Research by marine biologists from Wageningen University has shown that feeding on zooplankton by scleractinian corals has been greatly underestimated.
|How coral reefs grow|
|Written by Tim Wijgerde|
Coral reefs are widely known for their majestic beauty; these porous underwater mountains belong to the most species-rich biotopes on the planet. They are home to countless vertebrate and invertebrate animals, and have been documented and visited by many. These unique ecosystems have been created by the combined forces of billions of tiny invertebrate animals; the coral polyps. After many scientific studies, it has become clear how these animals have been able to create a Garden of Eden from virtually nothing.
Coral polyps; the bringers of life
Corals are mostly sessile, colonial polyps, although solitary species exist. Coral polyps have tentacles, a mouth, a gastrovascular cavity and are connected to one another by common tissue called coenosarc. The outer, cellular layer of a polyp's tentacles is highly loaded with nematocysts; cells which can fire stinging barbs filled with neurotoxins. This allows corals and anemones to paralyze prey, ranging from small plankton to even small fish, depending on the size of the polyp. The polyp gut is a simple sac, and many coral species actually have guts which are connected together, allowing them to share nutrients. The gut is also the location where its gonads are located. Along the gut mesenteries, ovaries and testes will produce oocytes and spermatocytes, which are released during specific times of the year (for more info on coral anatomy read the article ‘coral reefs, an introduction').
Figure 1: Coral polyps provide life to a staggering amount of species, such as this yellow feather duster and deep blue tunicates (photograph: Hans Leijnse).
Many coral species build skeletons, which provide a refuge against predators. They also help newly settled coral polyps to attach themselves onto rocky substrate. These skeletons, which are secreted by the underside of the polyp skin, eventually created the colorful reefs which we know today. The basal plate of a polyp is where its skeleton starts (fig.1), which is made from calcium carbonate (or aragonite). The molecules which make up the skeleton are secreted by the calicoblastic layer or epithelium; the ectoderm or skin lining the lower part of the polyp. This process consumes significant amounts of energy, and the rate at which it occurs is quite slow. Some stony corals may grow about 5 mm (0.2 inches) each month, while others such as deep water corals may grow much slower. This so-called process of calcification is very energy-demanding; this energy is provided by algae residing in coral tissue. A group of algae from the genus Symbiodinium has formed a partnership with corals; these are called the zooxanthellae. They produce sugars by using the sun’s energy, just like higher plants do. We call this process photosynthesis, and it provides up to 95% of the energy corals need.
When coral reefs die, such as after bleaching due to warm summers, most reef inhabitants die as well, or simply leave the grounds. This is because the corals do not only provide a living space, but are also a key food source for many species such as fish and nudibranches.
Building a coral skeleton
Corals secrete their skeleton through the calicoblastic layer; this is the outer layer of skin or ectoderm located at the underside of all polyps. This layer contains specialized cells which continuously secrete calcium (Ca2+) and bicarbonate ions (HCO3-) to the external environment. Eventually, this leads to the deposition of a matrix of calcium carbonate (CaCO3 or aragonite). Pumping these ions against a gradient is quite energy-demanding, and this energy is provided by the coral’s symbiotic zooxanthellae. Many species are able to grow over 1 cm (0.4 inches) a month this way. According to estimations, tropical stony corals are able to deposit about 10 kg of aragonite per m2 per year (2,25 lbs per square ft per year)1.
Because light generates the bulk of the required energy to make this happen, through photosynthesis by the algae, this process is commonly referred to by scientists as “light-enhanced calcification”. From many experiments it has indeed become clear that this statement is accurate. Corals deposit significantly more calcium carbonate during the day; for the stony coral Stylophora pistillata this is about four times as much2. For Galaxea fascicularis this has been found as well; these differences in growth can be recorded as soon as 10 minutes after the light has been switched on.
Creating something from nothing, how does it work?
Building a coral skeleton is a complex process, and can be divided into two major steps:
Step 1: Taking up the building blocks
The first step is the uptake of calcium and bicarbonate ions from the water column through the oral pore and through the ectoderm. Next, the ions enter the gastrovascular cavity or coelenteron. This process is diffusion-dependent and therefore passive; no energy is required for this.
Figure 2: The uptake of bicarbonate ions from seawater by the ectoderm of a coral polyp. The ions diffuse through both cellular layers and the mesoglea, after which they enter the coelenteron. A part of the ions splits into CO2 and hydroxide ions (OH-). A major portion of the CO2-molecules is taken up by the zooxanthellae. The hydroxide ions help stabilize the pH of the coelenteron by reacting with protons (H+-ions). Zoox: zooxanthella (image compiled from Hans Leijnse and Furla et al, Journal of Exp. Biol., 2000).
A part of the ions splits into CO2 and hydroxide ions (OH-). A major portion of the CO2-molecules is taken up by the zooxanthellae. The hydroxide ions help stabilize the pH of the coelenteron by reacting with protons (H+-ions) into water (H2O).
Step 2: Transporting the building blocks to the growing skeleton
The next step is to transport the bicarbonate ions to the so-called calicoblastic fluid; this is the stagnant layer of water located directly beneath a coral polyp, where aragonite deposition takes place. This process is energy-demanding, which requires an energy carrier. This is provided by very commonly used molecule by all life on our planet, and it is called ATP (adenosine triphosphate). ATP itself is produced in the power reactors of a living cell; the mitochondria (fig.3). the calicoblastic cells in the outer skin layer are highly enriched with these cell organelles, and work hard on a daily basis to allow corals to build their skeleton. ATP is produced by oxidizing carbohydrates and fatty acids, and the yielded energy is used to transport mainly calcium ions over the calicoblastic layer (fig.3). The needed carbohydrates are produced by the zooxanthellae, and provide up to 95% of the energy budget4,5,6. The transport of bicarbonate ions takes place by exchanging of negatively charged molecules from the external environment (represented as A-). This principle is called antiport. The pumping of calcium ions over the cellular membrane is also carried out by an antiport system; the only difference is that the calcium ions as well as the protons (H+) have to be transported across a gradient. This is similar to a salmon trying to swim up a river against a strong countercurrent; this understandably uses up a lot of energy. ATP, in the end, is the energy carrier for this process allowing the calcium/H+-pump to perform its task.
Figure 3: The deposition of calcium carbonate by the outer skin layer or ectoderm at the basal plate of a coral polyp. The bicarbonate ions again diffuse through the mesoglea, although this process is not yet completely understood. The next step is however not passive, but active; bicarbonate ions are pumped into the calicoblastic fluid by an antiporter system which uses up negatively charged ions (A-). Calcium ions (Ca2+) are also translocated to the calcifying layer, and H+-ions are pumped into the calicoblastic cells at the same time. As this process works against a chemical gradient it uses up energy, which is provided by the hydrolysis of ATP to ADP and inorganic orthophosphate (Pi). Note that most bicarbonates originate from the coral cell’s own metabolism; the mitochondria exhale CO2, after which the enzyme carbonic anhydrase (CA) catalyzes the reaction to generate bicarbonate ions (HCO3-). Up to 75% of the available bicarbonate originates from the coral itself, and not from the water column! Eventually, the bicarbonate en calcium together precipitate as calcium carbonate (CaCO3). The released protons (H+) are constantly pumped back into the coral cells to ensure a continuous high pH value in the calicoblastic layer. This remains about 9.3 during the day, and drops to about 8 at night. This means that stony corals grow mostly during the day (modified from Furla et al, Journal of Exp. Biol., 2000).
Eventually, the bicarbonate and calcium together precipitate as calcium carbonate (CaCO3). The released protons (H+) are constantly pumped back into the coral cells to ensure a continuous high pH value in the calicoblastic layer. This has to do with a very important chemical equilibrium in seawater:
Figure 4: The CO2-equilibrium. As pH levels drop, more carbonate ions are converted into bicarbonate ions. This provides more room for new carbonate ions, such as those from the coral skeleton. For this reason, corals maintain high calicoblastic fluid pH levels to prevent newly produced skeleton from redissolving. The amount of free carbonate ions is called the aragonite saturation state. During the day calicoblastic fluid pH levels lie around 9.3, and around 8 at night. At these pH levels, calcium carbonate cannot dissolve properly and precipitates as aragonite (image: Tim Wijgerde).
Without this high pH level, coral skeleton would dissolve quickly. As pH levels drop, more carbonate ions are converted into bicarbonate ions. This provides more room for new carbonate ions to dissolve, such as those from the coral skeleton. For this reason, corals maintain high calicoblastic fluid pH levels to prevent newly produced skeleton from redissolving.
The concentrations of free calcium and carbonate ions are collectively called the aragonite saturation state. During the day, the pH-level of the calicoblastic fluid lies around 9.3, and around 8 at night. This means that corals mostly grow during the day! The current rise in atmospheric CO2-concentration causes oceanic pH levels to drop slowly, as they absorb about 20% of this greenhouse gas. When CO2 dissolves in water, it lowers the pH value by releasing H+-ions. If current CO2-emissions persist, this level will drop to about 7.4 in the year 2150, dissolving entire coral reefs4. Long before that, bleaching will have devastated virtually all reefs leaving behind barren patches of rubble. Even now, a decline in coral calcification is noticeable, and calcifying organisms in temperate seas are especially affected. This is has to with the physicochemical aspects of the ocean. Calcium dissolves more easily in cooler waters; think of the common calcium carbonate precipitation on aquarium heaters. This is simply the exact opposite phenomenon.
Alkalinity, the main source of bicarbonates?
Although the dissolving of CO2 in the oceans forms a major future threat, this process is very useful within coral tissue. Next to taking up bicarbonates, coral polyps produce a lot of these ions through their own metabolism. Research has shown that 70-75% of the bicarbonate budget originates from the conversion of intracellular CO2!2 This means that only 25-30% of the bicarbonate ions are extracted from the water column. Although corals produce more CO2 at higher light intensities, scientists have found that this ratio does not shift under different irradiance levels.
The production of bicarbonate ions from CO2 usually is a passive process and is pH-dependent. However, living cells possess enzymes; proteins which are able to catalyze chemical reactions. The carbonic anhydrase (CA) enzyme catalyzes the reaction between CO2 and water into bicarbonate, thereby generating large quantities of these building blocks. It is however recommended to keep alkalinity levels between 2,5 and 3 meq/l, as sufficient bicarbonate ions are still required for normal coral growth. Furthermore, (bi)carbonates help stabilize aquarium pH, especially during night time.
Figure 5: Corals acquire the bulk of their bicarbonate ions from their own metabolism; up to 75%. The deposition of calcium carbonate by coral polyps has created a habitat for countless species (photo: Hans Leijnse).
Why do corals grow faster during the day?
Laboratory experiments have shown that corals grow a lot faster during the day; why is this exactly? There are several possible explanations for this phenomenon. The first process which may increase aragonite precipitation is the high production of ATP by the calicoblastic cells, as they receive significant amounts of carbohydrates from the zooxanthellae; the measured ATP content in Galaxea fascicularis tissue was about 35% higher in light-incubated colonies compared to dark-incubated ones. A lot of ATP means that ample energy is available for transporting calcium and bicarbonate ions to the calicoblastic fluid. A second process which mediates light-enhanced calcification is an increase in tissue pH levels during the day, as zooxanthellae take up more CO2. Corals have less difficulty with depositing aragonite at higher pH-levels, as the aragonite saturation state increases. The third possible reason for elevated calcification during the day may be the activation of the Ca2+/H+ pump, which is light-sensitive, thereby pumping more building blocks to the skeleton3. Finally, extra bicarbonate production may yield extra building blocks for synthesizing the skeleton (table 1). In overall, the process of calcification can be summarized with the following equation:
Ca2+ + 2HCO3- --> CaCO3 + CO2 + H2O
Table 1: An overview of the calcium/bicarbonate concentrations and pH in different compartments of a coral polyp during the day and night. The red figures indicate the primary factors stimulating calcification; the high production of bicarbonate ions and high pH in the calicoblastic fluid. The calcium concentration is essential as well; this is even higher during the day, despite the large flux towards the calcium carbonate matrix. X: no data available (compiled from Furla et al, Journal of Exp. Biol., 2000 and Al-Horani, Marine Biology, 2003).
The fusion between coral and skeleton
Now that it is clear how corals are able to create something beautiful from seemingly nothing, the next question is how their tissue is connected to the aragonite matrix. This has to do with the calicoblastic epithelium, which contains other specialized cells next to calicoblastic cells. These other cells are specialized in adhesion, and are called desmocytes7. These cells uniquely connect the coral tissue to the skeletal matrix, by means of numerous protrusions running into the mesoglea. Figure 6 basically shows one giant desmocyte, which extends profoundly into the mesogleal connective tissue of the coral. From the protrusions, countless protein bundles called filaments extend even further into the tissue, effectively creating a very large surface contact area between coral and skeleton. A desmocyte is comparable to the outer calicoblastic cells as depicted in figure 3, however these anchoring cells are much more erratic in morphology. desmocytes are connected to coral skeleton with countless fibres which branch out into the aragonite; these proteins together form the organic matrix. Adding amino acids to aquaria has reportedly increased coral growth, which may be explained in part by stimulation of the organic matrix buildup (see the coral science archive for more information).
The models from this article have been compiled by scientists, by interpreting countless complex experiments which involved using radioactive isotopes of calcium and carbon. This allowed the biologists to conduct so-called pulse-chase experiments, which means that the uptake and translocation of chemicals by animals is carefully measured. Coral growth is a unique process, and it shows us how these remarkable creatures have adapted to the harsh oceanic environment. By utilizing biochemical processes in a smart way, many corals are able to build a skeleton which allows them to attach to substrates and hide from predators.
Figure 6, right: An overview of a desmocyte, which connects coral tissue (mesoglea, m) to the coral skeleton (lower right) via numerous protrusions. The protrusions again branch out into smaller fibres (sf). The desmocyte nucleus (n) is located on the top right, and a mitochondrion (mt) can be seen on far left. The desmocytes are connected to the skeleton through countless fibers which branch out into the skeleton (plaques, pq). It has become clear that sufficient amino acids are required for coral growth, which are ingested through particulate feeding and are taken up from the water column. The amino acids are used for tissue buildup, and for synthesizing the organic matrix which branches into the skeleton (image: Toby Wright).
Figure 7, left: Electronmicroscopic photo of a desmocyte (D) which stretches out into the skeleton. The skeletal matrix itself is no longer visible, as this has been removed for image processing (black domain on the photograph, Muscatine et al, Coral Reefs, 1997).
Chave, KE, Smith SV and Roy KJ, Carbonate production by coral reefs, Mar. Geol., 1975, pp 123–140(12)
Furla P, Galgani I, Durand I and Allemand D, Sources and mechanisms of inorganic carbon transport for coral calcification and photosynthesis, Journal of Experimental Biology, 2000, pp 3445-3457(203)
Al-Horani FA, Al-Moghrabi SM, de Beer D, The mechanism of calcification and its relation to photosynthesis and respiration in the scleractinian coral Galaxea fascicularis, Marine Biology, 2003, pp 419-426(142)
Falkowski, PG, Dubinsky, Z, Muscatine, L, Porter, JW, Light and bioenergetics of a symbiotic coral. Bioscience, 1984, pp 705–709(34)
Muscatine, L. Porter, JW, Reef corals: mutualistic symbioses adapted to nutrient-poor environments. Bioscience, 1977, pp 454– 460(27)
Edmunds, PJ, Davies, SP, An energy budget for Porites porites (Scleractinia). Mar. Biol, 1986, pp 339– 347(92)
Muscatine L, Tambutte E, Allemand D, Morphology of coral desmocytes, cells that anchor the calicoblastic epithelium to the skeleton, Coral Reefs, 1997, pp 205-213(16)