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Functional

Ecology 2004
18, 664 669

Increased photosynthetic performance in holly trees


infested by scale insects
Blackwell Publishing, Ltd.

R. RETUERTO,* B. FERNANDEZ-LEMA,* RODRIGUEZ-ROILOA* and


J. R. OBESO
*Area de Ecologa, Facultad de Biologa, Universidad de Santiago, 15782 Santiago de Compostela, and Dpto
Biologa Organismos y Sistemas, Unidad de Ecologa, Universidad de Oviedo, E33071 Oviedo, Spain

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

Author to whom correspondence should be addressed. Email: bfretuer@usc.es

hormones to the remaining foliage (McNaughton 1983;


Trumble, Kolodny-Hirsch & Ting 1993). Effects of
herbivores on host plant photosynthesis have also been
attributed to changes in carbon sourcesink relationships. According to the sourcesink hypothesis, photosynthetic rates are regulated, at least in part, by the
balance between plant tissues which are net exporters
of photosynthates (sources), and tissues which are net
consumers of carbohydrates (sinks) (Sweet & Wareing
1966; Neales & Incoll 1968; Meyer & Whitlow 1992).
According to this hypothesis, photosynthetic rates will
increase with reduced source supply relative to sink
demand, whereas a reduced sink demand will reduce
photosynthetic rates.
Remarkably little is known about effects of scale
insects on photosynthesis (see review by Vranjic 1997),
even though they may alter the balance between sink
and source tissues within the host plant (Schaffer &
Mason 1990). Given the variable effects of herbivores
on host photosynthesis (Warrington, Cottam & Whittaker
1989; Reich et al. 1993; Peterson, Higley & Spomer
1996; Oleksyn et al. 1998) and the potential of this for
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Scale insect effects
on photosynthesis

explaining plant responses to herbivory as changes in


food quality, defence investment or compensatory growth,
the objective of this study was to determine how feeding by scale insects affects photosynthetic energy conversion in holly plants. Photosynthesis was evaluated
by chlorophyll a fluorescence parameters, a noninvasive technique that has recently begun to be used to
assess physiological responses to herbivory (Bown,
Hall & MacGregor 2002; Zangerl et al. 2002; Macedo
et al. 2003; Thomson et al. 2003). We also examined if
possible impacts of scale insects on host plant photosynthesis extended beyond the infested leaf itself. To
do this, we measured photosynthetic performance on
infested leaves and on scale-free leaves adjacent to the
infested leaves (in the manner of Larson 1998). Based
on the assumptions of the sourcesink hypothesis, predictions can be made about the effect of herbivores on
photosynthetic rates, depending on whether herbivores
remove photosynthetic tissues acting as sources; remove
tissues acting as sinks; or induce additional sinks
for photosynthate. We predicted that scale insects, by
inducing supplementary sinks for photosynthates, would
increase photosynthetic rates by relieving photosynthesis
inhibition due to end-product accumulation (Welter
1989; Lambers, Chapin & Pons 1998).

Materials and methods

2004 British
Ecological Society,
Functional Ecology,
18, 664669

Ilex aquifolium L. (Aquifoliaceae), the European Holly,


is a dioecious, broadleaved evergreen tree that occurs
naturally throughout Europe and North Africa (Peterken
& Loyd 1967).
In June 1997 third-year holly trees that were being
monitored for chlorophyll fluorescence parameters at
the field station of the University of Santiago (northwest Spain) were naturally infested by the scale insect
Coccus sp. (Homoptera: Coccoidea). This insect, like
other soft scales, feeds from the phloem of the host
plant, excreting honeydew. This sweet excrement is fed
on by ants, wasps and other insects. The honeydew is
also a favourable substrate on which sooty moulds
may grow. Trees with heavy infestations were close
together, indicating that insects were distributed contagiously among the trees. The plants, of uniform size,
grew under natural light and temperature, with optimal
fertilization and water supply, in 30 l pots containing a
3 : 1 mixture of seedling substrate (Pind-strup PlusBlue, based on 70% blond peat, 30% black peat and
added nutrients) and perlite (Europerlita, Barcelona,
Spain). After insects became established, scales were
abundant on stems, twigs (more than one mature female
per cm) and leaves (mean number of mature females
per leaf = 377 24 SE, n = 35). Seven severely infested
plants were selected for the experiment. These plants
were ant-attended, which avoided accumulation of
honeydew and sooty moulds on the leaves (Bach 1991).
From the same pool of more than 200 plants grown at
the site, we randomly chose as control plants seven
scale-free individuals of similar size to the infested trees.

Photosynthetic efficiency was evaluated using


chlorophyll a fluorescence parameters. This technique
measures differences in leaf photochemistry without
disturbing the insects, and avoiding the effects of insect
respiration on leaf gas exchange. The principle underlying this technique is that light absorbed by chlorophyll can follow three alternative routes: it can drive
photosynthesis; is dissipated harmlessly as heat; or is
re-emitted at a longer wavelength as fluorescence. As
these three ways of de-excitation are competitive, an
increase in the efficiency of one of these processes (e.g.
photochemistry) will decrease the yield of the other.
Hence a feedback stimulation of photosynthesis by a
increase in sink strength can be detected by measuring
the increased yield of fluorescence. We measured in vivo
chlorophyll fluorescence on the upper surface of five
current-year fully expanded leaves per control plant,
using a pulse-amplitude-modulated fluorometer (PAM2000, Walz, Effeltrich, Germany). On each infested
plant we measured five scale-free and five infested
leaves. The parameters recorded were as follows.
The maximum quantum yield of photosystem II (PSII),
Fv /Fm = (Fm Fo)/Fm, where Fm and Fo are, respectively,
the maximum and minimum fluorescence yields induced
in a dark-adapted sample, was obtained at predawn after
overnight recovery: mean photosynthetically active
photon flux density (PPFD) = 183 mol m2 s1
067 SE; mean leaf temperature = 200 C 008 SE;
n = 84, using a pulse of saturating light (>4000 m
photons m 2 s 1, 08 s pulse length). The maximum
quantum yield estimates the efficiency of excitation
energy capture by open PSII reaction centres (Butler &
Kitajima 1975), and is correlated with the amount of
carbon gained per unit of light absorbed (BolhrNordenkampf & quist 1993).
The effective quantum yield of PSII photochemistry
(F/ Fm ) for leaves at steady-state photosynthesis, under
the prevailing ambient light and temperature (mean
PPFD = 953 mol m2 s1 219 SE, mean leaf temperature 341 C 018 SE; n = 105) was determined as
( Fm Ft )/ Fm (Genty, Briantais & Baker 1989), where
Ft is the steady-state fluorescence under the measuring
light and Fm is the maximum fluorescence reached in
a pulse of saturating light with an illuminated sample
(when the pool of primary quinone electron acceptor,
QA, of the PSII reaction centres is fully reduced, and
hence photochemistry is impeded). The effective quantum yield represents the overall efficiency of PSII reaction centres in light. Changes in the effective quantum
yield are correlated with the quantum efficiency of O2
evolution (Schreiber, Neubauer & Klughammer 1988;
Lovelock, Posada & Winter 1999) and CO2 assimilation
rates (Genty et al. 1989; Demmig-Adams et al. 1990;
Edwards & Baker 1993; Maxwell & Johnson 2000).
Lastly, the overall photosynthetic capacity in vivo
(Genty et al. 1989) was estimated by measuring the
electron transport rate, defined as F/ Fm PPFD
05 084, where 05 is a factor that accounts for the
partitioning of energy between the two photosystems,

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2004 British
Ecological Society,
Functional Ecology,
18, 664669

and 084 is the percentage of the incident quanta


absorbed by the leaf. We assumed that differences in
absorptance among the leaves being compared were
insignificant because all leaves were asymptomatic,
very dark green in colour, without yellowing or
visible chlorosis. The PPFD at the leaf surface, at the same
location as fluorescence, was measured using a microquantum sensor (Leaf-Clip Holder 2030-B, Walz).
From July to September 1996, before plants were
naturally infested by scale insects, we made 13 series of
fluorescence measurements. These data were used to
test the possibility that the scale insect preferentially
infected the more vigorous trees, those with higher
photosynthetic rates. We compared by analyses of
variance of repeated measures () the maximum
quantum yield of the two groups of plants assigned to
the infestation treatment (scale-infested and scale-free
trees). To avoid common methodological problems
associated with studying herbivore-induced compensatory photosynthesis (see criticisms expressed by Meyer
& Whitlow 1992; Larson 1998) we examined differences
in photosynthetic efficiency between leaves (infested
and scale-free) on infested trees, and scale-free leaves
on noninfested trees (as a control), by hierarchical
mixed-model (infestation as fixed factor, tree as
random factor nested within infestation). The inclusion of a random-effects nested factor (tree) was made
to account for some of the variability within the groups
of interest (infestation), and thus the variance of the
source infestation (our primary concern) is free of the
variability due to the tree effect. Differences between
infested and scale-free leaves on infested trees were
analysed by mixed crossed (leaf type as fixed
factor and tree as random). To take into account the effect
of PPFD on measures of maximum quantum yield
and effective quantum yield, this variable was included
as a covariate in s and subsequently eliminated
from the model when P > 005. Variable distributions
were examined for non-normality and heteroscedasticity. According to tests, effective quantum yield was

square-root transformed to meet the assumptions of


parametric statistics.

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)

Effective quantum yield (F/Fm )

Electron transport rate

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

Maximum quantum yield (Fv /Fm)

Effective quantum yield (F/ Fm )

Electron transport rate

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

with noninfested trees, demonstrate that photosynthetic


efficiency increased in response to insect infestation
(compensatory photosynthesis). Thus our findings
support the hypothesis that phloem-sap feeding insects,
by acting as additional sinks for photosynthate, might
increase the photosynthetic rates of their hosts (Crawley
1999). Similarly, gall insects, which do not cause
mechanical damage to photosynthetic cells, may also
increase the photosynthetic rates of their host plants
(Fay & Harnett 1991; Fay, Harnett & Knapp 1993).
However, some studies have observed reduced net CO2
assimilation, on a leaf area basis, in response to herbivory by sap-feeding insects (Sances et al. 1982; Wood,
Tedders & Thompson 1985; Youngman et al. 1986),
while others have reported no significant effects of
infestation by aphids on maximum and effective quantum
yields or electron transport rates (Macedo et al. 2003).
Larson (1998), studying the impact of gall-forming
arthropods on photosynthetic rates, found only
negative impacts, suggesting that sink competition for
nutrients may account for these results. Crawley (1999)
has also suggested that increased photosynthetic rates
in response to herbivore feeding are more likely to
occur under sink-limited conditions. In contrast to our
findings, Schaffer & Mason (1990) reported that a subtropical tree species (Guaiacum sanctum) infested by
the scale insect Toumeyella sp. generally had lower net
CO2 assimilation than noninfested trees. Possible reasons for this difference could include the effects of the
different environmental conditions on herbivore activity; the greater densities of scale insects in our study; or
the absence of scale insects from leaf laminae during
the study of Schaffer & Mason (1990).

Welter (1989) and Zangerl et al. (2002) reported that


folivory may affect photosynthetic rates on intact tissues at a considerable distance from where the damage
occurred. For effective quantum yields and electron
transport rates, but not for maximum quantum yields
(Table 2), we found that effects of scale insects on
photosynthesis may also extend beyond the infested leaf
itself, stimulating photosynthesis in scale-free leaves
adjacent to infested leaves. It is likely that scale insects
altered leaf metabolism by increasing assimilate demand
on infested leaves, and subsequently increasing translocation of assimilates from adjacent leaves, relieving
photosynthetic inhibition due to end-product accumulation. Our results are consistent with observations by
Welter (1989), who reported that increased photosynthetic rates seem to be more frequent (62% of studies
examined) when herbivores feed on the products of
photosynthesis without destroying the photosynthetic
machinery.
We found that insect infestation significantly
increased electron transport rates and effective quantum yields, which represent photosynthetic activities
measured under high temperature and light (see
Materials and methods). Otherwise, photosynthetic
efficiencies estimated by maximum quantum yields,
measured under lower temperature and light (at predawn),
were also higher in infested trees, but the differences
were less significant or not significant. These contrasting results can be explained by the feeding rhythm of
the scale insects. Activity and feeding intensity of scale
insects are enhanced by temperature and light (Damon
1996; Ponsonby & Copland 2000). Thus at midday
we would expect a greater scale insect demand for

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2004 British
Ecological Society,
Functional Ecology,
18, 664669

photosynthate, increasing sink strength and consequently


increasing photosynthetic rates by feedback regulation.
Ant attendance can also contribute to stimulating the
feeding rates of scale insects (Buckley 1987).
According to the plant vigour hypothesis (Price
1991), it could be argued that the photosynthetic performance of infested plants was higher because insects
simply preferred more vigorous plants. However, we
eliminated this explanation. Before plants were infested,
differences in maximum quantum yields between
infested and scale-free trees were nonsignificant. Thus
scale insects did not preferentially infest trees with
high photosynthetic performances. We also dismissed
the plant vigour hypothesis because of the contagious
distribution of the insect infestation among the trees.
Such a distribution would not be plausible if insects
preferentially infected trees with high photosynthetic
performances.
The increased photosynthesis we found may have
limited potential for mitigating the negative effects of
herbivory. Schaffer & Mason (1990) observed that the
removal of carbohydrates by scale insects resulted in
drastic reductions in plant biomass. Anten & Ackerly
(2001) found that only a small fraction (530%) of the
estimated loss in carbon gain caused by defoliation
was compensated for by a 10 18% increase in photosynthesis of defoliated Hamaedorea elegans plants.
However, Thomson et al. (2003), examining the effects
of herbivory by the garden snail on cucumber photosynthesis, suggested that small differences in photosynthetic efficiency compounded in time to contribute
substantially to differences in carbon gain.
We also recognize that the compensatory responses
observed in this study could be different in plants
grown under natural conditions, with limiting
resources and competitive conditions, as suggested by
Fay, Harnett & Knapp (1996). For example, the light
conditions in our study may have resulted in more
compensation than would be found in a natural environment, if compensation for herbivory is a physiological consequence of adaptations to low light
environments rather than an adaptation to herbivory
itself, as suggested by some studies (Jremo, Nilson &
Tuomi 1996; Simons & Johnston 1999; Thomson et al.
2003). The European Holly is well known for its adaptation to shaded habitats (Peterken & Loyd 1967).
To conclude, our study showed that changes induced
by scale insects in the balance between source and sink
tissues within a plant may explain some of the variability
in compensatory photosynthesis as a response to
herbivore impact. Provided that high temperature and
light conditions increase the feeding rates of scale
insects, we suggest that, under the conditions prevailing
when we measured effective quantum yield and electron
transport rates, scale insects would increase the plants
carbon demand, which would stimulate photosynthetic
rates in infested plants. By manipulating the leaf photosynthetic metabolism of their host plant, scale insects
can also affect the photosynthetic rates of scale-free

leaves surrounding infested leaves. Our study also


suggested that plant responses to scale insects may
be altered by growth conditions, and this could have
implications for the control of scale insect pests.

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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Received 26 November 2003; revised 13 April 2004;
accepted 10 May 2004

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