Egg production, hatching rates, and abbreviated larval development of Campylonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea), in subantarctic waters

Abstract

Early life history patterns were studied in the caridean shrimp, Campylonotus vagans Bate, 1888, from the subantarctic Beagle Channel (Tierra del Fuego). As a consequence of very large egg size (minimum 1.4 mm), fecundity was low, ranging from 83 to 608 eggs per female (carapace length [CL] 11–22.5 mm). Egg size increased continuously throughout embryonic development, reaching prior to hatching about 175% of the initial diameter. Due to low daily numbers of larval release, hatching of an egg batch lasted for about 2–3 weeks. The complete larval and early juvenile development was studied in laboratory cultures fed with Artemia sp. nauplii. At 7.0±0.5 °C, development from hatching to metamorphosis lasted for about 6 weeks. It comprised invariably two large zoeal stages and one decapodid, with mean stage durations of 12, 17, and 15 days, respectively. Larvae maintained without food survived on average for 18 days (maximum: 29 days), but did not reach the moult to the zoea II stage. Size increments at ecdysis were low in all larval stages (2.1–3.9%), indicating partial utilisation of internal energy reserves. A clearly higher increment (14%) was observed in the moult from the first to the second juvenile stage. Low fecundity, large size of eggs and larvae, an abbreviated mode of larval development, high larval survival rates during absence of food, demersal behaviour of the early life history stages, and an extended hatching period with low daily release rates are interpreted as adaptations to conditions typically prevailing in subantarctic regions, namely low temperatures (causing long durations of development) in combination with a pronounced seasonality in plankton production (i.e., short periods of food availability).

Full text

Egg production, hatching rates, and abbreviated
larval development of Campylonotus vagans
Bate, 1888 (Crustacea: Decapoda: Caridea),
in subantarctic waters
Sven Thatje
a,
*, Gustavo A. Lovrich
b
, Klaus Anger
c
a
Alfred Wegener Institute for Polar and Marine Research, PO Box 120 161, D-27515 Bremerhaven, Germany
b
Consejo Nacional de Investigaciones Cientı
´ficas y Te
´cnica, Centro Austral de Investigaciones Cientı
´ficas,
CC 92, Ushuaia, Tierra del Fuego, Argentina
c
Biologische Anstalt Helgoland, Stiftung Alfred Wegener Institute for Polar and Marine Research,
Helgoland, Germany
Received 1 January 2003; received in revised form 23 May 2003; accepted 1 September 2003
Abstract
Early life history patterns were studied in the caridean shrimp, Campylonotus vagans Bate, 1888,
from the subantarctic Beagle Channel (Tierra del Fuego). As a consequence of very large egg size
(minimum 1.4 mm), fecundity was low, ranging from 83 to 608 eggs per female (carapace length
[CL] 11–22.5 mm). Egg size increased continuously throughout embryonic development, reaching
prior to hatching about 175% of the initial diameter. Due to low daily numbers of larval release,
hatching of an egg batch lasted for about 2 – 3 weeks. The complete larval and early juvenile
development was studied in laboratory cultures fed with Artemia sp. nauplii. At 7.0 F0.5 jC,
development from hatching to metamorphosis lasted for about 6 weeks. It comprised invariably two
large zoeal stages and one decapodid, with mean stage durations of 12, 17, and 15 days, respectively.
Larvae maintained without food survived on average for 18 days (maximum: 29 days), but did not
reach the moult to the zoea II stage. Size increments at ecdysis were low in all larval stages (2.1 –
3.9%), indicating partial utilisation of internal energy reserves. A clearly higher increment (14%)
was observed in the moult from the first to the second juvenile stage. Low fecundity, large size of
eggs and larvae, an abbreviated mode of larval development, high larval survival rates during
absence of food, demersal behaviour of the early life history stages, and an extended hatching period
with low daily release rates are interpreted as adaptations to conditions typically prevailing in
subantarctic regions, namely low temperatures (causing long durations of development) in
0022-0981/$ - see front matter D2003 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2003.09.010
* Corresponding author. Tel.: +49-471-4831-1315; fax: +49-471-4831-1149.
E-mail address: sthatje@awi-bremerhaven.de (S. Thatje).
www.elsevier.com/locate/jembe
Journal of Experimental Marine Biology and Ecology
301 (2004) 15 – 27

combination with a pronounced seasonality in plankton production (i.e., short periods of food
availability).
D2003 Elsevier B.V. All rights reserved.
Keywords: Abbreviated larval development; Decapoda; Fecundity; Hatching; Mortality
1. Introduction
Several species of caridean shrimps have developed strong life history adaptations to both
latitudinally changing conditions of food and temperature (for reviews, see Clarke, 1982,
1987, 1993a). Among the most conspicuous adaptations, this includes an increasing egg size
with increasing latitude and decreasing average water temperature, associated with changes
in the biochemical composition of eggs, and often reduced fecundity (Gorny et al., 1992;
Wehrtmann and Kattner, 1998; Wehrtmann and Lardies, 1999; Anger et al., 2002).Asan
additional latitudinal trend, larval size at hatching appears to increase, while the number in
larval instars and the degree of morphological variability tend to decrease (cf. Wehrtmann
and Albornoz, 1998; Thatje and Bacardit, 2000). Low temperatures at high latitudes have
been observed to enhance not only larval development time, but also slower growth and
lower mortality as compared with boreal species (Clarke and Lakhani, 1979; Arntz et al.,
1992; Gorny et al., 1993).
The diversity of decapod crustaceans is comparably low in polar regions (Yaldwyn,
1965; Abele, 1982; Briggs, 1995). In the caridean shrimps, there is a strong decline in
species diversity from the subantarctic (Gorny, 1999) to Antarctic waters (see Yaldwyn,
1965; Kirkwood, 1984; Tiefenbacher, 1990), with only five representatives remaining on
the high Antarctic Weddell Sea shelf (Gorny, 1999).
The family Campylonotidae consists of four known subantarctic and one Antarctic
representative (Gorny, 1999; Thatje, 2003). The species of this family show a wide
bathymetric distribution, ranging from the shallow sublittoral to the deep sea (Thatje and
Lovrich, 2003). Within the subantarctic Magellan Region (South America), the two
species Campylonotus vagans Bate, 1888, and Campylonotus semistriatus Bate, 1888,
are known to occur in the Argentine Beagle Channel (54j53 S, 68j17 W, Fig. 1). C.
vagans is associated with the shallow sublittoral fauna and can be found as by-catch of the
dominating galatheid crab Munida subrugosa (Pe
´rez-Barros et al., in press; Tapella et al.,
2002).C. semistriatus Bate, 1888, in contrast, is more abundant in the sublittoral below
100 m depth (Wehrtmann and Lardies, 1996).
Little is generally known about the early life history of campylonotid shrimps.
Protandrous hermaphroditism is assumed to be a typical trait in this family (Yaldwyn,
1966; Torti and Boschi, 1973), but this has not been confirmed for all species. The
Campylonotidae shows apparently an abbreviated mode of larval development (Pike and
Williamson, 1966; Thatje et al., 2001). However, a complete description of larval and early
juvenile morphology is only available for C. vagans (Thatje et al., 2001; Thatje and
Lovrich, 2003).
The knowledge of early life history patterns in shrimps from high latitudes and, in
particular, from subantarctic waters, is scarce. In the present study, we document
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2716

laboratory observations on fecundity, egg size, hatching, as well as on larval and early
juvenile development in the caridean shrimp C. vagans from subantarctic waters. The
early life history of this species is discussed in relation to ecological conditions prevailing
in the cold to temperate subantarctic region of South America.
2. Materials and methods
2.1. Sampling of ovigerous females
Ovigerous C. vagans were caught in September 2001 from about 15 to 30 m depth in
the Beagle Channel (54j53VS, 68j17VW, Fig. 1) using an inflatable dinghy equipped with
an epibenthic trawl (1.7 m mouth width, net with 1 cm mesh size), which was especially
designed to be operated from a small boat (Tapella et al., 2002). Additional egg-carrying
Fig. 1. Sampling location of C. vagans in the subantarctic Beagle Channel, South America.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 17

females (fixed in 3 – 4% formalin buffered with hexamethylenetetramine) were obtained
from bottom trawls taken during the expedition ‘‘Cimar Fiordo III’’ on board the Chilean
vessel ‘‘Vidal Gormaz’’ to the Magellan region, the Straits of Magellan (53jS) and the
Beagle Channel (55jS) in October 1997 (Thatje and Mutschke, 1999). Both regions show
a comparable temperature regime ranging from about 4 to 9 jC in winter and summer,
respectively (Lovrich, 1999; Tapella et al., 2002).
2.2. Maintenance of ovigerous females
Maintenance of ovigerous females and rearing of larvae took place in the local institute
‘‘Centro Austral de Investigaciones Cientı
´ficas’’ (CADIC) in Ushuaia, Tierra del Fuego
(Argentina), under constant conditions of temperature (7.0 F0.5 jC), salinity (30x),
and a 12:12 h light/dark rhythm. The ovigerous shrimps were kept individually in tanks
(minimum 30 l water content) with permanent seawater flow from a closed circulation
filter system. Food (commercial TETRA AniMin pellets for aquaristics, TetraWerke,
Germany) was given twice a week.
2.3. Rearing of larvae and juveniles
Hatched larvae were sampled each 24 h and collected from the bottom of the aquaria
using long glass pipettes. Each day, randomly selected larvae were transferred to
individual rearing cups with about 100 ml seawater. They were checked daily for dead
or moulted individuals. Every second day, water was changed and food (Artemia sp.
nauplii; Argent Chemical Laboratories, USA) was supplied. In an additional rearing,
larvae from the same female (N= 48) were kept under starvation condition.
The appearance of exuvia and visual observation of conspicuous morphological
differences were used to distinguish between the different stages of larval and juvenile
development. The zoea II can be easily distinguished from the previous stage by the
presence of well-developed external uropods (see Thatje et al., 2001), while the decapodid
is characterised by fully developed pereiopods bearing reduced exopods and complete
formation of the telson (Thatje and Lovrich, 2003).
2.4. Estimation of fecundity, measurements of eggs and larvae
The term fecundity is herein considered as the number of eggs per clutch. For the
calculation of clutch size/number of eggs, pleopods with attached eggs were removed from
each female by cutting the pleopodal base. Eggs were directly enumerated, due to low
fecundity in C. vagans. Fecundity in the individually kept females for the study of hatching
patterns and larval development was inferred from the daily number of hatched larvae and
egg losses.
The embryonic state of the eggs was divided into five stages; the first three were
classified according to the criteria provided by Wehrtmann and Kattner (1998): stage I:
eggs recently produced, uniform yolk, no eye pigments visible; stage II: eye pigments
barely visible; stage III: eyes clearly visible and fully developed, abdomen free.
Additionally, two later developmental stages were distinguished: stage IV: eggs elongate,
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2718

appendages free, prezoea close to hatching; stage V: strongly elongate, appendages free,
not covered by the abdomen anymore, setae of tail fan elongate. Stage V eggs were
released from the female pleopods during the hatching of larvae.
After fixation of larvae in 4% buffered formalin, larval carapace length (CL) and total
length (TL) were measured from the base of the rostrum between the eyes to the posterior
dorsal margin of the carapace, and to the posterior margin of the telson, respectively. All
lengths in eggs (N= 25 in each stage) and larvae (see Table 2) were measured to the
nearest 0.05 and 0.01 mm, respectively, using an eyepiece micrometer and a Zeiss
stereomicroscope.
2.5. Statistical treatments
The relationship between fecundity and female size was analyzed with a linear regression
analysis (Sokal and Rohlf, 1995) previously log-transforming data to achieve linearity.
Table 1
Average egg lengths of developing embryos (stage I to V, N= 25 each) of C. vagans from the subantarctic Beagle
Channel, South America
Egg length (mm) S.D.
Stage I 1.40 0.05
Stage II 1.45 0
Stage III 1.60 0.05
Stage IV 1.65 0.10
Stage V before hatching 2.45 0.05
Fig. 2. Female fecundity in C. vagans from the subantarctic Beagle Channel, South America. Round dots indicate
females maintained for larval development studies.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 19

Fig. 3. Daily hatching rates in C. vagans from the subantarctic Beagle Channel in 2001. Bare bars represent the
egg losses.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2720

Significant differences in egg sizes among the different stages were tested using a one-way
ANOVA (Sokal and Rohlf, 1995). Assumptions of homoscedasticity and normality were
tested with Bartlett’s and Kolmogorov–Smirnov tests, respectively. For the ANOVA, we
pooled the egg size data of stages I and II because of strong similarity and no variability in
stage II (Table 1).
3. Results
3.1. Fecundity and developmental increase in egg sizes
Fecundity of C. vagans from the Beagle Channel was low, varying from 83 to 608 eggs
per female (N= 20, Fig. 2). In spite of high individual variability, the log number of eggs
increased significantly with log female size, and followed the linear function: log N
eggs = 2.2 log LC 0.5 (Fig. 2;F
regress
= 13.5; P= 0.002).
During embryonic development from stages I to IV, we observed a continuous increase
in egg size (Table 1). Eggs prior to hatching (stage V) were significantly larger than those
in earlier stages (stages I + II combined; F= 9061.7; P< 0.001), reaching eventually 175%
of the initial (stage I) size.
3.2. Hatching pattern and larval development
The first larvae hatched at night, about a fortnight after the capture of ovigerous
females, showing a strong demersal behaviour. Nocturnal hatching of larvae occurred
through an extended period varying from 10 to 21 days. Normally, about 4–17% of the
total egg clutch hatched during single nights, exceptionally up to 25% (see female A, Fig.
3). The amount of eggs lost during hatching usually corresponded to about 0 –15% of the
respective nocturnal hatching rate of larvae. In some cases, however, egg losses were very
high, and corresponded to about 35 – 50% of the respective nocturnal hatching rate of
larvae (females C, D, Fig. 3). In almost all cases, stage V eggs were lost, indicating
prezoeae close to hatching.
The development from hatching to metamorphosis lasted about 6 weeks. It comprised
two zoeal stages and one decapodid, with mean durations of 12, 17, and 15 days,
respectively (Table 2). Most of this time was spent in the zoea II stage, which showed also
Table 2
Average lengths (TL, CL) and developmental times in larvae and early juveniles of C. vagans from the
subantarctic Beagle Channel, South America
Total length, TL Carapace length, CL Developmental time (days)
Zoea I 4.76 (0.09; 29) 1.18 (0.05; 29) 11.7 (0.89; 32)
Zoea II 4.86 (0.09; 13) 1.12 (0.06;13) 16.7 (4.2; 15)
Decapodid 5.15 (0.04; 21) 1.25 (0.04; 21) 15.3 (2.3; 6)
Juvenile I 5.35 (0.07; 8) 1.45 (0.07; 8) 19.5 (0.7; 2)
Juvenile II 6.1 (0.3; 2) 1.55(0.05; 2)
In brackets: standard deviation; N.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 21

the highest variability in development time (Table 2). Highest mortality was found at
metamorphosis from the zoea II to the decapodid stage (about 60%), and during the
subsequent moult to the first juvenile stage (67%; Fig. 4A). The larvae were large already
Fig. 4. C. vagans, changes in the number of larvae throughout larval development (A) larvae and early juveniles
with food (Artemia sp.) and (B) zoea I without food (Artemia sp.).
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2722

at hatching (average TL = 4.8 mm; Table 2), but in the subsequent moults, they showed
low growth rates, with TL increments of 2.1%, 3.4% and 3.9%, respectively. The moult of
the first to the second juvenile stage, by contrast, was accompanied by an increment in size
of about 14%.
Larvae kept under starvation conditions (without Artemia sp.) did not reach the moult
to the zoea II stage. The average survival time lasted 18 days, although some larvae
survived for up to almost 1 month (29 days), i.e., about three times longer than the average
stage duration in fed zoeae (Fig. 4A,B).
4. Discussion
The Campylonotidae shows protandrous hermaphroditism, which is typical of caridean
shrimps (Bauer, 1989, and references therein) and has been interpreted as an energetic life
history response to low temperatures in high latitudes (Yaldwyn, 1966; Torti and Boschi,
1973). We suggest sex reversal in C. vagans to occur at a body size of approximately 11 mm
CL, which corresponds to the size of the smallest ovigerous female found in the present
study (Fig. 2). However, further investigations are needed to define exact size of sex
reversal in the Campylonotidae. Most females carrying eggs had a CL of >16.5 mm (Fig. 2),
and, therefore, the smallest ovigerous female found may not be representative for the
population.
Extended hatching periods in decapods of high latitudes were recently discussed to be a
mechanism for synchronising larval occurrence with short periods of primary production/
food availability in high latitudes (for a detailed discussion, see Thatje et al., 2003a).
Extended hatching periods may also allow for avoiding predation on the small offspring
(see Thatje et al., 2003a).
C. vagans showed low fecundity (compare with Reid and Corey, 1991), large eggs
(Anger et al., 2002) at extrusion, and a strong increase in egg size during embryonic
development (Table 1). The analyses of fecundity referred to all eggs independent of
the embryonic development, due to few adult specimens available. Our fecundity
estimates may therefore be biased by the high rates in egg losses during embryonic
development, as demonstrated during hatching (Fig. 3). However, despite the females
kept for rearing experiments of larvae, the eggs of all other preserved ovigerous
females utilised had not reached the embryo stages IV to V yet. Since egg size
increases dramatically in the very final stage of embryo development (Table 1), which
obviously causes an increase of the entire batch, high amounts of egg losses may be
typical of the hatching period only. In the final stage of embryo development,
abdominal pleurae and pleopods do not cover the entire egg mass anymore, thus the less
protected batch should be more sensitive to abrupt female behaviour and/or external
physical impact.
Clarke (1993b) demonstrated a positive relationship between the extent of increase in
egg size or volume and the level of nutrients stored in the eggs; this should indicate an
enhanced female energy investment per offspring. However, egg size is not always a good
indicator for nutrient contents, since nutrient contents of eggs may also be density
dependent (Anger et al., 2002). From an evolutionary point of view, large larval size at
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 23

hatching is commonly associated with an abbreviated mode of larval development (Thatje
et al., 2001), which is advantageous in regions with short periods of primary production.
Although low temperatures affect developmental rates negatively, a reduction in the
number of larval moults reduces the energetic costs for larval development (Anger, 1998;
Thatje et al., 2003a; Thatje et al., in press). Microscopical observations showed that the
zoea I of C. vagans starts feeding immediately after hatching. On the other hand,
starvation experiments indicated that the resistance of unfed larvae to nutritional stress is
extremely high, extending the zoea I duration up to threefold. Some larvae which
survived 3 weeks of starvation (N= 6) were re-fed and had retained the capability of
reaching the moult to the subsequent zoeal stage. This indicates a very late appearance of
a critical point, the point-of-no-return (Anger, 1987). This preliminary observation
suggests that the zoea I of C. vagans contains high initial energy reserves, and recent
investigation has shown that the larval energy supply in C. vagans mainly depends on
proteins (Thatje et al., 2003b; Thatje et al., in press). These internal reserves alone,
however, are insufficient to reach the moult to the zoea II stage in complete absence of
food.
Larval sizes in the present study showed a clear discrepancy when compared with
larvae from plankton catches obtained in the southwestern Atlantic Ocean (Thatje et al.,
2001, zoea I, CL = 1.9 mm, TL = 5.8 mm; zoea II, CL = 2.0 mm, TL = 6.9 mm). These
striking differences should indicate that intraspecific variability is high, and may be
correlated with female fitness and size. Plasticity in caridean larval developments was
shown to be responsible for changes in larval size and developmental pathways in
Nauticaris magellanica (Thatje and Bacardit, 2000; Wehrtmann and Albornoz, 2003),
being temperature dependent. In addition, differences in larval developments between
laboratory reared and field collected larvae were shown to be affected by rearing
conditions (Wehrtmann and Albornoz, 2003). Both patterns may help to explain the
observed size differences in larvae of C. vagans, since the study of fatty acid contents in
both larvae and Artemia sp. nauplii, may suggest that utilisation of the Artemia by larvae
of C. vagans is not optimal (Thatje et al., 2003b; Thatje et al., in press). Despite the great
intraspecific variability at hatching, this may explain the much slower growth in our
laboratory reared larvae (Table 2, zoea I to zoea II, about 2.1%) when compared with
previous work (zoea I to zoea II, about 19%, see Thatje et al., 2001).
In subantarctic regions, we find decapod crustacean species with both planktotrophic and
lecithotrophic modes of larval development. In the former category, however, there is a
tendency towards a reduction of the larval phase and an increase in initial larval size (Thatje
and Bacardit, 2000; Thatje et al., 2001). More abbreviated types of larval development
typically imply lecithotrophy, often associated with behavioural changes such as demersal
drifting rather than active planktonic swimming. Such patterns are typical for decapods in
the Magellan region (Thatje et al., 2003a), although complete lecithotrophy was, so far,
experimentally demonstrated only in larvae of lithodid crabs from this region (e.g., Lovrich
et al., 2003).
Future research should focus on early life histories of Antarctic shrimp species, which
should be still more adapted to conditions of cold and food limitation (see Clarke, 1977,
1993b; Gorny and George, 1997). If typical reproductive adaptations result in a partial or
complete food-independent larval development in high latitudes, we should expect to find
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2724

large sizes and a high initial lipid content of the eggs and larvae, an abbreviated larval
development, and a high degree of endotrophy.
Acknowledgements
We are grateful to the International Bureau of the German Ministry of Research
(BMBF, Project No. IB Arg 99/002) and the Argentine Secretarı
´a Nacional para la
Tecnologı
´a, Ciencia e Inovacio
´n Productiva (SETCIP) for continuous financial support of
this bilateral co-operation during the last years. Thanks are due to Marcelo Gutierrez for
assistance in the field. Federico Tapella provided the map on the study area. This work was
partially funded by the Alfred Wegener Institute for Polar and Marine Research,
Bremerhaven, Germany. The improvements of an earlier draft by the detailed comments of
two anonymous reviewers are greatly acknowledged. [RW]
References
Abele, L.G., 1982. Biogeography. In: Abele, L.G. (Ed.), The Biology of Crustacea: 1.1. Systematics, the Fossil
Record and Biogeography. Academic Press, New York, pp. 242– 304.
Anger, K., 1987. The D
o
threshold: a critical point in the larval development of decapod crustaceans. J. Exp. Mar.
Biol. Ecol. 108, 15 – 30.
Anger, K., 1998. Patterns of growth and chemical composition in decapod crustacean larvae. Invertebr. Reprod.
Dev. 33, 159 – 176.
Anger, K., Moreira, G.S., Ismael, D., 2002. Comparative size, biomass, chemical composition (C, N, H) and
energy concentration of caridean shrimp eggs. Invertebr. Reprod. Dev. 32, 83 – 93.
Arntz, W.E., Brey, T., Gerdes, D., Gorny, M., Gutt, J., Hain, S., Klages, M., 1992. Patterns of life history and
population dynamics of benthic invertebrates under the high Antarctic conditions of the Weddell Sea. In:
Colombo, G., Ferrari, I., Ceccherelli, V.U., Rossi, R. (Eds.), Marine Eutrophication and Population Dynam-
ics: Proceedings of the 25th European Marine Biology Symposium. Olsen & Olsen, Fredensborg, Denmark,
pp. 221 – 230.
Bauer, R.T., 1989. Continuous reproduction and episodic recruitment in nine shrimp species inhabiting a tropical
seagrass meadow. J. Exp. Mar. Biol. Ecol. 127, 175– 187.
Briggs, J.C., 1995. Global Biogeography Elsevier, Amsterdam.
Clarke, A., 1977. A preliminary investigation of the lipids of Chorismus antarcticus (Pfeffer) (Crustacea,
Decapoda) at South Georgia. In: Llano, G.A. (Ed.), Adaptations within Antarctic Ecosystems. Proceedings
of the 3rd SCAR Symposium of Antarctic Biology. Smithsonian Institution, Washington, DC, pp. 343– 350.
Clarke, A., 1982. Temperature and embryonic development in polar marine invertebrates. Int. J. Invertebr.
Reprod. 5, 71 – 82.
Clarke, A., 1987. Temperature, latitude and reproductive effort. Mar. Ecol. Prog. Ser. 38, 89 – 99.
Clarke, A., 1993a. Reproductive trade-offs in caridean shrimps. Funct. Ecol. 7, 411– 419.
Clarke, A., 1993b. Egg size and egg composition in polar shrimps (Caridea; Decapoda). J. Exp. Mar. Biol. Ecol.
168, 189 – 203.
Clarke, A., Lakhani, K.H., 1979. Measures of biomass, moulting behaviour and the pattern of early growth in
Chorismus antarcticus (Pfeffer). Bull. - Br. Antarct. Surv. 47, 61– 68.
Gorny, M., 1999. On the biogeography and ecology of the Southern Ocean decapod fauna. Sci. Mar. 63 (Suppl.
1), 367 – 382.
Gorny, M., George, M.R., 1997. Oocyte development and gonad production of Nematocarcinus lanceopes
(Decapoda: Caridea) in the eastern Weddell Sea, Antarctica. Polar Biol. 17, 191 – 198.
Gorny, M., Arntz, W.E., Clarke, A., Gore, D.J., 1992. Reproductive biology of caridean decapods from the
Weddell Sea. Polar Biol. 12, 111 – 120.
Gorny, M., Brey, T., Arntz, W., Bruns, T., 1993. Growth, development and productivity of Chorismus antarcticus
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 25

(Pfeffer) (Crustacea: Decapoda: Natantia) in the eastern Weddell Sea, Antarctica. J. Exp. Mar. Biol. Ecol. 174,
261 – 275.
Kirkwood, J.M., 1984. A guide to the Decapoda of the Southern Ocean. ANARE Res. Notes 11, 1 – 47.
Lovrich, G.A., 1999. Seasonality of larvae of Brachyura and Anomura (Crustacea Decapoda) in the Beagle
Channel, Argentina. Sci. Mar. 63 (Suppl. 1), 347 – 354.
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.
Pe
´rez-Barros, P., Tapella, F., Romero, M.C., Calcagno, J.A., Lovrich, G.A., in press. Benthic decapod crusta-
ceans associated to captures of Munida spp. (Decapoda: Anomura) in the Beagle Channel, Argentina. Sci.
Mar.
Pike, R.B., Williamson, D.I., 1966. The first zoeal stage of Campylonotus rathbunae Schmitt and its bearing on the
systematical position of the Campylonotidae (Decapoda, Caridea). Trans. R. Soc. N. Z., Zool. 7, 209– 213.
Reid, D.M., Corey, S., 1991. Comparative fecundity of decapod crustaceans: III. The fecundity of fifty-three
species of Decapoda from tropical, subtropical, and boreal waters. Crustaceana 61, 308 – 316.
Sokal, R.R., Rohlf, F.J., 1995. Biometry, The Principles and Practice of Statistics in Biological Research.
Freeman, New York, pp. 1 – 887.
Tapella, F., Lovrich, G.A., Romero, M.C., Thatje, S., 2002. Reproductive biology of the crab Munida subrugosa
(Decapoda: Anomura: Galatheidae) in the Beagle Channel, Argentina. J. Mar. Biol. Assoc. U.K. 82, 589– 595.
Thatje, S., 2003. Campylonotus arntzianus, a new species of the Campylonotidae (Crustacea: Decapoda: Caridea)
from the Scotia Sea (Antarctica). Polar Biol. 26, 242 – 248.
Thatje, S., Bacardit, R., 2000. Morphological variability in larval stages of Nauticaris magellanica (A. Milne
Edwards, 1891) (Decapoda: Caridea: Hippolytidae) from South American waters. Bull. Mar. Sci. 66,
375 – 398.
Thatje, S., Lovrich, G.A., 2003. Decapodid and early juvenile development in the protandrous shrimp Campy-
lonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea), with notes on larval morphology. J. Mar. Biol.
Assoc. U.K. 83 (1), 103 – 109.
Thatje, S., Mutschke, E., 1999. Macrofauna bento
´nica muestreada con un Reineck box corer. Resultados Crucero
Cimar-Fiordo 3 Comite Oceanogra
´f. Nac. Valparaı
´so, Chile, pp. 126– 128.
Thatje, S., Bacardit, R., Romero, M.C., Tapella, F., Lovrich, G.A., 2001. Description and key to the zoeal stages
of the Campylonotidae (Decapoda, Caridea) from the Magellan Region. J. Crustac. Biol. 21, 492– 505.
Thatje, S., Lovrich, G.A., Torres, G., Hagen, W., Anger, K., in press. Changes in biomass, lipid, fatty acid and
elemental composition during the abbreviated larval development of the subantarctic shrimp Campylonotus
vagans. J. Exp. Mar. Biol. Ecol.
Thatje, S., Calcagno, J.A., Lovrich, G.A., Sartoris, F.J., Anger, K., 2003a. Extended hatching periods in the
Subantarctic lithodid crabs Lithodes santolla and Paralomis granulosa (Crustacea: Decapoda). Helgol. Mar.
Res. 57, 110– 113.
Thatje, S., Schiel, S., Arntz, W.E., 2003b. Developmental trade-offs in Subantarctic meroplankton communities
and the enigma of low decapod diversity of high southern latitudes. Mar. Ecol. Prog. Ser. 60, 195– 207.
Tiefenbacher, L., 1990. Eualus kinzeri, a new hippolytid shrimp from the Weddell Sea (Antarctica) (Crustacea:
Decapoda: Natantia). Spixiana 13, 117– 120.
Torti, M.R., Boschi, E.E., 1973. Nuevos aportes al conocimiento de los crusta
´ceos deca
´podos Caridea del genero
Campylonotus Bate, 1888. Physis, Secc. A, Buenos Aires 32, 65 – 84.
Wehrtmann, I.S., Albornoz, L., 1998. Larval development of Nauticaris magellanica (A. Milne Edwards, 1891)
(Decapoda: Caridea: Hippolytidae), reared under laboratory conditions. Bull. Mar. Sci. 62, 45 – 72.
Wehrtmann, I.S., Albornoz, L., 2003. Morphological variability in the development of laboratory-reared Nauti-
caris magellanica (Decapoda: Caridea: Hippolytidae) larvae, with comparison to larvae collected from the
plankton. J. Mar. Biol. Ass. U.K. 83, 949 – 957.
Wehrtmann, I.S., Kattner, G., 1998. Changes in volume, biomass, and fatty acids of developing eggs in Nauti-
caris magellanica (Decapoda: Caridea): a latitudinal comparison. J. Crustac. Biol. 18, 413 – 422.
Wehrtmann, I.S., Lardies, M.A., 1996. Species composition and geographical distribution of caridean shrimps
(Decapoda: Caridea). In: Arntz, W., Gorny, M. (Eds.), Cruise Report of the Joint Chilean– German – Italian
Magellan ‘‘Victor Hensen’’ Campaign in 1994. Rep. Polar Res. 190, 63 – 67.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–2726

Wehrtmann, I.S., Lardies, M.A., 1999. Egg production of Austropandalus grayi (Decapoda, Caridea, Pandalidae)
from the Magellan region, South America. Sci. Mar. 63 (Suppl. 1), 325 – 331.
Yaldwyn, J.C., 1965. Antarctic and subantarctic decapod crustacea. In: van Mieghem, J., van Oye, P. (Eds.),
Biogeography and Ecology in the Antarctic. W. Junk Publ., The Hague, pp. 324 – 332.
Yaldwyn, J.C., 1966. Protandrous hermaphroditism in decapod prawns of the families Hippolytidae and Cam-
pylonotidae. Nature 209, 1366.
S. Thatje et al. / J. Exp. Mar. Biol. Ecol. 301 (2004) 15–27 27