Northeast Region IPM Grants Projects Funded, FY 2005

Site-specific Management of Resistance (SMOR) in the Control of Apple Scab: Final Phase of Development and Implementation

*Award shown is total amount to be used over the course of the project term.

Project Summary

Apples are the most important fruit crop grown in the NE-IPM region, with a value of $260 Million in 2003. The profitability of producing processing apples has sharply declined, and the sustained viability of the industry will rely on the fresh apple market. One of the most serious and most common causes of intolerable blemishes on fresh apples are scab lesions caused by Venturia inaequalis. The disease is ubiquitous in the NE and must be managed with 4-10 applications of fungicide per season.The arsenal of scab fungicides includes conventional protectants such as mancozeb or captan. These nonspecific and purely protective fungicides have been under continuous scrutiny regarding their toxicology and their poor fit into IPM programs. Several classes of ‘low-risk’ fungicides with post-infection activities are available as alternatives. Unfortunately, all ‘low-risk’ fungicides have developed or will develop resistance, rendering them ineffective in scab control. Outbreaks of scab caused by resistance are unexpected by the growers affected and have become increasingly damaging. Our research over the past 15 years has shown that levels of resistance can vary considerably from orchard to orchard. Many growers, who still could effectively use particular classes of ‘low-risk’ fungicides, have converted back to the conventional protectants to avoid potential crop losses caused by resistance. Other growers continue to apply ‘low-risk’ fungicides in spite of resistance, thereby risking unexpected and severe losses.The goal of the proposed work is to establish and implement Site-specific Management Of Resistance (SMOR) as a service to apple growers. The novel SMOR concept consists of orchard-specific sensitivity tests combined with management recommendations based upon the sensitivity of the particular scab population to all ‘low-risk’ options available. SMOR will allow growers to utilize ‘low-risk- fungicides without risking unexpected damage. Implementation of SMOR will require to validate the diagnostic precision of our orchard-specific sensitivity test, and to establish an infrastructure allowing the implementation of SMOR as a service on demand. The proposed work will be conducted in cooperation between New York as the most important apple-producing state, Massachusetts representing New England, and West Virginia as one of the southern regions of apple production in the NE.

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(1) Fine-tuning the sampling protocol, including selection of sampling sites, shipment of diseased apple leaves, establishing the number of orchard blocks to be tested per production unit, communication of results to participating growers, and evaluating the time after which the tests should be repeated.

(2) Verifying the reliability of management recommendations derived from orchard-specific sensitivities to all classes of modern low-risk fungicides.

‘implementation’ objectives:

(1) Broad dissemination of information and results to growers, consultants and cooperative extension educators.

(2) A targeted survey of apple growers subsequent to our initial dissemination of SMOR information and results to test the response of growers regarding the value they assign to the service.

(3) Design of a business plan to establish the infrastructure for a first example of SMOR as a service.

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Problem, Justification, and Background

Problem

In climates with cool and humid weather conditions during spring, apple scab caused by Venturia inaequalis represents the economically most important disease of apples (MacHardy 1996; MacHardy et al. 2001). Under severe infection conditions, diseased apple trees can be defoliated prematurely, but the economically most important symptoms are scab lesions on apple fruits, which are not tolerated on apple produced for the profitable fresh market. In the US, scab affects the production of apples in all states of the NE-IPM region, Michigan, Virginia, North Carolina and the coastal regions of Oregon and California.

Control of scab with fungicides continues to be the major management tool available to commercial apple growers (MacHardy et al. 2001), with 4-10 applications made during the scab season, depending on the quality of fungicides employed. During the past five decades, apple growers have utilized several classes of scab fungicides, starting in the 1940s with the introduction of the carbamates such as ferbam and progressing to the EBDCs (such as mancozeb) and captan both introduced in the 1950s. The mode of action of the EBDCs and captan, which remain in wide use, is nonspecific. Consequently, such fungicides must be confined to the surface of the plant tissue to be protected. If they were allowed to penetrate the cuticles of leaves and fruits in order to reach the scab pathogen already established inside the host, they would act phytotoxic (Köller 1999).

The nonspecific mode of action inherent to all older conventional protectants has advantages and disadvantages. The most striking advantage is that resistance to these fungicides has never become a problem. Disadvantages of the EBDCs and captan have been the continuous toxicological scrutiny by EPA. Captan was granted a Reregistration Eligibility Decision (RED) under FQPA and appears to remain available in the near future. However, a RED is still pending for the EBDCs, and their utility has further been restricted by a recent ban of EBDC use in the production of apples exported to Europe. Furthermore, captan is phytotoxic when applied with mineral oils and the EBDCs are toxic to predatory mites. Both effects are incompatible with the integrated control of mites (Agnello et al. 1999).

An additional important disadvantage of conventional protectants is the inherent lack of post-infection activities (Szkolnik 1981). They must be deposited on plant surfaces prior to infection events in order to prevent penetration of pathogen spores into the host tissue, and fungicide deposits must be renewed frequently in order to protect new growth and to replenish residues washed off during rain events. In order to be effective, control programs must be started very early, at the growth stage of ‘green tip’, and then continued with 6-9 applications at weekly intervals. These routine applications of conventional protectants do not comply with the IPM principle of employing pesticides only when needed.

Reliable forecasting models for scab infections have been developed, refined and implemented (MacHardy et al. 2001), and they enable apple growers to respond to infection periods after they have occurred. Such targeted responses would require highly specific scab fungicides active in a post-infection mode of application. The first post-infection scab fungicide introduced in the early 1960s was dodine (Syllit). Dodine was accepted rapidly as a new and very convenient tool in the post-infection management of scab (Gilpatrick 1982). Other classes of post-infection fungicides introduced in succession were the benzimidazoles benomyl (benlate) and thiophanate (Topsin M) in the early 1970s (Gilpatrick 1982), the sterol-demethylation inhibitors (DMIs) fenarimol (Rubigan), myclobutanil (Nova) and triflumizole (Procure) in the late 1980s (Köller et al. 1997), the strobilurins kresoxim-methyl (Sovran) and trifloxystrobin (Flint) in 1999 (Köller et al. 2004) and the anilinopyrimidine (AP) cyprodinil (Vangard), also in 1999, with the AP pyrimethanil (Scala) pending registration (Köller et al. 2005).

As described in greater detail below, populations of Venturia inaequalis, the causal agent of apple scab, have developed or will develop resistance to all classes of specific post-infection fungicides (Köller 1990; 1994; 1995; 1996; 2001). We define resistance as the sensitivity of a particular orchard population at which a formerly successful fungicide class failed to provide commercially acceptable control of scab (Köller et al. 1997; 1999). We have found over the past 15 years of monitoring sensitivities of V. inaequalis populations that outbreaks of resistance were unexpected by the growers affected and rarely caused by inadequate management practices (Köller et al. 1997; 1999). We also found that resistance, once established in an orchard, remained stable over several decades (Köller et al. 1997; Köller et al. 2001).

The economical losses incurred by unexpected outbreaks of resistance have increased dramatically over the past decade. Traditionally, apple production in the NE has served both the fresh and the processing market. During the past five years, however, the profitability of producing apples for the processing market (in particular the ‘juice’ market) has sharply declined in response to low-cost imports of juice concentrate. A statement made under the 2002 NE PMC “Crop Profile for Apples in Rhode Island” describes these economic constraints: “If adequate pest control products were not available, cider apples would be the only option with values at $ .03 per pound vs. $ .30 - .40 per pound of wholesale apples currently”. With a typical yield of 18,000 pounds/acre, the crop value would calculate to: ‘Juice apples’ = $540/acre; ‘Wholesale apples’ = $6,300/acre. A single fully developed scab lesion will downgrade an apple from “wholesale” to “juice” quality, and thus will decrease its value by 90%. Consequently, unexpected outbreaks of practical resistance to the various classes of ‘low-risk’ scab fungicides have caused and will cause increasingly severe economical losses. The question is, whether and how growers can be protected from such unexpected losses without being forced to abandon the use of all modern ‘low-risk’ fungicides.

Resolving this question would require that apple growers (1) are aware of the level of resistance to all post-infection fungicide options in their individual orchards, and that (2) this knowledge would allow them to design ‘state of the art’ scab management programs without risking unexpected control failures. This rational approach toward fungicide use and resistance management necessitates the development of a novel concept: The ‘Site-specific Management Of Resistance’ (SMOR). As described below, we have developed a set of tools that will allow us to introduce SMOR into the management of apple scab.

Background

Detection of fungicide resistance. We have measured in V. inaequalis populations, over the past 15 years, shifts toward resistance to the DMIs (Köller et al. 1991; 1997; Smith et al. 1991), dodine (Köller et al. 1999), the benzimidazoles (Köller and Wilcox 2001), the strobilurins (Köller et al. 2004) and the APs (Köller et al. 2005). Our results have contributed substantially to the characterization of two general routes of resistance development (Köller 1990; 2001). Resistance to fungicides can develop either as the rapid selection of immune target site mutants (with benomyl-resistance as the classical example), or as the gradual selection of phenotypes carrying several unrelated resistance genes, which individually confer a small degree of resistance (Köller 1990; 2001). However, isolates of the pathogen carrying the majority or all of these genes will respond least sensitive to a new fungicide and will be selected over time. In this scenario of multigenic resistance, however, selectable phenotypes remain accessible to inhibition at higher doses of the fungicide. Consequently, high application rates will slow the speed of their selection and thus, the development of resistance (Köller and Wilcox 1999). The gradual path of multigenic resistance was documented for dodine (Köller et al. 1999), for the DMIs (Köller et al. 1997), the APs (Köller et al 2005) and the strobilurins during their initial phase of resistance development (Köller et al. 2004). As apparent from this list of case studies, the importance and impact of resistance progressing through a multigenic path was underestimated in the past (Köller 2001).

The detection of multigenic shifts of orchard sensitivities requires (1) a quantitative sensitivity test, (2) tests conducted with a sufficiently large sample size of individual V. inaequalis isolates and (3) the establishment of data representing the two sensitivity extremes: baseline sensitivities prior to the use of a new fungicide class, and the threshold sensitivities constituting the stage of practical resistance (Köller et al. 1997; 1999). Starting in 1998, we have developed such test procedures for the DMIs (Smith et al. 1991; Köller et al. 1997), for dodine (Köller et al. 1999), the benzimidazoles (Köller and Wilcox 2001) and the strobilurins (Olaya and Köller 1999b).

During our monitoring of orchard sensitivities, we realized that many apple growers either under- or overestimated the resistance status of their orchards, leading either to the continued use of fungicides that had reached the status of resistance, or to the underutilization of fungicides that could still be used successfully (Köller et al. 1997; 1999). Our results also suggested that the level of resistance was largely orchard-specific, which was expected from the relatively local epidemiology of V. inaequalis (MacHardy 1996). However, we also realized that our previous sensitivity tests had too be simplified and unified in order to serve as a viable tool in SMOR. Respective projects were initiated in 2002 and continued during 2003 and 2004. Funding for the pilot studies was provided by the grower-governed NY Apple Research and Development Program.

We have developed a unified and simplified sensitivity test, and we found that the reproducibility and precision of our new test was sufficient to rank orchard sensitivities into four functional categories (manuscript in preparation). However, the SMOR concept would not only require sensitivity data but also predictions of fungicide performances deduced from such orchard-specific sensitivities. This correlation of sensitivities with expected fungicide performances was accomplished through performance trials in our experimental orchards with known levels of resistance and from fungicide performances in commercial orchards (Köller et al. 1999; Köller and Wilcox 1999; Köller et al. 2004; Turechek and Köller 2004; Köller et al. 2005). The four functional categories we have reported to growers are:

sensitive	good performance is expected
slight shift	good performance is expected under moderate disease pressure and/or at high label rates
strong shift	performance must be supplemented
resistant	insufficient contribution to scab management

History of resistance development in New York. Widespread resistance to dodine was documented in the early 1970s as the first case of fungicide resistance (Gilpatrick 1982). We showed retroactively that the path of resistance development was multigenic and gradual, and that practical resistance was reached after approximately 60 dodine applications in total were applied (Köller et al. 1999). In response to spreading resistance, dodine was rapidly replaced by the class of benzimidazoles. However, it was found that benzimidazole resistance developed even faster than resistance to dodine (Gilpatrick 1982), and by the early 1980s, benzimidazoles had lost their utility in the management of scab. The course of resistance development was characterized as the rapid selection of immune target site mutants, constituting the first case of monogenic target site resistance (Köller and Wilcox 2001). For several years, most apple growers in New York and elsewhere had to revert back to the management of scab with conventional protectants such as EBDCs or captan.

The new class of DMIs introduced in the late 1980s offered a new opportunity. These fungicides provided excellent post-infection activities and allowed the design and implementation of a highly efficacious and integrated ‘delayed four-spray program’ (Wilcox et al. 1992; Agnello et al. 1999). Our efforts were focused on characterizing the type of resistance to be expected for the DMIs, to proactively monitor resistance development to this new class of ‘low-risk’ fungicides, and to develop and test effective anti-resistance measures. We were able to document that DMI-resistance followed the multigenic route (Smith et al., 1997; Köller et al. 1997), and we could propose a novel high-dose strategy effectively slowing the speed of resistance development (Köller and Wilcox 1999). Although successful, these recommendations did not halt the slow emergence of DMI resistance (Köller et al. 1997; Köller et al. 2005).

In response, the new classes of strobilurins and APs were introduced in 1999. In the strobilurin case, we initiated a project to proactively assess the risk of resistance prior to their commercial introduction. Our risk assessment studies suggested that resistance to the strobilurins could be expected to develop as a gradual multigenic shift of population sensitivities (Olaya and Köller 1999a; 1999b), or as a target site mutation leading to immunity of respective mutants (Zheng et al. 2000). Our predictions were fully confirmed recently. Following initially multigenic sensitivity shifts, immune target site mutants had emerged after a total of 20-30 strobilurin applications were made in an apple orchard in Germany (Köller et al. 2004). Our current recommendation is to slow the initially multigenic sensitivity shifts by applying the highest label rates (Turechek and Köller 2004), a strategy that might also delay the emergence of immune target site mutants (Avila-Adame and Köller, 2002a; 2002b; 2003).

For the class of AP fungicides, we observed that orchard sensitivities varied widely prior to the first use of these fungicides. We were able to demonstrate that orchard sensitivities to the new class of APs were partly correlated with the status of DMI resistance (Köller et al. 2005), a new phenomenon most likely explained by repeated rounds of resistance development (Köller and Wilcox 2001; Köller et al. 2005). At our fully DMI-resistant test orchard, the contribution of APs to scab control was lower than for the more economical EBDCs used at their lowest label rates (Köller et al. 2005). Consequently, use of APs could not be recommended in such DMI-resistant orchards. In view of the observed performances, the AP sensitivity at our test site was designated as ‘strongly shifted’ (= scab control must be supplemented).

Status quo of fungicide resistance. With our new and unified test in hand, we have measured the sensitivities of 17 commercial orchard sites, mostly located in New York but also in Virginia. Many but not all orchards participated in a multi-state RAMP project aimed at comparing ‘conventional’ with ‘soft’ insecticide programs. Our sensitivity survey in 2003 and 2004
(Table 1) revealed that after 15 years of DMI use, 71% of the orchards we tested had reached the status of DMI resistance (Table 1). This picture is slightly biased by the fact that four of the orchards were tested, because growers had experienced unexpected control failures with their DMI programs. However, in all other resistant orchards, DMIs had not been used for several seasons.

Table 1. Sensitivities of Venturia inaequalis populations in commercial apple orchards tested in 2003 and 2004.

Orchard	DMIs	Dodine	Strobilurins	APs
1	strong shift	sensitive	slight shift	sensitive
2	resistant	resistant	slight shift	strong shift
3	resistant	slight shift	sensitive	strong shift
4	resistant	sensitive	slight shift	strong shift
5	resistant	resistant	strong shift	resistant
6	slight shift	sensitive	slight shift	strong shift
7	strong shift	slight shift	slight shift	strong shift
8	resistant	resistant	slight shift	strong shift
9	resistant	sensitive	sensitive	slight shift
10	slight shift	sensitive	slight shift	strong shift
11	strong shift	slight shift	slight shift	strong shift
12	resistant	slight shift	slight shift	slight shift
13	resistant	resistant	strong shift	resistant

We also found that the incidence of DMI-resistant orchards has surpassed the level of dodine resistance (Table 1). Unfortunately, all orchards diagnosed dodine-resistant were also resistant to the DMIs. We concluded that the re-integration of dodine into scab management programs, be it alone or in mixture with DMIs as an attractive alternative (Köller and Wilcox 1999), appears feasible, but only if growers are aware of the dodine sensitivity at their candidate orchards. Without that knowledge, many growers would risk to re-introduce dodine into a dodine-resistant environment. We had found previously that dodine resistance remained stable in orchards, where dodine had not been used for 20 years (Köller et al. 1999). In our most recent survey (Table 1), we also found that resistance persisted in orchards replanted at sites with resistance problems in the 1970s, and that orchard managers were not aware of the fact.

As apparent from our sensitivity survey, the initially multigenic shifts of orchard sensitivities to the new class of strobilurins, as predicted (Köller et al. 2004), have been initiated in the majority of orchards we tested (Table 1). Fortunately, we have not found immune target site mutants thus far (manuscript in preparation). Our survey (Table 1) also showed that AP sensitivities were lower than baseline in all DMI-resistant orchards, even though APs had never been used in any of the orchards tested. Based upon the poor performance of APs in our DMI-resistant experimental orchard (Köller et al. 2005), we had to rate the majority of orchards as “strongly shifted” (good performance must be supplemented). This AP example reflects the complications inherent to the new phenomenon of multiple fungicide resistance caused by repetitive rounds of resistance development (Köller and Wilcox 2001; Köller and Wilcox 2005). At present, the integration of APs into scab management programs without knowledge of their sensitivities in particular orchards appears risky, at least in New York but most likely also in other states of the NE-IPM region (Köller and Wilcox 2005).

Challenges and opportunities. The status quo described above for New York and Virginia (and most likely other states) is alarming. Although a total of nine post-infection fungicides are available to growers (Syllit, Topsin M, the three DMIs Nova, Procure and Rubigan, the two strobilurins Flint and Sovran, and the two APs Vangard and Scala, the repeated development of resistance has devalued their utility as tools in IPM and resistance management. Unfortunately, new classes of ‘low-risk’ fungicides with utility in post-infection control of scab are not forthcoming at present.

In order to assist the apple industry, the future IPM program for apple scab with ‘low-risk’ and post-infection fungicides will have to be guided by two equally important principles:

(1) The speed of resistance development must be slowed down. As we have documented (Köller and Wilcox 1999), the previously prominent anti-resistance strategy of mixing a post-infection fungicide under risk with a conventional protectant is unlikely to accomplish the task. The separation in space of the two mixture components allows resistant isolates to be selected. Consequently, the burden of scab control will shift steadily toward the conventional protectant. When the status of resistance is reached, the protectant applied at a low rate and at a post-infection schedule will fail to control scab. A high-dose strategy has been shown to be effective in slowing the speed of resistance, but this strategy is only applicable to the scenario of multigenic resistance (Köller and Wilcox 1999; Turechek and Köller 2004). It is undisputed, however, that the useful lifetime of any particular fungicide class will be prolonged if scab management programs involve several different fungicides per season. For example, a total of approximately 60 dodine applications were shown to establish the status of resistance. These 60 applications could be spread over 10 seasons with six applications per season, or over 30 years with two applications per season (Köller et al. 1999).

(2) Growers must be protected from unexpected losses caused by resistance. This task can only be accomplished by SMOR, the site-specific management of resistance aimed at employing all classes of efficacious ‘low-risk’ fungicides at a particular site. To be successful, SMOR must not only measure the sensitivities to all available fungicide options but also reliably predict fungicide performances deduced from their sensitivities. Although our current experience was limited in scope, the results are encouraging. All control failures coincided with the diagnosis of ‘resistance’ to the fungicides used, and management changes based upon orchard-specific sensitivities yielded excellent levels of scab control during the next following seasons (manuscript in preparation).

Implementation of SMOR as the major objective of our proposed project will allow apple growers to assess the sensitivity status of V. inaequalis in their individual orchards and then to design ‘tailor-made’ IPM programs without risking unexpected economical losses. Successful implementation of SMOR will require:

(1) A final technical development phase to refine the important questions of sampling and shipment of diseased apple leaves and, perhaps most importantly, to insure the safety and success of management recommendations based upon measured orchard sensitivities to all current ‘low-risk’ options.
(2) Promoting the awareness of current problems with resistance (= unexpected yet severe economical losses) and conveying the benefits offered by SMOR. This task will be crucial to a broad implementation of the SMOR service, because the cost for the service will have to be covered by the growers requesting the service and will necessitate the establishment of a fee structure to make this crucial service available to growers on demand.

Both tasks comprise the Objectives of the project proposed here.

Justification

With increasing cases of unexpected outbreaks of apple scab in well-managed orchards, which are most often caused by fungicide resistance, growers must be provided with tools to adequately assess the sensitivities to all fungicide options in their orchards to make fully informed and economically sustainable management decisions. In the past, sensitivity tests and the development of anti-resistance strategies were focused on single classes of fungicides. It became clear, however, that general tactics of proactive resistance management must not only involve one particular fungicide class but rather the entire arsenal of efficacious options. Only full knowledge of all options considered effective at a particular orchard site will protect growers from unexpected and increasingly costly crop losses and will, at the same time, prolong the useful lifetime of our modern ‘low-risk’ fungicides.

The task can only be accomplished by testing the sensitivities of V. inaequalis populations to all available fungicide classes at-site, followed by recommendations of effective management options deduced from the site-specific spectrum of fungicide sensitivities. The combination of sensitivity tests with management recommendations constitutes the principles of our novel SMOR concept, the site-specific management of resistance.

Our long-term work on the detection and management of fungicide resistance, which involved all modern ‘low-risk’ fungicides, culminated in the opportunity to implement a SMOR service. As described in detail elsewhere, we have developed a unified sensitivity test, and we have found that our predictions of fungicide performances deduced from orchard sensitivities were accurate and reliable. We concluded that our work has reached the proof-of-principle stage and justifies moving to the implementation phase. Broad implementation of SMOR will require: Optimization of several technical aspects with importance to SMOR, verification of its predictive value and preparing the ground for broadly implementing SMOR as a service offered to growers.

The need for SMOR in the management of apple scab with ‘low-risk’ fungicides has been emphasized as a research priority in the NE-IPM region:

(1) The current ‘New England Apple Pest Management Strategic Plan’ lists, under ‘Apple Scab’: “Cost effective resistance monitoring tools”.

(2) The Northeastern IPM Center lists, under “Fruit IPM Working Group Priorities”: “Resistance monitoring for fungicides in apples.”

(3) Under the 2003-2004 list of New York-IPM Stakeholder Research Priorities, ‘Fungicide resistance management and monitoring for apple scab and powdery mildew’ was entered as a ‘top research priority’. Stakeholder interest is also evident by the continuous funding of our pilot projects by the NY Apple Research and Development Program, a funding source governed by growers.

In addition to our focus on the management of apple scab, the general need for managing pesticide resistance has received renewed attention as a priority of future IPM research:

(1) The 2003 ‘National Roadmap for IPM’ states in its introduction: “Pest management systems are subject to constant change and must respond to a variety of pressures. For example, growers require access to a diverse array of pesticides because numerous pest species have developed resistance.” Under seven examples of IPM ‘research needs’, the roadmap lists: “Develop new diagnostic tools, particularly for plant diseases and for detection of pesticide resistance in pest populations, including weeds.”

(2) In a 2003 symposium organized by the Council for Agricultural Science and Technology (CAST) and entitled ‘Management of Pest Resistance: Strategies Using Crop Management, Biotechnology and Pesticides’, it was concluded that proactive resistance management will be required to prolong the useful lifetime of valuable ‘low-risk’ pesticides and to protect crop producers from unexpected economical losses (CAST 2004; Köller 2004).