Christina D. DiFonzo
Department of Entomology Michigan State University
East Lansing, MI 48824-1115
David W. Ragsdale and Edward B. Radcliffe
Department of Entomology, University of Minnesota
St. Paul, MN 55108-6125
Integrated pest management involves using multiple tactics to effectively manage pest populations while minimizing environmental impact and reducing pesticide use (an implied benefit). While this philosophy has been adopted successfully in a number of different systems, the routine use of pesticides is still considered necessary in situations where no damage is tolerated. Insect-vectored diseases of both plants and animals present such a problem, where defining a threshold for the vector is difficult due to low (or no) tolerance for disease. An example of such a system is aphid-vectored viruses in seed potato. This case study focuses on research conducted on potato in the midwestern United States, but can serve as a general example of how alternatives were found to reduce pesticide use even in situations of "no tolerance".
The potato (Solanum tuberosum L.) is an important crop worldwide. Potato production is not an easy task, as potatoes are affected by multiple key pests, including several viruses which contribute to "running out" , or degeneration, of seed stocks. Potato leafroll virus (PLRV) and potato virus Y (PVY) are the most important of these viruses worldwide. PLRV is a phloem-limited luteovirus which infects about 20 species, including potato and tomato, in five plant families (Harrison 1984). Mechanical transmission does not occur, although graft transmission is possible. Symptoms of PLRV in potato include reddening and brittleness of leaves, stunting, necrosis, and characteristic rolling or cupping of foliage. PVY is the type member of the Potyviridae, the largest family of plant viruses. PVY has a wide host range and is mechanically transmissible to approximately 120 species in five families (Edwardson 1974, Horvath 1983). Important hosts include pepper, tomato, tobacco, nightshade, and potato. Symptoms of PVY infection in potato are mosaic, crinkling, and necrosis of leaves; secondarily infected plants are stunted and have brittle foliage (de Bokx and Huttinga 1981). Both PLRV and PVY are transmitted by aphids (Homoptera: Aphididae).
Control of PLRV and PVY involves a number of general cultural techniques to reduce inoculum. Most seed lots originate in tissue culture to remove all pathogens. The resulting disease-free plantlets are used to produce minitubers in the greenhouse, which in turn go to the field to produce several generations of seed potato. To regulate seed production, certification schemes are in place in U.S. states and Canadian provinces; these limit the number of years a seed lot can remain in the system, and set virus tolerances for each generation. For example, in the Red River Valley (Minnesota), seed fields are inspected by state personnel several times during the growing season, and a tuber sample from every seed lot is entered in a winter grow out to assess virus incidence. Seed lots can only be recertified for five years, and each year must meet rigorous standards for PLRV and PVY . In the field, general practices of sanitation reduce PLRV and PVY inoculum - destroying cull piles to prevent sprouting, and roguing and removing infected plants from the field. Some growers in the Red River Valley stopped growing certain cultivars which do not show PVY symptoms very well and make state inspections and roguing more difficult. Others now plant early generation (G0 - G1) seed fields in isolated areas away from potentially "dirty" later generation seed and tablestock fields.
PLRV and PVY management, however, is not enough. Virus detection is never 100% effective, plus inoculum may come from sources beyond a grower's control. These sources include certified seed lots imported from other states with higher virus tolerances, seed fields managed by other growers, tablestock fields, garden plots, alternate weed hosts, and nearby crops such as pepper and tomato. Since an area is never virus-free, aphids responsible for transmission must also be managed to reduce virus incidence. The strategy for managing aphids differs for each virus depending on the insect/pathogen relationship.
In the field, aphids are the most important means of PLRV and PVY spread. However, the transmission is quite different for each virus. PLRV is transmitted by several aphid species, all potato colonizing species; green peach aphid is the most efficient vector (MacGillivray 1981). PLRV transmission is termed persistent, i.e., acquisition and inoculation take hours, and is favored by deep feeding in the phloem tissue. There is a latent period between acquisition and inoculation, time for PLRV particles to cross the gut wall and enter the salivary gland. Thus, the transmission process of PLRV by aphids takes a minimum of 12 hours, more often several days. However, once infective an aphid can transmit PLRV effectively for its entire life. This mode of transmission favors aphids which spend time in the crop, apterous (non-winged) individuals of species which colonize and feed on potato.
In contrast, PVY is transmitted by at least 50 different aphid species (DiFonzo 1996), although green peach aphid is again the most efficient vector. PVY transmission is non-persistent, i.e., acquisition and inoculation occur in minutes and is favored by brief epidermal probes. There is no latent period between acquisition and inoculation. Thus the entire transmission process takes just minutes, although infectivity is lost after several probes (Bradley and Rideout 1953). This mode of transmission favors aphids which probe frequently and move quickly from plant to plant, alate (winged) individuals of species which sample many plants including potato.
Traditionally, seed producers used calendar-based insecticide applications to control aphids in potato. Based on the transmission characteristics of PLRV, it is not surprising that aphid vectors of PLRV, and hence PLRV spread, are controlled by insecticides. This is particularly true in regions like the Red River Valley, where there are no PLRV sources (alternate weed or crop hosts) outside the potato crop itself, and winged aphids rarely arrive carrying PLRV (Hanafi et al. 1989). In this case, apterae within the crop are responsible for the majority of PLRV spread, and routine application of compounds like methamidophos (Monitor) disrupts the transmission cycle. Aphids are killed before they have a chance to acquire PLRV, or during the latent period when they are not yet infective. Since few effective aphicides are available to growers, it is important to manage the remaining compounds to prevent overuse. Compounds like methamidophos are not only hazardous to handle, but overuse could lead to adverse environmental consequences or insecticide resistance.
The most obvious way to manage insecticides is to treat on a threshold. A threshold for direct damage by aphids was already available for tablestock potatoes in the Red River Valley: 300 aphids per 105 leaves (Cancelado and Radcliffe 1979). This density was too high for use in seed fields, and it was considered impossible to develop a threshold for aphids in seed potato where the main concern was PLRV spread. However, Flanders et al. (1991) successfully developed such a threshold, 10 green peach aphids per 100 leaves. The PLRV spread from a point source in plots first sprayed with methamidophos at 10 aphids per 100 leaves was no greater than PLRV incidence in plots treated with a systemic aphicide at planting plus weekly sprays of methamidophos. This was the first threshold developed, based on limiting disease incidence, for a vector of a plant.
Flanders conducted her threshold experiments using the potato cultivar Russet Burbank, a widely grown potato that is notoriously susceptible to PLRV. Thresholds are fine tuned by taking other factors into consideration, such as host plant resistance. In the case of potato, no cultivars are resistant to aphids, but some are resistant to PLRV. Experiments using other cultivars showed that the action threshold for Kennebec (moderately PLRV resistant) could be raised to 30 aphids per 100 leaves, while that for Cascade (highly PLRV resistant) could be increased to 300 aphids per 100 leaves, compared to Russet Burbank (10 aphids per 100 leaves) (DiFonzo et al. 1995). The threshold for Cascade equalled the direct damage threshold for tablestock potato.
The bottom line is the decrease in insecticide use from treating on a threshold rather than applying calendar-based sprays. In the previous experiment, plots with calendar-based treatments (threshold = 0) received a systemic aphicide at planting as well as weekly applications of methamidophos for 7 weeks. In contrast, Russet Burbank plots first sprayed at a threshold of 10 aphids per 100 leaves received no systemic at planting and 6 methamidophos applications. Furthermore, Cascade plots first sprayed at 300 aphids per 100 leaves received just 3 methamidophos applications. Not only was it possible to determine a spray-saving threshold for an aphid vector of a virus, but the threshold for the vector could be modified to account for host plant disease resistance, reducing insecticide use even further..
In contrast to PLRV, PVY spread is usually not reduced by insecticide applications. In fact, large numbers of green peach aphid apterae within a field do not necessarily lead to a concomitant increase in PVY incidence. Ragsdale et al. (1992) demonstrated that Russet Burbank plots sprayed on the thresholds suggested previously for PLRV control (10 to 300 aphids per 100 leaves) and above (up to 10,000aphids per 100 leaves) did not have significantly more PVY than plots treated weekly with insecticide. Apparently apterae living on the potato were not mobile enough to contribute to PVY spread, and alate aphids from outside the plots were responsible for transmission. Insecticides cannot kill immigrating alate aphids quickly enough to prevent PVY acquisition and inoculation, and thus the weekly sprays did not reduce PVY spread. Alatae are now recognized as playing a significant role in PVY spread in many potato growing areas of the world, but the important species differ from region to region depending on local cropping practices and crop rotations.
In the Red River Valley, a situation arose in which potato virus Y was a problem, even in early generation (G0 and G1) seed lots with little field exposure. PVY inoculum was traced to seed lots imported from other states with less stringent virus limits, and infection probably increased via neglected cull piles of infected seed and in fields planted with the PVY-symptomless cultivar Russet Norkotah. During the epidemic, studies showed that PVY infection of indicator plants in the field correlated with the peak flight of aphids from common crops and weeds in the Red River Valley: pea, sunflower, thistle, and turnip aphids, as well as four grain aphid species (DiFonzo 1996). Protecting seed - especially early generation fields - from these alate aphids produced in neighboring crops and weeds was impossible with insecticides, although growers continued to apply insecticides in the mistaken belief that potato colonizing aphids within the crop were responsible for PVY spread in their fields. Alternative management strategies were needed that did not involve ineffective attempts to kill aphids, but which instead used knowledge of aphid behavior and PVY transmission characteristics to reduce virus spread.
Aphids tend to colonize (and thus spread virus to) edges of fields where the contrast between green plants and dark soil is greatest (A'Brook 1968 & 1973, Smith 1969, Storey and Godwin 1953) and where eddies in wind currents deposit aphids in large numbers (Broadbent et al. 1951, Johnson 1950). Unfortunately, producers of early generation seed potato tended to create conditions favorable for aphid colonization by surrounding their small green fields with a dark cultivated soil border. This cultivated border kept the area clean and reduced weeds, but it also created plant/soil edges attractive to landing aphids potentially carrying PVY. Early generation seed fields were particularly vulnerable because of their small size and large amount of edge relative to area.
To eliminate these edges and reduce PVY incidence, crop borders were tested around potato plots. Plot surrounded by a 12-15 foot border had significantly less PVY in tubers at the end of the season than plots surrounded by dark cultivated soil: 35.0% versus 47.8% in 1992, and 2.7% versus 6.8% in 1993 (DiFonzo et al. 1996). In every row sampled, PVY incidence was less in plots with, compared to plots without, a crop border. However, the most significant reductions in virus occurred on the outer edges of crop-bordered plots. Soybean was the preferred crop to use as a border because it was not a host for aphids or potato viruses, but sorghum and wheat (although hosts for grain aphids) also worked well as borders (DiFonzo et al. 1996). Even a border of potato itself reduced PVY spread to inner rows of potato plots (Ragsdale and Radcliffe, unpublished data).
Early work by Simons (1960) found that a 10-foot border of sunflower significantly reduced PVY spread to pepper crops. He speculated that the border acted as a barrier to flying aphids. However, in the potato experiments, landing rates of aphids in plots with and without a border were similar. Aphids were therefore not prevented from landing in the potato. Based on aphid behavior, aphids - some carrying PVY - were attracted to green plant/dark soil interfaces in the experiment. In the case of plots surrounded by dark soil, aphids landed on the potato/soil edge, the outer edge of the plot itself. In the case of plots surrounded by a crop border, aphids landed on the crop border/soil edge. Viruliferous aphids landing on the potato/soil edge probed and transmitted PVY to the potato; viruliferous aphids landing on the crop border/soil edge probed and, in the process, lost their charge of virus to the non-host crop. Outer edges of potato plots protected by a crop border were thus exposed to fewer viruliferous aphids than plots without a border because the border "filtered" PVY from aphid mouthparts.
It was thus possible to use a simple cultural technique to reduce virus incidence in seed potato. From a production standpoint, a crop border is easy to plant, requires no specialized equipment, needs no extra land (the grower would normally maintain a cultivated border) and is compatible with current production practices. It can be used with any cultivar, and around a field of any size or shape, although a border would be most effective around small, valuable early generation seed fields. Interestingly, a border targets viruliferous alate aphids, something that is impossible to do with traditional insecticides no matter how often they are applied.
Integrated control of aphid-vectored viruses is complex and must take into consideration both the virus and the vectors. In the Red River Valley, virus control in seed potato uses a variety of tactics to reduce inoculum levels and aphid numbers, both within and outside the crop. PLRV and PVY inoculum reduction is achieved by cultural techniques which have been recommended for years, and by seed certification schemes. Aphid reduction has generally been accomplished with insecticides, but recent work has demonstrated that chemical use can be reduced. Aphids which colonize potato are responsible for the majority of PLRV spread, and can be controlled with insecticides.
However, treatments should begin only when a threshold is reached. Winged aphids coming from outside the crop are responsible for the majority of PVY spread, and are not killed by insecticides sprayed used against potato-colonizing aphids. Instead, eliminating inoculum, isolating fields, and using a crop border to "clean" aphid mouthparts are a better strategy for PVY reduction. A seed producer integrating all these components would plant the cleanest certified seed possible in an isolated area; include a crop border around his field; rogue the field for virus several times during the season; and spray aphicide only when leaf samples determine a threshold has been reached. Thus, aphid-vectored virus management in Red River Valley seed potato is beginning to meet the goals of IPM - use of multiple tactics, integration of techniques to reduce both virus and vectors, and reduction of pesticide use - despite the complex nature of the system.
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