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Recognition and conservation of natural enemies of vegetable pests in Zimbabwe This field guide, also produced as Shona and Ndebele language versions, aims to help extension workers and agricultural trainers to recognise the most important groups of natural enemies of arthropod pests of vegetables (‘farmers’ friends’). It also provides information about the conservation and augmentation of these groups, from a variety of cultural practices to the selective use of pesticides. Multi-lingual posters intended for farmers have been produced to compliment the field guides. Farmers’ Friends Farmers’ Friends Recognition and Conservation A collaborative project ISBN: 0-9540132-0-4 A field guide for extension workers and trainers Collaborating Organisations Imperial College of Science, Technology & Medicine, UK Plant Protection Research Institute, Zimbabwe African Farmers for Research & Training, Zimbabwe Natural Resources Institute, UK Kenya Agricultural Research Institute, Kenya CABI Bioscience, Africa Regional Centre and UK Centre Participatory Ecological Land Use Management Association, Zimbabwe University of Zimbabwe

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Recognition and conservation ofnatural enemies of vegetablepests in Zimbabwe

This field guide, alsoproduced as Shona andNdebele language versions,aims to help extensionworkers and agriculturaltrainers to recognise the mostimportant groups of naturalenemies of arthropod pests of vegetables (‘farmers’friends’).

It also provides informationabout the conservation andaugmentation of thesegroups, from a variety of cultural practices to theselective use of pesticides.Multi-lingual posters intendedfor farmers have beenproduced to compliment the field guides.

Farmers’Friends

Farm

ers’ Frie

nd

sReco

gn

ition

an

d C

on

serva

tion

A collaborative project

ISBN: 0-9540132-0-4

A field guide for extension workers and trainers

Collaborating Organisations

Imperial College of Science,

Technology & Medicine, UK

Plant Protection Research Institute,

Zimbabwe

African Farmers for Research &

Training, Zimbabwe

Natural Resources Institute, UK

Kenya Agricultural Research Institute,

Kenya

CABI Bioscience, Africa Regional

Centre and UK Centre

Participatory Ecological Land Use

Management Association, Zimbabwe

University of Zimbabwe

1

FARMERS’ FRIENDS

Recognition and conservation of natural enemies of vegetable pests

A field guide for extension staff and trainers in Zimbabwe

This Field Guide is dedicated to the memory of Jason Ong'aro, a researcher, co-editor and team member, who passed away during the course of this project.

Published by:

Department of Biology, Imperial College of Science, Technology & Medicine,

University of London SW7 2AZ

ISBN 0-9540132-0-4

© 2001 Biology Department, Imperial College of Science, Technology & Medicine

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For further information, contact:

Zimbabwe

Dr S.Z Sithole, Plant Protection Research Institute, Departmentof Research and Specialist Services, PO Box CY550,Causeway, Harare, Zimbabwe. Email: [email protected]

Shepherd Musiyandaka, AfFOResT (African Farmers’ Organic Research & Training), PO Box CY301, Causeway, Harare, Zimbabwe.Email: [email protected]

Countries other than Zimbabwe

Dr R.H.J. Verkerk, Department of Biology, Imperial College, Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom.Email: [email protected]

This publication is an output from a research project funded by theDepartment for International Development of the United Kingdom(DFID project code R7587, Crop Protection Programme). However,the Department for International Development can accept noresponsibility for any information provided or views expressed.

For information about the DFID Crop Protection Programme, visitwww.nrinternational.co.uk (see also Natural Resources International,Contacts, p. 109).

Shona and Ndebele language versions of this guide and posters(Shona, Ndebele and English language versions) have also beenproduced as part of this project.

Photographs by R.H.J. Verkerk unless otherwise stated.

Design by deepblue, First Floor, 91a Rivington Street, London EC2A 3AY.

Printing by Fontline, Harare.

AUTHOR AND PRINCIPAL EDITORRobert VerkerkImperial College of Science Technology & Medicine, University of London, UK

PROJECT TEAM AND ASSOCIATE EDITORS

Simon Sithole, Joshua Karuma, Wilfred Chiimba, TumelaniWesile, Walter Manyangarirwa, Tafadzwa Sibanda:Plant Protection Research Institute, Department of Research &Specialist Services, Zimbabwe

Shepherd Musiyandaka, Fortunate Nyakanda, Rexon Hodzi,Todd Ndlovu, Sam Page: African Farmers’ Organic Research andTraining (AfFOResT), Zimbabwe

Hans Dobson: Natural Resources Institute, University ofGreenwich, UK

Gilbert Kibata, Jason Ong'aro, Samson Pete: NationalAgricultural Research Laboratories, Kenya Agricultural ResearchInstitute, Kenya

George Oduor, Peter Karanja, Sarah Simons, Martin Kimani:CABI Bioscience, Africa Regional Centre, Kenya

Peter Jowah: University of Zimbabwe (formerly IPPM WorkingGroup, Zimbabwe)

Tony Little: CABI Bioscience, UK

Denis Wright: Imperial College of Science Technology &Medicine, University of London, UK

4 ContentsContents

Acknowledgments 6

Foreword 7

Part 1. Introduction

Feeding levels in natural and agricultural systems 10

Some problems caused by intensive agriculture 12

What are natural controls? 15

Types of natural enemy 16

Biological control 18

Four steps for improving biological control of pests 18

Development and metamorphosis in insects and other arthropods 21

Part 2. Important natural enemies of vegetable pests 25

PredatorsLadybird beetles 26

Ground beetles 31

Rove beetles 34

Pirate bugs 37

Lacewings 39

Hover flies 42

Predatory mites 48

Predatory wasps 51

Mantids 53

Spiders 55

Other predators 58

ParasitoidsParasitoid wasps 64

Parasitoid flies 76

PathogensEntomopathogenic fungi 78

Baculoviruses 79

Bacteria 80

Entomopathogenic nematodes 81

Part 3. Evaluation of natural enemies, and pesticide selectivity 83

3.1 An introduction to natural enemy evaluation 84

3.2 Pesticide side effects on natural enemies 91

3.3 Selective pesticide application 104

Contacts 107

Appendix: Species lists 110

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6 ForewordAcknowledgments

I are indebted to the vegetable farmers, trainers, extension personnel and scientistsin Zimbabwe and Kenya whose input and enthusiastic cooperation made thecompilation of this natural enemy field guide, associated posters and trainingprogramme possible.

In Zimbabwe, we would like to extend particular thanks to the staff from the PlantProtection Research Institute (Department of Research & Specialist Services) and thenon-governmental organisation African Farmers’ Organic Research and Training(AfFOResT) for their dedication to the project and translation of the text to locallanguages (Shona and Ndebele). We are also grateful to AGRITEX, the IPPMWorking Group (Food and Agricultural Organization of the United Nations), PeterWilkinson (Xylocopa Systems, Harare) and the PELUM Association (Harare) whoprovided valuable input during the production of the materials.

Part of the research and development for this guide and its associated project wascarried out in Kenya (1998-1999), the work being made possible by the invaluablecontributions of our colleagues from the Kenya Agricultural Research Institute(KARI) and CABI Bioscience (Africa Regional Centre).

Dr Denis Wright (Imperial College, University of London) was responsible for theoverall management of the project, and Hans Dobson (Natural Resources Institute,UK) provided essential support and input throughout. Thanks are also due to TonyLittle (CABI Bioscience, UK Centre) who helped collate some of the data on sideeffects of pesticides on natural enemies (Part 3.2). Catherine Pinch (ImperialCollege, University of London) and Max Barclay (Natural History Museum, London)provided useful input to the section on carabid beetles. Tony Russell-Smith (NaturalResources Institute, UK) kindly identified the spiders shown in the guide. Furtherthanks are offered to Graham Matthews (Imperial College, University of London)and Hans Dobson for their useful suggestions on selective pesticide application inPart 3.

I would like to thank Andrew Jones and Mick Tomlinson from deepblue (London)for their work on the design and layout of the guide and associated posters.

Hans Dobson, Denis Wright and Misha Verkerk proof-read the manuscript and I am very grateful for their useful suggestions. I offer heartfelt thanks to my family,especially Ellie, Misha, Greta and Hannah, for all their support and encouragementthroughout the course of this project.

Finally, I am grateful to the Department for International Development (DFID) ofthe United Kingdom (Crop Protection Programme) for providing financial supportand advice.

Introducing this field guideThis field guide and its associated posters and ‘natural enemyflip-cards’ (available in English, Shona and Ndebele languages)are the result of collaboration between Imperial College(University of London), Plant Protection Research Institute(Department of Research & Specialist Services, Harare), AfricanFarmers’ Organic Research and Training (AfFOResT, Harare),National Agricultural Research Laboratories of the KenyaAgricultural Research Institute (NARL/KARI, Nairobi), CABIBioscience (Africa Regional Centre, Nairobi, and UK Centre) and Natural Resources Institute (University of Greenwich,Chatham, UK).

The purpose of the guide and its associated outputs is to helpextension staff and farmers recognise and conserve importantgroups of natural enemies by raising awareness of thepresence, abundance, diversity and benefits of natural enemieson smallholder farms in Zimbabwe. Nearly all of thephotographs within this guide were taken in the field duringsurveys in Zimbabwe and Kenya in October 1998, and inZimbabwe in May and October 2000.

During the October 1998 field surveys in Zimbabwe and Kenya, interviews with small-scale farmers were alsoundertaken. The interviews showed generally that littleinformation on natural enemies was available at the farm-level. However, it was also clear that farmers were veryinterested and enthusiastic about gaining more knowledge tohelp them recognise natural enemies and distinguish themfrom pests and other plant-feeding insects. Farmers wereparticularly keen to learn about conservation methods thatcould be used to encourage natural enemies on farms.

Learning about ways of improving the effectiveness of naturalenemies on small-scale, tropical, vegetable production systemsis likely to become increasingly important to many farmers as

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Robert Verkerk, Ascot, January 2001

1Introduction

Page

Feeding levels in natural and agricultural systems 10

Some problems caused by intensive agriculture 12

What are natural controls? 15

Types of natural enemy 16

Biological control 18

Four steps for improving biological control of pests 18

Development and metamorphosis in insects and other arthropods 21

Foreword

the cost of inputs such as pesticides and fertilisers continues to increase. In addition, many farmers are becoming moreconcerned over the possible human health and environmentalrisks of pesticides. There is also a growing worldwide interest in‘organic’ production where the use of synthetic pesticides (andfertilisers) is not permitted.

The English language version of this guide is divided into threeparts. Part 1 provides a general background to natural enemiesand biological control, while Part 2, the main body of theguide, considers in turn each of the major groups of naturalenemies and important methods for their conservation. Part 3is subdivided into three sub-sections, Part 3.1 being anintroduction to the evaluation of natural enemy effectiveness,emphasising common pitfalls to frequently used methods. Part3.2 contains information about the side effects of commonlyused pesticides on natural enemies, and it includes a table andcross references to websites aimed to help readers assess therelative hazards of different products to important naturalenemies. The final part, Part 3.3, presents various approachesto selective application of pesticides that can be used tominimise harm to natural enemies.

The Shona and Ndebele versions are essentially similar to theEnglish language version, except for Part 3. In these versions,Part 3.1 has been omitted, and the remaining two sub-partsare reduced slightly in scope and length.

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Feeding levels in natural and agriculturalsystemsNatural systems, such as forests and savannahs, support a wide range of plants and animals. The plants provide foodfor plant-eating animals such as antelopes and many insects,while the plant-eating animals are consumed by a wide rangeof carnivorous animals from lions to predatory and parasiticinsects. Even carnivorous animals generally have naturalenemies. These four feeding levels of life (see Table 1) exist inall stable natural and agricultural habitats. When a particulartype of plant-eating animal consumes too much of a crop or a commodity that we as humans value, we often call it a pest,while those animals which feed on plant-eating animals arecommonly referred to as natural enemies and should beconsidered farmers’ friends.

In most natural systems, the numbers of animals from thesedifferent groups are kept in check by complicated interactionsbetween the organisms present. This is why the leaves of mosttrees, shrubs and grasses in most natural systems remain moreor less intact most of the time. In stable agricultural systemsthis is also the case, with plant-eating organisms causing onlya small amount of damage to crops. The presence of some ofthese plant-eating organisms (so-called pest species) is oftenimportant to make sure that there is a food source available toallow establishment of natural enemies that in turn will help toprevent the development of pest outbreaks.

Frequently in agricultural systems, and very occasionally innatural ecosystems, the natural balances between these fourfeeding levels is upset and pest numbers increase rapidlyresulting in pest outbreaks. Outbreaks are most common inintensive agricultural systems. Three important reasons for thisare considered below.

Table 1: Four feeding levels common to natural andagricultural habitats

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FEEDINGLEVEL

Example 2 froman AGRICULTURALhabitat

Example froma NATURALhabitat

Example 1 froman AGRICULTURALhabitat

Type ofOrganism

Cabbage (crop)Grasses Tomato (crop)Plant

Aphid (pest)Antelope Caterpillar (pest)Plant-eating animal

Hover fly larva (natural enemy)

Lion Parasitic wasp (natural enemy)

Predatory or parasiticanimal

Parasitic wasp (natural enemy of natural enemy)

Tick Hyperparasitoid wasp (natural enemy of natural enemy)

Predatory or parasiticanimal

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Some problems caused by intensiveagriculture

■ Poorly adapted crop cultivarsMany plant cultivars grown as food crops in tropical countrieshave originated from Europe or other temperate latitudes. Theymay have been bred to enhance particular qualities such assize, colour or water content. They often have little naturalresistance to pests and diseases and have effectively been‘designed’ for high inputagriculture that is dependenton high fertiliser andpesticide inputs. Theresistance that is expressed bya given crop cultivar intemperate regions has beenshown to break downsometimes in the tropics (Picture 1).

■ MonoculturesIntensive agriculture ofteninvolves the planting of largetracts of land to a single croptype, this being referred to asa monoculture (Picture 2).This makes it easier for pest species to find the crop and oncefound, the pest can develop very quickly as its food source isplentiful and closely spaced. Monocultures usually contain fewsuitable refuges or adult food sources for natural enemies (e.g.,nectar and pollen from flowers). If they are heavily andregularly sprayed with insecticides (Picture 2), there is also ahigh chance that resistance to the insecticide will develop (seebelow).

■ Use of pesticidesThere is a large variety ofpesticides that can be usedagainst insect, mite andnematode pests, plantdiseases and weeds. However,in practice, it is theinsecticides and acaricidesthat are the most harmful tonatural enemies. This isbecause most naturalenemies, like the targets ofinsecticides and acaricides,

are either insects or closely related groups such as predatorymites or spiders. All these groups are arthropods. That is, theyhave jointed appendages and external skeletons.

Some of the general problems that may arise fromindiscriminate use of pesticides (particularly broad-spectruminsecticides or acaricides) are:

a) Death or harm to natural enemiesPesticides may affect the physiology (e.g., egg-laying rate,developmental period) or behaviour (e.g., host location,walking speed) of naturalenemies, and can cause lethalor sublethal effects.

Natural enemies are generallymore sensitive to pesticidesthan pests. This is partlybecause they spend more timesearching for potential hostsand prey, so risking contactwith residues. They are oftenalso smaller and morephysiologically sensitive,

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1. A cabbage variety (MinicoleF1) which has partial resistanceto cabbage aphid underEuropean conditions, but hasbeen shown to be highlysusceptible to aphid pests whengrown in Kenya

2. A broad bean monoculture,showing serious damage by leafminer fly larvae despitefrequent spraying withinsecticides

3. Adult hover fly dead on leafafter contacting a recentlysprayed crop

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and many important groups such as parasitoid wasps preenthemselves regularly so consuming residues they may havepicked up on their legs and antennae. If natural enemies areharmed or killed (Picture 3), pests multiply much more quickly,causing pest resurgence.

b) Pests may develop resistance or tolerance to pesticidesPesticide resistance or tolerance often occurs when farmersspray more and more frequently, often with increasing doses ofpesticide, with little impact on the pest populations (Picture 4).This is because the surviving populations contain a specificversion of a gene (an allele)that allows them to be lesssensitive to the pesticide insome way (e.g., detoxification,altered target site). Increasedfrequency of spraying withbroad spectrum pesticides,which often accompaniesresistance or tolerance, alsoincreases the harm to naturalenemies.

c) Pesticides may be harmful tohumans and the environmentExposure of operators is verycommon during application. Most pesticides are readilyabsorbed through the skin and the eyes, and droplets may beinhaled. Harmful levels of pesticides can also be consumed onproduce if pre-harvest intervals are not followed carefully.Pesticides may move in groundwater and contaminate drinkingwater supplies. They may contaminate water following theinappropriate disposal of pesticide concentrate containers(Picture 5). Pesticides may harm pollinators and a wide rangeof other beneficial or non-target organisms.

WHAT ARE NATURALCONTROLS?

Nature provides two basic linesof defence for plants againstplant-eating organisms(potential pests).

These are:

■ Plant defences Plants possess a wide range ofmechanisms that allow them to resist damage by mostplant-eating organisms. Theymay contain chemicals thatmake them distasteful orpoisonous to certain organisms(Picture 6), they may produce toxic secretions following attack, or they might have hairs on their leaves that make itdifficult for potential plant-eaters to settle and feed. This sortof plant resistance may be complete (making it impossible fora plant-eater to develop successfully on the plant) or it may be partial (where a plant-eatercan develop, but it does somore slowly or produces feweroffspring than on a susceptibleplant). A degree of partialplant resistance is often veryhelpful in low input cropproduction systems, as long as this resistance does notinterfere with the performanceof natural enemies.

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5. Pesticides can contaminatewater supplies

4. “I’ve been spraying once aweek for the last month andthe crop is being destroyed bypests. What is going on?”

6. “This plant

tastes bad and is

making me sick”

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■ Defence via naturalenemies

Natural enemies provide a veryimportant means of controllingthe abundance of plant-eatingorganisms. Crop plants underattack by pests have beenshown to ‘cry for help’ byreleasing particular chemicalsthat are attractive to specificnatural enemies (Picture 7).

In agricultural situations wherecrop losses need to be kept toa minimum, every effortshould be made to ensure thatthese natural controls work as well as possible beforeconsideration is given to more interventionist methods of pestcontrol, such as the application of pesticides.

TYPES OF NATURAL ENEMYNatural enemies of insect and mite pests can be divided intothree main groups:

■ Predators (see Part 2, pages 26-63)These are organisms that prey on and feed on other organisms.Each predator generally kills several prey during its lifetime.Immature and/or adult stages can be predatory. Somepredators feed on a wide range of species (generalists), whileothers are more specialised in their choice of prey, feeding ononly one or a few species (specialists).

Examples: ladybird beetles; ground beetles; mantids; dragonflies;predatory mites; predatory wasps; spiders.

■ Parasitoids (see Part 2, pages 64-77)Parasitoids are organisms that during their immature (larval)stages feed on and eventually kill a single arthropod, and intheir adult stage with very few exceptions are free-living.About 8.5% of insect species described to-date (i.e.,approximately 85,000 species) are parasitoids. They are nearlyall wasps or flies, but include a relatively small number ofbeetles and very occasionally other groups. The adults of mostagriculturally important parasitoids species feed on sugarysubstances such as the nectar of flowers or aphid honeydew.The larvae may feed from within or outside the body of theirhost. Many species are regarded as solitary with only oneparasitoid developing per host, or they may be gregarious withmany larvae (sometimes hundreds) developing per host. Mostparasitoids are highly or relatively specific (that is, arespecialists), selecting only a single host species or narrow rangeof species as targets. Natural enemies including parasitoids arethemselves also susceptible to attack by other parasitoids (andother natural enemies (see Table 1).

Examples: parasitoid wasps and flies

■ Pathogens (see Part 2, pages 78-82)Pathogens are disease organisms. They can be important incontrolling the growth of pest populations in agriculturalsystems. They include fungi, bacteria, viruses, nematode wormsand microsporidia. Many pathogens tend to be found morecommonly where pest populations are large or during rainyseasons.

Examples: Metarhizium, Zoophthora, Entomophthora(entomopathogenic fungi); GV (granulosis virus); NPV (nuclearpolyhedrosis virus); Bacillus thuringiensis (bacterium); EPNs(entomopathogenic nematodes)

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7. A plant ‘crying for help’ afterbeing attacked by caterpillars

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BIOLOGICAL CONTROLBiological control refers to the process of pest managementachieved through the use of living organisms, namely predators,parasitoids or pathogens. To be effective, cropping systemsneed to be designed and managed in such a way to enhancethe function of natural enemies that immigrate naturally intoand multiply within the crop. This approach to biologicalcontrol is called conservation and it has particular relevance for smallholder farmers in the tropics. In some cases, where a particular natural enemy species or group of natural enemiesis missing from a crop or a specific region, these can beintroduced from other areas (introduction, inoculation oraugmentation). In other cases, particular natural enemies canbe reared in large numbers in special facilities and released intothe crop at intervals (inundation).

FOUR STEPS FOR IMPROVING BIOLOGICAL CONTROL OF PESTSThis field guide is intended to help extension staff and fieldstaff provide support to farmers so that biological control canbe improved. In simple terms, four important steps aregenerally required.

STEP 1

■ Find out which natural enemies are present (see Part 2 ofthe guide)

In most cropping systems, natural enemies will either bepresent already or be close by and therefore do not need to beintroduced. It is critical that pests and natural enemies on acrop can be recognised (Picture 8). This field guide aims tohelp trainers recognise the most important groups of naturalenemies and in turn share this information with farmers.Farmers can be encouraged to set up ‘insect zoos’ where

groups of suspected pestsand natural enemies are kepttogether in ventilated jars orother small containers with aportion of the crop and aremaintained until all theanimals go through theircomplete development. Thiswill allow the farmer to seewho is eating who or what. Itwill also allow the effects ofparasitism to be observed if ithas occurred.

STEP 2

■ Select the most appropriate crop cultivars

It is important to choose crop cultivars that are not highlysusceptible to pests (and diseases), as discussed on p. 12(Picture 9). Information on the relative susceptibility ofparticular crops can often be obtained by talking to otherfarmers, relevant research institutes, extension staff or seedretailers. If data on cultivar tolerance or resistance are notavailable for a specific region, it may even be useful to run on-farm trials between different cultivars.

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8. “Is it a naturalenemy or apest?”

9. Kale variety Ahas beendamaged muchless by caterpillarsthan the othertwo varieties

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STEP 3

■ Conserve natural enemies by cultural means (see Part 2 ofthe guide)

There are many things that can be done on individual farms tohelp encourage natural enemies and improve their effectiveness(Picture 10). Some relevant techniques and information are givenin Part 2 of the guide under the subheading Conservation.Important methods of conservation include providing adultfood sources such as flowering plants (e.g., fennel, thistles,coriander, Indian mustard and other flowering brassicas) withinor close to the crop, mixed cropping or interplanting, providinglive fences (trees, hedges) and shelters, using mulches, andproviding water sourcesfor important predatorswith aquatic life stages.

10. “Can I grow someflowering plants toprovide adult foodsources and refuges formy natural enemies?”

STEP 4

■ Ensure that pest management practices are not disruptiveto natural enemies (see Part 3 of the guide)

The reader can use the information given in Part 3.2 of theguide as a starting point to help identify those pesticideproducts available in Zimbabwe that are likely to be lessharmful to natural enemies (Picture 11). Part 3.3 offers somesuggestions on ways of applying pesticides that minimise therisk of side effects on natural enemies. Obviously there aremany more pesticides available than those given in Part 3.2,

but the list given includes all the main pesticides used by thesmallholder sector during surveys conducted between 1998 and2000. Bear in mind that many pesticides have not been testedin a rigorous wayagainst naturalenemies and theside effects of mostbotanical pesticideshave not beentested at all (seeNote on use ofbotanical pesticides,pp. 101-102).

Development and metamorphosis of insectsand other arthropods

Most natural enemies that have a major influence on pestabundance are arthropods. Of these, the vast majority areinsects (see Part 2). Insects can be broadly classified into twotypes according to the way they develop. The process ofdevelopment is often referred to as metamorphosis. These types are:

■ Simple metamorphosisThese include those insects (and other arthropods) whoseimmature stages appear similar in basic form to the adults,varying mainly in size. Immature insects that undergo simple(or incomplete) metamorphosis are referred to as nymphs.

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11. “Is this spray going to kill my

natural enemies?”

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Adults arise following the last moult of the nymphs – there isno pupal stage. Insects that undergo simple metamorphosis areregarded as being more primitive than those that go throughcomplete metamorphosis. If wings are present in the adultform, these develop externally, and may be seen in nymphs aswing buds. Other arthropods, such as mites and spiders, alsoundergo simple metamorphosis.

■ Complete metamorphosis This group includes insects whose immature forms (larvae andpupae) appear very different, often live in different habitatsand have different habits, compared with the adults of thesame species. Examples include maggots, which turn into flies;grubs, which turn into beetles; and caterpillars, which turn intomoths or butterflies. The earlier immature stages (instars) ofthese insects are called larvae (singular = larva) and theirprinciple function is feeding. If wings are present in adults of a given species, these develop internally. Each larva sheds itsskin (moults) at intervals to allow growth, and then undergoespupation, from which the adult emerges. The pupa is inactiveand does not feed, but during this stage, a very large amountof change occurs as seen by the differences between larvae andadults of the same species. All parasitoids and many predatorsundergo complete metamorphosis.

Not all insects can readily be categorised as undergoing eithersimple or complete metamorphosis. Insects such as whiteflies,thrips and male scale insects are sometimes said to undergointermediate metamorphosis, as they have gone well down thepath towards the development of complete metamorphosis.

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EGG NYMPHS, several growth stages (instars) ADULT

IMMATURE FORMSExamples: ADULT FORMSInsects

Mantid nymph MantidPirate bug nymph Pirate bug

Other arthropodsMite nymph MiteSpiderling or nymph Spider

EGG LARVAE, several growth stages (instars) PUPA

LARVAL FORMSExamples: ADULT FORMSCaterpillar MothMaggot FlyAphid-lion LacewingWasp larva Wasp Ladybird beetle larva Ladybird

ADULT

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2Important natural enemies

of vegetable pests

Predators PageLadybird beetles 26

Ground beetles 31

Rove beetles 34

Pirate bugs 37

Lacewings 39

Hover flies 42

Predatory mites 48

Predatory wasps 51

Mantids 53

Spiders 55

Other predators 58

ParasitoidsParasitoid wasps 64

Parasitoid flies 76

PathogensEntomopathogenic fungi 78

Baculoviruses 79

Bacteria 80

Entomopathogenic nematodes 81

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Type: Predator (larvae and adults)Immatures: Different from adults (complete metamorphosis)Main prey: Aphids, mites, thrips, small caterpillars, insect eggsCrops: Vegetables, particularly brassicas, tomato, potato, beansGroup: Insect, beetle, ladybird beetle (Coleoptera: Coccinelidae)Common names: Ladybird, ‘Volkswagen’, coccinelid

APPEARANCEEggs: Usually yellow to orange incolour, and laid in groups near aphidcolonies (Picture 12).

Larvae: Crocodile-like, and can growup to about 1 cm before pupation(Picture 13).

Pupae: Seen less often than the other stages, oval-shaped and spiny (Picture 14).

Adults: Easy to recognise, dome-shaped bodies, wing coversmay be red or orange with black markings (Pictures 15 and16), or more or less completely brown or black (Picture 17).Adults may often be seen mating (Picture 18).

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12. A typical cluster ofladybird beetle eggs(Hippodamia variegata)

13. Ladybird beetle larva(Hippodamia variegata)

14. Ladybird beetlepupa (Coccinellaseptempunctata)

15. Adult ladybird beetle(Hippodamia variegata)

16. Adult ladybird beetle (Cheilomenes sp.)

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PEST LADYBIRD BEETLESNote that there are several species of plant-feeding ladybirdbeetles (notably, Epilachna and Henosepilachna spp.) that areoften regarded as pests because of the damage they can causeto solanaceous crops (such as tomato and potato) andcurcurbits (such as cucumber and marrow). These species arecommonly referred to as melon beetles. Both the adults andthe larvae eat leaves or damage fruits. The larvae are paleyellowish in colour and are covered in delicate spines. The adultwing cases are covered in fine hairs giving them a non-glossyor matt appearance (Picture 19).

EFFECTS ON PESTSThe larvae eat more pests (particularly aphids) than the adults.Usually, they are most abundant when aphid populations arelarge. A single ladybird beetle might consume 200-300 aphidsover its lifetime of 1-3 months. Ladybird beetle larvae tend tobe more active at night than by day so their activity is oftenunderestimated.

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19. Plant-feeding melon beetles(Henosepilachna sp.). Note finehairs on wing cases

18. Adult ladybirdbeetles mating(Hippodamia variegata)

17. Adult ladybird beetle(Exochomus sp.)

20. Fennel in a vegetable plotto help support natural enemies(such as ladybird beetles andhover flies) and pollinators(such as bees and hover flies)

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CONSERVATION■ Grow strips or groups ofnon-crop flowering plants(sometimes thought of as‘weeds’) that support non-pestaphid species within andaround the crop, such asfennel (Picture 20), coriander(Picture 21), thistles (Picture22) and milkweed. Theseprovide food sources andrefuge sites for beneficialinsects like ladybird beetles andthey allow populations of thenatural enemies to build-upand suppress the developmentof pest aphids on the crop.

■ Avoid spraying pesticidesunless absolutely necessary.Should spraying be considerednecessary, use a product andapplication method that isleast harmful to key naturalenemies (see Parts 3.2 and 3.3of this guide).

Type: Predator (larvae and adults)Immatures: Different from adults (complete metamorphosis)Main prey: Eggs and immature insects in or on soilCrops: Most, particularly on mixed crops and near natural vegetationand where mulches are presentGroup: Insect, beetle, ground beetle (Coleoptera: Carabidae)Common names: Ground beetle, carabid

APPEARANCEEggs: In soil and notoften seen.

Larvae: In soil, not seenunless soil is disturbed;elongated, clearlysegmented bodies,tapered towards theend, with 3 pairs oflegs. Head and thoraxare usually darker incolour than the bodiesthat vary in colour fromwhitish to brown.Mandibulate mouthparts (‘jaws’) can be seen readily (Picture 23).

Pupae: In soil and rarely seen.

Adults: Most species are mainly active at night (nocturnal), soare not often seen by day unless hiding places such as rocks,leaves on ground or mulches are disturbed. Adults vary in size(3 – 30 mm in length), are often brown or black in colour and

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23. Ground beetle larva (Pterostichus sp.)

21. Adult ladybird beetles andother beneficial insects areattracted to coriander (andmany other flowering plants),which can be grown as stripsbetween crop rows

22. Thistles growing amongbrassicas to help support aphidpredators like ladybird beetles

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have distinctive ridges on their wing cases (Picture 24). Somespecies may have a metallic sheen to their wing cases (Picture24), these often being more active by day (diurnal) than bynight. The legs are well developed allowing them to run fastand catch prey. The antennae are long and thread-like (Picture24). Most species of ground beetle are unable to fly.

EFFECTS ON PESTSAdult and larval ground beetles are often important generalistpredators (see p. 16) and are usually more abundant indiversified (mixed) crop environments, where mulches arepresent and soils are kept humid, or in crops close to naturalareas that are themselves diverse (e.g., scrub or forest). Asgeneralists, ground beetles eat a wide range of insects of alllife stages (eggs through to adults) usually in or on the soil.Thus, they may be important in helping to control a broadrange of pests including cutworms, beanflies and aphids.Although ground beetles do not climb up plants, they consumeaphids that have fallen from plants and would otherwise climbback up the plant and resume feeding.

CONSERVATION■ It is important to develop refuges for soil-dwellingbeneficial insects like carabid beetles. For example, rocks,stones and logs close to cropping areas can provide usefulharbourages for adult beetles.

■ Promote diversity in the cropping area, using crop and non-crop plants, including use of live fences (trees or hedgesaround or between crops) (Picture 25).

■ Use mulches to provide harbourages and maintain soilhumidity (Picture 26).

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

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26. Mulch around cropplants (in this case,rape) provides anattractive environmentfor carabid beetles andother ground-dwellingpredators

25. Live fences around a vegetable cropping area

24. Ground beetleadult (Chlaenius sp.)

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Type: Adults and larvae mainly predators; a few species areparasitoidsImmatures: Different from adults (complete metamorphosis). Free-ranging or parasitic larvaeMain Prey: Eggs, mites, aphids, scale insects, other small insects(including immatures, e.g., larvae and pupae)Crops: Most, may be seen on plants or on soilGroup: Insect, beetle, rove beetle (Coleoptera: Staphylinidae)Common names: Rove beetle, staphylinid

APPEARANCEEggs: Not oftenseen.

Larvae:These may be free-ranging,having distinctivesegmented, and,relative to theadults, long,narrow bodies andwell developedlegs and mandibles (‘jaws’), while some species are parasiticand feed within insect host pupae. Size is extremely variable.

Pupae: Not often seen.

Adults: May be earwig-like, but lack the well-developed‘pincers’ at the end of the abdomen (although smallerappendages or cerci may be clearly visible). The distinctiveshort wing cases (Picture 27) of adults do not conceal thesegments of the abdomen. The abdomen may be raised in

a threatening posture (like scorpions) when disturbed. Rovebeetles are often reddish-brown, brown or black. The wingcases may be coloured differently from the rest of the body(Picture 27). They are very variable in size, ranging from about1 mm to 20 mm in length. The smallest ones are difficult toidentify with the naked eye but often become more obvious,owing to their increased abundance, during heavy red spider(tetranychid) mite infestations. During the surveys undertakenfor the present work, one genus of very small staphylinid(Oligata sp., adult about 1mm in length) was found to becommon and predatory on red spider mites in both Zimbabweand Kenya.

EFFECTS ON PESTSSome species of rove beetles, both as adults and larvae, areimportant generalist predators, and are usually more abundantin cropped areas that have a diverse range of vegetation or areclose to natural areas that are themselves diverse (e.g., scrub orforest). These generalist species eat a wide range of insects ofall life stages (eggs through to adults) in the soil or on foliage.They may be important in helping to control pests such ascutworms, beanflies, spider mites and scale insects, althoughmore studies are needed to assess their importance more fully.Other species are parasitic; individual young larvae typicallysearch the soil for suitable host cocoons (containing pupae offly pests, for example), and they emerge from the host cocoonsome time later as adults, having consumed the pupa.

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27. An adult, generalist rove (staphylinid)beetle (Philonthus sp.) searching for prey on a leaf

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CONSERVATION■ It is important to develop refuges for soil-dwelling rovebeetles and other ground-dwelling predators like carabidbeetles. This might be by promoting diversity (crop and non-crop plants) in and around crop plots, using mulches andleaving or importing stones, logs or other items that provideharbourage areas (see also Conservation, Ground Beetles, p. 31)

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

Type: Predator (nymphs and adults)Immatures: Similar to adult (incomplete metamorphosis)Main prey: Thrips, mites, aphids, insect eggs, small caterpillarsCrops: Beans, potatoes, tomatoes, others crops (rarely brassicas)Group: Insect, anthocorid (Hemiptera: Anthocoridae)Common names: Orius bug, anthocorid

APPEARANCEEggs: Not often seen.

Generally laid in plant

tissue.Nymphs: The nymphsare minute (less than 2mm in length) and aretear-drop-shaped(similar to adults); oftenbrown, black or orangein colour.

Adults: Pirate bugs aretiny insects (true bugs),the adults being nolarger than 2-3 mm(Picture 28). The mostcommon genus onvegetable (or flower)crops (Orius andAnthocoris spp.) haveblack and white patcheson their wings. Adultsmove rapidly and can be

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28. Above: Pirate bug nymph(Anthocoris sp.) Below: adult(Photographs courtesy of HorticultureResearch International, UK)

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found hunting prey on leaves and flowers. They suck the bodycontents of their prey with their piercing/sucking mouthparts.Adults can feed on pollen and plant juices when prey are notavailable (Picture 28).

EFFECT ON PESTSPirate bugs can be very important predators of spider mites,thrips and aphids but will attack various stages (e.g., eggs,larvae and nymphs) of a wide range of other small arthropods.An anthocorid nymph may consume up to about 30 spidermites per day. They are particularly common on legume andsolanaceous crops. There are many native anthocorid species inAfrica and their relative effectiveness has yet to be adequatelydetermined.

CONSERVATION■ Planting or maintaining flowering plants (including weeds)near the crop can help to sustain adult pirate bugs when theirprimary prey (mites, thrips and aphids) are not available.

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

Type: Predator (larvae only)Immatures: Larvae (‘ant-lions‘ or ‘aphid-lions‘) different in form toadults (lacewings) (complete metamorphosis)Main Prey: Aphids, other plant-feeding bugs, small caterpillars, insecteggsCrops: Beans, potatoes, tomatoes, others crops (rarely brassicas)Group: Insect, lacewing (Neuroptera: Chrysopidae)Common names: Lacewing larva, aphid-lion, ant-lion, chrysopid

APPEARANCEEggs: Eggs are laid oncharacteristic fine silk stalks(Picture 29).

Larvae: Lacewing larvae areamong the fiercest predators inthe insect world! There are twomain types of larvae, thesebeing commonly known as‘aphid-lions’ (Picture 30) and‘ant-lions’ (Picture 31). Aphid-lions are usually brownand crocodile-like (Picture 30)and possess large pincer-type‘jaws’. They are very mobile and can be found in large numberson some crops (particularly cotton and coffee). They cansometimes be found on vegetable crops. Ant-lions reside justbeneath the soil surface in characteristic pits, with only theirrelatively huge pincer-like ‘jaws’ visible above the surface in theground. Ants are attacked on falling in the pit (Picture 31).

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29. A lacewing egg supportedon a silk stalk from a leaf

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Pupae: These are whitish and spherical, but are not often seenon vegetable crops. They can sometimes be confused withspider egg sacs.

Adults: The adults, commonly known as ‘lacewings’, are oftenseen indoors, near lights in the evenings, or feeding fromflowers. They can readily be distinguished by their finelyveined, net-like wings, large eyes and rather fragile-lookingbodies (Picture 32). The adults only feed on nectar fromflowers and other sugary substances like aphid honeydew.

EFFECT ON PESTSThe effectiveness of lacewing larvae as predators on crops hasbeen well documented on cotton and coffee where largenumbers of larvae (Chrysoperla spp.) can ‘clean up’ a widerange of pests (e.g., aphids and eggs of moth pests). Invegetable crops, which often have a relatively short growingseason, lacewing larvae appear not to be as common and theireffectiveness has yet to be evaluated adequately. Lacewinglarvae are available commercially in many countries forinoculation or augmentation, and are used widely on coveredcrops.

CONSERVATION■ Ensure flowers are present within or close to the crop toprovide a food supply for adult lacewings.

■ Populations can be maintained on non-pest species ofaphids and other alternative hosts on non-crop (weedy) areasaround field margins, between crop cycles.

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

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31. An ant-lion seizes an antwithin its in-ground pit

32. A greenlacewing adult(Chrysoperlacarnea)

30. A lacewing larva (aphid-lion type) (Chrysoperla carnea)searching for prey on a leaf

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tip) (Pictures 35 and 36). This contrasts with the well-definedhead, chewing mouthparts and prolegs of caterpillars. Thebodies of hover fly larvae, like all fly larvae, also lack theprolegs (short, stumpy, appendages used for ‘walking’) of mothand butterfly caterpillars, and sawfly larvae. They may betranslucent, green, or brown in colour, depending on speciesand prey consumed, and the bodies may be slimy-looking or

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Type: Predator (larvae only)Immatures: Different from adults (complete metamorphosis)Main Prey: AphidsCrops: Most where aphids are common, especially brassicas Group: Insect, fly, hover fly (Diptera: Syrphidae)Common names: Hover fly larvae, hover fly maggots, syrphid larvae,aphidophagous syrphids, ‘helicopter’ flies

APPEARANCE Eggs: The eggs, despite their small size, are often easy to seeon the leaves of plants, particularly where aphids are common.They are white,cylindrical and about1-2 mm long. Somespecies lay their eggssingly, close to aphidcolonies (Picture 33),while others lay eggsrandomly on plants inbatches (of often 2-5eggs) (Picture 34), evenon plants that are moreor less un-infested byaphids. The first larvato hatch from one ofthese egg batches cansurvive by eating the larvae within the unhatched eggs. Closeexamination of the egg will reveal whether the larvae havehatched.

Larvae: The larvae are often mistaken for caterpillars but onclose examination they are easily distinguished by their slug-like,tapered bodies and pointed heads (mouthparts retract into the

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33. A single hover fly egg adjacent toan aphid colony (non-pest species onthistle)

35. Last instar hover fly larvafeeding on cabbage aphids

36. Last instar hover fly larva(13mm length) just beforepupation. Note fat stripe alongtop of body

34. A batch of hover flyeggs (one egg has alreadyhatched)

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‘bristly’ in appearance. Some common species are greenish andmarked with one to three whitish (fat-containing) stripes alongthe length of their bodies (Pictures 35 and 36). The first instarlarvae are tiny (1-2 mm) and may not be visible if feedingwithin aphid colonies, while the last (third) instar (Picture 36)may grow up to 15 mm before pupating. However, overall sizedepends both on the species and the amount and quality offood that larvae are able to consume during their development.

Pupae: Pupae are pear-shaped and may be green (Pictures 37)or brown; they are either attached to leaves or develop in thesoil. They can sometimes be attacked by parasitoid wasps (e.g.,Diplazon sp.) that pupate within the hover fly pupa, turningthe pupal case dark brown (Picture 38).

Adults: The adult flies owe theircommon name to the ability ofthe males (in particular) tohover, helicopter-like (Picture39). They are often seen on orclose to flowers that providenectar and pollen as essentialadult food sources, required forthe production of viable eggs(Picture 40). The abdomen ofadult aphid-eating hover flies isoften striped yellow (Picture 39and 41), amber (Picture 40) orgrey on black and is alwaysrather flat when viewed fromthe side (Picture 42). When atrest, adults often raise andlower their abdomens, to assistin ‘breathing’. The adults aresometimes confused withwasps and bees, which belongto a different insect group(Order Hymenoptera). However,two common characteristics set all flies apart from the beesand wasps: flies have only onepair of wings, while wasps have two pairs; and flies havevery short, stumpy antennaethat originate from betweenlarge compound eyes (forminga ‘V’ shape) (Picture 41), whilebees and wasps have longerantennae.

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37. Hover fly pupaeattached to leaf

38. Parasitised hover flypupa

39. Adult hover fly ‘hovering’

40. Hover fly adult (Betasyrphusadligatus) feeding on nectarand pollen within kale flower

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EFFECT ON PESTSHover fly larvae feed on a widerange of food sources, but thegroup which is most importantto crop production are theaphid-eating (aphidophagous)hover fly larvae. In manysituations hover fly larvae arethe most important group ofaphid predators. The larvae are particularly active at nightand are extremely voracious - a single larva can eat well over 400 aphids in about thetwo weeks before it turns intoa pupa! Most of this eating is done in the final (third) instar.Some species only become abundant when aphid numbers are

large and their beneficial effect may be regarded by somefarmers as arriving too late. Others (e.g., Melanostoma andPlatycheirus spp. that lay their eggs in characteristic batches)are well adapted to dealing with low densities of aphids. Bothgroups should be regarded as complementary from a pestmanagement viewpoint. In addition, the adults, like bees, arevery important pollinators.

CONSERVATION■ Flowering plants (such as fennel, thistles, milkweed,sunnhemp, flowering brassica crops or ‘weeds’) must be grownwithin or at least around crop plots to provide an adult foodsource (Picture 43). This increases immigration of adults to theplots, and because adult females must feed on pollen andnectar before they can lay viable eggs, it also prevents ‘loss’ ofadults that emerge from pupae from within the crop. Theseflowering plants may also support aphids (often of non-pestspecies; Picture 33), which provide an on-going food supply tohelp maintain hover fly populations in the vicinity of the crop.

■ Live fences can contain flowering plants (see above) andalso reduce wind speed that might otherwise disturb the

egg-laying activities of gravid female hover flies.

■ Avoid spraying pesticidesunless absolutely necessary.Should spraying be considerednecessary, use a product andapplication method that is theleast harmful to key naturalenemies (see Parts 3.2 and 3.3of this guide).

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41. Hover fly adult feeding from a flower. Notesingle pair of wings and short antennae typicalof all adult flies

42. Hover fly adult femalesearching for egg-laying site on leaf

43. Abundance of floweringplants (including flowering kalepictured) provides plentiful foodsources (nectar and pollen) foradult hover flies

45. Predatory mites(Phytoseiidae) among largecolonies of red spider mites(Tetranychus sp.)

44. Tomato leaves showingsymptoms of heavy red spidermite infestation. Althoughpredatory mites can often befound on such heavily damagedplants, they probably arrivedtoo late from the farmer’sviewpoint

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Type: PredatorImmatures: Similar to adults (early stages with only three pairs oflegs) (incomplete metamorphosis)Main Prey: Plant-feeding mites (e.g., red spider mite), thrips, insecteggsCrops: Crops susceptible to spider mites and thrips (e.g., tomatoes,egg plant, beans)Group: Mite, phytoseiid (Acarina: Phytoseiidae)Common names: Mites, phytoseiids

APPEARANCEEggs: Laid on plants, round or oval in shape, too small to beseen with the naked eye.

Nymphs: Similar but smaller than adults, the early instars withonly three pairs of legs, compared with the four pairs of oldernymphal (and adult) stages.

Adults: Mites are so small that they can barely be seen withthe naked eye. They are not insects and are more closelyrelated to spiders and are even closer relatives of ticks. As such,the adults have four pairs of legs and two body segmentsrather than the three of insects. They can often be found onplants where plant-feeding tetranychid mites (red spider mites)are present (Picture 44). They are about the same size (lessthan 1 mm in length) as spider mites but they move muchmore rapidly, have longer legs and more oval (pear-shaped)bodies (Picture 45). They may be red in colour, dark or eventranslucent in colour, depending on species and growth stage.Unlike spider mites, predatory mites can also move backwards.Red spider mites are often distinguished by the presence of twodark spots on the body, and characteristic webbing which theyproduce on infested plant parts. Predatory mites such asPhytoseiulus, as with the plant feeding spider mites are variable

in colour, depending on their growth stage (Picture 45).Therefore, colour must not be used as the only way ofseparating these mite types!

EFFECT ON PESTSPredatory mites (e.g., Amblyseius, Phytoseiulus spp.) can be oneof the most effective natural enemies of spider mites. They cansearch out spider mite colonies effectively and can reach areasthat are difficult to target with pesticides. The most serious spidermite problems are often found on crops that are sprayed regularlywith acaricides or insecticides, pest resurgence being caused bythe pesticide killing predatory mites and other key predators(e.g., predatory thrips, rove beetles) (see also pp. 13-14). If

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predatory mites are not found on a crop being damaged byspider mites, they can be introduced (inoculated). They canreadily be reared for this purpose and in an increasing numberof countries they are commercially available as biologicalcontrol agents. However, most common species of predatorymites will starve and die if they run out of food, so theyshould only be introduced to crops where primary prey such asspider mites or thrips are already present. Some species (e.g.,Typhlodromus spp.) are able to survive on pollen and fungalspores in the absence of prey. Predatory mites can also be veryeffective against thrips.

CONSERVATION■ Predatory mites may be sustained in culture on pottedplants deliberately infested with spider mites, ready forintroduction as and when spider mite or thrips problems arise.They are available commercially in many countries forinoculation purposes.

■ There tends to be an association between the degree ofhairiness of crop leaves and abundance of predatory mites. Thereasons for this are not fully understood but cultivars withhairy leaves might help to reduce high temperatures, increasehumidity, provide protection from predators and help tocapture other food items such as pollen and fungal spores.

■ Maintain irrigation of crops to avoid dusty conditions whichoften contribute to spider mite outbreaks as they are harmfulto predatory mites.

■ Predatory mites are common on trees, shrubs and otherperennial plants, so the presence of these plants near vegetablecrops will often enhance the immigration rate of predatorymites into seasonal crops such as vegetables.

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

Type: PredatorImmatures: Different from adults (complete metamorphosis)Main prey: Caterpillars, sawfly larvae, heteropteran bugs Crops: Any crops on which caterpillars, sawfly larvae, bugs and otherprey are presentGroup: Insect, wasp (Hymenoptera: Polistinae, Sphecidae andVespidae)

APPEARANCEEggs: These are not seen as they are laid within wasp neststhat may be in the ground, in or on trees and other vegetation,or even around buildings and other structures.

Larvae and pupae: Wasp larvae and pupae are also not seenunless nests are opened up.

Adults: These are largewasps, often 12-30 mmin length, generallywith some form ofstriped marking on theabdomen (Pictures 46and 47). They may besolitary or they maylive in groups(eusocial). They includethe paper (polistine)wasps (Hymenoptera:Polistinae; Picture 46)that form characteristic‘papery’ andhoneycombed nests

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46. A paper wasp (Polistes sp.)collecting prey for its young

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Type: Predator (nymphs and adults)Immatures: Similar to adult (incomplete metamorphosis)Main prey: Moths, flies, crickets, small spidersCrops: VariousGroup: Insect, mantid (Order Mantodea)Common names: Praying mantis, mantis

APPEARANCE Eggs: Females lay these in a sac containing hardened foam.

Nymphs: Form and function similar to adults, although smallerin size.

Adults: Mantids have characteristic forelegs that assume a‘praying posture’ when at rest, hence the common name,praying mantis(Picture 48). Mantidswait motionless,often wellcamouflaged withinfoliage until preycome within theirgrasp. Then they willsuddenly pounce,grasping their preywith their powerfulforelegs – and thefeast begins! Theadults are strongflyers so can dispersewidely.

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often foundsuspended by a stalkfrom the leaves oftrees or sides ofbuildings, and thesphecid wasps(Hymenoptera:Sphecidae; Picture47) that can exceed40 mm in length.

EFFECTS ON PESTSOn crops wherecaterpillars, sawflylarvae or other preyare abundant,

predatory wasp adult females can be seen repeatedly on‘sorties’ in search of prey. Prey are stung, paralysed and takenback to the nest to provide a food source for developinglarvae. Nests may be in the ground, in natural cavities withintrees, stumps, or they may be constructed of mud or ‘paper’.Although the predatory habit of members of these waspfamilies is often highly conspicuous, their impact on pestpopulations has not been well studied and therefore is poorlyunderstood.

CONSERVATION■ Avoid destroying nesting sites, unless the presence of thewasps poses a threat to humans, especially young children, whocould be stung.

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

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48. A praying mantis adult in resting poseon a sunflower plant close to a vegetableplot

47. A sphecid wasp (Sphex sp.) in searchof prey, heteropteran bugs in particular

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EFFECTS ON PESTSAlthough the praying mantis is one of the most well-knowninsect predators, the extent of its value as a natural enemy ofagricultural pests has not been well evaluated. Since mantidsare rather indiscriminate feeders, eating natural enemies (e.g.,beneficial flies and spiders) as well as pest insects (e.g., somemoths and flies), their beneficial role may in some situations be partially offset by negative impacts on other naturalenemies. However, their presence is often an indication thatindiscriminate use of broad spectrum insecticides or acaricidesis not occurring.

CONSERVATION■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

Type: PredatorImmatures: Similar to adults (incomplete metamorphosis)Main prey: Flies (e.g., leaf miners), moths, small caterpillars, mites, aphidsCrops: Most Group: Spider (Arachnida: Araneae)

APPEARANCEEggs: Egg sacs ofspiders are usuallyspherical in shape and covered in whitish-coloured silk.The eggs within thesac hatch to releaseseveral or sometimeseven hundreds of tinyspider nymphs that aresometimes calledspiderlings.

Nymphs: These appearvery similar to theadults, except in size.Small, young spiderscan produce threads of silk that aid their dispersal by windcurrents. This behaviour is called ‘ballooning’ or ‘parachuting’.

Adults: Spiders are recognised by everyone! Like mites, they arenot insects. They have two body segments and four pairs oflegs. They feed by sucking the body fluids from theirarthropod prey. Many species trap their prey in nets or webs,

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49. Webbing spider and sheet web (Family Linyphiidae)

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while others forage actively or lie in wait before pouncing ontheir prey. Spiders from various families may be found onvegetable crops, including sheet webbing spiders (Linyphiidae,Picture 49), crab spiders (Thomisidae; Picture 50), lynx spiders(Oxyopidae; Picture 51), wolf or ground spiders (Lycosidae),jumping spiders (Salticidae) and orb weavers (Araneidae).

EFFECT ON PESTSAlthough spiders or their webs may sometimes be regarded as a nuisance around the home, spiders can be very importantpredators on agricultural crops including vegetables. Spidersfound on crops can be divided broadly into two groupsaccording to how they hunt their prey: webbing spiders (Picture49), such as sheet web spiders, which spin webs that in turntrap prey, and hunting spiders (Pictures 50 and 51), such ascrab, jumping or wolf spiders, that rely on their ability topounce on and overpower their prey. In some agriculturalsystems, such as rice in Asia, spiders, particularly wolf spiders,can be the dominant natural enemy of key pests. However, asgeneralist feeders, they may sometimes prey on natural enemyas well as pest species.

CONSERVATION■ Do not remove spider webbing or egg sacs from plants.

■ Avoid spraying insecticides or acaricides unless absolutelynecessary. Should spraying be considered necessary, use aproduct and application method that is the least harmful tokey natural enemies (see Parts 3.2 and 3.3 of this guide).

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50. Crab spider (FamilyThomisidae)

51. Lynx spider (Peucetia sp., Family Oxyopidae)

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There are many other types of predator, representing a diverse range of animal groups, that can prey on pests ofvegetable crops. Some of these other predators are consideredbelow.

OTHER INSECT PREDATORSAlthough the predatory role of particular life-stages of thefollowing insects is well known, the importance of each groupin tropical vegetable cropping systems is presently not wellunderstood.

■ AntsAnts (Hymenoptera: Formicidae), like all bees and many wasps,are social insects and so have a division of labour betweendifferent groups (i.e.,workers, soldiers andreproductives) withineach colony. Theworker ants,comprised of sexuallyundeveloped females,are responsible forfood collection andhence are the casteencountered mostcommonly (Pictures52 and 53). Workerants generally usetrails as a means ofsearching for and collecting food. Larvae and pupae, which arewhitish in colour and grub-like, are maintained in below- orabove-ground nests that can be some distance from foragingsites. Some species of ants can be important predators, whileothers, referred to as ‘attendant ants’, can protect aphids and

other sucking pestsfrom attack by naturalenemies as a means ofsecuring their supply ofhoneydew (the sticky,sugar-based secretionproduced by suckingpests).

■ Predatory bugsThese include three important predatory groups of true bug (Order Hemiptera): minute pirate bugs (Hemiptera:Anthocoridae; p. 37), nabid bugs (Hemiptera: Nabidae) andassassin bugs (Hemiptera: Reduviidae). Other families of truebug that include many plant-eating members, such as lygaeidbugs (Lygaeidae), mirid bugs(Miridae) and shield bugs(Pentatomidae) also containspecies that are predatory.Assassin bugs (Picture 54) arethe largest in size, with adultstypically being 30 - 40 mm inlength. They all undergoincomplete metamorphosis, sothe nymphs are similar inbasic form to the adults(although colours may varysubstantially) and they feedby sucking body fluids fromtheir prey.

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52. Ants removing a caterpillarfrom a bean pod

54. Assassin bug; notebeak used for sucking bodyfluids of prey

53. ‘Safari’ ants carrying adiamondback moth caterpillar afterclearing it from a kale plant

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■ Predatory thripsThrips (Order Thysanoptera), some of which are important plant-sucking pests, undergometamorphosis which isintermediate, with immatures which look essentially similar to the adults, although the first twoinstars, often referred to as larvae,never show wings externally. Wings,when present and fully developed,are four in number, and are long, narrow and fringed withlong hairs, giving them a feathery appearance when viewedunder magnification. The final two instars (usually the thirdand fourth) do not feed and are often referred to as the pre-pupal and pupal stages respectively. The pupae may beenclosed in a cocoon. Most thrips are plant feeders, attackingflowers, leaves, fruits and buds. However, a small number ofspecies are predatory on other small arthropods. These appearrather similar to plant-feeding thrips, being very small (often1-3 mm in length) with characteristic bullet-shaped bodies.Their colour may be uniform varying from opaque to black,while others may appear banded (Picture 55) or have spotmarkings on their ‘feathery’ wings. They can at times beabundant and important natural enemies of mites and many small insects, including leaf miner larvae.

■ Dragonflies and DamselfliesThese insects (Order Odonata) both have aquatic immature(nymph) life stages, so they are particularly common in cropsnear ponds, streams, rivers and irrigation canals. The fast-flyingadults are often seen resting on plants (Pictures 56 and 57)between bouts of searching for insect prey on vegetable andother crops. Most of the adult prey, which include a wide rangeof small flying insects such as flies and moths, are caught andoften eaten while the adults are in flight.

60 61

55. A predatory thripswithin a leaf mine onbroad bean

56. A dragonfly (SuborderAnisoptera) adult resting ona non-crop plant near avegetable crop

57. A damselfly (SuborderZygoptera) adult at rest on

reeds near water

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FROGS AND TOADSAmphibians such as frogs andtoads have a healthy appetitefor insects, although they mayeat pests as well as naturalenemies. Small ‘tree frogs’,about 20-30 mm in length(Picture 58), are notuncommon on unsprayedvegetable crops where theycan feed on a wide range ofinsects including aphids andcaterpillars. They need waterin which to lay eggs andallow development oftadpoles, but this may be in

any area where small quantities of water accumulate, such asthe axils of plants (Picture 58).

REPTILESChameleons (Picture 59) andlizards (Picture 60) are frequentlyfound in vegetable crops,particularly those where broadspectrum pesticides are not used.They feed on a wide range ofinsects and other arthropods, butbecause pests tend to be lessmobile than natural enemies, pestsare often a more important foodcomponent.

BIRDSMany bird species, such as shrikes, can forage for insects andother animals in vegetable crops. However, birds may alsodamage leaves and fruits.

MAMMALSRats are not uncommon visitors to vegetable crops, andalthough they may feed on certain insects present, they mayalso cause serious damage to crops. Humans can be naturalenemies too! Particular life stages of pests can be removedselectively by hand (Picture 61).

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58. Tree frog in axil of bananaplant, also found foraging forinsect pests on nearbyorganically-grown brassicacrops

60. A lizard searchingfor prey in a mixedorganic crop

61. Humans aspredators: hand-pickingbollworm (Helicoverpasp.) pupae fromcabbage plants on anorganic farm

59. A chameleon searching for foodsources, notably aphids, on kale

plants on an organic kale crop

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Type: ParasitoidImmatures: Different from adultsMain prey: All pest insects, including caterpillars (moth larvae),aphids, bugs, fly larvae, insect eggs, beetle and fly larvae, insect pupaeCrops: AllGroup: Insect, wasp (Hymenoptera: Braconidae [incl. Aphidiinae],Ichneumonidae, Chalcidae, Eulophidae, Trichogrammatidae, andothers)Other common names: Parasitoid, parasitic wasp, parasite, wasp

APPEARANCE AND BIOLOGYThere are about 50,000 described species of parasitoid waspand many of them are so small that they go unnoticed. To theuntrained eye, these wasps look rather like small flies or flyingants (see Pictures 65 and 66 on pp. 67-68). Some, notably eggand leaf miner parasitoids, are so small they often requiremagnification to be distinguished as wasps. Unlike the muchlarger predatory wasps (pp. 51-52), which have the ability toinflict a painful sting on unwary humans, parasitoid wasps,with very few exceptions, cannot sting any animal other thantheir insect host. In parasitoids, stinging by females is theprocess by which eggs are laid (oviposition). In many crop/pestsituations, parasitoid wasps are the single most importantgroup of natural enemy, although their impact can be hard toevaluate without detailed study (see Part 3.1 of this guide).

Parasitoid wasps comprise a very diverse group with complexand variable biologies, spread across a large number of familieswithin the Order Hymenoptera. Parasitoids also exist within thefly (Diptera: Tachinidae, p. 76) and beetle (e.g., Coleoptera:Staphylinidae, p. 34) families. Parasitoid wasps nearly always

64

lay their eggs within or on the body of their host (prey) andthe eggs hatch into larvae that feed on the host. After pupationwithin or outside the host’s body, the adult parasitoid waspemerges, usually as a small, dark-coloured, winged wasp(typically 1- 6 mm in length). Some species of parasitoid waspshave wingless adults that appear ant-like. The prime purposeof the adult stage is dispersal and reproduction, although someadults are predaceous and may host feed, killing pests (andpotential hosts) in the process. Host feeding is common inadult parasitoid wasps that attack leaf miner larvae (p. 70).Adults locate mates and, following mating and fertilisation,the females lay eggs, the cycle beginning once again.

There may be few or no outward symptoms of a larvalparasitoid’s presence within its insect host. In other cases, the host insect may become swollen or permanently paralysedafter being ‘stung’. Parasitoid wasps may pupate within oroutside the host’s body. Field collection and rearing of immaturestages of pests, to check if any adult parasitoids emerge, isoften a useful method for determining whether parasitism hasoccurred (see Part 3.1 of this guide). In vegetable crops,parasitoid wasps that attack aphids (pp. 65-66), moth pests(caterpillars and eggs) (pp. 68-70), leaf miners (pp. 70-71) and whiteflies (p. 72) are particularly important.

APHID PARASITOIDSThe first obvious indication of aphid parasitism is usually the

presence of aphid mummies (Pictures 62 - 63). Mummified

aphids have been killed by the wasp larva, which will have

consumed the aphid’s body contents, leaving only the aphid’s

cuticle (skin) as the parasitoid’s cocoon. The cuticle changes

colour, often becoming brown, golden, pinkish or black,

depending on the particular parasitoid wasp and aphid species

attacked. With many species, following pupation within the

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aphid, the newly-formed adult parasitoid wasp chews a circular

exit hole through the dead aphid’s cuticle (normally towards

the back of the aphid) (Picture 64) and emerges. Some aphid

parasitoids emerge as late stage larvae and spin their cocoons

beneath the dead aphid’s body. Adult aphid parasitoids

(Picture 65) are very small (2 - 3 mm in length), dark coloured

and have rather long antennae. The careful observer will be

able to watch adult females ‘stinging’ aphids, in the process

laying eggs, usually only one per aphid. Only a single

parasitoid develops within each host aphid. Each female will

typically lay between 50 and 100 eggs during her lifetime.

Many species of parasitoid are specific to only a single host or

a very narrow range of host species (specialists), while others

have a wider host range (generalists).Counts of aphid mummies compared with unparasitised aphids(often expressed as a percentage) will normally significantlyunderestimate the amount of parasitism, since these counts donot take into account parasitism of aphids that have yet to

become ‘mummified’ (see Part 3.1 of this guide). It is notpossible to tell visually whether un-mummified aphids havealready been parasitised as mummification does not occur untilthe parasitoid reaches the pupal stage within its host aphid.

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62. Cabbage aphid colonyshowing mummified (brown)and un-mummified (grey)aphids

63. Aphid colony (Myzuspersicae) with mummified aphidin centre

64. Cabbage aphid mummieswith exit holes, indicating thatadult parasitoid wasps havepupated and emerged

65. An adult aphid parasitoid,Diaeretiella rapae (Braconidae:Aphidiinae), one of the mostimportant parasitoids of aphidson brassicas

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PARASITOID WASPS OF CATERPILLARSThe larvae of these parasitoidsmay feed from within(endoparasitoids) or outside(exoparasitoids) their host’sbody. However, it is usuallythe former group that aremore important as naturalenemies of caterpillars onvegetable crops (Pictures 66to 72). Depending largely onthe species of parasitoid,either a single wasp, a smallnumber or a large number ofwasps (sometimes more than100) will develop within eachcaterpillar. Late stageparasitoid larvae may emergefrom their host, attachingtheir cocoon either to thedying caterpillar’s body or tothe plant surface (as inCotesia sp., Pictures 67 to 69)or they may consume thebulk of the caterpillar beforepupation (as in Diadegma sp.,Pictures 70 to 72). Parasitoidwasp cocoons (pupal cases)may be covered in white silkspun by the parasitoid itself(Pictures 68 and 69) or theymay be contained within thehost’s own pupal sheath(Pictures 71 and 72).

67. A braconid larva (Cotesiasp.) emerging through the sideof a final instar diamondbackmoth larva, prior to spinning itscocoon

66. Cotesia sp., a braconidparasitoid wasp and keyendoparasitoid of diamondbackmoth

68. Right: The silk-coveredcocoon containing the pupa ofa braconid parasitoid (Cotesiasp.) of diamondback mothlarvae. Left: The mortallywounded host larva, showingthe hole to the right side of itsbody from which the parasitoidlarva emerged before spinningits cocoon

69. A Cotesia sp. cocoon on aleaf. The neat cap on the leftside shows that an adult hasalready chewed its way out andemerged

70. Diadegma sp., an ichneumonidparasitoid wasp, and key endolarvalparasitoid of the diamondback moth

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LEAF MINER PARASITOIDSBlack-coloured, tiny parasitoid wasps (around 1 mm in length)can be very important in the control of leaf miner flies(Diptera: Agromyzidae), particularly in situations where broadspectrum insecticides are used regularly. However, leaf minerscan become a huge, induced problem where indiscriminatespraying occurs. This is because they readily become resistantto many insecticides and their key natural enemies that includevarious parasitoids and predatory thrips species are killed. Ifleaf miners are allowed to establish in a younger crop byavoiding applications of broad spectrum insecticides, it is often found that their abundance diminishes in response toincreasing numbers of leaf miner parasitoids over the croppingperiod.

Two genera of leaf miner parasitoids are commonly found inZimbabwe, these being Meruana and Diglyphus, although they

can usually only be separatedby specialist taxonomists.These wasps should not beconfused with the slightlylarger leaf miner flies. Themost common leaf miner fliesbelong to the genusLiriomyza, and these adultsare distinguished by a yellowspot on their thorax (Picture73). Eggs are laid by adultfemale wasps within leafminer larvae through the leafepidermis, larvae developwithin the body of the host(Picture 74) and pupationoccurs in the mine (Picture 75).

70 71

71. Left: A Diadegma sp.cocoon within a silken sheathof a diamondback mothprepupa. Right: anunparasitised diamondbackmoth pupa within its sheath

72. As for Picture 71, but thesilk sheaths of thediamondback moth have beenremoved to show more clearlythe differences between theparasitoid cocoon (left) anddiamondback moth pupa (right)

73. An adult leaf miner fly(Liriomyza huidobrensis) on abean leaf

74. A leaf miner parasitoidlarva visible within the body ofa leaf miner (Liriomyzahuidobrensis), exposed afterpeeling away the lowerepidermis of a bean leaf

75. A leaf minerparasitoid pupafound within aleaf mine

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WHITEFLY PARASITOIDSThese are tiny parasitoids (Family Aphelinidae e.g., Encarsiaformosa, less than 1 mm in length, available commercially insome countries for release on covered crops) and their presenceis often noticed in the field when parasitised whitefly nymphsturn black or brown (Picture 76). Apart from mortality causedby parasitism (larval feeding within the nymphs), adult waspsalso host feed, killing more whitefly in the process.

EGG PARASITOIDSThis is another important group of tiny parasitoids (FamilyTrichogrammatidae), the adults often being less than 0.5 mmin length. The adults generally have bright red eyes, shortantennae and their bodies may be coloured black and yellow,or yellow. They lay their eggs (one or several per host egg)within moth eggs on a wide range of vegetables and othercrops. Moth eggs turn black when the wasp pupates within theegg, this characteristic being a useful trait for recognition.

FIELD INTRODUCTIONSIf an important parasitoid often associated with a particularpest in other parts of the country or region is not present, itmay be possible to establish it locally by introducing a smallgroup of the parasitoid (perhaps 50 -1000, both sexes) in thevicinity of appropriate hosts. This process is sometimes referredto as introduction or inoculation (see also p. 18). This type ofintroduction may be appropriate in some smallholder systems,for example, a small highland plot isolated from othervegetable growing areas.

CONSERVATIONConservation techniques thatprovide parasitoids with adequatefood sources, shelter and means ofreproduction on the farm arerequired to ensure efficientpopulation growth. Some keymethods are considered below:

■ Ensure ample numbers offlowers, containing nectar, areprovided as adult food sources forparasitoids and other adult naturalenemies. This might include thegrowing of fennel (Picture 77),coriander, nasturtiums (Picture 78),flowering crucifers or sunnhempclose to, between, and/or aroundthe crop. The use of marigolds byorganic farmers (Picture 79) isthought to repel certain pests morethan it attracts natural enemies.

72 73

76. Parasitised (dark-coloured) andunparasitised (opaque)whitefly nymphs on theunderside of a leaf

77. Fennel (and manyother flowering plants)provide a useful nectarresource for adultparasitoids and othernatural enemies

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■ Encourage habitat, plant andanimal diversity in cropping areas(Pictures 80 and 81); develop amixed cropping system and includenon-crop plants (sometimesthought of as ‘weeds’) that providenectar sources and alternative hostsfor parasitoids.

■ Provide shelter and shade forparasitoids by growing live fences(Picture 82) around plots.

■ Grow trap crops that can allowsome build-up of plant-feeding

insects (that may be alternative hosts or pests) and theirnatural enemies, which can in turn provide early suppression ofpests on the nearby principle crop (Picture 83).

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

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78. Nasturtiums growing within asmallholder plot, used as a foodsource both for natural enemiesand humans

80. A smallholder organicfarm, including mixedcropping, livestock and useof compost

79. Marigolds growingadjacent to kale plants,

used more to repel peststhan attract natural

enemies

81. A diverse habitat fornatural enemies, based onmixed cropping and provisionof flowering plants

82. A live fence bordering avegetable growing area on anorganic farm

83. Sweet sorghum, a trap cropfor bollworms (Helicoverpa andDiparopsis spp.), used here in asmallholder organiccotton/vegetable mixed crop(Photograph by Meg Davies)

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markings (Picture 84). Being flies,they only have a single pair ofwings (which may also possessmarkings and be less translucentthan those of a house fly) andthese are often held slightly orpartially out-spread when at rest.

EFFECT ON PESTSTachinids make up a very largefamily of flies, containing bothhighly specialised types which

attack only a single or narrow range of species, as well asgeneralists which attack a much wider range of species. As withparasitoid wasps, it is the larval stages of parasitoid flies thatattack other insects (and occasionally other arthropods) and itis difficult to evaluate their population impact without detailedstudy. Generally, parasitoid flies have not been as well studiedas parasitoid wasps. However, their short generation timemeans that populations can build-up rapidly. On farms wherethese flies are found to be numerous, it is likely that they areexerting important regulatory pressure on pest populations.

CONSERVATION■ Ensure adequate, sugar-containing food sources areavailable for adults, such as flowers, plant sap or honeydew.

■ Encourage habitat diversity, as for parasitoid wasps (seeParasitoid Wasps; Conservation: p. 73).

■ Avoid spraying pesticides unless absolutely necessary.Should spraying be considered necessary, use a product andapplication method that is the least harmful to key naturalenemies (see Parts 3.2 and 3.3 of this guide).

77Parasitoid Flies

Type: ParasitoidImmatures: Different from adults (complete metamorphosis)Main prey: Cutworms, caterpillars, beetle larvae, fly larvae, bugsCrops: Brassicas, potatoes, cucurbits, maize and othersGroup: Insect, parasitic fly (Diptera: Tachinidae, and some otherFamilies)Other common names: Tachinid, parasitoid, parasitic fly, parasite, fly

APPEARANCEEggs: The eggs of tachinids, the most important group ofparasitoid flies, can sometimes be seen with the naked eye ontheir hosts such as caterpillars and beetle larvae. The eggs aretiny (less than 1 mm in length), white or off-white in colourand oval in shape. Some tachinids lay their eggs on leavesrather than directly on the host body.

Larvae and pupae: Eggs normally hatch on the host body andlarvae then burrow through the body and feed internally. Withspecies that lay their eggs on foliage, eggs or young flattenedlarvae (called planidia) are ingested by caterpillars or otherpests whose body contents provide a food source for thedeveloping larvae. Parasitism nearly always results in death ofthe host insect. Pupation occurs either within or outside thebody of their hosts. Some species pupate in the soil.

Adults: The adult flies look rather similar to common flies suchas house flies, flesh flies or blow flies, but they are more robustand hairy (or bristly) than house flies, typically being between8 – 12 mm in length. Their most identifiable feature are thelong and short bristles usually clearly visible on the abdomen(Picture 84). Their bodies are often grey in colour, with

84. Adult tachinid(parasitoid) fly. Notebristles on abdomen andsingle pair of wings.

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The most important naturally-occurring disease causingpathogens of vegetable pests are generally fungi and viruses.These disease organisms tend to be more common during rainyseasons, are difficult to manipulate and they may beunpredictable as to their presence or effect. However, onoccasions, disease outbreaks will occur and over a very shortperiod, can cause complete collapse of pest populations. Manypathogens (e.g., granulosis viruses, certain bacteria and fungi)are highly specific to particular pests. The primary pathogenswhich attack insects are specific to insects and closely relatedarthropods and cannot cause disease in unrelated organismssuch as humans.

Entomopathogenic fungiFungi, when sporulating,usually cause their insecthost to become covered ina cream-coloured (Picture85), green, red or greycoloured mould. Aphids,caterpillars and a widerange of other pests maybe found infected by fungi.Spores are transferred oninsect bodies, in rainwateror in the wind, and hyphae(fungal strands) enter theinsect body via openings(e.g., breathing holes, anus).The fungal hyphae ormycelia develop and consume the insect from the inside. Signsof infection tend to be quite easy to find during sustained wetor humid conditions, such as those found during rainy seasons.Considerable research is on-going to develop biologicalpesticides based on fungal pathogens, particularly Metarhizium

anisopliae. At particular times of year, other genera of fungisuch as Zoophthora and Entomophthora can be readilyencountered in the field infecting pests such as caterpillars and aphids.

BaculovirusesA wide range of viruses

specific to insects, known

as baculoviruses, have been

identified in wild populations

of insects and some have been

multiplied in sufficient

quantity to be used as

‘biological pesticides’.

Virus-infected insects, notably

caterpillars, tend to be found

more commonly in heavy

infestations, particularly during

prolonged wet seasons. The

two most common types of

baculovirus encountered are

species-specific granulosis

viruses (GVs) and nuclear

polyhedrosis viruses (NPVs).

Recent investigations in Kenya

have been carried out to assess

the potential for using a GV specific to the diamondback moth

(PxGV) in brassica crops. Infected larvae typically appear pale

and swollen (Picture 86), and the development of the final

instar is delayed considerably. Infected insects usually die prior

to adulthood and turn brown or black after death owing to

secondary infection by bacteria. NPVs, such as the soya-bean

85. Left: Fungal infecteddiamondback moth caterpillar(Zoophthora sp.). Right: healthycaterpillar

86. Left: A healthydiamondback moth larva(fourth and final larval instar).Right: a fourth instardiamonback moth larva in thelate stages of infection by PxGV

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semi-looper virus used in

Zimbabwe, often cause the

caterpillar’s cuticle (skin) to

become flaccid (weak and soft),

and heavily infected or dead

caterpillars tend to be found

hanging from leaves, the body

contents having turned to

liquid, charged with virus

particles (Picture 87).

Viruses need to be consumed(unlike fungi) in order to enterand replicate within the insectbody. One of the mainconstraints to the sustainableuse of viruses as ‘biologicalpesticides’, which can be applied to infected crops much in thesame way as conventional pesticides, is the cost of small-scaleor commercial virus production.

BacteriaInsects such as caterpillars infected by bacteria can sometimesbe found in the field. Following infection, they generally turnbrown or black and die. Bacillus thuringiensis (Bt) is a naturallyoccurring bacterium, found both in the soil and on plants, andis the most well-known bacterial pathogen of insects.

Several formulations of various Bt products are availablecommercially for use against caterpillar pests of vegetablessuch as diamondback moth (Plutella xylostella) and Africanbollworm (Helicoverpa armigera). These products tend to behighly effective against their target pests and have little or no

effect on natural enemies. Although a caterpillar may takeseveral days to die after ingesting the product, it stops feedingshortly after exposure, so dramatically reducing crop damage.

Bt products can be applied with spraying equipment in thesame variety of ways as conventional insecticides. However,they cannot be regarded properly as biological agents sinceeither the bacterial cells themselves are not present within theformulation, or if present, they are not living. Theseinsecticides are some of the least harmful to other arthropodsand natural enemies (see Part 3.2, p. 91). The often highlyspecific insecticidal effect is caused by toxic proteins(endotoxins) produced by various subspecies of the bacterium.

Entomopathogenic nematodes (EPNs)EPNs are found in soils all over the world, particularly inlighter soils and in coastal areas. They are small, long, thinroundworms that can usually only be seen under a microscope.Recent surveys have been carried out in both Zimbabwe andKenya, with the purpose of finding virulent isolates. EPNsbelong to two genera: Steinernema (Picture 88) andHeterorhabditis. The insect host is actively infected in the soilby a specialised third stage juvenile (about 1 mm in length),known as a dauer larva (or infective juveniles). EPNs have asymbiotic (mutually beneficial) relationship with particularspecies of bacteria: Steinernema with Xenorhabdus species andHeterorhabditis with Photorhabdus species. Infection by thesebacteria often provides a useful clue to the genus ofnematode: the bodies of insects killed by Xenorhabdus aretypically yellow to orange in colour while those killed byPhotorhabdus species can be bright red. These bacteria arereleased from the nematode into the body cavity of the insect,

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87. A semi-looper caterpillar onsoya, killed by a NuclearPolyhedrosis Virus (NPV)(Photograph courtesy of NaturalResources Institute, UK)

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3Evaluation of

natural enemies, and pesticide selectivity

Page

3.1 An introduction to natural enemy evaluation 84

3.2 Pesticide side effects on natural enemies 91

3.3 Selective pesticide application 103

multiply rapidly and kill the host within 48 hours bysepticaemia. The nematodes feed on the bacterial cells and host tissues, develop and reproduce. When food supplies runout, nematode development stops at the dauer larva stage and these escape into the soil to find new hosts.

The role of EPNs in regulating insect populations in soils isnot well understood. However, EPNs can be mass produced on a commercial scale on solid or liquid media and in anumber of countries around the world are now used as‘biological insecticides’ against a variety of insect pests(especially caterpillars and beetles). EPNs are regarded widelyas being very environmentally friendly with no adverse sideeffects reported.

88. Entomopathogenic nematodes [infective juveniles] (Steinernemacarpocapsae) emerging from their dead Spodoptera caterpillar hostin search of new hosts

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.13.1 Natural Enemy Evaluation3.1 Natural Enemy Evaluation

An introduction to natural enemy evaluation

BackgroundBeing able to distinguish natural enemies from pests and thencounting the numbers in each of the two categories will notprovide you with enough information to be able to makemeaningful judgements on the effectiveness of differentnatural enemies on specific pests. The whole subject of naturalenemy evaluation is complex and one that has only recentlybecome a major focus for researchers working in the field ofbiological control of pests. This part of the guide aims tooutline some of the important principles that need to be bornein mind when carrying out evaluations or interpreting data thathas already been collected. It serves particularly to provideinformation on some common shortcomings of evaluations.

Principles of field evaluationMany of the methods now being used by researchers to assessnatural enemy effectiveness involve studies of natural enemyegg production, consumption rates, lifespan, development time,movement rates and numerous other factors. These methodsrequire detailed laboratory and field investigations by highlyspecialised personnel over long periods of time, and are notappropriate for the extension worker or farmer. Nevertheless,some important principles of this type of work are relevant tothose involved in pest management decisions at the farm-leveland it is to these that we now turn.

Evaluations of abundance in the fieldCounts of natural enemies (and pests) are often the startingpoint of an evaluation. However, there are numerous problemswith how the count data are then interpreted. Some of themajor reasons why the numbers of natural enemies found onplants vary from one assessment to the next are consideredbelow:

a) Population fluctuations. Natural enemy numbers vary overtime because many populations follow a similar pattern offluctuation as their hosts or prey (i.e., pests). However, since many natural enemies multiply in response to theavailability of food, there is often a ‘time lag’ between pestand natural enemy population fluctuations. This is showngraphically in Figure 1. Therefore, if only a single assessmentwas undertaken and this was carried out at time 1 (t1), avery different picture of natural enemy abundance would beobserved compared with a later assessment at time 2 (t2).

Figure 1. Typical fluctuations of pest and natural enemy abundanceover time

This demonstrates the need to evaluate natural enemies andpests throughout the cropping season. In detailed studies,this is often carried out at weekly or two weekly intervals.Management practices, which may include applications ofpesticides or cultural manipulations, will also tend tocontribute to fluctuations of pest and natural enemyabundance, so the role of these must be taken into accountduring evaluations.

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b) Assessments at different times of the day. If an assessmentof natural enemy numbers is undertaken at 8.00 am oneday, 12.00 midday on another and 6.00 pm on yet another,differences in number of natural enemies betweenassessments could well be attributed to the different timesof day rather than to genuine differences in abundance.This is because natural enemies are more visible, or searchfor prey or hosts at specific times of day or night. Forexample, larvae of many species of hover fly and ladybirdbeetle are particularly active at night so assessments madein the middle of the day will tend to vastly underestimatenumbers. Natural enemies are also affected by other factorssuch as weather conditions, temperatures and condition ofthe plants. Adult parasitoids, for instance, are generally mostactive on mornings and afternoons and may be deterred byhigh midday temperatures or strong winds. Generally,assessments of most natural enemies are often bestundertaken under calm conditions in the early morning orlate afternoon. If the intention is to assess relative numbersover time, it is important to aim to carry out assessments atthe same time of each day.

c) Effects of crop growth stage. As a crop grows and matures,it can become progressively more difficult to locate naturalenemies both because the surface area of the plant becomesmuch larger, but also because there is a greater possibilityof natural enemies being hidden in plant parts of olderrather than younger plants.

d) Bias from assessors. There can be substantial variation inthe accuracy of data collected by different individuals. Thismeans that, as far as possible, the same individual or groupof individuals with known identification skills and trackrecords for accurate assessments, should be selected foreach of a series of assessments on a given crop. Alsodifferent techniques are required for different organisms; forexample, visual counts may be useful for parasitoid cocoons

or aphid ‘mummies’, while pitfall trapping is commonlyused for ground-dwelling predators.

e) Concealed life stages. Some life stages of natural enemies,notably parasitoids and pathogens, can be concealed withinthe bodies of their hosts that show no outward sign ofattack until the later stages of parasitism or infection. Forexample, aphids or caterpillars which are attacked byendoparasitoids (p. 68), do not show any obvious evidenceof parasitism until the parasitoids reach the pupal stage. Inthe case of parasitised aphids, there are no outward signsuntil each aphid becomes mummified, while withcaterpillars, no evidence of attack is revealed until parasitoidlarvae emerge from or consume their hosts just prior topupation.

f) Variable durations of exposure to natural enemies.A method commonly used for assessment of parasitism is by collecting potential hosts from the field and then rearingthrough in the laboratory or other controlled environment.With such methods, it is critical that the hosts that areremoved from the field (and therefore from exposure toparasitoids) have had the same period of susceptibility toparasitoids. For example, diamondback moth caterpillars areparticularly susceptible to endoparasitism in their secondand third instars and are rarely parasitised in the first orfinal (fourth) instar. Therefore, if caterpillars are collectedfrom the field these must not be of mixed ages (instars),otherwise there will be variations in the amount of timethat each will have been susceptible to parasitism.Accordingly, it is more appropriate to collect only fourthinstar caterpillars and determine the proportion of thesethat are killed by parasitoids when reared through in thelaboratory. This type of assessment is normally carried outat regular intervals (e.g., two-weekly) throughout thecropping cycle. This principle applies to all hosts andparasitoids. In addition, care must be taken to not include

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remnants of previous life stages in assessments. Forexample, when assessing numbers of hover fly or lacewingeggs laid on a crop over time, hatched eggs should not beincluded in the assessments, or, when evaluating aphidparasitism by periodic assessments of mummified aphidscompared with un-mummified aphids, mummified aphidsfrom which wasps have already emerged should also beexcluded from counts.

Counts of arthropod natural enemies alone, even when theabove factors have been taken into account, do not provide anindication of the relative effectiveness of a range of naturalenemies. This is because of the very great variations in lifecycle parameters between different natural enemies species,and within species at different times and places. One of themost important parameters is voracity (the number of hosts orprey consumed by the natural enemy), this being demonstratedby a generalised example given below.

The importance of voracity: a generalised example

An aphid pest, Species X, is preyed on by two key species ofnatural enemy, these being designated as A and B. Species A is aparasitoid wasp, while Species B is a hover fly predator. Each adult,fertilised female wasp of A can lay up to 50 viable eggs during itsadult lifespan, each being laid within an individual host aphid. Thismeans that each female has a ‘killing potential’ of 50 aphids.

Species B on the other hand, although having the same lifespan(about 30 days), lays twice the number of eggs compared withSpecies A (i.e., 100) on leaves close to the colonies of Species X. Thehatch rate from these eggs is 75%, and each of these larvae has thecapacity to consume 400 aphids during its average 12-day larvalperiod. The ‘killing potential’ of one fertilised female of Species B istherefore 30,000 (75 x 400), which is 600 times greater than that ofSpecies A.

There are many other factors that can be important inassessments of natural enemy effectiveness. Some of these aredifficult to measure in the field and have been poorly studied,but this does not necessarily detract from their importance inbiological control. Many of the most important life cycleparameters (which must be determined both for the naturalenemy and its hosts or prey) are listed in Table 2.

Table 2. Important life cycle parameters in relation to naturalenemies

Finally, and certainly not least, the size of the area (scale) over which natural enemies are evaluated will have a veryimportant bearing on the results. There are many reasons forthis, one being that natural enemies are often highly mobile socan readily move in or out of the study area. If a small area issprayed with a broad spectrum pesticide and is then evaluated,the natural enemies may appear relatively unharmed becausespecies that are killed are likely to be replaced relatively quicklyby those that immigrate from nearby untreated areas. As aresult, ‘recovery’ of natural enemy populations will tend to be considerably more rapid than when relatively large areas are sprayed.

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EGG OR PREY (PEST) PARAMETERS NATURAL ENEMY PARAMETERS

Immigration rate Immigration rate

Emigration rate Emigration rate

Fecundity Voracity (consumption rate)

Development time Development time

Juvenile mortality Fecundity

Adult mortality Egg mortality

Juvenile mortality

Adult mortality

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.23.2 Side Effects of Pesticides3.1 Natural Enemy Evaluation

ConclusionsThere are a large number of factors that relate to the biologyof natural enemies and their hosts or prey, as well as to theinfluence of climate, prevailing weather and other specificenvironmental factors, which need to be considered beforeappropriate methods of evaluation can be developed andimplemented. The range of methodologies that have been usedfor given crop-pest-natural enemy combinations is beyond thescope of this section. However, it is hoped that some of theprinciples given here might be helpful at the farm-level so thatsome information on the relative value of natural enemies canbe obtained or inferred.

It is anticipated that in the future, some practical methods,presently under development, will provide the basis for farmer-participatory evaluation of the effectiveness of keynatural enemies.

In the meantime, taking into account some of the potentialpitfalls as considered above, recognising which natural enemytypes are present and evaluating their relative numbers atseveral points during the cropping cycle should provide usefulinformation on the relative abundance of each natural enemyover time. Different management practices will tend to havedifferent impacts on natural enemies, and the nature of theseimpacts, particularly whether they are positive or negative, canbe assessed in general terms in this way. As with anyexperimental technique, it is essential that appropriate‘controls’ are included in these studies. These control areasshould be comparable to the ‘treatment’ areas in every wayexcept that they do not include the specific ‘treatment’ ormanipulation under investigation.

Lethal and sublethal effects of pesticidesIt is often thought that a pesticide that does not kill a naturalenemy must then be harmless to the natural enemy. This is notnecessarily true. By analogy to a human example, a productsurely could not be described as harmless, if when swallowedaccidentally it then makes a person ill and prevents them fromworking. Such a product is most certainly harmful, but itseffect does not lead directly to death. These effects are referredto as being sublethal, and they are common with pesticideexposure of natural enemies as well as other animals, includinghumans. It is therefore important to appreciate the differencesbetween lethal and sublethal effects, between direct andindirect effects and understand something about the possibleroutes of exposure.

Pesticides may kill or harm natural enemies following exposureby contact, ingestion or, less commonly by respiration. They mayalso affect natural enemies indirectly by killing or contaminatingtheir hosts or prey. Natural enemies are usually more susceptibleto the effects of pesticides than their plant-feeding hosts orprey owing to their generally smaller size, searching habits,usually less-developed enzyme-based detoxification systemsand preening behaviour (notably in parasitoids). Although theeffects of pesticides on natural enemies are often negative,pesticides can sometimes enhance natural enemy function (seeFigure 2) particularly if they are selective against the pests orare used at low dosages.

For a given population of natural enemies exposed to apesticide over a range of doses, some natural enemies willgenerally die within a relatively short period (e.g., 48 hours)while others may survive beyond that period. Sublethal effectsare those effects that occur in the pesticide-exposed survivors.The behavioural or physiological nature of sublethal effects onnatural enemies tends to be fundamentally similar, althoughless severe, compared with that of lethal effects.

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In field studies that attempt to assess pesticide impact onnatural enemies (at the population or community level), it isoften not possible to separate lethal from sublethal effects, oreven indirect from direct effects. As such, pesticides may giverise to a continuum of effects that affect natural enemypopulations positively or negatively or sometimes apparentlynot at all (Figure 2). Factors such as the inherent toxicity ofthe pesticide to a given natural enemy, the pesticide’spersistence in the environment and the natural enemy’sexposure will influence the severity of the effect.

Figure 2. Continuum of possible pesticide effects on naturalenemies

As mentioned above, sublethal effects may be generally sub-divided into two groups: behavioural and physiologicaleffects (Table 3). Such effects may be measured in thelaboratory but because a wide range of experimental protocolsare used by different researchers, comparisons between speciesare often difficult. Where sublethal effects occur in the field,they will give rise to effects on natural enemy populationswhich will in turn affect the capacity of natural enemies tolimit the abundance of hosts or prey (i.e., pests).

Table 3. Spectrum of sublethal effects on natural enemies caused bypesticides1

It should also be borne in mind that biological control agents,such as entomopathogenic fungi used to target pestpopulations, have the potential to cause negative side effectson other biological control agents.

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BEHAVIOURAL EFFECTS PHYSIOLOGICAL EFFECTS

Communication Development time

Locomotion Voracity/Consumption/Parasitism

Consumption Deformation

Repellency Longevity

Foraging/Parasitism Vigour

Reproduction

• fecundity

• fertility

• searching

• oviposition

• handling time

1 Adapted from: Wright, D.J. & Verkerk, R.H.J. (1995) Review - Integration ofchemical and biological control systems for arthropods: evaluation in amultitrophic context. Pesticide Science, 44: 207-218.

ZEROEFFECT

100%MORTALITY

Positive Effects

Lethal Effects

Negative Effects

Sublethal Effects

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Pesticide exposureInsects and other natural enemies can either be exposeddirectly, with the natural enemy coming into contact withdroplets or particles of the pesticide, or they can be exposedindirectly (Figure 3). In the case of indirect exposure, thepesticide is either accumulated from residual deposits, forexample on leaves, or it is consumed via treated hosts or prey.Another form of indirect effect results from impacts that apesticide might have on pest (prey or host) populations. Ifthese populations are depleted or eliminated by pesticideapplication, the change in the amount of food available fornatural enemies can have profound effects on predators andparasitoids (Figure 3).

Figure 3. Important types of natural enemy exposure to pesticides

Finally, it is important to bear in mind that the impact ofpesticides on pest and natural enemy populations within agro-ecological communities may have long-term consequences andmay occur on large spatial scales. This means that pesticideimpacts may not be detectable on individual farms sampledonly occasionally.

RiskWhen evaluating the impact of pesticides, we need to considerthe risk of using a pesticide under the particular range ofconditions under which it is used. These conditions, whichinclude both living and non-living elements, are likely to varyconsiderably with both time and scale. For example, applicationof a broad-spectrum (non-selective) insecticide during a timewhen the adult stage of an important parasitoid species isabundant may result in resurgence of pest populations causedby suppression of the natural enemy. On the other hand,although the pesticide may have localised impacts on naturalenemies, if it is sprayed selectively (e.g., spot or barrierapplication), the negative impact of the spray on the naturalenemy might be relatively unimportant on a larger scale.

In its simplest form, risk should be seen as a function of bothexposure and susceptibility of the target organism. Looked atfrom the point of view of the natural enemy, hazard isbasically a function of its exposure to the pesticide and thepesticide’s toxicity to the natural enemy in question. Theserelationships are shown by the following two simple formulae:

Risk = f (exposure + susceptibility)

Hazard = f (exposure + toxicity)

However, there are often substantial differences between short-term and long-term risks. Short-term risks include theamount that a natural enemy population is depleted after theapplication of a pesticide, but following this depletion therewill be a recovery phase. Recovery will depend on such factorsas the persistence of the pesticide in the environment and therate of immigration of the natural enemy. As a result, theranking of risk for a given pesticide application in a particular

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Natural enemy exposure Direct (topical)

Natural enemy exposure Indirect DietaryResidual

Host exposure Indirect(Population/community effects)

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agro-ecosystem will often be different when comparing theshort-term and long-term impacts.

There are very few data generally available on short- or long-term risks, and most farmers or pest managers are usuallyforced to use one or more of a limited range of products thatare available to them commercially. This section of the fieldguide aims to help extension staff and trainers decide whichpesticides might be less hazardous to natural enemies. Thedata on which this information are based is taken largely fromlaboratory experiments, not field studies.

The advantage of standardised laboratory experiments, as usedby the International Organisation of Biological Control (IOBC)(see pp. 98-99), is that they allow the relative toxicity ofspecific pesticides to be tested under standardised conditionsagainst a range of organisms from the most important naturalenemy groups. The pesticides are used at the maximumrecommended field rates under conditions where exposure isconsiderably greater than those usually encountered in thefield. Data from any table of pesticide side effects on naturalenemies, such as the one given in this guide (pp. 98-99) orthose produced by some pesticide manufacturers (e.g., p. 100),should therefore be interpreted with caution. It should beappreciated that these data reflect effects following muchhigher exposure rates than those normally encountered in thefield, and they give no indication of possible long-term orlarge-scale risks. However, if properly conducted tests (such asthose following the IOBC protocols) show a product to be‘harmless’ to a range of natural enemies under these laboratoryconditions, the likelihood is that the product will also be‘harmless’ to the same natural enemies under field conditions.

Introducing the Table of Pesticide Side Effectson Natural EnemiesThe table overleaf aims to provide some information on therelative toxicity to a range of natural enemies of somecommonly used insecticides and fungicides. The table alsoincludes a few newerhproducts that are known to be relativelyharmless to many species of natural enemies. The tableincludes all the main pesticides found to be used in Zimbabweor Kenya during surveys carried out for the present work.

The data aim to demonstrate both the variability of response topesticides by a range of key natural enemies as well as showingdifferences between the pesticides. Although the data provideuseful information on relative toxicity of different pesticides tospecific natural enemies, as discussed above, they do notprovide data on risk or hazard of these pesticides in use. Thistype of information is generally much harder to come by and isnot available for many pest/natural enemy/crop situations.Where data are available they are contained in scientificjournals. An attempt to collate this published work has beenmade by workers at Oregon State University in the USA, in theform of the SELCTV database (see SELCTV Database, p. 100).

Products that have different intrinsic toxicities to pestscompared with natural enemies are referred to as selectiveproducts (e.g., Bacillus thuringiensis [Bt] based products).However, even products that are classified as ‘harmless’ are veryrarely harmless to all non-target organisms. All pesticidesshould be used judiciously (see Conservation under eachnatural enemy group in Part 2), as over-use can lead to otherunforeseen problems including insecticide resistance (see p. 14).

Apart from the intrinsic selectivity of a given product, someadditional selectivity can be achieved by selective and judiciouspesticide application (Part 3.3).

96 97

Trichogrammacacoeciae

Encarsiaformosa

Leptomastixdactylopii

Phytoseiuluspersimilis

Chiracanthiummildei

Chrysoperlacarnea

Syrphusvitripennis

Pterostichusmelanarius

Aleocharabilineata

Anthocorisnemoralis

Verticiliumlecanii

EggParasitoid

Act

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(Piri

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Am

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Ba

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ParasitoidWasps

LarvalParasitoid

LarvalParasitoid

MitePredators

INSECTICIDES ANDACARACIDES

Spider

Lacewing

Hoverfly

Groundbeetle

Rovebeetle

Pirate bug

FungiPathogens

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FUNGICIDES

Harmful (adverse effects* in 99% tested).

*In most cases the tests only measure mortality (death rate).

Estimations made from data available in SELCTV database

Moderately harmful (adverse effects* in 80-99% tested).

Slightly harmful (adverse effects* in 50-79% tested).

No test results available

Harmless (adverse effects* in less than 50% tested).

?

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.23.2 Side Effects of Pesticides3.2 Side Effects of Pesticides98 99

These data are based on laboratory tests carried out according to International Organisation for BiologicalControl (IOBC) protocols between 1983 and 1998. Laboratory testing exposes the test organism to higherlevels of pesticide than would normally be experienced in the field. The tests consider the impact of eachpesticide on mortality (death rate) and sometimes include a range of sublethal effects such as effects onegg production. The effects of mixtures of pesticides are not tested. The IOBC supports a sequential testingsystem that includes up to three basic levels of testing: laboratory, semi-field and field. The basicassumption made is that since exposure is highest in the laboratory and least in the field, if a pesticide isshown to be ‘harmless’ in the laboratory, it is likely to be harmless in the field. If it is shown to be ‘slightlyharmful’, ‘moderately harmful’ or ‘harmful’ following one test, further testing is required, at the nextsuccessive level of exposure (i.e., extended laboratory test, semi-field test or field test).

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Koppert Side Effects DatabaseKoppert is one of the leading companies involved in theproduction of biological control agents and pollinators.Koppert’s headquarters and principal research base is in theNetherlands, but the company also has offices in England,France, Italy, Spain, the USA, Canada, Mexico, Turkey and NewZealand. It has developed a very useful Side Effects Databasewhich is accessible on the Internet at the following website:

http://www.koppert.nl/english/service/index.html

You can access the database free of charge, but you need togo through a simple registration process the first time you useit. The database allows you to select from a wide range ofinsecticides, acaricides and fungicides and compare theirtoxicity and persistence against a range of important naturalenemies (and bumblebees). Data are provided for immature aswell as adult insects and include estimates of the persistence ofeach product. The information is based on the results of theIOBC Working Group ‘Pesticides and Beneficial Organisms’,other published research, as well as Koppert’s own research andexperience. More than one hundred scientific publications wereincluded in the comparative literature study.

SELCTV DatabaseAlso requiring access to the Internet is a comprehensivedatabase dealing with side effects of pesticides on arthropodnatural enemies. Access is again free. It is known as theSELCTV (pronounced selective) database and it is based onpublished literature, including the results of many fieldexperiments. The website for the database is:

http://www.ent3.orst.edu/Phosure/database/selctv/selctv.htm

Development of the database began in 1986/87 in theDepartment of Entomology at Oregon State University, Corvallis (Oregon, USA.). The database represents a relativelycomprehensive compilation of the literature publishedworldwide, from approximately 12,500 data records describingpesticide effects on non-target arthropods. Records date from1921 to 1994, although at the time of writing the majority ofthe records originate from the pre-1986 literature. It is thusparticularly useful for older pesticides, many of which are stillwidely used. Each record in the output table represents theeffects of a pesticide on one natural enemy taxon underconditions described in the source publication.

An ‘average toxicity rating’ system is used (1 = no effect, 2 = <10% response, 3 = 10-30% response, 4 = 30-90%response, 5 = >90% response). Links are provided to thepublished sources for the data. The database allows you toinsert the pesticide, crop, country and other criteria of yourchoice before a search is run.

The database developers aim to create a self-funding,continuously updated, unbiased, international resource usefulfor both research and decision-making in pest management.For more information contact: Dr Phil Heneghan Departmentof Entomology, Oregon State University, 2046 Cordley Hall,Corvallis, Oregon 97331-2907, U.S.A; email:[email protected].

Note on Use of Botanical PesticidesAbout 20 pesticides extracted from plants are used widely bysome smallholder or organic growers in different parts ofZimbabwe. Some of these products are derived from plantsindigenous to the region (e.g., Schwartzia madagascariensis,snake beans), while others are from exotic plants now growing

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.33.3 Selective Application3.2 Side Effects of Pesticides

in Zimbabwe (e.g., tobacco) or from imported plant parts orextracts (e.g., many pyrethrum products).

Although there is some evidence that some botanical productsmight be quite selective against pests and relatively harmless tonatural enemies, the data on which these conclusions are basedare on the whole very limited. This is because, as yet, botanicalpesticides, which are often extracted from botanical productson-farm, have not been scrutinised by registration authoritiesor researchers in the same way as synthetically-producedpesticides. From the available data, we do know that somebotanical pesticides (e.g., nicotine extracted from tobaccoleaves) may be much more broadly toxic, to humans and othermammals as well as to arthropods, than many syntheticpesticides.

Until reliable data are available on the side effects of botanicalpesticides against both mammals and other non-targetorganisms, including natural enemies, these pesticides shouldbe treated as being of unknown hazard. Unless, there is a goodbody of evidence demonstrating the harmlessness of specificbotanical pesticides to natural enemies and other non-targetorganisms, their use should be avoided.

Selective pesticide application Apart from selecting pesticides that are likely to be lessharmful to natural enemies (Part 3.1) and other non-targetorganisms such as pollinators, further selectivity can be gainedby judicious pesticide application.

There are five important aspects of pesticide application thatcan be manipulated to help reduce non-target effects. Furtherinformation on this subject can be found in a companionmanual entitled ‘Integrated Vegetable Pest Management inZimbabwe’ (authored by Hans Dobson, Jerry Cooper, WalterManyangarirwa, Joshua Karuma and Wilfred Chiimba).

■ Target the spray carefully on to the pestIf the pest (in any of its life stages) cannot be exposed to therequired dose of an insecticide, for example because the pest isconcealed within stems or fruits or hidden within curled leaves,application may be ineffective, wasteful and may simplydisrupt natural enemies that may otherwise be able to ‘searchout’ prey. Many pests are present on the underside of leaves, sospraying the upper surface of leaves may result in insufficientexposure of the pest, or to be effective, may require use ofexcessive doses. In addition, such treatments will be harmful tonatural enemies, which often search all parts of plants. Carefultargeting of spray requires a thorough knowledge of the habitsof the pest, an experienced applicator, a good quality,calibrated sprayer, and appropriate nozzles.

■ Minimise the volume application rateBy careful targeting and use of good quality, calibratedsprayers and nozzles, volumes of pesticides used can beminimised. For control of most vegetable pests and diseases insmallholder, tropical vegetable systems, operators should ideallyapply water-based sprays at rates between 200 and 400 l/ha(even less for small or young crops), in the range known as

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.33.3 Selective Application3.3 Selective Application

Medium Volume spraying. In contrast, many sprayingoperations actually use High Volumes of over 1000 l/ha. This iswasteful and may cause greater exposure of natural enemiesthan lower volume applications - the excess liquid drips fromplants and adversely affects a wide range of natural enemiesthat are ground-dwelling or have a soil-based life stage. Also,since tank concentrations are usually calculated on theassumption of lower volume application rates, High Volumespraying means the operator is often applying many times therequired dose of the pesticide itself. The droplet size of thespray is very important for efficient application and needs tobe varied according to the type of application. A significantproportion of very fine droplets (less than 100 µm [microns] indiameter) in a spray may lead to pesticide drift which iswasteful, prevents much of the pesticide being deposited onthe target and can lead to undesirable impacts on naturalenemies and other non-target organisms. The most efficientcoverage for most applications targeting vegetable pests onfoliage involves deposition of small discrete droplets and doesnot involve spraying to the point of run-off. For manysituations, 5 -15 small droplets of around 100 - 300 µm indiameter of an appropriate formulation on each squarecentimetre of infested foliage provides reliable control.Knapsack sprayers fitted with a small hollow cone nozzle arecapable of achieving this, but it is difficult to achieve with flatfan and other types of nozzle. Although the sprayer may becalibrated to apply a rate of between 200 and 400 l/ha, theactual volume application rate per hectare of crop can bereduced considerably by selective spraying techniques. Thesetechniques include spot spraying (i.e., targeting areas ofsubstantial pest infestation only) or strip spraying (i.e.,applying bands of treatment through a crop, the width of the sprayed and untreated bands being dependent on factorssuch as the severity of the infestation and prevalence ofnatural enemies).

■ Timing of pesticide application

If it is decided that spraying must occur, make sure it is carriedout at a time of the day or even season when there is thelowest chance of adversely affecting natural enemies. Somenatural enemies like hover fly and ladybird beetle larvae aremost active at night, so spraying at dawn might expose moreto the pesticide. Other natural enemies, such as parasitoids, aremore likely to be searching plants during the daytime,sometimes avoiding the hottest times of day. However, otherfactors must also be taken into account. Conditions must beselected to avoid the risk of pesticide drift caused by very smalldroplets being carried by wind, or scorching of foliage byintense sunshine that can occur by magnification of thesunlight through pesticide/water droplets. Optimum weatherconditions for spraying are usually most likely to occur in theearly morning or late afternoon.

■ Minimise the pesticide concentration

Use the minimum concentration recommended on the productlabel (or less, if it still gives adequate control). Not all pesticideskill pests quickly so a slow result does not mean a poor result.In some cases, using a low concentration may give a betterlong-term result because it will suppress the pest numberswithout killing the natural enemies – the natural enemies canthen control most of the remaining pests. By spraying at theright time for example against more susceptible immaturestages of a pest (e.g., small, early instars of a caterpillar pest),it is often possible to use a low dosage. Once the pests havegrown to a larger size (e.g., large, late instar caterpillars), theyare often much more difficult to kill as their tolerance to manypesticides increases. This tolerance is usually caused by thepresence of enzyme-based detoxification systems within thepest that have evolved to cope with secondary plant products,which make most plants toxic to most plant-eating arthropods.

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Con

tact

sContacts3.3 Selective Application

■ Reduce the frequency of application

Apply pesticides as infrequently as possible, and only whenthere is clear evidence that natural enemies are providinginadequate levels of control. This might involve the need foronly a single application that either reduces the numbers ofpests or slows their rate of development. Combined withappropriate conservation practices, natural enemies should thenbe able to provide sustainable control of pests.

106 107

■ Plant Protection ResearchInstitute

PPRIDepartment of Research &Specialist ServicesPO Box CY550CausewayHarare

Contact:Dr Simon SitholeTel: 04-704531 / 706650 /704531 / 737193Email: [email protected]

■ AGRITEX

AGRITEXPO Box 639Harare

Contact:Marcus Hakutengwi (ChiefTraining Officer, AGRITEX)Tel: 04-707311Email: [email protected]

■ African Farmers’ OrganicResearch and Training

AfFOResTPO Box CY301CausewayHarare

Contacts:Shepherd Musiyandaka,Fortunate Nyakanda or Dr Sam PageTel: 04-336310Email: [email protected]

■ Participatory Ecological Land Use ManagementAssociation

PELUM AssociationPO Box MP1059Mt PleasantHarare

Contact:Mutizwa MukuteTel: 04-744509 / 744470 /744117 Email: [email protected]

ZIMBABWE

■ Imperial College of Science,Technology & Medicine(University of London)

Department of BiologyImperial CollegeSilwood ParkAscotBerkshire SL5 7PY, UK

Contacts: Dr Robert Verkerk or Dr Denis WrightEmails: [email protected]

[email protected]

■ CABI Bioscience, UK Centre

CABI BioscienceUK Centre (Egham)Bakeham LaneEghamSurrey TW20 9TY, UK

Contact:Tony Little (IPM Information Officer)Email: [email protected]

■ Natural Resources Institute

Natural Resources InstituteUniversity of GreenwichCentral AvenueChatham MaritimeChathamKent ME4 4TB, UK

(Natural Resources Institute contd.)

Contacts:Hans Dobson or Jerry CooperEmail: [email protected]

[email protected]

■ Natural ResourcesInternational

Natural Resources InternationalPembrokeChatham MaritimeChathamKent ME4 4NN, UK

Contact:Crop Protection ProgrammeManagerEmail: [email protected]

■ Global IPM Facility

Global IPM Facility SecretariatFood & Agricultural Organisationof the United NationsViale delle Terme di Caracalla00100 Rome, Italy

Contact:Coordinator or IPM SpecialistEmail: [email protected]

■ Kenya Agricultural ResearchInstitute / NationalAgricultural ResearchLaboratories

KARI/NARLPO Box 14733Nairobi

Contact:Gilbert KibataEmail: [email protected]

■ CABI Africa Regional Centre

CABI-ARCPO Box 633 Village MarketNairobi

Contacts: Dr George Oduor or Dr Sarah SimonsEmails: [email protected]

[email protected] [email protected]

■ International Centre forInsect Physiology andEcology

ICIPEPO Box 30772Nairobi

Contact:Director-GeneralE-mail: [email protected]

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KENYA UNITED KINGDOM / EUROPE

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dixSpecies List 2: ParasitoidsSpecies List 1: Predators

The following genera and species of predators (List 1) and parasitoids (List 2) havebeen identified, mainly between 1998 and 2000, on vegetable crops in Zimbabweand Kenya. This is by no means on exhaustive list but it does contain some of themost common natural enemies likely to be encountered.

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Order Family Genus/species

Coleoptera Coccinellidae Hippodamia variegata

Cheilomenes spp., including C. lunata,C. propinqua and C. sulphureaExochomus spp., including E. troberti and E. ventralis

Carabidae Calosoma spp.Chlaenius sp.Passlidius fortipesHarpalus agilisMicrolestes sp.Stenethmus sp.

Staphylinidae Philonthus sp.Oligata (Holobus) sp.

Anthicidae Anthicus biplagiatusFormicomus rubricollis

Nitidulidae Cybocephalus sp.

Hemiptera Anthocoridae Orius spp.Reduviidae Harpactor sp.

Neuroptera Chrysopidae Chrysoperla spp.

Diptera Syrphidae Metasyrphus corollaeSyritta flaviventrisIschiodon aegyptiusBetasyrphus adligatusMelanostoma annulipesAllobaccha sapphirinaParagus sp.

Mantodea Mantidae Sphodromantis spp.

Hymenoptera Vespidae Polistes sp.Sphecidae Sphex sp.

Acari Phytoseiidae Amblyseius spp., including A. teke and A. tutsiPhytoseiulus spp.Typhlodromus spp.

Arachnida Lycosidae Pardosa spp.Linyphiidae Microlinyphia spp.Oxyopidae Peucetia spp.

Order Family Genus/species

Hymenoptera Braconidae Meteorus sp.Apanteles sp.Cotesia spp., including C. ruficrus and C. plutellaeGlyptapanteles maculitarsisMicrochelonus curvimaculatus

Braconidae: Diaeretiella rapaeAphidiinae Aphidius spp., including A. colemani

Ichneumonidae Diadegma sp.Charops sp.Diplazon laetorius

Eulophidae Diglyphus spp., including D. isaeaMeruana liriomyzaeNeochrysocharis sp.Oomyzus sokolowskii

Scelionidae Telenomus sp.Chalcididae Brachymeria sp.Encyrtidae Syrphophagus africanus

Diptera Tachinidae Gonia bimaculataNemoraea rubellanaPalexorista spp., including P. laxaPeriscepsia carbonariaNemorilla sp.

Bombyliidae Bombylius sp.Calliphoridae Isomyia dubiosa

Note

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