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Notes & Unique Phenomena

Metarhizium anisopliae Seed Treatment Increases Yield of Field Corn When Applied for Wireworm Control

^a Agriculture and Agri-Food Canada, Pacific Agri-Food Research Centre, Box 1000/6947 No. 7 Hwy., Agassiz, BC, Canada, V0M 1A0
^b Dep. of Biological Sciences, Simon Fraser Univ., 8888 University Dr., Burnaby, BC, Canada V5A 1S6

^* Corresponding author (kabalukt{at}agr.gc.ca)

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
In an effort to protect field corn (Zea mays L.) from wireworm (Agriotes obscurus L.) herbivory and yield loss, seeds were treated with conidia of Metarhizium anisopliae strain F52 alone or in combination with clothianidin or spinosad before planting at three farm fields in south coastal British Columbia, Canada. Corn seed treated with M. anisopliae conidia (main effect) resulted in significant increases in stand density (78% M. anisopliae treated vs. 67% no M. anisopliae) and stock and foliage area fresh wt. yield (9.6 Mg ha^–1 M. anisopliae treated vs. 7.6 Mg ha^–1 no M. anisopliae), and significantly increased plant (stock and foliage) fresh wt. when it was applied together with spinosad or with no additional agrichemical at one location. Spinosad had no effect on corn yield, whereas clothianidin caused a significant increase in plant stand density and yield. Wireworm cadavers showing M. anisopliae strain F52 growth were retrieved from treated plots, suggesting that the increase in yield may have been due to wireworm control. Laboratory experiments provided no evidence that the increase in stand density and yield from the M. anisopliae-treated corn seed was attributable to an increase in germination rate or root growth. We concluded that seed treatment with this fungus may be a novel method to increase stand density and yield of corn.

Received for publication January 13, 2007.

Metarhizium anisopliae Seed Treatment Increases Yield of Field Corn When Applied for Wireworm Control

^a Agriculture and Agri-Food Canada, Pacific Agri-Food Research Centre, Box 1000/6947 No. 7 Hwy., Agassiz, BC, Canada, V0M 1A0
^b Dep. of Biological Sciences, Simon Fraser Univ., 8888 University Dr., Burnaby, BC, Canada V5A 1S6

^* Corresponding author (kabalukt{at}agr.gc.ca)

Received for publication January 13, 2007.
In an effort to protect field corn (Zea mays L.) from wireworm (Agriotes obscurus L.) herbivory and yield loss, seeds were treated with conidia of Metarhizium anisopliae strain F52 alone or in combination with clothianidin or spinosad before planting at three farm fields in south coastal British Columbia, Canada. Corn seed treated with M. anisopliae conidia (main effect) resulted in significant increases in stand density (78% M. anisopliae treated vs. 67% no M. anisopliae) and stock and foliage area fresh wt. yield (9.6 Mg ha^–1 M. anisopliae treated vs. 7.6 Mg ha^–1 no M. anisopliae), and significantly increased plant (stock and foliage) fresh wt. when it was applied together with spinosad or with no additional agrichemical at one location. Spinosad had no effect on corn yield, whereas clothianidin caused a significant increase in plant stand density and yield. Wireworm cadavers showing M. anisopliae strain F52 growth were retrieved from treated plots, suggesting that the increase in yield may have been due to wireworm control. Laboratory experiments provided no evidence that the increase in stand density and yield from the M. anisopliae-treated corn seed was attributable to an increase in germination rate or root growth. We concluded that seed treatment with this fungus may be a novel method to increase stand density and yield of corn.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
NUMEROUS SPECIES OF WIREWORMS are pests of field corn in North America and in various corn-growing regions worldwide. In a survey of crop profiles for the USA, they were identified as important pests of corn, potato (Solanum tuberosum L.), and sugar beet (Beta vulgaris L.) (see NSF Center for Integrated Pest Management, 2007). Wireworm larvae inhabit the soil for 3 to 6 yr feeding mostly on living plant material (Brian, 1947; Furlan, 1998). As they are attracted to volatile compounds emanating from roots and germinating seeds, they are efficient at detecting host plants (Doane et al., 1975; Johnson and Gregory, 2006). Established crops are usually able to withstand wireworm feeding injury while newly seeded crops are particularly susceptible. When wireworms encounter a newly seeded crop, they consume the seed embryo or newly emerged roots, causing death of the plant and a reduced stand. Less intense feeding on the seed or new roots severely inhibits growth and causes a reduction in yield (Anderson, 1987; Blossey and Hunt-Joshi, 2003).

Wireworms have been largely controlled in corn with synthetic pyrethroids, neonicotinoids, and organophosphate insecticides applied as granules with the seed or by using insecticide-treated seeds (Kuhar et al., 2003). Although the insecticide treatments are efficacious, concerns associated with human and environmental health have caused attention to be focused on the development of reduced-risk compounds and practices. Furthermore, while the majority of corn growers currently have access to agrichemicals for wireworm control, many compounds are unacceptable for organic corn production.

Microbial pesticides have been developed that capitalize on their antagonistic interaction with plant diseases and pathogenic interactions with pest plants and insects (Vakili, 1992). For insect pests however, there have been no reports of using microorganisms as seed treatments for crop protection. Metarhizium anisopliae Sorokin (Hypocreales: Clavicipitaceae) can infect wireworms in nature (Thomas, 1932; Rockwood, 1951; Madelin, 1966) and efforts have been made to consider its use as a biopesticide (Fox and Jaques, 1958; Fox, 1961; Zacharuk and Tinline, 1968). The only reported use of M. anisopliae against wireworms in a field trial was made by Filipchuk et al. (1995), who found that after drenching the soil with a conidia suspension, control of the tobacco wireworm Conoderus vespertinus Fabricius (Coleoptera: Elateridae) was comparable with that achieved with the organophosphate terbufos [O,O-diethyl S-(((1,1-dimethylethyl)thio)methyl) phosphorodithoic acid]. Recent efforts to develop M. anisopliae as a biopesticide for wireworms have been centered on the screening and isolation of unique and virulent isolates, including several that have shown good laboratory efficacy and some field efficacy (Kabaluk et al., 2005). Other studies have combined M. anisopliae with agrichemicals including spinosad to synergize the efficacy of the fungus in causing wireworm mycosis (Ericsson et al., 2007), but no reports of field testing spinosad against wireworms have been found. Spinosad is a commercially available mixture of spinosyn compounds produced during fermentation by the soil actinomycete Saccharopolyspora spinosa (Actinomycetales: Pseudonocardiaceae) whose neurotoxic mode of action is believed to act on gamma aminobutyric (GABA) receptors (Salgado, 1998). It is suitable for pest control in organic agriculture. Kabaluk et al. (2005) explored several M. anisopliae application methods for potatoes including seed treatments, and Hu and St. Leger (2002) showed that cabbage root systems were colonized by M. anisopliae applications in the field. Together, this information indicates that seed treatments could be an effective delivery method for M. anisopliae to field corn, and that combination treatments may positively interact in the field to optimize the control of wireworms.

We report increases in field corn stand density and area fresh weight yield following sowing seed treated with M. anisopliae (isolate F52) alone and in combination with spinosad or clothianidin for wireworm control. We also report the compatibility of spinosad and clothianidin on conidia germination, and the effect of conidia seed treatments on seedling growth.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Site Selection, Preparation, and Presampling
Land with a known history of heavy wireworm infestation [95% A. obscurus based on several years of beetle sampling (W.G. van Herk, 2007, unpublished data)] was selected for the field trials. Stratified soil-core sampling at each site confirmed the presence of high numbers of wireworms. The three field sites chosen were within a 10-km radius of –121.764° longitude, 49.239° latitude; two sites were located at the Pacific Agri-Food Research Centre, Agassiz BC (Agassiz Site 1 and Agassiz Site 2), and one site at the Seabird Island First Nation (Seabird). These sites were sprayed with glyphosate to kill the crop of orchard grass before being plowed and disked in 2004 (2 yr in advance of conducting the field trials) so that organic matter would have time to decompose and not detract the wireworms from the subject corn crop. The land was maintained fallow in 2005 with glyphosate applications and cultivation using an s-tine cultivator that was repeated before planting the corn trial in 2006.

Seed Treatment Combinations
Conidia of M. anisopliae strain F52 were produced by the USDA SIMRU, Stoneville, MS, using solid state fermentation and sterile rice as the substrate. Conidia were separated from the rice granules by screening through a sieve, and were then dried to 10% moisture content. Conidia viability was determined to be 94 ± 3%. Corn seed (hybrid Pioneer 39D81) was provided by Bayer CropScience, Calgary, AB, as both untreated and as Poncho 250 containing 2.5 x 10^–4 g clothianidin per seed. Spinosad was provided by Dow Agrosciences, Indianapolis, IN, as Entrust WP (80% spinosad). All treatments were applied to corn seeds before planting, and the six factorial treatment combinations included three levels of agrichemical (2.5 x 10^–4 g clothianidin per seed (32.9 g ha^–1), 1.522 x 10^–4 g spinosad per seed (20 g ha^–1, no agrichemical) and two levels of M. anisopliae conidia [3.8 x 10⁸ conidia per seed (5 x 10¹³ conidia ha^–1), no conidia] (seed level rates estimated according to bulk seed treatment rates). To ensure adherence of conidia to the seeds, 0.005 g of corn oil per seed was applied in advance of the conidia, and was also applied to seeds receiving no conidia.

For each treatment, 700 corn seeds and 3.5 g of corn oil were added to the stainless steel bowl of an electric kitchen mixer and mixed at medium-low speed for 3 min, stopping every 30 s to reincorporate oil from the sides of the bowl using a rubber scraper. Conidia-only, conidia-clothianidin, conidia-spinosad, spinosad-only, and clothianidin-only seeds were treated with oil as above. For all but the spinosad treatments, 3.5133 g of conidia were added and folded into the oil-treated corn seed with a whisk. The seeds and conidia were mixed for 5 min to ensure uniform coating, and the sides of the bowl were periodically scraped to ensure the free conidia were adequately mixed and adhered to the seeds. The same mixing procedure was followed for spinosad treatments, except 0.2664 g of Entrust (0.2131 g spinosad) was applied alone or was premixed with conidia before treating the corn seed. Following treatment, seeds were kept in Styrofoam bowls with fitted lids and stored at 5°C until planting 18 h later. This procedure was repeated before planting at each of the three field sites.

Field Trial Design
The experimental design was a randomized complete block with six treatment combinations. There were four blocks at Agassiz Site 1 and the Seabird site, and three blocks at Agassiz Site 2, and each block was separated by a 2.5-m cultivated buffer. Within each block at Agassiz Site 1 and the Seabird site, a treatment plot consisted of six 3.5-m-long rows with seeds spaced at 15 cm (23 seeds row^–1), whereas at Agassiz Site 2, a plot consisted of four rows. At all sites, a single guard row of untreated corn seed separated each plot, and all rows were spaced at 0.5 m. The seeds were hand-planted by poking a 5-cm deep hole in the soil, placing the seed at the bottom, and by covering the hole with soil followed by light firming. Planting dates were as follows: Agassiz Site 1, 15 June; Agassiz Site 2, 23 June; Seabird site, 20 June. The treatment plots were maintained free of weeds by hand hoeing. Harvesting of corn plants was conducted by cutting plants in the center four rows of each plot (Agassiz Site 1 and Seabird site) and the center two rows (Agassiz Site 2) at ground level using pruning shears. For each plot, plants were counted and weighed fresh in the field. Harvesting occurred on 21 August for Agassiz Sites 1 and 2, and 22 August for the Seabird site.

Plant weight (kg plant^–1, stock and foliage), area yield (Mg ha^–1 stock and foliage hectare^–1), and stand density (percentage of plants surviving out of the number of seeds planted) were analyzed with the PROC MIXED procedure of SAS (Littel et al., 1996). The effect of site and block were considered random, and the effects of M. anisopliae and agrichemical were considered fixed.

Testing the Compatibility of Conidia with Agrichemicals
To determine if the clothianidin and spinosad seed treatments would affect conidia germination, corn seed was coated in oil and then conidia as described above for the field experiments. For each treatment, conidia were added to 100 corn seeds which equated to an average of 3 x 10⁸ conidia per seed. After treatment, the 100 seeds were divided equally between two aluminum dishes and placed in a high-humidity environment at 22°C in the dark. At intervals of 1, 24, 48, and 192 h, two seeds were sampled from each aluminum dish (four seeds per treatment), and placed in a test tube containing 5 mL of deionized water and 0.025 mL L^–1 Triton X-100 [p-(1,1,3,3-Tetramethylbutyl)phenol ethoxylate, J.T. Baker, Inc., Phillipsburg, NJ] as a surfactant. Each tube was mechanically vortexed for 5 min to release the conidia from the seed. The conidia concentration in the resulting suspension was enumerated with an Improved Neubauer hemocytometer, and adjusted to 10⁶ conidia mL^–1 dH₂O (0.025 mL L^–1 Triton X-100). Four 100-µL samples were drawn from this suspension, spread evenly on individual 110-mm Petri plates of potato dextrose agar (28 g L^–1), and incubated at 22°C in the dark. After 24 h, conidia were observed under a microscope (250x magnification) and considered viable if a germ tube had formed and its length exceeded twice the diameter of the conidia.

Testing the Effect of Conidia on Corn Seed Germination
To determine if treating corn seed with conidia influenced corn germination, seeds were treated with corn oil and two levels of M. anisopliae, and were compared with an untreated control. One hundred and fifty seeds were coated with oil as described above, and divided into three groups of 50. Fifty corn seeds each were added to glass beakers containing 0.25 g of conidia and were mixed with a spatula until evenly coated, equating to an average of 3.8 x 10⁸ and 3.8 x 10⁹ conidia seed^–1. The remaining 50 oil-coated seeds represented the oil control. An additional 50 corn seeds without oil or conidia represented the untreated control. Each of the two germination trials consisted of five seeds from each treatment placed in a 110-mm petri plate lined with filter paper soaked with 2 mL of dH₂O. Ten replicate plates were prepared for each treatment. Each plate was sealed in parafilm, and placed randomly in a dark cabinet at 22°C. The length of the primary root was measured 72, 120, and 144 h after initiation of the experiment. In addition to these measurements, the secondary root number and length was measured 144 h after initiation in the second and third runs of the trial.

	RESULTS

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Field Trial
With the exception of the effect of spinosad on plant weight at Agassiz Site 1, all yield variables from treatment combinations receiving M. anisopliae were numerically greater than those without M. anisopliae (Fig. 1 ). Treatment of corn seed with M. anisopliae conidia resulted in a highly significant increase in stand density and yield, however no interaction between M. anisopliae and either two agrichemicals was apparent for any of the measured variables (Table 1). For plant weight, the significant site x M. anisopliae x agrichemical interaction revealed a positive effect of M. anisopliae with no agrichemical and spinosad at Agassiz Site 2 only, whereas there was no interaction between M. anisopliae and clothianidin at any site (Table 2, Fig. 1). Table 3 shows the magnitude of the difference between M. anisopliae and no M. anisopliae treatments on stand and yield, and that the agrichemical main effects on all three measured variables was due to clothianidin, and not spinosad.

View larger version (31K): [in this window] [in a new window]   Fig. 1. The effect of seed treatment combinations of Metarhizium anisopliae and agrichemicals on the stand density and yield variables of field corn. Yield variables are reported as the fresh wt. of stocks and leaves.

Effect of Conidia on Corn Seed Germination
Metarhizium anisopliae conidia had no effect on the percentage germination or root growth at the field rates tested (99% germination for conidia + oil-coated seeds vs. 93% for oil-coated seeds; F = 22.28, df = 3, P < 0.0001). However, the higher level of conidia significantly reduced both seed viability (40% germination) and root growth (mean primary root length: 11-mm for higher rate conidia + oil-coated seeds vs. 54-mm for oil-coated seeds; F = 80.33, df = 3, P < 0.0001; mean secondary root length: 11-mm for higher rate conidia + oil-coated seeds vs. 33-mm for oil-coated seeds; F = 22.28, df = 3, P < 0.0001).

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The results from this study showed that the treatment of corn seeds with M. anisopliae conidia conferred an increase in corn yield. While preplant observations revealed a high level of wireworm infestation, dry soil conditions during midseason and after harvest were inadequate to draw wireworms near to the soil surface, so relative pest levels among treatments could not be reliably measured. Therefore, the direct correlation between treatment effects and wireworm levels was not established. However, fungus emerging from wireworm cadavers retrieved from treated plots was identified as M. anisopliae strain F52 using amplified fragment length polymorphisms (G.M. Duke, 2006, unpublished data). Because strain F52 is not indigenous to the region, nor registered in Canada, we concluded that its application reached the target host. That stand density (in contrast with plant fresh wt.) was the yield variable most affected by seed treatment with M. anisopliae conidia suggests that seeds, newly germinated seeds, or seedlings were protected from wireworm herbivory with the M. anisopliae treatment (as wireworm feeding at this stage often causes whole plant loss), either by causing mortality or by repulsion, because whole plant loss did not occur after plants were established. In support of this suggestion, the main effect of M. anisopliae on yield increase was similar to the main effect of clothianidin (Table 3) which suggested that wireworms were successfully managed by the M. anisopliae treatment.

Metarhizium anisopliae strain F52 has a wide host range (Strasser et al., 2000). In testing this strain against wireworms, it has been found to be most virulent toward the Great Basin wireworm Ctenicera pruinina (Horn) found along the Columbia River bordering southern Washington and northern Oregon, but less virulent toward A. obscurus and A. lineatus wireworms found in south coastal British Columbia. Interestingly, M. anisopliae isolates from British Columbia have shown high virulence toward the local wireworms including both Agriotes species and Limonius californicus (Mannerheim) found in south-coast and south-central British Columbia (Kabaluk et al., 2005, 2007). Therefore, it is highly likely that greater effects than observed in this study could be achieved by using these more virulent isolates.

Alternatively, M. anisopliae has been shown to colonize the rhizosphere of plants (Hu and St. Leger, 2002; Bruck, 2005) and this could confer the uptake of nutrients from the soil. If this were the case in the current study, it is possible that M. anisopliae may have increased the corn germination rate faster in M. anisopliae treated plots such that plants became established earlier in the season, and were therefore better able to withstand wireworm feeding damage or other biotic and abiotic stressors. There was some evidence for this phenomenon in the higher plant fresh wt. at one location. Metarhizium anisopliae may have also protected corn seeds from soilborne seed-rotting organisms and thus improved their emergence. This phenomenon was observed to occur with beet (Phoma betae Fr.) seeds by Roberti et al. (1993).

While we did not find an increase in the germination rate of M. anisopliae-treated corn seeds in the laboratory experiment, it is reasonable to expect that the field soil environment would have a much different effect, particularly with an ambient nutrient source in the field soil. Infectivity of wireworms by M. anisopliae has been shown to be more influenced by soil moisture than soil type (sand, clay, organic), although the two factors can be related (Kabaluk et al., 2007). If our results were due to wireworm control, then this would likely affect the range of conditions and geographic regions under which conidia seed treatments would be effective. However, the increases in stand density and plant fresh weight in response to M. anisopliae seed treatment found in this study need further investigation to clearly identify the underlying causes.

	ACKNOWLEDGMENTS

 
We thank Ffion Cassidy, Nancy Yao, Christine Mcloughin, and Tegan Adams for field and technical assistance, and Grant Duke, Doug Inglis, and Mark Goettel for AFLP analysis of fungal samples. This work was supported by the Pest Management Centre of Agriculture and Agri-Food Canada, Pesticide Risk Reduction and Minor Use Programs.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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This Article Abstract Figures Only Full Text (PDF) Free Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via Google Scholar Google Scholar Articles by Kabaluk, J. T. Articles by Ericsson, J. D. Search for Related Content PubMed Articles by Kabaluk, J. T. Articles by Ericsson, J. D. Agricola Articles by Kabaluk, J. T. Articles by Ericsson, J. D. Related Collections Agricultural Pesticides Seed Treatment Pest Management Systems