To Spray, or Not To Spray

NATURAL RESOURCES INSTITUTE
To spray, or not to spray:

That is the question
Horticultural entomology in the
21st century
Jerry Cross, Visiting Professor of

Horticultural Entomology
11 February 2010
Inaugural Professorial Lecture

Horticultural entomology in
the 21st century
by
Jerry Cross, East Malling Research
Visiting Professor of Horticultural Entomology,
Natural Resources Institute, University of Greenwich
An Inaugural Professorial Lecture

delivered at the University of Greenwich
11 February 2010
© University of Greenwich 2010
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biography
Jerry Cross studied Natural Sciences at Trinity College Cambridge taking the advanced
physics options in his first two years. Because of a developing interest in farming and the
countryside, he changed to applied biology for his third year specialising in entomology.
After graduating in 1976, he joined ADAS as a trainee Science Specialist (Entomology)
at Shardlow Hall, Derbyshire. In 1978 he was transferred to ADAS Reading, then in
1982 to ADAS Wye. In ADAS he gained experience in consultancy and applied research
into crop protection on a wide range of arable and horticultural crops.
In 1993 he became a Research Leader in the Entomology Department at East Malling
Research (EMR) and in 2009 he became Science Team Leader for Entomology and Plant
Pathology. He leads a range of research projects on Integrated Pest Management and
spray application to fruit crops. Particular interests include development of sampling,
assessment and forecasting methods for pests, identification and exploitation of
pheromones of fruit pests, biological control by microbial agents and natural enemies
of fruit pests, developing and evaluating whole Integrated Pest Management systems
for fruit crops and optimising spray application methods.
Current emphasis is on the identification of sex pheromones and other
semiochemicals (e.g. host plant volatiles) of UK fruit pests, in collaboration with
Professor David Hall, Chemical Ecology Group, Natural Resources Institute, University
of Greenwich, and development of methods of exploiting them for monitoring and
control. Together with Dr Angela Berrie, EMR Plant Pathologist, he has been at the
forefront of developing minimal residues Integrated Pest and Disease Management
systems for fruit crops, starting a Defra-funded research programme developing zero
residue methods well before the issue came to the fore. Another recent important work
area, in collaboration with Dr Peter Walklate (formerly of Silsoe Research Institute), is
optimising sprayer use according to orchard structure taking account of the distribution
of spray deposits and their biological efficacy.
Jerry has served successive near 10 year terms as convenor of the Association
of Applied Biologists Pesticide Application Group followed by convenor of the
International Organisation of Biological Control (IOBC) Working Group on Integrated
Plant Protection in Fruit Crops. He has recently been elected as a council member of
the IOBC. In 2007, the University of Cambridge conferred a Doctor of Philosophy by
published works on him. He is a principal editor of the international science journal
Crop Protection. He has recently been appointed as visiting professor of Horticultural
Entomology at the University of Greenwich.
Contact Details:
Prof Jerry V Cross DPhil, MA, FRES, MBPR
East Malling Research
New Road
East Malling
Kent ME19 6BJ
Tel +44(0) 1732 523748
Fax +44(0) 1732 849067
Mob: +44(0) 7732 761488
jerry.cross@emr.ac.uk
Contents
1. Introduction 2
1.1. The pesticide dilemmas 2
1.2. The spraying process 4
1.3. Lecture topics 4
2. Avoiding the need for pesticide spraying 5

2.1. Resistant varieties 5
2.2. Conserving and exploiting natural enemies 7
2.3. Manipulating and exploiting ants in the management
of tree fruit aphid pests 8
2.3.1. Ant exclusion or supplementary feeding 9
2.3.2. Exploitation to vector entomopathogenic fungi 13
2.3.3. 21st century perspectives 17
2.4. Conservation biocontrol 18
2.4.1. Conservation biocontrol for pear sucker,
Cacopsylla spp. 19
2.4.2. 21st century perspectives 26
3. Deciding if and when to treat 26

3.1. Physically-acting monitoring traps 27
3.1.1. Mussel scale 27
3.2. Semiochemical monitoring traps 31
3.2.1. Gall midge sex pheromone monitoring traps 32
3.2.2. Capsid bug sex pheromone monitoring traps 36
3.2.3. Strawberry blossom weevil aggregation
pheromone/host volatile supertrap 42
3.3. Predictive models 44
3.3.1. Blackcurrant gall mite emergence forecasting model 45
4. Treating at different times of the season 50

4.1. Autumn control of aphids 50
5. Alternatives to pesticides 55
5.1. Semiochemical based control methods 56
5.1.1. Mating Disruption (MD) and Attract and Kill (A&K) 56
5.3.1. Mass trapping 66
6. Safer more efficient orchard spray application 68
6.2. Dose expression and adjustment 68
7. Integrated pest and disease management (IPDM) 72

7.1. Minimal residues IPDM 72
7.1.1. The EMR minimum residues IPDM programme
for apples 74
7.1.2. Minimal residue IPDM programmes for soft fruit crops 78
7.1.3. Recent developments 79
8. Summary, conclusions and future perspectives 82
Acknowledgements 83
References 83
1 Jerry Cross

Horticultural entomology in
the 21st century
by
Jerry Cross, East Malling Research
Visiting Professor of Horticultural Entomology,
Natural Resources Institute, University of Greenwich
Abstract
Pesticide sprays are relied on for pest and disease control in horticultural crops but they
are regarded by the public as undesirable and harmful to health and the environment
and, in any event, their use is not sustainable. The spraying process itself is inefficient
and wasteful, especially tree and bush fruit spraying. Growers face several dilemmas
and questions: 1) to use pesticides or not to use them; 2) to use few sprays of broad-
spectrum pesticides or make many more sprays of safer selective ones; 3) whether or not
and when to spray in a particular circumstance. Overcoming dependence on pesticide
sprays is one of the greatest challenges in horticulture. Research at East Malling
Research (EMR) with many excellent collaborators and especially with the Chemical
Ecology Group of the Natural Resources Institute (NRI), University of Greenwich, over the
last decade to help resolve these dilemmas and questions is overviewed. Approaches
include new pre-emptive measures to avoid the use of pesticide sprays, new methods
of deciding if and when to treat including treatment at different times of the season, new
alternative non-pesticidal control methods, safer and more efficient spray application
methods including adjustment of the dose rate to suit the crop and Integrated Pest
and Disease Management (IPDM) programmes which minimise the risk of reportable
pesticide residues. Examples of interesting and innovative approaches that have
resulted from our research and which have led or promise to lead to real change and
progress in commercial practice and which are at the leading edge of world research
are described. These include conservation biocontrol of pear sucker, exploiting ants
in the management of tree fruit aphid pests, physically acting emergence monitoring
traps for mussel scale and blackcurrant gall mite, a forecasting model for predicting the
emergence of the gall mite and semiochemical monitoring traps for gall midge pests of
fruit crops, capsid bugs and strawberry blossom weevil. Ongoing challenging research
to exploit semiochemicals for fruit pest control by mating disruption, attract and kill and
mass trapping is also described together with the development of PACE Pesticide dose
Adjustment to the Crop Environment, the first web-based dose adjustment calculator
and the EMR minimal residues IPDM programme for apple.
Applied entomological research is vital to horticulture. The crop protection
problems that occur on different crops are continually changing as a result of many
To spray, or not to spray: That is the question 2
factors including changing varieties and crop production methods, changing pesticide
availability, the development of pesticide resistance, the arrival of new pests and other
invasive species such as the ant Lasius neglectus and the Harlequin ladybird, crop
adaptation by native species and climate change. There is a continual need for research
to develop new technologies and solutions to the problems faced. Food production
needs to be increased for world population growth in the face of climate change, but
this needs to be done sustainably reducing dependence on pesticides. Research by
horticultural entomologists will be needed throughout the 21st century and beyond.
Progress will be most rapid if close and exemplary collaboration between research
institutes and universities with complementary skills and expertises, such as that
between EMR and NRI, University of Greenwich, as well as internationally, is supported
and strengthened.
1. Introduction
1.1. The pesticide dilemmas

Horticultural crops in the UK comprise a large and diverse range of subjects. There
are over 200 different crops, not including the vast range of many thousands of
ornamentals. Almost all are subject to attack by pests and diseases to a greater or
lesser extent. Many crops have several highly damaging pests and diseases and fruit
crops, which are perennial, all have large complexes of highly damaging species and
present the greatest crop protection challenges.
Unless pests and diseases are controlled effectively, the quality expected by the
market and the quality and yield required for economic production cannot be achieved.
In many crops, pesticides are relied on to a greater or lesser extent for pest and
disease control. Commercial apple orchards for instance receive particularly intensive
pesticide spray programmes. It remains a travesty that practically every commercially
grown apple variety world-wide is highly susceptible to apple scab and many are
highly susceptible to mildew. This means most commercial apple orchards have to
receive an intensive programme of sprays of fungicides to control these diseases. The
number of applications depends on the growing region, but in the wetter countries
15-20 fungicide spray rounds are required per season, many with more than one
fungicide. Organic orchards often receive as many or more sprays than conventional
ones and using fungicides (mainly sulphur and copper) at higher doses. The number
of insecticide applications is much lower, but they are significant because insecticide
products, especially older compounds, tend to be more harmful to the environment and
potentially to humans.
Unfortunately, there is a deep seated public mistrust and negative attitude towards
pesticides. They are regarded by many as being toxic or harmful, to cause long-term
adverse affects on health as well as being highly damaging to the environment. It is an
anathema that fruit crops, grown in the ‘Garden of England’, consumed fresh as part of
a healthy diet, are intensively treated with pesticides that are regarded by the public as
harmful to the environment and human health. This perception may be unbalanced and
irrational, but it is impossible to counter against a background of continuous negative
reporting in the media fuelled by pressure groups and non-government organisations.
It often seems that the media have pesticides firmly in their sights. Attempts have been
3 Jerry Cross
made in other countries to counter the adverse public perception of pesticides but
they have been ineffective. Though public opinion is sometimes poorly informed and
the adverse consequences of pesticide use are often unfounded or exaggerated, it is
difficult to change public opinion against such media campaigns. However, market
and consumer concerns do need to be addressed. Multiple retailers have identified
the use of pesticides and the occurrence of pesticide residues as being one of the
prime concerns of consumers about fresh produce, especially apples. For them,
consumer trust is of prime importance and pesticide use and residues are considered
to undermine that trust.
So growers who wish to use pesticides are faced with a real dilemma. They need
to use them to control damaging pests and diseases and produce crops profitably,
but by doing so they are going directly against the wishes of the public and markets.
In reality, pesticides are in general inexpensive in comparative terms, are easy to use
and are mainly fairly effective. The alternatives are often more complex and costly and
require greater management inputs and skill. Overcoming dependence on pesticides
is arguably the greatest and amongst the most important challenges faced by the
horticultural industry.
Pesticides themselves also pose a second, important dilemma, which is less
well recognised or publicly expressed. The ideal pesticide would be completely
selective, would control its target pest with a high degree of efficacy, would affect no
other targets, would be completely harmless to humans, animals, livestock and the
environment and leave no residues. Though baculovirus microbial agents, such as the
codling moth granulovirus, come close to having these properties, even the best most
selective chemical pesticides fall well short of these ideals. Many pesticides have a
broad spectrum of activity, killing not only the target pest but also a wide range of
other species including natural enemies and biocontrol agents. Even selective Insect
Growth Regulator insecticides affect a far broader range of species than the target pest.
Some older pesticides such as organophosphate, carbamate and synthetic pyrethroid
insecticides, which tend to be inexpensive, have a particularly broad spectrum of
activity as well as considerable persistence. They control several pests at once as
well as suppressing the myriad of minor pests which occur, especially on fruit crops.
The second dilemma faced by growers is ‘is it better to make one application of a low
cost, broad-spectrum pesticide, or make several applications of more expensive semi-
selective ones, at much higher cost?’ In purely economic terms the answer appears
straight forward: the former choice is clearly preferable. But the true answer is in fact
quite complex and requires a good understanding of the pest and natural enemy
complexes on the crop as well as detailed knowledge of the spectrum of activity,
persistence and fate and behaviour of the pesticide(s) in the crop and the environment.
The necessary detailed knowledge and understanding is usually lacking but most crop
protection specialists consider use of more selective pesticides against key target pest
species and avoiding the use of disruptive broad spectrum pesticides to be the best
approach for longer term stability in the agro-ecosystem and the avoidance of pesticide
resistance.
1.2. The spraying process

Spraying is an inefficient and wasteful process. Himel (1969) considered it to be the
most inefficient industrial process, a very high proportion of the active product being
wasted. It has been estimated that only 0.1% of applied pesticides reach their target
pests and the remaining 99.9% affect the environment (Pimentel, 1995). Foliar pesticide
applications to tree fruit orchards are made mainly with axial fan air blast sprayers
(Figure 1). These generate a large radial spray plume which is poorly targeted for
many modern dwarf trees resulting in large (typically 25-50%) losses to the soil and
high levels of long range spray drift (10-100 times greater than that from arable boom
spraying) and a high risk of operator contamination. A simple rough calculation shows
that for instance, for a spray of chlorpyrifos 480 g/l EC at a dose of 2 l product per ha
against a 5% attack by codling moth in an apple orchard bearing 50 tonnes fruit per
ha and with a leaf area index on 2.0, only about one millionth of the pesticide applied
is utilised to control the target pest, the rest being wasted. Although improved orchard
spraying machinery, such as cross flow and tunnel sprayers, has been developed, the
improvements offered are limited and because improved designs are costly and difficult
to operate they have not as yet been widely adopted into commercial practice.
Figure 1. Axial fan orchard airblast sprayers generate a large radial spray plume which can be
poorly targeted for modern dwarf fruit trees and which results in high losses to the soil and
through spray drift, especially early in the season
1.3. Lecture topics

The title of this lecture ‘To spray, or not to spray: That is the question’ is an adaptation of
the famous soliloquy in Shakespeare’s Hamlet ‘To be, or not to be: That is the question’.
A modern translation of Hamlet’s soliloquy would be ‘To die, or not to die: That is the
question’ a very vital question indeed. Hamlet feigned madness and eventually died
from the nick of a poisoned sword. Much treachery was involved. Though he was a
5 Jerry Cross
noble, principled soul, he did make some grave mistakes and misjudgements. Whilst
not perhaps being quite so dramatic and life threatening, the question ‘To spray, or
not to spray’ is an equally tricky one. The dilemmas posed by pesticides described
above and the wasteful, inefficient and contaminating nature of the spraying process
make the search for answers important and challenging. It has been the major focus for
horticultural entomologists since the advent of modern pesticides and will continue to
be well into the 21st century and probably beyond.
In this lecture, I will overview research in which I, with many excellent collaborators,
have been involved over the past 10 or so years to rationalise and reduce pesticide use
in fruit crops grown in the UK. The lecture is divided into logical sections as follows: 2)
Avoiding the need for pesticide spraying; 3) Deciding if and when to treat; 4) Treatment
at different times of season; 5) Alternatives to pesticides; 6) Safer and more efficient
pesticide application and dose adjustment to suit the crop; 7) Integrated Pest and
Disease Management.
The subject is clearly an enormous one with numerous interacting facets which
could be illustrated by numerous examples. I have not attempted to cover the subject
comprehensively but rather to describe some of the more interesting and innovative
approaches which have been the subject of my research with many excellent
collaborators and which have led or promise to lead to real change and progress in
commercial practice. This will provide a snapshot of some of the research approaches
of horticultural entomology for the 21st century but I will also look ahead at future
perspectives.
2. Avoiding the need for pesticide spraying

There are numerous pre-emptive ways in which the need for pesticide treatment
can be avoided. Perhaps the best known are the use of resistant varieties and the
conservation and enhancement of natural enemies. These are briefly discussed below,
but our work on two more unusual and innovative approaches which are the subject of
ongoing intensive investigation at East Malling Research are described in more detail;
the manipulation and exploitation of ants in management of fruit tree aphid pests and
conservation biocontrol of the pear sucker.
2.1. Resistant varieties

Perhaps the very best and most intelligent means of avoiding the need for pesticide
treatment is to grow resistant varieties. However, to date there has been lamentably
little progress in developing resistant varieties which also meet the quality requirements
of producers and markets. There are very few examples of successful deliberate use
of pest (or disease) resistant varieties to combat important pests (or diseases) in
commercial fruit production to date. The reason for this is that varieties are chosen for
market acceptability, productivity and ease of storage and handling and the resistant
varieties have not met these requirements. Examples of true pest resistance in tree
fruits include the use of the MM106 apple rootstock with good resistance to woolly
aphid (Eriosoma lanigerum (Hausmann)), and apple varieties bred at East Malling
Research with resistance to the rosy leaf curling aphid (Dysaphis devecta (Walker)),
sparse examples indeed.
There are a few more significant examples in bush fruit: Most varieties of blackcurrant
are susceptible to both blackcurrant gall mite (Cecidophyopsis ribis (Westwood)) and
the reversion virus disease it vectors, though they vary in degree of susceptibility.
However, in recent years new blackcurrant varieties resistant to either the gall mite
or to both the gall mite and reversion virus disease have been bred (Brennan, 2008;
Brennan et al., 2009). The first gall mite resistant varieties Farleigh and Foxendown had
resistance to gall mite from gooseberry. However, the juice quality produced by these
varieties was inadequate and they were only released on the amateur market. More
recently good juice quality varieties have been released from the breeding programme
at Scottish Crop Research Institute (SCRI). The variety Ben Gairn has apparently
complete resistance to reversion virus disease inherited from Ribes dikuscha Fisch.,
a wild species which occurs in Russia and E. Asia. This variety also has a high degree
of resistance to the gall mite. A six year (2000 – 2005 inclusive) replicated experiment
at East Malling Research examined the efficacy of combining early season sulphur
sprays with a gall mite resistant variety (Ben Hope) or a gall mite resistant, reversion
susceptible variety (Ben Gairn) in an integrated gall mite management programme
compared to a reversion virus and gall mite susceptible variety (Ben Alder). The IPM
programmes were highly effective in controlling gall mite and reversion virus (Cross
and Harris, 2004; Harris and Cross, 2008). SCRI have also produced elite material with
resistance to blackcurrant leaf midge (Dasineura tetensi (Rübsaamen)).
Similarly, raspberry breeding programmes at EMR and the SCRI have bred
resistance genes to the large raspberry aphid (Amphorophora idaei (Börner)) into
modern UK raspberry varieties. Different resistance genes confer resistance to different
biotypes of the aphid. For instance resistance gene A1 provides resistance against
colonisation from biotypes 1 and 3 but it is not useful against the initially uncommon
biotype 2. The exploitation of different A. idaei resistance genes in raspberry breeding
programmes has recently been reviewed by Sargent et al. (2007). The pyramiding of
several aphid resistance genes in breeding lines in order to provide more robust and
long-lasting resistances has been an objective at EMR for 40 years. Molecular markers
would be a key tool in differentiating reported genes, identifying their presence in
modern hybrid material and in managing strategies for pyramiding.
The failure to develop or exploit apple varieties with the high visual, taste and
other quality requirements of markets and consumers with resistance to apple scab
(Venturia inaequalis (Cooke) Winter) and/or powdery mildew (Podosphaera leuchotricha
(Ell. & Ev.) Salm.)) is clearly a most significant and staggering failure of apple breeding
programmes and Integrated Pest and Disease Management. It remains a travesty that
practically every commercially grown apple variety world-wide is highly susceptible
to apple scab and many are highly susceptible to powdery mildew. This means that
most commercial apple orchards have to receive an intensive programme of sprays
of fungicides to control these diseases. The number of applications depends on the
growing region, but in the wetter countries 15-20 fungicide spray rounds are required
per season, many with more than one fungicide. This cannot change until resistant, or
at least much less susceptible, varieties to these diseases are bred and are accepted
by growers and markets. Many scab resistant apple varieties with the Vf resistance
gene from Malus floribunda Siebold ex Van Houtte have been bred, but to date none
has found large scale market acceptance because their other fruit quality attributes are
not up to standard.
Investment into plant breeding has been woefully inadequate, not only into breeding
for pest and disease resistance but also for other traits that are vital for sustainable
horticulture such as tolerance to drought or low nutrition. Publicly funded breeding
7 Jerry Cross
programmes need to be expanded greatly if substantive progress is to be made. GM

technology also offers very important opportunities. The lack of public acceptance is
clearly barrier to progress currently. However, a clear distinction needs to be made
between cis-genesis technology, a form of GM technology where only genes from
crossable donor plants are transferred, and trans-genesis where the transfer of genes
is unrestricted. Recently, a cis-genic scab resistant transform of the apple variety Gala
has been produced by the Swiss Federal Institute of Technology, Zurich (Szankowski
et al., 2009; Gessler et al., 2010). Public acceptance of the enormous benefits of this
technology is necessary before it can be used.
2.2. Conserving and exploiting natural enemies

With the exception of strawberry, UK fruit crops are grown as a long-term perennials
and orchards and plantations provide relatively stable ecological habitats. The plant
canopy is semi-permanent and the soil is generally undisturbed by cultivation. Ground
herbage is usually present in the alleyways though a weed free strip is maintained
under the trees to minimise weed competition for moisture and nutrients. Unsprayed
fruit trees and bushes can support an enormous arthropod fauna. Apple for instance
supports >1000 arthropod species. Mészáros et al. (1984) found a total fauna of 1759
insect species in five apple orchards in Hungary. However, many species in this study
were collected exclusively with light traps, so the number of species connected to
the apple orchards was probably lower. About 25% of the arthropods connected with
apple are pests, 25 % are natural enemies of pests and the remaining 50% are benign,
though they are important as they act as buffers. However, application of even a single
spray of a broad-spectrum insecticide has a profound impact on the range and relative
abundance of arthropods. Most species are highly sensitive to insecticides and are
virtually eliminated by a single insecticide spray. However, others (especially those with
cryptic habits or those that are dispersive, have alternative hosts, or have developed
insecticide-resistant strains) thrive as important pests. Treatment with broad-spectrum
insecticides gives short-term control but usually eliminates or greatly reduces their
natural enemies, so making subsequent outbreaks more severe. UK tree fruits (apple,
pear, plum and cherry) are members of the Rosaceae and have many closely related
tree and shrub species (hawthorn, rose, rowan, wild cherry etc.) that are common
in the environment. Many tree fruit pests occur on other Rosaceae which provide a
source of infestation for orchards. Fortunately, only a small proportion of the arthropods
that feed on tree fruits are important pests. Key pests are those that attack the fruit
directly, frequently causing damage at low population densities. They are not effectively
regulated by their natural enemies to prevent economic damage and tend to reoccur
after control with insecticides. The best known key pest of apple is the codling moth
(Cydia pomonella (L.)). A second important pest group are the so-called secondary
pests. In the unsprayed situation they are effectively regulated by their natural enemies.
Outbreaks are caused by natural enemy disturbance. They have a tendency to develop
strains resistant to insecticides and are difficult to control chemically. The best known
secondary pests of apple and pear are the fruit tree red spider mite (Panonychus ulmi
(Koch)) and the pear sucker (Cacopsylla sp.). Most other pests are categorised as minor
pests. Either they do not cause a reduction in fruit yield or quality, are very localised or
sporadic in their occurrence or are easily controlled with insecticides.
The key to successful IPM is to find a range of effective methods to control the key
pests without harming important natural enemies of secondary pests as well as having
effective and non-disruptive management methods for the myriad of minor pests that
can become troublesome from time to time. This has to be done with methods that
have minimal adverse effects on humans and the environment.
The preservation of key natural enemies of important secondary pests is a crucial
part of successful IPM. One of the main success stories of apple IPM has been the
realisation of the crucial importance of OP-resistant strains of the orchard predatory
mite Typhlodromus pyri Scheuten. Up to the 1980s, insecticides and fungicides harmful
to the predatory mite were extensively used and phytophagous mites, which rapidly
developed resistance to new acaricides, were the most troublesome orchard pests. For
many years it was almost routine practice to spray pirimiphos-methyl (Blex) in spring for
apple rust mite (Aculus schlechtendali (Nalepa)) and cyhexatin (Plictran) after flowering
for fruit tree red spider mite. In the 1980s, once the importance of the orchard predatory
mite had been realized, growers stopped using pesticides harmful to it (e.g. synthetic
pyrethroids, pirimiphos-methyl, dinocap etc.). The predatory mite re-colonised most
commercial orchards and the phytophagous mites ceased to be a problem. There
are many fruit farms in the UK where acaricide treatment has not been necessary
for 30 years or more! Another natural enemy important in conservation biocontrol is
the common European earwig (Forficula auricularia L.). Earwigs are important natural
enemies of many apple pests, but most notably it has been found that orchards with
high populations of earwigs do not suffer from outbreaks of woolly aphid. Many other
apple pests are naturally regulated by natural enemies notably the guilds of parasitoids
that regulate a complex of leaf mining moth pests. For recent reviews of predators and
parasitoids in orchards see Cross et al. (1999a) and Solomon et al. (2000).
2.3. Manipulating and exploiting ants in the management of

tree fruit aphid pests
Mutualism between honeydew-producing homopterans and ants is a well-known
phenomenon (Way, 1963; Stadler and Dixon, 1999) (Figure 2a). Ants benefit from this
mutualism as they obtain honeydew from aphids. The honeydew is a complex mixture
of sugars, free amino-acids, amides, proteins, minerals and B-vitamins, composing
the main part of the food of the Lasius genus (Way, 1963). Aphids benefit from this
association in many ways. El-Ziady (1960) showed that Lasius niger (L.) has a direct
effect on Aphis fabae Seop. by reducing the aphid`s rates of feeding, assimilation,
growth and reproduction. Alate production and dispersal are also delayed (El-Ziady,
1960; Skinner, 1983). Sanitary behaviour by attendant ants reduces aphid mortality
by decreasing the number of aphids drowning or becoming immobilized in honeydew
(Nixon, 1951; Skinner, 1983). In the absence of attending ants, the accumulation of
honeydew can increase levels of leaf rotting and encourage the growth of various
sooty moulds (Capnodiaceae) (Hill and Blackmore, 1980; Skinner, 1983). Ants remove
dead and dying aphids including those infected with entomopathogenic fungi such as
Entomophthora sp. (Skinner, 1983). El-Ziady and Kennedy (1956) and Banks (1958)
described denser, cleaner and generally healthier A. fabae colonies tended by L. niger.
Additionally, the honeydew accumulations can be attractive to aphid predators (Carter
and Dixon, 1984; Sutherland et al., 2001; Choi et al., 2004) and aphid parasitoids
(Budenberg, 1990). Furthermore, tending ants have a direct effect on aphid colonies by
protecting them from predators (El-Ziady and Kennedy, 1956; Banks, 1962; Addicott,
1979; Tilles and Wood, 1982; Skinner, 1983; Buckley, 1987; Sadler and Dixon, 1999;
9 Jerry Cross
Yao et al., 2000; Kaneko, 2003) and aphid parasitoids (Völkl, 1992; Müller et al., 1999).
In contrast, aphids can suffer costs when attended by ants such as prolonged
development times, smaller body size, delayed offspring production, proportionally
smaller gonads and fewer well developed embryos (Stadler and Dixon, 1999; Yao et
al., 2000). Additionally, some parasitoids specialise in parasitising aphids attended by
ants (Völkl, 1992; Stadler and Dixon, 1999; Völkl and Mackauer, 2000; Kaneko, 2003).
Finally, ants also prey on their homopteran partners (Cherix, 1987; Rosengren and
Sungstrom, 1991; Sakata, 1994, 1995; Offenberg, 2001).
Orchards and other long term perennial fruit crops provide suitable habitats and
nesting sites for the common black ant, Lasius niger L. (Hymenoptera; Formicidae)
(Skinner and Allen, 1996) as the soil is normally undisturbed by cultivation over long
periods. L. niger is an omnivorous scavenger, predating on insects and collecting
carbohydrate rich honeydew from homopteran insects including aphids and scale
insects. In our arthropod biodiversity study in the conventionally sprayed, unsprayed
and IPM plots in Wiseman orchard at East Malling Research between 2000 and 2005,
L niger was the commonest arthropod in the apple tree canopy.
Many of the aphid pests of fruit crops have close mutualistic relationships with
L. niger. The strength of the relationship varies considerably with aphid species. For
instance, the rosy apple aphid, Dysaphis plantaginea (Passerini), is strongly attended
by L. niger whereas the mealy plum aphid, Hyalopterus pruni (Geoffroy), is not attended
by ants. L. niger benefits from the protein and carbohydrate rich honeydew food source
provided by the aphids which benefit by improved colony hygiene through ant removal
of honeydew and dead or diseased individuals (Buckley, 1987) and protection from
natural enemies. Ants have even been noted to re-locate aphids to new feeding sites
with high host plant quality (Collins and Leather, 2002).
We have been studying three different ways of manipulating and exploiting ants to
enhance biocontrol of aphid pests in orchards. These are: 1) excluding ants so aphids
are subject to early more effective predation by generalist predators such as ladybirds,
predatory bugs and hoverfly larvae; 2) providing ants with alternative artificial food
sources distracting them from tending aphid pests; 3) exploiting the ants to passively
vector entomopathogenic fungi for biocontrol of aphids.
Csaba Nagy, a most enthusiastic and dedicated entomologist and ant specialist
from Hungary has worked for our team at East Malling Research for the last 6 growing
seasons and started his PhD investigating the exploitation of ants for biocontrol of
aphid pest in orchards (registered at Eötvös Loránd University, Budapest and based at
EMR) in 2009.
2.3.1. Ant exclusion or supplementary feeding

In 2006, we conducted an intensive study of the effects of the common black ant, L.
niger, on populations of D. plantaginea, and green apple aphid, Aphis pomi Degeer
(Nagy et al., 2007). Two replicated experiments were conducted in an unsprayed
apple orchard (cv Discovery) at East Malling Research. Ants were either excluded from
trees by a sticky barrier band round the base of the trunk (experiment 1) or provided
with honey baits at the base of the trunk or in the canopy (experiment 2) (Figure 2b).
Trees where ants had free access and trees without artificial baits were provided as
experimental controls.
a)
b)
Figure 2. a) apple grass aphid (Rhopalosiphum insertum (Walker)) feeding on a young apple leaf
in spring tended by the common black ant Lasius niger.
b) honey feeders for L. niger provided at the base of Discovery apple trees in the ant exclusion/
supplementary feeding experiment in 2006
11 Jerry Cross
Exclusion of ants resulted in a rapid slow down in the increase of the populations
of D. plantaginea. During the experiment, the abundance of D. plantaginea increased
64-fold relative to the initial numbers on the control (CONT) trees but by just a bit more
than 3-fold on the trees where ants were excluded (EXCL) (Figure 3). Meanwhile, the
number of the ants tending D. plantaginea colonies on CONT trees rose in the first
three weeks of the experiment, but this increase stopped in the last week. During the
experiment the number of tending ants increased 7.6-fold relative to the initial number
on the CONT trees, so their increase was less than of the proportional increase in aphid
numbers.
The initial number of A. pomi was 7 times greater on the randomly chosen
EXCL trees, but this difference decreased during the experiment. At the end of the
experiment, the number was almost 25 times greater on the CONT trees. The number
of ants tending A. pomi colonies increased throughout the sampling period. At the end
of the experiment, the number of A. pomi was 6 times greater while the number of ants
tending A. pomi colonies was 15 times greater than it was at the beginning.
The total number of predators (coccinellid adults and larvae, predatory
Heteroptera, syrphid larvae, Dermaptera, Neuroptera larvae and Araneae) was
significantly greater on the EXCL trees at the start of the experiment, but later the
number equalised. By the end of the experiment, predator numbers were numerically
greater on the CONT trees, but this difference was not significant (Figure 4).
Figure 3. The effect of ant exclusion on the abundance of D. plantaginea (control trees: CONT;
ant excluded trees: EXCL; A-A: n.s.; A-B: p<0.01)
Figure 4. The effect of ant exclusion on the abundance of predators on the canopy of apple
trees (control trees: CONT; ant excluded trees: EXCL; A-A: n.s.; A-B: p<0.05)
Provision of artificial baits, either at the base (FTRUNK) or in the canopy (FCANOPY)
of the trees, caused reductions in the numbers of D. plantaginea (Figure 5) and their
tending ants, but the effects were weaker than in the case of exclusion. There was
no significant difference between the ants tending D. plantaginea on FTRUNK and
FCANOPY trees.
There were no significant differences in the total predator (coccinellid adults
and larvae, predatory Heteroptera, syrphid larvae, Dermaptera, Neuroptera larvae,
Aphidoletes aphidimyza (Rondani) larvae, Cantharidae and Araneae) numbers between
the treatments, but in the middle of June predator numbers were higher on the CONT
trees. Their abundances followed the aphid numbers.
Figure 5. The effect of ant feeding on the abundance of D. plantaginea (control trees:
CONT; trees where ants were fed at the trunk: FTRUNK; trees where ants fed in the canopy:
FCANOPY; A-A, B-B, a-a, b-b: n.s.; A-B: p<0.05; a-b: p<0.10)
13 Jerry Cross
Exclusion of ants resulted in rapid decreases in the populations of both aphid species
compared to control trees, but increased the populations of predatory insects and
spiders. In contrast, populations of both aphid species increased rapidly on control
trees where ants had not been excluded and where predator populations were smaller
at the beginning. These results are partly similar to the results of some previous
experiments (Skinner, 1983; Stewart-Jones et al., 2007).
The effect of the supplementary feeding on D. plantaginea was clear. The extra
food (honey) reduced the number of ants tending the D. plantaginea colonies probably
giving a chance for predators to destroy the aphid colonies. Reduction of aphid tending
by ants after honey feeding was shown in a laboratory experiment (Offenberg, 2001),
and our study showed this phenomenon also occurs in the field. The effects on A.
pomi were not so clear, but the FTRUNK treatment seemed to have an effect similar to
exclusion, though much weaker.
We concluded that the honey used was probably not as attractive and as
useful a food for L. niger as aphid honeydew and that honeydew contains additional
components which are important or essential for the ants. In 2009, as part of his PhD
investigations, Csaba Nagy started chemical analysis of the sugar composition of
honeydew from different ant species with different degrees of attractiveness to L. niger.
The sugar composition of the honeydew from two aphid species (D. plantaginea and
A. pomi) feeding on apple were analysed by HPLC. Glucose and fructose were the
most important components of D. plantaginea honeydew. Glucose, fructose, sucrose,
melezitose and trehalose were the most important components of A. pomi honeydew.
Melezitose is the most attractive sugar for L. niger (Kiss, 1981; Völkl et al., 1999) and
the presence of this sugar in A. pomi honeydew may be the reason of the higher
attendance of this aphid species by L. niger. This information can help us to make
a highly attractive sugar mixture for ant feeding studies in the future. Our research to
describe the role of aphid tending in the population increase of tree fruit aphid pests
and to work out methods which, through reducing the abundance of ants on the aphid
colonies, would enhance the efficacy of aphidophagous predators in apple orchards,
is ongoing.
2.3.2. Exploitation to vector entomopathogenic fungi

A further interesting and ongoing research avenue at EMR is the vectoring of
entomopathogenic fungi by ants to aphids. We are attempting to develop an innovative
biocontrol method which could provide an alternative or supplementary, non-pesticidal
control method for this important group of pests.
The potential for common black ant Lasius niger workers to vector conidia of
the entomopathogenic fungus Lecanicillium longisporum (Zimmerman) Zare & Gams
[Verticillium lecanii (Zimm.) Viégas] to colonies of the rosy apple aphid Dysaphis
plantaginea (Passerini) was demonstrated in laboratory and field experiments at EMR
by Imperial College at Wye student Annette Southgate née Bird for her MSc project in
2002 (Bird, 2002; Bird et al., 2004).
D. plantaginea is a common and damaging pests of apple throughout Europe,
North America and Central Asia and is currently controlled in commercial orchards
by early season foliar sprays of insecticides such as chlorpyrifos, pirimicarb or
thiacloprid. Recently however, populations in central and southern Europe have
developed resistance to insecticides (e.g., Schaub et al., 1999, 2001). D. plantaginea
has a wide range of natural enemies that have been well documented (Cross et al.,
1999a, b; Solomon et al., 2000). However, the naturally occurring microbial pathogens
of D. plantaginea have not been thoroughly studied. Thoizon (1970) is the only record
of fungal infection (Entomophthora planchoniana Cornu) in field populations of D.
plantaginea. There has also been little work to investigate the possible exploitation of
microbial pathogens for biocontrol of this aphid species (Tsinovskii and Egina, 1977).
Apple orchards provide suitable habitats and nesting sites for L. niger (Skinner and Allen,
1996). Effective dispersal of biocontrol agents to their target hosts is a requirement for
successful biocontrol. Targeted dispersal is especially important where pests have a
cryptic habit such as D. plantaginea which lives in leaf curls and may therefore be
protected from sprays. Although numerous studies have explored the potential of
non-target arthropods such as bees (Butt et al., 1998), collembola (Dromph, 2003),
mites (Schabel, 1982) and coccinellids (Pell et al., 1997; Roy et al., 2001) as vectors
of entomopathogenic fungi, studies concerning ants had previously been largely
neglected. This is somewhat surprising as ants often have intimate associations with
hemipteran pests. Gracia-Garza et al. (1997) showed that ants (Phediole spp.) could
vector propagules of the fungal biocontrol agent Fusarium oxysporum Schlechtend f.
sp. erythroxyli Sands of Fusarium wilt of cocoa on their cuticles. In a preliminary study
by an earlier Imperial College at Wye student, Elizabeth Flower, it was demonstrated
that in the laboratory, L. niger could vector conidia of the entomopathogenic fungus
Lecanicillium longisporum to the black bean aphid (A. fabae) resulting in significant
decline in aphid populations due to fungal infection.
Scanning electron microscope studies showed that L. niger workers which were
artificially contaminated with L. longisporum conidia, carried conidia primarily on their
tarsae but also on antennae and mandibles (Figure 6a). L. niger was able to passively
vector conidia of L. longisporum to D. plantaginea and, under the temperature and
humidity conditions in the experiments, the entomopathogen was able to infect and kill
the target aphids. There was no recorded mortality of workers or larvae due to infection
with the fungus. Neither L. niger workers nor larvae were susceptible to infection with
L. longisporum. This was in agreement with Hall (1981), who suggested that application
of Lecanicillium spp. in glasshouses was not detrimental to ants. Lecanicillium spp. are
known to infect a limited number of hosts, being recorded most frequently in aphids
(e.g., Feng et al., 1990; Hatting et al., 1999) and scale insects (Hall, 1981) but have
not been recorded as major pathogens of non-target natural enemies (Goettel et al.,
1990). As high relative humidity was maintained in the experiments to encourage
fungal infection and given the limited recorded host range of Lecanicillium spp., the L.
longisporum isolate used was clearly not pathogenic to this species of ant. In addition,
it has been suggested that ants are able to reduce infection with entomopathogenic
fungi by removing conidia through grooming (Oi and Pereira, 1993 and references
within). The earlier work by Flower (2002) suggested that L. niger workers could directly
remove L. longisporum conidia from the exoskeleton during grooming. The release of
antibiotic and phenyl acetic acid secretions by adult and juvenile ants is also thought
to inhibit growth of entomopathogenic fungi such as Beauveria bassiana (Balsamo)
Vuillemin and Paecilomyces lilacinus (Thom.) (Beattie et al., 1985). Contact between
L. longisporum-inoculated workers and non-inoculated workers occurred frequently
in the study, and it was therefore possible that transmission of conidia could occur.
Indeed, horizontal transmission of conidia of B. bassiana and Metharhizium anisopliae
(Metschnikoft Sarakin) between worker ants within nests has been shown to occur,
but in these cases was detrimental to ant populations (Pereira and Stimac, 1992;
15 Jerry Cross
Kelleytunis et al., 1995). In comparison, no infection was observed in either workers or

larvae that were contaminated with conidia of Lecanicillium sp. These results provided
encouraging indications that L. niger workers, larvae and pupae are not adversely
affected by Lecanicillium spp.
a) b)
Figure 6. a) Scanning Electron Micrograph of spores of the entomopathogenic fungus L.

longisporum carried on the body surface of a L. niger worker b) rosy apple aphid (D. plantaginea)
mycotised by L. longisporum after being infected by a spore-carrying L. niger worker. Photos
courtesy Annette Southgate née Bird, Imperial College at Wye
Behavioural experiments showed that L. niger workers removed both dead uninfected
aphids and L. longisporum-infected cadavers of D. plantaginea. Workers generally
moved dead uninfected aphids to the nest area within the ant cage. Similarly, Flatt and
Weisser (2000) showed that, under laboratory conditions, L. niger workers removed
dead uninfected aphids of two species to their nests. In the study by Bird (2002) and Bird
et al. (2004), ants differentiated between dead uninfected and L. longisporum-infected
aphid cadavers and generally abandoned the infected cadavers in areas where dead
ants were usually placed. The ability of L. niger to assess the ‘health’ of tended aphid
colonies was shown by Collins and Leather (2002) who reported that ants could remove
healthy aphids to start new colonies if the original aphid colony became overcrowded.
Under laboratory conditions, L. niger workers removed L. longisporum-infected D.
plantaginea cadavers and this behaviour may potentially reduce the total quantity of
fungal inoculum available for further infections within an aphid colony. In field trials,
Skinner (1983) found significantly fewer D. plantaginea infected with Entomophthora
spp. where colonies were tended by L. niger compared to colonies where ants were
excluded. The potential for L. niger to passively vector entomopathogenic fungi was
demonstrated under laboratory, semi-field and field conditions (Figure 6b). In the
laboratory vectoring experiment, L. niger workers inoculated with a maximum dose of
conidia were confined immediately following inoculation to small areas with a single
aphid. Hence, large numbers of L. longisporum conidia were likely to have been
transferred, resulting in 68.3% aphid mortality. Similar infection values were obtained in
the laboratory when the coccinellid Hippodamia convergens Guerin Meneville vectored
Paecilomyces fumosoroseus (Wize) Brown and Smith to the Russian wheat aphid,
Diuraphis noxia (Kurdj.), initiating infection in approximately 53% of the population (Pell
and Vandenberg, 2002). In the proof of concept studies by Bird (Bird, 2002; Bird et
al., 2004) aphid mortality of 30.8% was observed in the semi-field experiment, where
there were potentially fewer contacts to initiate infection between ants and aphids.
The experiments were designed to allow ants the freedom to clean themselves and
forage under more realistic conditions and hence conidia may have been removed
during grooming activity, prior to ants entering aphid colonies. In similar experiments
under semi-field conditions, Coccinella septempunctata L. adults and larvae have been
used as vectors of Pandora (Erynia) neoaphidis Remaudiére and Hennebert to the pea
aphid Acyrthosiphon pisum (Harris); infection was initiated in 10-11% and 11-13%
of the aphid population, respectively (Pell et al., 1997; Roy et al., 2001). Bird’s field
vectoring experiments resulted in low mortality of D. plantaginea due to L. longisporum
(3.7%). Similarly, results from a field study where coccinellid beetles inoculated with
P. neoaphidis were added to A. pisum colonies on bean plants and enclosed in mesh
bags, showed a comparable maximum value of 5% aphid mortality due to fungus (Roy
et al., 2001). During the 2002 field season, epizootics of the entomophthoralean fungus
E. planchoniana were noted to occur in colonies of D. plantaginea in several orchards in
Kent (H. Hesketh, pers. obs.). In addition, a casual survey of trees in the same orchard
in which field experiments were done, suggested that approximately 6% of aphids
in D. plantaginea colonies were infected with E. planchoniana (unpublished data)
indicating abiotic conditions were likely to have been conducive for fungal infection
and sporulation during the growing season. Roditakis et al. (2000) highlighted the
importance of secondary transmission of Lecanicillium spp. conidia to aphids from
surrounding vegetation in the dispersal of this fungus. These studies suggested both
ants and coccinellid beetles contaminated with conidia may deposit those conidia onto
leaf surfaces and that aphids are able to acquire sufficient numbers of conidia to cause
infection. Interestingly, preliminary data from experiments by Bird (2002) indicated that
secondary transmission of L. longisporum to D. plantaginea was possible from plant
material previously foraged on by L. longisporum contaminated L. niger. Similarly, Roy
et al. (2001) showed that 3-10% of aphids placed onto bean plants, previously foraged
by coccinellid beetles inoculated with P. neoaphidis, became infected with the fungus.
This is the first description of ants passively vectoring an entomopathogenic fungus
to aphids. The successful initiation of infections by L. longisporum in laboratory, semi-
field and field conditions indicated that there is the potential for use of this fungus in
biocontrol.
Csaba Nagy is now undertaking much more comprehensive and detailed studies
of ant vectoring of entomopthogenic fungi to the aphid pests of cherry and plum as part
of his PhD studies. The first stage of this work, which is still in progress, is to identify a
range of entomopathogenic fungi that are potentially pathogenic to aphids but which
are safe to L. niger. A laboratory based maximum challenge bioassay is being used
to evaluate the effects of 34 fungal isolates (including B. bassiana, M. anisopliae, and
Paecilomyces, Verticillium and Lecanicillium sp.) on ant workers and larvae. Special
bioassay arenas, each initially containing 20 L. niger workers and 10 larvae, have
been constructed. In the bioassay, the workers are forced to walk over the surface
of a colony of the fungus in order to reach their food, honey. Their bodies become
contaminated with spores which they then carry back to other workers and larvae in
the brood chamber. The affects on the ants are observed for a period of 3 months or
more. To date, 3 replicates of the bioassay have been completed. The results show
that though many of the fungi are pathogenic to L. niger with varying speeds of action,
a small number have proved to be safe. In the next stage of the work, aphids will be
17 Jerry Cross
introduced into the bioassay. Once the most suitable strain(s) of fungus have been
selected, the investigation will focus on exploiting the system in the field including
practical ways of contaminating the ants with the fungus.
2.3.3. 21st century perspectives

Our work on exploiting ants in pest management is at an early stage but it is clear
that the ongoing investigations above offer exciting and novel prospects. One recent
development which could have a profound effect on horticultural pest management in
Europe is the arrival of the invasive ant species Lasius neglectus Van Loon, Boomsma
and Andrásfalvy. The ant was identified in 1990 after establishing a colony in Budapest,
Hungary, although its presence in the garden of the Company for the Development
of Fruit and Ornamental Production at Budapest was already known from the early
seventies (Van Loon et al., 1990). L. neglectus has spread rapidly throughout much of
Europe (Seifert, 2000; Tartally, 2006; Espadaler et al., 2007) and a colony was reported
from Hidcote Gardens, Gloucestershire in England in 2009.
Superficially, L. neglectus is similar in appearance to L niger, but it is smaller in
body size, paler in colour, has less long hairs on its legs and antennae (Seifert, 1996)
(Figure 7), and has significantly different behavioural patterns, particularly in the social
structure within colonies (Van Loon et al., 1990).
Figure 7. Small colony of the invasive ant Lasius neglectus. Photo courtesy Csaba Nagy
L. neglectus forms ‘super colonies’, a system of interconnected nests with many

queens, estimated to number over 35,500 in some colonies (Espadaler et al., 2004).
The queens, instead of moving to a new nest to start a new colony, will mate within
the existing colony (Espadaler and Rey, 2001). Unlike most ant species, queens mate
underground and do not normally fly. As the occupants of these colonies are related,
they do not demonstrate territorial aggression. L. neglectus can outnumber native ant
species by 10 to 100 times in infested areas and, as such, may have important effects
on horticultural ecosystems if it becomes established. L. neglectus seems to be highly
dependent on aphid honeydew. It is active throughout the entire day and aphid tending
is continuous, aphids on different tree species being visited in huge numbers, from
late April to late October (Espadaler and Bernal, 2010). L. neglectus can collect more
honeydew and visit aphids in higher number, than native Lasius species (Paris, 2007). L.
neglectus has been shown to be highly aggressive against other Lasius species and it
is known that in the areas occupied by this species, other surface-foraging ant species
have vanished or have very reduced populations (Tartally, 2000; Cremer et al., 2006).
Other arthropod groups also seem to be affected in positive (= enhanced presence;
aphids, Dermestes laniarius Illeger (Coleoptera: Dermestidae), Lampyris noctiluca (L.)
(Coleoptera: Lampyridae)), negative (= lesser density; Lepidoptera larvae, Isopoda,
Galeruca tanaceti (L.) (Coleoptera: Chrysomelidae), Ocypus olens (Mull.) (Coleoptera:
Staphylinidae)) or neutral ways (Nagy et al., 2009; Espadaler and Bernal, 2010).
To date, L. neglectus has not been reported to have become established in
orchards or other fruit plantations or to have had significant affects on fruit crops or
their pests, but it is perhaps only a matter of time before it does so. The outcome is
unpredictable but it could displace L. niger and have profound positive or negative
consequences for pest management.
The recent arrival in 2004 of the invasive Harlequin ladybird (Harmonia axyridis
(Pallas)) in the UK is likely to have important consequences for the management of fruit
pests. H. axyridis is a voracious predator of aphids and is common in orchards and well
as on many other trees and plants that support aphids, including common (perennial)
stinging nettle (Urtica Dioica L.). For a review of its biology see Koch (2003) and for
management see Kenis et al. (2008). It competes with other predators and preys on
other ladybird species. It is unclear whether it will be of benefit or detriment to fruit
pest management but research is needed to understand its impacts and to find ways
to exploit it.
2.4. Conservation biocontrol

Conservation biocontrol is the practice of enhancing natural enemy efficacy through
modification of the environment or existing pesticide practices (Eilenberg et al., 2001)
(for reviews of conservation biocontrol see Barbosa (1998); Jonsson et al. (2008)). The
potential of conservation biocontrol is greatly underexploited. Developing conservation
biocontrol approaches will be one of the major challenges for horticultural entomology
in the 21st century. The approach is particularly applicable in tree fruit crops because
they are perennial and provide semi- permanent habitats where plants other than the
crop plant can be permanently maintained inside the cropping area itself. One way to
develop conservation biocontrol strategies is to search for plants or other resources that
benefit key natural enemies (Straub et al., 2008) but not their antagonists or the pest
(e.g. selective food plants; Lavandero et al., 2006; Fiedler and Landis, 2007a, b) or other
important pests or diseases. Such plants may provide alternative prey for key natural
19 Jerry Cross
enemies to enhance their populations at key times, especially when pest populations
are low. Many predators and parasitoids depend on non-prey food at least during parts
of their life cycle (Coll and Guershon, 2002; Wäckers et al., 2005) and increasing the
availability of such food sources is a further complementary aspect of this approach.
The use of strips of flowering plants sown adjacent to or within crops to provide nectar
and pollen for natural enemies to feed on is the commonest approach which has been
explored in many crops (Pfiffner and Wyss, 2004; Heimpel and Jervis, 2005; Gurr et
al., 2004). Aphid and psyllid honeydew may also provide a food source for predators
and parasitoids (Wäckers et al., 2005). Shelter is another key resource that can be
provided to improve efficacy of natural enemies (reviewed by Griffiths et al., 2008). The
primary purpose is to give natural enemies a habitat that is suitable for over wintering
or aestivation and a refuge from disturbances caused by agricultural practices. Beetle
banks, which are usually grass covered earth banks located in the middle of a field,
provide one of the most well known type of shelter habitats (Thomas et al., 1991).
These banks provide suitable over wintering sites for predatory beetles (Carabidae and
Staphylinidae) and spiders. Optimisation of conservation biocontrol requires in-depth
knowledge of the ecology of natural enemies and the ecological communities of which
they are part. It is likely to require a conspicuous change to the farm on a landscape
scale and has wider conservation and sustainability benefits.
2.4.1. Conservation biocontrol for pear sucker, Cacopsylla spp.

In 2008 a new 4 year Horticulture LINK project HL0194 ‘Exploiting semiochemicals,
conservation biocontrol and selective physical controls in integrated management of
pear sucker’ was started with EMR and NRI closely collaborating as the science based
partners. Expertise in arthropod biodiversity was provided by the research group of
Professor Viktor Marko at the Corvinus Agricultural University, Budapest, Hungary and
his students, especially Csaba Nagy who worked intensively on the project in the first
year until starting his PhD on ant vectoring of entomopathogens to aphids (see above).
Pear sucker (Cacopsylla spp.) (Figure 8) is a devastating pest of pears which is
currently out of control and causing serious widespread damage in many commercial
pear orchards in the UK and elsewhere wherever pears are grown. Nymphs suck sap
from leaves and fruits, excreting honeydew which turns black with sooty mould. This
contaminates the foliage and fruits, ruining the crop (Figure 8). Attacks weaken the trees
which suffer from severe depletion in fruit buds the year following attack or may even
be killed. The pest transmits pear decline, a debilitating phytoplasma disease of young
trees. Pear sucker is favoured by hot, dry conditions and is particularly devastating when
there are prolonged periods of dry weather. Climate change is seriously exacerbating
the problem which threatens the future of pear growing in the UK and threatens any
expansion of the area of production of this crop in the UK, which otherwise is favoured
by warmer conditions.
Figure 8. Pear sucker (Cacopsylla pyri); Top left) nymphs; Top right) adult; Bottom) severe sooty
mould blackening to pear foliage and shoots caused by honeydew contamination produced by
large numbers of mature nymphs. Bottom photo courtesy Colin Carter, Landseer
21 Jerry Cross
Anthocorid predatory bugs (Figure 9) (especially Anthocoris nemoralis Fabricius) have

long been known to be the key predators of pear sucker. If the pesticide programme
allows them to survive, they can naturally regulate populations of the pest (Solomon
et al., 1989; 2000). However, few anthocorids overwinter in pear orchards because
they do not provide sufficient food or shelter. Anthocorids migrate into pear orchards
in early summer. This migration is responsible for the major part of the population of
anthocorids found during summer. Biocontrol relies on a timely influx of adequate
numbers of anthocorids in spring so that there is a high density of predators in the pear
orchard early in the cropping season. Often the early season influx is inadequate and/or
too late and pear sucker populations increase to damaging levels in advance of those
of anthocorid predators.
Figure 9. Anthocoris nemorum (left) and Anthocoris nemoralis (right). Note that A. nemorum
has a shiny body and longer yellower antennae whereas A. nemoralis is dull with shorter black
antennae
Orchards in the UK are usually surrounded by windbreaks and/or hedgerows. The

origins and compositions of these are diverse. However, they have not been chosen
and are not managed for conservation biocontrol purposes. Purpose planted and
maintained (4-6 m tall, ~ 1m wide) windbreaks are the most common, the function
of which is physical/mechanical .i.e. to provide shelter from wind. The most common
windbreak species are grey alder (Alnus incarna (L.) Moench) and Italian alder (Alnus
cordata Desf.) (Figure 10).
Figure 10. A modern Italian alder (Alnus cordata) windbreak of the type commonly used for tree
fruit orchards. This tree species supports only sparse communities of arthropods and does not
contribute significantly to conservation biocontrol
One important objective of the Horticulture LINK project is to develop conservation

biocontrol methods to maximise anthocorid populations and other natural enemies of
pear sucker. The main aim is to identify woody species and herbaceous understory
plants for hedgerows/windbreaks to provide abundant sources of anthocorids
especially early in spring. To sustain anthocorids and other beneficials, hedgerows must
meet their dietary needs. Alternative, early season prey (e.g. psyllids, aphids and gall
midge larvae) must be provided. Rieux et al. (1999) showed that ash trees host specific
psyllids and gall midges that provide food and shelter for anthocorids. Solomon et al.
(1999) showed that various herbaceous flowering plants attract anthocorids and can be
used to enhance predator populations in orchards.
In 2008, the first year of the project, existing mature plant species diverse
hedgerows/windbreaks and the pear orchards which they surrounded were beat-
sampled through the season to identify which tree and herbaceous plant species are
good sources of anthocorids early in the season. Predator communities, especially
anthocorids, and key prey species present on them were characterised. A data base of
>30,000 specimens was collected and identified to species, a huge task.
Cacopsylla pyri L. was found to be the dominant (> 90%) pear sucker species
present at two sites. Cacopsylla pyricola Förster was the dominant species at the other
site. Both species occurred at all 3 sites. When the species compositions were last
characterised in the 1980s, C. pyricola was universally the dominant species in the UK.
23 Jerry Cross
This finding could have important implications for the management of pear sucker in
commercial orchards in the UK. Cacopsylla melanoneura (Förster) (from hawthorn) was
also present on pear in moderate numbers and Cacopsylla brunneipennis (Edwards) in
small numbers. Cacopsylla adults are identified by their genitalia.
A. nemoralis, as had previously been demonstrated, was the dominant anthocorid
predator of pear sucker. It is adapted to feed on psyllids (eggs and nymphs). A.
nemorum also occurred on pear, particularly later in the season, but it comprised at
most 30% of the total population. A. nemorum is adapted to feed on aphids, which
are more numerous later in the season. Psyllid larvae, on which A. nemoralis feeds,
were found to be more numerous on trees very early in the season with egg laying and
nymphs occurring from February onwards. Aphids become more numerous later in the
season (May onwards) with a population crash or moving to a secondary host in July.
Plant species that have psyllid nymphs early in the season (February – April)
were shown to be most likely to support A. nemoralis early in the season and be good
sources of anthocorid predators for pear sucker. During the early season, the highest
numbers of anthocorids were found on hawthorn (Crataegus monogyna Jacq.), goat
(pussy) willow (Salix caprea L.), grey willow (Salix cinerea L.) and nettle (U. dioica). The
results indicated that these species are good candidates for fostering early season A.
nemoralis. However, hawthorn is not a favoured choice because it is susceptible to
fireblight (Erwinia amylovora Burrill), a serious bacterial disease of pears.
Tree species that support aphids potentially provide large numbers of A. nemorum
later in the season. In comparison with psyllids, aphids tended to become more
numerous later in the season (May onwards) with a population crash or moving to a
secondary host in July. The highest numbers of aphids were found on field maple (Acer
campestre L.), sycamore (Acer pseudoplatanus L.), downy birch (Betula pubescens
Ehrh.), hazel (Corylus avellana L.), blackthorn (Prunus spinosa L.), white willow (Salix
alba L.) and grey willow (S. cinerea). Though birch and sycamore supported high
numbers of aphids, they had few anthocorids, perhaps because the aphids were not
good prey being ‘bad tasting’ or being too large and aggressive. Hazel was particularly
abundant in aphids and had higher numbers of anthocorids. Inclusion of hazel would
be beneficial as a source of late season A. nemorum. In parallel work on apple,
Sigsgaard and Kollmann (2007) showed that hedgerows containing flowering hawthorn
or elderberry (Sambucus nigra L.) and herbaceous layers with stinging nettle (U. dioica)
held high numbers of anthocorids in spring. Though pollen and sucrose diets were
inferior to arthropod diets, anthocorid nymphs could survive for over a month on them
when prey is temporarily scarce.
Nettle, goat willow (S. caprea), grey willow (S. cinerea) and hazel (C. avellana)
appear to have high potential for conservation biocontrol for pear sucker.
Nettle has previously been found to harbour high populations of anthocorids in
spring. The nettle aphid (Microlophium carnosum (Buckton)) (Perrin, 1975; Nguyen and
Merzoug, 1994) (Figure 11) is often very abundant providing prey for both anthocorid
species, but especially A. nemorum. Nettle is also host to the nettle psyllid Trioza urticae
(Linné), which we found was abundant throughout the year in the adult stage. The
nymphs are very flat and strongly attached to the plant and are not collected by sweep
sampling. Nettle is thus also a good source of A. nemorolis which prefers feeding on
psyllids. Nettles are thus an excellent source in general of anthocorids (Figure 11).
Goat and grey willow are hosts to high numbers of their associated psyllids
Cacopsylla ambigua Förster and C. brunneipennis at the critical time early in the season
as well as to several other psyllid species and these willows are particularly good early
sources of A. nemoralis. Aphids and leaf feeding spider mites are also abundant later
in the season providing a rich and varied food source for Anthocoris sp. throughout the
season. Previous research has shown that early in the season, anthocorids concentrate
on S. caprea when willow is flowering (Figure 11). Both A. nemorum and A. nemoralis
occur on it in very large numbers (Sands, 1957; Hill, 1957; Anderson, 1962). The
flowering period is very early, usually late March or early April, and anthocorids leave
the catkins after only a week or so. These willows are also host to a number of mirids
including Deraeocoris lutescens (Schilling), Malacocoris chlorizans (Panzer), Orthotylus
marginalis Reuter and Psallus sp. with which anthocorids may compete.
Aphids (Myzocallis sp.) are abundant on hazel in early and mid- summer and
appear to be a good food source for A. nemorum. Several other tree species native to
the UK are known to host large numbers of aphids (e.g. Betula and Tilia sp.) but these
do not appear to be good food sources for Anthocoris sp.
To summarise, the first years work indicated that goat willow, hazel and stinging
nettle have the greatest potential for conservation biocontrol of pear sucker of the large
number of species surveyed. Alders and especially Italian alder, the main windbreak
species, were found to be poor hosts of aphids and psyllids and were poor potential
sources of anthocorids.
In 2009, ongoing work is investigating these three species in more detail studying
the dynamics of the prey and anthocorids through the season and investigating the
extent to which competing predatory heteroptera influence their suitability for pear
sucker conservation biocontrol. Future work in the project will investigate whether
timely trimming of hedgerows and/ or their nettle understory can be used to manage a
timely anthocorid influx into adjacent pear orchards.
25 Jerry Cross
a) b)
c) d)
e) f)
Figure 11. Stinging nettle (Urtica dioica), goat willow (Salix caprea) and grey willow (Salix cinerea) are
excellent subjects for conservation biocontrol of pear sucker (Cacopsylla sp.). Nettle (a) supports large
numbers of the nettle aphid (Microlophium carnosum) (b) and the nettle psyllid (Trioza urticae) (c).
The willows have early season catkins (pussies) (d) which provide early sources of pollen and nectar,
large numbers of early season psyllids including Cacopsylla ambigua (e), and aphids (f) and the spider
mite Eotetranychus populi (Koch) later in the season. These are excellent alternative food sources
for Anthocoris sp., the pear sucker’s key natural enemies. Photo b) courtsey of Kim Taylor, Warren
Photographic. Photos c) and e) courtesy of Joseph Botting (www.britishbugs.org.uk).
2.4.2. 21st century perspectives

The work described above can only be regarded as scratching the surface of the
enormous potential of conservation biocontrol in UK horticulture. Careful choice of
hedgerow species may have substantive benefits for many other pests of fruit and
other horticultural crops. Obvious targets are the common European earwig (Forficula
auricularia L.) for woolly aphid (Eriosoma lanigerum (Hausmann)) and other aphids,
ground beetles and other predators for vine weevil (Otiorhynchus sulcatus (Fabricius))
and pirate bugs (Orius sp.) for western flower thrips (Frankliniella occidentatlis
(Pergande)) though there are numerous other possibilities. It would seem important
when embarking on research to have clear targets in mind rather than to search
haphazardly for favourable interactions but detailed investigation of the arthropod
communities on herbaceous plants and native tree and hedgerow species would
probably point to numerous opportunities. Practical considerations, such as easy
agronomy, durability, availability and costs are most important and a large proportion of
subjects can probably be ruled out at the outset, even more if subjects known to host
important pests or diseases are excluded.
3. Deciding if and when to treat

Deciding if and when to treat e.g. with pesticide sprays, is vital to rational and effective
pest management. Monitoring in IPM can be used to determine the geographical
distribution of pests or assess the effectiveness of control measures but in its widest
sense monitoring is the process of measuring the variables for the development and use
of forecasts to predict pest outbreaks (Conway, 1984). Predictions of pest outbreaks
or damage provide a warning of the timing and extent of pest attack and are essential
to deciding if and when to treat with pesticides or other control measures. Central to
any insect pest monitoring programme are the sampling techniques used to measure
changes in insect abundance and the damage or action thresholds used to interpret
them which together provide the essential measures by which control decisions should
be made.
Pest monitoring is a huge subject involving diverse methods. Here, a much narrower
focus on the use of physical and semiochemical monitoring traps and forecasting models
developed in recent research at EMR, much of it involving essential, close and excellent
collaboration with Professor David Hall and his colleagues Chemical Ecology Group,
NRI, University of Greenwich. The examples presented have proved transformative in
the understanding or management of their target pests, and/or represent internationally
significant scientific breakthroughs or achievements.
Traps potentially provide a relatively quick, easy and sensitive way for monitoring
pest populations and are preferable to population surveys by beat sampling or visual
inspection which are time-consuming and not favoured by growers. Most traps provide
only relative estimates and are prone to changes in environmental conditions, with
the consequence that the data collected on different occasions may not be strictly
comparable unless conditions have remained static. However, this major drawback is
compensated for by the fact that traps are generally operated over extended periods
and are usually used to provide total, integrated catches over extended periods of
several days, a week or longer periods.
27 Jerry Cross
3.1. Physically-acting monitoring traps

Physically-acting monitoring traps mainly use physical stimuli to attract target pests.
Coloured sticky traps are used effectively for many pests e.g. non-UV reflective white
sticky traps are used to monitor populations of apple sawfly (Hoplocampa testudinea
(Klug)) during blossom of apple and blue sticky traps are used to monitor populations of
western flower thrips (Frankliniella occidentalis (Pergande)) in a wide range of protected
horticultural crops in the UK. Unless there is an attraction component, physical traps
are usually insufficiently sensitive to catch sufficient pest numbers to be useful for
pest monitoring. Furthermore, yellow and white sticky traps are notoriously non-
selective, trapping large numbers of non-target arthropods such as honey bees (Apis
mellifera L.) and bumble bees (Bombus sp.). Here two examples of physically acting
monitoring traps without an attractive component, for mussel scale (Lepidosaphes ulmi
(L.)) and blackcurrant gall mite (Cecidophyopsis ribis (Westwood)), developed at EMR
are described (in sections 3.1.1 and 3.3.1, respectively). They both rely on trapping
individuals as they emerge from a point source or sources.
3.1.1. Mussel scale

Mussel scale (L. ulmi) is a common pest of apple (and sometimes pear) in the UK, and
has become more prevalent in recent years since the demise of winter tar oil wash
treatments. Populations on hawthorn and other wild plants are believed to be the main
sources of infestation of orchards. Adult female mussel scale are 2.0-3.5 mm long, flat
and mussel shell–shaped, grey to yellowish-brown in colour. They are found on the bark
and fruits of apple trees. The nymphs, known as crawlers in the first instar stage, are
oval and pale yellowish-brown. The eggs are minute, oval and white and are protected
beneath the scale. The main damage is caused by the presence of mussel scales on
the surface of fruits at harvest. The contamination is superficial but may downgrade
the fruit. Very heavy infestations on the bark may debilitate the tree and contaminate
the foliage and fruit with honeydew which becomes unsightly with the growth of sooty
mould.
Mussel scale is univoltine. The first eggs hatch in late April and the first stage
crawlers, wander over the host plant settling on the bark and, sometimes, on the
developing fruit. Each crawler moults to a second, then a third instar nymph, both stages
being sedentary and remaining in the same place, protected by the mussel-shaped
scale formed from wax and the cast nymphal skin. In late August and September, each
female lays up to 80 eggs beneath the scale, and then dies. The scale remains attached
to the bark and protects the eggs through the winter. Although males appear in some
races of mussel scale, only females occur on fruit crops and reproduction is entirely
parthenogenetic.
Traditional wisdom suggested that a mass hatch of the eggs of mussel scale
occurred in a short time period of a few days in late May or June and that insecticide
sprays needed to be targeted in this short time period against the young crawlers when
they emerge because more mature larvae are protected by their outer scale and are
much less susceptible to insecticides. For this reason, pinpointing the timing of the
mass hatch was considered vital to time sprays correctly.
Helsen et al. (1996) developed a temperature sum simulation model for the timing
of emergence of mussel scale crawlers in the Netherlands based on lab studies of the
timing of emergence from infested shoots held in constant temperature incubators in
the laboratory. The model was validated against 14 years of field observation data.
It forecast first emergence of crawlers to occur at 151 Day Degrees > 8 ºC (after 1
January), 90% emergence at 229 Day Degrees > 8 ºC (after 1 January). Mass egg
hatch was predicted to occur at about 190 Day Degrees, 90% hatch to occur at 230
Day Degrees. 90% hatch was considered to be the optimum timing for application of
commonly used pesticides. Early hatched nymphs may reach the second instar stage
by this time, but these are still susceptible to the commonly used insecticides.
A number of insecticides, approved for the control of other pests on top fruit,
have been used for mussel scale control with varying degrees of success by UK
apple growers. These include thiacloprid (Calypso), acetamiprid (Gazelle), fenoxycarb
(Insegar), chlorpyrifos (Equity etc.), and the synthetic pyrethroids cypermethrin (Toppel
10 etc.) and deltamethrin (Decis etc.). The use of synthetic pyrethroid insecticides is
usually avoided because they are harmful to the orchard predatory mite, T. pyri. For
growing season sprays, medium to high volume spraying is important to obtain good
cover.
Our work in 2007-2009, funded initially by HDC tree fruit panel, completely
overturned this view of how mussel scale should be controlled and provides an excellent
illustration of how emergence monitoring traps are invaluable in pest management.
We used sticky bands made of double-sided sellotape wrapped round the
branches of infested trees to monitor the emergence and dispersal of the mussel scale
crawlers. The bands were deployed in early April and monitored twice weekly till the
emergence had ceased in July. The double sided tape proved to be a good choice.
The crawlers, dispersing in both directions, avoided walking over it and attempted to
pass under it in places where there was an opening between the edge of the tape and
the irregular rough tree bark. Once underneath they became trapped (Figure 12). The
counts gave excellent data on the progress of the migration, which turned out to follow
a very different pattern to that previously believed.
Mussel scale emergence and dispersal followed a similar pattern in each of the
three years (Figure 13). However, the timing of the migration varied by about 2 weeks,
with first emergence on 23 April, 6 May and 27 April in the three years respectively. The
main period of emergence and dispersal lasted for about a month with small numbers
continuing to be captured for up to 9 weeks, far longer than been thought previously.
Interestingly, in all three years the emergence/dispersal showed a strongly bimodal
pattern. The cause of this is not known but it does not appear to have been caused by
weather conditions (rainfall or cold periods during migration).
29 Jerry Cross
Figure 12. Sticky band trap round trunk of tree to monitor numbers of migrating mussel scale
crawlers, which can be seen in large numbers
Figure 13. Mean numbers of mussel scale crawlers captured cm-1 of sticky band per day in
2007, 2008 and 2009
31 Jerry Cross
Temperature loggers were deployed to take hourly readings of air temperatures.

Day degree sums > 8 ºC after the 1 January were calculated from daily maximum
and minimum temperature readings, calculated using the triangulation method. The
temperature sums at the observed dates of emergence were compared with the
temperature sum predictions of the Dutch model. The accuracy of the model predictions
was erratic being incorrect by -7 to +18 days (Table 1), demonstrating the value of the
sticky bands for quantifying the time and magnitude of the emergence.
In parallel, we carried out replicated trials examining the efficacy of sprays of
different insecticides at different times during the migration. This work clearly showed
that sprays of neonicotinoid insecticides such as thiacloprid (Calypso) and acetamiprid
(Gazelle) were highly effective for control of mussel scale and the best time to apply
them, for a single spray, was at 90% crawler emergence. Where two sprays were
applied, e.g. for a high degree of control of heavy infestations, the best timings were at
50 and 90% emergence.
This work has transformed our understanding of best practice for mussel scale
control.
Table 1. Dates of first, 50% and 90% mussel scale emergence predicted by the temperature
sum model of Helsen et al. (1996) and observed dates from records of numbers captured in
sticky bands in 2007 and 2008
3.2. Semiochemical monitoring traps

Semiochemicals (Gk. semeon , a signal) are chemicals that mediate interactions
between organisms. Semiochemicals are subdivided into pheromones and
allelochemicals, depending on whether the interactions are intraspecific or interspecific,
respectively. Pheromones (Gk. phereum , to carry; horman , to excite or
stimulate) are released by one member of a species to cause a specific interaction with
another member of the same species. Pheromones may be further classified on the
basis of the interaction mediated, such as alarm, aggregation or sex pheromones. To
date sex pheromones of insects have been the subject of the bulk of semiochemical
research and are the most widely used in management of horticultural pests. The two
primary uses of insect pheromones are for detection and monitoring of populations and
for control by mating disruption, attract and kill or mass trapping. One of their limitations
is that sex pheromones are mainly emitted by females to attract males. Females are
unaffected directly, but it is the females that lay eggs and are thus the damaging sex.
Sex pheromone catches of males may not accurately reflect female or reproductive
activity and it may be difficult to significantly reduce the proportion of fertilised females
unless a very large proportion of males are prevented from mating.
Allelochemicals, are chemicals that are significant to individuals of a species different

from the source species. They are subdivided into three sub-groups depending on
whether the response of the receiver is adaptively favourable to the emitter but not the
receiver (allomones), is favourable to the receiver but not the emitter (kairomones) or is
favourable to both emitter and receiver (synomones). Host plant volatiles have a special
role in the management of horticultural pests because they can act as allelochemicals
in any of the three sub-groups, depending on the pest host plant interaction. Host plant
volatiles can be attractants in their own right. They are used by female insects to find
a host plant for ovipostion after mating and in some cases it has proved possible to
use host volatiles to attract females for monitoring purposes, though a major limitation
is that the host volatile attractants have to compete with large amounts of the same
substances produced by the host crop. However, in some insects the activity of
pheromones is greatly enhanced by host volatiles
Though perhaps the majority of insect pests rely on sex pheromones and
other semiochemicals to mediate reproduction, to date only the sex pheromones
of lepidopteran pests have been exploited to a significant extent in UK horticulture
and even for these exploitation is limited. The sex pheromones of practically every
lepidopteran horticultural pest have already been identified and are commercially
available. Sex pheromone traps have been widely used for monitoring moth pests in
orchards, especially of codling moth (C. pomonella), fruit tree tortrix moth (Archips
podana (Scolopi)) and summer fruit tortrix moth (Adoxophyes orana (Fischer von
Röslerstamm)) since the 1960s.
On 5 November 1997, a close collaboration between the Horticultural Entomology
Team at East Malling Research and the Chemical Ecology Group of the Natural Resources
Institute, University of Greenwich, lead by Prof. David Hall, was started with the primary
aim of identifying and exploiting the sex pheromones and other semiochemicals of UK
non-lepidopteran fruit pests. The sex pheromones of many of these important pests
were known to exist and pheromones of related species which were pests in other crops
in other continents, had already been identified. Synergising the pheromones with host
plant volatiles was an important quest. This close and fruitful collaboration between the
two teams lead to a number of breakthroughs of international significance, including
semiochemical monitoring systems for strawberry blossom weevil (Anthonomus rubi
(Herbst)), gall midges and capsid bugs as briefly described here. The first step was to
identify, synthesise and demonstrate the attractants then develop practical lures and
traps then calibrate them to establish thresholds for pest monitoring purposes.
3.2.1. Gall midge sex pheromone monitoring traps

Many horticultural crops, especially perennial fruit crops, are subject to pest attack
by various species of plant feeding gall midges (Cecidomyiidae). Some species such
as raspberry cane midge (Resseliella theobaldi (Barnes)) and blackcurrant leaf midge
(D.tetensi) are controlled currently with the broad-spectrum organophosphate (OP)
chlorpyrifos or with pyrethroid insecticides but use of these insecticides is undesirable
because they are harmful or toxic and because they disrupt Integrated Pest Management.
Methods for deciding when and where to spray were unsatisfactory and there was
widespread unnecessary and sometimes ineffective treatment. For other species, such
as the apple and pear leaf midges, there were no effective control methods and they
caused extensive damage, especially in nurseries and young orchards. Effective pest
monitoring and alternative, non-pesticidal control methods needed to be identified.
33 Jerry Cross
Plant-feeding midges are typically very short-lived as adults and highly specific
for their host-crop. In several species there was evidence for production of highly
potent sex pheromones by virgin female adults and strong attraction of mated females
to volatiles from host plants (Harris and Foster, 1999). Prior to our work, the chemical
structures of the components of the female-produced sex pheromones have been
identified from several species including: Hessian fly, Mayetolia destructor (Say)
(Foster et al., 1991), pea midge, Contarinia pisi (Winnertz) (Hillbur et al., 1999, 2000,
2001), orange wheat blossom midge, Sitodiplosis mosellana (Géhin) (Gries et al.,
2000), Douglas-fir cone gall midge, Contarinia oregonensis Foote (Gries et al., 2002),
aphidophagous gall midge, Aphidoletes aphidimyza (Choi et al., 2004) and swede
midge, Contarinia nasturtii (Kieffer) (Hillbur et al., 2005). The chemical structures of
these pheromones are related to each other, having carbon chains with an odd number
of carbon atoms and one or two ester functionalities.
However, we wanted to identify the sex pheromones of gall midges that were
important pests of UK fruit crops. Our first challenge was to identify the sex pheromone
of the apple leaf midge, Dasineura mali Kieffer, a pest of apples in Europe, North
America and New Zealand which is widespread and abundant in the UK and which
is damaging in nurseries and newly planted or re-grafted orchards. Identification of
the pheromone had proved extremely challenging due to the very small amounts of
chemical involved and the difficulties of carrying out laboratory bioassays with the
small and delicate insects. Stephen Foster and Marion Harris of the Horticulture and
Food Research Institute of New Zealand spent over five years trying to identify this
pheromone but never obtained enough material for the structure elucidation (Harris
et al., 1996, 1999). Jeremy Heath of the Atlantic Food and Horticulture Research
Centre, Nova Scotia, Canada, similarly demonstrated attraction of males by females
in a laboratory bioassay but was unable to isolate and identify the pheromone (Heath
et al., 1998, 2005). Wendell Roelofs (Cornell University, USA) reported obtaining an
EAG response from a male apple leaf midge in linked GC-EAG analyses of pheromone
collected on an SPME fibre at a meeting in 1998.
In view of the difficulties encountered by other highly experienced chemical
ecologists, we decided to concentrate on collecting pheromone volatiles from a large
number of males and females using the air entrainment method to maximise the
amount of pheromone collected and minimise impurities. We collected volatiles from
over 2,000 virgin female midges which proved more effective than gland extraction
methods used previously. Analysis of collections by gas chromatography (GC) coupled
to electroantennographic (EAG) recording from the antenna of a male midge antenna
showed a single active component which was not present in similar collections from virgin
male midges and was assumed to be the sex pheromone. Although this was present
at less than 20 pg per female, mass spectra were obtained and the compound was
identified as (Z)-13-acetoxy-8-heptadecen-2-one by comparison of GC retention times
and mass spectra with those of synthetic standards and microanalytical reactions. The
synthetic compound had GC and MS data identical with those of the natural compound
and elicited a strong EAG response from a male D. mali midge. A convenient route
was developed for synthesis of the compound giving 63% yield in eight steps. The
two enantiomers of the compound were separated and isolated by high performance
liquid chromatography on a chiral column. The first-eluting enantiomer was predicted
to be the S enantiomer by nuclear magnetic resonance spectroscopy of the (R)-2-
methoxy-2-trifluoromethyl-2-phenylacetyl esters. This work is reported by Cross and
Hall (2005) and Hall and Cross (2006). The main reason why we were successful where
others failed was because entomologists, electrophysiologists, analytical and synthesis
chemists with the necessary skills from EMR and NRI worked together in a team rather
than working in isolation.
The pheromone racemate was found to be highly attractive to male apple leaf midge
in the field with rubber septa lures containing 1 μg being significantly attractive. Only
one enantiomer of the pheromone, probably that with S configuration, was attractive,
but the racemic mixture was equally attractive, the latter being much more economic
and easier to synthesise. A series of replicated field experiments was carried out during
2004–2006 to develop an optimised pheromone trap system for monitoring populations
of D. mali in commercial orchards (Cross et al., 2009a; Cross and Hall, 2009). With
rubber septum dispensers, numbers of midges caught increased with increase in
loading of pheromone over the range tested from 1 μg to 100 μg and a loading of 3 μg
was found to be suitable for pest monitoring purposes. Polyethylene vial dispensers
were unattractive during these tests. Release rate studies in the laboratory showed
reasonably uniform release of pheromone from the septa for at least 574 days at 27 ˚C
and 8 km/h wind speed. With the vials there was a delay of 10 days before the start of
release of pheromone under these conditions. Funnel, bottle, Petri dish, delta and dish
traps all caught midges, those with the larger catching surfaces being more sensitive.
In practice, it was concluded that the standard delta trap is the best design for use by
growers. The colour of the trap had no effect on attractiveness to D. mali males, but
catches of non-target arthropods in red, green and black traps were significantly lower
than in white, yellow or blue traps. The red traps are recommended for use by growers.
Numbers of male midges caught were greatest in traps at ground level and decreased
strongly with increasing height of trap deployment. A standard deployment height of
0.5 m was chosen. Males were attracted to traps over a distance of at least 50 m from
an infested orchard. They showed a strong diurnal pattern of flight activity. Numbers
caught rose steeply in the morning starting at 07:00 h (2 h after dawn), reached a peak
at 09:00 h and steadily declined throughout the day thereafter. Conversely, numbers of
ovipositing females were very low at 09:00 h but increased steadily, reaching a peak at
11:00–12:00 h and declining thereafter.
We then investigated of the use of the standard apple leaf midge sex pheromone
trap for pest monitoring (Cross et al., 2009a). Early monitoring using pheromone traps
is a useful strategy for predicting damage and timing sprays (Jones, 1998). The traps
were deployed in commercial orchards in England, Italy and New Zealand over two
seasons and the timing of generations and the relationships between trap catches and
galling damage were investigated to calibrate the traps in order to aid interpretation of
catches.
Catches of D. mali in sex pheromone traps and subsequent galling damage to
shoots over four successive midge generations per season were investigated during
2004 and 2005 in apple orchards in Kent, south eastern England, Trentino, northern
Italy and South Island, New Zealand. The orchards were newly planted or established,
had widely varying apple leaf midge populations and were subjected to different
pesticide management regimes. The Julian date of the peak catch of midges in the sex
pheromone traps increased approximately linearly with increasing generation number.
There was also a strong increasing relationship between the Julian date of peak catch
and increasing absolute value of latitude. A linear relationship was fitted within the
range of 41 –51 degrees latitude included.
35 Jerry Cross
Strong linear relationships on log-log transformed scales were found between the
total and peak numbers of midges caught per generation and the populations of galls
that developed subsequently (Figure 14). The best fit of log10(total galls/ha) = 2.138
+ log10(total no. midges caught/generation) was obtained for the first and second
generations. The relationship indicates that each male midge caught in a trap for a
particular generation corresponds to approximately 137 galls being formed per hectare
subsequently for that generation, providing that there are sufficient shoots and tender
young leaves present to accommodate them.
Figure 14. Relationship between total catch per generation of first or second generation apple
leaf midge males in standard sex pheromone traps and the number of galls formed per ha for
that generation subsequently. Best fit linear regressions on a log-log scale through the origin
(dashed line) or unconstrained (solid line) are included
Clearly the proportion of shoots and leaves galled per hectare will depend on the
numbers of shoots and leaves present in the particular orchard but knowledge of these
parameters should allow simple estimates to be made. The regressions were significantly
weakened when the third and especially the fourth generations were included, largely
because of gall saturation or because tree growth had ceased. The relationships were
not significantly affected by pesticide management regime, orchard age or country of
location. In a further study, a good correspondence was found between pheromone
trap catches and the percentage of shoots infested with eggs of D. mali for the first and
second generation in an experimental orchard in Kent during 2006.
The results indicated that the sex pheromone traps are effective for monitoring the
flight activity of successive generations of D. mali, can be used to predict the severity of
galling attacks to shoots and recently we have shown that the D. mali sex pheromone
trap is valuable for timing insecticide sprays (Hall and Cross, 2006).
Following this first success we used similar methods to identify the sex pheromones
of most of the other economically important midge pests of fruit crops. The identification
of the sex pheromone of the raspberry cane midge (R. theobaldi) was completed
shortly after D. mali. (Hall et al., 2009). In subsequent work we showed good linear
relationships between sex pheromone trap catches of this species and the numbers of
larvae infesting splits in raspberry canes (Cross et al., 2008). Lakmali Amarawardana
has just completed her 3 year PhD at the University of Greenwich studying the
chemical diversity of midge pheromones where she identified the sex pheromones of
pear leaf midge (Dasineura pyri (Bouché), pear midge (Contarinia pyrivora (Riley)) and
blackcurrant leaf midge (D. tetensi) as well as partially identifying the sex pheromone of
the blackberry leaf midge (Dasineura plicatrix (Loew)) (Amarawardana, 2009). Attractive
sex pheromone monitoring traps will transform the management of these pests.
3.2.2. Capsid bug sex pheromone monitoring traps

Capsid bugs (Heteroptera, Miridae, Mirinae) are common and important pests of many
horticultural and some agricultural crops world wide. Three of the most important
species in the UK are the European tarnished plant bug, Lygus rugulipennis Poppius,
the common green capsid, Lygocoris pabulinus (L.), and the nettle capsid, Liocoris
tripustulatus (Fabricius) (Jacobson and Hargreaves, 1996; Jacobson, 1999, 2001, 2002;
Jay et al., 2004; Cross, 2004). In late season strawberry crops L. rugulipennis is a most
important pest requiring almost routine treatement with broad-spectrum insecticides
in mid and late summer. Feeding in flowers and on green fruits can cause up to 80%
crop loss, rendering production uneconomic (Cross, 2004). The economic threshold for
L. rugulipennis has been estimated as 1 capsid per 40 plants, a very low level which is
difficult to detect by visual insepection (Jay et al., 2004). L. rugulipennis causes similar
damage in raspberry as in strawberry and L. pabulinus is a frequent pest killing fruiting
laterals (Cross, 2004). On apple and pear, L. pabulinus is an important but sporadic pest
requiring treatment with broad-spectrum insecticides at petal fall. The fruit is attacked
directly, and economically significant losses occur at population densities as low as
one infested shoot per 6 trees (Bus et al., 1995). Worst case attacks reported are 50%
and 33% fruit losses on apple and pear respectively (Umpelby et al.,1995). L. pabulinus
is also a damaging pest of blackcurrant, attacking the shoots in spring and summer. It
is controlled by routine sprays of synethetic pyrethroids or chlorpyrifos to control other
pests, but a reduction in the use of broad-spectrum insecticides in IPM programmes is
causing a resurgence of the pest.
In conventional crops capsids are controlled by sprays of broad-spectrum
insecticides, organophosphorus insecticides being the most effective and frequently
used. Neonicotinoids and other modern insecticide groups are only partially effective
against capsids and insect growth regulators are totally ineffective. Application of
broad-spectrum pesticides to control L. rugulipennis is an important barrier to the
implementation of biocontrol in strawberries. In organic crops they cause high levels
of damage because insecticides available are inadequate and of short persistence.
37 Jerry Cross
Capsids have few natural enemies and effective biocontrol methods have not been
developed for them. They present a bottle neck in the development of IPM programmes.
Crop invasion by capsids is sporadic and unpredictable, and, in the absence of effective
control measures, capsid bugs cause severe economic losses. They cause damage
at low population densities and are difficult to detect at such levels in normal crop
inspections. Bug sampling methods (sweep-net or beating-tray sampling) are time
consuming and unsuitable for use by growers. The importance of capsid pests is likely
to increase, as has already been noticed in other northern European countries.
The family Miridae contains about 10,000 species worldwide, making it the largest
Heteropteran family. Several species of capsids have been shown to produce sex
pheromones. Thus traps baited with virgin females of both L. rugulipennis (Innocenzi
et al., 1998; Glinwood et al., 2003) and L. pabulinus (Blommers et al., 1988) have been
shown to attract conspecific males. During 30 years of work in the USA and Canada
on the sex pheromones of congeners of the UK species, Lygus lineolaris (Palisot de
Beauvois) (Gueldner and Parrot, 1978; Aldrich, 1988; Wardle et al., 2003) and Lygus
hesperus (Knight) (Ho and Millar, 2002), several potential pheromone components were
identified but attraction to a synthetic lure was never shown. Until recently attraction
to synthetic pheromone lures has been demonstrated in only seven mirid species
belonging to different genera, i.e. Camplyomma verbasci (Meyer) (Smith et al., 1991),
Phytocoris relativus Knight (Millar et al., 1997), P. californicus Knight (Millar and Rice,
1998), P. difficilis Knight (Zhang et al., 2003), P. breviusculus Reuter (Zhang et al., 2003),
Trigonotylus caelestialium (Kirkaldy) (Kakizaki and Sugie, 2001), Distantiella theobroma
(Dist.) and Sahlbergella singularis Haglund (Downham et al., 2002). Sex pheromone
identification in capsid and related bugs has been hampered by the abundant
defensive secretions, present in the metathoracic scent gland, that are released upon
disturbance (Aldrich, 1988). Furthermore, in many species it is probable that certain
compounds can function as components both of the pheromone and of defensive
secretions, depending upon the blend and concentration (cf. Blum, 1981, 1996).
EMR and NRI started collaborative work to identify and exploit the sex pheromones
of capsid bugs in 1997 with the appointment of PhD student Paul Innocenzi. Work
started on L. rugulipennis funded by Defra (Project HH1939SSF) (Cross and Hall, 2003)
and HEFCE through a studentship. Three female-specific pheromone components were
identified and synthesised, hexyl butyrate (HB), (E)-2-hexenyl butyrate (E2HB) and the
ketoaldehyde (E)-4-oxo-2-hexenal (KA). However, in initial field trials, traps baited with
blends of these chemicals dispensed from standard pheromone dispensers failed to
catch significant numbers of males (Innocenzi et al., 2004). An important breakthrough
occurred in subsequent field trials by Paul Innocenzi at EMR in which the chemicals
were released from glass micro capillary tubes, as reported by Kakizaki and Sugie
(2001) for another insect pheromone. Different blends of the components were found
to attract L. rugulipennis and its congener Lygus pratensis L.. This was the first time
a Lygus bug pheromone had been identified and attraction in the field demonstrated
(Innocenzi et al., 2005). However, the reason why the pheromone blends are attractive
when dispensed from glass micro-capillaries was not known – for example it may have
been that release rate and/or release from a small point source was critical. Also
release rates from glass-micro capillary dispensers are erratic; they have only a very
short field life and are impractical for operational use.
Further scientific work was needed to understand the mechanisms and

requirements for attraction so that long-lived, practical dispensers can be developed.
Between 1996 and 2000, intensive investigations were undertaken at the University of
Wageningen, The Netherlands, to identify the sex pheromone of L. pabulinus (Drifout,
2001; Groot, 2000). Both female and male bugs were shown to produce hexyl butyrate,
(E)-2-hexenyl butyrate and (E)-4-oxo-2-hexenal, the same compounds identified from
females only in L. rugulipennis (Drijfhout et al., 2000). These compounds caused
electroantennogram responses from antennae of males but not from those of females
(Drijfhout et al., 2002). Although these compounds were proposed to be components
of the female sex pheromone, no attraction of males could be demonstrated in
laboratory or field when they were dispensed in various blends and release rates from
standard pheromone dispensers (Groot, 2000). Groot et al. (2001) reported that hexyl
butyrate inhibited pheromone release by the females. Groot et al. (1999) showed that
the antennae of both male and female L. pabulinus were stimulated by synthetic plant
volatiles.
The Dutch workers also showed that compounds on the legs of female L. pabulinus
caused the males to vibrate their abdomens when presented at short-range (Drijfhout
and Groot, 2001). (Z)-7-pentacosene and (Z)-9-pentacosene were shown to be present
in the cuticle of the legs and to cause some abdominal vibration by the males (Drijfhout
and Groot, 2001; Drijfhout et al., 2003). However, the significance of this vibration is
unknown and it is unlikely that the chemicals can be put to any practical use because
they are of very low volatility only effective over very short range or on contact. Conti et
al. (2006) reported results of wind tunnel bioassays with L. rugulipennis which indicated
rather complex responses of the two sexes to undamaged bean plants and to plants
damaged by feeding of the capsids with and without the insects. They listed five
components of host-plant volatiles for which release from the plant was increased by
feeding and also reported that pheromone production by females was increased when
they were feeding.
In 2007 we started a new ongoing collaborative project funded under the
Horticulture LINK scheme (project HL0184). We have made spectacular further progress
in our understanding of capsid pheromone systems and have developed effective lures
and traps for two species, L rugulipennis and L. pratensis. This has been the result of
excellent and dedicated work by Michelle Fountain and David Hall.
Based on volatile collections (entrainment) from females at different times of
day (morning, daytime, evening, night) we have shown that single females of the four
different species we have been studying (L. rugulipennis, L. pratensis, L. pabulinus
and L. tripustulatus) all produce different ratios of the same three compounds, hexyl
butyrate, (E)-2-hexenyl butyrate and (E)-4-oxo-2-hexenal. The ratios are very different
from those we obtained in our original work and which proved unattractive. For these
collection was made over long periods throughout the whole day/night cycle from
groups of insects including ones that died in the apparatus. It appears that at times
of day when they are not calling and when females are in groups, they produce the
same compounds for defensive purposes in different amounts and ratios from the
ratios used for sexual attraction. It also appears that dead and dying insects produce
large amounts of these compounds from their metathoracic glands. These factors
have distorted the ratios in our collections from those that are used by the insects for
sexual attraction and the realisation of this has allowed us to overcome the problem
and determine the correct ratios for sexual attraction. We have good evidence that
39 Jerry Cross
species specificity of sex attraction for this group of insects is based on different ratios
of these three compounds, plus other factors such as time of day of attraction and
possibly host plant. Indeed, it has been known for some time that there is some cross-
attraction between some Lygus species. Wardle and Borden (2003) demonstrated that
L. lineolaris females in traps in a weedy fallow field attracted congener species L. shulli
Knight and L. elisus Van Duzee suggesting these species had similar pheromones.
An excellent demonstration of the behavioural response of male L. rugulipennis
to the correct pheromone blend was provided by work by Michelle Fountain with a
piezoelectric pheromone sprayer. She used this device to spray the attractive blend of
the pheromone components in dilute solutions in hexane from a glass micro-capillary
needle in the field. The needle was attached to a piezoelectric disc which vibrated at a
high frequency, volatilizing the liquid which passed through the needle creating a spray
plum of the material being dispensed. The tests were done in the hours after dawn on
sunny days when we had shown that males of L. rugulipennis are attracted to females.
The work was done in a cherry orchard at EMR which had a dense cover of weed host
plants including Matricaria recutita L. and Chenopodium album L. heavily infested with
L. ruguilipennis and L. pratensis growing in the alleyways. Observations were made of
the mirids attracted to the plume which were sexed and identified.
Attraction was clearly demonstrated. There was no clear response to increasing
the release rate (Figure 15) though any affects may have been masked by day-to-day
variability in catches (the results are unreplicated). Many males flew to the source of
release whilst others walked along the needle. Some males sat in the plume with
their antennae raised, but never approached the tip of the needle. This highlights the
intraspecies variation in response and the need to develop an efficient trap design.
Figure 15. Number of male L. rugulipennis attracted to plume of piezoelectric sprayer releasing
the 3 way mix of HB:E2HB:KA at different concentrations and rates. Each histogram bar
represents a single test done in most cases done on different days
A further important advancement has been the development of artificial point source
lures which can release the required correct blends of the three components at a
steady rate over long periods. Although hexyl butyrate and (E)-2-hexenyl butyrate are
chemically stable, compatible and rather similar in their physiochemical properties,
(E)-4-oxo-2-hexenal is unstable in sunlight and has very different physiochemical
properties. Adjusting concentrations of the three components to get the desired
release rate ratios has been challenging. The point source lures are each made from
a polypropylene pipette tip containing a cigarette filter loaded with blend of synthetic
chemicals in sunflower oil pipette onto the filter and sealed at the wide end with a
Teflon-lined metal crimp seal (Figure 16). The pipette tip lures have proved much more
attractive than the glass micro-capillary lures (Figure 17) and provide the basis for a
practical commercial lure for use by growers.
a) b) c)
d) e)
Figure 16. a) Green cross vanes bucket trap with caged virgin female Lygus rugulipennis
as a lure b) Glass micro-capillary dispenser with reservoir c) pipette tip dispensers for L.
rugulipennis pheromone components, the centre and right ones are covered with tape to
prevent UV degradation of the ketoaldehyde component d) pipette tip dispenser deployed in
green cross vane bucker trap e) a male L. rugulipennis approaching the tip of the piezzo-electric
pheromone sprayer emitting a coarse spray of the correct blend of pheromone components
in a hexane solution
41 Jerry Cross
Figure 17. Numbers of male L. pratensis and L. rugulipennis trapped at the strawberry site,
between 29 July – 26 August, using different pheromone dispensers in green cross vane traps
(4 reps; bars with * are significantly different to other bars P<0.05)
Another crucial advancement has been the development of a much more effective
practical trap design. Sticky stake traps were used in the original work where attraction
of L rugulipennis was demonstrated (Innocenzi et al., 2005) but these were of low
efficacy and impractical for use by growers. We have tested a range of other trap
designs and have shown that bucket traps with green cross vanes (Figure 16) give
vastly improved catches compared to delta traps or other designs. Bucket traps with
white cross vanes were less effective and also capture higher numbers of non-target
insects including bees and bumble bees. These can be excluded by place a mesh grid
over the orifice bit this renders the trap ineffective for L. rugulipennis.
Thus we have made important advancement in our understanding of capsid
pheromone systems and have developed effective lures and traps for both L. rugulipennis
and L. pratensis. To date we have not been able to attract either L. pablulinus or L.
tripustulatus using what our entrainment data indicates are the correct blends for these
species. The reason for this is unclear, but it may be that the cross vane trap design we
have been using in our evaluations is inappropriate for these species or perhaps other
factors crucial to short range attraction, such as short range pheromone components
or in the case of nettle capsid host specific plant volatiles, are missing from our lures.
Our work is ongoing to solve these problems and also to calibrate the L. rugulipennis
trap for pest monitoring in commercial strawberry and cucumber crops.
3.2.3. Strawberry blossom weevil aggregation pheromone/host

volatile supertrap
The strawberry blossom weevil (A. rubi) is an important pest of early season strawberries
throughout Western and Central Europe. After laying an egg in an unopened flower
bud, the female walks a few millimetres down the flower stalk and partially severs it with
her rostrum. The flower bud withers and often falls from the plant. The larva develops
within the damaged bud, pupates, and the adult emerges early in summer. The emerged
adults, which are in reproductive diapause, feed in and around the crop for a few
weeks before migrating to overwintering sites. Each female may sever large numbers
of flower buds and damage can be severe. A. rubi is controlled by the application of
broad-spectrum insecticides, such as chlorpyrifos or synthetic pyrethroids, in spring
to kill adults when the flower truss (inflorescence) petioles have partially grown, before
flowering and before significant damage is done. Sprays are often applied routinely or
when the first flower bud severing damage is seen, but it is difficult to quantify the likely
severity of attack by brief visual crop inspection.
The pheromones of other curculionid species had been identified, and several
found to be useful in monitoring and control (Bartelt, 1999). The first PhD student of
the NRI/EMR collaboration, Paul Innocenzi, identified grandlure I, grandlure II and
lavandulol as components of the aggregation pheromone produced by male A. rubi
( Innocenzi et al., 2001). Note: ‘grandlure’ is the name given to four components of
the aggregation pheromone lure of the cotton boll weevil, Anthonomus grandis Boh.
In A rubi, the components occurred naturally in the ratio 1:4:1, respectively, and the
blend of synthetic compounds attracted both male and female weevils to traps in the
field. Germacrene-D, a known volatile from strawberry plants, was also collected in
increased amounts in the presence of pheromone-producing weevils. Innocenzi et al.
(2001) used a simple prototype trap design for initial field evaluation and optimisation
of the pheromone lure. This consisted of a horizontal white plastic board coated with
adhesive on both sides and fixed to the top of a wooden stake. The lure was held on top
in a small cage made from a hair curler. Although this first prototype proved satisfactory
for the purposes of initial testing, no other work had been done to test alternative
trap designs or improve on the prototype design. However, approximately 75% of the
weevils were captured on the lower surface of the prototype trap. Pheromone traps
provide a potentially efficient and practical method for monitoring of A. rubi.
In subsequent collaborative research the first pheromone lure and trap were
developed (Cross et al., 2006a). Low-cost, robust and reliable polyethylene sachet
dispensers containing 100 ml of a blend of grandlures I, II and (±)-lavandulol in the
naturally occurring 1:4:1 ratio were shown to have constant release rates of 0.64 and
0.96 mg/day at 20 and 27 ˚C, respectively and a life of over 8 weeks in the field. Field
experiments showed that increasing the release rate by approximately five times
marginally increased attractiveness but a four times reduction in the release rate
significantly decreased attractiveness. It was concluded that the standard release rate
was satisfactory. Male A. rubi weevils were shown to produce the R-enantiomer of
lavandulol, but it was also demonstrated that the S-enantiomer is not repellent and
that low-cost racemic (±)-lavandulol is equally attractive. Although (-)-germacrene-D
showed a weak synergistic effect when added to the pheromone components,
inclusion in a commercial lure was uneconomic. Further experiments examined the
effect of reducing the amount of grandlure I, a costly chemical, in the blend. In one
43 Jerry Cross
experiment it was found that reducing the amount of grandlure I by a factor of four did
not decrease attractiveness significantly, though the ratio of males to females decreased
significantly. A four fold reduction in grandlure I content gives a 40% reduction in the
cost of the chemicals in the lures. Experiments were carried out to develop an effective
and practical trap design. Various modifications of the sticky board trap used in the
original work were compared with boll weevil, funnel, delta and sticky stake designs.
Most weevils were caught with the sticky stake design, made from a pointed wooden
stake inserted vertically into the ground with a band of polybutene sticker around the
circumference and a plastic board fixed horizontally on top of the stake to provide
protection of the sticky surface from rain. A lure was hung from one corner of the board.
Following optimisation of pheromone lure and trap, the potential of the pheromone
traps for monitoring the pest was investigated (Cross et al., 2006b). Good correlations
were obtained at five sites during two seasons between the cumulative numbers of
weevils and the amount of severing damage on the crop. Early catches of weevils
preceded the first occurrence of damage by at least 1 week in several instances,
providing useful information for timing the application of insecticide sprays against the
adults to prevent occurrence of damage. The number of flowers severed was usually in
the range of 0.5–2.0 times the cumulative number of weevils captured per trap. Adult
weevil catches started at a low level in April or early May with similar numbers of males
and females. The catches showed a marked increase in mid June coinciding with the
emergence of new adults from the damaged flower buds, even though these are in
reproductive diapause. Male weevils predominated in catches beyond this date by a
factor of approximately 2:1.
The A. rubi sticky stake monitoring trap was commercialised by International
Pheromone Systems in 2006. Disappointingly, very few traps were bought and used by
UK growers. The problem was the sticky stake design made the trap difficult to use and
catches of weevils were rather small and failed to impress.
A new collaboration with Atle Wibe, Bioforsk, Norway led to two important new
developments. Investigations by Anna-Karin Borg-Carlson, Group of Ecological
Chemistry, Royal Institute of Technology KTH, Stockholm, had identified a number
of host volatile substances produced by strawberry including one of which was
produced in large amounts by wild strawberry flowers. Field experiments in Norway
in 2007 evaluated the use of this host volatile as a synergist for the A rubi pheromone.
Fortuitously, white cross vane green bucket traps, which were under development
for monitoring raspberry beetle (Byturus tormentosus (Degeer)), by Agrisense BCS
and the Scottish Crop Research Institute, were used. The combination of the A. rubi
pheromone, the wild strawberry flower host volatile, dispensed from polythene vials
and the white cross vane bucket trap proved to be a winner. In one for the first field
tests in Kise, Norway, a heavily infested site, the new traps caught on average > 200
weevils, far higher than had ever been obtained with the pheromone sachet lures and
sticky stake traps. Subsequent collaborative investigations have explore the use of
other host volatiles from strawberry some of which have given marginal benefits
Furthermore, the attractiveness of the strawberry blossom weevil pheromone to
both males and females theoretically made it more likely that the pheromone could be
exploited for control of the pest by mass trapping (see section 5.3.1)
3.3. Predictive models

Predictive models can be very helpful in determining when to spray to control
insect pests or to perform other management practices (see Dent, 1991). Numerous
temperature based phenological models predicting the development stage of a pest
have been developed but there are few useful models predicting the magnitude of
insect populations. The rate of development of most arthropods is proportional to
temperature above a developmental temperature threshold. The relationships between
temperature and development rate have been determined for numerous insects and
threshold temperatures and day-degree sums required for completion of either the
whole life cycle or for some or all of its developmental stages have been derived. These
parameters have been used to develop temperature based phenological forecasting
models for numerous insect pests. The accuracy with which a day-degree model
predicts a biological event will depend on the accuracy of the developmental threshold
and day degree requirement, the type of temperature measure used and the time that the
day-degree accumulation begins (Collier and Finch, 1985). In situations where models
are used to predict development after a period of dormancy or diapause, initiation
times for an accumulation may not be easily defined, and may be arbitrarily chosen
providing the day-degree accumulation before that date is likely to be negligible. It is
clearly preferable to base the starting dates on meaningful biological criteria, but this
cannot always be done.
Although the development data is available for phenological forecasting models for
numerous horticultural pests in the UK, very few models have actually been produced
and made available or used by growers in commercial practice. There are several
reasons for this: Simple general purpose modern software into which development
parameters can be input for successive development stages of a pest has not been
developed. Where models have been produced, in many cases have not been made
available to growers; The gathering of temperature data and loading into the model
and running of the model may be complex, time consuming and require specialist
knowledge; better information may be available from local crop monitoring or trapping
data.
One excellent example where these difficulties have been overcome by our
work was the development of a model predicting the emergence of blackcurrant gall
mite from galls in spring which is now used universally by UK blackcurrant growers
and which together with identification of sulphur as a safer more effective acaricide,
has transformed management of this most important pest of the crop. Field work
on blackcurrant in our entomology team at East Malling Research is largely done by
Adrian Harris, who is also extensively involved in the practical aspects of our work on
many other crops. Adrian is a dedicated worker with excellent practical skills and has
contributed greatly to our successes.
45 Jerry Cross
3.3.1. Blackcurrant gall mite emergence forecasting model

The blackcurrant gall mite (C. ribis) is the most important pest of commercial
blackcurrant crops world-wide. It is the vector of reversion virus disease, which causes
sterility in blackcurrant bushes, and is the principal factor limiting the life of blackcurrant
plantations. The biology of the mite, its pest and virus vector status and strategies for
control have been reviewed by Gordon et al. (1994). The mite colonises developing
blackcurrant buds in spring and its feeding initiates prolific growth of cells within the
bud resulting in the characteristic ‘big bud’ disorder.
The mites overwinter in the buds mainly as adult females in diapause, galls
typically containing several thousand individuals. Mass emigration of mites from the
gall occurs generally from the end of March until the end of June with a peak in May.
After emergence from the galls, the mites crawl over the gall’s surface and up the stem
moving towards higher light intensities, seeking new buds to infest. Mites arriving near
newly forming buds are attracted to the leaf axils and enter the new bud tissue by
crawling inside the outer scales and continuing to the centre of the bud. However, only
a very small proportion of migrating mites reach their destination. There is very high
mortality, mainly due to desiccation and starvation (Smith, 1961).
Control with acaricides is aimed at preventing successful migration and infestation
of the new axillary buds during this time. Control of mites within the galls is not possible
with the acaricides currently available and approved for use on blackcurrants. A surface
deposit is needed. Before our transforming research, a typical spray programme for
blackcurrants consisted of three sprays of an acaricide applied per season for control
of the mite, the first just before flowering, the second at the end of flowering and the
third 10 days later. Traditionally, lime sulphur was used, but this was superseded by
the organochlorine insecticide endosulfan in the 1950s and 1960s. In the early 1990s,
endosulfan in turn, was superseded by the synthetic pyrethroid fenpropathrin. However,
despite intensive routine spraying, the gall mite and reversion virus disease remained
widespread and damaging in blackcurrant plantations.
Although it has long been recognised that the timing of the emigration of the gall
mite is not closely associated with a particular growth stage of the plant (Smith, 1960),
commercial acaricide applications were still timed according to plant growth stage.
Such timings were often less than optimal and may contribute to poor control. Direct
observation of the emigration of mites from the galls is possible but is difficult and time-
consuming and is unlikely to be practiced by growers who, in any event, try to rid their
plantations of galls in the dormant period.
In the late 1990s we investigated the emigration of C. ribis from galls in spring
(henceforth termed ‘emergence’) in relation to meteorological and plant growth
conditions and developed a predictive models that would provide more precise
information on the timing of the emigration in different years as an aid to the timing of
acaricide sprays (Cross and Ridout, 2001). It had long been known that the migration
of mites is influenced by temperature. However, predictive models for the migration of
the mite had not previously been developed.
The emergence of C. ribis from galls on the blackcurrant cultivars Ben Lomond and
Ben Tirran was monitored closely each year from 1995-1999 using miniature sticky
traps to capture mites after they had emerged from an individual gall. Each trap consisted
of a plastic cap 3.5 cm in diameter (the lid of a 30 ml specimen tube) with a c. 2 x 2 cm
square of double-sided sticky tape adhered to its underside centrally. The shoot above
the gall to be monitored was cut off 5 cm above the gall with secateurs. Care was taken
to make the cut cleanly and at right angles to the shoot. The trap was then pinned to the
end of the truncated shoot above the gall (Figure 18). After emergence from the gall, the
mites climbed the stem above the gall moving upwards towards higher light intensities
(Smith, 1960). When they reached the trap they became stuck to the sticky tape. The
captured mites occurred in a ring round the place of contact of the tape and the end of
the shoot. The mites captured on a trap were then counted under a binocular microscope
in the laboratory.
Figure 18. The miniature sticky traps devised to capture blackcurrant gall mites after they had
emerged from a blackcurrant gall mite ‘big bud’ gall
Each year from 1995 to 1999, the numbers of mites emerging from 30 randomly selected
galls on each cultivar were monitored from early March (c. Julian day 60) until the
emergence had ceased. The daily numbers of mites captured per gall from Ben Lomond
and Ben Tirran in 1995 are shown in Figure 19.
47 Jerry Cross
Figure 19. Emergence of blackcurrant gall mite (C. ribis) in 1995 and daily maximum and
minimum temperature, rainfall and sunshine hours. Arrows indicate the date of first flowering
Emergence was preceded by swelling of the galls. There was great day-to-day variability
in the mean number of mites that emerged: There was a positive correlation between the
number of mites emerging and mean or maximum daily temperature but numbers were
suppressed on days when there was rainfall. There was great variability in the timing
of emergence of mites from individual galls and the variance of the number of mites
emerging was related to the mean according to Taylor’s power law. The emergence
of mites had a strong diurnal rhythm, controlled by both light and temperature, with
virtually no mites emerging between 23:00 hrs and 09:30 hrs. Galls contained several
thousand motile mites and roughly double the number of eggs during the early part of
the migration when the internal tissue of the galls was green and succulent. The internal
tissue of the galls became progressively dry and chlorotic as the migration progressed
and the numbers of mites and the emergence dwindled and eventually ceased.
First, 5% and 50% emergences varied from Julian day 74-112, 84-121 and 101-
129 respectively in the different years but were virtually identical on the two varieties,
even though Ben Tirran flowered on average 14 days later than Ben Lomond. First
emergence was often associated with the first day after 1 March when the maximum air
⩾
temperature 16 ºC. More satisfactory predictions of the seasonal timing of emergence
were made by accumulated temperature sums above a threshold of 4 ºC from Julian
day 46 (15 February). The start date was chosen because it gave the best predictions,
and because it is my birthday! The average accumulated temperatures for first, 5% and
50% emergences were 122, 199 and 316 degree-days which gave mean errors in the
predictions of 3.1, 1.3 and 7.2 days respectively. Observed Julian days of first, 5% and
50% emergence and predicted Julian days of the same emergences from accumulated
temperature sums above 4 °C from 15 February (Julian day 46) for Ben Lomond are
shown in Table 2. In 1998, the onset of emergence was delayed by a prolonged period
of wet weather during which the internal tissue of the galls became necrotic, particularly
on Ben Tirran. In subsequent years, the accumulated temperature model predicted the
first, 5% and 50% emergences to within 4, 4 and 5 days respectively.
Table 2. Observed Julian days of first, 5% and 50% emergence of C. ribis from galls on the
variety Ben Lomond and predicted Julian days of the same emergences from accumulated
temperature sums above 4 °C from 15 February (Julian day 46)
In subsequent work (Cross and Harris, 2006), sulphur was shown to be the most
effective acaricide for control of the gall mite, two early season sprays giving superior
control to the fenpropathrin (Meothrin) spray programme. However, it was shown that
sulphur can cause substantial phytotoxicity to blackcurrant but the severity of visual
49 Jerry Cross
symptoms, yield loss and growth reduction depended greatly on variety, temperature
conditions and growth stage of application. Optimum timing and use of sulphur to gain
maximum efficacy with minimal risk of phytotoxicity was established. The preferred gall
mite treatment consists of a spray of sulphur 800 g/l at 10 kg /ha at bud burst, followed
by a second spray at the start of migration, preferably just before the grape visible
growth stage to minimise the risks of phytotoxicity. These early treatments gave over
80% control. Supplementary sprays of tebufenpyrad (Masai), which was shown to be
a non-phytotoxic, moderately effective acaricide for gall mite, could be applied at the
peak of migration in plantations at higher risk from gall mite.
The gall mite forecasting model is now in regular use and is the basis of
management of this most important pest in UK blackcurrant plantations. Rob Saunders,
GlaxoSmithKline technical advisor to UK blackcurrant growers, sends a weekly forecast
generated in Excel (Figure 20) to UK blackcurrant growers by email in spring, which
together with the use of sulphur as a safer more effective acaricide, has transformed
management of this blackcurrant pest. Rob is a very knowledgeable and effective
advisor and has been a great supporter of our work at EMR and as a result we have
made several important improvements in pest management methods for blackcurrants.
Figure 20. Example of the blackcurrant gall mite emergence forecast sent to all growers by
email on a weekly basis in spring by GlaxoSmithKline advisor Rob Saunders
4. Treating at different times of the season

Many pests are vulnerable to control at a number of stages in their life history through
the year. However, application of control measures at a particular time of year, e.g. after
bud burst in early spring on tree fruits, has developed historically as standard practice.
There may be opportunity to actually achieve better control at other times than the one
historically adopted, or treatment at other times may have other important advantages.
Aphids are one important group of fruit pests where our work at EMR has shown that
control at a completely different time of the year, in the autumn, is preferable and that
control at this time has important advantages over control in spring, the time adopted
historically.
4.1. Autumn control of aphids

The aphid species that are significant pests of tree and bush fruit crops in Europe are
mostly host-alternating. They spend the autumn, spring and early summer on their
winter woody tree/bush fruit host but migrate to herbaceous hosts in summer. In the
autumn, there is a return migration to the winter woody host by males and pre-sexual
females (gynoparae), the latter producing sexual females (oviparae) which mate with
the males and lay overwintering eggs on the bark (Figure 21). Other important fruit
pest aphid species, e.g. the large raspberry aphid (A. idaei), and the strawberry aphid
(Chaetosiphon fragaefolii (Cockerell)) also have a migration period in summer or autumn
but do not host alternate.
The normal strategy to control aphid pests is to make one or more aphicide
applications in spring when plant growth has recommenced and after the eggs have
hatched to avoid the subsequent development of damaging colonies, which cause
severe curling of leaves in shoots tips and stunting. Over the past 5 years or so, we
have investigated whether good control of the most important aphid pests of tree and
bush fruit crops can be achieved by autumn application of an aphicide timed to kill the
returning winged forms before egg-laying occurs.
There are several important advantages of autumn as opposed to spring control
of aphids by use of insecticide sprays. The main advantage is that at this time the
gynoparae and oviparae are vulnerable of on the flat undersides of leaves (i.e. leaves
not curled by aphid feeding) in the autumn where they can be directly intercepted with
sprays, compared to the inaccessibility of fundatrices and fundatrigeniae enclosed in
blossom clusters and leaves curled by aphid feeding in spring. Furthermore, in the
spring the foliage is growing rapidly and insecticide active ingredients are diluted by
rapid tissue expansion. Active ingredients may be more rapidly metabolised by the
plant. Other advantages are that autumn sprays are less likely to impact on spring
populations of aphid predators and will not result in pesticide residues, providing they
are applied after harvest.
We first investigated autumn control of the rosy apple aphid, D. plantaginea, a key
pest in western European apple orchards and which has developed strains resistant
to insecticides in some southern and central European countries (Schaub et al., 1999,
2001). The common strategy to control this aphid pest in conventional apple production
is application of an aphicide just before flowering, very often followed by a second
application after flowering or in early summer. Systemic aphicides are preferred as they
can control aphids protected in curled foliage. In autumn, winged males and gynoparae
of D. plantaginea migrate from the secondary host, ribwort plantain, Plantago lanceolata
L., to the primary host, apple (Figure 21).
51 Jerry Cross
Figure 21. Host alternating life cycle of the rosy apple aphid, Dysaphis plantaginea
The triggers for the autumn migration for this species are unknown, though it is probably
connected with a combination of shortening days, host plant condition and weather
conditions. The possibility of controlling rosy apple aphid in the autumn was recognised
by Theobald (1922). He conducted tests spraying ‘hot lime’ (prepared by mixing quick
lime (CaO) with water to form Ca(OH)2, the exothermic reaction that occurs raises the
temperature of the solution) and concluded that ‘much better results can be obtained
in the autumn to kill males and ovipositing females which occur in great numbers under
the flat leaves. Soft soap (10 lb.–100 gals. water) is as effectual for this purpose as
paraffin emulsion’. Theobald also recognised the importance of controlling the aphid
before it could protect itself in the curled foliage. In the late 1990s and early 2000s,
several research groups in Europe investigated autumn control of rosy apple aphid
by defoliation of apple trees in the autumn (Hoehn et al., 2003; Romet, 2004) or by
sprays of organically acceptable (Wyss, 1997; Wyss and Daniel, 2004) or conventional
insecticides (Helsen, 2001; Helsen and Simonse, 2002) with mixed results.
If and when to spray is a key question, the subject of this lecture. The aim of autumn
application is to control a very high proportion of the gynoparae, males and oviparae
before overwintering eggs are laid. Logically, the best time to treat is immediately before
egg laying commences, catching the maximum proportion of the migrants i.e. when the
autumn migration of gynoparae is near its end and at the start of the male migration
because oviparae cannot lay eggs unless they are mated. There is normally a 2-3 week
delay between the migration of gynoparae and males.
A network of suction traps (Macaulay et al., 1988) has been operated by
Rothamsted Research since 1966. Traps are currently located at 12 sites in England.
The trap aperture is 12.2m above ground level and the samples are representative of
the aphids flying at that height up to about 80 km away (Taylor, 1979; Cocu et al., 2005),
although much variation in numbers in orchards is to be expected as a result of local
characteristics. The traps are emptied daily during the aphid season (mid- March to late
November), weekly at other times, and aphids identified. A data base of over 40 years
of weekly records of the numbers of several important tree and bush fruit aphid pests
including rosy apple aphid, apple-grass aphid (Rhopalosiphum insertum (Walker)) and
currant-sowthistle aphid (Hyperomyzus lactucae (L.)) are available. The data can be
used to examine the timings of the autumn migrations of the different species.
The Rothamsted Insect Survey suction trap catches of Dysaphis sp. at Wye in Kent
from 1967 to 2005 inclusive (Figure 21) show considerable annual variation in the size
but limited variation in timing of the autumn migrations. On average, the migration of
gynoparae starts in week 37 (mid September) and ends in week 43 (end October) with
a peak in week 39 (end September). Small numbers of males start to occur in week 38
but the main male migration is in weeks 40-42. The data suggest that the optimum time
to spray would be in week 40 (1st week October).
Figure 21. Thirty nine year (1967–2005) average catches of Dysaphis sp. in the Rothamsted
Insect Survey suction trap at Wye in Kent
Between 2000 and 2005 we conducted a series of eight large-scale replicated orchard
experiments evaluating control of rosy apple aphid by autumn applications of aphicides.
The experiments showed that control of the aphid in the autumn with pirimicarb or
pirimicarb+cypermethrin can be highly effective (Cross et al., 2007). The optimum time
for spraying was week 40–41 (early–mid October), coinciding with the start of migration
of males and before mating and egg laying, as indicated by Rothamsted Insect Survey
suction traps. Pyrethrum was found to be partially effective but the other organically
acceptable materials tested (potassium soap, rotenone, garlic extract, kaolin, neem
extract, starch-based plant extracts) did not give useful control.
Subsequently, we have shown that the same approach can be highly effective for
control of large raspberry aphid (A. idaei) on raspberry, all the important aphid pests of
blackcurrant and the strawberry aphid (C. fragaefolii) on strawberry. We are currently
investigating autumn control of the aphid pests of cherry and plum. For some aphid
species, e.g. the blackcurrant aphid (Cryptomyzus galeopsidis (Kaltenbach), time of
spray application made little difference to the degree of control though two sprays were
better than one, but for other species e.g. the currant-sowthistle (H. lactucae) and large
raspberry aphid and strawberry aphid, the degree of control depended on the date of
application with best control being achieved by sprays in early October (Figure 22)
53 Jerry Cross
Thus, we have demonstrated that autumn application of aphicides gives good

control of all the most important aphid pests of tree and bush fruit crops. Where timing
was critical, the best time of application was in early October, coinciding with the end
of the migration of gynoparae and the start of the migration of males. There is a need
to develop assessment methods and treatment thresholds for autumn treatment so
routine spraying can be avoided. Possible methods for gauging the size and timing of
the autumn migrations to rationalise the use of autumn aphicide sprays include suction
and sex pheromone trapping and surveying the incidence of gynoparae and oviparae
on trees in the autumn, challenges for horticultural entomologists in the 21st century.
Figure 22. Effects of sprays of the aphicides pirimicarb or thiacloprid on populations of aphid
pests of blackcurrant, raspberry and strawberry the following spring
55 Jerry Cross
5. Alternatives to pesticides
Research into alternatives to pesticides has been vast over many decades, numerous
and diverse alternative control methods have been developed and there is a vast
literature.
Biocontrol, including the use of introduced predators and parasites and the use
of microbial biocontrol agents and nematodes, is perhaps the most widely exploited.
There are several well known and important established uses of introduced natural
enemies to control pests of soft fruit crops in the UK (e.g. use of the predatory mite
Phytoseiulus persimilis Athias-Henriot to control two spotted spider mite (Tetranychus
urticae Koch) and the predatory mite Amblyseius cucumeris (Oudemans) to control
strawberry mite (Phytonemus pallidus ssp. fragariae (Zimmerman)) and western flower
thrips (F. occidentalis) and the number and extent of use of these have grown in recent
years in response to the increase in the protected cropping, the development of
pesticide resistance, loss of pesticides and other factors (for a recent review see Cross
et al., 2001). There have been very few instances where natural enemies have been
introduced to regulate an invasive pest in tree fruit crops. On apple, the best known is
the introduction in the 1920s of the parasitoid Aphelinus mali (Hald.) to control woolly
aphid, an invasive pest from America. A. mali is now an important natural enemy of
woolly aphid present in most places where the pest occurs. It certainly greatly helps to
regulate woolly aphid outbreaks, but is often not quite good enough on its own requiring
the assistance of earwigs. Inundative releases of arthropod predators or parasites as
biocontrol agents to orchards are generally too costly and are often not successful
because of climatic instability.
There are a small number of significant success stories of the use of microbial
agents and nematodes for pest control in fruit growing. For recent reviews see Cross
et al. (1999a) and Lacey and Shapiro-Ilan (2008). The widespread use of codling moth
granulovirus is the most important (reviewed by Lacey et al., 2008). Formulations of
the virus are approved in most European countries and are applied to the foliage as
sprays. The virus is highly selective and virulent. In orchards, only codling moth can
be infected. A single virus particle is sufficient to kill a first instar codling moth larva.
The virus is safe to humans, plants and the environment. It has to be ingested by the
newly hatched larva when feeding on the skin of the apple before it penetrates the flesh.
The larva continues feeding for a few days before the virus acts. This results in small,
shallow, larval feeding holes in the surface of the fruit, known as ‘sting’ injury. Although
sting injury is superficial, it can result in downgrading of fruit to a lower quality class.
The virus is sensitive to UV light and high temperatures which limit its persistence.
A programme of sprays of the virus through the egg hatch period is required. No
‘pesticide residues’ occur on fruits at harvest. Strains of the codling moth resistant to
the virus have developed in some regions in continental Europe where the virus has
been relied upon for control for many years. The problem has been overcome by using
a different strain of the virus. However, this development highlights the need to use
multiple suppressive control tactics to minimise the risk of resistance.
However, the subject is clearly too vast to cover in any depth here so for the
purposes of this lecture I have concentrated on semiochemical based control methods
as these have been the subject of intensive ongoing collaborative research between
EMR and the Chemical Ecology Group of NRI here at the University of Greenwich.
5.1. Semiochemical based control methods

Although numerous sex pheromones, aggregation pheromones and other
semiochemicals of insect pests have been identified there have to date been relatively
few commercially viable products and techniques to control only a limited number of
pest species, mainly moths, though this number is now starting to increase. There
has been a tendency for scientists to consider that most of the critical research has
been conducted once the semiochemical has been identified. However, this is not the
case and effective development and deployment of semiochemicals requires extensive
long term research with close collaboration between chemists and entomologists
specialising in insect behaviour and field evaluation.
There are three principle means of using sex pheromones, aggregation pheromones
and other semiochemicals for control of insect pests: 1) mating disruption (MD); 2)
attract and kill (A&K); 3) mass trapping (MT). Semiochemical control methods usually
have to be deployed on a large, preferably area-wide, scale and initial pest populations
generally have to be low for control to be effective. Here, two examples of our ongoing
work to exploit for control some of the non-lepidopteran semiochemicals we have
discovered is described below briefly.
5.1.1. Mating Disruption (MD) and Attract and Kill (A&K)

The use of sex pheromones for mating disruption (MD) or attract and kill (A&K) are
potentially very powerful tools in IPM. Most sex pheromones are produced by female
insects and only attract males of the same species. The MD technique is based on the
premise that male insects are unable to locate females if the environment around the
females is permeated with sex pheromone. The precise mode of action is speculative.
Three factors may act alone or in combination to produce mating disruption; sensory
adaptation, habituation and direct competition.
In theory, mating disruption may be accomplished in two principle ways: false
trail following or confusion. False trail following results from placing many more point
sources of pheromone per unit area than the anticipated numbers of females in the
crop. The chances of males finding females at the end of the pheromone trail must be
greatly reduced. Emission of pheromone is relatively low from each source such that a
downwind trail is created and not lost in a background of released pheromone. Males
following these trails are thought to spend their mating energies in pursuit of artificial
pheromone sources. In contrast, male confusion is thought to be the result of ambient
pheromone concentrations sufficient to hide the trails of calling females (large doses
from point or diffuse sources).
A&K is an extension of the false trail following MD method, and is closely related
to the mass trapping method described below. In false trail following, the males come
in close vicinity of the artificial pheromone sources and may try to mate with them. In
A&K formulations, the pheromone dispensers or the target devices on which they are
held are coated with a contact insecticide, often formulated in a sticky carrier. The
males become contaminated with insecticide and are disabled and eventually die.
Females are thus less likely to encounter males by chance. However, in many cases
the effectiveness and benefits of the added insecticide is largely unknown under field
conditions. A further combination of pheromones and insecticides is occasionally
encountered. Dual applications of pheromone and insecticides (either separately or, in
the case of sprayable pheromone formulations, in tank mixes) are applied, sometimes
57 Jerry Cross
with the idea of increasing insect flight activity and thus increasing the chance of
insecticide exposure.
The MD technique is widely used for control of a number of economically important
lepidopteran pests including codling moth (C. pomonella), the oriental fruit moth (Cydia
molesta (Busck)) and the vine moth (Eupoecilia ambiguella Hübner). The subject has
recently been reviewed by Miller et al. (2006a, b). In comparison, there have been very
few investigations of the use of sex pheromones of non-lepidopteran pests for MD
or A&K. Our discovery of the sex pheromones of many of the midge pests of UK fruit
crops presented an important opportunity to attempt to exploit these for control. The
midge pheromones were active at very low doses, several orders of magnitude lower
than those of most Lepidoptera.
We first attempted to exploit the female sex pheromone of apple leaf midge (D. mali)
for control in newly planted versus established apple orchards in 2004 and 2005 (Cross
and Hall, 2007). This pheromone, (Z)-13-acetoxy-8-heptadecen-2-one, was present at
less than 20 pg per female (Cross and Hall, 2005; Hall and Cross, 2006). Although only
one enantiomer of the pheromone, probably that with S configuration, is attractive, the
racemic mixture is equally attractive, the latter being much more economic and easier
to synthesise. The pheromone is extraordinarily active. Rubber septa lures containing 1
μg and emitting only a few pg of pheromone per hour are highly attractive. A consumer
assessed experimental permit was obtained from the Pesticides Safety Directorate
to conduct large scale field trials of the pheromone without the need to destroy the
crop from fruiting trees. By analogy with similar compounds, the sex pheromone was
considered to be comparatively safe to humans and the environment but because
no data was available, the experimental permit restricted the dose applied to 1 g per
ha per season on the basis that the local concentration of the pheromone would not
exceed the maximum concentration that occurs naturally.
In July 2004, a preliminary field experiment was done at EMR to investigate use of
the apple leaf midge sex pheromone for control of apple leaf midge using an attract-
and-kill (A&K) strategy. A&K devices were 20 x 20 cm squares of plastic laminated
cardboard surface coated on both sides with a microencapsulated formulation of
the SP insecticide lambda-cyhalothrin developed for control of olive fly (Agrisense).
These were positioned 5 cm above ground level and baited with a rubber septum lure
impregnated with 100 µg of apple leaf midge pheromone fixed centrally.
Four small heavily infested apple orchards at EMR were selected for the experiment:
On 5 July, a single standard white delta trap baited with a standard 3 µg rubber septum
lure was deployed in the centre of each plot. Catches of males were counted on six
occasions between 7-27 July 2004. On 7 July, 28 and 12 A&K devices respectively
were deployed in lattices in two of the plots to give a density of approximately 100/ha.
On 27 July, 100 shoot terminals in the centre of each plot were examined for ovipositing
females and presence of apple leaf midge galls.
Table 3. Pheromone trap catches of male D. mali and damage assessments in preliminary
attract and kill experiment at EMR (pheromone trapping 7-27 July; damage assessments on
27 July 2004)
The two orchards where the A&K treatment was deployed had considerably lower
trap catches than the untreated plots, but the treatments failed to shut down catches
completely (Table 3). The shoots assessment on 27 July revealed that 100% of
shoots were galled on 3 of the plots with 84% galled on the other. Small numbers of
ovipositing females were also recorded. The results showed the treatment was not able
to adequately suppress mating and that a much higher dosage of pheromone would be
required probably with many more devices per ha.
Bioassays of the effect of contact of apple leaf midge adult males with the
lambda-cyhalothrin target devices were conducted on 1 and 2 September 2004. A&K
devices were observed in the field and at intervals. Ten attracted male midges were
pootered from the surface of the device or shortly after they had made contact, and
held in tubes. Midges were pootered in a similar way from the surface of a similar
device not treated with lambda-cyhalothrin. After 1 hr, all the midges that had been
exposed to the lambda-cyhalothrin card, even for 5 min, were severely affected by
the insecticide. They were unable to fly and lay trembling in the bottom of the tube.
After 2 hr, all were trembling or moribund. After 3 hr, all were dead. Similar results
were obtained with cards from A&K devices that had previously been exposed for two
months in the field.
A very large scale field trial was carried out in commercial apple orchards in Kent
during 2005 to evaluate the use of the apple leaf midge sex pheromone for control of
apple leaf midge by mating disruption (MD) or attract and kill (A&K) approaches. MD
devices were polythene caps each initially loaded with 500 µg of the apple leaf midge sex
pheromone (Figure 23a). These caps each released the pheromone at approximately
10 ng/hr at 27 ºC in the laboratory. The A&K target devices were 10 cm x 6.7 cm
oblongs of the microencapsulated lambda cyhalothrin surface treated cardboard with
a polythene cap lure containing 100 µg of the apple leaf midge sex pheromone fixed to
the centre with a drawing pin (Figure 23b). These caps each released the pheromone
at approximately 2 ng/hr at 27 ºC in the laboratory. Both MD and A&K devices were
deployed at 500 devices/ha or 2000 devices/ha, fixed to tree stakes so that the lure
was at a height of approximately 15 cm above the ground in a regularly spaced lattice.
Thus for the MD treatments, pheromone application rates were 0.25 g/ha or 1 g/ha
respectively and release rates were approximately 5 µg/ha/hr and 20 µg/ha/hr. For the
A&K treatments, pheromone application rates were 0.05 g/ha or 0.2 g/ha respectively
and release rates were approximately 1 µg/ha/hr and 4 µg/ha/hr.
59 Jerry Cross
a) b)
Figure 23. First large scale field trials to exploit the apple leaf midge (D. mali) sex pheromone
for control a) MD devices were polythene caps each initially loaded with 500 µg of the apple
leaf midge sex pheromone racemate; b) A&K devices were 10 cm x 6.7 cm oblongs of the
microencapsulated lambda cyhalothrin surface treated cardboard with a polythene cap lure
containing 100 µg of the apple leaf midge sex pheromone fixed to the centre with a drawing pin
A fully randomised experimental design was used with six replicate 1 ha plots of
each treatment, requiring 30 plots of 1 ha in 11 orchards on six different fruit farms in
Kent. Three of the plots for each treatment were in newly planted orchards where leaf
midge populations were low and three were in established orchards where leaf midge
populations were high. Untreated plots were well separated from those which had MD
or A&K treatments which themselves were adjacent. The effectiveness of the treatments
was assessed by weekly monitoring of catches of adult male midges in a delta trap
baited with a 3 µg rubber septum lure in the centre of each plot and by counting the
number of galls present in 200 shoots in the centre of each plot for each of the three main
generations, at the peak of damage expression on 17-23 May, 20-25 June, 4-6 July and
30-31 August 2005.
Table 4. Mean pheromone trap catches of male D. mali and damage assessments in mating
disruption (MD) and attract-and-kill (A&K) trials (April-September 2005; 1 ha plots, 3 replicates
per treatment)
In the analyses of variance of the log transformed total counts, the only differences of
significance were whether or not any ‘treatment’ had been applied, with no differences
between type and number of lures. All the MD and A&K treatments suppressed the
catches of males in the traps in the centres of the plots compared to the untreated
control (Table 4). In the established orchards with higher populations, catches were
decreased by > 98% in April-May, by > 99% in June-July, but by only >91% in August-
September (Table 4). In the newly planted orchards with very low populations of the
midge, trap catches were zero in April-May in all plots, were very low but suppressed
by 90% by the MD and A&K treatments in June-July, but rose somewhat in August
September being suppressed by about 80% in the treated plots (Table 4).
Regrettably, there was no evidence that either the MD or A&K treatments were
suppressing numbers of galls in shoots in the established orchards (Table 4). In the
newly planted orchards, it appeared that the MD and A&K treatments were failing in
July and certainly by August, no suppression of galling damage was evident.
On 9 September 2005, bioassays of the effectiveness of target devices which
had been deployed in the field since the start of the A&K trials were conducted in a
similar way to that described above for the preliminary experiment. The results were
less clear cut than in the previous bioassays with substantial mortality in the untreated
controls. However, the experiments did show that the devices maintained their activity.
Measurement of release of pheromone from the open polyethylene caps used
in these trials for both MD and A&K treatments showed relatively uniform release for
at least 270 days under laboratory conditions. However, lures recovered from the field
at the end of the above experiments were found to contain no detectable pheromone.
This was subsequently been shown to be due to degradation of the pheromone, the
lures being unprotected from direct sunlight in both MD and A&K treatments.
Why did these first attempts at exploiting the pheromone fail? In the Cecidomyiidae,
unmated females are evidently not able to lay viable eggs (Gagne, 1984, 1989) though
monogeny often occurs in some species (Murchie and Hume, 2003). The bioassays
indicated the A&K devices did kill the males, albeit only after a few hours. Males
are known to be able to mate several times, though females only need to be mated
once to be fertilised. Clearly, sufficient mating was still occurring to provide enough
fertilised females to oviposit in the shoots that were present. There are several possible
explanations for the failure:
• The dose (1 g/ha) was too small
• An insufficient number of dispensers/devices was deployed per ha
• UV degradation of the pheromone occurred rapidly
• The 1 ha scale of deployment of treatments was insufficient and there was
ingress of mated females into the plots from the edges
• The initial populations of the midge were too high to prevent some mating
occurring
The above work clearly needs to be continued using higher doses of pheromone
protected from UV degradation. Unfortunately, our funding for working on exploiting the
apple leaf midge sex pheromone was not continued to allow us to investigate further,
but, as part of Horticulture LINK project HL0175, we did start work on exploiting for
control the raspberry cane midge sex pheromone, which we had already identified (Hall
et al., 2009).
61 Jerry Cross
To date we have conducted four years of field trials testing a wide range of
formulations of the R. theobaldi pheromone. At the outset, we determined the effect
of the release rate of raspberry cane midge pheromone from rubber septum lures on
attractiveness to male raspberry cane midge. The results (Figure 24) were surprising.
Lures which released 600 pg of pheromone/hr (in the NRI laboratory wind tunnel at 27
˚C and 8 km/hr wind speed ) and initially loaded with 0.1 μg of the pheromone racemate
were significantly attractive. Maximum attractancy occurred ay 600 ng/hr though 60
ng/hr (initial loading 10 μg) performed nearly as well. Attractancy was significantly
reduced at greater release rates. Three alternative control strategies were apparent: 1)
MD or A&K using false trail following using large numbers devices with release rates of
~60 ng/hr; 2) male confusion using high ambient pheromone concentrations sufficient
to hide the trails of calling females using smaller numbers of devices with high release
rates (> 6 μg/hr).
Figure 24. Effect of release rate of sex pheromone racemate from rubber septum lures on
catches of male R. theobaldi in 2006 (release rates were estimated from measurements made
on rubber septa loaded with 100 μg in the laboratory wind tunnel at NRI at 27°C and 8 km/hr
wind speed in 2005, which release 600 ng of pheromone per hour)
Each year for four years to date, large scale (~ 1 ha plots) field experiments have been
done in commercial raspberry plantations in SE and E England to evaluate the efficacy
of MD and A&K treatments in comparison with an untreated control for control of
raspberry cane midge.
In 2006, a MD treatment evaluated comprised 2000 polythene cap dispensers per
ha, each initially loaded with 1 mg of raspberry cane midge sex pheromone racemate,
deployed in a regular lattice through the crop at a height of 15 cm (Figure 25a). The
A&K treatment tested comprised 2000 plastic laminated cards surface coated with
a microencapsulated formulation of the SP insecticide lambda-cyhalothrin and which
had a polythene cap dispenser (initially loaded with 100 μg of the pheromone) fixed to
the centre per ha (Figure 25b).
a) b)
Figure 25. R. theobaldi pheromone control 2006: (a) MD device fixed to primocane (b) A&K device
fixed to primocane.
The MD and A&K treatments were effective outdoors where a high degree of trap
suppression was achieved but were ineffective in the polytunnel crops where trap
suppression was less effective (Table 5). Possible explanations for this difference
in efficacy are that pheromone release was too rapid from the dispensers when they
were deployed in the polytunnels where temperatures were much higher than outdoors
and/or is that the pheromone did not disperse so effectively in the enclosed polytunnel
environment.
Table 5. Effectiveness of MD and A&K treatments in suppressing sex pheromone trap catches
and larval infestations of R. theobaldi in 2006
In 2007, we tested 200 polythene sachet MD devices and 200 Mass Trapping (MT)
devices per ha (Figure 26a). The sachets were each initially loaded with 50 mg of the
midge sex pheromone racemate and released the pheromone racemate at rates of
approximately 0.5 mg/day at 28 ºC in the laboratory. The mass trapping (MT) devices
were Lynfield type traps each baited with a rubber septa lure initially loaded with 200 µg
of the pheromone racemate and released 60 ng pheromone/hr at 28 ºC in the laboratory.
The traps contained 50 ml of water + 50% glycol, and were suspended at a height of 15
cm from the ground (Figure 26b). The MT rather than A&K devices were used because
they gave records of whether or not attracted midges were killed (by drowning)
63 Jerry Cross
a) b)
Figure 26. R. theobaldi pheromone control 2007: (a) polythene sachet MD device fixed to a post
(b) Lynfield MT device
Results in 2007 were disappointing (Table 6). Although the MD treatment gave fairly
good suppression of trap catches the MT treatment was less effective in this respect and
neither treatment prevented larval attack in artificial splits in the canes. It was concluded
that 200 devices per ha was probably too small a number.
In 2008, a new MD treatment comprising 3 kg/ha of 0.5% w/w pheromone racemate

EVA granules (~ 150,000 granules/ha) (Figure 27a) broadcast by hand to the soil surface
between the rows was tested in comparison an A&K treatment comprising 2000 plastic
laminated lambda cyhalothrin cards (similar to those tested in 2006) each with a rubber
septum dispenser loaded with 200 μg of the pheromone racemate (Figure 27b) and an
untreated control.
a) b)
Figure 27. R. theobaldi pheromone control 2008: (a) 0.5% w/w EVA granule formulation broadcast
at 3 kg/ha as an MD treatment (b) A&K device fixed to crop strings with a twist tie
Although both the MD and A&K treatments failed at one site (Decoy farm), very good
control was achieved at another (Belks Farm) and intermediate results at a third
(Salmans farm) (Table 7). The reasons for the different results at the different sites
are unclear. There was evidence that the MD treatment was losing it’s efficacy as
the season progressed with better results for the first generation. Lab measurements
of release rate indicated that the EVA granules used for the MD treatment released
60% of their pheromone in the first 31 days at 27°C. One explanation of the decline in
trap catch reduction may be that the pheromone release rate from the EVA granules
declined steeply through the season. Another possible explanation is that the granules
progressively worked themselves into the soil surface, some being trampled by pickers
as they walked through the tunnels. The trap catch reductions achieved by the A&K
treatments remained consistent through the season.
The above MD/A&K/MT formulations were either impractical for use by growers or
were ineffective. In 2009, we developed and tested a new R. theobaldi sex pheromone
MD/A&K method which we thought would be practical for use by growers, would not
get lost in soil and would have a large number of pheromone sources per ha so having
a better chance of success. We also used the method in conjunction with a directed
spray of a contact acting insecticide, deltamethrin. The aim was to use a competitive
MD approach to attract the male midges with the sex pheromone to numerous artificial
pheromone sources where they would then be killed by a surface deposit of insecticide,
to be applied subsequently. The insecticide chosen was deltamethrin (Decis), a product
already approved for use in raspberry. It is a light stable synthetic pyrethroid with
excellent knock down properties and good persistence. It was used as a separate
spray to avoid registration difficulties. A new SPLAT formulation of the cane midge
pheromone (Figure 28) was produced in the laboratory at NRI by mixing 4 g of the
raspberry cane midge sex pheromone racemate per kg of SPLAT base formulation
supplied by ISCA technologies, California (contact Agenor Mafra-Neto). The formulation
was then transferred to caulking guns. The IPDM plots were then treated with 2.5 kg
of SPLAT containing 10 g of raspberry cane midge pheromone racemate per ha. The
SPLAT was applied in 5000 0.5 g, 7 cm long strings per ha to the polythene mulch or lay
flat polythene irrigation pipe. Depending on the row spacing, approximately 1 SPLAT
string was dispensed per metre of row (Figure 28). 1-3 days after SPLAT application,
Decis was applied by the grower to the polythene at 600 ml of product in 200 l of water
per ha to polythene mulch on which SPLAT has been applied.
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a) b)
Figure 28. The SPLAT R. theobaldi pheromone formulation evaluated for control 2008: a) being
extruded from a mastic (caulking) gun to the polythene mulch surface; b) a 0.5 g SPLAT string,
extruded from an uncut mastic gun nozzle, ~ 3 mm diameter and ~ 7 cm long
Regrettably, the SPLAT + deltamethrin treatment was unsuccessful in suppressing

pheromone trap catches of males and at the one site where they were found, the
treatment was ineffective in controlling larvae (Table 8).
Table 8. Effectiveness of the SPLAT MD/A&K treatment in suppressing sex pheromone trap
catches and larval infestations of R. theobaldi in 2009
The weekly pheromone trap catches did show that the SPLAT formulation gave a very
high degree of trap shut down for the first 2-3 weeks, but thereafter the suppression of
catches declined sharply. Measurements of the amount of pheromone remaining in the
formulation also showed a sharp decline in the first few weeks (Figure 29), which may be
at least in part the explanation for the poor results.
Figure 29. Release of raspberry cane midge pheromone from SPLAT applied in the field (dotted
line is exponential fit y=100exp(-0.11)x; R2 = 0.81)
So to date, despite much effort, we have not managed to produce a successful

formulation for exploiting the R. theobaldi sex pheromone for control. The reasons for
this are unclear but appear to be a combination of an inadequate sustained release rate
and deployment where populations are too high initially. In 2010, we hope to test the
SPLAT formulation again but at higher doses and possibly with repeated applications,
and in fields with low to moderate R. theobaldi populations. We will devote more
attention to behavioural observations of the effect of the formulation on the midges.
5.3.1. Mass trapping

In mass trapping (MT), traps are deployed with the objective of destroying insects
for population control. As stated above, most sex pheromones are female produced
and attract males only. For mass trapping to be effective using female produced sex
pheromones, enough traps have to be deployed to catch enough males to leave the
females of the species without mates. But it is difficult to get good results because any
untrapped males simply mate more frequently. Large numbers of traps (> 50/ha) are
likely to be too costly.
However, aggregation pheromones often attract both sexes and are therefore
better suited for mass trapping applications. The strawberry blossom weevil (A,
rubi) aggregation pheromone is male produced and attracts both males and females
(see section 3.2.3 above). We evaluated the aggregation pheromone in sticky stake
traps for MT of A rubi but achieved poor results (Cross et al., 2006b). Importantly, its
attractiveness can be greatly enhanced by addition of host volatiles, especially the host
volatile from wild strawberry flowers. Furthermore, bucket traps with white cross vanes
are far superior to sticky stake traps used in our previous work and the combination
of these factors has enabled us to develop a supertrap for this pest (see section 3.2.3
above) (Figure 30).
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In 2010, we will start large scale field trials to evaluate the use of this supertrap for
control of A. rubi by mass trapping.
Figure 30. The green bucket trap with white cross vanes with aggregation pheromone plus host
volatile sachet lure is an A rubi supertrap. Photo courtesy Atle Wibe, Bioforsk, Norway
6. Safer more efficient orchard spray

application
Foliar pesticide applications to temperate tree fruit orchards are made mainly with
axial fan air blast sprayers. These generate a large radial spray plume which is poorly
targeted for many modern dwarf trees resulting in large losses to the soil and as long
range spray drift. An important aim is to improve the safety and efficacy of such spray
applications.
Axial fan sprayers are easy to use, are comparatively low in cost and have a long
life. It is widely recognised that alternative, more efficient designs are unlikely to be
widely adopted in the foreseeable future.
Collaboration with Dr Peter Walklate (formerly of the Silsoe Research Institute)
in this field of research has been close and very productive over many years. Peter is
an engineer with an excellent understanding of spray physics and application. In the
1990s and early 2000s, funded by the Pesticides Safety Directorate (now the Chemicals
Regulation Directorate, CRD) of Defra we aimed to improve the safety and efficiency of
air-assisted spraying to orchards and other fruit crops. We investigated the effects of
adjusting the operational parameters of the sprayer including spray volume rate (Cross
et al., 2001a), spray quality (Cross et al., 2001b)) and volumetric air output (Cross et al.,
2003) on sprayer performance including average spray deposits on foliage and fruits
and losses to the soil and as spray drift. New methodology for determining multiple
spray deposits using chelated metal salts as tracers was developed so that the work
could be done efficiently (Murray et al., 2001). The work showed that modest reductions
in spray losses and increases in deposits could be achieved by sprayer adjustment, in
particular greatly decreasing volumetric airflow and coarsening spray quality. Based
partly on this work, a case to CRD has recently been prepared for an application to grant
low drift status to various orchard spraying equipment and practices under the Local
Environment Risk Assessment for Pesticides (LERAP) scheme (Cross et al., 2009b).
6.2. Dose expression and adjustment

Dose rates on pesticide labels for tree fruit spraying in the UK prescribe a fixed dose rate
of product to be applied per unit ground area, regardless of crop structure. Pesticide
manufacturers often increase the normal margin-for-error on the label recommended
dose-rate to ensure that reliable efficacy is achieved across a broad range of target
structures. However, the practical experience of some fruit growers demonstrated
that label recommended dose-rates can be greatly reduced in some circumstances
without a significant reduction of efficacy. Before we started out work on this topic, we
suspected that orchard structure had a very large effect on average spray deposits and
that there was huge opportunity to adjust the dose to suit the crop to achieve desired
constant average spray deposits in different orchards, thereby making substantive
savings in pesticide use.
Working closely with Peter Walklate and Geoff Richardson over a period of over 10
years and funded by the Pesticides Safety Directorate (now the Chemicals Regulation
Directorate), we quantified spray deposits in a very wide range of orchards with widely
differing canopy structures at the full range of growth stages using tracers applied
with commonly used commercial air-assisted sprayers. We used a vertical scanning
LiDAR (Light Detection and RAnge) system (Figure 31a) to rapidly make attendant crop
structure measurements. The LiDAR uses a high frequency pulse modulated near infra
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red laser beam which scans the tree canopy to make range measurements from -90 to
90 degrees relative to the horizontal with an angular resolution of 0.5 degrees and a range
resolution of 1 cm. This set up gives 361 range vector measurements per scan at a rate of
37.5 scans per second. The LiDAR together with a GPS and a laptop PC are mounted on
a small tractor which moves at a constant speed (c 0.5 m/s) through the orchard (Figure
31b). The sequential output from the LiDAR and GPS are recorded and processed by
the PC using LidarAssistant software which runs under Microsoft Windows XP or Vista
operating systems. LidarAssistant produces operator feed-back information in the form
of a colour rendered range-map of the tree-row (Figure 31c) and this is reduced to a
2-D distribution of interception probability (Figure 31d) to represent the tree-row cross-
section.
a) b)
c) d)
Figure 31. a) LiDAR (Light Detection and Range) b) LiDAR, GPS and laptop PC mounted on
a small tractor which moves at a constant speed (c 0.5 m/s) through the orchard c) colour
rendered range-map of the tree-row produced by LidarAssistant for operator feedback d) 2-D
distribution of interception probability to represent the tree-row cross-section. Photos and
images courtesy of Peter Walklate
The LiDAR recordings of different orchards at different farms and growth stages were
used to construct an exemplar database of UK pome fruit structures. These recordings
were processed initially to reduce each database entry to a set of four parameters
describing the tree-row structure, namely: spacing, height, width and area-density.
Average deposits varied by almost an order of magnitude. An exact model of label
recommended dose rate adjustment, assuming minimum spray volume loss and based
on all four tree-row structure parameters, was used as a comparator to evaluate the
relative performance of different approximation models (i.e. typical regression models
based on a reduced set of tree-row parameters). Various approximation models that
included the scaling effects of treerow area-density gave significant agreement with
the population of label recommended dose rate adjustments predicted by the exact
model. Of the single parameter models, the tree-row area-density model gave the best
agreement with 80% of adjustments correctly predicted to within an error tolerance
±1/8th of the label recommended dose rate. An adjustment model based on tree-row
height and areadensity correctly predicted 93% of adjustments. Other approximation
models of practical interest gave less significant agreement with the exact model (i.e.
66% for the tree-row volume model, 55% for the fruit-wall-area model, 50% for the
constant adjustment model, 5% for no adjustment).
We used this data and results to develop Pesticide dose Adjustment to the
Crop Environment (PACE) as a generalised method for optimising broadcast spray
applications to pome and stone fruit orchards (Walklate et al., 2006). This was developed
into a practical scheme which made use of a grower assessment of crop height and
density to determine appropriate dose-related reductions (Walklate and Cross, 2005).
In 2009, Peter Walklate produced the first webpage based user interface to perform
dose adjustment calculations (Figure 32) (Walklate and Cross, 2010) using Microsoft
Active Server Pages technology (ASP.NET) and Visual Web Developer 2008 Express.
This has eliminated problems with the original PACE factsheet and is much easier for
growers and advisors to use. The system is currently available to internet users via
the URL http://www.pjwrc.co.uk/DoseAdjustment.aspx. This technology simplifies the
selection of inputs to describe: the sprayer set-up, the appropriate pesticide category
and the orchard canopy structure (i.e. density and height). It provides UK growers with
perhaps the best and most advanced dose adjustment method in the world.
71 Jerry Cross
Figure 32. The PACE dose adjustment calculator web page. See http://www.pjwrc.co.uk/
DoseAdjustment.aspx
7. Integrated Pest and Disease Management

(IPDM)
Integrated Pest Management (IPM) is a decision-based process involving coordinated
use of multiple tactics for optimising control of all classes of pests (insects, mites,
diseases, weeds etc.) in an ecologically and economically sound manner (Bajwa and
Kogan (2002) list 67 published definitions of IPM the one used here being a short
synopsis of the key aspects of IPM). The concept of IPM is based on the recognition
that no single approach to pest control offers a universal solution, and that the best
crop protection can be provided by a fusion of various tactics and practices based on
sound ecological principles. Key aspects are: 1) Priority given to non-pesticidal control
methods including natural, genetic, cultural, biological and biotechnological methods;
2) Multiple, compatible suppressive tactics; 3) Monitoring of pest and natural enemy
populations and risks and the use of economic treatment or risk thresholds; and 4)
Minimal use of the safest pesticides. This is a definition of an ideal IPM system, which
is the target for attainment in all crops. However, real IPM systems fall short of this
ideal to varying degrees. For a detailed review of IPM of orchard arthropod pests see
Blommers (1994).
Although the above definition of IPM (and many of the numerous other definitions)
encompass disease management, this is not explicitly expressed and often not
understood. To overcome this problem, at EMR we refer to the concept as Integrated
Pest and Disease Management (IPDM). Developing, evaluating and refining IPDM
programmes for fruit crops has been a central component of research at EMR for many
years. It requires close collaboration between plant pathologists and entomologists
and since 1982 I have collaborated closely with Dr Angela Berrie, plant pathologist, in
IPDM research on fruit crops.
7.1. Minimal residues IPDM

An important development, which first came to prominence in the UK, is the requirement
by multiple retailers to minimise, ideally to eliminate, pesticide residues from fresh
produce. Minimal Pesticide Residues IPDM imposes important additional requirements
on IPDM, but is also a powerful driving force in the development and implementation
of IPDM practices. Our work to develop Minimal Residues IPDM for apples (Berrie and
Cross, 2005, 2006; Cross and Berrie, 2005, 2008) started in the late 1990s before the
market requirement came to the fore. We were the first in the world to work seriously
on this topic.
Apples have traditionally been treated intensively with pesticides. As described
above, apple varieties grown in the UK and worldwide are highly susceptible to a wide
range of damaging pests and diseases. Adequate yields of fruit of acceptable quality
cannot be produced and the crops cannot be grown profitably unless these pests and
diseases are efficiently controlled. Efficient weed control is also vital. Apple industries
rely on pesticides for these purposes. With current methods of crop protection for
apples, foliar pesticide applications for pest and disease control are often made in
summer during fruit development and sometimes close to harvest. Furthermore, in
the past it has been common practice to drench apple fruits in fungicides and/or an
antioxidant post harvest to control post harvest rots and the physiological disorder
superficial scald. Use of pesticides in this way inevitably gives rise to detectable
levels of pesticide residues in a high proportion of fruit and many samples contain
73 Jerry Cross
multiple residues. Despite the intensive use of pesticides, residue levels do not exceed
Maximum Residue Levels (MRLs) if Good Agricultural Practice (GAP) is adhered to.
UK government agencies (CRD, Food and Environment Research Agency) conduct
regular retail surveillance of pesticide residues in samples of fresh produce. The results
are published quarterly on the web. Apples, an important dietary constituent, are
surveyed every year. In 2003, 301 apple samples, 82 UK produced and 219 imported,
were taken from retail outlets and analysed for residues of 109 pesticides. 71% of
UK produced and 71% of imported samples contained residues above the reporting
limits (5.3% had two residues, 5.0% had 3 residues, 3% had 4 residues and 1%
had 5 residues) (Anonymous, 2004). There were 3 MRL exceedences, all in imported
produce. A number of pesticides are found at levels above the accepted reporting
limits (RL) in UK produced fruit (Table 9). There is a high level of unit-to-unit variability
in pesticide residues, the extent of which appears to be determined at the time of
pesticide application (Hill and Reynolds, 2002). Absence of a mean residue above the
reporting limit in a bulk sample does not necessarily mean that the residue is below the
reporting limit on all individual apples. Amounts below the reporting limit are regarded
as zero, even though trace amounts might be present which could be measured by
a more sensitive method of analysis than the standard methods. The results for UK
produced fruit showed a substantive reduction in the incidence of residues from post
harvest treatments to fruit compared to earlier surveys, but an increase in the incidence
of chlorpyrifos residues.
Table 9. Occurrence of pesticide residues above reporting limits in 2003 government

surveillance of UK produced apples
UK multiple retailers do not wish to be ‘named and shamed’ by the official reporting
of residues below legal limits. A defining moment occurred in an article in the daily
Telegraph Newspaper on 16 August 2001 ‘Pesticide Report “names and shames”
superstores: Retailers Marks and Spencer (M&S) and Somerfield were “named and
shamed” by Friends of the Earth for the levels of pesticide residues on their fruit and
vegetables. The environmental campaign group claimed that M&S was the worst
offender, with 63 per cent of its fruit and vegetables containing residues. Somerfield
followed with 59 per cent. In response, several important retailers in the UK began
asking their suppliers to strive towards elimination of pesticide residues from fresh
produce including apples, to maintain and improve consumer trust.
There are a number of well known generic approaches to reducing pesticide
residues. The most important are 1) Grow resistant varieties; 2) Use non chemical
control methods, especially cultural, biological and biotechnological methods,
wherever possible. More attention needs to be devoted to developing and using new
biopesticide products which do not leave pesticide residues; 3) Avoid use of pesticides
except where absolutely necessary. This is done by frequent crop monitoring and risk
forecasting; 4) Use products more intensively earlier or later in the season (e.g. pre-
flowering or post fruiting to minimise problems during fruit development and fruiting);
5) Use shorter persistence products; 6) Use products that have a high reporting limit
relative to their dose. Reduce the dose of applications closer to harvest; 7) Increase the
harvest interval; 8) By training, improve knowledge and expertise of all those involved
in decision making.
7.1.1. The EMR minimum residues IPDM programme for

apples
Prior to our work, there are very few reports in the literature of concerted research efforts
focussed primarily on the development of pest and disease management programmes
to eliminate reportable residues from apple, or from other fresh produce for that matter.
Investigations by Jones et al. (1993) reduced but did not eliminate residues. We devised
a minimum residues IPDM programme for apples based on the use of conventional
pesticides (excluding organophosphorus (OP) insecticides) up to petal fall and after
harvest, but during the fruit development period to rely on biocontrol for dealing with
pests and diseases. The key features are:
• Integrated pest and disease management (IPDM) from bud burst to petal fall
based on conventional pesticides (thiacloprid, fenoxycarb, diflubenzuron,
methoxyfenozide) but excluding organophosphate insecticides. Management
of scab and mildew using the ADEM disease risk forecasting model to optimise
timing and dose of fungicides (Berrie and Xu, 2003)
• Use of biocontrol agents (Bacillus thuringiensis (Bt) or codling moth granulovirus)
for pest control from petal fall to harvest
• No conventional fungicides for disease control post petal fall except for reduced
dose sulphur for mildew control. Frequent assessment of secondary mildew to
determine dose of sulphur to be applied
• Cultural control. Removal of primary mildew, cankered shoots and brown rot
• Rot risk assessment to determine likely rot problems in the orchard (Full details in
Defra Best Practice Guide for apples (Cross and Berrie, 2001))
• Cultural control and selective picking to reduce / control rot problems in store. Only
sound fruit (to avoid brown rot) and fruit above knee height (to avoid Phytophthora
rot) picked for storage (Berrie, 2000)
75 Jerry Cross
• During the post harvest / dormant period, a DMI fungicide (e.g. myclobutanil)
applied for late mildew and scab control, urea for leaf rotting and scab control,
copper sprays for canker control at leaf fall and copper pre budburst for
overwintering scab
• Post harvest application of an aphicide for control of rosy apple aphid
In 2001 a 6 year study, funded for the first 3 years by Defra alone and subsequently
by Defra, the Horticultural Development Council and the producer organisation
WorldWideFruit, was established to investigate the feasibility of developing a zero
pesticide residue system for apples. A large scale randomised block field experiment
was established in Wiseman orchard at East Malling Research which had 12 existing
established plots, 6 of disease-susceptible apple varieties (Cox, Gala, Fiesta) and 6
of scab-resistant apples (Saturn, Ahra, Ecolette). The variety Discovery occurred in all
plots as an internal standard. Each plot consisted of 144 trees on M9 rootstock and
was separated from adjacent plots by alder windbreaks. In these plots the pest and
disease control achieved following a routine conventional pesticide programme was
compared to that achieved following a ‘zero residue’ management system. Untreated
plots of disease-susceptible and resistant varieties were included.
Good results were obtained with the minimal residues IPDM programme. Scab
control was as good and often better in the zero residue plots than in the conventional
plots, even on Gala, a variety which is exceptionally scab susceptible and including in
2002 and 2004, when scab risk was high (Table 10). This also demonstrated that the
reduced scab programme did not result in a build up of scab inoculum.
Table 10. Incidence of scab on the highly susceptible variety Gala in the first minimal
pesticide residues orchard experiment at EMR in 2001-2006
Mildew control in the zero residue plots was also similar to that in the routine treated
plots, and did not exceed 20% of shoots mildewed (Table 11). The primary mildew
in managed plots in 2002-2006 was negligible, indicating that the system was not
resulting in a build up of primary mildew. Primary mildew incidence was high at the
outset of the experiment on the variety Ahra in one of the Zero residue management
plots as prior to 2001 this plot had been untreated.
Table 11. Incidence of mildew on the highly mildew susceptible varieties Cox and Ahra in the
first minimal pesticide residues orchard experiment at EMR in 2001-2006
The incidence of rots in Cox after long-term controlled atmosphere storage is shown
in Table 12. Post harvest rots can be a significant commercial problem in Cox. The rot
management system applied in the zero residue programme gave satisfactory control
and in most years the lowest incidence of rots was in fruit from the zero residues plots.
The predominant rots were brown rot (Monilinia fructigena Honey) and Nectria galligena
Bres..
Table 12. Incidence of rots in the rot susceptible variety Cox after long term CA storage
(3.5 °C, 1.25% O2, < 1% CO2) in the first minimal pesticide residues orchard experiment at EMR
in 2001-2005
Pest damage to fruit at harvest is shown in Table 13. A high incidence of pest damage
was recorded in the untreated plots in all years and especially in 2004. In 2001 and
2002, pest damage in the zero residues plots was greater than in the conventional plots
due to poorer control of rosy apple aphid, sawfly and tortrix. These problems were
overcome in 2003 and 2004 by use of two early season thiacloprid sprays, one just
before blossom and one at petal fall, by the use of fenoxycarb pre-blossom against
tortrix moth caterpillars and by post harvest spraying of pirimicarb against rosy apple
aphid. Codling moth incidence was low and it was not necessary to apply sprays of
codling moth granulovirus for control.
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Table 13. % fruits (averaged across all varieties) damaged by rosy apple aphid (upper part of
table) an by all pests (including rosy apple aphid) (lower part of table) at harvest in the first
minimal pesticide residues orchard experiment at EMR in 2001-2005
The results achieved in the six years of the project (2001-2006) for the zero pesticide
residue strategy were excellent. They showed that the EMR Minimum Residues IPDM
programme for apples can give satisfactory results, even on highly disease susceptible
varieties in years when there is a high risk of scab. The zero residue programme
resulted in as good as or better control of scab than in the conventional. The key to
success depends on dealing with disease problems during the winter dormant period
and pre-blossom, so that inoculum carryover from one season to the next, and into the
post blossom period, is negligible. Assuming disease control pre-blossom has been
successful, the main disease problems post bloom were powdery mildew and storage
rots.
Control of mildew during the summer in this experiment relied on the use of sulphur,
the dose applied and spray interval being determined by mildew risk identified by ADEM.
The zero residue strategy gave acceptable mildew control, but it was not as good as
the conventional. Further work is needed to investigate alternative methods of mildew
control, such as use of biocontrol agents and materials that increase the resistance of
apple leaves to mildew. If successful these methods will eventually replace sulphur for
mildew control in the summer. Storage rot control was also satisfactory under the zero
residue programme, but other approaches are needed for Nectria rot and other cheek
rots. Pest control in the zero residue system was also satisfactory.
Since completion of this 6 year field trial at EMR, large scale grower trials have
been conducted in apple orchards throughout southern England. Results have been
mixed. Difficulties with scab control on the highly susceptible variety Gala occurred in
2008, an exceptionally wet summer and autumn.
7.1.2. Minimal residue IPDM programmes for soft fruit crops

Soft fruit crops are also highly susceptible to a wide range of damaging pests and
diseases and adequate yields of fruit of acceptable quality cannot be produced and
the crops cannot be grown profitably unless these pests and diseases are efficiently
controlled. Although biological control agents are used for several important pests of
soft fruit, soft fruit producers rely on pesticides. Pesticide applications are often made
close to harvest, giving rise to detectable levels of pesticide residues in fruit. >50% of
harvested soft fruit contains reportable levels of pesticide residues and many samples
contain multiple residues. Similar approaches described above for apple can also be
applied to soft fruit crops.
A 5 year HortLINK project (HL0175) started on 1 April 2006 to develop sustainable
methods of integrated management of Botrytis, powdery mildew, raspberry beetle,
cane midge (with associated disorder ‘midge blight’) and aphids on protected raspberry
crops that do not rely on sprays of fungicides and insecticides during flowering or fruit
development so that quality fruit can be produced with minimal risk of occurrence of
detectable pesticide residues at harvest. Science partners are East Malling Research,
ADAS, Scottish Crop Research Institute, Natural Resources Institute and, as a sub-
contractor, the Central Science Laboratory. Industry partners are K G Growers Ltd,
Berry World Ltd, Summer Fruit Company, Marks & Spencer plc, Waitrose, AgriSense,
Horticultural Development Council, East Malling Trust, East Malling Ltd, Bayer Crop
Sciences, LEAF, The Worshipful Company of Fruiterers, Assured Food Standards 2003
Ltd and the Co-Op.
Based on the research conducted in the first 3 years of the project, a Minimal
Pesticide Residue Integrated Pest and Disease Management programme has been
devised ready for testing in years 4 and 5 of the project. The key features of this
programme are:
1. Good crop hygiene and cane management together with rapid fruit cooling and
high quality cool chain marketing to avoid the need for fungicide sprays for Botrytis
2. Application of 1-2 sprays of a powdery mildew fungicide in the spring as soon as the
tunnel is covered then spray potassium bicarbonate subsequently for eradication of
powdery mildew if the disease is observed
3. Use of 50+ raspberry beetle host volatile funnel traps with white cross vanes/ha
to direct sprays of Calypso only where exceeding threshold traps catches indicate
where local (e.g. hot spots within tunnels, whole tunnels or field-grown crops in
adjacent fields and whole farm level) treatment is necessary. Note that no Calypso
sprays were applied in the trial in Kent, even though the traps catch threshold was
greatly exceeded
4. Application a sex pheromone attract and kill treatment for raspberry cane midge.
5. Application an autumn spray of thiacloprid (Calypso) for aphid control supplemented
with introductions of predators and parasites for biocontrol in summer
In 2009, this minimal residues IPDM programme for raspberries was tested in large
scale (~ 1 ha) unreplicated plots at farms in Kent, Cambridgeshire and Scotland, with
promising results.
79 Jerry Cross
7.1.3. Recent developments

The mandatory harvest intervals on pesticide labels are designed to ensure that
pesticide residue levels do not exceed Maximum Residue Levels. Much longer harvest
intervals are likely to be required to minimise the residue levels above reporting limits.
With the help of guidance from Agrochemical companies in some instances, producer
organisations have attempted to correlate the occurrence of residues data from their
routine residue monitoring programmes with last application dates from their growers
spray programmes to determine what harvest intervals are necessary to minimise
the risk of reportable residues. Statutory and minimal residues harvest intervals used
currently in the UK and Belgium (Piet Creemers, pers. comm.) are given in Table 14
overleaf.
Table 14. Statutory harvest intervals and harvest intervals recommended for minimal risk of the occurrence of reportable residue at harvest
on apple in the UK and Belgium To spray, or not to spray: That is the question
80
81 Jerry Cross
Markets are now focussed on residue presence or absence and the numbers of residues
that occur above threshold levels they set well below Maximum Residue Levels, e.g.
30% of MRLs. Eliminating residues poses different levels of difficulty on different crops.
The NZ apple industry has risen to the challenge and will in future be supplying UK
retailers with residue free apples. Has the UK apple industry got the will to match them?
There are two factors that are making the task of eliminating residues difficult and
frustrating. These are 1) the lowering of official reporting limits for various pesticides
from 0.05 to 0.01 mg/kg (enabled by the new LC-MSMS analysis technology) 2) varying
results obtained in pesticide residue analysis in different accredited laboratories. This
large variation (up to 10 fold) in results from different laboratories is considered to be
largely due to sample taking and preparation rather than the chemical analysis itself.
The problems that these two factors cause are illustrated by the recent history
of residues on apples experienced by one of the UK’s major producer organisations,
WorldWideFruit. Since 2001, they have made ongoing serious efforts to reduce the
occurrence of residues in apples. Post harvest treatments for rots and scald have
been phased out. Harvest intervals for high residue risk pesticide products have been
extended. The result has been that the average pesticide residue level has fallen from
0.29 mg/kg in 2000 to 0.14 mg/kg in 2008, a 52% reduction. If the recent use of pre-
harvest sprays of boscalid + pyraclostrobin (Bellis, Signum) and cyprodinil + fludioxinil
(Switch) had not occurred, the average residue level would be 0.09 mg/kg, a 3.2 fold
reduction. But these efforts have been made against a background of reducing official
reporting limits. Very good progress in the reduction in the frequency of occurrence of
pesticide residue levels above Reporting Limits was being made until 2007, when 77%
of samples were residue free. The lowering of the reporting limit of boscalid (contained
in Bellis and Signum) and other active ingredients from 0.05 to 0.01 mg/kg in 2008
made elimination of residues much more difficult. In reality, WorldWideFruit have made
great progress achieving a 5 fold reduction in the frequency of occurrence residues
above 0.05 mg per kg between 2006 and 2008. But the percentage of samples with
residues above the official reporting limits has risen from 23% in 2006 to 78% in 2008.
The goal posts have been moved!
The UK apple industry should not give up! Experiences from other EU countries
(e.g. Belgium) suggest that some of our harvest intervals for zero residues need to
be extended. UK apple growers also need to consider carefully whether pre-harvest
spraying for rots (e.g. with Switch or Bellis) is really necessary. The main rots of apple
in the UK are brown rot, botrytis, phytophthora, penicillium and nectria, the importance
of which varies with season and orchard, rainfall being the most critical factor. Pre-
harvest fungicide application has little effect on control of brown rot but will control
phytophthora. However, the latter rot can be equally well controlled by selective picking
in place of late fungicide application. Fungicide applied at blossom and petal fall will
control other rots such as nectria.
8. Summary, conclusions and future

perspectives
The answer to the question ‘To spray, or not to spray’ is clearly a very complex one.
Currently, to abandon spraying altogether would be commercially disastrous for most
crops and particularly UK fruit crops which suffer from such a diverse range of damaging
pests and diseases. Even organic fruit growers spray intensively! Overcoming reliance
on pesticide spraying in production of horticultural crops is one of the greatest and
most important challenges we face. There are clearly huge opportunities to reduce
spraying, through pre-emptive avoidance strategies and the use of alternative non-
chemical control methods such as those described above and by using pest monitoring
and forecasting models so that pesticide sprays are only applied when absolutely
necessary. Many methods have been or are being developed but are not commercially
implemented on a significant scale. In many instances this is because there are practical
snags and difficulties with the systems, because they are more complex or difficult to
manage and/or because they are more costly than pesticides. Market forces including
retailer production protocols and quality assurance schemes will continue to pressurise
for reductions in pesticide use and the implementation of alternative pest and disease
management strategies. Markets and consumers will not countenance a reduction in
quality standards. Indeed, these are likely to continue to rise.
Applied entomological research is vital to horticulture. The crop protection
problems that occur on different crops are continually changing as a result of many
factors including changing varieties and crop production methods, changing pesticide
availability, the development of pesticide resistance, the arrival of new invasive pests,
crop adaptation by native species and climate change. There is a need to greatly
increase food production in the face of world population growth but this needs to be
done sustainably reducing dependence on pesticides. Use of pesticide sprays will not
die out suddenly. It will only reduce gradually as alternative solutions are developed as
a result of a sustained multi-facetted international research effort.
Research by horticultural entomologists to tackle the problems faced will be
needed throughout the 21st century and beyond. Progress will be most rapid if
close and exemplary collaboration between research institutes and universities with
complimentary and excellent expertises, such as that between EMR and NRI, University
of Greenwich, as well as internationally, is supported and strengthened.
83 Jerry Cross
Acknowledgements
I am greatly indebted to Michelle Fountain, Adrian Harris, Csaba Nagy and the many
temporary members of our team at EMR, and to my closest collaborators David Hall,
NRI, Peter Walklate and Angela Berrie, EMR, whose excellent skills and knowledge have
been vital to our joint successes, and to numerous other colleagues and collaborators,
only a few of whom are mentioned in this paper. Geoff Richardson and Dudley Farman
have provided excellent technical support in much of the work described above. PhD
studies by Paul Innocenzi, Lakmali Amarawardana and Csaba Nagy have made an
enormous contribution. Thanks to Mike Solomon, Csaba Nagy and David Hall for editing
this document. I am most grateful to Adrian Barlow, David Cole, Oliver Doubleday,
Richard Harnden, Martin Luton, Graham Matthews, Tom Maynard, Rob Saunders,
Robert Oliver and numerous others for their support and encouragement. In over 30
years as a fruit entomologist I have conducted hundreds of field experiments, mainly on
fruit farms in Kent. I am very grateful to all those who have so generously and patiently
hosted these trials. I am still often astonished by how accommodating and supportive
fruit growers are, and what a wonderful industry it is to work for.
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NATURAL RESOURCES INSTITUTE

To spray, or not to spray:

Jerry Cross, Visiting Professor of

Inaugural Professorial Lecture

An Inaugural Professorial Lecture

2. Avoiding the need for pesticide spraying 5

3. Deciding if and when to treat 26

4. Treating at different times of the season 50

7. Integrated pest and disease management (IPDM) 72

8. Summary, conclusions and future perspectives 82

To spray, or not to spray:

1.1. The pesticide dilemmas

1.2. The spraying process

1.3. Lecture topics

2. Avoiding the need for pesticide spraying

2.1. Resistant varieties

programmes need to be expanded greatly if substantive progress is to be made. GM

2.2. Conserving and exploiting natural enemies

2.3. Manipulating and exploiting ants in the management of

2.3.1. Ant exclusion or supplementary feeding

2.3.2. Exploitation to vector entomopathogenic fungi

Kelleytunis et al., 1995). In comparison, no infection was observed in either workers or

Figure 6. a) Scanning Electron Micrograph of spores of the entomopathogenic fungus L.

2.3.3. 21st century perspectives

L. neglectus forms ‘super colonies’, a system of interconnected nests with many

2.4. Conservation biocontrol

2.4.1. Conservation biocontrol for pear sucker, Cacopsylla spp.

Anthocorid predatory bugs (Figure 9) (especially Anthocoris nemoralis Fabricius) have

Orchards in the UK are usually surrounded by windbreaks and/or hedgerows. The

One important objective of the Horticulture LINK project is to develop conservation

2.4.2. 21st century perspectives

3. Deciding if and when to treat

3.1. Physically-acting monitoring traps

3.1.1. Mussel scale

Temperature loggers were deployed to take hourly readings of air temperatures.

3.2. Semiochemical monitoring traps

Allelochemicals, are chemicals that are significant to individuals of a species different

3.2.1. Gall midge sex pheromone monitoring traps

3.2.2. Capsid bug sex pheromone monitoring traps

Further scientific work was needed to understand the mechanisms and

3.2.3. Strawberry blossom weevil aggregation pheromone/host

3.3. Predictive models

3.3.1. Blackcurrant gall mite emergence forecasting model

4. Treating at different times of the season

4.1. Autumn control of aphids

Thus, we have demonstrated that autumn application of aphicides gives good

5.1. Semiochemical based control methods

5.1.1. Mating Disruption (MD) and Attract and Kill (A&K)

In 2008, a new MD treatment comprising 3 kg/ha of 0.5% w/w pheromone racemate

Regrettably, the SPLAT + deltamethrin treatment was unsuccessful in suppressing

So to date, despite much effort, we have not managed to produce a successful

5.3.1. Mass trapping

6. Safer more efficient orchard spray

6.2. Dose expression and adjustment

7. Integrated Pest and Disease Management

7.1. Minimal residues IPDM

Table 9. Occurrence of pesticide residues above reporting limits in 2003 government

7.1.1. The EMR minimum residues IPDM programme for

7.1.2. Minimal residue IPDM programmes for soft fruit crops

7.1.3. Recent developments

8. Summary, conclusions and future

D3076-9 February 2010

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