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The effect of food quantity and food quality on Daphnia: morphology of feeding
structures and life history.
Repka, S.H.
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Repka, S. H. (1999). The effect of food quantity and food quality on Daphnia: morphology of feeding structures
and life history.
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Download date: 17 Jun 2017
CHAPTER 7
Plasticity in filter screen morphology and clearance rate of
Daphnia galeata, Daphnia cucullata and their interspecific
hybrids Daphnia cucullata * galeata
Sari Repka, Sârka Veselé, Anke Weber and Klaus Schwenk
Abstract
Areas and mesh sizes of filtering structures in Daphnia galeata, D. cucullata and
their interspecific hybrid D. cucullata * galeata cultivated at low and high food
concentrations were measured. The clearance rates and somatic growth rates of the
animals were also determined. When reared at low food concentration, the filtering
areas of all taxa were larger. Larger filtering areas resulted also in higher clearance
rates. Differences between taxa in both filtering area and clearance rate were
caused mainly by interspecific size differences. Hybrids had the largest absolute
mesh sizes and the parental species smaller mesh sizes. Hybrids also showed
heterosis in somatic growth rate at high food concentration. The differences in mesh
size and somatic growth rate contribute to resource partitioning between the taxa
and thus to their successful coexistence in lakes.
63
Introduction
The density and species composition of phytoplankton in lakes vary considerably
during the growing season (Sommer et al. 1986). To persist, herbivorous
zooplankton must be able to cope with extremely low and extremely high
concentrations of food. Daphnia, key grazers in many types of lakes, have been
shown to possess the ability to increase the area of their food filtering structures in
response to food limitation (Koza and Korinek 1985; Korinek et al. 1986; Pop 1991;
Lampert 1994; Lampert and Brendelberger 1996). This is effective because the
individual filtering efficiency is positively correlated to the filtering area (Egloff and
Palmer 1971; Arruda 1983; Stuchlik 1991; Lampert 1994). The mesh size of the filter
screens determines the smallest particle that can be captured (Lampert 1987).
The taxa studied here, Daphnia galeata, D. cucullata and their interspecific hybrids
D. cucullata x galeata are commonly found in Dutch lakes. They can co-exist or to
occur solely (Schwenk and Spaak 1995). These taxa belong to the D. longispina
group in which interspecific hybridisation is common (Wolf and Mort 1986; Wolf
1987; Hebert et al. 1989; Schwenk and Spaak 1995). When coexisting, these taxa
may compete for the same food resources.
Although a variety of results have been reported, the mesh sizes of adult D.
cucullata and adult D. galeata most probably differ (Geller and Müller 1981;
Brendelberger and Geller 1985). Differentiation in the mesh size of the taxa might
facilitate resource partitioning and niche differentiation. Assuming a polygenic basis
of traits such as mesh size, interspecific hybrids are expected to harbour
intermediate trait values compared to parental species (Falconer 1989). Intermediate
trait values for e.g. size at maturity were found for Daphnia interspecific hybrids
(Weider and Wolf 1991; Weider 1993; Spaak and Hoekstra 1995). It may be that the
overlap in the mesh sizes is larger between the parental species and the hybrid than
between the parental species. Boersma (1995) reported that both parental species
compete with the hybrid but competition between the parentals seemed negligible in
the highly eutrophic lake Tjeukemeer.
Theoretically, heterozygous organisms have been indicated to be better buffered
against environmental variability (Lemer 1954). In other words, plasticity and
developmental instability should increase with increasing homozygozity (Lemer
1954). It is generally assumed that genomic coadaptation and heterozygozity are the
two genetic factors that increase developmental stability (Graham and Felley 1985).
Developmental instability is defined as phenotypic variation among individuals with
identical genotypes living in an uniform environment (Scheiner et al. 1991;
Yampolsky and Scheiner 1994). Hybrid populations are therefore thought either to
benefit from an increase in heterozygozity or to suffer from disruption of
coadaptation, depending on the degree of divergence between hybridising taxa
(Harrison 1990). Until recently, it was assumed that, at the level of genetic
divergence observed between most naturally hybridising taxa, breakdown in the
coadaptation of gene complexes was more important than heterotic effects (Harrison
1990). Therefore we expect the hybrids to be more plastic and developmentally
unstable than the parental species. Here we compared phenotypic traits of the
parental species D. cucullata and D. galeata to their interspecific hybrids, D.
cucullata * galeata, using hybrid clones collected from the field and crossed in the
laboratory. The hybrids crossed in the laboratory originate from the same, known,
parental clones whereas the parental clones of the field collected hybrids are
unknown. Thus we expect the hybrids from the laboratory crossings to exhibit less
variation than hybrids collected from the field.
Specifically, we addressed three questions in this study. Firstly, are there
differences in filter screen morphology or plasticity between D. galeata, D. cucullata
and their interspecific hybrid D. cucullata « galeata, secondly, are the hybrids more
plastic and developmentally unstable than the parental species, and thirdly are the
traits of hybrids collected from the field more variable than hybrids crossed in the
laboratory?
64
Materials and methods
D. galeata, D. cucullata and D. cucullata * galeata clones were collected from
the Netherlands and from northern Germany (Table 1). The clones were kept in the
laboratory under standard conditions. To produce D. cucullata * galeata hybrids from
known parental species in the laboratory D. galeata clone TG100 was used as the
father clone and D. cucullata clone TC33 as the mother clone (Table 1). To produce
males and sexual females the clones were kept in 1 I Erlenmeyer beakers at high
densities with a lightidark regime of 16:8 hrs and low food level. Ten males and five
to ten sexual females were placed together in 40 ml of 0.45 urn membrane filtered
and sterilised Maarsseveen water. The ephippia they produced were collected and
kept in + 4" C in the dark for at least 5 months. After this period, the ephippia were
transferred to 0.45 urn membrane filtered water supplemented with the green alga
Scenedesmus acutus as food. The hatching neonates were transferred to larger
vessels and clonal cultures were established.
Table 1. Daphnia clones used in the two experiments.
Code
Species
TC33
D. cucullata
V50
D. cucullata
TG100
D. galeata
GB44
D. galeata
D.cucullata x galeata
T181
D.cucullata » galeata
T190
T2CO
D.cucullata « galeata
D.cucullata * galeata
T203
X1
D.cucullata * galeata
X3
D.cucullata x galeata
X4
D.cucullata * galeata
X5
D.cucullata » galeata
D.cucullata x galeata
X16
Origin
Tjeukemeer
Vechten
Tjeukemeer
Grote Brekken
Tjeukemeer
Tjeukemeer
Tjeukemeer
Tjeukemeer
crossed in laboratory
crossed in laboratory
crossed in laboratory
crossed in laboratory
crossed in laboratory
To record somatic growth rate, filter screen morphology and clearance rates of D.
cucullata, D. galeata and D. cucullata * galeata, two subsequent experiments were
performed. In both experiments, the mothers of the experimental animals were
reared singly from neonates on a food concentration of 1 mg C I"1 S. acutus in 100
ml tubes with 0.45 urn membrane filtered lake Maarsseveen water as the basic
medium. In the first experiment, several D. galeata, D. cucullata and D. cucullata *
galeata hybrids were used (Table 1). The experimental animals were randomly
chosen from the second brood of the mothers. The experimental animals were
cultivated in a flow-through system with a flow rate of 500 ml per 24 hrs. The body
lengths at birth were measured and the neonates were randomly exposed to two
food treatments: low S. acufus concentration (0.07 mg C I"1, 4000 cells ml"1) and high
S. acutus concentration (1 mg C I"1, 59 000 cells ml"1). There were two replicate
tubes per series and 5 animals per 50 ml tube. The Daphnia were kept in culture
until their 2nd adult instar. Two animals from each tube were used for clearance rate
measurements and the rest was preserved for filter screen measurements.
Afterwards body lengths were measured and the animals were preserved in 4 %
sugar formaline (Haney and Hall 1973). The filter screens at the third limb were
dissected out of the animal, spread on a microscopic slide with a drop of glycerine
and covered with a cover glass. The setae numbers (SN) were counted and filtering
areas (FA) were measured with an image analyser to the nearest 0.01 mm .
The clearance rates were measured with the 14C-tracer technique. To 125 ml of
the basic algae medium 1.85 kBq 14CHC03 was added. The algae were grown in a
climate chamber for four days. The algal solution was then centrifugea to remove
the inorganic nutrient medium and most of the tracer and the pellet was resuspended
in 0.45 urn membrane filtered lake water. After sieving over a 33 urn gauze, 0.1 ml
algal solution was filtered over 0.45 urn membrane filters. The filters were dried and
dissolved in toluene to count 14C activity in the medium with a scintillation counter.
The radioactively labelled suspension of algae was added to the filtered lake water in
a concentration of 0.10 mg C I"1 that was used to fill individual tubes (100 ml each).
65
One ml was filtered through a 0.45 urn membrane filter, rinsed with unlabelled water
and dried to determine radioactivity of the experimental suspension. Daphnids in
their second adult instar were transferred into individual tubes (100 ml) which
contained lake water and 14C-free algae. The daphnids were allowed to adapt to the
test concentration (0.10 mg CI"1) of algae for approximately three hrs. After this the
daphnids were transferred to the tubes with labelled algae. To measure the
clearance
rate, individual daphnids were allowed to feed for 5 min in the water with 14C-labelled
algae and then transferred back into the unlabelled water they were kept in
previously. Here they were allowed to stay for 1 min in order to rinse the body
surface from adhered 14C-containing fluid, and were subsequently transferred into
scintillation vials. The scintillation vials containing daphnids for the measurements of
clearance rate were dried in an oven at 55 °C. Subsequently, 100 ^m of distilled
water was added and the well-mixed vials were again dried for at least for 30 min.
After the addition of 250 urn soluene the well-mixed vials were again dried (> 4 hrs).
Finally, 10 ml of toluene scintillation mix were added, the vials well mixed and
placed in the scintillation counter to count radioactivity.
In the second experiment Daphnia for mesh size measurements were reared. The
same clones (Table 1), food concentrations and absolute flow rates as in the first
experiment were used. This time there were only two replicate Daphnia per tube.
The mesh sizes (ME) were measured with electron microscope using the same
methods as described in Chapter 6.
In the first experiment, mean somatic growth rate (SGR) per tube was calculated
as
SGR=(ln SAE-ln SAB)/AAT,
(1)
where SAE is size at the end of the experiment, SAB is size at birth and AAT is age
at the end of the experiment.
The clearance rate (Re) was calculated according to the formula:
Re = Ra / Rt * ((60 * 24) /1) ml / individual / day,
(2)
where Ra= radioactivity of the Daphnia, Rt= radioactivity of the experimental
medium (per ml), t= time allowed for consumption (5 min).
After ln-transformation of Re and FA, the data were analysed by analysis of
covariance, taking the logarithm of body length as a covariate (Statistical Analysis
Systems Institute 1989). SGR, SN and ME were, however, analysed with analysis of
variance. In these analyses, D. cucullata, D. galeata, D. cucullata x galeata field
hybrids and laboratory hybrids were regarded as separate groups. Tukey's a
posteriori test was applied to test differences between these four groups. A
sequential Bonnferoni procedure (Rice 1989) was used to maintain an
experimentwise type 1 error rate of 0.05. Coefficients for developmental instability of
filtering area for the different taxa were calculated using a variance partitioning
technique (Yampolsky and Scheiner 1994). In short, variance components were
estimated with SAS procedure VARCOMP (Statistical Analysis Systems Institute
1989), assuming all main effects random. The residual variance was used as a
relative measure of developmental noise. The coefficients of variation for each
taxon were calculated as the square root of the variance component divided by the
mean of the trait.
Results
The animals cultivated at the low algal concentration exhibited significantly slower
somatic growth rate (Table 2). The SGR of the animals cultivated at the low algal
concentration was 39 % slower than of those cultivated at the high algal
concentration.
66
Table 2. Results of two-way ANCOVAs and ANOVAs for data sets of two experiments for Daphnia galeata, D.
cucullata and D. cucullata x galeata reared at two food concentration. The analysed variables in ANCOVA
(corrected for body length) were clearance rate (Re) and filtering area (FA). Setae number (SN), somatic
growth rate (SGR) and mesh size (ME) were analysed with ANOVA. Df denotes the degrees of freedom and
MS is mean square.
Re
FA
Source
df, df,™
MS
F
MS
F
df, df.„„
P
P
Food
1.2
22.0
0.001*"
1,61
1,64
0.41
11.9
0.001 —
Taxa
0.02
0.34
0.798
3,64
0.17
5.1
0.003"
3,61
0.05
0.87
0.464
F»T
3,64
0.05
1.5
0.219
3,61
2.1
39.8
0.001*"
1,64
0.45
13.2
0.001""
Length
1,61
SN
SGR
Food
1,61
10.3
3.05
0.086
1,38
0.004
192.4 0.001""
Taxa
3,61
485
143
0.001"*
3,38
0.0002
11.68 0.001"*
FxT
3,61
0.18
0.05
0.983
3,38
0.0001
4.64
0.009"
ME
Food
1,31
0.005
0.94
0.339
Taxa
3,31
0.019
3.89
0.018'
F»T
3,31
0.105
0.011
2.23
*: 0.05>p>0.01, *": 0.01 >p>0.001, '**: p<0.001.
The SGRs of the taxa responded differently to food limitation as was manifested by
a significant interaction between taxa and food concentration (Table 2). Both field
and laboratory hybrids were growing faster than the parental species at high food
concentration. At low food concentration, the differences in growth between the taxa
were not large (Fig. 1).
Figure 1. Somatic growth rate of Daphnia cucullata (CUC), Daphnia galeata (GAL), and their interspecific
hybrid D. cucullata * galeata collected from the field (FCG) and crossed in the laboratory (LCG) when reared
under low and high concentrations of Scenedesmus acutus.
Filtering area is dependent on body length (Fig. 2) and that can be taken into
account in the analysis of covariance. After correcting for body length, the animals
cultivated at low food concentration exhibited significantly larger filtering areas than
animals cultivated at high food concentration (Table 2, Fig. 2). The taxa also
significantly differed in their filtering area (Table 2). The filtering area (corrected for
body length) of D. cucullata (adjusted mean ± SE 0.051 ± 0.004 mm2) was the
smallest and that of D. galeata the largest (0.085 ± 0.004 mm2). The hybrids had
intermediate filtering areas (0.061 ± 0.002 mm2 and 0.066 ± 0.002 mm2 for field and
laboratory hybrids, respectively). Because the taxa * food interaction was not
significant (Table 2) the taxa did not differ in the degree of plasticity. The
developmental instability in filtering area was the highest for D. cucullata (CV=0.23),
the lowest for D. galeata (CV=0.07 ). The hybrids had intermediate values (CV=0.09
and CV=0.14 for field and laboratory hybrids, respectively).
67
OLC
0.12-
DLG
i-:"-
0.09 <
• HC
w
K4 *
0.06'
• 4
0.03'
ALFCG
XLLCG
A
\
• HG
AHFCG
XHLCG
• °<4
X
•
-H
0.5
1.5
2.5
Body length (mm)
Figure 2. Filter screen area of Daphnia cucullata (C), Daphnia galeata (G) and their interspecific hybrid
collected from the field (FCG) and crossed in the laboratory (LCG) as a function of body length when reared
under low (L) and high (H) concentrations of Scenedesmus acutus.
Clearance rate is also dependent on the size of the animal (Table 2, Fig. 3). The
largest taxa, D. galeata, filtered more than the smaller taxa. After correcting for body
length, the Daphnia cultivated at low food concentration exhibited significantly higher
clearance rates than the Daphnia cultivated at high food concentration (Table 2, Fig.
3). In relation to their body size the taxa filtered at equal efficiency (Table 1).
ody length (mm)
Figure 3. Clearance rate of Daphnia cucullata (C), Daphnia galeata (G) and their interspecific hybrid (CG) as a
function of body length when reared under low (L) and high (H) concentrations of Scenedesmus acutus.
The numbers of setae in the filter screens were not significantly affected by the food
conditions (Table 2, Fig. 4). There were, however, differences between the taxa. D.
cucullata had significantly lowest number of setae and D. galeata the highest. The
values for the hybrids did not significantly differ from those of the parentals but were
intermediate (Fig. 4).
The animals reared at the two food concentrations did not differ in mesh size
(Table 2). The taxa, however, exhibited significantly different mesh sizes (Table 2).
The filter screens of the hybrids had the largest meshes (mean ± SE 0.51 ± 0.03 urn
and 0.49 ± 0.02 urn for field and laboratory hybrids, respectively). Daphnia cucullata
(0.44 ±0.02 urn) and D. galeata (0.45 ± 0.02 urn) exhibited smaller mesh sizes.
68
Figure 4. Setae number of Daphnia cucullata (CUC), Daphnia galeata (GAL) and D. cucullata « galeata
collected from the field (FCG) and D. cucullata*galeata from laboratory crosses (LCG) when reared under low
and high concentrations of Scenedesmus acutus.
Discussion
Daphnia reared at low food concentration exhibited larger filter screen area than
Daphnia reared at high food concentration. This is in accordance with earlier work
(Koza and Korinek 1985; Korinek era/. 1986; Pop 1991; Lampert 1994; Lampert and
Brendelberger 1996; Chapter 6). The larger filtering areas of the animals cultivated
at low food level also translated into higher clearance rates. Earlier, it has been
shown that area of the filtering screens and clearance rate are positively correlated
in Daphnia (Egloff and Palmer 1971; Arruda 1983; Stuchlik 1991; Lampert 1994). In
the present study, clearance rates were measured at a food concentration below the
Incipient Limiting Level (0.10 mg C I"1) to be able to measure close to maximal
clearance rates. It was hypothesised that the advantages of a larger filter screen are
evident at low food concentrations when the animal has to increase filtering effort.
Generally, the clearance rates measured in this experiment were slightly higher than
those reported in the literature for D. galeata and D. cucullata (see Lampert 1987 for
a review). This may well result from the low algal concentration used during
clearance rate measurements.
The body size of the animal was the most important factor explaining variance in
clearance rate and filtering area indicating that both these features are functions of
body size. Thus the largest taxon, D. galeata, exhibited the highest absolute filtering
rate and the largest filtering area. As the smallest taxon D. cucullata exhibited the
lowest filtering rate and the smallest filtering area. The filtering areas of the hybrids
were intermediate to the parentals. Generally, the filtering areas of D. galeata and D.
cucullata were in the same range as reported earlier (Brendelberger and Geller 1985;
Lampert 1994).
To compare the relative filtering areas and clearance rates of the taxa these
features can be statistically corrected for the body size by ANCOVA. Even after
correcting for body size, the filtering areas of D. cucullata were smaller than that of
D. galeata. After correcting for body size, there were, however, no differences
between the taxa in clearance rate. D. cucullata can thus maintain relative clearance
rates comparable to D. galeata and the hybrids even if the relative filtering area of
this taxon is smaller.
The number of setae in the filter screens is specific for the examined taxa. This
trait seems to be fixed within the taxon and does not show phenotypic plasticity. At
low food concentrations, filtering area grows by growth of the setae not by producing
more setae (Pop 1991). The filtering screens of D. galeata consisted of higher
number of setae than those of D. cucullata or the hybrids. The filtering screens of D.
cucullata had the lowest number of setae.
The mesh sizes were not related to the size of the animals. D. cucullata, the smallest
taxon and D. galeata the largest taxon exhibited almost identical mesh sizes. The
hybrids exhibited slightly larger mesh sizes than the parental species. The mesh size
was not statistically corrected for the body length because the absolute mesh sizes
are relevant for resource partitioning in lakes. Earlier, Geller and Müller (1981)
69
reported for adult D. cucullata mesh sizes in the range of 0.23-0.45 urn and for adult
D. galeata 0.32-1.0 urn. In a later study, however, D. cucullata was found to have
larger meshes (0.63-0.88 urn vs 0.25-0.62 urn) than D. galeata (Brendelberger and
Geller 1985). As discussed in Brendelberger and Geller (1985), the observed
differences between studies may be accounted for by different habitats from which
the specimens were collected. Food regime may also affect the mesh size. D.
magna and D. pulicaria cultivated at low food concentration exhibited smaller mesh
sizes than those cultivated at high food concentration (Lampert and Brendelberger
1996). We cultivated all the taxa in controlled laboratory conditions. In this study,
the mesh sizes of D. galeata, D. cucullata and D. cucullata x galeata were not
affected by the food concentrations at which the animals were cultivated. In
accordance, in an earlier study with D. galeata the mesh size neither responded to
the food concentrations (Chapter 6).
Differences in mesh sizes and SGR of the taxa indicate resource partitioning among
them. This may, among other factors (Spaak 1994), account for the successful
coexistence of the D. cucullata x galeata hybrid with its parental species. The
competition in the field is assumed to be more severe among parental species and
the hybrid than between the parental species (Boersma 1995). Our results on mesh
sizes of these taxa do not, however, explain the apparent lack of competition
between the parental species noticed by Boersma (1995). The mean mesh sizes of
D. cucullata and D. galeata were nearly identical (0.44 vs 0.45 urn). The mesh sizes
of the hybrids were larger than this. Mesh sizes of all the taxa are small enough to
collect most algae and cyanobacteria. However, the smaller meshes of the parental
species enable more efficient feeding on bacteria which may be important when
algal food is limiting. Since water flows easier through a larger filter mesh, a filter
screen with a larger mesh size is energetically less costly (Lampert and
Brendelberger 1996). This might partly explain why D. cucullata x galeata hybrids at
high food concentration exhibited the highest somatic growth rate of the taxa.
Spaak (1994) attributed the successful coexistence of the hybrid to its relatively high
population growth rate, r, and efficient avoidance of fish prédation. In addition, also
differences in resource utilisation contribute to the coexistence of the taxa. The
somatic growth rate of the hybrids showed heterosis at high food concentrations that
gives them an advantage. Somatic growth rate is a component of population growth
rate and has been used to predict population growth rate (Lampert and Trubetskova
1996).
The degree of filter screen plasticity did not differ among the taxa. D. cucullata was
developmental^ more unstable than the other two taxa. In earlier empirical studies
both animal and plant hybrids have shown greater variability and less developmental
stability than their parental populations (Strauss 1987; Ross and Robertson 1990;
Graham and Felley 1985; Leary et al. 1985). Probably phenotypic plasticity and
developmental stability are not tightly related to the heterozygozity of a hybrid taxon
due to disruption of coadapted loci.
The field and laboratory hybrids did not differ in any of the measured parameters.
Although field and laboratory hybrids differed in their origin, they showed a high level
of similarity in the traits measured in this study. Because the field hybrids originated
from the same lake and were collected at the same time, they have encountered the
same selective factors. Therefore, one would expect them to show less variation
than hybrids collected from different lakes or at different times. Because laboratory
hybrids in this study shared the same parental clones they should show less variation
than hybrids with more diverse origin. In particular the heterotic effects in SGR and
ME in field and laboratory hybrids indicate which traits facilitate coexistence with
parental taxa.
To conclude, phenotypic plasticity in filtering area enabled higher clearance rates in
low food adapted D. galeata, D. cucullata and their interspecific hybrid D. cucullata x
galeata. In relation to the body length, the clearance rates of the taxa were similar.
At high food concentrations, the hybrids might have an advantage over the parental
species as indicated by the highest somatic growth rates. The larger mesh size of
the hybrids allows niche segregation and may contribute to the successful
coexistence of the hybrid with its parental species. The differences among the taxa
may contribute to the seasonal succession observed in the lakes.
70
Acknowledgements
We thank Maartje Bijl for crossing the Daphnia clones. We also thank Wim
Admiraal, Ramesh Gulati, Wolf Mooij, Koos Vijverberg and Ellen van Donk for
critically commenting on an earlier version of the manuscript.
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