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MARINE ECOLOGY PROGRESS SERIES
Mar Ecol Prog Ser
Vol. 260: 195–207, 2003 Published September 30
INTRODUCTION
The Southern Ocean decapod fauna still provides one
of the most conspicuous unsolved mysteries in marine
biodiversity research, with an Antarctic decapod fauna
of only about a dozen caridean shrimp representatives
compared with more than 120 benthic and pelagic de-
capod species in the circumpolar antiboreal environ-
ment north of the Antarctic Convergence (Gorny 1999).
Apart from a few species of lithodid crabs in the deeper
waters off the Antarctic continental shelf (Macpherson
1988, Klages et al. 1995, Arana & Retamal 2000),
caridean shrimps represent the only decapod infra-
order which endures the high Antarctic regime of very
low temperatures combined with a marked seasonality
of primary production (Clarke 1988).
The absence of reptant decapods, in particular
brachyuran crabs, from polar environments of both
hemispheres was recently discussed to be predomi-
nantly due to physiological constraints, i.e. the failure
of adults to control high Mg
2+
concentrations in their
haemolymph, which in combination with low tempera-
© Inter-Research 2003 · www.int-res.com*Email: sthatje@awi-bremerhaven.de
Developmental trade-offs in Subantarctic
meroplankton communities and the enigma of
low decapod diversity in high southern latitudes
S. Thatje*, S. Schnack-Schiel, W. E. Arntz
Alfred Wegener Institute for Polar and Marine Research, PO Box 120 161, 27515 Bremerhaven, Germany
ABSTRACT: Developmental modes, occurrence and distribution patterns of invertebrate larvae were
studied in the Subantarctic Magellan region of South America on the basis of quantitative plankton
hauls obtained during the ‘Victor Hensen’ campaign in November 1994. The meroplankton commu-
nity was found to be numerically dominated by decapod crustacean larvae (47%), followed by poly-
chaetes (20%), echinoderms (16%), cirripedes (8%) and molluscs (7%). A rich decapod community
was detected, with 2 thalassinid, 5 brachyuran, 4 anomuran, 6 caridean, 1 astacid and 1 palinurid
species/morphotypes identified. Cluster analyses clearly distinguished deep-water stations (250 to
400 m) south of the Straits of Magellan from shallow-water stations (30 to 100 m) in the Beagle
Channel, where meroplankton was dominated by decapod larvae (>90%). Three main larval
developmental modes, characterised by morphogenesis, mode of larval nutrition and site of larval
development, were observed in Magellan decapods: (1) Extended, planktotrophic development of
planktonic larvae; (2) abbreviated, planktotrophic development of planktonic larvae; and (3) abbre-
viated, endotrophic (lecithotrophic) development of demersally living larvae. Several caridean
shrimps with abbreviated larval development, which have congeners in the Antarctic, suggest a
strong synchronisation between abbreviated planktotrophic larval development and short periods
of primary production. This seems to be an essential factor in early life history adaptation for the
colonisation of the Antarctic environment. The impoverished Antarctic decapod fauna, with only a
few representatives of caridean shrimp species left, may be related to the lack in flexibility of reptant
decapods in distributing energy resources between adults and their offspring, which would allow
abbreviated planktotrophic larval development.
KEY WORDS: Decapoda · Reproductive strategies · Southern Ocean · Abbreviated larval
development · Magellan region · Antarctic
Resale or republication not permitted without written consent of the publisher
Mar Ecol Prog Ser 260: 195–207, 2003
tures, leads to a paralysing condition affecting all kinds
of behaviour (Frederich et al. 2001). However, this
explanation of physiological constraints on ecological
demands alone cannot explain the observed decapod
biodiversity patterns, since at least lithodid (anomuran)
crabs have been shown to respond to physiological con-
straints in the cold by life history adaptation of both
adults and larvae (see Anger et al. 2003, Lovrich et al.
2003, Thatje et al. 2003). In an attempt to elucidate the
reason for the impoverished decapod fauna in high
latitudes, we revisited Thorson’s old ecological concept
(Thorson 1936, 1950), which, in summary, argues that
the mismatch between a marked seasonality of primary
production (i.e. food availability) and prolonged lar-
val developmental times due to low temperatures at
high latitudes, should strongly select against plankto-
trophic larval development (see Mileikowsky 1971,
who created the term ‘Thorson’s rule’, Clarke 1988,
Pearse et al. 1991, Arntz & Gili 2001).
In this study, we present information on develop-
mental trade-offs in early life history of benthic deca-
pod crustaceans from the Magellan region and the
position of decapod larvae within the Subantarctic
meroplankton community. This information is aug-
mented by literature data, including findings on early
life history adaptation of Antarctic shrimps to a cold
and seasonally food-limited environment.
MATERIALS AND METHODS
Sampling and sample treatment. Quantitative mero-
plankton samples were obtained during the Joint
Chilean-German-Italian Magellan ‘Victor Hensen’
Campaign to the channel and fjord system
of the cold-temperate Subantarctic Magel-
lan region (Fig. 1) from 12 to 24 November
1994 (see also Arntz & Gorny 1996, Defren-
Jansen et al. 1999). Zooplankton samples
were obtained using a multiple opening-
closing net of 300 µm mesh size. Daytime
vertical hauls were conducted from the
seafloor or 400 m maximum wire length to
the surface, covering standard depth inter-
vals (see Figs. 6 & 7). Zooplankton samples
were directly preserved in 4% borax-
buffered formaldehyde seawater solution,
and later in the laboratory split into two.
Assuming 100% filtering efficiency of
the multinet for meroplankton, the filtered
volume was calculated by multiplying the
vertical distance of the tow by the mouth
area of the net (0.25 m
2
).
Species identification and larval devel-
opmental mode. The meroplankton frac-
tion was sorted only from one part of the sample, and
identified to the most resolved taxonomic level pos-
sible. Special focus was given to species determination
of decapod crustacean larvae as well as their develop-
mental stages (for literature used for larval identifica-
tion see Table 2). To detect relevant developmental
patterns in decapod larvae, we distinguished 3 larval
developmental modes, characterised as follows (for
review see Williamson 1982, Anger 2001):
(1) Morphogenesis
• Extended larval development — number of instars
typical of the family/genus.
• Abbreviated larval development — comprises a con-
siderable reduction in larval instars compared with
typical trait of family/genus representatives from
lower latitudes and/or intraspecific changes with
latitude/temperature regime.
(2) Mode of larval nutrition
• Planktotrophic larval development — most of the
larval development requires actively feeding plank-
tonic larvae. This may include partial utilisation of
energy reserves of maternal origin in an early stage
of development.
• Lecithotrophic larval development — complete endo-
trophic larval development (complete lecithotrophy)
with planktonically and/or demersally living larvae.
(3) Site of larval development
• Planktonic larval development — larval develop-
ment is spent mostly in the water column.
• Demersal larval development — larval development
is predominantly epibenthic.
Cluster analyses. We used the software package
PRIMER (Plymouth Routines in Multivariate Ecological
Research) developed at Plymouth Marine Laboratory,
196
Fig. 1. Meroplankton sampling locations (black dots/station numbers) during
the Joint Chilean-German-Italian Magellan ‘Victor Hensen’ Campaign to
the Magellan region (South America) in November 1994
Thatje et al.: Decapods in Subantarctic meroplankton communities
197
Species/group Stage Station (Sampling depth, m)
1313 1309 1297 1288 1281 1265 1254 1244 1238 1222 1212 1211 1196 1185 1202
(340) (250) (380) (400) (340) (400) (270) (30) (100) (30) (50) (50) (100) (100) (30)
Bryozoa Cyphonautes 227 – 310 1240 44 47 55 7 4 13 5 – 24 4 –
Cirripedia Nauplius 458 75 298 1291 2020 64 2445 27 108 480 10 – 468 16 53
Gastropoda Veliger 202 25 268 1262 100 42 18 20 244 120 35 50 28 28 133
Bivalvia Veliger 376 13 1055 2113 24 – 3 – 4 7 5 – 4 – –
Polychaeta Larvae 5489 1110 5093 2793 1267 298 613 120 372 193 65 5 416 248 67
Ophiuroidea Ophiopluteus 702 65 755 1060 529 56 1370 – – – – – – – –
Juvenile – 93 – – – 58 – – – – – – – – –
Asteroidea Brachiolaria 751 25 610 564 84 – 135 – – – – – 8 – –
Echinoidea Echinopluteus 3051 625 2413 853 451 129 1210 – 12 – – – 36 – –
Decapoda
Thalassinidea
Notiax sp. (?) Zoea 1 – – – – – – 30 1440 9224 20 35 30 6424 3756 240
Zoea 2 – – – – – – – 127 3076 – – – 520 1808 13
Upogebia sp. Decapodid – – – – – – – 7 – – – – – 8 –
Brachyura
Pinnotheridae Early zoea 4 – – 2 – – 3 100 – – – – – 36 –
Libidoclaea granaria Zoea 1 – – – – – – – 7 – – – – – – –
Eurypodius latreillei Early zoea 69 150 255 231 27 82 128 3107 304 – 80 35 504 184 –
Adv. zoea 76 148 188 598 120 44 90 1100 68 – 40 15 68 24 –
Peltarion spinosulum Zoea 1 – – 13 – – – 13 – 4 133 – 5 4 – 147
Zoea 2 – – – – – 7 – – 8 33 – – – – 7
Halicarcinus planatus
Zoea 1 – – – 36 – – – 53 – – 5 – 8 12 –
Zoea 2 – – – – – – – – – – – – 4 – –
Anomura
Pagurus spp. Zoea 1 – – – 11 – – – 160 12 20 25 20 4 72 –
Zoea 2 – – – – – 11 – 247 16 – 60 100 12 20 –
Zoea 3 – – – 67 – – 13 240 76 33 35 50 20 8 7
Zoea 4 11 28 25 213 – – – 293 52 20 90 100 152 16 20
Megalopa – 13 – 33 – – – 147 20 13 10 20 36 28 47
Parapagurus Early zoea – – – – – – – – – – – 5 20 4 –
dimorphus (?) Adv. zoea – – – – – – – – – – – – – 8 –
Munida spp. Zoea 1 – – – – – 11 10 647 344 20 30 5 96 76 7
Zoea 2 – – – – – – – 320 892 7 20 – 40 44 7
Zoea 3 2 – – – – – – 173 8 40 5 65 4 – 7
Zoea 4 – – – – – – 35 147 260 13 70 10 132 20 13
Megalopa – – – – – – – 80 – 7 – – – – –
Caridea
Betaeus truncatus Zoea 1 – – – – – – – – – 7 – – – – –
Eualus dozei Zoea 1 – – – – – – – 7 – – – – – – –
Campylonotus vagans
Zoea 1 – – – – – – – – – – 10 – – – –
Zoea 2 – – – – – – – – – – 10 – 8 – –
Decapodid – – – – – – – – – – – – – 40 –
C. semistriatus Decapodid 22 – – – – – – – – – – – – – –
Nauticaris magellanica
Zoea 1 – – – 31 – – 3 – 12 – 5 – 28 – 7
Zoea 2 – – – – – – 13 – 16 – – – 4 – 7
Zoea 3 – – – – – – – – – – – – 4 – –
Zoea 4 4 – – – – – – – – – 10 – – – –
Zoea 5 – – – – – – – – – – – – 4 – –
Decapodid 11 – – 22 – – – – – – – – 4 – –
Austropandalus grayi Zoea 1 – – – – 4 22 8 – 12 – 5 – 16 32 –
Zoea 2 – – – 22 – 22 – 7 4 – – – 8 16 –
Zoea 3 – – – 89 – – – 7 4 – – – – 8 7
Zoea 4 – 38 – 311 11 – – 13 – 7 – – – 4 –
Zoea 5 – – – 122 4 – – – 60 – – – – – 7
Decapodid – 3 – 111 – 13 – – – – – 10 – 4 –
Astacidea
Thymops birsteini Decapodid – 13 – – – 22 – – 8 – – – – – –
Palinura
Stereomastis (suhmi ?)
Early zoea – – – – 22 – – 7 – – – – – 8 –
Adv. zoea – – – – 22 – – – – – 10 – – – –
Sum 11 455 2424 11 283 13 075 4729 928 6195 8610 15 224 1196 665 525 9108 6532 796
Table 1. Station means (ind. m
–3
) of meroplankton taxa found in the channel and fjord system of the Subantarctic Magellan region during
the Joint Chilean-German-Italian ‘Victor Hensen’ Campaign in November 1994 (adv. = advanced). (?) Species identification not certain
Mar Ecol Prog Ser 260: 195–207, 2003
UK. The hierarchical agglomerate cluster method
(Clarke & Gorley 2001) was applied on the basis of
abundance means per station to differentiate mero-
plankton communities utilising the Bray-Curtis simi-
larity index. Data were previously log(x+1) transformed
to remove the bias of highly abundant taxa.
RESULTS
Meroplankton composition and distribution pattern
The average spring meroplankton community found
in the Magellan region is characterised by highly
variable abundances (Table 1) and an overwhelming
amount of crustaceans, namely decapod and cirripede
larvae, contributing 47 and 8% to overall abundance
means, respectively (Table 1, Fig. 2A). Polychaete
larvae ran second (20%) followed by echinoderms
(16%); molluscs and bryozoans had much lower frac-
tions (Fig. 2A). Within the decapod fraction, thalassinid
larvae were found to be most abundant (62%), fol-
lowed by brachyurans (20%) and anomurans (15%)
(Fig. 2B). Caridean shrimp larvae, Astacidea and Pali-
nura were of minor importance (Fig 2B). Also, in terms
of species/morphotype richness, decapods were the
dominant group within the meroplankton, with 2 tha-
lassinid, 1 astacid, 1 palinurid, 5 brachyuran, 4 anomuran
and 6 caridean species distinguished (the 2 pagurid
species Pagurus forceps and P. comptus are combined
as Pagurus spp., due to the lack of knowledge of the
complete larval development in P. forceps; S. Thatje &
G. Lovrich unpubl. data). Species determination of all
other groups was complicated by the lack of adequate
taxonomic keys, and therefore species richness must
be considered as a minimum estimate on the basis of
distinguished morphotypes: 3 bivalve, 2 gastropod, 2
to 4 ophiuroid, 1 echinoid, 1 cirripede and 1 bryozoan
morphotypes were found. Polychaetes were more di-
verse, but remain to be further taxonomically identi-
fied. However, in relation to abundance, spionid larvae
were the most dominant taxon (>60%).
Cluster analyses of the meroplankton composition re-
vealed 2 groupings at the 55% similarity level (Fig. 3).
Group 1 comprises shallow-water stations with depths
varying from 30 to 100 m (Table 1) at the eastern
entrance of the Beagle Channel, including Stn 1202 off
Isla Wollaston (Fig. 1, Stns 1185 to 1244). Group 2 com-
198
Fig. 2. Relative abundance of meroplankton fractions found
in the channel and fjord system of the Magellan region in
November 1994. Given on the basis of (A) major taxonomic
groups and (B) decapod infraorder
Fig. 3. Cluster dendrogramm (Bray-Curtis similarity) showing
classification of meroplankton stations on the basis of
abundance means
Thatje et al.: Decapods in Subantarctic meroplankton communities
bines 7 deep-water stations on a transect from the
Straits of Magellan south to the Beagle Channel, with
depths varying from 250 to 400 m (Figs. 1 & 3, Table 1).
Shallow-water stations are overwhelmingly domi-
nated by decapods (91%, Fig. 4C) of which thalassinid
larvae are most important (68%, Fig. 4D), followed by
brachyuran (16%) and anomuran larvae (15%). Poly-
chaete, cirripede and gastropod larvae contribute with
only 4, 3 and 2%, respectively (Fig. 4C). Deep-water
stations showed a more heterogeneous meroplankton
composition (Fig. 4A), with polychaetes contributing
33%, followed by echinoderms (27%), cirripedes (13%),
decapods (12%), bivalves (7%), gastropods (4%) and
bryozoans (4%). The generally less important decapod
fraction is dominated by brachyuran crab larvae (61%),
carideans (24%) and anomurans (12%, Fig. 4B).
The meroplankton composition on a transect of deep-
water station from the Straits of Magellan southward to
the Beagle Channel differed totally from that of shallow-
water stations (Figs. 1 & 5). Here, polychaetes and echi-
noderms were the dominant taxa. Only Stns 1281 and
1254 showed a percentage of cirripede larvae untypical
of deep-water stations, although they were very similar
in their taxonomic composition, despite the lack of echin-
oderms, to Stn 1222 from the eastern entrance of the
Beagle Channel. The numerical dominance of decapod
larvae at the shallow-water stations is correlated with a
mass-occurrence of thalassinid larvae at almost all sta-
tions (Fig. 5A,B). At shallow-water stations, in contrast to
deep-water stations, anomuran larvae were pro-
portionally dominant over brachyuran larvae (Fig. 5B).
Vertical distribution of larvae
At some stations with a strong thermocline, a
concentration of meroplanktonic larvae was found
(Stns 1254, 1281, 1288, Fig. 6). This holds true espe-
cially for cirripede nauplii and echinoderm larvae
(Fig. 6), which were concentrated in the thermocline.
199
Fig. 4. Relative abundance of meroplankton fractions found in the channel and fjord system of the Magellan region in November
1994. Comparison of deep-water station means (A,B) with that of shallow-water stations. Given on the basis of (A,C) major
taxonomic groups, (B,D) decapod infraorder
Mar Ecol Prog Ser 260: 195–207, 2003200
Fig. 5. Relative abundance of meroplankton fractions found at each station sampled in the Magellan region in November 1994.
Given on the basis of (A) major taxonomic groups, (B) decapod infraorder
Fig. 6. Vertical distribution of echinoderm and cirripede larvae at Stn 1281. Dotted line = thermocline (at 70 to 80 m water depth,
see Antezana et al. 1996)
Decapod larvae presented a distinct distribution: tha-
lassinid larvae (Notiax sp.) were found in conspicuous
numbers demersally just above the seafloor (Fig. 7),
especially in an advanced stage of larval development.
The brachyuran Eurypodius latreillei and the caridean
Austropandalus grayi were found in high abundances
at Stn 1288, which presented a strong thermocline
(Fig. 7, see also Antezana et al. 1996). All larval stages
of these 2 species were found below the thermocline,
but only in the case of A. grayi did their distribution
extend to the seafloor (Fig. 7). A very similar pattern to
E. latreillei was found for larvae of Munida spp. and
Notiax spp. (Fig. 7) at Stn 1238. Data on temperature
and salinity are not available from this station, and
therefore it is not known whether a well-developed
thermocline was present there.
Developmental modes in decapod larvae
Three basic criteria of (1) morphogenesis, (2) mode
of larval nutrition and (3) site of larval develop-
ment were applied to characterise developmental
modes in decapod larvae (cf. ‘Materials and meth-
ods’). Independent of decapod infraorder, 3 basic lar-
val developmental patterns were detected for the
Magellan and south-western Atlantic decapod fauna
(Table 2).
• Extended, planktotrophic development of plank-
tonic larvae
• Abbreviated, planktotrophic development of plank-
tonic larvae
• Abbreviated, lecithotrophic development of dem-
ersally living larvae.
201
Fig. 7. Vertical distribution of selected decapod taxa from different sampling stations; Notiax sp. (Stn 1238), Munida spp.
(Stn 1238), Eurypodius latreillei (Stn 1288), Austropandalus grayi (Stn 1288). Dotted line = thermocline (at 80 to 90 m water depth,
see Antezana et al. 1996)
Mar Ecol Prog Ser 260: 195–207, 2003
Brachyuran crabs seem to follow a general pattern of
extended larval development, whereas caridean shrimp
genera (Chorismus, Campylonotus, Table 2), which
also have Antarctic representatives, follow an ab-
breviated larval development. Complete endotrophy
in abbreviated larval development has so far only
been recorded in lithodid crabs from the study area
(Table 2).
DISCUSSION
Sampling method and identification of decapod
larvae
Among several key ecological problems in high lati-
tude marine larval biology is the general lack of early
life history studies in marine invertebrates (but see
202
Species/Group Duration Nutrition Habitat Source
Extend- Abbre- Plankto- Lecitho- Plank- Demer-
ed viated trophic trophic tonic sal
Caridea
Campylonotus vagans Bate, 1888 x x x 28, 30
Campylonotus semistriatus Bate, 1888 x x x 28
Chorismus antarcticus (Pfeffer, 1887) x x x 6, 19
Chorismus tuberculatus Bate, 1888 x x x 26
Betaeus truncatus Dana, 1852 ? x x 1, 29
Eualus dozei (A. Milne Edwards, 1891) ? 1
Nauticaris magellanica A. Milne Edwards, 1891 x x x 1, 27, 33, 34
Austropandalus grayi (Cunningham, 1871) x x x 25
Palinura
Stereomastis (suhmi Bate, 1878, ?) x 21
Anomura
Munida subrugosa Henderson, 1847 x x x 17, 22, 32, 35, 36
Munida gregaria (Fabricius, 1793) x x x 17, 32, 35, 36
Lithodes santolla (Molina, 1782) x x x 7, 9, 16, 18, 19
Paralomis granulosa (Jaquinot, 1847) x x x 7, 8, 10, 16, 20
Pagurus comptus White, 1847 x x x 17, 23, 24, 31
Pagurus forceps H. Milne Edwards, 1836 x x x 17, 23, 24, 31
Parapagurus (dimorphus Smith, ?) x 3, 21
Brachyura
Eurypodius latreillei Guérin, 1828 x x x 2, 4, 11, 17
Libidoclaea granaria (H. Mil. Edw. & Lucas, 1842) x x x 4, 12, 17
Halicarcinus planatus (Fabricius, 1775) x x x 5, 17
Peltarion spinosulum (White, 1843) x x x 14, 17
Pinnixia sp. ? x x 13, 17
Cancer edwardsi Bell, 1835 x x x 15
Astacidea
Thymops birsteini (Zarenkov & Semenov, 1972) ? 21
Thalassinidea
Notiax sp. (?) x21
Sources
(1) Albornoz & Wehrtmann (1997) (13) Gutierrez-Martinez (1971) (25) Thatje & Bacardit (2000a)
(2) Bacardit (1985b) (14) Iorio (1983) (26) Thatje & Bacardit (2000b)
(3) Bacardit (1985a) (15) Quintana (1983) (27) Thatje & Bacardit (2000c)
(4) Bacardit & Vera (1986) (16) Kattner et al. (2003) (28) Thatje et al. (2001)
(5) Boschi et al. (1969) (17) Lovrich (1999) (29) Thatje & Bacardit (2001)
(6) Bruns (1992) (18) Lovrich et al. (2003) (30) Thatje & Lovrich (2003)
(7) Calcagno et al. (2003a) (19) McLaughlin et al. (2001) (31) Thatje & Lovrich (unpubl.)
(8) Calcagno et al. (2003b) (20) McLaughlin et al. (2003) (32) Vera & Bacardit (1986)
(9) Campodonico (1971) (21) Present study (33) Wehrtmann & Albornoz (1998)
(10) Campodonico & Guzman (1972) (22) Roberts (1973) (34) Wehrtmann & Kattner (1998)
(11) Campodonico & Guzman (1981) (23) Scelzo & Boschi (1969) (35) Williams (1973)
(12) Fagetti (1969) (24) Scelzo (1976) (36) Williams (1980)
Table 2. Selected decapod taxa from the Magellan region and the southwestern Atlantic Ocean with partially or completely known
mode of larval development. Biogeographical information was obtained from Gorny (1999). (?) Uncertain information
Thatje et al.: Decapods in Subantarctic meroplankton communities
Pearse et al. 1991). This deficiency affects many
aspects of ecological work and the development of
ecological concepts, and only allows for broad general-
isations as to larval developmental modes in the pre-
sent study (Table 2). Sampling of meroplankton com-
munities with a plankton net of 300 µm mesh size
underestimated the true amount of invertebrate lar-
vae. This should have affected meroplankton com-
position in particular, and especially smaller larval
types, such as molluscs and echinderms, should be
underrepresented. This should reduce the real deca-
pod larval dominance to some extent. However, inver-
tebrate larvae tend to be larger in cold temperate
and polar regions (Thorson 1936, Mileikowsky 1971,
Pearse et al. 1991), and this holds especially true for
decapod larvae (Thatje & Bacardit 2000b,c, Thatje et
al. 2001). The smallest decapod larvae known from the
Beagle Channel is that of Betaeus truncatus (the Zoea
I instar has an average total length of about 3.5 mm,
see Thatje & Bacardit 2001), which was found in low
abundance in our samples, and this species is gener-
ally known to occur in minor abundances within the
benthic community (Pérez-Barros et al. in press).
All decapods which spend the greater part of their
larval development in the plankton were considered
planktotrophic, assuming that active feeding is neces-
sary at least during part of the larval development,
although development might be temporarily food inde-
pendent, relying on high initial/maternal energy sour-
ces (for a review see Anger 2001). Since endotrophic
larval development in benthic decapods tends to avoid
pelagic phases (Anger et al. 2003, Lovrich et al. 2003)
and complete lecithotrophic larval development is
scarcely reported in marine carideans, we believe our
generalisation in larval developmental modes to be a
useful tool in describing decapod reproductive pat-
terns. The definition of ‘abbreviated’ larval develop-
ment in reptants is easy to apply, since most represen-
tatives (especially brachyuran crabs) usually develop
through 4 to 6 zoeal stages and 1 megalopa stage
(Williamson 1982, Anger 2001). A great variation in
larval developmental pathways and larval instars has
been described for caridean shrimps. We considered
caridean larval developments as abbreviated when
passing through 4 or less zoeal stages only, i.e. as in the
genera Campylonotus (Thatje et al. in press) and Cho-
rismus (Bruns 1992, Thatje & Bacardit 2000b). How-
ever, it has to be considered that this is a rather
arbitrary definition of abbreviated development in
carideans, which is only based on the number of
instars, but does not take larval developmental times
into account. The larval development of Nauticaris ma-
gellanica was also considered abbreviated (Table 2), as
it was found to be reduced with increasing latitude
(5 to 6 zoeal stages found in the present study area
compared with 9 to 11 stages in central southern
Chile, Wehrtmann & Albornoz 1998, Thatje & Bacardit
2000c).
Occurrence and distribution of invertebrate larvae
The difference in faunal composition between deep-
and shallow-water stations (cf. Fig. 5) is due to the
dominance of decapod crustaceans in the semi-
enclosed hydrographic environment of the Beagle
Channel, which is known for its richness in decapods
(Gorny 1999, Pérez-Barros et al. unpubl.). Species rich-
ness in Subantarctic meroplankton is low and domi-
nated in terms of abundance and diversity by decapod
crustaceans with clear seasonal reproduction mainly
taking place in spring (Lovrich 1999). It is not certain
whether the high proportion of thalassinid larvae
found in the Beagle Channel is due to the local distrib-
ution of the few species of this infraorder known from
the area (see Thatje 2000, Thatje & Gerdes 2000), or to
a direct coupling with larval release at the Beagle
Channel stations. However, thalassinid shrimps de-
pend on muddy to sandy sediments, which are abun-
dant in the Beagle Channel, but coarser and more
heterogeneous sediments are known on the station
transect northward to the Straits of Magellan (Fig. 1)
(Brambati et al. 1991). Decapod larval development
seems to take place mainly in the midwater masses
below the thermocline (if developed), where plankton
particles are enriched, and consequently food avail-
ability is high. However, further studies are needed to
define whether larvae show a vertical migration ten-
dency, which may affect this distribution pattern.
Decapod species that develop through demersally
occurring larvae only, which are mostly of abbreviated
and food-independent development as in lithodid
crabs (McLaughlin et al. 2001, Calcagno et al. 2003a,
Kattner et al. 2003), are rarely found in plankton hauls
(Lovrich 1999).
The phylogenetic constraint of being tied to
planktotrophic larval developments
The reason why caridean shrimps are successful in
Antarctic waters has been assigned to their ability to
down-regulate high Mg
2+
concentrations in the hae-
molymph (Frederich et al. 2001); a mechanism which
functions insufficiently in reptants. Despite this physi-
ological ability to maintain activity levels in the cold
(which remains scarcely studied in larvae), carideans
show a great flexibility in larval developmental path-
ways at lower latitudes. This flexibility increases with
the number of larval instars, and enhances larval dis-
203
Mar Ecol Prog Ser 260: 195–207, 2003
persal and survival (Anger 2001). The requirements for
exogenous energy from food allowing for developmen-
tal flexibility and extended modes of larval develop-
ment should be high, as metabolic costs for additional
moults as well as energy losses with cast exuviae imply
a high degree of dependence on plankton produc-
tivity (Wehrtmann 1991, Anger 2001). Nevertheless,
the flexibility in larval developmental pathways also
allowed carideans to evolve energy saving strategies
when low temperatures and limited food availability
selected for abbreviated and partially endotrophic
modes of larval development. This has been hypothe-
sised as a latitudinal pattern in reproductive traits
in carideans such as an increase, from the equator
towards the poles, in egg size, in initial energy
reserves of eggs and larvae, and in larval size, coincid-
ing with a reduction in fecundity and in the age at first
maturity (Arntz et al. 1992, Thatje et al. in press a,b).
The need for such energy saving strategies under con-
ditions of low temperatures and a seasonally limited
primary production in high latitudes has suppressed
the extent and flexibility of developmental pathways in
caridean larvae. For instance, strongly abbreviated lar-
val developments passing invariably through only 2 or
4 larval instars in the sub- and high Antarctic genera
Campylonotus and Chorismus, respectively (Table 2)
(Bruns 1992, Thatje & Bacardit 2000b, Thatje et al. in
press a), combined with high larval resistance to star-
vation, especially in the Zoea 1 instar (Thatje et al. in
press a,b), allow for an enhanced synchronisation with
short and pulsed periods of primary production, and
simultaneously reduce the degree of larval depen-
dence on planktonic food sources (Clarke 1988, Anger
et al. 2003). Similar early life history adaptations are
known also from the Antarctic crangonid Notocrangon
antarcticus (Bruns 1992). In the high Antarctic Weddell
Sea, carideans are able to spawn only every second
year (Arntz et al. 1992, Gorny et al. 1992, Gorny &
George 1997), suggesting a lack of sufficient energy
supply to female reproduction, due to short periods of
primary production during summer, which may be
insufficient for the level of somatic growth allowing for
an annual reproductive cycle (Clarke 1982). In polar
environments, the mismatch between energy avail-
ability and high costs for female energy investment
into large embryos might thus have selected against
complete lecithotrophy in caridean larval develop-
ment. On the other hand, complete endotrophic larval
development of pelagic larvae is rare in marine
caridean shrimps (although frequently recorded in
shrimps from limnic systems, especially Palaemonidae,
cf. Magalhães 1988, Odinetz Collart & Magalhães
1994), which may indicate a phylogenetic constraint
for the evolution of lecithotrophic developments in
the sea. One known exception, which should be men-
tioned here, is the Subarctic Sclerocrangon boreas,
which has a direct and abbreviated (lecithotrophic)
development of benthic larvae, including a high degree
of parental care (Makarov 1968, Miglavs 1992).
In general, brachyuran crabs have an extended
planktotrophic mode of larval development. Cases of
an abbreviated development or flexibility in the num-
ber of instars have usually been observed under condi-
tions of physiological stress (Anger 2001) and as spe-
cial adaptations to breeding in land-locked limnic or
terrestrial habitats (Montú et al. 1990, Anger & Schuh
1992, Anger 2001). An abbreviated larval develop-
ment in some endemic terrestrial grapsoid crabs from
Jamaica, for instance, has been shown to be a recent
evolutionary adaptation to semi-terrestrial or terres-
trial life (Schubart et al. 1998), which evolved only
about 4 million years ago (for a discussion see Anger
2001). Resistance of brachyuran larvae to starvation is
generally low, and examples of larval exposure to low
temperatures have indicated that the use of energy
sources is hampered by metabolic disturbance below
critical temperatures (Anger et al. 1981, Pörtner 2002).
The inability of most reptant decapods to suppress the
number of larval stages should therefore have selected
against their occurrence in high latitudes when the
Antarctic region began to become cooler (Clarke
1990). However, one family of anomuran crabs, the
lithodid crabs, which in evolutionary terms evolved
quite recently, developed complete endotrophic larval
development of demersal larvae. They evolved from
hermit crab ancestors (Cunningham et al. 1992, this
phylogenetic relation is the subject of recent contro-
versial discussion, see also McLaughlin & Lemaitre
2000), and were recorded for the first time between 13
to 25 million years ago, when other much older
brachyuran and anomuran taxa (hermit crabs evolved
more than 150 million years ago, Cunningham et al.
1992 and references therein) were already extinct in
high southern latitudes due to Antarctic cooling (Zins-
meister & Feldmann 1984, Feldmann & Tshudy 1989).
Lithodid crabs from the Magellan region (Paralomis
granulosa, Lithodes santolla) developed special adap-
tations in life history, such as prolonged brooding of
egg masses and, most importantly, complete leci-
thotrophy in larval development, which allowed for
adaptation to ecological and physiological constraints
in high latitudes (Frederich et al. 2001, Anger et al.
2003, Lovrich et al. 2003, Thatje et al. 2003). This evo-
lutionarily young taxon of anomuran crabs, which is
represented by several species in high latitudes of both
hemispheres and also appears to be a common deep-
sea representative (Anger et al. 2003 and references
therein), is obviously about to release itself from the
apparent phylogenetic constraints that have prevented
reptants from conquering the polar marine realm as a
204
Thatje et al.: Decapods in Subantarctic meroplankton communities
life habitat (Macpherson 1988, Klages et al. 1995,
Arana & Retamal 2000). We suggest a similar recent
evolutionary trait to be responsible for abbreviated lar-
val developments in spider crabs (Majidae), which are
already present in both the Subarctic (e.g. Hyas ara-
neus, Dyer 1985) and the Subantarctic (Eurypodius
latreillei). Eurypodius latreillei Guerin, which at pre-
sent is the southernmost known spider crab in the
southern hemisphere, was recently confirmed to occur
in waters off South Georgia (Romero et al. 2003). The
Majidae are suggested as further possible recolonisers
of the Polar marine realm.
Acknowledgements. We would like to thank the crew of
the German RV ‘Victor Hensen’ for assistance at sea. Tanja
Joschko and Mario Hubo helped in separating the mero-
plankton fraction. Claudio Richter (ZMT, Bremen) kindly pro-
vided the plankton samples. The authors would like to thank
Klaus Anger and Gustavo Lovrich as well as Ingo Wehrtmann
and 3 anonymous reviewers for critically commenting on
the manuscript. Thanks are due to Ruth Alheit for her revision
of the English.
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Editorial responsibility: Otto Kinne (Editor),
Oldendorf/Luhe, Germany
Submitted: April 23, 2003; Accepted: July 15, 2003
Proofs received from author(s): September 4, 2003
