Content uploaded by Gustavo A Lovrich
Author content
All content in this area was uploaded by Gustavo A Lovrich on Sep 18, 2021
Content may be subject to copyright.
Larval and early juvenile development of Lithodes
santolla (Molina, 1782) (Decapoda: Anomura:
Lithodidae) reared at different temperatures in
the laboratory
Klaus Anger
a,
*, Gustavo A. Lovrich
b
,
Sven Thatje
c
, Javier A. Calcagno
d
a
Biologische Anstalt Helgoland, Stiftung Alfred-Wegener-Institut fu
¨r Polar-und Meeresforschung,
27498 Helgoland, Germany
b
Centro Austral de Investigaciones Cientı
´ficas (CADIC), 9410 Ushuaia, Argentina
c
Alfred-Wegener-Institut fu
¨r Polar-und Meeresforschung, 27568 Bremerhaven, Germany
d
Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
Received 25 November 2003; accepted 15 January 2004
Abstract
The southern king crab, Lithodes santolla Molina, is distributed in cold-temperate and
subantarctic waters ranging from the southeastern Pacific island of Chiloe
´(Chile) and the deep
Atlantic waters off Uruguay, south to the Beagle Channel (Tierra del Fuego, Argentina/Chile).
Recent investigations have shown that its complete larval development from hatching to
metamorphosis, comprising three zoeal stages and a megalopa, is fully lecithotrophic, i.e.
independent of food. In the present study, larvae were individually reared in the laboratory at seven
constant temperatures ranging from 1 to 18 jC, and rates of survival and development through
successive larval and early juvenile stages were monitored throughout a period of 1 year. The highest
temperature (18 jC) caused complete mortality within 1 week; only a single individual moulted
under this condition, 2 days after hatching, to the second zoeal stage, while all other larvae died later
in the zoea I stage. At the coldest condition (1 jC), 71% of the larvae reached the zoea III stage, but
none of these moulted successfully to a megalopa. A temperature of 3 jC allowed for some survival
to the megalopa stage (17 – 33% in larvae obtained from two different females), but only a single
individual passed successfully, 129 days after hatching, through metamorphosis to the first juvenile
crab instar. At all other experimental conditions (6, 9, 12 and 15 jC), survival through
metamorphosis varied among temperatures and two hatches from 29% to 90% without showing a
0022-0981/$ - see front matter D2004 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2004.01.010
* Corresponding author. Tel.: +49-4725-819348.
E-mail address: kanger@awi-bremerhaven.de (K. Anger).
www.elsevier.com/locate/jembe
Journal of Experimental Marine Biology and Ecology
306 (2004) 217 – 230
consistent trend. The time of nonfeeding development from hatching to metamorphosis lasted, on
average, from 19 days at 15 jC to 65 days at 6 jC. The relationship between the time of development
through individual larval or juvenile stages (D) and temperature (T) was described as a power
function (D=aT
b
, or log[D]=log[a]blog[T]). The same model was also used to describe the
temperature dependence of cumulative periods of development from hatching to later larval or
juvenile stages. One year after hatching, the 7th (6 jC) to 9th (15 jC) crab instar was reached. Under
natural temperature conditions in the region of origin of our material (Beagle Channel, Argentina), L.
santolla should reach metamorphosis in October – December, i.e. ca. 2 months after hatching (taking
place in winter and early spring). Within 1 year from hatching, the crabs should grow approximately
to juvenile instars VII– VIII. Our results indicate that the early life-history stages of L. santolla
tolerate moderate cold stress as well as planktonic food-limitation in winter, implying that this
species is well adapted to subantarctic environments with low temperatures and a short seasonal
plankton production.
D2004 Elsevier B.V. All rights reserved.
Keywords: Lithodidae; Larval development; Temperature; Reproductive strategies
1. Introduction
While the diversity of decapod crustaceans, in general, tends to decline in cold-
temperate and subpolar waters as compared to warm-temperate and tropical regions, the
number of lithodid crab species remains stable or increases with increasing latitude (e.g.
Arntz et al., 1994, 1997; Klages et al., 1995; Gorny, 1999; Zaklan, 2002). Recent
experimental studies suggested that this deviating distributional pattern of the Lithodidae
among the reptant decapods is due to special adaptations of their early life-history stages
to conditions of cold and food-limitation in high latitudes, namely tolerance of low
temperatures and lecithotrophic (i.e. food-independent) larval development (Anger et al.,
2003; Calcagno et al., 2003, 2004; Kattner et al., 2003; Lovrich et al., 2003; Thatje et
al., 2003).
Since lithodids have generally a large body size and a high market value as ‘‘king
crabs’’ or ‘‘stone crabs’’, several species are commercially fished, representing econom-
ically valuable fishery resources in subpolar regions (Dawson, 1989; Lovrich, 1997;
Sundet and Hjelset, 2002). The southern king crab, Lithodes santolla Molina, is one of
those species, although its commercially exploited populations have dramatically declined
in recent years, due to heavy overfishing in preceding times (Lovrich and Vinuesa, 1999).
L. santolla is distributed in a large area along the southeastern Pacific and southwestern
Atlantic coasts, stretching from the subantarctic waters of the Beagle Channel (Tierra del
Fuego, southernmost parts of Argentina and Chile; 55jS) to the cold-temperate region
around the island of Chiloe
´(southern-central Chile; 42jS; see Retamal, 1981; Boschi et
al., 1992; Gorny, 1999) and the deeper parts (ca. 700 m depth) of the continental slope off
Uruguay (Vinuesa, 1991). Its larval development comprises three zoeal stages and a
megalopa which were morphologically described by Campodonico (1971) and McLaugh-
lin et al. (2001). Recent biochemical and elemental analyses of fed and unfed larvae
showed that all four larval stages are completely nonfeeding, which was interpreted as an
adaptation to early development under conditions of low water temperature and low or
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230218
short planktonic productivity during the austral winter (Calcagno et al., 2003, 2004;
Kattner et al., 2003; Lovrich et al., 2003).
In the present study, we reared larval and early juvenile southern king crabs at various
constant temperatures in the laboratory (1) to identify the tolerated or preferred thermal
range for successful postembryonic development and growth, and (2) to quantify the effect
of variation in temperature on the rate of moulting and development through the early life-
history stages.
2. Materials and methods
The capture, maintenance, and transport of L. santolla as well as the rearing of their larvae
were described in detail by Lovrich et al. (2003). Briefly, ovigerous females were collected
in April 2001 in the Beagle Channel (Tierra del Fuego, southern Argentina; 54j53.8VS,
68j17.0VW) using commercial fishing boats (Lovrich, 1997), subsequently kept in
submerged cages in the Beagle Channel, and eventually transported with the German
research icebreaker ‘‘Polarstern’’ to the marine biological laboratory Helgoland, Germany
(Biologische Anstalt Helgoland, BAH). Subsequently, the crabs were maintained in flow-
through seawater aquaria at constant 6 jC, ca. 32xsalinity, and a 12:12-h light/dark cycle.
Freshly hatched larvae were collected in filters receiving the overflow from the aquaria.
Since most larvae hatched at night, sampling was done every morning. Filters were
cleaned every evening to ensure that larval age did not vary more than by 12 h. Actively
swimming larvae obtained from one female (A) were randomly selected and subsequently
reared in individual 100-ml bowls kept under the same conditions of salinity and light. As
rearing temperatures, we tested 1, 3, 6, 9, 12, 15, and 18 jC. Since L. santolla releases
only low numbers of larvae per night (normally <100, see Thatje et al., 2003), we were
forced to start ‘‘parallel’’ experiments (i.e. testing different rearing temperatures with
larvae originating from the same female) using sibling larvae that hatched on different
days. An additional (less complete) series of experiments was conducted with larvae from
a second female (hatch B; testing only 3, 6, 9, and 12 jC). The initial number of larvae per
treatment and hatch was n=48.
The larvae were reared without addition of food, since previous experiments
(McLaughlin et al., 2001; Lovrich et al., 2003; Kattner et al., 2003; Calcagno et al.,
2004) had shown that all larval stages of L. santolla are nonfeeding. From the day of
metamorphosis, juvenile crabs were fed with Artemia nauplii (Argent Chemical Labora-
tories, USA). At 9– 15 jC, the culture water (in juveniles also food) was changed every
other day, at lower temperatures every third day, at 18jC daily. In all treatments, the larvae
or juveniles were checked daily for moults or mortality. Due to technical problems, the
moult from the zoea II – III stage was not recorded in larvae from hatch B reared at 3 and
12 jC, so that no data of development duration through these two individual stages were
obtained in these exceptional cases (Table 2). Upon reaching the benthic megalopa, a piece
of nylon mesh was placed in each bowl as an artificial substrate, which facilitated the
settlement and metamorphosis of the megalopa.
The rearing experiments with hatch A were continued throughout one year, from
August 2001 to August 2002, while the additional experiments with hatch B were
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 219
terminated earlier (at 6 and 9 jC as soon as the crab stage II was reached; at 12 jC in the
crab IV). Due to an accident, the experiment with hatch A larvae reared at 12 jC was
prematurely terminated during the crab III instar, so that no data for later juvenile instars in
this treatment were obtained.
Our statistical analyses followed Sokal and Rohlf (1995). One-way ANOVA followed
by comparisons between pairs of means was used for comparing survival and time of
development at each larval stage. The durations of individual (larval or juvenile) stages as
well as cumulative periods of development (e.g. from hatching to metamorphosis) were
described as power functions of temperature (i.e., as linear regressions after log-
transformation of both variables). Arithmetic mean values obtained from different females
rather than individual data were used as replicate values in regression analyses. Slope
parameters of the linearized regressions were compared with a test for heterogeneity of
slopes using the Fstatistics. Where average values with error estimates are given in the
text or in figures and tables, these represent arithmetic mean valuesFone standard
deviation (S.D.).
3. Results
3.1. Rates of survival
The rate of survival through successive larval and juvenile stages varied greatly among
the various temperature conditions and the two hatches obtained from different females
(Table 1). In the temperature range for which sufficient comparative data are available for
both hatches (6 – 12 jC), larvae from hatch B showed generally a higher cumulative rate
of survival to metamorphosis and through the first juvenile crab instar than those
obtained from hatch A. Zoeal survival at 3 jC, however, was higher in larvae from
hatch A (Table 1).
When larval survival rates are compared in the full range of experimental temperatures,
we see clearly that the extreme conditions of 1 and 18 jC exerted thermal stress not
allowing for successful development through metamorphosis. While most larvae (71%)
survived at 1 jC through two zoeal moults to the zoea III stage, none of these was able to
moult to the megalopa. At the second coldest condition, 3 jC, 17 – 33% of the larvae
originating from hatches B and A, respectively, developed successfully to the megalopa
stage. A single individual (from hatch A) survived in this treatment through metamor-
phosis to the first juvenile crab instar. It died two months later without moulting again. At
the highest temperature tested (18 jC), most larvae (98%) remained alive for up to one
week but all of these died eventually without moulting. A single individual reached 2 days
after hatching the second zoeal stage, but it also died the next day. The intermediate
temperature conditions (6 – 15 jC) allowed for substantial (35 – 90%) survival through
complete larval development to metamorphosis.
When the experiments were terminated, 1 year after hatching, the survivors had
maximally reached juvenile instar VI (6 jC), VII (9 jC), and IX (15 jC), respectively,
with cumulative survival rates ranging from 8% to 17% (Table 1); the 12 jC treatment was
accidentally lost during the crab III stage so that it cannot be included in this comparison.
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230220
Table 1
L. santolla. Rates of survival in individual developmental stages (in % of survivors to a given stage) in larvae obtained from two different females (A, B); cumulative
survival (from hatching through a given stage, cum.%; in % of initial number at hatching, n=48, highlighted in italics)
TFemale Stage
(jC) Zoea I Zoea II Zoea III Megalopa Crab I Crab II Crab III Crab IV Crab V Crab VI Crab VII Crab VIII
% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.% % cum.%
1 A 75 89 71 00
3 A 98 62 63 55 33 13 2
B775146 42 17 00
6 A 94 89 83 93 77 95 73 94 69 85 58 61 33 47 17 100 17
B968581 97 79 90 71 100 71
9 A 90 67 60 62 38 78 29 93 27 100 27 92 25 50 13 83 10 80 8
B 94 100 94 98 90 98 90 88 79
12 A 90 67 60 79 48 74 35 47 17 50 8
B907981 85 69 93 56 85 48 78 38 17 8
15 A 94 91 85 90 77 84 65 94 60 72 44 86 38 83 31 93 29 57 17 88 15 71 10
18 A 2 0 0
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 221
Table 2
L. santolla. Time of development through successive larval and early juvenile stages (days, meanF1 standard deviation) in larvae obtained from two different females (A,
B) and reared at different temperatures (T,jC); nd=not determined; *=no S.D. available (n=1)
TFemale Stage
(jC) Zoea I Zoea II Zoea III Megalopa Crab I Crab II Crab III Crab IV Crab V Crab VI Crab VII Crab VIII
xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D.
1 A 17.5 3.0 22.6 3.1
3 A 10.1 2.6 24.1 4.7 24.3 6.9 80.0 *
B 13.6 3.1 nd nd nd nd
6 A 5.6 1.9 7.8 0.5 11.0 0.6 36.1 1.8 42.8 2.9 56 9 64 10 67 6 68 10
B 5.5 0.8 8.6 1.2 10.6 0.8 38.7 2.4 46.1 4.2
9 A 3.2 0.4 4.4 0.6 6.9 0.5 29.1 1.4 30.0 1.8 38 6 39 7 48 13 56 7 62 17
B 3.8 0.5 4.4 0.5 7.5 0.7 30.1 3.2 31.9 4.2
12 A 2.4 0.5 4.2 0.7 4.9 0.4 21.6 2.6 22.8 1.7 32 5
B 3.1 0.4 nd nd nd nd 22.2 2.8 26.4 3.1 34 9
15 A 3.0 0.4 2.6 0.6 4.2 0.5 15.1 1.0 20.5 3.3 23 5 28 9 25 9 30 9 32 7 36 7 54 14
18 A 2.0 *
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230222
Table 3
L. santolla. Cumulative time of development from hatching to successive stages (days, meanF1 standard deviation) in larvae obtained from two different females (A, B)
and reared at different temperatures (T,jC); *=no S.D. available (n=1)
TFemale Stage
(jC) Megalopa Crab I Crab II Crab III Crab IV Crab V Crab VI Crab VII Crab VIII Crab IX
xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D. xFS.D.
3 A 56.9 4.4 129 *
B 51.3 5.3
6 A 24.0 0.9 60.1 2.1 103 4.0 161 15 221 15 289 16 356 11
B 24.6 0.8 64.9 10 110 5.2
9 A 14.2 0.4 43.4 1.3 73.4 2.0 111 6 150 11 203 20 263 24 330 33
B 15.7 0.6 45.8 3.1 77.3 5.8
12 A 11.4 0.6 32.9 2.4 56.1 4.2 90 6
B 12.6 0.5 34.7 2.8 60.9 4.6 95 10
15 A 9.7 0.5 19.3 1.0 45.3 3.9 68 6 97 12 121 13 150 19 187 22 226 26 278 20
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 223
3.2. Rates of development
Development durations of individual larval and juvenile stages are given in Table 2;
cumulative development times (from hatching) are shown in Table 3. No statistically
significant differences in individual stage durations were observed between larvae
originating from two different females (Table 2). As a consequence, also the cumulative
durations to successive stages at identical temperatures were generally similar and
differences were statistically insignificant (Table 3).
Increasing temperature had in general a significant accelerating effect on development,
especially in the lower temperature range. As a single exception, there was no significant
difference between zoea II durations recorded in hatch A at 1 and 3 jC(Table 2). While an
increase from 3 to 6 or from 6 to 9 jC caused in all three zoeal stages a substantial (and
statistically highly significant; all P<0.0001) decrease in moult-cycle durations, the stage
durations measured at 9 and 12 jC were much more similar to each other. With the
exception of the zoea II stage (hatch A) and crab I (hatch B), however, all differences
between these two temperatures were statistically significant. The differences observed
between 12 and 15 jC were still smaller; in the zoea I and crab I stages they were
statistically insignificant ( P>0.05).
Within the entire temperature range tested in this study (1 – 18 jC), the zoea I lasted on
average 2– 18 days. The zoea II took 3 – 23 days (data available only for the range from 1
to 15 jC), and the zoea III stage lasted 4 –24 days (at 3 – 15 jC). The mean duration of the
megalopa varied in the same temperature range from 15 to 80 days (Table 2).
Complete zoeal development from hatching to the moult of the zoea III to the megalopa
stage varied, at temperatures of 3 – 15 jC, from about 10 – 57 days, while the complete
nonfeeding larval development from hatching to metamorphosis took from 19 days (at 15
jC) to 129 days (at 3 jC), i.e. from less than 3 weeks to more than 4 months (Table 3).
The moult-cycle durations of successive juvenile instars also showed consistently a
decrease with increasing temperature. The duration of the crab I stage, for instance, varied
from 20 days (at 15 jC) to 46 days (6 jC). As another consistent trend, the young crab
Table 4
L. santolla. Fitted parameters (a,b) and coefficients of determination (r
2
) of nonlinear regression equations
(power functions, y=aT
b
) describing development time ( y, days) as a function of temperature (T,jC); (i) time of
development in individual stages (dev./stage); (ii) cumulative time of development from hatching to later stages
(cum.dev.)
Parameter Stage
Zoea I Zoea II Zoea III Megalopa Crab I Crab II Crab III
(i) Dev./stage
a22.7 33.7 79.6 200.1 201.5 273.2
b0.812 0.860 1.102 0.906 0.848 0.879
r
2
0.934 0.855 0.995 0.936 0.971 0.945
(ii) Cum.dev.
a52.8 173.3 430.6 537.8 788.5
b0.814 1.086 1.061 0.900 0.881
r
2
0.916 0.990 0.960 0.985 0.974
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230224
stages showed at each temperature increasing moult-cycle durations and an increasing
variability in successively later instars (Table 2).At15jC, for example, the crab I instar
lasted, on average, 20.5F3.3 days, while the time in the crab VIII stage was more than
twice as long (54F14 days). At 9 jC, the moult-cycle duration doubled from the crab I to
the crab VI (30F1.8 vs. 62F17 days).
Fig. 1. L. santolla. Duration of larval and early juvenile development in relation to temperature. (a) Illustration of
the nonlinear relationship (power function, see text): zoea I stage duration at 1 – 18 jC; (b) cumulative time of
development from hatching to later stages (megalopa – crab III, at 3 – 15 jC).
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 225
The patterns of development duration (D, in days) in relation to temperature (T,injC)
could be described as a power function, D=aT
b
, where aand bare fitted parameters (Table
4). Almost all coefficients of determination (r
2
) were >0.9 (only exception: duration of the
zoea II, with r
2
=0.855). The best fit between observed and predicted data (r
2
z0.99) was
found in the duration of the zoea III stage and in the cumulative time of development from
hatching to metamorphosis.
These nonlinear patterns are illustrated in Fig. 1a using the untransformed zoea I data as
an example. Linearized regressions (after log-log transformation) of cumulative develop-
ment times in relation to temperature are shown in Fig. 1b for all individual stages where
complete data sets for a minimum of four different temperatures were available (i.e., up to
the crab III stage, cf. Table 3). The slopes of these regression lines were not significantly
different from each other (ANCOVA, P>0.05), indicating a similar degree of temperature
dependence in successive developmental stages.
4. Discussion
The early life history of the southern king crab, L. santolla, has until recently very little
been known, although this species used to have, and potentially still has, a high economic
value as a fishery resource in southern Argentina and Chile. Moreover, there is
considerable interest in the commercial aquaculture and stock enhancement of king crabs
in general (for discussion and references, see, e.g. Konishi, 1998; Konishi and Shikatani,
1999; Stevens, 2003). Thus, an improved knowledge of the early development and growth
of king crabs should be crucial not only for resource management and the implementation
of fishery regulations (Lovrich, 1997; Lovrich and Vinuesa, 1999), but it also is a major
prerequisite for the development of technically and commercially feasible artificial
cultivation techniques.
Recent studies on the same species (Kattner et al., 2003; Lovrich et al., 2003) showed
that the entire larval development from hatching to metamorphosis is in L. santolla fully
independent of food. This trait should greatly facilitate the otherwise much more
complicated, labour-intensive, and expensive rearing from the egg to the first juvenile
stage. The present study now provides an indication of the optimal temperature range for
larviculture: it should be most successful between ca. 6 and 15 jC; the initial rearing, at
least through the zoeal stages, should also be possible at lower temperatures down to about
3jC. For rearing facilities located in the Magellan region, where average sea surface
temperatures vary seasonally between about 5 and 10 jC(Fig. 2), our results indicate that
the larvae of this king crab species can simply be reared under ambient-temperature flow-
through conditions.
The same holds true for rearing sites at the northern distributional limit of this species in
the Pacific, although the average water temperatures in this region are about 4– 9 jC
higher than in the Beagle Channel (Fig. 2). Since the larvae of this species hatch during the
austral winter and spring, i.e. from early August to October (present observations; cf.
Lovrich and Vinuesa, 1999; Thatje et al., 2003), ambient water temperatures of about 10 –
12 jC in southern-central Chile (see Fig. 2) would still be within the optimal range for
larval rearing. Later juvenile stages, however, might have problems at summer temper-
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230226
atures rising up to about 18 jC. On the other hand, the benthic juveniles may be more
tolerant of those conditions compared to the larval stages, in particular those of northern,
more warm-adapted populations. This implies that, like in the Beagle Channel and the
adjacent Magellan region, a continued cultivation of juveniles in this area would probably
not require energy-consuming and expensive cooling of cultivation tanks.
Our experimental laboratory study not only provides information on optimal temper-
ature conditions for larval and early juvenile rearing of the southern king crab, but our data
(cf. Tables 2 and 3) also allow for estimates of seasonal variation of development and
growth in the field. In the area of origin of our material, the Beagle Channel, hatching
begins in early August when water temperature is about 5 jC(Fig. 2). First settlement of
megalopae, which show largely benthic behaviour and thus terminate the period of
demersal planktonic dispersal (see Lovrich et al., 2003, Thatje et al., 2003), should occur
from late August or beginning of September; earliest metamorphosis to the first juvenile
instar should be expected for early October, roughly coinciding with the end of the
hatching period (Lovrich and Vinuesa, 1999). Latest metamorphosis should thus occur
about 2 months later, implying that the entire spring season, from October through
December, represents the principal period of juvenile settlement and metamorphosis in the
Beagle Channel and adjacent areas. In next winter, about 1 year after hatching of a cohort,
juvenile king crabs may reach approximately instars VII –VIII.
Assuming a similar temperature dependence of early development in the offspring of
northern populations of L. santolla, we may estimate also the approximate timing of key
events such as settlement and metamorphosis in the region off the island of Chiloe
´and
Fig. 2. Thermal climate near the southern and northern limits of geographic distribution of L. santolla: seasonal
variation of average sea surface temperatures in the Beagle Channel (55jS; monthly mean valuesFS.D. for the
period 1994 – 1998; Servicio Centralizado de Documentacio
´n, CADIC, unpublished data; open squares) and off
the Pacific Island of Chiloe
´(42jS; monthly mean values; data from Lardies and Wehrtmann, 2001; filled plot
symbols).
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 227
adjacent areas in the Pacific Ocean. Larval hatching appears to occur there slightly earlier
than in the Beagle Channel (mostly in August; Paschke, personal communication). At
average water temperatures of about 10 – 12 jC (see Fig. 2), the demersal-planktonic zoeal
phase should be very short, probably not exceeding ca. two weeks (cf. Table 3), and
metamorphosis from the megalopa to the first juvenile stage may occur already in
September. Within 1 year from hatching, juvenile king crabs may grow there to
approximately instar IX.
Similar predictions may be made also for the region where L. santolla reaches its
northernmost distributional limit in the Atlantic Ocean, i.e. on the continental slope off
Uruguay in ca. 700 m depth (Vinuesa, 1991). Since the temperatures in this deep-water
environment are, throughout the year, similar to those in the Beagle Channel during winter
(Guerrero and Piola, 1997), the larval and early juvenile development should be similar as
observed in our experiments at 6 jC. This implies that juvenile growth should be slower
than in the Beagle Channel, probably reaching only crab instar VI during the first year of
postembryonic life.
While it appears that such extrapolations from laboratory observations should allow for
fairly reliable predictions of early development and growth in the field, in particular in a
species where larval feeding is not a potentially confounding factor, future studies must
scrutinize if the temperature dependence of developmental rates in southern and northern
populations is really independent of regionally varying climatic conditions. If the relation-
ships between development duration and temperature show a latitudinal shift, this may
indicate the occurrence of an evolutionary temperature adaptation (for recent discussion,
see Clarke, 2003). As a consequence of physiological compensation mechanisms, the
northern populations of L. santolla in Chile would, in this case, show longer periods of
larval and early juvenile development than expected from the extrapolation of our present
experimental data.
Our observations of larval and early juvenile temperature tolerance suggest that L.
santolla is a typical cold-eurythermal species, which also explains its wide distributional
range extending over about 13jlatitude in the Pacific and almost 20jin the Atlantic
Ocean. Its larvae are able to develop from hatching to at least the last zoeal stage at
temperatures as low as 1 – 3 jC, and all larval stages including the benthic megalopa are
fully lecithotrophic, i.e. nonfeeding even when food is available. Very similar develop-
mental traits were recently observed also in another, closely related species from the
Beagle Channel, the lithodid crab Paralomis granulosa (Anger et al., 2003; Calcagno et
al., 2003, 2004; Kattner et al., 2003). An extreme degree of larval independence from
plankton production, in combination with tolerance of low temperatures, has been
interpreted as an early life-history adaptation to conditions typically prevailing at high
latitudes, i.e. cold stress and seasonally short or unpredictable plankton productivity in
winter, when king crab larvae predominantly hatch.
Similar traits have been observed in two lithodid species from the northern hemispere
(Anger, 1996; Shirley and Zhou, 1997) and may thus be expected to occur also in further
king crab species whose developmental patterns have remained unknown. This suggests
that lithodid crabs, including the subantarctic species L. santolla and P. granulosa, belong
to the most likely candidates for a possible scenario of a future repopulation of Antarctic
waters, from where reptant decapod crustaceans have virtually disappeared during
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230228
Antarctic cooling until the middle Miocene about 15 million years ago (Crame, 1999).If
our global climate continues to warm, this might allow for a gradual invasion of polar
regions by preadapted subpolar, and perhaps deep-sea dwelling lithodid crabs. Since king
crabs show a high species diversity in subpolar and deep sea regions of both hemispheres,
and in most of these species the early life history is completely unknown, future
experimental studies may reveal further candidates with cold-tolerant and starvation-
resistant larvae.
Acknowledgements
We greatly appreciate the help of the crew of PFS ‘‘Polarstern’’ during the transport of
live crabs. U. Nettelmann and several students helped in maintaining larval and juvenile
cultures. Thanks are also due to Dr. I. Wehrtmann for providing temperature data for
Chiloe
´, Chile. J. Calcagno is grateful to the German Academic Exchange Service (DAAD,
Bonn) and the Alfred-Wegener-Institut fu
¨r Polar- und Meeresforschung (AWI,
Bremerhaven) for funding his research visits to Helgoland. G. Lovrich acknowledges
additional support from the International Foundation for Science (grant A2507-2). This
project was principally funded by the International Bureau of the German Ministry of
Scientific Research (BMBF, project no. ARG 99/002), and the Argentine Secretarı
´ade
Ciencia, Tecnologı
´a e Inovacio
´n Productiva (SeCyT). [SS]
References
Anger, K., 1996. Physiological and biochemical changes during lecithotrophic larval development and early
juvenile growth in the northern stone crab, Lithodes maja (Decapoda: Anomura). Mar. Biol. 126, 283 – 296.
Anger, K., Thatje, S., Lovrich, G., Calcagno, J., 2003. Larval and early juvenile development of Paralomis
granulosa reared at different temperatures: tolerance of cold and food limitation in a lithodid crab from
high latitudes. Mar. Ecol. Prog. Ser. 253, 243 – 251.
Arntz, W.E., Brey, T., Gallardo, V.A., 1994. Antarctic zoobenthos. Oceanogr. Mar. Biol. Annu. Rev. 32, 241– 304.
Arntz, W.E., Gutt, J., Klages, M., 1997. Antarctic marine biodiversity: an overview. In: Battaglia, B., Valencia, J.,
Walton, D.W.H. (Eds.), Antarctic Communities: Species, Structure and Survival. Cambridge Univ. Press,
Cambridge, UK, pp. 3 – 14.
Boschi, E.E., Fischbach, C.E., Iorio, M.I., 1992. Cata
´lago ilustrado de los crusta
´ceos estomato
´podos y deca
´podos
marinos de Argentina. Frente Marı
´t., Uruguay 10, 7 – 94.
Calcagno, J.A., Thatje, S., Anger, K., Lovrich, G.A., Kaffenberger, A., 2003. Changes in biomass and chemical
composition during lecithotrophic larval development of the southern stone crab Paralomis granulosa. Mar.
Ecol. Prog. Ser. 257, 189 – 196.
Calcagno, J.A., Anger, K., Lovrich, G.A., Thatje, S., Kaffenberger, A., 2004. Larval development of the sub-
antarctic king crabs Lithodes santolla and Paralomis granulosa reared in the laboratory. Helgol. Mar. Res. 58,
11– 14.
Campodonico, G.I., 1971. Desarrollo larval de la centolla Lithodes antarctica Jacquinot en condiciones de
laboratorio (Crusta
´cea Decapoda, Anomura: Lithodidae). An. Inst. Patagon., Ser. Cienc. Nat. (Punta Arenas,
Chile) 2, 181 – 190.
Clarke, A., 2003. Costs and consequences of evolutionary temperature adaptation. Trends Ecol. Evol. 18, 573 – 581.
Crame, J.A., 1999. An evolutionary perspective on marine faunal connections between southernmost South
America and Antarctica. Sci. Mar. 63 (Suppl. 1), 1 – 14.
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230 229
Dawson, E.W., 1989. King crabs of the world (Crustacea: Lithodidae) and their fisheries: a comprehensive
bibliography. Misc. Publ.-N.Z. Oceanogr. Inst. Div. Water Sci., vol. 101. DSIR, Wellington, pp. 1– 338.
Gorny, M., 1999. On the biogeography and ecology of the Southern Ocean decapod fauna. Sci. Mar. 63 (Suppl. 1),
367 – 382.
Guerrero, R.A., Piola, A.R., 1997. Masas de agua en la plataforma continental. In: Boschi, E.E. (Ed.), El Mar
Argentino y sus recursos pesqueros. Antecedentes histo
´ricos de las exploraciones en el mar y las caracter-
ı
´sticas ambientales, vol. 1. Instituto Nacional de Investigacio
´n y Desarrollo Pesquero (INIDEP), Mar del Plata,
Argentina, pp. 107 – 118.
Kattner, G., Graeve, M., Calcagno, J.A., Lovrich, G.A., Thatje, S., Anger, K., 2003. Lipid, fatty acid and protein
utilization during lecithotrophic larval development of Lithodes santolla (Molina) and Paralomis granulosa
(Jacquinot). J. Exp. Mar. Biol. Ecol. 292, 61– 74.
Klages, M., Gutt, J., Starmans, A., Bruns, T., 1995. Stone crabs close to the Antarctic continent: Lithodes murrayi
Henderson, 1888 (Crustacea; Decapoda; Anomura) off Peter I Islands (68j51VS, 90j51VW). Polar Biol. 15,
73 – 75.
Konishi, K., 1998. Production of juveniles of shrimps and crabs in Japan. Farming Jpn. 32, 28 – 37.
Konishi, K., Shikatani, N., 1999. Identification manual for larvae of commercially important crabs in Japan: II.
Anomuran crabs. Bull. Natl. Res. Inst. Aquac. 28, 5 – 13.
Lardies, M.A., Wehrtmann, I.S., 2001. Latitudinal variation in the reproductive biology of Betaeus truncatus
(Decapoda: Alpheidae) along the Chilean coast. Ophelia 55, 55 – 67.
Lovrich, G.A., 1997. La pesquerı
´a mixta de las centollas Lithodes santolla y Paralomis granulosa (Anomura:
Lithodidae) en Tierra del Fuego, Argentina. Invest. Mar. (Valparaı
´so) 25, 41 – 57.
Lovrich, G.A., Vinuesa, J.H., 1999. Reproductive potential of the lithodids Lithodes santolla and Paralomis
granulosa (Anomura, Decapoda) in the Beagle Channel, Argentina. Sci. Mar. 63 (Suppl. 1), 355 – 360.
Lovrich, G.A., Thatje, S., Calcagno, J.A., Anger, K., Kaffenberger, A., 2003. Changes in biomass and chemical
composition during lecithotrophic larval development of the southern king crab, Lithodes santolla (Molina).
J. Exp. Mar. Biol. Ecol. 288, 65 – 79.
McLaughlin, P.A., Anger, K., Kaffenberger, A., Lovrich, G.A., 2001. Megalopal and early juvenile development
in Lithodes santolla (Molina, 1782) (Decapoda: Anomura; Paguroidea: Lithodidae), with notes on zoeal
variations. Invertebr. Reprod. Dev. 40, 53 – 67.
Retamal, M.A., 1981. Cata
´logo ilustrado de los Crusta
´ceos Deca
´podos de Chile. Gayana, Zool., vol. 44 Uni-
versidad De Concepcio
´n, Chile, pp. 1 – 110.
Shirley, T.C., Zhou, S., 1997. Lecithotrophic development of the golden king crab Lithodes aequispinus (Anom-
ura: Lithodidae). J. Crustac. Biol. 17, 207 – 216.
Sokal, R.R., Rohlf, F.J., 1995. Biometry. The Principles and Practice of Statistics in Biological Research.
Freeman, New York, NY. 887 pp.
Stevens, B.G., 2003. Settlement, substratum preference, and survival of red king crab Paralithodes camtschaticus
(Tilesius, 1815) glaucothoe on natural substrata in the laboratory. J. Exp. Mar. Biol. Ecol. 283, 63 – 78.
Sundet, J.H., Hjelset, A.M., 2002. The Norwegian red king crab (Paralithodes camtschaticus) fishery: man-
agement and bycatch issues. In: Paul, A.J., Dawe, E.G., Elner, R., Jamieson, G.S., Kruse, G.H., Otto, R.S.,
Sainte-Marie, B., Shirley, T.C., Woodby, D. (Eds.), Crabs in Cold Water Regions: Biology, Management,
and Economics, University of Alaska, Fairbanks, AK, USA, pp. 681 – 692. Sea Grant College Program
AK-SG-02-01.
Thatje, S., Calcagno, J.A., Lovrich, G.A., Sartoris, F.J., Anger, K., 2003. Extended hatching periods in the
subantarctic lithodid crabs Lithodes santolla and Paralomis granulosa (Crustacea: Decapoda: Lithodidae).
Helgol. Mar. Res. 57, 110 – 113.
Vinuesa, J.H., 1991. Biologia y pesqueria de la centolla (Lithodes santolla). Rio Grande (Atlantica) 13, 233 – 244.
Zaklan, S.D., 2002. Review of the family Lithodidae (Crustacea: Anomura: Paguroidea): distribution, biology,
and fisheries. In: Paul, A.J., Dawe, E.G., Elner, R., Jamieson, G.S., Kruse, G.H., Otto, R.S., Sainte-Marie, B.,
Shirley, T.C., Woodby, D. (Eds.), Crabs in Cold Water Regions: Biology, Management, and Economics,
University of Alaska, Fairbanks, AK, USA, pp. 751 – 845. Sea Grant College Program AK-SG-02-01.
K. Anger et al. / J. Exp. Mar. Biol. Ecol. 306 (2004) 217–230230
