USING HABITAT MANAGEMENT TO IMPROVE BIOLOGICAL CONTROL ON COMMERCIAL ORGANIC FARMS IN CALIFORNIA

Ramy Colfer, Mission Organics, Salinas, CA 93902, U.S.A.

INTRODUCTION Mission Organics grows organic vegetables on over 5500 acres per year. We do not grow any conventional crops. Like all vegetable producers, we frequently encounter disease and pest problems in many of the crops we grow. We employ many different strategies to manage these pest and disease problems. A major group of pests that we encounter are aphids. One of the key strategies that we use to manage aphids is conservation biological control. Conservation biological control entails the management of resources in the environment to enhance the survival, fecundity, longevity and behavior of natural enemies to increase their effectiveness (Landis et al., 2000). Conservation biological control has recently received greater attention in the biological control literature (Barbosa, 1998; Pickett and Bugg, 1998; Landis et al., 2000). In this manuscript, I describe how we have implemented conservation biological control through habitat manipulation to improve the biological control of aphids. In our row crop lettuces (romaine and iceberg lettuce) and cole crops (broccoli and cauliflower), we intercrop with annual flowering plants to improve our aphid biological control. The flowering plants provide a food source for aphid predators and parasitoids. The group of aphid natural enemies of primary importance is the syrphid flies or hoverflies. The use of flowering intercrops and hedgerows in organic agriculture has been criticized by some university researchers and extension personnel because the purpose of these habitat manipulations has not been clearly defined by growers. Questions such as ‘What pest are you trying do control?’ and ‘What beneficial arthropods are being attracted by the beneficial habitats to control the target pest?’ have not be clearly answered. However, in our row-crop production, we clearly identify the answers to these questions. In our cropping systems, we clearly define the pests that we are attempting to control with intercropping of flowering plants: the pests of primary importance include (i) the lettuce aphid Nasonovia ribisnigri and (ii) the cabbage aphid Brevicoryne brassicae; the pests of secondary importance include (i) the green peach aphid Myzus persicae,(ii) Potato aphid Macrosiphum euphorbiae, and (iii) foxglove aphid Aulacorthum solani. The most important group of natural enemies that we are attempting to increase with intercropping of flowering plants is the syrphid flies (Diptera: Syrphidae). A very diverse group of syrphid species are generally observed in our crops; common genera include Sphaerophoria, Syphus, Eupeodes, Allograpta, and Toxomerus. Some of the most abundant species of syrphids that we find in lettuce and cole crops include Sphaerophoria sulfuripes, Syrphus opinator, and Eupeodes fumipennis. Other important natural enemies that we observe in our crops include lady beetles (common spp.: Hippodamia convergens, Coccinella novemnotata , and Coccinella septempunctata), aphidiid parasitic wasps (Diaeretiella rapae, Aphidius matricariae, and Lysiphlebus testaceipes), brown lacewings (Hemerobius spp.), green lacewings (Chrysoperla spp.), bigeyed bugs (Geocoris spp.), and minute pirate bug (Orius tristicolor). In my presentation, I will focus on the use of intercropping of flowering plants in romaine lettuce to improve the biological control of the lettuce aphid N. ribisnigri in the central coast of California. I will begin by going through some evidence that shows that the lettuce aphid is generally controlled through the naturally- occurring biological control of syrphid flies in organically-grown romaine lettuce. This will include a description of some aspects of the ecology of syrphid populations. Then, I will present and discuss some results that support the premise that intercropping with sweet alyssum (Lobularia maritime) can improve the control of the lettuce aphid in romaine lettuce.

PRELIMINARY OBSERVATION – HOW CAN WE BEST CONTROL LETTUCE APHID POPULATIONS? Early experiments testing the efficacy of organic materials to suppress lettuce aphid populations indicated that most materials had little impact on aphid populations and could interfere with aphid biological control. For example, results from an open-plot, replicated (n = 4) field trial in a romaine lettuce provided evidence that insecticidal soap could cause more harm than good for lettuce aphid control. This experiment was conducted in a 5 acre field of romaine lettuce in San Benito County during July, 2000. Plots were sprayed with insecticidal soap (2%, 100 gpa) twice on a weekly interval. Aphid and syrphid larval populations were monitored twice; five and three days after each soap application, respectively. Lettuce aphid populations tended be larger and increasing in the

55 insecticidal soap treatment but smaller and decreasing in the unsprayed plots causing aphid numbers to marginally differ between treatments (Figure 1A, Manova, Wilks’ lambda test, F = 4.41, P = 0.08). Syrphid larval populations tended to increase in the unsprayed plots but not in the soap-sprayed plots; syrphid larval populations in the second sampling tended to be higher in the unsprayed plots than the sprayed plots though this difference was not statistically significant (Figure 1B, t-test, t = 1.24, P = 0.26). These experimental results and others where the presence of syrphid populations predated the elimination of lettuce aphid populations led us to believe that syrphid populations are very important in reducing lettuce aphid populations. A large number of observational results of fields where syrphid larval populations were strongly correlated with a subsequent crash and elimination of lettuce aphid populations prior to lettuce harvest led us to the realization that the most effective strategy for controlling lettuce aphid populations in organic romaine lettuce was through conservation biological control. Also, we have observed that syrphid biological control is consistent across a wide range of regions (Monterey, Santa Cruz , and San Benito Counties) and through many seasons (spring, summer, and fall). This is in contrast to other lettuce aphid natural enemies that are important during certain times of year and/or certain locations.

SYRPHID ECOLOGY - FACTORS CONTRIBUTING TO EFFECTIVE APHID CONTROL Aphid- syrphid population dynamics The interactions between lettuce aphid and syrphid populations appear to fairly simple: a Lokta-Voltera model predictions of prey and predator populations dynamics through time appears to be similar to the populations dynamics observed in a typical romaine lettuce field. Lettuce aphid populations establish and increase; this is followed by the establishment of syrphid populations. Then, aphid populations are generally eliminated once syrphid populations are sufficiently abundant. Lettuce aphid populations generally do not persist for a sufficiently long period to cause the degradation of the romaine plants due to aphid feeding (over exploitation of the prey resource). Whether syrphid activity is successful at controlling the lettuce aphid for romaine production is dependent on the timing: do syrphid larvae ‘clean up’ aphids prior to harvest? The optimum scenario occurs when both the aphid and syrphid populations are no longer present in the lettuce at the time of harvest. The goal for the organic pest management practitioner is to promote the early establishment of syrphid populations. Figure (2) graphically displays the acceptability of a romaine field in relation to the population cycling of lettuce aphid and syrphid populations and the type of harvest (romaine hearts or processed romaine). Romaine hearts go directly from the field to the consumer and cannot contain more than a low number of aphids per plant; processed romaine is cut and washed at a processing plant and can have more aphids. However, processed romaine with heavy aphid populations is not desirable because it requires more washing and is therefore more expensive to process.

Aphid and syrphid spatial population dispersion An important aspect of the ecology of syrphid flies is that they are generally more widely dispersed across a romaine field than lettuce aphid populations. When lettuce aphid populations are high, syrphid eggs can generally be found on every plant within a romaine field. Here, monitoring of three romaine lettuce fields demonstrates the most common situations we encounter in our fields. The dispersion of lettuce aphid and syrphid egg populations are presented in three different types of fields. The results presented are from fields that were two-to-three weeks prior to harvest. Situation one; these results come from the Bypass ranch in Hollister (San Benito Co.) where we generally encounter heavy lettuce aphid pressure. Lettuce aphid populations were high and the majority of plants had aphid population above what would be acceptable for harvest (Figure 3A). However, syrphid egg numbers were also abundant and eggs were found on all romaine plants (Figure 3B). Under these conditions, romaine plants will become clean enough for both hearts and processed romaine harvest but the elimination of aphid populations may occur near harvest time (sometimes within days). Situation two; these results come from the Home ranch in Gilroy (San Benito Co.) where we generally encounter low-to-moderate aphid populations combined with consistently high syrphid populations. Lettuce aphids were not present on a majority of romaine plants, and the plant with aphids contained fairly small populations (Figure 4A). Syrphid eggs were more widely distributed (69% plants contained syrphid eggs) and the mean syrphid egg number was above our threshold (2 eggs per plant)(Figure 4B). Under these conditions, we would anticipate to harvest romaine hearts in optimum condition in terms of aphid control (nearly all plants without aphids or syrphid larvae). Situation three, these results come from the Murphy ranch in Watsonville (Santa Cruz Co.) where both high and low aphid pest pressure can be encountered. In this particular field we observed very low aphid populations and high syrphid egg populations (Figure 5). Syrphid eggs were much more widely distributed than lettuce aphids (93%

56 plants contained syrphid eggs vs. 17% contained lettuce aphids) and the mean syrphid egg population was more than two times greater than the mean aphid population ( 4.2 ± 0.5 syrphid eggs per plant vs. 2.0 ± 1.2 aphids per plant). This situation is an organic pest management practitioner’s ideal status in terms of lettuce aphid control. Under these conditions, we would expect to harvest romaine hearts in optimum condition in terms of aphid control. In summary, two key ecological factor to the successful control of lettuce aphids by syrphids are due to the fact that (1) syrphid egg population spatial distribution is generally equal-to or greater-than the spatial distribution of lettuce aphid populations and (2) syrphid larval populations are generally sufficiently abundant to completely eliminate lettuce aphid populations (strong numeric response).

INTERCROPPING WITH SWEET ALYSSUM TO IMPROVE THE BIOLOGICAL CONTROL OF LETTUCE APHID Selection of sweet alyssum as the favored flowering intercrop plant Habitat management involves the altering of an agroecosystem to improve the availability of resources required for natural enemies to achieve optimal performance. Landis et al. (2000) address five key issues that are important for the implementation of habitat management: (1) the selection of the most appropriate plant species, (2) the predator/parasitoid behavioral mechanisms that are influenced by the manipulation, (3) the spatial scale over which the habitat enhancement operates, (4) the negative aspects associated with adding new plants to an agroecosystem, such as the use of the plant resources by key pests, and (5) the degree of uptake by the agricultural/horticultural community of the proposed habitat changes. We have addressed these preceding issues in regards to our choice to use sweet alyssum as the primary flowering plant to intercrop with our cash crops. Specifically, an effective intercropping flower plant species has to meeting the following requirements to fit within our management practices. (1) The plant species needs to be highly attractive and utilized to our target natural enemy groups. (2) The plant species must fit into our cultural practices so that it can be easily farmed in conjunction with our cash crops. (3) The plant species must be aggressive so that it competes with weeds. (4) The plant species should rapidly become attractive to natural enemies (i.e. begin to bloom quickly) and the attractiveness should last for at least as long as the life of the cash crop. (5) The seed for the plant species should be economical and available in large quantities. (6) The plant species should not attract substantial populations of pest species (i.e. Diabrotica undecimpunctata, Lygus hesperus; note: it is unrealistic and naïve to believe that a plant species will only attracts natural enemies and not pest insects. We refer here to the avoidance of plant species that are highly attractive to pests). (7) The amount of land allocated to an attractive plant species must sufficiently small so that it is economical (≤ 5% of a field should be occupied by the flowering intercrop). (8) The plant species should not become a substantial weed problem during subsequent years (note: any strong blooming plant species will also generally be a large seed producer. We prefer plant species where seed banks can easily be exhausted through pre-irrigation). (9) The plant species should not require an extreme amount of post-crop tillage to incorporate the plant species into the soil. All of these factors have been evaluated in choosing sweet alyssum.

Evidence supporting the benefit of sweet alyssum intercropping for lettuce aphid biological control Quantifying the full benefits and costs of habitat manipulations can be very difficult, especially for natural enemies that are good dispersers such as syrphid flies. The ideal experimental design to evaluate the benefits to biological control would require comparing multiple ranches with and without flower-plant intercropping. Based on my observations of our vegetable-aphid-syrphid systems, I believe that the level of replication would need to be at the ranch scale (potentially hundreds of acres per replicate) to truly quantify the benefits of intercropping on syrphid biological control. Nonetheless, observations and experimental results conducted at a smaller scale have convinced us that intercropping with sweet alyssum improves aphid biological control. First, we commonly observe adult syrphid fly species that we know to be important aphid predators at larval stage, feeding on alyssum floral resources then foraging within romaine plants. The populations of adult syrphids foraging within alyssum strips are generally abundant. For example, alyssum strips with average attractiveness were monitored at the Home ranch during June 2002. We observed a mean adult population = 212 ± 24 flies per plot (530 ft2 ). For a twenty acre field of romaine lettuce intercropped with sweet alyssum, the estimate population of adult syrphids utilizing the alyssum would be 17424 ± 1973. It is important to note that not all species of syrphid adults that we observe utilizing the alyssum strips are predaceous of lettuce aphids as larvae. Nonetheless, adult syrphid fly utilization of alyssum strips is one piece of evidence supporting their benefit to aphid biological control. Research performed in other systems have also observed increases of adult syrphid populations associated with the addition of flowering plants to agroecosystems (Lovei et al, 1997; White, 1995). Second, when syrphid populations first begin to establish within a romaine field, we will sometimes observe higher syrphid egg numbers on romaine plants adjacent to alyssum strips compared to romaine plants that

57 are some distance apart from the alyssum. For example, syrphid egg monitoring was done at two distances away from alyssum strips (adjacent, 2-10 ft from strips; eight-beds apart, >53 ft away from strips) at the Matulich Ranch during July 2002 (Watsonville, Santa Cruz Co.) soon after syrphid eggs were detected within the field (6 plants per sample, 5 replicates per treatment). Results from monitoring this field showed that syrphid eggs were three times more abundant on romaine plants adjacent to alyssum strips compared to romaine plants that were eight beds apart (Figure 6; Kruskal-Wallis test, χ2 = 4.1, P = 0.043). Another good example of flowering plants increasing syrphid egg oviposition was described by Hickman and Wratten (1996). Differences in syrphid egg abundance in relation to flower strips is generally transient; syrphid egg and larval populations become more spatially uniform across a field soon after syrphid population establishment. However, the initial increase in syrphid egg and larval populations near alyssum strips can lead to accelerated suppression of lettuce aphid populations. For example, syrphid egg monitoring was performed at three distances away from alyssum strips (adjacent, 2-5 ft from strips; four-beds apart, 26-30 ft from strips; eight-beds apart, 53-57 ft away from strips) at the Home Ranch during June 2002 after both syrphid egg and larval population were detected within the field (6 plants per sample, 6 replicates per treatment). In this field, syrphid egg and larval numbers were similar throughout the field, regardless of the distance from the alyssum strips (Figure 7; syrphid eggs: Kruskal- Wallis test, χ2 = 0.04, P = 0.98; syrphid larvae: Kruskal-Wallis test, χ2 = 2.16, P = 0.34). However, lettuce aphid populations were more than two times greater in romaine beds apart from alyssum strips compared to the romaine beds adjacent to alyssum strips (Figure 8, adjacent vs. four-beds apart, Kruskal-Wallis test, χ2 = 4.71, P = 0.030; adjacent vs. eight-beds apart, Kruskal-Wallis test, χ2 = 5.10, P = 0.024). Other studies have also shown aphid reductions and improved plant effects associated with habitat manipulations (Landis et al., 2000). Again it should be noted that these differences in aphid populations in relation to distance from alyssum strips tend to be transient. This evidence shows that alyssum strips can attract large populations of syrphid adults, which can lead to early increases in egg oviposition near the alyssum, which can then lead to early decreases in lettuce aphid suppression. The take home message is that alyssum strips appear to increase the rate at which syrphid populations establish and decimate lettuce aphid populations. Any factor that accelerates the elimination of lettuce aphid populations ensures a cleaner romaine crop at harvest. Beginning in the 2002 growing season, we began consistently using alyssum intercropping as part of our lettuce aphid control program. Since that time, we have had good success in managing the lettuce aphid in romaine lettuce. During 2002 and 2003, 99 - 100 percent of our romaine production was sufficiently free of lettuce aphids to allow romaine to be used for romaine hearts (Figure 9); over one-thousand acres of organically-grown romaine lettuce. During the 2004 growing season, we have encountered very heavy lettuce aphid pressure in some regions. This has forced at least one planting (10 acres) to be harvested for processed romaine instead of romaine hearts. If the year continues in a similar fashion, we will have the opportunity to put conservation biological control to a rigorous test at a commercial scale. In summary, we initially observed that the disruption of syrphid larval populations increase lettuce aphid problems. Through research and observations, we determined that fostering syrphid populations was key to managing lettuce aphid populations in organically-grown romaine lettuce. Some key ecological factors that contribute to the effectiveness of syrphid biological control include high syrphid population abundance and wide spatial distribution. Sweet alyssum was found to be a good plant species for intercropping in our cropping system. Evidence was presented that alyssum intercropping can improve the control of lettuce aphid populations. The organic agriculture industry has dramatically grown in the last fifteen years. There is now over 100,000 acres of certified organic farmland in California. This industry provides a great opportunity for university researchers and extension personnel to implement innovative, biologically-based techniques to manage pest and diseases. It is an opportunity to implement integrated pest management strategies where pesticides really do represent a small percent of the tools growers use to manage pests and diseases.

REFERENCES Barbosa, P., (ed.), 1998. Conservation Biological Control. Academic Press, San Diego, California. Hickman, J.M., Wratten, S.D., 1996., Use of Phacelia tanacetifolia strips to enhance biological control of aphids by hoverfly larvae in cereal fields. J. Econ. Ent. 89, 834-840. Landis, D.A., Wratten, S.D., Gurr, G.M., 2000. Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann. Rev. Ent. 45, 175-201. Lovei, G.L., Macleod, A., Hickman, J.M. 1997. Dispersal and effects of barriers on the movement of the New Zealand hoverfly Melanostoma fasciatum (Dipt., Syrphidae) on cultivated land. J. Appl. Ent. 122, 1-6. Pickett, C.H., Bugg, R.L., (eds.), 1998. Enhancing Biological Control: Habitat Management to Promote Natural Enemies of Agricultural Pests. University of California Press, Berkeley, California.

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White, A.J., Wratten, S.D., Berry, N.A., Weigmann, U., 1995. Habitat manipulation to enhance biological control of Brassica pests by hover flies (Diptera: Syrphidae). J. Econ. Entomol. 88, 1171-1176.

Fig. 1. (A) Population dynamics of lettuce aphid (N. ribisnigri) populations that received insecticidal-soap applications (2 applications on weekly interval) compared with unsprayed-control populations. (B) Corresponding syrphid larval populations in treatments with and without insecticidal-soap applications.

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Fig. 2. Simplified version of lettuce aphid and syrphid population dynamics in relation to the harvest quality of romaine plants. Romaine hearts require romaine plants to be harvested when there are close to zero aphids per plant. Processed romaine can be harvested when there are small-to-moderate aphid populations but it increases processing costs.

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59 Fig. 3. Situation One, high aphid populations/ high syrphid populations. Bypass Ranch. Spatial population distribution of (A) lettuce aphid and (B) syrphid eggs across romaine plants within a 15 acre romaine field. Nearly all plants contained lettuce aphid populations too high for harvesting hearts at the time of monitoring; however, large syrphid egg population were sufficient to eliminate aphid populations by harvest (2 weeks later). This situation is the most common.

14 Bypass Ranch, Apr i l '04 22 A Mean aphi ds per pl ant = 120 ± 14 B Bypass Ranch, Apr i l '04. 12 20 A Mean syr phi d eggs per pl ant = 7. 5 ± 0. 7 18

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Fig. 4. Situation Two, low aphid populations/ moderate syrphid populations. Home Ranch. Spatial distribution of (A) lettuce aphid and (B) syrphid eggs across romaine plants within a 20 acre romaine field. 70 % of romaine plants contained at least one syrphid egg even though only 49 % of romaine plants were infested with lettuce aphids. Mean syrphid egg population exceeded mean aphid population. This situation is also common.

60 35 A Home Lot 4, Jul y '02. B Home Lot 4, Jul y '02. A Mean aphi ds per pl ant = 2.2 ± 0.2 B Mean syr phi d eggs per pl ant = 2.9 ± 0.3

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60 Fig. 5. Situation Three, low aphid populations/ high syrphid populations. Murphy Ranch. Spatial distribution of (A) lettuce aphid and (B) syrphid eggs across romaine plants within a 15 acre romaine field. 93 % of romaine plants contained at least one syrphid egg even though only 17 % of romaine plants were infested with lettuce aphids. Mean syrphid egg population was two times greater than the mean aphid population. This situation is fairly uncommon.

25 B M ur phy Ranch, M ay '04. 90 B M ean syr phi d eggs per pl ant = 4.2 ± 0.5 A Mur phy Ranch May ' 04. 80 A Meanaphi ds per pl ant =2. 0±1. 2 20 70

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Fig. 6. Syrphid egg abundance per plant in romaine beds that were adjacent to flowering sweet alyssum strips (L. maritime) vs. romaine beds that were at least eight beds apart from alyssum (>53 ft away from strips).

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61 Fig. 7. (A) Syrphid egg and larval and (B) lettuce aphid abundance per plant in romaine beds that were adjacent to flowering sweet alyssum strips vs. romaine beds that were (i) four bed apart form alyssum (26-30 ft) and (ii) eight beds apart from alyssum (53-57 ft).

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Fig. 8. Percentage of romaine fields differ in their harvest status due to lettuce aphid contamination at harvest during 2002, 2003, and 2004 (fifth of the season). For romaine lettuce to be acceptable for ‘hearts’ harvest, close to zero aphids per plant is required. For romaine to be acceptable for ‘processed’ harvest, plants must not have more than moderate aphid populations. Romaine is generally not harvestable when heavy aphid populations contaminate plants.

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