An odd and ordinary world

Seventy-one percent of the earth surface is covered by water accumulated by outgassing, over the past 4.6 billion years, or from extraterrestrial origin (brought with comets). Oceans represent 97.3% of this water and are, for 95%, considered as deep sea, i.e.

deeper than 200 m below the sea level. Therefore, it is correct to affirm that the deep sea is the most common environment of the planet. However, it is still regarded by many scientists as one of the most unusual and fairyland-like biotope of the world. For a long time, deep sea was even not fully considered as a biotope and many have speculated that life would not occur very deep. In the early 19^th century, how deep extended oceans and living organisms was still a complete mystery. After a dredging campaign on Aegean Sea in 1841, Edward Forbes proposed the “azoic theory” based on his observations of a fauna getting rarer with depth.

According to his extrapolated curve of rarefaction, life should disappear around 550 m (Forbes, 1844). It is remarkable that this erroneous theory held for almost 25 years, despite contrary evidences (Anderson and Rice, 2006). The “recording telegraph” invention, two years later, was about to bring one of those evidences and change the history of marine biology. The installation of transatlantic telegraphic cable between Ireland and the Newfoundland revealed deep-sea bottoms of 5000 m and a living specimen of Caryophyllia borealis (a stony coral) attached to the cable at 1800 m. From that moment, marine biologists’

mind got carried away by this question alone: “How deep occurs life in the oceans?”. Still, they will have to wait more than a century to get the answer. Finally, in 1960, Jacques Piccard and Don Walsh on board submersible “Trieste II” reached the deepest known ocean point at 10’911 m disturbing, by the way, flounders and shrimps of the Mariana Trench. Today, almost fifty years later, this record is waiting to be repeated and less than 1% of the deep sea has been explored. One of the reasons why abysses were unstudied during such a long time and why they still remain more mysterious than the dark side of the moon, is probably that they drastically differ from the terrestrial environment scientists are living in. First, because this aquatic milieu has a density about 830 times that of air and a viscosity about 60 times greater, directly ruling the morphology, metabolism and behavior of its inhabitants. Then, considering an average depth of 3800 m, deep sea is largely deprived of natural light except that produced by the organisms themselves. As a major consequence, primary production can

not be processed through photosynthesis, which induces a very low average concentration in nutrients and thus also, low concentration of organisms. High pressures, low temperatures and oxygen concentrations also participate to increase differences between terrestrial and deep marine environments. Since the late 1970’s, exceptions to those general features are known.

Vents and seeps, for instance, are forming real biological “hot-spots” at the opposite of other typical deep-sea ecosystems. They emphasize even more the singularity of this world.

Deep sea consists in a prodigious volume of water (1.3 billion km³) over a floor shaped by plate accretion and particle sedimentation. Traditionally, deep-sea pelagic volume is divided into four vertical zones: the mesopelagic (from 200 to 1000 m), the bathypelagic (from 1000 to 4000 m), the abyssopelagic (from 4000 to 6000 m) and the hadopelagic (from 6000 m to the bottom). The mesopelagic, also called “twilight” is clearly different from the other three realms. Just below the surface water forming the photic epipelagic, reduced light still penetrates but not sufficiently for photosynthesis. Biomass is getting poorer and is almost deprived of phytoplankton. It is also the place of vertical migrations for zooplankton, fishes, crustaceans and mollusks which follow the phytoplankton up through the water every night.

Physiological adaptations linked to the reduced light conditions, as tubular eyes or well-developed phototactic organs, can be observed in the species that do not participate in this migration. Bioluminescence is another feature widely spread among mesopelagic organisms and is known to be linked to varied function as communication (Rees et al., 1998), camouflage (Young and Mencher, 1980) or prey illumination (Douglas et al., 2000). Light is produced in photophores by specialized tissues or symbiotic bacteria (Shimomura et al., 1972). Temperature is getting down from over 20°C at the top of the mesopelagic zone (200 m) to around 4°C at its border with the bathyal zone (1000 m). Oxygen minimum zone (OMZ) also occurs in the same depths interval, depending on the atmospheric conditions and the local mixing of water masses. In the upper layers, close to the water-air interface, oxygen concentration is high (around 6 ml.L^-1). Oxygen that is dissolved from atmosphere into the water and oxygen produced by photosynthesis exceed that consumed by respiration and by decomposition of sinking organic matter. Between 80 and 90% of these sinking particles are consumed by bacteria in the first 1000 meters. Going down from the surface to the OMZ, where oxygen concentration can reach less than 1 ml.L^-1, contribution of atmosphere and photosynthesis is getting weaker. Deeper than the OMZ, organic matter degradation is weak, since there are only few particles left. There, oxygen concentration, also supported by cold

deep waters (oxygen-rich) supply, increases again but remains lower than near the surface (up to 3 ml.L^-1). Organisms living in oxygen deprived environment present metabolic adaptations that enable them to consume less oxygen (some bacteria and foraminifera use rather nitrate) or to extract it from the water with high efficiency, as the vampire squid with its haemocyanin of enhanced oxygen affinity (Seibel et al., 1999). It is not the point here to describe each and every chemico-physical mechanism occurring in the deep sea but OMZ plays indeed an important role by regulating the productivity and the ecological community structure of pelagic systems (Deutsch et al., 2007), both affecting the benthos. While the mesopelagic zone is the place of strong gradients and temporal variability, the rest of the deep sea consists in a much more homogenous environment with relatively stable parameters. Bathypelagic, abyssopelagic and hadopelagic zones are globally cold, poor in nutrient and oxygen, and totally deprived of solar light. At 1000 m, less than 10 % of the sinking organic matter from the upper layers remains, making all the food chains energy-poor and poorer with depth.

Organisms are therefore sparse and have to cope with nutrients limitation, cold temperature and hypoxic conditions. Numerous adaptations aim to increase their chance to eat and meet mating partners and to reduce energy consumption. Fishes, for instance, tend to be opportunist predator able to catch and swallow huge preys regarding their own size (Ebeling and Caillet, 1974; Hopkins and Baird, 1973). It has also been reported that copepods use extremely efficient mechano- and chemoreceptors to track female and food (Yen, 2000). Another striking example is angler fish male, which follows female’s pheromones, bits her and remains attached to her body for the rest of his life, saving energy and being exclusively devoted to the reproduction (Munk, 2000). In conclusion, the deeper part of the oceans is a diluted world where each source of energy is exploited to the uttermost and each opportunity is seized.

The benthic realm does not escape the poor energy and food resources constraints.

Even if the deep-sea bottom presents various sorts of topological features, nutrients density seems to shape almost alone the spatial distribution of organisms. The deep-sea relief starts near the coast with the continental slopes, usually in the range of 300-2000 m, and meets up the abyssal plain at 4000 m in the mean and deep trenches at the deepest points. These three major environments are actually connected with those not only above but also beneath the ground. Oceans bottoms receive unevenly organic matter from the upper water layers depending not only on the surface production and consumption but also on the ability of their

form to retain the sediment. Upstream input consists first in marine snow accumulated especially in the bowl-shaped places (Alldredge and Silver, 1988; Lampitt, 1996), then in carcasses of larger organisms like whales or kelps (Graham et al., 2007; Lorion et al., 2009), and finally in terrestrial sediments dragged from the coast through submarine canyons (Canals et al., 2006). Consequently, the surface of most areas consists in mud and organic ooze, except for some rocky bathyal slopes and trenches. Matter input also comes from underneath the ocean floor due to geological activity of the tectonic plates. Under the mid-oceanic ridges, convection currents in the magma rise from the mantle core through the oceanic crust and emerge as lava. This induces a high volcanic activity with frequent earthquakes and faulting.

Hydrothermal vents, discovered only 30 years ago (Corliss et al., 1979), are among the features created by these events. Seawater that has permeated into the ocean floor is heated by the hot magma (up to 350-400°C) and enriched in metals (mainly iron, copper and zinc) and hydrogen sulfide by dissolution from the surrounding crust. The hot and less dense hydrothermal fluids rise up through the ocean crust before exiting the chimney and mixing with the seawater. Because the seawater is cold and oxygen-rich, it induces the precipitation of metal sulfides and oxides resulting in a black smoke which led to the nomination of “black smokers”. When the water reaches only 250-300°C, hydrothermal fluids flow more slowly than in a black smoker and thus, can mix with closely permeated sea water (cold) already under the sea floor. In this case, metal sulfides and oxides precipitate into black minerals before exiting the chimney. When the fluids finally get out in the open ocean, only silica and calcium sulfate (white) are left to precipitate, leading to the white color of the “white smokers”. A huge biomass is associated with the smokers, starting with thermophile chemosynthetic bacteria, which insure the primary production without photosynthesis by oxidizing sulfite ions from the vents into sulfur (CO2 + H2S + O2 → CH2O + H2SO4) (Kaiser, 2005; Ruby et al., 1981). This primary production enables directly or indirectly the occurrence of many other life forms each of them deeply specialized and typically associated with most of hydrothermal vents ecosystems. Some organisms graze on bacteria, while others host them in their tissues or feed on primary and secondary consumers. A famous example of endosymbiosis with the chemosynthetic bacteria from the vents is the giant gutless tube worm Riftia pachyptila, consumed by the hydrothermal crab Bythograea thermydron, which is itself hunted by both octopus Vulcanoctopus hydrothermalis and eelpout fish Thermarces cerberus (Childress and Fischer, 1992).

Along continental margins occur other special features of the deep-sea bottom called

“cold seeps” and consisting in seepage of hydrogen sulfide, methane (sometime methane-hydrate ice) or hydrocarbonated fluids (Dugan and Flemings, 2000). These fluids are released in the form of brine and settle along the bottom like lakes, because of their high density.

Living communities associated with the cold seeps are similar in density and composition to those found near the hydrothermal vents and include, at the base of the food web, chemosynthetic bacteria metabolizing sulfides and methane (Knittel et al., 2005). Compared with the short lasting vents (a couple of years only) cold seeps are relatively stable systems sheltering among the longest living invertebrates, as the tube worm Lamellibrachia luymesi, which can live up to 250 years (Bergquist et al., 2000).

The third kind of special habitat induced by geothermal activity is also found near the continental margins and is composed of mud volcanoes and seamounts. Mud volcanoes are also considered as a kind of seep and consist in a mixture of mud, water and gases (mainly methane) forming characteristic domes at the surface of the sea floor. Immediate surroundings of mud volcanoes are found to be rich in micro-organisms and notably, there again, in chemosynthetic bacteria (Niemann et al., 2006). Seamounts consist in undersea mountains (typically extinct volcanoes progressively covered by sediment) higher than 1000 m. Because they are from volcanic rock, they offer a substrate much harder than the surrounding sedimentary floor and thus shelter different types of organisms including suspension feeders as sponges and corals. Moreover, their shapes disturb deep currents and induce upwelling, which bring nutrients to the euphotic zone. This locally enhances biological activity and increases concentration of living organisms. For that reason, seamounts are strategic stops for large migratory animals and also aggregate numerous visitors (Morato et al., 2008). Finally, the deep-sea bottom appears to be much less featureless than it has been supposed during the past. Local geological events create remarkable habitats for remarkable organisms.