Ecosystem function and services provided by the deep sea

Abstract

The deep sea is often viewed as a vast, dark, remote,
and inhospitable environment, yet the deep ocean and
seafloor are crucial to our lives through the services that
they provide. Our understanding of how the deep sea functions
remains limited, but when treated synoptically, a diversity
of supporting, provisioning, regulating and cultural
services becomes apparent. The biological pump transports
carbon from the atmosphere into deep-ocean water masses
that are separated over prolonged periods, reducing the impact
of anthropogenic carbon release. Microbial oxidation
of methane keeps another potent greenhouse gas out of the
atmosphere while trapping carbon in authigenic carbonates.
Nutrient regeneration by all faunal size classes provides the
elements necessary for fueling surface productivity and fisheries,
and microbial processes detoxify a diversity of compounds.
Each of these processes occur on a very small scale,
yet considering the vast area over which they occur they become
important for the global functioning of the ocean. The
deep sea also provides a wealth of resources, including fish
stocks, enormous bioprospecting potential, and elements and
energy reserves that are currently being extracted and will
be increasingly important in the near future. Society benefits
from the intrigue and mystery, the strange life forms, and the
great unknown that has acted as a muse for inspiration and
imagination since near the beginning of civilization. While
many functions occur on the scale of microns to meters and
timescales up to years, the derived services that result are
only useful after centuries of integrated activity. This vast
dark habitat, which covers the majority of the globe, harbors
processes that directly impact humans in a variety of ways;
however, the same traits that differentiate it from terrestrial
or shallow marine systems also result in a greater need for
integrated spatial and temporal understanding as it experiences
increased use by society. In this manuscript we aim to
provide a foundation for informed conservation and management
of the deep sea by summarizing the important role of
the deep sea in society.

Full text

Biogeosciences, 11, 3941–3963, 2014
www.biogeosciences.net/11/3941/2014/
doi:10.5194/bg-11-3941-2014
© Author(s) 2014. CC Attribution 3.0 License.
Ecosystem function and services provided by the deep sea
A. R. Thurber
1
, A. K. Sweetman
2
, B. E. Narayanaswamy
3
, D. O. B. Jones
4
, J. Ingels
5
, and R. L. Hansman
6
1
College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR 97331, USA
2
International Research Institute of Stavanger, Randaberg, Norway
3
Scottish Association for Marine Science, Scottish Marine Institute, Oban, Argyll, PA37 1QA, UK
4
National Oceanography Centre, European Way, Southampton, SO14 3ZH, UK
5
Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth, PL1 3DH, UK
6
Department of Limnology and Oceanography, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
Correspondence to: A. R. Thurber (athurber@coas.oregonstate.edu)
Received: 4 November 2013 – Published in Biogeosciences Discuss.: 25 November 2013
Revised: 19 June 2014 – Accepted: 19 June 2014 – Published: 29 July 2014
Abstract. The deep sea is often viewed as a vast, dark, re-
mote, and inhospitable environment, yet the deep ocean and
seafloor are crucial to our lives through the services that
they provide. Our understanding of how the deep sea func-
tions remains limited, but when treated synoptically, a di-
versity of supporting, provisioning, regulating and cultural
services becomes apparent. The biological pump transports
carbon from the atmosphere into deep-ocean water masses
that are separated over prolonged periods, reducing the im-
pact of anthropogenic carbon release. Microbial oxidation
of methane keeps another potent greenhouse gas out of the
atmosphere while trapping carbon in authigenic carbonates.
Nutrient regeneration by all faunal size classes provides the
elements necessary for fueling surface productivity and fish-
eries, and microbial processes detoxify a diversity of com-
pounds. Each of these processes occur on a very small scale,
yet considering the vast area over which they occur they be-
come important for the global functioning of the ocean. The
deep sea also provides a wealth of resources, including fish
stocks, enormous bioprospecting potential, and elements and
energy reserves that are currently being extracted and will
be increasingly important in the near future. Society benefits
from the intrigue and mystery, the strange life forms, and the
great unknown that has acted as a muse for inspiration and
imagination since near the beginning of civilization. While
many functions occur on the scale of microns to meters and
timescales up to years, the derived services that result are
only useful after centuries of integrated activity. This vast
dark habitat, which covers the majority of the globe, harbors
processes that directly impact humans in a variety of ways;
however, the same traits that differentiate it from terrestrial
or shallow marine systems also result in a greater need for
integrated spatial and temporal understanding as it experi-
ences increased use by society. In this manuscript we aim to
provide a foundation for informed conservation and manage-
ment of the deep sea by summarizing the important role of
the deep sea in society.
1 Introduction
To meet the needs of humans, it is vitally important to im-
prove the management of the Earth’s ecosystems to ensure
their conservation and sustainable use (Millennium Ecosys-
tem Assessment (MA, 2005)). To improve this stewardship
of the natural environment, it has become common prac-
tice to attempt to value ecosystems by assessing their func-
tions and the services they provide to humans (Mace et al.,
2009). This approach differentiates ecosystem functions or
the processes operating in an ecosystem (Loreau, 2008) from
ecosystem services, which are the benefits that people obtain
from ecosystems (Armstrong et al., 2010, 2012). There is of-
ten confusion about the definition of functions and processes
in an ecosystem services context, but they can be treated as
synonyms providing appropriate definitions (Wallace, 2007).
Here we refer to processes and functions as the interactions
that occur between abiotic and biotic elements of ecosys-
tems and habitats. The concept of ecosystem functions and
services are related, whereby functions can be characterized
outside a human context and may (but not all do) provide
Published by Copernicus Publications on behalf of the European Geosciences Union.

3942 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
ecosystem serviceswithdirect or indirect human benefit (Van
den Hove and Moreau, 2007).
The first step in ecosystem services evaluation is to iden-
tify and assess the full range of services provided by an
ecosystem (TEEB, 2010). To guide these discussions, the-
oretical frameworks have been developed to help differen-
tiate, give structure to, and provide the basis on which to
evaluate the variety of ecosystem services (Beaumont et al.,
2005; MA, 2005; TEEB, 2010; UK National Ecosystem As-
sessment, 2011; CICES: Haines-Young and Potschin, 2013;
Liquete et al., 2013). These frameworks attempt to generate
clarity by creating a uniform structure across all ecosystems
and habitats (Wallace, 2007), a development that has been
criticized because it does not follow the reality of the com-
plex and diverse natural world we inhabit (Costanza, 2008).
One of the main problems that the assessment of marine,
and in particular deep-sea, ecosystem services is facing is
that the established frameworks do not provide an appro-
priate structure to classify marine ecosystem services accu-
rately (e.g., Liquete et al., 2013). Notably, the most appropri-
ate description and classification of deep-sea ecosystem ser-
vices was performed by Armstrong et al. (2010, 2012) and
Van den Hove and Moreau (2007); the classification takes
into account the specific characteristics of deep-sea ecosys-
tems and acknowledges the complex and integrated nature
of ecosystem processes as well as the distinct spatial and
temporal scales at which deep-sea ecology and evolution op-
erates. These authors used the Millennium Ecosystem As-
sessment (MA, 2005) as the foundation of their description
(but included abiotic factors that are crucial in the context of
deep-sea ecosystem services), using supporting, provision-
ing, regulating, and cultural services (MA, 2005; Mace et
al., 2009). Supporting services are those that are necessary
to produce other ecosystem services, provisioning services
are products used by humans that are obtained from ecosys-
tems, regulating services are the benefits obtained from the
regulation of ecosystem processes, and cultural services are
the non-material benefits people obtain from habitats and
ecosystems (Armstrong et al., 2010, 2012; CICES, 2012).
In an extensive review of ecosystem services publications
on marine issues (Liquete et al., 2013), the MA (2005) was
the most-used ecosystem services framework, illustrating its
wide and established use in marine ecosystem services as-
sessments. Although this framework has been criticized as
reducing the focus on mechanisms underpinning the sys-
tem (e.g., O’Neill, 2001), the ecosystem function and ser-
vices assessment framework(MA, 2005) givesdecision mak-
ers a mechanism to identify options that can (1) improve
the achievement of human development and sustainability
goals, (2) better the understanding of the trade-offs involved
– across sectors and stakeholders – in decisions concerning
the environment,and (3) align response options with the level
of governance where they can be most effective. Moreover,
the separation inherent to this framework allows for the clear
identification of deep-sea functions and services needed to
establish the mechanistic links that will increase our under-
standing of how deep-sea functions and services contribute
to human welfare.
The deep sea, defined here as waters and seafloor deeper
than 200m (Gage and Tyler, 1991), is the largest environ-
ment on Earth – the seafloor represents 63 % of the area and
the water column represents ∼ 98.5% of the volume of the
planet that can be permanently inhabited by animals. Its role
in driving nutrient regeneration and global biogeochemical
cycles is essential for sustaining primary and secondary pro-
duction in the oceans (Danovaro et al., 2008b). In addition,
it supports a high diversity of habitats and species (Hessler
and Sanders, 1967; Grassle and Maciolek, 1992; Sogin et
al., 2006; Ramirez-Llodra et al., 2010; Mora et al., 2011)
as well as huge mineral resources (Herzig and Hannington,
1995; Kato et al., 2011). Deep-sea habitats receive much less
attention than environments closer to home, as they are in-
hospitable to humans, remote and there are numerous chal-
lenges associated with studying this environment directly. As
a result, this has delayed the acknowledgement of the vitally
important ecosystem functions and services the deep sea pro-
vides (but see Armstrong et al., 2012). Unfortunately, this
comes at a time when services from the deep sea are in in-
creasing demand and under great pressure for its products
(Mengerink et al., 2014), such as those from fishing, hydro-
carbon extraction, and mining, all of which are expanding
(e.g., Morato et al., 2006; Benn et al., 2010). Furthermore,
the buffering capacity of the deep ocean is vital for miti-
gating the climatic changes caused by anthropogenic emis-
sions. Here we review current knowledge on the functions
and services provided by the deep sea, providing a founda-
tion of knowledge for effective management, while identify-
ing the traits that differentiate deep-sea habitats from other
global biomes. Whilst it is not our intention to provide a
comprehensive classification of deep-sea ecosystem services
that fits with existing frameworks, we want to provide the
reader with an overview of the importance of the functions
and/or processes that take place in the deep sea, the complex-
ity and integration of these processes and their scalability,
and how they contribute to ecosystem services that benefit
humankind.
1.1 Major deep-sea habitats
The pelagic deep sea below 200m comprises ∼ 95 % of
the volume of the ocean and harbors on the order of 10
28
prokaryotes (Whitman et al., 1998), a great diversity of fish,
and large pelagics such as the infamous giant squid (Archi-
teuthis spp.). In addition, this habitat provides a foraging
ground for surface predators including fish, pinnipeds, and
cetaceans. In general, this high-pressure, dark environment
is primarily cold and well oxygenated. However, wide en-
vironmental variations do occur throughout the deep ocean,
including the hypoxic to anoxic waters of oxygen mini-
mum zones (OMZs); these relatively small areas (∼ 0.1%
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3943
of the ocean’s volume; Codispoti et al., 2001) harbor signif-
icant biogeochemical processes including denitrification and
anaerobic ammonium oxidation (anammox; Paulmier and
Ruiz-Pino, 2009; Lam and Kuypers, 2011). Other chemically
and thermally diverse deep-sea pelagic habitats include hy-
drothermal vent plumes (de Angelis et al., 1993; Dick et al.,
2013) and the water column above cold seeps (Wakeham et
al., 2003; Tavormina et al., 2008) that are hotspots of micro-
bial diversity and are an area where the pelagic environment
gains energy from the seafloor. While this may be the largest
habitat on the globe, it also remains the least known and un-
derstood.
The deep-sea floor is generally made up of soft-sediment
habitats that are treated as different environments based on
their depth. The continental margins extend from a water
depth of ∼ 200 to ∼ 4000m, whilst the abyssal plains occur
from ∼ 4000 to 6000 m (Smith et al., 2008; Levin and Day-
ton, 2009; Ramirez-Llodra et al., 2010). Combined, these
two habitats account for ∼ 85% of the total deep seafloor.
Separating the ocean basins are large underwater volcanic
mountain ranges, which are termed mid-ocean ridges. These
chains extend up to 55000km in length and cover ∼ 9.2%
of the ocean floor (Ramirez-Llodra et al., 2010). In con-
trast to these topographic highs, deep valleys, or trenches,
are formed along subduction zones, where they punctuate the
bathyal and abyssal habitats and range in depth from 6000 to
11000m and cover 2× 10
6
km
2
(Harris et al., 2014).
In addition to broad-scale deep-sea habitats, there are
manysmaller habitats that add to the heterogeneity and diver-
sity of the deep sea. Some of the more pervasive, important
regional habitats include seamounts, canyons and channels,
fjords, hydrothermal vents, and methane seeps (Ramirez-
Llodra et al., 2010; Treude et al., 2011; Fig. 1). Seamounts,
large underwater mountains, occur either singularly or as a
chain and rise up in stark contrast to the surrounding “fea-
tureless” seafloor (Rowden et al., 2005; Narayanaswamy et
al., 2013). These undersea mountains comprise a mixture
of soft and hard substrata and often harbor numerous frag-
ile, vulnerable and long-lived epifauna that create areas of
high biodiversity and rich fishing grounds (Clark et al., 2008,
2010; Chivers et al., 2013; Fig. 1f) that together cover 3 % of
the globe (Harris et al. 2014). Canyons form deep incisions
on the margin, where they act as conduits for shelf–slope ex-
change and create essential habitats for the local fauna (Sardá
et al., 2009; de Leo et al., 2013; Fig. 1a) while making up
25% of the continental margins (Harris et al., 2014). They
are also regions of increased biomass and productivity (de
Leo et al., 2010, 2013; Vetter et al., 2010) and are subject
to disturbances such as when dense water from the shelf de-
scends down the continental slope (Canals et al., 2006) or via
mass wasting events(de Stigter et al., 2007). Chemosynthetic
habitats, including vents and seeps, have a very distinct high-
density faunal community associated with them (Fig. 1e).
Although they do not necessarily have a high level of diver-
sity, they do exhibit a high level of endemism; an endemism
Figure 1. Examples of the species and habitats found in, and
art work inspired by, the deep sea. (A) A field of the protists,
Bathysiphon filiformis in Kaikoura Canyon, NZ (credit: D. Bow-
den (NIWA)); (B) a large authigenic carbonate at Hydrate Ridge,
CA, USA being used as a refuge by rockfish, Sebastes sp. (courtesy
of L. Levin); (C) the basket star, Gorgonocephalus caputmedusae,
was the first species ever sampled from the deep sea. (D) Art has
been inspired by the strange fauna of the deep sea for many years.
This is an example by Lily Simonson (http://oldgenres.com/), who
uses deep-sea fauna as a muse for her paintings. (E) Hydrothermal
vents provide areas of intense secondary production and potential
resources for mining (courtesy of B. Grupe/R. Lee). (F) Ecosystem
engineers, such as these deep-sea corals, provide both jewelry as
well as areas of increased secondary production and demineraliza-
tion (credit: Department BIS, UK).
that appears to increase with increasing depth (Levin et al.,
2000). Estimates vary for how many of each of these indi-
vidual habitats exist; for example, the total number of known
seamounts increases with satellite and sub-sea surface explo-
ration (Morato et al., 2013, and references therein) and other
habitats are constantly being created (Biastoch et al., 2011),
both of which increase the number of known deep-sea fea-
tures.
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3944 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Biogenic habitats, areas of extensive three-dimensional
structure created by organisms themselves, can cover tens of
square kilometers of the deep seafloor (Fig. 1a and f). The
structure of these habitats and the actions of their denizens
can change according to the surrounding environment by
shifting near-bed hydrodynamic regimes, aggregating or-
ganic matter and changing sediment characteristics (Roberts
et al., 2006). Biogenic habitats often harbor high diversities
of associated species as a result of increasing habitat diver-
sity (for example providing hard and stable substratum for
benthic organisms) and access to enhanced dietary resources,
and provide a refuge from predators or physical disturbance.
Owing to several of these characteristics, biogenic habitats
provide a nursery for several deep-sea species including fish
(Miller et al., 2012).
Probably the best known example of biogenic habitat in
the deep sea is created by cold-water corals. Scleractinian
(e.g., Lophelia pertusa, Madrepora oculata; Fig. 1f), gor-
gonian and antipatharian corals can form complex hard struc-
tures with their skeletons (Roberts et al., 2006). These reefs
occur globally in deep waters (> 300m depth) and are col-
onized by a huge range of benthic and demersal organisms
(Serpetti et al., 2013). In addition, many other examples of
biogenic habitat occur in the deep sea. Habitats formed of
large sponges and their spicules occur in many high-latitude
areas (Rice et al., 1990; Gutt and Starmans, 1998; Klitgaard
and Tendal, 2004; Hasemann and Soltwedel, 2011). Seabed
fluid flow can often support large complex habitats com-
prised of clams, mussels and tube worms (Van Dover, 2000;
Cordes et al., 2010a, b). Deep-sea deposit feeders, such as
thalassinid shrimps and worms (including polychaetes, echi-
urans and sipunculans), create extensive burrow systems that
irrigate and transport organic material into subsurface sedi-
ments (Levin et al., 1997; Hughes et al., 2005; Shields and
Kedra, 2009), resulting in a complex three-dimensional sed-
imentary matrix providing particular niches for other ben-
thic fauna such as the microscopic meiofauna and microbes
(e.g., Braeckman et al., 2011; Laverock et al., 2011). Mo-
bile epifaunal megabenthic organisms can create and modify
seabed habitats in high densities, especially urchins (echi-
noids; Vardaro et al., 2009) and sea cucumbers (holothuri-
ans; Billett et al., 2010), and large beds of featherstars
(crinoids; Bowden et al., 2011). Even large-sized single-
celled eukaryotic microorganisms, protists, can form exten-
sive habitats and alter local biodiversity. These include xeno-
phyophore (a multinucleate protist) grounds in many deep-
water areas (Levin, 1991) and beds of the tube-forming pro-
tist Bathysiphon filiformis in submarine canyons (De Leo et
al., 2010; Fig. 1a).
1.2 Diversity and ecosystem function
It is now well acknowledged that the deep sea has a relatively
high diversity (Hessler and Sanders, 1967; Grassle and Maci-
olek, 1992; Rex and Etter, 2010), although this can vary dra-
matically depending on the habitat being investigated (Levin
et al., 2001). A general positive relationship has been estab-
lished between diversity and ecosystem functioning and ef-
ficiency in a wide range of deep-sea ecosystems. However,
the strength of this diversity–function relationship may differ
substantially among habitats (Danovaro et al., 2012). For in-
stance, in deep-sea sediments, species richness and diversity
of functional traits are positivelyrelated to changes in species
numbers affecting functional diversity and related ecologi-
cal processes such as prokaryote production (Danovaro et
al., 2008b). However, this relationship is stronger on conti-
nental slopes, where reduced diversity may lead to a greater
loss of function in comparison to deep basins (Danovaro et
al., 2012). In other slope areas there is no relationship be-
tween diversity and ecosystem function measurements such
as sediment community oxygen consumption and bacterial
biomass (Leduc et al., 2013). It is often assumed that the pos-
itive relationship between biodiversity and ecosystem func-
tion can reach saturation (Loreau, 2008). After this level has
been reached, there is the potential for species with particu-
lar ecological traits that may enhance the overall functioning
of the ecosystem (including ecosystem engineers, e.g., cold-
water corals) to increase in dominance or for species to be-
come established that may deteriorate ecosystem processes
(e.g., the king crabs found on the western Antarctic Penin-
sula shelf that has reduced megafaunal abundance; Smith
et al., 2012). In addition, it is thought that these more di-
verse systems induce a complementarity between species
with facilitation and resource partitioning leading to overall
higher function (Loreau et al., 2001). Facilitative, or posi-
tive, interactions between species may contribute positively
to ecosystem function, whilst other, more negative, interac-
tions such as selective predation and niche displacement may
counteract an increase in function. Whatever the causal pro-
cesses underlying deep-sea diversity and ecosystem function,
the richness and variety of organisms in the deep sea are
important, as they underpin the many facets of ecosystem
function and the goods and services we ultimately receive
(e.g., biodiversity supports the ability of the deep-sea sedi-
mentary ecosystem to use the photic zone’s primary produc-
tion, its ability to use and recycle organic matter deposited
on the seafloor and its ability to channel detritus to higher
trophic levels; Danovaro et al., 2008b). In addition, biodiver-
sity contributes to ecosystem resilience, a supporting service
(cf. Armstrong et al., 2013), with increased morphological,
genetic and functional diversity leading to greater stability
in terms of being able to respond rapidly to changes in the
environment. A variety of recent papers have discussed this
topic in detail (e.g., Loreau, 2008; Levin and Dayton, 2009;
Leduc et al., 2013). In addition to the aforementioned ser-
vices, we should also note that biological regulation is a reg-
ulating service resulting from biodiversity itself (i.e., inter-
actions between species and genotypes, including biological
pest control, trophic transfer and interactions). Biodiversity
also includes supporting services that need to be considered
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3945
as necessary for the production of all other – more direct –
ecosystem services, including its influence on primary pro-
duction and nutrient cycling (Armstrong et al., 2012).
2 Supporting and regulating functions and services
2.1 Water circulation and CO
2
exchange
Many of the functions and services of the deep sea result
from a combination of its vast size and the long duration of
time that it is separated from the Earth’s atmosphere. The wa-
ter masses that bathe the deep-sea environment are formed
largely in the North Atlantic and the Southern Ocean, with
additional input from the Sea of Okhotsk and the Mediter-
ranean and Red seas. As soon as these cold (mean tem-
perature 4
◦
C) dense water masses sink below the photic
zone, they are cut off from the atmosphere for approximately
1000 years, supplying all the world’s deep ocean areas in the
“global conveyor belt” also known as the “thermohaline cir-
culation” that eventually resurfaces in areas of upwelling and
the North Pacific. This creates more than one billion square
kilometers of water separated from direct contact with the at-
mosphere, allowing an incredible buffering capacity for nu-
trient and carbon cycles. Water circulation is generally rec-
ognized as a supporting service, but it is the buffering ca-
pacity that also renders it a regulating service to the bene-
fit of other ecosystem services such as nutrient cycling, cli-
mate and weather regulation in part and, importantly, CO
2
exchange.
Since the industrial revolution ∼ 300 Gton of the green-
house gas CO
2
has been released by anthropogenic activities
into the atmosphere (Canadell et al., 2007; Fig. 2). The im-
pact of this CO
2
on the temperature of the globe is largely
mediated by dissolution of this gas in the surface ocean
and its transport through the thermohaline circulation into
the deep sea. The deep sea currently stores approximately
37000Gton of carbon and has already absorbed a quarter
of the carbon released from human activities (Canadell et
al., 2007; Sabine and Feely, 2007); this CO
2
absorbance is
a very important regulating service influencing climate and
many other deep-sea functions and services.
2.2 Nutrient cycling and the biological pump
As particles sink through the water column, they are stripped
of their easy-to-digest (labile) compounds, releasing nutri-
ents and energy into the deep sea. This process, termed the
biological pump, both sequesters atmospheric carbon and re-
leases nutrients that eventually fuel production (Fig. 2). The
vast majority of the deep sea relies on this primary pro-
duction that occurs in surface waters (i.e., photosynthesis
by phytoplankton). As these particles sink through the deep
pelagic, they are degraded by microbes and higher trophic
levels, such as zooplankton and especially large gelatinous
fauna (Robison, 2004). This biological activity dictates the
duration that the exported carbon is separated from the at-
mosphere. If biomass is respired in the water column or on
the seafloor, this carbon will be kept out of the atmosphere
until the water rises to the surface again and releases the
carbon back (1000-year timescales). However, if this car-
bon is buried in sediments, the CO
2
is removed from the at-
mosphere for geologic timescales (thousands to millions of
years). Around 55 % of the carbon that sinks below 1000m
is respired in the water column prior to its deposition on the
seafloor (Jahnke, 1996), leaving only ∼ 1% of the carbon
fixedat the surfaceto be deposited on the seafloor (Lutz et al.,
2007); the majority of the carbon fixed at the surface is not
exported into the deep ocean. The quantity of carbon from
the surface water exponentially declines with increasing wa-
ter depth (Martin et al., 1987), although the rate of decline
is location specific with a more rapid decline in oligotrophic
compared to eutrophic waters (Buesseler et al., 2007) and
asymptotic for much of the deep sea. While most of the car-
bon that is deposited is difficult to digest (refractory) (Kiri-
akoulakis et al., 2001), areas of high deposition, including
oxygen minimum zones and areas of river discharge (Berner,
1989, and see the discussion in Cowie et al., 1999), can result
in labile carbon being buried within the seafloor because it is
deposited faster than it can be degraded at the sediment sur-
face. This flux of particles out of the surface waters provides
a second way in which carbon is naturally captured from the
atmosphere and transferred to the deep sea, further mitigat-
ing the climate impacts of CO
2
emission, but over different
timescales. Considering the different processes and functions
associated with nutrient cycling and the biological pump, it
becomes clear that these act both as supporting services (e.g.,
crucial to biomass production in provisioning services) and
regulating services (natural carbon sequestration – reducing
anthropogenic carbon in the atmosphere).
Although we focus on carbon here, the deep-sea environ-
ment plays a key role in the cycling of other nutrients such
as nitrogen, silica, phosphorus, hydrogen and sulfur (Fig. 2).
Specifically with regards to nitrogen cycling, microbially
mediated processes including nitrification, nitrogen fixation,
denitrification, and anaerobic ammonium oxidation occur in
both the pelagic and benthic deep ocean, providing sources,
sinks, and transformation of nitrogen among nitrogen pools
(Gruber and Sarmiento, 1997; Wuchter et al., 2006; Francis
et al., 2007; Ward et al., 2009; Ulloa et al., 2012; Fig. 2).
Nitrogen is selectively removed from dissolved organic ma-
terial throughout biological processing in the water column
and sediments (Bronk, 2002; Hunter et al., 2012), and nitro-
gen cycling in the benthos releases nutrients such as nitrate,
nitrite, and ammonium back into the water column (Lave-
rock et al., 2011). Nutrients regenerated at the seafloor are
ultimately recycled and returned back to the surface through
thermohaline circulation (often in areas of upwelling) for the
process to start again (Fig. 2).
Methane provides another key greenhouse gas whose po-
tency is mitigated through deep-sea biological activity; a
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3946 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Figure 2. Schematic of carbon flow and a subset of the resources and functions of the deep sea. Data include the Keeling and Martin curves
(Martin, 1987) and values from Longhurst (1991), Sabine and Feely (2007), Canadell et al. (2007), and the US EPA. Arrows represent the
flow of matter or carbon and the upwelling of nutrients. Dotted lines are potential or unquantified flows. NO
x
= NO
2
and NO
3
. Not to scale.
molecule of methane is 25 times more efficient at warm-
ing our atmosphere than a molecule of CO
2
(see IPCC
2007). Vast reservoirs of methane exist in the deep sea (455–
10000GtC methane; Kvenvolden, 1993; Klauda and San-
dler, 2005; Reeburg, 2007; Wallmann et al. 2012) and while
most of this potential fuel source is kept trapped either as
or by hydrates, the latter forming by the temperature and
pressure pervasive there, one of the key services provided
by deep-sea communities is the rapid consumption of the
small proportion that is released (Reeburg, 2007; Knittel and
Boetius, 2009). As a result, while methane itself provides
17% of greenhouse gas forcing, oceanic sources currently
only contribute approximately 2–4 % of the methane emitted
into the atmosphere (Judd et al., 2002; IPCC 2007; Reeburg,
2007). The majority of methane that is released from marine
reservoirs is consumed within the sediment, leaving pelagic
communities to oxidize methane only in areas where there
is sufficient methane release to surpass this benthic filter
(sensu Sommer et al., 2006). Often this is caused by geo-
logical activity such as explosive mud volcanoes (Niemann
et al., 2006; Reeburg, 2007), hydrothermal vents and cold
seeps (e.g., Sommer et al., 2010), or inadvertent hydrocar-
bon releases (Valentine et al., 2010; Rivers et al., 2013). As
an added benefit, the anaerobic oxidation of methane leads to
the precipitation of authigenic carbonates, creating an addi-
tional trap of carbon (Aloisi et al., 2002), sequestering it for
an indefinite time period. While this service of consuming
methane may largely be keeping methane sources in check, at
times throughout Earth’s history perturbations have released
these methane reservoirs, causing massive extinction events,
including a loss of > 70% of marine invertebrate species
183mya (Kemp et al., 2005). Thus the marine oxidation of
methane is a function inherent to deep-sea benthic primary
(chemosynthetic) production, which is asupporting function,
but at the same time it provides a regulating service (i.e., re-
ducing geological and biological methane release, promoting
carbonate precipitation and habitat formation) with indirect
benefits to human populations. In addition to benthic pri-
mary production, we also need to consider chemosynthetic
primary production in the pelagic realm, where it constitutes
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3947
a supporting and regulating service as well, as discussed be-
low.
2.3 In situ primary and secondary production
One of the greatest paradigm shifts in the past decade is the
role of chemosynthetic production in non-“extreme” deep-
sea environments (Middelburg, 2011). Organisms attached
to sinking particles produce hydrolytic enzymes that trans-
fer organic material from the sinking particles into the water
column at a rate faster than at which it is consumed (Fig. 2).
This imbalance in enzyme efficiency and consumption re-
sults in a “plume” of fresh dissolved organic carbon (DOC)
that trails these particles as theysink, providing substrates for
planktonic microbes in the deep ocean (Smith et al., 1992;
Vetter et al., 1998). Although the DOC pool in the deep
ocean is approximately equal to that of CO
2
in the atmo-
sphere at around 700GtC, it is largely refractory and inac-
cessible, even to microbes (Hansell et al., 2012). However,
the significantly larger dissolved inorganic carbon (DIC)
pool (∼ 38100GtC) is utilized by microbes in the deep sea
through chemoautotrophic primary production (Ingalls et al.,
2006; Hansman et al., 2009; Herndl and Reinthaler, 2013).
This dark CO
2
fixation is on the order of heterotrophic pro-
duction (Alonso-Sáez et al., 2010; Reinthaler et al., 2010;
Herndl and Reinthaler, 2013), and can be performed by both
bacteria and archaea (Herndl et al., 2005). Chemoautotrophs
require reduced inorganic compounds as energy sources to
fuel DIC fixation, and evidence is mounting that these may
include ammonia, urea, sulfide, and hydrogen (Wuchter et
al., 2006; Swan et al., 2011; Alonso-Sáez et al., 2012; Anan-
tharaman et al., 2013). Many of these compounds are often
provided by the degradation of sinking organic matter.
Ultimately, secondary production, the formation of
biomass fueled by organic carbon degradation and assimi-
lation, is arguably the primary function resulting in the pro-
vision of biomass for human consumption, most notably fin-
fish, shellfish, and cetaceans (treated below in the provision-
ing section). Additionally, this production is the result of res-
piration – where CO
2
is released and oxygen consumed –
and thus is involved in the regulation of gas cycling and car-
bon sequestration in the deep sea. Secondary production is
driven by the quality andquantity of the foodresources avail-
able (Ruhl et al., 2008; Smith et al., 2008). Depth is often
cited as the driving factor of secondary production as a result
of reduced particulate organic carbon (POC) flux at greater
depths; however,interannual variabilityand total surface pro-
duction also impact the distribution of biomass (Ruhl et al.,
2008; Wei et al., 2010). Despite this clear benthic–pelagic
link, deep ocean communities’ carbon demand can exceed
the vertical supply, with this imbalance being potentially met
by lateral advection or by food resources not accounted for in
current assessments (Burd et al., 2010). A similar situation is
observed in submarine canyons and trenches, which act as
depocenters by topographically channeling organic matter,
allowing biomass to exceed that of other deep-sea habitats
by orders of magnitude (de Leo et al., 2010).
While secondary production is difficult to measure di-
rectly, it can be estimated as a function of benthic biomass,
trophic transfer efficiency, and metabolic rate. Compared to
the rest of the marine environment, the deep-sea floor is es-
timated to contain 78.9% of the total benthic biomass; 50%
of total marine benthic biomass is found below 3000m (Wei
et al., 2010). Deep-sea floor biomass is also high at high lati-
tudes, with over a quarter of global biomass contained within
the 13.4% of the seafloor found at > 60
◦
N or S (Wei et al.,
2010). Whilst the nuances of how depth and organic mat-
ter input influence secondary production remain debated, the
total biomass of all benthic size classes generally declines
with increasing water depth from the continental margins
to the abyssal plains. The exceptions to this are bacteria,
which dominate the biomass of the abyssal plain and below
(Wei et al., 2010). Thus the activities of microbes, including
their respiration and biochemical processes (e.g., nitrifica-
tion/denitrification, amino acid oxidation), are a key compo-
nent as to the type and abundance of nutrients released back
into the pelagic realm. These microbes also experience top-
down forcing from viral populations (Suttle, 2005; Danovaro
et al., 2008a) and grazing by many size classes of animals
(e.g., Howell et al., 2003, Ingels et al., 2010). In addition,
the faunal–bacterial interactions within the benthic food web
regulate uptake of C and N (Hunter et al., 2012). The over-
all production by animals is further influenced by predatory
and competitive interactions, facilitation and complementar-
ity among species, and environmental driverssuch as temper-
ature and oxygen availability. For example, low oxygen tends
to reduce macrofaunal abundance and biomass, while lead-
ing to increased densities of meiofauna and bacteria (Levin,
2003). The suite of interactions forms regulatingservices that
affect the magnitude and complexity of secondary biomass
production in the deep sea (and ultimately translates into the
provisionary service of fish, shellfish and other marine bio-
logical products used by humans).
A variety of habitats are created by large deposits of or-
ganic matter, including fish, whale, jellyfish, wood, and kelp
“falls”, creating areas of enhanced secondary and primary
production on the scale of meters to tens of meters. Among
the best studied of these are whale falls, where large cetacean
biomass can support communities that are divergent from
background communities for up to a century (Smith and
Baco, 2003). However, this time period is dependent on the
size of the cetacean and can be an input of energy for less
than a decade. In addition, over these time periods a diver-
sity of successional stages occurs from scavenger, to spe-
cialist fauna and finally with the bones acting as hard sub-
strate for filter feeders. Wood and leaf deposits create an
additional type of similar habitat on shelf, fjord, slope, and
abyssal habitats near wooded continental margins (Wolff,
1979; Pailleret et al., 2007). These terrigenous deposits cre-
ate both an additional type of carbon sequestration, while
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3948 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
providing high levels of primary and secondary production
to the deep-sea floor (Turner, 1977; Bernardino et al., 2010)
and its associated supporting, regulating, and provisioning
services. Somewhat surprisingly, many falls also result in
in situ production. Degrading wood material can stimulate
chemosynthetic production with trophic transfer up to fishes
and lobsters (McLeod and Wing, 2007, 2009), and whale
falls have worms whose heterotrophic symbionts harness the
energy stored in the whales to build their biomass (Rouse et
al., 2004), while free-living bacteria perform a diverse suite
of chemical magic to produce energy for their cell growth
from the whale (Treude et al., 2009).
Methane seep and hydrothermal ventcommunities provide
an outlier of intense secondary production in the deep sea,
both due to high levels of chemoautotrophic primary pro-
duction as well as the abundance of hard substrate in these
habitats. Biomasses of methane-consuming bacteria and ar-
chaea (3molC m
−2
; Boetius and Suess 2004) are directly
consumed by a diversity of metazoans (Levin and Michener,
2002; Van Gaever et al., 2009; Levin et al., 2010; Thurber et
al., 2012, 2013), and the flux of energy out of the benthos,
largely in dissolved form (seep fluids can contain ∼ 22mM
of dissolved organic carbon; Valentine et al., 2005), may
be an important source of support for deep-sea populations.
This results in a vent and seep biomass that far exceeds
that of the background community; vents can be found with
> 70kganimalm
−2
(Gebruk et al., 2000) and seeps can ex-
ceed 30–51kganimalm
−2
(Olu et al., 1996). Even just con-
sidering the microbial community in this context, these habi-
tats are an important sink for oxygen (Boetius and Wen-
zhofer, 2013) and thus both primary and secondary produc-
tion. Furthermore, the hard substrate habitat created by the
microbial processes at seeps provides a habitat for corals and
other ecosystem engineers that create additional hotspots of
secondary production (Cordes et al., 2008; Lessard-Pilon et
al., 2010) and fish (Sellanes et al., 2012; Fig. 1).
2.4 Waste absorption and detoxification
The deep sea provides an area where waste products are
stored as well as detoxified through biotic and abiotic pro-
cesses (note, however, that the deep-sea provision of space
for the dumping or sequestration of waste products is consid-
ered a provisioning service; sensu Armstrong et al., 2010).
Contaminant absorption onto sinking particles (reviewed in
Dachs et al., 2002), dense shelf water cascades (Canals et
al., 2006), and deliberate human activity (Thiel, 2003) trans-
port pollutants from surface waters and continental shelf sed-
iments to the deep ocean basin. These pollutants include
persistent organic pollutants, macro- and micro-plastics,
sewage, and oil, and can sometimes be removed through
bioremediation, that can be facilitated by bioturbation. Bio-
turbation is considered a regulating service in the sense that
– through biogenic mixing of sediments by burrowing or-
ganisms – it regulates the decomposition and/or sequestra-
tion of organic wastes (Armstrong et al., 2012). Of special
note to bioremediation are the organic pollutants; these ac-
cumulate in the tissue of higher predators that are harvested
and thus remain a threat to humans. While pollutants trans-
ported to the deep sea could be viewed as a benefit, since
it removes them from being in contact with food stocks that
are harvested from the surface ocean, deep-sea fish live much
longer, allowing for a greater time to concentrate these com-
pounds, meaning that when deep-sea fish are harvested they
can provide a concentrated source of pollutants to human
consumers through bioaccumulation. Therefore the deposi-
tion and assimilation of these compounds in the deep sea
is a temporary regulatory service if viewed as a service at
all (Froescheis et al., 2000; Looser et al., 2000). A variety
of biotic processes can detoxify “waste” or potential pol-
lutants contributing to the regulating service of biological
waste remediation in the deep sea. A recent example of this
occurred during the 2010 Macondo oil spill (also known as
the Deepwater Horizon Spill) where members of the deep-
sea microbial community in the Gulf of Mexico were capa-
ble of degrading hydrocarbons and gases released from the
well (Valentine et al., 2010; Lu et al., 2012; Crespo-Medina
et al., 2014), and recently more bacteria with the potential
to oxidize hydrocarbons have been recognized (Kube et al.,
2013; Naether et al., 2013).
While biological bioremediation and detoxification of
compounds in the deep sea are considered regulating services
(partially driven by biodiversity; see Sect. 1.2), the space
that the deep sea provides to dispose of waste or sequester
CO
2
artificially (inherently an abiotic element) is considered
a provisioning service (Armstrong et al., 2010; see Sect. 3.4).
3 Provisioning services
3.1 Fisheries/nutrition
One of the most tangible ecosystem services from the deep
sea are fish stocks, which are increasingly finding their way
into human diets. Overexploitation of shallow water and
shelf-depth fish stocks has led to an increase in the harvest-
ing of deeper fish stocks over the past 40 years (Morato et
al., 2006, 2013). These deep-sea fisheries are one mecha-
nism by which the energy contained in fish species from be-
low 200m, and in certain cases below 1000 m (Bailey et al.,
2009), is transferred back to the surface water and ultimately
into the human food cycle. Currently at least 27 species of
fish are harvested in the deep sea (Norse et al., 2012), and
the mean depth of fishing is increasing at a rate of 62.5 m
per decade (Watson and Morato, 2013). However, in many
cases, these fisheries are not deemed sustainable owing to
the incredibly slow growth of the species of interest (cer-
tain fish live > 100 years; Cailliet et al., 2001), the large by-
catch of non-target species produced by certain fishing gears
(Norse et al., 2012), and populations showing major declines
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3949
(Bailey et al., 2009). While some fisheries are more suscep-
tible to overharvesting than others and in some cases pro-
tective area management is implemented, even exploitation
under precautionary management practices may nevertheless
lead to a population decline, such as the case of the orange
roughy off New Zealand, which has remained harvestable but
is still in decline (Norse et al., 2012). One of the few ex-
ceptions is an artisanal fishery for black scabbardfish, which
has not experienced the same decline as most other deep-
water fish stocks (Norse et al., 2012). While the stocks them-
selves are the target, the use of trawls to capture these fish can
greatly impact the services provided by the deep sea owing
to damage of three-dimensional seafloor structures (Roberts,
2002; Puig et al., 2012) and the resulting impacts on biodi-
versity,carbon turnover, and abundance and biomass of fauna
(Pusceddu et al., 2014). In addition, illegal, unregulated, and
unreported fishing practices undermine sustainable fisheries
management at a substantial social and economic cost (Floth-
mann et al., 2010).
However, one of the main links between global fisheries
and the deep sea results from nutrient regeneration. The most
productive fisheries in the world occur in areas of strong up-
welling, where deep-sea nutrients are brought back to the
surface where they fuel photosynthetic production and har-
vested food stocks (Fig. 2). Fisheries in these areas are some
of the most productive on the planet, including the sardine
and anchovy fisheries off South America, which have pro-
duced over 10 million and 5 million tons of fish, respec-
tively, during certain years (GLOBEC NMFS 1996). In ad-
dition, many cetacean, pinniped, and fish species, including
sperm whales (Physeter macrocephalus) and elephant seals
(Mirounga spp.), forage in the deep sea even though they are
(or historically have been) caught in surface waters.
3.2 Oil and gas/energy
Once oil and gas reserves on land had been proven prof-
itable, industrial exploitation of this resource quickly moved
into shallow marine areas and, in the 1960s, into offshore ar-
eas. As easily accessible resources declined, technology for
offshore drilling improved, and large reserves of hydrocar-
bons were found, the oil and gas industry moved into deeper
and deeper waters. In the Gulf of Mexico, major reserves
are being accessed in waters as deep as 3000m. Currently
drilling for oil and gas is routine in the deep sea (UK > 9000
wells> 30m depth and 328 > 200 m depth – data from the
UK Department of Energy and Climate Change; Norway
1390> 30m and 546> 200m depth – data from the Norwe-
gian Petroleum Directorate; Gulf of Mexico 3800 offshore
wells – data from the National Ocean and Atmospheric As-
sociation), with major deep-water production in areas such as
the Arctic, northern North Atlantic (UK and Norwegian wa-
ters), east and west Africa, Gulf of Mexico, South America,
India, Indonesia, and Australia. Oil and gas revenues from
offshore areas are enormous: the industry is a major em-
ployer, and technological developments have many ramifica-
tions for other deep-water industries. Clearly, although this
provisioning service is important, exploitation of these re-
sources needs to proceed with caution to avoid major broad-
scale disturbance to the deep-sea environment, as shown dra-
matically by the destruction of Deepwater Horizon and the
subsequent oil spill from the Macondo well affecting a large
area of the Gulf of Mexico (White et al., 2012; Montagna et
al., 2013).
While oil represents a utilized service, vast deposits of
methane on the seafloor may be a fuel that can bridge the
gap of dwindling oil supplies prior to more sustainable solu-
tions being implemented. As a result of anaerobic respiration
in the deep-sea floor by archaea, the reservoirs of methane
discussed above are produced and trapped in the deep subsur-
face or, under certain circumstances, form methane hydrates
on or below the seafloor. These reserves are extremely ex-
tensive in some areas, including the Arctic, and are globally
estimated to hold twice the combustible carbon known from
all other fossil fuels (Klauda and Sandler, 2005; Wallmann
et al., 2012). Commercial exploitation of methane hydrates
is an advancing technology, adopting similar methods to tra-
ditional oil and gas drilling activities, and several industrial
concerns are considering commercial exploitation of this re-
source on a large scale. While the exploitation of methane
reservoirs is being developed further, the potential of hydro-
gen generation, subsequent mixing of the produced hydro-
gen with natural gas, its transport via the existing pipeline
network and the introduction of it into existing subsurface
storage facilities as an energy reserve to be called upon in
the future are also being considered (Schmitz, 2011; Pichler,
2013).
In addition to oil and gas, there are other ways in which
energy can be extracted from the deep sea. One example is
the collection of power from the hydrothermal vent fields
using thermoelectric generators, either by tapping a temper-
ature gradient directly from the plumes of a hydrothermal
vent, or using high-pressure thermosyphons installed in a
well on the hydrothermal mounds (Parada et al., 2012). Since
the 1980s, ocean thermal energy conversion (OTEC) tech-
nology has provided the opportunity to harness the tempera-
ture differences between cool surface water and colder deep-
sea water to create electricity, and it is estimated that OTEC
is theoretically capable of providing 4000 times the global
energy need (Vega, 2002). The interest in the implementa-
tion of such technology on industrial scales is rising quickly
with increasing energy demand globally (Yeh et al., 2005)
and several (test) plants are planned or proposed worldwide
(Knight, 2014), although there are still doubts as to the eco-
nomic and logistic feasibility of the technology. However, on
Kume Island in Okinawa, Japan, OTEC has been tested at a
50kW plant since April 2013, whereby deep water (600m) is
pumped up to be used in convection turbines, and in Ansan,
South Korea, a 20kW plant is operated only in summer
when the temperature difference between surface and deep
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3950 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
water exceeds the 20
◦
C minimum (Knight, 2014). Aside
from energy, there are multiple uses for the pathogen-free
and nutrient-rich cold seawaterpumped up from the deep sea,
such as mariculture, refrigeration, air conditioning, and the
production of potable water (Dylan, 1995; Yeh et al., 2005).
Despite the perception of OTEC technology as being sus-
tainable exploitation of renewable energy, the construction of
the needed large-scale deep-water infrastructure and poten-
tial alteration of oceanic thermohaline circulation because of
necessary massive OTEC seawater flow rates (Nihous, 2007)
means that it is a potential threat to other functions and ser-
vices the deep ocean provides.
3.3 Mining/non-nutritional materials
A variety of processes in the deep sea leads to large areas
of concentrated metals reserves on the abyssal floor, at hy-
drothermal vents, and in certain areas covered by rich crusts
of minerals (e.g., Hein et al, 2013). Many of these metals are
integral to current electronics, and since terrestrial supplies
are dwindling and/or becoming harder to extract, deep-sea
mineral resources are likely to be extensively mined within
the next few decades. Precipitation of manganese, phosphate,
and other metals around seed particles under deep-sea con-
ditions over timescales of millions of years has produced
extensive deposits of fist-sized polymetallic nodules (reach-
ing densities of hundreds per m
2
) and crusts (thin (< 20cm)
surficial deposits). Although these deposits occur across a
lot of the world’s deep water areas (Table 1), the ore qual-
ity and nodule density varies and the most likely commer-
cial deposits are found in the Clarion–Clipperton Fracture
Zone (CCFZ) in the Pacific Ocean (Glover and Smith, 2003).
Seabed fluid flow and precipitation of geological minerals
at the seafloor (for example at hydrothermal vents) has led
to the creation of massive seafloor sulfides (SMS deposits
or volcanogenic massive sulfides/VMS as it is often called
within the mining literature), which contain high-grademetal
ores in significant and commercially attractive quantities.
The deep sea also contains areas of sediment rich in metals
(Atlantis II Deep, Red Sea; Thiel, 2003), significant phos-
phorus deposits (Cullen, 1980; Thiel, 2003) and sediments
elevated in rare Earth elements (Kato et al., 2011), which
may all also be profitable to exploit. Commercial-scale min-
ing of deep-sea mineral deposits has been considered and tri-
aled since the 1970s. There are current exploration claims
and active investigation throughout the CCFZ for manganese
nodules, on the Mid-Atlantic Ridge (for SMS deposits) and
production activities beginning imminently in Papua New
Guinea (SMS; Nautilus Minerals). Mining is not limited to
utilitarian resources; cold water corals supply both a provi-
sioning as well as cultural service as they are harvested for
jewelry (Foley and Armstrong, 2010).
3.4 Waste disposal
The vast depth of the deep sea makes it an area that has been
used as a dumping ground for many types of waste, including
radioactive substances, munitions, animal carcasses (Mor-
ton, 2003), sewage sludge, plastics, mine waste (reviewed
in Thiel, 2003, and Ramirez-Llodra et al., 2011, 2013, but
see Pham et al., 2014, for the most recent report on human
waste in the deep sea), and munitions disposal (Thiel, 2003;
HUMMA final report, 2010), in addition to being a sink or
deposition area for pollutants and organic wastes. If these
compounds accumulate on the seafloor, or are buried within
the sediment, the habitats provide a more long-term benefit
to society as a provisioning service. The slow turnover time
of the deep sea (1000 years) and the low oxygen concentra-
tion (relative to air) mean that many substances disposed of
in the deep sea will be sequestered in relatively stable states
for long periods of time, during which some may be bro-
ken down into non- or less harmful substances (through de-
composition, rusting and the aforementioned detoxification,
which are regulating services; see Sect. 2.4). However, this
detoxification is substance specific; some chemical weapons
(of which there are some 150000 tons that were disposed of
in marine habitats) will degrade and others retain their po-
tency (Thiel, 2003). Of note, while the deep sea has been
an area where radioactive waste has been disposed of (Thiel,
2003), no biotic or abiotic processes degrade or ameliorate
the problems associated with this type of waste. In addition,
certain munition deposits are known to cover several km
2
per deposit, and have occurred in many locations around the
world (see the review by Thiel, 2003).
The deep sea has also been considered a potentialdumping
ground for gas, because at the high pressures and low tem-
peratures found there, certain gases, including CO
2
, form a
fluid, easing its sequestration. However, depositing CO
2
in
this manner leads to the acidification of surrounding waters,
with detrimental impacts on marine life (Thistle et al., 2006,
2007; Bernhard et al., 2009). These impacts may limit the
expansion of CO
2
deposition in the deep sea from an ex-
perimental to a realized service. A more plausible solution
is to use carbon capture and storage whereby CO
2
is cap-
tured and then stored under the seafloor in depleted oil, gas,
or gas hydrate reservoirs or deep saline aquifers. Recently,
however, concerns about potential leakage of CO
2
and es-
cape of formation water for the benthic environment have
been investigated in numerous scientific projects (Wallmann
and Bialas, 2009). It is also important to note that as we are
seeing increasing exploitation of deep-sea resources, the ar-
eas that may currently seem opportune areas for depositing
waste may be future areas of bioprospecting or fishing, activ-
ities that could be hampered by waste disposal efforts.
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3951
Table 1. The distribution of regulating and provisioning services among the habitats present in the deep sea. Blank= unknown or not present.
P= present. W = widespread or abundant.
Abyssal Biogenic Can- Deep Margins Mid-ocean Sea- Tren- Vents and
plains habitats yons pelagic ridges mounts ches seeps
Alternative energy sources P P P P P P
Bioprospecting P P P P P P P P W
Carbon capture and disposal P W P
Communication cables P P W P P
Fisheries W W P W W W
Metal-rich sediments P
Methane harvesting W P P
Military P W P P
Oil and gas extraction W
Phosphate mining P
Polymetallic crusts W W P
Polymetallic nodules W
Rare Earth elements P
Seafloor massive sulfides P P W
Waste disposal W W P W P
3.5 Bioprospecting
Resources in the deep sea are increasingly being exploited by
bioprospecting, or the search for natural products within bi-
ological resources. The deep ocean is the source of a number
of novel natural products isolated from the highly diverse and
species-rich deep-sea faunal communities (Skropeta, 2008),
in particular from those found at hydrothermal vents (Thorn-
burg et al., 2010; Martins et al. 2013). As of 2008, 78 natural
products have been isolated from as many as 19 classes and
from all Domains of life (Skropeta, 2008). These chemicals
show potential for having pharmaceutical properties and ap-
plications, including antibiotics (Liu et al., 2013) and anti-
cancer compounds (Wu et al., 2013). Albeit surprising com-
ing from a habitat with no light, even photoprotectives for
potential use in sunscreens and cosmetics have been found in
deep-sea hydrothermal vent habitats (Martins et al., 2013).
While less than 2% of the marine natural products being
explored come from the deep sea (Skropeta, 2013), the po-
tential of novel molecules and genetic pathways within this
habitat is vast.
3.6 Other provisionary services derived from vast size
The deep sea has long been an environment hosting mili-
tary activities, allowing for covert transportation and surveil-
lance. Technological advances from deep-sea military oper-
ations have led to numerous commercial marine applications
in underwater communications, navigation, and propulsion.
As a result of the stability of the deep-sea environment,
an additional provisioning service provided by the deep sea
is its ability to connect civilizations as well as human infras-
tructure (e.g., oil and gas derricks with land-based refineries).
The first trans-Atlantic cable was laid in 1858and thus, along
with fishing, use of the deep sea as an environment to lay
communication cables is among its oldest and most widely
used services (Ramirez-Ilondra et al. 2011).
4 Cultural services
Cultural services provided by the deep sea are the non-
material benefits humans enjoy. These services can range
from the valuable scientific knowledge that can be obtained
from deep-sea environments, the educational value and the
economic benefits generated by science, exploration and dis-
covery (and the technological development that accompa-
nies these), to the more purely aesthetic and inspirational
services, including literature, entertainment, ethical consid-
erations, tourism, and spiritual wealth and well-being. The
deep-sea’s vast expanse has often led to excitement, for ex-
ample, the discovery of unique habitats, including hydrother-
mal vents (Corliss et al., 1979), the yeti crabs that live there
(Macpherson et al., 2005) and the diversity of life that lives
on seamounts and in deep-sea coral habitats (Fig. 1). The
mystery and great unknown of the deep-ocean realm pro-
vides a nearly endless supply of facts stranger than fiction.
As a result, despite the obvious distance and inaccessibility
of the deep sea, these environments have pervaded ancient
and modern culture to a surprising degree.
Some of the main cultural services provided by the deep
sea can be described as educational and scientific, two ser-
vices that receive significant investment despite today’s eco-
nomic climate. The apparent lack of general public and sci-
entific knowledge on the deep sea stands in contrast to the
size of the deep sea and its importance in the Earth’s bi-
ological and climatic systems. As a result, education man-
agement organizations are currently promoting the ocean
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3952 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
literacy concept, which includes the understanding of the es-
sential principles and fundamental concepts of the ocean,
communication about the ocean in a meaningful way and
the stewardship involved (Strang and Tran, 2010). One of
the roles provided by the deep sea to human culture is in
providing a repository of information on past conditions of
the planet, stored in the fossil remains of planktonic or-
ganisms (e.g., foraminifera, coccolithophores) preserved in
deep-marine sediments. This deep-sea paleo-climatological
service is of immediate benefit to assessing and predicting
current and future climatic effects on our environment and
human well-being. For example, foraminifera studies have
identified how the ocean temperature has changed over the
last 125 000 years (Labeyrie et al., 1987). In a similar way,
deep-sea environmental conditions are suitable for excep-
tional preservation of historical cultural artifacts, including
ancient Black Sea shipwrecks (Ballard et al., 2001) and po-
tentially much more recent artifacts from polar expeditions
(Shackleton’s Endurance, Glover et al., 2013).
Although the anthropocentric view of the Earth has mostly
revolved around terrestrial environments, references to the
deep sea and its importance for humanity can be found
throughout history and literature. While the history of the
study of deep-sea fauna spans a mere 130 years, references to
exploring the deep ocean go much further back. The impor-
tance of deep sea cartography in Hellenic civilizations, for
instance (Oleson, 2000), illustrates the fascination and ex-
ploration potential of the deep ocean dating from several mil-
lennia ago. Exploration of the deep ocean has grown vastly
since technological advances have allowed easier access to
the deep sea. Modern high-resolution deep-water biologi-
cal investigations are far removed in scope and technology
from the first glimpses of deep-sea life recovered in the early
1800s on sounding casts or from the hand-hauled nets de-
ployed in the 1870s from the sailing vessel HMS Challenger.
Scientific advances and the linked exploitation of deep-sea
marine resources today elicit significant investment, which
drives increasing marine technological development, involv-
ing industries that generate substantial economic wealth and
extraction of deep-sea resources beneficial to human welfare
and development.
With historical exploration and the ensuing fascination
with deep-sea life also came inspiration for literature, arts
and entertainment, which can all be seen as more purely
aesthetic services (Fig. 1). The deep sea has inspired lit-
erature since early human civilization. Plato first mentions
the myth of the engulfing of Atlantis by the ocean around
360BC. This tradition has continued with novels like 20000
Leagues Under the Sea and Moby Dick. The entertainment
value provided by the deep sea is still very much present to-
day, as exemplified by numerous recent documentaries, films
and even cartoons (e.g., the BBC documentary Blue Planet
– The Deep, the children’s program Octonauts, and the Dis-
ney/Pixarfilm Finding Nemo). Another service with aesthetic
and entertainment value that benefits from deep-sea func-
tions is the growing whale-watching tourist industry, which
can provide substantial economic benefits to coastal commu-
nities. Growth and aggregation of whales and dolphins de-
pend to a large extent on deep-sea supporting services, such
as biomass production over seamounts or water circulation
in upwelling areas (Johnston et al., 2008). A newly emerging
industry is that of in situ deep-sea tourism, whereby human-
occupied underwater vehicles are being offered to the public
to explore deep-water environments in person, an example
of a cultural service with exploration and entertainmentvalue
that is – for now – only accessible to wealthy individuals. The
inspiration and awe that the deep ocean brings us at many dif-
ferent levels of human culture is also present spiritually, with
numerous examples mentioned in scripture (e.g., the Bible:
Genesis 1:1–3, Proverbs 8:26–28; Quran: 24:40) as well as
various indigenous cultures and classical religions display-
ing important elements of worship and ceremony related to
marine mammals (e.g., New Zealand Maoris) and gods rep-
resenting oceans and seas (the Greek Poseidon). Related to
spiritual values are the ethical values that are often assigned
to marine life and increasingly to deep-sea animals and en-
vironments. Public pressure to conserve deep-sea habitats,
such as coral reefs and vents, can be seen as an important
contributor to, or the result of the increasing non-use or exis-
tential value of, the deep sea (Mengerink et al., 2014).
5 Discussion
It is difficult to discuss the deep sea without being waylaid
by the severe lack of deep-sea environmental and biologi-
cal data, the conceptual challenge of its size, and the unex-
plored habitats (e.g., hadal trenches and vast deep pelagic
areas; Ramirez-Ilondra et al. 2011) that likely add hetero-
geneity and diversity in unknown ways. However, when the
current state of knowledge is viewed synoptically, these in-
tellectual shortcomings can be reduced through integrationof
the diverse chemical, micro- and macro-biological, and envi-
ronmental information that has been discovered over more
than a century of study. What results is a basic understanding
of how the temporal and spatial diversity in the deep sea cre-
ates a system with far-reaching linkages both within its realm
as well as to society as a whole.
5.1 Temporal and spatial relationships
Many of the functions provided by the deep sea, even though
they occur on small scales in time and space, have direct im-
plications for global services owing to the large size of the
environment (Fig. 3). Even regional-scale activities, such as
harvesting of deep-sea fish, may have broad temporal and
spatial implications for ecosystem services – as these are
usually species that are often very long lived (Cailliet et al.,
2001) or have either little spatial pattern potentially lead-
ing to broad ranges (Haedrich and Merrett, 1990) or ranges
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3953
that reflect a similar distribution to water masses (Koslow,
1993). Even processes thought to proceed at low rates and by
bacteria or archaea, such as chemoautotrophy in the pelagic
and abyssal seafloor (Nauhaus et al., 2007; Reinthaler et al.,
2010; Middelburg, 2011), can have major implications when
scaled up to the huge areas and volumesof the deep sea, play-
ing an important role in processes such as energy flow, and
carbon sequestration on the global scale.
In addition to the vast nature of the habitat, there can also
be a long separation of function and service within the deep
sea (Fig. 3). An example of this is that nutrient regeneration,
often dominated by microbial activity (Azam et al., 1983),
is a feature that occurs so pervasively that its provisioning
and regulation of surface production has global application
due to the resulting generation of oxygen and foodstuffs.
This is even more provocative since in certain instances there
are great spatial and temporal distances between function
and service; for example, nutrients regenerated in the North
Atlantic may not reach surface waters in the North Pacific
for millennia. There is even greater separation of service
and function for the creation of oil and gas reservoirs. Oil
reserves are the result of geological transformation of or-
ganic matter buried in deep-ocean sediments (once a biotic
entity, but when extracted considered abiotic). Methane hy-
drate reserves are largely formed through microbially medi-
ated methanogenesis, and although the formation occurs on
relatively “rapid” timescales it takes centuries to build up to
potentially harvestable concentrations. The same is true of
manganese nodules and polymetallic crusts, whose forma-
tion takes millions of years, but which even now have yet to
provide a service, although they likely will in the very near
future.
5.2 Interrelatedness and threats to ecosystem services
and functions
The biological, physical, and chemical properties of the
ecosystem combine to form complex processes that result in
globally important services. These supporting, regulating and
provisional services are connected both totheir functions and
to each other in a variety of ways (Fig. 4). In many instances,
one function provides a diversity of services; for example,
circulation, or more specifically the separation of the deep
sea from the atmosphere over long periods of time, provides
at least one regulating service and four provisioning services.
The services provided by the deep sea are not impervi-
ous to human impacts. The concern as to the susceptibility
to overfishing of slow-growing and long-lived species of fish
and coral in the deep sea is a topic of debate and concern
(Bett, 2001; Morato et al., 2006; Althaus et al., 2009). Cli-
mate change itself will impact the functions discussed in the
deep sea through ocean acidification, declining oxygen and
productivity and increasing temperature (Mora et al., 2013;
Levin et al., 2014). These impacts are likely to affect the di-
versity of the supporting functions discussed here, including
biodiversity, nutrient cycling, biomass, and primary and sec-
ondary productivity (Jones et al., 2014). While the scale and
magnitude of these impacts are difficult to predict, the inter-
related nature of the impacts indicates that they will be per-
vasive in the overall function. For example, the reduced rate
of global circulation as a result of human impacts (Bryden et
al., 2005) will affect not only many marine systems (Schmit-
tner, 2005), but also the services that are gained from those
and deep-sea habitats.
5.3 Ecosystem services frameworks and the need for
integrating deep-sea complexity
Multiple frameworks have been posed as the initial step to
communicate the ecosystem functions and services provided
by different habitats. Generally these frameworks or classi-
fications are traditionally centered around terrestrial assess-
ments, partially owing to the limited availability of data and
methods to assess the provision of marine and coastal ecosys-
tem services. Other reasons are the low resolution of spa-
tially explicit marine information, the difficulty of quantify-
ing ecosystem functions and processes in the highly dynamic
and connected three-dimensional marine environments, and
the fact that ecosystem service studies just rarely take ma-
rine characteristics into account. It is therefore not surprising
that the applications of ecosystem services in marine contexts
span a short history (Liquete et al., 2013).
Among the most commonly adopted frameworks is the
MA (2005), on which we have largely based our treatise.
The most recent general frameworks and classifications have
omitted the group of supporting services and the services
related to abiotic factors. The MA includes the supporting
services category but omits abiotic resources such as miner-
als, despite its importance for understanding the true extent
of deep-sea ecosystem services (Armstrong, 2012). More re-
cently, the CICES (Haines-Young and Potschin, 2013) has
been proposed as an update of the MA, and even though it
mentions abiotic factors such as abiotic renewables it fails
to recognize fossil fuels, and it excludes supporting services.
Instead, CICES proposes a “Regulation & Maintenance” ser-
vices category (in addition to the provisioning and cultural
services). Armstrong et al. (2012) followed the MA, as they
argued that there is a myriad of supporting functions that to-
gether form important “intermediate” services in the deep sea
and that are crucial to other “more final” services. For in-
stance, the remineralization of nutrients is largely a support-
ing function that feeds into the service of primary production
both in situ (i.e., deep-sea chemoautotrophy) and in surface
waters, and is critical to the functioning of the global ecosys-
tem. Excluding abiotic factors from ecosystem services is
questionable. For instance, it is the abiotic function of CO
2
that makes it a greenhouse gas, and one of the main services
of the deep sea is its ability to absorb a large proportion of
the gas emitted by humans; however, this service is largely
due to gas solubility. While abiotic, gas solubility is driven in
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3954 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Figure 3. (A) The spatial extent of each of the main deep-sea habitats (pelagic is in km
3
, while all other habitats are in km
2
; derived from
Ramirez-Llodra et al., 2010.). Note that many of these habitats can be any range of size from small to those depicted. The relationship
between spatial and temporal scales for (B) supporting, (C) regulating and (D) provisioning services of the deep sea. Note the log scale in
(A) and the approximate scales in (B–D). Geological= thousands to millions of years.
the ocean by temperature, a factor that we are modifying by
our release of CO
2
, leading to a feedback on our climate. As
such, the deep sea is an area where the exclusion of abiotic
processes and functions in a classification framework would
be a disservice to our understanding of deep-sea ecosys-
tem services and the interrelatedness and complexity of the
processes and functions involved. Recent efforts by Liquete
et al. (2013) produced an adaptation of the CICES frame-
work to cater for marine and coastal ecosystem services, and
took into account the classification of the MA (2005), TEEB
(2010) and the work of Beaumont et al. (2007). Despite the
focus on marine ecosystem services, the adaptation of Li-
quete et al. (2013) came up short in addressing the concerns
put forward by Armstrong et al. (2012) and Van den Hove
and Moreau (2007) about our understanding of the deep sea
and the ecosystem services it provides. It is therefore imper-
ative that renewed efforts are undertaken to adapt existing
ecosystem services frameworks (Armstrong et al., 2012), or
to create new solutions, since defining away unique char-
acteristics of different ecosystems in a uniform system is
not desirable. Instead, the challenge in developing multiple
appropriately structured classification systems for different
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3955
Figure 4. The links between the supporting, provisioning, and reg-
ulating services within the deep sea. Color is used to indicate the
linkages between each of the different overarching service classes.
purposes presents an opportunity to enrich our thinking about
ecosystem services and find appropriate solutions (Costanza,
2008). The current ecosystem service classifications seem in-
compatible with the needs of the deep-sea realm, its habitats
and the ecosystems it contains, and this further makes both
the deep sea and the management of it unique. However, a
portable framework is essential for management of the deep
sea, as the majority of it lies outside of national jurisdiction,
meaning that international collaboration is the only means of
managing many of its services effectively.
5.4 Current challenges in function and service
evaluation
While numerous studies have sought to quantify various
ecosystem functions in the deep sea (for a review see Smith et
al., 2008) and have described the various services provided
by the different functions, we know of only one study that
has as yet put a monetary value on the extent of ecosys-
tem functions and services in the deep sea (Jobstvogt et
al., 2014). However, multiple frameworks have been con-
structed to facilitate this sort of key analysis (van den Hove
and Moreau, 2007; Armstrong et al., 2010, 2012). This lack
of knowledge makes ocean management extremely difficult,
especially with regards to managing the exploitation of ma-
rine resources, as it is presently impossible to know the full
“cost” that we will have to pay for exploiting a specific re-
source. By evaluating ecosystem functions and services pro-
vided by the deep sea, we will be able to understand the cost
versus benefit of exploitation, which will assist us in making
better informed management decisions, as it pertains to the
exploitation of deep-sea services.
To understand fully the ecosystem functions provided by
the deep sea as a whole, it is important to be able to com-
pare specific functions across a variety of spatial and tempo-
ral scales. However, comparisons between studies are often
plagued by the fact that different techniques are used. A good
example of this is in studies that use different mesh sizes to
separate animals by body size, with some separating macro-
fauna on a 300-micron mesh, while others use a 500-micron
mesh. The use of two techniques automatically imposes dif-
ferences on various properties that relate to ecosystem func-
tioning (e.g., biomass) and services (e.g., biodiversity, pro-
ductivity), hampering comparisons across ecosystems.
By the very nature of the mechanisms that lead to ecosys-
tem services, a standardized holistic and multidisciplinary
approach is necessary for studying it. Collaborations be-
tween biogeochemists, physiologists, empirical and observa-
tional ecologists who deal with microbes to megafauna in
both pelagic and benthic environments, and climate scien-
tists, but also socio-economists are required to understand
and further quantify the services provided by the deep sea.
However, owing to the pervasive nature of the function of the
deep sea, and the threats to it, an important additional link is
needed between the stakeholders of the deep sea, which is
the global population.
6 Conclusions
– The deep sea is the world’s largest environment and
comprises a multitude of different habitats and a major
proportion of the world’s species.
– Although over a century of research has been under-
taken in the deep sea, our understanding of this environ-
ment is limited. However, with the advances we have al-
ready made we can begin to understand its role in global
energy, nutrients, and biological cycles.
– Services provided by the deep sea are vital to support
the current way of life for many humans, providing en-
ergy,metal and mineral resources, food and other goods.
– Vast area and long residence times typify deep-sea en-
vironments, meaning that even fast processes on small
spatial scales create massive services, although in many
cases the processes are far removed from their resultant
services.
– Many of the functions of the deep sea result in interre-
lated regulating and provisioning services.
– The stakeholders of the deep sea are not limited to one
country or area, but instead consist of the entire global
population.
– The deep sea plays an important cultural role, providing
inspiration for the arts and having a far-reaching influ-
ence even on those that never leave the land.
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3956 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
– Further research should aim to adapt an existing or to
build an appropriate ecosystem services framework that
can be applied to the deep sea to quantify its mone-
tary value while creating a more uniform approach to
its study.
Acknowledgements. This review was the result of a workshop
supported by the International Network for scientific investigation
of DEEP-sea ecosystems (INDEEP) through a grant awarded by
the Total Foundation. We thank the INDEEP PIs, especially Maria
Baker, for making this workshop possible and the International
Research Institute of Stavanger for generously hosting the meeting.
This manuscript has greatly benefited from comments by three
anonymous reviewers and we thank Nicola Beaumont for her
advice during the revision of the original manuscript. J. Ingels
was supported by a Marie Curie Intra-European Fellowship within
the 7th European Community Framework Programme (grant
agreement FP7-PEOPLE-2011-IEF no. 300879). A. R. Thurber
was supported by National Science Foundation grant 1103428
and LOL provided support throughout the workshop. We declare
no competing interests and the funding agency had no input in
the content of this manuscript. The order of authorship is reverse
alphabetical.
Edited by: T. Treude
References
Aloisi, G., Bouloubassi, I., Heijs, S. K., Pancost, R. D., Pierre,
C., Sinninghe Damsté, J. S., Gottschal, J. C., Forney, L. J., and
Rouchy, J.-M.: CH
4
-consuming microorganisms and the forma-
tion of carbonatecrusts at cold seeps, EarthPlanet. Sc. Lett., 203,
195–203, 2002.
Alonso-Sáez, L., Galand, P. E., Casamayor, E. O., Pedrós-Alió, C.,
and Bertilsson, S.: High bicarbonate assimilation in the dark by
Arctic bacteria, ISME J., 4, 1581–1590, 2010.
Alonso-Sáez, L., Waller, A. S., Mende, D. R., Bakker, K., Farnelid,
H., Yager, P.L., Lovejoy, C., Tremblay, J.-E., Potvin, M., Hein-
rich, F., Estrada, M., Riemann, L., Bork, P., Pedrós-Alió, C., and
Bertilsson, S.: Role for urea in nitrification by polar marine Ar-
chaea, P. Natl. Acad. Sci., 109, 17989–17994, 2012.
Althaus, F., Williams, A., Schlacher, T. A., Kloser, R. J., Green,
M. A., Barker, B. A., Bax, N. J., Brodie, P., and Schlacher-
Hoenlinger, M. A.: Impacts of bottom trawling on deep-coral
ecosystems of seamounts are long-lasting, Mar. Ecol.-Prog. Ser.,
397, 40, 2009.
Anantharaman, K., Breier, J. A., Sheik, C. S., and Dick, G. J.:
Evidence for hydrogen oxidation and metabolic plasticity in
widespread deep-sea sulfur-oxidizing bacteria, P. Natl. Acad.
Sci., 110, 330–335, 2013.
Armstrong, C. W., Foley, N., Tinch, R., and Hove, S. v. d.: Ecosys-
tem Goods and Services of the Deep Sea, HERMIONE (Hotspot
Ecosystem Research and Man’s impact on European Seas), De-
liverable D6.2: Ecosystem Goods and Services of the Deep Sea,
WP6: Socioeconomics, Ocean Governance and Science-Policy
Interfaces, 2010.
Armstrong, C. W., Foley, N. S., Tinch, R., and van den Hove, S.:
Services from the deep: Steps towards valuation of deep sea
goods and services, Ecosyst. Serv., 2, 2–13, 2012.
Azam, F., Fenchel, T., Field, J. G., Gray, J. S., Meyer-Reil, L. A.,
and Thingstad, F.: The ecological role of water-column microbes
in the sea, Mar. Ecol.-Prog. Ser., 10, 257–263, 1983.
Bailey, D. M., Collins, M. A., Gordon, J. D. M., Zuur, A. F., and
Priede, I. G.: Long-term changes in deep-water fish populations
in the northeast Atlantic: a deeper reaching effect of fisheries?, P.
R. Soc. B, 276, 1965–1969, 2009.
Ballard, R. D., Hiebert, F. T., Coleman, D. F., Ward, C., Smith, J. S.,
Willis, K., Foley, B., Croff, K., Major, C., and Torre, F.: Deep-
water archaeology of the black sea: the 2000 season at Sinop,
Turkey, Am. J. Archaeol., 105, 607–623, 2001.
Beaumont, N. J., Austen, M. C., Atkins, J. P., Burdon, D., Degraer,
S., Dentinho, T. P., Derous, S., Holm, P., Horton, T., van Ier-
land, E., Marboe, A. H., Starkey, D. J., Townsend, M., and Zarzy-
cki, T.: Identification, definition and quantification of goods and
services provided by marine biodiversity: Implications for the
ecosystem approach, Mar. Pollut. Bull., 54, 253–265, 2007.
Benn, A. R., Weaver, P. P., Billet, D. S. M., van den Hove,
S., Murdock, A. P., Doneghan, G. B., and Le Bas, T.: Hu-
man Activities on the Deep Seafloor in the North East At-
lantic: An Assessment of Spatial Extent, PLoS ONE, 5, e12730,
doi:
10.1371/journal.pone.0012730, 2010.
Bernardino, A. F., Smith, C. R., Baco, A., Altamira, I., and Sumida,
P. Y. G.: Macrofaunal succession in sediments around kelp and
wood falls in the deep NE Pacific and community overlap with
other reducing habitats, Deep-Sea Res. Pt. I, 57, 708–723, 2010.
Berner, R. A.: Biogeochemical cycles of carbon and sulfur and their
effect on atmospheric oxygen over phanerozoic time, Palaeo-
geogr. Palaeocl., 75, 97–122, 1989.
Bernhard, J. M., Barry, J. P., Buck, K. R., and Starczak, V. R.: Im-
pact of intentionally injected carbon dioxide hydrate on deep-sea
benthic foraminiferal survival, Glob. Change Biol., 15, 2078–
2088, 2009.
Bett, B. J.: UK Atlantic Margin Environmental Survey: introduction
and overview of bathyal benthic ecology, Cont. Shelf Res., 21,
917–956, 2001.
Biastoch, A., Treude, T., Rüpke, L. H., Riebesell, U., Roth, C., Bur-
wicz, E. B., Park, W., Latif, M., Böning, C. W., and Madec, G.:
Rising Arctic Ocean temperatures cause gas hydrate destabiliza-
tion and ocean acidification, Geophys. Res. Lett., 38, L08602,
doi:10.1029/2011GL047222, 2011.
Billett, D. S. M., Bett, B. J., Reid, W. D. K., Boorman, B., and
Priede, I. G.: Long-term change in the abyssal NE Atlantic: The
“Amperima Event” revisited, Deep-Sea Res. Pt. II, 57, 1406–
1417, 2010.
Boetius, A. and Suess, E.: Hydrate Ridge: a natural labo-
ratory for the study of microbial life fueled by methane
from near-surface gas hydrates, Chem. Geol., 205, 291–310,
doi:10.1016/j.chemgeo.2003.12.034, 2004.
Boetius, A. and Wenzhöfer, F.: Seafloor oxygen consumption fu-
elled by methane from cold seeps, Nat. Geosci., 6, 725–734,
2013.
Bowden, D. A., Schiaparelli, S., Clark, M. R., and Rickard, G.
J.: A lost world? Archaic crinoid-dominated assemblages on an
Antarctic seamount, Deep-Sea Res. Pt. II, 58, 119–127, 2011.
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3957
Braeckman, U., Provoost, P., Moens, T., Soetaert,K., Middelburg, J.
J., Vincx, M. and Vanaverbeke, J.: Biological vs. physical mixing
effects on benthic food web dynamics, PLoS ONE, 6, e18078,
doi:
10.1371/journal.pone.0018078, 2011.
Bronk, D. A.: Dynamics of DON, in: Biogeochemistry of Marine
Dissolved Organic Matter, edited by: Hansell, D. A. and Carlson,
C. A., Academic Press, San Diego, 153–247, 2002.
Bryden, H. L., Longworth, H. R., and Cunningham, S. A.: Slow-
ing of the Atlantic meridional overturning circulation at 25
◦
N,
Nature, 438, 655–657, 2005.
Buesseler, K. O., Lamborg, C. H., Boyd, P. W., Lam, P. J., Trull, T.
W., Bidigare, R. R., Bishop, J. K. B., Casciotti, K. L., Dehairs,
F., Elskens, M., Honda, M., Karl, D. M., Siegel, D. A., Silver, M.
W., Steinberg, D. K., Valdes, J., Mooy, B. V., and Wilson, S.: Re-
visiting carbon flux through the ocean’s twilight zone, Science,
316, 567–570, 2007.
Burd, A. B., Hansell, D. A., Steinberg, D. K., Anderson, T. R.,
Arístegui, J., Baltar, F., Beaupré, S. R., Buesseler, K. O., De-
Hairs, F., Jackson, G. A., Kadko, D. C., Koppelmann, R.,
Lampitt, R. S., Nagata, T., Reinthaler, T., Robinson, C., Robi-
son, B. H., Tamburini, C., and Tanaka, T.: Assessing the appar-
ent imbalance between geochemical and biochemical indicators
of meso- and bathypelagic biological activity: What the @$#! is
wrong with present calculations of carbon budgets?, Deep-Sea
Res. Pt. II, 57, 1557–1571, 2010.
Cailliet, G., Andrews, A., Burton, E., Watters, D., Kline, D., and
Ferry-Graham, L.: Age determination and validation studies of
marine fishes: do deep-dwellers live longer?, Exp. Gerontol., 36,
739–764, 2001.
Canadell, J. G., Quéré, C. L., Raupach, M. R., Field, C. B., Buiten-
huis, E. T., Ciais, P., Conway, T. J., Gillett, N. P., Houghton, R.
A., and Marland, G.: Contributions to accelerating atmospheric
CO
2
growth from economic activity, carbon intensity, and effi-
ciency of natural sinks, P. Natl. Acad. Sci., 104, 18866–18870,
2007.
Canals, M., Puig, P., de Madron, X. D., Heussner, S., Palanques, A.,
and Fabres, J.: Flushing submarine canyons, Nature, 444, 354–
357, 2006.
Chivers, A. J., Narayanaswamy, B. E., Lamont, P. A., Dale, A., and
Turnewitsch, R.: Changes in polychaete standing stock and di-
versity on the northern side of Senghor Seamount (NE Atlantic),
Biogeosciences, 10, 3535–3546, doi:10.5194/bg-10-3535-2013,
2013.
Clark, M. R. and Koslow, J. A.: Impacts of Fisheries on Seamounts,
in: Seamounts: Ecology, Fisheries & Conservation, edited by:
Pitcher, T. J., Morato, T., Hart, P. J. B., Clark, M. R., Haggan,
N., and Santos, R. S., Blackwell Publishing Ltd, Oxford, Uk,
doi:10.1002/9780470691953.ch19, 2008.
Clark, M. R., Rowden, A. A., Schlacher, T., Williams, A., Con-
salvey, M., Stocks, K. I., Rogers, A. D., O’Hara, T. D., White,
M., Shank, T. M., and Hall-Spencer, J. M.: The Ecology of
Seamounts: Structure, Function, and Human Impacts, Annu.
Rev. Mar. Sci., 2, 253–278, 2010.
Codispoti, L. A., Brandes, J. A., Christensen, J. P., Devol, A. H.,
Naqvi, S. W. A., Paerl, H. W., and Yoshinari, T.: The oceanic
fixed nitrogen and nitrous oxide budgets: Moving targets as we
enter the anthropocene?, Sci. Mar., 65, 85–105, 2001.
Cordes, E. E., McGinley, M. P., Podowski, E. L., Becker, E. L.,
Lessard-Pilon, S., Viada, S. T., and Fisher, C. R.: Coral com-
munities of the deep Gulf of Mexico, Deep-Sea Res. Pt. I, 55,
777–787, 2008.
Cordes, E. E., Becker, E. L., Hourdez, S., and Fisher, C. R.: In-
fluence of foundation species, depth, and location on diversity
and community composition at Gulf of Mexico lower-slope cold
seeps, Deep-Sea Res. Pt. II, 57, 1870–1881, 2010a.
Cordes, E. E., Cunha, M. R., Galéron, J., Mora, C., Olu-Le Roy,
K., Sibuet, M., Van Gaever, S., Vanreusel, A., and Levin, L. A.:
The influence of geological, geochemical, and biogenic habitat
heterogeneity on seep biodiversity, Mar. Ecol., 31, 51–65, 2010b.
Corliss, J. B., Dymond, J., Gordon, L. I., Edmond, J. M., Herzen,
R. P. von, Ballard, R. D., Green, K., Williams, D., Bain-
bridge, A., Crane, K., and van Andel, T. H.: Submarine Ther-
mal Sprirngs on the Galápagos Rift, Science, 203, 1073–1083,
doi:10.1126/science.203.4385.1073, 1979.
Costanza, R.: Ecosystem services: Multiple classification systems
are needed, Biol. Conserv., 141, 350–352, 2008..
Cowie, G. L., Calvert, S. E., Pedersen, T. F., Schulz, H., and von
Rad, U.: Organic content and preservational controls in surficial
shelf and slope sediments from the Arabian Sea (Pakistan mar-
gin), Mar. Geol., 161, 23–38, 1999.
Cullen, D. J.: Distribution composition and age of submarine phos-
phorites on Chatham Rise east of New Zealand, SEPM Special
Publication 29, 139–148, 1980.
Dachs, J., Lohmann, R., Ockenden, W. A., Méjanelle, L., Eisenre-
ich, S. J., and Jones, K. C.: Oceanic biogeochemical controls on
global dynamics of persistent organic pollutants, Environ. Sci.
Technol., 36, 4229–4237, 2002.
Danovaro, R.: Extending the approaches of biodiversity and ecosys-
tem functioning to the deep ocean, in: Marine Biodiversity and
Ecosystem Functioning: Frameworks, methodologies, and inte-
gration, edited by: Solan, M., Aspden, R. J., and Paterson, D. M.,
Oxford University Press, Oxford, 115–126, 2012.
Danovaro, R., Dell’Anno, A., Corinaldesi, C., Magagnini, M., No-
ble, R., Tamburini, C., and Weinbauer, M.: Major viral impact
on the functioning of benthic deep-sea ecosystems, Nature, 454,
1084–1087, 2008a.
Danovaro, R., Gambi, C., Dell’Anno, A., Corinaldesi, C.,
Fraschetti, S., Vanreusel, A., Vincx, M., and Gooday, A. J.: Ex-
ponential decline of deep-sea ecosystem functioning linked to
benthic biodiversity loss, Curr. Biol., 18, 1–8, 2008b.
De Angelis, M. A., Lilley, M. D., and Baross, J. A.: Methane oxida-
tion in deep-sea hydrothermal plumes of the endeavour segment
of the Juan de Fuca Ridge, Deep-Sea Res. Pt. I, 40, 1169–1186,
doi:10.1016/0967-0637(93)90132-M, 1993.
De Leo, F. C., Smith, C. R., Rowden, A. A., Bowden, D. A., and
Clark, M. R.: Submarine canyons: hotspots of benthic biomass
and productivity in the deep sea, P. R. Soc. B, 277, 2783–2792,
2010.
De Leo, F. C., Vetter, E. W., Smith, C. R., Rowden, A. A., and Mc-
Granaghan, M.: Spatial scale-dependent habitat heterogeneityin-
fluences submarine canyon macrofaunal abundance and diversity
off the Main and Northwest Hawaiian Islands, Deep-Sea Res. Pt.
II, 104, 267–290, doi:10.1016/j.dsr2.2013.06.015, 2013.
De Stigter, H. C., Boer, W., de Jesus Mendes, P. A., Jesus, C. C.,
Thomsen, L., van den Bergh, G. D., and van Weering, T. C. E.:
Recent sediment transport and deposition in the Nazaré Canyon,
Portuguese continental margin, Mar. Geol., 246, 144–164, 2007.
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3958 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Dick, G. J., Anantharaman, K., Baker, B. J., Li, M., Reed, D.
C., and Sheik, C. S.: The microbiology of deep-sea hydrother-
mal vent plumes: ecological and biogeographic linkages to
seafloor and water column habitats, Front. Microbiol., 4, 124,
doi:10.3389/fmicb.2013.00124, 2013.
Dylan, T.: Ocean thermal energy conversion: current overview and
future outlook, Renew. Energy, 6, 367–373, 1995.
Flothmann, S., von Kistowski, K., Dolan, E., Lee, E., Meere, F.,
and Album, G.: Closing loopholes: getting illegal fishing under
control, Science, 328, 1235–1236, 2010.
Foley, N. and Armstrong, C. W.: The ecological and economic value
of cold-water coral ecosystems, Ocean Coast. Manage., 53, 313–
326, 2010.
Francis, C. A., Beman, J. M., and Kuypers, M. M. M.: New pro-
cesses and players in the nitrogen cycle: the microbial ecology
of anaerobic and archaeal ammonia oxidation, ISME J., 1, 19–
27, 2007.
Froescheis, O., Looser, R., Cailliet, G. M., Jarman, W. M.,
and Ballschmiter, K.: The deep-sea as a final global sink of
semivolatile persistent organic pollutants? Part I: PCBs in sur-
face and deep-sea dwelling fish of the North and South Atlantic
and the Monterey Bay Canyon (California), Chemosphere, 40,
651–660, 2000.
Gage, J. D. and Tyler, P. A.: Deep-sea biology: a natural history
of organisms at the deep-sea floor, Cambridge University Press,
1991.
Gebruk, A. V., Chevaldonné, P., Shank, T., Lutz, R. A., and Vrijen-
hoek, R. C.: Deep-sea hydrothermal vent communities of the Lo-
gatchev area (14
◦
45
0
N, Mid-Atlantic Ridge): Diverse biotopes
and high biomass, J. Mar. Biol. Assoc. UK, 80, 383–393, 2000.
Glover, A. G. and Smith, C. R.: The deep-sea floor ecosystem: cur-
rent status and prospects of anthropogenic change by the year
2025, Environ. Conserv., 30, 219–241, 2003.
Glover, A. G., Wiklund, H., Taboada, S., Avila, C., Cristobo, J.,
Smith, C. R., Kemp, K. M., Jamieson, A. J., and Dahlgren, T.
G.: Bone-eating worms from the Antarctic: the contrasting fate
of whale and wood remains on the Southern Ocean seafloor, P.
R. Soc. B, 280, 1768, doi:10.1098/rspb.2013.1390, 2013.
Grassle, J. F. and Maciolek, N. J.: Deep-sea species richness: re-
gional and local diversity estimates from quantitative bottom
samples, Am. Natural., 139, 313–341, 1992.
Gruber, N. and Sarmiento, J. L.: Global patterns of marine nitrogen
fixation and denitrification, Global Biogeochem. Cy., 11, 235–
266, 1997.
Gutt, J. and Starmans, A.: Structure and biodiversity of megaben-
thos in the Weddell and Lazarev Seas (Antarctica): Ecological
role of physical parameters and biological interactions, Polar
Biol., 20, 229–247, 1998.
Haedrich, R. L. and Merrett, N. R.: Little evidence for faunal zona-
tion or communities in deep sea demersal fish faunas, Progr.
Oceanogr., 24, 239–250, 1990.
Haines-Young, R. and Potschin, M.: Common International Clas-
sification of Ecosystem Services (CICES): Consultation on Ver-
sion 4, August–December 2012, 2013.
Hansell, D. A., Carlson,C. A., and Schlitzer, R.: Net removalof ma-
jor marine dissolved organic carbon fractions in the subsurface
ocean: Removal of exported DOC, Global Biogeochem. Cy., 26,
GB1016, doi:10.1029/2011GB004069, 2012.
Hansman, R. L., Griffin, S., Watson, J. T., Druffel, E. R., Ingalls, A.
E., Pearson, A., and Aluwihare, L. I.: The radiocarbon signature
of microorganisms in the mesopelagic ocean, P. Natl. Acad. Sci.,
106, 6513–6518, 2009.
Harris, P. T., Mamillan-Lawler, M., Rupp, J., and Baker, E.
K.: Geomorphology of the oceans, Mar. Geol., 352, 4–24„
doi:10.1016/j.margeo.2014.01.011, 2014.
Hasemann, C. and Soltwedel, T.: Small-scaleheterogeneity indeep-
sea nematode communities around biogenic structures, PLoS
One 6, e29152, doi:10.1371/journal.pone.0029152, 2011.
Hawaii Undersea Military Munitions Assessment (HUMMA) – Fi-
nal Investigation Report (No. HI-05): University of Hawaii at
Manoa, Environet, Inc., 2010.
Hein, J. R., Mizell, K., Koschinsky, A., and Conrad, T. A.: Deep-
ocean mineral deposits as a source of critical metals for high-
and green-technology applications: Comparison with land-based
resources, Ore Geol. Rev., 51, 1–14, 2013..
Herndl, G. J. and Reinthaler, T.: Microbial control of the dark end
of the biological pump, Nat. Geosci., 6, 718–724, 2013.
Herndl, G. J., Reinthaler, T., Teira, E., van Aken, H., Veth, C., Pern-
thaler, A., and Pernthaler, J.: Contribution of Archaea to total
prokaryotic production in the deep Atlantic Ocean, Appl. Envi-
ron. Microbiol., 71, 2303–2309, 2005.
Herzig, P. M. and Hannington, M. D.: Polymetallic massive sul-
fides at the modernseafloor a review, Ore Geol. Rev., 10, 95–115,
1995.
Hessler, R. R. and Sanders, H. L.: Faunal diversity in the deep-sea,
Deep-Sea Res., 14, 65–78, 1967.
Howell, K. L., Pond, D. W., Billett, D. S., and Tyler, P. A.: Feed-
ing ecology of deep-sea seastars (Echinodermata: Asteroidea): a
fatty-acid biomarker approach, Mar. Ecol.-Prog. Ser., 255, 193–
206, 2003.
Hughes, D. J., Brown,L., Cook, G. T., Cowie, G., Gage, J. D., Good,
E., Kennedy, H., MacKenzie, A. B., Papadimitriou, S., and Shim-
mield, G. B.: The effects of megafaunal burrows on radiotracer
profiles and organic composition in deep-sea sediments: prelim-
inary results from two sites in the bathyal north-east Atlantic,
Deep-Sea Res. Pt. I, 52, 1–13, 2005.
Hunter, W. R., Veuger, B. and Witte, U.: Macrofauna regulate het-
erotrophic bacterial carbon and nitrogen incorporation in low-
oxygen sediments, ISME J, 6, 2140–2151, 2012.
Ingalls, A. E., Shah, S. R., Hansman, R. L., Aluwihare, L. I., San-
tos, G. M., Druffel, E. R., and Pearson, A.: Quantifying archaeal
community autotrophy in the mesopelagic ocean using natural
radiocarbon, P. Natl. Acad. Sci., 103, 6442–6447, 2006.
Ingels, J., Van den Driessche, P., De Mesel, I., Vanhove, S., Moens,
T., and Vanreusel, A.: Preferred use of bacteria over phytoplank-
ton by deep-sea nematodes in polar regions, Mar. Ecol.-Prog.
Ser., 406, 121–133, 2010.
Intergovernmental Panel on Climate Change (IPCC), Climate
Change 2007: The Physical Science Basis, Contribution of
Working Group I to the Fourth Assessment Report of the Inter-
governmental Panel on Climate Change, edited by: Solomon, S.,
Qin, D., Manning, M., Chen, Z., Marquis, M., Averyt, K. B., Tig-
nor, M., and Miller, H. L., Cambridge Univ. Press, Cambridge,
UK, 2007.
Jahnke, R. A.: The global ocean flux of particulate organic carbon:
Areal distribution and magnitude, Global Biogeochem. Cy., 10,
71–88, 1996.
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3959
Jobstvogt, N., Hanley, N., Hynes, S., Kenter, J., and Witte, U.:
Twenty thousand sterling under the sea: Estimating the value of
protecting deep-sea biodiversity, Ecol. Econ., 97, 10–19, 2014.
Johnston, D. W., McDonald, M., Polovina, J., Domokos, R., Wig-
gins, S., and Hildebrand, J.: Temporal patterns in the acoustic
signals of beaked whales at Cross Seamount, Biol. Lett., 4, 208–
211, 2008.
Jones, D. O. B., Yool, A., Wei, C.-L., Henson, S. A., Ruhl, H. A.,
Watson, R. A., and Gehlen, M.: Global reductions in seafloor
biomass in response to climate change, Glob. Change Biol., 20,
1861–1872, doi:10.1111/gcb.12480, 2014.
Judd, A. G., Hovland, M., Dimitrov, L. I., Garcia Gil, S., and Jukes,
V.: The geological methane budget at continental margins and its
influence on climate change, Geofluids, 2, 109–126, 2002.
Kato, Y., Fujinaga, K., Nakamura, K., Takaya, Y., Kitamura, K.,
Ohta, J., Toda, R., Nakashima, T., and Iwamori, H.: Deep-sea
mud in the Pacific Ocean as a potential resource for rare-earth
elements, Nat. Geosci, 4, 535–539, 2011.
Kemp, D. B., Coe, A. L., Cohen, A. S., and Schwark, L.: Astro-
nomical pacing of methane release in the Early Jurassic period,
Nature, 437, 396–399, 2005.
Kiriakoulakis, K., Stutt, E., Rowland, S. J., Annick, V., Lampitt, R.
S., and Wolff, G. A.: Controls on the organic chemical composi-
tion of settling particles in the Northeast Atlantic Ocean, Progr.
Oceanogr., 50, 65–87, 2001.
Klauda, J. B. and Sandler, S. I.; Global distribution of methane hy-
drate in ocean sediment, Energ. Fuels, 19, 459–470, 2005.
Klitgaard, A. B. and Tendal, O. S. Distribution and species compo-
sition of mass occurrences of large-sized sponges in the northeast
Atlantic, Progr. Oceanogr., 61, 57–98, 2004.
Knight, H.: 20,000 megawatts under the sea: Oceanic steam
engines. In: New Scientist, 1 March 2014, 48–51, avail-
able at: http://www.newscientist.com/article/mg22129580.
900-20000-megawatts-under-the-sea-oceanic-steam-engines.
html, (last access: 3 March 2014), 2014.
Knittel, K. and Boetius, A.: Anaerobic Oxidation of Methane:
Progress with an Unknown Process, Annu. Rev. Microbiol., 63,
311–334, 2009.
Koslow, J. A.: Community structure in North Atlantic deep-sea
fishes, Progr. Oceanogr., 31, 321–338, 1993.
Kube, M., Chernikova, T. N., Al-Ramahi, Y., Beloqui, A., Lopez-
Cortez, N., Guazzaroni, M. E., Heipieper, H. J., Klages, S., Kot-
syrbenko, O. R., Langer, I., Nechitaylo, T. Y., Lünsdorf, H.,
Fernández, M., Juárez, S., Ciordia, S., Singer, S., Kagan, O.,
Egorova, O., Petit, P. A., Stogios, P., Kim, Y., Tchigvintsev,
A., Flick, R., Denaro, R., Genovese, M., Albar, J. P., Reva, O.
N., Martínez-Gomariz, M., Tran, H., Ferrer, M., Savchenko, A.,
Yakunin, A. F., Yakimov, M. M., Golyshina, O. V., Reinhardt, R.,
and Golyshin, P. N.: Genome sequence and functional genomic
analysis of the oil-degrading bacterium Oleispiraantarctica,Nat.
Commun., 4, 2156, doi:10.1038/ncomms3156, 2013.
Kvassnes, A. J. S. and Iversen, E.: Waste sites from mines in Nor-
wegian Fjords, Mineralproduksjon., 3, A27–A38, 2013.
Kvenvolden, K. A.: Gas hydrates-geological perspective and global
change, Rev. Geoph., 31, 173–187, 1993.
Labeyrie, L. D., Duplessy, J. C., and Blanc, P. L.: Varia-
tions in mode of formation and temperature of oceanic deep
waters over the past 125,000 years, Nature, 327, 477–482,
doi:10.1038/327477a0, 1987.
Lam, P. and Kuypers, M. M. M.: Microbial nitrogen cycling pro-
cesses in oxygen minimum zones, Annu. Rev. Mar. Sci., 3, 317–
345, 2011.
Laverock, B., Gilbert, J., Tait, K., Osborn, A. M., and Widdicombe,
S.: Bioturbation: impact on the marine nitrogen cycle, Biochem.
Soc. Trans., 39, 315–320, doi:10.1042/BST0390315, 2011.
Leduc, D., Rowden, A. A., Bowden, D. A., Probert, P. K., Pilditch,
C. A., and Nodder, S. D.: Unimodal relationship between
biomass and species richness of deep-sea nematodes: implica-
tions for the link between productivity and diversity, Mar. Ecol.-
Prog. Ser., 454, 53–64, doi:10.3354/meps09609, 2012.
Lessard-Pilon, S. A., Podowski, E. L., Cordes, E. E., and Fisher, C.
R.: Megafaunacommunity composition associated with Lophelia
pertusa colonies in the Gulf of Mexico, Deep-Sea Res. Pt. II, 57,
1882–1890, 2010.
Levin, L. A.: Interactions between metazoans and large, aggluti-
nating protozoans: implications for the community structure of
deep-sea benthos, Am. Zool., 31, 886–900, 1991.
Levin, L. A.: Oxygen minimum zone benthos: adaptation and com-
munity response to hypoxia, Oceanogr. Mar. Biol., 41, 1–45,
2003.
Levin, L. A. and Dayton, P. K.: Ecological theory and continen-
tal margins: Where shallow meets deep, Trends Ecol. Evol., 24,
606–617, 2009.
Levin, L. A. and Michener, R. H.: Isotopic evidence for
chemosynthesis-based nutrition of macrobenthos: the lightness
of being at Pacific methane seeps, Limnol. Oceanogr., 47, 1336–
1345, 2002.
Levin, L., Blair, N., DeMaster, D., Plaia, G., Fornes, W., Martin, C.,
and Thomas, C.: Rapid subduction of organic matter by maldanid
polychaetes on the North Carolina slope, J. Mar. Res., 55, 595–
611, 1997.
Levin, L. A., James, D. W., Martin, C. M., Rathburn, A. E., Harris,
L. H., and Michener, R. H.: Do methane seeps support distinct
macrofaunal assemblages? Observations on community structure
and nutrition from the northern California slope and shelf, Mar.
Ecol.-Prog. Ser., 208, 21–39, 2000.
Levin, L. A., Etter, R. J., Rex, M. A., Gooday, A. J., Smith, C. R.,
Pineda, J., Stuart, C. T., Hessler, R. R., and Pawson, D.: Environ-
mental influences on regional deep-sea species diversity, Annu.
Rev. Ecol. Sys., 32, 51–93, 2001.
Levin, L. A., Mendoza, G. F., Gonzalez, J. P., Thurber, A. R., and
Cordes, E. E.: Diversity of bathyal macrofauna on the Northeast-
ern Pacific Margin: the influence of methane seeps and oxygen
minimum zones, Mar. Ecol., 31, 94–110, 2010.
Levin, L. A., Liu, K.-K., Emeis, K.-C., Breitburg, D.L., Cloern, J.,
Deutsch, C., Giani, M., Goffart, A., Hofmann, E. E., Lachkar,
Z., Limburg, K., Liu, S.-M., Montes, E., Naqvi, W., Ragueneau,
O., Rabouille, C., Sarkar, S. K., Swaney, D. P., Wassman, P., and
Wishner, K. F.: Comparative biogeochemistry-ecosystem-human
interactions on dynamic continental margins, J. Mar. Syst., in
press, doi:10.1016/j.jmarsys.2014.04.016, 2014.
Liquete, C., Piroddi, C., Drakou, E. G., Gurney, L., Katsanevakis,
S., Charef, A., and Egoh, B.: Current Status and Future
Prospects for the Assessment of Marine and Coastal Ecosys-
tem Services: A Systematic Review, Plos One, 8, e67737,
doi:10.1371/journal.pone.0067737, 2013.
Liu, N., Shang, F., Xi, L., and Huang, Y.: Tetroazolemycins A
and B, Two New Oxazole-Thiazole Siderophores from Deep-Sea
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3960 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Streptomyces olivaceus FXJ8.012, Mar. Drugs, 11, 1524–1533,
doi:10.3390/md11051524, 2013.
Longhurst, A. R.: Role of the marine biosphere in the global carbon
cycle, Limnol. Oceanogr., 36, 1507–1526, 1991.
Looser, R., Froescheis, O., Cailliet, G. M., Jarman, W. M.,
and Ballschmiter, K.: The deep-sea as a final global sink of
semivolatile persistent organic pollutants? Part II: Organochlo-
rine pesticides in surface and deep-sea dwelling fish of the North
and South Atlantic and the Monterey Bay Canyon (California),
Chemosphere, 40, 661–670, 2000.
Loreau, M.: Biodiversity and ecosystem functioning: the mystery of
the deep sea, Curr. Biol., 18, R126–R128, 2008.
Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J. P.,
Hector, A., Hooper, D. U., Huston, M. A., Raffaelli, D., Schmid,
B., Tilman, D., and Wardle, D. A.: Biodiversity and ecosystem
functioning: current knowledge and future challenges, Science,
294, 804–808, 2001.
Lu, Z., Deng, Y., Van Nostrand, J. D., He, Z., Voordeckers, J.,
Zhou, A., Lee, Y.-J., Mason, O. U., Dubinsky, E. A., Chavar-
ria, K. L., Tom, L. M., Fortney, J. L., Lamendella, R., Jansson,
J. K., D’haeseleer, P., Hazen, T. C., and Zhou, J.: Microbial gene
functions enriched in the Deepwater Horizon deep-sea oil plume,
ISME J., 6, 451–460, 2012.
Lutz, M. J., Caldeira, K., Dunbar, R. B., and Behrenfeld, M. J.:
Seasonal rhythms of net primary production and particulate or-
ganic carbon flux to depth describe the efficiency of biologi-
cal pump in the global ocean, J. Geophys. Res.-Oceans, 112,
C10011, doi:10.1029/2006JC003706, 2007.
Mace, G., Bateman, I. J., Albon, S., Balmford, A., Church, A., and
Winn, J.: Conceptual framework and methodology, Report to the
UK National Ecosystem Assessment, 2009.
Macpherson, E., Jones, W., and Segonzac, M.: A new squat lobster
family of Galatheoidea (Crustacea, Decapoda: Anomura) from
the hydrothermal vents of the Pacific-Antarctic Ridge, Zoosys-
tema, 27, 709–723, 2005.
Martin, J. H., Knauer, G. A., Karl, D. M., and Broenkow, W. W.:
VERTEX: Carbon cycling in the northeast Pacific, Deep-Sea
Res., 34, 267–285, 1987.
Martins, A., Tenreiro, T., Andrade, G., Gadanho, M., Chaves, S.,
Abrantes, M., Calado, P., Tenreiro, R., and Vieira, H.: Photopro-
tective Bioactivity Present in a Unique Marine Bacteria Collec-
tion from Portuguese Deep Sea Hydrothermal Vents, Mar. Drugs,
11, 1506–1523, doi:10.3390/md11051506, 2013.
McLeod, R. J. and Wing, S. R.: Hagfish in the New Zealand Fjords
are supported by chemoautotrophy of forest carbon, Ecology, 88,
809–816, 2007.
McLeod, R. J. and Wing, S. R.: Strong pathways for incorporation
of terrestrially derived organic matter into benthic communities,
Estuar. Coast. Shelf Sci., 82, 645–653, 2009.
Mengerink, K. J., Van Dover, C. L., Ardron, J., Baker, M., Escobar-
Briones, E., Gjerde, K., Koslow, J. A., Ramirez-Llodra, E., Lara-
Lopez, A., Squires, D., Sweetman, A. K., and Levin, L. A.: A
call for deep-ocean stewardship, Science, 344, 696–698, 2014.
Middelburg, J. J.: Chemoautotrophy in the ocean, Geophys. Res.
Lett., 38, 2011.
Millennium assessment Ecosystem Assessment: Ecosystems and
Human Well-being: Synthesis, Millennium Ecosystem Assess-
ment, Island Press, Washington DC, 2005.
Miller, R. J., Hocevar, J., Stone, R. P., and Fedorov, D. V.:
Structure-forming corals and sponges and their use as fish habi-
tat in bering sea submarine canyons, PLoS ONE 7, e33885,
doi:
10.1371/journal.pone.0033885, 2012.
Montagna, P. A., Baguley, J. G., Cooksey, C., Hartwell, I.,
Hyde, L. J., Hyland, J. L., Kalke, R. D., Kracker, L. M.,
Reuscher, M., and Rhodes, A. C.: Deep-Sea Benthic Footprint
of the Deepwater Horizon Blowout, PloS ONE, 8, e70540,
doi:10.1371/journal.pone.0070540, 2013.
Mora, C., Tittensor, D. P., Adl, S., Simpson,A. G. B.,and Worm, B.:
How Many Species Are There on Earth and in the Ocean?, PLoS
Biol., 9, e1001127, doi:10.1371/journal.pbio.1001127, 2011.
Mora, C., Wei, C.-L., Rollo, A., Amaro, T., Baco, A. R., Billett,
D., Bopp, L., Chen, Q., Collier, M., Danovaro, R., Gooday, A. J.,
Grupe, B. M., Halloran, P.R., Ingels, J., Jones, D. O. B., Levin, L.
A., Nakano, H., Norling, K., Ramirez-Llodra, E., Rex, M., Ruhl,
H. A., Smith, C. R., Sweetman, A. K., Thurber, A. R., Tjiputra,
J. F., Usseglio, P., Watling, L., Wu, T., and Yasuhara, M.: Bi-
otic and human vulnerability to projected changes in ocean bio-
geochemistry over the 21st century, PLoS Biol., 11, e1001682,
doi:10.1371/journal.pbio.1001682, 2013.
Morato, T., Watson, R., Pitcher, T. J. and Pauly, D.: Fishing down
the deep, Fish Fisher., 7, 24–34, 2006.
Morato, T., Kvile, K. Ø., Taranto, G. H., Tempera, F.,
Narayanaswamy, B. E., Hebbeln, D., Menezes, G. M., Wien-
berg, C., Santos, R. S., and Pitcher, T. J.: Seamount physiography
and biology in the north-east Atlantic and Mediterranean Sea,
Biogeosciences, 10, 3039–3054, doi:10.5194/bg-10-3039-2013,
2013.
Morton, B.: Slaughter at sea, Mar. Poll. Bull., 46, 379–380, 2003.
Naether, D. J., Slawtschew, S., Stasik, S., Engel, M., Olzog, M.,
Wick, L. Y., Timmis, K. N., and Heipieper, H. J.: Adaptation
of hydrocarbonoclastic Alcanivorax borkumensis SK2 to alka-
nes and toxic organic compounds – a physiological and tran-
scriptomic approach, Appl. Environ. Microbiol., 79, 4282–4293,
doi:10.1128/AEM.00694-13, 2013.
Narayanaswamy, B. E., Hughes, D. J., Howell, K. L., Davies, J., and
Jacobs, C.: First observations of megafaunal communities inhab-
iting George Bligh Bank, Northeast Atlantic, Deep-Sea Res. Pt.
II, 92, 79–86, 2013.
Nauhaus, K., Albrecht, M., Elvert, M., Boetius, A., and Widdel, F.:
In vitro cell growth of marine archaeal-bacterial consortia dur-
ing anaerobic oxidation of methane with sulfate, Environ. Micro-
biol., 9, 187–196, doi:10.1111/j.1462-2920.2006.01127.x, 2007.
Niemann, H., Losekann, T., de Beer, D., Elvert, M., Nadalig, T.,
Knittel, K., Amann, R., Sauter, E. J., Schluter, M., Klages, M.,
Foucher, J. P., and Boetius, A.: Novel microbial communities of
the Haakon Mosby mud volcano and their role as a methane sink,
Nature, 443, 854–858, 2006
Nihous, G. C.: A preliminary assessment of ocean thermal energy
conversion resources, J. Energy Res. Tech., 129, 10–17, 2007.
Norse, E. A., Brooke, S., Cheung, W. W. L., Clark, M. R., Ekeland,
I., Froese, R., Gjerde, K. M., Haedrich, R. L., Heppell, S. S.,
Morato, T., Morgan, L. E., Pauly, D., Sumaila, R., and Watson,
R. Sustainability of deep-sea fisheries, Mar. Policy, 36, 307–320,
2012.
Oleson, J. P.: Herodotus, Aristotle, and sounding weights: the deep
sea as a frontier in the classical world, J. Roman Archaeol., 13,
293–310, 2000.
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3961
Olu, K., Duperret, A., Sibuet, M., Foucher, J., and Fiala-Mdioni,
A.: Structure and distribution of cold seep communities along
the Peruvian active margin: relationship to geological and fluid
patterns, Mar. Ecol.-Prog. Ser., 132, 109–125, 1996.
O’Neill, R. V.: Is it time to bury the ecosystem concept? (with full
military honors, of course!), Ecology, 82, 3275–3284, 2001.
Pailleret, M., Haga, T., Petit, P., Privé-Gill, C., Saedlou, N., Gaill,
F., and Zbinden, M.: Sunken wood from the Vanuatu Islands:
identification of wood substrates and preliminary description of
associated fauna, Mar. Ecol., 28, 233–241, 2007.
Parada, J., Feng, X., Hauerhof, E., Suzuki, R., and Abubakar, U.:
The deep sea energy park: harvesting hydrothermal energy for
seabed exploration, University of Southampton, Southampton,
England, 111 pp., 2012.
Paulmier, A. and Ruiz-Pino, D.: Oxygen minimum zones (OMZs)
in the modern ocean, Progr. Oceanogr., 80, 113–128, 2009.
Pham, C. K., Ramirez-Llodra, E., Alt, C. H. S., Amaro, T.,
Bergmann, M., Canals, M., Company, J. B., Davies, J., Duin-
eveld, G., Galgani, F., Howell, K. L., Huvenne, V. A. I., Isidro,
E., Jones, D. O. B., Lastras, G., Morato, T., Gomes-Pereira, J.
N., Purser, A., Stewart, H., Tojeira, I., Tubau, X., Van Rooij, D.,
and Tyler, P. A.: Marine Litter Distribution and Density in Euro-
pean Seas, from the Shelves to Deep Basins, Plos One, 9, e95839,
doi:10.1371/journal.pone.0095839, 2014.
Pichler, M.: Assesment of hydrogen – rock interactions during geo-
logical storage of CH
4
– H
2
mixtures, MSc thesis at Department
Mineral Resources & Petroleum Engineering Chair of Reservoir
Engineering, 97 pp., 2013.
Puig, P., Canals, M., Martín, J., Amblas, D., Lastras, G., Palanques,
A., and Calafat, A. M.:Ploughing the deep sea floor, Nature, 489,
286–289, 2012.
Pusceddu, A., Bianchelli, S., Martín, J., Puig, P., Palanques, A.,
Masqué, P., Danovaro, R.,: 2014. Chronic and intensive bottom
trawling impairs deep-sea biodiversity and ecosystem function-
ing, P. Natl. Acad. Sci., in press, doi:10.1073/pnas.1405454111,
2014.
Ramirez-Llodra, E., Brandt, A., Danovaro, R., De Mol, B., Es-
cobar, E., German, C. R., Levin, L. A., Martinez Arbizu, P.,
Menot, L., Buhl-Mortensen, P., Narayanaswamy, B. E., Smith,
C. R., Tittensor, D. P., Tyler, P. A., Vanreusel, A., and Vecchione,
M.: Deep, diverse and definitely different: unique attributes of
the world’s largest ecosystem, Biogeosciences, 7, 2851–2899,
doi:10.5194/bg-7-2851-2010, 2010.
Ramirez-Llodra, E., Tyler, P. A., Baker, M. C., Bergstad, O. A.,
Clark, M. R., Escobar, E., Levin, L. A., Menot, L., Rowden,
A. A., Smith, C. R., and Van Dover, C. L.: Man and the Last
Great Wilderness: Human Impact on the Deep Sea, PLoS ONE,
6, e22588, doi:10.1371/journal.pone.0022588, 2011.
Ramirez-Llodra, E., De Mol, B., Company, J. B., Coll, M., and
Sardà, F.: Effects of natural and anthropogenic processes in the
distribution of marine litter in the deep Mediterranean Sea, Progr.
Oceanogr., 118, 273–287, doi:10.1016/j.pocean.2013.07.027,
2013.
Reeburgh, W. S.: Oceanic Methane Biogeochemistry, Chem. Rev.,
107, 486–513, 2007.
Reinthaler, T., van Aken, H. M., and Herndl, G. J.: Major contribu-
tion of autotrophy to microbial carbon cycling in the deep North
Atlantic’s interior, Deep-Sea Res. Pt. II, 57, 1572–1580, 2010.
Rex, M. A. and Etter, R. J.: Deep-sea biodiversity:pattern and scale,
Harvard Univ. Pr., 354 pp. 2010.
Rice, A. L.,Thurston, M. H., and New, A. L.: Dense aggregations of
a hexactinellid sponge, Pheronema carpenteri, in the Porcupine
Seabight (Northeast Atlantic Ocean) and possible causes, Progr.
Oceanogr., 24, 179–196, 1990.
Rivers, A. R., Sharma, S., Tringe, S. G., Martin, J., Joye, S. B., and
Moran, M. A.: Transcriptional response of bathypelagic marine
bacterioplankton to the Deepwater Horizon oil spill, ISME J., 7,
2315–2329, doi:10.1038/ismej.2013.129, 2013.
Roberts, C. M.: Deep impact: the rising toll of fishing in the deep
sea, Trends Ecol. Evol., 17, 242–245, 2002.
Roberts, J. M., Wheeler, A. J., and Freiwald, A.: Reefs of the deep:
The biology and geology of cold-water coral ecosystems, Sci-
ence, 312, 543–547, 2006.
Robison, B. H.: Deep pelagic biology, J. Exp. Mar. Biol. Ecol., 300,
253–272, 2004.
Rouse, G. W., Goffredi, S. K., and Vrijenhoek, R. C.: Osedax:
Bone-Eating Marine Worms with Dwarf Males, Science, 305,
668–671, 2004.
Rowden, A. A., Clark, M. R., and Wright, I. C.: Physical character-
isation and a biologically focused classification of “seamounts”
in the New Zealand region, New Zealand J. Mar. Freshw. Res.,
39, 1039–1059, 2005.
Ruhl, H. A., Ellena, J. A., and Smith, K. L.: Connections between
climate, food limitation, and carbon cycling in abyssal sediment
communities, P. Natl. Acad. Sci., 105, 17006–17011, 2008.
Sabine, C. L. and Feely, R. A.: The oceanic sink for carbon dioxide,
in: Greenhouse Gas Sinks, edited by: Reay, D., Hewitt,N., Grace,
J., and Smith, K., CABI Publishing, Oxfordshire, UK, 31–49,
2007.
Sardá, R., Gil, J., Taboada, S., and Gili, J. M.: Polychaete species
captured in sediment traps moored in northwestern Mediter-
ranean submarine canyons, Zool. J. Linn. Soc., 155, 1–21, 2009.
Schmittner, A.: Decline of the marine ecosystem caused by a re-
duction in the Atlantic overturning circulation, Nature, 434, 628–
633, doi:10.1038/nature03476, 2005.
Schmitz, S.: “Einfluss von Wasserstoff als Gasbegleitstoff auf Un-
tertagespeicherung”, 2011.
Sellanes, J., Pedraza-García, M. J. and Zapata-Hernández, G.: Las
áreas de filtraciónde metano constituyen zonas de agregación del
bacalao de profundidad (Dissostichus eleginoides) frente a Chile
central?, Lat. Am. J. Aquat. Res., 40, 980–991, 2012.
Serpetti, N., Gontikaki, E., Narayanaswamy, B. E., and Witte,
U.: Macrofaunal community inside and outside of the Darwin
Mounds Special Area of Conservation, NE Atlantic, Biogeo-
sciences, 10, 3705–3714, doi:10.5194/bg-10-3705-2013, 2013.
Shields, M. A. and Kedra, M.: A deep burrowing sipunculan of eco-
logical and geochemical importance, Deep-Sea Res. Pt. I, 56,
2057–2064, 2009.
Skropeta, D.: Deep-sea natural products, Natural Product Reports
25, 1131, 2008.
Smith, C. R. and Baco, A. R.: Ecology of whale falls at the deep-sea
floor, Oceanogr. Mar. Biol., 41, 311–354, 2003.
Smith, C. R., De Leo, F. C., Bernardino, A. F., Sweetman, A. K.,
and Arbizu, P. M.: Abyssal food limitation, ecosystem structure
and climate change, Trends Ecol. Evol., 23, 518–528, 2008.
Smith, C. R., Grange, L. J., Honig, D. L., Naudts, L., Huber, B.,
Guidi, L., and Domack E.: A large population of king crabs in
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014

3962 A. R. Thurber et al.: Ecosystem function and services provided by the deep sea
Palmer Deep on the west Antarctic Peninsula shelf and potential
invasive impacts, P. R. Soc. B., 279, 1017–1026, 2012.
Smith, D. C., Simon, M., Alldredge, A. L., and Azam, F.: Intense
hydrolytic enzyme activity on marine aggregates and implica-
tions for rapid particle dissolution, Nature 359, 139–142, 1992.
Sogin, M. L., Morrison, H. G., Huber, J. A., Welch, D. M., Huse,
S. M., Neal, P. R., Arrieta, J. M., and Herndl, G. J.: Microbial
diversity in the deep sea and the underexplored “rare biosphere,”
P. Natl. Acad. Sci., 103, 12115–12120, 2006.
Sommer, S., Pfannkuche, O., Linke, P., Luff,R., Greinert, J., Drews,
M., Gubsch, S., Pieper, M., Poser, M. and Viergutz, T.: Effi-
ciency of the benthic filter: Biological control of the emission
of dissolved methane from sediments containing shallow gas hy-
drates at Hydrate Ridge, Global Biogeochem. Cy., 20, GB2019,
doi:10.1029/2004GB002389, 2006.
Sommer, S., Linke, P., Pfannkuche, O., Niemann, H., and Treude,
T.: Benthic respiration in a seep habitat dominated by dense
beds of ampharetid polychaetes at the Hikurangi Margin (New
Zealand), Mar. Geol., 272, 223–232, 2010.
Strang, C., and Tran, L. U.: National Marine Educations Associa-
tion, Special Report 3: The Ocean Literacy Campaign, 80 pp.,
2010.
Suttle, C. A.: Viruses in the sea, Nature 437, 356–361, 2005.
Swan, B. K.: Martinez-Garcia, M., Preston, C. M., Sczyrba, A.,
Woyke, T., Lamy, D., Reinthaler, T., Poulton, N. J., Masland, E.
D. P., Gomez, M. L., Sieracki, M. E., DeLong, E. F., Herndl,
G. J., and Stepanauskas, R.: Potential for chemolithoautotrophy
among ubiquitous bacteria lineages in the dark ocean, Science
333, 1296–1300, 2011.
Tavormina, P. L., Ussler, W., and Orphan, V. J.: Planktonic and
Sediment-Associated Aerobic Methanotrophs in Two Seep Sys-
tems along the North American Margin, Appl. Environ. Micro-
biol., 74, 3985–3995, 2008.
TEEB: The Economics of Ecosystems and Biodiversity: Ecological
and Economic Foundations, in: Earthscan, edited by: Kumar, P.,
London and Washington. 2010.
Thiel, H.: Anthropogenic impacts on the deep sea, Ecosystems of
the World, 427–472, 2003.
Thistle, D., Sedlacek, L., Carman, K. R., Fleeger, J. W., Brewer,
P. G., and Barry, J. P.: Simulated sequestration of industrial car-
bon dioxide at a deep-sea site: Effects on species of harpacticoid
copepods, J. Exp. Mar. Biol. Ecol., 330, 151–158, 2006.
Thistle, D., Sedlacek, L., Carman, K. R., Fleeger, J. W., Brewer, P.
G., and Barry, J. P.: Exposure to carbon dioxide-rich seawater is
stressful for some deep-sea species: an in situ, behavioral study,
Mar. Ecol.-Prog. Ser., 340, 9–16, 2007.
Thornburg, C. C., Zabriskie, T. M., and McPhail, K. L.: Deep-Sea
Hydrothermal Vents: Potential Hot Spots for Natural Products
Discovery?, J. Nat. Prod. 73, 489–499, 2010.
Thurber, A. R., Levin, L. A., Orphan, V. J., and Marlow, J. J.: Ar-
chaea in metazoan diets: implications for food webs and biogeo-
chemical cycling, ISME J., 6, 1602–1612, 2012.
Thurber, A. R., Levin, L. A., Rowden, A. A., Sommer, S., Linke,
P., and Kröger, K.: Microbes, macrofauna, and methane: A
novel seep community fueled by aerobic methanotrophy, Lim-
nol. Oceanogr., 58, 1640–1656, 2013.
Treude, T., Smith, C. R., Wenzhfer, F., Carney, E., Bernardino, A.
F., Hannides, A. K., Krger, M., and Boetius, A.: Biogeochem-
istry of a deep-sea whale fall: sulfate reduction, sulfide efflux
and methanogenesis, Mar. Ecol.-Prog. Ser., 382, 1–21, 2009.
Treude, T., Kiel, S., Linke, P., Peckmann, J., and Goedert, J. L.:
Elasmobranch egg capsules associated with modern and ancient
cold seeps: A nursery for non-seep marine predators, Mar. Ecol.-
Prog. Ser., 437, 175–181, 2011.
Turner, R. D.: Wood, mollusks, and deep-sea food chains, B. Am.
Malacol. Un., 1976, 13–19, 1977.
UK National Ecosystem Assessment: The UK National Ecosys-
tem Assessment Technical Report, UNEP-WCMC, Cambridge,
2011.
Ulloa, O., Canfield, D. E., DeLong, E. F., Letelier, R. M., and Stew-
art, F. J.: Microbial oceanography of anoxic oxygen minimum
zones, P. Natl. Acad. Sci., 109, 15996–16003, 2012.
Valentine, D. L., Kastner, M., Wardlaw, G. D., Wang, X., Purdy,
A., and Bartlett, D. H.: Biogeochemical investigations of marine
methane seeps, Hydrate Ridge, Oregon, J. Geophys. Res., 110,
G02005, doi:10.1029/2005JG000025, 2005.
Valentine, D. L., Kessler, J. D., Redmond, M. C., Mendes, S. D.,
Heintz, M. B., Farwell, C., Hu, L., Kinnaman, F. S., Yvon-Lewis,
S., Du, M., Chan, E. W., Tigreros, F. G., and Villanueva, C. J.:
Propane respiration jump-starts microbial response to a deep oil
spill, Science, 330, 208–211, 2010.
Van den Hove, S. and Moreau, V.: Deep-sea Biodiversity and
Ecosystems: A Scoping Report on Their Socio-economy, Man-
agement and Governanace, UNEP/Earthprint, 2007.
Van Dover, C. L.: The ecology of deep-sea hydrothermal vents,
Princeton University Press, Princeton, NJ, 2000.
Van Gaever, S., Moodley, L., Pasotti, F., Houtekamer, M., Middel-
burg, J. J., Danovaro, R., and Vanreusel, A.: Trophic specialisa-
tion of metazoan meiofauna at the Håkon Mosby Mud Volcano:
fatty acid biomarker isotope evidence, Mar. Biol., 156, 1289–
1296, 2009.
Vardaro, M. F., Ruhl, H. A., and Smith, K. L.: Climate variation,
carbon flux, and bioturbation in the abyssal North Pacific, Lim-
nol. Oceanogr., 54, 2081–2088, 2009.
Vega, L. A.: Ocean Thermal Energy Conversion Primer, Mar. Tech-
nol. Soc. J., 36, 25–35, 2002.
Vetter, E. W., Smith, C. R., and De Leo, F. C.: Hawaiian hotspots:
enhanced megafaunal abundance and diversity in submarine
canyons on the oceanic islands of Hawaii, Mar. Ecol., 31, 183–
199, 2010.
Vetter, Y., Deming, J., Jumars, P., and Krieger-Brockett, B.: A pre-
dictive model of bacterial foraging by means of freely released
extracellular enzymes, Microbial Ecol., 36, 75–92, 1998.
Wakeham, S. G., Lewis, C. M., Hopmans, E. C., Schouten, S.,
and Sinninghe Damsté, J. S.: Archaea mediate anaerobic ox-
idation of methane in deep euxinic waters of the Black Sea,
Geochim. Cosmochim. Ac., 67, 1359–1374, doi:10.1016/S0016-
7037(02)01220-6, 2003.
Wallace, K. J.: Classification of ecosystem services: Problems and
solutions, Biol. Conserv., 139, 235–246, 2007.
Wallmann, K. and Bialas, J.: International viewpoint and news, En-
viron. Earth Sci., 59, 485–487, doi:10.1007/s12665-009-0235-x,
2009.
Wallmann, K., Pinero, E., Burwicz, E., Haeckel, M., Hensen, C.,
Dale, A. W., and Ruepke, L.; The global inventory of methane
hydrate in marine sediments: A theoretical approach, Energies,
5, 2449–2498, 2012.
Biogeosciences, 11, 3941–3963, 2014 www.biogeosciences.net/11/3941/2014/

A. R. Thurber et al.: Ecosystem function and services provided by the deep sea 3963
Ward, B. B., Devol, A. H., Rich, J. J., Chang, B. X., Bulow, S. E.,
Naik, H., Pratihary, A., and Jayakumar, A.: Denitrification as the
dominant nitrogen loss process in the Arabian Sea, Nature, 461,
78–81, 2009.
Watson, R. A. and Morato, T.: Fishing down the deep: Accounting
for within-species changes in depth of fishing, Fish. Res., 140,
63–65, 2013.
Wei, C.-L., Rowe, G. T., Escobar-Briones, E., Boetius, A.,
Soltwedel, T., Caley, M. J., Soliman, Y., Huettmann, F., Qu, F.,
Yu, Z., Pitcher, C. R., Haedrich, R. L., Wicksten, M. K., Rex,
M. A., Baguley, J. G., Sharma, J., Danovaro, R., MacDonald,
I. R., Nunnally, C. C., Deming, J. W., Montagna, P., Lévesque,
M., Weslawski, J. M., Wlodarska-Kowalczuk, M., Ingole, B. S.,
Bett, B. J., Billett, D. S. M., Yool, A., Bluhm, B. A., Iken, K.,
and Narayanaswamy, B. E.: Global patterns and predictions of
seafloor biomass using random forests, PLoS ONE, 5, e15323,
doi:10.1371/journal.pone.0015323, 2010.
White, H. K., Hsing, P.-Y., Cho, W., Shank, T. M., Cordes, E. E.,
Quattrini, A. M., Nelson, R. K., Camilli, R., Demopoulos, A. W.,
and German, C. R.: Impact of the Deepwater Horizon oil spill
on a deep-water coral community in the Gulf of Mexico, P. Natl.
Acad. Sci., 109, 20303–20308, 2012.
Whitman, W. B., Coleman, D. C., and Wiebe, W. J.: Prokaryotes:
The unseen majority, P. Natl. Acad. Sci., 95, 6578–6583, 1998.
Wolff, T.: Magrofaunal utilization of plant remains in the deep sea,
Sarsia, 64, 117–143, 1979.
Wu, G., Lin, A., Gu, Q., Zhu, T., and Li, D.: Four New Chloro-
Eremophilane Sesquiterpenes from an Antarctic Deep-Sea De-
rived Fungus, Penicillium sp. PR19N-1, Mar. Drugs, 11, 1399–
1408, doi:10.3390/md11041399, 2013.
Wuchter, C., Abbas, B., Coolen, M. J., Herfort, L., van Bleijswijk,
J., Timmers, P., Strous, M., Teira, E., Herndl, G. J., and Middel-
burg, J. J.: Archaeal nitrification in the ocean, P. Natl. Acad. Sci.,
103, 12317–12322, 2006.
Yeh, R.-H., Su, T.-Z., and Yang, M.-S.: Maximum output of an
OTEC power plant, Ocean Eng., 32, 685–700, 2005.
www.biogeosciences.net/11/3941/2014/ Biogeosciences, 11, 3941–3963, 2014