We usually think of coral reefs as the diver’s gardens of Eden in the warm and sunlit shallow waters of the tropics. However, there are other coral reefs that mostly escape the reach of the ordinary scuba diver—cold-water reefs. They thrive in the ocean’s bathyal zone along the continental margins. Like their tropical counterparts, these reefs are built by stony corals (Scleractinia) and harbour a stunning array of marine life. Unfortunately, these enigmatic deep reefs are also threatened by human impacts. 

Reefs beyond reach

There are actually more species of deep-sea than of shallow-water corals (29), but only six coral species are involved in the formation of cold-water reefs: Lophelia pertusa, Madrepora oculata, Goniocorella dumosa, Oculina varicosa, Enallopsammia profunda and Solenosmilia variabilis (14). The main contributors to this buildup are L. pertusa and M. oculata, the former being also the best studied cold-water coral species today. Therefore, this article will focus mainly on L. pertusa (order Scleractinia, family Caryophylliidae).

Figure 1: Red and white colonies of L. pertusa with associated sponges on a cold-water coral reef off Norway (photograph: C. Dullo, IFM-GEOMAR).

Lophelia pertusa

The name Lophelia pertusa is derived from the Greek lophos (crest) and helios (sun), and the Latin word pertusus (perforated), alluding to the sun-like appearance of the polyp with its many tentacles and prominent mouth. Norwegian fishermen call the animal ‘glass coral’ or ‘white coral’ (10). In the scientific literature, it is commonly referred to as a ‘deep-water’ or ‘deep-sea’ coral. In fact, the species is found at a global mean depth of 480 m (6), and even down to 3,000 m (31), but it does not live exclusively in the deep ocean. Its distribution is predominantly defined by temperature (4 to 12°C; preferred range, 6 to 8°C). Thus, the term ‘deep-water’ rather describes the coral’s preference to thrive at greater water depths, where temperature is usually low. L. pertusa also inhabits shallow waters, namely in Norwegian fjords: In one location in the Trondheimsfjord, the coral is found at only 39 m (16), and this is because water is quite cold there even at relatively shallow depths. Thus, it is more appropriate to call this species a ‘cold-water’ coral.

"Lophelia pertusa can live for almost 400 years, and this longevity allows the coral to build colonies up to 1.5 m in height."

The coral occurs in two colour varieties, white and red (32) (Fig. 1). Except for their different colouring, the two varieties look similar and also grow in direct vicinity where they occur together. However, the two colour morphs differ in their distribution: The white colour variety occurs more frequently along the North-East Atlantic continental margin than the red one. cold-water reefs along the southern and central parts of this margin comprise exclusively white L. pertusa. The question whether L. pertusa represents in fact two species of different colour is still unanswered.

The coral prefers regions of high biological production and vigorous currents (30). It is thought to feed primarily on zooplankton (19), but also on dead organic particles that are exported from the euphotic zone or transported laterally by the current (9). Unlike tropical corals, L. pertusa has no symbiotic algae that could help the animal to build up its skeleton. Because of this, L. pertusa is slow-growing (5.5 to 25 mm·yr^-1) (11, 25) compared to branching warm-water corals (100 to 200 mm·yr^‑1) (2). However, the coral can live for almost 400 years, and this longevity allows L. pertusa to build colonies up to 1.5 m in height (35). The colonies form thickets, the tightness of which is enhanced by frequent anastomosis of individual branches.

Only the last few centimeters of a Lophelia colony branch are covered by living tissue. Below that, the exposed coral skeleton is subject to bioerosion by bacteria, fungi, bryozoans, foraminifera, and boring sponges (1). Eventually, the riddled thickets collapse and contribute to a growing pile of coral rubble that forms the substrate for further coral growth. Furthermore, the coral framework acts as a trap for drifting sediment particles. In that way, the cold-water reefs slowly grow upwards, which can result in the formation of so-called carbonate mounds reaching heights up to 200 m above the sea floor (7).

Figure 2: Global distribution of known cold-water coral reefs (red), predictive distribution of L. pertusa (orange, very likely occurrence; yellow, conceivable occurrence), and distribution of warm-water reefs (magenta). Source: World Conservation Monitoring Centre of the United Nations Environment Programme (UNEP-WCMC). The map was modified graphically after compilation with the UNEP-WCMC IMapS tool.

Today’s Lophelia reefs developed after the last ice age over periods of 1,000 to 10,000 years (30). The largest reef complex is the Røst reef off Northern Norway, extending over 100 km² (33). Although these Lophelia reefs are often discontinuous patches and banks rather than large continuous structures such as the Great Barrier Reef or the Belize Barrier Reef, their overall area exceeds by far the extent of all tropical coral reefs (12) (Fig. 2). The continental margins of Europe and Africa are hemmed by a girdle of Lophelia reefs extending over 7,000 km, from the North Cape to the Canaries. Albeit L. pertusa is known to science for over 250 years (22), it is only since the past three decades (34) that scientists have realized the immense distribution and ecological significance of this coral species.

Oases in the dark

The deep-ocean floor is dominated by vast abyssal plains. Since almost all biomass produced in the upper ocean is recycled during its sinking through the vast water column, only little food reaches the ground to sustain animal life. But some oases exist in this vastest of all deserts. There are Hot Vents and Cold Seeps at the edges of the tectonic plates, supporting a rich fauna that is solely based on the energy that bacteria draw from reduced sulfur compounds. And there are cold-water coral reefs at the continental slopes. More than 980 invertebrate species are known to be associated with cold-water corals (3). They belong to a broad range of animal groups, such as foraminiferans, sponges, cnidarians, ribbon worms, bristle worms, crustaceans, mollusks, and sea urchins. cold-water reefs are particularly important as nurseries for juvenile fish, which also makes them a key factor in fisheries biology. In a study on fish associated with cold-water reefs, 25 fish species were observed, 17 of which were commercially important and comprised 82% of all individuals (5). Although most of the organisms found on Lophelia reefs do not live there exclusively, many of them are much less common in other habitats (5, 24). Some animals are found regularly associated with L. pertusa: The foraminiferan Hyrrokkin sarcophaga (Fig. 3), for example, is a common parasite that also infests mussels and sponges. It settles under the ectoderm of Lophelia polyps and feeds on their tissue. The polychaete Eunice norvegica (Fig. 4) has quite an intimate relationship with the coral. It secretes parchment-like tubes woven into the coral colony. These tubes are successively covered by the coral tissue and calcified. Eunice appears to defend “its” coral by biting, even if the reputed aggressor is just a cleaning rod in an aquarium (24). As “protection money” the worm steals food from the polyps, obviously unimpaired by the coral’s stinging cells (24).

"Cold-water reefs slowly grow upwards, which can result in the formation of carbonate mounds reaching heights up to 200 m above the sea floor."

Even though invertebrates and fish are the most conspicuous concomitant biota of corals, they are not the only and certainly not the most numerous. The close symbiosis of hermatypic stony corals with dinoflagellate algae of the genus Symbiodinium, called ‘ zooxanthellae,’ is perhaps the best known example of an interaction between corals and a single-celled organism. But there are even smaller and more widespread tenants: bacteria.

Small lodgers—big impact

The influence of bacteria on the life and health of tropical corals has been studied for many decades. For example, reef-building corals might take advantage from the bacteria inhabiting their mucus, as the latter are able to recycle nutrients that are very scarce in tropical waters (21). On the other hand, bacteria were shown to be responsible for breakdown of the organic skeletal matrix of the Indo-Pacific shallow-water species Porites lobata (8). Many coral diseases such as black band disease and white plague are induced by bacteria. They can also mediate or even cause coral bleaching. To prevent surface fouling, many hard corals use antibiotics to launch chemical warfare on bacteria. Amazingly, substances produced in certain corals show activity against potentially pathogenic marine bacteria, but not against the associated microbes from the animals’ tissue and mucus. While corals might be able to differentiate between “enemy” and “friend", the source of antimicrobial activity could also be the coral-associated bacteria themselves (18).

Though bacteria are certainly important for cold-water corals as well, microbiologists have been facing this aspect for only a few years. In 2006, researchers showed that Mediterranean specimens of L. pertusa shelter a microbial community different from that of dead corals, sediment, or surrounding water (36). L. pertusa has both antimicrobial and growth-stimulating substances to influence bacterial growth on its surface (13). L. pertusa’s bacterial community is quite variable. Specimens from Norway and from the Gulf of Mexico show similar microbial colonisation; on the other hand, L. pertusa from the Mediterranean, a rather extreme habitat for cold-water corals because of high temperatures and salinity, hosts an entirely unique microbial community (17, 27, 36). Surprisingly, even the two colour varieties of the coral show differences in bacterial colonization (27). Many bacteria, however, are found not only on L. pertusa, but also on other corals, namely so-called “bamboo corals” (17, 27, 28). The ecological requirements of these deep-sea gorgonians, named after their similarity to bamboo plants, are very similar to those of L. pertusa. This led to the assumption that there might be “cold-water, coral-specific” bacteria (27).

Figure 4: The polychaete Eunice norvegica, which often forms a mutualistic symbiosis with L. pertusa colonies (photograph: Erling Svensen).

Two groups of L. pertusa-associated bacteria are particularly intriguing. One group is closely related to symbionts that live in the gills of deep-sea mussels colonizing hydrothermal vents (17, 27). These bacteria can produce energy and biomass by oxidising sulphur compounds contained in the vent fluids. The so-called ‘Hydraulic Theory’ (15) states that such bacteria might provide L. pertusa with additional nutriment at sites where hydrocarbon-rich fluids emanate from the seafloor. Most cold-water reefs, however, do not appear to be influenced by such fluid seepage. But sulfur compounds can also be produced by L. pertusa itself or other microbes residing on the coral, and the sulfur-oxidizing bacteria might play an important role in the recycling of these compounds.

The other intriguing group of bacteria belongs to the genus Mycoplasma. What makes these microbes interesting is the fact that they are always found associated with multicellular organisms, whereat each Mycoplasma species resides on a particular host species. Unlike most other bacteria, mycoplasmas don’t have a cell wall. They also have the smallest genomes of all organisms and are quite limited in their metabolic capabilities. Consequently, they take what they need from their host. Mycoplasmas were found on L. pertusa from Norway (26, 27) and from the Gulf of Mexico (17). These “Candidatus Mycoplasma corallicola” are found exclusively on the nematocyst batteries of the coral tentacles (Fig. 5), which gave way to the theory that they live on body fluids of crustaceans that leak during prey capture activity of the polyp (26).

Menace mankind

Divers and coral enthusiasts are well aware of the threats posed on warm-water reefs in the shape of environmental pollution, mass tourism, and souvenir or toy fish hunting. But human influence has long reached the realms of cold-water corals, too. Lophelia reefs are directly affected by mechanical damage. Aside from seabed mining, cable and pipe laying, and oil and gas exploration, the most massive harm is done by bottom trawling (10, 33). This form of deep-sea fishing uses pouchy nets with heavy rollers to keep them close to the bottom. As the nets are hauled across the sea floor to startle fish, these rollers smash everything underneath. The effect on Lophelia reefs, preferred targets for trawling because of their richness in fish, is devastating: It is estimated that between 30 and 50% of the Norwegian reefs are either impacted or destroyed by trawling (10). While the damage done by the fishing industry can in principle be limited through the establishment of protection zones, the corals cannot be shielded from ocean acidification and global warming. To understand the effects of these two processes on Lophelia reefs, we have to make a side trip into marine chemistry.

"In a study on fish associated with cold-water reefs, 25 fish species were observed, 17 of which were commercially important and comprised 82% of all individuals."

Figure 5: “Candidatus Mycoplasma corallicola” on the nematocyst batteries of an L. pertusa polyp tentacle. The bacteria are visualized with a molecular biological technique called CARD-FISH and photographed under a fluorescence microscope. Scale bar: 20 µm. Copyright © American Society for Microbiology, Appl. Environ. Microbiol. 75:1437-1444 (supplementary material), 2009.

The shells and skeletons of many marine organisms, including corals, are made of calcium carbonate. There, the mineral occurs in two variants, calcite and aragonite. Scleractinian corals such as L. pertusa build their skeletons of aragonite. The solubility of calcium carbonate depends on several factors, such as temperature, pressure (i.e., depth), and pH. The colder, deeper, and more acidic a water mass, the more carbonate can dissolve in it. Below the so-called ‘carbonate saturation horizon,’ also known as ‘carbonate compensation depth,’ all calcium carbonate will eventually be dissolved because the water is undersaturated with respect to this mineral. As aragonite is more soluble than calcite, the aragonite saturation horizon is generally less deep than the calcite saturation horizon. The depth of the saturation horizon also depends on the oceanic region. The older a deep water mass, the more carbon dioxide (CO₂) from biological decomposition processes accumulates in it. This CO₂ forms carbonic acid which lowers the pH of the water, thereby increasing carbonate solubility. In upwelling regions where the deep ocean water reaches the surface again, namely in the Eastern Pacific, the aragonite saturation horizon is thus by far shallower (50 to 600 m) than in the North Atlantic (>2000 m) (6).

Now, what does this have to do with human influence on cold-water reefs? As mankind continues to burn fossil fuels, the atmosphere gets enriched in CO₂ that had been detracted from the global carbon cycle for several millions of years. This enrichment has two tremendous effects: On the one hand, CO₂ acts as a greenhouse gas, and its rising concentration in the atmosphere causes the average global temperature to rise as well. On the other hand, as already explained above, the gas forms carbonic acid upon contact with seawater, which lowers the pH of the surface ocean. This process is termed ‘ocean acidification.’ The global current system gradually distributes the more acidic ocean surface water to greater depths. Ocean pH has already fallen by 0.1 unit and will fall another 0.3 to 0.4 units by the year 2100 if the burning of fossil fuels continues at the current rate (4). This will cause the saturation horizons for calcite and aragonite to rise by several hundreds to thousands of meters. By the year 2100, 70% of the known cold-water reefs will be surrounded by water that is undersaturated with respect to aragonite and thus corrosive to coral skeletons (14). Though L. pertusa will still be able to build up its skeleton, the speed at which this calcification takes place will be reduced by up to 59% at a pH assumed to prevail in the year 2100 (4, 23). What is more, the skeletons of dead corals will dissolve in the undersaturated water, entailing a loss of substrate for reef formation (14). Even today, very few incidences of Lophelia are reported from the North-East Pacific (Fig. 2) where the aragonite saturation horizon is shallowest, and there are no spacious cold-water reefs found in that region at all (14). If mankind continues with “business as usual” burning of fossil fuels, this scenario will become true for most regions of the world’s oceans by the end of this century.

Figure 6: cold-water reefs harbour a stunning variety of marine species, including corals, clams, worms, crustaceans, mollusks and fish. Their destruction would result in a huge loss of marine biodiversity (photographs: Erling Svensen, locations: Tautraryggen, Trondheimsfjord and Lysefjorden, Rogaland, Norway).

As explained above, anthropogenic CO₂ also promotes global warming. This poses another threat to L. pertusa. While direct thermal stress can enfeeble the coral and restrict its range of distribution, the coral-associated bacteria mentioned above may also  play an important role, again—this time to the detriment of L. pertusa. Several L. pertusa-associated microbes are potential coral pathogens (27). The coral specimens harbouring these bacteria were apparently healthy (27), so the bacteria in question might be not dangerous for their hosts under regular circumstances. But disruption of the balance between the coral and its associated—even normally harmless—microbiota is known to trigger coral mortality (20). We must be apprehensive about the possibility that both ocean acidification and global warming will eventually disrupt this balance.

"By the year 2100, 70% of the known cold-water reefs will be surrounded by water that is undersaturated with respect to aragonite and thus corrosive to coral skeletons."

What would be the result? The loss of cold-water reefs will surely reduce the habitat for many commercially important fish species and thus impair the fishing industry. But can we really price-tag this loss? Do we have the moral right to deprive our own children of one of the oceans biggest treasures?

Lophelia pertusa community in Garden Banks region in the Gulf of Mexico. The video shows habitat structure created by live and dead Lophelia coral. Video is narrated by Dr. Erik Cordes. Video courtesy of Lophelia II 2009: Deepwater Coral Expedition: Reefs, Rigs and Wrecks.

Follow this link to the United Nations Environment Programme to compare cold-water reefs with tropical shallow  water reefs. Please note that this information is subject to future changes.

References:

1.       Beuck, L., and A. Freiwald. 2005. Bioerosion patterns in a deep-water Lophelia pertusa (Scleractinia) thicket (Propeller Mound, Northern Porcupine Seabight), p. 915-936. In A. Freiwald and J. M. Roberts (ed.), Cold-water corals and ecosystems. Springer, Berlin, Heidelberg.

2.       Buddemeier, R. W., and R. A. Kienze.