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Comparative size, biomass, elemental composition
(C, N, H), and energy concentration of caridean
shrimp eggs
KLAUS ANGER a , GLORIA S. MOREIRA b & DEBORAH ISMAEL b
a Biologische Anstalt Helgoland, Stiftung Alfred-Wegener-Institut für Polar-und
Meeresforschung, Meeresstation, 27498, Helgoland, Germany Phone: +49 (4725)
819-348 Fax: +49 (4725) 819-348 E-mail: kanger@awi-bremerhaven.de
b Universidade de São Paulo (USP), Instituto de Biociências, Caixa Postal 11.461, CEP
05422-970, São Paulo, SP, Brazil
Available online: 01 Dec 2010
To cite this article: KLAUS ANGER, GLORIA S. MOREIRA & DEBORAH ISMAEL (2002): Comparative size, biomass,
elemental composition (C, N, H), and energy concentration of caridean shrimp eggs, Invertebrate Reproduction &
Development, 42:2-3, 83-93
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Invertebrate Reproduction and Development,
42:2-3 (2002) 83-93
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0168-8170/02/$05.00
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2002 Balaban
83
Comparative size, biomass, elemental composition
(C,
N,
H),
and
energy concentration
of
caridean shrimp eggs
KLAUS ANGER'., GLORIA
S.
MOREIRA2
and
DEBORAH ISMAEL2
'Biologische Anstalt Helgoland, Stiftung Aped- Wegener-Institutfirr Polar- und Meeresforschung,
Meeresstation, 2 7498 Helgolad, Germany
Tel. +49 (4725) 819-348;
Far
+49 (4725) 819-369; email:
kanger@awi-bremerhaven.de
'Universidade
de
Sio
Paul0 (USP), Instituto
de
Biocitkias, Caixa Postal 11.461, CEP 05422-970
SZo
Paulo, SP, Brazil
Received 20 May 2002; Accepted
3
1
October 2002
Summary
In the evolution of decapod crustaceans, interspecific variation in egg size is considered as an
important life-history trait that is linked with the duration of embryonic and larval development,
the number and type of larval stages, and with juvenile size. Aiming to provide a quantitative
characterization of reproductive traits in related decapod
taxa
differing in lifestyle (freshwater,
estuarine, marine) and geographic-climatic distribution (tropical-temperate), we compared
size,
biomass, and elemental composition of eggs of caridean shrimps from three families: seven
species of Palaemonidae (three congeners of
Macrobrachium:
M.
olfesii, M. carcinus,
M.
acanthurus;
four species of
Palaemon: P. northropi, P. pandaliformis, P. elegans, P.
adrpersus),
two
Atyidae
(Potimirim potimirim, Atya scabra),
and one Pandalid
(Pandalus
montagui).
Egg size was measured
as
larger and smaller diameter
(DI,
DJ,
volume was
calculated fiom
D,
and
Dz,
and biomass was measured
as
dry
mass
(W),
carbon
(C),
nitrogen
(N),
hydrogen
(H),
and energy
(E,
estimated from
C)
contents. The smallest size and lowest
biomass were found in the eggs of
two
freshwater atyids (both originating from Brazil); the
largest size occurred in a marine species,
P. montagui
(from the
North
Sea); and intermediate
values in freshwater, estuarine, and marine palaemonid species (from Brazil and the Baltic
Sea,
respectively). Among the
Palaemon
species, the most limnic
(P. pandaliformis)
showed a
significantly larger
egg
size and volume
(P<O.OOl)
than the estuarine and marine congeners,
P. elegans, P. adrpersus
and
P. northropi.
This suggests that the generally postulated relation-
ship between egg size and lifestyle (freshwater vs. estuarine
or
marine) may appear at a generic
but not at the family level. On the other hand, individual biomass (in pg
or
Joules per egg) of
early eggs was significantly higher in
P. elegans
and
P. adspersus,
indicating interspecific
variability in biomass and energy concentration (in pg
or
Joules per unit volume,
mm').
Generally lower biomass concentrations in early eggs of freshwater shrimps may be caused by
a
higher average water content. Eggs in late embryonic stages were generally larger than earlier
eggs of the same species, reflecting an increase in the water content, while an increasing
D,:D,
quotient indicated an increasingly elongated egg shape. The biomass per egg decreased during
embryonic development due to metabolic degradation of organic reserves.
As
a consequence
of
inverse ontogenetic changes in size and organic biomass of developing eggs, the mass-specific
biomass values
(C,
N,
H
in percent of
W;
E in Joules per mg
W)
and volume-specific
'Corresponding author
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concentrations (pg
or
Joules per unit volume) decreased. This change was consistently stronger
in the C,
H,
and
E
contents than in other measures of biomass
(W,
N).
In consequence, the C:N
mass ratio also decreased, suggesting that lipid degradation rather than protein utilization was the
principal fie1 for embryonic development.
Our
results indicate high intra- (mainly develop-
mental)
and
interspecific variation in reproductive traits of closely related species. While
volume-specific biomass and energy concentrations of early eggs appear to be associated with
variation in habitat salinity (freshwater, brackish, marine), individual egg size and biomass may
be related more with the climatic-geographic distribution (temperate, tropical)
of
different taxa.
Key
wordr:
Crustacea, Caridea, Palaemonidae, Atyidae, Pandalidae, reproduction, egg size,
elemental composition (C,
N,
H),
freshwater, brackish, marine
Introduction
Knowledge of quantitatively measured reproductive
traits is of utmost importance for understanding the
evolution of different life history patterns, especially in
ecological and phylogenetic comparisons among
related taxa. Among those traits, the size and biomass
of eggs are particularly important because they are
closely linked with the durations of both embryonic
and larval development,
as
well
as
with the number and
type of larval stages, and with juvenile size (for review
of the crustacean literature and general theoretical
implications, see Herring, 1974; Steele, 1977; Strath-
mann, 1977, Clarke, 1982; Bauer, 1991, Havenhand,
1995; Jaeckle, 1995, Bemardo, 1996; Marques and
Pohle, 1996).
For
the Crustacea in general, reproductive traits
have been compared in various books and review
articles (see, e.g., Sastry, 1983; Wenner et al., 1985;
Wenner and Kuris, 1991; Forest, 1994). Dealing
specifically with caridean shrimps, which are the
subject of the present study, comparative data of
female
size
in relation to egg production (fecundity),
size at the onset of maturity, and egg size have been
presented, for instance, in the papers by Corey and
Reid (1991), Reid and Corey (1991), and Anger and
Moreira (1998). In the latter study, morphometric
traits, egg numbers, and reproductive output (i.e.,
weight of total
egg
mass in relation to female body
mass) were compared between several tropical shrimp
species from Brazil differing in female body size and
life style (freshwater vs. marine). All these studies of
reproductive traits of shrimps and other decapods have
mainly considered the characteristics of ovigerous
females in relation to total egg clutch size, while much
less
attention has been paid
to
size dimensions and
chemical characteristics of individual eggs. In
particular, the degrees of intra- and interspecific
variability in size and biomass
of
eggs have remained
little known, developmental changes in the volume and
shape of eggs have frequently been observed but barely
quantified, and it has remained unclear if large egg size
is always consistent with large energy reserves.
The present paper provides comparative measure-
ments of size, biomass, and chemical composition of
caridean shrimp eggs. These data were obtained during
an earlier study (Anger and Moreira, 1998) and
complemented with additional data from other species
belonging to three families (Palaemonidae, Atyidae,
Pandalidae). This comparison of reproductive traits
considers primarily interspecific variation in egg size
and shape (1ength:width index), volume, dry mass,
carbon, nitrogen, and hydrogen contents (C,
N,
H),
as
well
as
in dry-mass-specific and volume-specific
concentrations of C,
N,
H,
and energy (the latter
estimated fiom carbon data).
As
far
as
eggs in different
embryonic stages were available (obtained from differ-
ent females), ontogenetic changes were are also
considered. Only a few egg size data (for three species)
-
but no comparative data
of
egg biomass
-
were
available from the literature, allowing for some
estimates of intraspecific variability, which was not
otherwise studied in the present investigation.
Materials and Methods
Species studied
As in the preceding investigation by Anger and
Moreira (1 998), the neotropical palaemonid shrimp
species
Macrobrachium olfrsii
(Wiegman),
M
car-
cinus
(Linnaeus),
M
acanthurus
(Wiegman),
Palae-
mon northropi
(Rankin),
P. pandaliformis
(Stimpson),
and the atyid
Potimirim potimirim
(Muller) (all from
Brazil) were included in the present study. General
life-history traits, ecology, and geographical distri-
bution of these species were summarized in the
previous paper. The present study shows additional
data from two further palaemonid species from the
Baltic Sea,
Palaemon elegans
Rathke and
P. adspersus
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85
Rathke, from another Brazilian atyid shrimp,
Atya
scabra
Leach, and a pandalid species from the North
Sea,
Pandalus montagui
Leach.
All three
Macrobrachium
species
as
well
as
Palaemon pandaliformis, Potimirim potimirim
and
Atya scahra
live
as
adults in freshwater, while their
larvae require,
as
far
as
this is known, brackish or
marine conditions for successful development through
metamorphosis (for references, see Anger and Moreira,
1998;
Galviio and Bueno,
2000).
The other four
species (to some extent
P.
pandaliformis
also) occur
throughout their life cycles in estuarine and/or marine
environments (cf. Fincham,
1977, 1985;
Moreira and
McNamara;
1984,
Schultze and Anger,
1997).
The
type of larval development consists,
as
far
as
known, in
all species, of a sequence of numerous (ranging from
ca.
6-12,
varying also intraspecifically) and morpho-
logically similar stages (for exhaustive review of
developmental patterns in decapod crustacean larvae,
see Williamson,
1982;
Gore,
1985;
Anger,
2001).
Obtaining ovigerous females
The places (all located near the marine biological
centre, CEBIMAR,
Siio
Sebastiiio,
Siio
Paulo State,
Brazil), time (February
1996),
and methods of catching
(with hand nets) ovigerous females of
M.
olfrsii,
M
carcinus,
M.
acanthurus, Palaemon pandaliformis,
P.
northropi,
and
Potimirim potimirim
were the same
as
described in the study by Anger and Moreira
(1998).
Likewise,
Atya scabra
was caught near the CEBIMAR,
from the Guaeci River (for more details, see also
Galvb and Bueno,
2000).
P. elegans
and
P. adspersus
were originally obtained from shallow nearshore sites
in the Kiel Fjord, western Baltic Sea, and transferred to
the Helgoland Marine Station (BAH); from this
material, a subsequent generation was reared from
hatching through sexual maturity in seawater from the
North Sea
(32960).
Ovigerous females of
Pandalus
montagui
were caught from ca.
40-60
m depth near the
island of Helgoland, North Sea, and also maintained in
seawater (for more details, see Schultze and Anger,
1997).
Egg
size, volume, embryonic stage
Eggs were removed from ovigerous females and
measured under a dissecting microscope (Wild M3B)
with a calibrated eye piece micrometer to the nearest
0.01
mm. For each female, egg size was determined
as
longer and shorter
axis
(diameters D,, D,; of n
=
10
eggs each), and their volume
(V)
was calculated using
the formula for oblate spheroids,
V=
(n*D~*D,)/6.
The embryonic egg stage was checked micro-
scopically and assigned to one of three developmental
categories:
I,
more than two-thirds of the egg volume
occupied by yolk, no eye pigments visible, embryo
shows little
or
no differentiation;
11,
phase of eye
formation and advanced embryonic differentiation
(segmentation, development of appendices visible),
heart beat apparent but often irregular, yolk occupying
more than one third of the
egg
volume;
111,
eye fully
developed, heart beat regular, differentiation of appen-
dages in their final phase, yolk occupying less than
one-third of the
egg
volume.
Egg
biomass, elemental composition
Aliquot samples from each egg clutch were taken
for subsequent determinations of dry mass (W), carbon
(C), nitrogen
(N),
and hydrogen content (H). Each
measurement had five replicate analyses. Depending
on species-specific
egg
size and estimated dry mass,
five
(Pandalus montagui),
seven
(Palaemon elegans,
P. adspersus),
15
(Atya scabra, Potimirim potimirim),
or
10
eggs (all other species) were weighed and
analysed in each replicate determination of W, C, N,
and H. The eggs were briefly blotted on filter paper
(fluff-free Kleenex for optical use; in marine and
brackish water species, after previous rinsing for
a
few
seconds in water from an ion exchanger), subsequently
transferred to preweighed tin cartridges, and vacuum-
dried overnight at
<0.01
mbar in a Lyovac GT
2E
(Leybold-Heraeus) apparatus.
After determination of dry mass on a Mettler UM3
microbalance, C,
N
and H were measured in
a
Fisons
(Carlo Erba Science) Model
1
108
Elemental Analyzer,
using acetanilid
as
a standard. The energy content of
the eggs (E, in Joules) was estimated from carbon data
using the empirical conversion proposed by Salonen et
al.
(1976),
and assuming an ash content of
2%
(embryonic stage
I),
4%
(stage
11),
or
6%
of dry mass
(stage
111)
(cf. Katre,
1977;
Rao et al.,
198
1
;
Clarke et
al.,
1990;
Petersen and Anger,
1997).
All C,
N,
H, and
E data are given here in absolute terms (in pg or Joules
per egg),
as
mass-specific values (in percent of W
or
Jouledmg W), and
as
volume-specific quantities or
densities (in pg
or
Joules per mm’).
Statistical methods
All statistical analyses followed standard techniques
(Sokal and Rohlf,
1995).
When data deviated signi-
ficantly from a normal distribution (Kolmogorov-
Smirnov test)
or
when variances deviated significantly
from homogeneity (Levene’s median test), the non-
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parametric Mann-Whitney rank sum test was used for
comparisons
of
mean values, otherwise Student’s t-test
was used. Percentage values (e.g.,
C
in percent
of
W)
and ratios
(D,:D,,
C:N)
were arc-sin transformed prior
to statistical analysis. Differences between mean values
were considered
as
statistically “significant” when the
probability of error for rejecting the null hypothesis
was
Pc0.05;
differences are referred to
as
“highly
significant” when
P<O.Ol.
Results
Egg
size
and
volume
Among the caridean shrimps considered in this
study, smallest egg size was observed in the two atyid
species,
Atya
scabra
and
Potimirim potimirim
(ca.
0.04
mm’ volume in eggs in an early to intermediate
stage of embryonic development), largest in the
pandalid shrimp,
Pandalus montagui
(>0.20
mm3), and
intermediate values in palaemonid species (Table
1).
Within the latter taxon,
Palaemon pandaliformis
had
the largest eggs, similar to those
of
Pandalus mon-
tagui.
When early (stage
I)
egg size data are compared
within a single genus (this is possible here only among
Palaemon
spp.), the most limnic species
(P.
panda-
liformis)
shows significantly larger eggs than any
of
the estuarine and marine congeners studied here (all
P<O.
00
1
).
Where data from eggs in different stages of
embryonic development were available, egg size
tended to increase during the course
of
egg develop-
ment (Table
1).
Late eggs (stages
I1
and
111)
were in
most cases significantly larger than early eggs (stage
I)
of the same species. Exceptions from this rule were
observed only between stages
11-111
in
P. pandaliformis
and
Pandalus montagui,
and between stages
1-11
in
Potimirim potimirim.
In
two
species,
Macrobrachium
olfersii
and
Palaemon pandaliformis,
estimates of egg
volume increase between a very early and a very late
stage of embryonic development, yielded values of
33.7
and
22.4%,
respectively.
Table
1.
Egg
size
of
caridean
shrimps,
measured
as
larger
and
smaller
diameter
(D,,
D2),
1ength:width
ratio
(Dl:D2),
and
volume
(V);
embryonic
stages
I,
11,111,
see
text;
arthmethic
mean
values
f
1
standard
deviation
(SD);
occasional
comparison
with
values
from
the
literature
(see
references, ref.)
P
ALAEMONIDAE
Macrobrachium olfrsii
M.
carcinus
M.
acanthurus
Palaemon northropi
P.
pandaliformis
P.
elegans
P.
aakpersus
ATYIDAE
Atya scabra
Potimirim potimirim
PANDALIDAE
Pandalus montagui
I
11
Ill
111
(1)
I
I
I1
I
I1
I
I1
111
I
I
I
?
(2)
I(3)
I11
(3)
I
I1
I1
626
70
1
715
630
609
732
782
65
1
74
1
770
886
903
635
683
590
546
583
556
564
944
-
I11
966
17 512
18 527
29 553
480
14 532
28 5 74
26 573
27 479
13 594
24 63 1
41 672
18 645
26 473
24 552
11 373
39 345
37 382
16 389
18 372
24 642
12
19
30
13
34
19
15
23
32
35
26
4
14
9
30
14
14
26
7
1.22 0.04 0.086
1.33 0.04
0.102
1.30 0.06 0.1 15
1.31 0.076
1.14 0.03 0.090
1.28 0.07 0.127
1.37 0.06 0.134
1.36 0.08 0.078
1.25 0.04 0.137
0.200
1.22 0.03 0.161
1.32 0.06 0.209
1.40 0.05 0.197
1.34
0.06
0.074
1.24 0.07 0.109
1.58 0.05 0.043
1.58 0.034
1.53 0.045
1.43 0.05 0.044
1.51
0.08 0.041
1.47 0.05 0.204
34 639 6 1.51 0.06 0.207
0.005
0.009
0.016
0.005
0.019
0.01 1
0.005
0.012
0.021
0.030
0.018
0.003
0.004
0.002
0.004
0.007
0.005
0.007
References:
(I),
Dugger
and
Dobkin
(1975); (2),
Corey
and
Reid
(1991); (3)
Galvio
and
Bueno
(2000);
all
others:
present
study.
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87
The generally observed developmental increase in
egg volume is due to an increase in both diameters, D,
and D,. However, the larger egg dimension (D,)
appears to increase proportionally more than the
smaller one (DJ,
so
that the 1ength:width quotient
(D,:D, index) tended to increase. This was observed in
five of the six species where
egg
size data from
different embryonic stages were available (Table 1);
exceptionally, this was not apparent
in
Palaemon
northropi.
Besides interspecific and developmental variation
in
egg size, Table
1
shows also examples of intra-
specific variability among eggs obtained from different
females or populations (comparison with values from
the literature), namely in early eggs ofAtya
scabra
and
in late eggs of
Macrobrachium olfrsii.
Egg
biomass, elemental composition
(C,
N,
H),
energy
content
Individual dry mass (W), carbon
(C),
nitrogen
(N),
hydrogen
(H),
and energy content
(E,
estimated from
C
data) per egg showed similar patterns of interspecific
variation
as
egg size, although some differences also
occurred (Table
2).
While atyid shrimp eggs had the
lowest biomass, corresponding with smallest egg
volume among the species studied here (cf. Table
l),
the eggs of
Palaemon adspersus
showed at least
as
high biomass values
as
those of
Pandalus montagui,
although egg volume was almost twice
as
high in the
latter species.
Palaemon elegans
and
P.
northropi
eggs
also showed higher biomass levels than would be
expected from their volumes.
The relative (dry-mass-specific) values of
C,
N,
H,
and
E
showed little interspecific variation among the
taxa studied here (Table
3).
The dry mass of freshly
laid eggs contained between'
52%
and 60%
C,
9.2%
to
11.6%
N,
and 7.6%
io
8.7%
H;
the mass-specific
energy content varied between
22
and
27
Jlmg W.
When successive developmental stages are
compared in a given species, the various measure-
ments of egg biomass showed almost consistently a
significant decrease in later stages (exceptions
occurred only in stages
11-111
of
Macrobrachium
olfesii
and
Palaemon pandalgormis;
Table
2).
The
decrease in egg biomass was consistently stronger in
C,
N,
H, and energy content
as
compared with total W.
As
a consequence, a highly significant decrease occurred
not only in the absolute (per individual) but also
in
the
percentage values of
C,
N,
and
H
as
well
as
in
the
mass-specific energy content (Table
3).
Table
2.
Dry mass
(W),
carbon
(C),
nitrogen
(N),
hydrogen
(H),
and energy content (E; estimated from
C)
of
caridean shrimp
eggs; arithmetic mean values
f
1
standard deviation (SD)
Species
Stage
W
(pglind)
C
(pglind)
N
(pglind)
H
(pglind)
E
(Jlind)
X
+SD
x
*SD
x
*SD
x
*SD
x
+SD
PALAEMONIDAE
Macrobrachium olfersii
I
27.1 1.1 14.1 0.6 2.60 0.12 2.08
I1
24.2 2.0 11.5
1.1
2.22 0.19 1.68
I11
24.3 0.2 11.2 0.1 2.46
0.05
1.65
M
carcinus
I
38.7 0.4 21.2 0.2 3.58 0.04 3.27
M. acanthurus
I
49.5 0.4 27.0 0.2 5.22 0.04 4.10
11
41.9 0.4 21.2 0.2 4.51 0.03 3.22
Palaemon northropi
I
41.9 0.7 23.8 0.6 4.83 0.12 3.65
I1
40.1 0.5 21.5 0.2 4.65
0.05
3.33
P. pandaliformis
I
53.0 0.3 27.7 0.3 5.67 0.06 4.23
I1
49.2 0.2 24.1 0.2 5.34
0.04
3.71
111
50.0
0.2 24.5 0.1 5.69 0.03 3.72
P.
elegans
I
56.5 1.4 31.0 0.9 5.80 0.18 4.53
P.
aakpersus
I
73.8 0.7 40.8 0.5 7.97 0.10 6.05
ATYIDAE
Atya scabra
I
19.9
0.1
10.7
0.1
1.92 0.01 1.58
Potimirim potimirim
I
13.1 0.2 7.8 0.1 1.42
0.01
1.14
I1
12.4
0.1
7.2 0.0 1.39 0.01 1.04
PANDALIDAE
Pandalus montagui
11
70.3 1.5 32.8 0.6 7.89 0.11 4.84
I11
61.8 0.4 27.6 0.1 7.08 0.02 3.98
0.12 0.59 0.02
0.19 0.46
0.05
0.06 0.44 0.01
0.01 0.91 0.01
0.05
1.15 0.01
0.03 0.87 0.01
0.09 1.03 0.04
0.05
0.91 0.01
0.08 1.16 0.02
0.02 0.97 0.01
0.04 0.99 0.01
0.15
1.32 0.04
0.10 1.76 0.03
0.01 0.45 0.01
0.02 0.35 0.01
0.01 0.32
0.01
0.12 1.29 0.02
0.11 1.07
0.01
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Table
3.
Dry-mass-specific carbon (C), nitrogen
(N),
and hydrogen
(H)
contents, C:N
mass
ratio, and energy content
(E,
estimated from C)
of
caridean shrimp eggs; arithmetic mean values
f
1
standard deviation (SD)
Species Stage C(%W) N
(%
W)
H
(%
W)
C:N ratio E (J/mg
W)
PALAEMONIDAE
Macrobrachium olfrsii
M
carcinus
M.
acanthurus
Palaemon northropi
P.
pandaliformis
P.
elegans
P.
adrpersus
ATYIDAE
Atya scabra
Potimirim potimirim
PANDALIDAE
Pandalus montagui
X
+SD
x
fSD
x
fSD
x
+SD
x
*SD
I
51.9
I1
47.6
111
46.3
I
54.9
1
54.5
11 50.6
I
56.7
I1 53.5
I
52.3
I1
49.0
I11
49.0
1 54.8
I
55.4
I
53.7
I
59.9
I1
57.9
I1
46.7
I11
44.7
0.3
0.6
0.4
0.2
0.2
0.3
1.2
0.4
0.7
0.2
0.2
0.6
0.6
0.4
0.6
0.4
0.5
0.3
9.6 0.1 7.65 0.12
9.2 0.1 6.94 0.25
10.1 0.2 6.78 0.20
9.3 0.1 8.45 0.06
10.5
0.0
8.28 0.06
10.8
0.0
7.68 0.04
11.6 0.2 8.71 0.29
11.6 0.0 8.32 0.06
10.7 0.2 7.98 0.19
10.9
0.1
7.54 0.03
11.4 0.1 7.45 0.06
10.3 0.1 8.02 0.13
10.7 0.1 8.20 0.11
9.6 0.1 7.93 0.10
10.9 0.1 8.77 0.20
11.2 0.1 8.41 0.13
11.2 0.1 6.89 0.13
11.5 0.1 6.44 0.18
5.42 0.05 21.6 0.2
5.19 0.07 18.9 0.4
4.57 0.06 18.1 0.3
5.93 0.04 23.5 0.1
5.18 0.01 23.3
0.1
4.69 0.03 20.7 0.2
4.91 0.02 24.7 0.8
4.62 0.03 22.6 0.2
4.89 0.01 21.8 0.5
4.51 0.02 19.8 0.1
4.30 0.02 19.7 0.1
5.33 0.01 23.4 0.4
5.16 0.01 23.8 0.4
5.57 0.02 22.7 0.2
5.50 0.02 26.9 0.4
5.16 0.02 25.5 0.3
4.16 0.03 18.4 0.3
3.90 0.01 17.2 0.2
Table
4.
Volume-specific carbon (C), nitrogen
(N),
hydrogen
(H),
and energy concentration
(E,
estimated
from
C)
of
caridean
shrimp eggs; arithmetic mean values
f
1
standard deviation (SD)
~
Species stage
W
(pdmm’)
X
hSD
PALAEMONIDAE
Macrobrachiurn olfrsii
M.
carcinus
M.
acanthurus
Palaemon northropi
P.
pandaliformis
P.
elegans
P.
aakpersus
ATY IDAE
Atya scabra
Potimirim potimirim
PANDALIDAE
Pandaius montagui
I
316 18
I1
239 21
111
215 28
I
430 25
I
396
51
I1
313 23
I
538 39
I1
294 25
I
334 43
11
238 30
111
255 24
I
762 34
I
679 26
1
464 25
I
298 25
I1
312 46
I1
337 15
I11
301 11
c
(pdmm’)
X
+SD
164 9
114 10
100 13
236 14
216 28
158 12
305 22
158 14
174 22
117 15
125 12
417 19
376 14
249 13
179 15
181 27
158 6
143 19
N (pdmm’)
X
fSD
30.3 1.7
21.9 1.9
21.8 2.9
39.8 2.4
41.8 5.4
33.7 2.5
62.1 4.6
34.2 2.9
35.7 4.6
25.8 3.3
29.1 2.7
78.2 3.5
72.8 2.8
44.8 2.4
32.5 2.7
35.0 5.2
37.6 2.2
32.5 1.2
H
(pdmm’)
X
+SD
24.2 1.4
16.6 1.5
14.6 2.0
36.4 2.1
32.8 4.3
24.1 1.8
46.9 3.4
24.5 2.1
26.6 3.4
17.9 2.3
19.0 1.8
61.1 2.7
55.7 2.1
36.8 2.0
26.1 2.2
26.2 3.9
23.7 0.5
19.0 0.7
E
(J/mrn’)
x
+SD
6.9 0.4
4.5 0.4
3.9 0.5
10.1 0.6
9.2 1.2
6.5 0.5
13.2 1.0
6.7 0.6
7.3 0.9
4.7 0.6
5.1 0.5
17.8 0.8
16.2 0.6
10.5 0.6
8.0 0.7
8.1 1.2
5.7 0.2
5.6 0.2
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89
Volume-specific egg biomass and energy
concentration
When volume-specific values (concentrations) of
W, C,
N,
H,
and
E
are calculated from the data given in
Tables
1
and
2,
a great deal of both interspecific and
developmental variation becomes conspicuous
(Table
4).
Among freshly laid eggs, the dry mass
content per unit volume, for instance, varied between
3
16
pg/mm3 in
Macrobrachium olfersii
and
762
pLg/
mm3 in
Palaemon elegans.
Similarly, the carbon
concentration varied between
164
and
4 17
pg C/mm3,
respectively. As a general tendency, the eggs of
shrimps that reproduce in freshwater
(Macrobrachium
spp.,
Palaemon pandalformis,
Atyidae) showed lower
initial biomass and energy concentrations than the
estuarine and marine species.
In two species,
M.
olfersii
and
P.
pandalformis,
our
data provide estimates of the total percentage changes
in egg volume and individual biomass,
as
well
as
in
volume-specific biomass
or
energy concentration, of
early vs. late eggs, reflecting the overall changes in egg
size and chemical composition during the course of
embryonic development (Table
5).
These quantitative
estimates represent minimum changes,
as
the egg
materials used in this study may not actually have been
in
the very initial
or
in the very final stage of
development, respectively. Since the egg volume
increased by
22-34%,
while the individual biomass and
energy values per egg decreasd concomitantly (Table
4;
cf. Table
2),
the percentage biomass losses were
most conspicuous in the volume-specific concen-
trations (Table
5).
The extent of developmental changes varied greatly
among the various measures of egg biomass. While the
total content of dry mass and
N
per egg decreased only
Table
5.
Percentage changes during embryonic development
from stage
I
(freshly laid) to stage
Ill
(shortly before
hatching)
in
egg volume
(Vol.;
cf. Table
I),
individual
biomass
or
energy (percent per egg; cf. Table
2)
and
in
the
volume-specific concentrations (conc.; cf. Table
4)
of dry
mass
(W),
carbon (C), nitrogen
(N),
hydrogen
(H),
and
energy
(E)
in
two caridean shrimp species
M.
olfersii
P.
pandalformis
%
per egg Conc.
%
per egg Conc.
Vol.
+33.7 +22.4
W
-
10.5 -32.0
-
5.8 -23.4
C
-
20.2 -39.4 -11.8 -28.3
N
-
5.4 -28.0
+
0.3
-
18.5
H
-20.7 -40.0 -12.1 -28.6
E
-25.4 -43.5
-
14.7 -30.1
a little, the individual C,
H,
and energy contents
dropped significantly (by up to
25%).
These losses
were generally much higher (almost twice
as
high) in
M.
olfersii
than in
P. pandalformis.
As a consequence
of contrasting changes in egg volume (increase) and
biomass (decrease), the volume-specific concentrations
of all measures of organic biomass decreased
markedly, by
2844%.
Again, these changes were
higher in
M.
olfrsii
than in
P. pandalformis.
Discussion
Although the present comparative study
is
certainly
limited
as
to the number of species and developmental
stages considered, our data of egg size and biomass in
various caridean shrimp species allow for several
preliminary conclusions, and they contribute to a
broadening data base for future comparisons between
more taxa, geographic-climatic regions, and life
histories. In our data of egg size in several caridean
shrimp species belonging to different families,
interspecific variability may reflect phylogenetic
variation among clades rather than different life styles
(freshwater vs. marine
or
estuarine)
or
latitudes
(tropical vs. temperate).
One of the major limitations in our present
knowledge is associated with the generally unknown
degree of intraspecific variability both between and
within populations. In the present study, indications of
intraspecific variability (other than developmentally
caused changes, which are discussed below) were
found in
Macrobrachium olfersii, Palaemon northropi,
and
Aqa
scabra
(see Table
1).
Differences in the early
egg size of
A. scabra
probably represent intra-
populational (seasonal or individual) variability among
females,
as
our material originated from the same
location as that studied by Galvao and Bueno
(2000).
In
M
olfersii,
on the other hand, differences in the size
of late eggs may indicate variability among geo-
graphically separated populations (Brazil vs. Florida;
cf. Dugger and Dobkin,
1975).
The larger
egg
size in
Palaemon northropi
from Florida (Corey and Reid,
1991)
than Brazil (present study) cannot be compared,
as
the developmental stage of the former material is
unknown.
From other comparative studies of decapod
crustaceans we know that reproductive traits may vary
significantly with seasonal changes in temperature
andor daylength. For instance, there are larger winter
and smaller summer eggs in the North Sea shrimp,
Crangon crangon
(Boddeke,
1982);
in the same
species, interannual differences have also been
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documented (Kattner et al., 1994). In some euryhaline
species, there are physiological and genetic differences
between partially isolated freshwater and estuarine
populations. This phenomenon has extensively been
studied in two palaemonid shrimp species from Japan,
Macrobrachium nipponense
and
Palaemon pauc idens
(see Mashiko, 1999; Mashiko and Numachi, 2000, and
numerous earlier papers cited therein). In
P.
paucidens,
up to seven times larger eggs (by volume) were found
in freshwater than in brackish water populations
(Nishino, 1980). In
Macrobrachium amazonicum,
which is widely distributed within the Amazon River
system, from the Atlantic coast to more than 3400
km
inland,
egg
size
is
positively correlated with the
distance of a population from the estuary (Odinetz
Collard and Rabelo, 1996). Similarly, egg size of an
atyid shrimp from Australia,
Paraya australiensis,
is
larger in the upper than in the lower parts of rivers and
creeks (Hancock, 1998; Hancock et al., 1998). In all
these cases, however, it remains unknown if the
tendency in egg size
(or
volume)
is
consistent with a
similar tendency in egg biomass.
Even among females from the same population,
small-scale and short-term local salinity variations may
exert significant effects on the size and energy content
of
eggs, as was experimentally shown
in
a
euryhaline
crab (GimCnez and Anger,
2001;
GimCnez, 2002).
Large-scale geographic-climatic temperature gradients
have also been shown to influence egg size and
biomass (Gorny et al., 1992; Wehrtmann and Kattner,
1998; Lardies and Castilla, 2001). In addition to all
these sources of intraspecific variation, successive egg
clutches produced by the same female may also vary
significantly (Charles, 1987, Palacios et al., 1998,
1999), and the body size (Clarke, 1993; Gardner, 200 1)
as
well
as
the nutritional condition of the mother may
exert a significant influence on the size and chemical
composition of its
eggs
(Cavalli et al., 1999; Lin and
Zhang, 2001). At the population level, predation
pressure (e.g., by fisheries) may also exert a selective
pressure on egg size (Huner and Lindqvist, 1991).
In conclusion, there remains some uncertainty about
the interspecific comparison of reproductive traits in
the context of different geographic-climatic distribu-
tions
or
lifestyles of different taxa. Among the species
considered in the present study, it seems that egg size
(by volume
or
biomass per egg) varies in each genus
or
family within a typical range. The two atyid species
produced the smallest eggs, the only pandalid studied
had the largest eggs, and all Palaemonidae fell within
an intermediate category (Tables 1,2). Future reviews
of egg size data from more species may show if these
levels are in fact typical of the respective families.
Such broad comparisons, however, must consider also
the developmental mode,
as
most higher taxa also
include species with an abbreviated mode of larval
development, which is generally associated with an
enlarged egg size (Gore, 1985, Rabalais and Gore,
1985, Anger, 200 1). Probably all species studied here
belong to the “extended” mode (sensu Gore, 1985),
i.e., they pass through numerous larval stages.
While size, volume, and biomass per egg
vary
greatly among
taxa,
the dry-mass-specific contents of
the major organically bound elements, namely C, N,
and H, are fairly constant (see Table
3).
Comparable
results were obtained in previous studies
of
elemental
composition of shrimp and crab eggs (Clarke et al.,
1990; Petersen and Anger, 1997). If low intra- and
interspecific variability in the elemental composition of
shrimp eggs
(or
decapod crustacean eggs, in general)
can be confirmed in future studies, easily obtained dry
mass data (including those from the earlier literature)
may be used to estimate quantities of organic matter
and energy. In comparisons
of
reproductive traits, this
should be a better comparative reference base than egg
size
or
volume alone. In contrast to mass-specific
values of biomass and energy, volume-based concen-
trations show great interspecific variability. This
suggests that size and volume measurements may be
poor predictors of organic reserves stored in the eggs.
All measures of egg size compared here (diameter,
volume, biomass, energy) vary significantly during the
course of embryonic development. Although our
materials for the study of egg size in different develop-
mental stages had to be obtained from different
females, our data show quite consistently the generally
known tendency of increasing volume (see Wenner and
Kuris, 199
1
),
concomitantly decreasing biomass and
energy contents, and in consequence, greatly declining
biomass and energy concentrations per unit volume
(Table
5).
The developmental increase in egg size of
aquatic crustaceans is due to an uptake andor internal
production of water during the course of embryonic
development. Exceptions were observed only between
stages 11-111
in
Palaemon pandaliformis
and
Pandalus
montagui,
and between stages
1-11
in
Potimirim
potimirim.
This apparent lack of volume increase must
have been caused by individual variability among
conspecific females.
Volume-specific biomass concentrations may vary
also among lifestyles. When equal developmental
stages are compared (e.g., only stage
I,
Table 4), it
appears that estuarine
or
marine species
(Palaemon
northropi,
P.
elegans,
P.
adspersus)
show generally
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91
higher values than those producing their eggs in
freshwater
(P. pandalijormis, Macrobrachium
spp.,
Atya scabra, Potimirim potimirim).
This difference
should be due a passive uptake of water in the eggs of
the latter species, causing a generally higher water
content. This interpretation can easily be scrutinized in
future studies, measuring not only dry mass
(W)
but
also wet mass of crustacean eggs from various habitats.
When successive developmental stages of a given
species are compared, the various measurements of egg
biomass also showed, almost consistently, a significant
decrease in later stages (exceptions, due to individual
variability among females, occurred only in stages
II-
I11
of
Macrobrachium olfrsii
and
Palaemon
pandalijormis;
see Table
2).
This general pattern re-
flects metabolic losses during embryonic development.
Due to degradation of organic matter, the decrease in
egg biomass was consistently stronger in C, N, H, and
energy content
as
compared with total W, which
comprises also inorganic constituents. As a conse-
quence, a highly significant decrease occurred not only
in
the absolute (per individual) but also in the
percentage values of C, N, and H
as
well
as
in the
mass-specific energy content (Table
3).
Among the principal organically bound elements
within egg biomass, the fractions
of
C
and H declined
at a higher rate than N; this is indicated also by
consistently decreasing C:N mass ratios (see Table
3).
This general trend suggests that the principal fuel for
embryonic energy metabolism was obtained from a
preferential degradation of lipids (which have high C,
H,
and energy contents) rather than from a utilization
of protein stores (rich in N). Preferential lipid
degradation may be considered to be a rule in crus-
tacean eggs (e.g., Katre, 1977; Rao et al., 198
1
;
Clarke
et a]., 1990; Petersen and Anger, 1997, Heras et al.,
In addition to the increase in egg size and volume,
there is a tendency of a gradually changing
-
namely
an
increasingly elongated
-
egg shape in later stages
of embryonic development. This was observed in five
of the six species where the present study provided egg
size data from different stages (Table 1); exceptionally,
this was not apparent in
Palaemon northropi,
just
as
Galvgo and Bueno
(2000)
did not observe it in
A.
scabra.
Again, this inconsistency in the data should
be attributed to intraspecific variability.
When only eggs at an early stage are compared, the
1ength:width quotient (D, :D2) also seems to vary
among species and families. Higher index values in
atyid and pandalid shrimps indicate that the eggs were,
in the species studied here, more elongated than in the
2000).
palaemonids included in
our
study. If future inves-
tigations can identify phylogenetically typical
or
average 1ength:width indices for various taxa, this
would allow also for conversions of older literature
data, which are often limited to measurements of one
egg dimension (usually D,), to volume data, and these
estimates may be compared with biomass data. In later
reviews of the evolution of reproductive traits in
decapod crustaceans, a better understanding of such
quantitative relationships will allow for broader phylo-
genetical and ecological comparisons of life-history
patterns.
Acknowledgements
We wish to express our thanks to the staff of the
CEBIMar for kind hospitality and support for our
investigation, and to Mrs.
C.
Puschel (Helgoland)
for
carrying
out
elemental analyses. The first author
acknowledges financial support from the German
Academic Exchange Service, DAAD (Bonn) and the
Coordenadoria de Aperfeigoamento de Pessoal do
Ensino Superior, CAPES (Brasilia).
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