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Oviposition responses to patch quality in the larch ladybird Aphidecta obliterata (Coleoptera: Coccinellidae): Effects of aphid density, and con- and heterospecific tracks

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The effects and persistence of oviposition-deterring semiochemical cues from conspecific and heterospecific larval tracks on the oviposition rate of Aphidecta obliterata (Linnaeus) females were investigated. In addition, the effects of varying aphid prey density were considered and also whether any resulting response originated from differential nutritional status of females and/or due to aphid odour stimuli. The existence of oviposition responses to conspecific egg chemicals was also considered. Gravid A. obliterata females were deterred from oviposition by conspecific larval tracks and the effect was density dependent. Females actively avoided searching in these contaminated areas. Tracks induced a significant effect on oviposition for up to three days. Heterospecific tracks of the coccinellid Adalia bipunctata (Fabricius) or the chrysopid Chrysoperla carnea (Stephens) did not induce any oviposition response in A. obliterata females. Increasing aphid density induced increased oviposition rate in A. obliterata females. Nutritional status of females was an important factor in the relationship between aphid density and oviposition rate, but aphid associated cues (odours) were not. There was an inhibitory effect of extracts of conspecific egg-surface chemicals on oviposition by A. obliterata females. In the field, cannibalism, competition and limited food availability represent the major threats to egg and larval survival. Patch quality assessment mechanisms enable females to lay eggs at sites where offspring survival is maximized. Oviposition-deterring semiochemicals tend to promote more even distribution of predators over prey patches.
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Oviposition responses to patch quality in
the larch ladybird Aphidecta
obliterata (Coleoptera: Coccinellidae):
effects of aphid density, and con- and
heterospecific tracks
T.H. Oliver, J.E.L. Timms, A. Taylor and S.R. Leather
*
Division of Biology, Imperial College London, Silwood Park Campus,
Ascot, Berkshire, SL5 7PY, UK
Abstract
The effects and persistence of oviposition-deterring semiochemical cues from
conspecific and heterospecific larval tracks on the oviposition rate of Aphidecta
obliterata (Linnaeus) females were investigated. In addition, the effects of varying
aphid prey density were considered and also whether any resulting response
originated from differential nutritional status of females and/or due to aphid odour
stimuli. The existence of oviposition responses to conspecific egg chemicals was also
considered. Gravid A. obliterata females were deterred from oviposition by conspecific
larval tracksand the effectwas density dependent. Females activelyavoided searching
in these contaminated areas.Tracksinduceda significant effect on oviposition for up to
three days. Heterospecific tracks of the coccinellid Adalia bipunctata (Fabricius) or the
chrysopid Chrysoperla carnea (Stephens) did not induce any oviposition response
in A. obliterata females. Increasing aphid density induced increased oviposition rate in
A. obliterata females. Nutritional status of females was an important factor in the
relationship between aphid density and oviposition rate, but aphid associated cues
(odours) were not. There was an inhibitory effect of extracts of conspecific egg-surface
chemicals on oviposition by A. obliterata females. In the field, cannibalism, competition
and limited food availability represent the major threats to egg and larval survival.
Patch quality assessment mechanisms enable females to lay eggs at sites where
offspring survival is maximized. Oviposition-deterring semiochemicals tend to
promote more even distribution of predators over prey patches.
Keywords: Aphidecta obliterata, Adalia bipunctata, Chrysoperla carnea, ladybirds,
oviposition, prey density, semiochemicals, patch quality
Introduction
The larch ladybird Aphidecta obliterata (Linnaeus)
(Coleoptera: Coccinellidae) is an important natural enemy
of the green spruce aphid, Elatobium abietinum (Walker)
(Hemiptera: Aphididae), a serious pest of Sitka spruce (Picea
sitchensis Bong. (Carr.)), Britain’s main commercially grown
tree (Carter & Halldorson, 1998). Aphidecta obliterata has been
used in a biological control programme in Germany to
control Adelges piceae (Ratzeburg) (Hemiptera: Adelgidae), a
pest of Abies spp. (Hodek, 1973). The foraging behaviour of
aphidophagous coccinellids (Dixon, 1959; Wratten, 1973;
Mills, 1982; Carter & Dixon, 1984) and the interactions
between larvae and adults (Hassell, 1978; Hemptinne et al.,
1992) have been much studied, but relatively little attention
*
Author for correspondence
Fax: ++ 44 (0)2075942339
E-mail: s.leather@ic.ac.uk
Bulletin of Entomological Research (2006) 96, 25–34 DOI: 10.1079/BER2005395
has been paid to semiochemical spacing of aphidophagous
predators over prey patches of different quality (Evans &
Dixon, 1986).
Potential oviposition sites differ in the probability of
offspring survival due to spatial variation in prey, predator
and competitor abundance. Egg-laying females obtain
different fitness returns depending on oviposition site,
setting up selection pressures facilitating the evolution of
patch quality assessment mechanisms by females. These
mechanisms involve receiving appropriate stimulation
from mechano- and chemoreceptors to induce oviposition
(Chapman, 1998). Many species of aphidophagous preda-
tors, from three insect orders: Neuroptera, Coleoptera and
Diptera, have been shown to possess larvae whose tracks
contain semiochemicals acting to deter oviposition by
conspecific females. Coccinellids studied include Adalia
bipunctata (Fabricius) (Doumbia et al., 1998), Coccinella
septempunctata (Linnaeus) (Ru
˚
z
ˇ
ic
ˇ
ka 1997; Doumbia et al.,
1998), Cycloneda limbifer (Casey), Semiadalia undecimnotata
(Schneider) (Ru
˚
z
ˇ
ic
ˇ
ka, 2001) and Harmonia axyridis (Pallas)
(Yasuda et al., 2000).
Coccinellid larvae may deposit oviposition-deterring
semiochemicals (ODS) from the tip of their abdomen, which
they use as a pseudopod (Ru
˚
z
ˇ
ic
ˇ
ka, 2001). The chemicals are
possibly detected by adults using the maxillary palpi
(Ru
˚
z
ˇ
ic
ˇ
ka, 2003). Oviposition-deterring semiochemicals have
been shown to be soluble in chloroform (Ru
˚
z
ˇ
ic
ˇ
ka, 1994;
Doumbia et al., 1998) and also water (Ru
˚
z
ˇ
ic
ˇ
ka, 1994; Ru
˚
z
ˇ
ic
ˇ
ka
& Havelka, 1998). However, this conflicts with evidence that
they comprise mixtures of (hydrophobic) alkanes similar to
those found on the elytra of the adults and on the surface of
conspecific eggs (Hemptinne et al., 1998, 2001). The alkanes
on elytra are used in mate recognition (Hemptinne et al.,
2000c), and those on the surface of eggs may be important in
chemical defence from intraguild predation (Agarwala &
Yasuda, 2001). A similar mixture of alkanes is also secreted
from the under-surface of ladybird tarsi aiding adhesion
onto smooth surfaces (Kosaki & Yamaoka, 1996). Hemptinne
et al. (2000c) speculate that these similar molecules, with
different context dependent messages, are an example
of semiochemical parsimony. The alkane semiochemicals of
larval tracks show some degree of persistence. Ten-day-old
fourth-instar larval tracks of A. bipunctata are sufficient to
prevent oviposition in gravid females (Hemptinne et al.,
2001). Other coccinellids studied include C. septempunctata,
C. limbifer and S. undecimnotata (Ru
˚
z
ˇ
ic
ˇ
ka, 2002). It appears
persistence of oviposition-deterring semiochemical tracks
varies between species.
Coccinellids refrain from ovipositing at sites where there
are few aphids present (Dixon, 1959). It has been established
that aphidophagous ladybirds lay most of their eggs over a
relatively short period of time early in the development of
aphid colonies (Hemptinne et al., 2000a), the ‘egg window’
(Dixon, 1997). The window opens when aphids are abundant
enough for sufficient survival of larvae developing from
eggs. ‘Closing of the window’ probably occurs when
conspecific larvae become so abundant in a patch that any
further eggs laid are likely to be cannibalized (Hemptinne
et al., 1992). Increased oviposition with prey density may
simply result from the correlation between satiation level
and oviposition rate (Banks, 1954). External aphid-associated
cues, however, may also stimulate increased oviposition:
oviposition by coccinellids can be triggered by chemical
traces of their prey (Evans & Dixon, 1986).
The current study considers the nature and persistence of
the effects of con- and heterospecific tracks on oviposition in
the previously unstudied larch ladybird, Aphidecta obliterata.
Any results will contribute usefully to an expanding frame-
work of knowledge allowing us to further understand the
extent of ovipostion-deterring behaviour in response to
larval tracks. The effects of varying aphid density while
simultaneously varying the conspecific larval track contam-
ination of filter paper substrates is also examined, allowing
us to undertake a multivariate analysis and consider the
combined effects of both variables (aphid density and
oviposition-deterring semiochemical concentration) on
oviposition behaviour in A. obliterata. The study then
determines whether increased oviposition rate with aphid
density can be partly attributed to chemical cues from aphids
stimulating oviposition, rather than solely satiation-induced
effects. Finally we test Hemptinne et al.’s (2000c) hypothesis
of semiochemical parsimony by considering whether
A. obliterata egg surface chemicals also inhibit oviposition.
Materials and methods
Insect culture
Larch ladybirds Aphidecta obliterata and two-spot lady-
birds Adalia bipunctata were reared at 20
C+2
C and a
photoperiod of 16 h light and 8 h darkness, kept in 5-l plastic
containers, which also included a piece of corrugated filter
paper on which the ladybirds often laid eggs. Each day, the
box was cleaned of debris and a fresh filter paper placed
inside. Any filter papers containing eggs were transferred to
an 18 cm Petri dish and incubated under the same laboratory
conditions as the adults. Larvae hatching from eggs were
kept in the same conditions. Each day, adults and larvae
were fed an excess of aphids. Aphidecta obliterata were
preferentially fed on an excess of bird-cherry–oat aphids,
Rhopalosiphum padi (Linnaeus) from the laboratory culture
(described below). If the cultures became exhausted, spruce
aphids E. abietinum, rose aphids Macrosiphum rosae (Walker)
and artificial food mix (Majerus & Kearns, 1989) were used
to supplement the diet. Adalia bipunctata were preferentially
reared on an excess of pea aphids Acyrthosiphon pisum
(Harris). If these were unavailable then spruce aphids
E. abietinum, rose aphids M. rosae, nettle aphids Microlophium
carnosum (Theobald) and artificial food supplement was
used. Once a week the adults were transferred to clean
containers to stimulate egg laying. Lacewing larvae, Chryso-
perla carnea (Stephens) (Neuroptera: Chrysopidae) were
obtained as third instars (supplier: the ‘Green Gardener
1
’)
and fed a similar diet to A. bipunctata.
Female ladybirds were used in the experiments. Lady-
birds were sexed under a low power dissecting microscope
(Majerus & Kearns, 1989). After sexing, females were kept in
5-l plastic boxes with approximately 25 individuals per box.
Broad bean plants (Vicia fabae), obtained from Nickerson-
Zwaan
1
, were kept in the laboratory to culture pea aphids
A. pisum and barley plants (Hordeum vulgare L.) (same
supplier) used to culture bird-cherry–oat aphids, R. padi.If
the cultures became exhausted, spruce E. abietinum, rose
M. rosae and nettle M. carnosum aphids were collected from
outside the laboratory.
26
T.H. Oliver et al.
Searching behaviour
To establish the effect of larval secretions on the searching
behaviour of adult larch ladybirds, a choice test was carried
out. Four third-instar A. obliterata larvae were kept in a
4.5 cm diameter Petri dish containing a 4.25 cm filter paper in
the base. After 4 h the larvae were returned to the stocks and
the filter papers were removed. The choice test arena
involved a 4.5 cm Petri dish with half a clean filter paper
and half a paper that had previously been stored with the
larvae. An adult female A. obliterata was then placed in the
Petri dish, covered with a non-airtight lid, and left for 5 min.
After this initial time the location of the ladybird was noted
down every minute for 30 min. This procedure was repeated
20 times.
Oviposition deterrence by con- and heterospecific tracks
Aphidecta obliterata females were offered a choice of
oviposition sites (contaminated with larval tracks or uncon-
taminated). A 4.25 cm filter paper was placed inside each of
four 4.5 cm Petri dishes. Two, five or ten fourth instar larvae
of A. obliterata were placed inside each dish. One dish
contained no larvae as a control. Larvae were allowed
to remain in the dishes for 3.5 h to enable larval pheromones
to adequately contaminate the filter paper, without being so
long that cannibalism occurred. Larvae were then removed
and faecal spots brushed off each filter paper using a fine
paintbrush. Each filter paper was labelled with a number
using a ballpoint pen, referring to the number of larvae
contained in each dish. The filter paper in the dish which
had held no larvae was also labelled with a ‘zero’. It is
assumed that an approximately equal amount of ink was
marked on each paper, therefore this should not affect the
results. Each filter paper was folded in a similar way to make
it corrugated and a small piece of Blu-tack
1
attached to the
centre of one side. The four filter papers were then secured
onto the base of an 18 cm Petri dish in a square arrangement
so that each filter paper was equidistant from the others and
the centre of the square arrangement in the centre of the Petri
dish (i.e. so that differences in oviposition rate on the
different filter paper substrates could not be attributed to
effects of spatial positioning; light on the Petri dishes was
from directly above and the external environment in the
laboratory was relatively uniform). Ten satiated A. obliterata
females were then placed into the large Petri dish and left for
24 h. A preliminary investigation found that sometimes eggs
observed part way through the 24 h period were not always
present at the end of experiment. Therefore the number of
eggs present on each filter paper was recorded at intervals of
5 and 10 h in addition to the final 24 h count, and any eggs
thus known to have been cannibalized in the intervening
periods were added to the final count. All replicates were
started at approximately 0900 h each day. Infrequently, eggs
were on the base of the Petri dish directly below a filter
paper; these were assumed to have been dislodged during
the experiment and included in the egg count of the paper
which they were below. If eggs were present on the Petri
dish, but not below any filter paper, they were omitted from
the filter paper egg counts. Each test was replicated ten
times.
The same procedure was followed using fourth instar
A. bipunctata and third instar C. carnea to test for effects of
heterospecific tracks.
Persistence
The persistence of the tracks produced by the larvae was
investigated by first obtaining filter papers with A. obliterata
larval tracks on using the method described above. These
were then stored in ventilated plastic boxes for three, five,
seven, nine or 11 days. On each of the appropriate days an
adult female was placed in a Petri dish containing the
contaminated paper along with an excess of R. padi aphids.
As before, the number of eggs produced was recorded, and
the procedure was repeated 20 times for each of the
treatments.
Conspecific tracks and aphid density
An identical procedure to the one above for the
investigation of effects of conspecific tracks on oviposition
rate was employed, except that aphids were present during
the 24 h oviposition period, allowing us to consider the
effects of conspecific tracks and aphid density simulta-
neously. No, 200, 400 or 600 aphids were placed with the ten
A. obliterata females for the duration of the 24 h period. To
ensure the aphids did not escape during the experiment the
sides of the Petri dish were coated in Fluon
1
. Eggs on each
filter paper were then counted and recorded in the same way
as before. A preliminary control investigation ensured that
aphids in the Petri dish without predators, over a 24 h
period, did not have a tendency to aggregate to any one of
the filter papers in particular, showing that any differences
in oviposition rate on the differentially contaminated filter
papers were not due to differences in local aphid density. To
control for variation in fecundity over time, each test (0, 200,
400 and 600 aphids) was carried out once per day. This
ensured that any variation in fecundity over time (ladybirds
have been shown to have triangular reproductive functions
(Dixon, 2000)) was not mistakenly attributed to be due to
changes in our explanatory variables. Each test was
replicated ten times except for the 600 aphid treatment
which was only repeated five times due to lack of available
aphids.
Satiation
Before the experiment, ten A. obliterata females were
starved for 12 h; all kept in an 18 cm Petri dish with a piece of
9 cm corrugated filter paper. Another ten females were kept
in similar conditions except that excess aphids were present
in the dish so that these females would begin the experiment
in a satiated condition. For the experiment, each female was
placed into an individual 9 cm Petri dish with a piece of
corrugated 4.25 cm filter paper. The total number of eggs
each female had laid after 12 h was recorded. Ten replica-
tions were carried out.
Prey-associated chemical cues
Before the experiment, ten pieces of 4.25 cm filter paper
had 50 R. padi aphids pressed onto them. Another ten were
left untouched as a control. Ten satiated A. obliterata females
were each placed in an individual 18 cm Petri dish contain-
ing two pieces of 4.25 cm corrugated filter paper (one clean,
one contaminated), arranged to mitigate spatial positioning
biases. After 24 h, the relative number of eggs on each filter
paper across the ten replications was recorded.
Oviposition responses to patch quality in larch ladybird
27
Egg surface chemicals
To determine whether egg surface chemicals had an
effect on the oviposition rate of A. obliterata, 50 eggs were
placed in a small vial and washed with 0.5 ml hexane
solution (97% ) (Hemptinne et al. (2000b) successfully used
n-hexane to wash defensive chemicals off egg surfaces in
order to quantify their effects on intraguild predation). Eggs
used were approximately 3 days old, as eggs recently laid
were too soft and presented a risk of contaminating the
solution with egg yolk chemicals. Another vial contained
0.5 ml hexane, but no eggs. The vials were left for 1 h then,
using a fine paintbrush, tracks were painted onto pieces of
4.25 cm filter paper. An 18 cm Petri dish was set up with two
pieces of filter paper (one with hexane egg-wash tracks,
the other with hexane control tracks) and ten satiated
A. obliterata were placed inside and left for 24 h. The
experiment was replicated ten times.
Statistical analysis
The experiments concerning oviposition deterrence by
con- and heterospecific tracks and persistence of oviposition-
deterring semiochemicals were analysed using ANOVA in
the program ‘R’. A generalized linear model was used for
egg count data, as the response variable was not normally
distributed (there were many cases when zero eggs were
recorded). In some cases the scale parameter was greater
than one (residual deviance/d.f. > 1), indicating the data
were overdispersed, therefore the ‘quasi’ function was used
to define a different family of error structures. Treatment
degrees of freedom followed by error degrees of freedom are
quoted in subscript beside each F value. Other data were
analysed using t-tests; paired tests when appropriate. If the
variances were significantly different, as deduced from a
Fisher’s F test, then variances were estimated separately for
both groups, and a t-test with the Welch modification to the
degrees of freedom was used. For the searching behaviour
data, the time spent on uncontaminated filter papers
compared with the time spent on larval-track contaminated
filter paper was non-independent. Therefore the proportion
of time spent on uncontaminated papers was calculated and
a Wilcoxon’s signed rank test was used to determine
whether the mean was significantly greater than 0.5.
Results
Searching behaviour
Aphidecta obliterata females spent significantly more time
on clean filter papers compared with filter paper contami-
nated with conspecific larval tracks (Wilcoxon’s signed rank
test: P < 0.01, n = 20) (fig. 1). The average percentage of times
which the females were found on each of the substrates was
33% (147/442 occasions) for the contaminated filter paper
and 67% (295/442 occasions) on the clean filter paper.
Oviposition deterrence by con- and heterospecific tracks
Conspecific larval tracks significantly inhibited oviposi-
tion by A. obliterata females (ANOVA: F
1,38
= 10.665, P < 0.01).
In addition, the oviposition-deterring effects of conspecific
larvae were positively density dependent, with increasing
larval density increasing the degree of oviposition inhibition
(fig. 2). The control treatment (zero larvae) was significantly
different compared with all the larvae treatments (ANOVA:
t = 4.011, P < 0.001). The two-larvae treatment was signifi-
cantly different to the five- and ten-larvae treatments
(t = 2.838, P < 0.01). The five-larvae treatment, however, was
not significantly different from the ten-larvae treatment
(t = 0.951, P = 0.34, NS).
In contrast, using ANOVA with a four-level factor,
contamination of filter paper substrates by A. bipunctata
larvae had no significant effect on oviposition rate of
A. obliterata females (ANOVA: F
3,36
= 1.510, P = 0.23, NS)
(fig. 3). Model simplification, however, led to a marginally
significant single-degree-of-freedom contrast between the
uncontaminated control (zero larvae) and the larval treat-
ments (ANOVA: t = 2.126, P < 0.05). The different larval
treatments (two, five and ten larvae) were not significantly
different (ANOVA: t = 4.82e
x14
, NS).
Similarly, larval tracks of the chrysopid C. carnea did not
significantly affect oviposition by A. obliterata females
(ANOVA: F
3,36
= 2.739, P = 0.058, NS) (fig. 4). There was a
significant difference between number of eggs laid in the
highest density of C. carnea treatment compared with the
control (ANOVA: t = 2.211, P < 0.05). This ten-larvae treat-
ment, however, was not significantly different to the other
treatments combined (ANOVA: t = 1.893, P = 0.066, NS).
0
2
4
6
8
10
12
14
16
18
Clean substrate Contaminated substrate
Mean time spent on treatment
Fig. 1. Average time spent by 20 female Aphidecta obliterata on
clean filter papers (14.75+1.56 (S.E., n = 20) min) and filter
papers contaminated with larval tracks (7.35+1.18 (S.E., n = 20)
min).
0
0.5
1
1.5
2
2.5
02510
No.
A. obliterata
larvae
Mean no. eggs
Fig. 2. Mean number of eggs laid by Aphidecta obliterata females
over 24 h on four filter paper substrates contaminated with
tracks of different numbers of conspecific larvae. Bars indicate
standard errors of means.
28
T.H. Oliver et al.
Persistence
Age of larval track was found to have a significant effect
on the number of eggs laid by A. obliterata females (ANOVA,
F
2,137
= 4.6273, P < 0.05). To obtain the minimum adequate
model the age of tracks was collapsed into three levels:
control, fresh tracks (1–3 days) and old tracks (5–11 days).
Fresh tracks elicited a significantly different oviposition rate
than the uncontaminated control (ANOVA: t = 2.791,
P < 0.01). Oviposition response to old tracks, however, was
not found to be significantly different to the control
(ANOVA: t = 1.150, P = 0.252, NS) (table 1).
After the initial deterrent effect from the production of
larval tracks, the total number of eggs produced increased on
each of the following days. The numbers of eggs produced on
subsequent days formed a linear relationship with the age of
the tracks, with a high correlation coefficient (r
2
= 0.96) (fig. 5).
Conspecific tracks and aphid density
A factorial two-way ANOVA was used to analyse the
results. Both explanatory variables (larval tracks and prey
density) had a significant effect on oviposition rate of
A. obliterata: Increasing the degree of conspecific larval track
contamination of filter papers significantly inhibited ovipo-
sition by A. obliterata females (ANOVA: F
3,136
= 18.149,
P < 0.001). Simultaneously, increasing the density of aphid
prey present significantly increased oviposition rate
(ANOVA: F
3,136
= 25.256, P < 0.001) (fig. 6). There was no
significant difference, however, between the 400 and 600
aphid treatments and these could be combined with no
significant loss in explanatory power to the minimum
adequate model (ANOVA: F
1,136
= 0.0127, P = 0.91, NS).
Therefore at very high aphid densities ( > 400) there was no
significant further increase in oviposition (fig. 7). This
suggests there is some upper threshold of aphid density at
which maximum oviposition occurs. Beyond this threshold,
further increases in aphid density have little effect on
oviposition rate of A. obliterata.
There was no significant interaction between prey density
and contamination by larval tracks (ANOVA: F
9,124
= 0.4564,
P = 0.9, NS).
Satiation
Aphidecta obliterata females starved 12 h prior to the
experiment laid significantly fewer eggs than those satiated
when the experiment began (t = 3.76, df = 18, P < 0.001), with
an average oviposition rate of 4.0+2.2 (S.E., n = 10) per
female per 12 h, compared with 7.9+2.4 (S.E., n = 10) for
satiated individuals.
Prey-associated chemical cues
Oviposition rate of A. obliterata females did not differ
significantly between filter papers contaminated with aphid
chemicals and clean filter papers (control) (t = 0.2095, d.f. = 9,
0
1
2
3
02510
No.
A. bipunctata
larvae
Mean no. eggs
Fig. 3. Mean number of eggs laid by Aphidecta obliterata females
over 24 h on four filter paper substrates contaminated with
tracks of different numbers of Adalia bipunctata larvae. Bars
indicate standard errors of means.
0
0.5
1
1.5
2
2.5
3
02510
No.
C. carnea
larvae
Mean no. eggs
Fig. 4. Mean number of eggs laid by Aphidecta obliterata females
over 24 h on four filter paper substrates contaminated with
tracks of different numbers of Chrysoperla carnea larvae. Bars
indicate standard errors of means.
0
10
20
30
40
50
60
70
1357911
Age of tracks (days)
Total no. eggs
Fig. 5. Linear relationship between age and increase in number
of eggs produced. The line representing the relationship has the
equation y = 4.3x+15.03 (r
2
= 0.96).
0
2
5
10
0
200
400
600
0
2
4
6
8
10
12
Mean no. eggs
No. conspecific
larvae
No. of aphids
Fig. 6. Mean number of eggs laid by Aphidecta obliterata females
over 24 h on filter paper substrates differentially contaminated
with conspecific larval tracks across a range of prey densities.
Standard error bars have been omitted for clarity of expression.
Oviposition responses to patch quality in larch ladybird
29
P = 0.84, NS). The average number of eggs laid per 10 females
on clean papers was 3.8+1.2 (S.E., n = 10) compared with
4.3+1.9 (S.E., n = 10) on papers contaminated with pressed
aphids.
Egg surface chemicals
Contaminating the filter papers with the chemical extract
of the surface chemicals from conspecific eggs reduced
oviposition from an average of 6.0+1.5 (S.E., n = 10) eggs
per 10 females on clean papers, to 2.6+0.5 (S.E., n = 10) eggs
per 10 females on contaminated papers. The difference
between the means was close to significance, but above
the conventional Type I error margin (a = 0.05) (t = 2.134,
d.f. = 11, P = 0.0559).
Discussion
Oviposition deterrence by con- and heterospecific tracks
Aphidecta obliterata is significantly less likely to oviposit
on sites contaminated with pheromones from conspecific
larval tracks and the deterrence effects of these pheromones
appear to be positively dependent on the density of larvae
present, thus adults can determine the relative densities of
larval tracks. Similar effects of conspecific larval tracks in
other coccinellid species include A. bipunctata (Doumbia
et al., 1998), C. septempunctata (Ru
˚
z
ˇ
ic
ˇ
ka, 1997; Doumbia et al.,
1998), C. limbifer and S. unidecimnotata (Ru
˚
z
ˇ
ic
ˇ
ka, 2001).
Originally it was assumed that oviposition deterrence
occurred in relation to the frequency of encounters with
larvae (Hemptinne et al., 1992). It is clear, however, that an
alternative mechanism that does not rely on physical
encounters, exists to assess the density of conspecific larvae:
oviposition-inhibition by oviposition-deterring semiochem-
icals. The frequency of female contact with a network of
oviposition-deterring tracks is likely to be higher than the
frequency of female encounter with the larvae (Ru
˚
z
ˇ
ic
ˇ
ka,
2001). Oviposition-deterrence in response to larval phero-
mones has evolved as a patch quality-assessment and
response adaptation to reduce the risk of intraguild preda-
tion and increase the availability of prey for developing
offspring. It reduces the risk of cannibalism and competition
and allows coccinellids to synchronize generations with
transient aphid colonies. Density of larval tracks positively
correlates to degree of egg cannibalism both under labora-
tory conditions (Dixon, 2000), and in the field (Mills, 1982).
Cannibalism can be a major source of egg and early instar
larval mortality in aphidophagous coccinellids (Agarwala &
Dixon, 1992; Agarwala et al., 1998; Gagne
´
et al., 2002). High
densities of competing larvae result in smaller individuals
with reduced fecundity in adulthood (Dixon, 2000). This is
especially true in the competitive environment of patchy
resources (Agarwala et al., 2003). Also, exceeding the
optimum number of predators per patch may severely
restrict the rate of increase of aphid prey and cause an earlier
collapse of the colony (Hemptinne & Dixon, 1997). On
average, aphid colonies rarely last for more than a month
(Hemptinne & Dixon, 1997). The total development time of
A. obliterata larvae depends on the temperature, but ranges
from 38 to 41 days (Wylie, 1958). If eggs are laid too late in
the development of an aphid colony, the larvae will not
mature before prey becomes scarce. The closing of the ‘egg
window’ (the relatively short period of time, in comparison
with aphid colony development, over which aphidophagous
ladybirds lay most of their eggs), is likely to be induced
by the presence of conspecific larval tracks. This form of
habitat assessment is probably a common feature of insects
that exploit resources that vary in abundance over time
(Hemptinne et al., 1992). Thus it appears that coccinellids
may not be required to judge the age of an aphid colony
through aphid associated cues, if they instead use oviposi-
tion cues from conspecific larvae. One drawback of this
mechanism is that previously unexploited aphid colonies at
any stage of development, if they had no resident predators,
would induce gravid females to lay eggs, even if these
colonies are past the optimum temporal window for egg-
laying. The relative importance of cannibalism, competition
and aphid colony transience has not been considered and
further work could proceed in this area.
The present study shows the searching behaviour of
A. obliterata is affected by conspecific larval tracks. Aphidecta
obliterata actively avoids areas contaminated with conspecific
larval tracks. This behaviour alone would result in
the reproductive response described above. Alternatively,
coccinellids may actively withhold oviposition in response
to the oviposition-deterring semiochemicals. The exact
mechanism of oviposition inhibition in response to these
semiochemicals has yet to be elucidated.
In regards to the persistence of A. obliterata oviposition-
deterring semiochemicals, larval tracks were found to
significantly deter oviposition by conspecific females for
up to three days. There was a strong linear relationship
between the age of tracks and the number of eggs laid, thus
implying a constant rate at which the oviposition-deterring
semiochemicals decay or evaporate (r
2
= 0.96). The strong
0
1
2
3
4
5
6
7
0 200 400 600
No. aphids present
Mean no. eggs
Fig. 7. Mean number of eggs laid by Aphidecta obliterata females
over 24 h, averaged over all four larval treatments, to show the
effect of increasing aphid density on oviposition rate. Bars
indicate standard errors of the means. Same letters above bars
indicate no significant difference between the treatments
(ANOVA, P < 0.05).
Table 1. Number of eggs laid by Aphidecta obliterata females on
filter papers contaminated by conspecific larval tracks of
different ages. Displayed are means, sample size (n) and
standard errors (S.E.).
Age of tracks
(days)
n Mean eggs
laid (and S.E.)
Fresh (1–3 days) 40 1.08+0.42
Old (5–11 days) 80 2.53+0.37
None (control) 20 3.60+0.91
30
T.H. Oliver et al.
persistence of these semiochemicals is likely to relate to their
chemical composition. Larval tracks of A. bipunctata consist
largely of alkanes, mostly methyl branched and straight
chain hydrocarbons, whose stability results from their
saturated nature preventing oxidation (Hemptinne et al.,
2001). The persistence time of larval oviposition-deterring
semiochemicals is an emergent property of the chemicals
that comprise them, but it is also likely to have fitness effects
on gravid females. It is therefore tempting to speculate
that persistence times will be shaped by evolution to the
benefit of the egg-laying female. This is however, invalid;
only fitness effects on the larvae emitting the tracks
present selection pressures on the persistence time
of oviposition-deterring semiochemicals. Low persistence
oviposition-deterring semiochemicals will be selected
against as larvae face increased competition from new
predators on their patch. High persistence oviposition-
deterring semiochemicals benefit the larvae, but only up to
a point as there is a limited time until larvae pupate, emerge
as adults and leave the patch. There may also simply be a
maximum threshold to the stability of the chemicals that
comprise oviposition-deterring semiochemicals. Previous
studies with larval tracks of other species report a range of
oviposition-deterring semiochemical persistence from only
one day (Ru
˚
z
ˇ
ic
ˇ
ka, 2002), to ten days or more (Dixon, 2000;
Hemptinne et al., 2001).
The present study confirms that, like other coccinellid
predators, the larvae of A. obliterata also produce oviposition-
deterring tracks. In concurrence with previous studies of
A. bipunctata by Doumbia et al. (1998) and Hemptinne et al.
(2001), and H. axyridis by Yasuda et al. (2000), the adults were
deterred from ovipositing by the presence of conspecific
tracks, but were generally unaffected by those of hetero-
specifics. In the present study, tracks of A. bipunctata and
C. carnea larvae induced no significant overall response by
A. obliterata females. There were, however, some marginally
significant effects of contrasts between treatments. This
offers some evidence for oviposition effects of heterospecific
tracks, although the marginal significance and small sample
size dictate the necessity for further empirical tests.
Although heterospecific tracks are usually found to be
ineffective deterrents, the finding is not unprecedented.
Ru
˚
z
ˇ
ic
ˇ
ka (2001) found that heterospecific tracks of
C. septempunctata and S. undecimnotata did deter oviposition
between these two coccinellids. These two species are
sympatric (Ru
˚
z
ˇ
ic
ˇ
ka, 2001). A later study also revealed that
coccinellids can be deterred from ovipositing by the presence
of chrysopid tracks (Ru
˚
z
ˇ
ic
ˇ
ka, 2003). It is possible that
coexisting species which share a common, limited resource
and/or engage in heterospecific predation of eggs and larvae
may impose adequate selection pressures for the evolution
of heterospecific semiochemical detection and response
mechanisms. Persistence of semiochemicals is, of course,
mediated by fitness effects on the emitter but in this case
deterring competing heterospecifics is of clear benefit to the
emitter. Thus, in effect, the semiochemical would be a
synomone facilitating interspecific communication between
individuals to their mutual benefit. Considering the present
study: A. obliterata and A. bipunctata are geographically
sympatric (both widespread throughout Britain) yet they
forage in different habitats. The habitat of A. obliterata
comprises needled conifers of all ages, including isolated
trees, natural and plantation woodlands. In contrast,
A. bipunctata tend to forage on a diverse range of herbaceous
plants, shrubs and trees (Majerus, 1994). In addition, they
also have different prey preferences: A. obliterata prefers to
feed on adelgids, e.g. Adelges picea , Adelges nu
¨
sslini (Bo
¨
rner),
although it will feed on some aphids, e.g. E. abietinum (Wylie,
1958). In contrast, A. bipunctata feeds on a diverse range
of aphids (Majerus & Kearns, 1989). With regards to further
study, Scymnus suturalis (Thunberg) and A. obliterata
have been found admixed to aggregations of Myrrha
octodecimguttata (Linnaeus) (all Coleoptera: Coccinellidae)
on pine trees (Pulliainen, 1966). Perhaps A. obliterata is more
likely to show heterospecific oviposition responses to
S. suturalis?
Aphid density
Increasing density of aphid prey leads to significant
increases in the oviposition rate of A. obliterata females. Thus
a trade-off occurs between the amount of prey present
(inducing oviposition) and the concentration of larval tracks
(inhibiting oviposition) (fig. 6). Ru
˚
z
ˇ
ic
ˇ
ka & Havelka (1998)
stated that tracks of larvae prevent egg-laying on plants in
spite of aphid prey. This study considered both larval track
density and prey density simultaneously and showed
that patch assessment is mediated through at least two cues
(prey density and oviposition-deterring semiochemical
concentration) that trade off, and the relative intensity of
these stimuli determines the readiness of A. obliterata to lay
eggs.
Dixon (1959) reports a lower critical density of aphids for
egg-laying and that this is determined by the minimum
density of aphids required for the survival of first instar
larvae. This study found no such lower limit. Even when no
aphids were present some eggs were still laid. At low to high
prey densities (0–400 aphids), the degree of oviposition-
stimulation was positively correlated with the density of
aphid prey present. At very high prey densities, there was
no further positive correlation between oviposition and prey
density, suggesting that there is some upper threshold of
prey density at which maximum oviposition occurs. It was
demonstrated that A. obliterata females show a maximum per
capita egg production in relation to prey density of
approximately 40 aphids per day. This supports findings
by Agarwala & Yasuda (2001) showing the numerical
response of the aphidophagous coccinellid Menochilus
sexmaculatus (Fabricius) to increasing aphid density to be
positive and sigmoidal in nature, similarly achieving a
plateau at approximately 40 aphids per day.
Agarwala & Yasuda (2001) noticed that the ratio of
eggs produced to dry mass of aphids consumed by
M. sexmaculatus (conversion ratio), is highest at lowest prey
densites (0–10 aphids per day). They take this finding to be
in agreement with the preference of ladybird predators for
laying eggs when aphid colonies are still small or growing as
suggested by Hemptinne et al. (1992). However, even if
prey:egg conversion rate is highest at low prey densities, the
numerical response is still clearly positive and larger aphid
colonies will receive more eggs, contradicting the above
view. It is more likely that conspecific larval pheromone cues
are the main mechanism by which ladybirds respond to
aphid colonies late in development (which will not support
new eggs), with an inverse numerical response, i.e. closing
the ‘egg window’. Larval tracks have been shown to have a
obvious inhibitory effect on oviposition, whereas Agarwala
Oviposition responses to patch quality in larch ladybird
31
& Yasuda’s (2001) numerical response is still clearly
positively correlated with prey density even if prey:egg
conversion rate does show some small tendency to decline at
higher prey densities.
Age structure of prey colony may also be an important
factor affecting coccinellid offspring success. The density of
smaller aphids must be high enough for neonates to obtain
their first meal. First instar coccinellids are inefficient at
capturing prey and their survival relies on the successful
obtainment of their first meal soon after they leave the egg
case (Dixon, 1959). Although co-existing with conspecifics
can pose dangers from cannibalism, there are also advan-
tages related to social feeding, where larvae share prey
captured by other individuals (Hemptinne et al., 2000b).
Whether gravid coccinellid females use aphid colony
age-structure in assessing patch quality is yet undetermined.
Satiation and prey-associated olfactory cues
Increasing the density of aphid prey present stimulates
oviposition in A. obliterata, as described above. It has not
been determined however, whether this increased oviposi-
tion is a behavioural response to externally detected aphid
allelochemicals, or simply an increased fecundity facilitated
by satiation, i.e. an internally mediated response. In this
experiment it was shown that previously satiated females lay
significantly more eggs than those starved for 12 h prior.
Thus satiation is an important contributing factor to the
increased oviposition response with increasing aphid prey
densities. In contrast, olfactory cues from aphids did not
significantly affect the ovipostion rate of A. obliterata. These
results are in accordance with the view that increased
oviposition near aphid colonies results simply from the
nutritional status of females, i.e. satiation facilitating
increased oviposition (Banks, 1954). The results contrast with
a study which claims that honeydew is an arrestant stimulus
for searching coccinellids (Carter & Dixon, 1984), and also a
study demonstrating that C. septempunctata withholds eggs in
the absence of aphids, yet when aphid odours and honeydew
are present (without aphids) oviposition occurs as normal
(Evans & Dixon, 1986). Resolution of these conflicting studies
may result from investigation into the effects of different
specific aphid-derived chemicals over a range of concentra-
tions. It is possible that pressed aphids do not accurately
represent the non-physical aspects of undisturbed aphid prey;
alarm pheromones may be present at elevated levels affecting
the oviposition response of females.
Egg-surface chemicals
Aphidecta obliterata females were not significantly deterred
from oviposition by non-tactile cues from conspecific eggs in
this experiment. The results, however, were on the margin of
significance. The means of the two treatments (control and
egg-surface chemicals) were very different (6.0+1.5 (S.E.,
n = 10) eggs per 10 females and 2.6+0.5 (S.E., n = 10) eggs per
10 females respectively) but because of the large difference in
variance a paired t-test was invalid. Further work with larger
sample sizes may reduce the variance and lead to significant
results. Avoiding sites with high concentrations of egg surface
chemicals could provide similar fitness benefits to females as
avoiding sites with conspecific larval tracks, namely increased
offspring survival probability due to reduced cannibalism
and competition, and increased food availability. Studies on
A. bipunctata, however, failed to produce such a response
to conspecific eggs or pupae (Hemptinne et al., 1992).
In contrast, the current study found results very close to
significance. If this non-significance is simply a result of
limited replication, then the discrepancy between this experi-
ment and that of Hemptinne et al. (1992) may arise from
the fact that the present study used egg surface chemical
extract at high concentrations (50 eggs), yet Hemptinne et al.
(1992) used only a single batch of whole A. bipunctata eggs.
Egg surface chemicals would be present at a much lower
concentrations and therefore fail to elicit a reproductive
response. Hemptinne et al.’s (1992) experimental set up is
much more typical of situations in the field, where a female
infrequently encounters batches of eggs together. Therefore
the observed (marked, but not significant) response in the
current study with A. obliterata may not be adaptive,
but simply artefactual. An explanation for the response
is that these chemicals found on egg surfaces have similar
structures to the oviposition-deterring semiochemicals
in larval tracks (as shown by the oviposition-deterring
Egg surface chemicals
SIGNALLING TOXICITY
Elytra compounds
MATE RECOGNITION
SEMIOCHEMICAL
PARSIMONY
STRUCTURAL FUNCTION
CHEMICAL COMMUNICATION
Ladybird tarsi
ADHESION
Larval tracks
OVIPOSITION
DETERRENCE
Fig. 8. Diagram of the semiochemical parsimony occurring in ladybirds. Similar alkanes are claimed to be used on egg surfaces, elytra
compounds and in larval tracks, as intra- and interspecific chemical messengers (Hemptinne et al., 1998, 2000c). The same compounds
have also been found to function in adhesion to smooth surfaces (Kosaki & Yamaoka, 1996).
32
T.H. Oliver et al.
response at high concentrations), but actually serve a different
function. Blum (1996) was the first to suggest that some
insects exploit their natural product with parsimonious
versatility. Egg surface alkanes are important in signalling
the toxicity of eggs to heterospecific predators (Hemptinne
et al., 2000c). Further work has shown these alkanes are
also present on the surface of adult elytra and function in
mate recognition (Hemptinne et al., 1998). In addition, a
similar mixture of alkanes is secreted from the under-
surface of ladybird tarsi aiding adhesion onto smooth
surfaces (Kosaki & Yamaoka, 1996). Thus it appears the
same alkanes, also functioning in adhesion, are used
to transmit several different context-dependent messages
(fig. 8).
Implications for biocontrol
The ideal result of introducing a natural enemy as a
biological control agent is to begin a persistent and
stable interaction which will maintain pest numbers at
equilibrium below an economic threshold. Aphidecta oblite-
rata has been used in attempted biological control
programmes in the past. Hodek (1973) reported that
A. obliterata was imported from Germany to North Carolina
to control Adelges piceae, the cause of considerable damage to
Abies spp. The coccinellid was released in 1960 and 1963.
Amman (1966) stated that after four years of survival it was
reported as a permanent addition to the predator complex.
There are, however, no quantitative reports of its efficiency
as a biocontrol agent. In some cases, A. obliterata has been
recommended as a potential biocontrol agent. Salom (1998),
after preliminary studies demonstrated encouraging vorac-
ity, recommended A. obliterata as a biocontrol agent for the
hemlock woolly aphid. Aphidecta obliterata may also be an
important natural enemy of the green spruce aphid,
E. abietinum, a pest of spruce (Picea) spp., including Sitka
spruce (Picea sitchenisis), Britain’s main commercially grown
tree (Carter & Halldorson, 1998).
There are a number or reasons why A. obliterata, and
aphidophagous coccinellids in general, may make for poor
biocontrol agents. Stabilizing the abundance of a pest well
below an economic threshold is often achieved by a strong
aggregative response (functional and numerical) to high
densities of prey. The present study shows that the positive
numerical response of A. obliterata to increasing prey density
is weakened by its tendency to avoid ovipositing in patches
already exploited by conspecific larvae. The numerical
response of A. obliterata is important in determining spatial
variation in predators (oviposition-deterring semiochemicals
tend to cause predators to distribute themselves more evenly
between patches). This spatial variation may have important
implications for the stability of predator–prey interactions.
Mathematical models often assume that predators choose
prey patches independently of the distribution of other
predators which leads to aggregation of risk of predation
(Jansen et al., 1997). With oviposition-deterring semio-
chemicals at play, however, this is clearly not the case.
Van Baalen & Sabelis (1993) relaxed this assumption and in a
combination of the classic Nicholson-Bailey model and a
game theoretical model they allow parasitiods and hosts to
distribute themselves in an evolutionary stable manner. This
resulted in a significant decrease in the parameter space in
which the model achieved a stable equilibrium. Beddington
et al. (1978) stated that differential exploitation of patches in
a spatially heterogeneous environment provides the most
likely mechanism to account for known biological control
successes. This contradicts Ru
˚
z
ˇ
ic
ˇ
ka’s (1998) statement
claiming that oviposition-deterring semiochemicals, causing
a more even distribution of predators between patches, may
allow them to achieve a higher efficiency of aphid control.
Ladybirds also tend to become satiated at a relatively low
prey density. Thus the maximum reproductive response
occurs at low prey densities thereby contributing to the
destabilization of the predator–prey interaction (Hemptinne
et al., 1992).
To summarize, the effects of ladybird oviposition-
deterring semiochemicals on their numerical response tends
to affect the spatial variation of these predators, causing
them to be distributed more evenly across prey patches.
This dampening of the aggregative response of predators
to heterogeneous prey patches leads to destabilization of
the predator–prey interaction. This instability is further
accentuated by the low satiation threshold of predators,
leading to a maximum reproductive response at low prey
densities thereby further counteracting any aggregation of
predation risk faced by patches of high prey density.
Acknowledgements
JELT was funded through a NERC/CASE studentship
held with the Forestry Commission. THO is in receipt of a
BBSRC studentship. We are grateful to Tilly Collins and
Denis Wright who provided useful comments on the
manuscript.
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34
T.H. Oliver et al.
... Ladybirds select oviposition sites based on factors, such as (1) patch quality in terms of prey quantity (Hemptinne et al. 2000a;Fréchette et al. 2006;Oliver et al. 2006;Omkar et al. 2010), (2) age of aphid colony (Hemptinne et al. 2000a), (3) age of host plant (Seagraves 2009), (4) presence of larval tracks (Ruzicka 2006;Mishra et al. 2012Mishra et al. , 2013, (5) physical presence of adults (Mishra and Omkar 2006), (6) cost of interpatch movement in terms of energy and time, and (7) mortality risks to the offspring (Seagraves 2009). A few studies suggest that egg presence also modulates oviposition (Hemptinne and Dixon 1991;Mishra et al. 2012Mishra et al. , 2013. ...
... A few studies suggest that egg presence also modulates oviposition (Hemptinne and Dixon 1991;Mishra et al. 2012Mishra et al. , 2013. In response to poor prey quantity and quality, ladybirds are known to either reduce oviposition (Oliver et al. 2006;Fréchette et al. 2006;Omkar et al. 2010; Barbosa et al. 2014;Santos et al. 2016;Singh et al. 2016), or completely avoid oviposition by resorbing their ovarioles (Osawa 2005;Kajita and Evans 2009;Ferrer et al. 2010) or search for further new patches for oviposition (Sloggett and Majerus 2000). In prey-scarce conditions, instead of avoiding such patches completely, ladybirds tend to lay extra non-viable eggs only for the purpose of nutrition, so as to provide for their viable eggs in the same egg batch (Perry and Roitberg 2005) and also for themselves (Santi and Maini 2007). ...
Article
Full-text available
Oviposition site selection in ladybirds is a dynamic process influenced by a number of abiotic and biotic factors. In this study we investigated whether prey quantity and egg presence (varying in relatedness and age) influence oviposition behavior in the zigzag ladybird, Menochilus sexmaculatus (Fabricius). Influence of these factors on cannibalism by females was also investigated and we tried to observe whether cannibalism was a modifying mechanism during oviposition site selection. Females were placed in prey abundant or scarce conditions in presence of related or unrelated eggs of varying ages, and their oviposition (for 24 h), egg viability and cannibalism were recorded. Prey-scarce conditions significantly decreased oviposition but had no influence on egg viability. Prey scarcity also increased the incidence of cannibalism by females. Females avoided laying eggs in the presence of related eggs regardless of their age. On the other hand, cannibalism was more in related eggs that were older in age. This increased cannibalism in presence of older related eggs, may be a comprehensive way of eliminating potential competition threats from a potential oviposition site already having eggs. All the independent factors (prey quantity, egg relatedness and egg age) did not affect egg viability, is the suggestive of male nutritional status rather than female.
... In P+ plants the perceived predation risk was achieved by attaching a filter paper (Fisherbrand QL100, 5 cm diameter) on which the tracks of harlequin larvae had been deposited (from two unfed larvae that had been allowed to walk on the filter paper in a dish for 12 h; Carter and Dixon, 1982;Doumbia et al., 1998;Magro et al., 2007). These "larval tracks" are low volatility contact cues and as such have high temporal persistence Ruzicka, 2002;Oliver et al., 2006. Papers with tracks and control papers (clean filter papers for use on P-plants), were each cut into four strips. ...
... The influence of the treatments and of female weight and age on the time of egg laying was assessed using a GLM with negative binomial errors and a log link function (error structure used to account for over-dispersion in each model). For those females that moved from the focal plant when aphids where absent and predator cues were present (A−/P+), this altered the laying environment of females in this treatment as "larval tracks" are low volatility contact cues (Ruzicka, 2002;Oliver et al., 2006). Analyses for reproductive investment [i.e., egg number and egg (-)-adaline level and concentration] were therefore carried out with predation risk level altered to P-if females in the A−/P+ treatment moved from and laid eggs away from the focal plant. ...
Article
Full-text available
Invasive species commonly predate the offspring of native species and eggs are the life stage most vulnerable to this predation. In many species with no maternal care, females can alter the phenotype of eggs to protect them, for instance through chemical defense. In ladybirds egg alkaloids deter predators, including invasive predatory species of ladybirds, but conversely may attract cannibals who benefit from the consumption of eggs with higher alkaloid levels. Invasive predators tend to be more abundant where resources are also abundant, but in high resource environments the maternal fitness benefits of sibling cannibalism are low. Consequently this presents a conflict for female ladybirds between the different factors that influence egg alkaloid level, as protecting her eggs from predators might come with the cost of inadvertently encouraging within-clutch cannibalism under circumstances where it is not beneficial. We investigated how the ladybird Adalia bipunctata addresses this trade-off experimentally, by measuring the quantity of alkaloids in eggs laid by ladybirds in environments that differed in levels of resource availability and perceived predation risk from an invasive predator Harmonia axyridis. Females did lay eggs with higher egg alkaloid levels under poor resource conditions, but only when predator cues were absent. The resulting negative correlation between egg number and egg alkaloid level under poor resource conditions indicates a trade-off between these two attributes of maternal investment, mediated by female response to offspring predation risk. This implies that selection pressures on mothers to adaptively adjust the risk of siblicide may outweigh the need to protect offspring from interspecific predation. Our results demonstrate that maternal effects are an important aspect of species' responses to invasive predators, and highlight the value of studying maternal effects in the context of the multifaceted environments in which they occur.
... pheromone (infochemical uses for intraspecific communication), kairomone (infochemical that benefits the receiver but not the emitter), allomone (infochemical that benefits the producer and harms the receiver), synomone (infochemical that benefits both the receiver and the emitter)], remains open for debate (Martini et al., 2009). However, these long-chain hydrocarbon molecules (Hemptinne et al., 2001;Magro et al., 2007) provide a long-lasting signal (Hemptinne et al., 2001) and females typically avoid laying eggs on substrates marked by conspecific and heterospecific competitors or predators (Doumbia et al., 1998;Oliver et al., 2006;Magro et al., 2007;Seagraves, 2009). Ladybeetles therefore provide an excellent model to study the effects of temperature on chemical communication. ...
... Our results also indicate that the effects of temperature on infochemical emission indirectly influence the behaviour of the receiver (Fig. 1a, indirect effects); ladybeetles refrained more to lay eggs and laid fewer eggs in the presence of larval infochemicals emitted at the highest temperature. Interestingly, the quantity of infochemicals emitted at different temperatures seems to correlate positively with the strength of oviposition inhibition (see Figs 3 and 4), which supports prior results showing that females rely on the amount of infochemicals to assess the risk of their eggs being eaten by conspecifics (Doumbia et al., 1998;Oliver et al., 2006). Given that enzymatic pathways for hydrocarbons production are similar for most arthropods (Blomquist & Bagn eres, 2010) and that most insects can detect small changes in the composition or concentration of chemical cues (Card e & Millar, 2004;Heil, 2008;Hansson, 2014), we expect the direct and indirect effects of temperature on chemical communication to significantly influence intra-and interspecific interactions in most ecosystems. ...
... pheromone (infochemical uses for intraspecific communication), kairomone (infochemical that benefits the receiver but not the emitter), allomone (infochemical that benefits the producer and harms the receiver), synomone (infochemical that benefits both the receiver and the emitter)], remains open for debate (Martini et al., 2009). However, these long-chain hydrocarbon molecules (Hemptinne et al., 2001;Magro et al., 2007) provide a long-lasting signal (Hemptinne et al., 2001) and females typically avoid laying eggs on substrates marked by conspecific and heterospecific competitors or predators (Doumbia et al., 1998;Oliver et al., 2006;Magro et al., 2007;Seagraves, 2009). Ladybeetles therefore provide an excellent model to study the effects of temperature on chemical communication. ...
... Our results also indicate that the effects of temperature on infochemical emission indirectly influence the behaviour of the receiver (Fig. 1a, indirect effects); ladybeetles refrained more to lay eggs and laid fewer eggs in the presence of larval infochemicals emitted at the highest temperature. Interestingly, the quantity of infochemicals emitted at different temperatures seems to correlate positively with the strength of oviposition inhibition (see Figs 3 and 4), which supports prior results showing that females rely on the amount of infochemicals to assess the risk of their eggs being eaten by conspecifics (Doumbia et al., 1998;Oliver et al., 2006). Given that enzymatic pathways for hydrocarbons production are similar for most arthropods (Blomquist & Bagn eres, 2010) and that most insects can detect small changes in the composition or concentration of chemical cues (Card e & Millar, 2004;Heil, 2008;Hansson, 2014), we expect the direct and indirect effects of temperature on chemical communication to significantly influence intra-and interspecific interactions in most ecosystems. ...
... undecimnotata and only 1 day in C. septempunctata (Ruzicka 2002). In the predator of adelgids and the green spruce aphid, Aphidecta obliter ata, the inhibition effect of larval track density was studied simultaneously with the stimulatory effect of prey density (Oliver et al. 2006;Fig. 5.42). ...
... 42 Mean number of eggs laid by Aphidecta obliterata females over 24 hours on filter paper substrates differentially contaminated with conspecific larval tracks made by different numbers of larvae across a range of prey densities (fromOliver et al. 2006). ...
Chapter
IntroductionFood SpecificityQuantitative Aspects of Food RelationsFood-Related BehaviourConclusions AcknowledgementsReferences
... A good oviposition site is particularly important for coccinellids since their larvae have limited dispersal capabilities and their survival thus depends on the mothers' choice of a high-quality oviposition site Seagraves 2009). Therefore, female ladybeetles need to find oviposition sites where their prey is both abundant and young (Dixon 1959(Dixon , 2000 and where mortality due to natural enemies is low (Mills 1982;Osawa 1989Osawa , 1992Burgio et al. 2002;Oliver et al 2006). Areas where their hemipteran prey are tended by ants represent potentially high-quality habitats since these frequently have all these qualities plus the additional advantage of sustaining relatively more persistent prey populations compared to those not tended by ants Mahdi and Whitaker 1993;Sloggett and Majerus 2000a). ...
... Azya orbigera larvae, however, were not completely restricted to ant-tended areas. Adult ladybeetles have a high predisposition to disperse even from high-quality habitats (Ives 1981;Frazer 1988), partly because they are known to be deterred from ovipositing in areas with abundant conspecific larvae to avoid intraspecific competition and cannibalism (Doumbia et al. 1998;Merlin et al. 1996;Hemptine et al. 2000;Oliver et al. 2006). Furthermore, given their inability to feed in ant-tended scale colonies, they are likely forced to move around the farm, probably looking for the sparsely distributed nontended scale colonies. ...
Article
As an implicit justification for the importance of conserving biological diversity it is postulated that biodiversity confers benefits to ecosystems. However, how does it promote ecosystem function and stability is not fully understood. Natural pest control is an example of an ecosystem service thought to be enhanced by the high biodiversity and embedded biocomplexity of diverse agroecosystems. My PhD. research addresses how the biocomplexity of an agroecosystem allows the population persistence of important natural enemies, which in turn, help to maintain the populations of potentially harmful pests below damaging levels. I focused on a subsystem of a complex ecological insect web in an organic coffee farm in Chiapas, Mexico, where I studied the interactions between a tree-nesting aggressive ant (Azteca instabilis), a potential coffee pest (the green coffee scale, Coccus viridis), and a predatory ladybeetle (Azya orbigera). This voracious predator of green scales is very abundant in the farm and, therefore, a potential natural controller of green scale populations. I used a combination of laboratory and field experiments to understand the local interactions between all the organisms involved; large scale field surveys to determine the spatial distribution and persistence of the organisms; and computer simulations to experiment with different hypothetical scenarios. I show that, contrary to previous reports, the mutualism between A. instabilis and green scales can be beneficial to the ladybeetle populations. I showed how the complex interactions associated with the this mutualism influence the persistence, spatial distribution, and dispersal of the voracious A. orbigera, which in turn, is imposing the control that is likely preventing green scale population outbreaks. The result is a healthy agroecosystem with little necessity for external inputs for green scale management. Since green scales are persistent pests in many coffee producing areas in the world, its maintenance below damaging levels in this particular farm may be an example of an important ecosystem service provided by complex local and spatial dynamics characteristic of diverse agroecosystems.
... Interspecific competition between ladybeetle species determines their foraging behavior, especially in patch selection for oviposition [53,[81][82][83]. In the present study, ladybeetle densities were significantly positively related toaphid densities at the local field and landscapescales, hinting at the absence of differential specialization to aphid densitiesby different ladybeetle species. ...
Article
Full-text available
In agroecosystems, predatory ladybeetles play an important role in restraining aphid population growth and suppressing aphid populations. They can adapt to various habitats and make use of various aphid species associated with multiple host plants during their life cycle. Agricultural landscapes in China are composed of a mosaic of small fields with a diverse range of crops, and how ladybeetles make use of host plant diversity in such landscapes has rarely been documented. In this study, we examined the relationship between aphid densities and ladybeetle densities in two different settings: (i) on the majority of plant species (including crops, trees, and weeds) at a local field scale in 2013 and 2014, and (ii) in paired cotton and maize crop fields at a regional landscape scale in 2013. Overall, we found that aphid abundance determined predatory ladybeetle abundance at both the local field and landscape scales, and there was a positive correlation between aphid densities and ladybeetle densities. However, plant taxa had no significant influence on the predatory ladybeetle abundance at the local field scale. In addition, the effect of aphids on ladybeetles abundance was influenced by the crop type and growing season at the regional landscape scale. There was a significant positive correlation between aphids and ladybeetles populations on cotton only in July and August, whereas the correlation was significant for maize throughout the whole growing season. We also conducted an analysis of the stable carbon isotope ratios of the adult ladybeetles caught in cotton and maize fields (C3 and C4 crops, respectively) in a regional landscape-scale survey in 2013. The δ13Cvalue indicated that most prey aphids for ladybeetles originated from crops where aphids are abundant (cotton in June and July; both maize and cotton in August).These findings improved our understanding of the migration and dispersal of ladybeetles among different habitats and plant species and provided insight into the promotion of the regional conservation and pest control of natural enemies in northern China.
... The oviposition activity of aphidophagous coccinellids is limited to a period (window) limited by two terms: It begins when the prey abundance reaches the level necessary for the females to start laying eggs and ends when the females are discouraged from further reproduction by an oviposition-deterring pheromone (Ruzicka 1997). Under laboratory conditions, the closing of the oviposition window has been studied in several coccinellid species (Oliver et al. 2006), including H. axyridis (Almohamad et al. 2010;Verheggen et al. 2017). Even in the wild oviposition likely terminates at the moment when the concentration of pheromone is high enough for the females to stop laying eggs. ...
Article
1. Understanding the conditions that allow for the occurrence of an additional generation in populations that are usually univoltine is important under the present climate warming. In temperate areas, a second generation is enabled through the emergence of a time window that opens when first‐generation individuals are ready to reproduce and closes when second‐generation individuals cannot complete development before the onset of winter. 2. The conditions that limit the width of this window were studied in Pyrrhocoris apterus (Heteroptera: Pyrrhocoridae), a ground‐inhabiting heteropteran overwintering in facultative adult diapause, whose populations in Central Europe have typically been univoltine until the 1980s. 3. The frequency of females of the first generation that started to lay eggs decreased from 70% in June to zero in early August, but oviposition of these females continued until the end of August. Using thermal constants for egg–adult development and temperature data, this study found that the development of most second‐generation individuals could only be completed before the start of winter if hastened through behavioural thermoregulation. 4. Consequences of temperature increase on the width of the thermal window were calculated. Increasing temperature causes the time window to open earlier and close later by accelerating maturation of first‐generation females and improving conditions for maturing of the second‐generation individuals in late summer and autumn. 5. Climate warming will create conditions that facilitate the occurrence of a second generation in a year in typically univoltine populations of this species.
... The oviposition activity of aphidophagous coccinellids is limited to a period (window) limited by two terms: It begins when the prey abundance reaches the level necessary for the females to start laying eggs and ends when the females are discouraged from further reproduction by an oviposition-deterring pheromone (Ruzicka 1997). Under laboratory conditions, the closing of the oviposition window has been studied in several coccinellid species (Oliver et al. 2006), including H. axyridis (Almohamad et al. 2010;Verheggen et al. 2017). Even in the wild oviposition likely terminates at the moment when the concentration of pheromone is high enough for the females to stop laying eggs. ...
Article
The population density of Eucallipterus tiliae (L.) (Hemiptera: Aphididae) required for initiating oviposition in Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae) was established in Tilia cordata Mill. (Dicotyledoneae: Tiliaceae) stands sampled weekly throughout the vegetative seasons of 2017–2019. The number of aphids per leaf area and oviposition in H. axyridis females were determined at each sampling session. Seasonal changes in aphid abundance and the presence of ovipositing females in natural populations varied across years but in all years H. axyridis started oviposition as soon as the aphid density increased above 10.2 aphids per ten sweeps, which equals 1.04 aphids per 100 cm2 leaf area. These values exceed the threshold aphid density for starting oviposition in Coccinella septempunctata L. (Coleoptera: Coccinellidae), which is 0.40 aphids per 100 cm2 leaf area. This difference is in line with H. axyridis preference for trees, host plants with complex architecture and hard to search, and preference of C. septempunctata for spatially simple herbs.
... Oftentimes, oviposition is stimulated by the availability of natural (essential) prey, in abundance and of high quality. [15][16][17][18] Thus, a major challenge is stimulating C. maculata and other ladybirds to oviposit their full potential of eggs when restricted to feeding on alternative foods rather than natural prey (eg, aphids). In addition, cues that guide ovipositing females to suitable sites for egg laying are often connected to natural prey. ...
Article
Full-text available
Maximizing the reproductive potential of ladybird beetles fed factitious foods or artificial diets, in lieu of natural prey, is a major challenge to cost-effective mass rearing for augmentative biological control. In this study, we tested the hypothesis that compounds in redcedar, Juniperus virginiana, stimulate oviposition in the ladybird Coleomegilla maculata. We also tested the prediction that several bioflavonoids, identified in heartwood fractions, elicited this behavioral response. Phenolic compounds were extracted from J. virginiana heartwood sawdust, separated into several fractions, then presented to adult beetles, in a powdered, pure form, in the laboratory. Females preferentially oviposited within 1 to 2 cm of fractions B, C, D, and E, but not A or the unfractionated extract, at the base of test cages. Chemical analysis identified bioflavonoids in heartwood fractions and subsequent bioassays using several identified in fractions C, D, and E confirmed that quercetin, taxifolin, and naringenin (to a lesser extent) stimulated oviposition. All tested fractions and bioflavonoids readily adhered to the chorion of freshly laid eggs but did not reduce egg hatch. This study demonstrates that several bioflavonoids stimulate oviposition by C. maculata and could be useful for mass rearing programs.
Article
This book provides the first monograph of Coccinellidae. Although the group finds inclusion both in Clausen's (1940) "Entomophagous Insects" and in Balduf's (1935) "Entomophagous Coleoptera", reference in these works is limited to three and twenty pages respectively. Moreover, the last thirty years since these books appeared have ~een a great deal of work on the group. The use of insecticides largely destroyed the early attempts at biological control and interest remained low for as long as insecticides appeared quite successfuL However, the problems of insecticides soon became apparent, and in the last decade there have been tremendous developments in biological control, particularly in eombin
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Females of species predatory as adults, Chrysopa commata Kis & Ujhelyi, C. oculata Say and C. perla (L.), and also species not predatory as adults, Chrysoperla carnea (Stephens), laid more eggs on clean substrates, than on those exposed previously to conspecific or heterospecific first-instar larvae. Substrates contaminated with oviposition-deterring allomones (ODAs) deterred females of C. oculata most. On the average the deterrent effects of substrates contaminated by larvae of C. oculata or C. perla were greater than those contaminated by C. carnea or C. commata. Results indicate that both intra-and interspecific responses to ODA occur in chrysopids and may enable them to distribute their larvae more uniformly between prey patches.
Article
Preface Part A. The Head, Ingestion, Utilization and Distribuiton of Food: 1. Head 2. Mouthparts and feeding 3. Alimentary canal, digestion and absorption 4. Nutrition 5. Circulatory system, blood and immune system 6. Fat body Part B. The Thorax, Muscles and Locomotion: 7. Thorax 8. Legs and locomotion 9. Wings and flight 10. Muscles Part C. The Abdomen, Reproductive System and Development: 11. Abdomen 12. Reproductive system: male 13. Reproductive system: female 14. The egg and embryology 15. Postembryonic development Part D. The Integument, Gas Exchange and Homeostasis: 16. Integument 17. Gaseous exchange 18. Excretion and salt and water regulation 19. Thermal relations Part E. Communication: I. Physiological Co-ordination within the Insects: 20. Nervous system 21. Endocrine System II. Perception of the Environment: 22. Visual system 23. Mechanoreception 24. Chemoreception III. Communication with other Organisms: 25. Color and light production 26. Mechanical communication: sound production 27. Chemical communication: pheromones and chemicals with interspecific significance Species index Subject index.
Article
Semiochemicals, the pheromones and allomones, have been detected in arthropod species in six orders. Multifunctional pheromones have been especially characteristic of the queens of eusocial species. Compounds such as the queen substance of the honey bee Apis mellifera possess unrelated primer and releaser functions for the workers and act as a sex attractant for drones. Females of other hymenopterous species exploit the secretions of sting-associated glands as sex pheromones. A variety of nonhymenopterous species have adapted components in diverse defensive secretions to function as sex pheromones. The alarm pheromones of many arthropods are also used as defensive allomones, activity inhibitors, cryptic alarm pheromones, aggregative attractants, robbing agents, digging agents, trail pheromones, and antimicrobial agents. Some of these compounds also possess highly distinctive roles, eg functioning as lethal attractants for prey or, in the aquatic milieu, cuticular wetting agents. -from Author
Article
Larvae of Aphidoletes aphidimyza (Rondani) (Diptera: Cecidomyiidae) secrete an oviposition-deterring pheromone (ODP). In choice tests, females of A. aphidimyza laid significantly fewer eggs on Vicia faba L. plants infested with Aphis fabae Scopoli (Homoptera: Aphidoidea) that were previously exposed to conspecific third-instar larvae or a water extract of their ODP. A. aphidimyza females also laid fewer eggs on aphid-infested plants that were previously exposed to unfed first-instar larvae of Chrvsopa oculata Say, Chrysopa perla (L.) or Chrysoperla camea (Stephens) (Neuroptera: Chrysopidae), or second-instar larvae of Coccinella septempunctata L. (Coleoptera: Coccinellidae). However, the response to traces of C. cornea larvae was very weak.
Article
Females of Coccinella septempunctata L. were deterred from ovipositing at sites previously exposed to larvae of C. septempunctata or Chrysopa oculata Say. If aphidophagous predators can respond to one another's deterring allomone then they may avoid competing for prey. The deterrent effect from exposure to C. septempunctata or C. oculata larvae considerably decreased when contaminated sites were kept in open air for 24 h. Females of C. oculata avoided ovipositing at sites exposed to larvae of C. oculata, but the deterrent effect of sites exposed to larvae of C. septempunctata was negligible.
Chapter
Ladybirds are regarded with affection by people who have no interest in, or even an aversion to insects in general. This is reflected in the prevalence of holy attributives in the colloquial names, in many languages, of these much-befriended insects. That the first great success in biological control came in 1889 with the introduction of the Australian ladybird (Rodolia cardinalis) into California to combat a coccid scale insect that was threatening the existence of the Californian citrus industry further popularised ladybirds.