Effects of the nematicide 1,3-dichloropropene on weed populations and stem canker disease severity in potatoes

Effects of the nematicide 1,3-dichloropropene on weed populations and stem canker disease severity in potatoes

Crop Protection 29 (2010) 1084e1090 Contents lists available at ScienceDirect Crop Protection journal homepage: www.elsevier.com/locate/cropro Effe...

171KB Sizes 2 Downloads 43 Views

Crop Protection 29 (2010) 1084e1090

Contents lists available at ScienceDirect

Crop Protection journal homepage: www.elsevier.com/locate/cropro

Effects of the nematicide 1,3-dichloropropene on weed populations and stem canker disease severity in potatoes Patrick P.J. Haydock a, *, Thomas Deliopoulos a, Ken Evans b, Stephen T. Minnis a a b

Nematology and Entomology Group, Crop and Environment Research Centre, Harper Adams University College, Newport, Shropshire TF10 8NB, UK Plant Pathology and Microbiology Department, Nematode Interactions Unit, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK

a r t i c l e i n f o

a b s t r a c t

Article history: Received 6 May 2009 Received in revised form 10 June 2010 Accepted 21 June 2010

The soil fumigant 1,3-dichloropropene (1,3-D) has been used in the UK for the control of potato cyst nematodes (PCN), Globodera pallida (Stone) and Globodera rostochiensis (Wollenweber), but its potential herbicidal activity has not been extensively investigated in this country. Field and glasshouse studies were therefore conducted to evaluate the potential of 1,3-D for the control of weeds in potatoes, and observations were made on the severity of potato stem canker, caused by the fungus Rhizoctonia solani Kühn [teleomorph: Thanatephorus cucumeris (Frank) Donk]. Autumn application of 1,3-D at 211.5 L active substance (a.s.) ha1 significantly suppressed the number of germinating weeds and the percentage of weed ground cover by 83% and 79%, respectively, relative to controls. There were also species-specific significant decreases (field pansy, Viola arvensis, in particular) in the number of weed seeds germinating in field soil in the glasshouse post-1,3-D treatment. The effect of 1,3-D declined in time and single (autumn or spring) or combined application produced a slight, but not significant, reduction in the number of weeds germinated on potato ridges relative to those recorded in untreated soil. The severity of stem canker on potato plants was not significantly reduced by 1,3-D but both mean number and weight of stems per plant were significantly increased compared with plants from untreated plots. These studies demonstrated that 1,3-D, in addition to giving PCN control, has efficacy against weeds; implications are the potential for reduced herbicide input in the crop rotation with accompanying economic and environmental benefits. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: 1,3-Dichloropropene Weeds Rhizoctonia solani Soil fumigation Potato

1. Introduction 1,3-dichloropropene (1,3-D) is a soil fumigant biocide that is effective against nematodes. In the UK, its use was permitted until March 2009 (as Telone II; Dow AgroSciences Ltd, Hitchin, Hertfordshire, UK) for use on potatoes, hops, raspberries, strawberries and narcissi as a pre-plant treatment to control all species of cyst and migratory nematodes. Telone II is formulated as a liquid concentrate consisting of 94% w/w 1,3-D and in the UK it has been applied mainly for the control of potato cyst nematodes (PCN), Globodera pallida and Globodera rostochiensis (Minnis et al., 2004). Whilst Telone II is a relatively expensive pesticide, costing approximately £700/ha, it was applied to 1197 ha of potato land in Great Britain in 2006 (FERA, 2010). The fumigant is applied into the soil by chisel injection at 20e25 cm depth and the surface is sealed using a powered roller. Once in soil, 1,3-D volatilises and permeates

* Corresponding author. Tel./fax: þ44 1952 815292. E-mail address: [email protected] (P.P.J. Haydock). 0261-2194/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2010.06.018

upwards through the soil killing nematodes in the zone where crop roots subsequently develop (Haydock and Evans, 1998). However, its efficacy is dependent upon achieving an appropriate soil structure and moisture content at application followed by effective sealing of the soil surface to reduce losses directly to the atmosphere. Within the European Union, on 15 May 2007, 1,3-D was not included in Annex 1 of Council Directive 91/414/EEC and as a result, sales and supply of Telone II were suspended from 20 March 2008. Growers, however, were allowed to use remaining stocks until 20 March 2009, date when registration of 1,3-D was revoked. However, the manufacturer has resubmitted a dossier to support the EU re-registration of 1,3-D and the Rapporteur Member State (Spain) has proposed inclusion (J. Sellars, pers. comm.). Outside Europe, in 2010, 1,3-D had registration approval in Australia, India, New Zealand, Philippines, South Africa and the USA (Kegley et al., 2010). Since 1,3-D is phytotoxic, it may have an additional herbicidal activity when used primarily as a soil fumigant for nematode control. There have been limited reports on incidental control of

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

various weeds by either 1,3-D or the soil fumigant DeD (mixture of 1,3-D and 1,2-dichloropropane; Shell Chemical Corporation, Ohio, USA) from outside the UK and details are available in Altman and Fitzgerald (1960), Jacobsohn et al. (1991) and Uhlig et al. (2007). In the USA, in 2007, Telone II (97.5% w/w 1,3-D; Dow AgroSciences LLC, Indianapolis, USA) received supplemental labelling approval by the Environmental Protection Agency (EPA) for use in the suppression of certain perennial weeds, such as Canada thistle (Cirsium arvense), field bindweed (Convolvulus arvensis) and quackgrass (Agropyron repens). The soil fumigant 1,3-D, as a broad spectrum soil sterilant, affects many organisms in the soil other than nematodes. In the USA, for example, the 2008 revised, EPA-approved, specimen label for Telone II states that it can be also used in the control of bacterial canker of peaches (Pseudomonas syringae pv. syringae), fusarium wilt of cotton (Fusarium oxysporum f. sp. vasinfectum), verticillium wilt of mint (Verticillium dahliae) and sugar beet rhizomania (beet necrotic yellow vein virus, BNYVV). There is therefore the possibility that 1,3-D could also have an effect on the control of the fungus Rhizoctonia solani Kühn [teleomorph: Thanatephorus cucumeris (Frank) Donk], a soil-borne pathogen with a great diversity of host plants, including potatoes where it is the causal agent of black scurf and stem canker. Nematodes and pathogenic fungi may interact synergistically to increase plant damage (Back et al., 2002). The combination of the symptoms caused by R. solani together with PCN has been called “potato sickness” (Morgan, 1926). It would therefore be highly beneficial if a single chemical treatment could control both R. solani and PCN since the benefits could also be greater than the reduction in damage caused by either organism alone (Back et al., 2006). The effects of crop rotation and granular nematicides on the development of R. solani have been investigated by Leach and Frank (1982), Ruppel and Hecker (1982) and Scholte (1992). These authors reported increased infection of potatoes and sugar beet by R. solani after application of the granular nematicides aldicarb, oxamyl or ethoprophos. In some cases, double the levels of infection were observed but the reasons for this increase were unexplained (Scholte, 1992). Hofman and Bollen (1987) demonstrated that the increased infection of potato stems and stolons with R. solani in nematicide-treated fields was not the result of a direct nematicidal effect on fungal growth or of suppression of microbial antagonism. Although little is known about the effects of 1,3-D on R. solani, some work has been conducted on the control of other soil-borne fungi by 1,3-D, but the results have been inconsistent in terms of efficacy. Data on fungal species and efficacy of the fumigation are provided, for example, by Stevenson et al. (1976), Baines et al. (1977), Davies (1990), Read and Hide (1995) and Sumner et al. (1997). R. solani was controlled by 1,3-D fumigation in a sugar beet field with a high incidence of Rhizoctonia treated the previous year (Altman and Fitzgerald, 1960). Tu (1993) found that 1,3-D had inhibitory effects on soil microbial populations 1 day after treatment but, after 3 weeks, fungal populations recovered to the level of abundance found in the untreated control. Although there has been some evidence for the efficacy of 1,3-D against soil-borne fungi, its effect on R. solani on potatoes at the rates used for PCN control has not been investigated. The aim of the work presented here was to assess the efficacy of 1,3-D on the control of various weeds and R. solani on potatoes at the rate and timing of application used for PCN control. Field and glasshouse experiments were conducted to measure the number of weeds germinating in the soil, to compare the viability of seeds collected from treated and untreated soil, and to assess the severity of R. solani on stems.

1085

2. Materials and methods 2.1. Observations on weeds 2.1.1. Field site The plots used for weed number and weed ground cover assessments and the field soil used in the weed seed germination experiments were part of a larger experiment conducted by this research group at the Common Field site, on the Harper Adams University College farm (Minnis et al., 2004). This experiment is referred to hereafter as Experiment 1 and information on the history of the field, soil properties and crop management practices can be seen in Minnis et al. (2004). 2.1.2. Experimental design The experiment of Minnis et al. (2004) had a two by five factorial randomised block design with five replicate plots per treatment. There were two levels for autumn fumigation of 1,3-D, either treated or untreated, and these were combined with five spring treatments (four nematicide treatments, including 1,3-D, plus untreated controls). In the present study, 20 plots were used, made up of five replicates of: (a) untreated, (b) spring application of 1,3-D, (c) autumn application of 1,3-D and (d) autumn and spring application of 1,3-D. Assessments were made over a period of several months and some were made before the spring 1,3-D had been applied. This effectively meant that for assessments made before the spring application of 1,3-D there were only two treatments; (a) and (b) were untreated and (c) and (d) were treated with 1,3-D, and the results were analysed and presented on this basis. After the spring application of 1,3-D, the four treatments (a), (b), (c) and (d) were analysed and presented separately. 2.1.3. Application of 1,3-dichloropropene The autumn treatment of 1,3-D at 211.5 L a.s. ha1 (as Telone II) was applied on 29 October at 15 cm depth with a soil temperature of 7.5  C. For the spring treatment, 1,3-D was injected into the soil on 16 March, at the same rate and soil depth with a soil temperature of 6.5  C. Injection of 1,3-D was conducted with the aid of a Rumpstadt Combiject (Rumpstadt, Haringvliet, The Netherlands) which sealed the soil surface by a powered-roller (Minnis et al., 2004). The Rumpstadt Combiject also went through the untreated plots but with the chisel injector turned off. For all treatments, the soil was cultivated prior to fumigation to prepare a weed-free surface and consequently no weeds were present in the field after the application of 1,3-D. Fumigation took place prior to bed formation and no tarp was used. 2.1.4. Crop planting Following the spring application of 1,3-D, the site was left undisturbed until 6 April, when it was chisel-ploughed to release any gas remaining in the soil. The potato cultivar Estima (Super Elite 2, size grade: 50e55 mm) was then planted at 20e25 cm depth and 28 cm in-row spacing on 11 May with the aid of a tractor-mounted potato planter. 2.1.5. Number of weeds germinating in soil after application of 1,3-D Immediately following the autumn application of 1,3-D, the ground was rolled to seal the surface, which was then left undisturbed over winter (Minnis et al., 2004). The weeds that had germinated and grown were counted on 11 December (43 days after fumigation), using a square quadrat of side 0.25 m and 16 random assessments were made on each plot.

1086

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

2.1.6. Percentage of ground covered by weeds The percentage of ground covered by weeds was assessed on 18 February (112 days after autumn fumigation). A square quadrat of side 1 m was used and eight assessments were made at random on each plot. 2.1.7. Number of weeds germinating on potato ridges A second assessment of the number of weeds that had germinated and grown was made on 27 May (210 days after autumn fumigation and 72 days after spring fumigation). The assessment was made 16 days after planting the crop on the top of the potato ridges. A square quadrat of side 0.25 m was again used and eight random assessments were made on each plot. 2.1.8. Germination of weed seeds in soil treated with 1,3-D The effect of 1,3-D on the weed seed bank was determined by assessing the germination of seeds from both treated and untreated soil. The number of seeds that germinated under glasshouse conditions (16 h photoperiod e temperature 15e25  C), was counted using a protocol similar to that of Roberts and Neilson (1981). Soil samples consisting of 12 cores (20 cm  3.5 cm) were taken at random from each plot to give approximately 2.5 kg of soil. The soil was thoroughly mixed and sieved and 2 kg was weighed into trays 30 cm long by 15 cm wide. The depth of soil in each tray was approximately 5 cm. Two sets of soil samples were collected from the treated and untreated soils. The first set was collected on 25 February (119 days after autumn fumigation) and the second on 21 April (174 days after autumn fumigation; 36 days after spring fumigation). The numbers of germinating weeds were counted and the weeds were removed as they appeared. This was done for the first set of samples on 24 March; 4, 14, 24 April; 12, 25 May; 25, 31 July; 8 October and 2 November, and for the second set on 27 May; 11, 25, 31 July; 8 October and 2 November. 2.2. Observations on R. solani 2.2.1. Field sites The plants assessed for R. solani severity were selected from two separate experimental field sites; Common Field (as described above for the weed experiment and hence, is referred to hereafter as Experiment 1) and Four Gates, which is also part of the Harper Adams University College farm (Experiment 2). 2.2.2. Field experiment one (Common Field) The plants were collected from the 10 plots that made up treatments (a) (untreated) and (c) (autumn application of 1,3-D) as described above for the weed experiment. Five plants were removed from each plot for assessment. The plants were randomly selected from the two outer rows of the non-harvest beds at 50 days after planting. All plots were three beds wide (5.5 m) and 9 m long and the middle two rows in each plot were used as the harvest rows in the study of Minnis et al. (2004). 2.2.3. Field experiment two (Four Gates) The second set of plants assessed for R. solani severity was from a larger experiment investigating the use of the soil fumigant 1,3-D in combination with the resistant cultivar Santé and the granular nematicide oxamyl at full and half rates for the control of PCN (Minnis et al., 2004). The site was infested with both G. pallida and G. rostochiensis but the latter was the predominant PCN species present. Only results from the assessments of stem canker disease severity are presented here, together with a summary of the main effects and interactions between the three treatments (cultivar, 1,3-

D and oxamyl) on the number and weight of stems. The results of PCN incidence, as well as potato plant emergence, percentage ground cover and yield, are available in Minnis et al. (2004). The experiment was of a two by two by three factorial design, making a total of 12 treatment combinations with five replicate plots per treatment. Plot size and design was as described in Experiment 1. There were two cultivars (Estima, for continuity with Experiment 1, and Santé), two levels for fumigation (treated and untreated) and three levels for the granular nematicide treatment (zero, half and full recommended application rates). Poor soil conditions during autumn meant that 1,3-D could not be applied, so fumigation took place on 1 April at 20 cm depth with a soil temperature of 9.5  C. After application of 1,3-D (at 211.5 L a. s. ha1, as Telone II) and soil surface sealing, the site was left undisturbed for 26 days and then ploughed to release any remaining gas in the soil, before forming the beds, on 27 April. On 30 April, the site was bed-tilled and stone-separated. The granular nematicide oxamyl was applied to the beds using a land-wheelmetered granule distributor on the day of planting (1 May). Oxamyl (as Vydate 10 G; 10% a.s. w/w; DuPont Ltd, Stevenage, UK) was applied as granules at two rates: 2.75 kg a.s. ha1 and 5.5 kg a. s. ha1. The nematicide was incorporated using a tractor-mounted rotavator to a depth of 15 cm. Fertiliser was applied according to soil analysis and standard agrochemical practices were followed for the control of weeds and diseases. Assessment of R. solani disease severity was conducted on stems from plants collected 44 days after planting. The twelfth plant was selected from the end of each of the two outer rows of the nonharvest beds, for each of the five replicate plots per treatment. Therefore, 120 assessments for stem canker severity were made in total (two sub-samples per plot  five replicate pots  12 treatments). The overall result was established by first calculating the mean of the two sub-samples in each of the 60 plots and then using these means to calculate the overall treatment mean. The same approach was followed in the calculation of the means for number of stems and total stem weight per plant. 2.2.4. R. solani disease severity and stem assessments The R. solani disease severity was determined using the key described by Simons and Gilligan (1997). Each harvested plant was initially examined to determine the number of stems and the proportion of infected stems per plant (disease incidence). The severity of stem canker on each stem was subsequently determined by assigning a severity score of 1e4 to each stem, as described below: 1. 2. 3. 4.

no stem canker up to one-third of the stem length affected by lesions one- to two-thirds of the length affected more than two-thirds of the length affected

A weighted estimate of disease severity was computed for each plant as (SXiWi)/(3SXi), in which Xi was the number of stems in each of the four categories and Wi took the value 0, 1, 2 or 3 for i ¼ 1, 2, 3 or 4, respectively (Simons and Gilligan, 1997). In addition to the R. solani disease severity, the total weight of stems per plant was also determined. 2.3. Statistical analysis The data were analysed using the software Genstat 5, Release 4.1 (Lawes Agricultural Trust, IACR-Rothamsted, UK). Analysis of variance was performed where possible on untransformed data, but the data were transformed when necessary by natural logarithm to normalise their distributions. For the glasshouse germination tests,

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

statistical analysis was conducted on the total number of weeds germinating and on the most abundant species present in each set of samples.

1087

Table 2 Species and total number of weed seeds germinated in soil from all plots (untreated and treated with 1,3-D). Weed species

3. Results 3.1. Weed numbers in the field and percentage ground cover Assessments conducted on 11 December (43 days after autumn fumigation) revealed that the mean number of weeds per m2 germinating in plots treated with 1,3-D was nearly six-fold lower than in untreated plots, a significant difference at P < 0.001 (Table 1A). On 18 February (112 days after autumn fumigation), ground cover by weeds in 1,3-D-treated plots was almost one-fifth of that measured in untreated plots (P < 0.001; Table 1B). The mean number of weeds growing on 27 May (210 days after autumn fumigation; 72 days after spring fumigation) on potato ridges in plots that included both a spring and an autumn application of 1,3D was less than the half of that of untreated plots. Similarly, plots that had been treated with 1,3-D in spring or autumn only, contained fewer weeds than their untreated counterparts, but none of these differences were significant (Table 1C). 3.2. Weed seed germination in the glasshouse In total, 23 weed species germinated in the field soil collected from all untreated and 1,3-D-treated plots (21 broad-leaved weeds and two grasses; Table 2). The most abundantly germinated weeds were fat-hen (Chenopodium album), field pansy (Viola arvensis) and annual meadow-grass (Poa annua), representing 77% of the total number of weeds germinated. Thirteen species were common in the two sets of soil samples and the rest were detected only in one set. On 25 February, 119 days after autumn fumigation, significantly lower numbers (P < 0.05) of weed seeds had germinated from plots treated with 1,3-D than from untreated plots (Table 3). Significantly fewer field pansies (P < 0.01) and small nettles (Urtica urens) (P < 0.01) germinated in treated than in untreated soil. The number of fat-hen seedlings was substantially less (P ¼ 0.06) in treated than

No. of weeds in second set of samplesb

No. of weeds in first set of samplesa

Broad-leaved weeds Annual sowthistle (Sonchus oleraceus) Black nightshade (Solanum nigrum) Black-bindweed (Fallopia convolvulus) Bugloss (Anchusa arvensis) Common chickweed (Stellaria media) Common field-speedwell (Veronica persica) Common fumitory (Fumaria officinalis) Common orache (Atriplex patula) Corn mint (Mentha arvensis) Fat-hen (Chenopodium album) Field pansy (Viola arvensis) Groundsel (Senecio vulgaris) Ivy-leaved speedwell (Veronica hederifolia) Knotgrass (Polygonum aviculare) Perennial sowthistle (Sonchus arvensis) Rayless mayweed (Chamomilla suaveolens) Redshank (Polygonum persicaria) Runch (Raphanus raphanistrum) Scarlet pimpernel (Anagallis arvensis) Shepherd’s-purse (Capsella bursa-pastoris) Small nettle (Urtica urens)

7 12 30 3 50 1 0 4 3 450 370 10 1 7 1 0 33 1 7 8 64

2 0 7 0 11 0 6 0 0 277 46 56 0 1 9 1 14 1 1 0 22

95 1

36 0

1158

490

Grass species Annual meadow-grass (Poa annua) Rough meadow-grass (Poa trivialis) Totals a

Collected 119 days after autumn fumigation. Collected 174 days after autumn fumigation and 36 days after spring fumigation. b

in untreated plots but the numbers of annual meadow-grass, blackbindweed (Fallopia convolvulus) and common chickweed (Stellaria media) seeds germinating were not significantly decreased following autumn application of 1,3-D (Table 3). On 21 April (174 days after autumn fumigation and 36 days after spring fumigation), the greatest population of weeds was found in the soil from untreated plots and the lowest in the soil from the plots that had been treated in both autumn and spring with 1,3-D (Table 4). The population of weeds in the soil from plots that had

Table 1 The effect of the soil fumigant 1,3-dichloropropene (1,3-D) on the germination of weeds in the field (untransformed data in parentheses). (A) 43 days after autumn fumigation e No. of weeds emerged Treatment

Number of weeds/m2

Statistics

Autumn 1,3-D: e Autumn 1,3-D: þ

6353 1099

SED ¼ 450.0 df ¼ 18 P < 0.001

(B) 112 days after autumn fumigation e Percentage ground cover by weeds Treatment

Loge (% ground cover)

Statistics

Autumn 1,3-D: e Autumn 1,3-D: þ

3.729 (42) 2.128 (9)

SED ¼ 0.086 df ¼ 18 P < 0.001

(C) 210 days after autumn fumigation; 72 days after spring fumigation e No. of weeds on potato ridges Treatment Autumn 1,3-D

Spring 1,3-D

e e þ þ

e þ e þ

Loge (no. of weeds/m2)

Statistics

3.01 2.62 2.52 2.31

SED ¼ 0.574 df ¼ 16 P ¼ NS

(27.9) (15.5) (17.1) (12.5)

SED, standard error of difference between means; df, degrees of freedom; e, 1,3-D not added; þ, 1,3-D added; NS, not significant.

Table 3 The number of weeds per 2 kg sample germinating in soil collected 119 days after autumn fumigation with 1,3-D. Treatment

Autumn 1,3-D: e

Autumn 1,3-D: þ

Total number of weeds Field pansy (V. arvensis) Small nettle (U. urens)a Fat-hen (C. album)a Annual meadow-grass (P. annua)a Black-bindweed (F. convolvulus)a Common chickweed (S. media)b

85.3 24.8 1.52 2.66 1.58 0.84 2.9

49.2 12.2 0.71 2.00 1.17 0.70 2.1

Total number of weeds Field pansy (V. arvensis) Small nettle (U. urens) Fat-hen (C. album) Annual meadow-grass (P. annua) Black-bindweed (F. convolvulus)

(4.8) (26.9) (5.2) (1.7)

(1.6) (18.1) (4.3) (1.3)

SED (18 df)

Probability

CV %

13.43 3.91 0.255 0.323 0.404 0.272

<0.05 <0.01 <0.01 0.06 NS NS

44.6 47.2 51.0 31.0 65.6 79.3

SED, standard error of difference between means; df, degrees of freedom; CV, coefficient of variation; e, 1,3-D not added; þ, 1,3-D added; NS, not significant. a Values transformed (to normalise) by natural logarithm (untransformed data in parentheses). b Data were skewed with no suitable transformation available.

1088

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

Table 4 The number of weeds per 2 kg sample germinating in soil collected 174 days after autumn fumigation and 36 days after spring fumigation with 1,3-D. Weeds

Total no. of weeds Field pansy (V. arvensis)a Fat-hen (C. album)a Annual meadow-grass (P. annua)a Groundsel (S. vulgaris)b

Loge (total no. of weeds) Field pansy (V. arvensis) Fat-hen (C. album) Annual meadow-grass (P. annua)

1,3-D Treatment Autumn: e

Autumn: e

Autumn: þ

Autumn: þ

Spring: e

Spring: þ

Spring: e

Spring: þ

3.50 1.74 2.22 1.11

2.65 0.74 1.71 1.13

2.97 0.72 2.23 0.50

2.42 0.55 1.87 0.64

(36) (5.4) (14.2) (2.20) (6.0)

(22) (1.6) (8.4) (3.00) (2.0)

(27) (1.2) (19.2) (1.00) (2.0)

(19) (1.0) (13.6) (1.00) (1.2)

SED (16 df)

Probability

CV %

0.406 0.312 0.381 0.405

0.09 0.01 NS NS

22.2 52.6 30.0 75.8

SED, standard error of difference between means; df, degrees of freedom; CV, coefficient of variation; e, 1,3-D not added; þ, 1,3-D added; NS, not significant. a Values transformed (to normalise) by natural logarithm (untransformed data in parentheses). b Data were skewed with no suitable transformation available.

received an autumn or a spring 1,3-D treatment was intermediate between those of untreated and double-treated (autumn and spring) plots. Analysis of the results indicated a trend towards a reduction (P ¼ 0.09) in weed populations following treatment with 1,3-D and a significant decrease (P ¼ 0.01) in the population of field pansy (Table 4). 3.3. Severity of R. solani, number and weight of stems In Experiment 1, plants from 1,3-D-treated plots exhibited approximately 20% lower stem canker severity than those from untreated plots, but the difference was out of range of statistical significance (df ¼ 18, P ¼ 0.12, SED ¼ 0.043). Similarly, no significant differences in stem canker disease severity were detected between plants from 1,3-D-fumigated plots and those from untreated plots in Experiment 2. Oxamyl and cultivar also did not produce a significant main effect on stem canker disease severity but their interaction was close to being significant (P ¼ 0.06). This was because the levels of R. solani were decreased for Estima with the use of oxamyl at full rate, whereas for Santé they were increased. Soil fumigation with 1,3-D resulted in significant increases in both the mean number (P < 0.05) and weight of stems (P < 0.01) per plant. There were also significant interactions between cultivar and oxamyl on both number (P < 0.001) and weight (P < 0.01) of stems, with both parameters decreased for Estima by oxamyl and increased for Santé. 4. Discussion The results from both experiments indicated that fumigation of soil with 1,3-D was not detrimental to R. solani. In Experiment 1, the high CV (58%) indicated a high degree of variability that would have meant that any differences would have to be large to be statistically significant. In Experiment 2, the observed increase in the number and weight of stems as a result of 1,3-D application was at first thought to be due in part to the slight decrease in stem canker, but this possibility was dismissed when estimations of correlations between the incidence of stem canker and the number and weight of stems were not found to be significant. This effect was possibly the result of extra inorganic nitrogen becoming available to plants because 1,3-D fumigation would have diminished the populations

of denitrifying bacteria. Denitrifying bacteria in the soil are known to deplete soil fertility by converting nitrates to gaseous nitrogen which is released into the atmosphere (Phillips, 2007). It has been reported, however, that 1,3-D kills such bacteria, thereby preventing loss of nitrogen into the atmosphere and increasing crop productivity (Lebbink and Kolenbrander, 1974). This is attributed to the greater amounts of nitrates available to plants in the 1,3-Dtreated relative to the untreated fields. Lebbink and Kolenbrander (1974) reported that the gain in inorganic nitrogen in the spring after autumn fumigation ranges typically from 5 to 10 kg ha1. This increase in the accumulation of nitrates in the soil-water solution nevertheless means that there is some risk of a proportion leaching and contaminating ground water (Elmi et al., 2002). Field assessments of the germinating weeds and weed ground cover revealed significant suppressive effects on weeds by the autumn 1,3-D fumigation. In particular, there was an almost fivefold decrease in percentage ground cover by weeds in 1,3-D-treated plots compared with the untreated plots, an order of magnitude comparable to the reduction size in the number of weeds germinating in the field. The reduced percentage of ground covered by weeds in 1,3-D-treated plots compared with the untreated controls was attributed to the lower number of weeds found to have germinated 69 days earlier in treated than in untreated soil. Despite the lack of a significant effect, which was clearly the consequence of the very high coefficient of variation (94.9% and 31% in untransformed and transformed data, respectively), plots that received at least one 1,3-D treatment had slightly lower weeds germinating on potato ridges relative to the untreated. Data on the degradation rate of 1,3-D from various studies, which were reviewed by Dungan and Yates (2003), indicated a half-life for this fumigant ranging from a few days (minimum: 0.3 days) to a few weeks (maximum: 38.5 days), depending on soil microbial activity, type, moisture and temperature (e.g. 9.9e33 days at 15  C; Smelt et al., 1989). Consequently, since the assessments on potato ridges were made 72 days after spring fumigation and 16 days after planting, any residual fumigant concentration in the soil would have been minimal, thus posing a low phytotoxicity risk to weed growing tissues. Furthermore, at this time potato plants had not yet fully emerged and were not competing with the weed population. It therefore appears that the inhibitory effect of 1,3-D on weeds shown here in the three field assessments discussed above may not have been simply the result of direct phytotoxicity on the developing roots or rhizomes but also of a potential decrease in the number of viable seeds in the weed seed bank. This speculation was in agreement with the report of Monaco et al. (2002, pp. 105e106) that gaseous fumigants can affect plants prior to germination, in contrast with herbicides, which entry into ungerminated seeds does not usually lead to viability loss like in fumigants. Various mechanisms have been previously proposed to explain the suppressing effects of soil fumigants on weeds and some examples are discussed below. In the experiments of Altman and Fitzgerald (1960), which have been described earlier, reductions in weed germination and growth by the soil fumigant DeD were attributed in part to a direct effect on the weed seed and in part to shading from the more vigorous growth of beet foliage in treated plots relative to the untreated. A study to evaluate the use of 1,3-D for the control of field horsetail (Equisetum arvense) was conducted by Coupland and Peabody (1980). The extensive rhizome system of this weed, which can penetrate deeply into the soil, is the main factor contributing to its success. The results of their experiments suggested that 1,3-D was an effective treatment for the control of this weed and its success was attributed to phytotoxic effects on the rhizome tissue and the prevention of rhizome and shoot development by fumigant residues.

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

In the study presented here, there was a wide range of weed species on the experimental site but apart from one, corn mint (Mentha arvensis), they were all species that survive and disperse as seeds. The significant (first set) or substantial (second set) decrease in the number of weed seeds germinating under glasshouse conditions from 1,3-D-treated soil relative to the untreated, confirmed the findings of the field assessments (in-soil germination and ground cover) and the above speculation that 1,3-D fumigation had a suppressive effect on the weed seed bank population. Almost double the number of weed seeds germinated in the first set of samples as compared with the second set. This could be attributed to the time intervals between fumigations with 1,3-D and assessments of weed seeds germination. In contrast with the first set which was collected 119 days after autumn fumigation, the second set was collected just 36 days after spring application of 1,3-D, consequently resulting in greater numbers of seeds being killed in the latter than the former. According to Caetano et al. (2001) and Lutman et al. (2002), cultural operations play a major role in the quantitative and qualitative composition of weed seed banks, seed germination and survival. In the study presented here, chisel ploughing took place 15 days prior collection of the second set of soil samples. Ploughing may have therefore effectively reduced the weed seed bank by burying a significant number of viable seeds to depths unsuitable for germination (>15e20 cm) without simultaneously bringing deeply buried seeds near the surface. In contrast with the single autumn application of 1,3-D, the combined autumn and spring fumigation did not produce a significant main effect on the weed seed bank but just a weak trend for reduction instead. In particular, from the four individual weeds tested, only one (field pansy) was present in significantly lower levels in soil from 1,3-D-treated plots than from untreated controls. Field pansy was the only species with significantly decreased germination in both set of samples, demonstrating a high susceptibility of this species to the soil fumigant 1,3-D. Statistical significance may sometimes be of limited practical significance, such as in Table 3 here. This is because a significant suppression in weed seed bank germination levels following spring fumigation (Table 4), and therefore closer to planting, is expected to have obviously brought a larger benefit to the potato farmer, than the reduction presented in Table 3. The results showed that 1,3-D reduced weed seed germination in the field, with some six times fewer weeds being recorded after autumn and prior to spring treatment. On the other hand, glasshouse germination tests revealed a two-fold decrease in the number of seeds germinating. This variation in the degree of weed suppression between field and glasshouse experiments may be attributed to the fact that seeds are generally harder to kill than growing plant tissues. The subsequent assessments in the field showed that the beneficial effect of 1,3-D fumigation decreased in time and the reasons for this are explained below. Based on the overall findings, however, it appears that the mode of action of 1,3-D was by a combination of phytotoxicity towards young seedlings in treated soil and seed viability suppression in the weed seed bank. Lawson (1984) published a study on the effectiveness of soil sterilants, including 1,3-D, against weeds in soft fruit crops. Injection of 1,3-D was done by a Rumpstadt Combiject to a depth of 20 cm and the soil surface was then slightly sealed by rolling. The author reported that 1,3-D had only a little effect on population of weed seeds germinating from the top 10 cm of soil. However, the lack of effect could have been because much of the gas escaped from the top 5 cm. If samples had been taken from 20 cm deep, greater kill of weed seeds might have been recorded. Control of organisms close to the soil surface with fumigants is often poor. The efficacy of the product is

1089

a function of chemical concentration  time of exposure. As the fumigant diffuses to the surface, its concentration decreases as there is usually more air space for diffusion and there is rapid loss from the soil, thus reducing the effectiveness of the chemical (Turner et al., 1974). In consequence, it can be speculated that data from the glasshouse assessments (Tables 3 and 4) were possibly more representative of the results achieved in the bulk of soil, whereas in the field assessments (Table 1), the effects were from the surface layers, where gas concentrations tend to be lower as explained above. The variability in the data obtained prevented in some cases the detection of statistical significance. For example, as Table 1C shows, 1,3-D application suppressed the number of weeds that germinated on potato ridges by between 39 and 55% compared with the untreated, but the F-probability was 0.57. In Table 4, with an interaction F-probability of 0.09, 25e47% less weeds germinated in the glasshouse from the 1,3-D-treated field soil sample relative to the corresponding untreated sample. This problem may be resolved in relevant future research, thus possibly ensuring a higher degree of confidence in the results, if more replicate plots are utilised and sampling methods are improved, for instance, by increasing the number of random assessments per plot. In the present study, however, these were the maximum number of replicates the resources would allow our research team to use when the experiments were performed. As a consequence of the withdrawal of methyl bromide from use as a soil fumigant in 2005, a considerable amount of research has been undertaken to investigate the effectiveness of alternative, nonozone-depleting soil fumigants for controlling soil-borne fungi, nematodes and weeds. In the UK, the possible chemical alternatives to methyl bromide include 1,3-D, chloropicrin, dazomet, formaldehyde and methamesodium (ADAS, 2005). In particular, the effect of a mixed 1,3-D-chloropicrin treatment (as Telone C-17 or Telone C-35, Dow AgroSciences LLC; not registered in the UK) in the control of various weed species has been extensively tested (Gilreath and Santos, 2005; Chase et al., 2006; Santos et al., 2006; Klose et al., 2007). Most of these studies have been conducted in the USA in strawberry or vegetable crops (tomato in particular) and were confined to the control of a few or a single weed species (especially nutsedge, Cyperus spp.). In the UK, there is insufficient information on the efficacy of 1,3-D, alone or in combination with other soil fumigants, in the management of weeds in field vegetable or arable crops, including potatoes. The study presented here is the first to provide both quantitative and qualitative analyses on the effects of the soil fumigant 1,3-D on the germination of a wide range of weed species growing in UK potato fields. An economic cost/benefit analysis of the use of 1,3-D by Minnis et al. (2004) showed a clear economic benefit from its use when applied in the autumn preceding potato production whether used as the sole nematicide or when followed by a spring application of a granular nematicide. Further to these benefits from the use of 1,3-D, the suppressive effect on the weed seed bank, as shown in this study, could be of additional benefit to potato farmers in crop rotation, in terms of weed control on subsequent crops within the rotation.

Acknowledgments This research was funded by Dow Agrosciences Ltd and by the Department for the Environment, Food and Rural Affairs, UK. The authors wish to acknowledge help from the Crop and Environment Research Centre at Harper Adams University College, UK, for their assistance and Robin Barker (EG Barker & Son), Peter Blaylock (Independent Soil Analysis) and Pete Richardson (Supacrop) for the application of 1,3-D. Rothamsted Research receives grant-aided

1090

P.P.J. Haydock et al. / Crop Protection 29 (2010) 1084e1090

support from the UK Biotechnology and Biological Sciences Research Council. References ADAS, 2005. UK Application of Methyl Bromide and Its Alternatives. Final Report on Defra Project GA01062. Defra (Global Atmosphere Division), York, UK. http://randd.defra.gov.uk/Document.aspx?Document¼GA01062_3953_FRP.pdf 161 pp. Altman, J., Fitzgerald, B.J., 1960. Late fall application of fumigants for the control of sugar beet nematodes, certain fungi, and weeds. Plant Dis. Rep. 44, 868e871. Back, M.A., Haydock, P.P.J., Jenkinson, P., 2002. Disease complexes involving plant parasitic nematodes and soilborne pathogens. Plant Pathol. 51, 683e697. Back, M., Haydock, P., Jenkinson, P., 2006. Interactions between the potato cyst nematode Globodera rostochiensis and diseases caused by Rhizoctonia solani AG3 in potatoes under field conditions. Eur. J. Plant Pathol. 114, 215e223. Baines, R.C., Klotz, L.J., DeWolfe, T.A., 1977. Some biocidal properties of 1,3-D and its degradation product. Phytopathology 67, 936e940. Caetano, R.S.X., Christoffoleti, P.J., Filho, R.V., 2001. “Banco” de sementes de plantas daninhas em pomar de laranjeira ‘pera’. Sci. Agric. 58, 509e517. Chase, C.A., Stall, W.M., Simonne, E.H., Hochmuth, R.C., Dukes, M.D., Weiss, A.W., 2006. Nutsedge control with drip-applied 1,3-dichloropropene plus chloropicrin in a sandy soil. Horttechnology 16, 641e648. Coupland, D., Peabody, D.V., 1980. Control of field horsetail using a soil fumigant containing 1,3-dichloropropene. Proceedings of the 1980 Crop Protection Conference e Weeds, 17e20 November, Brighton, UK. Davies, J.M.L., 1990. Onion white rot control e sterilant or stimulant? Proceedings of the 1990 Crop Protection Conference e Pests and Diseases, vol. 1, 19 November, Brighton, UK, pp. 109e110. Dungan, R.S., Yates, S.R., 2003. Degradation of fumigant pesticides: 1,3-Dichloropropene, methyl isothiocyanate, chloropicrin and methyl bromide. Vadose Zone J., 279e286. Elmi, A.A., Madramootoo, C., Egeh, M., Liu, A.G., Hamel, C., 2002. Environmental and agronomic implications of water table and nitrogen fertilization management. J. Environ. Qual. 31, 1858e1867. FERA, 2010. Pesticide Usage Statistics. The Food and Environment Research Agency, York, UK. http://pusstats.csl.gov.uk/index.cfm. Gilreath, J.P., Santos, B.M., 2005. Efficacy of 1,3-dichloropropene plus chloropicrin in combination with herbicides on purple nutsedge (Cyperus rotundus) control in tomato. Weed Technol. 19, 137e140. Haydock, P.P.J., Evans, K., 1998. Management of potato cyst nematodes in the UK: an integrated approach? Outlook Agric. 27, 253e260. Hofman, T.W., Bollen, G.J., 1987. Effects of granular nematicides on growth and microbial antagonism to Rhizoctonia solani. Neth. J. Plant Pathol. 93, 201e214. Jacobsohn, R., Kleifeld, Y., Agrawal, V.P., Jha, P., Marton, K., 1991. Soil fumigation with Telone II for broomrape (Orobanche spp.) control. In: Wegmann, K., Musselman, L.J. (Eds.), Progress in Orobanche Research. Eberhard Karls Universität, Tübingen, Germany, pp. 185e190.

Kegley, S.E., Hill, B.R., Orme, S., Choi, A.H., 2010. PAN Pesticide Database. Pesticide Action Network North America, San Francisco, CA. http://www.pesticideinfo.org. Klose, S., Ajwa, H.A., Fennimore, S.A., Martin, F.N., Browne, G.T., Subbarao, K.V., 2007. Dose response of weed seeds and soilborne pathogens to 1,3-D and chloropicrin. Crop Prot. 26, 535e542. Lawson, H.M., 1984. The contribution of soil partial sterilants to weed control in soft fruit crops. Asp. Appl. Biol. 8, 199e204. Leach, S.S., Frank, J.A., 1982. Influence of three systemic insecticides on Verticillium wilt and Rhizoctonia disease complex of potato. Plant Dis. 66, 1180e1182. Lebbink, G., Kolenbrander, G.J., 1974. Quantitative effect of fumigation with 1,3dichloropropene mixtures and with metham sodium on the soil nitrogen status. Agric. Environ. 1, 283e292. Lutman, P.J.W., Cussans, G.W., Wright, K.J., Wilson, B.J., Wright, G.M., Lawson, H.M., 2002. The persistence of seeds of 16 weed species over six years in two arable fields. Weed Res. 42, 231e241. Minnis, S.T., Haydock, P.P.J., Evans, K., 2004. Control of potato cyst nematodes and economic benefits of application of 1,3-dichloropropene and granular nematicides. Ann. Appl. Biol. 145, 145e156. Monaco, T.J., Weller, S.C., Ashton, F.M., 2002. Weed Science: Principles and Practices, fourth ed. John Wiley & Sons Inc., New York, NY, 688 pp. Morgan, D.O., 1926. Some remarks on the etiology of potato disease in Lincolnshire. J. Helminthol. 4, 49e52. Phillips, R.L., 2007. Denitrification in frozen agricultural soil. A review. Agron. Sustain. Dev. 28, 1e7. Read, P.J., Hide, G.A., 1995. Effects of fungicides on the growth and conidial germination of Colletotrichum coccodes and on the development of black dot disease of potatoes. Ann. Appl. Biol. 126, 437e447. Roberts, H.A., Neilson, J.E., 1981. Seed survival and periodicity of seedling emergence in 12 weedy species of Compositae. Ann. Appl. Biol. 97, 325e334. Ruppel, E.G., Hecker, R.J., 1982. Increased severity of Rhizoctonia root rot in sugar beet treated with systemic insecticides. Crop Prot. 1, 75e81. Santos, B.M., Gilreath, J.P., Motis, T.N., von Hulten, M., Siham, M.N., 2006. Effects of mulch types and concentrations of 1,3-dichloropropene plus chloropicrin on fumigant retention and nutsedge control. Horttechnology 16, 637e640. Scholte, K., 1992. Effect of crop rotation on the incidence of soil-borne fungal diseases of potato. Neth. J. Plant Pathol. 98, 93e101. Simons, S.A., Gilligan, C.A.,1997. Factors affecting the temporal progress of stem canker (Rhizoctonia solani) on potatoes (Solanum tuberosum). Plant Pathol. 46, 642e650. Smelt, J.H., Teunissen, W., Crum, S.J.H., Leistra, M., 1989. Accelerated transformation of 1,3-dichloropropene in loamy soils. Neth. J. Agric. Sci. 37, 173e183. Stevenson, W.R., Green, R.J., Bergeson, G.B., 1976. Occurrence and control of potato black dot root-rot in Indiana. Plant Dis. Rep. 60, 248e251. Sumner, D.R., Gitaitis, R.D., Gay, J.D., Smittle, D.A., Maw, B.W., Tollner, E.W., Hung, Y. C., 1997. Control of soilborne pathogenic fungi in fields of sweet onion. Plant Dis. 81, 885e891. Tu, C.M., 1993. Effect of nematicides, Telone II and Vorlex, on microflora and nitrification in tobacco soil. Bull. Environ. Contam. Toxicol. 50, 43e48. Turner, G.O., Greathead, A.S., Welch, N.C., 1974. Control of annual weed seeds with soil fumigants containing 1,3-dichloropropenes. Down Earth 29, 25e28. Uhlig, R.E., Bird, G., Richardson, R.J., Zandstra, B.H., 2007. Soil fumigants to replace methyl bromide for weed control in ornamentals. Horttechnology 17, 111e114.