BUGS101:

Insect-Human Interactions
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Module 10

Sustainable Human-Insect Interactions:

IPM (Biological and Cultural Control)

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Course Notes

Module 10: Sustainable Human-Insect Interactions: IPM (Biological & Cultural

Control) 4

10.00 Introduction 4

10.01 Concepts Underlying Biological Control 5

10.02 Biological Control Agents 6

10.02.01 Parasitoids 6

10.02.02 Parasitoids: Types of Parasitism 8

10.02.03 Parasitoids: Dealing with the Host’s Immune Response 10

10.02.04 Predators 11

10.02.05 Pathogens: Bacteria 12

10.02.06 Pathogens: Fungi 13

10.02.07 Pathogens: Viruses 14

10.02.08 Other Biological Control Agents: Manipulating Endosymbionts 14

10.02.09 Other Biological Control Agents: Herbivores 15

10.03 Types of Biological Control 16

10.03.01 Importation/Classical Biological Control 16

10.03.02 Augmentative Biological Control 17

10.03.03 Conservation Biological Control 18

10.04 Pros and Cons of Biological Control 19

10.04.01 Advantages of Biological Control 20

10.04.02 Disadvantages of Biological Control 21

10.05 Cultural Control 23

10.05.01 Reducing Favourability of the Habitat 23

10.05.02 Manipulating Timing 24

10.05.03 Diverting Pests 25

10.05.04 Host Resistance 26

10.06 Conclusion 30

APPENDIX A 31
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SUPPLEMENTARY READINGS AND MATERIALS 31

Online Resources 31

Further Readings 31

REFERENCES 31
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Module 10: Sustainable Human-Insect Interactions: IPM

(Biological & Cultural Control)

Learning Objectives:

Upon completion of this lesson you will be able to:

● Evaluate biological control in IPM and discuss the bene its and drawbacks to this
tactic

● Compare and contrast classical, augmentative and conservation biological

control

● Differentiate parasitoids, predators and pathogens as biological control agents

● De ine cultural control as an IPM tactic

● Compare ways to implement cultural control and the impact on pest

populations

● Evaluate host resistance as a cultural control measure

10.00 Introduction

Integrated pest management (IPM) requires the

use of multiple approaches to manage pest
populations. While the use of action and economic
thresholds, monitoring tools, and preventative
measures form the foundation of IPM programs, the
types of pest control methods need to be diverse to
provide sustainable control. In the previous
module, we introduced chemical control. The use of
chemical insecticides improves global crop
production and pest management, but comes with
its own set of risks such as pollution and
contamination, as well as the “three R’s”- pest
resurgence, replacement, and resistance. This
module will focus on two non-insecticidal
categories of pest control: biological control
and cultural control.
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BIOLOGICAL CONTROL takes advantage of natural trophic interactions through the use
of a pest’s natural enemies, such as predators, parasitoids, pathogens, and even
herbivores of pestiferous plants or weeds. Typically these natural enemies have little effect
on non-target organisms. In CULTURAL CONTROL, environmental factors are manipulated
to reduce pest development, survival, and reproduction to restrict pest access to essential
resources. Cultural control can also involve manipulation of the environment to draw pests
away from target hosts, or to modify host resistance to pest damage through selective
breeding and genetic manipulation. Together, these two methods contribute to the overall
goal of IPM, to effectively reduce pest populations in an economically and ecologically
sound manner.

10.01 Concepts Underlying Biological Control

Natural enemies are manipulated in a pest

management approach known as BIOLOGICAL
CONTROL. Biological control affects pest
populations through naturally occurring trophic
interactions, a term used in ecology to refer to
an organism’s position within a food web.

We generally categorise organisms into four

basic trophic levels. The irst trophic level is
composed of organisms that create their own
food. These are called autotrophs (or
“producers”), and they can obtain energy from
inorganic chemicals, or from other energy
sources, like the sun that produces energy
captured by green plants to produce sugars via
photosynthesis. The second trophic level
consists of irst-order consumers, organisms
that obtain energy by feeding on autotrophs.
Herbivores, which feed on plants, are in the
second trophic level. In the third trophic level,
we ind second-order consumers, carnivores
that obtain energy by feeding on herbivores,
the irst-order consumers. Third-order
consumers are top predators that feed on other
carnivores, and make up the fourth trophic
level. Many organisms do not it neatly into these categories. For example, a large predator
may feed on both irst-order and second-order consumers. Omnivores also feed on both
plant and animal material.

The interactions between trophic levels are natural aspects of a healthy ecosystem that
help keep conditions at a stable equilibrium. In most pest management situations, the
herbivore is the management target. These are kept in check by natural enemies in the
third trophic level. Natural enemies can include predators, parasitoids, parasites, and
pathogens such as bacteria, viruses, and fungi. In fact, even herbivores can be considered
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natural enemies of weedy plant species, and are sometimes used to control populations of
weeds. Managers seek to use biological control to manage a target pest, or complex of pest
species, by exploiting the activity of natural enemies of the pests. This is achieved by
introducing, augmenting, or conserving populations of natural enemies within a managed
habitat.

Interesting Fact:

The irst historical instance of biological

control occurred almost 1700 years ago in
regions of China. Citrus ants build their nests
in citrus trees and feed on a variety of insects
that attack the trees and their fruit. Chinese
citrus farmers would tie bamboo strips
between citrus trees to help the ants establish
nests in nearby trees. Nests were even moved
between trees when a new stand of trees was
yet to be colonised by these bene icial ants.
Since the ants are aggressive towards
humans, they are primarily used as a natural
form of pest control rather than a managed
one in modern day agriculture.

10.02 Biological Control Agents

When natural enemies are recruited or managed by humans in order to reduce pests
populations they are referred to as biological control agents. We will discuss four types
of biological control agents recruited to kill pests. The irst two types, predators and
parasitoids, kill arthropod pest species through their regular feeding activities. The third
type, pathogens, includes microorganisms, such as bacteria, viruses and fungi, that infect
and often kill their hosts. The fourth and inal group is herbivorous insects, which can be
used as biological control agents to combat invasive weeds.

10.02.01 Parasitoids

The most widely used biological control agents fall into the category of parasitoids.
PARASITOIDS are insects that are parasitic as larvae, and eventually kill the arthropod
host. This is in contrast to parasites, which do not normally kill the host to complete their
life cycle. Interestingly, only larval parasitoids parasitise the host, while adult parasitoids
are free-living and do not feed on the host.

A female parasitoid lays her eggs either on or inside the body of a host, after which the
larvae hatch and feed on the host’s internal organs and hemolymph. This eventually kills
the host, but some parasitoid larvae postpone the death of their host by feeding on
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non-essential organs and tissues. The larvae

may pupate within their host, or emerge to
pupate outside of the host. Afterwards, the
free-living adult parasitoids emerge, mate, and
seek out a new host for their offspring.

Some parasitoids are specialists that target

speci ic host species, while others are
generalists that exploit multiple hosts.
Parasitoids affect fewer non-target species than
chemical insecticides. This, combined with
specialised host- inding, makes them effective
control agents in IPM systems with minimal
impact on non-target species. On the downside,
only ovipositing female parasitoids search for
hosts, and their reproductive capacity is
dependant on host availability.

Most parasitoids, especially those used as

biological control agents, are in the orders
Hymenoptera and Diptera (Fig. 4). It is
estimated that over 65,000 species of
Hymenoptera, and 15,000 species of Diptera are
parasitoids.

The Strepsiptera is a small order of only about

600 species, but all members of the order are
parasitoids of other insects. The most
well-studied strepsipterans parasitise insects
in the orders Hymenoptera and Hemiptera.
Insects in this order are rarely used as
biological control agents, although their
biology is rather interesting. Most studied
strepsipteran species have free-living males
that seek out and mate with paedogenic
females lodged between the sclerites of their
host (Fig. 5). The adult females never leave the
host, instead the irst instar larvae are the
mobile stage specialised to seek out new hosts.
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Interesting Fact:

Strepsiptera are sometimes called parasites,

but they can in fact be considered
parasitoids. Although they are not very well
studied, the insects they parasitise often die
once a female’s brood emerges from the
host, or after the males of a brood leave the
host. In addition, insects parasitised by
strepsipterans may become sterilised as a
result. This sort of “reproductive death” from
the sterilisation is another argument that
supports the status of strepsipterans as
parasitoids.

Another interesting thing about the

Strepsiptera is that they go through
something often termed hypermetamorphosis. The irst instar larvae, called triungulin
larvae, are specialised for dispersal and are quite different than the other larval instars,
resulting in another drastic change in body form between the irst and second instars.

10.02.02 Parasitoids: Types of Parasitism

We can categorise parasitoids based on where they occur on the host during the
feeding stages of their life cycle. Some parasitoids develop within the host, and these
are referred to as endoparasitoids. They feed on tissues within the host, and have
specialised adaptations for living within another organism, such as fusing their
tracheal network with that of their host to facilitate gas exchange. Other parasitoids
feed from outside the host, and live on the host during larval development. These are
known as ectoparasitoids.
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Parasitoids can also be categorised by the impact they have on the host. Some
parasitoids, called koinobiont parasitoids, develop while the host continues to feed
and grow. Other parasitoids, known as idiobiont parasitoids, paralyze and inhibit the
development of their hosts. Idiobiont parasitoids often conceal their hosts in a
burrow prior to parasitisation to offer some protection. Most idiobiont parasitoids
are ectoparasitoids.

There are three parasitism strategies that involve more than a single parasitoid larva
within the host. SUPERPARASITISM occurs when a host is attacked multiple times by
individual parasitoids of a single species. Superparasitism is not common as parasitoids
typically avoid laying eggs in already parasitised hosts to reduce intraspeci ic competition
among larvae. Avoidance is dictated by response to cues from the parasitised host detected
by chemoreceptors on the antennae or ovipositor of the adult female parasitoid. However,
if there is a high density of parasitoids relative to hosts, or small parasitoids with high
fecundity, superparasitism may occur.

Parasitoids of multiple species can parasitise a single host simultaneously in a process

known as MULTIPARASITISM. In these cases,, interspeci ic competition between larvae of
different parasitoid species usually results in only a single species completing
development.

In other cases, the parasitoid larvae or pupae may serve as a host for yet another
parasitoid species. This is termed HYPERPARASITISM, and this interaction occurs at the
fourth trophic level. Hyperparasitoids may be facultative or obligate, as some may act as
regular parasitoids if conditions are suitable to this strategy. In pest management,
hyperparasitoids can interfere with management programs in which parasitoids are used
as biological control agents.
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10.02.03 Parasitoids: Dealing with the Host’s Immune Response

Endoparasitoids live within their hosts and so are at the mercy of the host’s immune
system. As a result, endoparasitoids have developed adaptations that allow them to evade
or suppress the host’s immune responses.

The host response to endoparasitism can

include encasing the foreign body, such as a
parasitoid, with hemocytes to form a cover in
a process known as encapsulation. This can
kill a parasitoid egg or larva by cutting off its
access to nutrients and oxygen. Of course,
many parasitoids have evolved mechanisms to
overcome this host defense. For example,
some dipteran parasitoids hijack this capsule
and use it as a protective sheath. In the
species Exorista larvarum, larvae form a
“respiratory funnel” to survive encapsulation. The capsule formed by the host’s hemocytes
serves to protect the parasitoid larva and shield it from future host immune responses.

Another way an endoparasitoid can evade a host’s immune system is by carefully placing
offspring in regions within the host’s body that have a weak immune response. For
example, eggs oviposited within the ganglia of the host’s central nervous system are
shielded from host immune responses.

Some parasitoid species suppress their host’s

immune responses rather than simply evading
them. This occurs in parasitoid wasps from the
families Braconidae and Ichneumonidae, which
harbour symbiotic viruses that are injected into
the host with their eggs. These polydnaviruses
infect the host and suppress its immune
responses, allowing the parasitoid larvae to
successfully complete development within the
host. Polydnaviruses can even alter the host’s
metabolism and development to create
conditions that bene it the growth and survival
of the parasitoid larva.

Parasitoids have coevolved with their hosts,

which has resulted in some pretty extraordinary
adaptations for their survival. Some parasitoid
species can not only manipulate the host’s
immune responses but even the host’s
behavior. Some endoparasitic braconid wasps
that pupate outside of their caterpillar hosts, induce a behaviour in the caterpillar hosts
known as bodyguard manipulation. The host is not killed, even after the wasps emerge to
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pupate, but instead its behaviour

is modi ied to protect the
parasitoid pupae. Not only does
the caterpillar remain stationary,
guarding the parasitoid pupae, but
it also defends the pupae from
potential predators and
hyperparasitoids by violently
thrashing its body from side to
side, a behaviour that does not
occur in non-parasitised
caterpillars. Some parasitoids
take this mind control a step
further, by causing their hosts to
seek shelter prior to the
parasitoid’s pupation, or inducing
the host to spin a protective
cocoon over the parasitoid pupae.

Interesting Fact:

A fascinating example of mind control by

parasitoids occurs in the crypt keeper
wasp, Euderus set. This parasitoid
typically attacks Bassettia pallida,
gall-forming wasps that attack oak trees.
Normally, the gall-formers pupate inside
the gall and then chew open a hole
through which the adult wasps emerge.
However, when parasitised by a crypt
keeper wasp the gall-formers are not able
to emerge. Just as the adult wasp begins
to chew its way out, the parasitoid larva
growing within causes it to stop forming a hole so that the gall-former can not emerge.
Instead, the gall-forming wasp’s head may get stuck in the hole and plug it, after which the
crypt keeper wasp chews out through its victim’s head, which is easier than chewing its
way out of the plant tissue. Interestingly, unlike most parasitoids, crypt-keeper wasps feed
on a variety of unrelated species, all of which are oak gall-forming wasps. What the
gall-forming hosts have in common is that they all produce smooth thin galls, which is
likely the reason they are targeted by the crypt keeper.

10.02.04 Predators

Another group of organisms used as biological control agents are predators. PREDATORS
are free-living organisms that feed on other animals, killing their prey more rapidly than
parasitoids. Predators can be great biological control agents because they require multiple
prey items to survive, and therefore they attack and kill several animals in their lifespan.
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In contrast to parasitoids, most predators feed on multiple prey species. Many predators
are commonly used in biological control. Ladybird beetles are used to manage populations
of aphids and herbivorous mites. Predatory mites are used to control herbivorous mite
species, and lacewings are effective predators of aphids. These three groups of predatory
arthropods have the added bene it of being predators in both larval and adult stages,
unlike parasitoids, which only feed on hosts during their larval stages.

The effectiveness of generalist predators depends on the population density of the pests.
Generalist predators are typically most effective when pest populations are low. At high
pest densities, generalist predators can not keep up with prey populations. In these cases,
specialised parasitoids that target certain hosts may be more effective at keeping pace with
prey population cycles. Since most predators are generalists, a diversity of predators
permits host-switching without loss of pest control.

10.02.05 Pathogens: Bacteria

Pathogenic microbes are also important natural enemies that kill arthropod pests.
PATHOGENS include microorganisms such as bacteria, fungi, and viruses. These are
sometimes available as commercial formulations that can be applied to control insect
pests.

Bacterial pathogens are commonly used in formulations of microbial insecticides for

biological control. The bacteria enter the pest species and may release toxins that kill the
insects. One of the most widely used bacterial biological control agents is Bacillus
thuringiensis or Bt.

Bacillus thuringiensis naturally occurs as a

soil-borne bacterium, but has been
harnessed by humans for biological control.
Multiple strains of Bt exist, which can be toxic
to different groups of insect pests. This
enables speci ic Bt formulations to provide
targeted control. To control plant-feeding
insects, the bacterial formulation is applied
to the surface of plants, and must be ingested
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by the insect. Once ingested, the bacterium produces crystals that contain endotoxins
which damage and paralyze the midgut of the insect, causing death by starvation and
infection as the gut contents leak out into the hemocoel.

Formulations of Bt are applied in a variety of ways. There are emulsi ied concentrates or
wettable powders that can be applied to plant surfaces, and granular formulations for
application in aquatic ecosystems to control mosquito larvae. In fact, genes from the
bacterium have even been introduced into the genomes of various crop plants. This
enables the plants to produce the insecticidal toxin throughout the plant’s tissues. These
plants are called Bt transgenic crops, and will be discussed later in this module when we
introduce cultural control.

10.02.06 Pathogens: Fungi

Fungal pathogens are also used as biological control

agents. This kingdom of diverse organisms contains
over 750 species that infect insects, contributing to
natural population regulation. Fungi are valuable
biological control agents because, unlike most other
insect pathogens, they can penetrate intact insect
cuticle. Once the spores land on and attach to the
insect’s exoskeleton, they germinate and penetrate the
cuticle, gradually infecting the hemocoel, and
typically killing the insect in the process. Many of
these fungi produce toxins that incapacitate the insect
and may even kill them before the fungal growth
does. Beauveria bassiana is a species of fungus
commonly used as a biological control agent against
many pests world wide

Interesting Fact:

Recall from M07 that there are multiple pests and pathogens that af lict managed honey
bees, and that Varroa mites are one of the most destructive of these pests. While chemical
controls for Varroa mites are available, IPM programs are being studied to ensure effective
control and prevent resistance to acaricides. Treatment for Varroa mites generally includes
a preventative fall treatment, and the number of varroa mites present in a colony is also
taken into account, with spring and summer treatments only applied as necessary. Several
potential biological control agents are currently being studied to determine their ef icacy
against varroa mites. These include predatory mites, parasitoid wasps, and pathogenic
fungi. While free-living predatory mites are effective biological control agents of several
other pest arthropods, they are likely ineffective against Varroa mites. This has been
attributed to the fact that predatory mites are unlikely to search for varroa mites attached
to live bees, and there is a very limited window of opportunity for female Varroa mites to be
attacked before they are sealed into brood cells. Ongoing research into other biological
control agents, such as pathogenic fungi, may still yield an effective control agent to
combat one of the most signi icant pests of managed honey bees worldwide.
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10.02.07 Pathogens: Viruses

The inal group of pathogens used as biological control agents are viruses. Viruses infect
and replicate within the cells of a living organism, and can kill them in the process. Many
viruses only attack speci ic insects and break down quickly in the environment, which
enables viruses to be used effectively in IPM systems. As a virus replicates it kills the host
cell, and the insect appears to dissolve. As the insect falls apart, viral particles are released
onto surrounding surfaces to infect other insects.

A group of viruses that have been formulated to target

speci ic insect pests are baculoviruses. A formulation
was developed for the gypsy moth, an invasive pest and
major defoliator of hardwood forests in North America.
Since registration in 1978, this formulation has been
sprayed over thousands of acres of forest to control
gypsy moth. Baculoviruses are also used to control
codling moth, a cosmopolitan pest of tree fruits, and are
applied to over 150,000 hectares of orchards each year
in the United states.

Microbial insecticides made up of bacteria, fungi, and

viruses, are becoming increasingly important. Many of
them are relatively easy to mass-produce for wide-scale
application. Not only do they rapidly impact pest
populations, but they also line up well with the goals
of IPM. The use of pathogens as biological control
agents reduces the amount of harmful chemicals
introduced into the environment and has little impact
on non-target vertebrate species.

10.02.08 Other Biological Control Agents: Manipulating Endosymbionts

A relatively novel way to manage pest populations is to manipulate the symbiotic

microorganisms already carried in their bodies. Some of these endosymbionts are
bene icial while others are simply benign. Together this community of microorganisms is
referred to as a microbiome, and it protects the host against diseases, produces essential
vitamins, and assists in digestion. We can in lict various kinds of effects on insect pests by
disturbing or manipulating this microbiome. These effects may include decreased growth
rates, diminished reproductive success, or even a reduction in the ability of insect vectors
to transmit diseases.

Three basic techniques are under development for this pest management tactic. The irst
technique involves the introduction of novel microorganisms into an insect’s microbiome.
This has been done in Aedes aegypti mosquitoes, an important vector of dengue fever.
Bacteria in the genus Wolbachia, which are not normally found in Aedes mosquitoes, have
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been introduced into the mosquitoes and negatively affect the mosquito’s reproductive
success, and ability to transmit dengue fever.

The second technique to manipulate the

microbiome is genetic modi ication of the
microorganisms already present within the pest
species. Endosymbionts can be genetically
modi ied to produce insecticidal compounds that
have negative impacts on the host. For example,
genetically modi ied E. coli have been introduced
into the kissing bugs that vector of Chagas
disease. After ingestion and establishment in the
microbiome, the modi ied bacteria produce
molecules that interfere with natural gene
expression in the insects, and disrupt protein
synthesis that causes a reduction in oviposition
success and an increase in juvenile mortality.

The third and inal technique involves the targeted elimination of microorganisms
essential to the pest’s survival. If we can remove symbionts on which a pest relies for
growth, reproduction, or survival, pest populations and their associated damage could be
reduced. The manipulation of endosymbionts in biological pest control remains a novel
ield that is still undergoing much research to improve its effectiveness, speci icity, and
sustainability.

10.02.09 Other Biological Control Agents:

Herbivores

In some cases insect herbivores, or even plant

pathogens, can be employed as biological control
agents in order to control weeds. Weeds are any
unwanted plant that grows in competition with
other plants and crops. They are often invasive
species without natural enemies, and some may
be poisonous to humans and other animals.

Herbivorous arthropods can help keep weed

populations under control by consumption of
different parts of weedy plants, such as lowers,
roots, stems, and seeds. Such a program has been
developed to control the invasive yellow toad lax
in Alberta, Canada. A gall-forming weevil,
Rhinusa pilosa, has been released in areas
where the toad lax weed is abundant to reduce
the prevalence of the weed. Through their
feeding activity, these beetles have effectively
reduced the presence of toad lax in these areas,
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and populations have become established for continued control of the weed species.
Biological control of weeds involves a lot of research, as the herbivores need to speci ically
attack only the weed species and prevent impact on native lora.

10.03 Types of Biological Control

There are multiple approaches to biological control that depend on the objectives
managers hope to achieve. We classify these approaches into three major categories:
classical or importation biological control, augmentative biological control, and
conservation biological control.

10.03.01 Importation/Classical Biological Control

IMPORTATION BIOLOGICAL CONTROL previously known as CLASSICAL BIOLOGICAL

CONTROL, involves the introduction of non-native biological control agents to control
non-native pest species in its expanded range.

When an exotic pest species becomes established in

an area outside of its native range, it can quickly
reach high population levels due to the absence of
natural enemies in the new region. Natural enemies
from the native range of the pest species are
identi ied, studied, and recruited to act as biological
control agents of the pest in the introduced range.
There is a thorough evaluation of the effectiveness
of the potential biological control agent for control
of the target pest, and perhaps more importantly,
for its potential impact in the new ecosystem.
Once these natural enemies have been
determined suitable, they are imported under
strict government regulation. The goal of
importation biological control is to ensure that
these introduced populations of natural enemies
become self-sustaining.

Importation biological control is the preferred

approach to biological control for invasive pests
on non-cultivated land, but may work against
pests on cultivated land as well. The natural
enemies are intended to control, but not
eliminate, an invasive pest species, to maintain a
self-sustaining population that provides
continuous control of the pest species without
the need for further introductions.

Managers have implemented this pest control

approach to mitigate damage from the alfalfa
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weevil in the United States. This pest beetle was introduced from Europe in the early 20th
century and has since spread across the continental United States. In 1957, twelve species
of specialist parasitoids were imported from the native range of the alfalfa weevil to
become established and control the weevil in its introduced range. Since then, six of these
parasitoids have established populations in the United States, and have successfully
managed to suppress alfalfa weevil populations.

10.03.02 Augmentative Biological Control

AUGMENTATIVE BIOLOGICAL CONTROL involves the active manipulation of populations

of biological control agents to control pest species that can be either native or invasive.
Unlike importation biological control, the control agents are not expected to become fully
established in the area, and future management is necessary for continued control in later
seasons. Augmentative biological control typically requires the mass production and
semi-regular release of natural enemies into a managed system, and can be categorized by
two different methods of application: inoculative and inundative augmentative biological
control.

Inoculative augmentative biological control

involves the release of small numbers of natural
enemies at well-timed intervals throughout the
activity period of the pest species, and sometimes
even prior to pest activity. The control agents are
expected to reproduce to provide continued
control by the progeny, but additional
applications are typically necessary to support
their populations. An example of a natural enemy
commonly released using this strategy is Encarsia
formosa, a parasitoid wasp used to control
greenhouse white ly populations. Upon detection
of the pest, a small number of parasitoid wasps is
released into the crop, and some ongoing control
is provided from the next generation. The wasps
may need to be released again if pest
populations are high, and will typically be
re-released each growing season. The primary
goal of this approach is to keep pest population
densities from reaching the economic injury
level. Therefore, inoculative augmentative
biological control can be considered a
preventative approach.

Inundative augmentative biological control on the other hand, involves the release of large
numbers of natural enemies to immediately reduce pest populations during or just prior to
an outbreak. It is more of a corrective measure than preventative, since the goal is for the
natural enemy to quickly overwhelm the pest population and provide immediate pest
control. The control agents are not expected to become established, with little to no
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activity from the progeny. Microbial insecticides, such as Bacillus thuringiensis (Bt)
formulations, typically fall under this category. Application of Bt to a target crop can
rapidly reduce the pest population since the soil-borne bacterium produces a fast-acting
insecticidal toxin. Crops are sprayed with the bacterial formulation to quickly kill pest
populations. The formulation will need to be applied again during the next pest outbreak
since the bacteria and its toxin are susceptible to degradation by sunlight, although the
bacteria can survive in the soil for more than a year.

Both inoculative and inundative augmentative biological control require commercially

available control agents. Bt can be maintained outside an arthropod host, so mass
production is possible. The production of arthropod control agents is a bit more complex.
They are bred in large numbers at insectaries and shipped to producers just prior to
release.

The future of biological control agents will likely include natural enemies that are
genetically modi ied with recombinant DNA technology. In this way, researchers can
introduce bene icial traits to make these natural enemies more effective. For example,
genes can be added or modi ied in order to confer pesticide and disease resistance,
temperature hardiness, or even to manipulate sex ratios, which may be important in cases
where the activity of only one sex impacts the pest.

10.03.03 Conservation Biological Control

The inal type of biological control we will introduce is CONSERVATION BIOLOGICAL

CONTROL. This refers to the manipulation of speci ic variables in the environment to
enhance the ef iciency and persistence of natural enemies already present in the
ecosystem. Managers can achieve this either by reducing factors that interfere with the
success of natural enemies, such as insecticide use, or by enhancing resources necessary
for their survival, such as food supply.

Managers help conserve natural enemies by reducing activities that disturb the managed
system. Practices such as pesticide application, tillage, and weed removal, can be limited to
reduce disturbance of natural enemies present in the area.

Managers may also provision natural enemy

habitats with additional resources that promote
their success and effectiveness as biological
control agents. This can involve the provision of
alternative hosts, food sources, or favourable
overwintering habitats. This approach can be
extremely bene icial for natural enemies since
managed ecosystems typically have limited
resources for natural enemies. Parasitoids,
which are crucial to natural pest control, have
relatively poor dispersal ability. The presence of
loral resources close to the crop can provide
carbohydrates from nectar that increases the
 19

longevity and fecundity of parasitoids in the

area.

Managers can also support natural enemy

populations by enhancing certain habitat
features that provide refuge and resources
for natural enemies. Forested areas and
hedgerows around the crop may be suitable
nesting sites or overwintering habitats for
natural enemies. Natural habitats can also be
a source of additional prey items for
predators, and alternative hosts required
by some parasitoids to complete their life
cycles.

Alternative hosts can be important for

parasitoids when the pest species is not
present in the life stage needed for parasitoid
development, or simply when pest
populations are low. Banker plants are
non-crop plants deliberately infested with a
non-pest herbivore that acts as an alternative
food supply for natural enemies in the
cropping system. Banker plants help support
natural enemies, but their use is not
restricted to conservation biological control.
Banker plants can also be used by managers
to support biological control agents
introduced into the system, and enable
managers to use a single species of natural
enemy throughout the growing season
rather than a suite of natural enemies that
may compete or even prey on each other.

10.04 Pros and Cons of Biological Control

Biological control tactics are used in pest management for a variety of reasons. One of the
main bene its of biological control is simply that it offers another approach to pest
management in IPM systems. It also mitigates unintentional harm to the environment and
tends to target speci ic species, though the latter is dependant on the host breadth of the
biological control agents. However, the use of biological control requires extensive
research and knowledge of both the managed system and ecosystem surrounding it. In
addition, biological control agents are live organisms. This presents its own dif iculties in
terms of the production, transport, and storage of control agents.
 20

10.04.01 Advantages of Biological Control

There are many bene its associated with the use

of biological control in pest management. One of
the main bene its is the reduced impact
biological control methods have on the
environment when compared to chemical
controls. While some chemical insecticides have
very stable molecular structures that cause
them to persist in the environment and
accumulate at higher trophic levels, biological
control agents are living organisms and as such
have a de initive lifespan. While some fungi and
virus formulations can persist in the
environment for a period of time, the activity of
biological control agents is generally dependant
on the presence of the pest. In addition to the
reduced presence of harmful chemicals in the environment, biological control partially
addresses the growing problem of pesticide resistance. Biological control agents can
evolve with the pests, and there may be contrasting selective pressures from other natural
enemy species, which can reduce the development of resistance in some biological control
systems.

The reduced environmental impact of

biological control exempli ies how its use
is a movement towards sustainability.
This itself is a bene it of biological
control, as the increasing awareness of
our impacts on the environment have
created a growing demand for organic
and sustainable farming practices. This
has an added bene it for farmers, since
products grown under these practices
may command a higher market price.

Biological control can also be economically

justi iable in many cases. With the
increasing costs of new pesticides, as well
as stricter rules governing the use of
chemical pesticides, biological control
tactics may be cheaper to implement than
traditional controls. Biological control is
also less likely to cause damage to plants,
which sometimes occurs when pesticides
must be applied repeatedly to perennial
crops. As new technologies such as
 21

mechanized applicators and banker plants are developed, the cost of biological control
becomes more affordable.

Classical or importation biological control can be extremely cost effective when

successfully implemented. While the short-term costs are high, populations of natural
enemies that become established and self-sustaining in the new habitat provide
continuous control at no additional cost. In contrast, the cost of augmentative biological
control tends to remain similar over time since multiple applications are usually required.
Conservation biological control is typically associated with low costs overall, since the
measures taken in this approach do not require direct manipulation of natural enemies.
Biological control may not be new by any means, but its increased popularity promises a
bright future for this pest management tactic.

10.04.02 Disadvantages of Biological Control

While the use of biological control provides many bene its, this pest management tactic is
not without its laws. Biological control can require a more research regarding the biology
and ecology of all species within the habitat compared to conventional pest management
tactics, and therefore more time to develop. This knowledge helps ensure the ef iciency of
biological control, and helps prevent possible ecological damage.

The fact that biological control agents are living

organisms can be problematic. For one, it means
they may require additional resources for
survival, such as alternate hosts or refuges. Their
activity may be affected by environmental
conditions as well, such as temperature or day
length. It also means that they interact with other
organisms in the environment. A lack of
information about the pest, the control agent, and
the surrounding ecosystem, can cause biological
control to back ire. This occurred in the case of
the Asian lady beetle, Harmonia axyridis, that was
brought to North America in the 20th century to
suppress aphid populations. While the beetles do
help control aphids, they have outcompeted
native ladybird beetles to the point that they are
now the predominant lady beetle species in many
regions of North America.

The diet breadth of a natural enemy can also impact ef iciency of a biological control agent.
If the control agent has a broad diet breadth, its impact on the pest can be diluted through
the consumption of non-pest species. Host-speci ic parasitoids and predators are
preferable since they have adaptations to ef iciently search out speci ic pests and will not
attack non-target species. However, a restricted host range can mean that multiple types of
biological control agents are necessary to control a complex of pests, which increases
management costs. This can be common, since most managed ecosystems support a
 22

complex of different pest species. Natural enemies

of different species can interfere with each other.
They may compete for resources, or be vulnerable
to predation and parasitism by other natural
enemies. The interactions between the players in
the managed system become more complex as the
diversity of plants and pests increases.

Biological control agents not only need to be

compatible with each other, but also with other
control tactics used in the managed system. For
example, broad spectrum insecticides are unlikely
to be used simultaneously with the release of
predators or parastioids since they may harm the
biological control agents.

A major limitation of biological control is that much

of the time the effects are not as instantaneous as
with chemical controls. Although some microbial
insecticides can act quickly, other biological control
agents may take time to reach levels high enough
for effective pest control, or require time to ind
and kill their prey or hosts. This lag in effect can be
problematic in the management of high-value
crops, extremely damaging pests, or in cases like
greenhouses where ideal conditions can cause
quick buildup of pest populations. Large pest
outbreaks, such as an in lux of pests from a nearby
harvested agricultural ield, can be dif icult to deal
with using biological control alone.

The inal challenge associated with biological

control is the regulations restricting the
movement of living organisms between regions. The number of available biological control
agents in a certain region may be limited by these regulations, which are ultimately set in
place to prevent potential damage to the ecosystem.

Interesting Fact:

Today, the use of new biological control agents

only occurs after years of careful research to
determine their ef icacy and test for any other
potential ecological effects. Despite this, the use
of biological control agents can still be
controversial. This likely results from fears
about the negative ecological effects that
occurred after the introduction of a few species,
such as the cane toad. Cane toads were
 23

intentionally introduced to Australia in an effort to control populations of herbivorous

beetles that attack sugar cane. The toads were released despite being largely untested.
They are now an invasive species in Australia, where the toads threaten multiple native
species. Aside from outcompeting native species and reducing available prey populations,
the toads, which are the largest in the world, are also poisonous to most potential
predators. Today, the rigorous testing of potential biological control agents is done to
prevent the story of the cane toad from repeating itself.

While biological control can be an effective management tool, there are hurdles that must
be overcome for it to become a regular part of an IPM system. Overall biological control
requires a more informed approach than chemical control, but it can be more sustainable
and economic in the long-term. The key is to educate users and the public so that biological
control can be effectively integrated into pest management systems.

10.05 Cultural Control

Also known as ECOLOGICAL MANAGEMENT,

CULTURAL CONTROL involves purposeful
manipulation of the environment to reduce the
number of pests present and mitigate the damage
they cause. Cultural control encompasses virtually
all pest control methods that are not chemical
controls, and do not manipulate natural trophic
interactions as is done in biological control. Like
biological control, it requires a thorough
understanding of the biology, behaviour, and
ecology of a pest species so that managers can
manipulate speci ic environmental factors to
reduce the impact of a pest species.

10.05.01 Reducing Favourability of the Habitat

Some methods used in cultural control aim to

reduce pest populations and survival by reducing
the suitability of a managed ecosystem for the
pest. This can be achieved by eliminating suitable
pest habitats or restricting pest access to
resources, or sometimes even by modifying
environmental conditions.

Mosquito management often involves the

elimination of suitable egg-laying sites by draining
looded ields and eliminating standing water.
Urban pests such as cockroaches and bedbugs can
be managed by removing REFUGIA available to the
insects through cleaning and sealing cracks and
 24

crevices. Physical barriers can also prevent a

pest from accessing resources. Insect netting is
sometimes used to protect vulnerable crops, and
insecticide-treated mosquito nets are one of the
main ways to protect people from contracting
malaria. Tillage is an agricultural technique that
mechanically disturbs the soil to prepare land
for cultivation, but can also be used to expose
soil-dwelling life-stages of an insect pest to
predators and environmental conditions.
Another habitat that can be manipulated in pest
management is overwintering sites. The classic
example would be the removal of crop residue
after harvest. This is an approach commonly
used to control the apple maggot in North
America. Fallen apples are removed in the fall
before the larvae inside inish development and
emerge to pupate in the soil. These apples are
then destroyed or discarded far from the
orchard so that lies do not ind their way back
the following spring. This type of management
helps control infestations and reduces crop
damage from this important orchard pest.

Another way managers eliminate pest access

to resources is by destroying alternate plant
hosts, plants that the pest depends on when the target host is unavailable. This may be
another type of plant, but more often involves the removal of the same crop outside of the
managed area. For example, volunteer wheat, which grows freely around the margins of
the ield, is removed early in the season to prevent the buildup of populations of mites that
vector the wheat streak mosaic virus.

10.05.02 Manipulating Timing

Another way to control pest populations is by disrupting the chronological continuity

between pests and their hosts. A classic example is crop rotation, in which different crops
are planted in the same area over consecutive seasons. While this can help keep the soil
healthy and full of nutrients, crop rotation has the added bene it of helping to control pest
populations. It mitigates the buildup of a pest species that specialise on one type of crop,
since that crop is not present in the area during the following year. This technique works
best for insects with an immobile life stage that relies on the crop to prevent them from
moving between agroecosystems. Crop rotation is used in the management of the Western
Corn Rootworm in North America. In the spring, newly hatched larvae emerge from the
eggs in which they overwintered to feed on the roots of young corn plants. By planting a
different crop in the area the following season, managers ensure that emerging larvae have
no food source in the area, and their populations will be reduced as a result. Interestingly,
 25

insects can even evolve resistance to

cultural control tactics such as crop
rotation. Some populations of the
Western Corn Rootworm remain in
diapause for an extra year, which
allows them to be dormant while the
alternate crop is in rotation, and
emerge again the following year. This
is yet another reminder that it is
important to use multiple different
pest management tactics in an IPM
system.

Managers can also disrupt the

temporal synchrony between pests
and their hosts within a single year by
having a clear understanding of the
phenology of both the pest and its
host. Some insect specialists feed only on the host plant at a speci ic stage of development.
By changing the planting and harvest dates of annually produced crops, we can alter the
crop’s phenology and hopefully reduce pest impact. Wheat farmers reduce the presence of
aphids that vector barley yellow dwarf virus by seeding earlier in the season. Since the
aphids prefer young plants, mature plants in an early seeded ield will be less attractive to
the vectors of the disease.

Even the timing of insect activity during the day can be important information that allows
us to reduce the impact of pests. For example, outdoor activities can be scheduled when
mosquitoes are the least active, from dawn until dusk. Similarly, farmers may release
livestock into pastures when the activity of biting lies is at its lowest, after dusk. By
understanding the timing of insect activity, we can use this information to reduce a pest’s
access to its hosts.

10.05.03 Diverting Pests

Cultural control can involve techniques that aim to

divert or lure pests away from the target resource.
This can include methods such as trap cropping,
intercropping, and the use of semiochemical lures.

Trap cropping is the practice of planting crops

adjacent to the main crop that are attractive to the
target pest to divert the pest infestation and dilute
damage to the crop. Insects in trap crops can then be
controlled without worrying about damage to the
main crop, and in some cases the trap crop may even
be destroyed to prevent pests from spreading.
Trap cropping is used in soybean cultivation to
 26

control major pests such as stink bugs. In this case, the trap crops are soybeans that are
planted early, and thus mature early and are attractive to the insects. A section from 1-10%
of the cropping area is planted early, and attracts up to 85% of the pest population, after
which the pests can be controlled more thoroughly in a speci ic area with targeted and
appropriately timed insecticide applications. Trap cropping often involves the use of
semiochemical lures that help attract insects to the trap crop.

Synthetic pheromones can also be used to divert insect pests away from a protected
resource. This is done in some cases of bark beetle management in infested forest stands. A
baited trap tree lures in beetles to concentrate the attack on the trap tree, after which the
tree can be removed or the beetles can be killed with insecticides. This reduces the damage
from the beetles to surrounding trees.

Intercropping can also divert pests away from a

target crop. It involves the planting of multiple
types of crops in the same area. The goal is often to
increase crop yield by making the most ef icient
use of resources on the land, but it can also be used
to make the ield or main crop less attractive to
insect pests. In some cases, it can be purely
physical, such as making host plants less apparent
by hiding them under other crops with a higher
canopy or a strong aroma. In other cases, the
intercrop may be selected speci ically because it is
repellant to pest insects. For instance, sometimes
leeks are interplanted within bean crops since they
repel insect pests of bean, like the bean ly, and
reduce crop damage. In the home garden, onions
planted next to carrots deter carrot rust ly, and
tansies grown next to potatoes deter the Colorado
potato beetle. Unfortunately, intercropping comes
with its own set of challenges, particularly in the
large-scale harvest of different crops, at different
times, and sometimes with different types of
machinery.

Outside of agriculture, we regularly divert pests away from animal hosts using insect
repellants. Chemicals such as DEET provide personal protection by making humans and
other animals less attractive to biting insects. The chemicals do not harm the insects, but
rather interfere with the insect’s ability to sense chemical cues.

10.05.04 Host Resistance

Most managers emphasize the need to kill pests in management programs, but this is a
one-sided approach that can lead to other problems, such as the overuse of insecticides. In
order to tackle pests, managers can also shift the emphasis from management of pests to
management of host plant stress. By reducing host injury to acceptable levels, other pest
 27

management techniques can be used at reduced frequencies. The manipulation of host

resistance to insect activity can be considered a method of cultural control, although it is
often considered to be its own category of pest control tactics. Host resistance is
manipulated in crops and livestock through SELECTIVE BREEDING as well as GENETIC
ENGINEERING. Through selection for certain traits, we can enhance the resistance to pest
damage in the crop.

We can categorize traits of host resistance based on the way they operate. Some crop
plants are bred to express defensive traits that deter pests from inding or feeding on the
host plant. These traits result in non-preference plant defense. Other plant defenses may
work by disrupting a pests metabolism after ingestion by producing toxic compounds that
harm the pest species. This type of plant defense is called antibiosis, and it is the primary
method by which crops in the family Brassicaceae have been bred to defend themselves.

The inal trait of host plant resistance for which

crops are bred is tolerance, so that crop yield can
be maintained despite pest damage. For example,
hybrid corn responds to feeding by corn
rootworm larvae by inducing compensatory
growth in the plant to the point that slightly
damaged plants have greater root mass and
produce higher yields than undamaged plants.
Tolerance to pest damage can even be improved
by something as simple as fertilizers and good
growing conditions that strengthen the target
crop. An important advantage of tolerance
compared to other plant resistance traits is that
it does not place selective pressure on the pest as
a result. Therefore, pests are unlikely to evolve
resistance to traits that confer tolerance. Many of
these host resistance traits, including tolerance,
are affected by the state of the host.
Poor environmental conditions can
lead to hosts that are stressed, which
tend to be more vulnerable to pests.

SELECTIVE BREEDING has occurred

since early farming practices took hold,
and has resulted in the variety of crops
and livestock on the market today. It
involves the selection of speci ic
parents that express bene icial traits to
pass on to offspring. It is a slow
process that takes several
generations to achieve the desired
traits in a particular crop or animal
variety. Modern crops have been
 28

historically selectively bred for traits such as taste, high yield, pest resistance, and
tolerance.

GENETIC ENGINEERING on the other hand operates much more quickly and allows
manipulation of targeted genes directly using molecular processes and DNA editing tools.
It also allows us to incorporate genes from one species into another, creating a transgenic
organism. Desired genes can be transferred into the genome of another organism by
injecting DNA into fertilised eggs at the single cell stage, or by using a bacterial vector that
introduces and integrates genes into the DNA of the target organism. Two types of
transgenic crops currently used in agriculture include Bt crops and RNAi crops.

Bt crops have been produced by

inserting genes from Bacillus
thuringiensis into plant genomes.
Speci ically, genes that express the
Delta endotoxin have been
inserted, resulting in plants that
produce the Bt toxin throughout
all of their cells. When ingested,
the crystals of this toxin pass
through the peritrophic membrane
in an insect’s midgut and
perforates the gut lining, causing
its contents to leak. This stomach
poison paralyses the insect’s
digestive system and the damage
the toxin induces causes death by
starvation and infection. This toxin
is expressed at all times in Bt
crops, which exerts strong
selective pressures on the insect
pests active in the transgenic crop. This consistent pressure promotes the evolution of
resistance to Bt toxins in the target pest. Managers can slow the development of resistance
through the use of refugia, crops planted near the Bt crops that are susceptible to the
target pest. This prevents some of the insects from exposure to the Bt toxin, which
minimizes the selective pressure. This works well for Bt crops because Bt resistance is a
recessive trait, so its effect is suppressed by the presence of a dominant, susceptible allele.
Heterozygous offspring produced from one resistant and one susceptible parent will not
exhibit Bt resistance.

Interesting Fact:

Humans have been modifying their food for centuries; replanting some of the grains which
produced the largest and greatest abundance of seeds was likely our irst foray into
arti icial selection for yield. Recent techniques allow for direct control by scientists to move
desirable genes between organisms. The GMOs produced in modern times are often still
selected for traits like yield, however other traits like pathogen or herbivore resistance,
 29

drought tolerance, and nutritional

value are also of interest to scientists,
growers, governments, and the public.
These GMOs have attracted
controversy in recent years though,
particularly about the safety of such
foods; although no negative impacts
on consumers have been found, and
approximately 90% of scientists
report GMOs to be safe for
consumption. Studies of livestock,
which consume the majority of GMO
crops globally, have indicated no
difference in animal health compared
to animals fed non-GMO crops.
Additionally, plants have been
genetically modi ied to address global
nutritional concerns. “Golden rice”, for
example, was produced to address
vitamin A de iciencies which lead to blindness, reduced immune function, and human death
in many countries. However, opposition to GMOs has prevented the adoption of golden rice
where vitamin A de iciencies are most problematic. Although some concerns about GMOs,
such as farmers becoming indebted to corporations for seeds, are valid concerns which
must be addressed; the common public fears about GMOs such as toxicity and allergens are
largely unfounded, and require improvements in communication between scientists and the
public about genetic modi ication.

A relatively novel technology is the use of RNAi (a.k.a.

RNA interference) to create transgenic crops as an
alternative to Bt crops. RNAi functions by blocking
protein synthesis in the target. It involves the production
of RNA molecules that bind to mRNA strands in the cells
of the target organism. Produced in the nucleus during
early stages of protein synthesis, mRNA’s are templates
read by ribosomes in the cytoplasm to produce speci ic
proteins. When RNAi molecules bind to the mRNA
strands, ribosomes can no longer read the mRNA and
protein synthesis stops. Since this activity stops protein
production after RNA has been transcribed from the
genes, this approach is referred to as
“post-transcriptional gene silencing”. RNAi can be used
to silence genes used to synthesize proteins necessary
for a pest’s survival in order to kill the pest. For
example, RNAi cotton has been created that silences
the expression of an enzyme in cotton bollworms (a
lepidopteran pest) used to detoxify the defensive
chemical (gossypol) produced by cotton. As such, the
 30

insect that evolved to specialize on cotton plants becomes susceptible to the plant’s
chemical defenses.

Genetic engineering is not only used to modify crop plants. Recall from an earlier module
that genetic engineering can also be used used in the sterile insect technique (SIT),
whereby members of the pest species are irradiated or genetically modi ied to become
reproductively sterile. These sterile individuals mate with wild conspeci ics, reducing the
population size of the next generation. Trial SIT programs in Brazil, Malaysia, and the
Cayman Islands have successfully reduced local mosquito population levels by up to 95%.
This technique does not involve manipulation of trophic interactions or chemical control,
and while it may not be an example of host resistance, it does fall under the category of
cultural control.

10.06 Conclusion

This module completes our overview of

Integrated Pest Management by introducing two
important tactics used in IPM, biological control
and cultural control. The use of these two tactics
reduces our input of harmful chemicals into the
ecosystem and allows us to tackle pest outbreaks
from multiple angles.

Biological control revolves around the

manipulation of trophic interactions to control
pests by using natural enemies recruited as
biological control agents. Predators, parasitoids,
and pathogens of insect pests are released or
supported to impact populations of the pest.
Biological control can also involve the
manipulation of endosymbionts to affect insect
pests, or the use of herbivores to control weed
pests. It can be implemented in a few different
approaches depending on the goal of the
managers.

Cultural control is a bit of a “catch-all” term that

describes any manipulation to the environment
in order to manage pests. This can be
accomplished by making the habitat less suitable
for the pest, by disrupting the timing in activity between the pest and their host, diverting
pests away from their hosts, or by manipulating host resistance to reduce pest damage.

These two tactics are critical components of Integrated Pest Management systems. The
more weapons we have in our arsenal against insect pests, the more we can manipulate
our pest management strategies to reduce management costs and protect the environment
while providing effective pest control.
 31

APPENDIX A

SUPPLEMENTARY READINGS AND MATERIALS

Online Resources

● The North American Biocontrol Index provides information about biocontrol

agents used in classical biocontrol in North America since 1985:
[Link]

Further Readings

REFERENCES

1. Addison, J. A. (1993). Persistence and nontarget effects of Bacillus thuringiensis in

soil: a review. Canadian Journal of Forest Research, 23(11), 2329-2342.

2. Bandara, K. A. N. P., Kumar, V., Ninkovic, V., Ahmed, E., Pettersson, J., & Glinwood, R.
(2009). Can Leek Interfere With Bean Plant–Bean Fly Interaction? Test of
Ecological Pest Management in Mixed Cropping. Journal of economic entomology,
102(3), 999-1008.

3. Carvalho, D. O., McKemey, A. R., Garziera, L., Lacroix, R., Donnelly, C. A., Alphey, L., ...
& Capurro, M. L. (2015). Suppression of a ield population of Aedes aegypti in
Brazil by sustained release of transgenic male mosquitoes. PLoS neglected tropical
diseases, 9(7), e0003864.

4. Cutler, H. G., & Cutler, S. J. (Eds.). (1999). Biologically active natural products:
agrochemicals. CRC Press.

5. De Moura, F. F., Moursi, M., Donahue Angel, M., Angeles-Agdeppa, I., Atmarita, A.,
Gironella, G. M., ... & Carriquiry, A. (2016). Bioforti ied β-carotene rice improves
vitamin A intake and reduces the prevalence of inadequacy among women and
young children in a simulated analysis in Bangladesh, Indonesia, and the
Philippines. The American journal of clinical nutrition, 104(3), 769-775.

6. Feener Jr, D. H., & Brown, B. V. (1997). Diptera as parasitoids. Annual review of
entomology, 42(1), 73-97.

7. Furlong, M. J., & Zalucki, M. P. (2010). Exploiting predators for pest management:
the need for sound ecological assessment. Entomologia Experimentalis et
Applicata, 135(3), 225-236.

8. Gaillard, M. D., Glauser, G., Robert, C. A., & Turlings, T. C. (2018). Fine-tuning the
‘plant domestication-reduced defence’hypothesis: specialist vs generalist
herbivores. New Phytologist, 217(1), 355-366.
 32

9. Gohole, L. S., Overholt, W. A., Khan, Z. R., Pickett, J. A., & Vet, L. E. (2003). Effects of
molasses grass, Melinis minuti lora volatiles on the foraging behavior of the cereal
stemborer parasitoid, Cotesia sesamiae. Journal of chemical ecology, 29(3),
731-745.

10. Goolsby, J. A., Spencer, D., & Whitehand, L. (2009). Pre-release assessment of impact
on Arundo donax by the candidate biological control agents Tetramesa romana
(Hymenoptera: Eurytomidae) and Rhizaspidiotus donacis (Hemiptera:
Diaspididae) under quarantine conditions. Southwestern Entomologist, 34(4),
359-376.

11. Hajek, A. E., & Eilenberg, J. (2018). Natural enemies: an introduction to biological
control. Cambridge University Press.

12. Hokkanen, H. M. (1991). Trap cropping in pest management. Annual Review of

Entomology, 36(1), 119-138.

13. Huang, H. T., & Yang, P. (1987). The ancient cultured citrus ant. BioScience, 37(9),
665-671.

14. Kido, H., Flaherty, D., Bosch, D., & Valero, K. (1983). Biological control of grape
lea hopper. California agriculture, 37(5), 4-6.

15. Khan, Z. R., Chiliswa, P., Ampong-Nyarko, K., Smart, L. E., Polaszek, A., Wandera, J., &
Mulaa, M. A. (1997). Utilisation of wild gramineous plants for management of
cereal stemborers in Africa. International Journal of Tropical Insect Science, 17(1),
143-150.

16. Knight, A. L., Basoalto, E., & Witzgall, P. (2015). Improving the performance of the
granulosis virus of codling moth (Lepidoptera: Tortricidae) by adding the yeast
Saccharomyces cerevisiae with sugar. Environmental Entomology, 44(2), 252-259.

17. Maure, F., Daoust, S. P., Brodeur, J., Mitta, G., & Thomas, F. (2013). Diversity and
evolution of bodyguard manipulation. Journal of Experimental Biology, 216(1),
36-42.

18. Moran, P. J., & Goolsby, J. A. (2009). Biology of the galling wasp Tetramesa romana, a
biological control agent of giant reed. Biological Control, 49(2), 169-179.

19. Parrella, M. P., & Lewis, E. (2017). Biological Control in Greenhouse and Nursery
Production: Present Status and Future Direction. American Entomologist, Vol 63
(No 4), pp. 237-250.
 33

20. Pellegrino, E., Bedini, S., Nuti, M., & Ercoli, L. (2018). Impact of genetically
engineered maize on agronomic, environmental and toxicological traits: a
meta-analysis of 21 years of ield data. Scienti ic reports, 8(1), 3113.

21. Quicke, D. L. (2014). The braconid and ichneumonid parasitoid wasps: biology,
systematics, evolution and ecology. John Wiley & Sons.

22. Racelis, A. E., Goolsby, J. A., Penk, R., Jones, W. K., & Roland, T. J. (2010).
Development of an inundative, aerial release technique for the arundo wasp,
biological control agent of the invasive Arundo donax L. Southwestern
Entomologist, 35(4), 495-501.

23. Rondeau, S., Giovenazzo, P., & Fournier, V. (2019). The Use of the Predatory Mite
Stratiolaelaps scimitus (Mesostigmata: Laelapidae) to Control Varroa destructor
(Mesostigmata: Varroidae) in Honey Bee Colonies in Early and Late Fall. Journal of
economic entomology, 112(2), 534-542.

24. Taracena, M. L., Oliveira, P. L., Almendares, O., Umañ a, C., Lowenberger, C., Dotson,
E. M., ... & Pennington, P. M. (2015). Genetically modifying the insect gut microbiota
to control Chagas disease vectors through systemic RNAi. PLoS neglected tropical
diseases, 9(2), e0003358.

25. Van Eenennaam, A. L., & Young, A. E. (2014). Prevalence and impacts of genetically
engineered feedstuffs on livestock populations. Journal of Animal Science, 92(10),
4255-4278.

26. Valigurová , A., Michalková , V., Konı́k, P., Dindo, M. L., Gelnar, M., & Vaň hara, J. (2014).
Penetration and encapsulation of the larval endoparasitoid Exorista larvarum
(Diptera: Tachinidae) in the factitious host Galleria mellonella (Lepidoptera:
Pyralidae). Bulletin of entomological research, 104(2), 203-212.

27. Ward, A. K., Khodor, O. S., Egan, S. P., Weinersmith, K. L., & Forbes, A. A. (2019). A
keeper of many crypts: a behaviour-manipulating parasite attacks a taxonomically
diverse array of oak gall wasp species. Biology letters, 15(9), 20190428.

28. Whiting, M. F. (2003). "Strepsiptera". In Resh, V. H.; Cardé , R. T. (eds.). Encyclopedia

of Insects. Academic Press. pp. 1094–1096

29. Wright, E. J. (1986). Immature stages of Encyrtus saliens (Hymenoptera:

Encyrtidae), an imported parasite of ice plant scales (Homoptera: Coccidae) in
California. Annals of the Entomological Society of America, 79(2), 273-279.

30. [Link] iles/FieldCrop_Chapter1.pdf

31. [Link]
Text-Version/Physical-and-Biological-Processes-In-Crop-Production/Management-
of-Insect-Pests-with-Crop-Rotation-and-Field-Layout
 34

32. [Link]
ry/agribusiness-farmers-and-ranchers/crops-and-irrigation/organic-crops/organi
c-crop-production-disease-management

33. [Link]
- Pg 125