ecology). The fact that Fungia scutaria larvae are able to take up and retain zooxanthellae from three different clades (A, B and C), probably makes this species quite tolerant to future climate changes.
Figure 5: A: Initial contact between an endodermal cell and a zooxanthella. The larva’s endodermal membranes are very closely associated with the alga. B: Endodermal cell taking up a zooxanthella (modified from Schwarz et al, Biol. Bull, 1999).
We gratefully thank Professor Virginia Weis and Jessi Kershner, M.Sc. from Oregon State University for their pictures and scientific comments.
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