ICES Journal of Marine Science, 63: 995e1004 (2006)
doi:10.1016/j.icesjms.2006.04.007
Life history of a short-lived squid (Sepioteuthis australis):
resource allocation as a function of size, growth,
maturation, and hatching season
Gretta T. Pecl and Natalie A. Moltschaniwskyj
Pecl, G. T., and Moltschaniwskyj, N. A. 2006. Life history of a short-lived squid
(Sepioteuthis australis): resource allocation as a function of size, growth, maturation,
and hatching season. e ICES Journal of Marine Science, 63: 995e1004.
Many cephalopods continue growing while laying multiple egg batches over the adult life,
with repro-somatic allocation continuing beyond attainment of reproductive maturity. Many
species show extreme individual variation in reproductive investment. Factors driving this
variation in adult Sepioteuthis australis were evaluated by examining allocation of energy
to somatic and reproductive growth as a function of body shape, growth rate, maturation,
and hatching season. Hatching season influence was sex-specific; males hatched in warmer
months had greater reproductive investment, faster growth, and better somatic and reproductive condition, whereas females hatched in spring and summer had less reproductive
investment. Seasonal impacts on life history resulted in an ‘‘alternation of generations’’,
with slow-growing squid in poor condition and with high levels of reproductive investment
producing a generation with completely different life-history characteristics. This suggests
that abiotic and biotic conditions that change seasonally could play a large role in determining energy allocated to reproduction. However, this was not driving trade-offs between size
and number of offspring. Life-history trade-offs should be detectable as negative correlations between relevant traits. However, in Sepioteuthis australis there was little evidence
of trade-offs between reproduction and growth or condition of individuals, suggesting
a ‘‘live for today’’ lifestyle.
Ó 2006 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: energy allocation, life-history trade-offs, multiple spawning, phenotypic
variation, somatic condition.
Received 9 November 2005; accepted 15 April 2006.
G. T. Pecl: School of Marine Biology and Aquaculture, James Cook University, Townsville,
Queensland 4811, Australia, and Marine Research Laboratories, Tasmanian Aquaculture
and Fisheries Institute and University of Tasmania, Private Bag 49, Tasmania 7001,
Australia. N. A. Moltschaniwskyj: School of Marine Biology and Aquaculture, James
Cook University, Townsville, Queensland 4811, Australia, and School of Aquaculture,
Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, Locked Bag
1370, Launceston, Tasmania 7250, Australia. Correspondence to G. T. Pecl: Marine
Research Laboratories, Tasmanian Aquaculture and Fisheries Institute and University of
Tasmania, Private Bag 49, Tasmania 7001, Australia; tel: þ61 3 62277277; fax: þ61 3
62278035; e-mail: [email protected].
Introduction
For squid species that continue to grow while laying multiple batches of eggs over a significant portion of the lifespan,
the allocation of energy to somatic and reproductive growth
continues beyond the attainment of reproductive maturity.
Energy is viewed by most biologists as being the closest
thing there is to a common currency of life (Calow,
1985), with lifetime patterns of energy allocation central
to life-history theory. Individual fitness and the contribution
to future generations are partially determined by the
1054-3139/$32.00
dynamics of energy allocation to somatic and reproductive
growth. The amount of energy allocated to reproduction
influences the number and success of offspring, and ultimately determines population size and stability over time
(Boggs, 1997). Here we examine the process of resource
allocation between growth and reproduction in multiplespawning southern calamary (Sepioteuthis australis) as
a function of body shape, growth, maturation, and hatching
season.
Considerable flexibility in reproductive characteristics
is evident among individuals within some cephalopod
Ó 2006 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
996
G. T. Pecl and N. A. Moltschaniwskyj
populations, particularly age and size at maturation (Boyle
et al., 1995; Arkhipkin et al., 2000). Additionally, once reproductive maturation has been achieved, many cephalopod
species show a great degree of individual variation in the
extent of anatomical investment in reproductive structures
(usually reported as percentage of body mass), particularly
females (e.g. Loligo chinensis and Idiosepius pygmaeus;
Jackson, 1993). The size of egg batches and frequency of
batch deposition may also vary substantially among females of a species (Moltschaniwskyj, 1995a), with neither
parameter tightly constrained by size or age (Maxwell
and Hanlon, 2000). Sepioteuthis australis also exhibits considerable variation in mature egg size among females
(5e10 mm), with evidence of an energy trade-off between
egg size and number (Pecl, 2001). Multiple-spawning species have a greater potential for inter-individual variability
in resource allocation than terminal spawning species, because reproductive output is a function of size at first maturity, in addition to batch fecundity, spawning frequency,
and duration of individual maturity (Lowerre-Barbieri
et al., 1998). Therefore, a simple assessment of age and
size at maturity may not provide the resolution necessary
to understand the reproductive strategy adopted by an individual, or to identify the factors that have a role in the
development of different strategies.
For species with non-asymptotic growth patterns, growth
and reproduction necessarily proceed together over much of
the life cycle, and it is likely that the diversity of reproductive strategies is related to growth patterns (Mangold et al.,
1993). Typically, cephalopod growth is analysed by examining individuals in groups based on when they are caught.
Recently, there has been a shift to grouping individuals
based on their date of birth, on the assumption that they
are likely to have experienced similar environmental conditions. This approach has revealed that the patterns and rates
of growth exhibited by many cephalopods are influenced by
the season in which individuals hatch (Illex argentinus:
Rodhouse and Hatfield, 1990; Arkhipkin and Laptikhovsky,
1994; Lolliguncula brevis: Jackson et al., 1997; Sepioteuthis australis: Pecl, 2004). Likewise, size and age at maturation are also largely influenced by season of hatching
(Illex argentinus: Arkhipkin and Laptikhovsky, 1994;
Loligo pealei: Brodziak and Macy, 1996). However, there
is little field-based information currently available that explores how life-history characteristics other than growth,
and age and size at maturation may vary as a function of
the environmental conditions experienced, in particular,
the role that season of hatching may play in explaining
some of the intraspecific variation in repro-somatic allocation evident among mature individuals.
Assessment of the allocation of energy is usually based
on measurements of whole body growth rate. However, better understanding of the process of energy allocation may
be obtained by exploring the growth characteristics of discrete somatic and reproductive body elements. Ontogenetic
changes in shape are associated with the lifestyle of squid
(Vecchione, 1981; Moltschaniwskyj, 1995b), but there are
gender differences (Moltschaniwskyj, 1995b). Although ontogenetic changes in shape are associated with changes in
drag forces in water with size, gender differences are
more likely to be associated with differential somatic
growth associated with reproduction. Examining changes
in the size and shape of component body parts may therefore be of particular importance for understanding the
reproductive biology of animals with short lifespans and
highly flexible life-history strategies.
Flexible life-history characteristics in squid appear to be
crucial to the success of a short-lived species that must
reproduce and survive across a range of biological and
physical conditions (Boyle et al., 1995; Moltschaniwskyj,
1995a; Pecl, 2001). Lifetime reproductive allocation, and
therefore the life-history strategy adopted by an animal,
needs to be understood in terms of resource allocation between reproduction and other competing needs, such as
maintenance and growth (Heino and Kaitala, 1999). This
work examined the relationship between the level of investment in reproduction and somatic condition at the whole
animal level, as a function of body shape, growth, maturation, and hatching season in Sepioteuthis australis from the
east coast of Tasmania. It also assessed the extent to which
hatching season and individual somatic condition are
responsible for variation in batch and egg size in mature
S. australis females.
Sepioteuthis australis is a relatively large (1e4 kg), sexually dimorphic squid (males being larger than females) with
a lifespan of approximately one year (Pecl, 2004). Females
lay multiple batches of large eggs (Pecl, 2001) over several
months (GTP, unpublished), in strands attached to seagrass
or macroalgae in inshore shallow areas (Moltschaniwskyj
and Pecl, 2003). The main aim of this research was to evaluate the factors driving the generation of flexible reproductive
strategies evident among individuals within cephalopod
populations, and to assess the relationship of alternative
reproductive strategies with other aspects of the life cycle.
Material and methods
Sepioteuthis australis were collected from shallow inshore
waters on the east coast of Tasmania, Australia (42(150 S
148(100 E) from January 1996 to July 1997. In all, 493 squid
were caught (196 females, 237 males, 60 juveniles) either by
jigging or modified purse-seine. Most were refrigerated or
placed on ice within a few hours of capture, then dissected
within 12 h. All squid were sexed and via macroscopic
examination assigned a maturity stage following a six-stage
maturity scale (Lipiński, 1979). Squid with undifferentiated
gonads were defined as juveniles. Dorsal mantle length
(ML) was measured to the nearest millimetre, and total
body weight, mantle weight, and reproductive organs were
weighed to the nearest 0.01 g. Age was determined from
daily increments in the statolith (see Pecl, 2004).
Squid resource allocation as function of size, growth, maturation, and hatching season
Changes in shape with size and maturation
From 61 Sepioteuthis australis caught in Tasmania, ranging
in dorsal mantle length from 34.7 to 436.74 mm, 13 linear
measurements were taken (dorsal mantle length, maximum
mantle width, maximum head width, funnel diameter, fin
width, fin length, eye diameter, length of each of the four
arms, tentacle length, and club length). Using Model I regression analysis for each linear measure against ML
(logelog scale), a series of regressions were used around
the putative breakpoint, starting at 80 mm (1.9 on the log
scale), and increasing the breakpoint by 0.1 log (ML) up
to a maximum of 319 mm (2.5 on the log scale). For
each pair of regressions around the breakpoint, the residual
sum of squares (RSS) was calculated and summed to generate a pooled sum of squares (SS). This pooled SS was
then compared with the RSS for the single regression line
(combined RSS) generated for the total data set using an
F-test (Chen et al., 1992). If a breakpoint was present at
a specific ML, then the pooled RSS will be significantly
less than the combined RSS, indicating a better fit from
two separate lines than a single line. As data were repeatedly used, i.e. seven analyses were done for each linear
measurement, the probability value for the F-test was
adjusted to 0.007 using a Bonferroni correction.
Using the log-transformed data set and the correlation
matrix, a principal component analysis (PCA) on the linear
measurements was used to assess changes in shape associated with the allocation of resources to reproductive maturation. An assessment of allometric growth in shape was
assessed using the PCA components on the first axis, as
described in Moltschaniwskyj (1995b). Although linear
dimensions were measured on 61 squid, because of missing
measurements (e.g. lost arms or tentacles), 50e61 were
used in the breakpoint analysis and 41 for the multivariate
analysis.
Maturation, somatic condition, and growth
Ratios calculated from somatic and reproductive measurements are not size-independent (Hayes and Shonkwiler,
2001), but residuals of the mantle weighteML relationship
provide a size-independent measure of the condition of an
individual at the whole animal level (Moltschaniwskyj
and Semmens, 2000). To obtain measures of somatic condition, mantle weighteML geometric mean linear regression (Model II) equations were calculated for males and
females separately using log-transformed data, and from
these equations, residuals were calculated for each individual. A residual is the difference between an individual’s
actual measured weight and the weight predicted by the
regression equation. Residuals were standardized by dividing each by the standard deviation of the predicted values.
An individual that is lighter for its length than predicted
from the regression equation (negative residual) is suggested to be in poorer somatic condition than one that is
heavier for its length than predicted from the regression
997
equation (with a positive residual). As a size-independent
measure of reproductive investment, residuals were generated from reproductive weighteML regressions for each
sex. Reproductive weight was calculated as the combined
mass of the testis, spermatophoric complex, Needhams
sac, and penis for males, and of the ovary, oviduct, and
oviducal and nidamental glands for females. To test for
an association between somatic condition and level of
reproductive investment, residuals from mantle weighte
ML and reproductive weighteML regressions were correlated against each other for each sex separately. Residuals
were also generated from the size-at-age relationship (see
Pecl, 2004) as a measure of the difference in an individual’s
lifetime growth from the population average, and correlated
against residuals from the reproductive weighteML relationship to assess the association between growth rate and
level of reproductive investment.
A correlation between the residuals from the mantle
weighteML relationship and egg size was used to evaluate
the relationship between a female’s condition and egg size.
As larger females have the capacity to hold more eggs,
a partial correlation using body weight as a controlling variable was employed to examine the relationship between
female condition and the number of eggs within the
oviduct.
To determine if the magnitude of mantle weighteML
residuals were a function of reproductive maturation, the
average residuals among the maturity stages were analysed
separately for females using one-way ANOVA. Hochberg’s
GT2 method post hoc test for unequal sample sizes was
then used to determine where differences among means
occurred (Day and Quinn, 1989). Residuals from the sizeat-age relationship were analysed in the same way to determine if rate of growth was similar among maturity stages.
These analyses could not be undertaken for males because
there were insufficient immature and maturing males in the
population (see Jackson and Pecl, 2003).
Season of hatching
Squid were assigned to seasonal hatching groups (austral
summer, autumn, winter, spring) based on estimated
back-calculated hatching dates (Pecl, 2004). To determine
if the magnitude of mantle weighteML or reproductive
weighteML residuals were a function of hatching season,
the average residuals were compared among seasonal
hatching groups, separately for each sex, with one-way
ANOVA. Hochberg’s GT2 method post hoc test for unequal sample sizes was then used to determine where the
differences were among means. To examine the relationship
between somatic condition, growth, and reproductive
investment, residual pairs were correlated across all individuals for each sex (see above), and for each season of
hatching separately. Spring-hatched females were, however, not analysed separately owing to insufficient sample
size of this group for correlation purposes.
998
G. T. Pecl and N. A. Moltschaniwskyj
Sepioteuthis australis females are multiple spawners
(Pecl, 2001), so another factor of interest was how individual females born in each season were allocating their reproductive investment into discrete egg batches. The number
of ovulated oocytes in the oviduct of mature squid and
the sizes of mature oocytes were estimated as per Pecl
(2001). Analysis of covariance, using body weight as a covariate, was used to assess the number of eggs within the
oviduct of females as a function of hatching season.
Results
Changes in shape with size and maturation
The breakpoint analysis indicated that two of the linear body
measurements demonstrated changes in the allometric relationship with ML across the size range measured (Table 1).
Tentacle length grew isometrically until 126 mm ML, when
growth of this body component then slowed relative to ML.
Funnel diameter also grew isometrically until 315 mm ML,
whereafter funnel growth slowed dramatically. The growth
relationship of the other 11 variables did not change as squid
increased in size, suggesting that a multivariate approach is
an appropriate analysis for the other 11 linear body
measurements.
The second and third axes in the PCA typically contain
more shape information, whereas the first axis, which explained 97.2% of the variation, contains largely size information. The separation of individual squid on the second
and third PCA axes was a function of eye diameter, length
of arm 1, tentacle length, tentacular club length, fin width,
and funnel diameter (Figure 1). However, there was no evidence that variation in shape among individuals on either
axis was related to gonad weight for either females (Axis
2: r ¼ 0.37, n ¼ 23, p ¼ 0.08; Axis 3: r ¼ 0.13, n ¼ 23,
p ¼ 0.550) or males (Axis 2: r ¼ 0.19, n ¼ 28, p ¼ 0.330;
Axis 3: r ¼ 0.09, n ¼ 28, p ¼ 0.657). The shape analysis
found that both mantle width and head width were increasing in size at a slower rate than ML (Table 2), indicating
that individuals were getting narrower as they grew longer.
Table 1. Results of the F-test for the Sepioteuthis australis breakpoint analysis for each linear measurement vs. ML (logelog scale). Type
1 error rate was set at 0.007, given multiple tests for each variable. Significant results are emboldened.
Breakpoint (log ML)
Variable
1.9
2.0
2.1
2.2
2.3
2.4
2.5
Mantle width (d.f. 3,53)
F
Prob > F
0.818
0.490
1.618
0.196
1.911
0.139
1.876
0.145
2.334
0.084
1.754
0.167
0.444
0.722
Head width (d.f. 3,55)
F
Prob > F
0.174
0.914
0.712
0.549
1.267
0.295
2.182
0.100
2.601
0.061
1.023
0.390
0.789
0.505
Fin length (d.f. 3,53)
F
Prob > F
0.361
0.781
0.201
0.896
0.161
0.922
0.104
0.957
0.823
0.487
0.167
0.918
0.074
0.974
Fin width (d.f. 3,52)
F
Prob > F
0.361
0.781
0.201
0.896
0.161
0.922
0.104
0.957
0.823
0.487
0.167
0.918
0.074
0.974
Eye diameter (d.f. 3,48)
F
Prob > F
0.334
0.801
0.352
0.788
0.342
0.795
0.392
0.759
0.432
0.731
0.207
0.891
1.562
0.211
Funnel diameter (d.f. 3,44)
F
Prob > F
1.223
0.313
1.747
0.171
1.975
0.132
1.214
0.316
2.777
0.052
0.765
0.520
3.717
0.018
Arm 1 (d.f. 3,55)
F
Prob > F
2.375
0.080
2.220
0.096
1.962
0.130
1.770
0.164
2.462
0.072
1.604
0.199
0.586
0.627
Arm 2 (d.f. 3,55)
F
Prob > F
0.639
0.593
1.207
0.316
1.087
0.362
1.089
0.362
1.116
0.351
1.178
0.327
0.979
0.409
Arm 3 (d.f. 3,54)
F
Prob > F
0.086
0.968
0.249
0.862
1.442
0.241
0.674
0.572
0.425
0.736
0.631
0.598
0.620
0.605
Arm 4 (d.f. 3,54)
F
Prob > F
0.502
0.682
1.614
0.197
1.919
0.137
1.762
0.165
1.931
0.135
1.603
0.199
0.199
0.897
Tentacle (d.f. 3,54)
F
Prob > F
0.142
0.934
2.843
0.046
3.356
0.025
2.083
0.113
2.513
0.068
1.142
0.341
0.707
0.552
Tentacular club (d.f. 3,53)
F
Prob > F
1.147
0.339
1.991
0.126
2.416
0.077
1.810
0.157
2.387
0.079
0.734
0.536
0.215
0.886
Squid resource allocation as function of size, growth, maturation, and hatching season
PCA 3 (0.58%)
FW
ED
TC
TL
Table 3. Summary of Model II linear regression statistics for log
mantle and log reproductive weight vs. log ML relationships for
mature Sepioteuthis australis males and females.
A1
Relationship
FD
PCA 2 (0.81%)
Figure 1. Analysis of the Sepioteuthis australis PCA, showing the
variation of individuals on the second and third PCA axes. Crosses,
females, circles, males, and triangles, immatures. Only the largest
of the vectors have been identified for clarity. TC, tentacle club;
TL, tentacle length; A1, arm 1; FW, fin width; ED, eye diameter;
FD, funnel diameter.
Eye diameter also grew slower than ML. All other components were growing isometrically, i.e. these elements were
growing in length at the same rate as ML (Table 2). This
suggests that there was no change in shape associated
with these body elements.
Maturation, somatic condition, and growth
The increase in total reproductive weight with ML was
twice as fast in female Sepioteuthis australis as in males.
Although most of the variability in reproductive weight
was explained by ML, 64% and 60% in females and males,
respectively (Table 3), it was clear that other factors are
Table 2. Mean and standard error (s.e.) of the Sepioteuthis australis
PCA component for each linear measurement on the first PCA axis.
If somatic variables grew isometrically relative to dorsal mantle
length, then the component score would be 0.28.
Linear Measurement
Mean
s.e.
Growth
Maximum mantle width
Fin length
Fin width
Maximum head width
Eye diameter
Funnel diameter
Arm 1
Arm 2
Arm 3
Arm 4
Tentacle
Tentacular club
0.24
0.28
0.27
0.23
0.19
0.22
0.29
0.28
0.27
0.26
0.30
0.29
0.004
0.004
0.004
0.004
0.003
0.005
0.005
0.005
0.004
0.004
0.005
0.006
Negative allometric
Isometric
Isometric
Negative allometric
Negative allometric
)
Isometric
Isometric
Isometric
Isometric
)
Isometric
)Not able to be interpreted due to breakpoint.
999
n
Slope
95% C.I.
of slope
Intercept
(lna)
r2
Female
Mantle weight
Reproductive
weight
159
159
2.71 2.532e2.897
3.13 2.824e3.429
9.831
12.875
0.82
0.64
Male
Mantle weight
Reproductive
weight
228
190
2.54 2.438e2.644
1.70 1.504e1.888
8.873
6.375
0.91
0.60
also involved in determining repro-somatic investment in
mature squid. For males, the increase in reproductive
weight with ML was 1.5 times slower than that of the mantle muscle mass, but females demonstrated an increase in
reproductive weight that was 15% faster than that of mantle
muscle with ML (Table 3). Mature females also demonstrated greater variability in mantle weight with ML, compared with males (Table 3).
There was considerable variation among individuals
of both sexes in the relationship between the mantle
weighteML residuals and the reproductive weighteML residuals (Figure 2). Across all males, there was a positive correlation between the residuals from the mantle weighteML
and reproductive weighteML relationships (r ¼ 0.52,
n ¼ 190, p < 0.001), suggesting that males in better somatic
condition also had a greater commitment to reproductive
structures. Females, however, did not show an association
between the mantle weighteML residuals and the reproductive weighteML residuals (r ¼ 0.08, n ¼ 129, p ¼ 0.378;
Figure 2). Size of eggs within the oviduct of mature females
was not associated with female condition at the whole animal
level, given the lack of correlation between residuals
from the mantle weighteML relationship and egg size (r ¼
0.01, n ¼ 111, p ¼ 0.996). There was a weak negative correlation between egg number and residuals from the mantle
weighteML relationship when controlling for body weight
(r ¼ 0.23, n ¼ 119, p ¼ 0.01), suggesting that females in
poorer condition may have been producing larger batches
of eggs.
Residuals from the size-at-age relationship are a measure
of the difference in an individual’s lifetime growth from the
population average. As growth (Pecl, 2004), somatic condition, and reproductive investment vary substantially among
individual squid, the nature and degree of any association between these characteristics was of interest. Across all males
there was a weak significant positive correlation between
the reproductive weighteML and size-at-age residuals
(r ¼ 0.18, n ¼ 146, p ¼ 0.034), indicating that males that
had grown faster may also have had a higher anatomical
investment in reproductive structures than slower-growing
1000
(a)
G. T. Pecl and N. A. Moltschaniwskyj
Reproductive weight-ML
residuals
(a) 2.0
3
Summer
1.5
lighter mantle &
heavier reproductive
weight
Winter
2
Spring
1
0
-2
-1
0
1
2
Mantle weight-ML
residuals
Mean residual ± se
Autumn
1.0
(9)
0.5
(8)
(10)
(119)
(19)
0.0
-0.5
-1.0
-1.5
-2.0
-1
a
b
b
b
b
1
2
3
4
5
-2.5
heavier mantle &
lower reproductive
weight
-2
0
(b) 0.4
-3
4
heavier mantle &
higher reproductive
weight
3
(8)
(14)
Reproductive weight-ML
residuals
2
Mean residual ± se
(b)
(9)
6
0.2
(20)
(145)
0.0
-0.2
1
0
-1
0
1
Mantle weight-ML
residuals
-1
-2
-3
lighter mantle &
lower reproductive
weight
a
ab
b
ab
c
1
2
3
4
5
-0.4
0
6
Figure 3. Average residuals for each of the reproductive maturation
stages for Sepioteuthis australis females for (a) the size-at-age
relationship, and (b) the mantle weighteML relationship. The
values above each bar are the number of individuals in each stage.
The letters indicate means that are similar to those determined using
Hochberg’s GT2 method post hoc test.
-4
Figure 2. Residual values for each Sepioteuthis australis individual
from the mantle weighteML and reproductive weighteML relationships for (a) females and (b) males.
males. There was no relationship evident between the reproductive weighteML and size-at-age residuals for females
(r ¼ 0.10, n ¼ 129, p ¼ 0.277).
For female squid, both size at age and somatic condition
were related to stage of maturity. An examination of the
average mantle weighteML residuals between maturity
stages suggested that mature females had lighter mantles
for their length than immature females (F ¼ 16.51,
d.f. 4,195, p < 0.001; Figure 3a). Size-at-age residuals also
differed between female maturity stages, immature females
growing more slowly for their size than females at other
maturity stages (F ¼ 9.479, d.f. 4,164, p < 0.001; Figure 3b).
Season of hatching
The average residuals from the reproductive weighteML
regression equations differed as a function of hatching
season for both sexes (Figure 4), and are a measure of
the divergence in an individual’s investment in reproductive structures from the population average. Spring-hatched
males had a greater commitment to reproductive structures
than autumn- and winter-hatchers (F ¼ 5.329, d.f. 3,142,
p ¼ 0.002), although summer-hatched males had reproductive weights that were neither heavy nor light for their
length. In stark contrast to male squid, autumn- and
winter-hatched females had more energy invested in reproductive structures than summer- and spring-hatched
females (F ¼ 20.827, d.f. 3,125, p < 0.001).
The positive correlation between residuals from the mantle weighteML and reproductive weighteML relationships
evident across all males was clearly associated with season
of hatching (Figure 2). Males hatched in spring generally
had both heavier mantles and more investment committed
to reproductive structures than males hatched in autumn
and winter. Female squid did have a significant positive
correlation between mantle weighteML and reproductive
weighteML residuals for autumn (r ¼ 0.410, n ¼ 30,
p ¼ 0.025) and winter (r ¼ 0.502, n ¼ 81, p < 0.001), but
Squid resource allocation as function of size, growth, maturation, and hatching season
1.5
1001
800
Females
Summer
1.0
14
30
81
4
0.0
-0.5
-1.0
-1.5
a
b
1.5
b
a
Males
9
1.0
0.5
Oviduct egg number
Mean standardized residual ± se
0.5
700
Autumn
Winter
600
Spring
500
400
300
200
100
0
0
24
55
200
58
400
600
800
1000 1200 1400 1600 1800
Total body weight (g)
0.0
Figure 5. Estimated number of Sepioteuthis australis eggs in the
oviduct of mature females hatched in each season.
-0.5
ab
b
b
a
Summer
Autumn
Winter
Spring
-1.0
Figure 4. The average residuals from the reproductive weighteML
relationships for Sepioteuthis australis females and males hatched
in different seasons. The values above each bar are the number of
individuals in each hatching season. The letters below each bar indicate means that are similar to those determined using Hochberg’s
GT2 method post hoc test.
not summer-hatched females (r ¼ 0.303, n ¼ 14, p ¼ 0.292).
Nevertheless, summer-hatched females clearly have heavier
mantles and lower reproductive weights than the population
average (Figure 2). Interestingly, summer-hatched females
showed a positive correlation between reproductive
weighteML and size-at-age residuals (r ¼ 0.567, n ¼ 14,
p ¼ 0.034), suggesting that females that had grown faster
also had a larger commitment to reproductive structures for
their ML.
The disparities in somatic condition and reproductive
investment observed between squid hatched in different
seasons are substantial in real terms. A male hatched in
spring has a reproductive system that weighs 24% more
than an autumn- or winter-hatched male. The divergence
in mantle weight-at-length is even larger; a 300-mm-ML
male hatched in spring or summer may have a mantle
that weighs 400 g in contrast to 200 g for an autumn- or
winter-hatched male. Reproductive investment of an
autumn- or winter-hatched female is double that of springand summer-hatched females, although at 300 mm ML the
mantle weight is 100 g lighter in an autumn- or winterhatched female squid of the same length.
As there was a seasonal component influencing the degree
to which females invested in reproductive structures, it was
relevant to quantify the role of hatching season in explaining
variation in batch sizes of mature eggs and egg size within
the oviduct among females. Winter-hatched female squid
produced larger batches of eggs than spring- and summerhatched females (F ¼ 6.12, d.f. 3,94, p ¼ 0.001; Figure 5).
However, variability in mature egg size in the oviduct was
not a function of hatching season (F ¼ 0.72, d.f. 3,91,
p ¼ 0.545).
The ratio of females at different stages of maturation
differed between spring- and summer-hatched individuals
and females hatched in autumn and winter (Figure 6). In
the spring- and summer-hatched group, the proportion of
mature females (stages IV and V) >100 days old was
low, whereas the proportion of maturing females (stages
II and III) as old as 200 days was high. In the autumnand winter-hatched group, >75% of females older than
120 days were mature, and the proportion of maturing
females did not exceed 8% in any of the age classes
(Figure 6). Only four immature and maturing males were
caught (aged 100e160 days), and these were hatched in
autumn and winter. All other males from both hatching
groups were mature at 92 days of age.
Discussion
Mature Sepioteuthis australis had a high level of variation
in both reproductive effort and somatic condition. Reprosomatic allocation did not appear to be closely related to
size or shape of squid. Simultaneous change in physical
characters may give insight into associated important ecological changes (Shea and Vecchione, 2002), or potentially,
changes in the allocation of energy between somatic and
reproductive components. Although there was a good relationship between body size and gonad weight for both sexes
of S. australis, narrowing of the body appears to be more
related to moving from a globular shape to a more streamlined shape, not to the allocation of energy towards reproduction in bigger animals. Most body dimensions showed
a consistent growth relationship as squid increased in
size. The slowing of tentacle growth at 126 mm ML may
be associated with a change in the feeding ecology of
animals around that size. Funnel diameter also slowed in
growth (at around 315 mm ML) and is likely to be associated with speed of movement (Shea and Vecchione, 2002).
1002
G. T. Pecl and N. A. Moltschaniwskyj
% Frequency
(a)
(b)
100
100
75
75
50
50
25
25
0
0
90 110 130 150 170 190 210 230
90 110 130 150 170 190 210 230
Midpoint of age group (days)
Immature
Maturing
Mature
Figure 6. Proportion of immature (stage I), maturing (stages II and III), and mature (stages IV and V) Sepioteuthis australis females in
each 20-day age class for (a) spring- and summer-hatched, and (b) winter- and autumn-hatched individuals.
Once on the spawning grounds squid may undertake
smaller movements on and off the spawning beds, rather
than moving larger distances where speed may be important. Clearly, factors other than body size or shape have
major effects on the repro-somatic allocation of S. australis.
Season of hatching had a major influence on the life cycle
of both male and female Sepioteuthis australis, but the
effects were sex-specific. Although males and females
showed similar seasonal patterns in condition and growth
(see also Pecl, 2004), the relative levels of reproductive
investment responded differently with hatching season
between the sexes. Males hatched in warmer months had
a higher level of reproductive investment, whereas females
hatched in spring and summer had lower levels of reproductive investment relative to their autumn- and winter-hatched
counterparts. For males hatched in warmer temperatures,
faster growth and better somatic and reproductive condition
suggest that, when environmental conditions are favourable
for growth, males achieve faster somatic and reproductive
growth (Pecl, 2004; Pecl et al., 2004). A positive relationship between gamete production and increased growth rate
has also been attributed to favourable environmental conditions in other invertebrates (O’Dea and Okamura, 1999).
Although it appears that males did not experience energy
trade-offs between the processes of growth and reproduction, it is critical to note that the energetic costs associated
with reproductive behaviour have not been quantified.
Behavioural investment is likely to be substantial for males
competing with other males for mates and who subsequently defend their mates from other males (Hanlon and
Messenger, 1996; Jantzen and Havenhand, 2003). Additionally, although life-history trade-offs should be detectable as negative correlations between the relevant traits
(e.g. reproductive output vs. energy storage; Roff, 1986),
trade-offs may be masked by variation in accrual of
resources (Doughty and Shine, 1997). van Noordwijk and
de Jong (1986) use the analogy of the positive correlation
commonly evident in the value of a person’s house and
car e a higher income may provide for both an expensive
house and an expensive car, rather than a more expensive
house equating to a cheaper car. This explanation implies
that male Sepioteuthis australis may be better at acquiring
resources than females. However, this is unlikely, given
that females are caught more frequently with ingested
food than are males (Jackson and Pecl, 2003). Instead, it
may be a reflection of the greater total energy commitment
of females to reproduction than males.
Female Sepioteuthis australis hatched during the cooler
temperatures of autumn and winter grew more slowly, and
were in poorer somatic condition. However, they had
a greater level of reproductive investment, and may have
been producing larger egg batches than spring- and summerhatched females. Batch fecundity at size also has a seasonal
component in some fish species (Kjesbu et al., 1996),
whereas others may adjust both egg size and egg number
according to energy resources and environmental conditions
(e.g. Pacific herring; Hay and Brett, 1988). In cephalopods,
batch size may have a corresponding relationship with
frequency of batch deposition. Spring- and summer-hatched
S. australis females may have allocated lower levels of
investment into reproduction at any point in time, but the
allocation to reproduction may have been partitioned into
smaller, more numerous egg batches. Conversely, autumnand winter-hatched females may have produced larger and
fewer egg batches. Captive female Loligo pealei (Maxwell
and Hanlon, 2000) and Idiosepius pygmaeus (van Camp,
1997) also lay smaller batches of eggs more frequently or
larger batches less frequently. This dichotomy in reproductive strategy adopted by individuals within a population
appears common for cephalopods (Boyle et al., 1995;
Moltschaniwskyj, 1995a) and has been suggested to be
a function of when energy reserves are available for gametogenesis (Moltschaniwskyj and Semmens, 2000). This study
suggests that seasonal differences in biotic and abiotic conditions experienced by individual squid may play a large role in
determining when energy is made available for reproduction.
Squid resource allocation as function of size, growth, maturation, and hatching season
Interestingly, the extreme variation evident in mature egg size
among females could not be attributed to hatching season or
female condition. Whereas reproductive output is apparently
determined at least in part by factors associated with season
of hatching, the way in which it is partitioned between size
and number of offspring varies independently of season.
Males that grow faster are more likely to be in better
somatic condition (Pecl, 2000), and males that had grown
faster also had greater levels of reproductive investment
(this study). Although there was a positive relationship
between these factors for summer-hatched females, the
same positive relationship between growth and reproductive investment was not evident across all females. This
suggests that, although level of reproductive investment is
related to season of hatching, as is growth and condition,
reproductive investment is not necessarily directly associated with growth rate. Energy used for reproduction is
not driving the growth patterns observed in tropical and
subtropical populations of Sepioteuthis lessoniana or
S. australis from more sub-temperate locations (Pecl,
2000). This pattern is not restricted to neritic squid; the
oceanic ommastrephid Nototodarus gouldi has levels of
reproduction and somatic condition that are primarily independent of growth rate as well (McGrath-Steer, 2004).
The influence of hatching season on the life-history characteristics of Sepioteuthis australis results in a very interesting population cycle. Females that hatched over spring and
summer deposited eggs over the next winter, 5e9 months
later, and females hatched in autumn and winter reproduced
the next summer. This is an alternation of generations, where
squid that are slow growing and in poor condition but with
a high level of reproductive investment produce the next
generation with a completely different set of life history characteristics. However, it must be emphasized that squid from
this study were caught over discrete time periods, and the
reality of any consistent temporal change in life history characteristics is going to be a progression between these two
extremes, one that will only be fully elucidated by intensive
sampling at regular intervals throughout the year.
Sepioteuthis australis has a high degree of plasticity in its
life history processes in terms of growth, reproduction, and
repro-somatic investment, and such flexibility in life history
strategy within populations is consistent with an opportunistic lifestyle (Moltschaniwskyj and Semmens, 2000). This
study revealed little evidence of trade-offs between
reproduction and growth or condition of individuals. This
is usually evident in species in which there is a defined
and obvious accumulation of stored energy prior to gonad
growth, followed by use of stored energy for gonad growth,
a process that is often associated with an environmental trigger (e.g. photoperiod or temperature). However, the general
model for many cephalopods is that energy for reproduction
is sourced directly from ingested food, not from stored
energy (e.g. Loligo gahi: Guerra and Castro, 1994; Loligo
forbesi: Collins et al., 1995; Illex argentinus: Rodhouse
and Hatfield, 1990; Photololigo sp.: Moltschaniwskyj, 1995a;
1003
Sepioteuthis lessoniana: Moltschaniwskyj and Semmens,
2000; Sepia pharaonis: Gabr et al., 1999; Eledone spp.:
Rosa et al., 2004; Illex coindetii and Todaropsis eblanae:
Rosa et al., 2005). Cephalopods ‘‘live for today’’, an approach to life that places no reliance or dependence on
‘‘savings’’. Therefore, reproductive growth is determined
by the amount of food being acquired. However, like
any currency or resource, the availability and use of
food will be the summation of both long- and shortterm processes that lack predictability, and more
importantly a record of use. The opportunistic and immediate use of resources is a logical strategy for species that
have no long-term future or have reliable access to
resources. However, the environmental or biological triggers that initiate gonad growth and maturation are
unknown, yet are important in determining the timing
of energy allocation to somatic and reproductive growth
during the maturation process.
Acknowledgements
This project would not have been possible without the substantial cooperation of Tasmanian commercial squid
fishers. We are grateful to George Jackson for determining
the age of some of the S. australis individuals from Tasmania, and to all those people who provided assistance in the
field. The Freycinet Lodge in Coles Bay, Tasmania,
provided support for this project. The work was supported
by a grant from Marine Research Laboratories, Tasmania,
a James Cook University Merit Research Grant (George
Jackson and GP), and a JCU Collaborative Grant (George
Jackson and GP). The research was conducted while GP
was supported by an Australian Postgraduate Award.
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