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How corals feed
Written by T. Wijgerde, M.Sc., F. Houlbrèque, Ph.D. & C. Ferrier-Pagès, Ph.D.   

Stylophora catching Artemia naupliiCorals have developed several unique ways of feeding; they receive nutrients from symbiotic algae, capture particles such as plankton, and take up dissolved substances from the water. A proper understanding of these processes contributes to successful coral husbandry practices.

Corals are fascinating animals; although their morphology appears simple, these ancient organisms are highly complex. This also holds true for the way they feed; over the last decades, scientists have unraveled much about coral diets. Although many species harbour symbiotic algae which provide them with energy, corals also need building blocks to grow. A common saying amongst scientists states that "fed corals are happy corals". According to latest insights, this philosophy appears to be right on the money.

Figure 1: A Stylophora pistillata colony catching Artemia nauplii (photograph: Jean-Louis Teyssié, IAEA Monaco).

This review will discuss major coral nutrient sources, and their crucial roles in the existence of these marine invertebrates.

"A common saying amongst scientists states that ‘fed corals are happy corals’.  According to latest insights, this philosophy appears to be right on the money."

Autotrophy and heterotrophy

Life on earth is always classified into systematic groups by biologists, on the basis of external appearance (e.g. birds and mammals), behaviour (diurnal or nocturnal) or the characteristics of living cells (e.g. plant- or animal cells). A fourth means of distinction is metabolism, which can be autotrophic or heterotrophic. These terms are commonly used in marine biology, especially when regarding bacteria. Autotrophy means that organisms use inorganic molecules (such as CO2 and bicarbonate) to build organic ones, such as carbohydrates. Examples are plants, which convert CO2 into carbohydrates by using  sun's energy, or sulphur bacteria, which utilize the chemical energy stored in sulphur to convert CO2 to organics. For plants, we call this photoautotrophy (photo: light, auto: self and trophy: feeding) and for bacteria, in this case, we call this chemoautotrophy (chemo: chemical reaction). Another term for photoautotrophy is photosynthesis, another word for chemoautotrophy is chemosynthesis. Autotrophic organisms are also called primary producers, as they are the first link in the food chain which leads to biomass production from inorganic molecules.

Heterotrophy means that organisms make direct use of organic molecules, which are either present in the environment, or have been produced by autotrophic organisms. The consumption of plants by snails or cows is a form of heterotrophic feeding. From CO2, carbohydrates have been formed by using sunlight, which the plants have converted into biomass; this is subsequently consumed and converted into animal biomass.

"Autotrophic organisms are also called primary producers, as they are the first link in the food chain which leads to biomass production from inorganic molecules."

A diver next to a feather star

Figure 2: Two heterotrophic organisms. A human and a feather star (Comanthina sp., photograph: Hans Leijnse).

Corals; both autotrophic and heterotrophic?

Corals are somewhat more complex in this respect; the animals themselves are heterotrophic and consume plankton and dissolved molecules. Next to this, many species receive photosynthates from symbiotic algae, which are commonly called zooxanthellae. These photosynthates are produced by means of photosynthesis, and comprise sugars, fatty acids, glycerol and amino acids. Although corals themselves are heterotrophic just like all other animals, both hetero- and autotrophic processes take place inside their tissues (excluding corals which lack zooxanthellae). Corals are often considered as being either autotrophic or heterotrophic. They are probably best viewed as polytrophic, using both ingested and translocated carbon as energy sources.

Energy and building blocks

The photosynthates which zooxanthellae provide their hosts with can deliver up to 100% of the daily required energy budget for corals1,2,3. These are often deficient in nitrogen and phosphorus, and are thought to be mainly used as fuel for respiration and mucus secretion, rather than being assimilated into biomass1,5. Zooxanthellae transfer glucose, glycerol, fatty acids, triglycerids and even amino acids to their hosts; these compounds are quickly metabolized or built into coral tissue. A part of the energy gained from photosynthesis is also utilized to continuously translocate calcium- and bicarbonate ions to the calicoblastic layer, thereby creating a skeleton (see the coral science archive for more information). The skeleton mainly serves as a refuge to hide from potential predators, and as a means to attach the coral onto a substrate. Unfortunately, photosynthates alone are not sufficient to build animal tissue2,4-9. These elements are ingested by corals by removing particulate organic matter (plankton, detritus) from the water, and by absorbing dissolved molecules.  Heterotrophy is essential for all corals and can meet up to 100% of the daily required energy in corals which are bleached or inhabit deep or turbid waters1,12-18. Moreover, for azooxanthellate corals such as Dendronephthya sp. (a genus of soft corals) or Tubastrea sp. (a genus of stony corals), heterotrophy is the only means of nutrition. Recent findings indicate that the interaction between auto- and heterotrophy, in this case light and nutrition, is the key to high coral growth19.

"The photosynthates which zooxanthellae provide their hosts with can deliver up to 100% of the daily required energy for corals. This energy is in part utilized to continuously translocate calcium- and bicarbonate ions, thereby creating a skeleton."

A high diversity of nutritive sources

The ways in which corals feed are diverse; they receive photosynthates from their zooxanthellae, they take up countless elements such as nitrogen, phosphorus and calcium from the water and they catch plankton and detritus. Next, we will discuss these various sources in more detail.

- photosynthesis

The bulk of the energy budget for many corals is delivered by zooxanthellae photosynthesis. The conversion of inorganic CO2 to organic carbohydrates is a complex biochemical process, which can be split into two phases. Figure 3 depicts the main components schematically, which are called photosystem II/I and the Calvin cycle. The essence is that a pigment stored in the zooxanthellae, called chlorophyll, absorbs sunlight which activates an electron current. The energy provided by this electric current induces the production of carbohydrates. The same process occurs in seaweeds and higher plants.

Chlorophyll is a protein which is stored in the chloroplasts of the zooxanthellae; these are cellular organelles in which photosynthesis takes place. The chloroplasts themselves harbour even smaller structures called thylakoid bodies; these compartments eventually form the center of the reactions.  Here, water is split into oxygen and protons (acidic particles, denoted as H+). This first reaction can be summarized as follows:

2 H2O --> 4 H+ + O2 + 4 e-

PhotosynthesisAs this process requires light energy, it is called the light reaction. The released electrons eventually allow for the production of ATP (adenosine triphosphate) and NADPH (nicotinamide adenine dinucleotide phosphate). These molecules transfer the energy required to fuel to the Calvin cycle; a series of reactions which convert CO2 into carbohydrates. These are referred to as the dark reactions, as no light is required for this part of the process. They also occur during the day.

Figure 3: Simplified overview of the light reaction which takes place in the chloroplasts of the zooxanthellae. So-called thylakoid membranes form the center of the reaction. Light energy splits water into oxygen, causing a release of electrons. This generates ATP and NADPH, which provide the required energy for the Calvin cycle. This eventually converts CO2 into carbohydrates. In reality, all thylakoids in all of the chloroplasts take part in the process (© Benjamin Cummings).

When all photosynthetic processes are combined, the reaction becomes this:

6 CO2 + 6 H2O --> C6H12O6 + 6 O2

This reaction thus yields both carbohydrates and oxygen, which are subsequently partially transferred to the coral tissue. Both the algae and the corals burn these sugars, which provides the necessary energy. When this happens, the above reaction simply takes place in reverse order. For stony corals, this process delivers about 30-100% of the daily required energy, of which a large part is used to build a skeleton. Photosynthates, often deficient in nitrogen and phosphorus, are thought to be used as fuel for respiration, rather than assimilated into biomass1,5 .

Respiration causes a drop in aquarium pH at night from 8.2 to about 7.8, depending on stocking densities. Algae, seaweeds and higher plants also exhale CO2 at night. Sometimes, this causes mortality in aquaria or natural water bodies, especially during summer; this is because the warmer the water, the less oxygen it contains. A proper aeration of the aquarium is therefore required.

Sometimes, algae produce too much oxygen; this is harmful for all living cells, as a part of these molecules is converted into radicals. These are reactive molecules which contain extra electron pairs, which is why they love to interact with other substances. This causes DNA and cellular damage in the cell. Fortunately, corals have found a way to deal with this nuisance, by producing molecules called anti-oxidants. These bodyguards absorb dangerous radicals, thereby protecting the cells. They can also expel zooxanthellae which produce too much of these molecules. This eviction notice, which leads to coral bleaching, has two main causes: First, high levels of photosynthesis are a common culprit. This sometimes happens in the aquarium when we switch from T5 to metal halide lighting too quickly. This means it is important to allow corals to adapt slowly to new and stronger lighting.

Second, many coral species bleach at water temperatures of 30°C (86°F) or higher; this is because zooxanthellae are damaged at such high temperatures. The thylakoid membranes inside the chloroplasts simply fall apart, allowing many oxygen radicals to flood the coral tissue. This again triggers algae expulsion. Some zooxanthellae, however, are resistant to temperatures of up to 32°C (90°F), and this explains why some corals do not bleach during a hot summer (see archive).

After bleaching, corals have to reacquire their algae population in time, before they starve to death. Fortunately, this process is often successful. This also occurs in the aquarium, and this is possibly due to the reuptake of free-living zooxanthellae through the mouth and gastrovascular cavity. Many coral larvae also do this before they metamorphose into primary polyps (see archive). In addition, partially bleached corals simply regrow their remaining zooxanthellae.

Corals which inhabit deeper waters, or corals which have not formed a symbiotic relationship with algae, will have to acquire their energy through the uptake of plankton, particulate organic matter  and dissolved organic matter. This is exactly what has been found for these species8,64,65.

- dissolved organic matter (DOM)

Dissolved organic matter (DOM) forms an important food source for many corals and related animals such as Zoanthus sp. Already in 1960, scientists found that stony corals from the genus Fungia were able to take up radioactively labeled glucose from the water20. This was demonstrated by subsequent tissue analysis.

In science, DOM is often split into various elements such as DON (dissolved organic nitrogen) and DOC (dissolved organic carbon). Important examples are carbohydrates (DOC), amino acids (DON, often referred to as DFAA or dissolved free amino acids) and urea; as less poisonous variant of ammonia which is produced by many animals. All of these molecules are taken up by corals at even very low concentrations in the nanomolar range6,20-26. A nanomolar (nM) indicates 1 nanomole per liter of water. For nitrate, 1 nM converts into 0.06 microgram/l, which is only 0.06 ppb! Stylophora pistillata for example takes up various amino acids (fig. 4), and together they comprise about 21% of the nitrogen budget for this species26 (fig. 5). These values are likely in the same ranges for many other stony corals. This indicates the importance of aquarium supplements for nutrient-poor aquaria, which contain many coral colonies and few fish. These are mostly aquaria from the aquaculture industry, as most hobbyists tanks are densely stocked with fish.

Amind acid uptakeFigure 4: Uptake of 11 different amino acids (DFAA) by Stylophora pistillata (Renaud Grover et al, Journal of Experimental biology 2008).

It is intriguing that many corals also take up urea from the water, and they can do this in even greater quantities compared to nitrate (at least in nature). This indicates these animals may have adapted to the presence of higher animals on the reef, such as fish, which collectively produce large amounts of this nitrogen-rich compound on a daily basis27.

Scientists also found that urea, similar to amino acids, is more actively taken up during the day. These molecules may be important for building the organic matrix, the 'protein-scaffold' around which calcium carbonate is deposited. It was shown that this matrix is mainly produced at night, whereas calcification mainly takes place during the day34 (see archive). The organic matrix helps the formation of aragonite crystals, increasing both the density and strength of the coral skeleton35-37.

Nitrogen budgetFigure 5: Nitrogen budget for Stylophora pistillata colonies in their natural environment. It is clear that ammonia and nitrate provide the bulk of the nitrogen, and that organic nitrogen in the form of amino acids provides 21%. The balance between dissolved molecules and particles such as plankton however depends on what is available to the coral (Renaud Grover et al, Journal of Experimental biology 2008). 

Aquarists often notice polyp expansion after feeding plankton or 'boosters' which contain plenty dissolved organics. This is because corals, similar to humans, are probably capable of tasting food which is present in the water. Just like the human tongue has receptors to detect many substances, so too may corals have evolved receptors which recognize amino acids.

Adding amino acids such as glycine, alanine or glutamate to the water results in reactions such as polyp extension, swelling of common tissue ( coenenchyme) and on occasion the extrusion of the gut wall (or gastrovascular cavity)23,28. This mechanism possibly serves to detect zooplankton, which allows for more efficient capture of prey. Corals may also recognize neighbouring colonies, which they sometimes attack by literally throwing their stomachs onto them, after which the target is slowly digested.

"Aquarists often notice polyp expansion after feeding plankton or 'boosters' which contain plenty dissolved organics. This is because corals, just like humans, are capable of tasting food which is present in the water."

- dissolved inorganic matter (DIM)

The uptake of inorganic matter by corals encompasses macro-elements such as calcium, magnesium, bicarbonates and potassium, gases such as oxygen and carbon dioxide, and trace elements. Macro-elements largely play a role in calcification, and are added to the aquarium by means of calcium hydroxide (Ca(OH)2, also called kalkwasser), the Balling-method or a calcium reactor.

Trace elements are available in seawater only in minute concentrations, hence their name. Examples are iodine (50 ppb), nitrogen (300 ppb, nitrate is a part of this), phosphorus (phosphate is a part of this), halogens such as fluorine (1 ppm) and metals such as iron (10 ppb), zinc (10 ppb) and aluminum (10 ppb). Table 1 gives an overview of the most common elements present in marine water.

"Copper, chromium and zinc are highly toxic to life, and this holds especially true for invertebrates. These animals, mainly corals and anemones, have not evolved efficient ways of dealing with these molecules."

Manufacturers of aquarium supplements have tapped into this knowledge over the years, and this has led to a variety of available products. Adding metals, for example, supposedly augments the blue and green colouration of stony corals. Although evidence is limited regarding this (Heliopora coerulea is an exception to this rule), metals do have key functions for all life on earth. Many enzymes, proteins which catalyze chemical reactions allowing life to persist, have metal cores. Without these, they simply cannot function42-44. A nice example is the enzyme carbonic anhydrase, which catalyzes the conversion of CO2 to bicarbonate ions. This process is essential for building the coral skeleton (see archive). This enzyme contains a core of zinc; without sufficient ingestion of this metal, stony corals would not be able to photosynthesize and grow properly76.

Table 1: An overview of the main elements present in natural seawater. Concentrations are represented in ppt (parts-per-thousand, g/l), ppm (parts-per-million, mg/l) and ppb (parts-per-billion, μg/l). Sulphate and bicarbonate are not elements, but rather molecules which consist of different elements (or atoms). As they play important roles in oceanic biological processes they have been included in the table (source: www.invista.com).

element

ppt

element

ppm

element

ppb

oxygen (O)

857.8

bromine (Br)

65  

nitrogen (N)

300

hydrogen (H)

107.2

strontium (Sr)

8

lithium (Li)

170

chlorine (Cl)

18.98

boron (B)

4

phosphorus (P)

70

sodium (Na)

10.556

silicon (Si)

3

iodine (I)

50

sulphate (SO42-)

2.649

fluorine (F)

1

zinc (Zi)

10

magnesium (Mg)

1.272

 

 

iron (Fe)

10

calcium (Ca)

0.4

 

 

aluminum (Al)

10

potassium (K)

0.38

 

 

manganese (Mn)

2

bicarbonate (HCO3-)

0.14

 

 

lead (Pb)

0.04

 

 

 

 

mercury (Hg)

0.03

 

 

 

 

gold (Au)

0.000004

 

Table 1 shows that metals truly are trace elements, which is why supplementing them to the aquarium should be done with care. Metals such as copper, chromium and zinc are highly toxic to life, and this holds especially true for invertebrates. These animals, mainly corals and anemones, have not evolved efficient ways of dealing with these molecules. Higher animals have evolved a liver and kidneys, which together quickly dispose of toxins through the urine and feces. Corals and their relatives are highly dependent on external water concentrations, and can only pump in or out molecules to some extent.

It is also clear that metals can be bound by organic molecules such as metallothionins; these proteins actively bind to metals rendering them harmless. This allows transport of these molecules through the bodies of countless organisms. This process is called chelation, and the involved organic molecule is called the chelator. It takes place in bacteria, algae and numerous animal species. Bacteria and algae also secrete these molecules into the water, thereby neutralizing metals for safe uptake. It has also been shown by some aquarists that corals do not incorporate heavy metals into their skeletons to such an extent as would be expected based on water concentrations46. Even at high metal concentrations, skeletal contents of aquarium corals often show a deficit in metal composition compared to wild specimens. This indicates many metals in the aquarium are not biologically available. Either way, supplementing heavy metals should be done with care.

"Phosphates possibly inhibit the buildup of the coral skeleton, by binding to the growing crystal lattice. Coralline algae, which also calcify, show a decrease in growth at higher phosphate levels."

Phosphorus also is a widely discussed element, often causing problems in aquaria. As orthophosphate, PO43-, it regularly causes overgrowth of algae, cyanobacteria and coral mortality. Most aquarists are very much aware phosphates can be dangerous to aquarium life, and manufacturers have adapted to this by producing many phosphate-lowering products. Iron- and aluminum-based substrates have been known to bind phosphates for years, and this principle is perfectly applicable to aquaria.

There still is some controversy about the direct harmful effects of phosphate; it seems that predominantly stony corals are affected by this. Soft corals and gorgonians have been reported to grow at concentrations as high as 5 mg/l!59 Phosphates possibly inhibit the buildup of the coral skeleton, by binding to the growing crystal lattice. Coralline algae, which also calcify, show a decrease in growth at higher phosphate levels. Phosphates also cause negative indirect effects on marine animals by stimulating algal and bacterial growth62,63.

- particulate organic matter (POM)

This group of particles usually describes detritus; the small remnants of feces and decayed organisms. In the aquarium, food which is not consumed and removed also becomes detritus. Detritus eventually precipitates on the ocean floor or aquarium bottom as sediment. This layer of organic material is partially degraded by bacteria, and converted into inorganic molecules such as nitrate and phosphate. This process is called mineralization.

The sediment which is present on coral reefs contains bacteria, protozoa and their excrements, microscopic invertebrates, microalgae and organics29. These sedimentary sources can all serve as coral nutrients, especially for colonies which grow in turbid waters15,30. Experiments during which sedimentary carbon was radioactively labeled showed that corals such as Fungia horrida and Acropora millepora readily took up sediment31,32. The more sediment present, the more uptake is measured; 50-80% of this material is converted into biomass by several species. This has also been found for the Caribbean species Montastrea franksi, Diploria strigosa and Madracis mirabilis; detritus is taken up by the polyps, and the available nitrogen is converted into biomass.

It must be noted however that too much sediment which precipitates on the corals can be disastrous; reefs have disappeared in many bays inhabited by humans because of this. This is caused by the upwelling of soil sediments by tourists or boats, or by the presence of fish farms. This phenomenon can be seen in the Gulf of Aqaba (Red Sea), where the reef stops as soon as densely populated areas are reached. High sedimentation literally suffocates the reef by blocking light, food uptake and gas exchange.

Aquarium displaying suspension feeders

Figure 6: A Dutch aquarium which is enriched in detritus and plankton due to heavy feeding. Because of this, this aquarium also harbours increased populations of benthic crustaceans such as amphipods, which inhabit the live rock. By feeding phyto- and zooplankton, or an artificial feed such as Reef Pearls, a somewhat natural nutrient cycle can be created. The resulting amphipods and other small invertebrates are an important food source for e.g. dragonets (Synchiropus sp.). The available particles are essential to the animals present, which include Menella gorgonians, Dendronephthya sp., Scleronephthya sp., stony corals such as Tubastrea coccinea and Rhizotrochus typus, sponges and tunicates. The 'dirty' aquarium, which allows more animals to thrive, is becoming a new hype in the marine hobby. The ultimate trick remains the availability of particles whilst ensuring high water quality (low ammonia, nitrate and phosphate levels, photographs: Pieter van Suylekom).

"The sediment which is present on coral reefs contains bacteria, protozoa and their excrements, microscopic invertebrates, microalgae and organics. These sedimentary sources can all serve as coral nutrients, especially for colonies which grow in turbid waters."

- plankton

This group is sometimes regarded as the living component of POM. The term plankton is a common name for an astoundingly large group of organisms which can be categorized in different ways. Figure 7 shows a commonly accepted division into pico-, nano-, micro- and mesoplankton. These groups consist of (cyano)bacteria and protozoa (picoplankton), algae and protozoa (nanoplankton), microscopic crustaceans such as rotifers and large protozoa (microplankton) and countless other species of crustaceans (mesoplankton). Fish and invertebrate larvae can further be categorized into micro- and mesoplankton, depending on the species.

Overview plankton

Figure 7: Plankton size classes: picoplankton, nanoplankton, microplankton and mesozooplankton included in the diet of scleractinian corals. (A, B) Scanning electron micrographs of (A) Prochloroccocus sp. (0.6 μm) and (B) Synechococcus sp. (1 μm). (C) Epifluorescence microscope image showing one nanoflagellate cell indicated by a yellow arrow. Image of (D) ciliates (mean total length is 100 – 200 μm) taken under a phase contrast microscope and (E) crab zoea (mean total length is 1000 μm) (Houlbrèque & Ferrier-Pagès, Biological Reviews, 2009).

Plankton was not considered as an important coral food source for many years; it was believed concentrations on the reef were too low to have any significant effect. In the meantime, more accurate estimations have been made, based on improved measuring techniques39. These values are particularly high during summers, which is probably due to the abundance of phytoplankton. This leads to increased concentrations of zooplankton, as they feed on the extra available phytoplankton.

Astroides calycularisFigure 8: Astroides calycularis, a Mediterranean azooxanthellate coral species. For corals within this group, catching plankton is a crucial means of survival (photograph: Jean-Louis Teyssié, IAEA Monaco).

The amount of available plankton not only fluctuates during the year, but also during the day. Zooplankton consists of actively swimming animals, which constantly migrate between the reef and the water column. During sunset, the free zooplankton concentration rises quickly, as these animals migrate to the water column. This causes a rise in copepod (500-700 μm) concentration which is five times higher compared to daytime levels!36-38

For other small invertebrates, this nocturnal concentration quadruples. Many larvae of animals such as tunicates and polychaetes larger than 700 microns also appear. When the aquarium is viewed at night by using a flashlight, this phenomenon can also be seen. Unfortunately, this nocturnal festivity is somewhat ruined by the presence of a protein skimmer, which cannot tell the difference between what is useful and what is not.

The nightly migration of plankton also explains why most stony corals mainly expand their polyps at night, as more prey can be caught during this time. This strategy also protects the polyps against predation from fish and other animals during the day. Nowadays, many aquarists have found that corals are able to adapt to a change in food availability; a nice example is Tubastrea coccinea, which learns to expand its tentacles during the day and even seems to anticipate feedings.

"Plankton was not considered as an important coral food source for many years; it was believed concentrations on the reef were too low to have any significant effect. In the meantime, more accurate estimations have been made, based on improved measuring techniques".

In the Gulf of Aqaba, the tentacles of massive coral species such as Favites sp., Favia favus and Platygyra daedalea expand 15-45 minutes after sunset. After 70 minutes, full expansion is reached36. Many corals also expand during the day, such as most species of Porites39 and numerous soft corals.

View at gulf of Aqaba Figure 9: On the reef, such as in the Gulf of Aqaba, Red Sea, a high concentration of phytoplankton is present. This can be clearly seen by the green haze in the water (photograph: Tim Wijgerde).

The uptake of particles by corals depends on many factors, such as prey type and concentration, irradiance, colony and polyp morphology, and water flow velocity. Especially this last aspect has become a popular point of discussion amongst aquarists, as the husbandry of azooxanthellate corals is becoming increasingly popular. Research indicates that many of these corals are quite limited in their capacity to catch particles various water flow speeds. A good example are the colourful Dendronephthya's, which often do not last long in aquaria. They most efficiently catch phytoplankton at flow speeds between 12,5 and 17,5 cm/s. This has been demonstrated by determining the amount of accumulated chlorophyll inside of the polyps at various flow speeds. This value is a measure for the amount of ingested phytoplankton, as algae are rich in this protein. These results also correlated well with the increase in colony polyp number; this value was about 7% per day! This means these corals can grow quite fast if supplied with ample nutrition, which forms a striking contrast with the meager results obtained so far in aquaria.

"The nightly migration of zooplankton explains why most stony corals expand their polyps at night, as more prey can be caught during this time."

Next to azooxanthellate soft corals, some gorgonians are also quite picky about water current; in 1993, Taiwanese biologists found that the gorgonians Subergorgia suberosa, Melithaea ochracea and Acanthogorgia vegae displayed large differences in capture rate at different flow speeds51. Figure 10 shows that mainly Subergorgia suberosa has adapted to a very constant water flow. This is indicative for the environment which this species inhabits. The scientists hypothesized this result was due to its polyp morphology; because of their length, they were subject to increased flow resistance which caused them to deform quickly at higher flow speeds. This made it difficult for the polyps to catch particles. Melithaea ochracea has much shorter polyps which makes this species much more flexible. The biologists also think a balance exists between the amount of expended energy and that which is received from ingested prey. This is likely another factor which determines the maximum speeds at which plankton can be caught.

Interestingly, soft corals from the genus Dendronephthya have evolved large spicules, which are found in the body column and around polyps. These seem to function in holding the body column and polyps erect in strong water currents, allowing the corals to strain phytoplankton effectively from the passing waters. Their polyps also increase in size as water velocity increases7. Finally, polyp reaction time may also be limiting capture rates at higher flow speeds. 

Feeding behaviour vegae

Figure 10: A series of drawings depicting the feeding behaviour of Acanthogorgia vegae, based on video recordings. Both polyp reaction time and morphology may determine the maximum flow speeds at which plankton can be caught (Lin et al, Zoological Studies, 2002).

Not only water flow speed, but also the orientation of coral colonies may influence feeding efficiency. Many gorgonians which grow in large fan-shapes, such as Gorgonia ventalina and Leptogorgia sp., do so perpendicular to water currents. This allows them to catch plankton from the water more efficiently50. If aquarists are determined to keep such species successfully, they should consider building a custom aquarium which respects colony orientation, (the absence of) lighting, water current, nutrition and water quality. Herein lie of course new challenges.

Flow-dependent capture rateFigure 11: Certain coral species such as Subergorgia suberosa are difficult to keep alive because of high demands to their environment. Only around a water current of 8 cm/s, this species is able to properly ingest plankton (Dai & Lin, JEMBE, 1993).

According to a study from the seventies, colony shape is supposedly important as well; the higher the ratio between colony surface area and volume, the more efficient particle capture. Later studies have challenged this view; Pocillopora damicornis, Pavona cactus and P. gigantea are able to catch more plankton when this ratio decreases53. Polyp capture efficiency was also found to be independent of polyp size for these species.

"Many gorgonians which grow in large fan-shapes, such as Gorgonia ventalina and Leptogorgia sp., do so perpendicularly to water currents. This allows them to catch plankton from the water more efficiently."

Other branched SPS corals are however capable of catching more zooplankton per unit of weight compared to species with larger polyps38. It seems that polyp size is not a solid predictor of capture efficiency, but rather determines maximum prey size.

It has also been found that ratio's between different components of zooplankton are not necessarily accurate predictors of what corals mainly feed on. This is often quite species-specific. The species Pocillopora damicornis and Pavona gigantea which inhabit the Gulf of Panama were found to mainly feed on isopods, amphipods and crab zoea (200-400 μm), despite the fact that 61% of the available plankton consisted of copepods66. This is likely due to the fact that these crustaceans, such as Oithona sp., are much harder to catch. These animals swim quite quickly and powerful, making it hard to hold on to them. Nowadays, aquarium products containing dried copepods exist, such as Cyclop Eeze®. These are probably ingested more efficiently.

Although not all prey animals are caught equally effective, coral polyps are not too bad at fishing. Individual polyps of the Atlantic species Madracis mirabilis and Montastrea cavernosa are able to capture and ingest 0.5 to 2 prey per hour37. On a colony level, these numbers get big pretty quickly. A small Seriatopora colony of 14 ml in volume is able to capture 10,000 Artemia in 15 minutes!38 This however requires very high aquarium zooplankton concentrations of 10,000 to 20,000 Artemia per liter.

Other results show that an aquarium concentration of 2000 nauplii/l (about 500 nauplii /gallon) is ideal for stony corals such as Pocillopora damicornis38. To reach this concentration, it will take a daily amount of one million nauplii for the average 500 l (130 USG) aquarium. When culturing Artemia with a starting dose of 30 g/l (1 oz/33 fl. oz), concentrations of one million nauplii per liter are easily obtained. A daily dosage of one liter (34 fl. oz) on such an aquarium is quite a lot, and this depends on the amount of biomass present. For the average aquarium of this size, filled with stony corals, 200 ml (7 fl. oz) is a guideline. The fish however will consume quite a lot of this food; it remains difficult to translate laboratory tests to the average household aquarium. For these aquaria, of which about two million worldwide exist according to estimations, the optimal dosage will have to be found by experimentation. Feeding at night is also recommended, as many stony corals will have their tentacles expanded and will respond more vigorously.

"Coral polyps are not too bad at fishing; a small Seriatopora colony is able to capture 10,000 Artemia in 15 minutes!"

Next to the fish, protein skimmers also are voracious particle predators. All forms of mechanical filtration will decrease available nutrients, unfortunately. Without this filtration however, water quality declines quickly. Water changes, phosphate reactors, refugia with Chaetomorpha macro algae and denitrification reactors all work well to allow plankton populations to persist, however these are often quite labour intensive. Keeping many organisms in a small aquarium, be it corals or fish, simply degrades water quality quicky. In nature, the ratio between biomass to water volume is much lower. Next to this, many waste products are quickly converted into new biomass such as plankton and sponges. This also occurs in the aquarium, to some extent, however this does not outweigh the amount of nutrients which is introduced on a daily basis. Moreover, benthic algae start growing easily, which will outcompete corals if herbivores are not present in sufficient numbers. This phenomenon also seems to affect some reefs, on which too many herbivores such as surgeon fish have been collected.

A Dendronephthya sp.

Figure 12: Corals from the Nephtheidae family are true suspension feeders; with their finely branched tentacles they mainly capture phytoplankton (photograph: Pieter van Suylekom).

There has been much debate about how selective corals are about their diets, especially regarding phyto- and zooplankton. Various studies show that stony corals predominantly feed on zooplankton, and that soft corals are mostly herbivores. Gorgonians seem to have placed themselves somewhere in the middle of this spectrum, with a tendency towards zooplankton. New research indicates that stony corals such as Pocillopora damicornis do not grow well on phytoplankton, such as Nannochloropsis oculata73. Other pelagic phytoplankton such as Tetraselmis sp. may yield better results. Conversely, Artemia and rotifers gave much better results with this species74.

Various studies indicate that soft corals mainly feed on phytoplankton. Many species display so-called pinnula; these are the finely branched structures which provide polyp tentacles with a feather-like appearance. A nice example is Xenia umbellata, although it seems this species has lost its polyp mouths in evolution74, which are now rudimentary. Pinnula of Dendronephthya colonies are interspersed at 60-80 μm intervals (a bacteria is about 2 μm), which is adequate to capture phytoplankton. Furthermore, plant-digesting enzymes have been found in three soft coral species from the genus Alcyonium; amylase  and laminarinase, in contrast to stony corals47. Finally, many soft corals and gorgonians only display small and ineffective nematocytes, unlike their stony coral relatives48. As an example, touching Cynarina's, Trachyphyllia's, Favia's and Acanthastrea's sometimes leads to skin irritation. For D. hemprichi, it was found that particles larger than 750 μm were not successfully caught. After an average of 50 seconds, zooplankters escaped from its tentacles. Even after three attempts, zooplankton did not show signs of paralysis47. These observations indicate that at least some soft coral species are not well adapted to catching actively swimming particles such as zooplankton. As most aquaria nowadays are stocked with both soft and stony corals, dosing different types of plankton is recommended.

"Captured particles are eventually ingested through the oral pore, by means of flagella or cilia. These hair-like appendages propel the food into the mouth and through the pharynx, after which it ends up in the gastric cavity."

The uptake of pico- and nanoplankton by corals is difficult to determine, as these are quickly degraded. Bacteria and protozoa do have been found in coral digestive cavities, and these microbes play an important role in the marine food chain. In terms of biomass and photosynthesis, these organisms form the most important part of pelagic plankton52-54. On the reef, bacterial concentrations sometimes lie around one million per milliliter! For cyanobacteria, the number fluctuates around 10.000-100.000 per ml and for flagellates around 10.000 per ml. As these microbes grow fast, they are highly important for the nitrogen and carbon cycles in the ocean. For the model species Stylophora pistillata, if has been found that digesting microbes yields almost three times as much nitrogen as ammonia, nitrate and amino acids together (figure 13). This of course depends on availability. Research on Favia favus and Fungia granulosa showed that the highest concentrations of micro-organisms were found around the mouth area, supporting the idea they are consumed by various species57.

Nitrogen budget Stylophora pistillata

Figure 13: Daily nitrogen budget for Stylophora pistillata. For these estimations, scientists took an average of 50 polyps per cm2. When this species is fed with natural zooplankton at a concentration of 1500 prey/l, this provides the coral with 1.8 μg nitrogen/cm2/day.  The uptake of pico- and nanoplankton provides up to 1.4 μg N/cm2/day. Dissolved organic nitrogen, at the lowest concentrations found in seawater, contributes 0.5 μg N/cm2/day. In total, this yields 3.7 μg N/cm2/day. Although these values may fluctuate under various conditions, they provide a unique insight into the balance between different nutrient sources. Plankton may deliver over six times the amount of nitrogen compared to dissolved organic nitrogen (Houlbrèque & Ferrier-Pagès, Biological Reviews, 2009).

"The uptake of non-visible particles may be an explanation for the 'mysterious' success of Goniopora and Alveopora corals in plankton-rich aquaria."

The uptake of small particles is stimulated by mucus production58; nowadays, products are available which are based on this principle, although results remain sparse. By means of polymer-mediated adhesion, various types of plankton can be bound which could stimulate their uptake by coral polyps. Detritus and larger plankton may also be more effectively captured by mucus. Additionally, bacteria thrive in this slimy secretion; the bacterial density of mucus has been found to be four times that of seawater58.

Captured particles are eventually ingested through the oral pore, by means of  flagella, cilia and mucus embedding. Flagella and cilia are hair-like appendages which are localised on epidermal cells. They transport particles to the mouth and pharynx, after which it ends up in the gastric cavity. This process likely takes place in most corals, and this can be clearly seen when Fungia mushroom corals are fed with Mysis or Artemia. The uptake of non-visible particles may be an explanation for the 'mysterious' success of Goniopora and Alveopora corals in plankton-rich aquaria.

The dynamic balance between light and nutrition

Some corals are able to shift the balance between energy gained from photosynthesis, particles and dissolved molecules when required15,30. Specimens which inhabit deeper waters receive less light, and bleached or azooxanthellate corals have to gain energy from other sources than photosynthesis. Montipora capitata colonies have been found to increase their plankton feeding rates after bleaching, which completely satisfies their daily metabolic requirements12 (table 2).

Table 2: Average feeding rates of several coral species under bleached and non-bleached conditions. Bleached Montipora capitata colonies increased their feeding rates, which allowed them to sustain their energy reserves. After induced bleaching, M. capitata fragments captured about six times more zooplankton compared to control colonies. Porites sp. do not seem to have evolved this adaptation, as changes in feeding rates were not statistically significant. Average feeding rates equal zooplankton particles caught per gram of coral per hour (Grottoli et al, Nature, 2006).

 

Average feeding rates

 

                                         

control

bleached

Porites compressa

12.8

10.9

Porites lobata

18.8

20.6

Montipora capitata

5.7

32.6

The increase in M. capitata feeding rates allowed these corals to sustain their lipid and carbohydrate reserves, which may permit them to continue to reproduce annually. Bleached corals are known to lose their ability to reproduce (also called a decrease in fecundity) for about 2 years. This recovery period can deteriorate reefs, as less offspring is produced. The ability of M. capitata to maintain its health status by increasing zooplankton feeding, in contrast to corals such as Porites sp., may lead to decreased biodiversity in the future. Corals which are able to feed more when times get tough are more likely to survive in the end. Others might disappear when the oceans get warmer.

Species-specific adaptation has also been found for Goniastrea reniformis and Porites cylindrica. During an experiment, these species were subjected to either detritus and ample lighting, or detritus and shade. After prolonged exposure to a shady environment G. reniformis more than doubled its feeding rate, which allowed it to grow at a normal rate. P. cylindrica was not able to compensate for its loss of zooxanthellae carbon input, as it did not increase its feeding rate sufficiently.

The synergistic effects of light and nutrition on coral physiology

The positive effects of nutrition on corals are profound; essential processes such as photosynthesis, calcification and the buildup of the organic matrix are stimulated by feeding (fig.14). Plankton supplementation is thus useful, but how does it actually work?

- nutrition and photosynthesis

Although it may seem that feeding and photosynthesis are two separate processes, these are in fact intricately linked. Nutrient exchange between corals and symbiotic algae is diverse, and this is increased by extra light and feeding. More feeding stimulates zooxanthellae growth and buildup of pigments such as chlorophyll77-79. This makes the coral a more effective 'solar cell', which is able to convert more light into chemical energy. This benefits both the coral and the algae. It has become clear from CORALZOO-experiments corals grow less than expected under high intensity lighting (irradiance of 500 μE/m2/s, which is reached when corals grow very close to high-power T5 fluorescent bulbs, see archive). This is most likely due to other limiting factors which serve as building blocks; French scientists found that this limitation can be reduced by providing extra nutrition in the form of zooplankton70,71. This in fact occurs in nature as well, mostly during summers, when ample light and zooplankton particles are available. This situation can be simulated in the aquarium as well, by providing extra plankton in combination with T5 or metal halide lighting. Zooxanthellae also produce extra amino acids as a result of this, next to glycerol and glucose. A part of this is again transferred to the coral host tissue72,73.

- nutrition and calcification

Various mechanisms mediate the positive effects of nutrition on coral skeleton buildup, however this seems to take somewhat longer compared to increases in tissue growth69-71. After eight weeks of zooplankton feeding (such as Artemia nauplii), calcification rates of Stylophora pistillata doubled (figure 14). As tissues grew faster compared to skeleton, this led to fleshier corals. When these corals received less light, a decline in growth rate could be prevented by providing additional plankton. This fact is interesting for aquarists who do not want to make use of heavy lighting above the aquarium, for obvious reasons.

How does feeding with e.g. zooplankton stimulate calcification? First, increases in coral tissue due to extra feeding lead to the production of more metabolic CO2. Corals acquire 75% of their dissolved inorganic carbon from metabolism, and only 25% from the water column;  more CO2 leads to higher bicarbonate production, which may provide more building blocks for synthesizing the coral skeleton (see archive). Second, more nutrition provides more energy, also indirectly by increased photosynthetic capacity, which allows more calcium ions to be transported to the growing skeleton.

It was also found that the incorporation of aspartic acid (an amino acid) into the organic matrix about doubled after feeding. Aspartic acid is a major component of the organic matrix, and its buildup also increased twofold at night and by 60% during the day after additional feeding (figure 14). This matrix is mainly synthesized during daytime, and is of vital importance for depositing the skeleton as it plays a major role in the regulation of aragonite crystal formation.

"When corals receive less light, a decline in growth rate can be prevented by providing additional plankton. This fact is interesting for aquarists who do not want to make use of heavy lighting above the aquarium."

- nutrition and coral tissue

The effects of light and feeding

Coral feeding quickly leads to increased tissue production and protein concentration (figure 14)67,68. This increase was about 2-8x for Stylophora pistillata after three weeks of zooplankton feeding!69-71. Next to proteins, lipid content also increased. Both saturated and unsaturated fatty acids increased in Galaxea fascicularis tissue after feeding with Artemia nauplii68. More light actually decreased tissue fat contents. Although this seems contradictory, these corals probably invested more fatty acids into growth and zooxanthellae production to enhance usage of extra light. 

Figure 14: An overview of the studies discussed in this article, which shows the diverse effects of feeding on coral physiology. Fed corals display (1) twofold greater protein concentrations and photosynthetic rates per unit skeletal surface area; (2) twofold higher dark and light calcification rates; (3) twofold greater organic matrix synthesis in the dark and a 60% increase during daytime (Dubinsky et al., 1990; Witting, 1999; Titlyanov et al., 2000a,b, 2001; Ferrier-Pagès et al., 2003; Houlbrèque et al., 2003, 2004a).

For S. pistillata, zooxanthellae tissue concentrations doubled within several weeks of zooplankton feeding, both at low and high light levels. This also applied to the number of algae residing in a single host cell; even coral cells with four algae increased in number (from 0.4% to 0.7% of the cell population). Chlorophyll a and c2, which are used for photosynthesis, also increased in concentration.

As proteins, fatty acids as well as chlorophyll increase in concentrations, this indicates that both the coral host as the symbiotic algae profit from plankton uptake. Chlorophyll increase may also be reached by adding inorganic nitrogen such as nitrate to the aquarium; this is the reason why corals turn brown in nutrient-rich aquaria.

Concluding remarks

During the last decades, it has become increasingly clear to biologists that food sources other than photosynthesis are essential to many coral species. Although photosynthesis provides the 'junk food' for zooxanthellate corals, and allows for the creation of vast coral reefs, other building blocks are required. In addition, extra building blocks increase a coral's capacity  to harness the sun's energy, by stimulating zooxanthellae growth and chlorophyll buildup. During times of coral bleaching, the reefs may be saved by the presence of alternative energy sources such as zooplankton, until algae tissue populations have been restored. Furthermore, many (soft) corals and gorgonians have not formed a symbiotic relationship with Symbiodinium algae, which makes heterotrophy necessary.

"Major differences exist between the fastest growing coral and the most attractive one. Aquarists favour bright colours, which arise due to coral host pigmentation."

These insights are of major importance to coral aquaculture, and allow for optimal coral husbandry. Light, dissolved matter such as amino acids, and plankton; together, these can greatly stimulate coral growth.

The effects of nutrtion on Pocillopora damicornis

Figure 15: Which coral wins the beauty contest? Increased feeding of stony corals such as Pocillopora damicornis leads to increased zooxanthellae density, pigmentation and growth. These fragments were fed every other day with fish powder, varying from 0 to 0.5 grams (photograph: Dr. Shai Shafir, Red Sea Corals Ltd., Israel).

It must be noted that major differences exist between the fastest growing coral, and the most attractive one (figure 15). Most aquarists favor bright colours, which arise by coral host pigmentation. Brown zooxanthellate pigments such as chlorophyll are considered to be unattractive. These last pigments do provide the energy for increased growth, in contrast to brightly coloured pigments which act as sunscreens. Producing them also goes at the expense of coral growth.

In both nature and aquaria, we find both colour variations for many corals. The question remains which is more important; growth or looks? A solution to this problem might be to rear corals under ideal conditions, followed by an acclimation phase of decreased nutrients and high irradiance levels. This last phase stimulates colour intensity and therefore coral aesthetic value. Of course, water quality has to be controlled at all times; high particle concentrations and low phosphate levels seem to be the ideal combination.

This information is also useful for the home aquarium; using strong lighting has always prevailed over additional coral feeding, which might not be the best approach. It is often said corals require light, and the fish require feeding; now we know that our corals also benefit from this last source. Even though we may not be able to see corals taking up amino acids, protozoa and detritus; this indeed does occur. Although the discussed results have shown different coral species respond differently to provided food sources, one very important conclusion can be drawn; fed corals are happy corals. "My corals don't eat" is a statement you won't make that easily anymore after having read this article..

An Egyptian coral reef

Figure 16: In the wild, coral reefs are not only exposed to strong irradiance, they also receive ample nutrition from the available plankton and detritus. The interaction between light and feeding, in combination with high water quality, is the key to high coral growth (photograph: Leo Roest).

We thank Dr. Fanny Houlbrèque (International Atomic Energy Agency, Monaco) and Dr. Christine Ferrier-Pagès (Centre Scientifique de Monaco), two experts on coral physiology and nutrition, for their support.

Proud sponsor:

Coral-shop

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Preliminary CORALZOO-results (Dr. Sylvia Lavorano, Acquario di Genova), in preparation

Prof.Dr. Baruch Rinkevich, IOLR, personal communication

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