Download Evaluation of alternative hypotheses to explain

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Evaluation of alternative hypotheses
to explain temperature-induced life
history shifts in Daphnia
D. WEETMAN1* AND D. ATKINSON
POPULATION AND EVOLUTIONARY BIOLOGY RESEARCH GROUP, SCH7OOL OF BIOLOGICAL SCIENCES, UNIVERSITY OF LIVERPOOL, LIVERPOOL L69 7ZB, UK
1
PRESENT ADDRESS: MOLECULAR ECOLOGY AND FISHERIES GENETICS LABORATORY, DEPARTMENT OF BIOLOGICAL SCIENCES, UNIVERSITY OF HULL,
HULL HU6 7RX, UK
*CORRESPONDING AUTHOR:
[email protected]
Negative correlations between environmental temperature and body size are widespread in planktonic
organisms, and ectotherms generally, but remain poorly understood. Here we evaluate experimentally
two alternative hypotheses suggested to explain life history shifts induced by raised temperature using
parthenogenetic clones from two Daphnia species. Explanation 1 proposes that the life history shifts
could be adaptive if increased temperature is used as an indirect cue to indicate increased risk from
size-selective predators. Explanation 2 proposes that at larger body size energy becomes more
limiting as temperature increases because of a less favourable assimilation: metabolism balance. In a
factorial laboratory experiment we examine the effects of three rearing temperatures on the growth
and reproductive traits of Daphnia raised in water with fish kairomone, Chaoborus kairomone, or in
uncontaminated water. None of the three predictions of explanation 1 were met by the data. In both
D. pulex and D. curvirostris, and some other published studies, data suggested that at larger body
sizes the sum of growth and reproduction was lower at high temperature, supporting our prediction
from explanation 2. However, we propose a novel third explanation based on new evidence of
temperature-dependence in both reproductive effort and cost in D. pulex.
INTRODUCTION
In ectotherms, survival, fecundity and competitive ability
often depend strongly upon body size (Stearns, 1992).
Temperature is a critical environmental factor affecting
ectotherm life histories, with pre-adult growth rates generally faster in warmer conditions (Cossins and Bowler,
1987). Faster growth mediated by higher temperature
would be expected to provide an advantage in allowing
more rapid attainment of a large body size, but smaller
adult size at raised temperature has been recorded in
over 80% of organisms studied [reviewed by (Ray, 1960;
Atkinson, 1994)]. Most planktonic organisms studied to
date under controlled laboratory conditions have been
found to conform to this temperature–body size rule
[reviewed by (Moore et al., 1996)], including copepods
(Campbell et al., 2001; Lee et al., 2003), rotifers (Stelzer,
2002), a wide range of protists (Montagnes and Franklin,
2001; Atkinson et al., 2003), and some [e.g. (Perrin,
1988; Sakwinska, 1998; Giebelhausen and Lampert,
2001)], but not all [e.g. (Doksaeter and Vijverberg,
2001; Kappes and Sinsch, 2002; Lass and Spaak, 2003)]
cladocerans.
Among the hypotheses that have been proposed to
explain the counter-intuitive temperature–body size rule
are adaptive explanations and biophysical models
[reviewed by (Atkinson and Sibly, 1997)]. Adaptive explanations proposed to explain body size reduction at higher
temperature are based on the potential temperaturedependence of advantages provided by either precocious
reproduction or small body size (Atkinson, 1994). One
such explanation proposes that because ectothermic predators are likely to be more active and often more abundant during warmer periods, particularly in seasonal
environments, earlier maturation at a smaller size could
be an adaptive strategy if risk of mortality is correlated with
temperature (Culver, 1980; Atkinson, 1994). The generality of this prediction depends somewhat on the nature of
predator–prey interactions assumed by life history models,
doi: 10.1093/plankt/fbh013, available online at www.plankt.oupjournals.org
Journal of Plankton Research Vol. 26 No. 2 Ó Oxford University Press 2004; all rights reserved
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but it is applicable in any case where animals are at
risk from predators preferring larger-bodied prey, when
smaller body size and higher, earlier, reproductive effort
are favoured (Michod, 1979; Law, 1979).
As major grazers of phytoplankton and prey for planktivorous fish, Daphnia are important members of lake
communities in many temperate regions. Most species
show pronounced indeterminate growth, and both
resource acquisition (Lynch, 1980) and mortality (Zaret,
1980) are usually size-dependent. Taylor and Gabriel
(Taylor and Gabriel, 1992) modelled optimal age and
size at maturity for Daphnia, using categories of survivorship curves reflecting either vertebrate or invertebrate
predation. Their model predicts that when survivorship
decreases with increasing Daphnia body size (vertebrate
predator), females should mature earlier and at a smaller
size, investing more resources into reproduction to maximize the number of offspring produced. Under the
opposite predation regime, where survivorship increases
with body size (invertebrate predator), Daphnia should
delay reproductive investment and mature later and at
a larger size. Female Daphnia in many experiments have
shown the predicted life history responses in the presence
of fish kairomone (Riessen, 1999). Life history responses
to Chaoborus kairomone show somewhat more variability
between studies (Riessen, 1999), but many authors report
some correspondence to Taylor and Gabriel’s model
[references in (Riessen, 1999)].
Higher water temperature has frequently been implicated as a causal agent involved in the summertime
decrease in population mean body size observed in
field studies of Daphnia and other Cladocera (Kerfoot,
1974; Threlkeld, 1979; Culver, 1980; Brambilla, 1982;
Pijanowska, 1990). If Daphnia use warmer temperature as
a cue to indicate increased risk from predators preferring
larger-bodied daphnids (e.g. fish), it can be predicted
that (i) responses to temperature should be qualitatively
similar to those shown to fish kairomone. Furthermore,
an increase in risk should lead to an increase in response,
thus we also predict that (ii) responses to fish kairomone
should be enhanced at higher temperature. However,
(iii) responses to temperature should be reversed in the
presence of a predator electing smaller-bodied daphnids
(e.g. late-instar phantom midge larvae, Chaoborus sp.).
A widely applicable biophysical model, devised by
Perrin (Perrin, 1988, 1995) and von Bertalanffy (von
Bertalanffy, 1960) suggests a greater progressive reduction in the balance of energy assimilated:metabolic
energy lost as body size increases in warm, than in
cool, conditions. Although this model does not necessarily predict smaller body size at higher temperature,
particularly in taxa such as Daphnia that show pronounced indeterminate growth, it does make the general
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prediction that energy should become relatively more
limiting at larger body sizes in warmer conditions,
which may make large size unfavourable. Thus, our
prediction is that at large body sizes the sum of growth
+ reproduction would be expected to be lower (decline
more) at higher temperatures.
In a factorial experiment we investigate the effects of
temperature and kairomones from fish and Chaoborus on
the life histories of single sympatric clones of D. pulex and
D. curvirostris to test the three predictions from the adaptive
explanation described above (explanation 1) and the prediction from the Perrin–von Bertalanffy biophysical model
(explanation 2). Our results do not support any of the
predictions of explanation 1 and although the data could
be compatible with the prediction from explanation 2, based
on evidence for temperature-dependence of reproductive
effort and costs we propose a novel third explanation.
METHOD
Experimental animals and conditions
Experimental females were genetically identical descendants of a single clone of either D. pulex or D. curvirostris
taken from Sefton Park Lake, Liverpool, UK
(54 220 4800 N, 2 530 2400 W). This man-made lake is a
shallow (generally <1.5 m depth) isolated water body, the
base of which is largely covered in dense weed. The lake
is stocked with roach, Rutilus rutilus, crucian carp, Carassius
carassius, tench, Tinca tinca, and also contains three-spined
sticklebacks, Gasterosteus aculeatus. In summer, particularly
in the shallow littoral areas, the lake becomes densely
populated with young-of-the-year roach and stickleback
fry. Identity of the Daphnia species was confirmed according to Johnson ( Johnson, 1952), and Scourfield and
Harding (Scourfield and Harding, 1966).
Daphnia were raised individually in 30 mL vessels
containing 22 mL of aged, filtered (through Whatman
grade 6 filter paper) water from their source lake, with
diffuse lighting from a 60 W cool fluorescent tube set
to a 16 h light:8 h dark regime. The vessels were loosely
suspended at the neck on racks in large water baths
(within a controlled temperature room), in which constant thermal conditions were maintained. Females were
raised under experimental temperatures of 13, 18 or
21 C and a food concentration of 3 105 cells
of (frequently subcultured) Scenedesmus subspicatus mL1
(2.5 mg C mL1). The algae was added to large
volumes of experimental water, which was then divided
into the individual vessels to provide fresh medium and
food each day. Sinking of algae was reduced by aeration
in the water bath under each experimental vessel, which
caused agitation of the vessels within the racks. In a
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batch culture system such as ours, the use of a relatively
small water volume in which to rear Daphnia will
inevitably lead to a reduction in food concentration
within experimental vessels during the 24 h period
prior to replenishment. However, Lynch et al. (Lynch
et al., 1986) found that D. pulex reared in 40 mL vessels,
containing a total daily carbon provision similar to that
in our experiment, showed very similar long-term net
production to those reared in 200 mL water that contained five-fold higher total daily algal carbon but at
lower concentration. Since the change in algal concentration would have been much less marked in the larger
vessels, and these were not expected to provide limiting
conditions, the data of Lynch et al. suggest that the food
concentration provided in our experiment would not
reduce maximum Daphnia net production, even in the
small water volumes used.
In order to ensure adequate acclimation to treatment
temperatures all experimental animals were third generation descendants of a single large female isolated from
stock culture, with each generation raised under experimental temperature and food conditions. Daphnia were
raised individually in the vessels from birth and carefully
transferred by wide-mouth pipette to new water (with
food) each day. Animals were measured during transfer
(following moults) by placing them on a glass slide in a
small volume of water, and recording their length (excluding tail-spine) under a compound microscope fitted with
optical micrometer. Any offspring produced were also
removed at this time, counted, and for D. pulex these
were preserved for measurement. Body lengths were converted to dry weights using the regressions ln W (mg) =
2.559 ln length (mm) – 15.372 (R2 = 0.97) for D. pulex and
ln W (mg) = 2.564 ln length (mm) – 15.419 (R2 = 0.97) for
D. curvirostris. A further regression was calculated to convert
offspring dry weight to egg dry weight in D. pulex: egg
dry weight (mg) = 0.820 offspring dry weight (mg) + 0.258
(R2 = 0.74). All regression equations were calculated from
length:weight measurements specific to these Daphnia
clones (Weetman, 2000). Experimental treatments were
continued until individuals had produced five broods of
offspring. Because of a thermostat malfunction, data for
the D. curvirostris clone at 13 C were only available until the
sixth instar. Sample sizes were equal for predator cue and
control groups and for each temperature were: n = 19
(13 C); n = 19 (18 C); n = 13 (21 C) for D. pulex, and
n = 15 (13 C), n = 19 (18 C); n = 13 (21 C) for D. curvirostris.
Water conditioned by Chaoborus sp. was produced by
keeping 12 fourth instar larvae in 500 mL of aged, filtered
lake water for 24 h at 17–18 C (equivalent to 24 L1).
Fifty early instar D. pulex or D. curvirostris (whichever was
the experimental species) were provided as food. To give
a concentration equivalent to 6 Chaoborus L1, 5.5 mL of
this water containing predator kairomone was diluted
four-fold by addition to 16.5 mL of aged, filtered lake
water in each experimental container, following filtration
and 1 h strong aeration of the conditioned water. Water
conditioned by fish was produced by keeping two sticklebacks (4 cm standard length) in 2 L of lake water for 24 h
at 18 C (equivalent to 1 fish L1) with 50 large daphnids
as prey. Again, this conditioned water was filtered and
aerated before a ten-fold dilution by addition of 2.2 mL of
conditioned water to 19.8 mL of aged, filtered lake water
per vessel, giving a concentration equivalent to 0.1 fish L1.
Control vessels received 22 mL of lake water that had
been filtered and aerated in the same way. The medium
in all vessels was changed daily and all were cleaned in very
hot water (to destroy bacteria) and dried before each use.
High numbers of predators were used to condition water,
and this was changed daily, in an attempt to maintain
kairomone concentrations above the level required to elicit
maximum responses [e.g. (Reede, 1995; Weetman and
Atkinson, 2002)]. Within each water bath, predator cue
and control group individuals were distributed randomly.
Data analysis
All data were tested for normality using the one-sample
Kolmogrov–Smirnov procedure. Homogeneity of variances was checked using Levene’s test. ANOVA and
t-tests were used wherever possible, but when parametric
assumptions could not be met following natural log
transformation, Kruskal–Wallis tests and Mann–Whitney
U-tests were employed. Patterns of growth were analysed using the von Bertalanffy equation in the form
suggested by Perrin (Perrin, 1988): Wt = WA(1 – c.exp–k.t )3.
Wt is weight at time t, WA is asymptotic weight, parameter
c relates to the proportion of the maximum weight
remaining for growth at time 0 (= birth), and k is the
growth coefficient, describing the degree of curvature in
the weight–time function. Parameters were fitted to raw
growth data for individuals by non-linear regression.
Juvenile growth rate (gj) was calculated as (lnW – lnW0)
a1; where a is age at maturity. Adult growth rate (ga)
was calculated as (lnW10 – lnW) (t10 – a)1 where t10 is
age and W10 is weight at the beginning of the tenth instar
when the experiment was terminated. ANCOVA was
used to test for differences among the slopes of relationships between reproductive variables and maternal body
weight. Because this necessarily used more than one data
point from each female, the significance of F-ratios
was calculated using degrees of freedom based on the
number of replicate females rather than the number of
data points. For D. pulex total clutch weight was determined
by multiplying the mean weight of a mother’s offspring by
the number of offspring to give the total weight of the
brood, then converting this to the total weight of eggs
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(C ). Total growth plus reproduction (P, mg dry weight)
during an instar was calculated as the sum of the clutch
weight carried in the following instar (Ci + 1) and the
growth increment (Wi + 1 – Wi). Reproductive allocation
(RA) reflects the division of resources between growth and
reproduction and is defined here as the proportion of dry
weight produced that was invested into reproduction during an instar: C.P 1 100. Finally, the relationship
between early and later reproduction was tested in
D. pulex. Such relationships are frequently masked by
covariation of reproductive output with body weight (Bell
and Koufapanou, 1986; Stearns, 1992), therefore, comparison was made between relative clutch weights (e.g.
Ci.Wi1). Moreover, to facilitate interpretation we chose
to make the comparison linear by designating the mean
relative clutch weights of reproductive events one and
two as ‘early stage’ reproduction, with that of relative
clutch weights three, four and five as ‘later stage’ reproduction. This division is appropriate because for many organisms the first two reproductive events often make the
greatest contribution to fitness (Stearns, 1992). This relationship was then analysed by linear contrasts using ‘stage’
as a within-subject term and interactions with the temperature and different predator kairomone treatments (betweensubjects terms) to show the effects of these on the linear
contrast. SPSS 8.0 for Windows was used for all tests.
RESULTS
Body size and growth
Weight at maturity (W) was significantly influenced by
temperature in the clone of each species (Table I). In the
absence of predator kairomones, maturation weight was
similar at the two higher temperatures in D. pulex (Figure 1a).
Yet when differences in birthweight were taken into
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account by calculating the ratio of weight at maturity:
birth, mean values increased with temperature in both
species with all pairwise comparisons between temperatures highly significant (P < 0.01). W was significantly
smaller for D. pulex, but not D. curvirostris, raised in the
presence of fish kairomone (Figure 1a, Table I). There
was no significant interaction between fish kairomone
treatment and temperature in either species (Table I).
Asymptotic weight estimates (WA) decreased significantly
with increasing temperature in D. pulex but the opposite was
observed in D. curvirostris (Figure 1b, Table I). For D. pulex,
but not D. curvirostris, fish kairomone treatment reduced
WA, and there were no significant interactions with temperature. Body size responses to Chaoborus kairomone in
both species were rather minor (Figure 1a,b) and significant
only as interaction terms with temperature (Table I), with
the exception of WA in D. curvirostris, which was significant as
a main effect, being reduced to some extent by the presence
of Chaoborus kairomone at both temperatures (Figure 1b).
Age at maturity decreased and juvenile growth rate
increased with temperature in both D. pulex and D. curvirostris (Table II). Following maturity, D. curvirostris continued
to grow more rapidly at higher temperature but in D. pulex
adult growth rate was lowest at 21 C (Table II). Neither
class of predator kairomone affected age at maturity in
either species (all Kruskal–Wallis test results within each
temperature, NS), and the only effect on growth rates was
for D. pulex raised with Chaoborus kairomone, which at
18 C grew significantly more slowly than controls before
maturity (P < 0.05) but faster as adults (P < 0.01).
Reproduction
In general the number of offspring produced per brood
was strongly dependent upon maternal weight in both
species (Pearson’s r = 0.71, P < 0.001 for D. pulex;
Pearson’s r = 0.75, P < 0.001 for D. curvirostris). However,
Table I: ANOVA F-ratio values showing the effects of temperature and the presence/absence of different
predator kairomones on body weight measures in D. pulex (D.p.) and D. curvirostris (D.c.)
Species
Trait
D.p.
W
D.c.
D.p.
Temperature
Fish
53.6***
26.5***
28.9***
WA
D.c.
3.3
280.8***
38.7***
Temperature
D.p.
W
D.c.
D.p.
WA
D.c.
Temp Fish
2.3
1.3
8.7**
1.0
2.5
0.3
Chaoborus
Temp Chao
24.0***
0.4
3.9*
24.3***
0.1
3.5*
274.1***
1.3
3.3*
23.7***
4.4*
0.6
***P < 0.001, **P < 0.01, *P < 0.05.
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Asymptotic weight (µg, ln transformed)
Weight at maturity (µg, ln transformed)
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a
4.1
3.9
3.7
3.5
3.3
4.9
4.7
4.5
4.3
4.1
b
3.9
13
18
21
Temperature (˚C)
Fig. 1. Mean (± 95% confidence interval) size-at-stage measures for
D. curvirostris (open symbols) and D. pulex (closed symbols) raised at
three experimental temperatures, in uncontaminated lake water
(circles), water containing kairomones from Chaoborus larvae (squares)
or from fish (triangles). (a) Weight at maturity, W. (b) Asymptotic
weight, WA.
the slope of this regression differed between temperatures in both species, but not between predator cue
treatments. (Table III). This is evident in both D. pulex
and D. curvirostris (Figure 2) as a decrease in the slope of
clutch size on maternal size as temperature increased. In
the clone of D. pulex, mean relative clutch size was very
similar at the two lower temperatures but significantly
smaller at 21 C (P < 0.001), and significantly higher
than controls at all temperatures when raised with fish
kairomone (Table III). Considered across all clutches,
the effect of temperature on mean relative clutch size
was rather minor in D. curvirostris, largely because of
ontogenetic variation in clutch sizes (Figure 2), and
some inconsistency between predator kairomone treatments (significant interaction term in Table III). The
trend however, albeit non-significant, was the same as
for D. pulex: larger mean relative clutch sizes in the fish
kairomone treatment and smaller in the Chaoborus treatment, with controls intermediate.
In D. pulex reproductive allocation (RA) depended
strongly on body weight (Pearson’s r = 0.76, P < 0.001)
but temperature significantly affected the slope of this
regression (Figure 3a) such that maximum reproductive
allocation was reached both at an earlier stage and
smaller size as temperature increased. Relative RA (i.e.
RA relative to body weight) was significantly affected by
the presence of both fish and Chaoborus kairomone,
although in neither case was there a significant interaction with temperature (Table IV). The response to fish
kairomone, of higher relative RA than controls, was
much greater than that to Chaoborus kairomone, which
was slightly, but consistently, lower than controls (Figure 3b).
RA was reduced between ‘early’ and ‘late’ reproductive stages (r = 0.39, P < 0.001). Temperature significantly altered the effect of reproductive stage on RA,
Table II: Means (standard deviation) for some growth parameters in each Daphnia species, with effects
of temperature tested by ANOVA (F), Kruska–Wallis tests (2) or t-tests (t)
13 C
18 C
21 C
Effect of
x
x
x
temperature
10.89 (0.47)
5.56 (0.51)
5.00 (0.00)
w22
38.96***
gj (day )
0.72 (0.06)
1.93 (0.27)
2.36 (0.14)
w 22
38.28***
ga (day1)
0.07 (0.01)
0.08 (0.01)
0.06 (0.01)
w22
17.73***
12.69 (0.48)
6.26 (0.73)
5.00 (0.00)
w 22
41.82***
0.58 (0.01)
1.70 (0.18)
2.80 (0.21)
w 22
38.61***
0.07 (0.01)
0.09 (0.01)
t26
6.50*
D. pulex
a (day)
1
D. curvirostris
a (day)
1
gj (day )
ga (day1)
n/a
***P < 0.001, **P < 0.01, *P < 0.05.
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Table III: Effects of temperature and predator kairomones on the interaction between ln number of offspring
per clutch and ln maternal weight (slope, ANCOVA F-ratio), and on the mean number of offspring produced
relative to maternal weight (mean, ANOVA F) in D. pulex (D.p.) and D. curvirostris (D.c.)
Species
Effect on
D.p.
Slope
45.2***
Mean
12.5***
Slope
33.9***
D.c.
Temperature
Mean
0.1
D.c.
0.9
18.2***
0.6
Temperature
D.p.
Temp Fish
Fish
0.6
2.2
1.7
1.1
3.1*
Temp Chao
Chaoborus
Slope
44.5***
0.0
0.6
Mean
14.5***
1.0
0.7
Slope
38.7***
2.0
2.6
Mean
3.7*
0.6
0.2
(ln) Number of offspring per clutch
***P < 0.001,**P < 0.01,*P < 0.05.
3.3
3.3
D. curvirostris
D. pulex
2.9
2.9
2.5
2.5
2.1
2.1
1.7
3.3
3.5
3.7
3.9
4.1
4.3
1.7
3.6
4.5
(ln) maternal weight (µg)
3.8
4.0
4.2
4.4
4.6
(ln) maternal weight (µg)
4.8
Fig. 2. The influence of rearing temperature on the relationship between fecundity and maternal weight across five clutches (mean ± 95%
confidence interval shown for each) in both Daphnia species. Triangles, 21 C; squares, 18 C; circles, 13 C. Slopes of all lines are significantly
different from zero (P < 0.05), other than for D. pulex at 21 C (line not plotted), and the effect of temperature on slopes was significant (see text).
but predator kairomones did not (Table IV). The trend in
correlation coefficients (0.05 at 13 C; 0.20 at 18 C;
0.35 at 21 C) suggests that the relationship between
early and later reproduction became more negative as
temperature increased.
DISCUSSION
Evaluation of explanation 1: temperature
acts as a cue for increased predation risk
and enhances responses to predator cues
We predicted that if warmer conditions are used as a cue
to indicate raised risk from fish predators, which prefer
larger-bodied Daphnia, (i) life history responses to temperature should be qualitatively similar to those induced
by fish kairomone. Furthermore, if temperature
enhances responses to predator cues (ii) life history shifts
induced by fish kairomone should be quantitatively
greater at higher temperature, but (iii) responses to temperature should be reversed by the presence of Chaoborus
kairomone.
D. pulex raised in the presence of fish chemical cues,
largely showed the adaptive responses predicted by
Taylor and Gabriel (Taylor and Gabriel, 1992) with
body weight reduced relative to controls, both at maturity
(W) and at its asymptote (WA). Reproductive allocation
(RA) was also raised, as were numbers of offspring
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(ln) Reproductive allocation (RA)
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4.6
13 degrees
18 degrees
4.5
21 degrees
4.4
4.3
4.2
a
4.1
2.8
3.3
3.8
4.3
(ln) Reproductive allocation (RA)
4.5
Fish
Chaoborus
4.4
Control
4.3
4.2
b
4.1
2.8
3.3
3.8
4.3
(ln) maternal weight (µg)
Fig. 3. Mean (± 95% confidence interval) percentage reproductive
allocation (RA) in D. pulex plotted against body weight during five
reproductive instars. All slopes are significant (P < 0.05). (a) Effect of
temperature (predator cue treatments pooled). (b) Effect of predator
cues (temperatures pooled). Both intercepts and slopes were significantly affected by rearing temperature (see text for test results).
produced, relative to the reduced maternal size. The
responses of D. curvirostris to fish kairomone were qualitatively similar but of a much lesser magnitude.
Responses to raised temperature were generally more
pronounced than those to kairomone and also qualitatively somewhat different. Higher temperature did not
result in a decrease in Wa, but did reduce WA in the
clone of D. pulex. RA was greater in warmer conditions in
D. pulex, but not in the same way as the shift induced by
fish kairomone, because not only the mean level of RA,
but also the slope of the RA on body weight regression,
increased at higher temperature. Moreover, raised temperature did not induce a greater level of response to fish
kairomone in any of the traits analysed. Therefore, the
predictions (i) and (ii) of explanation 1 are not supported.
The lack of temperature-dependence of responses to fish
kairomone corroborates the findings of recent studies on a
clone of D. magna (Sakwinska, 1998), a clone of D. hyalina
galeata (Doksaeter and Vijverberg, 2001) and several
clones of D. galeata (Lass and Spaak, 2003).
Following the rejection of predictions (i) and (ii), prediction (iii) becomes somewhat redundant as a component of explanation 1. However, it is still valid to test the
prediction that responses to Chaoborus kairomone might
be temperature-dependent, because of the accelerating
effect of temperature on Chaoborus feeding on Daphnia
(Spitze, 1985). Compared with those induced by fish
kairomone, life history responses to Chaoborus kairomone
were fairly minor in both species. Nevertheless, in
D. pulex, reproductive allocation was reduced, relative
to controls, concordant with model predictions (Taylor
and Gabriel, 1992), but treatment with Chaoborus kairomone showed no significant ANOVA interaction with
rearing temperature. Significant kairomone temperature
Table IV: Effects of temperature and predator kairomones on: the interaction between ln reproductive
allocation (RA) and ln body weight (slope, ANCOVA F-ratio); mass-specific RA (mean, ANOVA F)
and on the within-subjects stage contrast between relative clutch weights at early and later
reproductive stages in D. pulex
Effect on
Temperature
Slope
38.4***
Mean
110.4***
Stage contrast
Fish
4.0
40.6***
86.6***
Temperature
0.2
Chaoborus
Temp Fish
0.8
2.9
0.8
Temp Chao
Slope
33.9***
0.3
0.8
Mean
71.6***
5.8*
0.6
Stage contrast
75.8***
0.0
1.1
***P < 0.001, **P < 0.01, *P < 0.05.
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interactions were found for body weight measures in
both species, but these did not reflect an enhanced
response at higher temperature. Walls and Ventelä
(Walls and Ventelä, 1998) have also tested the life history
responses of D. pulex to Chaoborus cues at two temperatures. Their results were similar in that some significant
ANOVA interactions were found, but these did not
reflect an enhancement of response. The biological significance of these inconsistent anti-Chaoborus responses at
different temperatures is currently unclear.
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(Richman, 1958), so pronounced adult growth at high
temperatures, unless accompanied by high fecundity,
does not necessarily indicate a favourable energetic balance. Thus, data from the present study and at least two
others seem to support the prediction we derived from
the Perrin–von Bertalanffy biophysical model, that at
larger body sizes the net energy available for growth
and reproduction will act as a greater constraint as
temperature increases.
Temperature dependence of reproductive
effort and cost: is a third explanation
required?
Evaluation of explanation 2: higher
temperature reduces energy availability
at large size
The effect of temperature on the life histories was far
greater than that of predator cues. As expected for
Daphnia (Goss and Bunting, 1983) and ectotherms generally (Atkinson, 1994), age at maturity declined and
juvenile growth rate increased significantly with raised
temperature in both species. However, contrary to what
is observed in most ectotherms, size at maturity
increased with temperature in D. pulex and D. curvirostris,
at least once differences in birthweight were accounted
for. Following maturity the growth patterns of the two
species diverged. At the highest temperature, adult
growth rate in D. pulex fell below that recorded in cool
conditions and estimated asymptotic weight declined
very markedly with increasing temperature. Yet in
D. curvirostris adult growth continued to proceed more
rapidly at high temperature toward the largest asymptotic weight. Nevertheless, despite these divergent adult
growth patterns, the effect of temperature on reproduction showed some similarity. In both D. pulex and
D. curvirostris, temperature significantly reduced the
slope of the regression of offspring number on maternal
weight, i.e. larger (and older) adult females produced
fewer offspring for their size in warmer conditions.
This has been recorded in two other studies of Daphnia:
on mixed clonal groups of D. pulex (Brambilla, 1982) and
a D. magna clone (McKee and Ebert, 1996). Although the
number of offspring is considered here, the effect on
total brood weight is in fact likely to be greater because
most studies of Daphnia show smaller offspring at higher
temperatures (Atkinson et al., 2001).
This consistent effect of temperature on fecundity is
found despite variable thermal effects on body size: in
both the present and Brambilla’s study of D. pulex, raised
temperature led to smaller body size, at least by later
adult stages, yet a warmer environment had the opposite
effect on D. curvirostris (this study) and D. magna (McKee
and Ebert, 1996). Adult Daphnia expend the vast majority of their available resources on reproduction
Reproductive effort, measured by reproductive allocation,
was increased relative to body size at higher temperature.
To our knowledge, this has not been previously reported in
zooplankton. Indeed, examples of temperature-dependent
changes in indices of reproductive effort appear to be very
rare in ectotherms, e.g. in the fishes Oryzias latipes
(Hirshfield, 1980) and Poecilia latipinna (McManus and
Travis, 1998). Diversion of resources from growth to reproduction may have been the proximate cause of smaller
asymptotic size at higher temperature in D. pulex.
Another potential trade-off is between early and later
reproductive output. This would be expressed as a negative correlation within individual mothers between
clutch weights of early (first and second) clutches relative
to body weight, and relative weight of later clutches
(3–5). We found a significant effect of temperature on this
ontogenetic relationship between early and later reproductive output. The increasingly negative trend between
early and later reproductive output across temperatures
suggests that increased temperature produced a more antagonistic relationship between early and later reproduction.
A thermally induced increase in reproductive effort
may be an adaptive response, but from the present data
it is unclear what correlate of raised temperature led to
this. Indeed, it is interesting that fish kairomone induced
a shift to a higher level of reproductive effort, while the
response induced by raised temperature was for a faster
increase towards maximum reproductive effort. Yet only
temperature affected the relationship between early and
later reproduction. Perhaps then reproduction may
become more costly for Daphnia at higher temperature,
e.g. because of a requirement for greater embryo spacing
(Lee and Strathmann, 1998), more active ventilation of
eggs within a brood pouch (Dick et al., 1998), or greater
loss of resources invested into eggs because of higher
embryonic respiration (Atkinson et al., 2001). This
could reduce potential for future reproduction, which
would favour increased early investment (Sibly and
Calow, 1984; Jönsson et al., 1998). Alternatively, raised
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TEMPERATURE-INDUCED PLASTICITY IN DAPHNIA
reproductive effort could have been induced by higher
temperature if the benefit of pronounced adult growth is
less than in cooler conditions, as appears to be true in
Drosophila melanogaster (McCabe and Partridge, 1997; Reeve
et al., 2000). If this is the case, these data on D. pulex could still
be compatible with the Perrin–von Bertalanffy biophysical
model. However, we suggest that the temperaturedependence of reproductive effort and costs should be
treated as a further potential explanation for shifts in growth
and fecundity induced by changes in rearing temperature.
Goss, L. B. and Bunting, D. L. (1983) Daphnia development and
reproduction: responses to temperature. J. Thermal Biol., 8, 375–380.
Hirshfield, M. F. (1980) An experimental analysis of reproductive effort
and cost in the Japanese medaka, Oryzias latipes. Ecology, 61, 282–292.
Johnson, D. S. (1952) The British species of the genus Daphnia (Crustacea, Cladocera). Proc. Zool. Soc. Lond., 122, 435–462.
Jönsson, K. I., Tuomi, J. and Järemo, J. (1998) Pre- and postbreeding
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ACKNOWLEDGEMENTS
We thank J. C. Chubb for comments on an earlier
version of this work. This work was funded by a
NERC (UK) studentship to D. W.
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Received on January 28, 2002; accepted on November 6, 2003
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