MAY/JUNE 2005 GRAPEGROWING

One acre insectory at Benziger Vineyards. (Photo by Mary Benziger.)

in which increased plant biodiversity can contribute to the design of pest-stable agro-ecosystems by creating an appropriate ecological infrastructure within and around vineyards. A key feature of that infrastructure are flower resources which can be provided in the form of cover crops, corridors, or islands. When choosing flowering plants to attract beneficial , it is important to note the size and shape of the blossoms, Designing biodiverse, pest-resilient because that is what dictates which insects will be able to access the flowers’ pollen and nectar. For most beneficials, including parasitic wasps, the most helpful blos- vineyards through habitat management soms should be small and relatively open. Plants from the Compositae (sunflower) and Umbelliferae (carrot) families are BY Miguel A. Altieri, Clara I. Nicholls, Luigi California vineyards to counteract such especially useful. Ponti, Alan York2 pest pressure, especially diseases as Timing of flower availability is as ESPM-Division of Insect Biology much of the chemical inputs comprise important to natural enemies as blossom University of California, Berkeley applications of sulfur dust. The envi- size and shape. Many beneficial insects are 2WHOLISTIC ESTATE MANAGEMENT ronmental impact of such pesticide load active only as adults and only for short can be serious. periods during the growing season; they ost typical California winegrape pro- Concerned about these problems, need pollen and nectar during these active duction is done in monocultures, that many people have proposed options to times, particularly in the early season totaled 568,000 acres in 2002 rectify this habitat decline by increasing when prey are scarce. One of the easiest M(although this acreage decreased the vegetational biodiversity of agricul- ways growers can help is to provide bene- slightly in 2003/2004), an agricultural tural landscapes. There are many ways ficials with mixtures of plants with rela- expansion that is slowly resulting in the tively long, overlapping bloom times. simplification of large landscapes. Since Biodiversity is crucial to crop the onset of such simplification, farmers defenses: the more diverse the plants, and researchers have been faced with a , and soil-borne organisms that major ecological dilemma arising from the inhabit a farming system, the more homogenization of vineyard systems: increased vulnerability of uniform, large- scale monocultures to insect pests and dis- eases, which, in many cases, can cause yield losses. Expansion of monocultures has decreased abundance and activity of natu- ral enemies due to removal of critical food resources and overwintering sites. Many scientists are concerned that, with acceler- ating rates of habitat removal, the contri- bution to pest suppression by biocontrol agents using these habitats will decline. It is possible that many pest problems affect- ing today’s vineyards have been exacer- Adult epos male, parasite of the bated by such trends. grape leafhopper. (Photos by Jack Kelly About 69 million lbs of active ingre- Clark for UC Statewide IPM Project. ©2000 Adult female wasp, Anagrus epos. dients of pesticides are used annually in Regents, University of California.) (57x magnification) MAY/JUNE 2005 2 GRAPEGROWING

Farmer 4. Designing corridors of plants that Along with cover crops come wasps management usher beneficials from nearby forests or (many moving in from riparian forests) natural vegetation to field centers; that seek out the nectar in the cover Planned biodiversity 5. Selecting non-crop plants grown as crop’s flowers. These wasps, in turn, are (cover crops, strips in fields, whose flowers match ben- natural parasitoids of pests that nor- corridors, etc.) eficials’ requirements; mally attack vines. Wasps are part of the Ecosystem 6. Preserve mosaics or islands of native associated biodiversity, some of which function vegetation within or near the vineyards. live in the riparian vegetation and move (i.e. pest regulation) All the above strategies provide alter- from there to vines or cover crops. The native food (pollen and nectar) and cover crops, then, enrich the soil (direct Associated refuge for predators and parasitoids of function) and attract wasps (indirect biodiversity (predators, leafhoppers, mites and lepitodpterous function). parasitoids) pests, thereby increasing natural enemy The challenge for growers is to iden- diversity and abundance in vineyards. tify the type of biodiversity that is desir- Surrounding able to maintain and/or enhance in biodiversity their vineyard in order to carry out spe- (riparian forest, Biodiversity in vineyards hedgerows, etc.) cific ecological services (such as pest and its function Biodiversity in vineyards refers to all Figure I. Relationship between several types plant and organisms (crops, native A of biodiversity and their role in pest 35 regulation in a diversified vineyard. vegetation, weeds, livestock, natural ene- mies, pollinators, and soil flora and fauna) 30 present in and around farms. How diverse the vegetation is within and around a 25 Effect of cover crops on farm, how many cover crops are grown, leafhopper population 20 450 how close a vineyard is to a forest, hedgerow, meadow, or other natural vege- 400 15 350 tation, are all factors that contribute to a 300 vineyard’s level of biodiversity. Mean No. Nymphs/leaf 10 250 Two distinct components of biodi- 200 5 150 versity can be recognized in agro- ecosystems. The first component, 100 0 / yellow sticky trap 50 planned biodiversity, includes the crops before 1 week 2 weeks 0 and other plants purposely included in mowing after after Cumulative number of leafhoppers 3-Jul a vineyard by a grower. The second No mow Mow 11-Jul 18-Jul 25-Jul 31-Jul 9-Aug 20-Jun 27-Jun 15-Aug 22-Aug 28-Aug component, associated biodiversity, Date B includes all soil flora and fauna, herbi- 8000 no cover cover vores, carnivores, and decomposers, 7000 that colonize the agroecosystem from Figure II. Densities of adult leafhoppers surrounding environments and will 6000 E. elegantula in cover-cropped and mono- culture vineyards in Hopland, CA, during thrive in a vineyard, depending on its 5000 1997 growing season. management and structure. The rela- tionship of both types of biodiversity 4000 components is illustrated in Figure I. 3000

Planned biodiversity has a direct Anagrus/YST Mean No. diverse the community of pest-fighting function, as illustrated by the bold 2000 beneficial organisms (predators, para- arrow connecting the planned biodiver- 1000 sitoids, and entomopathogens) a farm sity box with the ecosystem function can support. box (Figure I). Associated biodiversity 0 before 1 week 2 weeks Farmers can enhance biodiversity on also has a function, but it is mediated mowing after after their farms by: through planned biodiversity. Thus, No mow Mow 1. Increasing plant diversity with crop planned biodiversity also has an indi- rotations or with “polycultures” (crop rect function, which is realized through mixes) of cash crops grown on the same its influence on the associated biodiver- Figure III. A) Effect of cover crop mowing vineyard land at the same time; sity. in vineyards on densities of leafhopper 2. Planting cover crops between vines; nymphs during the 1997 growing season in For example, cover crops enrich the Hopland, CA. B) Effects of cover crop 3. Managing vegetation surrounding soil which helps vine growth. The direct mowing in vineyards on densities of fields to meet the needs of beneficial function of cover crops is to enhance Anagrus epos during the 1997 growing organisms; soil fertility and soil structure. season in Hopland, CA. 3 MAY/JUNE 2005 GRAPEGROWING

regulation) and then determine the best nymphs and adults (Figure II). Thrips practices that will encourage such bio- also exhibited reduced densities in cover- 160 diversity. Cover cropping and creation cropped vineyards in both seasons.7 140 of habitats within vineyards are key During both years, general predator 120 strategies. populations on the vines were higher in 100 the cover-cropped sections than in the 80 Enhancing vineyard biodiversity monoculture blocks. Generally, popula- 60 40 with cover crops tions were low early in the season, but 20 In California, many growers manage increased as prey became more numerous 0 resident vineyard floor vegetation or as the season progressed. Dominant pred- Number of predators/D-Vac sample plant cover crops as habitat manage- ators included spiders (mainly salticid Spiders Orius sp. Nabis sp. Carabidae ment to enhance natural enemies. [jumping spider] and thomisid species Thomisids Mordellidae Geocoris sp. Chrysopidae

Reductions in mite and grape leafhop- [crab spider], Nabis sp. [damsel bugs], Coccinellidae per populations have been observed in Orius sp. [Minute pirate bug], Geocoris sp. Erigeron Yarrow Buddleja Fennel cover cropped systems.2,4 But in many [Big eyed bugs], Coccinellidae [ladybugs] cases, such biological suppression has , and Chrysoperla sp. [lacewings]). Figure IV. Main predator groups associated not been sufficient from an economic Although Anagrus epos (the most impor- with dominant corridor flowering plants (Hopland, CA 1996). viewpoint.3 Usually the problem is that tant leafhopper parasitoid wasp), achieved most growers plant winter cover crops high numbers and inflicted noticeable mor- and/or allow weedy resident vegeta- tality of grape leafhopper eggs, this impact Leafhopper population gradient tion which are mowed or plowed was not substantial enough. Apparently the under at the beginning of the growing wasps encountered sufficient food 1000 900 season, mainly to avoid competition resources in the cover crops and few moved 800 with the vines for water. to the vines to search for leafhopper eggs, 700 In early summer, these vineyards especially when eggs are not abundant and 600 become virtual monocultures without despite the presence of leafhopper honey- 500 400 floral diversity. It is important to main- dew. For this reason, alternate tractor row 300 tain a green cover during the entire cover crops were mowed to force move- / yellow sticky trap 200 100 growing season in order to provide ment of Anagrus wasps and predators into 0 habitat and alternate food for natural the vines. Cumulative number of leafhoppers 3-Jul 6-Jun 11-Jul 18-Jul 25-Jul 31-Jul 9-Aug 13-Jun 20-Jun 27-Jun 15-Aug 22-Aug 28-Aug enemies, especially in areas affected by Before mowing, leafhopper nymphal 18-May 23-May 30-May grape leafhoppers. densities on vines were similar in all the Date One approach is to sow summer selected cover-cropped rows. One week Near Far cover crops that bloom early and after mowing, probably due to increased throughout the season, thus providing predation, numbers of nymphs declined Figure V. Seasonal patterns of adult a highly consistent, abundant, and on vines where the cover crop was leafhoppers in vineyard near and far from well-dispersed alternative food source, mowed, coinciding with an increase in the corridor (Hopland, CA 1996). and micro-habitats, for a diverse com- Anagrus densities in mowed cover crop munity of natural enemies. Such food rows. During the second week such supply decouples predators and para- decline was even more pronounced Predators population gradient sitoids from strict dependence on grape (Figure III). 70 herbivores, allowing an early build-up The mowing experiment suggests a 60 of natural enemies in the system, which direct ecological linkage, as mowing helps keep pest populations at accept- cover crop vegetation forced movement 50 able levels. of the Anagrus and predators harbored by 40 Maintaining floral diversity the flowers, resulting in a decline of 30 throughout the growing season in a leafhopper numbers on vines adjacent to 20 Northern California vineyard near the mowed cover crops (in both years). / yellow sticky trap Hopland in the form of summer cover Timing of mowing must coincide when 10 crops of buckwheat and sunflower, the eggs are present on vine leaves in order to Cumulative number of predators 0 abundance of grape leafhoppers and optimize the efficiency of arriving 3-Jul 6-Jun 11-Jul 18-Jul 25-Jul 31-Jul 9-Aug 13-Jun 20-Jun 27-Jun 15-Aug 22-Aug 28-Aug western flower thrips was substantially Anagrus wasps. 18-May 23-May 30-May reduced as associated natural enemies Date increased. Designing corridors Near Far During two consecutive years Several studies indicate that the (1996–1997), vineyard systems with abundance and diversity of ento- Figure VI. Seasonal patterns of predator flowering cover crops were character- mophagous (insect-eating bugs) insects catches (numbers per yellow sticky trap) in ized by lower densities of leafhoppers within a field is dependent on the plant vineyards as influenced by presence of the corridor (Hopland, CA 1996). MAY/JUNE 2005 4 GRAPEGROWING

(Foeniculum vulgare), yarrow (Achillea Vineyard Vineyard Vineyard millefolium), Erigeron annuus and Buddleja spp. 1% 2% 13% Certain predator species moved from the riparian forests, using the resources of the corridor as they were continuously 60 m found associated with specific flowering N=25689 N=11132 N=4033 plants (Figure IV), and many of them moved into the adjacent vineyard. 1% 2% 10% The flowering sequence of various plants species provided a continual source of pollen and nectar, and a rich and abun- Near Far 30 m

Distance from insectory dant supply of neutral insects (non-pestifer- N=18937 N=11344 N=4495 ous herbivores) for the various predator species, thus allowing the permanence and 5% 3% 5% circulation of viable populations of key predator species within the corridor. In both years, adult leafhoppers exhib- ited a clear population density gradient

INSECTORY reaching lowest numbers in vine rows near N=9951 N=7953 N=5294 the corridor and increasing in numbers Early Middle Late towards the center of the field. The highest concentration of adult and nymphal Growing season leafhoppers occurred after the first 20 to 25 Beneficials Neutrals Pests rows (30 to 40m) downwind from the corri- dor (Figure V). A similar population and Figure VII. The proportion of beneficials, neutral, and pestiferous insects (insects that feed on or distribution gradient was apparent for exert damage to vines) in the island, and in the vineyard at various distances from the island as thrips. In both years, thrip catches were sub- the season progressed (N = total number of insects caught in yellow sticky traps, stantially higher in the central rows than in % = proportion of beneficial insects). rows adjacent to the corridor. The abundance and spatial distribu- species composition of the surrounding To overcome this limitation, the tion of generalist predators in the fami- vegetation, and also on the spatial extent owners of an organic farm near lies Coccinellidae, Chrysopidae, of its influence on natural enemy abun- Hopland, CA, established a 600-meter Nabidae, and Syrphidae was influ- dance, which is determined by the dis- corridor containing at least 65 flower- enced by the presence of the corridor tance to which natural enemies disperse ing species, which was connected to a which channeled dispersal of insects into the crop. riparian forest and cut across the vine- into adjacent vines (Figure VI). The role of riparian habitats and espe- yard. The idea was that such a corridor Predator numbers were higher in the cially of wild blackberry patches near would serve as a biological highway first 25 meters adjacent to the corridor vineyards in enhancing the effectiveness for movement and dispersal of preda- which probably explains the reduction of A. epos in parasitizing the grape tors and parasitoids (especially Anagrus of leafhoppers and thrips observed in leafhopper is well known. wasps) into the center of the vineyard. the first 25 vine rows near the corridor. Based on this knowledge, researchers Movement by natural enemies from The presence of the corridor was established that French prunes adjacent nearby habitats to disperse readily associated with the early vineyard col- to vineyards could also serve as over- within crops, theoretically enhances the onization by Anagrus wasps but this wintering sites for A. epos and found speed with which a numerical aggrega- did not result in a net season-long higher leafhopper parasitism in grape tive response to pest foci may take prevalence in leafhopper egg para- vineyards with adjacent prune tree place. sitism rates in vine rows adjacent to refuges.8 However, the effect of prune Data collected within the corridor in the corridor. Despite the fact that the refuges is limited to only a few vine rows the 1996 and 1997 growing seasons vineyard had a flowering cover crop, downwind and A. epos exhibited a grad- showed that species such as Chrysoperla the proportion of eggs parasitized ual decline in vineyards with increasing carnea, Orius sp., Nabis sp., Geocoris sp., tended to be uniformly distributed distance from the refuge. This poses an and several members of the families across all vine rows in both blocks. important limitation to use of prune Coccinellidae, Syrphidae (hover flies), Eggs in the center rows had slightly trees, as the colonization of grapes by A. Mordellidae, and some species of higher mean parasitization rates than epos is limited to field borders leaving the thomisid spiders, to be predators com- eggs located in rows near the corridor. middle rows of the vineyard void of bio- monly found on flowers of the domi- Anagrus does not have the same logical control protection. nant corridor plants such as fennel pollen and nectar needs that many 5 MAY/JUNE 2005 GRAPEGROWING

other general predators and parasitic wasps have and apparently does not need Vineyard Vineyard Vineyard a diversity of hosts (neutral insects) for its population to be maintained, constituting Anagrus wasps an exception in this regard. Despite the Orius sp. Anagrus wasps fact that Anagrus is a key leafhopper reg- Coccinellids Coccinellids Anagrus wasps 60 m ulator, the habitat manipulations herein described aid in building a whole benefi- cial insect complex which confers stability to the vineyard. Anagrus wasps Anagrus wasps Anagrus wasps Orius sp. Syrphids Creating flowering islands Near Far 30 m as a push-pull system Distance from insectory Coccinellids Syrphids Coccinellids for natural enemies One good way to start integrating vineyard management and conservation of natural enemies is to develop a farm Insectory Insectory Insectory design, recognizing the reality that not all few parts of a farm can be managed to maxi- mize conservation objectives, such as Early Middle Late habitat enhancement for beneficial arthro- many pods. Growing season Creating habitat on the least produc- Figure VIII. Dispersal of Anagrus wasps and generalist predators from the island into the tive parts of the farm to concentrate natu- vineyard. ral enemies is a smart way to use and beautify marginal lands or less produc- tive areas in the vineyard such as a sp. and Coccinellids are prevalent colo- agroecosystem diversity and complex- ridgetop, a swale, etc. This is the biody- nizers at the beginning of the season, but ity as a foundation for establishing ben- namic approach used at Benziger Family later syrphid flies and Anagrus wasps eficial interactions that aid in keeping Estate (Glen Ellen, CA), where an island start dispersing from the island (insec- pest populations in check. of flowering herbaceous annuals and tory) into the vineyard (Figure VIII). Diverse and complex vineyards may perennials was created at the center of a Parasitization of leafhopper eggs by be harder to manage, but when prop- vineyard and which acts as a push-pull Anagrus wasps was particularly high on erly implemented, habitat management system for natural enemy species. vines near the island, with parasitiza- leads to establishment of the desired The island has been planted with a tion levels decreasing towards the cen- type of plant biodiversity and a unique mix of herbaceous plants, which provides ter of the vineyard away from the island ecological infrastructure necessary for flower resources from early April to late (Table I), a trend not observed at the attaining optimal natural enemy diver- September to a number of herbivore Hopland corridor vineyard interface. sity and abundance. insects (neutral non-pestiferous insects Planting flower strips (such as Current knowledge of which plants and pollinators), and associated natural Alyssum) that go from the island into a are the most useful sources of pollen, enemies. The island acts as a source of vineyard, could be tried as an effective nectar, habitat, and other critical needs pollen, nectar, and neutral insects which strategy to pull beneficials deeper into a is far from complete. Clearly, many serve as alternate food to a variety of vineyard and thus overcome the push- plants encourage natural enemies, but predators and parasites, including effect of the island which confines natu- scientists have much more to learn Anagrus wasps, a prevalent parasitoid in ral enemy activity to adjacent vine about which plants are associated with this vineyard (Figure VII). rows. which beneficials, and how and when During the 2004 season, sampling to make desirable plants available to revealed that the island was dominated Conclusions target organisms. Because beneficial’s by neutral insects that forage on the vari- A key strategy in sustainable viticul- interactions are site-specific, geographic ous plants, but also served as food to nat- ture is to enhance biodiversity at the location and overall farm management ural enemies which, starting in early June, landscape and field level through the are critical variables. ■ slowly built up in numbers in the adjacent use of cover crops, corridors, and vari- vineyard as the season progressed. ous habitats. Emergent ecological prop- The authors thank Aida Gamal, Andre Catches in yellow sticky traps placed erties develop in such diversified vine- Monteiro, Mariana Portella, Maira Ribeiro, inside the island and at various distances yards, allowing them to function in a and Marcos Westphal for their help in data within the vineyard, suggest that many self-regulating manner. collection. Luigi Ponti was supported by a natural enemies moved from the island The main approach in ecologically- fellowship from the Italian National into the vineyard (up to 60 meters). Orius based pest management is to increase Research Council (CNR n. 203.22 code 2). MAY/JUNE 2005 6 GRAPEGROWING

References 1. Altieri, M. A., C. I. Nicholls. (2004). Biodiversity and pest management in agro- ACTION PLAN Once growers have a thorough ecosystems. Food Products Press, Bingham- o design an effective plan for knowledge of the characteristics and ton USA. needs of key pests and natural ene- 2. Daane, K. M., M. J. Costello, G.Y. successful habitat management, in accordance with the proven mies, they are ready to design a habi- Yokota, W.J. Bentley. (1998) “Can we manip- T tat management strategy specific for principles of ecologically-based pest ulate leafhopper densities with management their vineyard. A few guidelines need practices?” Grape Grower 30 (4): 18–36. management, first growers should 3. Daane, K. M. and M. J. Costello. (1998) gather as much information as they to be considered when implementing “Can cover crops reduce leafhopper abun- can. Growers should make a list of the habitat management strategies: dance in vineyards?” California Agriculture most economically important pests 1. Select the most appropriate plant 52 (5): 27–32. and their associated natural enemies species; 4. Flaherty, D.L. (l969) “Ecosystem in the vineyard and find out: 2. Determine the most beneficial spa- complexity and the Willamette mite, 1. What are the pest’s food and habi- tial and temporal arrangement of such Eotetranychus willamettei (Acarine: Tetra- tat requirements? plants, within and/or around the nychidae) densities.” Ecology 50: 911–916. fields; 5. Landis, D. A., S. D. Wratten, G. M. 2. What factors influence pest abun- dance? 3. Consider the spatial scale at which Gurr. (2000). “Habitat management to con- the habitat enhancement operates serve natural enemies of pests in 3. When do pests build in the crop agriculture.” Annual Review of Entomology, and when do they become economi- (such as field or landscape level); 45, 175–201. cally damaging? 4. Understand the predator-para- 6. Nicholls, C. I., M. Parrella, M. A. 4. What are the most important pred- sitoid behavioral mechanisms influ- Altieri. (2001). “The effects of a vegetational ators, parasites, and pathogens? enced by the habitat manipulation; corridor on the abundance and dispersal of 5. What are the primary needs of 5. Anticipate potential conflicts that insect biodiversity within a northern Cali- those beneficial organisms? may emerge when adding new plants fornia organic vineyard.” Landscape Ecology, 6. Where do these beneficials over- to the agro-ecosystem. (For example, 16, 133–146. while blackberries may increase popu- 7. Nicholls, C. I., M. P. Parrella, M. A. winter, when do they appear in the field, where do they come from, what lations of Anagrus epos, a parasitoid of Altieri. (2000). “Reducing the abundance the grape leafhopper, they may also of leafhoppers and thrips in a northern attracts them to the crop, how and California organic vineyard through when do they build up in the crop, and host Xylella fastidiosa, the bacterium maintenance of full season floral diversity what keeps them in the field? that causes Pierce’s disease, as well as with summer cover crops.” Agricultural 7. When do the beneficials’ critical a disease vector, the blue-green sharp- and Forest Entomology, 2, 107–113. resources (nectar, pollen, and alternative shooter.) 8. Corbett, A. and J. A Rosenheim. hosts and prey) appear and how long are 6. Develop ways in which the added (1996) “Impact of a natural enemy over- they available? Are alternate food sources plants do not upset other agronomic wintering refuge and its interaction with accessible nearby and at right times? management practices, and select the surrounding environment.” Ecological plants that have multiple effects, such Entomology 21: 155–164 Which native annuals and perennials can compensate for critical gaps in timing, as improving pest regulation while at especially when prey are scarce? the same time contributing to soil fer- tility and weed suppression.

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