Abundance and natural control of the woolly aphid
Eriosoma lanigerum in an Australian apple orchard
Adrian H. NICHOLAS
*, Robert N. SPOONER-HART
NSW Agriculture, Tamworth Agricultural Institute, RMB 944 Calala Lane,
Tamworth, NSW 2340, Australia;
University of Western Sydney, Bourke Street,
Richmond, NSW 2753, Australia;
CSIRO Long Pocket Laboratories, 120 Meiers
Rd, Indooroopilly, Qld 4068, Australia
*Author for correspondence; e-mail: email@example.com
Received 26 April 2004; accepted in revised form 17 May 2004
Abstract. Woolly aphid (Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae), was
monitored over three growing seasons (1995–1998) to assess its abundance and man-
agement under apple IPM programs at Bathurst on the Central Tablelands of NSW,
Australia. Woolly aphid infestations were found to be extremely low in IPM programs
utilising mating disruption and fenoxycarb for codling moth Cydia pomonella L.
(Lepidoptera: Tortricidae) control. This was the direct result of increased numbers of
natural enemies. No insecticides were applied for woolly aphid control. Under the IPM
strategies tested the principal control agent was identiﬁed as European earwig (Forﬁcula
auricularia L.) (Dermaptera: Forﬁculidae). Earwigs in combination with Aphelinus mali
(Haldeman) (Hymenoptera: Aphelinidae) reduced woolly aphid infestations below the
action threshold set by commercial growers. However, A. mali together with other ﬂying
natural enemies, e.g., ladybirds, lacewings and hoverﬂies, did not provide commercially
acceptable control of woolly aphid in the absence of earwigs. Under the conventional
spray program, using the broad-spectrum insecticide azinphos-methyl for codling moth
control, the level of woolly aphid infestation increased with each successive season and
biological control was not established. When azinphos-methyl was withdrawn, natural
enemies migrated in and provided control of woolly aphid within one season. This is the
ﬁrst study to show that the biological control of woolly aphid can be achieved in a
commercially viable IPM program.
Key words: Aphelinus mali, biological control, Eriosoma lanigerum,Forﬁcula auricularia
Woolly aphid (Eriosoma lanigerum Hausmann) (Hemiptera: Aphididae) is an
important pest of apples causing hypertrophic gall formation on the roots and
limbs of the tree (Brown et al., 1991). The galls restrict sap ﬂow and frequently
BioControl (2005) 50: 271–291 Springer 2005
rupture providing further feeding sites for woolly aphid and allow the invasion
of fungal diseases (Childs, 1929; Weber and Brown, 1988). Heavy infestations
can reduce tree growth and vitality, destroy buds, reduce cropping, and lower
fruit quality (Childs, 1929; Essig, 1942; Bertus, 1986; Brown and Schmitt, 1990;
Brown et al., 1995).
Under Australian conditions, woolly aphid over-winter as adult females on
both the aerial and edaphic parts of the tree. Those over-wintering below
ground continue developing and reproducing at a slow rate, while those over-
wintering aerially are for the most part dormant, especially in the cooler regions
(Thwaite and Bower, 1983). In late spring–early summer, when the soil tem-
perature is approximately 10 C, young nymphs produced by over-wintering
females move up from below ground to the aerial parts of the tree (Nicholas
et al., 2003). Early colonies develop on vulnerable, thinly barked areas, such as
around pruning cuts, or splits caused by past heavy cropping. As the season
progresses colonies develop on the new season’s growth. Once feeding has
commenced woolly aphid remains sessile unless disturbed (Asante, 1994). In
autumn nymphs migrate to the roots (Lloyd, 1961). In Australia, where there
are few alternative winter hosts, e.g., American elms (Ulmus americana L.),
woolly aphid is for all practical purposes anholocyclic, living on apple as an
asexual viviparae (Nicholls, 1919). Commercial control of woolly aphid has
relied on resistant rootstocks and chemicals since the early 1900s (Froggatt,
1903; Nicholls, 1919; Thwaite, 1997). Woolly aphid has several natural enemies
in Australia, including lacewings, ladybirds, hoverﬂies and earwigs, all of which
are suppressed by azinphos-methyl (Asante, 1997; Nicholas et al., 1999).
Introduced in 1923 the parasitoid Aphelinus mali (Haldeman) (Hymenoptera:
Aphelinidae) is reported to have provided a signiﬁcant level of control (Wilson,
1960). The European earwig Forﬁcula auricularia L. (Dermaptera: Forﬁculi-
dae), which is wide spread in Australia, is capable of consuming up to 106
aphids per day (McLeod and Chant, 1952; Asante, 1995).
Earwigs have, by association, been shown to play an important part in
controlling woolly aphid in the absence of broad-spectrum insecticides (Anon,
1969; Ravenberg, 1981; Stap et al., 1987; Mueller et al., 1988). However none
of these trials showed that natural enemies could control woolly aphid under
commercial conditions, i.e., while controlling other key pests.
Two techniques, namely mating disruption and the insect growth regulator
fenoxycarb, are now ﬁrmly established in Australian apple orchards as viable
methods of controlling codling moth (Cydia pomonella L.), which is the key
pest of apples in mainland Eastern Australia (Thwaite, 1997). These techniques
are the basis of current commercial IPM programs in Australia (Thwaite,
1997). Codling moth mating disruption is highly species speciﬁc (Rumbo et al.,
1993) with no direct eﬀect on woolly aphid or its natural enemies. In con-
ventional pesticide programs, controlling codling moth with azinphos-methyl
ADRIAN H. NICHOLAS ET AL.272
requires 6–8 applications during the season (Thwaite et al., 1995) and these
sprays aﬀect many secondary pests and their natural enemies. Adopting an
IPM strategy, thereby reducing the use of broad-spectrum insecticides, is likely
to have indirect eﬀects the orchard’s other inhabitants, including the woolly
aphid and its natural enemies (Nicholas et al., 1999).
Woolly aphid has been studied extensively under conventional pesticide
programs, but its abundance in IPM programs was previously unknown. The
aim of this study was to assess the abundance of woolly aphid in IPM pro-
grams (i.e., in the absence of broad-spectrum insecticides) and investigate the
potential of natural enemies to suppress the pest population.
Materials and methods
The trial site
This study was conducted at Bathurst Agricultural Research Station located on
the Central Tablelands of New South Wales, Australia (Lat. 3326¢S. Long.
14934¢E). The orchard, planted in 1977, was a 1.7 ha block of apple trees
divided into six (3·2) discrete 0.3 ha blocks of 189 trees each. Each block had
nine rows of 21 trees, made up of three rows each of the cultivars Red Deli-
cious, Granny Smith and Jonathan. All trees were grafted on to Merton
Malling Series (MM) 106 (woolly aphid resistant) rootstock. Planting distances
were 5 m between rows and 3 m between trees. Blocks were 10 m and 12.5 m
apart on their long and short boundaries respectively. The trees were pruned to
the central leader system and an average height of 3 m. Groundcover was
controlled with herbicides within tree rows and mown between rows, as per
commercial practice. The trees were irrigated at the rate of 8 l/h for 4 h on
3 days/week, as required during dry periods.
Treatments 1995/1996 and 1996/1997 seasons
Two of the six blocks were treated with codling moth sex pheromone dis-
pensers (mating disruption technique (MD)), (Isomate
C, Biocontrol Ltd,
Brisbane, Qld, Australia), two with azinphos-methyl plus pheromone (AMD)
and two with fenoxycarb plus pheromone (FMD). The three treatments were
arranged so that all adjacent blocks received diﬀerent treatments. Pheromone
dispensers were applied each September at the rate of 1000 ha
. The azinphos-
methyl and fenoxycarb sprays were applied at the recommended label rates for
codling moth control, i.e., azinphos-methyl (Benthion
500 g/kg) 100 g/100 l
and fenoxycarb (Insegar
250 g/kg) 20 g/100 l early season and 40 g/100 l late
season (Thwaite et al., 1995). The azinphos-methyl program commenced the
ABUNDANCE AND NATURAL CONTROL 273
ﬁrst week of November each year. In 1995/1996 this program comprised six
sprays with the last applied on February 22 1996. The 1996/1997 program
comprised seven sprays with the last applied on February 24 1997. The 1995/
1996 and 1996/1997 fenoxycarb programs each comprised seven sprays applied
between October 20 and January 31 and October 21 and February 5 respec-
Treatment 1997/1998 season
The MD and AMD treatments were discontinued and all blocks were put
under a fenoxycarb only program. This consisted of nine applications of fen-
oxycarb commencing on October 13 1997. Thus, there were four blocks under
a fenoxycarb program for the ﬁrst time and two that were in their third season.
The ex-AMD blocks were used to monitor the migration and eﬃcacy of any
natural enemies of woolly aphid in the ﬁrst season of an IPM program.
Other pesticide applications
A minimal fungicide program using bupirimate, dithianon, dodine, fenarimol
and penconazole, as appropriate, to control apple scab (Venturia inequalis
(Cke.) Wint.) and powdery mildew (Podosphaera leucotricha ((Ell. & Ev.) E. S.
Salmon) was applied each season. Winter oil (Vicol
Victorian Chemical Co.)
was applied at the rate of 3%in September each year to control European red
mite (Panonychus ulmi (Koch)) and San Jose
´scale (Quadraspidiotus perniciosus
(Comstock)). All sprays were applied using a Hardi TS2082 air blast sprayer at
2300 l/ha (3.5 l/tree).
In the 1996/1997 season early colonies were observed to disappear quickly, and
prompted several colonies in each treatment to be tagged to aid further
observations. Colonies were tagged by tying a small length of ﬂuoro-pink wool
to the colonised limb approximately 75 mm above the colony.
Woolly aphid was monitored visually. Each tree was rated on a scale where:
0¼no infestation; 1 ¼trace infestation, 2 ¼up to 10%of the tree with severe
infestation; 3 ¼11–25%of the tree with severe infestation; 4 ¼more than 25%
of the tree with severe infestation (modiﬁed from Bower, 1987). Trace infes-
tation was deﬁned as £20 small colonies per tree and severe infestation as
laterals extensively covered with large colonies. One row of trees/cultivar/block
were assessed (21 trees ·3 treatment ·3 cultivars ·2 blocks). Assessment was
carried out every 2 weeks from the beginning of September to the end of May
ADRIAN H. NICHOLAS ET AL.274
Woolly aphid colonies were checked monthly throughout the 1996/1997 season
for parasitism by A. mali. Small colonies or short sections (22 mm) of woolly
aphid infested laterals were taken from each cultivar not monitored for other
purposes. The aphids were dip-washed in methylated spirit (70%ethyl alcohol,
30%methanol) to remove the wool, removed from the lateral and dried on
tissue paper. The proportion of black, mummiﬁed aphids was used as a relative
measure of parasitism.
Predators were monitored using rolled strips of corrugated cardboard
(100 mm ·400 mm) as artiﬁcial refuges (shelters). One shelter was pinned to
the trunk of each tree in a shady position. Predators occupying shelters were
counted every 2 weeks and released at the base of the tree. This method took
advantage of nocturnal species taking refuge during the day.
Non-ﬂying predators were prevented from entering the canopy of eight trees in
each cultivar in the MD and FMD treatments (four per replicate). The trunks
were banded with a 150 mm wide strip of green plastic sheet coated on both
sides with the sticky chemical polybutene (Tree Tanglefoot Pest Barrier,
Tanglefoot Co., USA). The polybutene was cleaned and replenished as re-
quired. A minimum air gap of 150 mm was maintained to reduce the move-
ment of non-ﬂying predators between adjacent trees.
Sticky bands have the potential to reduce the upward migration of woolly
aphid crawlers from the roots early in the season (Barnes et al., 1994). To
overcome this, an apple seedling, heavily infested with woolly aphid, was at-
tached in the canopy of each banded tree, and an adjacent unbanded tree.
Sticky bands and woolly aphid infested seedlings were applied on December 12
1996 (1996/1997 season) and October 27 1997 (1997/1998 season). Woolly
aphid infestation, excluding those on the infested seedlings, was monitored
every 2 weeks. The artiﬁcial shelters for predators were positioned above the
Analysis of variance (ANOVA) was used to determine signiﬁcant diﬀerences
between treatments and cultivars for levels of woolly aphid infestation, and the
number of predators in artiﬁcial shelters. All diﬀerences were compared at the
ABUNDANCE AND NATURAL CONTROL 275
5%level (p£0.05) of signiﬁcance and Tukey’s multiple comparison test was
used to separate means if signiﬁcant diﬀerences were found. Pearson’s prod-
uct–moment correlation coeﬃcients were calculated to test the relationship
between the number of earwigs occupying artiﬁcial shelters and the level of
woolly aphid infestation. Non-linear regression analysis of the combined data
from trees ﬁtted with predator exclusion bands and unbanded trees was used to
estimate the number of earwigs, as recorded in artiﬁcial shelters, required to
eliminate woolly aphid from each apple cultivar.
Woolly aphid infestation
In the 1995/1996 and 1996/1997 seasons, small isolated colonies of woolly
aphid were ﬁrst observed in early October in all treatments and in all cultivars
(Figures 1 and 4). These colonies (tagged with ﬂuoro-pink wool) were often not
present on subsequent monitoring dates. Under the AMD treatment there was
no signiﬁcant diﬀerence in the level of woolly aphid infestation between the
1995/1996 and 1996/1997 seasons, however it was signiﬁcantly lower during the
1997/1998 season when the AMD plots were put under a fenoxycarb only
program (Figure 2).
There was no signiﬁcant diﬀerence in the level of woolly aphid infestation
when comparing blocks in their ﬁrst season under a fenoxycarb only (IPM)
program with those in their third season (Figure 3).
There was no signiﬁcant diﬀerence between the cultivars in the level of woolly
aphid infestation within individual treatments, although in all treatments the
trend was for Red Delicious to have slightly higher infestation than Granny
Smith and Jonathon. However, pooling the treatment data showed that Red
Delicious had signiﬁcantly higher levels of infestation than in either Granny
Smith or Jonathan in both the 1995/1996 and 1996/1997 seasons (Figure 4a
After pooling the cultivar data, woolly aphid infestations in the AMD blocks
were shown to increase markedly from late November in 1995 and early
December in 1996. Infestation then remained signiﬁcantly higher than in the
MD and FMD treatments (Figure 1a and b). Infestation remained low in the
ADRIAN H. NICHOLAS ET AL.276
MD and FMD treatments throughout the season. There was no signiﬁcant
diﬀerence in infestation between the MD and FMD treatments in either season
(Figure 1a and b).
Due to the low levels of woolly aphid infestation in the MD and FMD
treatments, the samples collected were small (350–2,500 aphids) compared with
those from the AMD treatment (up to 8,000 aphids). On February 23 1997 the
level of parasitism by A. mali had reached 60, 55 and <1%in the MD, FMD
and AMD treatments respectively. The last application of azinphos-methyl was
made on February 24 1997 and by May 12 1997, the last sampling date, the
Figure 1. Woolly aphid infestation under three treatments for codling moth control,
mating disruption (MD, fenoxycarb plus MD (FMD), and azinphos-methyl plus MD
(AMD). Error bars ¼LSD (p£5%).
ABUNDANCE AND NATURAL CONTROL 277
level of parasitism had risen to 66, 78 and 24%in the MD, FMD and AMD
Ladybird, Harmonia conformis Boisduval, and hoverﬂy, Macrosyrphus conf-
rator (Weid.), larvae were occasionally observed feeding on woolly aphid
during the monitoring program. The only predators of woolly aphid found
occupying the artiﬁcial shelters were European earwig Forﬁcula auricularia L
(hereafter referred to as earwigs).
Figure 2. Seasonal comparison of woolly aphid infestation in AMD blocks over three
Figure 3. Comparison of woolly aphid infestation in the ﬁrst and third seasons of an
IPM program during the 1997/1998 season.
ADRIAN H. NICHOLAS ET AL.278
Eﬀect of predator exclusion bands
The predator exclusion bands signiﬁcantly reduced the number of earwigs
entering the tree canopy during the 1996/1997 season (p£0.001, assessed every
2 weeks). Banded trees had <1 tree
on each sampling date compared with
(range 3–14 decreasing towards the end of the season) in the un-
banded trees. There was no signiﬁcant diﬀerence between the MD and FMD
treatments in the number of earwigs in artiﬁcial shelters in trees ﬁtted with
exclusion bands, or between these treatments in unbanded trees. Trees ﬁtted
Figure 4. Woolly aphid infestation rating in three apple cultivars Red Delicious,
Granny Smith and Jonathan, as the mean of three treatments, MD, FMD and AMD.
Error bars ¼LSD (p£5%).
ABUNDANCE AND NATURAL CONTROL 279
with exclusion bands were found to have signiﬁcantly greater infestations of
woolly aphid than unbanded trees from December 24 1996 through until May
27 1997 when monitoring ceased. In the MD and FMD treatments there was a
high negative correlation between the mean number of earwigs/tree in the
artiﬁcial shelters and the mean woolly aphid seasonal infestation rating in all
cultivars (Delicious MD r¼)0.86 p¼0.01, FMD r¼)0.67 p¼0.02, Granny
Smith MD r¼)0.86 p¼0.005, FMD r¼)0.78 p¼0.005, Jonathan MD
r¼)0.78 p¼0.008, FMD r¼)0.82 p¼0.017). The 1996/1997 data, for each
cultivar in each treatment, was clustered into two groups, exclusion-banded
and unbanded trees (Figures 5 and 6). Data points from the exclusion-banded
trees were clustered close to the y-axis, showing high levels of woolly aphid
infestation with low numbers of earwigs in artiﬁcial shelters. Conversely, the
data points from unbanded trees were clustered close to the x-axis, showing
high numbers of earwigs in artiﬁcial shelters and low levels of woolly aphid
infestation. The exponential regression model y¼a+brx
a¼minimum number of earwigs counted, b¼estimated point of zero woolly
aphid infestation, and r¼0.1 (slope), was used to ﬁt a curve to the pooled
data, i.e., exclusion-banded and unbanded seasonal means of earwigs counted
in artiﬁcial shelters and woolly aphid infestation. This estimated the number of
earwigs required to occupy artiﬁcial shelters to prevent or eliminate woolly
aphid infestation, and was represented by the point at which the ﬁtted curve
crossed zero. The ﬁtted curve’s accuracy is given as the percentage of variance
accounted for by the curve and shown on each graph. For the 1996/1997
season the model estimated a required seasonal mean of 7.98 and 8.30 (Granny
Smith), and 4.98 and 5.02 (Jonathan) earwigs in the MD and FMD treatments
respectively to eliminate aerial colonies of woolly aphid. When applied to the
data from the cultivar Red Delicious the slope of the ﬁtted curve did not pass
through zero in either treatment (Figures 5a and 6a). The same analysis was
carried out on the 1997/1998 season data, when all plots were treated with
fenoxycarb. The results showed the data to be clustered as in the 1996/1997
season, but more varied in woolly aphid infestation between trees in all culti-
vars. The ﬁtted curve did not pass through zero for any cultivar and the
number of earwigs required to eliminate woolly aphid could not be predicted.
Predictions of woolly aphid infestation
Early season monitoring of earwigs would be a valuable tool if it could predict
the level of woolly aphid infestation later in the season, thus indicating whether
continued monitoring and control measures would become necessary. To
determine this the exponential regression model was used to ﬁt a curve to the
number of earwigs counted in artiﬁcial shelters in both exclusion-banded and
unbanded trees in the ﬁrst four sampling dates of the season (December 24,
ADRIAN H. NICHOLAS ET AL.280
January 8 and 22 and February 5) and the seasonal mean woolly aphid
infestation. The results showed that in the 1996/1997 season the prediction
model based on early season data supported the full season model. This
indicated that earwigs would eliminate, or reduce to extremely low levels, the
aerial colonies of woolly aphid in the cultivars Granny Smith and Jonathan
Figure 5. Relationship between European earwigs (seasonal mean) and woolly aphid
(seasonal mean) in trees ﬁtted with predator exclusion bands and unbanded trees under
a MD treatment for codling moth control during the 1996/1997 season.
ABUNDANCE AND NATURAL CONTROL 281
under MD and FMD treatments (Figures 7b, c, 8b and c). A higher level of
variation between trees was evident in data collected from the cultivar Red
Delicious early in the season and the model predicted that woolly aphid
Figure 6. Relationship between European earwigs (seasonal mean) and woolly aphid
(seasonal mean) in trees ﬁtted with predator exclusion bands and unbanded trees under
a FMD treatment for codling moth control during the 1996/1997 season.
ADRIAN H. NICHOLAS ET AL.282
infestation in this cultivar was going to be higher than in the other two cultivars
and supported the full season prediction model (Figures 7a and 8a). Early
season predictions could not be determined for the 1997/1998 season because
the full season data was too variable.
Figure 7. Relationship between European earwigs (mean of sampling dates, 24
December, 8, 22 January and 5 February) and woolly aphid (seasonal mean) in trees
ﬁtted with predator exclusion bands and unbanded trees under a MD treatment for
codling moth control during the 1996/1997 season.
ABUNDANCE AND NATURAL CONTROL 283
The signiﬁcantly lower levels of infestation in the MD and FMD treatments in
the 1995/1996 and 1996/1997 seasons, compared with that in the AMD treat-
Figure 8. Relationship between European earwigs (mean of sampling dates, December
24, January 8, 22 and February 5) and woolly aphid (seasonal mean) in trees ﬁtted with
predator exclusion bands and unbanded trees under a FMD treatment for codling moth
control during the 1996/1997 season.
ADRIAN H. NICHOLAS ET AL.284
ment, shows that under the conditions of this trial, the abundance of woolly
aphid in IPM programs was very low. The fungicide program was applied to all
treatments and, although it is unclear whether it adversely aﬀected beneﬁcial
species (or woolly aphid), it did not prevent biological control of woolly aphid.
The action threshold employed by Australian apple growers to woolly
aphid is very low. They usually apply an aphicide at the ﬁrst sight of infestation
or early in the season before the colonies become established, often purely as a
preventative measure. This is not because woolly aphid infestation causes
heavy crop loss but because severe infestation makes the task of picking fruit
messy and unpleasant. Contract pickers are reluctant to work in heavily in-
fested areas. Any infestation rated >1 would not be acceptable to Australian
growers. The level of infestation that occurred in the IPM treatments reported
here (where no trees were rated 2), would probably not have been detected by
most commercial growers, and therefore additional control measures would
not have been considered necessary. The woolly aphid infestation recorded in
trees treated with azinphos-methyl (many of which were rated 4), and those
ﬁtted with predator exclusion bands (i.e., those with fewer natural enemies),
would therefore not be tolerated by commercial growers. The higher levels of
infestation in Red Delicious occurred late in the season and were present well
past the harvest period of late February to mid-March, suggesting that natural
enemies may not provide adequate control in more susceptible cultivars.
Similarly, adequate control may not be possible in growing districts where
climatic conditions are more favourable to woolly aphid development or less
favourable to natural enemies.
The signiﬁcantly higher level of woolly aphid infestation in blocks treated
with azinphos-methyl, together with higher A. mali and earwig populations in
the MD and FMD treatments, supports the ﬁndings of Moreton (1969) and
Nicholas et al. (1999) that azinphos-methyl suppresses the woolly aphid’s
natural enemies and prevents eﬀective biological control. There was no evi-
dence in this trial, nor in the reviewed literature, that azinphos-methyl stimu-
lated development or fecundity in woolly aphid.
The lack of signiﬁcant diﬀerences in woolly aphid infestation between the
MD and FMD treated blocks indicate that either the full season program of
fenoxycarb did not negatively impact on the biological control of woolly aphid,
or its eﬀects were only short lived and natural enemies moved in from adjacent
blocks. It also shows that the use of MD allows for the establishment of
biological control agents. The levels of parasitism in the MD and FMD
treatments suggest that A. mali played an important role in suppressing the
woolly aphid population, although the data should be interpreted carefully
because of the small sample size. There was no signiﬁcant diﬀerence in the
percentage of parasitism per tree between these two treatments, indicating that
fenoxycarb did not suppress the A. mali population. This suggests that when
ABUNDANCE AND NATURAL CONTROL 285
applied as a spray to the aerial parts of the tree fenoxycarb did not adversely
aﬀect larvae developing in the mummiﬁed woolly aphid or the emerged adults.
In the AMD treatment however, parasitism remained below 1%until after the
spray program was completed, conﬁrming that azinphos-methyl was toxic to
A. mali. The results suggest that this toxic eﬀect lasts for up to 6 weeks fol-
lowing application. The level of parasitism in the MD and FMD treatments
had reached 60 and 55%respectively by February 1997, indicating A. mali was
playing a major role in reducing the level of woolly aphid infestation
throughout the 1996/1997 season. However, as A. mali is an alate and highly
mobile insect which would have been unaﬀected by the exclusion bands, it
could not have been responsible for the signiﬁcant diﬀerences recorded in
woolly aphid infestation between banded and unbanded trees.
Where woolly aphid appeared early in the season, tagged colonies frequently
disappeared, indicating that predators rather than parasites were playing a sig-
niﬁcant, if not the principal, role in controlling the population. In the exclusion
trial, signiﬁcant diﬀerences were found between trees ﬁtted with predator exclu-
sion bands and unbanded trees in both the numbers of earwigs in the artiﬁcial
shelters and the level of woolly aphid infestation. The correlation between the
level of woolly aphid and the number of earwigs in artiﬁcial shelters indicates the
earwig as the principal predator and hence control agent. Only another predator
of woolly aphid, similarly unaﬀected by fenoxycarb and able to access the tree
canopy principally by moving up the trunk could have produced the observed
result. No such predator was detected on the exclusion bands, in the artiﬁcial
shelters or during monitoring of the orchard fauna in earlier trials (Nicholas et al.,
1999). Adult earwigs can ﬂy but rarely take to the wing (Phillips, 1981).
The fact that earwigs can control woolly aphid is well known in Europe (Stap et
al., 1987; Mueller et al., 1988). However these trials appear to have been conducted
in experimental orchards where the management of other pests and diseases was
not addressed. As part of the present trials, laboratory experiments conﬁrmed that
earwigs were capable of consuming woolly aphid (unpublished data).
While earwigs were considered the key regulating agent of woolly aphid in
this study, it was not possible to investigate the control of woolly aphid in the
absence of A. mali or other ﬂying natural enemies. The reduced insecticide
programs used in this IPM ﬁeld trial would have allowed survival of other
natural enemies, including A. mali, lacewings, ladybirds and hoverﬂies. All
were known to occur at the trial site (Nicholas et al., 1999) and are likely to
have had a complementary eﬀect, further reducing the level of woolly aphid
infestation in the orchard. However, the high level of woolly aphid in the trees
ﬁtted with predator exclusion bands indicates they were not, individually or
collectively, capable of controlling woolly aphid in the absence of earwigs.
The polyphagous feeding habit of earwigs means that, although they have a
preference for live prey, particularly aphids (Asgari, 1966), their long term
ADRIAN H. NICHOLAS ET AL.286
survival in an orchard and hence their availability as a control agent is, unlike
A. mali, not wholly dependant on the presence of woolly aphid. This means
that earwigs can be introduced and remain established in orchards in the ab-
sence of woolly aphid. Noppert et al. (1987) used a simple deterministic sim-
ulation model to determine that eight earwigs, searching randomly, could
search the average apple tree for prey with 90%eﬃciency. They calculated the
earwig’s predation rate at approximately 70 aphids/earwig/night and found
that, even at the lowest predicted predation rate, earwigs could ‘eliminate’
woolly aphid. Counting earwigs in artiﬁcial shelters is a relative rather than
absolute measure of abundance, which can vary through the season depending
on factors such as the availability of alternative refuge sites and weather
(Phillips, 1981). However our ﬁnding, (based on the 1996/1997 season’s data),
that a seasonal mean of eight and ﬁve earwigs are required to eliminate woolly
aphid from the Granny Smith and Jonathan trees respectively supports the
ﬁndings of Noppert et al. (1987). The data suggest that to maintain eﬀective
control of woolly aphid in Red Delicious more earwigs would be required than
were present in the orchard during the 1996/1997 season. Earwigs eﬀectively
suppressed woolly aphid below the >1 rating in the cultivars Granny Smith
and Jonathan during the 1997/1998 season, although not as eﬀectively as in the
previous season. The regression model did not predict the elimination of aerial
colonies, indicating that naturally occurring populations of earwigs may not
always provide ‘full’ control, particularly in seasons favourable to woolly aphid
development. The failure of the model to predict the number of earwigs re-
quired to eliminate woolly aphid during the 1997/1998 season is probably due
to the variability in the data. The reason for this variability is unclear but
climate may have aﬀected woolly aphid development. Availability of alterna-
tive food and the eﬀects of sustained fenoxycarb use can also aﬀect earwig
development, their population and hence the predator–prey relationship
(Blaisinger et al., 1990; Sauphanor and Staubli, 1994).
The regression model predictions based on the ﬁrst four sampling dates for
earwigs in the 1996/1997 and 1997/1998 seasons follow the trend of the full
season models. These similarities suggest that with further research over suc-
cessive seasons, it may be possible to develop a strategy that would enable
growers to make decisions regarding the control of woolly aphid based on the
potential of earwig populations to provide adequate biological control.
In the 1997/1998 season, when the azinphos-methyl treatment was discon-
tinued, the plots were put under a fenoxycarb program to monitor the eﬀec-
tiveness of natural enemies in newly implemented IPM programs. The
signiﬁcantly lower woolly aphid infestation under fenoxycarb, compared with
the previous two seasons under azinphos-methyl, suggests that natural enemies
migrated into the blocks rapidly. Seasonal variation in weather patterns can
account for lower levels of woolly aphid infestation in some seasons, however
ABUNDANCE AND NATURAL CONTROL 287
this was not considered a contributing factor during this season, as a nearby
block of apples treated with azinphos-methyl recorded severe woolly aphid
infestation. Earwigs are highly mobile and known to migrate considerable
distances (up to 3 m/min) in search of food and shelter (Noppert et al., 1987).
This suggests that they have the potential to colonise orchards quickly following
the removal of broad-spectrum pesticides. The blocks used in this trial were
relatively small and further investigation is required to assess migration of
earwigs into larger orchards.
The lack of a signiﬁcant diﬀerence in woolly aphid infestation between the
blocks in the ﬁrst year of the fenoxycarb program and those in their third year,
together with the presence of earwigs early in the season, shows that earwigs
not only migrated into the blocks quickly, but their populations were suﬃcient
to provide a similar level of control. The lack of any signiﬁcant diﬀerence in
woolly aphid infestation between trees ﬁtted with artiﬁcial shelters and those
without shows that providing earwigs with artiﬁcial diurnal shelters in the tree
canopy did not improve the control of woolly aphid.
Fenoxycarb has low toxicity to earwigs and is known to reduce fertility when
applied to adults reaching or at the end of vitellogenesis (Blaisinger et al., 1990;
Sauphanor and Staubli, 1994). It also delays pre-oviposition in the oﬀspring of
earwigs treated at the third nymphal instar (Blaisinger et al., 1990). This could
result in a reduction in the earwig population, a delay in its spring emergence or
both. However no such eﬀects were observed over the 3 years of this study. The
lack of any signiﬁcant diﬀerence between the MD and FMD blocks in the
number of earwigs present in artiﬁcial shelters indicates that either the full
season program of fenoxycarb did not suppress the earwig populations, or that
they continually migrated in from the MD treatment or surrounding vegetation.
The physiological eﬀect of wing twisting observed in a few earwigs during this
trial is consistent with that caused by fenoxycarb in some other insects, e.g., the
German cockroach Blattella germanica L. (King and Bennett, 1989). This
observation indicates that at least some of the earwig population had been in
contact with and were adversely aﬀected by fenoxycarb. It is thought possible
that earwig fecundity could be reduced, as reported by Blaisinger et al.(1990),
and this may adversely aﬀect woolly aphid control in the longer term. The eﬀect
on earwigs of other pesticides commonly used in commercial apple orchards and
the possible impact of earwigs on fruit quality requires further investigation.
The authors thank the staﬀ at the Bathurst Agricultural Research Station and
Carol and Jason Nicholas for their assistance in the ﬁeld and laboratory. This
study was funded by NSW Agriculture, the Australian Apple and Pear
ADRIAN H. NICHOLAS ET AL.288
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