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Experiments with duckweed–moth systems suggest that
global warming may reduce rather than promote
herbivory

TJISSE VAN DER HEIDE, RUDI M. M. ROIJACKERS, EDWIN T. H. M. PEETERS AND

EGBERT H. VAN NES

Department of Environmental Sciences, Aquatic Ecology and Water Quality Management group, Wageningen University,

Wageningen, The Netherlands

SUMMARY

1. Wilf & Labandeira (1999) suggested that increased temperatures because of globa

l

warming will cause an increase in herbivory by insects. This conclusion was based on the

supposed effect of temperature on herbivores but did not consider an effect of temperature

on plant growth.

2. We studied the effect of temperature on grazing pressure by the small China-mark moth

(Cataclysta lemnata L.) on Lemna minor L. in laboratory experiments.

3. Between temperatures of 15 and 24 �C we found a sigmoidal increase in C. lemnat

a

grazing rates, and an approximately linear increase in L. minor growth rates. Therefore, a

n

increase in temperature did not always result in higher grazing pressure by this insect as

the regrowth of Lemna changes also.

4. At temperatures below 18.7 �C, Lemna benefited more than Cataclysta from an increase in
temperature, causing a decrease in grazing pressure.

5. In the context of global warming, we conclude that rising temperatures will not

necessarily increase grazing pressure by herbivorous insects.

Keywords: Cataclysta, grazing, herbivory, Lemna, temperature

Introduction

Duckweeds (Lemnaceae) are often abundant in dit-

ches and ponds (Landolt, 1986). Especially when

nitrogen and phosphorus concentrations in the water

column are high, the surface area can become covered

with dense floating mats of duckweed (Lüönd, 1980,

1983; Portielje & Roijackers, 1995). These mats have

large impacts on freshwater ecosystems, restricting

oxygen supply (Pokorny & Rejmánková, 1983), light

availability of algae and submerged macrophytes

(Wolek, 1974) and temperature fluxes (Dale &

Gillespie, 1976; Landolt, 1986; Goldsborough, 1993).

These changed conditions often have a negative effect

on the biodiversity of the ecosystem (Janse & van

Puijenbroek, 1998). Other free-floating plants such as

red water fern (Azolla filiculoides), water hyacinth

(Eichhornia crassipes) and water lettuce (Pistia stratiotes)

often cause serious problems in tropical and sub-

tropical regions (Mehra et al., 1999; Hill, 2003).

Various species of herbivorous insects consume

free-floating macrophytes. Several species of weevils

(Coleoptera: Curculionidae) are able to consume large

amounts of red water fern, water hyacinth and water

lettuce (Cilliers, 1991; Hill & Cilliers, 1999; Aguilar

et al., 2003), while the larvae of the semi-aquatic Small

China-mark moth (Cataclysta lemnata) are capable of

removing large parts of floating cover of Lemnaceae

covers (Wesenberg-Lund, 1943). Duckweed is not

only used as food source, but also as building material

Correspondence: Rudi M. M. Roijackers, Department of

Environmental Sciences, Aquatic Ecology and Water Quality

Management group, Wageningen University, PO Box 8080,

NL-6700 DD Wageningen, The Netherlands.

E-mail: rudi.roijackers@wur.nl

Freshwater Biology (2006) 51, 110–116 doi:10.1111/j.1365-2427.2005.01479.x

110 � 2005 Blackwell Publishing Ltd

for the cases for the larvae and pupae (Petrischak,

2000). The moth lays eggs on the undersides of

duckweeds. After approximately 1 week caterpillars

hatch and they immediately start building cases to

protect their bodies. After a few weeks pupation takes

place in floating cases of duckweed fronds.

In the last century the earth’s climate has warmed

by 0.6 �C (Houghton et al., 2001). As temperature is
one of the most important factors controlling biologi-

cal rates (Cossins & Bowler, 1987; Gillooly et al., 2002)

and especially the development of insects (Saunders,

1982; Huffaker & Gutierrez, 1999; Bale et al., 2002), it

can be expected that these changes will also influence

the grazing pressure of herbivorous insects on floating

macrophytes. In general, the diversity of herbivorous

insects and their grazing pressure on plant hosts

increases with decreasing latitude, suggesting a high-

er grazing pressure with rising temperatures (Wilf &

Labandeira, 1999). As the grazing pressure of modern

terrestrial insects generally increases with decreasing

latitude, Wilf & Labandeira (1999) hypothesised that

at a constant latitude grazing pressure of these insects

also increases with rising temperatures. This hypo-

thesis was confirmed in their study of the fossil record

in south-western Wyoming. However, the effect of

rising temperatures on the grazing pressure of a single

aquatic insect species on its plant host has never been

thoroughly investigated.

We tested the hypothesis that rising temperature

increases the grazing pressure of C. lemnata L. on

L. minor L. by conducting grazing experiments in the

laboratory at different temperatures.

Materials and methods

Experiments

In the laboratory, a population of C. lemnata, collected

for the field near Wageningen (The Netherlands),

was bred for several generations in 20-L aquaria

under controlled conditions (temperature 25 ± 1 �C,
day–night cycle 14–10 h, light intensity of

180 lmol m)2 s)1). Larvae of C. lemnata were fed with
L. minor, grown in the laboratory at 25 �C and a constant
irradiation of 180 lmol m)2 s)1. Both L. minor and
C. lemnata larvae were cultivated on the medium

described by Szabo, Roijackers & Scheffer (2003).

To determine the consumption rate and biomass

increase in larvae of C. lemnata a laboratory experi-

ment was conducted in climate chambers at five

different water temperatures (15, 19, 24, 28 and 33 �C).
In the climate chambers, a day–night cycle of 14–10 h

and a light-intensity of 85 lmol m)2 s)1 was main-
tained.

The dry weights (g DW; 24 h at 60 �C) of 1

0

randomly-selected third stage larvae (according to

Petrischak, 2000) and their cases were determined at

the start of the experiment. The remaining larvae

(approximately 500) were randomly divided between

the five different temperature regimes in 20-L

aquaria. After an acclimatisation period of 24 h at

each temperature, 14 round enclosures (surface area

of 25 cm2) were filled with 0.300 g (0.021 g dry

weight) of L. minor, covering about 75% of the

surface area. The enclosures were placed in 2-L

aquaria with acclimatised medium. Ten randomly

selected larvae were then moved to 10 of the

enclosures, while the remaining four enclosures were

used as controls to determine the growth rate of

L. minor at the different temperatures. After 2 days

the dry weight of L. minor, the larvae and the cases

was determined again.

Statistical analysis

Data sets smaller than 50 samples were tested for

normality using the Shapiro-Wilk test; larger datasets

were analysed with the Kolmogorov–Smirnov test.

Normally distributed datasets (P ‡ 0.05) were tested
using one-way analysis of variance (ANOVAANOVA) and

further analysed with either Tukey’s HSD post hoc test

(equal variances; P ‡ 0.05) or Tamhane’s T2 post ho

c

test (variances not equal; P < 0.05). For the post hoc

tests a significance level of 0.05 was used. When data

sets were not normally distributed (P < 0.05), they

were analysed using Kruskal–Wallis and Mann–

Whitney U-tests, for the latter using a significance

level of 0.005 (0.05/10).

Modelling

Increase in the larval biomass as well as in the dry

weight of the cases was estimated by calculating the

difference between the mean values at the start of

the experiment and the mean values at the end of the

experiment.

The consumption rate of the larvae in the experiment

was assessed using the following simple equation

Duckweed–moth interactions and global warming 111

� 2005 Blackwell Publishing Ltd, Freshwater Biology, 51, 110–116

(eqn 1). As the time scale in the experiments was

relatively short (2 days), we assumed that the con-

sumption rate of the larvae (C in g DW day)1) was

approximately constant. Furthermore, we assumed

that L. minor (Y in g DW) grew exponentially during

the period of the experiment:

dY

dt
¼ lY � C ð1Þ

This model can be solved as:

Y1 ¼

C

l
þ Y0 �

C
l

� �
elt ð2Þ

in which Y0 is the initial amount of L. minor (g DW), l
is the relative growth rate per day and t time in days.

The relative growth rate (l) at the different temper-
atures was estimated by calculating the mean growth

rates for the controls, where the consumption rate C

was zero.

The fraction of the consumed L. minor used for the

cases was obtained by dividing the mean weight

increase in the cases (g DW day)1) by the mean total

consumption of the larvae. Efficiency of the larvae

was calculated by dividing the mean biomass

increase in the larvae by the mean total consumption

rate (C) of Lemna minus the mean weight increase in

the cases.

Using regression, the effect of temperature on the

consumption rate and the larval biomass increase

were modelled, using two different functions.

For describing the effect of temperature on the

consumption rate (C), the sigmoid-shaped Hill-func-

tion was used (Hill, 1910):

CðTÞ ¼
CmaxT

n

Tnh þ Tn
ð3Þ

where Cmax is maximum consumption rate (g

DW day)1), T is the rearing temperature (�C), Th is
the temperature where 50% of the maximum con-

sumption is reached (�C) and n is an empirical
constant determining the shape of the curve.

To describe the temperature effect on the larval

biomass increase, the Brière-1-function (Brière et al.,

1999) was used. While this function is most often used

for describing the temperature-dependent develop-

ment rate of insects (day)1), it is here used to describe

the temperature-dependent biomass increase (B)

(g DW day)1):

BðTÞ ¼ aTðT � T0ÞðTL � TÞ1=2 ð4Þ

Here T is the rearing temperature (�C), T0 is the low
temperature development threshold (�C), TL is the
lethal temperature threshold (�C) and a is an empirical
(scaling) constant.

In order to explore changes in grazing pressure

with temperature, the sensitivity of both the larval

consumption rate and the growth rate of L. minor to

changes in temperature were determined.

Sensitivity of the larval consumption rate is des-

cribed by the first derivative of eqn 3, scaled to

percentages of the maximum performance. Based on

Landolt & Kandeler (1987) the growth capacity of

L. minor can be described by a linear equation in a

wide range of temperatures (from the minimum

temperature, 5 �C, to the optimum temperature,
26 �C). The slope of this equation is the sensitivity of
L. minor to changing temperatures.

Results

Experimental results

The growth rate of L. minor (Fig. 1) was highest at

24 �C. ANOVAANOVA showed significant differences among
the temperatures (F4,15 ¼ 10.96, P < 0.001). Tukey’s post hoc test demonstrated that the growth rate of

L. minor differed significantly for the two lowest

temperatures in comparison with 24 �C.
Differences between the temperatures were signifi-

cant for C. lemnata larval biomass increase (Kruskal–

Wallis test: v2 ¼ 39.809, d.f. ¼ 4, P < 0.001). Mann–

Water temperature (ºC)

10 15 20 25 30 35

R
e

la
tiv

e
g

ro
w

th
r

a
te

(
d

a
y–

1
)

0.00

0.0

2

0.0

4

0.0

6

0.0

8

0.

10

0.

12

0.

14

0.

16

0.18

0.

20

a

ac

b

bc

bc

Fig. 1 Effect of temperature on the relative growth rate of

L. minor. Error bars ±1 SD. Different letters indicate significant

differences (P < 0.05).

112 T. van der Heide et al.

� 2005 Blackwell Publishing Ltd, Freshwater Biology, 51, 110–116

Whitney U-tests demonstrated that the two lowest

temperatures differed significantly from the three

highest temperatures as well as from each other

(Fig. 2, top).

The increase in weight of larval cases was higher for

the three highest temperatures compared with 15 and

19 �C (Fig. 2, bottom). ANOVAANOVA indicated significant
differences between the temperatures (F4,55 ¼ 9.96,
P < 0.001) and Tukey’s post hoc test separated 15 and

19 �C from 24 and 33 �C.
ANOVAANOVA showed that the estimated consumption

rate differed significantly between the temperatures

(F4,65 ¼ 32.03, P < 0.001). Tamhane’s post hoc test divided the data into three groups, with the two

lowest temperatures in the first group, 24 �C as a
standalone and the two highest temperatures in the

latter group. The particularly high variance at 33 �C
suggests that tolerance of individual larvae to this

temperature varied substantially (Fig. 3, top).

The fraction of L. minor used for the cases dropped

rapidly with rising temperatures, from 28% at 15 �C
to approximately 8% at 28 and 33 �C (Fig. 3, bottom).
At 15 �C the efficiency of the larvae proved to be
extremely high (Fig. 5), with over 71% of the ingested

L. minor was converted into body weight. However, at

28 and 33 �C the efficiency dropped to 18–20%,
indicating an increase in metabolic rate of the larvae

with rising temperatures.

Modelling

The Brière-1-function described the relation between

larval growth and temperature quite well (Fig. 2, top).

The function fitted the minimum temperature thresh-

old (T0) at 13.4 �C and the lethal temperature thresh-
old (TL) at 36.3 �C. Maximum performance of the
larvae was estimated at 28.7 �C. The fitted Hill-
function predicted a maximum consumption rate

(Cmax) of 0.0103 g DW day
)1 (Fig. 3, top). At 23.2 �C

Water temperature (ºC)
10 15 20 25 30 35

D
ry

w
e
ig

h
t
in

cr
e
a
se

(

1
0

–
3
g

D
W

d
a

y–

1

)

G
ro

w
th

r
a

te

(
1
0
–
3
g
D
W
d
a
y–

1
)

–

0.2

0.0

0.2

0.4

0.6

0.8

1.0

1.2

1.4

1.6

a
ac
b

bc b

0.0

0.5

1.0

1.5

2.0

2.5

Larval biomass increase
Fitted Briere-1-function

a
b
c

c
c

Fig. 2 Effect of temperature on the growth rate of C. lemnata

larvae (top graph) and on the weight increase in the C. lemnata

larval cases (bottom graph). Error bars ±1 SD. R2 of the fitted

Brière-1-function: 0.62. Fitted parameters: a ¼ 1.465 10)6; T0 ¼
13.4 �C; TL ¼ 36.3 �C; optimum at 28.7 �C. Different letters
indicate significant differences (P < 0.05).

Water temperature (ºC)
10 15 20 25 30 35

P
e

rc
e

n
ta

g
e

s
(%

)
0
20

40

60

80

Efficiency of the larvae
Part of Lemna from the total
consumption used for the cases

0
2
4
6
8
10
12
14
16

C
o

n
su

m
p

tio
n

r
a

te
(

1
0
–
3
g
D
W
d
a

y–
1
) Larval consumption

Fitted Hill-function

Fig. 3 Effect of temperature on the consumption rate of C. lem-

nata larvae (top graph) and on the efficiency of C. lemnata larvae

and the fraction of total consumption of L. minor used for the

cases (bottom graph). Error bars ±1 SD. R2 of the fitted Hill-

function: 0.67. Fitted parameters: Cmax ¼ 0.0103; Th ¼ 23.2; n ¼
10,76. Different letters indicate significant differences (P < 0.05).

Duckweed–moth interactions and global warming 113

� 2005 Blackwell Publishing Ltd, Freshwater Biology, 51, 110–116

the consumption rate of the larvae was at 50% of the

maximum performance (Th).

The functions plotted in Fig. 4 show the sensitivities

of the L. minor growth rate and C. lemnata consump-

tion rate to changes in temperature. According to

Landolt & Kandeler (1987), the slope of the linear

equation of L. minor was 4.76 �C)1 day)1, which is
comparable with the value we obtained from our own

data (4.67 �C)1 day)1). The intersection of the two
functions is at 18.7 �C. This means that for tempera-
tures higher than 18.7 �C, the advantage of an increase
in temperature is higher for the C. lemnata larvae than

for L. minor.

Discussion

Based on a palaeontological survey of two climatolog-

ically different eras, Wilf & Labandeira (1999) con-

cluded that grazing pressure by insects on their plant

hosts generally increases with rising temperatures

induced by global warming or decreasing latitude.

We showed that the consumption rate of the C. lemnata

larvae indeed increased with rising temperatures.

However, as the growth of L. minor increased also, we

showed that at lower temperatures (below 18.7 �C) the
plant host benefited more from an increase in tempera-

ture than the herbivorous insect. Hence our results

suggested that at least for L. minor and C. lemnata, the

general conclusion of Wilf & Labandeira (1999) does

not hold. Whether grazing pressure increases or

decreases seems to be dependent on the conditions, as

the plant host and the herbivorous insect may benefit

differently from rising temperatures.

As for most other species of Lemnaceae the growth

rate also increases linearly with temperature (Landolt

& Kandeler, 1987), this phenomenon will not be

restricted to grazing on L. minor. In Europe, the

distribution of C. lemnata extends across the continent

from Scandinavia and Russia to Spain and Italy (Illies,

1978), and covers the isotherm of 19 �C. Therefore,
rising temperatures will not necessarily mean that

grazing pressure of C. lemnata on Lemnaceae will

increase. Predictions by climate scenarios of warming

vary per region from 0.1 to 0.4 �C by decade (McCar-
thy et al., 2001) and for summer periods from 0.08 to

0.6 �C per decade. Thus changes in grazing pressure
of C. lemnata on Lemnaceae will differ per region,

depending upon the prevailing temperatures and on

how much these temperatures will rise in the future.

Our study showed that L. minor is able to develop at

much lower temperatures than C. lemnata, indicating

that L. minor can start its development earlier and

extend it further into the season. The same is true when

comparing other Lemnaceae to the temperature thresh-

old of C. lemnata. Rejmánková (1973) reported growth

of L. minor in the field from April to November, whereas

C. lemnata was active from May till September (Petris-

chak, 2000). From an evolutionary perspective, the

suggestion that development of C. lemnata starts later in

the season compared with most Lemnaceae is very

plausible. By starting their development later, their

primary food source will most probably not be limiting.

Possibly, rising temperatures because of global warm-

ing will also affect this balance. The rising temperatures

will cause larvae of C. lemnata to start developing earlier

in the season, but the same will be true for most Lemna

species. How this balance will change with rising

temperatures is currently hard to predict.

In our experiments temperature was kept constant,

but in the field it fluctuates strongly, especially within

mats of Lemnaceae. Vertical temperature gradients

are observed within the mats (Dale & Gillespie, 1976;

Goldsborough, 1993). This will affect both the growth

of Lemnaceae and the development of the larvae of C.

lemnata. While temperature is the main factor control-

ling growth of Lemnaceae in the field (Rejmánková,

1973), it is not the only factor. Nutrient supply

(Lüönd, 1980, 1983; Portielje & Roijackers, 1995),

light-conditions (Wolek, 1974), currents (Landolt,

1986) and competition with other macrophytes

Water temperature (ºC)

5 10 15 20 25 30 35 40

S
e
n
si

tiv
ity

(
g

ºC
–
1
d

a
y–
1
)

0
2
4
6
8
10
12

Consumption rate
Lemna growth

Fig. 4 Sensitivity of C. lemnata larvae and L. minor to rising

temperatures, as described by the scaled derivatives of the L.

minor growth rate and larval consumption capacity. Intersection

of the two functions at 18.7 �C.

114 T. van der Heide et al.

� 2005 Blackwell Publishing Ltd, Freshwater Biology, 51, 110–116

(Landolt, 1986; Scheffer et al., 2003) all influence the

growth rate of Lemnaceae in the field.

In summary, we showed that rising temperatures

will not necessarily cause an increase in grazing

pressure, as predicted by Wilf & Labandeira (1999).

The impact of grazing is not only dependent on the

grazing rate of the herbivorous insect, but also on the

growth rate of the plants, and both can be affected

differently by temperature. In the case of the interac-

tion between Lemnacea and C. lemnata, this implies

that at low latitudes the effect of global warming is the

opposite of the effect at higher latitudes.

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