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Ecology 2004
18, 664 669
Summary
1. Changes in plant physiological features after herbivory may alleviate the adverse
effects of herbivores. We examined the ability of Ilex aquifolium L. (European Holly) plants
to compensate for scale insect herbivory through increased photosynthesis. Based on
assumptions of the sourcesink hypothesis, we predicted that scale insects, by inducing
supplementary sinks for photosynthates, would increase photosynthesis.
2. Photosynthetic performance was evaluated by measuring chlorophyll fluorescence
parameters in plants growing under natural light and temperature at the field station
of the University of Santiago (north-west Spain). We measured photosynthesis on
infested leaves of infested trees; scale-free leaves of infested trees; and scale-free leaves
of scale-free trees.
3. Insect infestation significantly increased photosynthetic efficiency. Effects of scale
insects on photosynthesis were particularly enhanced by high temperature and light.
Scale insects also altered the photosynthesis of leaves not directly affected by the insects.
4. Our study showed that changes in the balance between source and sink tissues,
induced by scale insects, may partly explain host plant photosynthesis. We suggest
that increased feeding rates of scale insects promoted by high temperature and light
conditions would increase the carbon demand of infested plants, resulting in greater
compensatory photosynthesis.
Key-words : chlorophyll fluorescence, compensatory photosynthesis, herbivory, sap-feeding insect, source
sink hypothesis
Functional Ecology (2004) 18, 664 669
Introduction
Increasing evidence indicates that, under certain conditions, plants can compensate for the adverse effects of
herbivores through changes in physiological features
(Ovaska, Walls & Mutikainen 1992; Oleksyn et al.
1998; Anten & Ackerly 2001; Thomson et al. 2003).
These include compensatory photosynthesis, defined
as an increase in photosynthetic rates on damaged
plants relative to undamaged ones (Nowak & Caldwell
1984), a response to herbivory that has been observed
to be very variable (Welter 1989). Apart from its influence
on leaf physiology, and on the age structure of leaves
(younger leaves typically have higher photosynthetic
rates), herbivores can affect photosynthesis by reducing environmental constraints, improving light penetration into partially defoliated canopies (Senock,
Sisson & Donart 1991; Anten & Ackerly 2001), and
increasing the availability of water, nutrients and
2004 British
Ecological Society
665
Scale insect effects
on photosynthesis
2004 British
Ecological Society,
Functional Ecology,
18, 664669
666
R. Retuerto et al.
2004 British
Ecological Society,
Functional Ecology,
18, 664669
Results
performed on the fluorescence data taken
before infestation by scale insects did not detect significant differences in maximum quantum yields between
the two groups of trees that later were assigned to the
treatments (F1,12 = 208, P = 0175), nor were there any
interactions with time (F1,12 = 0237, P = 0938). After
infestation by scale insects, maximum and effective
quantum yields and electron transport rates were
significantly higher in infested leaves of infested trees
than in scale-free leaves of control trees, indicating
increases in photosynthetic efficiency associated with
insect infestation (Fig. 1; Table 1). We also detected a
significant tree effect, nested within infestation, for the
fluorescence parameters. When we compared photosynthetic activities of scale-free leaves on infested trees
with scale-free leaves on control trees, the effective
quantum yield and electron transport rate, but not the
maximum quantum yield, revealed an improved photosynthetic performance associated with insect infestation (Fig. 1; Table 2). In these comparisons the tree
effect, nested within infestation, was significant only
for maximum quantum yield. Comparisons between
leaf types (infested vs scale-free leaves) of infested trees
(Fig. 1) did not reveal any significant difference for maximum quantum yield (F1,42 = 0006, P = 0940); effective
quantum yield (F1,56 = 1904, P = 0217); or electron
transport rate (F1,56 = 0271, P = 0622). These analyses
revealed no tree or tree leaf type effects (P = 0074
for maximum quantum yield; P = 0479 for effective
quantum yield; P = 0493 for electron transport rate).
Discussion
Higher maximum and effective quantum yields and
electron transport rates on infested trees, compared
Fig. 1. Mean values ( SE) of chlorophyll fluorescence parameters related to photosynthetic performance measured under high
temperature and light (effective quantum yield, F/ Fm and electron transport rate), and at predawn under lower temperature
and light (maximum quantum yield, Fv /Fm). We compared infested leaves on infested trees vs scale-free leaves on scale-free trees
(means with different capital letters are significantly different at P < 005) and scale-free leaves on infested trees vs scale-free
leaves on scale-free trees (means with different lower-case letters are significantly different at P < 005) by hierarchical mixedmodel . Infested leaves on infested trees vs scale-free leaves on infested trees were compared by mixed crossed
(means with different numbers are significantly different at P < 005).
667
Scale insect effects
on photosynthesis
Table 1. Hierarchical mixed-model (infestation as fixed factor, tree as random factor nested within infestation) for
differences in chlorophyll fluorescence parameters related to photosynthetic performance, between infested leaves on infested
trees and scale-free leaves on control trees. For maximum quantum yield, photosynthetically active photon flux density (PPFD)
was introduced as covariate in the model
Maximun quantum yield (Fv /Fm)
Source of variation
df
MS
df
MS
df
MS
PPFD
Infestation
Tree within infestation
Error
1
1
12
41
1526
878
148
071
2138
553
207
<0001
0038
0042
1
12
56
12340
1128
367
109
307
0006
0002
1
12
56
98177
15414
7067
637
218
0027
0025
Table 2. Hierarchical mixed-model (infestation as fixed factor, tree as random factor nested within infestation) for
differences in chlorophyll fluorescence parameters related to photosynthetic performance, between scale-free leaves on infested
trees and on control trees. For maximum quantum yield, photosynthetically active photon flux density (PPFD) was introduced
as covariate in the model
2004 British
Ecological Society,
Functional Ecology,
18, 664669
Source of variation
df
MS
df
MS
df
MS
PPFD
Infestation
Tree within infestation
Error
1
1
12
41
1399
790
230
089
1571
323
259
<0001
0100
0012
1
12
56
54043
6227
7435
868
084
0012
0612
1
12
56
143716
14334
16084
1003
089
0008
0561
668
R. Retuerto et al.
2004 British
Ecological Society,
Functional Ecology,
18, 664669
Acknowledgements
Financial support for this study was provided by the
Spanish Ministry of Science and Technology (grant
BOS2002-00714). We would also like to thank J. C.
Franco for help with the identification of the scale
insect. Comments by two anonymous referees improved
an earlier version of the manuscript.
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Scale insect effects
on photosynthesis
2004 British
Ecological Society,
Functional Ecology,
18, 664669