Professional Documents
Culture Documents
by
Jerry Cross, East Malling Research
Visiting Professor of Horticultural Entomology,
Natural Resources Institute, University of Greenwich
University of Greenwich, a charity and company limited by guarantee, registered in England (reg. no.
986729). Registered Office: Old Royal Naval College, Park Row, Greenwich, London SE10 9LS
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
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
Acknowledgements 83
References 83
1 Jerry Cross
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
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.
To spray, or not to spray: That is the question 4
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
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.
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
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).
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.
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)
To spray, or not to spray: That is the question 12
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.
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
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
To spray, or not to spray: That is the question 16
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.
Figure 7. Small colony of the invasive ant Lasius neglectus. Photo courtesy Csaba Nagy
To spray, or not to spray: That is the question 18
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.
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
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
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
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
To spray, or not to spray: That is the question 24
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).
To spray, or not to spray: That is the question 26
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
To spray, or not to spray: That is the question 30
Figure 13. Mean numbers of mussel scale crawlers captured cm-1 of sticky band per day in
2007, 2008 and 2009
31 Jerry Cross
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
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
To spray, or not to spray: That is the question 34
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
To spray, or not to spray: That is the question 36
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.
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.
To spray, or not to spray: That is the question 38
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
To spray, or not to spray: That is the question 40
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.
To spray, or not to spray: That is the question 42
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)
To spray, or not to spray: That is the question 44
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
To spray, or not to spray: That is the question 48
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
To spray, or not to spray: That is the question 50
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.
To spray, or not to spray: That is the question 52
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
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.
To spray, or not to spray: That is the question 56
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.
To spray, or not to spray: That is the question 58
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)
To spray, or not to spray: That is the question 60
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).
To spray, or not to spray: That is the question 62
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.
Table 6. Effectiveness of MD and A&K treatments in suppressing sex pheromone trap catches
and larval infestations of R. theobaldi in 2007
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
To spray, or not to spray: That is the question 64
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.
Table 7. Effectiveness of MD and A&K treatments in suppressing sex pheromone trap catches
and larval infestations of R. theobaldi in 2008
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.
65 Jerry Cross
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
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.
To spray, or not to spray: That is the question 66
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)
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
To spray, or not to spray: That is the question 68
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
To spray, or not to spray: That is the question 70
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
To spray, or not to spray: That is the question 72
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.
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”
To spray, or not to spray: That is the question 74
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.
• 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.
To spray, or not to spray: That is the question 76
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.
77 Jerry Cross
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.
To spray, or not to spray: That is the question 78
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
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.
To spray, or not to spray: That is the question 82
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.
References
Addicott, J. F., 1979. A multispecies aphid-ant association: density dependence and
species-specific effects. Canadian Journal of Zoology 57, 558-569.
Aldrich, J. R., 1988. Chemical ecology of the Heteroptera. Annual Review of Entomology
33, 211-238.
Amarawardana, L., 2009. The chemical diversity of midge pheromones. University of
Greenwich PhD thesis, December 2009, 184 pp.
Anderson, N. H., 1962. Bionomics of six species of Anthocoris (Heteroptera:
Anthocoridae) in England. Transactions of the Royal Entomological Society of
London 114, 67-95.
Anonymous., 2004. Pesticides Residues Committee: Pesticides Residues Monitoring
Report October-December 2004, 132 pp.
Bajwa, W. I., Kogan, M., 2002. Compendium of IPM Definitions (CID). Integrated Plant
Protection Centre (IPPC) Oregon State University, Corvallis Publication Number
998, 2002 (http://www.ipmnet.org/ipmdefinitions/index.pdf accessed 23 Dec 09)
Banks, C. J., 1958. Effects of the ant Lasius niger (L.) on the behaviour and reproduction
of the black bean aphid Aphis fabae Scop. Bulletin of Entomological Research
49, 701-714.
Banks, C. J., 1962. Effects of the ant Lasius niger (L.) on insects preying on small
populations of Aphis fabae Scop. on bean plants. Annals of Applied Biology 50,
669-679.
Barbosa, P. (Ed.), 1998. Conservation Biological Control. Academic Press, San Diego,
CA.
Bartelt, R. J., 1999. Weevils. In: Hardie, J., Minks, A. K. (Eds.), Pheromones of Non-
Lepidopteran Insects Associated with Agricultural Plants. CABI Publishing, UK,
pp. 91–112.
Beattie, A. J., Turnbull, C., Hough, T., Jobson, Knox, R. B., 1985. The vulnerability
of pollen and fungal spores to ant secretions: evidence and some evolutionary
implications. American Journal of Botany 72, 606-614.
To spray, or not to spray: That is the question 84
Berrie A. M., Cross., J. V., 2005. Development of an integrated pest and disease
management system for apples to produce fruit free from pesticide residues.
IOBC/WPRS Bulletin 28(7), 23-31.
Berrie, A. M., 2000. Pre-harvest assessment of the risk of storage rots in Cox apples.
IOBC/WPRS Bulletin 23, 159-169.
Berrie, A. M., Cross, J. V., 2006. Development of an integrated pest and disease
management system for apples to produce fruit free from pesticide residues -
aspects of disease control. IOBC/WPRS Bulletin 29 (1), 129-138.
Berrie, A. M., X. –M. Xu., 2003. Managing apple scab and powdery mildew using
ADEM™. International Journal of Pest Management 49, 243-250.
Bhatkar, A. P., Whitcomb, W. H., 1970. Artificial diet for rearing various species of ants.
Florida Entomologist 53, 229-232.
Bird, A. E., 2002. The common black ant (Lasius niger) as a vector for the entomopathogen
Verticillium lecanii to rosy apple aphid (Dysaphis plantaginea). M.Sc. thesis,
Imperial College of Science, Technology & Medicine, Wye, UK.
Bird, A. E., Hesketh, H., Cross, J. V., Copland, M., 2004. The common black ant,
Lasius niger (Hymenoptera: Formicidae), as a vector of the entomopathogen
Lecanicillium longisporum to rosy apple aphid, Dysaphis plantaginea (Homoptera:
Aphididae). Biocontrol Science and Technology 14, 757-767.
Blommers, L. H. M., 1994. Integrated pest management in European apple orchards.
Annual Review of Entomology 39, 213-41.
Blommers, L., Bus, V., de Jongh, E., Lentjes, G., 1988. Attraction of males by virgin
females of the green capsid bug, Lygocoris pabulinus (Heteroptera: Miridae).
Entomologische Berichten Amsterdam 48, 175-179.
Blum, M. S., 1981. Chemical Defenses of Arthropods. Academic Press Inc., New York.
Blum, M. S., 1996. Semiochemical parsimony in the arthropoda. Annual Review of
Entomology 41, 353-374.
Brennan, R. M., 2008. Currants and gooseberries (Ribes spp.). pp. 177-196. In:
Temperate Fruit Crop Breeding: Germplasm to Genomics, ed. J. Hancock
(Springer).
Brennan, R., Jorgensen, L., Gordon, S. L., Loades, K., Hackett, C., Russell, J., 2009.
The development of a PCR-based marker linked to resistance to the blackcurrant
gall mite (Cecidophyopsis ribis Acari: Eriophyidae). Theoretical and Applied
Genetics 118, 205-212.
Buckley, C. R., 1987 Interactions involving plants, Homoptera and ants. Annual Review
of Ecology and Systematics 18, 111-135.
Budenberg, W. J., 1990. Honeydew as a contact kairomone for aphid parasitoids.
Entomologia Experimentalis et Applicata 55, 139-148.
Bus, V. G. M., Mols, P. J. M., Blommers, L. H. M., 1985. Monitoring of green capsid bug
Lygocoris pabulinus (Hemiptera: Miridae) in apple orchards. Mededelingen van
de Faculteit Landbouwwentenschappen Rijksuniversiteit Gent 50(2b), 505-510.
Butt, T. M., Carreck, N. L., Ibrahim, L., Williams, I. H., 1998. Honeybee mediated
infection of pollen beetle (Meligethes aeneus Fab.) by the insect pathogenic
fungus, Metarhizium anisopliae. Biocontrol Science and Technology 8, 533-538.
Carter, M. C., Dixon, A. F. G., 1984. Honeydew: an arrestant stimulus for coccinellids.
Ecological Entomology 9, 383-387.
Cherix, D., 1987. Relation between diet and polyethism in Formica colonies. In.
Pasteels, J. M., Deneubourg, J. L. (eds). From Individual to Collective Behavior in
Social Insects Birkhausel, Basel, 93-115.
85 Jerry Cross
Choi, M. Y., Roitberg, B. D., Shani, A., Raworth, D. A., Lee, G. H., 2004. Olfactory
response by the aphidophagous gall midge, Aphidoletes aphidimyza to
honeydew from green peach aphid, Myzus persicae. Entomologia Experimentalis
et Applicata 111, 37-45.
Cocu, N., Harrington, R., Hullé, M., Rounsevell, M. D. A., 2005. Spatial autocorrelation
as a tool for identifying the geographical patterns of aphid annual abundance.
Agriculture and Forest Entomology 7, 31–43.
Coll, M., Guershon, M., 2002. Omnivory in terrestrial arthropods: mixing plant and prey
diets. Annual Review of Entomology 47, 267–297.
Collier, R. H., Finch, S., 1985. Accumulated temperatures for predicting the time
of emergence in spring of the cabbage root fly, Delia radicum (L.) (Diptera:
Anthomyiidae). Bulletin of Entomological Research 75, 395-404.
Collins, C. M., Leather, S. R., 2002. Ant mediated dispersal of the black willow aphid
Pterocomma salicis L.; does the ant Lasius niger L. judge aphid-host quality?
Ecological Entomology 27, 238-241.
Conti, E., Frati, F., Salerno, G., Bin, F., Birkett, M. A., Chamberlain, K., Pickett, J. A.,
Woodcock, C. M., 2006. Role of the host plant, Vicia faba, and induced volatiles
in host location and sexual communication of Lygus rugulipennis. 22nd Annual
Meeting of the International Sciety of Chemical Ecology, Barcelona, Spain, July
2006. Abstract S5-O2.
Conway, G. R., 1984. Tactical models. In: Conway, G. R. (ed.), Pest and Pathogen
Control: Strategic, Tactical and Policy Models. John Wiley & Sons, Cichester,
209-220.
Cremer, S., Ugelvig, L. V., Lommen, S. T. E., Petersen, K. S., Pedersen, J. S.,
2006. Attack of the invasive garden ant: aggression behaviour of Lasius
neglectus (Hymenoptera: Formicidae) against native Lasius species in Spain.
Myrmecologische Nachrichten 9, 13-19.
Cross J. V., Berrie, A. M., 2008. Eliminating Reportable Pesticide Residues from Apples.
9th Workshop on Sustainable Plant Protection Techniques in Fruit Growing at
Alnarp, Sweden on 11-14 September 2007. Agricultural Engineering International,
The CIGR Ejournal, 8 pp.
Cross J. V., Berrie, A. M., 2005. Producing apples free of pesticide residues. Proceedings
of 2005 BCPC International Congress, 775-782.
Cross, J. V., Baroffio, C., Grassi, A., Hall, D., Labanowska, B., Milenković, S., Nilsson, T.,
Shternshis, M., Tornéus, C., Trandem, N., Vétek, G., 2008. Monitoring raspberry
cane midge, Resseliella theobaldi, with sex pheromone traps: results from 2006.
IOBC/WPRS Bulletin 39, 11-17.
Cross, J. V., 2004. European tarnished plant bug on strawberries and other soft fruits.
Horticultural Development Council Fact Sheet 19/04, 6 pp.
Cross, J. V., Berrie, A. M., 1994. Sampling and assessment of pests and diseases as
the basis for decision making in orchards in the UK. Aspects of Applied Biology
37, 225-36.
Cross, J. V., Berrie, A. M., 2001. Integrated pest and disease management in apple
production. In: The Best Practice Guide for UK Apple Production, Department
for Environment, Food & Rural Affairs (Defra), Horticulture Research International,
Farm Advisory Services Team Ltd, ADAS, Worldwide Fruit/Qualytech, pp. 2.1-
2.94.
To spray, or not to spray: That is the question 86
Cross, J. V., Cubison, S., Harris, A., Harrington, R., 2007. Autumn control of rosy apple
aphid, Dysaphis plantaginea (Passerini), with aphicides. Crop Protection 26,
1140–1149.
Cross, J. V., Easterbrook M. A., Crook, M. A., Crook, D., Fitzgerald, J. D., Innocenzi,
P., Jay, C. N., Solomon, M. G., 2001. Review: natural enemies and biocontrol
of pests of strawberry in northern and central Europe. Biocontrol Science and
Technology 11, 165-216.
Cross, J. V., Hall, D. R., 2003. Pheromones of strawberry blossom weevil and European
tarnished plant bug for monitoring and control in strawberry crops. Final report of
Defra project HH1939SSF issued August 2003, 30 pp.
Cross, J. V., Hall, D. R., 2005. Pheromones. PCT/GB2005/002504.
Cross, J. V., Hall, D. R., 2007. Exploiting the sex pheromone of the apple leaf midge,
Dasineura mali, for pest monitoring and control. In: Proceedings of IOBC
Arthropods Sub Group Meeting Lleida Spain September 2006. IOBC Bulletin
30(4), 159–167.
Cross, J. V., Hall, D. R., Innocenzi, P. J., Hesketh, H., Jay, C. N., Burgess, C. M., 2006b.
Exploiting the aggregation pheromone of strawberry blossom weevil Anthonomus
rubi (Coleoptera: Curculionidae): Part 2. Pest monitoring and control. Crop
Protection 25, 155–166.
Cross, J. V., Hall, D. R., Shaw, P., Anfora, G., Shaw, P., Anfora, G., 2009a. Exploitation
of the sex pheromone of apple leaf midge Dasineura mali Kieffer (Diptera:
Cecidomyiidae): Part 2. Use of sex pheromone traps for pest monitoring. Crop
Protection 28, 128–133
Cross, J. V., Harris, A. L., 2004. Exploiting natural enemies in Integrated Pest
Management in blackcurrant crops. IOBC Bulletin 27(4), 9-16.
Cross, J. V., Harris, A. L., 2006. IPM methods for blackcurrant gall mite and leaf
midge: synthesis, validation and implementation in UK commercial blackcurrant
production. Report of Defra project HH3115STF issued December 2006, 30 pp.
Cross, J. V., Hesketh, H., Jay, C. N., Hall, D. R., Innocenzi, P. J., Farman, D. I., Burgess,
C. M., 2006a. Exploiting the aggregation pheromone of strawberry blossom
weevil Anthonomus rubi Herbst (Coleoptera: Curculionidae): Part 1. Development
of lure and trap. Crop Protection 25, 144–154
Cross, J. V., Ridout, M. S., 2001. Emergence of blackcurrant gall mite (Cecidophyopsis
ribis) from galls in spring. Journal of Horticultural Science and Biotechnology 76,
311-319.
Cross, J. V., Solomon, M. G., Babandreier, D., Blommers, L., Easterbrook, M. A., Jay,
C. N., Jenser, G., Jolly, R. L., Kuhlmann, U., Lilley, R., Olivella, E., Toepfer, S.,
Vidal, S., 1999a. Biocontrol of pests of apples and pears in Northern and Central
Europe: 2. Parasitoids. Biocontrol Science Technology 9, 277–314.
Cross, J. V., Solomon, M. G., Chandler, D., Jarrett, P., Richardson, P. N., Winstanley,
D., Bathon, H., Huber, J., Keller, B., Langenbruch, A., Zimmermann, G., 1999b.
Review of Biocontrol of Pests of Apples and Pears in Northern and Central
Europe: (1) Microbial Agents and Nematodes. Biocontrol Science and Technology
9, 125-149.
Cross, J. V., Walklate, P. J., Miller, P. N., 2009b. Low drift rating of broadcast air-assisted
sprayers for UK horticulture: a review to establish LERAP reduced drift status.
Report on Pesticides Safety Directorate project PS2019 issued 18 December
2009, 31 pp.
87 Jerry Cross
Cross, J. V., Yeo, H., 2002. Evaluation of Insecticides for Control of Apple Leaf Midge
2001 and 2002. Final Contract Report for APRC Project SP129. 22 pp.
Cross, J. V., Walklate, P. J., Murray, R. A., Richardson, G. M., 2003. Spray deposit and
losses in different size apple trees from an axial fan orchard sprayer; 3: effects of
air volumetric flow rate. Crop Protection 22, 381-394.
Cross, J. V., Walklate, P. J., Murray, R. A., Richardson, G. M., 2001a. Spray deposit and
losses in different size apple trees from an axial fan orchard sprayer: 1. Effects of
spray liquid flow rate. Crop Protection 20, 13–30
Cross, J. V., Walklate, P. J., Murray, R. A., Richardson, G. M., 2001b. Spray deposit and
losses in different size apple trees from an axial fan orchard sprayer; 2: effects of
spray quality. Crop Protection 20, 333–343
Dent, D., 1991. Insect Pest Management. CAB International, Wallingford, Oxon, UK.
Downham, M. C. A., Cork, A., Farman, D., Hall, D., Innocenzi, P., Phythian, S., Padi,
B., Lowor, S., Sarfo, J., 2002. Sex pheromone components of the cocoa mirids,
Distantiella theobroma and Sahlbergella singularis (Hetroptera: Miridae). p. 167 in
Abstract Book, 19th Annual Meeting of International Society of Chemical Ecology,
Hamburg, Germany, 3-7 August 2002.
Drijfhout, F. P., Groot, A. T, Posthumus, M. A, van Beek, T. A, de Groot, A., 2002. Coupled
gas chromatographic-electroantennographic responses of Lygocoris pabulinus
(L.) to female and male produced volatiles. Chemoecology 12, 113-118.
Drijfhout, F. P., Groot, A. T, van Beek, T. A., Visser, J. H., 2003. Mate location in the
green capsid bug, Lygocoris pabulinus. Entomologia Experimentalis et Applicata
106, 73-77.
Drijfhout, F. P., van Beek, T. A., Visser, J. H., de Groot, A., 2000. On-line thermal
desorption-gas chromatography of intact insects for pheromone analysis.
Journal of Chemical Ecology 26, 1383-1392.
Drijfhout, F. P., 2001. Studies towards the sex pheromone of the green capsid bug.
PhD thesis, Wageningen University, The Netherlands, pp. 152.
Drijfhout, F. P., Groot, A. T., 2001. Close-range attraction in Lygocoris pabulinus. Journal
of Chemical Ecology 27, 1133-1149.
Dromph, K. M., 2003. Collembolans as vectors of entomopathogenic fungi. Pedobiologia
47, 245-256.
Eilenberg, J., Hajek, A., Lomer, C., 2001. Suggestions for unifying the terminology in
biological control. BioControl 46, 387–400.
El-Ziady, S., 1960. Further effects of Lasius niger L. on Aphis fabae Scopoli. Proceedings
of the Royal Entomological Society of London A 35, 30-38.
El-Ziady, S., Kennedy, J. S., 1956. Beneficial effects of the common garden ant, Lasius
niger L., on the black been aphid, Aphis fabae Scopoli. Proceedings of the Royal
Entomological Society of London A 31, 61-65.
Espadaler, X., Rey, S., 2001. Biological constraints and colony founding in the
polygynous invasive ant Lasius neglectus (Hymenoptera, Formicidae). Insectes
Sociaux 48, 159-164.
Espadaler, X., Bernal, V., 2010. Lasius neglectus, a polygynous, sometimes invasive,
ant. – <http://www.creaf.uab.es/ xeg/Lasius/Ingles/index.htm>, retrieved on 4
January 2010.
Espadaler, X., Rey, S., Bernal, V., 2004. Queen number in a supercolony of the invasive
garden ant, Lasius neglectus. Insectes Sociaux 51, 232-238.
To spray, or not to spray: That is the question 88
Espadaler, X., Tartally, A., Schultz, R., Seifert, B. Nagy, C., 2007. Regional trends and
preliminary results on the local expansion rate in the invasive garden ant, Lasius
neglectus (Hymenoptera, Formicidae). Insectes Sociaux 54, 293-301.
Feng, M., Johnson, J. B. Kish, L. P., 1990. Virulence of Verticillium lecanii and an aphid-
derived isolate of Beauveria bassiana (Fungi: Hyphomycetes) for six species of
cereal-infesting aphids (Homoptera: Aphididae). Environmental Entomology 19,
815-820.
Fiedler, A. K., Landis, D.A., 2007a. Attractiveness of Michigan native plants to arthropod
natural enemies and herbivores. Environmental Entomology 36, 751–765.
Fiedler, A. K., Landis, D. A., 2007b. Plant characteristics associated with natural enemy
abundance at Michigan native plants. Environmental Entomology 36, 878–886.
Flatt, T., Weisser, W., 2000. The effect of mutualistic ants on aphid life history traits.
Ecology 81, 3522-3529.
Flower, E., 2002. The Trojan ant: infecting aphids with the fungus V. lecanii using the ant
Lasius niger. B.Sc. thesis, Imperial College of Science, Technology & Medicine,
Wye, UK.
Foster, S. P., Harris, M. O., Millar, J. G., 1991. Identification of the sex pheromone of the
Hessian fly, Mayetiola destructor (Say.) Naturwissenschaften 78, 130-131.
Gagne, R. J., 1989. The Plant Feeding Gall Midges of North America. Cornell University
press.
Gagne, R. J., 1994. The Gall Midges of the Neotropical Region. Cornell University press.
Garthwaite, D. G.,Thomas, M. R., 2001. Pesticide useage survey report 181: Soft fruit
in Great Britain, 42 pp
Garthwaite, D. G.,Thomas, M. R., Dean, S. M., 2000. Pesticide useage survey report
172: Orchards and fruit stores in Great Britain, 39 pp.
Gessler, C., Broggini, G., Parravicini1, G., Galli, P., Szankowski, I., Paris, R. Patocchi,
A., 2010. Genetic modification of apple to control diseases. IOBC Bulletin, 12-13
Glinwood, R., Pettersson, J., Kularatne, S., Ahmed, E., Kumar, V., 2003. Female
European tarnished plant bugs, Lygus rugulipennis (Heteroptera: Miridae), are
attracted to odours from conspecific females. Acta Agriculturæ Scandinavica
Section A, 53, 29-32.
Goettel, M. S., Poprawski, T. J., Vandenberg, J. D., Li, Z., Roberts, D. W., 1990. Safety
to nontarget invertebrates of fungal biocontrol agents, in Safety of Microbial
Insecticides (Laird, M., Lacey, L.A., Davidson, E.W., Eds.). CRC Press, Boca
Raton, FL, pp. 209-231.
Gordon, S. C., Brennan, R. M., Jones, A. T. Fenton, B., Birch, A. N. E., 1994. The
blackcurrant gall mite (Cecidophyopsis ribis): its biology and strategies for
control. Proceedings of the Brighton Crop Protection Conference 1994, 577-582.
Gracia-Garza, J. A., Fravel, D. R., Bailey, B. A., Hebbar, P. K., 1997. Dispersal of
formulations of Fusarium oxysporum f. sp. erythroxyli and F. oxysporum f. sp.
melonis by ants. Phytopathology 88, 185-189.
Gries, R., Gries, G., Khaskin, G., King, S., Olfert, O., Kaminski, L-A., Lamb, R.,
Bennett, R., 2000. Sex pheromone of orange wheat blossom midge, Sitodiplosis
mosellana. Naturwissenschaften 87, 450-454.
89 Jerry Cross
Gries, R., Khaskin, G., Gries, G., Bennett, R. G., Skip King, G. G., Morewood, P.,
Slessor, K. N., Morewood, D., 2002. (Z,Z)-4,7-Tridecadien-(S)-2-yl acetate: sex
pheromone of Douglas fir cone gall midge. Journal of Chemical Ecology 28,
2283-2297.
Griffiths, G. J. K., Holland, J. M., Bailey, A., Thomas, M. B., 2008. Efficacy and
economics of shelter habitats for conservation biological control. Biological
Control 45, 200–209.
Groot, A. T., 2000. Sexual behaviour of the green capsid bug. PhD thesis, Wageningen
University, The Netherlands, pp. 156.
Groot, A. T., Drijfhout, F. P., Heijboer, A., van Beek, T. A., Visser, J. H., 2001. Disruption
of sexual communication in the mirid bug Lygocoris pabulinus by hexyl butyrate.
Agriculture and Forest Entomology 3, 49-55.
Groot, A. T., Timmer, R., Gort, G., Lelyveld, G. P., Drijfhout, F. P., van Beek, T. A., Visser,
J. H., 1999. Sex-related perception of insect and plant volatiles in Lygocoris
pabulinus. Journal of Chemical Ecology 25, 2357-2371.
Gueldner R. C., Parrot W. L., 1978. Volatile constituents of the tarnished plant bug.
Insect Biochemistry 8, 389-391.
Gurr, G. M., Wratten, S. D., Altieri, M. A. (Eds.), 2004. Ecological Engineering for
Pest Management—Advances in Habitat Manipulation for Arthropods. CSIRO
Publishing, Melbourne, Australia.
Hall, D. R., Cross, J. V., 2006., Semiochemicals in Management of Apple Leaf Midge
Final report of Defra project HH3114TTF. Available from: http://www.defra.gov.
uk/science/Project_Data/DocumentLibrary/HH3114TTF/HH3114TTF_3999_FRP.
doc, 23 pp.
Hall, D. R., Farman, D. I., Cross, J. V. Pope, T. W., Ando, T., Yamamoto, M., 2009. (S)-2-
Acetoxy-5-Undecanone, Female Sex Pheromone of the Raspberry Cane Midge,
Resseliella theobaldi (Barnes). Journal of Chemical Ecology 35, 230-242.
Hall, R. A., 1981. The fungus Verticillium lecanii as a microbial insecticide against aphids
and scales, in Microbial Control of Pests and Plant Diseases 1970_/1980 (Burges,
H.D., Ed.). Academic Press, London, UK, pp. 483-498.
Harris, A. L., Cross, J. V., 2008. Advances in IPM for blackcurrant. IOBC Bulletin 39,
149-154
Harris, M. O., Foster, S. P., 1999. Gall midges, pp. 27–50. In: Hardie, J., Minks, A.
K. (eds.). Pheromones of Non-lepidopteran Insects Associated with Agricultural
Plants. CABI Publishing, Wallingford, UK.
Harris, M. O., Foster, S. P., Agee, K., Dhana, S., 1996. Sex pheromone communication
in the apple leafcurling midge (Dasineura mali). Proceedings of New Zealand
Plant Protection Conference 49, 52-58.
Harris, M. O., Galanhie, L. D., Sandanayake, M., 1999. Adult emergence and reproductive
behavior of the leafcurling midge Dasineura mali (Diptera: Cecidomyiidae). Annals
of the Entomological Society of America 92, 748–757.
Hatting, J. L., Humber, R. A., Poprawski, T. J., Miller, R. M., 1999. A survey of fungal
pathogens of aphids from South Africa, with special reference to cereal aphids.
Biological Control 16, 1-12.
Heath, J. J., Gaul, S. O., Nash, D. M., Smith, R. F., 1998. Evidence for a female-
produced sex pheromone in the apple leaf midge, Dasineura mali (Kieffer)
(Diptera: Cecidomyiidae). Canadian Entomologist 130, 109-110.
To spray, or not to spray: That is the question 90
Heath, J. J., Zhang, A. J., Roelofs, W. L., Smith, R. F., 2005. Flight activity and further
evidence for a female-produced sex pheromone of the apple leaf midge,
Dasineura mali, in Nova Scotia. Northeastern Naturalist 12, 93–102.
Heimpel, G. E., Jervis, M. A., 2005. Does floral nectar improve biological control by
parasitoids? In: Wäckers, F. L., van Rijn, P. C. J., Bruin, J. (Eds.), Plant-provided
Food for Carnivorous Insects: A Protective Mutualism and its Applications.
Cambridge University Press, Cambridge, UK, pp. 267–304.
Helsen, H. H. M., Blommers, L. H. M., Trapman, M. C., 1996. Timing observation and
control of mussel scale, Lepidosaphes ulmi. IOBC Bulletin 19(4), 145-149.
Helsen, H., 2001. Rosy apple aphid can also be controlled in autumn. Fruitteelt 91 (28),
12–13.
Helsen, H., Simonse, J., 2002. Influence of spray timing on the effectiveness of autumn
control of the rosy apple aphid. Fruitteelt 92 (27), 12–14.
Hill, A. R. C., Reynolds, S. L., 2002. Unit-to-unit variability of pesticide residues in fruit
and vegetables. Food Additives and Contaminants 19(8), 733-747.
Hill, A. R., 1957. The biology of Anthocoris nemorum (L.) in Scotland (Hemiptera:
Anthocoridae). Transactions of the Royal Entomological Society of London 109,
379-394.
Hill, M. G., Blackmore, P. J. M., 1980. Interactions between ants and the coccid Icerya
seychellarum on the Aldabra Atoll. Oecologia 45, 360-365.
Hillbur, Y., Anderson, P., Arn, H., Bengtsson, M., Löfqvist, J., Biddle, A. J., Smitt, O.,
Högberg, Plass, E., Franke, S., Francke, W., 1999. Identification of sex pheromone
components of the pea midge, Contarinia pisi (Diptera: Cecidomyiidae).
Naturwissenschaften 86, 292-294.
Hillbur, Y., Bengtsson, M. Löfqvist, J., Biddle, A. J., Pillon, O., Plass, E., Franke, W.,
Hallberg, E., 2001. A chiral sex pheromone system in the pea midge, Contarinia
pisi. Journal of Chemical Ecology 27, 1391-1407.
Hillbur, Y., Celander, M., Baur, R., Rauscher, S., Haftmann, J., Franke, S., Francke,
W., 2005. Identification of the sex pheromone of the swede midge, Contarinia
nasturtii. Journal of Chemical Ecology 31,1807–1828.
Hillbur, Y., El-Sayed, A., Bengtsson, M. Löfqvist, J., Biddle, A. J., Plass, E., Francke, W.,
2000. Laboratory and field study of the attraction of male pea midges, Contarinia
pisi, to synthetic sex pheromone components. Journal of Chemical Ecology 26,
1941-1952.
Himel, C. M., 1969. The optimum drop size for insecticide spray droplets. Journal of
Economic Entomology 62, 919-925.
Ho, H. Y., Millar, J. G., 2002. Identification, electroantennogram screening, and field
bioassays of volatile chemicals from Lygus hesperus Knight (Heteroptera:
Miridae). Zoological Studies 41, 311-320.
Hoehn, H., Graf, B., Hoepli, H., 2003. Control of rosy apple aphid (Dysaphis plantaginea)
in fall—preliminary results. IOBC WPRS Bulletin 26 (11), 59–64.
Innocenzi P. J., Hall, D. R., Sumathi, C., Cross J. V., Jacobson, R. J., 1998. Studies of
the sex pheromone of the European tarnished plant bug, Lygus rugulipennis (Het.
Miridae). Brighton Crop Protection Conference – Pests and Diseases 8, 829-832.
Innocenzi, P. J., Hall, D. R., Cross, J. V., Hesketh, H., 2005. Attraction of male European
tarnished plant bug, Lygus rugulipennis, to components of the female sex
pheromone in the field. Journal of Chemical Ecology 31, 1401-1413.
91 Jerry Cross
Innocenzi, P. J., Hall, D. R., Cross, J. V., Masuh, H., Phythian, S. J., Chittamuru, S.,
Guarino, S., 2004. Investigation of long-range female sex pheromone of the
European tarnished plant bug Lygus rugulipennis: chemical, electrophysiological
and field studies. Journal of Chemical Ecology 30, 1509-1529.
Innocenzi, P. J., Hall, D.R., Cross, J. V., 2001. Components of the male aggregation
pheromone of strawberry blossom weevil, Anthonomus rubi Herbst. (Coleoptera:
Curculionidae). Journal of Chemical Ecology 27, 1203–1218.
Jacobson, R. J., 1999. Capsids (Het. Miridae): A new challenge to IPM in protected
salad crops in the UK. Mededelingen van de Faculteit Landbouwwentenschappen
Rijksuniversiteit Gent 64/3a, 67-72.
Jacobson, R. J., 2001. Control of capsid bugs within IPM programmes in protected
crops. Report of contract work undertaken for HDC, October 2001, 38 pp.
Jacobson, R. J., 2002. Lygus rugulipennis Poppius (Het. Miridae): Options for integrated
control in glasshouse-grown cucumbers. IOBC/WPRS Bulletin 25 (1), 111-114.
Jacobson, R., Hargreaves, D., 1996. Capsid bugs in protected crops. A guide to the
recognition of capsids and the damage they cause. Horticultural Development
Council Fact Sheet 37/96, December 1996, 4 pp.
Jay, C. N., Cross, J. V., Burgess, C. M., 2004. The relationship between populations of
European tarnished plant bug (Lygus rugulipennis) and crop losses due to fruit
malformation in everbearer strawberries. Crop Protection 23, 825-834.
Jones, A. L., Ehret, G. R., El-Hadidi, M. F., Zabik, M. F., Cash, J. N., Johnson, J. W., 1993.
Potential For Zero Residue Disease-Control Programs For Fresh And Processed
Apples Using Sulfur, Fenarimol, And Myclobutanil. Plant Disease 77, 1114-1118.
Jones, O. T., 1998. Pest monitoring. In: Howse, P., Stevens, I.M., Jones, O. (Eds.),
Insect Pheromones and Their Use in Pest Management. Chapman and Hall,
London, UK, pp. 263–279.
Jonsson, M., Wratten, S. D., Landis, D. A., Gurr, G. M., 2008. Correct timing of treatment.
Recent advances in conservation biological control of arthropods by arthropods.
Biological Control 45, 172–175
Kakazaki, M., Sugie, H., 2001. Identification of female sex pheromone of the rice leaf
bug, Trigonotylus caelestialium. Journal of Chemical Ecology 27, 2447-2458.
Kaneko, S., 2003. Impacts of two ants, Lasius niger and Pristomyrmex pungens
(Hymenoptera: Formicidae), attending the brown citrus aphid, Toxoptera citricidus
(Homoptera: Aphididae), on the parasitism op the aphid by the primary parasitoid,
Lysiphlebus japonicus (Hymenoptera: Aphidiidae), and its larval survival. Applied
Entomology and Zoology 38, 347-357.
Kelleytunis, K. K., Reid, B. L., Andis, M., 1995. Activity of entomopathogenic fungi in
free foraging workers of Camponotus pennsylvanicus (Hymenoptera, Formicidae).
Journal of Economic Entomology 88, 937-943.
Kenis, M., Roy, H. E., Zindel, R., Majerus, M. E. N., 2008. Current and potential
management strategies against Harmonia axyridis. BioControl 53, 235–252.
Kiss, A., 1981. Melezitose aphids and ants. Oikos 37(3), 382.
Koch, R. L., 2003. The multicolored Asian lady beetle, Harmonia axyridis: A review of
its biology, uses in biological control, and non-target impacts. Journal of Insect
Science 3, 32.
Kolbe, W., 1982. Occurrence and control of pear leaf curling midge and apple leaf
curling midge. Pflanzenschutz Nachrichten Bayer 35, 291–308.
To spray, or not to spray: That is the question 92
Lacey, L. A., Shapiro-Ilan, D. I., 2008. Microbial control of pests in temperate orchard
systems: Potential for incorporation into IPM. Annual Review of Entomology 53,
121-44.
Lacey, L. A., Thomson, D., Vincent C., Arthurs, S. P., 2008. Codling moth granulovirus:
a comprehensive review. Biocontrol Science and Technology 18, 639-63.
Landis, D. A., Wratten, S. D., Gurr, G. M., 2000. Habitat management to conserve
natural enemies of arthropod pests in agriculture. Annual Review of Entomology
45, 175–201.
Lavandero, B. I., Wratten, S. D., Didham, R. K., Gurr, G. M., 2006. Increasing floral
diversity for selective enhancement of biological control agents: a double-edged
sward? Basic and Applied Ecology 7, 236–243.
Macaulay, E. D. M., Tatchell, G. M., Taylor, L. R., 1988. The Rothamsted Insect Survey
‘12-m’ suction trap. Bulletin of Entomological Research 78, 121–129.
Mészáros Z. (edit.), Ádám, L., Balázs, K., Benedek, M. I., Csikai, Cs., Draskovits, D.
Á., Kozár, F., Lővei, G., Mahunka, S., Meszleny, A., Mihályi, F., Mihályi, K., Nagy,
L., Oláh, B., Papp, J., Polgár, L., Radwan, Z., Rácz, V., Ronkay, L., Solymosi,
P., Soós, Á., Szabó, S., Szabóky, Cs., Szalay-Marzsó, L., Szarukán, I., Szelényi,
G., Szentkirályi, F., Sziráki, Gy., Szőke, L., Török, L., 1984. Result of faunistical
and floristical studies in Hungarian apple orchards. Acta Phytopathologica
Academiae Scientiarium Hungaricae 19, 91–176.
Millar J. G., Rice R. E., Wang Q., 1997. Sex pheromone of the Mirid bug Phytocoris
relativus. Journal of Chemical Ecology 23, 1743-1755.
Millar, J. G., Rice, R. E., 1998. Sex pheromone of the plant bug Phytocoris californicus.
Journal of Economic Entomology 23, 1743-1755.
Miller, J. R., Gut, L. J., de Lame, F. M., Stelinski, L. L., 2006a. Differentiation of
competitive vs. non-competitive mechanisms mediating disruption of moth
sexual communication by point sources of sex pheromone (Part I): Theory.
Journal of Chemical Ecology 32, 2089-114.
Miller, J. R., Gut, L. J., de Lame, F. M., Stelinski, L. L., 2006b. Differentiation of
competitive vs. non-competitive mechanisms mediating disruption of moth
sexual communication by point sources of sex pheromone (Part 2): Case studies.
Journal of Chemical Ecology 32, 2115-43.
Müller, C. B., Adriaanse, I. C. T., Belshaw, R., Godfray, H. C. J., 1999. The structure of
an aphid-parasitoid community. Journal of Animal Ecology 68, 346-370.
Murchie, A. K., Hume, K. D., 2003. Evidence for monogeny in the brassica pod midge
Dasineura brassicae. Entomologia Experimentalis et Applicata 107, 237-241.
Murray, R. A., Cross, J. V., Ridout, M. S., 2001. The measurement of multiple spray
deposits by sequential application of metal chelate tracers. Annals of Applied
Biology 137, 245-252.
Nagy, C., Markó, V., Cross, J. V., 2007. Effects of exclusion or supplementary honey
feeding of the common black ant, Lasius niger (L.), on aphid populations and
natural enemies on apple. IOBC Bulletin 30(4), 43-50.
Nagy, C., Tartally, A., Vilisics, F., Merkl, O., Szita, É., Szél, G., Podlussány, A., Rédei, D.,
Csösz, S., Pozsgai, G., Szövény, G., Markó, V., 2009. Effects of the invasive garden
ant, Lasius neglectus Van Loon, Boomsma and Andrásfalvy, 1990 (Hymenoptera,
Formicidae) on arthropod assemblages: pattern analyses in the type supercolony.
Myrmecological News 12, 171-181.
93 Jerry Cross
Nguyen, T. X., Merzoug, J., 1994. Research on the rational use of the predator
Anthocoris nemoralis (Heteroptera - Anthocoridae). IOBC Bulletin 17 (2), 104-107.
Nixon, G. J., 1951. The association of ants with aphids and coccids. Commonwealth
Institute of Entomology, London, 36p.
Offenberg, J., 2001. Balancing between mutualism and exploitation: the symbiotic
interaction between Lasius ants and aphids. Behav. Ecol. Sociobiol. 49, 304-310.
Oi, D. H., Pereira, R. M., 1993. Ant behaviour and microbial pathogens. Florida
Entomologist 76, 63-74.
Paris, C. I., 2007. Above-below ground effects of the invasive ant Lasius neglectus
in an urban holm oak forest. PhD thesis, Autonomous University of Barcelona,
Bellaterra, 150 pp.
Pell, J. K., Pluke, R., Clark, S. J., Kenward, M. G., Alderson, P. G., 1997. Interactions
between two aphid natural enemies, the entomopathogenic fungus Erynia
neoaphidis Remaudiére & Hennebert (Zygomycetes: Entomophthorales) and
the predatory beetle Coccinella septempunctata L. (Coleoptera: Coccinellidae).
Journal of Invertebrate Pathology 69, 261-268.
Pell, J. K., Vandenberg, J. D., 2002. Interactions among the aphid Diuraphis noxia,
the entomopathogenic fungus Paecilomyces fumosoroseus and the coccinellid
Hippodamia convergens. Biocontrol Science and Technology 12, 217-224.
Pereira, R. M., Stimac, J. L., 1992. Transmission of Beauveria bassiana within nests of
Solenopsis invicta. Environmental Entomology 21, 1427-1432.
Perrin, R. M., 1975. The role of the perennial stinging nettle, Urtica dioica, as a reservoir
of beneficial natural enemies. Annals of Applied Biology 81, 289-297.
Pfiffner, L., Wyss, E., 2004. Use of sown wildflower strips to enhance natural enemies
of agricultural pests. In: Gurr, G. M., Wratten, S. D., Altieri, M. A. (Eds.), Ecological
Engineering for Pest Management—Advances in Habitat Manipulation for
Arthropods. CSIRO Publishing, Melbourne, Australia, pp. 165–186.
Pimentel, D., 1995. Amounts of pesticides reaching target pests: Environmental
impacts and ethics. Journal of Agricultural and Environmental Ethics 8, 17–29.
Rieux, R., Simon, S., Defrance, H., 1999. Role of hedgerows and ground cover
management on arthropod populations in pear orchards. Agriculture, Ecosystems
and Environment 73,119–127
Roditakis, E., Couzin, I. D., Balrow, K., Franks, N. R., Charnley, A. K., 2000. Improving
secondary pick up of insect fungal pathogen conidia by manipulating host
behaviour. Annals of Applied Biology 137, 329-335.
Romet, L., 2004. The position of the autumnal control strategy for apple ash aphid. Fruit
Belge 72 (510), 124–129.
Rosengren, R., Sundström, L., 1991. The interaction between red wood ants, Cinara
aphids, and pines. A ghost of mutualism past? In: Ant plant interactions, eds.
Huxley, C. R. and Cutler, D. F. Oxford University Press, New York: 80-91.
Roy, H. E., Pell, J. K., Alderson, P. G., 2001. Targeted dispersal of the aphid pathogenic
fungus Erynia neoaphidis by the aphid predator Coccinella septempunctata.
Biocontrol Science and Technology 11, 99-110.
Sadler, B., Dixon, A. F. G., 1999. Ant attendance in aphids: why different degrees of
myrmecophily? Ecological Entomology 24, 363-369.
Sakata, H., 1994. How an ant decides to prey on or to attend aphids. Researches on
Population Ecology 36, 45-51.
To spray, or not to spray: That is the question 94
Sakata, H., 1995. Density-dependent predation of the ant Lasius niger (Hymenoptera:
Forminidae) on two attended aphids Lachnus tropicalis and Myzocallis kuricola
(Homoptera: Aphididae). Researches on Population Ecology 37: 159-164.
Sands, W. A., 1957. The immature stages of some British Anthocoridae (Hemiptera).
Transactions of the Royal Entomological Society of London 109, 295-310.
Sargent, D. J., Fernández-Fernández, F., Rys, A., Knight, V. H., Simpson, D.
W., Tobutt, K. R., 2007. Mapping of A1 conferring resistance to the aphid
Amphorophora idaei and dw (dwarfing habit) in red raspberry (Rubus idaeus L.)
using AFLP and Microsatellite markers. BMC Plant Biology 7, 15.
Schabel, H. G., 1982. Phoretic mites as carriers of entomopathogenic fungi. Journal of
Invertebrate Pathology 39, 410-412.
Schaub, L., Alame, M., Grandchamp, K., Bloesch, B., 2001. Laboratory evaluation
of the efficacy of neonicotinoids against rosy apple aphids. Revue Suisse de
Viticulture Arboriculture Horticulture 33, 109-111.
Schaub, L., Granchamp, K., Bloesch, B., 1999. Sensitivity of the rosy apple aphid to
pirimicarb and triazamate. Revue Suisse de Viticulture Arboriculture Horticulture
31, 73-76.
Seifert, B., 1996. Ameisen, beobachten, bestimmen. Naturbuch Verlag, Augsburg, 352
pp.
Seifert, B., 2000. Rapid range expansion in Lasius neglectus (Hymenoptera, Formicidae)-
an Asian invader swamps Europe. Mitteilungen aus dem Museum für Naturkunde
in Berlin - Deutsche Entomologische Zeitschrift Z. 47, 173-179.
Sigsgaard, L., Kollmann, J., 2007. Beneficial effects of hedgerow plants for insect
predators in adjacent orchards - the value of pollen and nectar to Anthocoris
nemorum (L.). IOBC Bulletin 30 (4), 9-13.
Skinner, G. J., Allen, G. W., 1996. Ants. The Richmond Publishing Co. Ltd., Slough, UK.
Skinner, R. N., 1983, The biology of apple aphids and their predators. PhD Thesis,
University of London. 277 pp.
Smith R. F., Pierce H. D., Borden J. H., 1991. Sex pheromone of the Mullein bug,
Campylomma verbasci (Meyer) (Heteroptera: Miridae). Journal of Chemical
Ecology 17, 1437-1447.
Smith, B. D., 1960. The behaviour of the black currant gall mite (Phytoptus ribis Nal.)
during the free living phase of its life cycle. Annual Report of the Agricultural and
Horticultural Research Station, Long Ashton, Bristol 1959, 130-136.
Smith, B. D., 1961. Population studies of the black currant gall mite (Phytoptus ribis
Nal.). Annual Report of the Agricultural and Horticultural Research Station, Long
Ashton, Bristol 1960, 120-124.
Solomon, M. G., Cranham, J. E., Easterbrook, M. A., Fitzgerald, J. D., 1989. Control
of pear psyllid, Cacopsylla pyricola, in South East England by predators and
pesticides. Crop Protection 8, 197-205.
Solomon, M. G., Cross, J. V., Fitzgerald, J. D., Campbell, C. A. M., Jolly, R. L., Olszak,
R. W., Niemczyk, E., Vogt, H., 2000. Biocontrol of pests of apples and pears in
northern and central Europe: 3. Predators. Biocontrol Science and Technology
10, 91-128.
Solomon, M. G., Fitzgerald, J., Jolly, R., 1999. Artificial refuges and flowering plants to
enhance predator populations in orchards. IOBC/wprs Bulletin 22(7), 31-37.
Stadler , B., Dixon, A. F. G., 1998. Costs of ant attendance for aphids. Journal of Animal
Ecology 67, 454-459.
95 Jerry Cross
Stadler, B., Dixon, A. F. G., 1999. Ant attendance in aphids: why different degrees of
myrmecophily? Ecological Entomology 24, 363-369.
Stewart-Jones, A., Pope, T. W., Fitzgerald, J. D., Poppy, G. M., 2007. The effect of
ant attendance on the success of rosy apple aphid populations, natural enemy
abundance and resultant fruit damage in apple orchards. Agricultural and Forest
Entomology 10, 37-43.
Straub, C. S., Finke, D. L., Snyder, W. E., 2008. Are the conservation of natural enemy
biodiversity and biological control compatible goals? Biological Control 45, 225–
237.
Sutherland, J. P., Sullivan, M. S., Poppy, G. M., 2001. Oviposition behaviour and host
colony size discrimination in Episyrphus balteatus (Diptera: Syrphidae). Bulletin of
Entomological Research 91, 411-417.
Szankowski, I., Waidmann, S., Degenhardt, J., Patocchi, A., Paris, R., Silfverberg-
Dilworth, E., Broggini, G., Gessler, C., 2009. Highly scab-resistant transgenic
apple lines achieved by introgression of HcrVf2 controlled by different native
promoter lengths. Tree Genetics and Genomes 5(2), 349-358.
Tartally, A., 2000. Notes on the coexistence of the supercolonial Lasius neglectus Van
Loon, Boomsma et Andrásfalvy 1990 (Hymenoptera: Formicidae) with other ant
species. Tiscia 32, 43-46.
Tartally, A., 2006. Long term expansion of a supercolony of the invasive garden ant
Lasius neglectus (Hymenoptera: Formicidae). Myrmecologische Nachrichten 9,
21-25.
Taylor, L. R., 1979. The Rothamsted Insect Survey—an approach to the theory and
practice of synoptic pest forecasting in agriculture. In: Rabb, R.L., Kennedy,
G.G. (Eds.), Movement of Highly Mobile Insects: Concepts and Methodology in
Research. University Graphics, Raleigh, NC, pp. 148–185.
Theobald, F. V., 1922. Annual Report of the Research and Advisory Department. S. E.
Agricultural College, Wye, pp. 10–13.
Thoizon, G., 1970. Spécificité du parasitisme des aphides par les Entomophthorales.
Annales de la Societe Entomologique de France 6, 517-562.
Thomas, M. B., Wratten, S. D., Sotherton, N. W., 1991. Creation of island habitats in
farmland to manipulate populations of beneficial arthropods—predator densities
and emigration. Journal of Applied Ecology 28, 906–917.
Tilles, D. A., Wood, D. L., 1982. The influence of carpenter ant (Camponotus modoc)
(Hymenoptera: Formicidae) attendance on the development and survival of
aphids (Cinara spp.) (Homoptera: Aphididae) in a giant Sequoia forest. Canadian
Entomologist 114, 1133-1142.
Tsinovskii, Y. A. P., Egina, K. Y. A., 1977. Entomophthoraceous fungi in the control of
apple aphids. Zaschchita Rastenii 7, 26-27.
Umpelby, R. A., Solomon, M. G., Cross, J. V., 1995. Review of pests of apple. Report
of Ministry of Agriculture, Fisheries and Food, Horticulture and Potatoes Division
project HH1722STF issued 10 August 1995, 51 pp.
Van Loon, A. J., Boomsma, J. J., Andrásfalvy, A., 1990. A new polygynous Lasius
species (Hymenoptera, Formicidae) from Central Europe. I. Description and
general biology. Insectes Sociaux 37, 348-362.
Völkl, W., 1992. Aphids or their parasitoids: Who actually benefits from ant tending?
Journal of Animal Ecology 61, 273-281.
To spray, or not to spray: That is the question 96
Völkl, W., Mackauer, M., 2000. The oviposition behaviour of aphidiine wasps
(Hymenoptera: Braconidae, Aphidiinae): morphological adaptations and
evolutionary traits. Canadian Entomologist 132, 197-212.
Völkl, W., Woodring, J., Fischer, M., Lorenz, M. W., Hoffmann, K. H., 1999. Ant-
aphid mutualisms: the impact of honeydew production and honeydew sugar
composition on ant preferences. Oecologia 118, 483-491.
Wackers, F. L., van Rijn, P. C. J., Bruin, J. (Eds.), 2005. Plant-provided Food for
Carnivorous Insects: A Protective Mutualism and its Applications. Cambridge
University Press, Cambridge, UK.
Walklate, P. J., Cross, J. V., 2005. Orchard spraying: Opportunities to reduce dose rates.
HDC (Horticultural Development Council, UK) factsheet 20/05 issued October
2005, 4 pp.
Walklate, P. J., Cross, J. V., 2010. A webpage calculator for dose rate adjustment of
orchard spraying Products. Aspects of Applied Biology 99, 359-366.
Walklate, P. J., Cross, J. V., Richardson, G. M., Baker, D. E., 2006. Optimising the
adjustment of label recommended dose rate for orchard spraying. Crop Protection
25 1080-1086.
Wardle, A, R., Borden, J. H., 2003. Sexual attraction among Lygus (Hemiptera: Miridae)
species. The Canadian Entomologist 135, 733-735
Wardle, A. R., Borden, J. H., Pierce, H. D. Jr., Gries, R., 2003. Volatile compounds
released by disturbed and calm adults of the tarnished plant bug, Lygus lineolaris.
Journal of Chemical Ecology 29, 931-944.
Way, M. J., 1963. Mutualism between ants and honeydew-producing Homoptera.
Annual Review of Entomolology 8, 307-344.
Witzgall, P., Stelinski, L., Gut, L., Thomson, D., 2008. Codling moth management and
chemical ecology. Annual Review of Entomology 53, 503-22
Wyss, E., 1997. Different strategies to control the rosy apple aphid Dysaphis plantaginea
in organic fruit growing. Mitteilungen der Deutschen Gesellschaft fur allgemeine
und angewandte Entomologie 11, 233–236.
Wyss, E., Daniel, C., 2004. Effects of autumn kaolin and pyrethrin treatments on the
spring population of Dysaphis plantaginea in apple orchards. Journal of Applied
Entomology 128, 147–149.
Yao, I., Shibao, H., Akimoto, S., 2000. Costs and benefits of ant attendance to the
drepanosiphid aphid Tuberculatus quercicola. Oikos 89, 3-10.
Zhang, Q. H., Aldrich, J. R., 2003. Pheromones of milkweed bugs (Heteroptera:
Lygaeidae) attract wayward plant bugs: sex pheromones of two Phytocoris
Mirids. Journal of Chemical Ecology 29, 1835-1851.
For more information, please contact:
Natural Resources Institute
University of Greenwich
Medway Campus
Central Avenue
Chatham Maritime
Kent ME4 4TB
Telephone: 01634 880088
Telephone from outside the UK: +44 1634 880088
E-mail: nri@gre.ac.uk
Website: www.nri.org
2008
REGISTER FOR
PUBLICATIONS/
GREENWICH VIP
This document is
available in other
formats on request
www.gre.ac.uk/study
University of Greenwich, a charity and company limited by guarantee, registered in England (reg. no. 986729).
Registered office: Old Royal Naval College, Park Row, Greenwich, London SE10 9LS