This field guide, also Farmers’ Friends produced as Shona and Farmers’ Ndebele language versions, aims to help extension Friends workers and agricultural trainers to recognise the most important groups of natural enemies of arthropod pests Recognition and conservation of of vegetables (‘farmers’ friends’). natural enemies of vegetable pests in Zimbabwe It also provides information

about the conservation and Recognition and Conservation augmentation of these groups, from a variety of cultural practices to the selective use of pesticides. Multi-lingual posters intended Collaborating Organisations for farmers have been Imperial College of Science, produced to compliment Technology & Medicine, UK the field guides. Plant Protection Research Institute, Zimbabwe African Farmers for Research & Training, Zimbabwe Natural Resources Institute, UK Kenya Agricultural Research Institute, Kenya A field guide for extension workers and trainers CABI Bioscience, Africa Regional Centre and UK Centre Participatory Ecological Land Use Management Association, Zimbabwe University of Zimbabwe

A collaborative project ISBN: 0-9540132-0-4 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 2 3

AUTHOR AND PRINCIPAL EDITOR For further information, contact: Robert Verkerk Zimbabwe Imperial College of Science Technology & Medicine, Dr S.Z Sithole, Plant Protection Research Institute, Department University of London, UK of Research and Specialist Services, PO Box CY550, Causeway, Harare, Zimbabwe. PROJECT TEAM AND ASSOCIATE EDITORS Email: [email protected] Simon Sithole, Joshua Karuma, Wilfred Chiimba, Tumelani Shepherd Musiyandaka, AfFOResT (African Farmers’ Organic Wesile, Walter Manyangarirwa, Tafadzwa Sibanda: Research & Training), PO Box CY301, Causeway, Harare, Zimbabwe. Plant Protection Research Institute, Department of Research & CountriesEmail: other [email protected] than Zimbabwe Specialist Services, Zimbabwe Dr R.H.J. Verkerk, Department of Biology, Imperial College, Shepherd Musiyandaka, Fortunate Nyakanda, Rexon Hodzi, Silwood Park, Ascot, Berkshire SL5 7PY, United Kingdom. Email: [email protected] Todd Ndlovu, Sam Page: African Farmers’ Organic Research and Training (AfFOResT), Zimbabwe Hans Dobson: Natural Resources Institute, University of Greenwich, UK Gilbert Kibata, Jason Ong'aro, Samson Pete: National This publication is an output from a research project funded by the Agricultural Research Laboratories, Kenya Agricultural Research Department for International Development of the United Kingdom (DFID project code R7587, Crop Protection Programme). However, Institute, Kenya the Department for International Development can accept no George Oduor, Peter Karanja, Sarah Simons, Martin Kimani: responsibility for any information provided or views expressed. CABI Bioscience, Africa Regional Centre, Kenya For information about the DFID Crop Protection Programme, visit www.nrinternational.co.uk (see also Natural Resources International, Peter Jowah: University of Zimbabwe (formerly IPPM Working Contacts, p. 109). Group, Zimbabwe) Shona and Ndebele language versions of this guide and posters Tony Little: CABI Bioscience, UK (Shona, Ndebele and English language versions) have also been produced as part of this project. Denis Wright: Imperial College of Science Technology & Medicine, University of London, UK Photographs by R.H.J. Verkerk unless otherwise stated.

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

Printing by Fontline, Harare. 4 Contents Contents 5

Page Page

Acknowledgments 6 Predatory mites 48 Predatory wasps 51 Foreword 7 Mantids 53 Spiders 55 Part 1. Introduction Other predators 58 Feeding levels in natural and agricultural systems 10 Parasitoids Some problems caused by intensive agriculture 12 Parasitoid wasps 64 What are natural controls? 15 Parasitoid flies 76 Types of natural enemy 16 Pathogens Biological control 18 Entomopathogenic fungi 78 Four steps for improving biological control of pests 18 Baculoviruses 79 Development and metamorphosis in insects and other arthropods 21 Bacteria 80 Entomopathogenic nematodes 81 Part 2. Important natural enemies of vegetable pests 25 Part 3. Evaluation of natural enemies, Predators and pesticide selectivity 83 Ladybird beetles 26 3.1 An introduction to natural enemy evaluation 84 Ground beetles 31 3.2 Pesticide side effects on natural enemies 91 Rove beetles 34 3.3 Selective pesticide application 104 Pirate bugs 37 Lacewings 39 Contacts 107 Hover flies 42 Appendix: Species lists 110 6 Acknowledgments Foreword 7

I are indebted to the vegetable farmers, trainers, extension personnel and scientists in Zimbabwe and Kenya whose input and enthusiastic cooperation made the Introducing this field guide compilation of this natural enemy field guide, associated posters and training programme possible. This field guide and its associated posters and ‘natural enemy In Zimbabwe, we would like to extend particular thanks to the staff from the Plant flip-cards’ (available in English, Shona and Ndebele languages) Protection Research Institute (Department of Research & Specialist Services) and the non-governmental organisation African Farmers’ Organic Research and Training are the result of collaboration between Imperial College (AfFOResT) for their dedication to the project and translation of the text to local (University of London), Plant Protection Research Institute languages (Shona and Ndebele). We are also grateful to AGRITEX, the IPPM Working Group (Food and Agricultural Organization of the United Nations), Peter (Department of Research & Specialist Services, Harare), African Wilkinson (Xylocopa Systems, Harare) and the PELUM Association (Harare) who Farmers’ Organic Research and Training (AfFOResT, Harare), provided valuable input during the production of the materials. National Agricultural Research Laboratories of the Kenya Part of the research and development for this guide and its associated project was carried out in Kenya (1998-1999), the work being made possible by the invaluable Agricultural Research Institute (NARL/KARI, Nairobi), CABI contributions of our colleagues from the Kenya Agricultural Research Institute Bioscience (Africa Regional Centre, Nairobi, and UK Centre) (KARI) and CABI Bioscience (Africa Regional Centre). and Natural Resources Institute (University of Greenwich, Dr Denis Wright (Imperial College, University of London) was responsible for the Chatham, UK). overall management of the project, and Hans Dobson (Natural Resources Institute, UK) provided essential support and input throughout. Thanks are also due to Tony Little (CABI Bioscience, UK Centre) who helped collate some of the data on side The purpose of the guide and its associated outputs is to help effects of pesticides on natural enemies (Part 3.2). Catherine Pinch (Imperial extension staff and farmers recognise and conserve important College, University of London) and Max Barclay (Natural History Museum, London) provided useful input to the section on carabid beetles. Tony Russell-Smith (Natural groups of natural enemies by raising awareness of the Resources Institute, UK) kindly identified the spiders shown in the guide. Further presence, abundance, diversity and benefits of natural enemies thanks are offered to Graham Matthews (Imperial College, University of London) and Hans Dobson for their useful suggestions on selective pesticide application in on smallholder farms in Zimbabwe. Nearly all of the Part 3. photographs within this guide were taken in the field during I would like to thank Andrew Jones and Mick Tomlinson from deepblue (London) surveys in Zimbabwe and Kenya in October 1998, and in for their work on the design and layout of the guide and associated posters. Zimbabwe in May and October 2000. 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, During the October 1998 field surveys in Zimbabwe and especially Ellie, Misha, Greta and Hannah, for all their support and encouragement throughout the course of this project. Kenya, interviews with small-scale farmers were also undertaken. The interviews showed generally that little Finally, I am grateful to the Department for International Development (DFID) of the United Kingdom (Crop Protection Programme) for providing financial support information on natural enemies was available at the and advice. farm-level. However, it was also clear that farmers were very Robert Verkerk, Ascot, January 2001 interested and enthusiastic about gaining more knowledge to help them recognise natural enemies and distinguish them from pests and other plant-feeding insects. Farmers were particularly keen to learn about conservation methods that could be used to encourage natural enemies on farms. Learning about ways of improving the effectiveness of natural enemies on small-scale, tropical, vegetable production systems is likely to become increasingly important to many farmers as 8 Foreword Introduction

the cost of inputs such as pesticides and fertilisers continues to increase. In addition, many farmers are becoming more concerned over the possible human health and environmental risks of pesticides. There is also a growing worldwide interest in ‘organic’ production where the use of synthetic pesticides (and fertilisers) is not permitted. The EnglishPart language 1 provides version a general of this background guide is divided to natural into enemiesthree Part 2, the main body of the parts.and biological control, while guide, considers in turn each of the major groups of natural 1Page enemies and important methods for their conservation. Part 3 is subdivided into three sub-sections, Part 3.1 being an introduction to the evaluation of natural enemy effectiveness, Feeding levels in natural and Part emphasising common pitfalls to frequently used methods. agricultural systems 10 3.2 contains information about the side effects of commonly used pesticides on natural enemies, and it includes a table and Some problems caused by intensive agriculture 12 cross references to websites aimed to help readers assess the What are natural controls? 15 relative hazards of different products to important natural Part 3.3, presents various approaches Types of natural enemy 16 enemies. The final part, to selective application of pesticides that can be used to Biological control 18 minimise harm to natural enemies. Four steps for improving biological The Shona and Ndebele versions are essentially similar to the control of pests 18 English language version, except for Part 3. In these versions, Development and metamorphosis Part 3.1 has been omitted, and the remaining two sub-parts in insects and other arthropods 21 are reduced slightly in scope and length. Introduction 10 In mostnatural systems, thenumbers ofanimals from these considered are considered below. intensive agricultural systems. Three importantreasons forthis resulting inpestoutbreaks. Outbreaks are mostcommon in feeding levels is upsetandpestnumbers increase rapidly natural ecosystems, thenatural balancesbetween thesefour Frequently inagricultural systems, andvery occasionally in prevent thedevelopment ofpestoutbreaks. allow establishment ofnatural enemiesthatinturnwillhelpto important tomakesure that there is afoodsource available to these plant-eatingorganisms (so-called pestspecies) is often a small amountofdamage tocrops. Thepresence ofsome this is also thecase,withplant-eating organisms causing only or lessintactmostofthe time. Instableagricultural systems trees, shrubs andgrasses inmostnatural systems remain more between theorganisms present. This is whytheleaves ofmost different groups are keptincheckby complicated interactions commonly referred toas while thoseanimals whichfeedonplant-eatinganimals are a commoditythatweashumans value, weoften callita type ofplant-eatinganimalconsumes toomuchof acrop or all stablenatural andagricultural habitats. Whenaparticular enemies. Thesefourfeedinglevels oflife(seeTable 1)exist in insects. Even carnivorous animals generally have natural of carnivorous animals from lions topredatory andparasitic while theplant-eatinganimals are consumed by awiderange for plant-eatinganimals suchasantelopesandmanyinsects, a widerange ofplantsandanimals. Theplantsprovide food Natural systems, suchasforests andsavannahs, support systems Feeding levelsinnaturalandagricultural farmers’ friends. Introduction natural enemies and should be pest , agricultural habitats Table 1: FEEDING LEVEL Four feedinglevelscommontonaturaland Plant Organism Type of animal Plant-eating animal parasitic Predatory or animal parasitic Predatory or ikHyperparasitoid Tick habitat a NATURAL Example from rse Tomato (crop) Grasses neoeCaterpillar(pest) Antelope inParasitic wasp Lion Introduction enemy) enemy ofnatural wasp (natural habitat an AGRICULTURAL Example 1from (natural enemy) habitat an AGRICULTURAL Example 2from Cabbage (crop) Aphid (pest) (natural enemy) Hover flylarva enemy) enemy ofnatural wasp (natural Parasitic 11

Introduction Introduction 12 below). high chancethat resistance totheinsecticide willdevelop (see regularly sprayed with insecticides (Picture 2),there is also a nectar andpollen from flowers). If they are heavilyand suitable refuges oradultfoodsources fornatural enemies(e.g., plentiful and closely spaced. Monocultures usually containfew found, thepestcandevelop very quicklyasitsfoodsource is This makesiteasierforpest species tofindthecrop andonce a type, this beingreferred toas tracts oflandtoasingle crop involves theplantingof large Intensive agriculture often (Picture 1). sometimes inthetropics shown tobreak down temperate regions hasbeen a given crop cultivar in resistance thatis expressed by pesticide inputs. The on highfertiliser and agriculture thatis dependent ‘designed’ forhighinput resistance topestsanddiseases andhave effectively been size, colourorwatercontent.Theyoftenhave little natural may have beenbred to enhanceparticularqualitiessuchas have originatedfrom Europe orothertemperate latitudes. They Many plantcultivars grown asfoodcrops in tropical countries agriculture Some problemscausedbyintensive monoculture Monocultures Poorly adaptedcropcultivars (Picture 2). Introduction grown inKenya susceptible toaphidpestswhen been showntobehighly European conditions,buthas to cabbageaphidunder F 1. 1 ) whichhaspartialresistance A cabbagevariety(Minicole with residues. and prey, searching for potentialhosts because they spend more time than pests. This is partly more sensitive topesticides Natural enemies are generally or sublethaleffects. enemies, andcancause lethal walking speed) ofnatural developmental period)orbehaviour(e.g.,hostlocation, Pesticides mayaffectthe physiology (e.g.,egg-layingrate, a) Deathorharmtonatural enemies mites orspiders. Allthesegroups are are eitherinsects orcloselyrelated groups such aspredatory insecticides oracaricides)are: indiscriminate use ofpesticides (particularlybroad-spectrum Some ofthegeneral problems thatmayarise from have jointedappendagesandexternalskeletons. physiologically sensitive, also smaller and more insecticides frequent sprayingwith miner flylarvaedespite showing seriousdamagebyleaf 2. A broadbeanmonoculture, so risking contact They are often Introduction sprayed crop after contacting arecently 3. insecticides andacaricides, enemies, likethetargets of because mostnatural natural enemies. This is that are themostharmfulto insecticides andacaricides in practice, itis the diseases andweeds. However, nematode pests, plant against insect, miteand pesticides thatcanbeused There is a large variety of Adult hover flydeadon leaf Use ofpesticides arthropods . Thatis, they 13

Introduction Introduction 14 of other beneficialor non-target organisms. (Picture 5).Pesticides mayharm pollinators andawide range inappropriate disposal ofpesticideconcentrate containers water supplies. Theymaycontaminate waterfollowingthe Pesticides may move ingroundwater andcontaminate drinking produce ifpre-harvest intervals are notfollowedcarefully. inhaled. Harmfullevels ofpesticidescanalso beconsumed on absorbed through theskin andtheeyes, anddroplets maybe common duringapplication. Mostpesticidesare readily Exposure ofoperators is very humans andtheenvironment c) Pesticides maybeharmfulto enemies. increases theharmtonatural resistance ortolerance, also which oftenaccompanies broad spectrum pesticides, frequency ofspraying with altered target site).Increased some way(e.g.,detoxification, sensitive tothepesticidein that allows themtobeless version ofagene(anallele) This is because thesurvivingpopulations contain aspecific pesticide, withlittleimpactonthepestpopulations (Picture 4). spray more andmore frequently, oftenwithincreasing dosesof Pesticide resistance b) Pests maydevelopresistanceortolerancetopesticides causing harmed orkilled(Picture 3),pestsmultiplymuchmore quickly, picked upontheirlegs andantennae.Ifnatural enemiesare themselves regularly soconsuming residues theymayhave and manyimportantgroups suchasparasitoid wasps preen pest resurgence or tolerance Introduction . often occurs whenfarmers pests. Whatisgoingon?” the cropisbeingdestroyedby week forthelastmonthand 4. “I’ve beensprayingoncea of difficult forpotentialplant-eaters tosettleandfeed. This sort attack, ortheymighthave hairs ontheirleaves thatmakeit (Picture 6),theymayproduce toxic secretions following poisonous tocertainorganisms make themdistasteful or may containchemicals that plant-eating organisms. They to resist damageby most mechanisms thatallowthem Plants possessawiderange of These are: (potential pests). plant-eating organisms of defenceforplantsagainst Nature provides twobasiclines CONTROLS? WHAT ARENATURAL be a plant-eatertodevelop successfullyontheplant)oritmay of natural enemies. interfere with theperformance as this resistance doesnot production systems, aslong helpful inlowinputcrop plant resistance plant). Adegree of offspring than onasusceptible more slowly orproduces fewer can develop, butitdoes so plant resistance Plant defences partial (where aplant-eater is oftenvery may be partial Introduction complete water supplies 5. Pesticides cancontaminate (making itimpossiblefor making mesick” tastes badandis 6. “This plant “This 15

Introduction Introduction 16 predatory mites;predatory wasps; spiders. Examples: ladybird beetles;ground beetles;mantids;dragonflies; only oneora fewspecies ( others are more specialised in their choiceofprey, feedingon predators feed onawiderange of species ( Immature and/oradultstages canbepredatory. Some Each predator generally kills several prey duringitslifetime. These are organisms thatprey onandfeedotherorganisms. three main groups: Natural enemiesofinsect andmitepestscanbedividedinto TYPES OFNATURAL ENEMY control, suchastheapplicationofpesticides. consideration is given tomore interventionist methodsofpest these natural controls workaswellpossiblebefore should bemadetoensure that a minimum,every effort crop lossesneedtobekept In agricultural situations where natural enemies(Picture 7). that are attractive tospecific releasing particularchemicals shown to‘cryforhelp’by attack by pestshave been organisms. Crop plantsunder the abundanceofplant-eating important means ofcontrolling Natural enemiesprovide avery enemies Predators Defence vianatural (see Part 2,pages26-63) Introduction specialists being attackedbycaterpillars 7. ). A plant generalists ‘ crying forhelp ), while ’ after other natural enemies(seeTable 1). themselves also susceptible toattackby other parasitoids (and of species astargets. Natural enemiesincludingparasitoids are specialists parasitoids are highlyorrelatively specific (that is, are many larvae (sometimeshundreds) developing per host.Most parasitoid developing perhost,ortheymaybe host. Manyspecies are regarded as The larvae mayfeedfrom withinoroutsidethe body oftheir substances suchasthenectarofflowers oraphid honeydew. agriculturally importantparasitoids species feedonsugary beetles andvery occasionallyothergroups. The adultsofmost all wasps orflies, but include arelatively small numberof approximately 85,000 species) are parasitoids. Theyare nearly About 8.5%ofinsect species describedto-date(i.e., their adultstagewithvery fewexceptions are free-living. stages feedonandeventually killasinglearthropod, andin Parasitoids are organisms thatduringtheirimmature (larval) (entomopathogenic nematodes) polyhedrosis virus); (entomopathogenic fungi);GV(granulosis virus);NPV(nuclear Examples: seasons. commonly where pestpopulations are large orduringrainy and microsporidia. Many pathogens tendtobefoundmore systems. Theyinclude fungi,bacteria,viruses, nematodeworms controlling thegrowth ofpestpopulations inagricultural Pathogens are disease organisms. Theycanbeimportantin Examples: parasitoidwasps andflies Parasitoids Pathogens Metarhizium ), selectingonlyasinglehostspecies ornarrow range (see Part 2,pages78-82) (see Part 2,pages64-77) Bacillus thuringiensis , Zoophthora Introduction , Entomophthora solitary (bacterium); EPNs with onlyone gregarious with 17

Introduction Introduction 18 Farmers canbe encouraged to setup ‘insect zoos’ where enemies andinturn share this information withfarmers. help trainers recognise the mostimportant groups ofnatural crop canbe recognised (Picture 8). This fieldguideaims to introduced. Itis critical thatpestsandnatural enemies ona present already orbecloseby and therefore donotneed tobe In mostcropping systems, natural enemieswilleither be the guide) STEP 1 generally required. be improved. Insimpleterms, fourimportantstepsare staff provide supporttofarmers sothatbiological control can This fieldguideis intended tohelpextension staffandfield OF PESTS FOUR STEPSFORIMPROVING BIOLOGICAL CONTROL control is called and multiplywithinthecrop. This approach to biological the functionofnatural enemiesthatimmigrate naturally into need tobedesignedandmanagedinsuchaway enhance parasitoids orpathogens. To beeffective, cropping systems achieved through theuse oflivingorganisms, namely predators, Biological control refers totheprocess ofpest management BIOLOGICAL CONTROL the crop atintervals ( be reared inlarge numbers inspecial facilitiesandreleased into augmentation introduced from otherareas ( is missing from acrop oraspecific region, thesecanbe a particularnatural enemyspecies orgroup of natural enemies for smallholder farmers inthetropics. Insome cases, where Find outwhichnatural enemiesarepresent ). Inothercases, particularnatural enemiescan conservation inundation Introduction introduction and ithasparticularrelevance ). , inoculation (see Part 2of or has occurred. parasitism tobeobserved ifit will also allowtheeffectsof who is eatingwhoorwhat.It will allowthefarmertosee complete development. This animals gothrough their maintained untilallthe portion ofthecrop andare other small containers witha together inventilated jars or and natural enemiesare kept groups ofsuspected pests on-farm trials betweendifferent cultivars. available foraspecific region, itmayeven beuseful torun retailers. Ifdataoncultivar tolerance orresistance are not farmers, relevant research institutes, extension stafforseed particular crops canoften beobtainedby talkingtoother (Picture 9).Information on therelative susceptibility of susceptible topests(and diseases), asdiscussed onp.12 It is importanttochoosecrop cultivars thatare nothighly STEP 2 two varieties than theother less bycaterpillars damaged much has been 9. Kale varietyA Select themostappropriatecropcultivars Introduction pest?” enemy ora 8. “Is itanatural 19

Introduction Introduction 20 many more pesticides available than those given in Part 3.2, risk ofsideeffects onnatural enemies. Obviously there are suggestions onways ofapplying pesticides thatminimise the harmful tonatural enemies(Picture 11). Part 3.3offers some products available inZimbabwethat are likely tobeless guide asastarting pointtohelpidentify thosepesticide The reader can use theinformation given inPart 3.2ofthe to naturalenemies STEP 4 my naturalenemies?” sources andrefugesfor provide adultfood flowering plantsto 10. in Part 2oftheguideundersubheading (Picture 10). Somerelevant techniquesandinformation are given help encourage natural enemiesandimprove theireffectiveness There are manythings thatcanbedoneonindividual farms to the guide) STEP 3 with aquaticlifestages. for importantpredators providing watersources live fences(trees, hedges)andshelters, using mulches, and or closetothecrop, mixed cropping orinterplanting,providing coriander, Indianmustard andotherfloweringbrassicas) within food sources suchasfloweringplants(e.g.,fennel,thistles, Important methodsofconservation includeproviding adult Ensure thatpestmanagement practicesarenotdisruptive Conserve naturalenemiesbyculturalmeans “Can Igrowsome (see Part 3oftheguide) Introduction Conservation (see Part 2of . pp. 101-102). botanical pesticides Note onuseof tested atall(see have notbeen botanical pesticides side effectsofmost enemies andthe against natural in arigorous way 2000. Bearinmindthatmanypesticideshave not beentested smallholder sectorduringsurveys conductedbetween1998and but thelist given includesallthemainpesticidesused by the (or incomplete) metamorphosis are referred toas varying mainlyin size.Immature insects thatundergo simple immature stagesappear similar inbasicform totheadults, These include thoseinsects (andother arthropods) whose types are: development is oftenreferred toasmetamorphosis. These types according totheway theydevelop. Theprocess of insects (seePart 2).Insects canbe broadly classifiedintotwo abundance are arthropods. Ofthese,thevast majorityare Most natural enemiesthat have amajorinfluenceonpest and otherarthropods Development and metamorphosisofinsects Simple metamorphosis , Introduction natural enemies?” 11. “Is thisspraygoingtokillmy nymphs . 21

Introduction Introduction 22 these insects are called moths orbutterflies. The earlierimmature stages(instars) of grubs, which turnintobeetles;andcaterpillars, whichturn into same species. Examples includemaggots, whichturninto flies; and have different habits, compared withtheadultsof pupae) appearvery different, oftenlive indifferent habitats This group includesinsects whoseimmature forms (larvae and undergo simplemetamorphosis. wing buds. Otherarthropods, suchasmitesandspiders, also form, thesedevelop externally, andmaybeseeninnymphs as complete metamorphosis. Ifwings are present intheadult regarded asbeingmore primitive thanthosethatgothrough no pupalstage.Insects thatundergo simplemetamorphosis are Adults arise followingthelastmoultofnymphs –there is undergo complete metamorphosis. adults of thesame species. All parasitoids andmany predators of change occurs as seenby the differences betweenlarvae and and doesnot feed,butduringthis stage, avery large amount pupation, from whichtheadultemerges. Thepupais inactive skin (moults) atintervals toallow growth, and thenundergoes a given species, thesedevelop internally. Eachlarva sheds its principle functionis feeding. Ifwings are present inadultsof Complete metamorphosis Examples: G YPS eea rwhsae isas ADULT NYMPHS, severalgrowthstages(instars) EGG Other arthropods Insects IMMATURE FORMS Introduction iaebgnmhPiratebug Spiderling ornymph Mite nymph Pirate bugnymph Mantid nymph larvae (singular = larva ) andtheir Spider Mite Mantid ADULT FORMS path towards thedevelopment ofcompletemetamorphosis. intermediate thrips andmalescaleinsects are sometimessaid toundergo simple orcompletemetamorphosis. Insects suchaswhiteflies, Not allinsects canreadily becategorised asundergoing either Examples: G AVE eea rwhsae isas PUPA LARVAE, severalgrowthstages(instars) EGG metamorphosis, astheyhave gonewelldownthe LARVAL FORMS Introduction pi-inLacewing Ladybird beetlelarva Wasp larva Aphid-lion Maggot Caterpillar Ladybird Wasp Fly Moth ADULT FORMS ADULT 23

Introduction 24 Important natural enemies of vegetable pests

Predators Page Ladybird beetles 26 Ground beetles 231 Rove beetles 34 Pirate bugs 37 Lacewings 39 Hover flies 42 Predatory mites 48 Predatory wasps 51 Mantids 53 Spiders 55 Other predators 58 Parasitoids Parasitoid wasps 64 Parasitoid flies 76 Pathogens Entomopathogenic fungi 78 Baculoviruses 79 Bacteria 80

Entomopathogenic nematodes 81 Predators 26 (Picture 14). other stages, oval-shaped andspiny (Picture 13). up toabout1cmbefore pupation colonies (Picture 12). colour, and laidingroups nearaphid Pupae: Larvae: Eggs: APPEARANCE Common names: Group: Crops: Main prey: Immatures: Type: Predator (larvaeandadults) Usually yellow toorange in Vegetables, particularlybrassicas,tomato,potato,beans Seen lessoftenthanthe Insect, beetle,ladybirdbeetle(Coleoptera:Coccinelidae) Crocodile-like, andcangrow Aphids, mites,thrips,smallcaterpillars,insecteggs Different fromadults(completemetamorphosis) Ladybird, ‘Volkswagen’, coccinelid Ladybird Beetles ( 13. ipdmavariegata Hippodamia ( ladybird beetleeggs 12. ipdmavariegata Hippodamia Ladybird beetlelarva A typicalclusterof ) ) 16. septempunctata pupa ( 14. Adults may often be seen mating (Picture 18). 16), or more orless completely brown or black (Picture 17). may be red ororange withblack markings (Pictures 15and Adults: Adult ladybird beetle ( Ladybird beetle Coccinella Easy torecognise, dome-shaped bodies, wingcovers ) Ladybird Beetles Cheilomenes ( 15. ipdmavariegata Hippodamia sp.) Adult ladybirdbeetle ) 27

Predators Predators 28 beetles (notably, Note thatthere are several species ofplant-feedingladybird PEST LADYBIRD BEETLES or matt appearance (Picture 19). wing cases are covered infinehairs givingthem anon-glossy yellowish in colour andare covered indelicate spines. Theadult the larvae eat leaves ordamagefruits. Thelarvae are pale commonly referred toas curcurbits (such ascucumberandmarrow). Thesespecies are to solanaceous crops (suchastomato andpotato) often regarded aspestsbecause of thedamagetheycancause Epilachna Ladybird Beetles melon beetles and Henosepilachna . Boththeadults and ( 17. ( beetles mating 18. Exochomus ipdmavariegata Hippodamia Adult ladybirdbeetle Adult ladybird spp.) thatare sp.) ) underestimated. be more active atnightthanby daysotheiractivity is often over its lifetime of1-3months. Ladybird beetlelarvae tendto large. Asingle ladybird beetlemight consume 200-300aphids Usually, theyare most abundantwhenaphidpopulations are The larvae eat more pests(particularlyaphids)than theadults. EFFECTS ONPESTS ( 19. hairs onwingcases Henosepilachna Plant-feeding melonbeetles sp.). Notefine Ladybird Beetles (such asbeesandhoverflies) hover flies)andpollinators (such asladybirdbeetlesand to helpsupportnaturalenemies 20. Fennel inavegetableplot 29

Predators Predators 30 of this guide). enemies (seeParts 3.2and 3.3 least harmfultokeynatural application methodthatis necessary, use aproduct and Should spraying beconsidered unless absolutelynecessary. of pestaphidsonthecrop. and suppress thedevelopment natural enemiestobuild-up they allowpopulations ofthe insects likeladybird beetles and refuge sitesforbeneficial provide foodsources and 22) andmilkweed.These (Picture 21), thistles (Picture fennel (Picture 20),coriander around thecrop, suchas aphid species withinand ‘weeds’) thatsupportnon-pest (sometimes thoughtofas non-crop floweringplants CONSERVATION Avoid spraying pesticides Grow stripsorgroups of Ladybird Beetles between croprows which canbegrownasstrips many otherfloweringplants), attracted tocoriander(and other beneficialinsectsare 21. predators likeladybird beetles brassicas tohelpsupport aphid 22. Adult ladybirdbeetlesand Thistles growing among (3 – 30mm inlength), are often brown orblack in colour and leaves onground ormulches are disturbed. Adults vary insize are not oftenseen by dayunless hidingplaces suchas rocks, (Picture 23). Mandibulate mouthparts (‘jaws’) canbeseenreadily whitish to brown. that vary in colourfrom colour thanthebodies are usually darkerin legs. Head andthorax end, with3pairs of tapered towards the segmented bodies, elongated, clearly unless soilis disturbed; often seen. Common names: Group: and wheremulchesarepresent Crops: Main prey: Immatures: Type: Adults: Pupae: Larvae: Eggs: APPEARANCE Predator (larvaeandadults) In soilandnot Most, particularlyonmixedcropsandnearnatural vegetation Most species are mainlyactive at night ( In soilandrarely seen. Insect, beetle,groundbeetle(Coleoptera:Carabidae) In soil,notseen Eggs andimmatureinsectsinoronsoil Different fromadults(completemetamorphosis) Ground beetle,carabid Ground Beetles ( 23. Pterostichus Ground beetlelarva sp.) nocturnal ), so 31

Predators Predators 32 harbourages for adult beetles. stones and logs close tocropping areas can provide useful beneficial insects like carabid beetles. For example, rocks, back uptheplant andresume feeding. aphids thathave fallenfrom plants andwouldotherwise climb Although ground beetles donotclimbupplants, theyconsume range ofpests includingcutworms, beanfliesandaphids. Thus, they maybeimportantinhelpingtocontrol abroad life stages(eggs through toadults)usually inoronthesoil. generalists, ground beetleseatawiderange ofinsects ofall areas thatare themselves diverse (e.g.,scruborforest). As present andsoils are kept humid,orincrops closetonatural diversified (mixed) crop environments, where mulchesare predators (seep.16)and are usually more abundantin 24). Mostspecies ofground beetleare unable to fly. and catchprey. Theantennaeare longandthread-like (Picture night. Thelegs are welldeveloped allowingthem torunfast CONSERVATION Adult andlarval ground beetlesare oftenimportant EFFECTS ONPESTS 24), theseoftenbeingmore active by day( species mayhave ametallicsheen totheirwingcases(Picture have distinctive ridgesontheirwingcases(Picture 24).Some It is important todevelop refuges forsoil-dwelling Ground Beetles adult ( 24. diurnal Ground beetle Chlaenius ) thanby generalist sp.) enemies (seeParts 3.2and3.3 of this guide). application method thatis the least harmful tokeynatural Should spraying beconsidered necessary, use aproduct and humidity (Picture 26). around orbetweencrops) (Picture 25). non-crop plants, including use oflive fences(trees orhedges 25. Avoid spraying pesticides unlessabsolutelynecessary. Use mulchestoprovide harbourages andmaintain soil Promote diversity in the cropping area, using crop and Live fencesaroundavegetablecroppingarea Ground Beetles predators other ground-dwelling for carabidbeetlesand attractive environment rape) providesan plants (inthiscase, 26. Mulch aroundcrop 33

Predators Predators 34 appendages or ‘pincers’ at the endofabdomen(although smaller segments of the abdomen. The abdomen may be raised in short wingcases(Picture 27) ofadultsdo notconceal the Adults: Pupae: and feedwithin insect hostpupae.Size is extremely variable. legs andmandibles (‘jaws’), whilesomespecies are parasitic well developed narrow bodiesand adults, long, relative to the segmented, and, having distinctive free-ranging, These maybe Larvae: Eggs: APPEARANCE Common names: Group: Crops: (including immatures,e.g., larvaeandpupae) Main Prey: Free-ranging orparasiticlarvae Immatures: parasitoids Type: seen. Adults andlarvaemainlypredators;afewspeciesare Not often Most, maybeseenonplantsorsoil Insect, beetle,rovebeetle(Coleoptera:Staphylinidae) May beearwig-like, butlackthewell-developed Not oftenseen. Eggs, mites,aphids,scaleinsects,othersmallinsects Different fromadults(completemetamorphosis). cerci Rove beetle,staphylinid may be clearlyvisible). Thedistinctive on aleaf beetle ( 27. Rove Beetles An adult,generalistrove(staphylinid) Philonthus sp.) searchingforprey and Kenya. common andpredatory onred spider mitesin both Zimbabwe ( for thepresent work,onegenus ofvery small staphylinid (tetranychid) miteinfestations. Duringthesurveys undertaken owing totheirincreased abundance,duringheavy red spider identify withthenakedeye butoftenbecomemore obvious, 1 mmto20inlength.Thesmallest onesare difficultto (Picture 27).Theyare very variable insize,ranging from about cases maybecoloured differently from therest ofthebody beetles are oftenreddish-brown, brown orblack.Thewing a threatening posture (likescorpions) whendisturbed. Rove some timelaterasadults, havingconsumed thepupa. fly pests, forexample), andtheyemerge from thehostcocoon search thesoilforsuitable hostcocoons (containingpupaeof Other species are parasitic; individual young larvae typically more studiesare needed toassesstheirimportancemore fully. cutworms, beanflies, spider mitesandscaleinsects, although They maybeimportantin helpingtocontrol pestssuchas all lifestages(eggs through toadults)inthesoiloronfoliage. forest). Thesegeneralist species eatawiderange ofinsects of close tonatural areas thatare themselves diverse (e.g.,scrubor in cropped areas thathave adiverse range ofvegetation orare important Some species ofrove beetles, bothasadultsandlarvae, are EFFECTS ONPESTS Oligata sp., adultabout1mminlength)wasfoundtobe generalist predators, andare usually more abundant Rove Beetles 35

Predators Predators 36 enemies (seeParts 3.2and3.3ofthis guide). application methodthatis theleastharmfultokey natural Should spraying beconsidered necessary, use aproduct and harbourage areas (seealso leaving orimportingstones, logs orotheritems thatprovide non-crop plants)inandaround crop plots, using mulchesand beetles. This mightbeby promoting diversity (crop and beetles andotherground-dwelling predators like carabid CONSERVATION Avoid spraying pesticidesunless absolutelynecessary. It is importanttodevelop refuges forsoil-dwellingrove Rove Beetles Conservation , Ground Beetles , p.31) move rapidly and canbe on their wings. Adults black andwhite patches Anthocoris crops ( vegetable (or flower) common genus on (Picture 28).Themost larger than2-3mm the adultsbeingno tiny insects (truebugs), tissue. Generally laidinplant Common names: Group: Crops: Main prey: Immatures: Type: Adults: Nymphs: in colour. brown, black ororange (similar toadults);often tear-drop-shaped mm inlength)andare are minute(lessthan2 Eggs: APPEARANCE Predator (nymphsandadults) Not oftenseen. Orius Beans, potatoes,tomatoes,otherscrops(rarelybrassicas) Pirate bugs are Insect, anthocorid(Hemiptera:Anthocoridae) The nymphs spp.) have Thrips, mites,aphids,insecteggs,smallcaterpillars Similar toadult(incompletemetamorphosis) and Orius bug, anthocorid Pirate Bugs Research International, UK) (Photographs courtesy ofHorticulture ( 28. Above: Anthocoris sp.) Pirate bugnymph Below : adult 37

Predators Predators 38 enemies (seeParts 3.2and3.3ofthis guide). application methodthatis theleastharmfultokeynatural Should spraying beconsidered necessary, use aproduct and primary prey (mites, thripsandaphids)are notavailable. near thecrop canhelptosustain adultpirate bugs whentheir CONSERVATION determined. Africa andtheirrelative effectiveness hasyet tobeadequately solanaceous crops. There are manynative anthocorid species in mites perday. Theyare particularlycommononlegumeand An anthocoridnymphmayconsume uptoabout 30 spider larvae andnymphs) ofawiderange ofothersmall arthropods. thrips andaphidsbutwillattackvarious stages(e.g.,eggs, Pirate bugs canbevery importantpredators ofspider mites, EFFECT ONPESTS available (Picture 28). Adults canfeedonpollenandplantjuiceswhenprey are not contents oftheirprey withtheirpiercing/sucking mouthparts. found huntingprey onleaves andflowers. Theysuckthebody Avoid spraying pesticidesunlessabsolutelynecessary. Planting ormaintainingfloweringplants(including weeds) Pirate Bugs ground. Antsare attackedon fallinginthe pit(Picture 31). relatively hugepincer-like ‘jaws’ visible above thesurfacein beneath thesoil surfaceincharacteristic pits, withonlytheir sometimes be foundonvegetable crops. Ant-lions reside just on somecrops (particularlycottonand coffee).Theycan ‘jaws’. Theyare very mobileandcanbe foundinlarge numbers and possesslarge pincer-type and crocodile-like (Picture 30) Aphid-lions are usually brown ‘ant-lions’ (Picture 31). ‘aphid-lions’ (Picture 30)and being commonlyknownas main typesoflarvae, these the insect world!There are two among thefiercest predators in (Picture 29). characteristic finesilk stalks Immatures: Type: Larvae: Eggs: APPEARANCE Common names: Group: Crops: eggs Main Prey: adults (lacewings)(completemetamorphosis) Predator (larvaeonly) Eggs are laidon Beans, potatoes,tomatoes,otherscrops(rarelybrassicas) Insect, lacewing(Neuroptera:Chrysopidae) Lacewing larvae are Aphids, otherplant-feeding bugs,small caterpillars,insect Larvae ( Lacewing larva,aphid-lion,ant-lion, chrysopid ‘ ant-lions Lacewings ‘ or ‘ aphid-lions on asilkstalkfromleaf 29. A lacewingeggsupported ‘ ) differentinformto 39

Predators Predators 40 spider eggsacs. on vegetable crops. They cansometimesbeconfused with flowers and other sugary substances like aphid honeydew. bodies (Picture 32). Theadults onlyfeedon nectarfrom veined, net-likewings, large eyes and rather fragile-looking flowers. They canreadily bedistinguished by theirfinely seen indoors, nearlightsintheevenings, or feedingfrom Adults: Pupae: carnea ( lacewing adult 32. searching forpreyonaleaf lion type)( 30. Chrysoperla A green A lacewinglarva(aphid- ) The adults, commonlyknown as‘lacewings’, are often These are whitish andspherical, butare notoftenseen Chrysoperla carnea Lacewings ) within itsin-groundpit 31. An ant-lion seizesanant enemies (seeParts 3.2and3.3ofthis guide). application methodthatis theleastharmfultokeynatural Should spraying beconsidered necessary, use aproduct and around fieldmargins, betweencrop cycles. aphids andotheralternative hostsonnon-crop (weedy) areas provide afoodsupply foradultlacewings. numbers oflarvae ( been welldocumentedoncottonandcoffeewhere large The effectiveness oflacewinglarvae aspredators oncrops has EFFECT ONPESTS CONSERVATION crops. inoculation oraugmentation,andare used widelyoncovered larvae are available commercially inmanycountriesfor effectiveness hasyet tobeevaluated adequately. Lacewing season, lacewinglarvae appearnottobeascommon andtheir vegetable crops, which oftenhave arelatively short growing range ofpests(e.g.,aphidsandeggs ofmothpests).In Avoid spraying pesticidesunless absolutelynecessary. Populations canbemaintainedonnon-pestspecies of Ensure flowers are present withinorcloseto thecrop to Chrysoperla Lacewings spp.) can‘cleanup’awide 41

Predators 42 Hover Flies Hover Flies 43

Type: Predator (larvae only) 34. A batch of hover fly Predators Predators Immatures: Different from adults (complete metamorphosis) eggs (one egg has already Main Prey: Aphids hatched) Crops: 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 see on the leaves of plants, particularly where aphids are common. They are white, cylindrical and about 1-2 mm long. Some species lay their eggs singly, close to aphid colonies (Picture 33), while others lay eggs randomly on plants in 35. Last instar hover fly larva 36. Last instar hover fly larva feeding on cabbage aphids (13mm length) just before batches (of often 2-5 33. A single hover fly egg adjacent to pupation. Note fat stripe along eggs) (Picture 34), even an aphid colony (non-pest species on top of body on plants that are more thistle) or less un-infested by aphids. The first larva tip) (Pictures 35 and 36). This contrasts with the well-defined to hatch from one of head, chewing mouthparts and prolegs of caterpillars. The these egg batches can bodies of hover fly larvae, like all fly larvae, also lack the Larvae:survive by The eating larvae the are larvae often within mistaken the unhatchedfor caterpillars eggs. but Close on prolegs (short, stumpy, appendages used for ‘walking’) of moth closeexamination examination of the they egg are will easily reveal distinguished whether the by larvae their haveslug-like, and butterfly caterpillars, and sawfly larvae. They may be taperedhatched. bodies and pointed heads (mouthparts retract into the translucent, green, or brown in colour, depending on species and prey consumed, and the bodies may be slimy-looking or Predators 44 the pupal casedark brown (Picture 38). Diplazon soil. Theycan sometimesbeattackedby parasitoid wasps (e.g., or brown; they are eitherattached to leaves ordevelop in the Pupae: food thatlarvae are abletoconsume duringtheirdevelopment. depends bothonthespecies andtheamountqualityof may grow upto15mm before pupating.However, overall size within aphidcolonies, whilethelast(third) instar (Picture 36) larvae are tiny(1-2mm) andmaynotbevisible iffeeding the lengthoftheirbodies (Pictures 35and36).Thefirst instar marked withonetothree whitish (fat-containing)stripesalong ‘bristly’ inappearance. Somecommonspecies are greenish and Pupae are pear-shaped andmaybe green (Pictures 37) sp.) that pupatewithin thehover flypupa, turning Hover Flies attached toleaf 37. pupa 38. Hover flypupae Parasitised hoverfly antennae. bees and wasps have longer a ‘V’shape) (Picture 41), while large compound eyes (forming that originate from between very short, stumpy antennae have twopairs; andflies have pair ofwings, whilewasps and wasps: flieshave only one set allfliesapartfrom thebees two commoncharacteristics (Order Hymenoptera). However, to adifferent insect group wasps andbees, which belong sometimes confused with in ‘breathing’. Theadultsare lower theirabdomens, toassist rest, adultsoftenraise and the side(Picture 42).Whenat rather flatwhenviewedfrom grey onblackandis always and 41), amber (Picture 40)or often stripedyellow (Picture 39 adult aphid-eatinghover fliesis (Picture 40).Theabdomenof the production ofviableeggs adult foodsources, required for nectar andpollenasessential close toflowers thatprovide 39). Theyare oftenseenonor hover, helicopter-like(Picture the males(inparticular)to common nametotheabilityof Adults: The adultfliesowetheir Hover Flies and pollenwithin kaleflower adligatus 40. 39. Hover flyadult( Adult hoverfly ) feedingonnectar ‘ hovering Betasyrphus ’ 45

Predators Predators 46 Some species only becomeabundant when aphid numbers are a pupa! Mostofthis eatingis doneinthe final(third) instar. two weeks before itturns into over 400 aphidsinaboutthe a singlelarva caneatwell and are extremely voracious - are particularlyactive atnight aphid predators. The larvae the mostimportantgroup of situations hover flylarvae are hover flylarvae. Inmany aphid-eating ( to crop production are the group whichis mostimportant range offood sources, butthe Hover flylarvae feedonawide EFFECT ONPESTS of alladultflies single pairofwingsandshortantennaetypical 41. Hover flyadultfeedingfromaflower. Note aphidophagous Hover Flies ) on leaf searching foregg-laying site 42. Hover flyadult female very importantpollinators. management viewpoint.Inaddition,theadults, likebees, are groups should beregarded ascomplementary from apest are welladaptedtodealingwithlowdensities of aphids. Both Platycheirus help maintainhover fly populations inthevicinityofcrop. species; Picture 33),whichprovide anon-goingfoodsupply to flowering plantsmayalso supportaphids(oftenof non-pest adults thatemerge from pupaefrom withinthe crop. These nectar before theycanlayviableeggs, italso prevents ‘loss’of plots, andbecause adultfemalesmust feedon pollenand source (Picture 43).This increases immigration ofadultstothe within oratleastaround crop plotstoprovide anadultfood sunnhemp, floweringbrassica crops or‘weeds’)must begrown also reduce windspeed thatmightotherwise disturb the farmers asarrivingtoolate.Others (e.g., large andtheirbeneficialeffectmayberegarded by some CONSERVATION adult hover flies sources (nectarandpollen) for pictured) provides plentifulfood plants (including floweringkale 43. Flowering plants(suchasfennel,thistles, milkweed, Live fencescancontain flowering plants(seeabove) and Abundance of flowering spp. thatlaytheireggs incharacteristic batches) Hover Flies of this guide). enemies (see Parts 3.2and 3.3 least harmful tokeynatural application methodthatis the necessary, use aproduct and Should spraying beconsidered unless absolutelynecessary. gravid femalehover flies. egg-laying activitiesof Avoid spraying pesticides Melanostoma and 47

Predators 48 Predatory Mites Predatory Mites 49

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

APPEARANCE Eggs: Laid on plants, round or oval in shape, too small to be seen with the naked eye. Nymphs: Similar but smaller than adults, the early instars with 44. Tomato leaves showing 45. Predatory mites only three pairs of legs, compared with the four pairs of older symptoms of heavy red spider (Phytoseiidae) among large mite infestation. Although colonies of red spider mites nymphal (and adult) stages. predatory mites can often be (Tetranychus sp.) Adults: Mites are so small that they can barely be seen with found on such heavily damaged the naked eye. They are not insects and are more closely plants, they probably arrived related to spiders and are even closer relatives of ticks. As such, too late from the farmer’s the adults have four pairs of legs and two body segments viewpoint rather than the three of insects. They can often be found on in colour, depending on their growth stage (Picture 45). plants where plant-feeding tetranychid mites (red spider mites) Therefore, colour must not be used as the only way of are present (Picture 44). They are about the same size (less separating theseEFFECT mite types!ON PESTS than 1 mm in length) as spider mites but they move much Predatory mites (e.g., Amblyseius, Phytoseiulus spp.) can be one more rapidly, have longer legs and more oval (pear-shaped) of the most effective natural enemies of spider mites. They can bodies (Picture 45). They may be red in colour, dark or even search out spider mite colonies effectively and can reach areas translucent in colour, depending on species and growth stage. that are difficult to target with pesticides. The most serious spider mite problems are often found on crops that are sprayed regularly Unlike spider mites, predatory mites can also move backwards. with acaricides or insecticides, pest resurgence being caused by Red spider mites are often distinguished by the presence of two the pesticide killing predatory mites and other key predators dark spots on the body, and characteristic webbing which they (e.g., predatory thrips, rove beetles) (see also pp. 13-14). If produce on infested plant parts. Predatory mites such as Phytoseiulus, as with the plant feeding spider mites are variable Predators 50 enemies (see Parts 3.2 and3.3 of this guide). application method thatis the least harmful tokeynatural Should spraying beconsidered necessary, use aproduct and mites intoseasonal crops suchasvegetables. crops willoften enhancetheimmigration rate ofpredatory perennial plants, sothepresence of theseplantsnearvegetable to predatory mites. often contributetospider miteoutbreaks astheyare harmful capture otherfooditems suchaspollenandfungalspores. humidity, provide protection from predators andhelp to hairy leaves mighthelpto reduce hightemperatures, increase reasons for this are notfullyunderstood butcultivars with hairiness ofcrop leaves andabundanceofpredatory mites. The inoculation purposes. They are available commercially inmanycountriesfor introduction asandwhenspider miteorthripsproblems arise. plants deliberately infestedwithspider mites, ready for CONSERVATION spider mites, theycanbeintroduced ( predatory mitesare notfoundonacrop beingdamagedby effective against thrips. spores intheabsenceofprey. Predatory mitescanalso bevery Typhlodromus spider mitesorthripsare already present. Somespecies (e.g., should onlybeintroduced tocrops where primaryprey suchas mites willstarve anddieiftheyrunoutoffood,so they control agents. However, mostcommonspecies ofpredatory of countriestheyare commercially available asbiological readily bereared forthis purpose andinanincreasing number Avoid spraying pesticidesunless absolutely necessary. Predatory mites are commonontrees, shrubs andother Maintain irrigationofcrops toavoid dusty conditions which There tendstobeanassociationbetweenthedegree of Predatory mitesmaybesustained inculture on potted spp.) are abletosurvive onpollenandfungal Predatory Mites inoculated ). Theycan honeycombed nests ‘papery’ and that form characteristic Polistinae; Picture 46) wasps (Hymenoptera: the paper(polistine) ( live ingroups solitary ortheymay and 47).Theymaybe abdomen (Pictures 46 striped markingonthe with someformof in length,generally wasps, often12-30mm unless nestsare openedup. or even around buildings andotherstructures. that maybeintheground, inorontrees andother vegetation, Eggs: APPEARANCE Vespidae) Group: prey arepresent Crops: Main prey: Immatures: Type: Adults: Larvae andpupae: eusocial Predator These are notseenastheyare laidwithinwasp nests Any cropsonwhichcaterpillars,sawflylarvae,bugs andother These are large Insect, wasp(Hymenoptera:Polistinae, Sphecidaeand ). Theyinclude Caterpillars, sawflylarvae,heteropteranbugs Different fromadults(completemetamorphosis) Predatory wasps Wasp larvae andpupaeare also notseen collecting preyforits young 46. A paper wasp( Polistes sp.) 51

Predators 52 Predatory wasps Mantids 53

often found Type: Predator (nymphs and adults) Predators Predators suspended by a stalk Immatures: Similar to adult (incomplete metamorphosis) from the leaves of Main prey: Moths, flies, crickets, small spiders trees or sides of Crops: Various buildings, and the Group: Insect, mantid (Order Mantodea) sphecid wasps Common names: Praying mantis, mantis (Hymenoptera: Sphecidae; Picture 47) that can exceed 40EFFECTS mm in ONlength. PESTS 47. A sphecid wasp (Sphex sp.) in search On crops where APPEARANCE of prey, heteropteran bugs in particular caterpillars, sawfly Eggs: Females lay these in a sac containing hardened foam. larvae or other prey Nymphs: Form and function similar to adults, although smaller are abundant, in size. predatory wasp adult females can be seen repeatedly on Adults: Mantids have characteristic forelegs that assume a ‘sorties’ in search of prey. Prey are stung, paralysed and taken ‘praying posture’ when at rest, hence the common name, back to the nest to provide a food source for developing praying mantis larvae. Nests may be in the ground, in natural cavities within (Picture 48). Mantids trees, stumps, or they may be constructed of mud or ‘paper’. wait motionless, Although the predatory habit of members of these wasp often well families is often highly conspicuous, their impact on pest camouflaged within CONSERVATIONpopulations has not been well studied and therefore is poorly foliage until prey Avoidunderstood. destroying nesting sites, unless the presence of the come within their wasps poses a threat to humans, especially young children, who grasp. Then they will could be stung. suddenly pounce, Avoid spraying pesticides unless absolutely necessary. grasping their prey Should spraying be considered necessary, use a product and with their powerful 48. A praying mantis adult in resting pose application method that is the least harmful to key natural forelegs – and the on a sunflower plant close to a vegetable enemies (see Parts 3.2 and 3.3 of this guide). feast begins! The plot adults are strong flyers so can disperse widely. Predators 54 enemies (seeParts 3.2and3.3ofthis guide). application methodthatis theleastharmfultokey natural Should spraying beconsidered necessary, use aproduct and CONSERVATION is notoccurring. indiscriminate use ofbroad spectrum insecticides oracaricides enemies. However, theirpresence is oftenanindicationthat be partiallyoffset by negative impactsonother natural moths andflies),theirbeneficialrole mayinsomesituations beneficial fliesandspiders) aswellpestinsects (e.g.,some are rather indiscriminate feeders, eatingnatural enemies(e.g., agricultural pestshasnotbeenwellevaluated. Sincemantids insect predators, theextentofitsvalue asanatural enemyof Although thepraying mantis is oneofthemost well-known EFFECTS ONPESTS Avoid spraying pesticidesunless absolutelynecessary. Mantids arthropod prey. Manyspecies trap theirprey in netsorwebs, legs. Theyfeed by suckingthe bodyfluids from their not insects. They have two body segments andfourpairs of spiderlings sometimes called spider nymphs thatare even hundreds oftiny several orsometimes sac hatchtorelease The eggs withinthe whitish-coloured silk. and covered in spherical inshape spiders are usually Eggs: APPEARANCE Group: Crops: mites, aphids Main prey: Immatures: Type: Adults: Nymphs: currents. This behaviour is called ‘ballooning’or‘parachuting’. can produce threads ofsilkthataid theirdispersal by wind Small, young spiders adults, except insize. very similartothe Predator Egg sacs of Most Spiders are recognised by everyone! Likemites, they are Spider (Arachnida:Araneae) These appear . Flies (e.g., leafminers),moths,smallcaterpillars, Similar toadults(incompletemetamorphosis) Spiders (Family Linyphiidae) 49. Webbing spiderandsheetweb 55

Predators Predators 56 trap prey, and 49), suchassheet webspiders, whichspin websthatinturn according tohowtheyhunttheirprey: found oncrops canbedividedbroadly intotwo groups predators onagricultural crops includingvegetables. Spiders a nuisance around thehome,spiders canbevery important Although spiders ortheirwebsmaysometimesbe regarded as EFFECT ONPESTS jumping spiders (Salticidae) andorbweavers (Araneidae). (Oxyopidae; Picture 51), wolforground spiders (Lycosidae), Picture 49),crab spiders (Thomisidae; Picture 50),lynxspiders vegetable crops, including sheet webbingspiders (Linyphiidae, their prey. Spiders from various familiesmaybefoundon while others forage actively orlieinwaitbefore pouncingon as wellpestspecies. generalist feeders, theymaysometimesprey onnatural enemy can bethedominantnatural enemyofkeypests. However, as systems, suchasriceinAsia,spiders, particularly wolfspiders, pounce onandoverpower theirprey. Insomeagricultural crab, jumpingorwolf spiders, thatrely ontheirabilityto 50. Crab spider(Family hunting spiders Thomisidae) Spiders (Pictures 50and51), suchas webbing spiders (Picture key natural enemies(seeParts 3.2and3.3ofthis guide). product andapplicationmethodthatis theleast harmfulto necessary. Shouldspraying beconsidered necessary, use a CONSERVATION 51. Avoid spraying insecticides oracaricidesunlessabsolutely Do notremove spider webbingoreggsacs from plants. Lynx spider( Peucetia sp., FamilyOxyopidae) Spiders 57

Predators Predators 58 others, referred toas‘attendant ants’, can protect aphids and sites. Somespecies ofantscan beimportant predators, while above-ground neststhatcan besomedistance from foraging whitish incolourand grub-like,are maintainedinbelow- or searching for andcollectingfood.Larvae andpupae,whichare trails asa means of ants generally use 52 and53).Worker commonly (Pictures encountered most hence are thecaste food collectionand are responsible for undeveloped females, comprised ofsexually worker ants, each colony. The reproductives) within workers, soldiers and different groups (i.e., are socialinsects andsohave adivision oflabour between Ants (Hymenoptera: Formicidae), likeallbeesandmanywasps, understood. in tropical vegetable cropping systems is presently notwell following insects is wellknown,theimportance of eachgroup Although thepredatory role ofparticularlife-stagesthe OTHER INSECTPREDATORS below. vegetable crops. Some oftheseotherpredators are considered a diverse range ofanimalgroups, thatcanprey onpestsof There are manyothertypesofpredator, representing Ants Other Predators from abeanpod 52. Ants removingacaterpillar 53. their prey. by sucking bodyfluids from substantially) andthey feed (although colours mayvary basic formto theadults the nymphs are similarin incomplete metamorphosis, so length. Theyallundergo typically being30-40mm in the largest in size,withadults Assassin bugs (Picture 54)are species that are predatory. (Pentatomidae) also contain (Miridae) andshield bugs bugs (Lygaeidae), miridbugs bug thatincludemanyplant-eating members, suchaslygaeid assassin bugs (Hemiptera: Reduviidae).Otherfamiliesoftrue Anthocoridae; p.37),nabidbugs (Hemiptera: Nabidae) and bug (Order Hemiptera): minutepirate bugs (Hemiptera: These includethree importantpredatory groups oftrue clearing itfromakaleplant diamondback mothcaterpillarafter Predatory bugs ‘ Safari ’ antscarryinga Other Predators fluids of prey beak used forsucking body 54. pests). produced by sucking sugar-based secretion honeydew (thesticky, securing theirsupplyof enemies asameans of from attackby natural other suckingpests Assassin bug;note 59

Predators Predators 60 many small insects, includingleaf minerlarvae. abundant andimportantnatural enemiesofmitesand markings on their‘feathery’wings. Theycanattimesbe while others mayappear banded(Picture 55)orhave spot Their colourmaybeuniform varying from opaque toblack, 1-3 mminlength)withcharacteristic bullet-shaped bodies. rather similartoplant-feedingthrips, beingvery small (often species are predatory onothersmall arthropods. Theseappear flowers, leaves, fruitsandbuds. However, asmall numberof enclosed inacocoon.Mostthripsare plantfeeders, attacking pre-pupal andpupalstagesrespectively. Thepupaemaybe and fourth)donotfeedare oftenreferred toasthe under magnification.Thefinaltwoinstars (usually thethird long hairs, givingthemafeatheryappearance whenviewed are fourinnumber, andare long,narrow andfringed with when present andfullydeveloped, never show wings externally. Wings, instars, oftenreferred toaslarvae, the adults, althoughthefirst two which lookessentiallysimilarto intermediate, withimmatures metamorphosis whichis plant-sucking pests, undergo some ofwhichare important Thrips (Order Thysanoptera), Predatory thrips Other Predators broad bean within aleafmineon 55. A predatorythrips often eatenwhiletheadultsare inflight. of small flyinginsects suchasfliesandmoths, are caughtand other crops. Mostoftheadultprey, whichincludeawiderange between boutsofsearching forinsect prey on vegetable and adults are oftenseenresting onplants(Pictures 56and57) near ponds, streams, rivers andirrigationcanals. Thefast-flying (nymph) lifestages, sotheyare particularlycommon incrops These insects (Order Odonata)bothhave aquatic immature Dragonflies andDamselflies Zygoptera) adult atreston 57. A damselfly(Suborder reeds nearwater Other Predators vegetable crop plantneara a non-crop Anisoptera) adultrestingon 56. A dragonfly(Suborder 61

Predators Predators 62 the axils ofplants(Picture 58). any area where small quantitiesofwateraccumulate,such as component. are oftena more importantfood mobile thannatural enemies, pests because pests tendtobeless insects andotherarthropods, but They feedonawiderange of spectrum pesticides are notused. particularly thosewhere broad found invegetable crops, lizards (Picture 60)are frequently Chameleons (Picture 59) and REPTILES crops organically-grown brassica insect pestsonnearby plant, alsofoundforagingfor 58. 59. Tree frogin axilofbanana sources, notablyaphids, onkale A chameleon searching forfood plants on anorganickale crop Other Predators tadpoles, butthis maybein allow development of in whichtolayeggs and caterpillars. Theyneedwater insects includingaphidsand can feedonawiderange of vegetable crops where they uncommon onunsprayed (Picture 58),are not about 20-30mminlength enemies. Small‘tree frogs’, eat pestsaswellnatural for insects, althoughtheymay toads have ahealthyappetite Amphibians suchasfrogs and FROGS ANDTOADS selectively by hand(Picture 61). enemies too!Particular life stagesofpestscanberemoved also cause serious damage tocrops. Humans canbenatural although theymayfeedoncertaininsects present, theymay Rats are notuncommonvisitors tovegetable crops, and MAMMALS damage leaves andfruits. other animals invegetable crops. However, birds mayalso Many bird species, suchasshrikes, canforage forinsects and BIRDS Other Predators organic farm cabbage plants onan sp.) pupaefrom bollworm ( predators: hand-picking 61. organic crop for preyinamixed 60. A lizardsearching Humans as Helicoverpa 63

Predators 64 Parasitoid Wasps Parasitoid Wasps 65

Type: Parasitoid lay their eggs within or on the body of their host (prey) and Parasitoids Immatures: Different from adults the eggs hatch into larvae that feed on the host. After pupation Parasitoids Main prey: All pest insects, including caterpillars (moth larvae), within or outside the host’s body, the adult parasitoid wasp aphids, bugs, fly larvae, insect eggs, beetle and fly larvae, insect pupae emerges, usually as a small, dark-coloured, winged wasp Crops: All (typically 1- 6 mm in length). Some species of parasitoid wasps Group: Insect, wasp (Hymenoptera: Braconidae [incl. Aphidiinae], have wingless adults that appear ant-like. The prime purpose Ichneumonidae, Chalcidae, Eulophidae, Trichogrammatidae, and of the adult stage is dispersal and reproduction, although some others) adults are predaceous and may host feed, killing pests (and Other common names: Parasitoid, parasitic wasp, parasite, wasp potential hosts) in the process. Host feeding is common in adult 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 larval APPEARANCE AND BIOLOGY parasitoid’s presence within its insect host. In other cases, outside the host’s body. Field collection and rearing of immature There are about 50,000 described species of parasitoid wasp the host insect may become swollen or permanently paralysed stages of pests, to check if any adult parasitoids emerge, is and many of them are so small that they go unnoticed. To the after being ‘stung’. Parasitoid wasps may pupate within or untrained eye, these wasps look rather like small flies or flying often a useful method for determining whether parasitism has ants (see Pictures 65 and 66 on pp. 67-68). Some, notably egg occurred (see Part 3.1 of this guide). In vegetable crops, and leaf miner parasitoids, are so small they often require parasitoid wasps that attack aphids (pp. 65-66), moth pests magnification to be distinguished as wasps. Unlike the much (caterpillars and eggs) (pp. 68-70), leaf miners (pp. 70-71) larger predatory wasps (pp. 51-52), which have the ability to and whiteflies (p. 72) are particularly important. inflict a painful sting on unwary humans, parasitoid wasps, APHID PARASITOIDS with very few exceptions, cannot sting any animal other than The first obvious indication of aphid parasitism is usually the their insect host. In parasitoids, stinging by females is the presence of aphid mummies (Pictures 62 - 63). Mummified process by which eggs are laid (oviposition). In many crop/pest aphids have been killed by the wasp larva, which will have situations, parasitoid wasps are the single most important consumed the aphid’s body contents, leaving only the aphid’s group of natural enemy, although their impact can be hard to evaluate without detailed study (see Part 3.1 of this guide). cuticle (skin) as the parasitoid’s cocoon. The cuticle changes colour, often becoming brown, golden, pinkish or black, Parasitoid wasps comprise a very diverse group with complex depending on the particular parasitoid wasp and aphid species and variable biologies, spread across a large number of families within the Order Hymenoptera. Parasitoids also exist within the attacked. With many species, following pupation within the fly (Diptera: Tachinidae, p. 76) and beetle (e.g., Coleoptera: Staphylinidae, p. 34) families. Parasitoid wasps nearly always Parasitoids 66 a very narrow range ofhostspecies ( Many species ofparasitoid are specific toonlyasinglehost or typically laybetween50and 100 eggs duringherlifetime. parasitoid develops withineachhostaphid.Each femalewill laying eggs, usually onlyoneperaphid.Onlyasingle able towatchadultfemales ‘stinging’aphids, intheprocess and have rather longantennae.The careful observer willbe (Picture 65) are very small (2-3mminlength),darkcoloured Adult aphidparasitoids beneath thedeadaphid’s body. parasitoids emerge aslatestagelarvae andspin theircocoons the backofaphid)(Picture 64)andemerges. Someaphid exit holethrough thedeadaphid’s cuticle(normally towards aphid, thenewly-formedadultparasitoid wasp chews acircular aphids and un-mummified(grey) showing mummified(brown) 62. have awider hostrange ( not takeinto account parasitism ofaphids that have yet to underestimate the amountofparasitism, sincethese countsdo (often expressed as apercentage) willnormally significantly Counts ofaphid mummiescompared withunparasitised aphids Cabbage aphidcolony Parasitoid Wasps generalists in centre persicae 63. ). specialists Aphid colony( ) withmummifiedaphid ), whileothers Myzus the parasitoid reaches thepupalstagewithinits hostaphid. already beenparasitised asmummificationdoes notoccuruntil possible totellvisually whetherun-mummifiedaphidshave become ‘mummified’(seePart 3.1ofthis guide).Itis not pupated andemerged adult parasitoidwaspshave with exitholes,indicatingthat 64. Cabbage aphidmummies Parasitoid Wasps on brassicas important parasitoidsofaphids Aphidiinae), oneofthemost Diaeretiella rapae 65. An adultaphidparasitoid, (Braconidae: 67

Parasitoids 68 Parasitoid Wasps Parasitoid Wasps 69

PARASITOID WASPS OF CATERPILLARS Parasitoids The larvae of these parasitoids Parasitoids may feed from within (endoparasitoids) or outside (exoparasitoids) their host’s body. However, it is usually the former group that are more important as natural enemies of caterpillars on 68. Right: The silk-covered vegetable crops (Pictures 66 cocoon containing the pupa of a braconid parasitoid (Cotesia to 72). Depending largely on sp.) of diamondback moth 69. A Cotesia sp. cocoon on a 66. Cotesia sp., a braconid the species of parasitoid, larvae. Left: The mortally leaf. The neat cap on the left side shows that an adult has parasitoid wasp and key either a single wasp, a small wounded host larva, showing endoparasitoid of diamondback already chewed its way out and number or a large number of the hole to the right side of its moth body from which the parasitoid emerged wasps (sometimes more than larva emerged before spinning 100) will develop within each its cocoon caterpillar. Late stage parasitoid larvae may emerge from their host, attaching their cocoon either to the dying caterpillar’s body or to the plant surface (as in Cotesia sp., Pictures 67 to 69) 67. A braconid larva (Cotesia or they may consume the sp.) emerging through the side bulk of the caterpillar before of a final instar diamondback 70. Diadegma sp., an ichneumonid pupation (as in Diadegma sp., moth larva, prior to spinning its parasitoid wasp, and key endolarval cocoon Pictures 70 to 72). Parasitoid parasitoid of the diamondback moth wasp cocoons (pupal cases) may be covered in white silk spun by the parasitoid itself (Pictures 68 and 69) or they may be contained within the host’s own pupal sheath (Pictures 71 and 72). Parasitoids 70 Zimbabwe, thesebeing Two genera of leafminerparasitoids are commonly foundin period. increasing numbers of leaf minerparasitoids over thecropping often foundthat theirabundancediminishes in response to avoiding applications ofbroad spectrum insecticides, it is leaf miners are allowedtoestablish inayounger crop by various parasitoids andpredatory thripsspecies are killed.If to manyinsecticides andtheirkeynatural enemies thatinclude spraying occurs. This is because theyreadily becomeresistant can becomeahuge,induced problem where indiscriminate spectrum insecticides are used regularly. However, leafminers (Diptera: Agromyzidae), particularlyinsituations where broad can bevery importantin thecontrol ofleafminerflies Black-coloured, tinyparasitoid wasps (around 1mminlength) LEAF MINERPARASITOIDS moth pupawithinitssheath unparasitised diamondback prepupa. of adiamondbackmoth cocoon withinasilkensheath 71. Left : A Right Diadegma : an Parasitoid Wasps sp. Meruana and 72. diamondback mothpupa( parasitoid cocoon( the differencesbetween removed toshowmoreclearly diamondback mothhavebeen silk sheathsofthe Diglyphus As for Picture 71 , although they left , butthe ) and right ) (Picture 75). occurs inthemine (Picture 74)andpupation within thebodyofhost epidermis, larvae develop miner larvae through theleaf female wasps withinleaf 73). Eggs are laidby adult spot ontheirthorax (Picture are distinguished by ayellow Liriomyza belong tothegenus most commonleafminerflies larger leafminerflies. The confused withtheslightly These wasps should notbe by specialist taxonomists. can usually onlybeseparated leaf mine found withina parasitoid pupa 75. A leafminer , andtheseadults Parasitoid Wasps epidermis ofabeanleaf peeling awaythelower huidobrensis a leafminer( larva visiblewithinthebody of 74. bean leaf ( 73. Liriomyza huidobrensis A leafminerparasitoid An adultleafminerfly ), exposedafter Liriomyza ) ona 71

Parasitoids Parasitoids 72 egg, this characteristic being auseful trait forrecognition. crops. Moth eggs turnblackwhen thewasp pupateswithin the within moth eggs onawiderange of vegetables andother or yellow. Theylaytheir eggs (oneorseveral perhostegg) antennae and theirbodiesmaybecoloured blackandyellow, in length.Theadultsgenerally have brightred eyes, short Trichogrammatidae), theadultsoftenbeingless than0.5mm This is anotherimportant group oftinyparasitoids (Family EGG PARASITOIDS These are tinyparasitoids (Family Aphelinidaee.g., WHITEFLY PARASITOIDS also hostfeed,killingmore whiteflyintheprocess. by parasitism (larval feedingwithinthenymphs), adultwasps turn blackorbrown (Picture 76).Apartfrom mortality caused is oftennoticedinthefieldwhenparasitised whitefly nymphs some countriesforrelease oncovered crops) andtheirpresence formosa , lessthan1mminlength,available commercially in Parasitoid Wasps underside ofaleaf whitefly nymphsonthe unparasitised (opaque) coloured) and 76. Parasitised (dark- Encarsia vegetable growing areas. for example, asmall highland plotisolated from other introduction maybeappropriate insomesmallholder systems, than it attracts natural enemies. thought torepel certainpestsmore organic farmers (Picture 79)is the crop. The use ofmarigoldsby close to,between, and/oraround flowering crucifers orsunnhemp coriander, nasturtiums (Picture 78), growing offennel(Picture 77), enemies. This mightinclude the parasitoids and otheradultnatural provided asadultfoodsources for flowers, containingnectar, are to as vicinity ofappropriate hosts. This process is sometimesreferred group oftheparasitoid (perhaps50-1000, bothsexes) in the may bepossibletoestablish itlocallyby introducing asmall pest inotherpartsofthecountryorregion is not present, it If animportantparasitoid oftenassociatedwitha particular FIELD INTRODUCTIONS methods are considered below: population growth. Somekey required toensure efficient reproduction onthefarmare food sources, shelter andmeans of provide parasitoids with adequate Conservation techniquesthat CONSERVATION Ensure amplenumbers of introduction or Parasitoid Wasps inoculation (see also p.18).This typeof natural enemies parasitoids and other resource foradult provide auseful nectar other flowering plants) 77. Fennel (andmany 73

Parasitoids Parasitoids 74 of compost cropping, livestock anduse farm, including mixed 80. used moretorepelpests adjacent tokaleplants, A smallholder organic 79. than attractnatural Marigolds growing enemies Parasitoid Wasps some build-up of plant-feeding (Picture 82)around plots. parasitoids by growing live fences for parasitoids. nectar sources andalternative hosts thought ofas‘weeds’)that provide non-crop plants(sometimes mixed cropping system andinclude (Pictures 80and81); develop a animal diversity incropping areas Grow trap crops thatcanallow Provide shelter andshade for Encourage habitat,plant and and humans source bothfornaturalenemies smallholder plot,usedasafood 78. Nasturtiums growingwithina enemies (see Parts 3.2 and3.3 of this guide). application method thatis the least harmful tokeynatural Should spraying beconsidered necessary, use aproduct and pests onthe nearby principlecrop (Picture 83). natural enemies, whichcaninturn provide earlysuppression of insects (that maybealternative hosts orpests)andtheir of floweringplants mixed croppingandprovision natural enemies,basedon 81. Avoid spraying pesticides unlessabsolutelynecessary. A diversehabitatfor Parasitoid Wasps for bollworms( 83. Meg Davies) (Photograph by cotton/vegetable mixedcrop smallholder organic Diparopsis organic farm vegetable growingareaonan 82. Sweet sorghum,atrapcrop A livefenceborderinga spp.), usedhereina Helicoverpa and 75

Parasitoids 76 Parasitoid Flies Parasitoid Flies 77

Type: Parasitoid markings (Picture 84). Being flies, Parasitoids Immatures: Different from adults (complete metamorphosis) they only have a single pair of Parasitoids Main prey: Cutworms, caterpillars, beetle larvae, fly larvae, bugs wings (which may also possess Crops: Brassicas, potatoes, cucurbits, maize and others markings and be less translucent Group: Insect, parasitic fly (Diptera: Tachinidae, and some other than those of a house fly) and Families) these are often held slightly or Other common names: Tachinid, parasitoid, parasitic fly, partially out-spread when at rest. parasite, fly 84. Adult tachinid (parasitoid) fly. Note EFFECT ON PESTS bristles on abdomen and Tachinids make up a very large single pair of wings. family of flies, containing both highly specialised types which APPEARANCE attack only a single or narrow range of species, as well as Eggs: The eggs of tachinids, the most important group of generalists which attack a much wider range of species. As with parasitoid flies, can sometimes be seen with the naked eye on parasitoid wasps, it is the larval stages of parasitoid flies that their hosts such as caterpillars and beetle larvae. The eggs are attack other insects (and occasionally other arthropods) and it tiny (less than 1 mm in length), white or off-white in colour is difficult to evaluate their population impact without detailed and oval in shape. Some tachinids lay their eggs on leaves study. Generally, parasitoid flies have not been as well studied rather than directly on the host body. Larvae and pupae: Eggs normally hatch on the host body and as parasitoid wasps. However, their short generation time larvae then burrow through the body and feed internally. With means that populations can build-up rapidly. On farms where species that lay their eggs on foliage, eggs or young flattened CONSERVATIONthese flies are found to be numerous, it is likely that they are larvae (called planidia) are ingested by caterpillars or other Ensureexerting adequate, important sugar-containing regulatory pressure food sourceson pest arepopulations. pests whose body contents provide a food source for the available for adults, such as flowers, plant sap or honeydew. developing larvae. Parasitism nearly always results in death of Encourage habitat diversity, as for parasitoid wasps (see the host insect. Pupation occurs either within or outside the Parasitoid Wasps; Conservation: p. 73). Adults:body Theof their adult hosts. flies Somelook rather species similar pupate to incommon the soil. flies such Avoid spraying pesticides unless absolutely necessary. as house flies, flesh flies or blow flies, but they are more robust Should spraying be considered necessary, use a product and and hairy (or bristly) than house flies, typically being between application method that is the least harmful to key natural 8 – 12 mm in length. Their most identifiable feature are the enemies (see Parts 3.2 and 3.3 of this guide). long and short bristles usually clearly visible on the abdomen (Picture 84). Their bodies are often grey in colour, with 78 Pathogens Pathogens 79

The most important naturally-occurring disease causing anisopliae. At particular times of year, other genera of fungi Pathogens pathogens of vegetable pests are generally fungi and viruses. such as Zoophthora and Entomophthora can be readily Pathogens These disease organisms tend to be more common during rainy encountered in the field infecting pests such as caterpillars seasons, are difficult to manipulate and they may be and aphids. unpredictable as to their presence or effect. However, on occasions, disease outbreaks will occur and over a very short Baculoviruses period, can cause complete collapse of pest populations. Many A wide range of viruses pathogens (e.g., granulosis viruses, certain bacteria and fungi) specific to insects, known are highly specific to particular pests. The primary pathogens as baculoviruses, have been which attack insects are specific to insects and closely related identified in wild populations arthropods and cannot cause disease in unrelated organisms of insects and some have been such as humans. Entomopathogenic fungi multiplied in sufficient Fungi, when sporulating, quantity to be used as usually cause their insect ‘biological pesticides’. host to become covered in Virus-infected insects, notably a cream-coloured (Picture caterpillars, tend to be found 85), green, red or grey more commonly in heavy coloured mould. Aphids, caterpillars and a wide infestations, particularly during 86. Left: A healthy range of other pests may prolonged wet seasons. The diamondback moth larva (fourth and final larval instar). be found infected by fungi. two most common types of Right: a fourth instar Spores are transferred on 85. Left: Fungal infected baculovirus encountered are diamonback moth larva in the insect bodies, in rainwater diamondback moth caterpillar species-specific granulosis late stages of infection by PxGV or in the wind, and hyphae (Zoophthora sp.). Right: healthy caterpillar viruses (GVs) and nuclear (fungal strands) enter the polyhedrosis viruses (NPVs). insect body via openings Recent investigations in Kenya (e.g., breathing holes, anus). have been carried out to assess The fungal hyphae or mycelia develop and consume the insect from the inside. Signs the potential for using a GV specific to the diamondback moth of infection tend to be quite easy to find during sustained wet (PxGV) in brassica crops. Infected larvae typically appear pale or humid conditions, such as those found during rainy seasons. and swollen (Picture 86), and the development of the final Considerable research is on-going to develop biological instar is delayed considerably. Infected insects usually die prior pesticides based on fungal pathogens, particularly Metarhizium to adulthood and turn brown or black after death owing to secondary infection by bacteria. NPVs, such as the soya-bean Pathogens 80 bollworm ( such as diamondback moth( commercially foruse against caterpillar pestsofvegetables Several formulations ofvarious Btproducts are available is themost well-known bacterialpathogen ofinsects. occurring bacterium, foundbothinthe soilandonplants, and highly effective against their target pests andhave little orno brown orblack anddie. be foundinthefield.Following infection,theygenerally turn Insects suchascaterpillars infectedby bacteriacansometimes Bacteria or commercial virus production. same wayas conventional pesticides, is thecostofsmall-scale pesticides’, whichcanbeapplied toinfectedcrops muchinthe use ofviruses as‘biological constraints tothesustainable body. One ofthemain and replicate withintheinsect (unlike fungi)inorder toenter Viruses needtobeconsumed particles (Picture 87). liquid, charged withvirus contents havingturnedto hanging from leaves, thebody caterpillars tendtobefound and heavilyinfectedordead become flaccid(weakandsoft), caterpillar’s cuticle(skin) to Zimbabwe, oftencause the semi-looper virus used in Helicoverpa armigera Pathogens Bacillus thuringiensis Plutella xylostella ). These products tend tobe Resources Institute, UK) (Photograph courtesyofNatural Polyhedrosis Virus(NPV) soya, killedbyaNuclear 87. A semi-loopercaterpillaron ) andAfrican (Bt) is anaturally nematode: the bodiesofinsects killed by bacteria oftenprovides auseful cluetothegenus of Heterorhabditis (endotoxins) produced by various subspecies ofthebacterium. specific insecticidal effectis caused by toxic proteins and natural enemies(seePart 3.2,p.91). Theoftenhighly insecticides are someoftheleastharmfultoother arthropods formulation, orifpresent, theyare notliving.These either thebacterialcells themselves are notpresent withinthe they cannotberegarded properly asbiologicalagentssince same variety ofways asconventional insecticides. However, products canbeappliedwithspraying equipmentinthe Bt shortly afterexposure, sodramatically reducing crop damage. several days todieafteringestingtheproduct, itstopsfeeding effect onnatural enemies. Althoughacaterpillarmaytake species ofbacteria: symbiotic (mutuallybeneficial) relationship withparticular known asa by aspecialised third stagejuvenile (about1mminlength), Heterorhabditis belong totwogenera: Kenya, withthepurposeoffindingvirulentisolates. EPNs Recent surveys have beencarriedoutinbothZimbabwe and roundworms thatcanusually onlybeseenunderamicroscope. lighter soils andincoastalareas. Theyare small, long,thin EPNs are foundinsoils allover theworld,particularlyin Entomopathogenic nematodes(EPNs) released from thenematode intothebodycavity oftheinsect, Photorhabdus typically yellow toorange incolour whilethosekilledby dauer larva species canbebrightred. Thesebacteriaare . Theinsect hostis actively infectedinthesoil with Steinernema Photorhabdus Steinernema (or Pathogens infective juveniles with species. Infection by these (Picture 88)and Xenorhabdus Xenorhabdus ). EPNshave a species and are 81

Pathogens 82 Pathogens Evaluation of natural enemies, Pathogens and pesticide selectivity

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3.1 An introduction to natural enemy evaluation 84 3.2 Pesticide side effects on natural enemies 91 88. Entomopathogenic nematodes [infective juveniles] (Steinernema 3.3 Selective pesticide application 103 carpocapsae) emerging from their dead Spodoptera caterpillar host in search of new hosts

multiply rapidly and kill the host within 48 hours by septicaemia. The nematodes feed on the bacterial cells and host tissues, develop and reproduce. When food supplies run out, 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 is not well understood. However, EPNs can be mass produced on a commercial scale on solid or liquid media and in a number of countries around the world are now used as ‘biological insecticides’ against a variety of insect pests (especially caterpillars and beetles). EPNs are regarded widely as being very environmentally friendly with no adverse side effects reported. Part 3.1 84 below: plants vary from oneassessment tothe next are considered major reasons why thenumbers ofnatural enemies foundon with howthe countdataare theninterpreted. Someofthe point ofanevaluation. However, there are numerous problems Counts ofnatural enemies(andpests) are oftenthestarting Evaluations ofabundanceinthe field and itis tothesethatwe nowturn. those involved inpest management decisions atthefarm-level some importantprinciples ofthis typeofworkare relevant to appropriate fortheextension workerorfarmer. Nevertheless, specialised personnel over longperiodsoftime,andare not require detailedlaboratory andfieldinvestigations by highly movement rates andnumerous otherfactors. Thesemethods egg production, consumption rates, lifespan, development time, natural enemyeffectiveness involve studiesof natural enemy Many ofthemethodsnowbeingused by researchers toassess Principles offieldevaluation information onsomecommonshortcomings of evaluations. has already beencollected.Itserves particularly to provide in mindwhencarryingoutevaluations orinterpreting data that outline someoftheimportantprinciplesthatneed to beborne biological control ofpests. This partoftheguide aims to become amajorfocus forresearchers working inthefieldof enemy evaluation is complexandonethathasonly recently natural enemiesonspecific pests. Thewholesubject ofnatural meaningful judgementsontheeffectiveness ofdifferent provide you withenough informationtobeablemake counting thenumbers ineachofthetwocategories willnot Being abletodistinguish natural enemiesfrom pestsandthen Background An introductiontonaturalenemyevaluation 3.1 NaturalEnemyEvaluation over time Figure 1. Population fluctuations. a) Numbers of arhropods observed compared withalaterassessment at time 2( very different picture ofnatural enemyabundancewouldbe was undertakenandthis wascarriedoutattime1 ( graphically inFigure 1.Therefore, ifonlyasingleassessment during evaluations. abundance, so therole ofthesemust betakenintoaccount contribute to fluctuations ofpestand natural enemy pesticides or cultural manipulations, willalso tendto Management practices, whichmay include applications of this is oftencarriedout atweeklyortwointervals. pests throughout thecropping season.Indetailedstudies, This demonstrates the needtoevaluate natural enemiesand and natural enemypopulationfluctuations. This is shown availability offood,there is oftena‘timelag’between pest since manynatural enemiesmultiplyinresponse tothe fluctuation astheirhostsorprey (i.e.,pests).However, time because manypopulations followasimilarpatternof Typical fluctuationsofpestandnaturalenemyabundance 3.1 NaturalEnemyEvaluation tt 12 Natural enemynumbers vary over enemies Natural Pests t 1 ), a t 2 Time ). 85

Part 3.1 Part 3.1 86 )Biasfromassessors. d) Effectsofcrop growthstage. c) Assessmentsatdifferenttimesoftheday. b) example, visual counts may beuseful forparasitoid cocoons different techniques are required fordifferent organisms; for each of aseriesofassessments onagiven crop. Also records foraccurate assessments, should be selectedfor of individuals withknownidentification skills andtrack means that,asfarpossible, thesame individualorgroup the accuracy ofdatacollectedby different individuals. This rather than younger plants. of natural enemies beinghiddeninplantpartsofolder much larger, butalso because there is agreater possibility enemies bothbecause the surfacearea oftheplantbecomes it canbecomeprogressively more difficulttolocatenatural the same timeofeachday. over time,itis important toaimcarryoutassessments at late afternoon.Iftheintentionis toassessrelative numbers undertaken undercalmconditions intheearlymorningor assessments ofmostnatural enemiesare often best high middaytemperatures orstrong winds. Generally, active onmornings andafternoons andmaybe deterred by the plants. Adult parasitoids, forinstance, are generally most such asweatherconditions, temperatures andconditionof numbers. Natural enemiesare also affected by otherfactors in themiddleofdaywilltendtovastly underestimate beetle are particularlyactive atnightsoassessments made example, larvae ofmanyspecies ofhover flyandladybird for prey orhostsatspecific timesofdayornight.For This is because natural enemiesare more visible, orsearch of dayrather thantogenuinedifferences inabundance. assessments couldwellbeattributedtothedifferent times differences innumberofnatural enemiesbetween day, 12.00 middayonanotherand6.00pmyet another, of natural enemynumbers is undertakenat8.00 amone 3.1 NaturalEnemyEvaluation There canbe substantialvariation in As acrop grows and matures, If anassessment )Concealed lifestages. e) )Variable durationsofexposure tonaturalenemies. f) used forground-dwelling predators. or aphid‘mummies’,whilepitfalltrapping is commonly parasitoids. In addition, care must be taken tonot include cropping cycle. This principle appliesto allhostsand at regular intervals (e.g.,two-weekly) throughout the laboratory. This type ofassessment is normallycarried out that are killed by parasitoids when reared through inthe instar caterpillars anddeterminethe proportion ofthese Accordingly, itis more appropriate tocollect onlyfourth that eachwill have beensusceptible toparasitism. otherwise there willbe variations intheamountoftime from thefieldthesemust notbeofmixed ages(instars), final (fourth)instar. Therefore, ifcaterpillars are collected and third instars and are rarely parasitised inthefirst or particularly susceptible to endoparasitism intheirsecond parasitoids. For example, diamondbackmothcaterpillars are parasitoids) have hadthe same periodofsusceptibility to removed from thefield(andtherefore from exposure to With suchmethods, itis criticalthatthehostsare through inthelaboratory orothercontrolled environment. by collectingpotentialhosts from thefieldandthenrearing A methodcommonlyused forassessment ofparasitism is pupation. larvae emerge from orconsume theirhostsjust priorto caterpillars, noevidenceofattackis revealed untilparasitoid until eachaphidbecomesmummified,whilewith the caseofparasitised aphids, there are no outward signs of parasitism untiltheparasitoids reach the pupalstage.In (p.68),donotshow anyobvious evidence endoparasitoids example, aphidsorcaterpillars whichare attackedby attack untilthelaterstagesofparasitism orinfection. For the bodiesoftheirhoststhatshow nooutward sign of notably parasitoids andpathogens, canbeconcealedwithin 3.1 NaturalEnemyEvaluation Some lifestagesofnatural enemies, 87

Part 3.1 Part 3.1 88 therefore 30,000 (75x400),whichis600 timesgreaterthanthatof period. The larval capacity toconsume 400aphidsduringits average12-day hatch ratefrom theseeggsis75%,andeach oftheselarvaehasthe The Species A(i.e., 100)onleavesclosetothe coloniesofSpeciesX. (about 30days), laystwicethenumberof eggs comparedwith by ageneralised example given below. prey consumed by thenatural enemy),this being demonstrated most importantparameters is and withinspecies atdifferent timesandplaces. Oneofthe cycle parameters betweendifferent natural enemies species, enemies. This is because ofthevery great variations inlife indication oftherelative effectiveness ofarange ofnatural above factors have beentakenintoaccount,donotprovide an Counts ofarthropod natural enemiesalone,even whenthe Species A. means thateachfemalehas a adult lifespan,eachbeinglaid withinanindividualhostaphid.This fertilised femalewaspofAcan layupto50viableeggsduringits parasitoid wasp,whileSpecies Bisahoverflypredator. Eachadult, natural enemy, thesebeingdesignated asAandB. SpeciesAisa The importanceofvoracity: ageneralisedexample Species Bontheotherhand, althoughhavingthesamelifespan An aphid pest, Species X, ispreyedonbytwokeyspeciesof An aphidpest,SpeciesX, excluded from counts. from whichwasps have already emerged should also be compared withun-mummifiedaphids, mummified aphids parasitism by periodicassessments ofmummifiedaphids included intheassessments, or, whenevaluating aphid eggs laidonacrop over time,hatchedeggs should notbe example, whenassessingnumbers ofhover flyorlacewing remnants ofprevious lifestagesinassessments. For 3.1 NaturalEnemyEvaluation ‘ killing potential ’ ofonefertilised femaleofSpeciesBis ‘ killing potential voracity (the numberofhostsor ’ of50aphids. enemies Table 2. enemy anditshostsorprey) are listed inTable 2. parameters (whichmust bedeterminedbothfor thenatural biological control. Manyofthemostimportantlife cycle but this doesnotnecessarily detract from their importancein difficult tomeasure inthefieldandhave beenpoorly studied, assessments ofnatural enemyeffectiveness. Some oftheseare There are manyotherfactors thatcanbeimportantin are sprayed. be considerably more rapid than whenrelatively large areas result, ‘recovery’ of natural enemypopulations willtendto by thosethat immigrate from nearby untreated areas. Asa species that are killed are likelyto bereplaced relatively quickly the natural enemies mayappearrelatively unharmedbecause sprayed withabroad spectrum pesticideandis thenevaluated, can readily move inoroutofthestudyarea. Ifasmall area is this, one being thatnatural enemiesare oftenhighlymobile so important bearingonthe results. There are manyreasons for over whichnatural enemiesare evaluated willhave avery Finally, andcertainly not least,thesizeofarea (scale) Immigration rate G RPE PS)PRMTR NATURAL ENEMYPARAMETERS EGG ORPREY(PEST)PARAMETERS dl otlt Eggmortality Voracity (consumptionrate) Adult mortality Juvenile mortality Development time Fecundity Emigration rate Important lifecycleparametersinrelationtonatural 3.1 NaturalEnemyEvaluation Adult mortality Juvenile mortality Fecundity Development time Emigration rate Immigration rate 89

Part 3.1 Part 3.1 90 types are present andevaluating their pitfalls asconsidered above, recognising whichnatural enemy In themeantime,takingintoaccountsomeofpotential natural enemies. farmer-participatory evaluation oftheeffectiveness ofkey presently underdevelopment, willprovide thebasis for It is anticipatedthatinthefuture, somepractical methods, be obtainedorinferred. some informationontherelative value ofnatural enemiescan principles given here mightbehelpfulatthefarm-level sothat scope ofthis section.However, itis hopedthatsomeofthe for given crop-pest-natural enemycombinations is beyond the implemented. Therange ofmethodologiesthathave beenused appropriate methodsofevaluation canbedeveloped and environmental factors, whichneedtobeconsidered before influence ofclimate,prevailing weatherandotherspecific of natural enemiesandtheirhostsorprey, aswelltothe There are alarge numberoffactors thatrelate tothebiology Conclusions manipulation underinvestigation. except that theydonotincludethespecific ‘treatment’ or should becomparable to the‘treatment’ areas inevery way ‘controls’ are includedinthesestudies. Thesecontrol areas experimental technique,it is essentialthatappropriate be assessedingeneral terms inthis way. Aswithany impacts, particularlywhether theyare positive ornegative, can different impactsonnatural enemies, andthenature ofthese over time.Different managementpractices willtendtohave information ontherelative abundanceofeachnatural enemy several pointsduringthe cropping cycle should provide useful 3.1 NaturalEnemyEvaluation relative numbers at Pesticides maykillorharmnatural enemiesfollowingexposure routes ofexposure. indirect between humans. Itis therefore importanttoappreciate thedifferences exposure ofnatural enemies aswellotheranimals, including to asbeingsublethal,andtheyare commonwith pesticide effect doesnotleaddirectly todeath.Theseeffects are referred working. Suchaproduct is mostcertainlyharmful,butits accidentally itthenmakesaperson illandprevents themfrom surely couldnotbedescribedasharmless, ifwhenswallowed necessarily true.Byanalogytoahumanexample, aproduct enemy must thenbeharmlesstothenatural enemy. This is not It is oftenthoughtthatapesticidedoesnotkill anatural Lethal andsublethaleffectsofpesticides less severe, compared with that oflethal effects. natural enemiestends tobefundamentally similar, although The behavioural or physiological nature of sublethaleffects on are thoseeffects thatoccurinthepesticide-exposed survivors. while others maysurvive beyond that period.Sublethaleffects generally diewithinarelatively short period(e.g.,48hours) pesticide over arange ofdoses, somenatural enemieswill For agiven population ofnatural enemiesexposed toa are used atlowdosages. Figure 2)particularly iftheyare selective against thepestsor pesticides cansometimes enhance natural enemyfunction(see effects ofpesticidesonnatural enemiesare oftennegative, and preening behaviour(notablyinparasitoids). Althoughthe usually less-developed enzyme-baseddetoxification systems prey owingtotheirgenerally smaller size,searching habits, to theeffectsofpesticides thantheirplant-feedinghostsor their hostsorprey. Natural enemiesare usually more susceptible also affectnatural enemiesindirectly by killingorcontaminating by contact,ingestionor, lesscommonlyby respiration. Theymay effects andunderstand somethingaboutthepossible lethal 3.2 SideEffectsofPesticides and sublethal effects, between direct and 91

Part 3.2 Part 3.2 92 limit theabundance ofhostsorprey (i.e., pests). which willin turn affectthecapacityof natural enemiesto they willgive rise toeffectsonnatural enemypopulations are oftendifficult. Where sublethal effects occurinthefield, are used by different researchers, comparisons betweenspecies laboratory butbecause awiderange ofexperimentalprotocols effects (Table 3).Sucheffects maybemeasured inthe sub-divided intotwogroups: behavioural andphysiological As mentionedabove, sublethaleffectsmaybegenerally enemies Figure 2. exposure willinfluencetheseverity oftheeffect. persistence intheenvironment andthenatural enemy’s the pesticidetoagiven natural enemy, thepesticide’s not atall(Figure 2).Factors suchastheinherent toxicity of populations positively ornegatively orsometimes apparently rise toacontinuumofeffectsthataffectnatural enemy even indirect from direct effects. Assuch,pesticidesmaygive often notpossibletoseparate lethalfrom sublethal effects, or natural enemies(atthepopulationorcommunity level), itis In fieldstudiesthatattempttoassesspesticideimpacton Positive Effects Continuum ofpossiblepesticide effectsonnatural 3.2 SideEffectsofPesticides Sublethal Effects EFFECT ZERO Negative Effects Lethal Effects MORTALITY 100% pesticides Table 3. on otherbiologicalcontrol agents. populations, have thepotentialtocause negative sideeffects such asentomopathogenicfungiused totarget pest It should also beborneinmindthatbiologicalcontrol agents, multitrophic context. chemical andbiological controlsystems forarthropods: evaluation ina 1 Adapted from:Wright, D.J. &Verkerk, R.H.J. (1995) Review -Integration of osmto Deformation Foraging/Parasitism Repellency PHYSIOLOGICALEFFECTS Consumption Locomotion Communication BEHAVIOURAL EFFECTS Spectrum ofsublethaleffectsonnaturalenemiescausedby 1 3.2 SideEffectsofPesticides • • • handlingtime oviposition searching Pesticide Science, 44: Reproduction Vigour Longevity Voracity/Consumption/Parasitism Development time 207-218 • • fertility fecundity . 93

Part 3.2 Part 3.2 94 only occasionally. impacts may not bedetectableonindividual farms sampled may occuron large spatial scales. This means thatpesticide ecological communitiesmay have long-termconsequences and pesticides onpestandnatural enemypopulations withinagro- Finally, itis importanttobearin mindthattheimpactof Figure 3. parasitoids (Figure 3). natural enemiescanhave profound effectson predators and application, thechangeinamountoffoodavailable for these populations are depletedoreliminatedby pesticide pesticide mighthave onpest(prey orhost)populations. If Another formofindirect effectresults from impacts thata example onleaves, oritis consumed viatreated hostsorprey. pesticide is eitheraccumulatedfrom residual deposits, for indirectly droplets orparticlesofthepesticide,theycanbe exposed directly Insects andothernatural enemiescaneitherbe exposed Pesticide exposure otepsr Indirect Direct(topical) Host exposure Natural enemyexposure Natural enemyexposure , withthenatural enemycomingintocontactwith Important typesofnaturalenemy exposuretopesticides (Figure 3).Inthecaseofindirect exposure, the 3.2 SideEffectsofPesticides nietDietary (Population/community effects) Indirect Residual relationships are shown by thefollowingtwo simpleformulae: pesticide’s basically afunctionofits from thepointofviewnatural enemy, exposure when theadultstageofanimportantparasitoid of abroad-spectrum (non-selective) insecticide duringatime considerably withboth timeandscale.For example, application include bothlivingandnon-livingelements, are likelytovary conditions underwhichitis used. Theseconditions, which In itssimplestform, enemy mightberelatively unimportantonalarger scale. application), thenegative impactofthespray onthenatural enemies, ifitis sprayed selectively (e.g.,spot orbarrier although thepesticidemayhave localised impacts onnatural by suppression ofthe natural enemy. Ontheotherhand, the When evaluating theimpactofpesticides, weneed toconsider Risk ranking ofrisk foragiven pesticideapplication in aparticular rate of immigration ofthenatural enemy. Asaresult, the as thepersistence ofthepesticidein theenvironment and the will bearecovery phase.Recovery willdependonsuch factors application of apesticide,butfollowing this depletionthere amount that a natural enemypopulation is depletedafterthe short-term However, there are oftensubstantial differences between abundant mayresult in resurgence ofpestpopulations risk of using apesticideundertheparticularrange of and toxicity 3.2 SideEffectsofPesticides and Hazard =f(exposure+toxicity) Risk =f(exposure+susceptibility) susceptibility long-term to thenatural enemyinquestion.These risk should beseenasafunctionofboth exposure risks. risks. of thetarget organism. Lookedat Short-term risks includethe to thepesticideand hazard species is is caused 95

Part 3.2 Part 3.2 96 ‘harmless’ to the same natural enemies underfieldconditions. conditions, thelikelihood is thattheproduct willalso be ‘harmless’ to a range of natural enemies undertheselaboratory those followingtheIOBC protocols) show aproduct tobe large-scale ri field, andtheygive noindicationofpossiblelong-termor higher exposure rates than thosenormallyencountered inthe appreciated thatthesedata reflect effectsfollowingmuch should therefore beinterpreted withcaution.Itshould be 100), those produced by some pesticidemanufacturers (e.g.,p. enemies, suchastheone given inthis guide(pp.98-99)or field. Datafrom anytable ofpesticidesideeffectsonnatural considerably greater thanthoseusually encountered inthe recommended fieldrates underconditions where exposure is enemy groups. Thepesticidesare used atthe maximum against arange oforganisms from themostimportant natural specific pesticidestobetestedunderstandardised conditions (see pp.98-99),is thattheyallowtherelative toxicity of by theInternationalOrganisation ofBiologicalControl (IOBC) The advantage ofstandardised laboratory experiments, asused laboratory experiments, notfieldstudies. data onwhichthis informationare basedis takenlargely from pesticides mightbelesshazardous tonatural enemies. The guide aims tohelpextension staffandtrainers decidewhich are available tothemcommercially. This sectionofthefield forced touse oneormore ofalimitedrange ofproducts that long-term ri There are very fewdatagenerally available on short- or short-term andlong-termimpacts. agro-ecosystem willoftenbedifferent whencomparingthe 3.2 SideEffectsofPesticides sks, and most most and sks, sks. sks. However, ifproperly conducted tests(suchas farmers orpestmanagers are usually pesticide application (Part 3.3). additional selectivity canbeachieved by selective and judicious Apart from the intrinsic selectivityof agiven product, some 14). unforeseen problems includinginsecticide resistance (see p. natural enemy group inPart 2),asover-use canleadtoother should beused judiciously (see rarely harmlesstoall non-target organisms. Allpesticides However, even products that are classifiedas‘harmless’are very products (e.g., compared withnatural enemiesare referred toasselective Products thathave different intrinsic toxicities topests form oftheSELCTVdatabase (see made by workers atOregon StateUniversity intheUSA, journals. An attempttocollatethis published workhasbeen Where dataare available theyare containedin scientific not available formanypest/natural enemy/crop situations. type ofinformationis generally muchharder to comeby andis provide dataonrisk orhazard ofthesepesticidesinuse. This specific natural enemies, asdiscussed above, theydo not useful informationon differences betweenthepesticides. Althoughthe dataprovide pesticides by arange ofkeynatural enemiesas wellasshowing The dataaimtodemonstrate boththevariability ofresponse to or Kenya duringsurveys carriedoutforthepresent work. includes allthemainpesticidesfoundtobeused inZimbabwe harmless tomanyspecies ofnatural enemies. The table includes afewnewerhproducts thatare knownto berelatively commonly used insecticides andfungicides. The tablealso relative toxicity toarange ofnatural enemiesofsome The tableoverleaf aims toprovide someinformationonthe on NaturalEnemies Introducing theTable ofPesticide SideEffects 3.2 SideEffectsofPesticides Bacillus thuringiensis relative toxicity ofdifferent pesticidesto Conservation SELCTV Database [Bt] basedproducts). under each , p.100). 97

Part 3.2 98 3.2 Side Effects of Pesticides 3.2 Side Effects of Pesticides 99

INSECTICIDES AND FUNGICIDES Part 3.2 Part ACARACIDES 3.2 Part Actellic (Pirimiphosmethyl) Ambush (permethrin) Applaud (bupofrezin) Basudin (diazinon) Dipel (Bacillus thuringiensis) Cymbush (cypermethrin) Decis (deltamethrin) Folithion, Sumithion (fenitrothion) Karate (lambda cyhalothrin) Kelthane (dicofol) Mitac (amitraz) Pirimor (pirimicarb) Rogor (dimethoate) Sevin (carbaryl) Sumicidin (fenvalerate) Thiodan (endosulfan) Trigard (cyromazine) Antracol (propineb) Dithane M45 (mancozeb) Neviken (lime-sulphur) Thiovit (sulphur) Vitrigran (copper oxychloride)

Parasitoid Egg Trichogramma Wasps Parasitoid cacoeciae

Larval Encarsia Parasitoid formosa ? ? ?

Larval Leptomastix Parasitoid dactylopii ? ?

Predators Mite Phytoseiulus persimilis ? ?

Spider Chiracanthium mildei ? ? ? ? ? ? ? ? ? ? ? ? ?

Lacewing Chrysoperla carnea

Hoverfly Syrphus vitripennis ? ? ? ? ?

Ground Pterostichus beetle melanarius ? ? ? ?

Rove Aleochara beetle bilineata ? ? ? ? ? ? ? ?

Pirate bug Anthocoris nemoralis ? ? ?

Pathogens Fungi Verticilium lecanii ? ? ? ? ? ? ?

Estimations made from data available in SELCTV database These data are based on laboratory tests carried out according to International Organisation for Biological Harmful (adverse effects* in 99% tested). Control (IOBC) protocols between 1983 and 1998. Laboratory testing exposes the test organism to higher Moderately harmful (adverse effects* in 80-99% tested). levels of pesticide than would normally be experienced in the field. The tests consider the impact of each pesticide on mortality (death rate) and sometimes include a range of sublethal effects such as effects on Slightly harmful (adverse effects* in 50-79% tested). egg production. The effects of mixtures of pesticides are not tested. The IOBC supports a sequential testing system that includes up to three basic levels of testing: laboratory, semi-field and field. The basic ? No test results available assumption made is that since exposure is highest in the laboratory and least in the field, if a pesticide is Harmless (adverse effects* in less than 50% tested). shown to be ‘harmless’ in the laboratory, it is likely to be harmless in the field. If it is shown to be ‘slightly harmful’, ‘moderately harmful’ or ‘harmful’ following one test, further testing is required, at the next *In most cases the tests only measure mortality (death rate). successive level of exposure (i.e., extended laboratory test, semi-field test or field test). Part 3.2 100 http://www.ent3.orst.edu/Phosure/database/selctv/selctv.htm experiments. Thewebsiteforthedatabase is: published literature, includingtheresults of manyfield SELCTV (pronounced natural enemies. Access is againfree. Itis known asthe database dealing withsideeffectsofpesticides onarthropod Also requiring accessto theInternetis acomprehensive SELCTV Database included inthecomparative literature study. experience. More thanone hundred scientificpublications were other published research, aswellKoppert’s ownresearch and IOBC WorkingGroup ‘Pesticides andBeneficialOrganisms’, each product. Theinformationis basedonthe results ofthe well asadultinsects andincludeestimatesofthe persistence of enemies (andbumblebees).Dataare provided forimmature as toxicity andpersistence against arange ofimportant natural insecticides, acaricides andfungicidescompare their it. Thedatabaseallows you toselectfrom awide range of go through asimpleregistration process the first timeyou use You canaccessthedatabasefree of charge, butyou needto http://www.koppert.nl/english/service/index.html which is accessibleontheInternetatfollowing website: Zealand. Ithasdeveloped avery useful SideEffects Database France, Italy, Spain,theUSA,Canada,Mexico,Turkey andNew Netherlands, butthecompanyalso hasofficesin England, Koppert’s headquarters andprincipalresearch baseis inthe production ofbiologicalcontrol agentsandpollinators. Koppert is oneoftheleadingcompaniesinvolved inthe Koppert SideEffectsDatabase 3.2 SideEffectsofPesticides selective ) databaseand itis basedon [email protected]. Corvallis, Oregon 97331-2907, U.S.A;email: of Entomology, Oregon StateUniversity, 2046Cordley Hall, For more informationcontact:DrPhilHeneghan for bothresearch anddecision-making inpestmanagement. continuously updated,unbiased,international resource useful The databasedevelopers aimtocreate aself-funding, choice before asearch is run. insert thepesticide,crop, countryandothercriteria ofyour published sources forthedata.Thedatabaseallows you to response, 5=>90% response). Links are provided tothe 2 =<10% response, 3=10-30% response, 4=30-90% An ‘average toxicity rating’ system is used (1=noeffect, conditions describedinthesource publication. effects ofapesticideononenatural enemytaxon under widely used. Eachrecord intheoutputtablerepresents the particularly useful forolder pesticides, manyofwhichare still the records originatefrom thepre-1986 literature. Itis thus 1921 to 1994, althoughatthetimeofwritingmajority pesticide effectsonnon-target arthropods. Records datefrom worldwide, from approximately 12,500datarecords describing comprehensive compilationoftheliterature published Corvallis (Oregon, USA.).Thedatabaserepresents arelatively Department ofEntomologyatOregon StateUniversity, Development ofthedatabasebeganin1986/87 snake beans), while others are from exotic plantsnow growing indigenous tothe region (e.g., Zimbabwe. Some oftheseproducts are derived from plants some smallholder ororganic growers indifferent partsof About 20pesticides extracted from plants are used widely by Note on UseofBotanical Pesticides 3.2 SideEffectsofPesticides Schwartzia madagascariensis Department , 101

Part 3.2 Part 3.2 102 organisms, theiruse should beavoided. botanical pesticidestonatural enemiesandothernon-target body ofevidencedemonstrating theharmlessnessofspecific be treated asbeingofunknownhazard. Unless, there is agood organisms, includingnatural enemies, thesepesticides should pesticides against bothmammals andothernon-target Until reliable dataare available onthesideeffects ofbotanical pesticides. mammals aswelltoarthropods, thanmany synthetic leaves) maybemuchmore broadly toxic, tohumans andother botanical pesticides(e.g.,nicotineextracted from tobacco pesticides. From theavailable data,wedoknow thatsome or researchers inthesame wayassynthetically-produced on-farm, have notbeenscrutinised by registration authorities pesticides, whichare oftenextracted from botanical products are onthewholevery limited.This is because, asyet, botanical natural enemies, thedataonwhichtheseconclusions are based might bequiteselective against pestsandrelatively harmlessto Although there is someevidencethatbotanical products extracts (e.g.,manypyrethrum products). in Zimbabwe(e.g.,tobacco)orfrom importedplantpartsor 3.2 SideEffectsofPesticides Manyangarirwa, Joshua Karuma andWilfred Chiimba). Zimbabwe’ (authored by Hans Dobson,JerryCooper, Walter manual entitled‘Integrated Vegetable Pest Managementin information onthis subjectcanbefoundinacompanion can bemanipulatedtohelpreduce non-target effects. Further There are five importantaspects ofpesticide application that by judicious pesticideapplication. organisms suchaspollinators, furtherselectivitycan begained harmful tonatural enemies(Part 3.1)andothernon-target Apart from selectingpesticidesthatare likelyto be less Selective pesticideapplication (even less forsmall oryoung crops), inthe range known as apply water-based sprays at rates between 200and 400l/ha smallholder, tropical vegetable systems, operators should ideally minimised. For control ofmostvegetable pestsanddiseases in sprayers andnozzles, volumes ofpesticides used canbe By careful targeting anduse ofgood quality, calibrated calibrated sprayer, andappropriate nozzles. of thepest,anexperienced applicator, agoodquality, targeting ofspray requires athorough knowledgeofthe habits natural enemies, which oftensearch allpartsofplants. Careful excessive doses. Inaddition, suchtreatments willbeharmfulto exposure ofthepest,or to beeffective, mayrequire use of spraying theuppersurfaceofleaves mayresult ininsufficient out’ prey. Manypestsare present ontheunderside ofleaves, so disrupt natural enemiesthatmayotherwise beableto‘search application maybeineffective, wastefulandmay simply concealed withinstems orfruitshiddenwithincurledleaves, required doseofaninsecticide, forexample because thepestis If thepest(inanyofitslifestages)cannotbeexposed tothe Minimise the volumeapplication rate Target thespraycarefullyontopest 3.3 SelectiveApplication 103

Part 3.3 Part 3.3 104 natural enemies). such as theseverity oftheinfestation andprevalence of the sprayed and untreated bandsbeing dependenton factors applying bands oftreatment through acrop, thewidthof substantial pest infestationonly)orstrip spraying (i.e., techniques include spot spraying (i.e.,targeting areas of reduced considerably by selective spraying techniques. These actual volume application rate perhectare ofcrop canbe calibrated toapplyarate ofbetween200and400l/ha,the fan andothertypesofnozzle. Althoughthesprayer maybe capable ofachievingthis, butitis difficulttoachieve withflat Knapsack sprayers fittedwith asmall hollowconenozzleare centimetre ofinfestedfoliage provides reliable control. diameter ofanappropriate formulationoneachsquare situations, 5-15small droplets ofaround 100 -300µmin not involve spraying tothepointofrun-off.For many foliage involves depositionofsmall discrete droplets anddoes coverage formostapplications targeting vegetable pestson enemies andothernon-target organisms. Themostefficient the target andcanleadtoundesirable impactson natural wasteful, prevents muchofthepesticidebeingdeposited on diameter) inaspray mayleadtopesticidedriftwhichis proportion ofvery finedroplets (lessthan100 µm[microns] in be varied according tothetypeofapplication.Asignificant spray is very important forefficientapplicationandneedsto required doseofthepesticideitself.Thedroplet sizeofthe spraying means the operator is oftenapplyingmanytimesthe assumption oflowervolume applicationrates, HighVolume since tankconcentrations are usually calculatedonthe that are ground-dwelling orhave asoil-basedlifestage.Also, plants andadversely affectsawiderange ofnatural enemies than lowervolume applications -theexcess liquiddripsfrom wasteful andmaycause greater exposure ofnatural enemies operations actuallyuse HighVolumes ofover 1000 l/ha.This is Medium Volume spraying. Incontrast, manyspraying 3.3 SelectiveApplication early morningorlateafternoon. conditions forspraying are usually mostlikelytooccurinthe sunlight through pesticide/waterdroplets. Optimum weather intense sunshine thatcanoccurby magnificationofthe droplets beingcarriedby wind,orscorching offoliageby selected toavoid therisk ofpesticidedriftcaused by very small factors must also betakenintoaccount.Conditions must be sometimes avoiding thehottesttimesofday. However, other more likelytobesearching plantsduringthedaytime, to thepesticide.Othernatural enemies, suchas parasitoids, are most active atnight,sospraying atdawnmightexposemore natural enemieslikehover flyand ladybird beetlelarvae are lowest chanceofadversely affectingnatural enemies. Some out atatimeofthedayoreven seasonwhenthere is the If itis decidedthatspraying must occur, makesure itis carried which make most plants toxic tomost plant-eating arthropods. pest that have evolved tocope withsecondary plantproducts, presence ofenzyme-based detoxification systems within the pesticides increases. This tolerance is usually caused by the are oftenmuchmore difficulttokill astheirtolerance tomany grown toalarger size(e.g.,large, lateinstar caterpillars), they it is oftenpossible touse alowdosage. Oncethepestshave stages ofapest (e.g.,small, earlyinstars ofa caterpillar pest), right timeforexample against more susceptible immature then control mostofthe remaining pests. Byspraying atthe without killingthenatural enemies–thenatural enemiescan long-term result because itwillsuppress thepestnumbers In somecases, using a lowconcentration maygive abetter kill pestsquicklysoaslow result doesnotmean apoorresult. label (orless, ifitstillgives adequatecontrol). Not all pesticides Use theminimum concentration recommended ontheproduct Timing ofpesticideapplication Minimise thepesticideconcentration 3.3 SelectiveApplication 105

Part 3.3 Part 3.3 106 be abletoprovide sustainable control ofpests. appropriate conservation practices, natural enemiesshould then pests orslows theirrate ofdevelopment. Combined with only asingleapplicationthateitherreduces thenumbers of inadequate levels ofcontrol. This mightinvolve theneedfor there is clearevidencethatnatural enemiesare providing Apply pesticidesasinfrequently aspossible,andonlywhen Reduce thefrequencyofapplication 3.3 SelectiveApplication Email: [email protected] 704531 /737193 Tel: 04-704531/706650 Dr SimonSithole Contact: Harare Causeway PO BoxCY550 Specialist Services Department ofResearch& PPRI Institute Plant ProtectionResearch Email: [email protected] Tel: 04-707311 Training Officer, AGRITEX) Marcus Hakutengwi(Chief Contact: Harare PO Box639 AGRITEX AGRITEX Contacts ZIMBABWE Email: [email protected] 744117 Tel: 04-744509/744470 / Mutizwa Mukute Contact: Harare Mt Pleasant PO BoxMP1059 PELUM Association Association Land UseManagement Participatory Ecological Email: [email protected] Tel: 04-336310 Dr SamPage Fortunate Nyakandaor Shepherd Musiyandaka, Contacts: Harare Causeway PO BoxCY301 AfFOResT Research andTraining African Farmers’Organic 107

Contacts 108 Contacts Contacts 109

Contacts KENYA UNITED KINGDOM / EUROPE Contacts

Kenya Agricultural Research International Centre for Imperial College of Science, (Natural Resources Institute contd.) Institute / National Insect Physiology and Technology & Medicine Contacts: Agricultural Research Ecology (University of London) Hans Dobson or Jerry Cooper Laboratories Email: [email protected] ICIPE Department of Biology [email protected] KARI/NARL PO Box 30772 Imperial College PO Box 14733 Nairobi Silwood Park Nairobi Ascot Natural Resources Contact: Berkshire SL5 7PY, UK International Contact: Director-General Gilbert Kibata E-mail: [email protected] Contacts: Natural Resources International Email: [email protected] Dr Robert Verkerk or Pembroke Dr Denis Wright Chatham Maritime Emails: [email protected] Chatham CABI Africa Regional Centre [email protected] Kent ME4 4NN, UK CABI-ARC Contact: PO Box 633 CABI Bioscience, UK Centre Crop Protection Programme Village Market Manager Nairobi CABI Bioscience Email: [email protected] UK Centre (Egham) Contacts: Bakeham Lane Dr George Oduor or Egham Global IPM Facility Dr Sarah Simons Surrey TW20 9TY, UK Emails: [email protected] Global IPM Facility Secretariat [email protected] Contact: Food & Agricultural Organisation [email protected] Tony Little of the United Nations (IPM Information Officer) Viale delle Terme di Caracalla Email: [email protected] 00100 Rome, Italy

Contact: Natural Resources Institute Coordinator or IPM Specialist Email: [email protected] Natural Resources Institute University of Greenwich Central Avenue Chatham Maritime Chatham Kent ME4 4TB, UK Appendix 110 most commonnaturalenemieslikelytobeencountered. and Kenya. Thisisbyno meansonexhaustivelistbutitdoescontainsomeofthe been identified,mainlybetween1998and2000,onvegetablecropsinZimbabwe The followinggeneraandspeciesofpredators(List1)parasitoids2)have yeotr Vespidae Mantidae Hymenoptera Mantodea rcnd Lycosidae Arachnida Coccinellidae Coleoptera cr Phytoseiidae Acari Syrphidae Diptera re aiyGenus/species Family Order erpeaChrysopidae Neuroptera Anthocoridae Hemiptera Oxyopidae Linyphiidae Carabidae Sphecidae Staphylinidae Reduviidae Nitidulidae Anthicidae Species List1:Predators C. propinqua Polistes Sphodromantis Peucetia Microlinyphia Pardosa Stenethmus Microlestes agilis Harpalus fortipes Passlidius Chlaenius Calosoma Exochomus Cheilomenes variegata Hippodamia Typhlodromus Phytoseiulus Amblyseius Sphex Paragus sapphirina Allobaccha annulipes Melanostoma adligatus Betasyrphus aegyptius Ischiodon flaviventris Syritta corollae Metasyrphus Oligata Philonthus Chrysoperla Harpactor Orius Cybocephalus rubricollis Formicomus biplagiatus Anthicus spp. sp. sp. ( spp. sp. Holobus spp. sp. spp. sp. sp. spp., includingA. tekeandA.tutsi sp. spp., including sp. spp. spp. spp., including and spp. spp. sp. spp. ) sp. C. sulphurea E. troberti E. C. lunata and , E. ventralis E. itr Tachinidae Diptera re aiyGenus/species Braconidae Family Hymenoptera Order Encyrtidae Chalcididae Scelionidae Bombyliidae Eulophidae Ichneumonidae Aphidiinae Braconidae: Calliphoridae Species List2:Parasitoids Nemorilla Periscepsia carbonaria Syrphophagus africanus Brachymeria Telenomus Oomyzus sokolowskii Palexorista Nemoraea rubellana Gonia bimaculata Neochrysocharis Meruana liriomyzae Bombylius Microchelonus curvimaculatus Glyptapanteles maculitarsis Cotesia Apanteles Meteorus Diglyphus Diplazon laetorius Charops Diadegma Aphidius Diaeretiella rapae smi dubiosa Isomyia spp., including sp. spp., including sp. sp. spp., including sp. sp. sp. sp. spp., including sp. sp. C. ruficrus A. colemani A. D. isaea P. laxa and C. plutellae 111

Appendix Notes 112 Notes