Science and Ecology ©Parker Forsell Designing and Implementing a Habitat Management Strategy to Enhance Biological Pest Control in Agroecosystems Clara Ines Nicholls and Miguel A. Altieri

Farmers can enhance the resistance and resilience of their larvae. A third group – beneficial disease-causing organisms crops and fields by reinforcing their built-in defenses against that include fungi, bacteria, viruses, protozoa and nema- pests. This can be done by following two main strategies: todes – fatally sicken pests or keep them from feeding or increasing above- and below-ground biodiversity and im- reproducing. Plants also form complex associations with or- proving soil health. This paper focuses on the role of ben- ganisms around their roots, which offer protection against eficial insect biodiversity in farms, and on the ways of en- disease. Soil fungi and ground beetles can destroy the seeds hancing functional biodiversity in agroecosystems as a of weeds that compete with plants. In addition the rich soil means of promoting biological control of insect pests. fauna play key roles in breaking up and decomposing or- Biodiversity is crucial to crop defenses: the more diverse ganic matter thus making nutrients available to plants. the plants, animals and soil-borne organisms that inhabit Biodiversity in the form of polycultures may also make a farming system, the more diverse the community of pest- plants less “apparent” to pests; crops growing in monocul- fighting beneficial organisms the farm can support. One tures may be so obvious to pests that the plants’ defenses group of partners – beneficial predators – chew up plant-eat- fall short of protecting them. ing insects and mites or sucks out their juices. Another Farmers can enhance biodiversity on their farms by: group – beneficial parasites – lay eggs inside pest eggs and/or • increasing plant diversity with crop rotations or with

26 WINTER, 2004–2005 “polycultures” of cash and cover crops grown on the same soil fauna, etc) present in and around farms. Biodiversity land at the same time; can be as varied as the various crops, weeds, arthropods, or • managing vegetation surrounding fields to meet the microorganisms involved, according to geographical loca- needs of beneficial organisms; tion, climatic, edaphic [soil-related], human, and • providing beneficial organisms with supplemental re- socioeconomic factors. In general the degree of biodiversity sources, such as artificial nesting structures, extra food in agroecosystems depends on four main characteristics of and alternative prey; the agroecosystem: • designing “corridors” of plants that usher beneficials • the diversity of vegetation within and around the agroe- from nearby forests or natural vegetation to field centers cosystem; • selecting non-crop plants grown as strips in fields, whose • the permanence of the various crops within the agroe- flowers match beneficials’ requirements. cosystem; Healthy soils are also essential to plant defenses. Un- • the intensity of management; healthy soils hinder crops’ abilities to use their natural de- • the extent of the isolation of the agroecosystem from nat- fenses and leave them vulnerable to potential pests. In con- ural vegetation. trast, healthy soils arm plants chemically with defense- How diverse is the vegetation within and around the boosting nutrients and are physically conducive to optimum farm, how many crops comprise the rotation, how close is root development and water use. Reduced susceptibility to the farm to a forest, hedgerow, meadow or other natural veg- pests is usually a reflection of differences in plant health as etation, are all factors that contribute to a particular farm’s mediated by soil fertility management. Many studies doc- level of biodiversity. ument lower abundance of several insect pests in low-input The biodiversity components of farms can be classified systems and they attribute partly such reductions to the in relation to the role they play in the functioning of crop- lower nitrogen content of organically farmed crops. In ad- ping systems. According to this, agricultural biodiversity can dition, the rich supplies of beneficial organisms that inhabit be grouped as follows: healthy soils can intensify nutrient uptake, release growth- • productive biota: crops, trees, and animals chosen by stimulating chemicals and antagonize disease-causing or- farmers that play a determining role in the diversity and ganisms. Healthy soils can also expose weed seeds to more complexity of the agroecosystem; predators and decomposers, and their slower release of ni- • resource biota: organisms that contribute to productiv- trogen in spring can delay small-seeded weeds – which ity through pollination, biological control, decomposi- often need a flush of nitrogen to germinate and begin rapid tion, etc; growth – thereby giving larger-seeded crops a head start. •destructive biota: weeds, insect pests, microbial Farmers can improve soil health by: pathogens, etc., which farmers aim at reducing through • diversifying crop rotations including legumes and peren- cultural management. nial forages Two distinct components of biodiversity can be recog- • keeping soils covered year-round with living vegetation nized in agroecosystems. The first component, planned bio- and/or crop residue diversity, includes the crops and livestock purposely in- • adding plenty of organic matter from animal manures, cluded in the agroecosystem by the farmer, and which will crop residues and other sources vary depending on the management inputs and crop spa- • reducing tillage intensity and protecting soils from ero- tial/temporal arrangements. The second component, asso- sion and compaction ciated biodiversity, includes all soil flora and fauna, herbi- • using best-management techniques to supply balanced vores, carnivores, decomposers, etc. that colonize the nutrients to plants without polluting water agroecosystem from surrounding environments and that When farmers adopt agricultural practices that increase will thrive in the agroecosystem depending on its manage- the abundance and diversity of above- and below-ground ment and structure. The relationship of both types of bio- organisms, they strengthen their crops’ abilities to withstand diversity components is illustrated in Figure 1. Planned pests. In the process, farmers also improve soil fertility and biodiversity has a direct function, as illustrated by the bold crop productivity. arrow connecting the planned biodiversity box with the ecosystem function box. Associated biodiversity also has a Biodiversity in farms and its function function, but it is mediated through planned biodiversity. Biodiversity in farms refers to all plant and animal organ- Thus, planned biodiversity also has an indirect function, il- isms (crops, weeds, livestock, natural enemies, pollinators, lustrated by the dotted arrow in the figure, which is real-

BIODYNAMICS 27 DESIGNING AND IMPLEMENTING A HABITAT MANAGEMENT STRATEGY TO ENHANCE BIOLOGICAL PEST CONTROL Figure 1. Relationships between several types of biodiversity and their role in agroecosystem function

Agroecosystem management

Planned biodiversity Ecosystem function (i.e., pest regulation, nutrient cycling, etc. Associated biodiversity

Surrounding biodiversity ized through its influence on the associated biodiversity. For requires an understanding of the numerous relationships be- example, the trees in an agroforestry system create shade, tween soils, microorganisms, plants, insect herbivores, and which makes it possible to grow only sun-intolerant crops. natural enemies. In fact the optimal behavior of agroeco- So, the direct function of this second species (the trees) is systems depends on the level of interactions between the var- to create shade. Yet along with the trees might come wasps ious biotic and abiotic components. By assembling a func- that seek out the nectar in the tree’s flowers. These wasps tional biodiversity (that is a collection of interacting may in turn be the natural parasitoids of pests that normally organisms that play key functions in the farm) it is possible attack crops. The wasps are part of the associated biodi- to initiate synergisms which subsidize farm processes by versity. The trees then create shade (direct function) and at- providing ecological services such as the activation of soil tract wasps (indirect function). biology, the recycling of nutrients, the enhancement of ben- Complementary interactions between the various bio- eficial arthropods and antagonists, and so on, all important diversity components can also be of a multiple nature. in determining the sustainability of agroecosystems (Figure 2). Some of these interactions can be used to induce positive In modern agroecosystems, the experimental evidence and direct effects on the biological control of specific crop suggests that biodiversity can be used for improved pest pests, soil fertility regeneration and/or enhancement and soil management. Several studies have shown that it is possible conservation. The exploitation of these interactions in real to stabilize the insect communities of agroecosystems by de- situations involves novel farm designs and management and signing diverse cropping systems that support populations

Figure 2. Components, functions and strategies to enhance functional biodiversity in agroecosystems

Components

Pollinators Predators and parasitoids Herbivores Earthworms Micro, macro, and mesofauna of the soil

BIODIVERSITY

Pollination Pest regulation Biomass consumption Soil structure, nutrient cycling Decomposition, predation, disease suppression

Functions

Polyculture Agroforestry Rotations Cover crops Zero tillage Composting Green manure

Techniques

28 WINTER, 2004–2005 Figure 3. The effects of agroecosystem management and associated cultural practices on the diversity of natural enemies and the abundance of insect pests

Increase in Natural Enemies Species Diversity – Lower Pest Populations Densities

hedgerows, shelterbelts, windbreaks polycultures rotations cover crops

Habitat diversification Organic soil management Low soil disturbance

AGROECOSYSTEM MANAGEMENT

Cultural practices Pesticides

conventional tillage total weed removal monoculture chemical fertilization

Decrease in Natural Enemies Species Diversity – Population Increases of Pestiferous Species of natural enemies or have direct deterrent effects on pest Biological pest control: a strategy to increase herbivores. The key is to identify the type of biodiversity biodiversity in farms that is desirable to maintain and/or enhance in order to Studies show that farmers can indeed bring pests and nat- carry out ecological services, and then to determine the best ural enemies into balance on biodiverse farms. One of the practices that will encourage the desired biodiversity com- most powerful and long-lasting ways to keep pests from ponents. There are many agricultural practices and designs causing economic damage on your farm is to boost exist- that have the potential to enhance functional biodiversity, ing or naturally occurring beneficial organisms to effective and others that negatively affect it. The idea is to apply the levels by supplying them with appropriate habitat and al- best management practices in order to enhance or regen- ternative food sources. Fewer beneficial organisms – preda- erate the kind of biodiversity that can subsidize the sus- tors, parasites and pest-sickening “pathogens” – live in tainability of agroecosystems by providing ecological ser- monocultures or in fields routinely treated with pesticides vices such as biological pest control, nutrient cycling, water than on more diverse farms where fewer pesticides are used. and soil conservation, etc. The role of farmers and re- In general farms sharing many of these characteristics host searchers should be to encourage those agricultural practices bountiful beneficials: that increase the abundance and diversity of above- and • fields are small and surrounded by natural vegetation; below-ground organisms, which in turn provide key eco- • cropping systems are diverse and plant populations in or logical services to agroecosystems (Figure 3). around fields include perennials and flowering plants; Thus, a key strategy in farming is to exploit the com- • crops are managed organically or with minimal syn- plementarity and synergy that result from the various com- thetic agrichemicals; binations of crops, trees, and animals in agroecosystems that • soils are high in organic matter and biological activity feature spatial and temporal arrangements such as poly- and – during the off-season – covered with mulch or veg- cultures, agroforestry systems and crop-livestock mixtures. etation. In real situations, the exploitation of these interactions in- Naturally occurring beneficials, at sufficient levels, can volves farming system design and management and re- take a big bite out of pest populations. To exploit them ef- quires an understanding of the numerous relationships fectively, farmers must: among soils, microorganisms, plants, insect herbivores, • identify which beneficial organisms are present; and natural enemies. • understand their individual biological cycles and re- source requirements.

BIODYNAMICS 29 DESIGNING AND IMPLEMENTING A HABITAT MANAGEMENT STRATEGY TO ENHANCE BIOLOGICAL PEST CONTROL With this information, farmers can devise management specialists, targeting either a single host species or several re- schemes that will increase the size and diversity of natural- lated species, or they can be generalists, developing in many enemy complexes and decrease pest problems. types of hosts. Typically, they attack hosts larger than them- selves, eating most or all of their hosts’ bodies before pu- Predators pating inside or outside them. With their uncanny ability Biodiverse farms are rich in predatory insects, spiders and to locate even sparsely populated hosts using chemical cues, mites. These beneficial arthropods prey on other insects and parasitoid adults are much more efficient than predators at spider mites, and are critical to natural biological control. ferreting out their quarry. Most predators are “generalist” feeders, attacking a wide va- Most parasitoids used in the biological control of insect riety of insect species and life stages. Predators occur in most pests are either Diptera flies – especially from the family Ta- orders of insects but primarily in Coleoptera, Odonata, Neu- chinidae – or Hymenoptera wasps from the superfamilies roptera, Hymenoptera, Diptera and Hemiptera. Their impacts Chalcidoidea, Ichneumonoidea, and Proctotrupoidea. Para- have been highlighted worldwide by eruptions of spider sitoid diversity is directly related to plant diversity: different mite pests where chemical insecticides have eliminated the crops, ground covers, weeds and adjacent vegetation support mites’ predators. Tetranychid mites, for example, are usu- different pests, which in turn attract their own groups of par- ally very abundant in apple orchards where pesticides have asitoids. In large-scale monocultures, parasitoid diversity is destroyed natural predator populations. suppressed by vegetational simplification; in less-disturbed The diversity of predator species in particular agroe- and pesticide-free agroecosystems, it is not unusual to find cosystems can be impressive. Researchers have reported eleven to fifteen species of parasitoids hard at work. In many more than six hundred species – from forty-five families – cases, just one or two species of parasitoids within these of predaceous arthropods in Arkansas cotton fields and complexes prove vital to the natural biological control of pri- about 1,000 species in Florida soybean fields. Such diver- mary insect pests. In California’s alfalfa fields, the braconid sity can apply major regulatory pressures on pests. Indeed, wasp Cotesia medicaginis plays a pivotal role in regulating the many entomologists consider native, or indigenous, preda- alfalfa caterpillar. This pristine butterfly-wasp system ap- tors a sort of balance wheel in the “pest-natural enemy parently moved into irrigated alfalfa from native clovers. complex” because they tend to feed on whatever pest is over- abundant. Even where predators can’t force pest populations Major characteristics of insect parasitoids: below economically damaging levels, they can and do slow down the rate at which potential pests increase. In spray- • They are specialized in their choice of host free apple orchards in Canada, five species of predaceous • They are smaller than host true bugs were responsible for 44 to 68 percent of the mor- • Only the female searches for host tality of codling moth eggs. • Different parasitoid species can attack different life stages of host • Eggs or larvae are usually laid in, on, or near host Major characteristics of arthropod predators: • Immatures remain on or in host; adults are free-liv- • Adults and immatures are often generalists rather ing, mobile, and may be predaceous than specialists • Immatures almost always kill host • They generally are larger than their prey • Adults also require pollen and nectar • They kill or consume many prey • Males, females, immatures, and adults may be predatory Enhancing beneficial insects by designing • They attack immature and adult prey biodiverse farms • They require pollen and nectar and additional food Natural enemies do not fare well in monocultures. Normal resources cultural activities like tilling, weeding, spraying and har- vesting take their toll, and overly simplified systems lack many of the resources essential to beneficials’ survival and Parasitoids reproduction. Most parasitoids – parasitic insects that kill their hosts – live To complete their life cycles, natural enemies need more freely and independently as adults; they are lethal and de- than prey and hosts: they need refuge sites and alternative food, pendent only in their immature stages. Parasitoids can be hosts and prey which are usually absent in monocultures. For

30 WINTER, 2004–2005 example, many adult parasites sustain themselves with Increasing within-field plant diversity pollen and nectar from nearby flowering weeds while search- By diversifying plants within agroecosystems, farmers can ing for hosts. Predaceous ground beetles – like many other expand environmental opportunities for natural enemies natural enemies – do not disperse far from their overwin- and thereby improve biological pest control. One way to do tering sites: access to permanent habitat near or within the this is to plant polycultures of annual crops – two or more field gives them a jump-start on early pest populations. crops simultaneously growing in close proximity. Farmers Farmers can minimize the disruptive impacts of modern can also let some flowering weeds reach tolerable levels or crop production by understanding and supporting the bi- use cover crops under orchards and vineyards. ological needs of natural enemies. With this same knowl- Numerous researchers have shown that increasing plant – edge, they can also design crop habitats that are friendlier and thereby habitat – diversity favors the abundance and to natural enemies. effectiveness of natural enemies. For example in cotton fields strip-cropped with alfalfa or sorghum, intensified Improving crop habitats for natural enemies populations of natural enemies have substantially decreased To conserve and develop rich complexes of natural enemies, plant bugs and moth and butterfly pests. Beneficials reduced farmers should avoid cropping practices that harm benefi- pest insects below economic threshold levels in Georgia cot- cials. Instead, they should substitute methods that enhance ton that was relay-cropped with crimson clover, eliminat- their survival. Start by reversing practices that disrupt nat- ing the need for insecticides. In Canadian apple orchards, ural biological control: these include insecticide applica- four to eighteen times as many pests were parasitized when tions, hedge removal and comprehensive herbicide use in- wildflowers were numerous compared to when they were tended to eliminate weeds in and around fields. few. In this research, wild parsnip, wild carrot and butter- cup proved essential to a number of parasitoids. In Cali- Providing supplementary resources fornia organic vineyards, the general predators and Anagrus Natural enemies benefit from many kinds of supplementary leafhopper egg parasites that control grape leafhoppers and resources. In North Carolina, erecting artificial nesting thrips thrive in the presence of buckwheat and sunflowers. structures for the red wasp Polistes annularis intensified its When these summer-blooming cover crops flower early, predation of cotton leafworms and tobacco hornworms. In they allow populations of beneficials to surge ahead of California alfalfa and cotton plots, furnishing mixtures of those of pests. When they keep flowering throughout the hydrolyzate, sugar and water multiplied egg-laying by green growing season, they provide constant supplies of pollen, lacewings six-fold and boosted populations of predatory syr- nectar and alternative prey. Mowing every other row of phid flies, lady beetles and soft-winged flower beetles. cover crops – an occasionally necessary practice – forces Farmers can increase the survival and reproduction of these beneficials out of the resource-rich cover crops and beneficial insects by allowing permanent populations of al- into vines. ternative prey to fluctuate below damaging levels. Use In polycultures, apart from the evident increase in plant plants that host alternative prey to achieve this: plant them species diversity, there are changes in plant density and around your fields or even as strips within your fields. In height, and therefore in vertical diversity. All these changes cabbage, the relative abundance of aphids helps determine affect density of pests and other organisms. The combina- the effectiveness of the general predators that consume di- tion of tall and short crops can also affect dispersal of in- amondback moth larvae. Similarly, in many regions, an- sects within a cropping system. For example, in Cuba farm- throcorid bugs benefit from alternative prey when their pre- ers grow strips of corn or sorghum every ten meters within ferred prey, the western flower thrip, is scarce. vegetables or beans in order to provide physical barriers to Another strategy – enhancing levels of a beneficial’s pre- reduce the dispersion of thrips (Thrips palmi). ferred host – has controlled cabbage white butterflies in cole In China, researchers working with farmers in ten town- crops. Supplemented with continual releases of fertile fe- ships in Yumman, China, covering an area of 5350 hectares, males, populations of this pest escalated nearly ten-fold in encouraged farmers to switch from rice monocultures to spring. This enabled populations of two of its parasites – planting variety mixtures of local tall rice with shorter hy- Trichogramma evanescens and Apanteles rebecula – to build brids. Tall plants provided a barrier for inoculum dispersal, up early and maintain themselves at effective levels all sea- but in addition enhanced genetic diversity reduced blast in- son long. Because of its obvious risks, this strategy should cidence by ninety-four percent and increased total yields by be restricted to situations where sources of pollen, nectar or eighty-nine percent. By the end of two years, it was con- alternative prey simply can’t be obtained. cluded that fungicides were no longer required.

BIODYNAMICS 31 DESIGNING AND IMPLEMENTING A HABITAT MANAGEMENT STRATEGY TO ENHANCE BIOLOGICAL PEST CONTROL Managing vegetation surrounding the field larly boosted populations of Dometrias atricapillus and Hedgerows and other vegetation in field margins can serve Tachyporus hypnorum, two important cereal aphid predators. as reservoirs for natural enemies. These habitats can be im- A 1994 study found that the natural enemies the beetle portant overwintering sites for the predators of crop pests. banks harbored were so cost-effective in preventing cereal They can also provide natural enemies with additional aphid outbreaks that pesticide savings outweighed the labor pollen, nectar and other resources. and seed costs required to establish them. The ridges can Many studies have shown that beneficial arthropods do be 1.3 feet high, 5 feet wide and 950 feet long (0.4 meters indeed move into crops from field margins, and biological by 1.5 meters by 290 meters). control is usually more intensive in crop rows near wild veg- For more extended effects, it is recommended to plant etation than in field centers: corridors with longer-flowering shrubs. In northern Cali- • In Germany, parasitism of the rape pollen beetle is about fornia, researchers connected a riparian forest with the cen- 50 percent greater at the edges of fields than in the middle. ter of a large monoculture vineyard using a vegetational cor- • In Michigan, European corn borers at the outskirts of ridor of sixty plant species. This corridor, which included fields are more prone to parasitism by the ichneumonid many woody and herbaceous perennials, bloomed through- wasp Eriborus terebrans. out the growing season, furnishing natural enemies with a • In Hawaiian sugar cane, nectar-bearing plants in field constant supply of alternative foods and breaking their margins improve the numbers and efficiency of the strict dependence on grape-eating pests. A complex of sugar cane weevil parasite Lixophaga sphenophori. predators entered the vineyard sooner, circulating contin- Practical management strategies arise from understanding uously and thoroughly through the vines. The subsequent these relationships. A classical example comes from Califor- food-chain interactions enriched populations of natural nia, where the egg parasite Anagrus epos controls the grape enemies and curbed numbers of leafhoppers and thrips. leafhopper in vineyards adjacent to French prunes. The prunes These impacts were measured on vines as far as one hun- harbor an economically insignificant leafhopper whose eggs dred to one hundred fity feet (thirty to forty-five meters) provide Anagrus with its only winter food and shelter. from the corridor.

Creating corridors for natural enemies Selecting the right flowers Sowing diverse flowering plants into strips that cut across When choosing flowering plants to attract beneficial insects, fields every 165 to 330 feet (50–100 meters) can provide nat- note the size and shape of the blossoms. That’s what dic- ural enemies with highways of habitat. Beneficials can use tates which insects will be able to access the flowers’ pollen these corridors to circulate and disperse into field centers. and nectar. For most beneficials, including parasitic wasps, European studies have confirmed that this practice in- the most helpful blossoms are small and relatively open. creases the diversity and abundance of natural enemies. Plants from the aster, carrot and buckwheat families are es- When sugar beet fields were drilled with corridors of tansy pecially useful. (See Table 1 on pages 35–36). leaf (Phacelia tanacetifolia) every twenty to thirty rows, It should also be noted when the flower produces pollen destruction of bean aphids by syrphids intensified. Similarly, and nectar: timing is as important to natural enemies as strips of buckwheat and tansy leaf in Swiss cabbage fields in- blossom size and shape. Many beneficial insects are active creased populations of a small parasitic wasp that attacks the only as adults and only for discrete periods during the cabbage aphid. Because of its long summer flowering period, growing season: they need pollen and nectar during these tansy leaf has also been used as a pollen source to boost syr- active times, particularly in the early season when prey are phid populations in cereal fields. On large organic farms in scarce. One of the easiest ways farmers can help is to pro- California, strips of Alyssum are commonly planted every vide them with mixtures of plants with relatively long, fifty to one hundred meters within lettuce and cruciferous overlapping bloom times. crop fields to attract syrphid flies that control aphids. Current knowledge of which plants are the most useful Some grass species can be important for natural enemies. sources of pollen, nectar, habitat and other critical needs For example, they can provide temperature-moderating is far from complete. Clearly, many plants encourage nat- overwintering habitats for predaceous ground beetles. In ural enemies, but scientists have much more to learn about England, researchers established “beetle banks” by sowing which plants are associated with which beneficials, and earth ridges with orchard grass at the centers of cereal fields. how and when to make desirable plants available to target Recreating the qualities of field boundaries that favor high organisms. Because beneficial interactions are site-specific, densities of overwintering predators, these banks particu- geographic location and overall farm management are

32 WINTER, 2004–2005 critical variables. In lieu of universal recommendations, • when do the beneficials’ critical resources – nectar, which are impossible to make, farmers can discover many pollen, alternative hosts and prey – appear and how answers by investigating the usefulness of alternative flow- long are they available; are alternate food sources acces- ering plants on their farms. sible nearby and at the right times; which native annu- als and perennials can compensate for critical gaps in timing, especially when prey are scarce. Enhancing biodiversity – checklist for farmers: • Diversify enterprises by including more species of crops and livestock. Key information needed in crafting a habitat manage- • Use legume-based crop rotations and mixed pas- ment plan: tures. 1) ecology of pests and beneficials • Intercrop or strip-crop annual crops where feasible. • What are the most important (economic) pests that • Mix varieties of the same crop. require management? • Use varieties that carry many genes – rather than • What are the most important predators and para- just one or two – for tolerating the same disease. sites of the pest? • Emphasize open-pollinated crops over hybrids for • What are the primary food sources, habitat, and their adaptability to local environments and greater other ecological requirements of both pests and genetic diversity. beneficials? (From where does the pest infest the • Grow cover crops in orchards, vineyards and crop field, how is it attracted to the crop, and how does fields. it develop in the crop? From where do the benefi- • Leave strips of wild vegetation at field edges. cials come, how are they attracted to the crop, and • Provide corridors for wildlife and beneficial insects. how do they develop in the crop?) • Practice agroforestry; where possible, combine trees 2) timing or shrubs with crops or livestock to improve habi- • When do pest populations generally first appear tat continuity for natural enemies. and when do these populations become economi- • Plant microclimate-modifying trees and native cally damaging? plants as windbreaks or hedgerows. • When do the most important predators and para- • Provide a source of water for birds and insects. sites of the pest appear? • Leave areas of the farm untouched as habitat for • When do food sources (nectar, pollen, alternate plant and animal diversity. hosts, and prey) for beneficials first appear? How long do they last? • What native annuals and perennials can provide Designing a habitat-management strategy such habitat needs? To design an effective plan for successful habitat manage- ment, first gather as much information as you can. Make a list of the most economically important pests on your Rolling out the strategy farm. For each pest, try to find out: This paper presents some ideas and principles for design- • what are its food and habitat requirements; ing and implementing healthy, pest-resilient farming sys- • what factors influence its abundance; tems. It has been explained why reincorporating complex- • when does it enter the field and from where; what at- ity and diversity is the first step towards sustainable pest tracts it to the crop; management, and the paper describes the two pillars of • how does it develop in the crop and when does it become agroecosystem health (Figure 4): economically damaging; • fostering crop habitats that support beneficial fauna • what are its most important predators, parasites and • developing soils rich in organic matter and microbial ac- pathogens; tivity • what are the primary needs of those beneficial organisms; Well-considered and well-implemented strategies for soil • where do these beneficials overwinter, when do they and habitat management lead to diverse and abundant – al- appear in the field, where do they come from, what at- though not always sufficient – populations of natural enemies. tracts them to the crop, how do they develop in the crop As farmers develop a healthier, more pest-resilient system and what keeps them in the field; for their farms they may ask themselves:

BIODYNAMICS 33 DESIGNING AND IMPLEMENTING A HABITAT MANAGEMENT STRATEGY TO ENHANCE BIOLOGICAL PEST CONTROL • How can species diversity be increased to improve pest suppression and pest regulation – and that don’t disrupt de- management, compensate for pest damage and make sirable farming practices. Avoid potential conflicts: in Cali- fuller use of resources? fornia, planting blackberries around vineyards boosts pop- • How can the system’s longevity be extended by includ- ulations of grape leafhopper parasites but can also exacerbate ing woody plants that capture and recirculate nutrients populations of the blue-green sharpshooter that spreads the and provide more sustained support for beneficials? vinekilling Pierce’s disease. In placing selected plants over • How can more organic matter be added to activate soil space and time, use the scale – field- or landscape-level – that biology, build soil nutrition and improve soil structure? is most consistent with intended results. And, finally, keep it • Finally, how can the landscape be diversified with mo- simple: the plan should be easy and inexpensive to imple- saics of agroecosystems in different stages of succession ment and maintain, and should be easy to modify as needs and with windbreaks, living fences, etc? change or results warrant change. Once farmers have a thorough knowledge of the char- acteristics and needs of key pests and natural enemies, they Clara I. Nicholls and Miguel A. Altieri are Research fellow and Profes- are ready to begin designing a habitat-management strat- sor, respectively, at the Division of Insect Biology–ESPM, University of egy specific for their farm. Choose plants that offer multiple California, Berkeley. benefits – for example, ones that improve soil fertility, weed

Figure 4. Pillars of agroecosystems health

Agroecological principles

Agroecosystem design

“Below-ground” habitat “Above-ground” habitat management and diversification management and diversification • Soil organic matter • Polyculture • Nutrient and compaction • Cover crops management • Rotations

Crop health

Agroecosystem health

Guidelines for designing healthy and pest-resilient farming systems • Increase species in time and space with crop rotations, with regular applications of organic matter. polycultures, agroforestry and crop-livestock systems. • Enhance nutrient recycling with legumes and live- • Expand genetic diversity with variety mixtures, multi- stock. lines and local germplasm. • Maintain vegetative cover with reduced tillage, cover • Conserve or introduce natural enemies and antago- crops or mulches. nists with habitat enhancement or augmentative re- • Enhance landscape diversity with biological corridors, leases. vegetationally diverse crop-field boundaries or mosaics • Boost soil biotic activity and improve soil structure of agroecosystems.

34 WINTER, 2004–2005 Table 1. Plants that attract beneficial insects spider many insects Caraway, dill, fennel, cosmos, marigold, spearmint spider mite destroyer spider mite Carrot family (goldenrod, yarrow), bishop’s weed; maintain permanent plantings Syrphid fly (hover flies) aphid Carrot family (Queen Anne's lace, dill, fennel, caraway, tansy, parsley, (Syrphidae family) coriander, bishop's weed), the sunflower family (coreopsis, Gloriosa daisy, yarrow, cosmos, sunflower), marigolds, candytuft, sweet alyssum, cean- othus, holly-leaved cherry (Prunus ilicifolia), buckwheat, scabiosa, spearmint, coyote brush (Baccharis pilulari), knotweed (Polygonum aviculare), California lilacs (Ceanothus spp.), soapbark tree, meadow foam (Linnanthes douglasii), baby-blue-eyes (Nemophila) Tachinid fly cutworm, armyworm, tent cater- Carrot family (caraway, bishop's weed, coriander, dill, parsley, Queen Anne's (Tachinidae family) pillar, cabbage lopper, gypsy lace, fennel), goldenrod, sweet clover, Phacelia spp., sweet alyssum, buck- moth, some attack sawfly, Japan- wheat, amaranth, buckthorn, Heteromeles arbutifolia ese beetle, May beetle, squash bug, green stink bug, sowbug Tiger beetle many insects Maintain permanent plantings and some exposed dirt or sand areas (Cicindelidae family) Minute Pirate Bug (Antho- Thrips, spider mite, leafhopper, Effective predators of corn earworm eggs. Carrot family (Queen Anne's lace, coridae family), corn earworm, small caterpil- tansy, coriander, bishop's weed, chervil), sunflower family (cosmos, tidy tips (Orius spp) lars, many other insects (Layia), goldenrod, daisies, yarrow), baby-blue-eyes (Nemophila), hairy vetch, alfalfa, corn, crimson clover, buckwheat, blue elderberry (Sambucus caerulea), willows, shrubs. Maintain permanent plantings or hedgerows. Parasitic nematodes Nematodes Marigolds, chrysanthemum, gaillardia, helenium, Eriophyllus lanatum, horseweed (Conyza canadensis), hairy indigo, castor bean, Crotalaria spp., Desmodium spp., sesbania, Mexican tea (Chenopodium ambrosioides), shat- tercane (Sorghum bicolor), lupines, Phaseolus atropurpurens Praying mantis (Mantis spp) Any insect Cosmos, brambles. Protect native species by avoiding pesticides. Predatory mites (Typhlodro- Spider mite There are many species of predatory mites with ecological requirements, mus spp) especially with respect to humidity and temperature, that are particular to the species. Avoid use of insecticides. Provide beneficial refugia for non- crop habitat of non-crop mite prey. Predatory thrips (Thripidae Spider mites, aphid, other There are several types of predatory thrips. Predatory thrips populations family) thrips, Oriental fruit moth, cod- may be conserved/maintained by having non-crop populations of plant- dling moth, bud moth, peach feeding mites (e.g. European red mite, two-spotted spider mite), scales, twig borer, alfalfa weevil, white- aphids, moth eggs, leafhoppers and other thrips. fly, leafminer, scale Rove beetle (Staphylinidae Aphid, springtail, nematodes, Permanent plantings; interplant strips of rye, grains, and cover crops; family) flies; some are parasitic on cab- mulch beds; make stone or plant walkways in garden to provide refuges. bage-root maggot Aphid midge (Aphidoletes Aphid Dill, mustard, thyme, sweet clover. Shelter garden from strong winds; pro- aphidimyza) (Larvae are vide water in a pan filled with gravel. aphid predators) Aphid parasites (Aphidius Aphid Nectar-rich plants with small flowers (anise, caraway, dill, parsley, mustard matricariae and others) family, white clover, Queen Anne's lace, yarrow) Assassin bug (Reduviidae Many insects, including flies, Permanent plantings for shelter (e.g., hedgerows) family) tomato hormworm, large cater- pillars

BIODYNAMICS 35 DESIGNING AND IMPLEMENTING A HABITAT MANAGEMENT STRATEGY TO ENHANCE BIOLOGICAL PEST CONTROL Table 1. Plants that attract beneficial insects, continued

Big-eyed bugs (Geocoris spp) Many insects, including other Can build up in cool-season cover crops such a berseem clover (Trifolium (Lyagaidae family) bugs, flea beetles, spider mites, alexandrium) and subterranean clovers (Trifolium subterraneum). Can be insect eggs and small caterpil- found on common knotweed (Polygonum aviculare). lars. Will also eat seeds. Braconid wasp (Braconidae Armyworm, cabbage worm, Nectar plants with small flowers (caraway, dill, parsley Queen Anne's lace, family) codling moth, gypsy moth, fennel, mustard, white clover, tansy, yarrow), sunflower, hairy vetch, buck- European corn borer, beetle lar- wheat, cowpea, common knotweed, crocuses, spearmint) vae, flies, aphid, caterpillars, other insects Damsel bug (Nabidae family) Aphid, thrips, leafhoppers, tree- Anything in the sunflower family (incuding goldenrod, yarrow), alfalfa. hopper, small caterpillars Ground beetle (Carabidae Slug, snail, cutworm, cabbage- Permanent plantings, amaranth; white clover in orchards, mulching. family) root maggot; some prey on Col- orado potato beetle, gypsy moth and tent caterpillar Lacewing (Neuroptera family) Soft-bodied insects including Carrot family (caraway, Queen Anne's lace, tansy, dill, angelica), sunflower (Chrysoperla and Chrysopa aphid, thrips, mealybug, scale, family (coreopsis, cosmos, sunflowers, dandelion, goldenrod), buckwheat, spp) caterpillars, mite corn, hollyleaf cherry (Prunus ilicifolia), flowering bottle tree (Brachychiton populneum), soapbark tree (Quillaja saponaria). Provide water during dry spells. Lady beetle or ladybug (Hip- Aphid, mealybug, spider mite, Once aphids leave a crop, lady beetles will also. To retain active lady beetles, podamia spp and others) soft scales maintain cover crops or other hosts of aphids or alternative prey. Carrot fam- (Coccinellidae family) ily (fennel, angelica, dill, tansy, bishop's weed, Queen Anne's lace), sun- flower family (goldenrod, coreopsis, cosmos, golden marguerite (Anthemis), dandelion, sunflower, yarrow), crimson clover, hairy vetch, grains and native grasses, butterfly weed (Asclepias), black locust, buckwheat, euonymus, rye, hemp sesbania (Sesbania exaltata), soapbark tree, buckthorn (Rhamnus), saltbush (Atriplex spp.), black locust (Robinia pseudoacacia). Mealybug destroyer (Crypto- Mealybug Carrot family (fennel, dill, angelica, tansy), sunflower family (goldenrod, laemus montrouzieri) coreopsis, sunflower, yarrow) (Coccinellidae family)

36 WINTER, 2004–2005