Ecosystem Sustainability and Global Change

1

Ocean, Biodiversity and Resources

1.1. The history of life in the oceans

The Earth was formed 4,600 million years ago. From ancestral geodiversity originating from prebiotic chemistry, which gave rise to the set of chain reactions that produced the first structured sugar, nitrogen base and amino-acid molecules, life appeared in oceans, fairly quickly after the initial cooling and condensation of water, over 3,800 million years ago.

Duve [DUV 96], 1974 Nobel Prize Laureate, said, in Dust of life in 1996, that Earth was so ideally positioned with respect to the Sun that it would not be possible for life not to appear (i.e. it was bound to), while J. Monod referred to it as an improbable occurrence. The oldest known sedimentary rocks (Akilia Island, in South Greenland) containing carbon of biological origin date back 3,850 million years. We must imagine very primitive life at the start, based on a world of ribonucleicacid (RNA) and protocells [MAU 03]. Current deposits of stromatolite (rocks that precipitate bicarbonate), with very rich deposits in Australia, are very precious since, in their silicified parts, they contain the most ancient known fossils of microorganisms: cyanobacteria. These began their conquest of the oceans around 3,400–3,200 million years ago, at the time without any atmospheric oxygen. In the presence of water, photosynthesis produces oxygen and sugars from light and carbon dioxide (CO2) due to specific pigments in the cells; this process began to take place on Earth around 3,500 million years ago. Oxygen started to diffuse beyond the confines of the aquatic environment around 3,200 million years ago; the current composition of the atmosphere, with its 21% of oxygen, dates back at around 100 million years, in the Cretaceous Era.

In this ancestral ocean, events occurred that were of critical importance both for the living world in general and for biodiversity:

– the appearance of the nuclear membrane and the individualized nucleus (prokaryote-eukaryote transition) around 2,200 million years ago;

– the capture of ambient cyanobacteria that would become symbionts and the organelles of the cell – mitochondria and plastids, with desoxyribonucleicacid (DNA) of their own – respectively, around 2,100 and 4,100 years ago;

– the appearance of multicellular organisms and metazoans around 2,100 million years ago.

Another exceptional occurrence took place in this ancestral ocean: the appearance of sexuality, first with prokaryotes, and later also with eukaryotes, which would prove to be essential for the explosion of biodiversity. Sexual reproduction allows for genetic mixing, which creates originality and unprecedented diversity: all individuals are different. A population endowed with sexuality evolves much more quickly. Furthermore, the prevalence of sexuality facilitates the development of an arms race between parasites and their hosts (coevolution and molecular dialogue [COM 01]), as genetic mixing ultimately leads to quicker neutralization of the parasite, and sexual selection that is clearly different to natural selection [DIM 05].

The exit of organized metazoan life from the oceans took place after the Cambrian explosion (570 million years ago), where the first plant life-forms (first vascular plants in the late Silurian, around 415 million years ago, with moss existing long before that) and terrestrial animal life-forms (arthropods and vertebrates, among others) would leave traces on the continents (myriapods, scorpions, later lungfish, rhipidistia and Ichthyostega, around 440 million years ago). Numerous new adaptations were developed, both by plants and animals; the transit to terrestrial life and air-breathing represent an exceptional occurrence in the history of life. The differences are fundamentally between aquatic and terrestrial animals. The former extract their oxygen from water through diffusion to the heart of the organism for small species, or through gills for larger ones. A volume of seawater at equilibrium with the air contains around 30 times less oxygen than the same volume of air. Anisosmotic aquatic breathers (whose internal environment is different to the surrounding water – e.g. fish) cannot develop too large an exchange surface (gills) due to the dangers inherent to the physical consequences of osmotic flows (water and electrolytes), with the animal losing water to the sea, or being flooded by river water. In fact, a fish is constantly subject to a difficult compromise, between developing a maximum gill surface, to capture the oxygen in an oxygen-poor and very changeable environment, and a minimum surface to help prevent serious water–mineral imbalances. Aquatic animals excrete ammonia and, for the vast majority, do not thermoregulate. By contrast, terrestrial animals must endure ultra violet (UV) rays, dehydration, a very different experience of gravity (consequently, requiring a much heavier and resistive skeleton and muscle mass), and must use excretion products that are not highly toxic or are non-toxic (such as, uric acid or urea). Much later, in the Triassic period, around 210 million years ago, after the third great species extinction crisis, the premises of thermoregulation were developed, and used to maximum efficiency first by large dinosaurs, and then mostly by birds and mammals. A very good example of the return to the ocean is the case of cetaceans, which began this reacclimatization to marine life based on the primitive terrestrial forms of artiodactyls (for example, hippopotami) similar to Diacodexis, and then amphibian forms (like the Pakicetus or Ambulocetus) around 55–50 million years ago, whose current giant forms (the largest animals to have populated the planet since the origins of life, which humans have been uncaringly massacring for 160 years) are very recent. Today, 12 phyla are exclusively marine animals and have never left the ocean (echinoderms, brachiopods, chaetnognaths, etc. – see Table 1.1). However, only two exclusively terrestrial groups (not phyla) exist: myriapods and amphibians. Additionally, the seas contain vast quantities of biomass: the bacteria in the subsurface layer of the ocean alone represent 10% of all carbonated biomass on the planet [PAR 94]. The marine environment has, therefore, played a decisive role in the history of life, and today the ocean continues to play a crucial role in the evolution of life and climate [BOE 08].

Today, we are searching for traces of extraterrestrial life, by concentrating efforts on DNA, amino-acids, Adenosine triphosphate (ATP), etc., without forgetting that the key molecule of life is water. The make-up of every living being contains water – ranging from a few percent, in the case of the driest organisms (e.g. plant seeds), to over 95%, for certain aquatic species (algae, jellyfish, ascidia, among others). The human body itself is made of two thirds of water; a human baby at birth has 75% of water and our brain has more than 80%. Water is life [BOE 12]: for example, take the borders of a Chilean desert which, every 10–12 years when it rains, becomes covered with flowers (along with vast numbers of insects) in the space of a few days, lasting a few weeks, and then returns to years of extreme aridity. This is natural; however, humans can also trigger explosions of life by irrigating the desert.

The departure from water was, therefore, a truly decisive event in the history of life. The ocean has been salty (essentially with sodium chloride) for a very long time, and today we are able to understand this stability in its salinity: the billions of tons of cations (calcium, potassium, magnesium, sodium, etc.) brought to the sea by the rivers since they began flowing, are compensated for: in the case of calcium, by the trapping of marine sediments and the formation of limestone; for potassium by the absorption of clay (see Chapter 4 in [MON 14a] and Chapter 2. Magnesium and sodium are retained in the oceanic ridges (serpentinization and clay-formation from pyroxenes and olivines). Serpentinization corresponds to the hydration of minerals, and alteration into clay corresponds to the deterioration into small grains of less than 2 μ in diameter. For anions, bicarbonates are constantly mixing with the atmosphere and biosphere, and for chlorides, which do not enter into any major biogeochemical cycles, we currently believe that chlorine was one of the original volatile elements that was dissolved in seawater initially and remained there (not much is carried by rivers today). This current salinity, of around 35 psu (internationally recognized practical salinity unit, corresponding to 35 g of sodium chloride per liter) causes osmolarity (meaning osmotic pressure) of 1,050 milliosmoles per liter (mOsm.l−1).

Marine life has always had to cope with this, and has developed a universal strategy of intercellular isosmotic regulation for which the vast majority (of animals only) of invertebrates and certain vertebrates have the same osmotic pressure (internal environment and cells) as that of seawater. Another strategy, which has arisen in certain crustaceans, referred to as extracellular anisosmotic regulation, has allowed for great migration capabilities and the ability to change environments, by maintaining the osmotic pressure of cells and body fluids within a very small range (between 300 and 400 mOsm.l−1; humans are at 302); regardless of the external salinity. In fact, in this latter case, we can die of dehydration in seawater; the presence of salts causing outakes of water from the organism to the external environment through exchange surfaces in close contact (blood–water) with salt water, such as the epithelium of the mouth and gills (with seawater salts migrating in the opposite direction). Marine osmoregulators (for example, boned fish) have had to establish strategies for the constant intake of seawater and the evacuation of salts through the gill, with the kidney proving to be incapable of fulfilling this function on its own. One of the main problems posed by terrestrial life is the conservation of water and the struggle against dehydration [BOE 12]. The role of the kidney is, therefore, essential: think of the small kangaroo rat from the desert, which never has access to drinking water and produces urine that is nine times more salty than seawater. For its part, terrestrial biodiversity would develop later on, after the establishment of specific mechanisms, and took off massively in the Carboniferous Era, from 345 million years BC onward.

We will, therefore, take inspiration from certain aspects related to life in the ocean: first its age and its often much simpler organization, and second its productivity and specific diversity:

– Which renewable living resources will humans be able to take from the ocean (fishing and aquaculture)?

– Which molecules of interest will we extract from marine organisms?

– Which marine models will be pertinent for a basic scientific approach or the resolution of fundamental questions in the field of biomedicine?

1.2. Specifics of marine biodiversity

Marine biodiversity is a very special case [BOE 11]. The recognized diversity of species in the oceans accounts for no more than 13% of the set of living species currently known: i.e. less than 250,000. There may be two reasons for this. The first is that our knowledge – especially of deepwater areas and microorganisms, bacteria and microalgae – is still only very incomplete (so we considerably underestimate the biodiversity of the oceans). New methods, such as coupling between flow cytometry (a technique that entails launching particles, molecules and cells at high speeds through a laser beam in order to characterize them) and molecular probes (which reveal an organism with specific features), are currently discovering a totally unforeseen, extraordinary level of biodiversity. Sequencing the ocean (C. Venter, sequencing all the DNA in a given volume of filtered seawater) moves in the same direction; the data obtained appear, for the most part, to be revelations. The recent round-the-world expedition Tara Océans has also produced exceptional data. For all prokaryotes and very small eukaryotes, recent molecular approaches (sequencing of 16S and 18S ribosomal RNA, among others) produce astonishing results daily. Furthermore, and this is the second reason, it is also obvious that marine ecosystems and the way of life in a continuous environment (by the dispersion of gametes and larval stages) of the species that populate it, are less predisposed to strict endemism (the notion of living exclusively here and nowhere else) than in terrestrial habitats. There are many more barriers and segregations favorable for speciation (the evolutionary process by which new living species arise) on land than in the sea. This leads to significant differences in terms of specific diversity; marine ecological niches do not achieve the richness of terrestrial ones, which are much more fragmented and are more favorable to new species. The stability of the open ocean in deep waters, over at least the past 100 million years, is also extraordinary: in terms of pH, osmotic pressure and salinity, temperature, hydrostatic pressure linked to depth, dissolved gas content, etc. The closer we are to the coast, the more this fluctuates. Human activity is changing this; we will revisit this point later on. This stability is less prone to give rise to new species. Consequently, marine biomasses can be considerable, and the performance of phytoplankton alone, with its capacity for self-regeneration, accounts for over 50% of the planet’s productivity.

Table 1.1. Exclusively marine phyla (according to [BOE 11])

This table is simply indicative of exclusively marine groups. How do we then chose them? Cephalochordata and tunicates are sub-phyla of Chordata (which have continental taxons), the Kinorhynca, Priapulida and Loricifera have been grouped within the Cephalorhyncha with the Nematomorpha, which are terrestrial; Xenoturbellida, Cycliophora and Mesozoa can be considered as valid phyla.

There are five to seven more terrestrial taxons today, compared to oceans, which is worthy of inquiry since initially life was exclusively marine, before the various great departures from the oceans, at different locations in different forms, 440 million years ago, for developed metazoans. The great Permian-Trias extinction played a primordial role with 96% of the extinction of species both marine and continental around 252 million years BC. The explosion of flower plant species, of insects and many other groups on Earth, around 130–110 million years ago, was decisive after the initial radiations (explosion in the number of species deriving from a single ancestral one) starting from the Carboniferous period. The coevolution between plants and pollinators, and the appearance of an infinite number of new niches, have often been proposed to explain the acceleration of speciation in continental environments of this era [BOE 11, BOY 10]. It is also evident that dispersion phenomena of reproductive products and larvae in the oceans played an important role in the distribution of current species and biogeography. Endemism is notably considerably more limited in the ocean, the stability in deep water and the continuity of this gigantic environment explaining this. If it is not rare to find living species over a few km² on land, then we do not know of any examples of such confined species in the sea. The large variety of methods of reproduction in the sea also draws from dispersion phenomena in water bodies, with males and females not constrained to being in close proximity. Thus, do connectivity and the much weaker variations in environmental factors create the great stability in the ocean at large and the particularly specific characteristics of the biodiversity that it houses? Coastal systems, intermediaries with strong land-related influences, are subject to much greater variations.

Finally, we must not forget that biodiversity is much more than just specific diversity, which includes both species and their relative abundance. The meaning of the word biodiversity has been interpreted in many ways but generally expresses the genetic information which contains each elementary unit of diversity, be it an individual, a species or a population. This determines its history, past, present and future. Even then, this history is determined by processes that are also components of biodiversity. In fact, today we group different approaches under this term together:

– the study of fundamental biological mechanisms that explain the diversity of species and their specific features and that require us to further study the mechanisms of speciation and evolution;

– the most recent and promising approaches in the field of functional ecology and biocomplexity, including the study of material and energy flows and the great biogeochemical cycles;

– the utility of nature as goods and services for mankind in their capacity to provide food, high-value substances for medicines, cosmetic products, etc., molecular probes or even obtaining ancient ancestral and original models for fundamental and finalized research, in order to resolve agronomical or biomedical questions;

– the establishment of conservation strategies for preserving and maintaining a natural inheritance consisting of a naturally expected heritage by/for future generations. We must also particularly insist on the fact that inventories and descriptive lists are not sufficient to specify what the biodiversity is: much more important are the relations established by the living beings between each other and their environment.

1.3. Renewable living resources

Humans have been fishing since ancient times, certainly tens of thousands of years. As soon as they reached shores, they began to collect shells, algae, etc. As in agriculture and continental environments, humans have been farming certain marine species on the coasts for at least 4,000 years (Egypt, China, etc.). The use of renewable living resources being very well outlined elsewhere in this work and in others in the collection Seas and Oceans, I will limit myself to only a few generalized remarks here.

The latest statistics available from the Food and Agriculture Administration (FAO) in 2012, for the year 2011, give values of 78.9 million tons (Mt) for maritime fishing, 11.5 Mt for continental fishing, 19 Mt for algae (with only one for fishing) and 63.6 Mt for aquaculture (of which 19.3 Mt are for the sea), thus a total, of all the groups and aquatic environments combined, of around 173 Mt (see also Chapter 4.

1.3.1. Fisheries

Until the 1950s (apart from some very particular stocks already, herring from the North Sea and especially whales, etc.), we did not really record any tax-related overexploitation of fish stocks in the world. This was all accelerated after the end of the Second World War and the establishment of the intensive practice of trawling and the big ocean seine or with huge drift-nets. The question that has already been posed, will fishing disappear, due to a lack of fish? [CUR 12, CUR 13]. The collapse of the Newfoundland cod stock at the beginning of the 1990s after 500 years of harmony between harsh, but not excessively destructive, fishing across all of the countries bordering the North Atlantic (see Pêcheurs d’Islande by Pierre Loti) and the maintaining of the stock has been a symbolic example of modern overfishing. Today, the FAO tells us that three quarters of the world’s fish stocks are fully exploited or overexploited. In a 2006 paper, Worm et al. [WOR 06] had even announced the end of fish before the end of the half century.

From around 30 million tons of world marine products (including algae) in 1950, this statistic has changed to 80–90 Mt in the 1990s and has practically remained unchanged since (bar certain fluctuations in industrial fishing, during the El Niño years) despite increasingly sophisticated (and formidably efficient) methods of animal detection and fishing techniques. In fact, fishing activity forms a strange type of exploitation that is still active, and which dates back to prehistory, in a world of finite resources. Of course, living marine resources are by definition renewable, however, the recent crossings of exploitation thresholds have shifted certain stocks toward an overtaking of the limit of renewability, with natural recruitment no longer being sufficient. As long as a certain threshold is not crossed, we can always attempt, with adapted and firmly controlled measures, to restore the resource, with this holding true particularly when it comes to fishing. However, the pressure of fishing activity, always being the largest, oldest and most interesting for the