Biological control of pests by natural enemies is dependent not only on local conditions, but also on the composition of the surrounding landscape. On-farm management, such as the creation of habitat for natural enemies, have been proven successful in many systems to increase biocontrol services provided by natural enemies. However, the most obvious potential disadvantage of increasing habitat diversity is that some land has to be taken out of production. This drawback may be a major consideration for high-value crops and many growers are reluctant to adopt these practices on their farms.
Another alternative is the release of natural enemies in large numbers to obtain an immediate control of pests. When the abundance of the resident natural enemies is not sufficient to constrain pest population below economic thresholds, their populations can sometimes be increased (augmented) through the purchase and release of commercially available beneficial species. However, it is still unclear how augmentative biocontrol as a local practice will affect pest densities in landscapes of varying complexity from landscapes dominated by agricultural land to landscapes dominates by natural habitats. We experimentally tested how landscape composition influenced the effectiveness of augmentative biocontrol of lepidopteran pests, using two native predators, the spined soldier bug, Podisus maculiventris, and the convergent lady beetle Hippodamia convergens. We selected 22 experimental plots along a gradient of landscape complexity to determine the effects of augmentative releases on biocontrol levels and consequent pest densities, plant damage, and yield. In addition, we assessed the effect of landscape complexity on the abundance and composition of the community of resident natural enemies. To ascertain the identity and effectiveness of the natural enemies attacking lepidopteran pest in the field, we used sentinel preys and surveillance video cameras.
Augmentative releases of predators led to a significant increase in biocontrol levels in complex, but not in simple, agricultural dominated landscapes. Augmented predators increased the biocontrol rate on sentinel larvae from 46% to 60% in complex landscapes. These differences were also significant at the level of plant damage. In complex landscapes, augmentative biocontrol reduced plant damage from 21% to 16% compared with controls.
In addition, farms surrounded by high proportion of agricultural land had more naturally occurring predators and fewer lepidopteran pests. The abundance of predators was increased up to 36% in simple landscapes when compared with their abundance in complex landscapes. The increase in density and activity of predators, were in line with the reduced plant damage in structurally simple landscapes. This may suggest a more efficient natural biocontrol in fields located in simple landscapes. Predators, principally ground beetles, harvestmen, spiders and lady beetles dominated the natural enemy community.
In summary, landscape context not only influenced the effectiveness of augmentative biocontrol, but also affected the biocontrol provided by naturally occurring predators. Based on our preliminary results, complex landscapes could be a better target for implementing augmentative biocontrol approaches in cabbage fields, whereas conservation of resident predators appear to be more effective to improve biocontrol services in simple landscapes. These results indicated that local and landscape-scale management practices may be important for increasing biocontrol services of lepidopteran pests.
Fresh market cabbage is one of the most economically important crop in New York state, with a yearly production of 254.016 tonnes valued at over US $105 million. Out of the 10,900 acres planted in NYS fresh market cabbage each year, 90% are sprayed with insecticides to control lepidopteran larvae such as the diamond back moth and the imported cabbage worm. Insecticide resistance is a key concern with lepidopteran pests on cole crops, showing that pesticide-based practices are unsustainable in the long term.
The use of natural enemies as biological control agents has great potential for the sustainable control of insect pests, such as the diamond back moth, that quickly develop resistance to insecticides (Furlong et al. 2004). Although early attempts on biological pest control focused on specialist parasitoids that attack a single pest, the use of generalist predators has lately increased substantially because they can control multiple pest simultaneously. Since the diamondback moth, the cabbage looper and the imported cabbageworm all attack cabbage crops, generalist predators that feed on all pest could be an effective control strategy. The spined soldier bug, Podisus maculiventris (Hemiptera: Pentatomidae), has been recently identified as the most promising predator of the major cabbage lepidopteran pests (Z. Szendrei. Pers. Comm.). However, natural densities of predators, specifically spined soldier bug, are extremely low in the field, and therefore they are unlikely to constrain pest populations below economic thresholds when considered alone.
One strategy to enhance biological control is the release of natural enemies in large numbers to obtain an immediate control of pests. When resident natural enemies are insufficient, such as in the case of the spined soldier bug, the abundance of natural control agents can sometimes be increased (augmented) through the purchase and release of commercially available beneficial species. In some crops, augmentative releases of natural enemies are an environmentally and economically sound alternative to chemical pest control (van Lenteren 2012). For example, augmentative releases of the spined soldier bug to control pests in tomato and cotton have been proven successful (Ables and McCommas 1982; De Clercq et al. 1998). Consequently, employing these two complementary control techniques, natural and augmentative pest control, in a single approach may be a promising new control strategy. Conservation biological control should be the first priority, with augmentative control being used when conservation control has been disrupted.
The effectiveness of biological control may also depend on the structure of the surrounding landscape. Complex landscapes, defined as landscapes with high proportions of natural or unmanaged habitat, are often positively correlated with higher natural enemy diversity and abundance (Chaplin-Kramer et al. 2011). As a result, biological pest control is often more effective in complex rather than simple landscapes (Thies and Tscharntke 1999). However, little is known about the role of landscape context in determining the efficacy of augmentative releases of natural enemies and their consequences for successful pest control. An additional difficulty is determining whether or not introductions of additional enemies via augmentative releases might help suppress pest even further. For example, natural enemies may combine synergistically to increase pest suppression or may interfere with each other, thus decreasing their combined effectiveness. Both landscape and trophic complexity are likely important for successful biological control, however, the interplay between them is not well understood. Thus, in a biological control context it becomes essential to critically assess the nature of interactions among natural enemies, how such interactions affect pest suppression, and how landscape structure might temper natural enemy interactions and enhance top-down controls (Denno and Finke 2006).
The research reported here aimed to evaluate the compatibility of augmentative releases of predators with the naturally occurring enemies in cabbage crops along a landscape complexity gradient. We specifically tested a modified version of the intermediate landscape-complexity hypothesis, which states that effectiveness of augmentative biological would be maximized at an intermediate level of landscape complexity (Tscharntke et al. 2005) (Fig.1.). To test this hypothesis, we measured the abundance of generalist predators across landscapes differing in structural complexity and conducted a sentinel prey experiment to determine the level of biocontrol provided by the resident and augmented natural enemies.
- Determine the effects of landscape complexity mediated by natural enemy community on lepidopteran pests control and cabbage yield
- Examine the role of landscape complexity on the effectiveness of augmentative releases of predators for biological control of lepidopteran pests.
The field data collection was conducted at 11 farms throughout the Finger Lakes Region in NY State during the summers of 2014 and 2015. Farm sites were characterized by either organic or low input agricultural areas of annual crops, pastures, patchily distributed forest fragments, and semi-natural habitat types. Landscapes ranged from simple, comprised primarily of cropland (73% cropland), to complex landscapes, characterized by a high proportion of semi-natural habitats (2% cropland). Information on land cover types was derived from the 2014 and 2015 National Agricultural Statistics Service Cropland Data Layer for New York (USDA 2015), and the total area of each land cover type was calculated in ArcGIS 10.2 at three scales: 250 m (field-scale), 500 m (intermediate-scale), and 1000 m radius (landscape scale).
Our experimental plots consisted of ten 7.5 m rows of plants spaced 0.9 m between rows, with 0.4 m spacing between plants with a total of 150 plants per plot. Cabbage seedlings were transplanted by hand the second and third week of June in both years. Throughout the growing season, weeds were removed manually at two-week intervals and no insecticides or fungicides were applied to the plants.
Arthropod sampling and plant damage
At each site, the abundance and diversity of arthropods were monitored by using pitfall traps, yellow sticky cards, and visual plant inspection (Fig. 2.). Arthropods were sampled at biweekly intervals starting 15 days after transplanting and continuing until 90 days after transplanting when plants were approaching commercial harvest. In addition, on each sampling date, ten randomly selected plants per plot were removed from the ground to determine pest abundance and overall insect damage (Fig. 2). Damage was quantified using a modified version of the method of Lim et al. (1986), where a plant is classified into one of the following five categories based on the percent of leaf damage: <5, 5-20, 20-60, 60-80 or ≥ 80%. At harvest, the yield was estimated by weighing the final biomass of 15 mature cabbage heads (>15.2 cm diameter) per plot.
Natural enemy identity and biocontrol rates
In each farm, we established two experimental plots separated by at least 200 m. One plot was used as a control (no biocontrol augmentation) and the other was used to release Podisus maculiventris and Hippodamia convergens (Fig. 3.). Predators were purchased from commercial suppliers (Green Methods and Arbico organics) and released at the rate of 0.5-1 nymphs/plant and 4-5 adults/plant for P. maculiventris and H. convergens, respectively. Predators were released three times during the growing season at biweekly intervals beginning 15 days after transplanting.
To measure predation rates by resident and augmented predators, we used four types of sentinel preys: Trichoplusia ni larvae, T.ni eggs, Plutella xylostella pupae and mealworms. To examine the effects of predators on sentinel eggs, paper discs containing approximately 30 eggs were fixed to the underside of 10X10 cm pieces of plastic board that provided a standardized foraging platform for predators. Five egg platforms rested atop a 30 cm long pole pounded into the ground. Larval predation was evaluated by using third to fourth instar larvae of T.ni as sentinel prey. Laboratory reared larvae were placed on the upper part of four randomly selected plants per plot. Egg and larva predation was measured at four sampling stations per plot at 2-week intervals. An enclosure (control) cage prevented both foliar-foraging and ground-dwelling predators from removing the sentinel prey, providing an estimate of losses due to handling and rainfall on each experimental plot (Fig. 4.)
To measure predation rates on sentinel pupae and mealworms, five plastic plates per plot (20 cm diameter) were placed flush with the soil surface just below canopy level to ensure that prey items were exposed to predators, particularly ground beetles, which actively seek prey on cabbage plants. On each plate, we placed seven pupae of P. xylostella on a petri dish, and five mealworms. Mealworms were affixed to the surface of each plate using masking tape that prevented them from crawling out of the plates, but made them accessible to foraging predators. The plates were covered with plastic roofs to prevent rain water from falling into the plates.
After 24 hours, the number of sentinel prey remaining on all plants/dishes/platforms were recorded to determine predation rates in each of the experimental plots. A prey item was considered recovered only if it was fully intact. Those prey remaining on the plot with evidence of predator damage such as bite marks were recorded as consumed.
We also used a camera to record predatory arthropods visiting sentinel eggs and pupae. On each plot, we took pictures using time lapse cameras (1 shot every minute), which were focused on a sentinel prey arena for 24 hours (Fig. 5.). The sentinel arenas were the same as those described above. We used the resulting pictures to identify predators attacking prey and to distinguish taxa that acted as predators from those that are secondary feeders or never interact with prey.
The overall abundance of ground-dwelling predators in our system was higher than that of the foliar-foraging predators. The most common ground-dwelling predators were ground beetles (27.2%), spiders (14.3%), ants (12.7%), and harvestmen (2.7%) that accounted for 57% of the total individuals collected. The most common taxa of foliar foraging-predators included Miridae (17.2%), Coccinellidae (9.4%), Nabidae (1.1%) and Geocoridae (0.8%). Only a few predator species, however, appeared in high enough numbers to have the potential to significantly affect populations of cabbage pests. These taxa included lady beetles (Coleomegilla maculata, and Propylea quatuordecimpunctata), ground beetles (Stelenophus comma, Bembidion quadrimaculatum, Poecilus chalcites, and Elaphropus sp.), and harvestmen. Spiders seem to be important in pitfall traps, but their densities were low on sticky cards and plant samples. We also observed a large number of parasitoid wasps mainly later in the season (Cotesia glomerata), but our results showed that parasitoids were abundant only in situations of high lepidopteran larvae densities. This high density of parasitoids was counteracted by stronger pest pressure, thus leading to little impact of parasitoids on reducing plant damage by caterpillars.
Across farms, the insect herbivore community was dominated by Lepidoptera (17%), aphids (11%) and flea beetles (55%). Other herbivores such as cabbage maggots (Delia radicum), thrips (Thrips tabaci), weevils (Ceutorhynchus obstrictus), leaf miners (Scaptomyza flava) and crickets (Scapteriscus spp.) accounted for less than 17% of all individuals. Three species of lepidopteran pests were recorded on plants, with P. rapae being the dominant species (15% of the total herbivores collected) followed by P. xyllostela (1.5%) and T. ni (0.3%). The average proportion of plants infested by caterpillars was 16 ± 4.7% (mean ± 1 SE) at the beginning of the season and then decreased to 7 ± 2.5% at the end of the season (Fig. 6.).
Predator abundance was best explained by the proportion of agricultural land at the 500 m scale (Linear regression: F1,20 = 3.907 P = 0.0685, Fig. 7a,7b.). This pattern was mainly driven by ground beetles, harvestmen, and spiders which significantly increased with the proportion of agricultural land (linear regressions: F1,20 = 5.694, P = 0.02702, F1, 20 = 5.898 p = 0.02471, F= 7.245 p = 0.0140 respectively). In contrast, predator diversity was negatively influenced by the proportion of agricultural land in the landscape (linear regression: F= 14.2 p < 0.001, Fig. 7b). This suggest that simple landscapes hold very simple predator communities made up of a few dominant species but rather abundant in individuals, while predator assemblages from complex landscapes exhibited lower densities, and higher species diversity.
Plant damage and yield
Plant damage was negatively influenced by the proportion of agricultural land at 250m and 500 m (linear regression 250 m: F1,20 = 7.408, P = 0.0139; linear regression 500 m: F1,20 = 4.69, P = 0.044, respectively). Crop yield, on the other hand, was not directly influenced by the proportion of different habitats in the landscape. The statistical analysis showed that crop yield was negatively related with an increase in plant damage caused by insect injury (linear regression F1,18 = 5.723, P = 0.027). Plant damage was positively related to an increase in Lepidoptera incidence (linear regression F1,17 = 9.435, P = 0.0069, and was not affected by neither aphid incidence nor flea beetle abundance (aphids: F1,17 = 1.115, P = 0.306, flea beetles: F1,18 = 0.0452, P = 0.834). Yield was not directly related to a specific herbivore abundance or incidence
Effects of augmentative releases of predators
The analysis of the 2016 dataset indicated that the proportion of eggs and mealworms removed by predators was not significantly different between the control and the augmentative releases plots (linear model eggs P = 0.5152; mealworms P= 0.7864, Fig. 8.). Augmentative releases of predators did, however, lead to a significant increase in the rate of predation on sentinel larvae in complex, and intermediate complex landscapes (linear model P= 0.0376, Fig. 9.). Augmented predators increased the pest control potential of lepidopteran larvae from 46% to 60%. In contrast, augmented predators in simple landscapes reduced biocontrol levels from 47% to 42%. These differences were also significant at the level of plant damage. From simple to complex landscapes, plant damage increased in the control plots, whereas plant damage decreased along the gradient in the augmentative releases plots (Fig. 9).
Natural enemy identity
The analysis of the pictures revealed the identity of the most important predators attacking lepidopteran pest in the field. Overall, 17 morphotaxa were detected in the video observations, with ladybeetles, harvestmen and hoverflies accounting for the majority of visits to sentinel eggs, while ants, harvestmen and ground beetles were the most common visitors foraging in the ground (Figs. 10 and 11.). Importantly, our data also showed a significant relationship between pest mortality and the activity of lady beetles, ground beetles and harvestmen highlighting their importance as predators of cabbage pest.
This study provides a comprehensive assessment of how landscape composition affects biocontrol services provided by both augmented and naturally occurring predators. Our results show significant positive effects of augmentative releases of predators on biocontrol of lepidopteran larvae. Effects of augmentative releases on pest control and plant damage were influenced as expected by differences in landscape composition. Contrary to our expectations, augmentative releases of predators presented the strongest potential for reducing lepidopteran larvae, under conditions of high landscape complexity. Importantly, our data also suggest that naturally occurring predators such as ground beetles, harvestmen, and lady beetles can also enhance biocontrol of lepidopteran pests in cabbage fields.
Previous studies have pointed out that predatory arthropods are significant agents of pest population suppression in brassica crops (Shmaedick and Shelton, 2000, Shelton et al. 1983). However, this study showed that the landscape context in which a particular farm is embedded is one of the most influential factors explaining the variation in predator abundance, and consequent pest control. Simple landscapes, defined as landscapes with high proportions of agricultural land, were positively correlated with the abundance and activity of ground beetles, harvestmen and some species of lady beetles (i.e. Coleomegilla maculata). The abundance of predators was increased up to 36% in simple landscapes when compared with their abundance in complex landscapes. The increase in density and activity of predators, were in line with the reduced plant damage in structurally simple landscapes. This may suggest a more efficient biocontrol in fields located in simple landscapes. To capitalize on the potential benefits from these naturally occurring predators in simple landscapes, we recommend that land managers should conserve habitats that foster and provide habitat for predator’s persistence. Specifically, preservation of habitats such as field edges, marginal lands or select areas within a crop field (“beetle banks”) can locally improve predator abundance. Fields managed under conservation tillage and the adoption of more selective pesticides with less impact on non-target invertebrates, may also contribute to support a more abundant community of predators.
We also found that augmentative releases of predators have a positive effect on biocontrol of lepidopteran larvae, suggesting that they may supplement the strength of pest control provided by the naturally occurring predators. Clearly, the direction of this effect will vary depending on the landscape context in which the farm is located. Augmentative releases were positive in complex landscapes, but negative in simple landscapes. Thus, complex landscapes could be a better target for implementing augmentative biocontrol approaches in cabbage fields, whereas conservation and enhancement of resident populations of natural enemies via habitat management schemes appear to be more effective to improve biocontrol services in simple landscapes.
While our findings suggest that biological control provided by predators can be an important component of a pest management strategy for lepidopteran pest, it has distinct advantages and disadvantages, which means it should be used as a part (rather than replace) of an integrated pest control program. Advantages over insecticide based approaches include to prevent or delay the development of pesticide resistance, and to contribute to preserve other beneficial arthropods that perform valued ecosystem services like pollination. One disadvantage of using predators is that their densities fluctuate greatly not only among landscapes, but also among years. Such variability could influence the magnitude and stability of pest control services provided by this community of resident natural enemies, so lepidopteran pest may not be adequately controlled by predators in some years. Our results showed that, in principle, augmentative releases of predators could compensate for the inconsistency in the control provided by the naturally occurring predators in complex landscapes. However, cost-calculations are needed to determine if augmentative biocontrol is an economically viable alternative to pesticides. The mechanism that explain the disruptive effect of augmentative releases for pest control in simple landscapes remains to be investigated. Further studies are also required to evaluate if local management manipulations can have the potential to increase pest suppression in simple landscapes. Thus, it can be said that predators can make significant contributions to pest control through their conservation and enhancement, but the reliance on predators as the only strategy of control is likely to be ineffective against lepidopteran pests.
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Education & Outreach Activities and Participation Summary
Outreach events and presentations have allowed us to share our results with the agricultural community. Our project was presented in a field day held at the Homer C. Thompson Vegetable Research farm at Cornell University in September 6th, 2014. In addition, we gave two oral presentations of the preliminary results of this project at the National Meeting of the Entomological Society of America in 2014 and 2015, and two others in the Entomology Department Symposium at Cornell University. We also compiled the objectives of the project as brochures (Biocontrol brochure), and results of my first year as fact sheets for participating growers (Example Fact Sheets). Following final data analysis, a manuscript based on the finding of this project will be submitted to Agriculture, Ecosystems and Environment. And two other publications are in preparation.
- PEREZ, R; NAULT, B.; POVEDA, K. Effects of landscape composition on crop yield mediated by specialist herbivores. Cornell Entomology Department Symposium. Ithaca, NY, USA. January.
- PEREZ, R; NAULT, B.; POVEDA, K. Effects of landscape composition on crop yield mediated by specialist herbivores. Annual meeting of the Entomological Society of America, Minneapolis, MN, USA. November.
- PEREZ, R; NAULT, B.; POVEDA, K. Landscape effect on biological control of cabbage Lepidoptera. Cornell Entomology Department Symposium. Ithaca, NY, USA. January.
- PEREZ, R; NAULT, B.; POVEDA, K. Testing the intermediate landscape complexity hypothesis for augmentative biological control. Annual meeting of the Entomological Society of America, Portland, OR, USA. November.
This project only worked directly with vegetable growers to receive permission to use their farms for the experiment, so in this early stage of the project we were not expecting to see adoption of the strategies studied here. However, we raise awareness about the community of natural enemies on their farms and its role on pest regulation. One of the important finding of this research is that it is not appropriate for all growers to use augmentative releases to control lepidopteran pest. The objectives of future outreach efforts will be to highlight the potential benefits to use augmentative biocontrol and to assist growers in determining where this strategy is more likely to be successful.
Areas needing additional study
Our research documented the diversity of predatory arthropods found in cabbage in central New York and showed that landscape-level processes can have large impacts on predator and pest populations. However, several important issues require further study:
What is the actual contribution that natural enemy complexes, particularly predators, make to pest mortality in cabbage crops? A measure of predator impact across time is critical for farmers to make informed pest management decisions. We need information about when and where natural enemy populations are insufficient to achieve pest control, so that other complementary alternatives can be implemented, for example augmentative releases.
How can we maximize the impact of predatory arthropods at landscape scale?. This study reveals some predator community composition and patterns of variation in response to landscape context, but detailed processes remain to be investigated at the level of species and population dynamics. Further studies are thus needed to explore the relative contribution of different predators on the dynamics of lepidopteran pest. Identifying which factors are driving the abundance of particular species will also help us understand how to maximize the biological control services being provided.
Finally, more studies are needed to evaluate how specific pest management strategies (i.e insecticides, habitat management) might influence natural pest control across different landscape contexts. Some of the questions above will be investigated with additional funding from a USDA-NIFA grant funded to K.P. We hope to continue the research and expand into the cabbage agricultural systems to address other questions related to the use of natural enemies within the framework of a pest-management program.