ARTICLE IN PRESS
Proc. R. Soc. B
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doi:10.1098/rspb.2005.3461
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University of Aberdeen, Oceanlab, Newburgh, Aberdeen AB41 6AA, UK
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Leibniz-Institut für Meereswissenschaften, IfM-GEOMAR, Düsternbrooker Weg 20, 24105 Kiel, Germany
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Marine Biology Research Division, Scripps Institution of Oceanography, UCSD 9500 Gilman Drive,
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La Jolla, CA 92093-0202, USA
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Institute of Marine Research, Flødevigen Marine Research Station, 4817 His, Norway
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British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road,
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Cambridge CB3 0ET, UK
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Møre Research, Section of Fisheries, PO Box 5075, 6021 Aalesund, Norway
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FRS Marine Laboratory, 375 Victoria Road, Aberdeen AB11 9DB, UK
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The oceanic abyss (depths greater than 3000 m), one of the largest environments on the planet, is
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characterized by absence of solar light, high pressures and remoteness from surface food supply
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necessitating special molecular, physiological, behavioural and ecological adaptations of organisms that
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live there. Sampling by trawl, baited hooks and cameras we show that the Chondrichthyes (sharks, rays and
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chimaeras) are absent from, or very rare in this region. Analysis of a global data set shows a trend of rapid
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disappearance of chondrichthyan species with depth when compared with bony fishes. Sharks, apparently
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well adapted to life at high pressures are conspicuous on slopes down to 2000 m including scavenging at
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food falls such as dead whales. We propose that they are excluded from the abyss by high-energy demand,
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including an oil-rich liver for buoyancy, which cannot be sustained in extreme oligotrophic conditions.
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Sharks are apparently confined to ca 30% of the total ocean and distribution of many species is fragmented
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around sea mounts, ocean ridges and ocean margins. All populations are therefore within reach of human
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fisheries, and there is no hidden reserve of chondrichthyan biomass or biodiversity in the deep sea. Sharks
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may be more vulnerable to over-exploitation than previously thought.
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Keywords: Chondrichthyes; sharks; deep-sea fishes; abyss; elasmobranches
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1. INTRODUCTION
sensitive to low light levels and possession of light organs
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The abyssal regions of the world’s seas and oceans (depth
(e.g. Isistius spp.; Widder 1998). They now form an
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above 3000 m) have been colonized by fishes during the
important component of deep-water fisheries down to
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last 70 Myr, contemporary with appearance of birds and
2000 m depth (Gordon et al. 2003) and are conspicuous as
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mammals on land. This was enabled and is sustained by
scavengers at whale carcasses (Smith & Baco 2003) and
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oxygenation of deep water by the modern global
baited cameras (Priede & Bagley 2000) suggesting that
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thermohaline circulation (Merrett & Haedrich 1997).
the deep sea may harbour a hidden diversity of
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Owing to stagnation events, final invasion of the eastern
Chondrichthyes.
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basins of the Mediterranean occurred only 6000 years ago
All the major classes of vertebrates, mammals, birds,
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(Rohling 1994). Deep-sea fishes were first discovered in
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reptiles, amphibians, bony fish (Osteichthyes) and
the 1860s and Günther (1880) reported the deepest bony
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Chondrichthyes (sharks, rays and chimaeras), are sufferfish as Gonostoma microdon at 5300 m from the Pacific
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ing declines in species number and population sizes
Ocean whereas the deepest Chondrichthyes were a ray
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owing to habitat changes or exploitation (IUCN 2004;
from 1033 m and a shark from 915 m. Deep-sea fishes are
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Şekercioğlu et al. 2004). Chondrichthyes are almost
not a distinct taxonomic group but are derived from a
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entirely marine, whereas bony fishes are found in all
diversity of shallow water types. Among the Chon55
aquatic environments from the highest altitude freshwater
drichthyes, including Holocephali (chimaeras) and Elas56
habitats through to the deep sea. Mammals, birds and
mobranchii (sharks and rays), many species show
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reptiles occur in terrestrial, freshwater and marine
anatomical adaptations to deep-sea life including eyes
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environments and sperm whales Physeter macrocephalus
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are capable of diving (Wahlberg 2002) to over 1000 m
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depth feeding on squid at bathyal depths. In comparison
Q1 * Author for correspondence ([email protected]).
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with the diversity of environments occupied by these
The electronic supplementary material is available at http://dx.doi.
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other classes of vertebrates, the Chondrichthyes are
org/10.1098/rspb.2005.3461 or via http://www.journals.royalsoc.ac.
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rather restricted in their habitat although mobility and
uk.
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The absence of sharks from abyssal regions
of the world’s oceans
Imants G. Priede *, Rainer Froese , David M. Bailey , Odd Aksel Bergstad ,
Martin A. Collins , Jan Erik Dyb , Camila Henriques , Emma G. Jones
and Nicola King
Received 29 September 2005
Accepted 20 December 2005
RSPB 20053461—1/2/2006—15:21—RAMESH—199724—XML – pp. 1–8
1
q 2006 The Royal Society
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Absence of sharks in the abyss
world-wide distribution of many species make this a
successful group.
From the earliest discoveries in the nineteenth century
to the present day, records have consistently shown that
Osteichthyes occur to much greater depths than Chondrichthyes. Nevertheless, it has been argued that biological sampling of the deep ocean (ESM) remains inadequate
and many species and populations of animals remain to be
discovered. However, if the depth distribution of Chondrichthyes is truncated at the boundary of the abyss, this
has important implications for management and conservation of these species, which are being heavily
exploited throughout their global distribution (Stevens
et al. 2000; Baum et al. 2003).
In this study, we deployed sampling equipment to
which both Chondrichthyes and Osteichthyes are susceptible over a depth range from less than 500 m on slopes
and over mid ocean ridges to the abyssal plains at 4800 m
in the Atlantic Ocean and 5900 m in the Pacific Ocean.
Three different techniques were used: baited cameras,
long-lines with baited hooks and demersal trawling. We
combine this with an analysis of the cumulative historical
record to examine the global depth limits of distribution of
Chondrichthyes compared with the Osteichthyes.
2. MATERIAL AND METHODS
(a) Trawling
A 45 ft (13.7 m) semi-balloon otter trawl was used. The trawl
was shot on twin warps with 120 kg otter boards bridled to a
single warp once the doors had spread (Merrett & Marshall
1981). Nominal spread of the mouth of the trawl (width of
sea-bed sampled) was 8.6 m. Haul duration was varied
between a bottom contact time of 30 min at the shallowest
stations to 3 h on the abyssal plain and the tow speed was
2–2.5 knots. Sampling was done over a period of 3 years
(2000–2002) during five cruises of the RRS Discovery in the
North East Atlantic in the region of the Porcupine Sea-Bight
and Porcupine Abyssal Plain. Cruises were in different
seasons to avoid biasing of sampling in relation to any fish
migrations that might occur (Priede et al. 2003).
(b) Baited hooks
Long-lining was done using the commercial vessel MS Loran,
which is fitted out as an autoliner. During 12 fishing days in
July 2004, 61 baited long line sets were done on the MidAtlantic Ridge between 42 and 558 N at depths from 450 to
4300 m. A total of 87 500 baited hooks were deployed.
(c) Baited camera
Baited cameras were deployed using a free-fall lander
technique (Priede & Bagley 2000). A piece of bait (usually
mackerel weighing ca 0.5 kg) was deployed on the sea floor
within the field of view of a downward looking video or timelapse stills (film or digital) camera attached to a lander frame
with an onboard computer, data storage, depth and current
sensors. The lander was left on the sea floor for up to 12 h
during which time images of fish approaching, consuming
and departing from the bait were recorded. The system was
recovered by acoustic command from the ship and images
were down-loaded for analysis. Species were identified by
reference to standard texts and comparison with voucher
specimens captured in trawls. Definitive species names could
not necessarily be allocated and cryptic species might not be
Proc. R. Soc. B
RSPB 20053461—1/2/2006—15:21—RAMESH—199724—XML – pp. 1–8
separable from images alone. Therefore, species counts in
photographs can be regarded as minimum estimates. Data
from 166 deployments are analysed (ESM).
(d) Archive data
Archive data for depth of occurrence of marine and brackish
water fish were abstracted from global data sets available on
FishBase (Froese & Pauly 2004). Original references were
checked for the deepest species including all occurrences of
Chondrichthyes deeper than 2500 m. Dubious records where
sampling gear traversed a wide depth range and depth of
capture was uncertain were rejected. Records of maximum
depth were accepted for 669 species of Chondrichthyes and
8691 species of Actinopterygii.
3. RESULTS
(a) Pelagic species
Chondrichthyes, notably sharks, are found near the
surface in the open waters throughout the world’s oceans.
Filter feeding planktivors clearly must swim near the
surface where most of their food is found, but maximum
dive depths of 850 m and over 1000 m have been recorded
for the basking shark (Cetorhinus; Sims et al. 2003).
Graham et al. (2005) recorded a dive of a whale shark
(Rhincodon) to over 980 m in the Atlantic Ocean off Belize
whereas studies around the Seychelles in the Indian Ocean
(ESM) logged dives to over 1000 m depth for 6 min but no
deeper than 1500 m. Pelagic predatory sharks also spend
most time at shallow depths (Sundström et al. 2001) but
we cannot exclude the possibility that occasional dives
deeper than 1000 m may occur. Discovery of the deeperliving megamouth shark (Megachasma; Taylor et al. 1983)
encouraged speculation on presence of new species of
deep-water pelagic sharks, but the depth of capture of the
first specimen was 400 m, Nelson et al. (1997) tracked one
in coastal waters at depths down to 166 m and putative
maximum depth for this species is cited as 1000 m (Froese
& Pauly 2004). We can find no evidence of any pelagic
chondrichthyan living at depths greater than 1500 m.
(b) Demersal species
The deepest living Chondrichthyes are bottom-living
species described as demersal, benthic. We have sampled
them in three distinctive ways: trawling, baited hooks on
long lines and baited cameras placed on the sea floor.
(i) Trawl capture
In the North East Atlantic Ocean, west of Ireland, we
carried out 52 bottom trawls at depths from 750 to
4800 m (figure 1) and found no Chondrichthyes in 17
trawls deeper than 2500 m depth. In contrast, the deepest
trawl (4835 m) returned eight species of bony fish
(Actinopterygii). In a series of 17 trawls on the MidAtlantic Ridge at 930–3505 m, we found no Chondrichthyes deeper than 2520 m except for one holocephalan, Harriota spp. at 3010 m.
(ii) Long lines
In a survey of the Mid-Atlantic Ridge in 61 baited long line
sets at 433–4200 m. The deepest Chondrichthyes below
3000 m, were a ray, Bathyraja pallida and a shark,
Centrophorus squamosus both captured at 3280 m. Bathyraja richardsoni, Hydrolagus affinis and Etmopterus princeps
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Absence of sharks in the abyss I. G. Priede and others
number of species
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number of species
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Figure 1. North East Atlantic Ocean, numbers of species
captured in trawls at different depths. Grey symbols,
Actinopterygii; black symbols, Chondrichthyes.
were caught at 2909 m and Hydrolagus pallidus at 2650 m
and Dipturus batis at 2619 m. Three deeper line sets
caught no Chondrichthyes, whereas bony fish were caught
at all depths (figure 2). All depths given are the minima for
lines which may follow the bottom slope over 100–200 m
of depth amplitude.
(iii) Baited cameras
We have colleted data from 166 deployments of baited
cameras placed on the sea floor at depths from 471 to
5900 m in the Atlantic Ocean at latitudes 538 N–548 S
(Armstrong et al. 1992; Priede et al. 1994a,b; Collins et al.
1999a,b), the North Pacific Ocean (Priede & Smith 1986;
Priede et al. 1990, 1994a,b), Indian Ocean (Witte 1999)
and Mediterranean Sea ( Jones et al. 2003). Of 84
deployments at depths greater than 2500 m, no Chondrichthyes were found (figure 3) except for observations of
rays at 2630 m in the Porcupine Sea-Bight (North East
Atlantic), and at 2908 and 3396 m on the slopes of the
Mid-Atlantic Ridge. The deepest sharks were Hexanchus
griseus and Etmopterus spinax at 2490 m in the Mediterranean Sea. The deepest chimaera was at 2355 m on the
Mid-Atlantic Ridge. Osteichthyes were present at all
depths.
(iv) Archive data
With the exception of seven species, Chondrichthyes were
confined to depths less than 2500 m (figure 4). Two
Holocephali were reported to occur to 2600 m, the
Rhinochimaeridae Harriotta haeckeli and Harriotta raleighana (Last & Stevens 1994). The deepest sharks were
Isistius brasiliensis reported from the surface to 3500 m
(Compagno et al. 1995) and Centroscymnus coelolepis
reported to 3700 m (Forster 1973) and observed from a
submersible at 3690 m depth (Clark & Kristof 1990). The
ray Rajella bigelowi is probably the deepest chondrichthyan
fish described as ‘Benthic on deeper continental slopes
and probably abyssal plains between 650 and 4156 m’
(Stehmann 1990). Thus, while Chondrichthyes are largely
confined to depths less than 2500 m, 260 species of bony
fish from several families were reported from depths
greater than 2500 m. The deepest recorded fish was the
Proc. R. Soc. B
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depth (m)
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Figure 2. Mid-Atlantic Ridge, numbers of species captured
on baited lines at different depths. Grey symbols, Actinopterygii; black symbols, Chondrichthyes.
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Figure 3. Number of species of fish attracted within view
baited cameras deployed at different depths, Atlantic, Pacific,
Indian Oceans and Mediterranean Sea. Grey symbols,
Actinopterygii; black symbols, Chondrichthyes. Horizontal
line at 3000 m indicates the upper limit of the abyss.
cuskeel Abyssobrotula galatheae trawled from 8370 m
(Nielson 1977).
Grouping the species into 500 m depth bins, we have
plotted the number of species as a function of their
maximum depth (figure 5). For Chondrichthyes, the slope
of decrease in species number with depth was 0.8 log units
(630%) per 1000 m compared with only 0.4 log units
(250%) per 1000 m for Actinopterygii. This indicated a
much more rapid disappearance of Chondrichthyes with
depth than the bony fish.
4. DISCUSSION
Recent data from a number of studies using depth sensing
devices attached to sharks indicate that pelagic species are
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Figure 6. The volume of ocean occupied by chondricthyes. A
hypsographic diagram showing the ‘chondrichthyan’ volume
in black. Apart from possible absence from the extreme
depths of the hadal ocean trenches (above 9000 m depth), the
Actinopterygii can be assumed to occur throughout the ocean
volume (grey).
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Figure 4. Maximum depth of occurrence of Chondrichthyes
and Actinopterygii. Global data set for maximum adult total
body length and depths of 669 species of Chondrichthyes
(black symbols) and 8691 species of Actinopterygii (grey
symbols).
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log species number
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Absence of sharks in the abyss
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Figure 5. Rates of decrease in species numbers with depth.
Log of number of species depth maxima per 500 m stratum
for the global data set. Black symbols and line, Chondrichthyes (log NZK0.0008xC2.9969, r2Z0.992); grey
symbols and line, Actinopterygii (log NZK0.0004xC
3.3227, r2Z0.9375); open symbols and thin line, large
Actinopterygii corresponding to the size range of the
Chondrichthyes (log NZK0.0004xC2.9733, r2 Z0.9176).
found no deeper than 1500 m in the open ocean. On
continental slopes, around islands, seamounts and on the
mid ocean ridges bottom-living or demersal Chondrichthyes were found down to 3000 m and with rare
occurrences down to just over 4000 m. Numerous trawl
and baited camera samples on the abyssal plains never
revealed the presence of any Chondrichthyes. The Beebe
project using deep-diving manned submersibles concluded that sharks may not normally inhabit waters deeper
than 2128 m but found rays and chimaeras at greater
Proc. R. Soc. B
RSPB 20053461—1/2/2006—15:21—RAMESH—199724—XML – pp. 1–8
depths and indicated that more research is needed to
reveal to true depth ranges (Clark & Kristof 1990). In the
present study except for one recorded capture, sharks were
absent from all samples deeper than 3000 m, whereas
bony fish were found at all depths. We believe the case is
already clear that Chondrichthyes have generally failed to
colonize the oceans deeper than 3000 m and it is very
unlikely that major new populations will be discovered in
abyssal regions.
The data presented in figures 4 and 5 are the maximum
recorded depths for each species and do not represent
typical depth of distribution. We conclude that the
cumulative sampling effort over almost 150 years since
the first discovery of the deep-sea ichthyofauna has now
accurately delineated the maximum depth limits for the
chondricthyes as essentially absent from the abyss at
depths greater than 3000 m. Extrapolation of the lines of
maximum depth in figure 5 gives a theoretical maximum
depth for the deepest chondrichthyan of 3893 m. For
bony fish, the corresponding depth of deepest occurrence
is 8350 m; very close to the actual depth of capture of the
A. galatheae.
(a) Volume of ocean occupied by Chondrichthyes
The total volume of the oceans is 1.37!109 km3.
Assuming that pelagic Chondrichthyes occur everywhere
to a depth of 1500 m, and demersal species down to 4000
and up to 250 m off the bottom, the ocean volume used by
Chondrichthyes is 0.395!109 km3 (figure 6). Hence, over
70% of the global ocean volume is devoid of Chondrichthyes, which are confined to the surface layers, ocean
margin region, around ocean islands, mid ocean ridges
and sea mounts. These areas are all intensively fished and
there is no evidence of a deep refuge of chondrichthyan
biodiversity or biomass in the abyss. Defining the abyss as
depths of 3–6 km (Herring 2002), Chondrichthyes are
essentially absent from this and the hadal zone more than
6 km. Furthermore, we hypothesize that the abyssal plains
may represent barriers to migration and dispersal
(especially given the lack of planktonic stages in Chondrichthyes) although such movement cannot be excluded
on the basis of existing evidence.
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(b) Explaining the absence of Chondrichthyes
from the abyss
Any hypothesis explaining the absence of Chondrichthyes
from the abyss should take into account the fact that many
species are well adapted to the deep-sea conditions at
2–3000 m. For example, chimaeras are generally coldwater deep-sea fish absent from shallow waters less than
80 m depth, abundant in the 1000–2000 m depth range
but never found in the abyss.
(i) Species number
In both bony fish and Chondrichthyes, species number
decreases with depth (figure 5). Simple probability implies
that the bony fish are more likely to have produced
representatives capable of surviving in deep environments
by virtue of much higher species number in shallow water,
rather than any underlying physical, physiological or
ecological cause. However, it is evident that species
number declines much more rapidly in Chondrichthyes
and the lower species reservoir in shallow water does not
explain lack of representation in the abyss. If Chondrichthyes had the same species extinction rate with depth
as the Actinopterygii, we would expect their maximum
depth to be 7500 m permitting survival throughout the
abyssal regions of the world and into the margins of the
hadal trench systems.
(ii) Body size
There is considerable debate regarding body size trends in
fish across depth strata in the oceans. A study of trends in
bony fish size between 500 and 5000 m depth in the North
East Atlantic shows that scavenging species are bigger
deeper whereas there is no significant size trend in nonscavengers. Metabolic modelling of foraging strategies
shows a clear advantage of increased size of scavengers in
the oligotrophic environment of the abyss (Collins et al.
2005). It is evident from figure 4 that Chondrichthyes are
predominantly bigger fish than Actinopterygii. Since
many Chondrichthyes can function as scavengers and
are attracted to bait, this would suggest a possible
advantage for their survival in the abyss. It is paradoxical
therefore to observe that it is the Chondrichthyes with
their larger size that show a higher extinction rate with
depth. Abstracting large Actinopterygii (more than 29 cm
max. length, spanning the same size range as the
Chondrichthyes) from the global data base, the number
of species decreases at a rate of 0.4 log units per 1000 m;
the same as for all Actinopterygii (figure 5). Compared
with Actinopterygii, Chondrichthyes are clearly deficient
in their ability to survive at increasing depth and this has
precluded their colonization of the abyss.
(iii) Water temperature
The deep sea is cold with typical temperatures of 2–4 8C,
but it is very unlikely that such temperatures exclude
Chondrichthyes from the abyss. There is no sharp
temperature discontinuity at the upper boundary of the
abyss and many species of fish are capable of living within
this temperature range. This does not exclude the
possibility that the presence of intermediate water masses
such as the Mediterranean intermediate water in the
North East Atlantic might act as an environmental cue
enabling deep slope-dwelling species to orientate to an
optimum depth. The influence of temperature as a barrier
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5
to colonization of the abyss is, however, further excluded
by the observation that Chondrichthyes are also absent
from the abyssal Mediterranean Sea, where we have
observed sharks attracted to baits at depths down to
2490 m and only Actinopterygii present at greater depths
(Jones et al. 2003). The Mediterranean Sea is warm all the
way to the bottom (ESM). It is evident that Chondrichthyes are excluded from abyssal regions of the seas
independently of the prevailing temperature regime.
(iv) Hydrostatic pressure
To preserve cellular function at high pressure, deep-sea
organisms require homeoviscous adaptation of membranes and structural adaptation of proteins (Macdonald
2001). These effects are evident in bony fish species living
deeper than 1000 m and while there are no data for
Chondrichthyes, we presume that pressure tolerance is
well developed in this group. Furthermore, Chondrichthyes generally have high concentrations of trimethylamine-N-oxide (TMAO) in their body fluids. In addition
to acting as an osmolyte, TMAO has been shown to act as
a universal stabilizer of protein structure. The muscles of
deep-sea shrimps, agnatha, Chondrichthyes and
Osteichthyes all have increased concentrations of TMAO
compared with shallow water species apparently conferring pressure tolerance on structural and enzyme proteins
(Yancey et al. 2002). With generally high TMAO
concentrations it seems that Chondrichthyes are preadapted to life at high pressures. Since many species of
Chondrichthyes can survive at 2000–3000 m, depth, and
there are occasional records to over 4000 m it is unlikely
that there is a fundamental physiological barrier to this
group extending its distribution to 6000 m, a modest
proportional change in pressure.
(v) Buoyancy
A characteristic of the deep-water sharks is large livers,
rich in lipids that enable them to attain almost neutral
buoyancy. Probably, the most successful demersal scavenging and predatory fish in the abyss is Coryphaenoides
(Nematonurus) armatus (Actinopterygii, Macrouridae),
which uses a gas-filled bladder for buoyancy. For 1 kg of
buoyancy using squalene (specific gravity 0.86) requires
7.14 kg of oil with an energy content of 264 MJ. The same
buoyancy using a gas-filled bladder entails a theoretical
pumping cost at 4000 m depth of 90 kJ, calculated for
oxygen (ESM). Even assuming efficiency of 5–10%, the
energy cost of buoyancy using an air bladder is trivial
compared with a lipid-based system, making incremental
increases in buoyancy during growth much less expensive,
assuming the swim bladder wall is gas impermeable. For
shallow-water fish adjusting the quantity of gas in the swim
bladder during vertical movements can be energetically
costly but for abyssal fish such movements, since they are a
small proportion of total water depth, result in negligible
volume changes and there is no requirement to adjust
quantity of gas in the bladder. Once the bladder is inflated,
given low permeability of the swim bladder wall,
maintenance cost of the swim bladder in abyssal fish is
lower than for shallower living species making the same
absolute vertical movements.
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Absence of sharks in the abyss
(vi) Metabolism
beyond the maximum depth of economically viable
Studies of swimming speed (Collins et al. 1999a,b) and
fisheries. For example, the roundnose grenadier Corymetabolism (Bailey et al. 2002) in bathyal (1000–3000 m)
phaenoides rupestris with a fishery targeted at shoals
and abyssal fish species indicate much lower activity in the
500–1000 m deep, occurs down to 2200 m. There is no
latter linked to a decrease in food supply with depth. We
such deep ‘protected area’ for Chondrichthyes, and the
believe the proximal reason for absence of Chondrichthyes
whole Class may potentially be at risk.
from the abyss is the absence of truly low energy forms for
survival in a deep oligotrophic environment. The penalty
of the need for a large lipid-rich liver may be decisive in
6. UNCITED REFERENCES
excluding Chondrichthyes from the abyss. The complete
lack of ‘whole-animal’ or tissue metabolic rate studies Q6 Clark & Kristof (1991) and Henriques et al. (2002).
leave this as an open question, which certainly demands
This work was supported by Census of Marine Life, NERC
further investigation.
grant no. GR3/12789 and NERC studentships to E.G.J and
(vii) Reproduction
Chondrichthyes have direct life cycles without larval
stages reproducing either through hatching of small
adult forms from egg cases (Stehmann & Merrett 2001)
or through bearing of live young. Such miniature adults
may be vulnerable in the abyss and some species migrate
into shallower water to breed. Many deep-water bony
fishes, however, produce buoyant eggs and larvae that are
presumed to develop remote from the sea floor and benefit
from greater food supply at surface layers of the oceans
(Merrett & Headrich 1997).
5. CONCLUSIONS
Observations or captures of Chondrichthyes at depths
over 4000 m are very rare whereas at these depths bony
fishes and other fauna can be quite abundant. The deepest
confirmed reports of a shark C. coelolepis at 3700 m and
the ray R. bigelowi at 4156 m are both species with their
main zone of distribution at much shallower depths;
minimum depths are 270, 650 m, respectively. This is in
contrast to a number of bony fishes that have minimum
depths in excess of 3000 m. The world’s deepest fish,
A. galatheae has a minimum depth of 3110 m and
Coryphaenoides yaquinae, which is an abundant macrourid
on the abyssal floor of the Pacific Ocean seen in our baited
camera images at 5900 m (figure 3), has a minimum depth
of 3400 m (Froese & Pauly 2004). Discovery of a new
shark, ray or chimaera at depths greater than 3000 m with
its predominant distribution in the abyss is very unlikely.
Special expeditions to reveal such a fauna may be difficult
to justify but as research expands in the deep sea more of
the ocean will be surveyed and gradually certainty
regarding faunal composition of the abyss will increase.
There is probably no single simple explanation for the
absence of Chondrichthyes from the abyss. More research
is needed on the effects of pressure on metabolic enzyme
activity, membrane structure and adaptations to pressure
in Chondrichthyes. Most information that is available is
for bony fishes.
The Chondrichthyes and Sharks in particular are
threatened world-wide by the intensity of human fishing
activity. The finding that they are largely absent from
regions of the deep sea beyond the reach of commercial
fisheries further emphasizes concern regarding the conservation of this class of vertebrates. Owing to low
productivity and slow growth rates in the deep sea,
exploitation of deep-water species is generally of doubtful
sustainability. However, some of the Actinopterygii that
are captured commercially have a depth distribution
Proc. R. Soc. B
RSPB 20053461—1/2/2006—15:22—RAMESH—199724—XML – pp. 1–8
N.K. C.H. was supported by Fundação para a Ciência e
Tecnologia, Portugal. Camera work off Angola and on the
Mid-Atlantic Ridge was supported by B.P. We thank
personnel on board the ships RRS Discovery, RV G.O. Sars
and MS Loran.
REFERENCES
Armstrong, J. D., Bagley, P. M. & Priede, I. G. 1992
Photographic and acoustic tracking observations of the
behaviour of the grenadier Coryphaenoides (Nematonurus)
armatus, the eel Synaphobranchus bathybius, and other
abyssal demersal fish in the North Atlantic Ocean. Mar.
Biol. 112, 535–544. (doi:10.1007/BF00346170)
Bailey, D. M., Jamieson, A. J., Bagley, P. M., Collins, M. A. &
Priede, I. G. 2002 Measurement of in situ oxygen
consumption of deep-sea fish using an autonomous lander
vehicle. Deep-Sea Res. I 49, 1519–1529. (doi:10.1016/
S0967-0637(02)00036-5)
Baum, J. K., Myers, R. A., Kehler, D. G., Worm, B., Harley,
S. J. & Doherty, P. A. 2003 Collapse and conservation of
shark populations in the Northwest Atlantic. Science 299,
389–392. (doi:10.1126/science.1079777)
Clark, E. & Kristof, E. 1990 Deep sea elasmobranchs
observed from submersibles in Grand Cayman, Bermuda
and Bahamas. In Elasmobranchs as living resources: advances
in the biology, ecology, systematics and status of fisheries (ed.
H. L. Pratt, S. H. Gruber & T. Tanuichi) Technical Report
90, pp. 275–290. Washington, DC: NOAA.
Clark, E. & Kristof, E. 1991 How deep do sharks go?
Reflections on deep sea sharks. In Discovering sharks (ed.
S. H. Gruber) Special Publication 14, pp. 79–84. Highlands, NJ: American Littoral Society.
Collins, M. A., Priede, I. G. & Bagley, P. M. 1999a In situ
comparison of activity in two deep-sea scavenging fishes
occupying different depth zones. Proc. R. Soc. B 266,
2011–2016. (doi:10.1098/rspb.1999.0924)
Collins, M. A., Yau, C., Nolan, C. P., Bagley, P. M. & Priede,
I. G. 1999b Behavioural observations on the scavenging
fauna of the Patagonian slope. J. Mar. Biol. Assoc. UK 79,
963–970. (doi:10.1017/S0025315499001198)
Collins, M. A., Bailey, D. M., Ruxton, G. D. & Priede, I. G.
2005 Trends in body size across an environmental
gradient: a differential response of scavenging and nonscavenging demersal deep-sea fish. Proc. R. Soc. B 272,
2051–2057. (doi:10.1098/rspb.2005.3189)
Compagno, L. J. V., Krupp, F. & Schneider, W. 1995
Tiburones. In Guia FAO para Identification de Especies para
los Fines de la Pesca. Pacifico Centro-Oriental (ed. W. Fischer
et al.), pp. 647–744. Rome: FAO.
Forster, G. R. 1973 Line fishing on the continental slope—
the selective effect of different hook patterns. J. Mar. Biol.
Assoc. UK 53, 749–751.
Froese, R. & Pauly, D. (eds) 2004 FishBase. World Wide Web
electronic publication. (www.fishbase.org)
705
706
707
708
709
710
711
712
713
714
715
716
717
718
719
720
721
722
723
724
725
726
727
728
729
730
731
732
733
734
735
736
737
738
739
740
741
742
743
744
745
746
747
748
749
750
751
752
753
754
755
756
757
758
759
760
761
762
763
764
765
766
767
768
ARTICLE IN PRESS
Absence of sharks in the abyss I. G. Priede and others
769
770
771
772
773
774
775 Q7
776
777
778
779
780
781
782
783
784
785
786
787
788
789
790
791
792
793
794
795
796
797
798
799
800
801
802
803
804
805
806
807
808
809
810
811
812
813
814
815
816
817
818
819
820
821
822
823
824
825
826
827
828
829
830
831
832
Gordon, J. D. M., Bergstad, O. A., Figueiredo, I. & Menezes,
G. 2003 The deep-water fisheries of the Northeast
Atlantic: I. Description and current trends. J. Northwest
Atl. Fish. Sci. 31, 137–150.
Graham, R. T., Roberts, C. M. & Smart, J. C. R. 2005 Diving
behaviour of whale sharks in relation to a predictable food
pulse. J. R. Soc. Interf. (doi:10.1098/rsif.2005.0082)
Published online.
Günther, A. C. L. G. 1880 An introduction to the study of fishes.
Edinburgh: Adam & Charles Black.
Henriques, C., Priede, I. G. & Bagley, P. M. 2002 Baited
camera observations of deep-sea demersal fishes of the
northeast Atlantic Ocean at 15–288 N off West Africa. Mar.
Biol. 141, 307–314. (doi:10.1007/s00227-002-0833-6)
Herring, P. J. 2002 The biology of the deep ocean. Oxford:
Oxford University Press.
International Union for Conservation of Nature and Natural
Resources 2004 IUCN Red List of Threatened Species.
(www.redlist.org)
Jones, E. G., Tselepides, A., Bagley, P. M., Collins, M. A. &
Priede, I. G. 2003 Bathymetric distribution of some
benthic and benthopelagic species attracted to baited
cameras and traps in the eastern Mediteranean. Mar. Ecol.
Prog. Ser. 251, 75–86.
Last, P. R. & Stevens, J. D. 1994 Sharks and rays of Australia.
Australia: CSIRO.
Macdonald, A. G. 2001 Effects of high pressure on cellular
processes. In Cell physiology sourcebook: a molecular
approach (ed. N. Sperelakis), pp. 1003–1023. San Diego,
CA: Academic Press.
Merrett, N. R. & Haedrich, R. L. 1997 Deep-sea demersal fish
and fisheries. London: Chapman & Hall.
Merrett, N. R. & Marshall, N. B. 1981 Observations on the
ecology deep-sea bottom-living fishes collected off northwest Africa (088–278 N). Prog. Oceanogr. 9, 185–244.
(doi:10.1016/0079-6611(80)90002-6)
Nelson, D. R., McKibben, J. N., Strong Jr, W. R., Lowe,
C. G., Sisneros, J. A., Schroeder, D. M. & Lavenberg, R. J.
1997 An acoustic tracking of a megamouth shark,
Megachasma pelagios: a crepuscular vertical migratory.
Environ. Biol. Fish. 49, 389–399. (doi:10.1023/
A:1007369619576)
Nielson, J. G. 1977 The deepest living fish Abyssobrotula
galathea. A new genus and species of oviparous ophidiids
(Pisces, Brotulidae). Galathea Rep. 14, 41–48.
Priede, I. G. & Bagley, P. M. 2000 In situ studies on deep-sea
demersal fishes using autonomous unmanned lander
platforms. Oceanogr. Mar. Biol. Annu. Rev. 38, 357–392.
Priede, I. G. & Smith Jr, K. L. 1986 Behaviour of the abyssal
grenadier Coryphaenoides yaquinae, monitored using
ingestible acoustic transmitters in the Pacific Ocean.
J. Fish Biol. 29, 199–206. (doi:10.1111/j.1095-8649.
1986.tb05011.x)
Priede, I. G., Smith Jr, K. L. & Armstrong, J. D. 1990
Foraging behaviour of abyssal grenadier fish: inferences
from acoustic tagging and tracking in the North Pacific
Ocean. Deep-Sea Res. 37, 81–101. (doi:10.1016/01980149(90)90030-Y)
Priede, I. G., Bagley, P. M., Smith, A., Creasey, S. & Merrett,
N. R. 1994a Scavenging deep demersal fishes of the
Porcupine Seabight, North-east Atlantic: observations by
baited camera, trap and trawl. J. Mar. Biol. Assoc. UK 74,
481–498.
Proc. R. Soc. B
RSPB 20053461—1/2/2006—15:22—RAMESH—199724—XML – pp. 1–8
7
Priede, I. G., Bagley, P. M. & Smith Jr, K. L. 1994b Seasonal
change in activity of abyssal demersal scavenging grenadiers Coryphaenoides (Nematonurus) armatus in the eastern
Pacific Ocean. Limnol. Oceanogr. 39, 279–285.
Priede, I. G., Deary, A. R., Bailey, D. M. & Smith Jr, K. L.
2003 Low activity and seasonal change in population size
structure of grenadiers in the oligotrophic central North
Pacific Ocean. J. Fish Biol. 63, 187–196. (doi:10.1046/j.
1095-8649.2003.00142.x)
Rohling, E. J. 1994 Review and new aspects concerning the
formation of eastern Mediterranean sapropels. Mar. Geol.
122, 1–28. (doi:10.1016/0025-3227(94)90202-X)
Şekercioğlu, Ç. H., Daily, G. C. & Ehrlich, P. R. 2004
Ecosystem consequences of bird declines. Proc. Natl Acad.
Sci. USA 101, 18 042–18 047. (doi:10.1073/pnas.
0408049101)
Sims, D. W., Southall, E. J., Richardson, A. J., Reid, P. C. &
Metcalfe, J. D. 2003 Seasonal movements and behaviour
of basking sharks from archival tagging: no evidence of
winter hibernation. Mar. Ecol. Prog. Ser. 248, 187–196.
Smith, C. R. & Baco, A. R. 2003 Ecology of whale falls at the
deep-sea floor. Oceanogr. Mar. Biol. Annu. Rev. 41,
311–354.
Stehmann, M. 1990 Rajidae. In Check-list of the fishes of the
eastern tropical Atlantic, vol. 1, (ed. J. C. Quero et al.)
pp. 29–50. Lisbon: Junta Nacional de Investigaçao
Cientifica e Tecnológica.
Stehmann, M. F. W. & Merrett, N. R. 2001 First records of
advanced embryos and egg capsules of Bathyraja skates
from the deep-north-eastern Atlantic. J. Fish Biol. 59,
338–349. (doi:10.1111/j.1095-8649.2001.tb00134.x)
Stevens, J. D., Bonfil, R., Dulvy, N. K. & Walker, P. A. 2000
The effects of fishing on sharks, rays and chimaeras
(chondrichthyans), and the implications for marine
systems. ICES J. Mar. Sci. 57, 476–494. (doi:10.1006/
jmsc.2000.0724)
Sundström, L. F., Gruber, S. H., Clermont, S. M., Correia,
J. P. S., de Marignac, J. R. C., Morrissey, J. F., Lowrance,
C. R., Thomassen, L. & Oliveira, M. T. 2001 Review of
elasmobranch behavioral studies using ultrasonic telemetry with special reference to the Lemon Shark,
Negaprion Brevirostris, around Bimini Islands, Bahamas.
Environ. Biol. Fish. 60, 225–250.
Taylor Jr, L. R., Compagno, L. J. V. & Struhsaker, P. J. 1983
Megamouth—a new species, genus and family of lamnoid
Shark (Megachasma pelagios, family Megachasmidae) from
the Hawaiian Islands. Proc. Calif. Acad. Sci. 4, 87–110.
Wahlberg, M. 2002 The acoustic behaviour of diving sperm
whales observed with a hydrophone array. J. Exp. Mar.
Biol.
Ecol.
281,
53–62.
(doi:10.1016/S00220981(02)00411-2)
Widder, E. A. 1998 A predatory use of counterillumination
by the squaloid shark, Isistius brasiliensis. Environ. Biol.
Fish. 53, 267–273. (doi:10.1023/A:1007498915860)
Witte, U. 1999 Consumption of large carcasses by scavenger
assemblages in the deep Arabian Sea: observations by
baited camera. Mar. Ecol. Prog. Ser. 183, 139–147.
Yancey, P. H., Blake, W. R. & Conley, J. 2002 Unusual
organic osmolytes in deep-sea animals: adaptations to
hydrostatic pressure and other perturbants. Comp. Biochem. Physiol. A 133, 667–676. (doi:10.1016/S10956433(02)00182-4)
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Absence of sharks in the abyss
Author Queries
JOB NUMBER: 20053461
JOURNAL: RSPB
Q1
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Please supply a title and a short description to appear
alongside the electronic supplementary material
online.
Please provide expansion for the acronym ‘ESM’ in its
first occurrence.
Please check the edit of reference Priede et al. (1994)
to Priede et al. (1994a,b) as per the reference list.
Please check the edit of reference Collins et al. (1999)
to Collins et al. (1999a,b) as per the reference list.
Please note the edit of the sentence "The deepest
confirmed reports of a shark.....respectively."
Please note that the references Clark & Kristof (1991)
and Henriques et al. (2002) are provided in the list, but
are not cited in the text.
Please provide volume number and page range for
reference: Graham et al. (2005).
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