Marjorie Ross¹, Emily E. Hoover^2
1 Research Assistant, Department of Horticultural Science, University of Minnesota;
² Professor, Department of Horticultural Science, University of Minnesota

This research has been supported by a grant from the North Central Region Sustainable Agriculture Research and Education (NCR-SARE) and in part by the Minnesota Agricultural Experiment Station.

Abstract

We investigated the effects of groundcover management and pesticide program on the arbuscular mycorrhizal fungi (AMF) symbiosis in strawberries. Establishment year groundcover strategies were: 1) wool mulch with interrow canola cover crop; 2) traditional herbicide and 3) hand-weeding. These treatments were combined during year two in a three by two factorial with two pesticide treatments: sprayed and unsprayed.

Total AMF and arbuscular colonization and plant growth responses were compared among treatments. There were no significant differences between pesticide treatments for total AMF or any plant biomass parameter. The wool-canola treatment supported significantly greater mycorrhizal colonization and root dry weights of mother plants compared to the herbicide and hand-weed treatments but total AMF was not positively correlated with biomass in this treatment. Total AMF was positively correlated with leaf N in all groundcover treatments but was not positively correlated to leaf P in any groundcover treatment. The lack of a significant correlation between leaf P and total AMF might be due to the high P soil of the research plots. In this study establishment year groundcover treatments were more important than pesticide treatments in year two for determining total AMF colonization and plant growth responses. Our results suggest that a mulch-type groundcover in strawberries does increase plant growth and total AMF colonization.

Keywords: arbuscular mycorrhizal fungi (AMF), percent colonization, arbuscules, vesicles, hyphal coils, hyphae

Introduction

As a complex system composed of multiple organisms and abiotic factors, the soil is a crucial component of agricultural systems. In addition to the physical role of the soil, the many soil microbiotic interactions and their effects on plant health and crop yield are also important. Possibly the most prevalent microbe-plant interaction is with arbuscular mycorrhizal fungi (AMF). Current research suggests that mycorrhizae benefit plants primarily through increased P uptake (Smith and Read, 1997). In strawberries, these associations have been shown to increase nutrient uptake (Dunne and Fitter, 1989), increase growth (de Silva et al., 1996; Robertson et al., 1988; Vestburg, 1992) and protect against pathogens (Norman et al., 1996). Other putative benefits include protection against drought and salinity stress, and increased N fixation (Barea et al., 1993).

In agricultural production systems, many factors affect AMF colonization and the functioning of the symbiosis including soil type, tillage, cover crops and soil amendments (Bethlenfalvay and Linderman, 1992; Hamel, 1996; Land et al., 1989). Specifically in strawberries, soil and groundcover management are important management factors. As a perennial crop, strawberries reproduce sexually through flowering and fruiting and asexually through the production of runner plants from existing mother plants (Galletta and Bringhurst, 1990). In Minnesota, the primary culture system used is the matted row in which runner plants are permitted to spread to a pre-determined row width (Galletta and Bringhurst, 1990). Within- and between-row areas are generally covered with mulch material for weed control and to protect fruit quality. After harvest, interrow organic mulches are generally tilled in during renovation. Some growers also use interrow herbicides for weed control.

The effects of residue management and cover cropping on AMF colonization and plant responses have not been investigated in strawberries. In a greenhouse inoculation study, Schreiner and Bethlenfalvay (2000) found that crop residues significantly increased mycorrhizal colonization of pea. Muthukumar and Udaiyan (2000) found that incorporated organic amendments from plant and animal sources increased natural mycorrhizal colonization of field grown cowpea. In field studies with natural AMF populations, mycorrhizal colonization of corn was significantly greater in plots that had been previously cover cropped (Boswell et al., 1998; Kabir and Koide, 2000). In both studies, the cover crop was incorporated, or killed with glyphosphate and then incorporated before seeding an annual crop. These effects might vary in perennial strawberry production systems where the cover crop and primary crop are grown simultaneously for all or part of the growing season, and organic mulches are not immediately incorporated.

AMF colonization and functioning may also be affected by pesticide applications, especially fungicides. While researchers have found negative effects of fungicides on AMF (Buttery et al., 1988), these effects may be highly variable among different compounds and conditions (Schreiner and Bethlenfalvay, 1997). Herbicides may also decrease AMF symbiosis by lowering viability and growth, or by decreasing host plant diversity (Bethlenfalvay and Linderman, 1992). Effects of pesticide sprays have not been investigated in strawberries under agricultural conditions although commercial strawberry production may involve multiple applications of fungicides, herbicides and insecticides.

Studies investigating the specific effects of common management practices on AMF are necessary to determine the importance of AMF in strawberry production and the effects of strawberry management practices on AMF. The current study was conducted to evaluate the AMF symbiosis in field grown strawberries with the specific objective of comparing levels of AMF colonization and plant growth response among three establishment year groundcover strategies combined with a conventional pesticide spray treatment or unsprayed treatment in the study year.

Materials and Methods

This study was conducted at the West Central Research and Outreach Center at Morris, Minnesota (45.5 ° N x 95.88 ° E). Plots of the strawberry cultivar 'Glooscap' were established in 2002 in a randomized complete block with four replications and three ground cover treatments. The groundcover treatments applied in the establishment year were: 1) 'Dwarf Essex' canola plus wool mulch (wool-canola), 2) traditional herbicide (herbicide) and 3) hand-weeding (hand-weed). The wool-canola treatment included a wool-fiber mulch placed between strawberry plants and an interrow canola cover crop. In the establishment year, the canola was planted on 15 May, and killed with Glyphosphate (Roundup) herbicide on 18 June. The establishment year herbicide treatment included two applications of DCPA (Dacthal W-75) herbicide and one application of Napropamide (Devrinol 50-DF) applied between rows. The hand-weed treatment did not receive any herbicide treatments. Each treatment plot consisted of three rows, each three meters long.

In 2003, two pesticide spray treatments (sprayed, unsprayed) were overlaid on each of the three ground cover treatments for a 2X3 factorial design with four replications. The sprayed treatment consisted of three fungicide applications and two insecticide applications from 4 June to 26 June 2003 (Ross, 2004). The unsprayed treatment did not receive any sprays in the 2003 season. In spring 2003, straw applied to all plots as winter mulch in Fall 2002 was removed and placed between rows. Canola residues and wool mulch materials remained in the wool-canola treatment plots. Each pesticide treatment (sprayed, unsprayed) was randomly applied to row 1 or 3 in each groundcover treatment. Soil and plant samples were collected in June, following pesticide application, prior to harvest; July post-harvest, pre-renovation; and late August.

On each sampling date we collected 8 to 10 random 15 cm deep soil cores from within the rows across the entire planting. Vegetation and mulch materials were removed prior to obtaining soil cores. Soil samples were pooled, dried, and analyzed for P, K and pH for each date at the University of Minnesota Research and Analytical Laboratory. Only P was used in statistical analyses because it has a demonstrated role in the AMF symbiosis (Smith and Gianinazzi-Pearson, 1988; Smith and Read, 1997). Soil pH values were not compared statistically but were used to interpret soil P test results. Where pH was greater than 7.5, P was analyzed using both Bray and Olsen test methods (Frank et al., 1998).

On each sampling date, we also randomly collected one mother plant and three runner plants from rows 1 and 3 by removing the plant and soil with roots. Runner plants were pooled by treatment for all measurements. After collection, plants were stored in a 2ºC cooler for approximately 18 hours until processing. Individual plants were carefully washed using a spray attachment to remove all soil adhering to the root system. Detached root pieces were retained in a fine sieve. Plants were separated into below- and aboveground sections by cutting just below the crown and fresh weight was recorded.

Six to eight sub-samples of fine, actively growing root tips were randomly collected from each root system. Root sub-samples from each plant were frozen until mycorrhizal scoring was possible. The remaining below- and aboveground parts were oven-dried at 65ºC and dry weights recorded. Percent water content was calculated for below- and aboveground sections.

All fully-expanded, non-senescent leaves from each plant sample were removed and analyzed for nutrient content including Al, B, C, Ca, Cd, Cr, Cu, Fe, K, Mg, Mn, N, Na, Ni, P, Pb, S and Zn. All nutrient analyses except C, N and S were conducted at the University of Minnesota Research and Analytical Laboratory using standard ICP analysis (Dahlquist and Knoll, 1978). Analyses for C, N and S were conducted using combustion techniques (Horneck and Miller, 1998). Statistical analyses were conducted for N and P as these nutrients are known to be of primary importance in the AMF symbiosis (Dunne and Fitter, 1989; Mathur and Vyas, 2000).

For AMF scoring, thawed root sub-samples from each plant were cleared in 10% KOH using a 121ºC autoclave for 11 minutes, acidified in 1% HCl (Kormanik et al., 1980), stained with 0.05% Aniline Blue (Grace and Stribley, 1991) and destained in 70% glycerol. Stained roots were cut into 1 cm pieces and mother and runner root sub-samples were pooled by treatment. Sub-samples were stored in 70% glycerol-water (v/v) until further processing (Koske and Gemma, 1989). Roots that appeared lightly stained were re-stained by soaking at room temperature in 0.05% Aniline Blue for 1 h.

Percent AMF colonization of root subsamples was estimated using a modification of the magnified intersection method (McGonigle et al., 1990). Sub-samples were letter-coded to insure observer objectivity. Using 40x magnification, 150 intersections per root sub-sample were analyzed for presence of mycorrhizal structures including: hyphae, hyphal coils, vesicles, arbuscules and absence of structures ("absent" intersections). If a structure was questionable, observation was done using 100x. Total number of intersections was used to estimate root length (McGonigle et al., 1990).

Calculations of Mycorrhizal Colonization

Parameters of mycorrhizal colonization were calculated as follows: % Arbuscular Colonization = (arbuscule intersects / total intersects) * 100 % Vesicle Colonization = (vesicle intersects / total intersects) * 100 % Hyphal Coils = (hyphal coil intersects / total intersects) * 100 % Hyphal Colonization = [(total intersects - absent intersects) / total intersects] * 100 % AMF Colonization = [(total intersects - absent intersects - hyphae only intersects) / total intersects] * 100

Hyphae only intersects were subtracted when calculating total AMF colonization because it is difficult to visually distinguish between AMF hyphae and hyphae of other soil fungi. We did use characteristics such as lack of septae and right angle branching patterns in our scoring. However, in order to obtain a more conservative estimate of total AMF colonization we subtracted this parameter (McGonigle et al., 1990).

Analysis

Sources of variation were date, replications, plot, groundcover treatment, pesticide treatment and the groundcover by pesticide interaction. Total percent AMF colonization, percent arbuscular colonization, plant nutrients, and root and shoot dry weights were pooled across dates and compared among treatments using ANOVA. Percent total AMF was regressed individually on shoot dry weight, root dry weight, leaf P and leaf N to determine the relationship between AMF and these factors.

Results

All treatments supported AMF colonization. The average total AMF colonization across all treatment combinations was 34%, ranging from 28% in the unsprayed/hand-weed treatment to 43% in the unsprayed/wool-canola treatment. Average arbuscular colonization ranged from 17% in the unsprayed/wool-canola to 21% in the unsprayed/hand-weed treatment (data not shown). There were no significant interactions for percent colonization between pesticide and groundcover treatment factors (Table 1).

Total AMF and arbuscular colonization were not significantly different between the sprayed and unsprayed treatments (Table 1). Comparing groundcover treatments, average total AMF colonization in the wool-canola groundcover treatment was 42% and was significantly greater than either the herbicide treatment (30%) or the hand-weed treatment (28%). There were no significant differences in average arbuscular colonization among groundcover treatments (Table 1).

Leaf P was not significantly different among groundcover or pesticide treatments and there were no significant interactions between groundcover and pesticide treatments for leaf P (Table 1). Leaf N was significantly greater in the wool-canola treatment compared to the other groundcover treatments (Table 1). There was significant interaction between groundcover and pesticide treatments for leaf N (Table 1). The only significant differences in leaf N between pesticide treatments were found in the herbicide groundcover treatment. In this case, the sprayed treatment had significantly greater leaf N.

Percent water did not differ significantly among plant samples. Therefore, dry weights were used for the remainder of the biomass analyses. Average root and shoot dry weights of mother plants across all treatment combinations ranged from 6.08 grams and 21.2 grams, respectively, in the unsprayed/herbicide treatment to 12.5 grams and 32.6 grams, respectively, in the unsprayed/wool-canola treatment. Runner plant root dry weights ranged from 1.54 grams in the unsprayed/herbicide treatment to 2.57 grams in the unsprayed/wool-canola treatment. Runner plant shoot dry weights ranged from 5.78 grams in the unsprayed/herbicide treatment to 8.90 grams in the sprayed/hand-weed treatment. There were no significant interactions between pesticide and groundcover treatments on plant biomass parameters for either mother plants or runner plants (data not shown).

There were no significant differences in any parameters of plant biomass among pesticide treatments for mother plants or runner plants (Table 2). However, there were significant differences in plant biomass among groundcover treatments. Average root dry weight of mother plants was significantly greater in the wool-canola treatment. Average root dry weight of runner plants was significantly greater in the wool/canola treatment compared to the herbicide treatment but not the hand-weed treatment. Average mother plant shoot dry weight was not significantly different among groundcover treatments. Average runner plant shoot dry weight was significantly greater in the hand-weed treatment compared to the herbicide treatment but not the wool/canola treatment (Table 2).

There was a significant positive correlation between total AMF colonization and shoot dry weight in the herbicide and hand-weed treatments for mother plants only (Table 3). Total AMF was negatively correlated to root dry weight in both mother and runner plants in the wool-canola treatment. However, root dry weight of mother plants was positively correlated to total AMF in the herbicide treatment (Table 3).

Total AMF colonization was only significantly correlated to leaf P in the herbicide treatment and the correlation was negative. In all groundcover treatments there was a significant positive correlation between leaf N and total AMF colonization (Table 3).

Discussion

In this study, pesticides did not have a major impact on AMF colonization. Previously, in studies using white bean and soybean, fungicides caused significant decreases in AMF populations (Buttery et al., 1988) but not in winter barley (Land et al., 1989). Miller and Jackson (1998) also found a negative correlation between AMF colonization and fungicide, herbicide or insecticide application in lettuce. The method of application, especially for fungicides, may be important, however. The significant effects of fungicides found by Buttery et al. (1988) might be attributed to the use of belowground fumigation while Land et al. (1989) and this study used foliar applications. The management of strawberries as a perennial crop with minimal tillage might also support a greater inoculum potential than the annual crops in the previous studies. Studies have shown mycorrhizal inoculum to be decreased by tillage (Hamel, 1996) and increased by cover cropping (Boswell et al., 1998; Kabir and Koide, 2000).

The wool-canola groundcover treatment had significantly greater total AMF colonization than the other two groundcovers. Although plants in the Brassicaceae family are known to be non-mycorrhizal (Glenn et al., 1988) we did not see negative effects of establishment-year canola (Brassica napus L.) on AMF colonization in the subsequent growing season. Many studies have shown that non-host plants do not affect AMF colonization of nearby host plants (Glenn et al., 1988; Kabir et al., 1996; Vierheilg et al., 1995). Researchers have speculated that the non-mycorrhizal status of the Brassicaceae may be controlled by the absence of fungal growth stimulators, rather than the presence of fungal growth inhibitors (Glenn et al., 1988). Kabir et al. (1996) also speculated that the presence of a host plant was a more important factor in hyphal spread than the presence of a non-host plant. In this study, conducted in the second year after planting the strawberries and killing the canola, any negative effects of the canola may have been minimized. The canola planted between strawberry rows was only actively growing in the first month of the establishment year, after which it was killed with herbicide. The canola was also planted in the aisles, possibly minimizing strawberry-canola root contact.

The greater colonization in the wool-canola treatment could be due to greater soil organic matter from the canola residues, though this parameter was not measured. Some organic amendments such as chicken litter, leaf compost and sheep or cow manure have been shown to increase mycorrhizal colonization (Boswell et al., 1998; Muthukumar and Udaiyan, 2000). The higher levels of colonization could also be attributed to the benefits of mulch. Although there have not been studies specifically examining the effects of mulches on AMF, the well-known benefits to plants, including moisture retention and temperature regulation might positively affect soil organisms as well.

In many cases, researchers have found greater strawberry plant growth in response to greater mycorrhizal colonization (de Silva et al., 1996; Vestburg, 1992). Although the wool-canola treatment had significantly greater root dry weights and total AMF colonization, the correlation between root dry weight and total AMF colonization was negative in this treatment. However, total AMF colonization was positively correlated to leaf N concentration in the wool-canola treatment indicating possible secondary effects of AMF on root biomass due to improved N uptake. Although P uptake is considered the primary benefit of AMF colonization (Smith and Read, 1997), researchers have documented increased N uptake in other mycorrhizal crops (Mathur and Vyas, 2000; Ruiz-Lozano et al., 1995; Tobar et al., 1994). The fact that the wool-canola treatment exhibited the positive correlation between total AMF and N without the accompanying positive correlation to biomass may also be attributed to the effects of the wool mulch. The temperature regulation and weed control provided by the mulch (Forcella et al., 2003) may have benefited plant growth while masking effects of AMF colonization.

Shoot dry weight was greatest in the hand-weed treatment and was positively correlated to total AMF in both the herbicide and hand-weed treatments. These correlations support the research of Vestburg (1992) and Robertson et al. (1988) who found significantly higher shoot dry weights in mycorrhizal strawberries compared to non-mycorrhizal controls. Furthermore, in all treatments, AMF was positively correlated with leaf N. These correlations imply an AMF-mediated increase in shoot dry weight, possibly as a result of increased N uptake.

The fact that we did not find a significant positive correlation between AMF and leaf P in any groundcover treatment may be due to the high P levels in the research plots. The benefits of mycorrhizal-increased P uptake are greatest in low-P environments (Miller et al., 1986; Smith and Gianinazzi-Pearson, 1988; Smith and Read, 1997). In Minnesota strawberry crops, P additions are recommended for soil-test values less than 41 ppm (Rosen and Eliason, 1996). The average P concentration of the research plots was 172 ppm.

We conclude that in strawberry production systems, establishment year groundcover treatments may be a more important factor than fruiting year pesticide sprays in determining AMF colonization levels and plant responses in the fruiting year. Further research with mulches and cover crops could result in mulch recommendations for encouraging AMF symbiosis in field grown strawberries.

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Table 1. Average total AMF and arbuscular colonization, leaf P and leaf N by pesticide treatment and groundcover treatment across three dates.

Within treatment averages followed by different letters were significantly different p= 0.05. * indicates significant interaction p= 0.05; ns indicates non-significant interaction p=0.05.

Table 2. Average mother and runner root and shoot dry weights by pesticide treatment and groundcover treatment across three dates.

Within treatment averages followed by different letters were significantly different p= 0.05.

Table 3. Total AMF correlations with shoot dry weight, root dry weight, leaf P and leaf N for mother and runner plants by groundcover treatment across three sampling dates.

p-values indicate significant effects p= 0.25. +/- indicates direction of effect. Mother and runner plants were pooled by treatment for leaf P and leaf N measurements.