doi:10.1016/j.cub.2008.01.022


Current Biology Vol 18 No 6
R252
Antarctic Ecosystem: Are Deep Krill
Ecological Outliers or Portents of
a Paradigm Shift?

Serendipitous observations of Antarctic krill feeding at abyssal depths may
revolutionise our view of the ecology of this supposed surface-dwelling animal
that is key to the function of the Southern Ocean ecosystem.
Andrew S. Brierley

In his poem ‘Thirteen Ways of Looking
at a Blackbird’ [1] Wallace Stevens’
description of a Turdus in a snowy
autumn landscape alludes to the
Cubist practice of observing subjects
simultaneously from numerous
viewpoints to present a novel
perspective. There is little direct
interaction between Cubism and
biology, but when biologists look at
systems in new ways, or with new
techniques, we often discover
something new, and data from
multiple perspectives can reveal
a view to which conventional
observations have been blind.
Observations from a remotely operated
vehicle (ROV) of apparently healthy
Antarctic krill, an animal thought to live
its adult life in the near-surface zone, in
the abyssal depths of the Southern
Ocean [2] provide a vivid illustration of
this. These observations may require
us to reappraise fundamentally our
notion of the biology of this key
Southern Ocean species, and affirm
that there are still discoveries to be
made by basic exploratory research.

Antarctic krill (Euphausia superba)
play a central role in the Southern
Ocean ecosystem. These diminutive
crustaceans, which reach a maximum
length of about 6 cm and wet mass
of about 2 g, consume phytoplankton
at the base of the food chain and,
so doing, make the carbon that
phytoplankton have fixed available to
the suite of higher predators, including
whales, penguins and fish, that feed
upon krill [3]. Without krill, many of
Antarctica’s iconic megafauna would
be absent. Adult krill have been
considered traditionally as occupants
of the upper ocean [4,5]. They
feed at the near-surface, where
photosynthesis occurs, and migrate to
depths of not much more than 250 m by
day to darker waters that provide some
refuge from predators that hunt by
sight. Krill mate and spawn in this
epipelagic zone. Although fertilized krill
eggs may sink to more than 1000 m [6],
adults have not previously been
thought to descend to the depths
from which some larvae emerge during
their ontogenetic ascent. Surveys of
krill distribution for fishery- and
ecosystem-management purposes
have been conducted on this premise
[7] and estimates of circumpolar krill
biomass — some in excess of
500 million tonnes, more than the
global human biomass — have been
calculated on the presumption of
a near-surface distribution [8]. The
observations by Clark and Tyler [2] of
mature krill feeding at depths as great
as 3500 m may necessitate a rethink of
this and many other aspects of the
biology and ecology of krill. In fact, if
these point observations turn out to be
representative of a wider geographic
or temporal phenomenon, they may
trigger a paradigm shift for our
understanding of the function of the
entire Southern Ocean ecosystem.

Stevens [1] observed his blackbird
among ‘twenty snowy mountains’.
Clark and Tyler [2] discovered krill in the
abyssal waters that are fringed by the
snowy mountains of Adelaide and
Alexander Islands to the west of the
Antarctic Peninsula. Their unexpected
observations were made off Marguerite
Bay during surveys in the austral
summer of 2006/07 with the ROV Isis
(Figure 1). The biologists were
piggybacking on a cruise run primarily
to look at deep sea geological
processes, and were hoping to use
video footage of the seabed taken by
the ROV to study large benthic
invertebrates such as sea cucumbers
and sponges. Krill were unexpected
in this abyssal environment: the
phytoplankton and smaller
zooplankton that are the mainstays of
krill diet are concentrated in the
photic zone near the sea surface
several thousand meters above. In the
short-lived Antarctic spring and
summer krill must eat large quantities
of food if they are to reproduce
successfully. The pronounced
seasonal nature of this high-latitude
location is characterised by a sharp
pulse of primary production as
phytoplankton proliferate in the
nutrient-rich surface waters that
become illuminated and warmed
following the passing of the long polar
night and the melting of the sea ice.
Grazers such as krill tune their lifecycles
to capitalize on this brief period of feast
and, whilst the summer months are
favourable for ship-based deep sea
research, conventional oceanographic
wisdom has it that grazers should be
near surface at this time.

The rate of phytoplankton production
during spring and summer blooms can,
however, sometimes be so great that
it exceeds the rate of consumption
by grazers in the shallows of the
watercolumn. Observations elsewhere
in the global ocean have shown that
heavy falls of ‘marine snow’ — dead and
decaying plankton remains sinking
from the surface — coincident with the
surface phytoplankton bloom provide
an important pulse of food to the
otherwise impoverished deep sea
environment [9]. The ‘snow’ particles
can accumulate to depths of
several mm on the seabed before
biodegrading. Clark and Tyler [2]
observed krill nose-diving into the
seabed in a behaviour that
resuspended particulate matter, which
the krill then ate. The authors suggest

Figure 1. The Isis ROV being deployed from
RRS James Clark Ross (photograph by Julian
Dowdeswell).



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that the krill they observed may have
migrated to the deep sea to exploit this
accumulated phytodetritus resource,
but lack the time series of observations
necessary to test this hypothesis. In
fact their paper is as stimulating for
the questions it tacitly poses as for the
truly fascinating observations it reports.
The observed krill might well have
migrated recently from the surface:
krill complete their twice-daily vertical
migrations of about 250 m in less than
2 hours around dawn and dusk and,
at that rate, could achieve a 3500 m
descent in about a day. Krill could have
swum downwards, feeding on the
falling ‘snow’ on the way [10], and might
remain near the seabed feeding on the
accumulated drifts before returning to
the surface once the table has emptied.

There have been reports of size
segregation of krill off the western
Antarctic Peninsula [11], with larger
animals being more abundant off shore
in summertime. Perhaps some
component of the adult population
migrates routinely down the shelf
slope — Clark and Tyler [2] observed
krill at all sampled depths between
550 m to 3500 m — and eventually
returns directly to the surface from the
abyss such that the post-bloom surface
distribution [11] is a consequence of
a deep sea foraging migration. This
raises the possibility of a previously
unrecognised carbon transport
pathway mediated by krill. Daily krill
migrations may play an important role
in transport of surface-fixed carbon to
the ocean interior [12]. If it turns out that
krill feed routinely on phytodetritus in
the deep sea and then return to the
surface, the carbon they re-import to
the surface could diminish the extent to
which carbon is naturally sequestered
to the deep sea by the ‘biological
pump’. It has been suggested that
physical processes have now rendered
the Southern Ocean less of a carbon
sink than it has been historically [13]:
the potential deep sea foraging
behaviour of krill could have additional
consequences for the global carbon
cycle and hence for the climate.

An alternative interpretation of the
observations of krill in deep water [2],
however, is that these animals are
members of a distinct and hitherto
unrecognised permanent deep sea
population that live out their life in the
deep sea. Given what we believe about
the dependence of krill on sea ice for
reproduction [14] this seems unlikely,
but then again it seemed unlikely 18
months ago that krill would be found
feeding at 3500 m. The only previously
published report of krill at the seabed
in deep water [15], observed by an ROV
at c. 400 m in the Weddell Sea, was
made in summer. The lack of
observations of krill in deep water in
winter so far may simply be a function
of zero sampling effort in winter.
Year-round sampling in the upper
water column has revealed previously
unknown patterns of variation in krill
abundance [16], and deep sea biology
has benefited from data gathered
remotely by long-term instrument
deployments [17]. The Global Ocean
Observing System (www.ioc-goos.org)
strives to collect data from ocean
environments at time and space scales
not practicable using standard
ship-borne sampling, and the deep
waters off Marguerite Bay are just one
of many global ocean environments
worthy of year-round monitoring.

In the shorter term, genetic studies
could provide insight to the degree of
exchange of animals between putative
surface and deep populations, and an
additional challenge for future ROV
deployments there would be to collect
large numbers of samples as well as
images. A deep sea population of krill
decoupled reproductively from sea
ice could be more resilient to the
environmental change manifesting to
the west of the Antarctic Peninsula
than surface cousins, since deep sea
temperatures are more stable than
surface temperatures. Krill in deep
water may literally and metaphorically
be out of hot water but, at this
stage, this remains little more than
speculation.

Yet another alternative explanation
for the deep-water krill [2] is that they
are unhealthy individuals that have
experienced difficulty in maintaining
depth by swimming and have sunk out
from the surface. Net caught krill can
appear to be swimming actively in the
bottom of buckets after removal from
the net, but sometimes lack the ability
to swim up into the water column,
perhaps due to injuries sustained
during capture. Clarke and Tyler [2]
noted cast-off exoskeletons at the
seabed that are indicative of moulting.
Crustaceans moult to grow and
animals that are growing are generally
healthy. However, intriguingly, for krill,
there are reports of stressed or starved
individuals moulting to attain a smaller
size with subsequently reduced
metabolic demands [18]: moulting
might be an act of desperation for an
animal struggling out of its depth or, as
Clarke and Tyler [2] suggest, the moults
might simply have accumulated at the
seabed following cast-off from healthy
animals near the surface.

Whilst our knowledge of temporal
variation in abundance of krill in the
deep sea is effectively nil, our
knowledge of spatial extent is not much
greater. There have been concerted
efforts to map the distribution of
krill abundance throughout various
sectors of the Southern Ocean [7] but,
frustratingly, the ROV observations
[2,15] have been off the grids of these
large scale surveys (Figure 2), and no
contemporaneous water column data
are available. Thus, we do not know
how seabed concentrations of krill are
related, if at all, to distributions in the
near surface. Clarke and Tyler [2] were
unable to estimate abundance of krill
on the seabed because their data,
collected with surveys of immobile or
slowly moving megabenthos in mind,
are not amenable to quantitative
appraisals of krill. We remain largely
ignorant of the biomass of krill in the
deep sea. All that we can say is that the
locations sampled so far by ROVs are
not considered centres of pelagic krill
concentration (Figure 2), raising the
possibility that elsewhere deep sea
abundances might be higher.

Given that krill play such a central role
in the Southern Ocean ecosystem,
efforts to determine circumpolar
abundance in the deep sea as well as in
the open ocean and under sea ice
should perhaps be encouraged.
Observations by SCUBA divers and
shallow-water ROVs first revealed the
importance to krill of feeding under ice,
and subsequent observations by an
Autonomous Underwater Vehicle (a
free-running vehicle not constrained by
an umbilical) have revealed something
of the extent to which krill are
distributed under ice [19]. The ROV
Isis is a powerful research tool with
full-ocean-depth capabilities, and
has provided another leap forward in
knowledge of krill: widespread use of
this and the arsenal of sampling devices
available to the modern-day marine
scientist will likely reveal additional
fascinating insights to the private lives
of krill and other ocean inhabitants.

The 2007 fieldwork by Clark and Tyler
[2] was part of the inaugural science
deployment of the Isis ROV. Their
startling and unexpected observations
make it clear that there is still a need for

http://www.ioc-goos.org


Current Biology Vol 18 No 6
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the type of basic exploration of the
planet’s inner space that remote and
autonomous technologies excel at
[2,19]. It can, however, be difficult to
persuade funders to support basic
exploratory research because, in the
absence of knowledge, it is difficult to
erect the kinds of credible null
hypotheses that grant review panels
are often directed to favour, and
‘fishing expeditions’ with no defined
endpoint can loose out in the
competition for finances. The Isis ROV
was delivered in 2003 and the joke for
too long was that Isis was Irretrievably
Stuck In Southampton (the city on
the south coast of the UK where the
National Oceanography Centre is
located). Whilst Cubists can create in
the studio, students of the deep sea
must embark to their natural
laboratory, and the difficulties in
getting Isis to sea were for several
years a source of major frustration.
Fortunately the research community
is learning to frame its proposals in
terms that make them competitive and
this, together with the attention to Isis
that has been drawn by the influential
House of Commons Science and
Technology Committee [20], will
hopefully ensure that the vehicle can be
exploited increasingly in the coming
years. As Apsley Cherry-Garrard and
companions learnt during their ‘Worst
Journey in the World’ to gather penguin
eggs in the winter of 1911, the quest
for knowledge in far-flung locations can
be fraught with risk. In the grand
scheme of things, however, 21st

century deep ocean exploration is likely
to deliver far greater reward than the
financial ‘risk’ it presents. Hopefully in
the coming years biologists will match
Cubists in their ability to portray their
subjects from multiple spatial and
temporal perspectives, and progress
towards the holistic view required for
fuller understanding of ecosystem
function.

References
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Deep water seabed observations of krill (red crosses) are at locations off the grid of the most
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17. Bett, B.J., Malzone, M.G., Narayanaswamy, B.E.,
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18. Ikeda, T., and Dixon, P. (1982). Body shrinkage
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19. Brierley, A.S., Fernandes, P.G., Brandon, M.A.,
Armstromg, F., Millard, N.W., McPhail, S.D.,
Stevenson, P., Pebody, M., Perrett, J.,
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20. House of Commons Science and Technology
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Tenth Report of Session 2006-07. Volume 1.
pp. 147. London.

Pelagic Ecology Research Group, Gatty
Marine Laboratory, University of St. Andrews,
Fife KY16 8LB, Scotland, UK.
E-mail: asb4@st-and.ac.uk

DOI: 10.1016/j.cub.2008.01.022

mailto:asb4@st-and.ac.uk

	Antarctic Ecosystem: Are Deep Krill Ecological Outliers or Portents of a Paradigm Shift?
	References