Download Hadal trenches: the ecology of the deepest places on Earth

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Hadal trenches: the ecology of the
deepest places on Earth
Alan J. Jamieson, Toyonobu Fujii, Daniel J. Mayor, Martin Solan and
Imants G. Priede
Oceanlab, University of Aberdeen, Newburgh, AB41 6AA, UK
Hadal trenches account for the deepest 45% of the
oceanic depth range and host active and diverse
biological communities. Advances in our understanding
of hadal community structure and function have, until
recently, relied on technologies that were unable to
document ecological information. Renewed international interest in exploring the deepest marine
environment on Earth provides impetus to re-evaluate
hadal community ecology. We review the abiotic and
biotic characteristics of trenches and offer a contemporary perspective of trench ecology. The application of
existing, rather than the generation of novel, ecological
theory offers the best prospect of understanding deep
ocean ecology.
The hadal environment
The deepest areas of the ocean, commonly referred to as the
hadal zone (6000–11 000 m [1]), represent 1–2% of the
global benthic area (see Glossary), but they constitute the
deepest 45% of the vertical depth gradient. They are almost
exclusively comprised of trenches representing spatially
disjunct environments separated by shallower areas
(Figure 1, Box 1). Hadal trenches remain one of the least
understood habitats on Earth.
Marine biozones that are based on observed faunal
transitions with depth [2] have been used as a convenient
means to divide the ocean into a series of realms. Indeed,
species composition, density, biomass and diversity of
hadal zones often contrast to that of the surrounding
abyssal area. This nomenclature ignores that depth is
continuous and that hadal trenches are intrinsically linked
to shallower ecosystems. Topography, geographical isolation and spatio-temporal variation in food supply, as
well as elevated hydrostatic pressure and low temperature
are all factors that might have encouraged speciation and,
thus, shaped present faunal assemblage structure.
The first major trench sampling campaigns were conducted during the early 1950s on the Danish Galathea and
Russian Vitjaz global expeditions. Using trawl and grab
methods, the diversity, abundance and biomass of benthic
epifaunal and infaunal invertebrates were described. Of
the 300 metazoan species documented in this relatively
sparse data set [1], 58% were thought to be endemic, a level
comparable to neighbouring abyssal environments. Since
all subsequent hadal reviews [1,3,4] have primarily been
based on these two data sets, the current perception of
Corresponding author: Jamieson, A.J. ([email protected]).
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hadal trench ecosystems lacks an up-to-date ecological
interpretation. Research efforts have continued over the
last 30 years although they have been sporadic and
uncoordinated. Recent advances in technological capacity
[e.g. 5,6] provide impetus for a renewed wave of hadal
exploration. Here, as a first step towards synthesising
and integrating available knowledge, we provide a contemporary perspective on hadal trench environments
and argue that the separation of environments by depth
zonation alone is likely to hamper our understanding of
deep ocean ecology.
Hydrographic and physical characteristics of hadal
trenches
It is now known that the bottom water of the hadal
trenches is not stagnant and that deep currents flow
through and ventilate the trenches [7]. For example, the
deep water flowing through the West Pacific Trenches
originates from the Southern Ocean. There are two major
water masses present in the deep Pacific (>1000 m); the
Lower Circum-Polar Water (LCPW) and the North Pacific
Deep Water (NPDW) [8]. The LCPW enters the Pacific from
Glossary
Adiabatic: a process in which, when a fluid is compressed, its pressure
increases and its temperature rises without the gain or loss of any heat.
Allochthonous: an external source [of food].
Autochthonous: an internal source [of food].
Benthic: organisms living on or in the seabed.
Biogeographical province: a biological subdivision of the surface of the Earth
incorporating both faunal and floral characteristics.
Biozone: biological depth zones: littoral (0–1000 m), bathyal (1000–3000 m),
abyssal (3000–6000 m), hadal (6000–11 000 m).
Carrion (food) falls: the deposit of dead or decaying flesh on the seafloor (e.g.
fish, jellyfish or cetacean carcasses).
Deposit feeding: a feeding strategy whereby organisms acquire food by
ingesting large volumes of sediment and extract nutrients from the small
organic fraction of the ingested sediment.
Eurybathy: the ability to occupy a wide range of depths.
Eurythermic: the tolerating of a wide temperature range.
Heterotrophic: requiring complex organic compounds of nitrogen and carbon
for metabolic synthesis.
Meiofauna: organisms passing through a 250–500-mm-sieve and retained on a
41–63-mm-sieve.
Necrophagy: feeding on carcasses.
Ocean acidification: the ongoing decrease in the pH of the Earth’s oceans,
caused by uptake of carbon dioxide from the atmosphere.
Ossified: hardened.
Particulate Organic Matter (POM): particles of organic solids >0.4 mm
suspended within the water column.
Phytopigments: a pigment that undergoes a physical or chemical change upon
exposure to light.
Primary production: the production of organic compounds from atmospheric
or aquatic carbon dioxide, principally through the process of photosynthesis.
Stenobathy: confined or restricted to a small depth range.
0169-5347/$ – see front matter ß 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.tree.2009.09.009 Available online 19 October 2009
Review
Figure 1. Major hadal trenches of the World. (a) Sunda (Java) Trench, 7450 m, (b)
Philippine Trench, 10 540 m, (c) Marianas Trench, 10 989 m, (d) Izu-Bonin (IzuOgasawara) Trench, 9810 m, (e) Japan Trench, 8412 m, (f) Kurile-Kamchatka
Trench, 10 542 m, (g) Aleutian Trench, 7820 m, (h) Tonga Trench, 10 800 m, (i)
Kermadec Trench, 10 047 m, (j) Middle America Trench, 6662 m, (k) Cayman
Trench, 7093 m, (l) Puerto Rico Trench, 8385 m, (m) Peru–Chile Trench, 8055 m,
and (n) South Sandwich Trench, 8428 m.
the south and flows northward [9,10], in a clockwise direction, passing through the trenches on the west of the Pacific
(i.e. the Kermadec Trench and the Tonga Trench [7]).
Through the Samoan Passage, it flows northwest across
the equator to the east Mariana Basin and into a north and
westward flow. The westward branch flows through the
west Mariana Basin [8], and through the Izu-Ogasawara,
Japan and Kuril-Kamchatka Trenches before heading
southwards around the Emperor Seamounts towards
the Aleutian Trench. As for the NPDW, trench currents
then flow westwards back around the Aleutian and
Box 1. The hadal zone: origins and characteristics
Early literature refers to the hadal zone as ‘ultra-abyssal’ [11]. The
term hadal is derived from the ancient Greek ‘Hades’, in reference to
the ancient Greek underworld, and the abode of Hades. It was
coined in the 1950s to avoid confusion between abyssal, lowerabyssal and ultra-abyssal, and in accordance with the terms littoral,
bathyal and abyssal [88].
The hadal zone consists of deep trenches that can plunge from
6000 m to as deep as 11 000 m where hydrostatic pressures reach
1000 bar. Trenches are formed as the tectonic plates of the Earth’s
crust move away from mid-oceanic ridges, causing neighbouring
plates to collide [89]. During this collision, the heavier oceanic plates
are forced down towards the mantle, whereas the lighter continental
plates rise upwards, resulting in narrow plate boundary zones, or
subduction zones, resulting in the formation of a trench [89]. As
newly formed magma rises from the mid-oceanic ridges and ages
with distance, the deep trenches represent the oldest seafloor [11].
The modern trenches were formed during the Cenozoic period when
the continents moved into their current positions and might have
existed for as long as 107 years [1]. Trenches are typically long and
narrow (few are more than 2000 km long) and run parallel to, and
near, extensive island-arc systems or continental landmasses.
Physically, trenches are typified by a V-shape cross-section with
an average steepness of 5–158, reaching on occasion 458. Most
trench floors have narrow, flat, sedimentary bottoms, typically 2–
5 km wide. Similar to the mid-oceanic ridges, the trenches are
seismically active, resulting in frequent earthquakes and volcanic
eruptions, resulting in occasional gravity-driven sediment slides
[67,68].
Of the 37 known hadal trenches and troughs, five are in the
Atlantic Ocean, four in the Indian Ocean and 28 (75%) are around
the Pacific Ocean rim, where the nine deepest trenches in the world
are found in the western region. Although nearly 75% of the ocean
floor is between 2000 and 6000 m deep, only 4.5 104 km2 of the
seafloor reaches depths >6000 m, accounting for just 1%.
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Kuril-Kamchatka Trenches and southwards through
the Japan and Izu-Ogasawara Trenches. This flow of
water brings sufficient dissolved oxygen (mean concentration = 3.43 mL L 1) to support aerobic organisms
[11].
Temperature is often a major environmental driver for
species distribution, varying vertically in the water column
and with latitude [12]. Small temperature changes can
mean the success or failure of species over time [12] or can
inhibit vertical or horizontal migration [13]. The temperature range beyond 6000 m is typically 1.0–2.5 8C. The in
situ bottom water of the Western Pacific Trenches warms
by 0.5 8C as the water masses flow from the Southern to
Northern Hemisphere (Box 2). Just as increases in bottom
temperature from south to north might affect the variation
in community structure between trenches, changes in
temperature with depth are trench specific. Temperature
generally decreases with increasing depth, but this trend
reverses below about 4000 m due to adiabatic heating with
increasing pressure (Box 2). South Pacific Trench temperature increases from 1.16 to 1.91 8C (40%) between 6000
and 10 000 m. In the North Pacific Trenches, over the same
depth range, temperature rises from 1.67 to 2.40 8C
(30%). These in situ temperatures are thus comparable
to those of the continental margins (3000 m). The salinity
of water within the trenches (salinity = 34–35 ppt) remains
similar to typical abyssal plain values and is unaffected by
pressure [11]. Bottom currents in the Marianas Trench, at
depths between 6000 and 10 890 m, are <1.5 cm s 1 for
22.9–63.8% of the time [14]. However, at 10 890 m, the
deepest point on Earth, current velocities reach a maximum of 8.1 cm s 1. These currents exhibit tidal cycles with
semi-lunar and lunar periodicity, comparable to those
observed on abyssal plains [15]. Thus, with the exception
of hydrostatic pressure, the physical characteristics of the
trenches are not exceptional and reflect those found at
shallower depths.
Life under high pressure
There is a general decrease in the abundance and biomass
of organisms with increasing depth [16,17]. Nonetheless,
sampling campaigns in hadal trenches have revealed a
diverse array of metazoan organisms [1,11] consisting
primarily of benthic fauna, such as fish, holothurians,
polychaetes, bivalves, isopods, actinians, amphipods and
gastropods (Figure 2). The richness of trench communities,
thought to originate from the abyssal plains [3,11,18], also
declines with depth [1], although the relative role of
increased pressure versus other environmental correlates
remains unresolved. Nevertheless, adaptations to high
hydrostatic pressures and low temperatures are common
[19–21]. Conspicuous examples include the use of intracellular protein-stabilising osmolytes, such as trimethylamine N-oxide (TMAO) [22], which act to maintain enzyme
function by increasing cell volume to counteract the effects
of pressure, and the increased use of unsaturated fatty
acids in cell membrane phospholipids to maintain their
fluidity and, hence, cellular function [19]. Linear relationships between such adaptations and the depth of capture in
marine fish, from shallow to >4500 m, have been interpreted as causal evidence for pressure adaptations [22,23].
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Box 2. In situ versus potential temperature
Temperature per se does not ultimately define species zonation but is
certainly one of the pivotal abiotic factors [12,90]. Small temperature
changes can influence the vertical or horizontal distribution of species
[13]. Unlike pressure, temperature is not linear with depth and can
vary between trenches at equivalent depths. The in situ bottom water
temperature within a trench warms with increasing hydrostatic
pressure (i.e. depth), since a compressibility effect occurs whereby
water molecules under increasing pressure warm in an adiabatic
process without exchanging (gaining) heat from their environment.
Oceanographers generally remove this pressure-influenced temperature increase (which has no dynamical effect) by conversion to
potential temperature, therefore enabling comparison of water
masses [91]. Potential temperature, derived from the laws of thermodynamics, is the temperature that a water parcel would have if it were
brought from its in situ depth to the sea surface without exchanging
heat or salt with its surroundings. These comparisons show a rise in
potential temperature of approximately 0.5 8C between the South
Pacific (Tonga and Kermadec Trenches) to the North Pacific (Marianas
and Japan Trenches) of 0.6–1 8C (Figure I), an increase of >30%.
Organisms inhabiting these depths only experience the in situ
temperature. Within the trench, the in situ bottom water temperature
rises by 1 8C between 6000 and 11 000 m. Similarly, by examining
surface to full ocean depth temperature, natural adiabatic heating can
be detected in the water column [92]. A steady decrease in
temperature occurs from the surface to 4000 m where upon it
begins to rise (Figure II). The in situ temperature at 10 000 m for
example, is therefore equivalent to that of shallower depths
(3000 m).
Figure I. In situ bottom temperature (closed symbols) and potential
temperature (open symbols) for pooled data from the Southern (blue) and
Northern (red) Pacific Trenches. The in situ bottom temperature increases with
depth by 1 8C. Although the trend remains the same, a temperature rise of
0.5 8C occurs between the southern and northern trenches. By conversion to
potential temperature (eliminating the effects of pressure), this south to north
rise is readily detected.
Figure II. Water column temperature profiles from surface to seafloor and a
magnified inset of the deep-water temperature (inset), in this example for the
Tonga Trench, SW Pacific Ocean. The adiabatic temperature rise can be seen
beyond 4000 m resulting in the temperature at 10 000 m equalling that of
3000 m (indicated by arrow).
Nonetheless, distinguishing between the contributing
effects of temperature and hydrostatic pressure is complex
because these variables are inversely related Figure 3.
Mobile pelagic fauna, such as decapod shrimps and fish,
show a well-defined reduction in metabolic rate with
increasing depth, irrespective of temperature [24]. However, the possibility of hydrostatic pressure as a key control
on the physiological characteristics of pelagic deep-sea
animals has been rejected because there is no consistent
relationship between pressure and metabolic rate across
taxa [25,26]. This suggests that pressure effects do not
necessarily influence energy generation for locomotory
activities, and thus do not inhibit the colonisation of
trenches by active animals.
The distribution of many deep-sea fauna are, nevertheless, constrained within species-specific defined depth
limits [18,27]. As this range might be influenced by
ontogenic stage, pressure might significantly influence
larval colonisation potential [27–29]. The relative change
in pressure experienced by shallow-water fauna, however,
exceeds that experienced by deep sea species; an organism
descending from the surface to 10 m undergoes a 10-fold
change in pressure (1–10 bar), whilst a descent from 6000
to 11 000 m will experience less than a doubling in pressure
(600–1100 bar). Thus, trenches are accessible to some
eurybathic abyssal fauna, including grenadier fishes
(Macrouridae) and natantian prawns (Benthesicymidae)
[30,31], although these are largely confined within 6000–
7000 m. Conversely, many species that inhabit the flat
topography of the abyssal plains never experience substantial variations in pressure (i.e. extreme stenobathy) and,
therefore, might be incapable of utilising adjacent steep
trench habitat. As evolutionary processes operate over
geological time-scales, however, stenobathic fauna may
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Figure 2. Examples of trench fauna. Recent observations and collections of animals from the deepest parts of the ocean. All these images were taken either by baited
camera or collected by baited traps. (a) Aggregation of endemic snailfish (Liparidae) Pseudoliparis amblystomopsis on the trench floor at 7703 m in the Japan Trench and
(b) a specimen caught simultaneously in a baited trap. (c) A natantian decapod Benthescymnus crenatus filmed feeding on small crustaceans at 6100 m in the Kermadec
Trench. (d) Soft-shelled gastropods (unidentified) from 7703 m in the Japan Trench. (e) Thousands of endemic amphipods (Hirondellea dubia) feeding at bait at 10 000 m in
the Tonga Trench. (f) Two large scavenging amphipods (unidentified) from 7703 m in the Japan Trench. (g) Thousands of amphipods being emptied from a baited trap after
just 8 h on the seafloor at 9316 m in the Izu-Ogasawara Trench. (h) Large unidentified amphipods from 7703 m in the Japan Trench. (i) Small scavenging amphipods from
8100 m in the Izu-Ogasawara Trench. (j) Unidentified leptostracan from 7100 m in the Japan Trench. Scales bars are 100 mm (thick line), 20 mm (medium line) and 5 mm
(thin line). All images reproduced with permission from the HADEEP project, Universities of Aberdeen (UK) and Tokyo (Japan).
have sufficient time to adapt to higher pressures as the
bottom descends, as has been speculated for snailfish
(Liparidae) [30]. In turn, this might explain why high
levels of intra-trench endemism at species level is found
alongside inter-trench similarities at higher taxonomic
levels within the same zoogeographic province, despite
common, shallower water ancestry [11,18].
The ‘carbonate compensation depth’ (CCD), the depth at
which calcium carbonate (calcite and aragonite) supply
equals the rate of solvation, has also been proposed as a
physiological barrier to deep ocean colonisation [4].
Calcium carbonate is widely used as a structural component by foraminiferans, corals, crustaceans and molluscs. The CCD range is 4000–5000 m in the Pacific
Ocean, but tends to occur at shallower depths towards
higher latitudes [32]. As carbonate solubility increases
with increasing hydrostatic pressure, ossification becomes
more difficult [33], explaining why ossified groups (e.g.
ophiuroids and echinoids) tend to be replaced by softbodied organisms (e.g. holothurians, and soft and organic
walled foraminifera) with increasing depth [34–36]. Of
contemporary importance, the physiological adaptations
that have permitted deep ocean colonisation to take place
beyond the CCD may yield important insights with respect
to the effects of ocean acidification on calcifiers in the
future upper ocean [37].
Food supply in trench environments
Chemosynthetic bacterial communities occur in trenches
[38], providing localised resources for a host of specialised
organisms. Few have been found to date, but their close
association with subduction zones and other geological
features [39,40] suggest that more will be discovered as
sampling effort increases. Surface-derived particulate
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Figure 3. Trench ecosystem. Each trench system can be characterised by extrinsic factors such as: (a) geological age, which is likely to affect the degree of endemism; (b)
pattern of primary productivity influencing overall food supply; (c) global hydrodynamics controlling oxygen supply and regional water temperature; (d) proximity to land
mass affecting sediment influx; (e) seismic activity, which could operate as one of the driving forces for sediment flux or catastrophic disturbance; and (f) topography, which
determines area, steepness or habitat heterogeneity. Within a trench, local ecological community (diversity and functional groups) can be structured by: (g) physiological
adaptation of individual species coping with various physical stresses; (h) local depth, which reflects hydrostatic pressure and local temperature; (i) predation and
competition for food; (j) local hydrodynamics, which can be utilised to locate food, obtain organic matter supply or disperse; (k) quality and quantity of food resources,
which appear to vary over time and space; (l) substratum can affect type of organisms settling; (m) life history (e.g. reproductive strategy or ontogenetic migration); and (n)
chemosynthetic community, which can provide local increases in food supply.
organic matter (POM) and carrion falls, such as the carcasses of mammals, fish and large invertebrates, evidently
play a role in the supply of food to trench organisms [41–
43]. The gravitational flux of POM into the deep sea varies
in space [44,45] and time [46], depending largely on biogeographical province [47], proximity to continental land
masses and variability in surface ocean and climatic processes. The proximity of each trench to these factors,
therefore results in temporal and spatial variation in
the quantity and quality of POM reaching the trench floor.
Such resource pulses are a widespread phenomenon in
both terrestrial and aquatic environments [48,49], and
can trigger biological responses, including increased reproductive activities [50], and large-scale changes in the
abundance, size distributions and compositions of deepsea benthic communities [51–53].
Most sinking POM is intercepted and either solubilised
or mineralised by heterotrophic bacteria and zooplankton
before it reaches deep waters [54,55]. Deep-sea communities are thus typically considered to be energy (organic
carbon)-limited systems [56]. Nonetheless, there is a growing appreciation that qualitative aspects of the POM, such
as proteins, essential fatty acids (EFAs) and phytopigments, also play a significant role in the ecology of deepsea communities [57–59]. Pelagic heterotrophs selectively
remove these highly labile compounds from POM during
its passage into the deep, reducing both the quantity and
quality of the POM that reaches bathyal depths and
beyond [60,61]. Much of the ‘food’ input to deep-sea systems
is therefore nutrient poor, consisting largely of refractory
compounds. Large carrion falls [62,63], which arrive at the
seabed relatively quickly compared to POM, potentially
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represent an exception. For example, pelagic fish are
known for their high EFA content [64], and could represent
an energy- and nutrient-rich resource for deep-dwelling
communities. Another exception is the occurrence of shortterm pulses of relatively ‘fresh’ phytoplankton aggregates
to the seabed [65]. These ‘phytodetrital’ pulses contribute
substantially to the export of both organic carbon and
nutritious compounds into the ocean interior [46,54,66].
The presence of large quantities of labile, phytoplanktonderived compounds in trench sediments confirms that
pulses of fresh POM are received occasionally, at least
at certain locations [58].
Patterns of food supply are also affected by the physical
topography of hadal environments. The steep slope of
trenches create a downward transport and subsequent
accumulation of POM along the trench axis [58,45,67,68],
making the supply of resources to trench systems fundamentally different to that on the flat neighbouring abyssal
plains. This accumulation of organic matter is evident in
continental-shelf submarine canyons that have similar
topography to trenches [69] and the increase in deposit
feeders (e.g. holothurians) on the trench floor act as an
indicator for increased food supply [11]. The availability
of food along the trench axis, or the ‘trench resource accumulation depth’ (TRAD), is occasionally influenced by mass
transport of sediment (slides) following seismic activity
[67,68,70]. Such events would result in the quantity of food
on the trench axis and slopes being respectively higher and
lower than what would have otherwise fallen on flat ground.
The food impoverished slopes above the TRAD might
serve as biological barriers, impeding exploitation of the
accumulated resources by downward migrating fauna.
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Observations of high numbers of deposit feeders (holothurians) and facultative scavengers (amphipods) at the deepest
parts of the trenches, regardless of depth [1,11,71,72], provide anecdotal support for resource accumulation. However,
conclusive evidence is lacking, and the relative importance
of autochthonous and allochthonous production in trench
communities remains to be established.
Ecological interactions at hadal depths
Scavenging amphipods represent a particularly conspicuous and ubiquitous component of trench fauna. Four
species of lyssianassoid amphipods have been collected
from the Tonga and Kermadec Trench, each occupying a
distinct vertical zone of 3.5 km [71,73]. Ontogenetic vertical partitioning has been proposed to explain the occurrence of juvenile stages towards the upper limit of the
depth range of an individual species [71]. This may result
in higher juvenile growth rates by relieving hydrostatically
induced metabolic suppression and/or allowing access to a
more nutritious food resource [71], although supporting
data are currently lacking.
Amphipods occurring at depths >6000 m have been
assumed to be obligate necrophages, and reports on the
rapid interception and consumption of bait by amphipods
in the trench confirm that these animals consume carrion
[30,31]. Nonetheless, cannibalism, carnivory and detritivory are also reported, with species-specific vertical and
ontogenetic variation in the apparent dominance of any
particular feeding mode [74]. The prevalence of sediment
in the guts of juvenile individuals [74] presumably provides
a source of both energy and nutrition, as hadal sediment
bacteria are known to synthesise large quantities of EFAs
[75,76]. The digestion of refractory organic compounds is
potentially enhanced by the presence of gut bacteria
[74,77,78], an adaptation apparent in shallower-water
counterparts [79,80].
Distinct differences among the morphologies and life
histories of the lyssianassoids enable them to be separated
into two guilds [43,81]. The relatively large benthopelagic
amphipods have shearing mandibles and capacious guts,
which are thought to enable them to take advantage of
sporadic food falls. They process food as discrete batches,
and are adapted for bursts of feeding activity followed by
lengthy periods of digestion and fasting. This lifestyle is
supported by the presence of wax esters in their tissues
[82], which serve as energy reserves in crustaceans that
encounter prolonged periods of food deprivation [83]. These
are also hypothesised to reduce the energetic costs of
swimming by helping to maintain neutral buoyancy [81].
By contrast, the smaller demersal species have triturative
(grinding) mandibles and a smaller gut, enabling them to
feed and process food continuously while retaining the
ability to brood young at the same time. Their relatively
quiescent life style and feeding mode possibly negate the
necessity for large lipid reserves, although this has yet to
be confirmed.
Seasonal and geographical changes in the quantity and
quality of POM reaching trench sediments have been
invoked to explain the high inter-trench variability in
meiofaunal biomass, which is reported to range from
44 10 [84] to 6378 3061 individuals per 10 cm 2 [57].
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The assemblages of benthic nematodes, harpacticoid copepods, kinorhynchs, polychaetes and gastrotrichs in the
Atacama Trench are approximately one third smaller than
their bathyal relatives, although the selective pressure(s)
driving this response remain unclear [57]. Meiofaunal
dwarfism contrasts starkly with the gigantism noted for
some trench-dwelling crustaceans, including amphipods,
tanaids, mysids and almost all isopods [1]. These species
are larger than any other representative of the genus, and
their unusually large size might be a response to ephemeral food resources, competition or predation [43,85]. For
example, the overlap of amphipod depth zones, and the
resulting ontogenetic partitioning of food resources,
suggests that competition may be an important structural
feature in food-limited environments [72] where predation
is reduced or absent. Recent observations in several
trenches using baited cameras at 6000–8000 m, however,
have revealed that larger crustaceans (decapods) and fish
(liparids) preferentially consume mid-sized (1.5 cm)
amphipods, presumably exploiting the high numbers of
prey that congregate at food falls [30,31]. Similarly,
tanaids also appear to prey on smaller individuals at the
deeper parts of the trenches (>8000 m). Whilst predation
provides a mechanistic explanation of why smaller sized
individuals of certain taxa may be absent [86], predation
along the deepest trench axes (10 000 m), where larger
amphipods are more abundant, has not been documented.
Thus, the relative abundance and size of amphipods is
most likely to be related to food supply and perhaps also to
predation risk, a pattern contrary to previous consensus
suggesting that invertebrate abundance declines only as a
function of depth [16,17,87].
Conclusion
An immediate challenge in understanding the ecology of
hadal trenches is to distinguish trench-specific community
structuring factors from those which are typically ‘hadal’.
This will require consideration of the effects of latitude,
overlying productivity and seasonality. There are no a
priori reasons to exclude the application of existing ecological theory to explain the diversity of trench communities; their generic environmental characteristics (e.g.
temperature, salinity and oxygen) are known to be comparable to those at shallower depths, and differences in
hydrostatic pressure are not overwhelming. Although it is
intuitive that some abrupt changes, such as formation of
the CCD, may form a physical barrier for some species [35],
there are numerous examples of adaptations that overcome this potential limitation. Exposure to high pressure
and difficulty in forming hard exoskeletons are not exclusively challenges faced by trench-dwelling organisms. The
ability to tolerate food deprivation and rapidly intercept
and capitalise on ephemeral food falls provides an
additional adaptation by which organisms can penetrate
beyond the impoverished upper trench slopes. We contend
that many features of the ‘hadal zone’ are merely extensions of those found at shallower depths. Nonetheless, it is
apparent that each trench system has unique characteristics owing to their geographical isolation. A naı̈ve hypothesis is that inter-trench variation in species composition is
likely to be primarily driven by the interaction of the
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overlying biogeographical province (POM quantity and
quality) and trench topography, rather than specific adaptations to hydrostatic pressure, temperature and/or any
other correlate of depth. However, the role of chemosynthetic production will need to be incorporated into this
hypothesis as knowledge of its distribution and importance
accumulates.
Trenches are poorly sampled and our knowledge of the
ecological structure and functioning of this environment
remains rudimentary. A current difficulty is that existing data are not sufficient to confidently apply overarching ecological theory. Indeed, it is not yet possible to
reliably distinguish between taxa of non-viable vagrants
from shallower populations and those which are trench
endemics. Considering all trenches to be a single habitat
is likely confound the interpretation of their ecology.
The collection of multidisciplinary observational and
experimental data, replicated across trenches, is a prerequisite for testing the generality of existing hypotheses. It will be essential to apply a broad spectrum of
techniques to examine phylogenetic relationships, physiological adaptations, diet, levels of biodiversity and
evolutionary traits of the inhabitants. Although a formidable task, technological advances, such as the Japanese remotely operated vehicle (ROV) Kaiko II, UK–
Japan HADEEP lander vehicles [6] and the US Hybrid
ROV Nereus vehicle [5], already exist and are operational. These present the opportunity for an internationally coordinated research campaign that considers
how ecological processes operate across the full span of
ocean depth.
Acknowledgements
This research, part of the HADEEP project (including T.F.), was
supported jointly by the Natural Environmental Research Council (UK)
and the Nippon Foundation (Japan) with additional support from the
University of Aberdeen, Scotland. D.J.M. is currently funded by the
Leverhulme Trust. We thank Dr. Henry Ruhl and Prof. Paul Tyler and
one other anonymous reviewer for their comments.
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