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x + 112 pp. Although Rodolia and other ladybirds have been successfully used to control pest coccids they have not proved effective in classical biological control programmes against aphids. A better understanding of the foraging behaviour of ladybirds and a more realistic theory of insect predator-prey dynamics are beginning to reveal the reason for this. Aphidophagous ladybirds exploit patches of aphid prey for feeding and reproduction. As suitable nurseries for their offspring patches of aphid prey generally only persist for about the same period of time as it takes the larvae of these ladybirds to complete their development. This is the case even in the absence of natural enemies. Thus aphids become scarce within a patch just when the food requirements of the ladybirds are greatest. Optimal foraging theory predicts that ladybirds should lay a few eggs early in the development of a patch and empirical data indicates that ladybirds appear to forage optimally. There have been several studies on the cues used by ladybirds when selecting patches of prey for oviposition. This review will consider how the responses shown by ladybirds may have shaped what has become known as the "egg window", how cannibalism may regulate the number of ladybirds within a patch, and the consequences of this for classical biological control.
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Biology, Ecology and Behaviour of Aphidophagous Insects
LADYBIRDS AND THE BIOLOGICAL CONTROL OF APHID POPULATIONS
A.F.G. DIXON & J.-L. HEMPTINNE
DIXON, A.F.G. & J.-L. HEMPTINNE 2003. Ladybirds and the biological control of
aphid populations. Pp. 1-10 in A.O. SOARES, M.A. VENTURA, V. GARCIA & J.-L.
HEMPTINNE (Eds) 2003. Proceedings of the 8th International Symposium on
Ecology of Aphidophaga: Biology, Ecology and Behaviour of Aphidophagous
Insects. Arquipélago. Life and Marine Sciences. Supplement 5: x + 112 pp.
Although Rodolia and other ladybirds have been successfully used to control pest coccids
they have not proved effective in classical biological control programmes against aphids. A
better understanding of the foraging behaviour of ladybirds and a more realistic theory of
insect predator- prey dynamics are beginning to reveal the reason for this.
Aphidophagous ladybirds exploit patches of aphid prey for feeding and reproduction. As
suitable nurseries for their offspring patches of aphid prey generally only persist for about
the same period of time as it takes the larvae of these ladybirds to complete their
development. This is the case even in the absence of natural enemies. Thus aphids become
scarce within a patch just when the food requirements of the ladybirds are greatest. Optimal
foraging theory predicts that ladybirds should lay a few eggs early in the development of a
patch and empirical data indicates that ladybirds appear to forage optimally.
There have been several studies on the cues used by ladybirds when selecting patches of
prey for oviposition. This review will consider how the responses shown by ladybirds may
have shaped what has become known as the "egg window", how cannibalism may regulate
the number of ladybirds within a patch, and the consequences of this for classical biological
control.
Anthony F.G. Dixon (e-mail: a.f.dixon@uea.ac.uk), School of Biological Sciences,
University of East Anglia, Norwich, NR4 7TJ, UK; Jean-Louis Hemptinne, Ecole Nationale
de Formation Agronomique, B.P. 87, FR-31326 Castanet-Tolosan, France.
THEORY
In classical insect predator-prey population
dynamics organisms in two trophic levels
interact; prey and predator (Fig. 1A).
A plant through it's morphology and
chemistry can directly affect the well being of
herbivores, and they similarly can affect
predators. That is, in addition to their effects on
one another's abundance a plant can have a direct
effect on a herbivore, which can have a direct
effect on a predator, and vice versa. In addition to
these direct effects there is a growing literature
that claims predators and parasitoids are attracted
by volatiles emitted by plants under attack by
herbivores. This is regarded as a mutualism, in
which the effectiveness of the searching
behaviour of the natural enemy is enhanced and
the herbivore pressure on the plant reduced
(P
RICE et al. 1980; Fig 1B). Predators are
considered to be part of a plant's defence. When
attacked by herbivores some plants emit volatiles
that are attractive to natural enemies, which has
resulted in them being likened to "body guards"
and the use of emotive phraseology like " the
enemy of my enemy is my ally" (D
ICKE &
S
ABELIS 1988; SABELIS et al. 2001). That
ladybirds respond to these volatiles is supported
by technically elegant studies in which gas
chromatography of plant volatiles was directly
coupled with recordings from the olfactory organs
of a ladybird. Herbivore damaged plants emit (Z)-
jasmone, which is attractive to adult Coccinella
septempunctata (B
IRKETT et al. 2000; NINKOVIC
et al. 2001). The central tenet of the mutualism
hypothesis is that herbivore-induced plant
volatiles enable natural enemies to more easily
find their prey and so reduce herbivore pressure.
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8th International Symposium on Ecology of Aphidophaga
University of the Azores, Ponta Delgada, 1-6 September 2002
Claims that such signals are so used by
parasitoids was scrutinized by VINSON (1999) and
VAN DER MEIJDEN & KLINKHAMMER (2000), who
found no field evidence for this.
Fig. 1. The direct and indirect effects on one another
of plants, herbivores and predators in classical insect
population dynamics (A) and plant predator
mutualisms (B).
Although there is no doubting that the
volatiles (synomones - DICKE & SABELIS 1988)
released by plants when attacked by herbivores
are attractive to predators and parasitoids, the way
in which they affect their searching behavior and
the distance over which they operate still needs to
be resolved. Discussions of this problem (e.g.
JANSSEN et al. 2002) tend to follow PRICE et al.
(1980) and only consider the adaptive
significance of herbivore-induced plant volatiles
in terms of plant fitness. It is generally assumed it
is advantageous for natural enemies to respond to
such signals. However, it is pertinent to ask -
What advantages would a predator gain by
responding to these signals? Here we consider
only ladybird beetles, but the principles are likely
to apply to all natural enemies.
It seems likely that the quantity of volatile
material released by a plant depends on the
intensity of herbivore attack, i.e., density-
dependent. If this is true then aphid-infested
plants are likely to be at their most attractive for
ladybirds when aphids are most abundant.
However, at this stage in the infestation it is
highly likely that ladybird larvae will already be
present. Therefore, responding to a strong cue
that a plant is under attack by aphids is not
necessarily advantageous. In addition, as not all
aphids are equally suitable as prey for ladybirds
(R
ANA et al. 2002) it is relevant to ask: - Is the
synomone emanating from a plant specific for a
particular species of aphid or a general response
to aphid infestation? Similarly, is the synomone
produced by a plant in response to being eaten by
lepidopterous larvae different from that produced
when infested with aphids? Therefore, in addition
to determining whether the odour originates
directly from the prey (prey pheromone
hypothesis) or indirectly - after feeding by the
prey - from the plant (plant synomone hypothesis)
there is an urgent need to determine whether the
signals are prey specific and how they affect
predators' searching behaviour. It is well
documented that bark beetles aggregate in
response to volatiles produced by trees and
attractant pheromones produced by the beetles,
and so overcome the host's defences by a mass
attack, but avoid heavily attacked trees, when the
beetles present produce deterrent pheromones
(WOOD 1982; RAFFA 2001). That is, if chemical
signaling by plants significantly influences
ladybird foraging then it is likely the signal is
complex, as in bark beetles.
Alternatively one can ignore plants when
considering predator-prey interactions, which is
the case in most mathematical models of
population dynamics. These have been widely
used to predict the behavior of predator-prey
systems, in particular their stability and the
outcome of introducing natural enemies on the
abundance of pests (B
EDDINGTON et al. 1976,
1978; HASSELL 1978; MURDOCH 1994). In spite
of the great and long-standing interest in these
models, there has been little success in using
them to account for why insect predators,
compared to parasitoids, have generally not been
very effective in suppressing the numbers of their
prey (D
EBACH 1964).
Our studies on the way insect predators, and
ladybirds in particular, forage, led to an
appreciation of the ecological significance of the
difference in mobility of juvenile and adult
insects; the latter can fly while the former cannot
(Fig. 2). That larvae generally stay within a prey
patch while adults may not was incorporated into
a model. Patch in this sense means the space that
a larva can explore by walking, usually one or
only a few adjacent plants, or even only part of an
individual plant as in the case of trees. Three
factors are likely to determine the reproductive
strategy of ladybirds to a much greater extent than
availability of food, which is the usual
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Biology, Ecology and Behaviour of Aphidophagous Insects
assumption of models of predator-prey systems:
(1) Ladybird developmental time is much longer
than that of its aphid prey and comparable with
the average duration of a patch of prey (Fig. 3;
H
EMPTINNE et al. 1990; HEMPTINNE & DIXON
1991). Thus it is maladaptive for a ladybird to lay
eggs in an old prey patch, as they are unlikely to
complete their development before the aphids
disappear. (2) As shown by KINDLMANN &
DIXON (1993), there should be a selective
advantage in optimizing the number of eggs laid
in a patch. This is because - as stated above -
ladybird developmental time is similar to the
duration of a patch of aphids. If many eggs are
laid, the ladybird larvae may reduce the rate of
increase of the aphids, cause an earlier decline in
aphid abundance, and thus food may become
scarce well before the larvae complete their
development (Fig. 3). (3) Cannibalism is common
in aphidophagous ladybirds and in nature often
reduces juvenile survival dramatically, as only
about 1% of the eggs laid in a patch survive
(D
IXON 2000). Cannibalism may be selected for
(see below) and even sibling cannibalism may
have a selective advantage, if prey becomes
scarce (OSAWA 1992). To avoid cannibalism,
adults should avoid patches of aphids where
ladybird larvae are already present.
Fig. 2. Aphidophagous ladybirds quickly leave patches
where aphids are scarce (A) but oviposit in patches
where prey is abundant (B). The larvae (D) that hatch
from the eggs (C) are confined to the patch, and have to
pursue and subdue the aphids they need for their
development.
Fig. 3.
Graphical presentation of the components of the ladybird-aphid interaction: temporal changes in the
abundance of aphids and relative developmental time of the ladybird, and the outcome if (A) the eggs are laid late,
(B) a few eggs are laid early, or (C) many eggs are laid early.
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8th International Symposium on Ecology of Aphidophaga
University of the Azores, Ponta Delgada, 1-6 September 2002
Assuming that the proportion of conspecifics
in the diet of ladybirds is proportional to their
relative abundance then if prey abundance is kept
constant the incidence of cannibalism increases
with increase in predator abundance. That is,
cannibalism is likely to act as a density dependent
mortality factor. Alternatively if the number of
predators is kept constant and that of their prey is
varied the incidence of cannibalism decreases
with increase in the abundance of prey (Fig. 4).
Fig. 4.
The predicted (A) increase in cannibalism with
increase in predator density, 50 and 150, and (B) the
decrease in cannibalism with increase in aphid density
when predator density is kept constant assuming that:
f(x, y) = ay/(x+y), where x is the number of prey, y is
the number of ladybirds and a is a scaling constant.
This is referred to as the "meet and eat"
hypothesis and accounts for the incidence of
cannibalism in time (D
IXON 2000). However, it is
just as plausible that the latter is due to the
occurrence in time of certain vulnerable stages -
eggs/hatchling larvae and pre-pupae/pupae, which
are unable to avoid or defend themselves against
active larvae. Whatever the reason for the
temporal incidence of cannibalism the outcome is
the same: cannibalism is proportional to the
relative abundance of the predator and therefore
likely to be density dependent.
Consideration of the above leads to the
prediction that there should be a strong selection
for ladybirds to lay eggs only in patches in the
early stages of development and avoid those
containing conspecific larvae (KINDLMANN &
DIXON 1993; DOSTALKOVA et al. 2002). Thus in
assessing the potential effectiveness of a predator
for biological control one should take into
account that selection maximizes predator fitness,
not its effectiveness as a biocontrol agent
(KINDLMANN & DIXON 1999a). In aphidophagous
ladybirds the major determinant of their
reproductive strategy is that their prey develops
much faster then they do (DIXON et al. 1995;
DIXON & KINDLMANN 1998; KINDLMANN &
DIXON 1999b). Therefore, the potential fitness of
an adult depends mainly on the future trends in
resource availability for its larvae, which unlike
the adult are confined to a patch (Fig. 2). This
leads to the following predictions. In arthropod
predator-prey systems in which the predator has a
long generation time relative to that of its prey
(ladybird/aphid systems), predator reproduction
should be correlated with the age of a prey patch
rather than the numbers of prey present, and top-
down regulation is unlikely. However, in
ladybird/ coccid systems, where both prey and
predator have similar developmental times,
ladybird reproduction is likely to be correlated
with prey abundance and top-down regulation is
possible (K
INDLMANN & DIXON 2001). In
addition there is evidence that specificity may
also be an important attribute of a biological
control agent. The coccidophagous ladybirds that
feed on Margarodidae, the group of coccids that
includes Icerya, are generally more specific than
those that feed on other groups of coccids. In
terms of successful control ladybirds have been
used 20 times more successfully to control
Margarodidae than other groups of coccids
(D
IXON 2000).
EXPERIMENTAL EVIDENCE FOR OPTIMAL
FORAGING IN LADYBIRDS
What evidence is there that selection maximizes
predator fitness? Below is presented the results of
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Biology, Ecology and Behaviour of Aphidophagous Insects
In the presence of conspecific larvae and/or
their tracks gravid females of Adalia bipunctata,
Coccinella septempunctata, Cycloneda limbifer,
Harmonia axyridis, and Semiadalia
undecimnotata become very active and if
prevented from leaving the area refrain from
laying eggs for a few hours (H
EMPTINNE et al.
1992; DOUMBIA et al. 1998; YASUDA et al. 2000;
R
ŮŽIČKA 2001b). Similar responses are observed
when females of A. bipunctata are placed on
plants in the field experimentally infested with
aphids and contaminated with larval tracks.
(Fréchette, unpublished). Although some species
of ladybird respond to the tracks left by larvae of
other species the response is generally statistically
insignificant and much weaker than that to
conspecific larvae or their tracks (H
EMPTINNE et
al. 1992; Y
ASUDA et al. 2000; RŮŽIČKA 1997b,
2001a, b). This is expected because the greatest
threat to the survival of a ladybird in its preferred
habitat, where it is likely to be the most abundant
ladybird, are individuals of the same species. In
addition, ladybirds appear to be well defended
chemically against intraguild predation
(A
GARWALA & DIXON 1992; HEMPTINNE et al.
2000). The deterrent effect of larval tracks is
density dependent and mediated via a pheromone
present in the tracks. In the case of A. bipunctata
the cue consists of a cocktail of alkanes, which
spread easily on the hydrophilic cuticle of plants
and so leave a large signal. In addition the
oviposition-deterring pheromone is very stable
lasting for at least 10 days (DOUMBIA et al. 1998;
H
EMPTINNE et al. 2001).
studies undertaken to assess this in the case of
aphidophagous ladybirds. In particular, this will
be done by examining the evidence for an egg
window, mechanisms for avoiding cannibalism
and the proposed consequences for aphid
abundance.
Egg Window
Experimental and field studies indicate there is a
density below which ladybirds are unlikely to lay
eggs (D
IXON 1959; WRATTEN 1973; HONĚK
1978). In addition, in the field ladybirds tend to
lay their eggs well before aphid populations peak
in abundance (Fig. 5; HEMPTINNE et al. 1992).
That is, there is a window in the development of a
patch of aphids when ladybirds are most likely to
lay their eggs. The opening of the window is
possibly determined by the minimum density of
aphids required for the survival of the first instar
larvae (DIXON 1959). The closing of the window
appears to be initiated by adults responding to the
presence of conspecific larvae (HEMPTINNE et al.
1992).
In summary, there is good field evidence that
aphidophagous ladybirds, as predicted by theory,
lay their eggs early in the development of patches
of aphids, and laboratory and field experiments
reveal the possible mechanisms by which this is
achieved.
Cannibalism
Fig. 5.
Distribution in time, relative to peak aphid
abundance of the laying of eggs by Adalia bipunctata
on lime trees. Development of aphid populations
expressed in weeks before and after the recorded peak
in aphid abundance in each year. (After H
EMPTINNE et
al. 1992)
Cannibalism is widely recorded for
aphidophagous ladybirds, but rarely mentioned in
the literature on coccidophagous species. Theory
predicts that it should occur when the relative
abundance of ladybirds is high and/or is
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8th International Symposium on Ecology of Aphidophaga
University of the Azores, Ponta Delgada, 1-6 September 2002
associated with an asymmetry between cannibal
and victim. The victim is usually at a vulnerable
stage in its development (AGARWALA & DIXON
1992), i.e., in the egg or pupal stage, or is smaller
or about to moult or pupate. That is, cannibalism
should be highest in the egg and pupal stages, and
in the fourth instar larval stage when prey is
likely to be scarce, and decrease with increase in
aphid abundance (Fig. 4). Life table studies done
on field populations and laboratory studies (Fig.
6) support these predictions (A
GARWALA &
DIXON 1992; YASUDA & SHINYA 1997).
Fig. 6.
The incidence of cannibalism in the laboratory
of clutches of eggs (A) and larvae (B) of Adalia
bipunctata in relation to aphid abundance (After
A
GARWALA & DIXON 1992)
In the grain beetle Tribolium there are strains
that show either a high or a low level of
cannibalism, which is genetically determined
(STEVENS 1992). This has also been shown for H.
axyridis (W
AGNER et al. 1999). Thus, selection
should favour an optimum level of cannibalism in
a given environment. That is, a species may be
more or less cannibalistic than one would expect
on the basis of the predicted frequency of
encounters between conspecifics outlined above.
Is there any evidence for this? Clearly some
species are more difficult to rear collectively
because they show higher levels of cannibalism
than other species (unpublished results). A recent
study of cannibalism in the aphidophagous
ladybird H. axyridis indicates it prefers to eat
conspecifics (G
AGNÉ et al. 2002). Thus
cannibalism would appear to have been selected
for in the individuals of H. axyridis used in this
study.
Not only does the high probability of egg
cannibalism make it advantageous for ladybirds
to avoid ovipositing in patches of prey already
occupied by conspecific larvae field, but evidence
indicates that cannibalism, as predicted by theory,
serves subsequently to regulate the numbers of
ladybird larvae within a patch (Fig. 7).
Fig. 7.
The relationship between egg cannibalism and
the number of eggs of Adalia bipunctata per unit area
of lime foliage in relation to aphid abundance in the
field (After M
ILLS 1982)
That is, cannibalism is strongly density
dependent and capable of regulating the
abundance of ladybird larvae within patches
(K
INDLMANN & DIXON 2001).
In summary, there is good field evidence that
cannibalism is widespread and an important
mortality factor potentially capable of regulating
the abundance of aphidophagous ladybird larvae
in a patch.
Aphid abundance
The prediction that ladybirds that forage
optimally have little affect on aphid abundance
(K
INDLMANN & DIXON 1993) is the most
contentious. The implied altruism on the part of
the ladybirds and criticism of biological control
practice has greatly impeded the general
acceptance of this supposedly counterintuitive
6
Biology, Ecology and Behaviour of Aphidophagous Insects
idea. There is good evidence that ladybirds forage
in a way similar to that predicted by optimal
foraging theory and they achieve this by
behaviour that is clearly adaptive at the individual
level. The fact that cannibalism is adaptive and
strongly density dependent indicates that ladybird
numbers are likely to be strongly auto-regulated.
Therefore, the prediction that ladybirds should
have little affect on aphid abundance is in reality
also not counterintuitive.
Unlike in other studies (e.g. ELLIOT &
KIECKHEFER 2000) the shrubs were not caged, so
the patches in effect were open to both
immigration and emigration of both aphids and
ladybirds as in natural ecosystems. That is, as
predicted by theory these predators do not have a
negative effect on the peak numbers of aphids in
nature.
In summary, although well based theoretically
and supported by a rigorous field experiment, the
prediction that aphidophagous ladybirds have
little affect on aphid abundance is likely to be
subject to further critical experimentation before
it is generally accepted.
This prediction was tested by monitoring the
numbers of the aphid, Aphis gossypii, on 34 two
metre high shrubs of Hibiscus syriacus in the
field. All the eggs of Coccinella septempunctata
brucki were removed from 8 of the shrubs, all
those of Harmonia axyridis from another 8, all
the eggs of both ladybirds from another 12 and no
eggs were removed from the remaining 6 shrubs
(control). Sticky bands were placed around the
base of the stem of each shrub to prevent the
immigration of larvae on to the shrubs from
surrounding plants. The results were very variable
but clearly indicate that the presence of
aphidophagous predators on the shrubs did not
significantly affect the peak number of aphids
(Fig. 8).
CONCLUSIONS
Although the idea of a mutualism between plants
and ladybirds is an attractive one there are no
compelling theoretical reasons for, or field
evidence of, such a relationship. Classical
predator-prey models do not account for why
insect predators are generally less effective in
suppressing the abundance of pests than
parasitoids. A model that includes the essential
features of the foraging behavior of larvae and
adults and the reproductive behavior of adult
ladybirds predicts the patterns observed in the
field. The major determinant of abundance in this
system is the relative developmental times of the
predator and prey - generation time ratio (GTR)
hypothesis. If that of the predator is considerably
longer than that of the prey, as in aphid/ladybird
systems, than top down regulation of prey
abundance is unlikely, whereas when it is of
similar length, as in coccid/ladybird systems, then
top down regulation is possible. The cues used by
aphidophagous ladybirds to assess the quality of
patches of prey have been identified and
rigorously assessed. That is, in the last ten years
there has been a great advance in our
understanding of the patterns and processes in
ladybird-prey interactions.
Fig. 8.
The peak number of Aphis gossypii on Hibiscus
shrubs in the field when aphid numbers were monitored
in the presence of all the naturally occurring natural
enemies (control), and when all the Harmonia axyridis
(H.a) or Coccinella septempuntata brucki (C.s.) or both
species of ladybird (H.a. + C.s.) were removed at the
egg stage.
The GTR model should apply to all insect
predators. However, as far as aphidophaga are
concerned it makes a prediction: those that have
longer generation times than aphids should
behave similarly to ladybirds. Although this has
not been studied intensively many are known to
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8th International Symposium on Ecology of Aphidophaga
University of the Azores, Ponta Delgada, 1-6 September 2002
be cannibalistic and show similar reproductive
behaviour. For example, the adults of some
cecidomyids, chrysopids and syrphids are
deterred from ovipositing by the presence of
conspecific larvae or their tracks (H
EMPTINNE et
al. 1993; R
ŮŽIČKA 1994, 1996, 1997a, 1998;
RŮŽIČKA & HAVELKA 1998). Thus, it is likely
that the GTR hypothesis holds for all insect
predators. At present the best support for this
comes from studies on aphidophagous insects.
DIXON, A.F.G. & P. KINDLMANN 1998. Generation ratio
and the effectiveness of ladybirds as classical
biological control agents. Pp. 315-320 in M.P.
ZALUCKI, R.A.I. DREW & G.G. WHITE (Eds.) Pest
Management - Future Challenges 1. University of
Queensland Printery.
D
OSTÁLKOVÁ, I., P. KINDLMANN & A.F.G. DIXON 2002.
Are classical predator-prey models relevant to the
real world? Journal of Theoretical Biology 218:
328-330
D
OUMBIA, M., J.-L. HEMPTINNE & A.F.G. DIXON 1998.
Assessment of patch quality by ladybirds: role of
larval tracks. Oecologia 113: 197-202.
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9
8th International Symposium on Ecology of Aphidophaga
University of the Azores, Ponta Delgada, 1-6 September 2002
interspecific predation in two predatory ladybirds
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Accepted 31 May 2003.
10
... Coccinellids feed primarily on aphids and only opportunistically upon other prey (Hodek & Honěk, 1996). As a consequence, the release of the larvae usually does not result in the establishment of self-perpetuating populations (Powell & Pell, 2007) since coccinellids lay eggs in patches with aphid colonies at an early stage of development, and their developmental time is similar to the average duration of an aphid colony (Dixon & Hemptinne, 2003). Mirids are broad generalists and polyvoltine species and their density is not only influenced by the density of a specific prey (Harmon & Andow, 2004). ...
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