Download Chapter I Deep-sea ecosystems: their functioning and biodiversity

Chapter I
Deep-sea ecosystems: their functioning and biodiversity
Deep-sea ecosystems
The average depth of the global oceans is ca. 3850m. Deep-sea ecosystems include the
waters and sediments beneath 1000 m depth. Deep-sea sediments cover 65% of the World
surface, and the dark areas of the oceans account for more than 95% of the habitable area for
life, representing the most extended ecosystem on Earth. 88% of the oceans beyond the continental shelves are deeper than 1 km and 76% have depths of 3-6 km. The deep-sea floor is
formed by hundreds of millions of km2 of continental slopes and abyssal plains. Embedded
within these slopes and deep basins are other geological structures (Figure 1.1 ), including
mid-ocean ridges, canyons, seamounts, cold-water coral reefs, hydrothermal vents, methane
seeps, mud volcanoes, faults and trenches, which support unique microbiological and faunal
communities. The exact coverage of each different deep-sea habitat is not known, as the vast
bulk of the deep sea remains unexplored: only 5% of the deep sea has been explored and less
than 0.01% of the deep-sea floor has been scientifically investigated. Nevertheless, what little
we know indicates that the deep sea supports one of the highest levels of biodiversity on Earth
(Etter and Mullineaux 2001, Grassle and Macioleck 1992, Hessler and Sanders 1967, Sanders
1968, Snelgrove and Smith 2002, Stuart et al. 2003), as well as important biological and mineral resources (Baker and German 2009, UNEP 2007).
The last few decades have been marked by an increase of number of studies to investigate the biodiversity in deep-sea ecosystems, but these studies are typically characterized by a
limited spatial or temporal scale of investigation. Nonetheless, the three last decades have
seen a number of unexpected discoveries of unique habitats, such as hydrothermal vents, cold
seeps, whale falls and cold-water corals, improving our understanding of the biodiversity and
functioning of deep-sea ecosystems. The potential vulnerability of these poorly known ecosystems to anthropogenic disturbance has to be assessed at in time they may become impacted
increasingly by the exploitation of marine resources (e.g. mining, oil reservoir exploitation).
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Figure 1.1 The NE Atlantic seafloor showing some of the distinct deep-sea
ecosystems: continental margins – which can include canyons (arrow), cold seeps and cold
water corals, abyssal plains,seamounts and the mid-ocean ridge, where hydrothermal vents
are found (from Ramirez-Llodra et al., 2009, modified).
The deep sea has a series of characteristics that make this environment both distinct
from other marine and land ecosystems and unique for the entire planet. The deep seafloor is
typically covered by fine sediments (medium sands to clays). However, hard substrates are
not uncommon, as they are associated with manganese nodules, fault scarps and seamounts,
and as blocks at the base of landslides along the continental margins. Some of abiotic factors
are relatively homogeneous: in deep waters the temperature is 2°C with the exception of Mediterranean Sea (14°C; Sardà et al. 2004) and Red Sea (21°C; Manasrah et al. 200) and salinity is 35 (with the exception of Mediterranean Sea and Red Sea >39); pressure increases at 1
atmosphere every 10m depth; photosynthetically useful light is absent below 250 m; deep waters are well oxygenated (with the dissolved oxygen near saturation) with the exception of the
oxygen minimum zones (Levin 2003). Deep-sea ecosystems were long considered to be stable
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environments and most of the abyssal seafloor is highly stable for long periods of time, but
evidence accumulated since 1960s has shown that the deep sea is in fact a dynamic environment: in some regions and especially along continental margins sediment instability, strong
bottom current, dense water cascading and benthic storms can be relatively frequent (Gage
and Tyler 1991, Gage 2003).
Many deep-sea floor habitats share ecological characteristics that make them especially
sensitive to environmental change and human impacts. Perhaps the most important characteristics are low biological productivity and the lack of photosynthetically useful light below
~250 m (Thistle 2003). Except for hydrothermal vent and cold-seep communities, the food of
deep-sea floor must be imported from the euphotic zone (Fig 1.2): the energy for the deep-sea
biota is ultimately derived from an attenuated “rain” of small particles (only 0.5 to 2% of the
net primary production in the euphotic zone reaches the deep-sea floor below 2000 m), which
decrease inversely with water depth (Buesseler et al. 2007) and varies regionally with the levels of primary production in the upper ocean (Yool et al. 2007). Therefore, the deep-sea benthic communities are among the most food-limited on the globe (Smith et al. 2008) and in
most cases, the extent of this limitation increases with increasing water depth. The purely detrital base of most deep-sea food webs contrasts sharply with those of other marine and terrestrial ecosystems, which typically are sustained by local production (Polunin et al. 2001). The
deep-sea is not uniformly food poor: embedded within this oligotrophic matrix are extraordinary oases of high productivity; these habitats occur when organic material from the euphotic
zone becomes concentrated by canyons, whale falls, wood falls and oxygen minimum zones
(Levin 2003, Smith and Baco 2003, Smith 2006, Vetter et al. 2010) or where seafloor effluxes
of chemical energy support intense chemolithoautotrophic primary production, as at hydrothermal vents and cold seeps (Karl et al. 1980, Kelley et al. 2005). Even though these foodrich habitats are often small in area, extremely isolated and ephemeral at the seafloor (e.g.,
spanning 10s of meters, separated by 100s of kilometres and lasting for years to decades in
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the case of vents and whale falls), they all support remarkable communities highly distinct
from the background deep sea.
Figure 1.2 Energy input in different deep-sea ecosystems. Heterotrophic communities
are fuelled by primary production of phytoplankton in the surface layers of the ocean that use
solar energy (photosynthesis) as the source of energy. Chemosynthetic communities are
fuelled by primary production of microorganisms that use chemical energy from reduced
chemical compounds (chemosynthesis) coming from the Earth’s interior, or by large detrital
parcels, such as whale falls and wood falls. Modified from Ramirez-Llodra et al. 2010).
Despite their limited food availability, due to the size of the deep-sea ecosystems and
the extent of the subfloor biosphere, these ecosystems are by far the largest reservoirs of biomass throughout the globe. With increasing water depth, there is a dramatic decrease in the
larger benthic components (i.e., megafauna) and a progressively less evident decrease in the
abundance and biomass of macrofauna, meiofauna and microbes. Thus at bathyal-abyssal
depths, the large majority of the biomass is accounted for by microbial components (i.e.,
mostly Bacteria and Archaea, Danovaro 2003). The microbial processes occurring there provide essential services, driving nutrient regeneration and global biogeochemical cycles, which
are essential to sustain the primary and secondary production of the oceans (Dell’Anno and
Danovaro 2005).
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Biodiversity and ecosystem functioning in the deep sea
The oceans host life at all depths and across the widest ranges of environmental conditions (that is, temperature, salinity, oxygen, pressure), and they represent a huge reservoir of
undiscovered biodiversity (Brandt et al. 2007, Todo et al. 2005). A recent study conducted in
the deep Mediterranean sea provide the first evidence of a metazoan life cycle that is spent entirely in permanently anoxic sediments (Danovaro et al. 2010).
Due to their the size and remoteness, the deep-sea ecosystems on the seafloor have historically been very poorly studied, and although the census of deep-sea life is in its infancy,
there is increasing evidence that the deep-sea ecosystems host the largest proportion of yet-tobe discovered biodiversity on our oceans; most of this biodiversity is likely to be accounted
for by small invertebrates. For example, more than 80% of the hundreds of species of seafloor
invertebrates collected at any abyssal station are new to science (Bouchet 2006, Glover et al.
2002, Martinez and Schminke 2005; Snelgrove and Smith 2003). As of today, the bulk of
these species remains undescribed, especially for smaller organisms and prokaryotes. Local
diversity (i.e., on spatial scales 0.1–1 m2) in deep-sea sediments can be moderate to high (e.g.,
with 50 species for every 150 individuals of polychaetes, and more than 100 macrofaunal
species per 0.25 m2; Bouchet 2006, Smith and Demoupolos 2003) and appears to be correlated with energy availability, much as it is in many terrestrial and shallow marine ecosystems
(Gaston 2000). However, like in other ecosystems (Gaston 2000), the mechanisms behind this
diversity–energy relationship are not obvious.
The taxonomic composition, size, diversity patterns and functioning of deep-sea communities are a product of evolutionary legacy and ecological processes. Of the approximately
one million animal species described on the planet, between 95 and 98% are 20 invertebrates
belonging to 30 phyla, although this number is ever increasing. Of these 30 phyla, all but one
– the Onychophora – occur in the ocean, and there is Cambrian fossil evidence that the Ony11
chophora may have once been marine. Echinoderms are found only in marine systems and
many of the other phyla occur only in water. None of these phyla are exclusively found in the
deep sea, but at a lower taxonomic level several groups of animals make the deep sea special.
In the deep sea, diversity varies on local, regional, and global scales (Levin et al. 2001,
Stuart et al. 2003). The best documented is the unimodal relationship between depth and species diversity (Rex 1981). A variety of biological explanations were proposed for why species
diversity peaks at intermediate depths (1000-2500m) including competition, predation, patch
dynamics, environmental heterogeneity, productivity and combinations of these. Various
processes may regulate species diversity such as speciation rates, climatic variability, productivity, variation in biotic interactions, and habitat heterogeneity (Ricklefs and Schluter 1993).
Mechanisms potentially controlling these macroecological trends are still largely unknown.
Ecosystem functioning involves several processes, which can be summarised as production, consumption and transfer of organic matter to higher trophic levels, decomposition of
organic matter and nutrient regeneration (Danovaro et al. 2008, Naeem et al. 1994). Deep-sea
ecosystem functioning reflects the collective activities of animals, protists and prokaryotes in
exploiting and recycling the inputs of material from the photic zone. However, as they lack
primary photosynthetic production, to a certain extent these systems have simplified functioning, when compared to coastal marine ecosystems. Investigations from terrestrial and shallow
water ecosystems suggest that altering the composition of communities has a strong potential
to alter ecosystem functioning: biodiversity loss might impair the functioning and sustainability of ecosystem (Hooper et al. 2005, Solan et al. 2004). A recent study of the relationship
between ecosystem functioning and biodiversity in the deep sea has shown that a higher biodiversity supports increased efficiency and higher rates of ecosystem processes (Danovaro et
al. 2008).
The mechanisms involved in the biodiversity effects on ecosystem functioning are typically grouped into two main classes of biodiversity effects (Loreau 2008):
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i) complementarity: this occurs when species in a mixed community perform better on
average than expected from their performances in monoculture, thereby contributing to enhanced ecosystem processes;
ii) selection: this occurs when specific species tend to dominate, thereby contributing to
either enhancing or deteriorating the ecosystem processes, depending on whether a better performing or a lesser performing species dominates.
The relative contributions of these two effects towards the results obtained in biodiversity experiments have been highly contentious, because they each have very different implications for the mechanisms that maintain the diversity in natural assemblages. However, studies
that have been conducted in deep-sea ecosystems have revealed, that the functioning of these
ecosystems is positively and exponentially related to their biodiversity in all deep-sea regions
investigated. While different mechanisms can contribute to the relationships between saturating biodiversity and ecosystem functioning, only positive species interactions are known to
yield accelerating relationships, and thus to generate exponential relationships (Bruno et al.
2003).
Many species modify their local environment and facilitate neighbouring species simply
through their presence (Bruno et al. 2003). Experimental investigations from a wide variety of
habitats have demonstrated the strong effects of facilitation on individual fitness, on population distribution and growth rates, on species composition and diversity, and even on landscape-scale community dynamics (Stachowicz 2001). The application of facilitative interactions is perfect for the deep-sea ecosystems, as results that have been reported from these ecosystems suggest that many deep-sea species can benefit from the presence of others, leading
to mutual enhancement of their performances. Exponential relationships are also found when
different biodiversity measures (including the richness of all of the higher fauna taxa) and independent measures of ecosystem functioning are used. Exponential relationships have been
observed in all of the different deep-sea regions investigated: the sub-tropical Pacific Ocean,
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the temperate north-eastern Atlantic, the warm deep Mediterranean, and the cold deep Antarctic (Danovaro et al. 2008).The systems investigated have shown different assemblage compositions, and environmental conditions (e.g., from very cold to warm, from very oligotrophic to
meso-eutrophic, different salinities, different topographic settings). These data have indicated
that exponential relationships are clearly independent of environmental conditions and constraints.
Similar data have been obtained in investigations of the relationships between deep-sea
ecosystem efficiency (which reflects the ability of an ecosystem to exploit the available energy -food sources- and thereby to maximise the biomass and its production; Loreau et al.
2001, Naeem et al. 1994) and benthic biodiversity. All of the independent indicators of ecosystem efficiency (e.g., ratio of fauna biomass to organic C fluxes, ratio of prokaryote C production to organic C flux, ratio of total benthic meiofauna biomass to biopolymeric C content
in the sediment) have been significantly and exponential related to benthic biodiversity. Overall, these findings indicate that the exponential relationships between deep-sea biodiversity
and ecosystem functioning and efficiency are consistent across a wide range of deep-sea ecosystems. Therefore, they reflect interactions between organism life and deep-sea-ecosystem
processes that occur on a global scale (Danovaro et al. 2008).
Recent studies have emphasised the importance of functional diversity traits that influence ecosystem functioning (Loreau et al. 2001, Tilman et al. 2001, Heemsbergen et al.
2004). Understanding how species interactions influence the relationships between biodiversity and ecosystem functioning or efficiency implies a thorough knowledge of the processes regulating deep-sea benthic food webs and the ecological role of each species.
In deep-sea sediments, species number and diversity of functional traits are directly and
positively related, so that changes in species richness apparently have a direct effect on functional diversity and related ecological processes. Taken together, these relationships suggest
that more diverse deep-sea systems are characterized by higher rates of ecosystem processes
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than less diverse systems, as well as by an increased efficiency with which these processes are
performed.
Although experimental approaches are the only tools to unequivocally demonstrate the
effects of biodiversity loss on deep-sea-ecosystem functioning, one case study from the deep
eastern Mediterranean identified a clear link between ecosystem functioning and functional
diversity (Danovaro et al. submitted). After the extreme climate event known as the Eastern
Mediterranean Transient, which caused a rapid change in water salinity and temperature (by
ca. 0.4 °C), significant changes in species compositions were seen. In particular, ca. 50% of
the species that were present before this episodic event were replaced. These changes resulted
in a decrease in the functional diversity (by ca. 35%), which, in turn, was linked to a decrease
in the benthic fauna biomass (ca. 40% reduction). Moreover, despite the apparent enhanced
input of organic nutrients associated with the Eastern Mediterranean Transient, a major decrease in the prokaryote biomass (by >80%) was seen, along with a significant accumulation
of organic C and N, which reflects a strong decrease in ecosystem functioning (e.g., nutrient
regeneration rates) (Danovaro et al. 2001). These data have promoted the hypothesis that there
is a direct link between ecosystem functioning and deep-sea biodiversity, and they support the
correlative finding that a reduction in biodiversity appears associated with an exponential decline in ecosystem processes.
There are several ways in which deep-sea benthic biodiversity (i.e., a higher functional
diversity) can promote ecosystem processes (Danovaro et al. 2004, Ptechey and Gaston
2006):
i) a higher benthic diversity might increase bioturbation, with a consequent increase in
benthic fluxes (Lorher et al. 2004, Meysman et al. 2006) and redistribution of foods within the
sediment (i.e., meiofauna, in particular for their numerical importance, Nematodes and Foraminifera are responsible for the crypto-bioturbation; Giere 2009, Pike et al. 2001);
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ii) a higher species richness can stimulate prokaryote carbon (C) production to a greater
extent than selective grazing by a few species (De Mesel et al. 2004);
iii) higher biodiversity levels can also promote higher rates of detritus processing, digestion and reworking, thus resulting in faster rates of organic matter re-mineralisation;
iv) higher numbers of predator species might influence the structural and functional diversity of meio-, macro- and megafauna assemblages, by preying selectively on the larvae of
organisms displaying lower mobility (Giere 2009).
The global scale of the biodiversity crisis has stimulated explorations into the relationships between biodiversity, productivity, stability and services in different ecosystems of the
World. The effects of biodiversity loss on ecosystem functioning have been the focus of an
explosion of research over the past decade, and several studies have predicted that species loss
will impair the functioning and sustainability of terrestrial ecosystems (Hooper et al. 2005,
Loreau et al. 2001, Naeem et al. 1994, Worm et al. 2006); however, this research field has
been explored only very recently in the deep sea. Now we have evidence that climate change
and human activities can also have severe impacts on deep-sea ecosystems (Glover and Smith
2003).
Understanding the relationships between biodiversity and deep-sea ecosystem functioning is therefore crucial for understanding the functioning of our biosphere.
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