Potential of Earthworms as Biocontrol Agents of Scab and Leafminers in New England Apple Orchards

Final Report for LNE97-081

Project Type: Research and Education
Funds awarded in 1997: $99,790.00
Projected End Date: 12/31/2001
Matching Federal Funds: $33,452.00
Matching Non-Federal Funds: $25,200.00
Region: Northeast
State: New Hampshire
Project Leader:
William E. MacHardy
University of New Hampshire
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Project Information


This project explored the use of the earthworm as a biocontrol agent for apple scab disease and leafminer pupae. It was hypothesized that orchards with a history of ecologically-oriented management practices would encourage earthworm populations, but there was no correlation with the type of management practices. However, levels of total leaf litter removed were >75% in 25% of the orchard evaluations. This could have important implications for decision-making with respect to pest management strategies, because the percentage loss of leaf litter is related directly to the percentage loss of potential inoculum for apple scab and overwintered leafminer pupae.


This study was intended to be Phase I of an eight year project that was divided into three phases, with Phase I to be completed in two years. Its main objective was to determine if earthworms have a potential to remove a substantial percentage, i.e., >75%, of the leaf litter by bud break under New England conditions. It was expected that Phase I would identify orchards with exceptionally high and poor leaf removal and that scrutiny of a detailed Orchard Information Form completed for each orchard would provide insight into practices and conditions that may be favorable or unfavorable for earthworm removal of leaf litter. Objective I was evaluated in each orchard by determining the percentage of leaves buried by earthworms in the orchard border, within the orchard, and within the orchard relative to the orchard border. It was expected that the diversity of crop management systems tested would identify orchards with very high and very low leaf burial (earthworm activity).

Success occurred in an orchard if leaf burial was within the range (≥ 75% burial) that can be coupled to a sanitation threshold/PAD threshold strategy and tactics that will improve the efficiency of fungicide usage to control scab and (ii) above a minimum amount needed to delay the buildup of leafminers on apple leaves to the extent that an action threshold to apply insecticide to control leafminers will be delayed or not reached.


There was no relationship between orchard management practices during the past five years and the amount of leaf litter removed by earthworms and the activities of other organisms that feed on the leaf litter, but leaf litter removal within an orchard was reasonably consistent: only two of 21 sites had a significant change in leaf removal in 1999 compared with 1998. One site had a significant decrease in leaf removal in 1999, i.e., 28% compared with 91% in 1998, and the other site had a significant increase in leaf removal in 1999, i.e., 69% compared with 18% in 1998.

A herbicide strip had little impact on leaf removal. Of 24 sites in 1998 and 1999, only two sites had significantly lower leaf removal from a herbicide strop compared to leaf removal from sod.

Leaf removal within an orchard was comparable to leaf removal from plots adjacent to the orchard. Of 21 sites in 1998 and 1999, only two sites had a significant difference in leaf removal between sod plots inside and outside an orchard. One site had a significant decrease in removal outside the orchard, i.e., 97% removal inside compared with 27% removal outside the orchard. The second site had a significant increase in leaf removal outside the orchard, i.e., 74% removal inside compared with 100% removal outside the orchard.

There was a significantly high loss of leaf tissue (>75%) in five of 22 orchards in 1998 and 9 of 36 orchards in 1999.

Impacts and Potential Contributions

The pest management program in each orchard was classified as (a) “organic,� (b) “advanced IPM,� (c) “minimal IPM,� or (d) “conventional� with respect to selecting and scheduling pesticides. It was hypothesized that orchards with a history of ecologically-oriented management practices would have the greatest leaf removal, but there was no correlation with the type of management practices. Because orchards that had been following organic and advanced IPM practices and guidelines were not correlated with the greatest amount of leaf removal, presumably due to the greatest earthworm activity, Phase II was not funded. Thus, this study will not impact in any noticeable way on apple pest management practices. However, it was demonstrated that in approximately 25% of the orchard trials, greater than 75% of the leaf litter was removed, indicating that if we understood more about the influence of environmental conditions, particularly soil health, on earthworm populations in an orchard, which was to be the main focus of Phase II, it is conceivable that earthworms could play an important role in the management of scab and leafminers.

Project Objectives:

a. Quantify leaf litter removal by earthworms as a measure of the potential of earthworms to reduce primary inoculum of Venturia inaequalis, the causal agent of scab, and overwintering populations of the apple blotch leafminer and spotted tentiform leafminer in New England apple orchards that use conventional, IPM/low-input sustainable, or certified organic pest and crop management practices or have been abandoned.

b. Develop case histories of orchard management in selected apple orchards throughout New England that have followed conventional, IPM/low-input sustainable, and certified-organic programs of pest and crop management and compare leaf litter burial with orchard case histories to provide insight into orchard practices favorable or unfavorable to earthworms and leaf burial.

c. Develop an EDUCATION/OUTREACH plan that will introduce apple growers, Fruit Extension Specialists, County Agricultural Extension Agents, commercial apple consultants, and others in New England involved in apple production to the project objectives and justification and inform them of the results and potential to increase the sustainability of their orchards, regardless of the crop production system employed.


Materials and methods:

Earthworm biomass and the species composition of earthworms in an orchard was not determined in this study. Instead, leaf removal was quantified in leaf burial test plots as an indirect measure of earthworm population size, species composition, and activity. In each orchard, when approximately 75% of the leaves have fallen in autumn, 600 apple leaves were collected at random and placed at random into 12 groups of 50 leaves each. Each group was placed on the orchard floor within a 4 m2 polyvinylchloride tubing frame and covered with a plastic mesh to prevent the leaves from being blown away. Four frames were located at random in tree rows and four frames were placed at the edge of the tree canopy adjacent to each “in-row� frame. The remaining four frames were placed on sod near the orchard, with the locations selected to best identify sites not affected by orchard practices and expected to receive little or no spray drift but with soil type the same as orchard soil. These latter plots served as checks to indicate the potential of earthworms to bury leaves in a natural sod system not subjected to orchard practices.

Placing a frame “in-row� and a second frame near it but at the canopy edge was intended to provide insight into the impact of ground management practices “in-row� relative to the remainder of the orchard floor. The plot procedure was developed in a preliminary study to measure earthworm populations and activities funded by the New England Apple Research Committee.

Grassed plots were mowed and cleared of debris and bare-ground herbicide “in-row� plots were cleared of debris before placing a frame in the plot. Leaf removal was determined by counting the leaves remaining under the frames in spring at bud break and at petal fall. Leaf removal in each orchard was expressed as a percentage of the original 50 leaves in the plot. The two assessments were timed to quantify the percentage of leaf removal in spring at the time susceptible tissue was first produced and ascosporic inoculum was available and at the end of the period ascospores were produced.

Earthworm activity is inversely proportional to soil temperature, and burial has been reported to stop at 2 C, so soil temperature in each orchard was monitored at a depth of 30 cm, beginning at the time of leaf fall and continuing to petal fall. Measurements were at 4 h intervals and then calculated and recorded as mean daily temperature.

Research results and discussion:

Leaf removal was monitored in 25 commercial apple orchards throughout New England and at the Woodman Farm research orchard at the University of New Hampshire in 1997-98 and in 30 commercial orchards and the Kingman and Woodman Farm research orchards at the University of New Hampshire in 1998-99. Four leaf-removal plots were established on herbicide strips adjacent to sod plots at 13 sites in 1997-98 and 16 sites in 1998-99. Four plots were established on sod adjacent to the orchard at 12 sites each year. Each leaf-removal plot consisted of 20 intact apple leaves of uniform size placed in a wood frame with a plastic mesh netting stretched over the frame to keep leaves within the frame. Before the leaves were placed within the frame, all existing leaf litter was removed and grass within the sod plots was cut to approximately 5 cm. The plots were established in late autumn each year and assessed for leaf removal next spring at the green tip growth stage of the apple trees.

Missing leaf tissue was attributed to leaf-burial by earthworms and litter-feeding by earthworms, slugs, and other organisms. The percentage of original leaf tissue missing in spring from sod plots within an orchard was <25% in nine orchards, 26-50% in three orchards, and 51-75% in eight orchards, and >75% in three orchards in 1998 and <25% in ten orchards, 26-50% in seven orchards, and 51-75% in thirteen orchards, and >75% in six orchards in 1999. Data were lost at four sites in 1998 due to disturbance of the plots.

The pest management program in each orchard was classified as (a) “organic,� (b) “advanced IPM,� (c) “minimal IPM,� or (d) “conventional� with respect to selecting and scheduling pesticides. One orchard classified as “organic� was not certified because of one application of Imidan for plum curculio control, but all other management practices conformed to certified organic guidelines. There were great differences in the amount of leaf tissue removed from plots among the orchards in both years, but there was no correlation between the percentage of leaf tissue removed and the pesticide program classification. The percentage of leaf tissue removed by bud-break in spring in 1998 and 1999 ranged, respectively, from 0-74% and 10-93% in orchards designated “organic�, 8-99% and 41-100% in orchards designated “advanced IPM,� 11-96% and 2-96% in orchards designated �minimal IPM,� and 2-69% and 0-75% in orchards designated “conventional.�

It was hypothesized that orchards with a history of using only “organic� practices or following “advanced IPM� guidelines would have a greater loss of leaf litter than orchards that had used “minimal IPM� practices or followed “conventional� pest management practices. However, there was no relationship between leaf litter removal and orchard management practices. What was shown, though, was that the total leaf litter removed by the beginning of the growing season in 1998 and 1999, respectively, was very high (>90%) in four and five orchards, high (80-90%) in two and 0 orchards, and moderately high (70-80%) in three and seven orchards. The high percentage loss of leaf litter in these orchards has important implications for decision-making with respect to pest management, because the percentage loss of leaf litter is related directly to the percentage loss of potential inoculum produced by the fungus causing apple scab and of overwintered leafminer pupae. Eliminating 85% of the leaf litter, for example, will reduce by approximately 85% the amount of the fungal spores (ascospores) that will infect the leaves and fruit for several weeks in early spring and approximately 85% of the initial population of adult leafminers that will emerge and mate during half-inch green to pink.

Participation Summary

Project Outcomes

Impacts of Results/Outcomes

The elimination of 75% or more of the leaf litter by earthworms and other organisms that feed on the leaf litter results in a reduction of potential primary inoculum of the fungus causing apple scab that is comparable to sanitation practices such as mulching the leaf litter with a flail mower or applying the nitrogen fertilizer urea to the leaf litter. It has been proposed that a loss of 75% or more of the leaf litter would allow a grower with a moderate amount of foliar scab in autumn to reduce the amount of recommended fungicide according to a “reduce-fungicide� action threshold) that has been developed for apple growers in the northeastern United States. One tactic recommended for orchards that qualify for using the “sanitation� action threshold is to perform sanitation and then delay the first application of a fungicide to control scab until after three infection periods have occurred or until the pink fruit bud stage, whichever comes first. This tactic has resulted in eliminating several early-season fungicide applications.

The elimination of 75% or more of the leaf litter by biotic agents may result in lowering the emerging leafminer population below action thresholds for applying leafminer insecticide based on counts of first-generation and second-generation sap-feeding mines. This could eliminate two leafminer insecticide treatments.

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.