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201
32 Biodiversity patterns in the Southern Ocean: lessons from
Crustacea
CLAUDE DE BROYERl, KRZYSZTOF JAZDZEWSKP AND PATRICK DAUBYl
lDepartement des Invertebres (Carcinologie), Institut Royal des Sciences Naturelles de Belgique, Rue Vautier 29, B-IOOO
Bruxelles, Belgium; 2Laboratory of Polar Biology and Oceanobiology, Department of Invertebrate Zoology and Hydrobiology,
University of Lodz, 12/16 Banacha st., 90-237 Lodz, Poland
e-mail: claude.debroyer@naturalsciences.be
ABSTRACT
The accurate assessment of Antarctic biodiversity, the understanding of its ecofunctional role and
the requirements for its conservation are recognized current priorities in the context of global
environmental change and accelerating loss of biodiversity.
Fauna and flora inventories, taxonomy and classification, processes driving the origin, maintenance
and change of biodiversity, roles of biodiversity in ecosystem functioning, conservation, restoration,
sustainable use and monitoring of biodiversity are on the biodiversity research agenda over the
world. On this background, a review of some recent developments in marine biodiversity research in
the Antarctic is made using the Crustacea as a model group.
Emphasis is put on some general patterns of biodiversity and biogeography. The up-to-date
coverage of surveys of the Antarctic marine fauna is tentatively assessed as well as the needs in
taxonomic expertise and tools, information technology resources and expanding exploratory surveys.
Key Words: Crustaceans, Antarctic, biodiversity, biogeography, latitudinal gradients, taxonomic
tools.
INTRODUCTION
In the present context of global environmental change and accelerating
loss of biodiversity and in relation with the ongoing efforts to
implement over the world sustainable development policies, the
accurate assessment of Antarctic biodiversity, the understanding of its
ecofunctional role as well as the requirements for its conservation
appear of critical importance.
Fauna and flora inventories, taxonomy and classification, processes
driving the origin, maintenance and change of biodiversity, role of
biodiversity in ecosystem functioning, conservation, restoration,
sustainable use and monitoring of biodiversity are today world wide
priorities for biodiversity research (Loreau & Olivieri 1999).
Basic biodiversity research has a very old background b'uta strong
resurgence of interest in biodiversity topics occurred in recent years,
partly as an effect of the implementation of the Convention on
Biological Diversity (CBD) signed in Rio de Janeiro in 1992. The
CBD had indeed a significant impact on public awareness ofthe rapid
loss of species and on the science of biodiversity world wide, even
though not all nations did ratifY the Convention. Signatory parties
were required to conserve biodiversity, to use it in a sustainable way
and to develop a biodiversity strategy and action plan at national level.
Other obligations include the development of a "clearing house"
mechanism to communicate efficiently all pertinent biodiversity
information and the redaction ofa country study, which includes i.a. a
comprehensive inventory of biodiversity at the country scale, an
evaluation of its status and its monitoring (Secretariat CBD 200 I).
It appears that the provisions of the CBD are applicable only to
sovereign territories so that, under the Antarctic Treaty, the Antarctic
south of 600S is not included (P. Clarkson, pers. com.). Many of the
CBD elements are already implicit or explicit in the Antarctic Treaty
instruments, but the provisions for a systematic inventory of bio-
diversity, for monitoring and for managing and disseminating the
biodiversity information (the "clearing house" mechanism), among
others, remain to be fully implemented within the Antarctic Treaty
System.
A recent European Science Foundation workshop on Polar
Biodiversity stressed that future work should be developed around
three themes: the polar biodiversity patterns (their nature and driving
processes), the ecofunctional role of biodiversity, polar biodiversity
and global change (Crame 200 I).
This paper concentrates on some recent progresses in the study of
compositional and structural aspects of Southern Ocean biodiversity
at the species level. Examples from the Crustacea will be used, as
Antarctic Biology in a Global Context. pp. 201-214.
Edited by A.H.I. Huiskes, WWc. Gieskes, 1. Ro=ema, R.M.I. Schorno, s.M. van del' Vies &W1. Woljj.
i[j2003 Backhuys Publishers, Leiden, The Netherlands.
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202 C. DE BROYER
crustaceans are a good model for biodiversity studies: they indeed
constitute the most speciose animal group in the Antarctic, they are
ubiquitous in the Southern Ocean habitats, they playa key role in its
pelagic and benthic ecosystems, and at least some of them are well
represented in the Antarctic fossil records.
BIODIVERSITY PATTERNS OF ANTARCTIC CRUSTACEA
Species richness
In a recent overview of the Antarctic marine biodiversity, Arntz et al.
(1997) compiled the species number per taxa for most groups of marine
animals and plants occurring south of the Polar Front (Fig. I). This
graph clearly shows the relative importance of polychaetes and
molluscs and the predominance of crustaceans. When considering such
compilation it must be kept in mind that if the Antarctic vertebrates
inventory can be considered close to completion, the invertebrates
inventory in general is hardly complete (Fig. 2). Speculative estimates
of remaining unknown taxa varied according to the groups and the
specialists. It has been estimated for instance that there could be as
many as 2000 nematode species in the Southern Ocean as a whole
where 331 species are presently known (De Broyer et al. 200 I a).
We have compiled the present data on species richness of the
different crustacean groups in the Southern Ocean (Table I). As far as
possible, a clear differentiation has been made between the strictly
Antarctic fauna, occurring south of the Polar Front, and the whole
Southern Ocean fauna, taken here in its wide sense (see e.g. Deacon
1984), thus including both the Antarctic and the Subantarctic regions
(Hedgpeth 1970). The table clearly shows the dominance of Per acarid a,
the scarcity of Decapoda and Cirripedia and the total absence of
Stomatopoda in the Antarctic. According to the presently available
knowledge, peracarid crustaceans -largely dominated by amphipods
and isopods - constitute the most speciose animal group in the Antarctic
and possibly in the whole Southern Ocean (De Broyer & Jazdzewski
1996).
o200 400
Macroalgae
Dlatomsa
Dlnonagsllata
foraminifera
Porlfsra
Cnldarla
Nematoda
Turbellarla
Prla pullda
Sipunculida
Polychaeta
Mollusca
Pentopoda
Pelagic Crustacea
Benthic Crustacea
echinodermata
Lophophorata
Ascldlacea
Thallacea
Pisces
Aves
Plnnlpedla
Cetacea
From their review Arntz et al. (1997) remarked that the Antarctic
marine ecosystem as a whole seems to have a lower percentage of
species known to date in most higher taxa than would be expected
from its sizeable share of the area of the world's oceans, which is
roughly 10%. This is the case for most crustaceans (Table I) but for
the benthic species a closer comparison remains to be made by taking
into account the relative surface of continental shelves instead of the
total ocean surface.
This remark draws attention to the crucial question of species: area
relationships in such a comparison. Species richness is known to
increase with area (e.g. Gaston & Blackburn 2000), and, this might be
because larger areas have more individuals, comprise more habitats
and more biogeographical regions (Rozenzweig 1995). But according
to Gray (200 Ia), these hypotheses have not been adequately tested yet
in the marine domain.
Arntz et al. (1997) also noted that there are no common patterns of
species richness between the different Antarctic subsystems, i.e.
between the various zones or belts surrounding the continent, between
the successive bathymetric zones or between the diverse habitats. For
example, the shallow subsystem (in particular less than 30m) - which
is strongly affected by physical disturbance due to ice - is much poorer
than the deep shelf and the upper slope where the richest communities
occur (see e.g. Gutt 2000).
These observations on the spatial variability of biodiversity patterns
stress the fundamental importance of defining the right scale of species
richness measurement for allowing meaningful comparison of
biodiversity. In this context, to avoid some confusion, Gray (200 Ia,b)
recently proposed a unifYing terminology (Fig 3). The scale pattern
has concrete implications: the local species richness depends on the
large area (or landscape) species pool, and the landscape in turn on
the biogeographical province level: it is a kind of « Russian doll-like»
system (Gaston & Blackburn 2000).
Moreover, it must be considered in comparative studies of
biodiversity that determinants of species richness are oftwo different
600 1000 14001200800
Fig.}. Number of marine Antarctic species (from Arntz et al. 1997, modified).
1...<)
)
.;-..,
BIODIVERSITY PATTERNS IN THE SOUTHERN OCEAN: LESSONS FROM CRUSTACEA 203
800
750
600
550 -NEMATODA
700
650 -AMPHIPODA
500
450
ECHINOIDEA
400
350
300
250
200
150
100
50
o
1770 1790 1810 1830 1850 1870 1890 1910 1930 1950 1970 1990
Year of description
Fig. 2. Rate of new species description in three representative groups of the Southern Ocean zoobenthos.
Table I. Species richness of Crustacea in the Southern Ocean (south of the Subtropical Front Zone) and in the Antarctic (south of the Antarctic Polar Front
Zone); B = benthic, benthopelagic and hyperbenthic species; mB= mostly benthic; P = pelagic species; (from various sources).
World Southern Ocean Antarctic
(south of STFZ) (south of APFZ)
323
74
60
7
182
% Antarctic:
world
Ostracoda (marine)
Myodocopa (mB)
Halocyprida (P)
Cladocopa (B)
Podocopa (mB)
Copepoda
Calanoidea (+ others)
(= All marine P)
Harpacticoidea
(marine B)
Cirripedia (B)
MALACOSTRACA
Leptostraca (B)
Stomatopoda (B)
Euphausiacea (P)
Peracarida (marine)
Mysidacea (mB)
Amphipoda (marine)
9500 3.4 (S.Oc.)
38
60
11500
2075 346 16.3 (S.Oc.)
3500 60 1.7
1000
30 000
20
400
86
16000
780
6000
45 28 2.8
7000
850
1253
10 000
3
7
32
1528
59
828 (B+P)
720 (B)
427
127
94
132
98 (B)+ 34 (P)
11
44 (B+P)
3
1
1
31
34
2
o
8
1049
37
539 (B+P)
470 (B)
365
74
63
24
12 (B)+ 12 (P)
3
21 (B+P)
o
o
o
4
1(P)
10
Isopoda (marine)
Tanaidacea (B)
Cumacea (B)
Decapoda
9.3
6.6
4.7
8.9
7.8
5.2
8.7
5
0.24
Peneidea (P)
Caridea (B+P)
Thalassinidea (B)
Palinura (B)
Astacidea (B)
Anomura (B)
Brachyura (mB)
.J;t '"
1.,.:.,;-.:;.,,", -:~;0X'k' ';,
SCALE OF SPECIES RICHNESS DEFINITION: THE SPECIES
RICHNESS OF
Point species richness: SRp A single sampling unit
Sample species richness: SRs ALPHA A number of sampling units from a site of
DIVERSITY defined area
Large area species richness: SRL GAMMA A large area which includes a variety of
DIVERSITY habitats and assemblages
Biogeographical province species richness: SRB EPSILON A biogeographical province
DIVERSITY
TYPE OF SPECIES RICHNESS
Habitat species richness: SRH A defined habitat
Assemblage species richness: SRA A defined assemblage of species
204 C. DE BROYER
Fig. 3. Terminology of scale and type of species richness according to Gray (200Ib).
kinds acting at different time and spatial scale. On one hand, long
term evolutionary processes like speciation and geographic dispersal
(or more generally all regional and historical processes which determine
the number of species able to be present in a community) and on the
other hand, short-term ecological processes which assure the
maintenance of the diversity and which involve all local physical factors
and biotic interactions controlling the numbers of actually coexisting
species (Gage & Tyler 1991).
Finally, it has been repeatedly stressed that meaningful comparisons
of marine species richness or other measurements of diversity are
hampered by lack or scarcity of comparable datasets obtained by
standardized equipment and procedures and relying on similar level
of taxonomic knowledge (Arntz et al. 1997).
Composition peculiarities of the Antarctic crustacean fauna
The absellce or scarcity of some groups
In terms of composition, the Antarctic crustacean fauna presents some
extremes: some taxa are totally absent or poorly represented, some
other groups on the contrary are very rich in terms of species number
and higher taxa (Table I).
Stomatopoda. The Stomatopoda, which number about 400 spp in
the world (Reaka & Manning 1986), are totally absent from the
Antarctic and the Arctic seas. Stomatopods are mostly tropical forms
inhabiting shallow waters. Seventeen species are known to occur below
400m (maximum depth record: 824m), most ofthem being sublittoral
species that frequent the outer shelf and upper slope (Manning 1991).
Seven species ofSquillidae have been found in cool temperate waters
at littoral and sublittoral depth south of42°S in southern South America
(Dahl 1954) and in Tasmania, southern New Zealand and surrounding
islands, as far south as Auckland Island (Manning 1966).
C;rr;ped;a. The outstanding feature oftheAntarctic cirripedan fauna
is the extremely high proportion of lepadiform versus balaniform
barnacles: approximately 32 to I (Newman & Ross 1971). Over the
world, the balaniform barnacles are usually well represented among
the littoral fauna and their scarcity in Antarctic waters was correlated
with the lack of suitable littoral habitats, but also with the geological
history of Antarctica (Dell 1972). During Cenozoic glaciations it seems
that shallow water balaniform species of Gondwanian origin were
completely eradicated. Most of the extant species of benthic cirripeds
known from south of the Polar Front are shelf species found below
100m or deep sea species (Newman & Ross 1971).
Decapoda. The scarcity of decapods in general and the total absence
of brachyuran crabs in particular are well known but still intriguing
features of the Antarctic invertebrate fauna. This scarcity is in sharp
contrast with the richness of the Cenozoic decapod fauna of both
macruran and brachyuran species on the Antarctic shelf as revealed
by paleontological records (e.g. Feldmann & Tshudy 1989, Feldmann
et al. 1993). Like other invertebrates and fish, this Cenozoic fauna
was probably eliminated by the periodic extensions of the Antarctic
ice cap on the continental shelf (Clarke & Crame 1989, 1992, Clarke
& Johnston 1996). But curiously enough most decapods were
apparently unable to re-invade the Antarctic shelf.
The decapod fauna composition was recently reviewed in details
by Gorny (1999). Twenty-four decapods (12 pelagic and 12 benthic
species) occur south of the Antarctic Convergence (Table I). They
represent only 0.25% of the world decapod fauna. Benthic taxa are
represented by 8 caridean shrimps (5 spp occurring on the Antarctic
shelf) and 4 anomuran crabs. Two of the latter species (Paralomis
birsteini Macpherson 1988a and Lithodes turkayi Macpherson 1988b)
have been found close to the Antarctic shelf on soft bottoms at locations
nevertheless separated from the continent by deep waters of more than
3000 or 4000m (Birstein & Vinogradov 1967, Klages et al. 1995,
Macpherson 1988a,b).
Different hypotheses -but stilI no convincing explanation - were
proposed to explain the depauperate decapod fauna and the absence
ofthe whole group ofbrachyurans. Clarke & Crame (1989) and Crame
(1999) have stressed that low temperature per se cannot be the reason
for the lack of evolutionary success of Southern Ocean Decapoda (and
of some other groups, like Bivalvia). They suggested that low and
seasonal availability of food supply and/or habitat limitation could be
;"-,j'";>1;;S:i",',,,'I,:~';~iGiJ,l~:6.{\:'i;;8!;1,\<7b:,
BIODIVERSITY PATTERNS IN THE SOUTHERN OCEAN: LESSONS FROM CRUSTACEA 205
more important factors. The larval development handicap was on the
other hand put forward by Wagele (1995).
Recently, Gorny (1999) proposed an explanation based on the lack
of suitable habitats. He observed that among the decapod groups
currently present in the Southern Ocean (s.I.) the caridean shrimps
and the anomuran crabs are characterised by a high degree of eurybathy
and a large spectrum of habitat preferences contrasting with the general
restriction ofBrachyura to sandy or muddy bottoms in shallow waters
above 200 m. He argued that, after their elimination during the
Cenozoic glaciations, brachyurans were unable to re-invade the
Antarctic shelf because soft bottoms mainly occur below 200 m, and
shallow water habitats are disturbed by anchor-ice and iceberg scouring.
It may be remarked that, at least in some places in the maritime Antarctic
(e.g. Admiralty Bay, King George Island), soft bottoms do occur
abundantly at depths of 50 to 150 m.
On the other hand, ice disturbance should not be more troublesome
for the vagile Brachyura than for the more sedentary Echinodermata
that are well represented in the Antarctic sublittoral.
The most recent hypothesis - the "magnesium regulation hy-
pothesis"- invoked ecophysiologicallimitations to the geographical
distribution ofreptant decapods. The different distribution patterns of
caridean shrimps and reptant decapods are explained by differences
in the capacity to regulate magnesium levels in the haemolymph. The
magnesium level is dependent of threshold temperatures below which
cold-induced failure of cardiac and ventilatory performance occurs in
brachyurans but not in carideans (Frederich et al. 200 I).
The high species richness of amphipotls anti isopotls
Among the Antarctic crustacean fauna, amphipods and isopods are
obviously highly speciose groups (Table I). The high species richness
of the Antarctic zoobenthos (or at least of some key macrobenthic
groups) has been usually attributed in the literature to the long evolution
in isolation ofthe southern polar ecosystem, the regular seasonality or
predictability of the system, the role of disturbance, and the high spatial
heterogeneity (see Arntz et al. 1994).
The relatively great age of the circumpolar Southern Ocean (23.5+/
- 2.5 Ma, Barker & Burell 1982) and the long evolutionary history in
isolation of the Antarctic marine fauna have been rather well
documented (e.g. Clarke & Johnston 1996). Relying on paleontological
and phylogenetic evidence, Crame (1999) suggested that a number of
key benthic groups present in the southern latitudes have Late
Cretaceous (i.e. 100-65 Ma) origins or even could have started their
diversification during Early Cretaceous times (130 Ma) when the first
significant marine incursion occurred across the Gondwana super-
continent and a high-latitude group of continents was isolated. He
then argued that one ofthe fundamental reason why some clades, such
as the peracarid crustaceans and the gastropod molluscs, are among
the most speciose in the Antarctic and Subantarctic regions may be
"simply because they are old".
Moreover, peracarid crustaceans feature some characters that
obviously may reduce gene flux between populations and facilitate
speciation. Their diversification success can be first of all attributed
to their brooding habit, which implies limited dispersal of juveniles
and enhanced reproductive isolation at least in some groups. Many
peracarids have also a rather low mobility, with the exception of the
typical pelagic and hyperbenthic swimmers among amphipods and
mysids. A substantial part of the amphipod species for instance are
known to be bottom crawlers, burrowers, nestlers, tube-dwellers, or
clingers on or associates to algae or benthic sessile suspensivores.
They are sedentary or weakly motile or have very limited swimming
~ crawling
swimming
walking
vertical migration
Fig. 4. Diversity of habitats of some representative gammaridean amphipod taxa in the eastern Weddell Sea (from De Broyer et at. 2001. updated).
~J »<4\"';i\~ ~~ ,
206 C. DE BROYER
periods (restricted for example to the reproductive male stage).
But other causes of diversification have been suggested for the
Antarctic peracarid crustaceans (e.g. Wagele 1992a, De Broyer &
Jazdzewski 1996, Brandt 1999). The most speciose group - the
amphipods - is known to be primarily a cold water adapted group,
which radiated more successfully in cold waters (Barnard & Barnard
1983).
The importance of the habitat heterogeneity has been stressed by
several recent studies (e.g. Clarke & Johnston 1996, De Broyer et al.
200 Ib). In the eastern Weddell Sea 230 amphipod species have been
recognised. This high species richness has been mainly attributed to
the diversity of habitats offered by the biogenic sediments such as the
sponge spicule mats and bryozoan debris and the abundant and diverse
sessile epibenthos which provide tri-dimensional substrates, food
resources and opportunities for symbioses (Fig. 4).
Another potential factor of diversification is the emergence of new
adaptive zones due to the faunal extinction events during the Tertiary
cooling of the Southern Ocean. In particular, the extinction of many
decapod crustaceans may have allowed some peracarid crustaceans to
fill their vacant ecological niches (Clarke & Crame 1989, De Broyer
& Jazdzewski 1996, Brandt 2000). By analogy with extant species,
extinct decapods can be supposed to have been mostly scavengers
and detritivores (and probably also partly predators), all trophic types
well represented among peracarids today. Part of the success of the
"reptant" iphimedioid amphipods or serolid isopods might be due to
the absence of reptant decapods through reduced predation and
competition. Moreover, decapod scarcity may have allowed a widening
ofthe size spectrum among the Antarctic amphipods and isopods which
comprise many large species (De Broyer 1977, Chapelle 200 I, see
Fig. 6).
A possible co-evolution with the Antarctic Notothenioidei was
suggested by different studies (Wage Ie 1992b, Brandt 2000). Like
some peracarid crustaceans, notothenoids have experienced an adaptive
radiation in the Southern Ocean during the Tertiary (e.g. Eastman &
Clarke 1998). As many of them predate on peracarid crustaceans,
Brandt (2000) suspected some links between the notothenoid evolution
and the success of some peracarid taxa. Several amphipod and isopod
families possess body ornamentation of teeth and spines, sometimes
strongly developed. On the other hand, some detailed analyses of the
feeding habits of nothothenoids by Grohsler (1992) and Olaso et al.
(2000) showed that the peracarid preys were mostly composed of
species lacking this strong body ornamentation. Relying on these results
and on a similar Baikal Lake example (Bazikalova 1954), Brandt
(2000) postulated that the development of such spiny ornamentation
in some isopods such as Serolidae and in some amphipods such as
Iphimediidae and Epimeriidae could confer some selective advantage
in terms of avoiding or limiting predation.
In the same line, it may be suggested that the very successful
radiation ofthe Antarctic iphimedioid and stenothoid amphipods could
be in some way related to the radiation of the abundant sessile
suspension feeders that constitute their prey or their hosts. Iphimediidae
and related families are mostly specialized micropredators on sponges,
bryozoans, hydrozoans or cnidarians and Stenothoidae are known as
associates to diverse benthic organisms (Coleman 1989a,b, Dauby et
al. 200 I, De Broyer et al. 200 Ib).
DISTRIBUTIONAL PATTERNS OF BIODIVERSITY
Latitudinal gradients in species richness
The question oflatitudinal gradients in species richness and taxonomic
diversity is a recurrent theme in the research agenda of macro ecology,
which examines patterns and processes at the geographic scale.
Latitudinal gradients are considered of particular interest as they are
complex phenomena which have arisen over a long period of time
(Ricklefs 1987, Crame 1999), and they can help to disentangle the
determinants of species richness at regional and local scales.
Anomuran decapods for example exhibit a clear latitudinal trend
in species richness along the different Atlantic biogeographical
provinces of America (Boschi 2000) (Fig. 5). A similar bell-shaped
curve was demonstrated for a few other groups, in particular in bivalve
molluscs (e.g. Crame 1999). This distribution type obviously parallels
the well established trend in terrestrial biota towards high latitude
decrease in species richness. However, there is growing evidence that
this cline is far from general in the Southern Hemisphere and might
be limited to taxa requiring skeletal carbonate (Clarke 1992, Clarke &
Crame 1997).
Recent regional data from important taxa support the contention
that the latitudinal gradient of decreasing species richness towards the
pole does not hold for the Southern Hemisphere. Despite incomplete
data, species richness in gammaridean amphipods (Fig. 5) does not
reveal a clear cut trend with high numbers at high as well as at low
latitudes (Carribean province). This might partly be due to the higher
structural heterogeneity of suitable habitats known to occur at these
different latitudes.
The issue of the Antarctic benthos species richness in a world-
wide latitudinal context was recently discussed in details in particular
by Clarke (1992), Clarke & Crame (1997), Crame & Clarke (1997),
Crame (1999) and Gray (200 I a). Some general conclusions can be
summarized as follows:
I. There are still very few ifany conclusive studies at the alpha diver-
sity level.
2. Useable data are still too few and of limited comparability.
3. Data are of two types: sample species richness from few very small
areas or large regional species lists. What is needed, according to
Gray (200Ia) is, on one hand, studies that examine species: area
relationships at intermediate scales, like for instance the landscape
scale, and on the other hand studies for defined habitats (e.g.
infauna, epifauna) and assemblages.
4. The reasons for latitudinal variation in marine species richness are
contentious but most likely related to variation in time available to
species diversification and to variation in the area (the species:
area relationships) and productivity (the energy input hypothesis)
(Gaston & Blackburn 200 I). Both of the latter explanatory
hypotheses have not been adequately tested so far according to
Gray (200Ia).
Latitudinal gradients in size spectra
Another interesting aspect of the latitudinal gradient issue is the
distribution of the size spectra among marine organisms. Significant
progress has been made recently in elucidating the trend towards
gigantism in polar Crustacea, in particular among the highly speciose
and widely distributed Amphipoda.
The first systematic analysis of the size spectra among the world
amphipod genera represented in the Southern Ocean had shown that
the Antarctic contained the greatest percentage of giant and the lowest
percentage of dwarf species (De Broyer 1977). Using a larger data set
and a different approach, Chapelle & Peck (1999) and Chapelle (200 I)
confirmed the existence of a clear trend toward larger amp hipod species
in polar regions and especially in the Antarctic. The maximum adult
size of more than 2000 species of benthic sublittoral amphipod was
compiled and converted to size spectra for 15 marine and freshwater
ecosystems over the world. (Fig. 6). It can be seen that from low to
high latitudes, the skewedness to the right of the 15 size spectra
gradually increases. These size spectra also allowed evaluation of the
relative importance of Antarctic and Lake Baikal gigantism. The curves
clearly showed that an outstanding size was indeed attained in these
c"'. ~~,:>';> ""
~{~«~<~:J:'; f~.~ ;;();,Y;1ffs~;'~fB:)1:Wii~
'"
.
';;;JJ11k[7st~L;L<D~;'W,' ~",,;<':;,, ~i":;:\{/f;<'",,';:;
?
I
.nGammarldean
I
Amphlpod spp
?
?
BIODIVERSITY PATTERNS IN THE SOUTHERN OCEAN: LESSONS FROM CRUSTACEA 207
50 150 200 350 400
100
an:tic
.nAnomouransp
b 1
virginian
carolinian
taxen
cartbbaan
brazlllan
argentlnlan
magallanlc
antan:tic
250 50 100
o150 200 250 300
Fig. 5. Latitudinal gradients of species richness of anomouran decapods (from Boschi 1999) and gammaridean amphipods (from diverse sources) along the
Atlantic biogeographic provinces of America.
regions but only for a very limited number of species, while the adult
length of the vast majority was situated in the lower half of the size
range.
A crucial finding was that this trend towards larger size at higher
latitudes followed an oxygen gradient rather than temperature, with
the largest species to be found in areas with the higher oxygen
concentration. Chapelle & Peck (1999) and Peck & Chapelle (1999)
demonstrated that the maximum potential size in amp hipod crustaceans
was dictated by oxygen availability. With the increase of the absolute
oxygen concentration, the increase in size is slight in small animals,
more pronounced in the middle of the spectrum and maximal in the
largest animals. The privileged hypothesis for explaining this
relationship is based on two physiological factors (Chapelle 2001).
The first one is the essentially passive nature of respiration in amphipod
crustaceans. The second consists in the decrease of the surface/volume
ratio with the increasing size ofthe animals, which leads to the setting
of an upper threshold beyond which the respiratory surface become
insufficient for supplying in oxygen the volume of the metabolically
active tissues.
This size spectra analysis revealed another common trend: the
minimum size appeared quite similar among these 15 different
environments and was shown to be close to the modal size (Fig. 6). As
opposed to the physico-chemical "ceiling" represented by oxygen
availability for the maximum size, the minimum size threshold seems
to be fixed by the "bauplan" (Chapelle 2001) and the underlying factor
was suggested to be egg size, as supported by an array of reproductive
bionomic data among aquatic amphipods (Sainte-Marie 1991).
Antarctic crustacean biogeography
The biogeography of several Antarctic crustacean groups was recently
reviewed either broadly or in some details: it was the case for the
Decapoda (Gorny 1999), Mysidacea (Brandt et al. 1999), Isopoda
(Brandt 1991, Winkler 1994), Tanaidacea (Sieg 1992 i.a.), Cumacea
(Miihlenhardt-SiegeI1999) and Amphipoda (De Broyer & Jazdzewski
1993, 1996). The results mostly fit into the broad distribution scheme
of benthic biogeographic provinces established by Hedgpeth (1970)
and Dell (1972) and widely confirmed by subsequent authors (e.g.
Knox & Lowry 1977). However, few thorough quantitive analyses of
the crustacean distribution data were performed in most of these
crustacean studies.
For decapods, Gorny (1999) conducted a multivariate cluster
analysis of the Southern Ocean distribution data that, on one hand,
mostly confirmed the biogeographic limits proposed by Hedgpeth for
the subantarctic (or "anti boreal") subregions. On the other hand,
Gorny's results, in contrast to Zarenkov (1968) and Hedgpeth (1970)
schemes, considerably enlarged the Antarctic region and set the
northern distribution limit for the Antarctic decapod fauna at
approximately 55°30'S, including species that are distributed on the
southern tip of South America (Fig. 7).
Distribution data of benthic species have increased enormously
since Hedgpeth's synthesis. Moreover extensive biogeographic
databases are now being built for some species-rich groups and new
insights are progressively provided by molecular analyses. New
biogeographic syntheses for the Antarctic benthos might timely be
attempted with an emphasis to better understand the origin of different
taxa and the processes driving the different distribution patterns of
particular groups and communities.
Circumpolarity ill benthos distribution: to be revisited?
Examples are accumulating in Antarctic benthic crustaceans of species
with wide circumpolar distribution or with so called "cosmopolitan"
distribution that, after detailed taxonomic revision, appeared to be
composed of several species with restricted distribution (e.g. Conlan
1990, Dahl 1990). The most striking progress in this context was
probably the recent detection of potential cryptic species by molecular
methods. The isopod Ceratosero/is tri/obitoides (Eights, 1833), for
example, was known to have a wide Southern Ocean distribution and
to be a highly plastic species (Wagele 1986). Held (this volume) after
analysing the sequences from the mitochondrial16S ribosomal RNA
gene showed that the molecular data strongly suggest that Ceratosero/is
trilobitoides s.l. contains at least one, perhaps more, previously
overlooked species with poorly overlapping distribution. In addition,
Held (pers. com.) conducted a phylogenetic analysis of the circumpolar
giant isopod Glyptonotus antarcticus Eights, 1853 based on two
mitochondrial gene fragments from specimens from different locations
around the Antarctic. He was able to conclude that there was a
good
evidence that four different Glyptonotus species might exist where
only one circumpolar species was recognized so far. Several other
cryptic species among Antarctic benthos are currently detected by
molecular methods. These findings may shed some trouble on our
current views of species richness and distribution.
LIMITATIONS OF THE PRESENT BIODIVERSITY
KNOWLEDGE OF THE SOUTHERN OCEAN
After this brief overview of various aspects of species richness,
composition and distribution of Antarctic crustaceans, some limitations
of the present biodiversity research on the Antarctic benthos are
emphasised hereafter in particular in terms of data sets and taxonomic
knowledge.
.~.,,,, "::;;.j_~,~l/,:"j',;".,
208 i
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n = 136 Magellanic region
n = 160
:IJ 60 90
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n = 142 ~Caspian Sea
n =69
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:IJ 60 90
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n = 314 Barents Sea
n = 134
:IJ 60 90
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n = 347 South Georgia
n = 147
:IJ 60 90
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~South Africa
n = 185
.... I I . I I
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n = 275
,. ""',_. t. t
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n=249 ~East Antarctica
n = 275
u...t ..t .t., .,
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n =92 Lake Baikal
n = 226
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n=145 L~,
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n=2805
:IJ 60 o90
:IJ
90 60
Fig. 6. Comparison of the gammaridean amphipods size spectra in 15 marine and freshwater ecosystems of the world. Sites are ordered in relation to water
oxygen content from top left to bottom right. The maximum size of each species in mm is plotted on X axis.
Y
axis gives the number of species. n =total number
of species in each area (from Chapelle
200 I).
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BIODIVERSITY PATTERNS IN THE SOUTHERN OCEAN: LESSONS FROM CRUSTACEA 209
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Antarctic region (Zarenkov, 1968) ~Antarctic region (Gorny, 1999)
Fig 7. Biogeographic regions for the decapod (benthic and pelagic) fauna of the Southern Ocean (from Gorny 1999), (1-3): South American Antiboreal
Subregions; (4): South New Zealand Antiboreal Subregion; (5): Kerguelen Antiboreal Subregion; (6): Auckland/Campbell Islands Province; (7, 8): Antarctic
Region (according to Zarenkov 1968), (A-B): Antiboreal Regions of South America; (C): Antarctic Region (according to Gorny 1999),
Terminology
In the literature dealing with the regional fauna there is a minor but
recurrent problem of terminology of geographic entities. Southern
Ocean for instance is either used in its wide sense, which, according
to Deacon (1984), includes all waters south of the Subtropical Front
zone to the coasts of the continent In its restricted sense, it comprises
only the waters extending south of the Polar Front (e,g, Dell 1972,
Clarke 1996a), For Antarctic, most benthologists have adopted the
definition proposed by Dell (1972), which included the continent and
all peri-Antarctic islands located south of the Antarctic Polar Front.
However, planktonologists for instance may use different schemes:
e,g, Razouls et a!. (2000) in their recent synthesis ofthe biodiversity
and biogeography of copepods, explicitly used the term Antarctic for
the occurrence south of 45°S.
The patchy nature of biodiversity surveys
The patchy nature of coverage of biodiversity and ecological surveys
in the Southern Ocean must continue to be stressed despite Winston's
(1992) assessment suggesting that the Southern Ocean benthic fauna
is at least as well described as those for many other geographical
regions.
Concerning geographical coverage, many taxonomists and
biogeographers who analysed the Antarctic benthic diversity noticed
that large parts of the Southern Ocean (sJ) still need basic taxonomic
inventory. In the West Antarctic, the littoral and shallow sublittoral
zones have been relatively well studied in some particular places (such
as Signy Island or King George Island) but the diversity of
environments along the Scotia Arc and the Antarctic Peninsula suggests
that more complete sampling is required before gaining an accurate
idea of the fauna and its precise distribution patterns, The deeper
continental shelf in the West Antarctic is still largely under-sampled
and the eastern side of the Peninsula and the Western Weddell Sea
remain nearly unknown, The Bellingshausen Sea has been very partially
sampled by relatively few expeditions starting by the Belgica expedition
one hundred years ago, Obviously, the more important gaps in the
Antarctic region survey are the western continental shelf between the
Bellingshausen Sea and the Ross Sea and also large parts of the east
Antarctic shelf between 0° and 150°£ where only few spots have been
reasonably well sampled,
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" " 'V <r; rs rs t>I tii '3 ~ <0 <0 "\ "\ '0 '0 q; C5 "cP ",:>I:S q,1:S q,<,;:,1:S
""cP ",,<oj
Fig. 8. Benthos sampling effort in relation to depth in the eastern Weddell Sea (Polar stern EPOS, EASIZ I and II cruises).
On the other hand, the Subantarctic Magellan region for a long
time remained relatively understudied in comparison for instance with
the Antarctic Peninsula and some parts of the Scotia Arc. Recently,
several co-ordinated expeditions investigated the region and produced
a substantial amount of new taxa and distribution data (see Arntz &
Rios 1999).
Concerning bathymetric coverage most investigations have been
made so far at coastal or shelf depths as illustrated for instance by the
sampling effort during three main Potarstern campaigns devoted to
benthic research in the Weddell Sea (Fig. 8). The vast expanses of
deep sea all around the Antarctic have been very poorly sampled so
far and the fauna of most of the deep continental slope and the peri-
antarctic abyssal basins remains nearly totally unknown (e.g. Arnaud
1992, De Broyer & Jazdzewski 1993, Brandt 1999). In this context it
is interesting to note that some studies ofthe deep sea macrofauna in
the north western Atlantic by Grassle & Maciolek (1992) and studies
of isopods in south-east Australia by Poore et at. (1994) pointed to
unexpected high species diversity at slope depths. In the former case,
64% of peracarid crustaceans were undescribed species, while in the
latter the proportion amounts to 90% of unknown isopods species.
The South Orkney Trench was recently investigated by Russian workers
to a depth of 6420m and, not surprisingly, provided among others
new species of benthic isopods and new records ofbathypelagic and
benthopelagic amphipods previously unreported from the Southern
Ocean (Kussakin & Vasina 1997, Vinogradov & Vinogradov 1993).
To improve our knowledge of the Antarctic deep sea biodiversity it
would probably be of outstanding interest to undertake some complete
transects from relatively well known Antarctic shelf area along the
slope to the contiguous abyssal basins, to investigate in details i.a. the
gradients in diversity and faunal composition, the phylogenetic links
between shelf and abyssal fauna, the habitat heterogeneity, the structure
of the successive benthic assemblages, and the limits ofthe shelf species
eurybathy.
In terms of habitat coverage, the epifauna and endofauna of soft
sediments and mixed bottom have received more attention than hard
bottoms more difficult to sample efficiently. However recent systematic
use of imaging techniques has greatly increased our knowledge of
these habitats (see e.g. Gutt & Starmans 1998). It must also be stressed
that benthic communities even when intensively sampled by classical
gears such as trawls, grabs or box corers, may reveal a number of
additional species, sometimes abundant and ecologically significant
when less commonly used equipment such as baited traps, fine meshed
size dredges or epibenthic sledges are used. The Benthic Boundary
Layer for instance that proved to be a critical habitat for peracarid
crustaceans, has been only recently sampled for the first time in few
places in the Antarctic and the Subantarctic by using epibenthic sledges
(Brandt et at. 1999). Cryopetagic and symbiotic habitats also remain
to be more systematically sampled. Crustacea fauna associated with
sponges, ascidians, gorgonians or hydrozoans for instance represent a
non negligible part ofthe Weddell Sea fauna (De Broyer et at. 2001 b).
Due to the rarefaction of substrates, symbioses are also expected to be
more common in the deep sea.
Taxonomic expertise and tools
The taxonomic impediment
It is a well known problem that there is a general lack of support to
taxonomy, that many taxonomic tools are not efficient enough, that a
number of classifications are in strong need of revision, and that around
the world taxonomic expertise in many groups is vanishing. At the
same time, there has never been a greater demand for taxonomy to
supply the increasing needs of biodiversity knowledge for fundamental
and applied science, environmental management, conservation and
sustainable exploitation purposes.(see e.g. Tillier & De Wever 2000).
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BIODIVERSITY PATTERNS IN THE SOUTHERN OCEAN: LESSONS FROM CRUSTACEA
211
SYSTEMATIC AGENDA 2000
ro ramme
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Synopsis
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Expert identification system
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CD-ROM /Web
electronic monograph
~BIODIVERSITY ASSESSEMENT TOOLS
~HELP MONITORING BIODIVERSITY
CHANGE
SCAR BIODIVERSITY INFORMATION NETWORK? GBIF- initiative
Fig. 9. Functional scheme of the "Biodiversity Reference Centre" for Antarctic Amphipoda (Ant'Phipoda) at IRScNB, Brussels.
New taxonomic tools: the end of taxonomy for taxonomists?
Taxonomy and systematics are fields that, in recent decades, have gone
through both a conceptual revolution with the cladistics or phylogenetic
systematics approach and a methodological revolution resulting from
the injection of molecular methods and the application of information
technologies.
Biodiversity studies require three different kinds of taxonomic tools:
1. faunistic (and floristic) inventories, 2. taxonomic systems ofrefe-
renee, 3. identitication tools.
For most groups ofCrustacea,faunistic inventories for the Southern
Ocean have now been published, some of them quite recently. But to
be more fully exploitable, species lists often remain to be linked with
more detailed distribution data to allow producing maps and atlases.
The taxonomic systems of reference provide accurate nomenclature,
synonymy and classification information. Detailed lists of Southern
Ocean crustacean species with synonymy have been compiled only in
a few cases (e.g. for amphipods: Lowry & Bullock 1976, De Broyer
& Jazdzewski 1993). For the other groups this basic information in
general still remains widely scattered in the literature.
Accurate species identification is fundamental in biodiversity
studies and relies on efficient identification tools. There is still a strong
need to continue to produce Antarctic fauna identification guides where
lacking, especially for highly diverse and taxonomically difficult groups
(such as polychaetes, copepods, amphipods,...). Only part of the
Antarctic crustacean fauna is already covered: the benthic Ostracoda,
some groups of Isopoda, the Euphausiacea, most benthic and pelagic
Decapoda and the pelagic Copepoda. In some cases however, in
particular for pelagic groups, existing southern hemisphere or world
fauna guides can help identifying Southern Ocean material (e.g.
Boltovskoi 1999).
A revolution is taking place in the way taxonomic tools are designed
and biodiversity information is packaged and presented to various
groups of users. Systematists are now increasingly developing
interactive identification keys available on-line or on CD-ROMS.
These interactive keys largely rely on abundant illustrations (sometimes
difficult to offer in conventional guides) and allow a more flexible
and efficient use of diagnostic characters (multi-entries keys) than the
rigid dichotomous keys of traditional handbooks. The role ofinteractive
databases in modern taxonomy is growing rapidly. For the Crustacea
for instance the "crustacea. net" project is developing Web based
interactive keys for all crustacean families on a global basis and keys
to genera and species of selected groups or areas using the DELTA
system (Lowry 200 I, www.crustacea.net).
Biodiversity information systems
There isa growing demand to develop biodiversity information systems
that integrate or link taxonomic, distribution and environmental
information and on the other hand efficiently allow interactive
biodiversity information retrieval (e.g. Fish Base: Froese & Pauly
2001).
At world scale, the Global Biodiversity Information Facility was
recently launched by OECD to organise and promote the use of
biodiversity information all over the world. GBIF intends to develop
a network of existing databases, to produce search engines and software
related to biodiversity (www.gbif.org).
--'
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212 C. DE BROYER
Another important initiative that may have some significance for
the Antarctic marine biodiversity is the "Census of Marine Life", a
programme "to assess and explain the diversity, distribution and
abundance of marine life" (Oceanography 1999). Noting that "the few
existing databases do not usefully summarize known distribution and
abundance of marine life nor are they organized to encourage frequent
use and intercomparison of datasets" the promoters developed the
"Ocean Biogeographic Information System" which is an on-line,
world-wide atlas for accessing, modelling and mapping marine
biological data in a multidimensional geographic context (Grassle
2000).
Concerning Antarctic Crustacea, a "Biodiversity Reference Centre"
for Antarctic Amphipoda was recently established (De Broyer et al.
200 Ib). This reference centre comprises on one hand a comprehensive
database on taxonomy, distribution and bio-ecology of Southern Ocean
species and on the other hand extensive reference collections and
specialised documentation. It operates with the collaboration of a
network of 13contributing specialists, the "Antarctic Amphipodologist
Network", engaged in the revision of the Antarctic fauna, the
preparation of identification tools and the synthesis of its distribution
and bio-ecological traits (Fig. 9).
CONCLUDING REMARKS
It appears that in the study of marine biodiversity patterns in the
Antarctic three main objectives are challenging biologists today:
i. To continue to discover, describe and assess what lives there, by
undertaking new exploratory surveys and exploiting all opportunities
to complete the inventory and the assessment ofa significant and unique
component ofthe World marine biodiversity. A substantial part of the
Southern Ocean biodiversity remains unknown or poorly known in
particular in the deep sea. There is a widely recognized need to establish
reliable and comprehensive baseline information about marine
biodiversity over the world to provide a reference state against which
subsequent changes (due to possible effects of changes in global
climate, increasing UVB radiation or anthropogenic impacts...) may
be monitored and compared. For the Antarctic marine biodiversity
(vertebrates excepted), this baseline information is still largely
incomplete, widely scattered and not easily available.
2. To understand the processes driving the biodiversity patterns at
the different pertinent spatial and time scales. In this respect Antarctica
seems to be a key place for contributing to elucidate some world
biodiversity patterns. New molecular approaches in particular may
allow new insights into evolutionary processes which resulted in the
marine biodiversity we observe today.
3. Tomanage, organize and communicate biodiversity knowledge for
the needs of science and society. It appears of increasing importance
to develop a co-ordinated Antarctic contribution to relevant global
initiatives on biodiversity information, and try to efficiently compile,
disseminate, and integrate the fundamental biodiversity information
on the Antarctic marine biodiversity for scientific, monitoring,
management and conservation purposes.
ACKNOWLEDGMENTS
The authors are very thankful to Gauthier Chapelle (IRScNB, Brussels),
Christoph Held (Bochum, Germany), Magda Blazewicz-Paszkowycz
(Lodz, Poland), Zdenek Duris (Ostrava, Czech Republic), Matthias
Gorny (Punta Arenas, Chile), Michael Klages (Bremerhaven, Germany)
and Karel Wouters (lRScNB, Brussels), for providing unpublished
information or useful comments and to Thierry Kuyken, Henri Robert
and Franyoise Weyland (lRScNB, Brussels) for their help in the
preparation of the manuscript.
/", ,/'.:')0<;- ".j>~<>, t~:'f!;Y;j;;9f0\,tlc!f§.L*,i.~
.\ .,~ ','",<
The first author likes to thank the organizing committee of the VIIIth
SCAR Biology Symposium for the invitation to present this keynote
address. For allowing participation in several Antarctic campaigns,
the support of the Alfred- Wegener-Institut (Bremerhaven, Germany),
the Polish Antarctic Station H. Arctowski and the Brazilian Antarctic
Programme is gratefully acknowledged. This work was carried out
under contracts A4/36/B02 and EV /36/24A ofthe « Belgian Antarctic
Research Programme» sponsored by the Federal Office for Scientific,
Technical and Cultural Affairs.
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