Challenging the cold: Crabs reconquer the Antarctic

Abstract

Recent records of lithodid crabs in deeper waters off the Antarctic continental slope raised the question of the return of crabs to Antarctic waters, following their extinction in the lower Miocene 15 million years ago. Antarctic cooling may be responsible for the impoverishment of the marine high Antarctic decapod fauna, presently comprising only five benthic shrimp species. Effects of polar conditions on marine life, including lowered metabolic rates and short seasonal food availability, are discussed as main evolutionary driving forces shaping Antarctic diversity. In particular, planktotrophic larval stages should be vulnerable to the mismatch of prolonged development and short periods of food avail-ability, selecting against complex life cycles. We hypothesize that larval lecithotrophy and cold tolerance, as recently observed in Subantarctic lithodids, represent, together with other adaptations in the adults, key features among the life-history adaptations of lithodids, potentially enabling them to conquer polar ecosystems. The return of benthic top predators to high Antarctic waters under conditions of climate change would considerably alter the benthic communities.

Full text

619
Ecology,
86(3), 2005, pp. 619–625
q
2005 by the Ecological Society of America
CHALLENGING THE COLD: CRABS RECONQUER THE ANTARCTIC
S
VEN
T
HATJE
,
1,5
K
LAUS
A
NGER
,
2
J
AVIER
A. C
ALCAGNO
,
3
G
USTAVO
A. L
OVRICH
,
4
H
ANS
-O
TTO
P
O
¨RTNER
,
1
AND
W
OLF
E. A
RNTZ
1
1
Alfred Wegener Institute for Polar and Marine Research, Columbusstr. D-27568 Bremerhaven, Germany
2
Biologische Anstalt Helgoland, Foundation Alfred Wegener Institute, Helgoland, Germany
3
Universidad de Buenos Aires, Facultad de Ciencias Exactas y Naturales, Intendente Gu¨iraldes 2160, C1428EHA,
Buenos Aires, Argentina
4
Consejo Nacional de Investigaciones Cientı´ficas y Te´cnicas, Centro Austral de Investigaciones Cientı´ficas, CC 92,
V9410BFD Ushuaia, Tierra del Fuego, Argentina
Abstract.
Recent records of lithodid crabs in deeper waters off the Antarctic continental
slope raised the question of the return of crabs to Antarctic waters, following their extinction
in the lower Miocene
;
15 million years ago. Antarctic cooling may be responsible for the
impoverishment of the marine high Antarctic decapod fauna, presently comprising only
five benthic shrimp species. Effects of polar conditions on marine life, including lowered
metabolic rates and short seasonal food availability, are discussed as main evolutionary
driving forces shaping Antarctic diversity. In particular, planktotrophic larval stages should
be vulnerable to the mismatch of prolonged development and short periods of food avail-
ability, selecting against complex life cycles. We hypothesize that larval lecithotrophy and
cold tolerance, as recently observed in Subantarctic lithodids, represent, together with other
adaptations in the adults, key features among the life-history adaptations of lithodids,
potentially enabling them to conquer polar ecosystems. The return of benthic top predators
to high Antarctic waters under conditions of climate change would considerably alter the
benthic communities.
Key words: Antarctic; biodiversity; climate change; crabs; evolution; marine ecosystems; tem-
perature adaptation.
S
OUTHERN
O
CEAN
D
ECAPODS IN AN
E
VOLUTIONARY
C
ONTEXT
High latitude decapod crustaceans comprise one of
the most unsolved mysteries in marine biodiversity re-
search, with
;
120 benthic shrimp and crab species in
the Subantarctic, compared with an extremely impov-
erished high Antarctic fauna, consisting of only five
benthic shrimp representatives on the continental shelf
of the Weddell Sea (Arntz and Gorny 1991, Gorny
1999; for zoogeographic classification see, Hedgpeth
1969). At the Late Cretaceous–Early Cenozoic bound-
ary, the Austral Province showed a temperate climate,
which was favorable for decapods, as evidenced by a
rich fossil record (Feldmann and Zinsmeister 1984,
Forster et al. 1987, Feldmann et al. 1997). Faunal im-
poverishment ending with the probable extinction of
crabs
;
15 million years ago is discussed as a result of
various processes involved, the principal factor being
Antarctic cooling. This process started as early as
;
35
million years ago as a consequence of continental drift
(Clarke 1990, 1993, Crame 1999), and affected in par-
ticular decapod diversity.
Cold tolerance requires, in the first place, an ad-
justment of the functional capacity of oxygen supply
Manuscript received 6 April 2004; revised 20 July 2004; ac-
cepted 11 August 2004. Corresponding Editor: P. T. Raimondi.
5
E-mail: sthatje@awi-bremerhaven.de
mechanisms such as ventilation and circulation (for
discussion see Po¨rtner 2002, Clarke 2003). In brach-
yuran crabs, this adjustment is hampered by a special
sensitivity to [Mg
2
1
], combined with a poor ability to
regulate [Mg
2
1
] levels in the haemolymph [Mg
2
1
]
HL
below those in the water. Consequently, their scope for
aerobic activity is reduced so that they may be nar-
cotized by a combination of temperatures below
,
0
8
C
and high ([Mg
2
1
]
HL
) levels (Frederich et al. 2001). Such
physiological constraints in crab species affect all pro-
cesses demanding aerobic energy, including their
brooding behavior. This makes crabs under cold con-
ditions less competitive as compared to other crusta-
ceans, which are able to down-regulate [Mg
2
1
]
HL
, e.g.,
shrimps, isopods, and amphipods. Differential capa-
bilities of [Mg
2
1
]
HL
regulation in crab vs. shrimp spe-
cies may thus be responsible for the comparatively late
worldwide radiation of brachyurans, which required
warmer Cretaceous temperatures (Schram 1982). Given
that most other decapod taxa are strong [Mg
2
1
]
HL
reg-
ulators at low [Mg
2
1
]
HL
, it is likely that ancestral brach-
yurans also had high [Mg
2
1
]
HL
levels (Frederich et al.
2001). However, during the radiation of brachyuran
crabs in the Cretaceous, the water temperature was
.
0
8
C worldwide, with a minimum polar temperature
of
;
0
8
C (Barron 1992), which may explain the scarcity
of improved [Mg
2
1
]
HL
regulation capacities in crabs.
This theory, however, does not coincide with the
observation of poor magnesium regulation capabilities

620
SVEN THATJE ET AL.
Ecology, Vol. 86, No. 3
P
LATE
. 1. (Left)
Lithodes confundens
from the southwestern Atlantic Ocean. Lithodid crabs are considered benthic top
predators. Their return to the high Antarctic continental shelves would certainly reshape benthic communities, which have
evolved unaffected by crabs during the last
;
15 million years. (Right) An unknown stone crab (
Paralomis
sp.) from the
Spiess seamount near Bouvet Island (
;
54
8
S, 03
8
W) in the Southern Ocean. The specimen was trawled using an Aggasiz
trawl during the German FS ‘‘Polarstern’’ cruise ANT XXI/2 in January 2004 (scale bar
5
5 cm). Photo credit: Martin
Rauscher.
in lithodid crabs (Anomura), which occur with high
species diversity in subpolar regions (Zaklan 2002).
This taxon represents probably one of the youngest
decapod families. The Lithodidae or king crabs evolved
;
15–23 million years ago (Cunningham et al. 1992,
Feldmann 1998; see Plate 1) when the world climate,
especially in the Southern Hemisphere, underwent a
considerable cooling process eventually resulting in the
present conditions.
The complexity of factors involved in decapod ex-
tinction also included glaciation events of the Antarctic
continental shelf, which may have affected especially
brachyuran crab species with a limited bathymetric dis-
tribution range. Eurybathic species with a refuge in
deeper waters, such as most caridean shrimps of the
Southern Ocean, were able to recolonize the shelf, and
this may explain why Antarctic invertebrates, in gen-
eral, show a wider bathymetric distribution than in-
vertebrates from other seas (Brey et al. 1996).
The exact geological timing of decapod extinction
is still under discussion, since the rich fossil record
principally reflects well established decapod commu-
nities until
;
15 million years ago, but does not indicate
how long these faunistic elements lasted (Feldmann and
Zinsmeister 1984, Forster et al. 1987, Feldmann et al.
1997, Crame 1999). In addition, the fossil record is
biased toward Seymour Island, and we know next to
nothing about the deep, offshore palaeontological re-
cord of the Antarctic. There is, e.g., only one fossil
record of deep-water lithodid crabs known from the
middle Miocene (
;
15 Ma ago, Feldmann 1998). Post-
Eocene diversity patterns are difficult to evaluate, but
the relatively scant yet existing fossil decapod record
from younger periods (see Feldmann et al. 2003) in-
dicates that at least some species may have survived
in refuges on the Antarctic continental slope, which
may have remained uncovered during glacial maxima
(Feldmann and Crame 1998) or they showed a eury-
bathic distribution and survived due to better cold ad-
aptation. The complete extinction process, therefore,
was certainly gradual, and the ecological processes in-
volved, for instance competition with other crustaceans
such as the brooding isopods and amphipods, which
flourished in terms of diversity as a consequence of
decapod extinction, are still far from being understood.
The observation of an undamaged and well-preserved
asteroid and ophiuroid fossil record without indication
of regenerated arms from Seymour Island suggests
scarcity or a lack of benthos crushers already in the
Eocene (Blake and Zinsmeister 1988, Aronson and
Blake 1997, 2001).
Recently, large populations of extant king crabs have
been discovered in deep waters off the continental shelf
in the high Antarctic Bellingshausen Sea at tempera-
tures
.
1
8
C (Klages et al. 1995, Arana and Retamal
1999: Fig. 1), reopening the debate about the return of
anomuran crabs to Antarctic waters. Since polar con-
ditions should in particular select against the sensitive
early life-history stages (Thorson 1936), we suggest
that special adaptations should occur in larval physi-
ology and ecology to survive in polar environments
with cold and seasonally pulsed planktonic food avail-
ability. Recent evidence of larval cold tolerance (Anger
et al. 2003, 2004) indicates the capability of lithodid
larvae to live under such conditions. Furthermore, it
shows physiological limits, which explain the lack of
lithodids in high Antarctic waters, where the temper-
ature is permanently
,
0
8
C (Arntz et al. 1992), in ac-
cordance with the Mg
2
1
limitation hypothesis (Fred-
erich et al. 2001).
C
OLD
A
DAPTATION VS
.E
XTINCTION
Although early life-history data from lithodid spe-
cies occurring in Antarctic waters are missing so far
due mainly to logistic constraints, it appears obvious
that lithodid crabs from higher southern latitudes must

March 2005 621
CRABS RETURN TO ANTARCTIC WATERS
F
IG
. 1. Occurrence of lithodid crabs in the Southern Ocean, not including records from Crozet and Kerguelen Islands
and from waters off New Zealand (see Macpherson 2004). Species occurring across the circum-Antarctic deep sea are
highlighted with symbols. Data are from Purves et al. (2003), Thatje and Arntz (2004), and references therein.
have adapted their life history to physiological con-
straints in the cold. From recent observations in Sub-
antarctic species we may expect traits that minimize
the need for activity in both adults and larvae, e.g.,
prolonged brooding periods of up to about two years
(see Lovrich and Vinuesa 1999), extended hatching
rhythms of up to several months per brood, and le-
cithotrophic larval development (see Kattner et al.,
2003, Thatje et al. 2003
a
). Food-independent larval
development provides independence from the polar
mismatch of distinctly seasonal food availability and
prolonged larval development at low temperatures.
Furthermore, metabolism should be minimized during
the extended, and food-independent, larval develop-
ment (up to four months in species from the Magellan
region; Anger et al. 2003, 2004, Calcagno et al. 2003).
Since harsh environmental conditions prevailing in po-
lar seas should, in the first place, affect the particularly
sensitive early life-history stages (Thorson 1936), we
hypothesize that the larval stages of lithodids must
show key adaptations to these conditions. This becomes
particularly evident when we consider the rarity of en-
dotrophic and abbreviated larval developments in
brachyuran crabs (Thatje et al. 2003
b
). Larvae of the
false southern king crab,
Paralomis granulosa
(see
Plate 1), seem to have a better cold tolerance than those
of the true southern king crab,
Lithodes santolla
, which
allows for completing larval developments at
;
1
8
C

622
SVEN THATJE ET AL.
Ecology, Vol. 86, No. 3
F
IG
. 2. Extrapolation of temperature-depen-
dent shifts in zoea I development duration (log
scale) in species of Lithodidae and Paguridae.
Plot symbols show experimental temperatures,
roughly representing the natural temperature
tolerance window of the zoea I instar. The Lith-
odidae represent species from high latitudes of
both hemispheres, whereas the closely related
Paguridae,
Pagurus bernhardus
and
P. criniti-
cornis
, represent boreal and tropical species, re-
spectively. Data are from Paul and Paul (1999)
for
L. aequispinus
, Anger et al. (2003) for
Par-
alomis granulosa
, Anger et al. (2004) for
L.
santolla
, Dawirs (1979) for
P. bernhardus
, and
Blaszkowski and Moreira (1986) for
P. crini-
ticornis
.
(Anger et al. 2003). This coincides with biogeographic
patterns, and consequently, is an indication for species-
specific latitudinal temperature adaptation (Anger et al.
2003, 2004; for discussion see Clarke 2003).
The outstanding capability of lithodid crabs with an
endotrophic mode of larval development to cope with
temperatures that are typical of deep-sea and high lat-
itudinal environments is conspicuous when we com-
pare it to the phylogenetically closely related hermit
crabs from lower and tropical latitudes. While lithodids
show a physiological threshold for successful larval
development only at
;
1
8
C (Fig. 2), hermit crabs, which
are not represented in the polar realm, show much high-
er temperature limits. An extrapolation of develop-
mental duration through the zoea I at high latitudes
would exceed theoretical periods of several years (Fig.
2). However, lithodids from the Antarctic Bellingshau-
sen Sea may not show much better larval temperature
adaptations than their congeners from the Subantarctic
(cf. Fig. 2), maybe explaining why lithodids are ap-
parently absent from the Weddell Sea, where temper-
atures permanently drop
,
0
8
C (compare Arntz et al.
1992 with Klages et al. 1995). In conclusion, it needs
to be emphasized that lithodid diversity and perfor-
mance in the cold is high, but does not reach below
the Mg
2
1
limits of 0
8
C. Hypometabolism and optimi-
zation of all life cycle stages to low temperature may
be the physiological key to the success of this group
in polar seas.
T
HE
D
EEP
-
SEA
C
ONNECTION
Although larval lecithotrophy seems to be a common
pattern in lithodid species from high latitudes of both
hemispheres (e.g., Anger 1996, Shirley and Zhou 1997,
Calcagno et al. 2003, Kattner et al. 2003, Lovrich et
al. 2003), the apparent lack of at least partially plank-
totrophic larval developments in lithodids from the
Southern Ocean and adjacent waters may be due to
their presumable origin from deep-sea ancestors, since
environmental conditions of polar and deep-sea envi-
ronments require very similar life-history adaptations
to cold and food limitation (Thiel et al. 1996). It has
been suggested that lithodid crabs evolved in shallow
waters of the northern Pacific and have radiated and
colonized the Southern Ocean through the Pacific deep
sea (Makarov 1962, Zaklan 2002). Since the cold-tol-
erant lithodid species are not able to cope with tropical
warm-water conditions, faunal exchange through the
deep sea is assumed as the only possibility connecting
the northern and southern hemisphere lithodid popu-
lations. In contrast, it has been suggested that lithodids
at high latitudes in the northern hemisphere radiated
widely through shallower and coastal waters, which
may explain the development of planktotrophic devel-
opments in some representatives (Makarov 1962, Paul
et al. 1989, Zaklan 2002).
We hypothesize that the recolonization of the Ant-
arctic by lithodid crabs should occur via the deep sea,
facilitated by similar evolutionary selection pressures
in both cold regions and deep-sea environments, name-
ly scarcity of food in combination with low tempera-
tures. A colonization of the Antarctic may also be pos-
sible via the shallows of the Subantarctic islands (Dell
1972), as suggested by patterns of distribution of lith-
odid species, along the islands of the Scotia Arc (Fig.
1). However, active migration via the deep sea appears
to be more likely, since lecithotrophic larvae are de-
mersal and show a low potential of dispersal (Thatje
et al. 2003
a
). The demersal behavior of rather immobile
lecithotrophic larvae makes it likely that the larvae of
deep-sea lithodids develop in the bathyal and are not
exported into the euphotic zone of shallow waters, im-
plying that they must be able to cope with the high-
pressure regime of the deep sea. Lithodid species have
been found in a range from the shallow sublittoral to
the deep sea, and many species must be considered
bathyal (Zaklan 2002: Fig. 3). Despite only a few stud-
ies on Antarctic deep-sea environments available, even

March 2005 623
CRABS RETURN TO ANTARCTIC WATERS
F
IG
. 3. Bathymetric distribution of lithodid crabs in the
Southern Ocean (antarctic and subantarctic). Continuous dis-
tribution between end point dots is assumed. Abbreviations
of genera are
Neolithodes
(
N
.),
Lithodes
(
L
.), and
Paralomis
(
P
.). Data are from Purves et al. (2003), Thatje and Arntz
(2004) and references therein, and Macpherson (2004) and
references therein.
our scarce knowledge of lithodid bathymetric distri-
bution patterns in the Southern Ocean already indicates
that some lithodid species found in both the Antarctic
and Subantarctic marine realm, should have the ca-
pability to cross the circum-Antarctic deep sea (com-
pare Figs. 1, 3), with, on average,
.
3000 m depth.
Although, from an evolutionary point of view, lith-
odids invaded the deeper waters off the Antarctic re-
cently (Cunningham et al. 1992), it remains uncertain
whether this process is continuing. Most lithodids col-
lected with bottom trawls or baited traps have been
recorded only during the last years (see Thatje and
Arntz 2004), although such gear (in particular bottom
trawls and video imaging) has been used frequently in
the high Antarctic Weddell and Lazarev Seas through-
out the last two decades (Arntz et al. 1994, Thatje and
Arntz 2004). The question of recolonization remains
thus as an exciting challenge and subject to speculation.
Nevertheless, it is certain that insufficient cold adap-
tation in lithodid larvae (Fig. 2) to temperatures typical
of the high Antarctic Weddell and Ross Seas (
;
0
8
Cto
2
1.9
8
C, Arntz et al. 1992) may explain why these crabs
have not yet invaded the high Antarctic continental
shelves (Gorny 1999). The formation of cold bottom
water in the high Antarctic Weddell and Ross Seas
(compared to higher bottom water temperatures, e.g.,
in the Bellingshausen Sea; Klages et al. 1995) may also
explain the lack of lithodid records in the southern
Weddell Sea and Lazarev Sea. Lithodids occur fre-
quently along the bordering Scotia Arc islands (Fig. 1)
and a species of
Paralomis
was found near Bouvet
Island (S. Thatje,
unpublished record
; see Plate 1).
Considering that a continued climate shift will lead to
more favorable temperature conditions for crabs in the
high Antarctic marine environment, the return of shell-
crushing benthic top predators, which are presently ex-
cluded from the ecosystem (Arntz et al. 1994, Dayton
et al. 1994), will considerably reshape and alter high
latitudinal benthos communities. We suggest that this
process has already started. In the present high Ant-
arctic system, amphipods and isopods occupy part of
the ecological niche of crabs (Brandt 1991), and as-
teroids are considered further benthic top predators
(Arntz et al. 1994, Dayton et al. 1994, Aronson and
Blake 2001). Echinoderms, in particular asteroids, as
well as peracarid crustaceans constitute an important
part of prey for lithodids (Jewett and Feder 1982, Com-
oglio and Amin 1999), implying a direct impact of
lithodids on the Antarctic food web, which may reshape
the benthic ecosystem.
Despite an invasion of adult lithodid crabs most like-
ly occurring across the deep sea, scant records of brach-
yuran and anomuran crab larvae near the Antarctic Pen-
insula, which have been suggested to cross the Polar
Front by means of eddies (Thatje and Fuentes 2003,
Glorioso et al.
in press
), suggest that there may be a
colonization pressure also from decapod taxa which,
under present climate conditions, remain excluded and
are not able to settle and establish populations in Ant-
arctic waters. Crossing the Antarctic Circumpolar Cur-
rent, which has always been considered as the main
oceanographic barrier isolating the Antarctic biota
from surrounding seas (Clarke 1990, Crame 1999), may
thus be another future colonization mechanism in the
Antarctic marine realm. Another phenomenon, the re-
cent record of two adult specimens of the spider crab
Hyas araneus
, native to boreal and subarctic waters,
off the Antarctic Peninsula (Tavares and De Melo
2004), has been suggested to be the first invasive ben-
thic invertebrate in Antarctic waters. According to the
authors this species may have been introduced by
means of ballast water or by biofouling organisms on
ship hulls, raising the question, however, how these
crabs (larvae or adults) managed to survive the high
temperatures in the tropics (for temperature thresholds
see Anger 1983). In summary, these examples suggest
that we have to remain flexible in our perspectives on
evolutionary time scales in the development of the Ant-
arctic marine fauna in response to climate shift.
Combined ecological and physiological studies on
marine invertebrates will help substantially to improve
our understanding of past, present, and future changes
in the marine biota under conditions of climate change.
In the case of the Decapoda, future research should
also focus on phylogenetic implications applying mo-
lecular techniques to elucidate the presumable but con-
troversially discussed relationships between the Lith-
odidae and the Paguridae (for discussion, see Cun-
ningham et al. 1992, McLaughlin and Lemaitre 2000),
and scrutinize whether Mg
2
1
regulation capacities are
phylogenetically significant. The relationships among
Mg
2
1
concentration, oxygen utilization, and behavioral
changes in both adults and larvae may help in under-
standing radiation processes on geological time scales,

624
SVEN THATJE ET AL.
Ecology, Vol. 86, No. 3
as in the Brachyura, which flourished during the rel-
atively warm Cretaceous period.
A
CKNOWLEDGMENTS
This work benefitted from discussions with Andrew Clarke
(British Antarctic Survey), Eduardo Olivero (CADIC, Us-
huaia), Alistair Crame (British Antarctic Survey), Katrin
Linse (British Antarctic Survey), and Christoph Held (Ruhr-
University Bochum). We are indebted to the International
Bureau of the German Ministry of Research (BMBF, project
number Arg 99/002) and the Argentine Secretarı´a Nacional
para la Ciencia, Tecnologı´a e Inovacio´n Productiva (SECyT)
for continuous financial support of this bilateral cooperation
during the last years. We would like to thanktwo anonymous
reviewers for their valuable comments on an earlier draft of
this work.
L
ITERATURE
C
ITED
Anger, K. 1983. Temperature and the larval development of
Hyas araneus
L. (Decapoda: Majidae); extrapolation of lab-
oratory data to field conditions. Journal of Experimental
Marine Biology and Ecology 69:203–215.
Anger, K. 1996. Physiological and biochemical changes dur-
ing lecithotrophic larval development and early juvenile
growth in the northern stone crab,
Lithodes maja
(Deca-
poda: Anomura). Marine Biology 126:283–296.
Anger, K., G. A. Lovrich, S.Thatje, and J. A. Calcagno. 2004.
Larval and early juvenile development of
Lithodes santolla
(Molina, 1782) (Decapoda: Anomura: Lithodidae) reared
at different temperatures in the laboratory. Journal of Ex-
perimental Marine Biology and Ecology 306:207–230.
Anger, K., S. Thatje, G. A.Lovrich, and J. A. Calcagno. 2003.
Larval and early juvenile development of
Paralomis gran-
ulosa
reared at different temperatures: tolerance of cold
and food limitation in a lithodid crab from high latitudes.
Marine Ecology Progress Series 253:243–251.
Arana, P. M., and M. A. Retamal. 1999. Nueva distribucio´n
de
Paralomis birsteini
Macpherson 1988 en aguas anta´r-
ticas (Anomura, Lithodidae, Lithodinae). Investigaciones
Marinas (Valparaı´so) 27:101–110.
Arntz, W. E., T. Brey, and V. A. Gallardo. 1994. Antarctic
zoobenthos. Oceanography and Marine Biology Annual
Review 32:241–304.
Arntz, W. E., T. Brey, D. Gerdes, M. Gorny, J. Gutt, S. Hain,
and M. Klages. 1992. Patterns of life history and popu-
lation dynamics of benthic invertebrates under the high
Antarctic conditions of the Weddell Sea. Pages221–230
in
G. Colombo, I. Ferrari, V. U. Ceccherelli, and R. Rossi,
editors. Marine eutrophication and population dynamics.
Proceedings of the 25th European Marine Biology Sym-
posium. Olsen and Olsen, Fredensborg, Denmark.
Arntz, W. E., and M. Gorny. 1991. Shrimp (Decapoda, Na-
tantia) occurrence and distribution in the eastern Weddell
Sea, Antarctica. Polar Biology 11:169–177.
Aronson, R. B., and D. B. Blake. 1997. Global climate change
and the paleoecology of echinoderm populations at Sey-
mour Island, Antarctica. Antarctic Journal of the United
States 32:20–22.
Aronson, R. B., and D. B. Blake. 2001. Global climate change
and the origin of modern benthic communities in Antarc-
tica. American Zoologist 41:27–39.
Barron, E. J. 1992. Paleoclimatology. Pages 485–505
in
G.
Brown, C. Hawkesworth, and C. Wolson, editors. Under-
standing the Earth. Cambridge University Press, Cam-
bridge, UK.
Blake, D. B., and W. J. Zinsmeister. 1988. Eocene asteroids
(Echinodermata) from Seymour Island, Antarctic Penin-
sula.
In
R. M. Feldmann and M. O. Woodburne, editors.
Geology and paleontology of Seymour Island, Antarctic
Peninsula. Geological Society of America, Memoirs 169:
489–498.
Blaszkowski, C., and G. S. Moreira. 1986. Combined effects
of temperature and salinity on the survival and duration of
larval stages of
Pagurus criniticornis
(Dana) (Crustacea,
Paguridae). Journal of Experimental Marine Biology and
Ecology 103:77–86.
Brandt, A. 1991. Origin of Antarctic Isopoda (Crustacea,
Malacostraca). Marine Biology 113:415–423.
Brey, T., C. Dahm, M. Gorny, M. Klages, M. Stiller, and W.
E. Arntz. 1996. Do Antarctic benthic invertebrates show
an extended level of eurybathy? Antarctic Science 8:3–6.
Calcagno, J. A., S. Thatje, K. Anger, G. A. Lovrich, and A.
Kaffenberger. 2003. Changes in biomass and chemical
composition during lecithotrophic larval development of
the Southern stone crab,
Paralomis granulosa
(Jacquinot).
Marine Ecology Progress Series 257:189–196.
Clarke, A. 1990. Temperature and evolution: southernOcean
cooling and the Antarctic marine fauna. Pages 9–22
in
K.
R. Kerry and G. Hempel, editors. Antarctic ecosystems.
Ecological change and conservation. Springer-Verlag Ber-
lin, Heidelberg, Germany.
Clarke, A. 1993. Temperature and extinction in the sea: a
physiologist’s view. Paleobiology 19:499–518.
Clarke, A. 2003. Costs and consequences of evolutionary
temperature adaptation. Trends in Ecology and Evolution
18:573–581.
Comoglio, L. I., and O. A. Amin. 1999. Feeding habits of
the false southern king crab
Paralomis granulosa
(Lith-
odidae) in the Beagle Channel, Tierra del Fuego, Argentina.
Scientia Marina 63(Supplement 1):361–366.
Crame, J. A. 1999. An evolutionary perspective on marine
faunal connections between southernmost South America
and Antarctica. Scientia Marina 63(Supplement 1):1–14.
Cunningham, C. W., N. W. Blackstone, and L. W. Buss. 1992.
Evolution of king crabs from hermit crab ancestors. Nature
355:539–542.
Dawirs, R. R. 1979. Effects of temperature and salinity on
larval development of
Pagurus bernhardus
(Decapoda, Pa-
guridae). Marine Ecology Progress Series 1:323–329.
Dayton, P. K., B. J. Mordida, and F. Bacon. 1994. Polar
marine communities. American Zoologist 34:90–99.
Dell, R. K. 1972. Antarctic benthos. Advances in Marine
Science 10:1–216.
Feldmann, R. M. 1998.
Paralomis debodeorum
, a new species
of decapod crustacean from the Miocene of New Zealand:
first notice of the Lithodidae in the fossil record. New Zea-
land Journal of Geology and Geophysics 41:35–38.
Feldmann, R. M., M. Aguirre-Urreta, L. Chirino-Halvez,and
S. Casadı´o. 1997. Palaeobiogeography of Cretaceous and
Tertiary decapod crustaceans from southern South Amer-
ica: the link with Antarctica. Pages 1007–1016
in
C. A.
Ricci, editor. The Antarctic region: geological evolution
and processess. Terra Antartica, Siena, Italy.
Feldmann, R. M., and J. A. Crame. 1998. The significance
of a new nephropid lobster from the Miocene of Antarctica.
Palaeontology 41:807–814.
Feldmann, R. M., C. W. Schweitzer, and A. Marenssi. 2003.
Decapod crustaceans from the Eocene La Meseta Forma-
tion, Seymour Island, Antarctica: a model for preservation
of decapods. Journal of the Geological Society London 160:
151–160.
Feldmann, R. M., and W. J. Zinsmeister. 1984. New fossil
crabs (Decapoda: Brachyura) from the La Meseta Forma-
tion (Eocene) of Antarctica: paleogeographic and biogeo-
graphic implications. Journal of Paleontology 58:1046–
1061.
Forster, R., A. Gazdzicki, and R. Wrona. 1987. Homolod-
romiid crabs from the Cape Melville formation (Lower
Miocene) of King George Island, West Antarctica.Palaeon-

March 2005 625
CRABS RETURN TO ANTARCTIC WATERS
tological Research of the Polish Antarctic Expedition 49:
147–161.
Frederich, M., F. J. Sartoris, and H. O. Po¨rtner. 2001. Dis-
tribution patterns of decapod crustaceans in polar areas: a
result of magnesium regulation? Polar Biology 24:719–
723.
Glorioso, P. D., A. R. Piola, and R. R. Leben.
In press
. Me-
soscale eddies in the Subantarctic Front–Southwest Atlan-
tic. Scientia Marina (Supplement).
Gorny, M. 1999. On the biogeography and ecology of the
Southern Ocean decapod fauna. Scientia Marina 63(Sup-
plement 1):367–382.
Hedgpeth, J. W. 1969. Introduction to Antarctic zoogeog-
raphy. American Geographical Society Antarctic Map Folio
Series 11:1–41.
Jewett, S. C., and H. M. Feder. 1982. Food and feeding habits
of the king crab
Paralithodes camtschatica
near Kodiak
Island, Alaska. Marine Biology 66:243–250.
Kattner, G., M. Graeve, J. A. Calcagno, G. A. Lovrich, S.
Thatje, and K. Anger. 2003. Lipid, fatty acid and protein
utilization during lecithotrophic larval development of
Lithodes santolla
(Molina) and
Paralomis granulosa
(Jac-
quinot). Journal of Experimental Marine Biology and Ecol-
ogy 292:61–74.
Klages, M., J. Gutt, A. Starmans, and T. Bruns. 1995. Stone
crabs close to the Antarctic continent:
Lithodes murrayi
Henderson, 1888 (Crustacea; Decapoda; Anomura) offPe-
ter I Island (68
8
51
9
S, 90
8
51
9
W). Polar Biology 15:73–75.
Lovrich, G. A., S. Thatje, J. A. Calcagno, K. Anger, and A.
Kaffenberger. 2003. Changes in biomass and chemical
composition during lecithotrophic larval development of
the Southern king crab,
Lithodes santolla
(Molina). Journal
of Experimental Marine Biology and Ecology 288:65–79.
Lovrich, G. A., and J. H. Vinuesa. 1999. Reproductive po-
tential of the lithodids
Lithodes santolla
and
Paralomis
granulosa
(Anomura, Decapoda) in the Beagle Channel,
Argentina. Scientia Marina 63(Supplement 1):355–360.
Macpherson, E. 2004. A new species and new records of
lithodid crabs (Crustacea: Decapoda: Lithodidae) from the
Crozet and Kerguelen Islands area (Subantarctica). Polar
Biology 27:418–422.
Makarov, V. V. 1962. Fauna of U.S.S.R. (Crustacea). Pages
1–283
in
A. A. Shtakelberg, editor. Israel Programme for
Scientific Translation. Jerusalem, Israel.
McLaughlin, P. A., and R. Lemaitre. 2000. Aspects of evo-
lution in the anomuran superfamily Paguroidea: one larval
perspective. Invertebrate Reproduction and Development
38:159–169.
Paul, A. J., and J. M. Paul. 1999. Development of larvae of
the golden king crab
Lithodes aequispinus
(Anomura: Lith-
odidae) reared at different temperatures. Journal of Crus-
tacean Biology 19:42–45.
Paul, A. J., J. M. Paul, and K. O. Coyle. 1989. Energy sources
for first-feeding zoeae of king crab
Paralithodes camtscha-
tica
(Tilesius) (Decapoda, Lithodidae). Journal of Experi-
mental Marine Biology and Ecology 130:55–69.
Po¨rtner, H. O. 2002. Climate variations and the physiological
basis of temperature dependent biogeography: systemic to
molecular hierarchy of thermal tolerance in animals. Com-
parative Biochemistry and Physiology 132A:739–761.
Purves, M. G., D. J. Agnew, G. Moreno, C. Yau, and G.
Pilling. 2003. Distribution, demography, and discard mor-
tality of crabs caught as bycatch in an experimental pot
fishery for toothfish (
Dissostichus eleginoides
) in the South
Atlantic. Fishery Bulletin 101:874–888.
Schram, F. R. 1982. The fossil record and evolution of Crus-
tacea. Pages 93–147
in
L. G. Abele, editor. The biology of
Crustacea. Volume 1. Academic Press, New York, New
York, USA.
Shirley, T. C., and S. Zhou. 1997. Lecithotrophic develop-
ment of the golden king crab
Lithodes aequispinus
(Ano-
mura: Lithodidae). Journal of Crustacean Biology 17:207–
216.
Tavares, M., and G. A. S. De Melo. 2004. Discovery of the
first known benthic invasive species in the Southern Ocean:
the North Atlantic spider crab
Hyas araneus
found in the
Antarctic Peninsula. Antarctic Science 16:129–131.
Thatje, S., and W. E. Arntz. 2004. Antarctic reptant decapods:
more than a myth? Polar Biology 27:195–201.
Thatje, S., J. A. Calcagno, G. A. Lovrich, F. J. Sartoris, and
K. Anger. 2003
a
. Extended hatching periods in the Sub-
antarctic lithodid crabs
Lithodes santolla
and
Paralomis
granulosa
(Crustacea: Decapoda). Helgoland Marine Re-
search 57:110–113.
Thatje, S., and V. Fuentes. 2003. First record of anomuran
and brachyuran larvae (Crustacea: Decapoda) from Ant-
arctic waters. Polar Biology 26:279–282.
Thatje, S., S. Schnack-Schiel, and W. E. Arntz. 2003
b
. De-
velopmental trade-offs in Subantarctic meroplankton com-
munities and the enigma of low decapod diversity in high
southern latitudes. Marine Ecology Progress Series 260:
195–207.
Thiel, H., H. O. Po¨rtner, and W. E. Arntz. 1996. Marine life
at low temperatures—a comparison of polar and deep-sea
characteristics.
In
F. Uiblein, J. Ott, and M. Stachowitsch,
editors. Deep-sea and extreme shallow-water habitats: af-
finities and adaptations. Biosystematics and Ecology Series
11:183–219.
Thorson, G. 1936. The larval development, growth and me-
tabolism of Arctic marine bottom invertebrates compared
with those of other seas. Meddelingen om Gro¨nland 100:
1–155.
Zaklan, S. D. 2002. Review of the family Lithodidae (Crus-
tacea: Anomura: Paguroidea): distribution, biology, and
fisheries. Pages 751–845
in
A. J. Paul, E. G. Dawe, R.
Elner, G. S. Jamieson, G. H. Kruse, R. S. Otto, B. Sainte-
Marie, T. C. Shirley, and D. Woodby, editors.Crabs in cold
water regions: biology, management, and economics. Uni-
versity of Alaska Sea Grant College Program AK-SG-02-
01, Fairbanks, Alaska, USA.